1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

and Urinary Tract Infections

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • XML
    375.87 Kb
  • PDF
    1.66 MB
  • HTML
    337.93 Kb
  • Authors: Jessica N. Schaffer1, Melanie M. Pearson2
  • Editors: Matthew A. Mulvey3, Ann E. Stapleton4, David J. Klumpp5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology, New York University Langone Medical Center, New York, NY 10016; 2: Department of Microbiology, New York University Langone Medical Center, New York, NY 10016; 3: University of Utah, Salt Lake City, UT; 4: University of Washington, Seattle, WA; 5: Northwestern University, Chicago, IL
    • Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
  • Received 03 April 2013 Accepted 29 July 2014 Published 18 September 2015
  • Melanie M. Pearson, [email protected]
image of <span class="jp-italic">Proteus mirabilis</span> and Urinary Tract Infections
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    and Urinary Tract Infections, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/3/5/UTI-0017-2013-1.gif /docserver/preview/fulltext/microbiolspec/3/5/UTI-0017-2013-2.gif

  • Abstract:

    is a Gram-negative bacterium and is well known for its ability to robustly swarm across surfaces in a striking bulls’-eye pattern. Clinically, this organism is most frequently a pathogen of the urinary tract, particularly in patients undergoing long-term catheterization. This review covers with a focus on urinary tract infections (UTI), including disease models, vaccine development efforts, and clinical perspectives. Flagella-mediated motility, both swimming and swarming, is a central facet of this organism. The regulation of this complex process and its contribution to virulence is discussed, along with the type VI-secretion system-dependent intra-strain competition, which occurs during swarming. uses a diverse set of virulence factors to access and colonize the host urinary tract, including urease and stone formation, fimbriae and other adhesins, iron and zinc acquisition, proteases and toxins, biofilm formation, and regulation of pathogenesis. While significant advances in this field have been made, challenges remain to combatting complicated UTI and deciphering pathogenesis.

  • Citation: Schaffer J, Pearson M. 2015. and Urinary Tract Infections. Microbiol Spectrum 3(5):UTI-0017-2013. doi:10.1128/microbiolspec.UTI-0017-2013.

References

1. O’Hara CM, Brenner FW, Miller JM. 2000. Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin Microbiol Rev 13:534–546. [PubMed][CrossRef]
2. Matthews SJ, Lancaster JW. 2011. Urinary tract infections in the elderly population. Am J Geriatr Pharmacother 9:286–309. [PubMed][CrossRef]
3. Papazafiropoulou A, Daniil I, Sotiropoulos A, Balampani E, Kokolaki A, Bousboulas S, Konstantopoulou S, Skliros E, Petropoulou D, Pappas S. 2010. Prevalence of asymptomatic bacteriuria in type 2 diabetic subjects with and without microalbuminuria. BMC Res Notes 3:169. [PubMed][CrossRef]
4. Janda JMA, Abbott SL. 2006. The Enterobacteria, 2 ed. ASM Press, Washington, D.C.
5. Mathur S, Sabbuba NA, Suller MT, Stickler DJ, Feneley RC. 2005. Genotyping of urinary and fecal Proteus mirabilis isolates from individuals with long-term urinary catheters. Eur J Clin Microbiol Infect Dis 24:643–644. [PubMed][CrossRef]
6. Jacobsen SM, Stickler DJ, Mobley HLT, Shirtliff ME. 2008. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin Microbiol Rev 21:26–59. [PubMed][CrossRef]
7. Gaston H. 1995. Proteus—is it a likely aetiological factor in chronic polyarthritis? Ann Rheum Dis 54:157–158. [PubMed][CrossRef]
8. Rashid T, Ebringer A. 2007. Rheumatoid arthritis is linked to Proteus—the evidence. Clin Rheumatol 26:1036–1043. [PubMed][CrossRef]
9. Karlowsky JA, Lagacé-Wiens PR, Simner PJ, DeCorby MR, Adam HJ, Walkty A, Hoban DJ, Zhanel GG. 2011. Antimicrobial resistance in urinary tract pathogens in Canada from 2007 to 2009: CANWARD surveillance study. Antimicrob Agents Chemother 55:3169–3175. [PubMed][CrossRef]
10. Nielubowicz GR, Mobley HLT. 2010. Host-pathogen interactions in urinary tract infection. Nat Rev Urol 7:430–441. [PubMed][CrossRef]
11. Nicolle LE. 2005. Catheter-related urinary tract infection. Drugs Aging 22:627–639. [PubMed][CrossRef]
12. Hung EW, Darouiche RO, Trautner BW. 2007. Proteus bacteriuria is associated with significant morbidity in spinal cord injury. Spinal Cord 45:616–620. [PubMed][CrossRef]
13. Adams-Sapper S, Sergeevna-Selezneva J, Tartof S, Raphael E, Diep BA, Perdreau-Remington F, Riley LW. 2012. Globally dispersed mobile drug-resistance genes in gram-negative bacterial isolates from patients with bloodstream infections in a US urban general hospital. J Med Microbiol 61:968–974. [PubMed][CrossRef]
14. Mylotte JM. 2005. Nursing home-acquired bloodstream infection. Infect Control Hosp Epidemiol 26:833–837. [PubMed][CrossRef]
15. Sader HS, Flamm RK, Jones RN. 2014. Frequency of occurrence and antimicrobial susceptibility of Gram-negative bacteremia isolates in patients with urinary tract infection: results from United States and European hospitals (2009–2011). J Chemother 26:133–138. [PubMed][CrossRef]
16. Lubart E, Segal R, Haimov E, Dan M, Baumoehl Y, Leibovitz A. 2011. Bacteremia in a multilevel geriatric hospital. J Am Med Dir Assoc 12:204–207. [PubMed][CrossRef]
17. Pearson MM, Sebaihia M, Churcher C, Quail MA, Seshasayee AS, Luscombe NM, Abdellah Z, Arrosmith C, Atkin B, Chillingworth T, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Walker D, Whithead S, Thomson NR, Rather PN, Parkhill J, Mobley HLT. 2008. Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J Bacteriol 190:4027–4037. [PubMed][CrossRef]
18. Mobley HLT. 2001. Urease. In Mobley HLT, Mendz GL, Hazell SL (ed), Helicobacter pylori: physiology and genetics doi:NBK2417. ASM Press, Washington, DC. [CrossRef]
19. Mobley HLT. 1996. Virulence of Proteus mirabilis, p 245–269. In Mobley HL, Warren JW (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management. ASM Press, Washington, D.C.
20. Griffith DP, Musher DM, Itin C. 1976. Urease. The primary cause of infection-induced urinary stones. Invest Urol 13:346–350. [PubMed]
21. Nicholson EB, Concaugh EA, Foxall PA, Island MD, Mobley HLT. 1993. Proteus mirabilis urease: transcriptional regulation by UreR. J Bacteriol 175:465–473. [PubMed]
22. Dattelbaum JD, Lockatell CV, Johnson DE, Mobley HLT. 2003. UreR, the transcriptional activator of the Proteus mirabilis urease gene cluster, is required for urease activity and virulence in experimental urinary tract infections. Infect Immun 71:1026. [PubMed][CrossRef]
23. Poore CA, Mobley HLT. 2003. Differential regulation of the Proteus mirabilis urease gene cluster by UreR and H-NS. Microbiology 149:3383–3394. [PubMed][CrossRef]
24. Zhao H, Thompson RB, Lockatell V, Johnson DE, Mobley HLT. 1998. Use of green fluorescent protein to assess urease gene expression by uropathogenic Proteus mirabilis during experimental ascending urinary tract infection. Infect Immun 66:330–335. [PubMed]
25. Pearson MM, Yep A, Smith SN, Mobley HLT. 2011. Transcriptome of Proteus mirabilis in the murine urinary tract: virulence and nitrogen assimilation gene expression. Infect Immun 79:2619–2631. [PubMed][CrossRef]
26. Munns J, Amawi F. 2010. A large urinary bladder stone: an unusual cause of rectal prolapse. Arch Dis Child 95:1026. [PubMed][CrossRef]
27. Chew R, Thomas S, Mantha ML, Killen JP, Cho Y, Baer RA. 2012. Large urate cystolith associated with Proteus urinary tract infection. Kidney Int 81:802. [PubMed][CrossRef]
28. Jones BV, Mahenthiralingam E, Sabbuba NA, Stickler DJ. 2005. Role of swarming in the formation of crystalline Proteus mirabilis biofilms on urinary catheters. J Med Microbiol 54:807–813. [PubMed][CrossRef]
29. Stickler DJ. 2008. Bacterial biofilms in patients with indwelling urinary catheters. Nat Clin Pract Urol 5:598–608. [PubMed][CrossRef]
30. Torzewska A, Budzyńska A, Białczak-Kokot M, Różalski A. 2014. In vitro studies of epithelium-associated crystallization caused by uropathogens during urinary calculi development. Microb Pathog 71–72C:25–31.
31. Mobley HLT, Warren JW. 1987. Urease-positive bacteriuria and obstruction of long-term urinary catheters. J Clin Microbiol 25:2216–2217. [PubMed]
32. Li X, Zhao H, Lockatell CV, Drachenberg CB, Johnson DE, Mobley HLT. 2002. Visualization of Proteus mirabilis within the matrix of urease-induced bladder stones during experimental urinary tract infection. Infect Immun 70:389–394. [PubMed][CrossRef]
33. Jones BD, Lockatell CV, Johnson DE, Warren JW, Mobley HLT. 1990. Construction of a urease-negative mutant of Proteus mirabilis: analysis of virulence in a mouse model of ascending urinary tract infection. Infect Immun 58:1120–1123. [PubMed]
34. Johnson DE, Russell RG, Lockatell CV, Zulty JC, Warren JW, Mobley HLT. 1993. Contribution of Proteus mirabilis urease to persistence, urolithiasis, and acute pyelonephritis in a mouse model of ascending urinary tract infection. Infect Immun 61:2748–2754. [PubMed]
35. Armbruster CE, Smith SN, Yep A, Mobley HLT. 2014. Increased incidence of urolithiasis and bacteremia during Proteus mirabilis and Providencia stuartii coinfection due to synergistic induction of urease activity. J Infect Dis 209:1524–1532. [PubMed][CrossRef]
36. Follmer C. 2010. Ureases as a target for the treatment of gastric and urinary infections. J Clin Pathol 63:424–430. [PubMed][CrossRef]
37. Suller MT, Anthony VJ, Mathur S, Feneley RC, Greenman J, Stickler DJ. 2005. Factors modulating the pH at which calcium and magnesium phosphates precipitate from human urine. Urol Res 33:254–260. [PubMed][CrossRef]
38. Khan A, Housami F, Melotti R, Timoney A, Stickler D. 2010. Strategy to control catheter encrustation with citrated drinks: a randomized crossover study. J Urol 183:1390–1394. [PubMed][CrossRef]
39. Macnab RM. 2003. How bacteria assemble flagella. Annu Rev Microbiol 57:77–100. [PubMed][CrossRef]
40. Belas R, Flaherty D. 1994. Sequence and genetic analysis of multiple flagellin-encoding genes from Proteus mirabilis. Gene 148:33–41. [PubMed][CrossRef]
41. Belas R. 1994. Expression of multiple flagellin-encoding genes of Proteus mirabilis. J Bacteriol 176:7169–7181. [PubMed]
42. Murphy CA, Belas R. 1999. Genomic rearrangements in the flagellin genes of Proteus mirabilis. Mol Microbiol 31:679–690. [PubMed][CrossRef]
43. Manos J, Belas R. 2004. Transcription of Proteus mirabilis flaAB. Microbiology 150:2857–2863. [PubMed][CrossRef]
44. Manos J, Artimovich E, Belas R. 2004. Enhanced motility of a Proteus mirabilis strain expressing hybrid FlaAB flagella. Microbiology 150:1291–1299. [PubMed][CrossRef]
45. Nielubowicz GR, Smith SN, Mobley HLT. 2008. Outer membrane antigens of the uropathogen Proteus mirabilis recognized by the humoral response during experimental murine urinary tract infection. Infect Immun 76:4222–4231. [PubMed][CrossRef]
46. Chevance FF, Hughes KT. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol 6:455–465. [PubMed][CrossRef]
47. Claret L, Hughes C. 2000. Functions of the subunits in the FlhD(2)C(2) transcriptional master regulator of bacterial flagellum biogenesis and swarming. J Mol Biol 303:467–478. [PubMed][CrossRef]
48. Wang S, Fleming RT, Westbrook EM, Matsumura P, McKay DB. 2006. Structure of the Escherichia coli FlhDC complex, a prokaryotic heteromeric regulator of transcription. J Mol Biol 355:798–808. [PubMed][CrossRef]
49. Bahrani FK, Johnson DE, Robbins D, Mobley HLT. 1991. Proteus mirabilis flagella and MR/P fimbriae: isolation, purification, N-terminal analysis, and serum antibody response following experimental urinary tract infection. Infect Immun 59:3574–3580. [PubMed]
50. Snyder JA, Haugen BJ, Buckles EL, Lockatell CV, Johnson DE, Donnenberg MS, Welch RA, Mobley HLT. 2004. Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72:6373. [PubMed][CrossRef]
51. Lane MC, Alteri CJ, Smith SN, Mobley HLT. 2007. Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. Proc Natl Acad Sci USA 104:16669–16674. [PubMed][CrossRef]
52. Mobley HLT, Belas R, Lockatell V, Chippendale G, Trifillis AL, Johnson DE, Warren JW. 1996. Construction of a flagellum-negative mutant of Proteus mirabilis: effect on internalization by human renal epithelial cells and virulence in a mouse model of ascending urinary tract infection. Infect Immun 64:5332–5340. [PubMed]
53. Pazin GJ, Braude AI. 1974. Immobilizing antibodies in urine. II. Prevention of ascending spread of Proteus mirabilis. Invest Urol 12:129–133. [PubMed]
54. Zunino P, Piccini C, Legnani-Fajardo C. 1994. Flagellate and non-flagellate Proteus mirabilis in the development of experimental urinary tract infection. Microb Pathog 16:379–385. [PubMed][CrossRef]
55. Legnani-Fajardo C, Zunino P, Piccini C, Allen A, Maskell D. 1996. Defined mutants of Proteus mirabilis lacking flagella cause ascending urinary tract infection in mice. Microb Pathog 21:395–405. [PubMed][CrossRef]
56. Burall LS, Harro JM, Li X, Lockatell CV, Himpsl SD, Hebel JR, Johnson DE, Mobley HLT. 2004. Proteus mirabilis genes that contribute to pathogenesis of urinary tract infection: identification of 25 signature-tagged mutants attenuated at least 100-fold. Infect Immun 72:2922–2938. [PubMed][CrossRef]
57. Himpsl SD, Lockatell CV, Hebel JR, Johnson DE, Mobley HLT. 2008. Identification of virulence determinants in uropathogenic Proteus mirabilis using signature-tagged mutagenesis. J Med Microbiol 57:1068–1078. [PubMed][CrossRef]
58. Williams FD, Schwarzhoff RH. 1978. Nature of the swarming phenomenon in Proteus. Annu Rev Microbiol 32:101–122. [PubMed][CrossRef]
59. Gué M, Dupont V, Dufour A, Sire O. 2001. Bacterial swarming: a biochemical time-resolved FTIR-ATR study of Proteus mirabilis swarm-cell differentiation. Biochemistry 40:11938–11945. [PubMed][CrossRef]
60. Strating H, Vandenende C, Clarke AJ. 2012. Changes in peptidoglycan structure and metabolism during differentiation of Proteus mirabilis into swarmer cells. Can J Microbiol 58:1183–1194. [PubMed][CrossRef]
61. Jones BV, Young R, Mahenthiralingam E, Stickler DJ. 2004. Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated urinary tract infection. Infect Immun 72:3941–3950. [PubMed][CrossRef]
62. Stahl SJ, Stewart KR, Williams FD. 1983. Extracellular slime associated with Proteus mirabilis during swarming. J Bacteriol 154:930–937. [PubMed]
63. Gygi D, Rahman MM, Lai HC, Carlson R, Guard-Petter J, Hughes C. 1995. A cell-surface polysaccharide that facilitates rapid population migration by differentiated swarm cells of Proteus mirabilis. Mol Microbiol 17:1167–1175. [PubMed][CrossRef]
64. Rahman MM, Guard-Petter J, Asokan K, Hughes C, Carlson RW. 1999. The structure of the colony migration factor from pathogenic Proteus mirabilis: a capsular polysaccharide that facilitates swarming. J Biol Chem 274:22993–22998. [PubMed][CrossRef]
65. Pearson MM, Rasko DA, Smith SN, Mobley HLT. 2010. Transcriptome of swarming Proteus mirabilis. Infect Immun 78:2834–2845. [PubMed][CrossRef]
66. Allison C, Lai HC, Hughes C. 1992. Co-ordinate expression of virulence genes during swarm-cell differentiation and population migration of Proteus mirabilis. Mol Microbiol 6:1583–1591. [PubMed][CrossRef]
67. Harshey RM. 2003. Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57:249–273. [PubMed][CrossRef]
68. Inoue T, Shingaki R, Hirose S, Waki K, Mori H, Fukui K. 2007. Genome-wide screening of genes required for swarming motility in Escherichia coli K–12. J Bacteriol 189:950–957. [PubMed][CrossRef]
69. Wang Q, Frye JG, McClelland M, Harshey RM. 2004. Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes. Mol Microbiol 52:169–187. [PubMed][CrossRef]
70. Kim W, Surette MG. 2004. Metabolic differentiation in actively swarming Salmonella. Mol Microbiol 54:702–714. [PubMed][CrossRef]
71. Allison C, Lai HC, Gygi D, Hughes C. 1993. Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells. Mol Microbiol 8:53–60. [PubMed][CrossRef]
72. Senior BW. 1978. p-nitrophenylglycerol—a superior antiswarming agent for isolating and identifying pathogens from clinical material. J Med Microbiol 11:59–61. [PubMed][CrossRef]
73. Belas R, Erskine D, Flaherty D. 1991. Transposon mutagenesis in Proteus mirabilis. J Bacteriol 173:6289–6293. [PubMed]
74. Liu MC, Lin SB, Chien HF, Wang WB, Yuan YH, Hsueh PR, Liaw SJ. 2012. 10′( Z),13′( E)-heptadecadienylhydroquinone inhibits swarming and virulence factors and increases polymyxin B susceptibility in Proteus mirabilis. PLoS One 7:e45563. [PubMed][CrossRef]
75. Wang WB, Lai HC, Hsueh PR, Chiou RY, Lin SB, Liaw SJ. 2006. Inhibition of swarming and virulence factor expression in Proteus mirabilis by resveratrol. J Med Microbiol 55:1313–1321. [PubMed][CrossRef]
76. Hernandez E, Ramisse F, Cavalho JD. 1999. Abolition of swarming of Proteus. J Clin Microbiol 37:3435. [PubMed]
77. Ayati BP. 2006. A structured-population model of Proteus mirabilis swarm-colony development. J Math Biol 52:93–114. [PubMed][CrossRef]
78. Esipov SE, Shapiro JA. 1998. Kinetic model of Proteus mirabilis swarm colony development. Journal of Mathematical Biology 36:249–268. [CrossRef]
79. Frénod E, Sire O. 2009. An explanatory model to validate the way water activity rules periodic terrace generation in Proteus mirabilis swarm. J Math Biol 59:439–466. [PubMed][CrossRef]
80. Xue C, Budrene EO, Othmer HG. 2011. Radial and spiral stream formation in Proteus mirabilis colonies. PLoS Comput Biol 7:e1002332. [PubMed][CrossRef]
81. Belas R, Suvanasuthi R. 2005. The ability of Proteus mirabilis to sense surfaces and regulate virulence gene expression involves FliL, a flagellar basal body protein. J Bacteriol 187:6789–6803. [PubMed][CrossRef]
82. Belas R. 1996. Proteus mirabilis swarmer cell differentiation and urinary tract infection, p 271–298. In Mobley HL, Warren JW (ed), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management. ASM Press, Washington, D.C.
83. Gygi D, Bailey MJ, Allison C, Hughes C. 1995. Requirement for FlhA in flagella assembly and swarm-cell differentiation by Proteus mirabilis. Mol Microbiol 15:761–769. [PubMed][CrossRef]
84. Belas R, Erskine D, Flaherty D. 1991. Proteus mirabilis mutants defective in swarmer cell differentiation and multicellular behavior. J Bacteriol 173:6279–6288. [PubMed]
85. Gygi D, Fraser G, Dufour A, Hughes C. 1997. A motile but non-swarming mutant of Proteus mirabilis lacks FlgN, a facilitator of flagella filament assembly. Mol Microbiol 25:597–604. [PubMed][CrossRef]
86. Allison C, Hughes C. 1991. Closely linked genetic loci required for swarm cell differentiation and multicellular migration by Proteus mirabilis. Mol Microbiol 5:1975–1982. [PubMed][CrossRef]
87. Belas R, Goldman M, Ashliman K. 1995. Genetic analysis of Proteus mirabilis mutants defective in swarmer cell elongation. J Bacteriol 177:823–828. [PubMed]
88. Furness RB, Fraser GM, Hay NA, Hughes C. 1997. Negative feedback from a Proteus class II flagellum export defect to the flhDC master operon controlling cell division and flagellum assembly. J Bacteriol 179:5585–5588. [PubMed]
89. Lee YY, Patellis J, Belas R. 2013. Activity of Proteus mirabilis FliL is viscosity dependent and requires extragenic DNA. J Bacteriol 195:823–832. [PubMed][CrossRef]
90. Cusick K, Lee YY, Youchak B, Belas R. 2012. Perturbation of FliL interferes with Proteus mirabilis swarmer cell gene expression and differentiation. J Bacteriol 194:437–447. [PubMed][CrossRef]
91. Dufour A, Furness RB, Hughes C. 1998. Novel genes that upregulate the Proteus mirabilis flhDC master operon controlling flagellar biogenesis and swarming. Mol Microbiol 29:741–751. [PubMed][CrossRef]
92. Clemmer KM, Rather PN. 2007. Regulation of flhDC expression in Proteus mirabilis. Res Microbiol 158:295–302. [PubMed][CrossRef]
93. Claret L, Hughes C. 2000. Rapid turnover of FlhD and FlhC, the flagellar regulon transcriptional activator proteins, during Proteus swarming. J Bacteriol 182:833–836. [PubMed][CrossRef]
94. Clemmer KM, Rather PN. 2008. The Lon protease regulates swarming motility and virulence gene expression in Proteus mirabilis. J Med Microbiol 57:931–937. [PubMed][CrossRef]
95. Hay NA, Tipper DJ, Gygi D, Hughes C. 1997. A nonswarming mutant of Proteus mirabilis lacks the Lrp global transcriptional regulator. J Bacteriol 179:4741–4746. [PubMed]
96. Lintner RE, Mishra PK, Srivastava P, Martinez-Vaz BM, Khodursky AB, Blumenthal RM. 2008. Limited functional conservation of a global regulator among related bacterial genera: Lrp in Escherichia, Proteus and Vibrio. BMC Microbiol 8:60. [PubMed][CrossRef]
97. Stevenson LG, Rather PN. 2006. A novel gene involved in regulating the flagellar gene cascade in Proteus mirabilis. J Bacteriol 188:7830–7839. [PubMed][CrossRef]
98. Szostek BA, Rather PN. 2013. Regulation of the swarming inhibitor disA in Proteus mirabilis. J Bacteriol 195:3237–3243. [PubMed][CrossRef]
99. Hatt JK, Rather PN. 2008. Characterization of a novel gene, wosA, regulating FlhDC expression in Proteus mirabilis. J Bacteriol 190:1946–1955. [PubMed][CrossRef]
100. Liaw SJ, Lai HC, Ho SW, Luh KT, Wang WB. 2003. Role of RsmA in the regulation of swarming motility and virulence factor expression in Proteus mirabilis. J Med Microbiol 52:19–28. [PubMed][CrossRef]
101. Wei BL, Brun-Zinkernagel AM, Simecka JW, Pruss BM, Babitzke P, Romeo T. 2001. Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40:245–256. [PubMed][CrossRef]
102. Cano DA, Dominguez-Bernal G, Tierrez A, Garcia-Del Portillo F, Casadesus J. 2002. Regulation of capsule synthesis and cell motility in Salmonella enterica by the essential gene igaA. Genetics 162:1513–1523. [PubMed]
103. Morgenstein RM, Rather PN. 2012. Role of the Umo proteins and the Rcs phosphorelay in the swarming motility of the wild type and an O-antigen ( waaL) mutant of Proteus mirabilis. J Bacteriol 194:669–676. [PubMed][CrossRef]
104. Huang YH, Ferrieres L, Clarke DJ. 2006. The role of the Rcs phosphorelay in Enterobacteriaceae. Res Microbiol 157:206–212. [PubMed][CrossRef]
105. Liaw SJ, Lai HC, Ho SW, Luh KT, Wang WB. 2001. Characterisation of p-nitrophenylglycerol-resistant Proteus mirabilis super-swarming mutants. J Med Microbiol 50:1039–1048. [PubMed][CrossRef]
106. Belas R, Schneider R, Melch M. 1998. Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J Bacteriol 180:6126–6139. [PubMed]
107. Liaw SJ, Lai HC, Wang WB. 2004. Modulation of swarming and virulence by fatty acids through the RsbA protein in Proteus mirabilis. Infect Immun 72:6836–6845. [PubMed][CrossRef]
108. Wang WB, Chen IC, Jiang SS, Chen HR, Hsu CY, Hsueh PR, Hsu WB, Liaw SJ. 2008. Role of RppA in the regulation of polymyxin b susceptibility, swarming, and virulence factor expression in Proteus mirabilis. Infect Immun 76:2051–2062. [PubMed][CrossRef]
109. Jiang SS, Liu MC, Teng LJ, Wang WB, Hsueh PR, Liaw SJ. 2010. Proteus mirabilis pmrI, an RppA-regulated gene necessary for polymyxin B resistance, biofilm formation, and urothelial cell invasion. Antimicrob Agents Chemother 54:1564–1571. [PubMed][CrossRef]
110. Kato A, Groisman EA. 2008. The PhoQ/PhoP regulatory network of Salmonella enterica. Adv Exp Med Biol 631:7–21. [PubMed][CrossRef]
111. Jiang SS, Lin TY, Wang WB, Liu MC, Hsueh PR, Liaw SJ. 2010. Characterization of UDP-glucose dehydrogenase and UDP-glucose pyrophosphorylase mutants of Proteus mirabilis: defectiveness in polymyxin B resistance, swarming, and virulence. Antimicrob Agents Chemother 54:2000–2009. [PubMed][CrossRef]
112. McCoy AJ, Liu H, Falla TJ, Gunn JS. 2001. Identification of Proteus mirabilis mutants with increased sensitivity to antimicrobial peptides. Antimicrob Agents Chemother 45:2030–2037. [PubMed][CrossRef]
113. Morgenstein RM, Clemmer KM, Rather PN. 2010. Loss of the waaL O-antigen ligase prevents surface activation of the flagellar gene cascade in Proteus mirabilis. J Bacteriol 192:3213–3221. [PubMed][CrossRef]
114. Allison C, Emody L, Coleman N, Hughes C. 1994. The role of swarm cell differentiation and multicellular migration in the uropathogenicity of Proteus mirabilis. J Infect Dis 169:1155–1158. [PubMed][CrossRef]
115. Hay NA, Tipper DJ, Gygi D, Hughes C. 1999. A novel membrane protein influencing cell shape and multicellular swarming of Proteus mirabilis. J Bacteriol 181:2008–2016. [PubMed]
116. Lai HC, Gygi D, Fraser GM, Hughes C. 1998. A swarming-defective mutant of Proteus mirabilis lacking a putative cation-transporting membrane P-type ATPase. Microbiology 144(Pt 7) :1957–1961. [PubMed][CrossRef]
117. Rensing C, Mitra B, Rosen BP. 1998. A Zn(II)-translocating P-type ATPase from Proteus mirabilis. Biochem Cell Biol 76:787–790. [PubMed][CrossRef]
118. Nielubowicz GR, Smith SN, Mobley HLT. 2010. Zinc uptake contributes to motility and provides a competitive advantage to Proteus mirabilis during experimental urinary tract infection. Infect Immun 78:2823–2833. [PubMed][CrossRef]
119. Gaisser S, Hughes C. 1997. A locus coding for putative non-ribosomal peptide/polyketide synthase functions is mutated in a swarming-defective Proteus mirabilis strain. Mol Gen Genet 253:415–427. [PubMed][CrossRef]
120. Armbruster CE, Hodges SA, Mobley HLT. 2013. Initiation of swarming motility by Proteus mirabilis occurs in response to specific cues present in urine and requires excess L-glutamine. J Bacteriol 195:1305–1319. [PubMed][CrossRef]
121. Sturgill G, Rather PN. 2004. Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol Microbiol 51:437–446. [PubMed][CrossRef]
122. Vinogradov E, Perry MB. 2000. Structural analysis of the core region of lipopolysaccharides from Proteus mirabilis serotypes O6, O48 and O57. Eur J Biochem 267:2439–2446. [PubMed][CrossRef]
123. Sturgill GM, Siddiqui S, Ding X, Pecora ND, Rather PN. 2002. Isolation of lacZ fusions to Proteus mirabilis genes regulated by intercellular signaling: potential role for the sugar phosphotransferase (Pts) system in regulation. FEMS Microbiol Lett 217:43–50. [PubMed][CrossRef]
124. Kurihara S, Sakai Y, Suzuki H, Muth A, Phanstiel Ot, Rather PN. 2013. Putrescine importer PlaP contributes to swarming motility and urothelial cell invasion in Proteus mirabilis. J Biol Chem 288:15668–15676. [PubMed][CrossRef]
125. Rather PN. 2005. Swarmer cell differentiation in Proteus mirabilis. Environ Microbiol 7:1065–1073. [PubMed][CrossRef]
126. Holden MT, Ram Chhabra S, de Nys R, Stead P, Bainton NJ, Hill PJ, Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov M, Salmond GP, Stewart GS, Bycroft BW, Kjelleberg S, Williams P. 1999. Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol Microbiol 33:1254–1266. [PubMed][CrossRef]
127. Campbell J, Lin Q, Geske GD, Blackwell HE. 2009. New and unexpected insights into the modulation of LuxR-type quorum sensing by cyclic dipeptides. ACS Chem Biol 4:1051–1059. [PubMed][CrossRef]
128. Eberl L, Winson MK, Sternberg C, Stewart GS, Christiansen G, Chhabra SR, Bycroft B, Williams P, Molin S, Givskov M. 1996. Involvement of N-acyl-L-hormoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol Microbiol 20:127–136. [PubMed][CrossRef]
129. Stankowska D, Kwinkowski M, Kaca W. 2008. Quantification of Proteus mirabilis virulence factors and modulation by acylated homoserine lactones. J Microbiol Immunol Infect 41:243–253. [PubMed]
130. Schneider R, Lockatell CV, Johnson D, Belas R. 2002. Detection and mutation of a luxS-encoded autoinducer in Proteus mirabilis. Microbiology 148:773–782. [PubMed][CrossRef]
131. Rauprich O, Matsushita M, Weijer CJ, Siegert F, Esipov SE, Shapiro JA. 1996. Periodic phenomena in Proteus mirabilis swarm colony development. J Bacteriol 178:6525–6538. [PubMed]
132. Armitage JP. 1981. Changes in metabolic activity of Proteus mirabilis during swarming. J Gen Microbiol 125:445–450. [PubMed][CrossRef]
133. Falkinham JO, 3rd, Hoffman PS. 1984. Unique developmental characteristics of the swarm and short cells of Proteus vulgaris and Proteus mirabilis. J Bacteriol 158:1037–1040. [PubMed]
134. Alteri CJ, Himpsl SD, Engstrom MD, Mobley HLT. 2012. Anaerobic respiration using a complete oxidative TCA cycle drives multicellular swarming in Proteus mirabilis. mBio 3. [CrossRef]
135. Allison C, Coleman N, Jones PL, Hughes C. 1992. Ability of Proteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation. Infect Immun 60:4740–4746. [PubMed]
136. Peerbooms PG, Verweij AM, MacLaren DM. 1984. Vero cell invasiveness of Proteus mirabilis. Infect Immun 43:1068–1071. [PubMed]
137. Chippendale GR, Warren JW, Trifillis AL, Mobley HLT. 1994. Internalization of Proteus mirabilis by human renal epithelial cells. Infect Immun 62:3115–3121. [PubMed]
138. Oelschlaeger TA, Tall BD. 1996. Uptake pathways of clinical isolates of Proteus mirabilis into human epithelial cell lines. Microb Pathog 21:1–16. [PubMed][CrossRef]
139. Alamuri P, Lower M, Hiss JA, Himpsl SD, Schneider G, Mobley HLT. 2010. Adhesion, invasion, and agglutination mediated by two trimeric autotransporters in the human uropathogen Proteus mirabilis. Infect Immun 78:4882–4894. [PubMed][CrossRef]
140. Mathoera RB, Kok DJ, Verduin CM, Nijman RJ. 2002. Pathological and therapeutic significance of cellular invasion by Proteus mirabilis in an enterocystoplasty infection stone model. Infect Immun 70:7022–7032. [PubMed][CrossRef]
141. Fraser GM, Claret L, Furness R, Gupta S, Hughes C. 2002. Swarming-coupled expression of the Proteus mirabilis hpmBA haemolysin operon. Microbiology 148:2191–2201. [PubMed][CrossRef]
142. Sabbuba N, Hughes G, Stickler DJ. 2002. The migration of Proteus mirabilis and other urinary tract pathogens over Foley catheters. BJU Int 89:55–60. [PubMed][CrossRef]
143. Jansen AM, Lockatell CV, Johnson DE, Mobley HLT. 2003. Visualization of Proteus mirabilis morphotypes in the urinary tract: the elongated swarmer cell is rarely observed in ascending urinary tract infection. Infect Immun 71:3607–3613. [PubMed][CrossRef]
144. Dienes L. 1946. Reproductive processes in Proteus cultures. Proc Soc Exp Biol Med 63:265–270. [PubMed][CrossRef]
145. De Louvois J. 1969. Serotyping and the Dienes reaction on Proteus mirabilis from hospital infections. J Clin Pathol 22:263–268. [PubMed][CrossRef]
146. Pfaller MA, Mujeeb I, Hollis RJ, Jones RN, Doern GV. 2000. Evaluation of the discriminatory powers of the Dienes test and ribotyping as typing methods for Proteus mirabilis. J Clin Microbiol 38:1077–1080. [PubMed]
147. Senior BW, Larsson P. 1983. A highly discriminatory multi-typing scheme for Proteus mirabilis and Proteus vulgaris. J Med Microbiol 16:193–202. [PubMed][CrossRef]
148. Budding AE, Ingham CJ, Bitter W, Vandenbroucke-Grauls CM, Schneeberger PM. 2009. The Dienes phenomenon: competition and territoriality in swarming Proteus mirabilis. J Bacteriol 191:3892–3900. [PubMed][CrossRef]
149. Gibbs KA, Urbanowski ML, Greenberg EP. 2008. Genetic determinants of self identity and social recognition in bacteria. Science 321:256–259. [PubMed][CrossRef]
150. Gibbs KA, Wenren LM, Greenberg EP. 2011. Identity gene expression in Proteus mirabilis. J Bacteriol 193:3286–3292. [PubMed][CrossRef]
151. Silverman JM, Brunet YR, Cascales E, Mougous JD. 2012. Structure and regulation of the type VI secretion system. Annu Rev Microbiol 66:453–472. [PubMed][CrossRef]
152. Jani AJ, Cotter PA. 2010. Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe 8:2–6. [PubMed][CrossRef]
153. Russell AB, Peterson SB, Mougous JD. 2014. Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 12:137–148. [PubMed][CrossRef]
154. Sullivan NL, Septer AN, Fields AT, Wenren LM, Gibbs KA. 2013. The complete genome sequence of Proteus mirabilis strain BB2000 reveals differences from the P. mirabilis reference strain. Genome Announc 1:e00024-13. [PubMed][CrossRef]
155. Wenren LM, Sullivan NL, Cardarelli L, Septer AN, Gibbs KA. 2013. Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. mBio 4. [CrossRef]
156. Alteri CJ, Himpsl SD, Pickens SR, Lindner JR, Zora JS, Miller JE, Arno PD, Straight SW, Mobley HLT. 2013. Multicellular bacteria deploy the type VI secretion system to preemptively strike neighboring cells. PLoS Pathog 9:e1003608. [PubMed][CrossRef]
157. Old DC, Adegbola RA. 1982. Haemagglutinins and fimbriae of Morganella, Proteus and Providencia. J Medl Microbiol 15:551. [PubMed][CrossRef]
158. Wray SK, Hull SI, Cook RG, Barrish J, Hull RA. 1986. Identification and characterization of a uroepithelial cell adhesin from a uropathogenic isolate of Proteus mirabilis. Infect Immun 54:43–49. [PubMed]
159. Bahrani FK, Cook S, Hull RA, Massad G, Mobley HLT. 1993. Proteus mirabilis fimbriae: N-terminal amino acid sequence of a major fimbrial subunit and nucleotide sequences of the genes from two strains. Infect Immun 61:884–891. [PubMed]
160. Welch RA, Burland V, Plunkett G, 3rd, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, Stroud D, Mayhew GF, Rose DJ, Zhou S, Schwartz DC, Perna NT, Mobley HLT, Donnenberg MS, Blattner FR. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99:17020–17024. [PubMed][CrossRef]
161. Nuccio SP, Baumler AJ. 2007. Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71:551–575. [PubMed][CrossRef]
162. Pearson MM, Mobley HLT. 2008. Repression of motility during fimbrial expression: identification of 14 mrpJ gene paralogues in Proteus mirabilis. Mol Microbiol 69:548–558. [PubMed][CrossRef]
163. Li X, Johnson DE, Mobley HLT. 1999. Requirement of MrpH for mannose-resistant Proteus-like fimbria-mediated hemagglutination by Proteus mirabilis. Infect Immun 67:2822–2833. [PubMed]
164. Bahrani FK, Mobley HLT. 1994. Proteus mirabilis MR/P fimbrial operon: genetic organization, nucleotide sequence, and conditions for expression. J Bacteriol 176:3412–3419. [PubMed]
165. Zhao H, Li X, Johnson DE, Blomfield I, Mobley HLT. 1997. In vivo phase variation of MR/P fimbrial gene expression in Proteus mirabilis infecting the urinary tract. Molec Microbiol 23:1009–1019. [PubMed][CrossRef]
166. Lane MC, Li X, Pearson MM, Simms AN, Mobley HLT. 2009. Oxygen-limiting conditions enrich for fimbriate cells of uropathogenic Proteus mirabilis and Escherichia coli. J Bacteriol 191:1382–1392. [PubMed][CrossRef]
167. Li X, Lockatell CV, Johnson DE, Mobley HLT. 2002. Identification of MrpI as the sole recombinase that regulates the phase variation of MR/P fimbria, a bladder colonization factor of uropathogenic Proteus mirabilis. Mol Microbiol 45:865–874. [PubMed][CrossRef]
168. Bahrani FK, Mobley HLT. 1993. Proteus mirabilis MR/P fimbriae: molecular cloning, expression, and nucleotide sequence of the major fimbrial subunit gene. J Bacteriol 175:457–464. [PubMed]
169. Båga M, Norgren M, Normark S. 1987. Biogenesis of E. coli Pap pili: PapH, a minor pilin subunit involved in cell anchoring and length modulation. Cell 49:241–251. [PubMed][CrossRef]
170. Verger D, Miller E, Remaut H, Waksman G, Hultgren S. 2006. Molecular mechanism of P pilus termination in uropathogenic Escherichia coli. EMBO Rep 7:1228–1232. [PubMed][CrossRef]
171. Li X, Mobley HLT. 1998. MrpB functions as the terminator for assembly of Proteus mirabilis mannose-resistant Proteus-like fimbriae. Infect Immun 66:1759–1763. [PubMed]
172. Li X, Zhao H, Geymonat L, Bahrani F, Johnson DE, Mobley HLT. 1997. Proteus mirabilis mannose-resistant, Proteus-like fimbriae: MrpG is located at the fimbrial tip and is required for fimbrial assembly. Infect Immun 65:1327–1334. [PubMed]
173. Kline KA, Falker S, Dahlberg S, Normark S, Henriques-Normark B. 2009. Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5:580–592. [PubMed][CrossRef]
174. Kuehn MJ, Normark S, Hultgren SJ. 1991. Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits. Proc Natl Acad Sci U S A 88:10586–10590. [PubMed][CrossRef]
175. Carnoy C, Moseley SL. 1997. Mutational analysis of receptor binding mediated by the Dr family of Escherichia coli adhesins. Mol Microbiol 23:365–379. [PubMed][CrossRef]
176. Heras B, Shouldice SR, Totsika M, Scanlon MJ, Schembri MA, Martin JL. 2009. DSB proteins and bacterial pathogenicity. Nat Rev Microbiol 7:215–225. [PubMed][CrossRef]
177. Jansen AM, Lockatell V, Johnson DE, Mobley HLT. 2004. Mannose-resistant Proteus-like fimbriae are produced by most Proteus mirabilis strains infecting the urinary tract, dictate the in vivo localization of bacteria, and contribute to biofilm formation. Infect Immun 72:7294–7305. [PubMed][CrossRef]
178. Rocha SP, Elias WP, Cianciarullo AM, Menezes MA, Nara JM, Piazza RM, Silva MR, Moreira CG, Pelayo JS. 2007. Aggregative adherence of uropathogenic Proteus mirabilis to cultured epithelial cells. FEMS Immunol Med Microbiol 51:319–326. [PubMed][CrossRef]
179. Johnson DE, Bahrani FK, Lockatell CV, Drachenberg CB, Hebel JR, Belas R, Warren JW, Mobley HLT. 1999. Serum immunoglobulin response and protection from homologous challenge by Proteus mirabilis in a mouse model of ascending urinary tract infection. Infect Immun 67:6683–6687. [PubMed]
180. Bahrani FK, Massad G, Lockatell CV, Johnson DE, Russell RG, Warren JW, Mobley HLT. 1994. Construction of an MR/P fimbrial mutant of Proteus mirabilis: role in virulence in a mouse model of ascending urinary tract infection. Infect Immun 62:3363–3371. [PubMed]
181. Li X, Johnson DE, Mobley HLT. 1999. Requirement of MrpH for Mannose-Resistant Proteus-Like Fimbria-Mediated Hemagglutination by Proteus mirabilis. Infect Immun 67:2822–2833. [PubMed]
182. Cook SW, Mody N, Valle J, Hull R. 1995. Molecular cloning of Proteus mirabilis uroepithelial cell adherence ( uca) genes. Infect Immun 63:2082–2086. [PubMed]
183. Tolson DL, Barrigar DL, McLean RJ, Altman E. 1995. Expression of a nonagglutinating fimbria by Proteus mirabilis. Infect Immun 63:1127–1129. [PubMed]
184. Pellegrino R, Scavone P, Umpiérrez A, Maskell DJ, Zunino P. 2013. Proteus mirabilis uroepithelial cell adhesin (UCA) fimbria plays a role in the colonization of the urinary tract. Pathog Dis 67:104–107. [PubMed][CrossRef]
185. Kuan L, Schaffer JN, Zouzias CD, Pearson MM. 2014. Characterization of 17 chaperone-usher fimbriae encoded by Proteus mirabilis reveals strong conservation. J Med Microbiol doi:10.1099/jmm.0.069971–0. [CrossRef]
186. Väisänen-Rhen V, Korhonen TK, Finne J. 1983. Novel cell-binding activity specific for N-acetyl-D-glucosamine in an Escherichia coli strain. FEBS Lett 159:233–236. [PubMed][CrossRef]
187. Saarela S, Westerlund-Wikström B, Rhen M, Korhonen TK. 1996. The GafD protein of the G (F17) fimbrial complex confers adhesiveness of Escherichia coli to laminin. Infect Immun 64:2857–2860. [PubMed]
188. Dorofeyev AE, Vasilenko IV, Rassokhina OA. 2009. Joint extraintestinal manifestations in ulcerative colitis. Dig Dis 27:502–510. [PubMed][CrossRef]
189. Lee KK, Harrison BA, Latta R, Altman E. 2000. The binding of Proteus mirabilis nonagglutinating fimbriae to ganglio-series asialoglycolipids and lactosyl ceramide. Can J Microbiol 46:961–966. [PubMed][CrossRef]
190. Ortaldo JR, Sharrow SO, Timonen T, Herberman RB. 1981. Determination of surface antigens on highly purified human NK cells by flow cytometry with monoclonal antibodies. J Immunol 127:2401–2409. [PubMed]
191. Saiman L, Prince A. 1993. Pseudomonas aeruginosa pili bind to asialoGM1 which is increased on the surface of cystic fibrosis epithelial cells. J Clin Invest 92:1875–1880. [PubMed][CrossRef]
192. Zunino P, Sosa V, Allen AG, Preston A, Schlapp G, Maskell DJ. 2003. Proteus mirabilis fimbriae (PMF) are important for both bladder and kidney colonization in mice. Microbiology 149:3231–3237. [PubMed][CrossRef]
193. Massad G, Lockatell CV, Johnson DE, Mobley HLT. 1994. Proteus mirabilis fimbriae: construction of an isogenic pmfA mutant and analysis of virulence in a CBA mouse model of ascending urinary tract infection. Infect Immun 62:536–542. [PubMed]
194. Zunino P, Sosa V, Schlapp G, Allen AG, Preston A, Maskell DJ. 2007. Mannose-resistant Proteus-like and P. mirabilis fimbriae have specific and additive roles in P. mirabilis urinary tract infections. FEMS Immunol Med Microbiol 51:125–133. [PubMed][CrossRef]
195. Massad G, Bahrani FK, Mobley HLT. 1994. Proteus mirabilis fimbriae: identification, isolation, and characterization of a new ambient-temperature fimbria. Infect Immun 62:1989–1994. [PubMed]
196. Massad G, Fulkerson JF, Jr., Watson DC, Mobley HLT. 1996. Proteus mirabilis ambient-temperature fimbriae: cloning and nucleotide sequence of the atf gene cluster. Infect Immun 64:4390–4395. [PubMed]
197. Zunino P, Geymonat L, Allen AG, Legnani-Fajardo C, Maskell DJ. 2000. Virulence of a Proteus mirabilis ATF isogenic mutant is not impaired in a mouse model of ascending urinary tract infection. FEMS Immunol Med Microbiol 29:137–143. [PubMed][CrossRef]
198. Bijlsma IG, van Dijk L, Kusters JG, Gaastra W. 1995. Nucleotide sequences of two fimbrial major subunit genes, pmpA and ucaA, from canine-uropathogenic Proteus mirabilis strains. Microbiology 141(Pt 6) :1349–1357. [PubMed]
199. Spurbeck RR, Stapleton AE, Johnson JR, Walk ST, Hooton TM, Mobley HLT. 2011. Fimbrial profiles predict virulence of uropathogenic Escherichia coli strains: contribution of Ygi and Yad fimbriae. Infect Immun 79:4753–4763. [PubMed][CrossRef]
200. Townsend SM, Kramer NE, Edwards R, Baker S, Hamlin N, Simmonds M, Stevens K, Maloy S, Parkhill J, Dougan G, Bäumler AJ. 2001. Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect Immun 69:2894–2901. [PubMed][CrossRef]
201. Wurpel DJ, Beatson SA, Totsika M, Petty NK, Schembri MA. 2013. Chaperone-usher fimbriae of Escherichia coli. PLoS One 8:e52835. [PubMed][CrossRef]
202. Snyder JA, Haugen BJ, Lockatell CV, Maroncle N, Hagan EC, Johnson DE, Welch RA, Mobley HLT. 2005. Coordinate expression of fimbriae in uropathogenic Escherichia coli. Infect Immun 73:7588–7596. [PubMed][CrossRef]
203. Li X, Rasko DA, Lockatell CV, Johnson DE, Mobley HLT. 2001. Repression of bacterial motility by a novel fimbrial gene product. EMBO J 20:4854–4862. [PubMed][CrossRef]
204. Simms AN, Mobley HLT. 2008. PapX, a P fimbrial operon-encoded inhibitor of motility in uropathogenic Escherichia coli. Infect Immun 76:4833–4841. [PubMed][CrossRef]
205. Reiss DJ, Mobley HLT. 2011. Determination of target sequence bound by PapX, repressor of bacterial motility, in flhD promoter using systematic evolution of ligands by exponential enrichment (SELEX) and high throughput sequencing. J Biol Chem 286:44726–44738. [PubMed][CrossRef]
206. Chen YT, Peng HL, Shia WC, Hsu FR, Ken CF, Tsao YM, Chen CH, Liu CE, Hsieh MF, Chen HC, Tang CY, Ku TH. 2012. Whole-genome sequencing and identification of Morganella morganii KT pathogenicity-related genes. BMC Genomics 13(Suppl 7) :S4. [PubMed][CrossRef]
207. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Molec Biol 215:403. [CrossRef]
208. Meslet-Cladiere LM, Pimenta A, Duchaud E, Holland IB, Blight MA. 2004. In vivo expression of the mannose-resistant fimbriae of Photorhabdus temperata K122 during insect infection. J Bacteriol 186:611–622. [PubMed][CrossRef]
209. Allison SE, Silphaduang U, Mascarenhas M, Konczy P, Quan Q, Karmali M, Coombes BK. 2012. Novel repressor of Escherichia coli O157:H7 motility encoded in the putative fimbrial cluster OI-1. J Bacteriol 194:5343–5352. [PubMed][CrossRef]
210. He H, Snyder HA, Forst S. 2004. Unique organization and regulation of the mrx fimbrial operon in Xenorhabdus nematophila. Microbiology 150:1439–1446. [PubMed][CrossRef]
211. Leyton DL, Rossiter AE, Henderson IR. 2012. From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 10:213–225. [PubMed][CrossRef]
212. Cotter SE, Surana NK, St Geme JW, 3rd. 2005. Trimeric autotransporters: a distinct subfamily of autotransporter proteins. Trends Microbiol 13:199–205. [PubMed][CrossRef]
213. Alamuri P, Mobley HLT. 2008. A novel autotransporter of uropathogenic Proteus mirabilis is both a cytotoxin and an agglutinin. Mol Microbiol 68:997–1017. [PubMed][CrossRef]
214. Flannery EL, Mody L, Mobley HLT. 2009. Identification of a modular pathogenicity island that is widespread among urease-producing uropathogens and shares features with a diverse group of mobile elements. Infect Immun 77:4887–4894. [PubMed][CrossRef]
215. Silverblatt FJ. 1974. Host-parasite interaction in the rat renal pelvis: a possible role for pili in the pathogenesis of pyelonephritis. J Exp Med 140:1696–1711. [PubMed][CrossRef]
216. Hola V, Peroutkova T, Ruzicka F. 2012. Virulence factors in Proteus bacteria from biofilm communities of catheter-associated urinary tract infections. FEMS Immunol Med Microbiol 65:343–349. [PubMed][CrossRef]
217. Mattick JS. 2002. Type IV pili and twitching motility. Annu Rev Microbiol 56:289–314. [PubMed][CrossRef]
218. Uphoff TS, Welch RA. 1990. Nucleotide sequencing of the Proteus mirabilis calcium-independent hemolysin genes ( hpmA and hpmB) reveals sequence similarity with the Serratia marcescens hemolysin genes ( shlA and shlB). J Bacteriol 172:1206. [PubMed]
219. Swihart KG, Welch RA. 1990. Cytotoxic activity of the Proteus hemolysin HpmA. Infect Immun 58:1861–1869. [PubMed]
220. Cestari SE, Ludovico MS, Martins FH, da Rocha SP, Elias WP, Pelayo JS. 2013. Molecular detection of HpmA and HlyA hemolysin of uropathogenic Proteus mirabilis. Curr Microbiol 67:703–707. [PubMed][CrossRef]
221. Weaver TM, Hocking JM, Bailey LJ, Wawrzyn GT, Howard DR, Sikkink LA, Ramirez-Alvarado M, Thompson JR. 2009. Structural and functional studies of truncated hemolysin A from Proteus mirabilis. J Biol Chem 284:22297–22309. [PubMed][CrossRef]
222. Wassif C, Cheek D, Belas R. 1995. Molecular analysis of a metalloprotease from Proteus mirabilis. J Bacteriol 177:5790. [PubMed]
223. Belas R, Manos J, Suvanasuthi R. 2004. Proteus mirabilis ZapA metalloprotease degrades a broad spectrum of substrates, including antimicrobial peptides. Infect Immun 72:5159–5167. [PubMed][CrossRef]
224. Walker KE, Moghaddame-Jafari S, Lockatell CV, Johnson D, Belas R. 1999. ZapA, the IgA-degrading metalloprotease of Proteus mirabilis, is a virulence factor expressed specifically in swarmer cells. Mol Microbiol 32:825–836. [PubMed][CrossRef]
225. Chromek M, Slamova Z, Bergman P, Kovacs L, Podracka L, Ehren I, Hokfelt T, Gudmundsson GH, Gallo RL, Agerberth B, Brauner A. 2006. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med 12:636–641. [PubMed][CrossRef]
226. Ganz T. 2001. Defensins in the urinary tract and other tissues. J Infect Dis 183(Suppl 1) :S41–42. [PubMed][CrossRef]
227. Phan V, Belas R, Gilmore BF, Ceri H. 2008. ZapA, a virulence factor in a rat model of Proteus mirabilis-induced acute and chronic prostatitis. Infect Immun 76:4859–4864. [PubMed][CrossRef]
228. Senior BW, Loomes LM, Kerr MA. 1991. The production and activity in vivo of Proteus mirabilis IgA protease in infections of the urinary tract. J Med Microbiol 35:203–207. [PubMed][CrossRef]
229. Carson L, Cathcart GR, Scott CJ, Hollenberg MD, Walker B, Ceri H, Gilmore BF. 2011. Comprehensive inhibitor profiling of the Proteus mirabilis metalloprotease virulence factor ZapA (mirabilysin). Biochimie 93:1824–1827. [PubMed][CrossRef]
230. Zhao H, Li X, Johnson DE, Mobley HLT. 1999. Identification of protease and rpoN-associated genes of uropathogenic Proteus mirabilis by negative selection in a mouse model of ascending urinary tract infection. Microbiology 145(Pt 1) :185–195. [PubMed][CrossRef]
231. Hood MI, Skaar EP. 2012. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10:525–537. [PubMed][CrossRef]
232. Andrews SC, Robinson AK, Rodriguez-Quiñones F. 2003. Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237. [PubMed][CrossRef]
233. Piccini CD, Barbe FM, Legnani-Fajardo CL. 1998. Identification of iron-regulated outer membrane proteins in uropathogenic Proteus mirabilis and its relationship with heme uptake. FEMS Microbiol Lett 166:243–248. [PubMed][CrossRef]
234. Drechsel H, Thieken A, Reissbrodt R, Jung G, Winkelmann G. 1993. Alpha-keto acids are novel siderophores in the genera Proteus, Providencia, and Morganella and are produced by amino acid deaminases. J Bacteriol 175:2727–2733. [PubMed]
235. Massad G, Zhao H, Mobley HLT. 1995. Proteus mirabilis amino acid deaminase: cloning, nucleotide sequence, and characterization of aad. J Bacteriol 177:5878–5883. [PubMed]
236. Reissbrodt R, Kingsley R, Rabsch W, Beer W, Roberts M, Williams PH. 1997. Iron-regulated excretion of alpha-keto acids by Salmonella typhimurium. J Bacteriol 179:4538–4544. [PubMed]
237. Kingsley R, Rabsch W, Roberts M, Reissbrodt R, Williams PH. 1996. TonB-dependent iron supply in Salmonella by alpha-ketoacids and alpha-hydroxyacids. FEMS Microbiol Lett 140:65–70. [PubMed]
238. Himpsl SD, Pearson MM, Arewang CJ, Nusca TD, Sherman DH, Mobley HLT. 2010. Proteobactin and a yersiniabactin-related siderophore mediate iron acquisition in Proteus mirabilis. Mol Microbiol 78:138–157. [PubMed][CrossRef]
239. Lima A, Zunino P, D’Alessandro B, Piccini C. 2007. An iron-regulated outer-membrane protein of Proteus mirabilis is a haem receptor that plays an important role in urinary tract infection and in in vivo growth. J Med Microbiol 56:1600–1607. [PubMed][CrossRef]
240. Sabri M, Houle S, Dozois CM. 2009. Roles of the extraintestinal pathogenic Escherichia coli ZnuACB and ZupT zinc transporters during urinary tract infection. Infect Immun 77:1155–1164. [PubMed][CrossRef]
241. Jacobsen SM, Lane MC, Harro JM, Shirtliff ME, Mobley HLT. 2008. The high-affinity phosphate transporter Pst is a virulence factor for Proteus mirabilis during complicated urinary tract infection. FEMS Immunol Med Microbiol 52:180–193. [PubMed][CrossRef]
242. O’May GA, Jacobsen SM, Longwell M, Stoodley P, Mobley HL, Shirtliff ME. 2009. The high-affinity phosphate transporter Pst in Proteus mirabilis HI4320 and its importance in biofilm formation. Microbiology 155:1523–1535. [PubMed][CrossRef]
243. Shi X, Zhu Y, Li Y, Jiang M, Lin Y, Qiu Y, Chen Q, Yuan Y, Ni P, Hu Q, Huang S. 2014. Genome sequence of Proteus mirabilis clinical isolate C05028. Genome Announc 2. [CrossRef]
244. Khalid MI, Teh LK, Lee LS, Zakaria ZA, Salleh MZ. 2013. Genome sequence of Proteus mirabilis strain PR03, isolated from a local hospital in Malaysia. Genome Announc 1. [CrossRef]
245. Pearson MM, Mobley HLT. 2007. The type III secretion system of Proteus mirabilis HI4320 does not contribute to virulence in the mouse model of ascending urinary tract infection. J Med Microbiol 56:1277–1283. [PubMed][CrossRef]
246. Lloyd AL, Rasko DA, Mobley HLT. 2007. Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli. J Bacteriol 189:3532–3546. [PubMed][CrossRef]
247. Flannery EL, Antczak SM, Mobley HL. 2011. Self-transmissibility of the integrative and conjugative element ICE Pm1 between clinical isolates requires a functional integrase, relaxase, and type IV secretion system. J Bacteriol 193:4104–4112. [PubMed][CrossRef]
248. Jacobsen SM, Shirtliff ME. 2011. Proteus mirabilis biofilms and catheter-associated urinary tract infections. Virulence 2:460–465. [PubMed][CrossRef]
249. Dumanski AJ, Hedelin H, Edin-Liljegren A, Beauchemin D, McLean RJ. 1994. Unique ability of the Proteus mirabilis capsule to enhance mineral growth in infectious urinary calculi. Infect Immun 62:2998–3003. [PubMed]
250. Holling N, Lednor D, Tsang S, Bissell A, Campbell L, Nzakizwanayo J, Dedi C, Hawthorne JA, Hanlon G, Ogilvie LA, Salvage JP, Patel BA, Barnes LM, Jones BV. 2014. Elucidating the genetic basis of crystalline biofilm formation in Proteus mirabilis. Infect Immun 82:1616–1626. [PubMed][CrossRef]
251. Gupta K, Hooton TM, Naber KG, Wullt B, Colgan R, Miller LG, Moran GJ, Nicolle LE, Raz R, Schaeffer AJ, Soper DE. 2011. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: A 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis 52:e103–120. [PubMed][CrossRef]
252. Ma KL, Wang CX. 2013. Analysis of the spectrum and antibiotic resistance of uropathogens in vitro: Results based on a retrospective study from a tertiary hospital. Am J Infect Control 41:610-601–606.
253. Schito GC, Naber KG, Botto H, Palou J, Mazzei T, Gualco L, Marchese A. 2009. The ARESC study: an international survey on the antimicrobial resistance of pathogens involved in uncomplicated urinary tract infections. Int J Antimicrob Agents 34:407–413. [PubMed][CrossRef]
254. Bichler KH, Eipper E, Naber K, Braun V, Zimmermann R, Lahme S. 2002. Urinary infection stones. Int J Antimicrob Agents 19:488–498. [PubMed][CrossRef]
255. Adamus-Bialek W, Zajac E, Parniewski P, Kaca W. 2013. Comparison of antibiotic resistance patterns in collections of Escherichia coli and Proteus mirabilis uropathogenic strains. Mol Biol Rep 40:3426–3435. [PubMed][CrossRef]
256. Kaca W, Radziejewska-Lebrecht J, Bhat UR. 1990. Effect of polymyxins on the lipopolysaccharide-defective mutants of Proteus mirabilis. Microbios 61:23–32. [PubMed]
257. Li X, Lockatell CV, Johnson DE, Lane MC, Warren JW, Mobley HLT. 2004. Development of an intranasal vaccine to prevent urinary tract infection by Proteus mirabilis. Infect Immun 72:66–75. [PubMed][CrossRef]
258. Brumbaugh AR, Mobley HLT. 2012. Preventing urinary tract infection: progress toward an effective Escherichia coli vaccine. Expert Rev Vaccines 11:663–676. [PubMed][CrossRef]
259. Scavone P, Rial A, Umpierrez A, Chabalgoity A, Zunino P. 2009. Effects of the administration of cholera toxin as a mucosal adjuvant on the immune and protective response induced by Proteus mirabilis MrpA fimbrial protein in the urinary tract. Microbiol Immunol 53:233–240. [PubMed][CrossRef]
260. Jones RJ. 1976. Oral vaccination against Proteus mirabilis. Br J Exp Pathol 57:395–399. [PubMed]
261. Moayeri N, Collins CM, O’Hanley P. 1991. Efficacy of a Proteus mirabilis outer membrane protein vaccine in preventing experimental Proteus pyelonephritis in a BALB/c mouse model. Infect Immun 59:3778–3786. [PubMed]
262. Pellegrino R, Galvalisi U, Scavone P, Sosa V, Zunino P. 2003. Evaluation of Proteus mirabilis structural fimbrial proteins as antigens against urinary tract infections. FEMS Immunol Med Microbiol 36:103–110. [PubMed][CrossRef]
263. Alamuri P, Eaton KA, Himpsl SD, Smith SN, Mobley HLT. 2009. Vaccination with Proteus toxic agglutinin, a hemolysin-independent cytotoxin in vivo, protects against Proteus mirabilis urinary tract infection. Infect Immun 77:632–641. [PubMed][CrossRef]
264. Scavone P, Sosa V, Pellegrino R, Galvalisi U, Zunino P. 2004. Mucosal vaccination of mice with recombinant Proteus mirabilis structural fimbrial proteins. Microbes Infect 6:853–860. [PubMed][CrossRef]
265. Alteri CJ, Hagan EC, Sivick KE, Smith SN, Mobley HLT. 2009. Mucosal immunization with iron receptor antigens protects against urinary tract infection. PLoS Pathog 5:e1000586. [PubMed][CrossRef]
266. Scavone P, Miyoshi A, Rial A, Chabalgoity A, Langella P, Azevedo V, Zunino P. 2007. Intranasal immunisation with recombinant Lactococcus lactis displaying either anchored or secreted forms of Proteus mirabilis MrpA fimbrial protein confers specific immune response and induces a significant reduction of kidney bacterial colonisation in mice. Microbes Infect 9:821–828. [PubMed][CrossRef]
267. Scavone P, Umpierrez A, Maskell DJ, Zunino P. 2011. Nasal immunization with attenuated Salmonella Typhimurium expressing an MrpA-TetC fusion protein significantly reduces Proteus mirabilis colonization in the mouse urinary tract. J Med Microbiol 60:899–904. [PubMed][CrossRef]
268. Siddiq DM, Darouiche RO. 2012. New strategies to prevent catheter-associated urinary tract infections. Nat Rev Urol 9:305–314. [PubMed][CrossRef]
269. Levering V, Wang Q, Shivapooja P, Zhao X, López GP. 2014. Soft Robotic Concepts in Catheter Design: An On-Demand Fouling-Release Urinary Catheter. Adv Healthc Mater 3:1588–1596. [PubMed][CrossRef]
270. Stickler DJ, Jones SM, Adusei GO, Waters MG, Cloete J, Mathur S, Feneley RC. 2006. A clinical assessment of the performance of a sensor to detect crystalline biofilm formation on indwelling bladder catheters. BJU Int 98:1244–1249. [PubMed][CrossRef]
271. Malic S, Waters MG, Basil L, Stickler DJ, Williams DW. 2012. Development of an “early warning” sensor for encrustation of urinary catheters following Proteus infection. J Biomed Mater Res B Appl Biomater 100:133–137. [PubMed][CrossRef]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.UTI-0017-2013
2015-09-18
2019-10-18

Abstract:

is a Gram-negative bacterium and is well known for its ability to robustly swarm across surfaces in a striking bulls’-eye pattern. Clinically, this organism is most frequently a pathogen of the urinary tract, particularly in patients undergoing long-term catheterization. This review covers with a focus on urinary tract infections (UTI), including disease models, vaccine development efforts, and clinical perspectives. Flagella-mediated motility, both swimming and swarming, is a central facet of this organism. The regulation of this complex process and its contribution to virulence is discussed, along with the type VI-secretion system-dependent intra-strain competition, which occurs during swarming. uses a diverse set of virulence factors to access and colonize the host urinary tract, including urease and stone formation, fimbriae and other adhesins, iron and zinc acquisition, proteases and toxins, biofilm formation, and regulation of pathogenesis. While significant advances in this field have been made, challenges remain to combatting complicated UTI and deciphering pathogenesis.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/3/5/UTI-0017-2013.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.UTI-0017-2013&mimeType=html&fmt=ahah

Figures

and Urinary Tract Infections
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-1,properties={foaf_givenname=Jessica N., foaf_name=Jessica N. Schaffer, foaf_surname=Schaffer, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-2,properties={foaf_givenname=Melanie M., foaf_name=Melanie M. Pearson, foaf_surname=Pearson, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-aff2]]}]]
Citation: Schaffer J, Pearson M. 2015. and urinary tract infections. microbiolspec 3(5): doi:10.1128/microbiolspec.UTI-0017-2013
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.fig1
FIGURE 1
in urease-induced bladder stone. , One-quarter bladder of experimentally infected mouse (bar, 500 μm). , Higher magnification of the area indicated in panel A (bar, 100 μm). , Higher magnification of the area indicated in panel B with individual bacteria visible (bar, 5 μm). Modified from ( 32 ), with permission.
microbiolspec/3/5/UTI-0017-2013-fig1_thmb.gif
microbiolspec/3/5/UTI-0017-2013-fig1.gif
Image of FIGURE 1

Click to view

FIGURE 1

in urease-induced bladder stone. , One-quarter bladder of experimentally infected mouse (bar, 500 μm). , Higher magnification of the area indicated in panel A (bar, 100 μm). , Higher magnification of the area indicated in panel B with individual bacteria visible (bar, 5 μm). Modified from ( 32 ), with permission.

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.fig2
FIGURE 2
Adherence and motility genes are inversely regulated during UTI. Each line represents fold-change of a specific flagellar (left panel) or fimbrial (right panel) gene relative to mid-logarithmic phase culture . Genes in the operon are highly induced early during infection, but expression falls by 7 days post infection. Flagellar genes are initially repressed, but expression increases late in infection. Modified from ( 25 ), with permission.
microbiolspec/3/5/UTI-0017-2013-fig2_thmb.gif
microbiolspec/3/5/UTI-0017-2013-fig2.gif
Image of FIGURE 2

Click to view

FIGURE 2

Adherence and motility genes are inversely regulated during UTI. Each line represents fold-change of a specific flagellar (left panel) or fimbrial (right panel) gene relative to mid-logarithmic phase culture . Genes in the operon are highly induced early during infection, but expression falls by 7 days post infection. Flagellar genes are initially repressed, but expression increases late in infection. Modified from ( 25 ), with permission.

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.fig3
FIGURE 3
Swarming colony of .
microbiolspec/3/5/UTI-0017-2013-fig3_thmb.gif
microbiolspec/3/5/UTI-0017-2013-fig3.gif
Image of FIGURE 3

Click to view

FIGURE 3

Swarming colony of .

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.fig4
FIGURE 4
switches between swimming and swarming forms. On the left is a transmission electron micrograph (TEM) of broth-cultured, vegetative cells displaying peritrichous flagella. On the right is a TEM of differentiated swarm cells. Bundles of flagella are visible.
microbiolspec/3/5/UTI-0017-2013-fig4_thmb.gif
microbiolspec/3/5/UTI-0017-2013-fig4.gif
Image of FIGURE 4

Click to view

FIGURE 4

switches between swimming and swarming forms. On the left is a transmission electron micrograph (TEM) of broth-cultured, vegetative cells displaying peritrichous flagella. On the right is a TEM of differentiated swarm cells. Bundles of flagella are visible.

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.fig5
FIGURE 5
swarms across sections of latex catheter. Reproduced from ( 61 ), with permission.
microbiolspec/3/5/UTI-0017-2013-fig5_thmb.gif
microbiolspec/3/5/UTI-0017-2013-fig5.gif
Image of FIGURE 5

Click to view

FIGURE 5

swarms across sections of latex catheter. Reproduced from ( 61 ), with permission.

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.fig6
FIGURE 6
Expression of MR/P fimbriae is phase-variable and induced during UTI. , Immunogold electron microscopy of wild-type HI4320 labeled with gold particles targeting the MrpH tip adhesin. The cell on the left is expressing MR/P fimbriae, and the cell on the right is not (bar, 500 nm). , The amount of MR/P fimbriae present positively correlates with murine bladder colonization. Data were obtained seven days post-inoculation. Modified from ( 166 ), with permission.
microbiolspec/3/5/UTI-0017-2013-fig6_thmb.gif
microbiolspec/3/5/UTI-0017-2013-fig6.gif
Image of FIGURE 6

Click to view

FIGURE 6

Expression of MR/P fimbriae is phase-variable and induced during UTI. , Immunogold electron microscopy of wild-type HI4320 labeled with gold particles targeting the MrpH tip adhesin. The cell on the left is expressing MR/P fimbriae, and the cell on the right is not (bar, 500 nm). , The amount of MR/P fimbriae present positively correlates with murine bladder colonization. Data were obtained seven days post-inoculation. Modified from ( 166 ), with permission.

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.fig7
FIGURE 7
biofilm formation is MR/P-dependent. bacteria expressing GFP were grown on a cover glass in urine for 7 days. The resulting biofilm was imaged with confocal microscopy, and the 30 resulting z-stacks were stitched together to form the sagittal view. Wild-type forms thick, robust biofilms. MR/P L-ON forms dense, but thin, biofilms while MR/P L-OFF forms weak biofilms. Reprinted from ( 177 ), with permission.
microbiolspec/3/5/UTI-0017-2013-fig7_thmb.gif
microbiolspec/3/5/UTI-0017-2013-fig7.gif
Image of FIGURE 7

Click to view

FIGURE 7

biofilm formation is MR/P-dependent. bacteria expressing GFP were grown on a cover glass in urine for 7 days. The resulting biofilm was imaged with confocal microscopy, and the 30 resulting z-stacks were stitched together to form the sagittal view. Wild-type forms thick, robust biofilms. MR/P L-ON forms dense, but thin, biofilms while MR/P L-OFF forms weak biofilms. Reprinted from ( 177 ), with permission.

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.fig8
FIGURE 8
Overexpression of and its paralogs results in distinct phenotypes. , Swarming assays of with an empty vector or expressing or an paralog. , Gram-stained bacteria from the edge of the swarm front (bar, 50 μm). Modified from ( 162 ), with permission.
microbiolspec/3/5/UTI-0017-2013-fig8_thmb.gif
microbiolspec/3/5/UTI-0017-2013-fig8.gif
Image of FIGURE 8

Click to view

FIGURE 8

Overexpression of and its paralogs results in distinct phenotypes. , Swarming assays of with an empty vector or expressing or an paralog. , Gram-stained bacteria from the edge of the swarm front (bar, 50 μm). Modified from ( 162 ), with permission.

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.fig9
FIGURE 9
iron chelation is Nrp and proteobactin dependent. , agar; and , solution chrome azurol S (CAS) assays of uropathogenic CFT073 and HI4320; a color change from blue to orange indicates iron chelation. In , supernatants from log-phase cultures grown in MOPS defined media either with 0.1 mM FeCl·6HO (black bars) or without supplementation (white bars) were concentrated 50-fold before being used in a liquid CAS assay ( supernatants were not concentrated). Single and mutants are not impaired in iron chelation, but the double mutant is. Reprinted from ( 238 ), with permission.
microbiolspec/3/5/UTI-0017-2013-fig9_thmb.gif
microbiolspec/3/5/UTI-0017-2013-fig9.gif
Image of FIGURE 9

Click to view

FIGURE 9

iron chelation is Nrp and proteobactin dependent. , agar; and , solution chrome azurol S (CAS) assays of uropathogenic CFT073 and HI4320; a color change from blue to orange indicates iron chelation. In , supernatants from log-phase cultures grown in MOPS defined media either with 0.1 mM FeCl·6HO (black bars) or without supplementation (white bars) were concentrated 50-fold before being used in a liquid CAS assay ( supernatants were not concentrated). Single and mutants are not impaired in iron chelation, but the double mutant is. Reprinted from ( 238 ), with permission.

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

and Urinary Tract Infections
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-1,properties={foaf_givenname=Jessica N., foaf_name=Jessica N. Schaffer, foaf_surname=Schaffer, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-2,properties={foaf_givenname=Melanie M., foaf_name=Melanie M. Pearson, foaf_surname=Pearson, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.UTI-0017-2013-aff2]]}]]
Citation: Schaffer J, Pearson M. 2015. and urinary tract infections. microbiolspec 3(5): doi:10.1128/microbiolspec.UTI-0017-2013
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.T1
TABLE 1
Genes that contribute to swarming in
Generic image for table

Click to view

TABLE 1

Genes that contribute to swarming in

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.T2
TABLE 2
The fimbriae of . The name, genomic location, Greek classification, determination of virulence, and MrpJ homolog of each fimbrial operon in
Generic image for table

Click to view

TABLE 2

The fimbriae of . The name, genomic location, Greek classification, determination of virulence, and MrpJ homolog of each fimbrial operon in

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013
/content/microbiolspec/10.1128/microbiolspec.UTI-0017-2013.T3
TABLE 3
Iron-related genes in . Iron-related genes from were identified by homology to other iron-related genes. Genes identified as iron-related by homology but not identified using one of the four conditions shown were excluded. A checkmark indicates that one or more of the genes in the row were identified using the condition specified
Generic image for table

Click to view

TABLE 3

Iron-related genes in . Iron-related genes from were identified by homology to other iron-related genes. Genes identified as iron-related by homology but not identified using one of the four conditions shown were excluded. A checkmark indicates that one or more of the genes in the row were identified using the condition specified

Source: microbiolspec September 2015 vol. 3 no. 5 doi:10.1128/microbiolspec.UTI-0017-2013

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error