1887

Chapter 11 : Bacterial Metabolism in the Host Environment: Pathogen Growth and Nutrient Assimilation in the Mammalian Upper Respiratory Tract

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Bacterial Metabolism in the Host Environment: Pathogen Growth and Nutrient Assimilation in the Mammalian Upper Respiratory Tract, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818883/9781555818869_Chap11-1.gif /docserver/preview/fulltext/10.1128/9781555818883/9781555818869_Chap11-2.gif

Abstract:

Pathogens evolve in specific host niches and microenvironments that provide the physical and nutritional requirements conducive to their growth. In addition to using the host as a source of food, bacterial pathogens must avoid the immune response to their presence. The mammalian upper respiratory tract is a site that is exposed to the external environment, and is readily colonized by bacteria that live as resident flora or as pathogens. These bacteria can remain localized, descend to the lower respiratory tract, or traverse the epithelium to disseminate throughout the body. By virtue of their successful colonization of the respiratory epithelium, these bacteria obtain the nutrients needed for growth, either directly from host resources or from other microbes. This chapter describes the upper respiratory tract environment, including its tissue and mucosal structure, prokaryotic biota, and biochemical composition that would support microbial life. and the species are discussed as examples of bacteria that have no known external reservoirs but have evolved to obligately colonize the mammalian upper respiratory tract.

Citation: Armstrong S. 2015. Bacterial Metabolism in the Host Environment: Pathogen Growth and Nutrient Assimilation in the Mammalian Upper Respiratory Tract, p 211-261. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0007-2014
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Diagram showing regions of the human upper respiratory tract.

Citation: Armstrong S. 2015. Bacterial Metabolism in the Host Environment: Pathogen Growth and Nutrient Assimilation in the Mammalian Upper Respiratory Tract, p 211-261. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0007-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818883.chap11
1. Fahy JV,, Dickey BF . 2010. Airway mucus function and dysfunction. N Engl J Med 363 : 2233 2247.[PubMed] [CrossRef]
2. Sahin-Yilmaz A,, Naclerio RM . 2011. Anatomy and physiology of the upper airway. Proc Am Thorac Soc 8 : 31 39.[PubMed] [CrossRef]
3. Holt PG,, Strickland DH,, Wikstrom ME,, Jahnsen FL . 2008. Regulation of immunological homeostasis in the respiratory tract. Nat Rev Immunol 8 : 142 152.[PubMed] [CrossRef]
4. Cauley LS,, Lefrançois L . 2013. Guarding the perimeter: protection of the mucosa by tissue-resident memory T cells. Mucosal Immunol 6 : 14 23.[PubMed] [CrossRef]
5. Kim DY,, Sato A,, Fukuyama S,, Sagara H,, Nagatake T,, Kong IG,, Goda K,, Nochi T,, Kunisawa J,, Sato S,, Yokota Y,, Lee CH,, Kiyono H . 2011. The airway antigen sampling system: respiratory M cells as an alternative gateway for inhaled antigens. J Immunol 186 : 4253 4262.[PubMed] [CrossRef]
6. Serikov VB,, Choi H,, Chmiel KJ,, Wu R,, Widdicombe JH . 2004. Activation of extracellular regulated kinases is required for the increase in airway epithelial permeability during leukocyte transmigration. Am J Respir Cell Mol Biol 30 : 261 270.[PubMed] [CrossRef]
7. Persson CG,, Erjefalt JS,, Greiff L,, Andersson M,, Erjefält I,, Godfrey RW,, Korsgren M,, Linden M,, Sundler F,, Svensson C . 1998. Plasma-derived proteins in airway defence, disease and repair of epithelial injury. Eur Respir J 11 : 958 970.[PubMed] [CrossRef]
8. Knowles MR,, Boucher RC . 2002. Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 109 : 571 577.[PubMed] [CrossRef]
9. Rubin BK . 2002. Physiology of airway mucus clearance. Respir Care 47 : 761 768.[PubMed]
10. Evans CM,, Koo JS . 2009. Airway mucus: the good, the bad, the sticky. Pharmacol Ther 121 : 332 348.[PubMed] [CrossRef]
11. Ali MS,, Pearson JP . 2007. Upper airway mucin gene expression: a review. Laryngoscope 117 : 932 938.[PubMed] [CrossRef]
12. Davis CW,, Dickey BF . 2008. Regulated airway goblet cell mucin secretion. Annu Rev Physiol 70 : 487 512.[PubMed] [CrossRef]
13. Cone RA . 2009. Barrier properties of mucus. Adv Drug Deliv Rev 61 : 75 85.[PubMed] [CrossRef]
14. Button B,, Cai LH,, Ehre C,, Kesimer M,, Hill DB,, Sheehan JK,, Boucher RC,, Rubinstein M . 2012. A periciliary brush promotes the lung health by separating the mucus layer from airway epithelia. Science 337 : 937 941.[PubMed] [CrossRef]
15. Frank DN,, Feazel LM,, Bessesen MT,, Price CS,, Janoff EN,, Pace NR . 2010. The human nasal microbiota and Staphylococcus aureus carriage. PLoS ONE 5 : e10598. doi:10.1371/journal.pone.0010598. [PubMed] [CrossRef]
16. Lemon KP,, Klepac-Ceraj V,, Schiffer HK,, Brodie EL,, Lynch SV,, Kolter R . 2010. Comparative analyses of the bacterial microbiota of the human nostril and oropharynx. mBio 1( 3) : e00129-10. doi:10.1128/mBio.00129-10. [PubMed] [CrossRef]
17. Pettigrew MM,, Laufer AS,, Gent JF,, Kong Y,, Fennie KP,, Metlay JP . 2012. Upper respiratory tract microbial communities, acute otitis media pathogens, and antibiotic use in healthy and sick children. Appl Environ Microbiol 78 : 6262 6270.[PubMed] [CrossRef]
18. Hilty M,, Burke C,, Pedro H,, Cardenas P,, Bush A,, Bossley C,, Davies J,, Ervine A,, Poulter L,, Pachter L,, Moffatt MF,, Cookson WOC . 2010. Disordered microbial communities in asthmatic airways. PLoS ONE 5 : e8578. doi:10.1371/journal.pone.0008578. [PubMed] [CrossRef]
19. Charlson ES,, Bittinger K,, Haas AR,, Fitzgerald AS,, Frank I,, Yadav A,, Bushman FD,, Collman RG . 2011. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 184 : 957 963.[PubMed] [CrossRef]
20. Huang YJ,, Nelson CE,, Brodie EL,, DeSantis TZ,, Baek MS,, Liu J,, Woyke T,, Allgaier M,, Bristow J,, Wiener-Kronish JP,, Sutherland ER,, King TS,, Icitovic N,, Martin RJ,, Calhoun WJ,, Castro M,, Denlinger LC,, Dimango E,, Kraft M,, Peters SP,, Wasserman SI,, Wechsler ME,, Boushey HA,, Lynch SV ; National Heart, Lung, and Blood Institute’s Asthma Clinical Research Network . 2011. Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. J Allergy Clin Immunol 127 : 372 381.[PubMed] [CrossRef]
21. Sze MA,, Dimitriu PA,, Hayashi S,, Elliott WM,, McDonough JE,, Gosselink JV,, Cooper J,, Sin DD,, Mohn WW,, Hogg JC . 2012. The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 185 : 1073 1080.[PubMed] [CrossRef]
22. Yan M,, Pamp SJ,, Fukuyama J,, Hwang PH,, Cho DY,, Holmes S,, Relman DA . 2013. Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe 14 : 631 640.[PubMed] [CrossRef]
23. Thjötta T,, Avery OT . 1921. Studies on bacterial nutrition: II. Growth accessory substances in the cultivation of hemophilic bacilli. J Exp Med 34 : 97 114.[PubMed] [CrossRef]
24. Thjötta T,, Avery OT . 1921. Studies on bacterial nutrition: III. Plant tissue, as a source of growth accessory substances, in the cultivation of Bacillus influenzae . J Exp Med 34 : 455 466.[PubMed] [CrossRef]
25. Evans NM,, Smith DD . 1972. The effect of the medium and source of growth factors on the satellitism test for Haemophilus species. J Med Microbiol 5 : 509 514.[PubMed] [CrossRef]
26. Dinges MM,, Orwin PM,, Schlievert PM . 2000. Exotoxins of Staphylococcus aureus . Clin Microbiol Rev 13 : 16 34.[PubMed] [CrossRef]
27. Vandenesch F,, Lina G,, Henry T . 2012. Staphylococcus aureus hemolysins, bi-component leukocidins, and cytolytic peptides: a redundant arsenal of membrane-damaging virulence factors? Front Cell Infect Microbiol 2 : 12. doi:10.3389/fcimb.2012.00012. [CrossRef]
28. Cole JN,, Barnett TC,, Nizet V,, Walker MJ . 2011. Molecular insight into invasive group A streptococcal disease. Nat Rev Microbiol 9 : 724 736.[PubMed] [CrossRef]
29. Spaulding AR,, Salgado-Pabón W,, Kohler PL,, Horswill AR,, Leung DY,, Schlievert PM . 2013. Staphylococcal and streptococcal superantigen exotoxins. Clin Microbiol Rev 26 : 422 447.[PubMed] [CrossRef]
30. Cole AM,, Dewan P,, Ganz T . 1999. Innate antimicrobial activity of nasal secretions. Infect Immun 67 : 3267 3275.[PubMed]
31. Ganz T . 2003. Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3 : 710 720.[PubMed] [CrossRef]
32. Ganz T . 2004. Antimicrobial polypeptides. J Leukoc Biol 75 : 34 38.[PubMed] [CrossRef]
33. Hong JH,, Lee WC,, Hsu YM,, Liang HJ,, Wan CH,, Chien CL,, Lin CY . 2014. Characterization of the biochemical effects of naphthalene on the mouse respiratory system using NMR-based metabolomics. J Appl Toxicol 34 : 1379 1388.[PubMed] [CrossRef]
34. Grahl N,, Puttikamonkul S,, Macdonald JM,, Gamcsik MP,, Ngo LY,, Hohl TM,, Cramer RA . 2011. In vivo hypoxia and a fungal alcohol dehydrogenase influence the pathogenesis of invasive pulmonary aspergillosis. PLoS Pathog 7 : e1002145. doi:101371/journal.ppat.1002145.
35. Hu JZ,, Rommereim DN,, Minard KR,, Woodstock A,, Harrer BJ,, Wind RA,, Phipps RP,, Sime PJ . 2008. Metabolomics in lung inflammation: a high-resolution (1) h NMR study of mice exposed to silica dust. Toxicol Mech Methods 18 : 385 398.[PubMed] [CrossRef]
36. Evans CR,, Karnovsky A,, Kovach MA,, Standiford TJ,, Burant CF,, Stringer KA . 2014. Untargeted LC-MS metabolomics of bronchoalveolar lavage fluid differentiates acute respiratory distress syndrome from health. J Proteome Res 13 : 640 649.[PubMed] [CrossRef]
37. Rai RK,, Azim A,, Sinha N,, Sahoo JN,, Singh C,, Ahmed A,, Saigal S,, Baronia AK,, Gupta D,, Gurjar M,, Poddar B,, Singh RK . 2013. Metabolic profiling in human lung injuries by high-resolution nuclear magnetic resonance spectroscopy of bronchoalveolar lavage fluid (BALF). Metabolomics 9 : 667 676.[CrossRef]
38. Schock BC,, Koostra J,, Kwack S,, Hackman RM,, van der Vliet A,, Cross CE . 2004. Ascorbic acid in nasal and tracheobronchial airway lining fluids. Free Radic Biol Med 37 : 1393 1401.[PubMed] [CrossRef]
39. Gould NS,, Min E,, Gauthier S,, Martin RJ,, Day BJ . 2011. Lung glutathione adaptive responses to cigarette smoke exposure. Respir Res 12 : 133. [PubMed] [CrossRef]
40. Lankford CE . 1973. Bacterial assimilation of iron. Crit Rev Microbiol 2 : 273 331.[CrossRef]
41. Neilands JB . 1981. Iron absorption and transport in microorganisms. Annu Rev Nutr 1 : 27 46.[PubMed] [CrossRef]
42. Ratledge C,, Dover LG . 2000. Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54 : 881 941.[PubMed] [CrossRef]
43. Hentze MW,, Muckenthaler MU,, Andrews NC . 2004. Balancing acts: molecular control of mammalian iron metabolism. Cell 117 : 285 297.[PubMed] [CrossRef]
44. Andrews NC . 2008. Forging a field: the golden age of iron biology. Blood 112 : 219 230.[PubMed] [CrossRef]
45. Ganz T,, Nemeth E . 2012. Hepcidin and iron homeostasis. Biochim Biophys Acta 1823 : 1434 1443.[PubMed] [CrossRef]
46. Alexander DB,, Iigo M,, Yamauchi K,, Suzui M,, Tsuda H . 2012. Lactoferrin: an alternative view of its role in human biological fluids. Biochem Cell Biol 90 : 279 306.[PubMed] [CrossRef]
47. Hantke K . 1981. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet 182 : 288 292.[PubMed] [CrossRef]
48. Mahan MJ,, Heithoff DM,, Sinsheimer RL,, Low DA . 2000. Assessment of bacterial pathogenesis by analysis of gene expression in the host. Annu Rev Genet 34 : 139 164.[PubMed] [CrossRef]
49. Murphy JR,, Michel JL,, Teng M . 1978. Evidence that the regulation of diphtheria toxin production is directed at the level of transcription. J Bacteriol 135 : 511 516.[PubMed]
50. Grant C,, Vasil ML . 1986. Analysis of transcription of the exotoxin A gene of Pseudomonas aeruginosa . J Bacteriol 168 : 1112 1119.[PubMed]
51. Neilands JB . 1995. Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270 : 26723 26726.[PubMed] [CrossRef]
52. Budzikiewicz H,, Bössenkamp A,, Taraz K,, Pandey A,, Meyer JM . 1997. Corynebactin, a cyclic catecholate siderophore from Corynebacterium glutamicum ATCC 14067 ( Brevibacterium sp DSM 20411). Z Naturforsch C 52 : 551 554.
53. Zajdowicz S,, Haller JC,, Krafft AE,, Hunsucker SW,, Mant CT,, Duncan MW,, Hodges RS,, Jones DN,, Holmes RK . 2012. Purification and structural characterization of siderophore (corynebactin) from Corynebacterium diphtheriae . PLoS ONE 7 : e34591. doi:10.1371/journal.pone.0034591. [PubMed] [CrossRef]
54. Moelling C,, Oberschlacke R,, Ward P,, Karijolich J,, Borisova K,, Bjelos N,, Bergeron L . 2007. Metal-dependent repression of siderophore and biofilm formation in Actinomyces naeslundii . FEMS Microbiol Lett 275 : 214 220.[PubMed] [CrossRef]
55. Beasley FC,, Marolda CL,, Cheung J,, Buac S,, Heinrichs DE . 2011. Staphylococcus aureus transporters Hts, Sir, and Sst capture iron liberated from human transferrin by Staphyloferrin A, Staphyloferrin B, and catecholamine stress hormones, respectively, and contribute to virulence. Infect Immun 79 : 2345 2355.[PubMed] [CrossRef]
56. Cox CD,, Rinehart KL,, Moore ML,, Cook JC Jr . 1981. Pyochelin: novel structure of an iron-chelating growth promoter for Pseudomonas aeruginosa . Proc Natl Acad Sci U S A 78 : 4256 4260.[PubMed] [CrossRef]
57. Cox CD,, Adams P . 1985. Siderophore activity of pyoverdin for Pseudomonas aeruginosa . Infect Immun 48 : 130 138.[PubMed]
58. Beall B,, Sanden GN . 1995. A Bordetella pertussis fepA homologue required for utilization of exogenous ferric enterobactin. Microbiology 141( Pt 12) : 3193 3205.[PubMed] [CrossRef]
59. Yancey RJ,, Finkelstein RA . 1981. Assimilation of iron by pathogenic Neisseria spp. Infect Immun 32 : 600 608.[PubMed]
60. Dyer DW,, West EP,, McKenna W,, Thompson SA,, Sparling PF . 1988. A pleiotropic iron-uptake mutant of Neisseria meningitidis lacks a 70-kilodalton iron-regulated protein. Infect Immun 56 : 977 983.[PubMed]
61. Williams P,, Morton DJ,, Towner KJ,, Stevenson P,, Griffiths E . 1990. Utilization of enterobactin and other exogenous iron sources by Haemophilus influenzae, H. parainfluenzae and H. paraphrophilus . J Gen Microbiol 136 : 2343 2350.[PubMed] [CrossRef]
62. Genco CA,, Dixon DW . 2001. Emerging strategies in microbial haem capture. Mol Microbiol 39 : 1 11.[PubMed] [CrossRef]
63. Hantke K . 1987. Ferrous iron transport mutants in Escherichia coli K12. FEMS Microbiol Lett 44 : 53 57.[CrossRef]
64. Andrews SC,, Robinson AK,, Rodríguez-Quiñones F . 2003. Bacterial iron homeostasis. FEMS Microbiol Rev 27 : 215 237.[PubMed] [CrossRef]
65. Freestone PP,, Sandrini SM,, Haigh RD,, Lyte M . 2008. Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol 16 : 55 64.[PubMed] [CrossRef]
66. Lyte M . 2004. Microbial endocrinology and infectious disease in the 21st century. Trends Microbiol 12 : 14 20.[PubMed] [CrossRef]
67. Burton CL,, Chhabra SR,, Swift S,, Baldwin TJ,, Withers H,, Hill SJ,, Williams P . 2002. The growth response of Escherichia coli to neurotransmitters and related catecholamine drugs requires a functional enterobactin biosynthesis and uptake system. Infect Immun 70 : 5913 5923.[PubMed] [CrossRef]
68. Freestone PP,, Haigh RD,, Williams PH,, Lyte M . 2003. Involvement of enterobactin in norepinephrine-mediated iron supply from transferrin to enterohaemorrhagic Escherichia coli . FEMS Microbiol Lett 222 : 39 43.[PubMed] [CrossRef]
69. Sandrini SM,, Shergill R,, Woodward J,, Muralikuttan R,, Haigh RD,, Lyte M,, Freestone PP . 2010. Elucidation of the mechanism by which catecholamine stress hormones liberate iron from the innate immune defense proteins transferrin and lactoferrin. J Bacteriol 192 : 587 594.[PubMed] [CrossRef]
70. Armstrong SK,, Brickman TJ,, Suhadolc RJ . 2012. Involvement of multiple distinct Bordetella receptor proteins in the utilization of iron liberated from transferrin by host catecholamine stress hormones. Mol Microbiol 84 : 446 462.[PubMed] [CrossRef]
71. Zeng X,, Xu F,, Lin J . 2009. Molecular, antigenic, and functional characteristics of ferric enterobactin receptor CfrA in Campylobacter jejuni . Infect Immun 77 : 5437 5448.[PubMed] [CrossRef]
72. Barnes PJ . 2001. Neurogenic inflammation in the airways. Respir Physiol 125 : 145 154.[PubMed] [CrossRef]
73. Cavallotti C,, Bruzzone P,, Tonnarini G,, Cavallotti D . 2004. Distribution of catecholaminergic neurotransmitters and related receptors in human bronchus-associated lymphoid tissue. Respiration 71 : 635 640.[PubMed] [CrossRef]
74. Lucero MT,, Squires A . 1998. Catecholamine concentrations in rat nasal mucus are modulated by trigeminal stimulation of the nasal cavity. Brain Res 807 : 234 236.[PubMed] [CrossRef]
75. Flower DR,, North AC,, Sansom CE . 2000. The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta 1482 : 9 24.[PubMed] [CrossRef]
76. Kjeldsen L,, Cowland JB,, Borregaard N . 2000. Human neutrophil gelatinase-associated lipocalin and homologous proteins in rat and mouse. Biochim Biophys Acta 1482 : 272 283.[PubMed] [CrossRef]
77. Dittrich AM,, Meyer HA,, Hamelmann E . 2013. The role of lipocalins in airway disease. Clin Exp Allergy 43 : 503 511.[PubMed] [CrossRef]
78. Fluckinger M,, Haas H,, Merschak P,, Glasgow BJ,, Redl B . 2004. Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores. Antimicrob Agents Chemother 48 : 3367 3372.[PubMed] [CrossRef]
79. Goetz DH,, Holmes MA,, Borregaard N,, Bluhm ME,, Raymond KN,, Strong RK . 2002. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 10 : 1033 1043.[PubMed] [CrossRef]
80. Miethke M,, Skerra A . 2010. Neutrophil gelatinase-associated lipocalin expresses antimicrobial activity by interfering with L-norepinephrine-mediated bacterial iron acquisition. Antimicrob Agents Chemother 54 : 1580 1589.[PubMed] [CrossRef]
81. Bao G,, Clifton M,, Hoette TM,, Mori K,, Deng SX,, Qiu A,, Viltard M,, Williams D,, Paragas N,, Leete T,, Kulkarni R,, Li X,, Lee B,, Kalandadze A,, Ratner AJ,, Pizarro JC,, Schmidt-Ott KM,, Landry DW,, Raymond KN,, Strong RK,, Barasch J . 2010. Iron traffics in circulation bound to a siderocalin (Ngal)-catechol complex. Nat Chem Biol 6 : 602 609.[PubMed] [CrossRef]
82. Devireddy LR,, Hart DO,, Goetz DH,, Green MR . 2010. A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. Cell 141 : 1006 1017.[PubMed] [CrossRef]
83. Liu Z,, Ciocea A,, Devireddy L . 2014. Endogenous siderophore 2,5-dihydroxybenzoic acid deficiency promotes anemia and splenic iron overload in mice. Mol Cell Biol 34 : 2533 2546.[PubMed] [CrossRef]
84. Nelson AL,, Barasch JM,, Bunte RM,, Weiser JN . 2005. Bacterial colonization of nasal mucosa induces expression of siderocalin, an iron-sequestering component of innate immunity. Cell Microbiol 7 : 1404 1417.[PubMed] [CrossRef]
85. Chan YR,, Liu JS,, Pociask DA,, Zheng M,, Mietzner TA,, Berger T,, Mak TW,, Clifton MC,, Strong RK,, Ray P,, Kolls JK . 2009. Lipocalin 2 Is required for pulmonary host defense against Klebsiella infection. J Immunol 182 : 4947 4956.[PubMed] [CrossRef]
86. Stein DC, . 2006. The Genus Neisseria , p 602 647. In Dworkin M,, Falkow S,, Rosenberg E,, Schleifer KH,, Stackebrandt E (eds), The Prokaryotes: vol. 5: Proteobacteria: alpha and beta subclasses. Springer-Verlag, Berlin/Heidelberg.
87. Stephens DS . 2007. Conquering the meningococcus. FEMS Microbiol Rev 31 : 3 14.[PubMed] [CrossRef]
88. Hill DJ,, Griffiths NJ,, Borodina E,, Virji M . 2010. Cellular and molecular biology of Neisseria meningitidis colonization and invasive disease. Clin Sci 118 : 547 564.[PubMed]
89. Trivedi K,, Tang CM,, Exley RM . 2011. Mechanisms of meningococcal colonisation. Trends Microbiol 19 : 456 463.[PubMed] [CrossRef]
90. Cornelissen CN,, Sparling PF, . 2004. Neisseria , p 256 272. In Crosa JH,, Mey AR,, Payne SM (eds), Iron transport in bacteria. ASM Press, Washington, DC. [CrossRef]
91. Hobbs MM,, Seiler A,, Achtman M,, Cannon JG . 1994. Microevolution within a clonal population of pathogenic bacteria: recombination, gene duplication and horizontal genetic exchange in the opa gene family of Neisseria meningitidis . Mol Microbiol 12 : 171 180.[PubMed] [CrossRef]
92. Jerse AE,, Cohen MS,, Drown PM,, Whicker LG,, Isbey SF,, Seifert HS,, Cannon JG . 1994. Multiple gonococcal opacity proteins are expressed during experimental urethral infection in the male. J Exp Med 179 : 911 920.[PubMed] [CrossRef]
93. Rayner CF,, Dewar A,, Moxon ER,, Virji M,, Wilson R . 1995. The effect of variations in the expression of pili on the interaction of Neisseria meningitidis with human nasopharyngeal epithelium. J Infect Dis 171 : 113 121.[PubMed] [CrossRef]
94. Chamot-Rooke J,, Mikaty G,, Malosse C,, Soyer M,, Dumont A,, Gault J,, Imhaus AF,, Martin P,, Trellet M,, Clary G,, Chafey P,, Camoin L,, Nilges M,, Nassif X,, Duménil G . 2011. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331 : 778 782.[PubMed] [CrossRef]
95. Jennings MP,, Hood DW,, Peak IR,, Virgi M,, Moxon ER . 1995. Molecular analysis of a locus for the biosynthesis and phase-variable expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis . Mol Microbiol 18 : 729 740.[PubMed] [CrossRef]
96. Lewis LA,, Gipson M,, Hartman K,, Ownbey T,, Vaughn J,, Dyer DW . 1999. Phase variation of HpuAB and HmbR, two distinct haemoglobin receptors of Neisseria meningitidis DNM2. Mol Microbiol 32 : 977 989.[PubMed] [CrossRef]
97. Pujol C,, Eugène E,, de Saint Martin L,, Nassif X . 1997. Interaction of Neisseria meningitidis with a polarized monolayer of epithelial cells. Infect Immun 65 : 4836 4842.[PubMed]
98. Exley RM,, Goodwin L,, Mowe E,, Shaw J,, Smith H,, Read RC,, Tang CM . 2005. Neisseria meningitidis lactate permease is required for nasopharyngeal colonization. Infect Immun 73 : 5762 5766.[PubMed] [CrossRef]
99. Virji M,, Makepeace K,, Ferguson DJ,, Achtman M,, Moxon ER . 1993. Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol Microbiol 10 : 499 510.[PubMed] [CrossRef]
100. Rudel T,, Scheurerpflug I,, Meyer TF . 1995. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373 : 357 359.[PubMed] [CrossRef]
101. Deghmane AE,, Giorgini D,, Larribe M,, Alonso JM,, Taha MK . 2002. Down-regulation of pili and capsule of Neisseria meningitidis upon contact with epithelial cells is mediated by CrgA regulatory protein. Mol Microbiol 43 : 1555 1564.[PubMed] [CrossRef]
102. Ieva R,, Alaimo C,, Delany I,, Spohn G,, Rappuoli R,, Scarlato V . 2005. CrgA is an inducible LysR-type regulator of Neisseria meningitidis, acting both as a repressor and as an activator of gene transcription. J Bacteriol 187 : 3421 3430.[PubMed] [CrossRef]
103. Jamet A,, Rousseau C,, Monfort JB,, Frapy E,, Nassif X,, Martin P . 2009. A two-component system is required for colonization of host cells by meningococcus. Microbiology 155 : 2288 2295.[PubMed] [CrossRef]
104. Johnson CR,, Newcombe J,, Thorne S,, Borde HA,, Eales-Reynolds LJ,, Gorringe AR,, Funnell SG,, McFadden JJ . 2001. Generation and characterization of a PhoP homologue mutant of Neisseria meningitidis . Mol Microbiol 39 : 1345 1355.[PubMed] [CrossRef]
105. Hey A,, Li MS,, Hudson MJ,, Langford PR,, Kroll JS . 2013. Transcriptional profiling of Neisseria meningitidis interacting with human epithelial cells in a long-term in vitro colonization model. Infect Immun 81 : 4149 4159.[PubMed] [CrossRef]
106. Madico G,, Welsch JA,, Lewis LA,, McNaughton A,, Perlman DH,, Costello CE,, Ngampasutadol J,, Vogel U,, Granoff DM,, Ram S . 2006. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J Immunol 177 : 501 510.[PubMed] [CrossRef]
107. Comanducci M,, Bambini S,, Brunelli B,, Adu-Bobie J,, Aricò B,, Capecchi B,, Giuliani MM,, Masignani V,, Santini L,, Savino S,, Granoff DM,, Caugant DA,, Pizza M,, Rappuoli R,, Mora M . 2002. NadA, a novel vaccine candidate of Neisseria meningitidis . J Exp Med 195 : 1445 1454.[PubMed] [CrossRef]
108. Oldfield NJ,, Bland SJ,, Taraktsoglou M,, Dos Ramos FJ,, Robinson K,, Wooldridge KG,, Ala’Aldeen DA . 2007. T-cell stimulating protein A (TspA) of Neisseria meningitidis is required for optimal adhesion to human cells. Cell Microbiol 9 : 463 478.[PubMed] [CrossRef]
109. Sjölinder H,, Eriksson J,, Maudsdotter L,, Aro H,, Jonsson AB . 2008. Meningococcal outer membrane protein NhhA is essential for colonization and disease by preventing phagocytosis and complement attack. Infect Immun 76 : 5412 5420.[PubMed] [CrossRef]
110. Talà A,, Progida C,, De Stefano M,, Cogli L,, Spinosa MR,, Bucci C,, Alifano P . 2008. The HrpB-HrpA two-partner secretion system is essential for intracellular survival of Neisseria meningitidis . Cell Microbiol 10 : 2461 2482.[PubMed] [CrossRef]
111. Plaut AG,, Gilbert JV,, Artenstein MS,, Capra JD . 1975. Neisseria gonorrhoeae and Neisseria meningitidis: extracellular enzyme cleaves human immunoglobulin A. Science 190 : 1103 1105.[PubMed] [CrossRef]
112. Ayala P,, Lin L,, Hopper S,, Fukuda M,, So M . 1998. Infection of epithelial cells by pathogenic Neisseriae reduces the levels of multiple lysosomal constituents. Infect Immun 66 : 5001 5007.[PubMed]
113. Neil RB,, Apicella MA . 2009. Clinical and laboratory evidence for Neisseria meningitidis biofilms. Future Microbiol 4 : 555 563.[PubMed] [CrossRef]
114. Sim RJ,, Harrison MM,, Moxon ER,, Tang CM . 2000. Underestimation of meningococci in tonsillar tissue by nasopharyngeal swabbing. Lancet 356 : 1653 1654.[PubMed] [CrossRef]
115. Yi K,, Rasmussen AW,, Gudlavalleti SK,, Stephens DS,, Stojiljkovic I . 2004. Biofilm formation by Neisseria meningitidis . Infect Immun 72 : 6132 6138.[PubMed] [CrossRef]
116. Lappann M,, Vogel U . 2010. Biofilm formation by the human pathogen Neisseria meningitidis . Med Microbiol Immunol 199 : 173 183.[PubMed] [CrossRef]
117. Leighton MP,, Kelly DJ,, Williamson MP,, Shaw JG . 2001. An NMR and enzyme study of the carbon metabolism of Neisseria meningitidis . Microbiology 147 : 1473 1482.[PubMed]
118. Exley RM,, Shaw J,, Mowe E,, Sun YH,, West NP,, Williamson M,, Botto M,, Smith H,, Tang CM . 2005. Available carbon source influences the resistance of Neisseria meningitidis against complement. J Exp Med 201 : 1637 1645.[PubMed] [CrossRef]
119. Erwin AL,, Gotschlich EC . 1993. Oxidation of D-lactate and L-lactate by Neisseria meningitidis: purification and cloning of meningococcal D-lactate dehydrogenase. J Bacteriol 175 : 6382 6391.[PubMed]
120. KEGG: Kyoto Encyclopedia of Genes and Genomes . (http://www.genome.jp/kegg/).
121. Pagliarulo C,, Salvatore P,, De Vitis LR,, Colicchio R,, Monaco C,, Tredici M,, Talà A,, Bardaro M,, Lavitola A,, Bruni CB,, Alifano P . 2004. Regulation and differential expression of gdhA encoding NADP-specific glutamate dehydrogenase in Neisseria meningitidis clinical isolates. Mol Microbiol 51 : 1757 1772.[PubMed] [CrossRef]
122. Talà A,, Monaco C,, Nagorska K,, Exley RM,, Corbett A,, Zychlinsky A,, Alifano P,, Tang CM . 2011. Glutamate utilization promotes meningococcal survival in vivo through avoidance of the neutrophil oxidative burst. Mol Microbiol 81 : 1330 1342.[PubMed] [CrossRef]
123. Knapp JS,, Clark VL . 1984. Anaerobic growth of Neisseria gonorrhoeae coupled to nitrite reduction. Infect Immun 46 : 176 181.[PubMed]
124. Moir JW . 2011. A snapshot of a pathogenic bacterium mid-evolution: Neisseria meningitidis is becoming a nitric oxide-tolerant aerobe. Biochem Soc Trans 39 : 1890 1894.[PubMed] [CrossRef]
125. Norrod P,, Morse SA . 1979. Absence of superoxide dismutase in some strains of Neisseria gonorrhoeae . Biochem Biophys Res Com 90 : 1287 1294.[PubMed] [CrossRef]
126. Wilks KE,, Dunn KL,, Farrant JL,, Reddin KM,, Gorringe AR,, Langford PR,, Kroll JS . 1998. Periplasmic superoxide dismutase in meningococcal pathogenicity. Infect Immun 66 : 213 217.[PubMed]
127. Archibald FS,, Duong MN . 1986. Superoxide dismutase and oxygen toxicity defenses in the genus Neisseria . Infect Immun 51 : 631 641.[PubMed]
128. Moore TD,, Sparling PF . 1995. Isolation and identification of a glutathione peroxidase homolog gene, gpxA, present in Neisseria meningitidis but absent in Neisseria gonorrhoeae . Infect Immun 63 : 1603 1607.[PubMed]
129. Tettelin H,, Saunders NJ,, Heidelberg J,, Jeffries AC,, Nelson KE,, Eisen JA,, Ketchum KA,, Hood DW,, Peden JF,, Dodson RJ,, Nelson WC,, Gwinn ML,, DeBoy R,, Peterson JD,, Hickey EK,, Haft DH,, Salzberg SL,, White O,, Fleischmann RD,, Dougherty BA,, Mason T,, Ciecko A,, Parksey DS,, Blair E,, Cittone H,, Clark EB,, Cotton MD,, Utterback TR,, Khouri H,, Qin H,, Vamathevan J,, GILL J,, Scarlato V,, Masignani V,, Pizza M,, Grandi G,, Sun L,, Smith HO,, Fraser CM,, Moxon ER,, Rappuoli R,, Venter JC . 2000. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287 : 1809 1815.[PubMed] [CrossRef]
130. Seib KL,, Tseng H-J,, McEwan AG,, Apicella MA,, Jennings MP . 2004. Defenses against oxidative stress in Neisseria gonorrhoeae and Neisseria meningitidis: distinctive systems for different lifestyles. J Infect Dis 190 : 136 147.[PubMed] [CrossRef]
131. Le Faou A . 1984. Sulphur nutrition and metabolism in various species of Neisseria . Ann Microbiol (Paris) 135B : 3 11.[PubMed] [CrossRef]
132. Iwanicka-Nowicka R,, Zielak A,, Cook AM,, Thomas MS,, Hryniewicz MM . 2007. Regulation of sulfur assimilation pathways in Burkholderia cenocepacia: identification of transcription factors CysB and SsuR and their role in control of target genes. J Bacteriol 189 : 1675 1688.[PubMed] [CrossRef]
133. Tinsley CR,, Manjula BN,, Gotschlich EC . 1993. Purification and characterization of polyphosphate kinase from Neisseria meningitidis . Infect Immun 61 : 3703 3710.[PubMed]
134. Zhang Q,, Li Y,, Tang CM . 2010. The role of the exopolyphosphatase PPX in avoidance by Neisseria meningitidis of complement-mediated killing. J Biol Chem 285 : 34259 34268.[PubMed] [CrossRef]
135. Stork M,, Bos MP,, Jongerius I,, de Kok N,, Schilders I,, Weynants VE,, Poolman JT,, Tommassen J . 2010. An outer membrane receptor of Neisseria meningitidis involved in zinc acquisition with vaccine potential. PLoS Pathog 6 : e1000969. doi:10.1371/journal.ppat.1000969. [PubMed] [CrossRef]
136. Perkins-Balding D,, Ratliff-Griffin M,, Stojiljkovic I . 2004. Iron transport systems in Neisseria meningitidis . Microbiol Mol Biol Rev 68 : 154 171.[PubMed] [CrossRef]
137. Schryvers AB,, Morris LJ . 1988. Identification and characterization of the human lactoferrin-binding protein from Neisseria meningitidis . Infect Immun 56 : 1144 1149.[PubMed]
138. Tsai J,, Dyer DW,, Sparling PF . 1988. Loss of transferrin receptor activity in Neisseria meningitidis correlates with inability to use transferrin as an iron source. Infect Immun 56 : 3132 3138.[PubMed]
139. Noinaj N,, Easley NC,, Oke M,, Mizuno N,, Gumbart J,, Boura E,, Steere AN,, Zak O,, Aisen P,, Tajkhorshid E,, Evans RW,, Gorringe AR,, Mason AB,, Steven AC,, Buchanan SK . 2012. Structural basis for iron piracy by pathogenic Neisseria . Nature 483 : 53 58.[PubMed] [CrossRef]
140. Noinaj N,, Cornelissen CN,, Buchanan SK . 2013. Structural insight into the lactoferrin receptors from pathogenic Neisseria . J Struct Biol 184 : 83 92.[PubMed] [CrossRef]
141. Postle K,, Larsen RA . 2007. TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20 : 453 465.[PubMed] [CrossRef]
142. Adhikari P,, Berish SA,, Nowalk AJ,, Veraldi KL,, Morse SA,, Mietzner TA . 1996. The fbpABC locus of Neisseria gonorrhoeae functions in the periplasm-to-cytosol transport of iron. J Bacteriol 178 : 2145 2149.[PubMed]
143. Morgenthau A,, Beddek A,, Schryvers AB . 2014. The negatively charged regions of lactoferrin binding protein B, an adaptation against anti-microbial peptides. PLoS ONE 9 : e86243. doi:10.1371/journal.pone.0086243. [PubMed]
144. Cornelissen CN,, Kelley M,, Hobbs MM,, Anderson JE,, Cannon JG,, Cohen MS,, Sparling PF . 1998. The transferrin receptor expressed by gonococcal strain FA1090 is required for the experimental infection of human male volunteers. Mol Microbiol 27 : 611 616.[PubMed] [CrossRef]
145. Anderson JE,, Hobbs MM,, Biswas GD,, Sparling PF . 2003. Opposing selective forces for expression of the gonococcal lactoferrin receptor. Mol Microbiol 48 : 1325 1337.[PubMed] [CrossRef]
146. Vanderpool CK,, Armstrong SK . 2001. The Bordetella bhu locus is required for heme iron utilization. J Bacteriol 183 : 4278 4287.[PubMed] [CrossRef]
147. Thompson EA,, Feavers IM,, Maiden MC . 2003. Antigenic diversity of meningococcal enterobactin receptor FetA, a vaccine component. Microbiology 149 : 1849 1858.[PubMed] [CrossRef]
148. Marsh JW,, O’Leary MM,, Shutt KA,, Harrison LH . 2007. Deletion of fetA gene sequences in serogroup B and C Neisseria meningitidis isolates. J Clin Microbiol 45 : 1333 1335.[PubMed] [CrossRef]
149. Yu C,, Genco CA . 2012. Fur-mediated global regulatory circuits in pathogenic Neisseria species. J Bacteriol 194 : 6372 6381.[PubMed] [CrossRef]
150. Massé E,, Gottesman S . 2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli . Proc Natl Acad Sci U S A 99 : 4620 4625.[PubMed] [CrossRef]
151. Mellin JR,, Goswami S,, Grogan S,, Tjaden B,, Genco CA . 2007. A novel fur-and iron-regulated small RNA, NrrF, is required for indirect fur-mediated regulation of the sdhA and sdhC genes in Neisseria meningitidis . J Bacteriol 189 : 3686 3694.[PubMed] [CrossRef]
152. Jordan PW,, Saunders NJ . 2009. Host iron binding proteins acting as niche indicators for Neisseria meningitidis . PLoS ONE 4 : e5198. doi:10.1371/journal.pone.0005198. [PubMed] [CrossRef]
153. Mattoo S,, Cherry JD . 2005. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev 18 : 326 382.[PubMed] [CrossRef]
154. Melvin JA,, Scheller EV,, Miller JF,, Cotter PA . 2014. Bordetella pertussis pathogenesis: current and future challenges. Nat Rev Microbiol 12 : 274 288.[PubMed] [CrossRef]
155. Parkhill J,, Sebaihia M,, Preston A,, Murphy LD,, Thomson N,, Harris DE,, Holden MT,, Churcher CM,, Bentley SD,, Mungall KL,, Cerdeño-Tárraga AM,, Temple L,, James K,, Harris B,, Quail MA,, Achtman M,, Atkin R,, Baker S,, Basham D,, Bason N,, Cherevach I,, Chillingworth T,, Collins M,, Cronin A,, Davis P,, Doggett J,, Feltwell T,, Goble A,, Hamlin N,, Hauser H,, Holroyd S,, Jagels K,, Leather S,, Moule S,, Norberczak H,, O’Neil S,, Ormond D,, Price C,, Rabbinowitsch E,, Rutter S,, Sanders M,, Saunders D,, Seeger K,, Sharp S,, Simmonds M,, Skelton J,, Squares R,, Squares S,, Stevens K,, Unwin L,, Whitehead S,, Barrell BG,, Maskell DJ . 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica . Nat Genet 35 : 32 40.[PubMed] [CrossRef]
156. Katada T,, Tamura M,, Ui M . 1983. The A protomer of islet-activating protein, pertussis toxin, as an active peptide catalyzing ADP-ribosylation of a membrane protein. Arch Biochem Biophys 224 : 290 298.[PubMed] [CrossRef]
157. Carbonetti NH . 2010. Pertussis toxin and adenylate cyclase toxin: key virulence factors of Bordetella pertussis and cell biology tools. Future Microbiol 5 : 455 469.[PubMed] [CrossRef]
158. Hewlett E,, Wolff J . 1976. Soluble adenylate cyclase from the culture medium of Bordetella pertussis: purification and characterization. J Bacteriol 127 : 890 898.[PubMed]
159. Eby JC,, Gray MC,, Warfel JM,, Paddock CD,, Jones TF,, Day SR,, Bowden J,, Poulter MD,, Donato GM,, Merkel TJ,, Hewlett EL . 2013. Quantification of the adenylate cyclase toxin of Bordetella pertussis in vitro and during respiratory infection. Infect Immun 81 : 1390 1398.[PubMed] [CrossRef]
160. Horiguchi Y,, Senda T,, Sugimoto N,, Katahira J,, Matsuda M . 1995. Bordetella bronchiseptica dermonecrotizing toxin stimulates assembly of actin stress fibers and focal adhesions by modifying the small GTP-binding protein rho. J Cell Sci 108 : 3243 3251.[PubMed]
161. Stockbauer KE,, Foreman-Wykert AK,, Miller JF . 2003. Bordetella type III secretion induces caspase 1-independent necrosis. Cell Microbiol 5 : 123 132.[PubMed] [CrossRef]
162. Yuk MH,, Harvill ET,, Miller JF . 1998. The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica . Mol Microbiol 28 : 945 959.[PubMed] [CrossRef]
163. Nicholson TL,, Brockmeier SL,, Loving CL,, Register KB,, Kehrli ME Jr,, Shore SM . 2014. The Bordetella bronchiseptica type III secretion system Is required for persistence and disease severity but not transmission in swine. Infect Immun 82 : 1092 1103.[PubMed] [CrossRef]
164. Flak TA,, Goldman WE . 1999. Signalling and cellular specificity of airway nitric oxide production in pertussis. Cell Microbiol 1 : 51 60.[PubMed] [CrossRef]
165. Woodhams KL,, Chan JM,, Lenz JD,, Hackett KT,, Dillard JP . 2013. Peptidoglycan fragment release from Neisseria meningitidis . Infect Immun 81 : 3490 3498.[PubMed] [CrossRef]
166. Koropatnick TA,, Engle JT,, Apicella MA,, Stabb EV,, Goldman WE,, McFall-Ngai MJ . 2004. Microbial factor-mediated development in a host-bacterial mutualism. Science 306 : 1186 1188.[PubMed] [CrossRef]
167. Weiss AA,, Hewlett EL,, Myers GA,, Falkow S . 1983. Tn 5-induced mutations affecting virulence factors of Bordetella pertussis . Infect Immun 42 : 33 41.[PubMed]
168. Aricó B,, Miller JF,, Roy C,, Stibitz S,, Monack D,, Falkow S,, Gross R,, Rappuoli R . 1989. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc Nat Acad Sci U S A 86 : 6671 6675.[PubMed] [CrossRef]
169. Cotter PA,, Jones AM . 2003. Phosphorelay control of virulence gene expression in Bordetella . Trends Microbiol 11 : 367 373.[PubMed] [CrossRef]
170. Lacey BW . 1960. Antigenic modulation of Bordetella pertussis . J Hyg 58 : 57 93.[PubMed] [CrossRef]
171. Pusztai Z,, Joó I . 1967. Influence of nicotinic acid on the antigenic structure of Bordetella pertussis . Ann Immunol Hung 10 : 63 67.
172. Miller JF,, Johnson SA,, Black WJ,, Beattie DT,, Mekalanos JJ,, Falkow S . 1992. Constitutive sensory transduction mutations in the Bordetella pertussis bvgS gene. J Bacteriol 174 : 970 979.[PubMed]
173. Cotter PA,, Miller JF . 1994. BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect Immun 62 : 3381 3390.[PubMed]
174. Martinez de Tejada G,, Cotter PA,, Heininger U,, Camilli A,, Akerley BJ,, Mekalanos JJ,, Miller JF . 1998. Neither the Bvg- phase nor the vrg6 locus of Bordetella pertussis is required for respiratory infection in mice. Infect Immun 66 : 2762 2768.[PubMed]
175. Nicholson TL,, Brockmeier SL,, Loving CL,, Register KB,, Kehrli ME Jr,, Stibitz SE,, Shore SM . 2012. Phenotypic modulation of the virulent Bvg phase is not required for pathogenesis and transmission of Bordetella bronchiseptica in swine. Infect Immun 80 : 1025 1036.[PubMed] [CrossRef]
176. Mason E,, Henderson MW,, Scheller EV,, Byrd MS,, Cotter PA . 2013. Evidence for phenotypic bistability resulting from transcriptional interference of bvgAS in Bordetella bronchiseptica . Mol Microbiol 90 : 716 733.[PubMed] [CrossRef]
177. Weyrich LS,, Feaga HA,, Park J,, Muse SJ,, Safi CY,, Rolin OY,, Young SE,, Harvill ET . 2014. Resident microbiota affect Bordetella pertussis infectious dose and host specificity. J Infect Dis 209 : 913 921.[PubMed] [CrossRef]
178. Mallory FB,, Hornor AA . 1912. Pertussis: the histological lesion in the respiratory tract. J Med Res 27 : 115 1243.[PubMed]
179. Edwards JA,, Groathouse NA,, Boitano S . 2005. Bordetella bronchiseptica adherence to cilia is mediated by multiple adhesin factors and blocked by surfactant protein A. Infect Immun 73 : 3618 3626.[PubMed] [CrossRef]
180. Paddock CD,, Sanden GN,, Cherry JD,, Gal AA,, Langston C,, Tatti KM,, Wu KH,, Goldsmith CS,, Greer PW,, Montague JL,, Eliason MT,, Holman RC,, Guarner J,, Shieh WJ,, Zaki SR . 2008. Pathology and pathogenesis of fatal Bordetella pertussis infection in infants. Clin Infect Dis 47 : 328 338.[PubMed] [CrossRef]
181. Anderton TL,, Maskell DJ,, Preston A . 2004. Ciliostasis is a key early event during colonization of canine tracheal tissue by Bordetella bronchiseptica . Microbiology 150 : 2843 2855.[PubMed] [CrossRef]
182. Belcher CE,, Drenkow J,, Kehoe B,, Gingeras TR,, McNamara N,, Lemjabbar H,, Basbaum C,, Relman DA . 2000. The transcriptional responses of respiratory epithelial cells to Bordetella pertussis reveal host defensive and pathogen counter-defensive strategies. Proc Natl Acad Sci U S A 97 : 13847 13852.[PubMed] [CrossRef]
183. Warfel JM,, Beren J,, Kelly VK,, Lee G,, Merkel TJ . 2012. Nonhuman primate model of pertussis. Infect Immun 80 : 1530 1536.[PubMed] [CrossRef]
184. Geuijen CA,, Willems RJ,, Bongaerts M,, Top J,, Gielen H,, Mooi FR . 1997. Role of the Bordetella pertussis minor fimbrial subunit, FimD, in colonization of the mouse respiratory tract. Infect Immun 65 : 4222 4228.[PubMed]
185. Mattoo S,, Miller JF,, Cotter PA . 2000. Role of Bordetella bronchiseptica fimbriae in tracheal colonization and development of a humoral immune response. Infect Immun 68 : 2024 2033.[PubMed] [CrossRef]
186. Mazar J,, Cotter PA . 2006. Topology and maturation of filamentous haemagglutinin suggest a new model for two-partner secretion. Mol Microbiol 62 : 641 654.[PubMed] [CrossRef]
187. Julio SM,, Inatsuka CS,, Mazar J,, Dieterich C,, Relman DA,, Cotter PA . 2009. Natural-host animal models indicate functional interchangeability between the filamentous haemagglutinins of Bordetella pertussis and Bordetella bronchiseptica and reveal a role for the mature C-terminal domain, but not the RGD motif, during infection. Mol Microbiol 71 : 1574 1590.[PubMed] [CrossRef]
188. Nicholson TL,, Brockmeier SL,, Loving CL . 2009. Contribution of Bordetella bronchiseptica filamentous hemagglutinin and pertactin to respiratory disease in swine. Infect Immun 77 : 2136 2146.[PubMed] [CrossRef]
189. Henderson MW,, Inatsuka CS,, Sheets AJ,, Williams CL,, Benaron DJ,, Donato GM,, Gray MC,, Hewlett EL,, Cotter PA . 2012. Contribution of Bordetella filamentous hemagglutinin and adenylate cyclase toxin to suppression and evasion of interleukin-17-mediated inflammation. Infect Immun 80 : 2061 2075.[PubMed] [CrossRef]
190. Irie Y,, Mattoo S,, Yuk MH . 2004. The Bvg virulence control system regulates biofilm formation in Bordetella bronchiseptica . J Bacteriol 186 : 5692 5698.[PubMed] [CrossRef]
191. Sloan GP,, Love CF,, Sukumar N,, Mishra M,, Deora R . 2007. The Bordetella Bps polysaccharide is critical for biofilm development in the mouse respiratory tract. J Bacteriol 189 : 8270 8276.[PubMed] [CrossRef]
192. Conover MS,, Mishra M,, Deora R . 2011. Extracellular DNA is essential for maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS ONE 6 : e16861. doi:10.1371/journal.pone.0016861. [PubMed] [CrossRef]
193. Conover MS,, Sloan GP,, Love CF,, Sukumar N,, Deora R . 2010. The Bps polysaccharide of Bordetella pertussis promotes colonization and biofilm formation in the nose by functioning as an adhesin. Mol Microbiol 77 : 1439 1455.[PubMed] [CrossRef]
194. Ganguly T,, Johnson JB,, Kock ND,, Parks GD,, Deora R . 2014. The Bordetella pertussis Bps polysaccharide enhances lung colonization by conferring protection from complement-mediated killing. Cell Microbiol 16 : 1105 1118.[PubMed] [CrossRef]
195. Fernandez RC,, Weiss AA . 1994. Cloning and sequencing of a Bordetella pertussis serum resistance locus. Infect Immun 62 : 4727 4738.[PubMed]
196. Marr N,, Shah NR,, Lee R,, Kim EJ,, Fernandez RC . 2011. Bordetella pertussis autotransporter Vag8 binds human C1 esterase inhibitor and confers serum resistance. PLoS ONE 6 : e20585. doi:10.1371/journal/pone.0020585. [PubMed]
197. Nicholson TL,, Conover MS,, Deora R . 2012. Transcriptome profiling reveals stage-specific production and requirement of flagella during biofilm development in Bordetella bronchiseptica . PLoS ONE 7 : e49166. doi:10:1371/journal.pone.0049166.
198. Sugisaki K,, Hanawa T,, Yonezawa H,, Osaki T,, Fukutomi T,, Kawakami