Chapter 34 : Bacterial Strategies for Survival in the Host

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

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Bacterial Strategies for Survival in the Host, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816872/9781555815141_Chap34-1.gif /docserver/preview/fulltext/10.1128/9781555816872/9781555815141_Chap34-2.gif


This chapter focuses on the strategies that persistent bacterial pathogens use to evade, subvert, and disarm the host immune system. Bacteria can avoid these host defense mechanisms by presenting the immune system with a continuously evolving antigen repertoire. Two related processes, antigenic variation and phase variation, generate molecular variants that escape antibody detection. The widespread human pathogen has evolved stress resistance mechanisms that allow it to persist within the phagolysosome of activated macrophages. Bacterial biofilms are now recognized as the cause of many persistent infections that are refractory to antibiotic treatment. Some biofilm infections are associated with surfaces of medical devices such as catheters, shunts, prostheses, and mechanical heart valves. IL-10 is a potent anti-inflammatory and immunesuppressive cytokine that affects antigen presenting cells and T cells. For some bacterial pathogens, persistence in the host depends on the production of protein toxins that interfere with cellular physiology. Intoxication of antigen-presenting cells by CyaA may promote the expansion of regulatory T-cell populations and suppress immunity.

Citation: Tischler A, McKinney J. 2011. Bacterial Strategies for Survival in the Host, p 425-440. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch34

Key Concept Ranking

Immune System Proteins
Complement System
Bacterial Proteins
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Replication dynamics of transient and persistent bacterial pathogens in animal infection models. The transient pathogen (gray line) rapidly replicates to high bacterial titers in the mouse gastrointestinal tract, but the infection is quickly resolved by the adaptive immune response. The immune response also generates immunologic memory that largely prevents replication upon secondary reinfection (gray dashed line). The persistent pathogen (black line) also replicates to high bacterial loads in the lungs of infected mice, but these bacteria persist despite inducing a robust immune response. In addition, this immune response does not generate effective protective memory, such that infected mice can be superinfected upon secondary exposure to (black dashed line).

Citation: Tischler A, McKinney J. 2011. Bacterial Strategies for Survival in the Host, p 425-440. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch34
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Mechanisms of antigenic and phase variation pilus expression. (A) Antigenic variation. Nonreciprocal recombination of variant pilin sequences from silent cassettes to the expressed locus generates variant PilE pilin subunits. sequences are not expressed because they lack the coding sequence and promoter of but they can replace, either in whole or in part, the sequence at to yield mosaic PilE variants that escape recognition by specific host antibodies. (B) Phase variation. Slipped-strand mispairing occurs during DNA replication at a poly-guanosine (poly-G) tract near the end of the gene, which encodes a minor pilin subunit that is required for pilus assembly. This changes the number of G residues and alters the translational reading frame such that downstream sequences are either in or out of frame for translation. Strains of that have switched PilC to the “off” phase do not express pili on their surface and therefore escape detection by pilin-specific antibodies.

Citation: Tischler A, McKinney J. 2011. Bacterial Strategies for Survival in the Host, p 425-440. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch34
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

complement inhibitors. expresses several factors that prevent opsonization by C3b. The staphylococcal complement inhibitors (SCINs) bind to and stabilize C3 convertases to block their activity and prevent C3b deposition. Efb and Ehp bind directly to C3 to interfere with C3 cleavage. The secreted protein Sbi indirectly blocks C3b deposition on the surface by cleaving C3 in the fluid phase. also recruits host proteases that degrade surface associated C3b: clumping factor A (ClfA) recruits host factor I (fI) that cleaves C3b to C3d, and staphylokinase (SK) recruits host plasminogen and activates it to the protease plasmin that degrades C3b. interferes with signaling between complement proteins and cells of the immune system. prevents neutrophil migration to the site of infection by blocking neutrophil detection of C5a, a chemoattractant released upon complement activation. CHIPS (chemotaxis inhibitory protein of binds and antagonizes the neutrophil C5a receptor. The C3 binding proteins Efb and Ehp also interfere with communication between the complement system and B cells by blocking the interaction between C3d and complement receptor 2 (CR2).

Citation: Tischler A, McKinney J. 2011. Bacterial Strategies for Survival in the Host, p 425-440. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch34
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

Antimicrobial factors in the macrophage phagolysosome and resistance mechanisms. In the maturing phagosome, bacteria encounter reactive oxygen species (ROS) synthesized by the NADPH phagocyte oxidase (NOX2); reactive nitrogen species (RNS) synthesized by the inducible nitric oxide synthase (iNOS); acidic pH resulting from the action of vacuolar ATPase (V-ATPase) proton pumps; and cationic antimicrobial peptides (CAMPs). resists ROS and RNS using various detoxification enzymes (described in the text) including degradation of hydrogen peroxide (HO) by the catalase/peroxidase KatG. repairs oxidative and nitrosative damage to DNA by the nucleotide excision repair pathway (UvrB) and uses the proteasome to degrade proteins damaged by oxidation. The complex cell wall serves as a permeability barrier to the influx of protons and the membrane-associated protease Rv367 lc maintains cytoplasmic pH homeostasis during growth in the acidified phagolysosome. resists the action of CAMPs by lysinylation of the membrane lipid phosphatidyl glycerol (PG).

Citation: Tischler A, McKinney J. 2011. Bacterial Strategies for Survival in the Host, p 425-440. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch34
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Algood, H. M. S., and, T. L. Cover. 2006. Helicobacter pylori persistence: an overview of interactions between H. pylori and host immune defenses. Clin. Microbiol. Rev. 19:597613.
2. Alonso, S.,, K. Pethe,, D. G. Russell, and, G. E. Purdy. 2007. Lysosomal killing of Mycobacterium tuberculosis mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc, Natl. Acad. Sci. USA 104:60316036.
3. Anderson,, G. G.,, J. J. Palermo,, J. D. Schilling,, R. Roth,, J. Heuser, and, S. J. Hultgren. 2003. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301:105107.
4. Anderson,, G. G.,, K. W. Dodson,, T. M. Hooton, and, S. J. Hultgren. 2004. Intracellular bacterial communities of uropathogenic Escherichia coli in urinary tract pathogenesis. Trends Microbiol. 12:424430.
5. Ascenzi, P.,, M. Bolognesi,, M. Milani,, M. Guertin, and, P. Visca. 2007. Mycobacterial truncated hemoglobins: from genes to functions. Gene 398:4251.
6. Backert, S., and, M. Selbach. 2008. Role of type IV secretion in Helicobacter pylori pathogenesis. Cell. Microbiol. 10:15731581.
7. Baker, S., and, G. Dougan. 2007. The genome of Salmonella enterica serovar Typhi. Clin. Infect. Dis. 45:S29S33.
8. Belkaid, Y. 2007. Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 7:875888.
9. Blom, A. M.,, T. Hallström, and, K. Riesbeck. 2009. Complement evasion strategies of pathogens—acquisition of inhibitors and beyond. Mol. Immunol. 46:28082817.
10. Boncristiano,, M.,, S. R. Paccani,, S. Barone,, C. Ulivieri,, L. Patrussi,, D. Ilver,, A. Amedei,, M. M. D’Elios,, J. L. Telford, and, C. T. Baldari. 2003. The Helicobacter pylori vacuolating cytotoxin inhibits T cell activation by two independent mechanisms. J. Exp. Med. 198:18871897.
11. Brown,, J. P.,, J. F. Zachary,, C. Teuscher,, J. H. Weis, and, R. M. Wooten. 1999. Dual role of interleukin-10 in murine Lyme disease: regulation of arthritis severity and host defense. Infect. Immun. 67:51425150.
12. Brubaker, R. R. 2003. Interleukin-10 and inhibition of innate immunity to yersiniae: roles of Yops and LcrV (V antigen). Infect. Immun. 71:36733681.
13. Bryk, R.,, C. D. Lima,, H. Erdjument-Bromage,, P. Tempst, and, C. Nathan. 2002. Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295:10731077.
14. Burman,, J. D.,, E. Leung,, K. L. Atkins,, M. N. O’Seaghdha,, L. Lango,, P. Bernadó,, S. Bagby,, D. I. Svergun,, T. J. Foster,, D. E. Isenman, and, J. M. H. van den Elsen. 2008. Interaction of human complement with Sbi, a staphylococcal immunoglobulin-binding protein: indications of a novel mechanism of complement evasion by Staphylococcus aureus. J. Biol. Chem. 283:1757917593.
15. Carroll, M. C. 2004. The complement system in regulation of adaptive immunity. Nat. Immunol. 5:981986.
16. Centurion-Lara,, A.,, R. E. LaFond,, K. Hevner,, C. Godornes,, B. J. Molini,, W. C. Van Voorhis, and, S. A. Lukehart. 2004. Gene conversion: a mechanism for generation of heterogeneity in the tprK gene of Treponema pallidum during infection. Mol. Microbiol. 52:15791596.
17. Chavakis, T.,, K. T. Preissner, and, M. Herrmann. 2007. The anti-inflammatory activities of Staphylococcus aureus. Trends Immunol. 28:408418.
18. Cover,, T. L. 2005. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat. Rev. Microbiol. 3:320332.
19. Craig, L.,, M. E. Pique, and, J. A. Tainer. 2004. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2:363378.
20. Cullen, P. A.,, D. A. Haake, and, B. Adler. 2004. Outer membrane proteins of pathogenic spirochetes. FEMS Microbiol. Rev. 28:291318.
21. Darwin,, K. H.,, S. Ehrt,, J. C. Gutierrez-Ramos,, N. Weich, and, C. F. Nathan. 2003. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302:19631966.
22. Darwin, K. H., and, C. F. Nathan. 2005. Role for nucleotide excision repair in virulence of Mycobacterium tuberculosis. Infect. Immun. 73:45814587.
23. Darwin, K. H. 2009. Prokaryotic ubiquitin-like protein (Pup), proteasomes and pathogenesis. Nat. Rev. Microbiol. 7:485491.
24. Deitsch, K. W.,, S. A. Lukehart, and, J. R. Stringer. 2009. Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat. Rev. Microbiol. 7:493503.
25. DePaolo,, R. W.,, F. Tang,, I. Kim,, M. Han,, N. Levin,, N. Ciletti,, A. Lin,, D. Anderson,, O. Schneewind, and, B. Jabri. 2008. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 4:350361.
26. Diterich, I.,, C. Rauter,, C. J. Kirschning, and, T. Hartung. 2003. Borrelia burgdorferi-induced tolerance as a model of persistence via immunosuppression. Infect. Immun. 71:39793987.
27. Dubois, A., and, T. Boren. 2007. Helicobacter pylori is invasive and it may be a facultative intracellular organism. Cell. Microbiol. 9:11081116.
28. Ehrt, S., and, D. Schnappinger. 2009. Mycobacterial survival strategies in the phagosome: defense against host stresses. Cell. Microbiol. 11:11701178.
29. Ernst, R. K.,, T. Guina, and, S. I. Miller. 2001. Salmonella typhimurium outer membrane remodeling: role in resistance to host innate immunity. Microbes Infect. 3:13271334.
30. Fang, F. C. 2004. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2:820832.
31. Flannagan, R. S.,, G. Cosîo, and, S. Grinstein. 2009. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7:355366.
32. Foster,, T. J. 2005. Immune evasion by Staphylococci. Nat. Rev. Microbiol. 5:948958.
33. Fux,, C. A.,, J. W. Costerson,, P. S. Stewart, and, P. Stoodley. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13:3440.
34. Galán, J. E. 2009. Common themes in the design and function of bacterial effectors. Cell Host Microbe 5:571579.
35. Garcia-Medina, R.,, W. M. Dunne,, P. K. Singh, and, S. L. Brody. 2005. Pseudomonas aeruginosa acquires biofilm-like properties within airway epithelial cells. Infect. Immun. 73:82988305.
36. Ge, Z.,, D. B. Schauer, and, J. G. Fox. 2008. In vivo virulence properties of bacterial cytolethal-distending toxin. Cell. Microbiol. 10:15991607.
37. Gebert, B.,, W. Fischer,, E. Weiss,, R. Hoffmann, and, R. Haas. 2003. Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301:10991102.
38. Geijtenbeek,, T. B. H.,, S. J. van Vliet,, E. J. Koppel,, M. Sanchez-Hernandez,, C. M. J. E. Vandenbroucke-Grauls,, B. Appelmelk, and, Y. van Kooyk. 2003. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197:717.
39. Geijtenbeek, T. B. H., and, S. I. Gringhuis. 2009. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9:469479.
40. Gerhard, M.,, C. Schmees,, P. Voland,, N. Endres,, M. Sander,, W. Reindl,, R. Rad,, M. Oelsner,, T. Decker,, M. Mempel,, L. Hengst, and, C. Prinz. 2005. A secreted low-molecularweight protein from Helicobacter pylori induces cell-cycle arrest of T cells. Gastroenterology 128:13271339.
41. Gringhuis,, S. I.,, J. den Dunnen,, M. Litjens,, B. van het Hof,, Y. van Kooyk, and, T. B. H. Geijtenbeek. 2007. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-κB. Immunity 26:605616.
42. Guillermo,, G. H.,, V. A. Dennis,, B. L. Lasater,, P. K. Murthy, and, M. T. Philipp. 2002. Autocrine and exocrine regulation of IL-10 production in THP-1 cells stimulated with B. burgdorferi lipoproteins. Infect. Immun. 70:18811888.
43. Hair,, P. S.,, M. D. Ward,, O. J. Semmes,, T. J. Foster, and, K M. Cunnion. 2008. Staphylococcus aureus clumping factor A binds to complement regulator factor I and increases factor I cleavage of C3b. J. Infect. Dis. 198:125133.
44. Hall-Stoodley, L.,, J. W. Costerson, and, P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2:95108.
45. Hall-Stoodley, L., and, P. Stoodley. 2009. Evolving concepts in biofilm infections. Cell. Microbiol. 11:10341043.
46. Hammel, M.,, G. Sfyroera,, S. Pyrpassopoulos,, D. Ricklin,, K. X. Ramyar,, M. Pop,, Z. Jin,, J. D. Lambris, and, B. V. Geisbrecht. 2007. Characterization of Ehp, a secreted complement inhibitory protein for Staphylococcus aureus. J. Biol. Chem. 282.
47. Hassett,, D. J.,, M. D. Sutton,, M. J. Schurr,, A. B. Herr,, C. C. Caldwell, and, J. O. Matu. 2009. Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol. 17:130138.
48. Hill, S. A., and, J. K. Davies. 2009. Pilin gene variation in Neisseria gonorrhoeae: reassessing the old paradigms. FEMS Microbiol. Rev. 33:521530.
49. Hu,, Y., and, A. R., M. Coates. 2009. Acute and persistent Mycobacterium tuberculosis infections depend on the thiol peroxidase TPX. PLoS ONE 4:e5150.
50. Huynh, K. K., and, S. Grinstein. 2007. Regulation of vacuolar pH and its modulation by some microbial species. Microbiol. Mol. Biol. Rev. 71:452462.
51. Isberg, R. R.,, T. J. O’Connor, and, M. Heidtman. 2009. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat. Rev. Microbiol. 7:1324.
52. Jaeger, T.,, H. Budde,, L. Flohé,, U. Menge,, M. Singh,, M. Trujillo, and, R. Radi. 2004. Multiple thioredoxin-mediated routes to detoxify hydroperoxides in Mycobacterium tuberculosis. Arch. Biochem. Biophys. 423:182191.
53. Jongerius, I.,, J. Köhl,, M. K. Pandey,, M. Ruyken,, K. P. M. van Kessel,, J. A. G. van Strijp, and, S. H. M. Rooijakkers. 2007. Staphylococcal complement evasion by various convertaseblocking molecules. J. Exp. Med. 204:24612471.
54. Jonsson, A. B.,, G. Nyberg, and, S. Normark. 1991. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J. 10:477488.
55. Justice,, S. S.,, C. Hung,, J. A. Theriot,, D. A. Fletcher,, G. G. Anderson,, M. J. Footer, and, S. J. Hultgren. 2004. Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc. Natl. Acad. Sci. USA 101:13331338.
56. Justice,, S. S.,, D. A. Hunstad,, P. C. Seed, and, S. J. Hultgren. 2006. Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. Proc. Natl. Acad. Sci. USA 103:1988419889.
57. Justice,, S. S.,, D. A. Hunstad,, L. Cegelski, and, S. J. Hultgren. 2008. Morphological plasticity as a bacterial survival strategy. Nat. Rev. Microbiol. 6:162168.
58. Kau, A. L.,, D. A. Hunstad, and, S. J. Hultgren. 2005. Interaction of uropathogenic Escherichia coli with host uroepithelium. Curr. Opin. Microbiol. 8:5459.
59. Kline,, K. A.,, E. V. Sechman,, E. P. Skaar, and, H. S. Seifert. 2003. Recombination, repair and replication in the pathogenic Neisseriae: the 3 R’s of molecular genetics of two human-specific bacterial pathogens. Mol. Microbiol. 50:313.
60. Kusters, J. G.,, A. H. M. van Vliet, and, E. J. Kuipers. 2006. Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev. 19:449490.
61. LaFond,, R. E.,, A. Centurion-Lara,, C. Godornes,, W. C. Van Voorhis, and, S. A. Lukehart. 2006a. TprK sequence diversity accumulates during infection of rabbits with Treponema pallidum subsp. pallidum Nichols strain. Infect. Immun. 74:18961906.
62. LaFond, R. E., and, S. A. Lukehart. 2006. Biological basis for syphilis. Clin. Microbiol. Rev. 19:2949.
63. LaFond,, R. E.,, B. J. Molini,, W. C. Van Voorhis, and, S. A. Lukehart. 2006b. Antigenic variation of TprK V regions abrogates specific antibody binding in syphilis. Infect. Immun. 74:62446251.
64. Lambris, J. D.,, D. Ricklin, and, B. V. Geisbrecht. 2008. Complement evasion by human pathogens. Nat. Rev. Microbiol. 6:132142.
65. Lazarus,, J. J.,, M. A. Kay,, A. L. McCarter, and, R. M. Wooten. 2008. Viable Borrelia burgdorferi enhances interleukin-10 production and suppresses activation of murine macrophages. Infect. Immun. 76:11531162.
66. Lee,, L. Y. L.,, M. Höök,, D. Haviland,, R. A. Wetsel,, E. O. Yonter,, P. Syribeys,, J. Vernachio, and, E. L. Brown. 2004. Inhibition of complement activation by a secreted Staphylococcus aureus protein. J. Infect, Dis. 190:571579.
67. Lillebaek, T.,, A. Dirksen,, I. Baess,, B. Strunge,, V. Ø. Thomsen, and, A. B. Andersen. 2002. Molecular evidence of endogenous reactivation of Mycobacterium tuberculosis after 33 years of latent infection. J. Infect. Dis. 185:401404.
68. Lillebaek, T.,, A. Dirksen,, E. Vynnycky,, I. Baess,, V. Ø. Thomsen, and, A. B. Andersen. 2003. Stability of DNA patterns and evidence of Mycobacterium tuberculosis reactivation occurring decades after the initial infection. J. Infect. Dis. 188:10321039.
69. Liu, P. T.,, S. Stenger,, D. H. Tang, and, R. L. Modlin. 2007. Cutting edge: vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J. Immunol. 179:20602063.
70. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339:520532.
71. Mahnke, K.,, J. Knop, and, A. H. Enk. 2003. Induction of tolerogenic DCs: “you are what you eat”. Trends Immunol. 24:646651.
72. Maloney, E.,, D. Stankowska,, J. Zhang,, M. Fol,, Q.-J. Cheng,, S. Lun,, W. R. Bishai,, M. Rajagopalan,, D. Chatterjee, and, M. V. Madiraju. 2009. The two-domain LysX protein of Mycobacterium tuberculosis is required for production of lysinylated phosphatidylglycerol and resistance to cationic antimicrobial peptides. PLoS Pathog. 5:e1000534.
73. Mattoo, S.,, Y. M. Lee, and, J. E. Dixon. 2007. Interactions of bacterial effector proteins with host proteins. Curr. Opin. Immunol. 19:392401.
74. McGuirk, P., and, K. H. G. Mills. 2002. Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends Immunol. 23:450455.
75. Morgan, C. A.,, S. A. Lukehart, and, W. C. Van Voorhis. 2003. Protection against syphilis correlates with specificity of antibodies to the variable regions of Treponema pallidum repeat protein K. Infect. Immun. 71:56055612.
76. Moxon, R.,, C. Bayliss, and, D. Hood. 2006. Bacterial contingency loci: the role of simple sequence repeats in bacterial adaptation. Annu. Rev. Genet. 40:307333.
77. Murthy,, P. K.,, V. A. Dennis,, B. L. Lasater, and, M. T. Philipp. 2000. Interleukin-10 modulates proinflammatory cytokines in the human monocytic cell line THP-1 stimulated with Borrelia burgdorferi lipoproteins. Infect. Immun. 68:66636669.
78. Mysorekar, I. U., and, S. J. Hultgren. 2006. Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc. Natl. Acad. Sci. USA 103:1417014175.
79. Navarro, L.,, N. M. Alto, and, J. E. Dixon. 2005. Functions of the Yersinia effector proteins inhibiting host immune responses. Curr. Opin. Microbiol. 8:2127.
80. Netea, M. G.,, J. W. M. Van der Meer, and, B.-J. Kullbert. 2004. Toll-like receptors as an escape mechanism from the host defense. Trends Microbiol. 12:484488.
81. Newton, G. L.,, N. Buchmeier, and, R. C. Fahey. 2008. Biosynthesis and functions of mycothiol, the unique protective thiol of Actinobacteria. Microbiol. Mol. Biol. Rev. 72:471494.
82. Ng,, V. H., J. S. Cox,, A. O. Sousa,, J. D. MacMicking, and, J. D. McKinney. 2004. Role of KatG catalase-peroxidase in mycobacterial pathogenesis: countering the phagocyte oxidative burst. Mol. Microbiol. 52:12911302.
83. Ngampasutadol, J.,, S. Ram,, A. M. Blom,, H. Jarva,, A. E. Jerse,, E. Lien,, J. Goguen,, S. Gulati, and, P. A. Rice. 2005. Human C4b-binding protein selectively interacts with Neisseria gonorrhoeae and results in species-specific infection. Proc. Natl. Acad. Sci. USA 102:1714217147.
84. Ngampasutadol, J.,, S. Ram,, S. Gulati,, S. Agarwal,, C. Li,, A. Visintin,, B. Monks,, G. Madico, and, P. A. Rice. 2008. Human factor H interacts selectively with Neisseria gonorrhoeae and results in species-specific complement evasion. J. Immunol. 180:34263435.
85. Parry,, C. M.,, T. T. Hien,, G. Dougan,, N. White, and, J. J. Farrar. 2002. Typhoid fever. N. Engl. J. Med. 347:17701782.
86. Philips, J. A. 2008. Mycobacterial manipulation of vacuolar sorting. Cell. Microbiol. 10:24082415.
87. Proctor,, R. A.,, C. von Eiff,, B. C. Kahl,, K. Becker,, P. McNamara,, M. Herrmann, and, G. Peters. 2006. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat. Rev. Microbiol. 4:295305.
88. Purdy, G. E. 2007. Lysosomal ubiquitin and the demise of Mycobacterium tuberculosis. Cell. Microbiol. 9:27682774.
89. Radolf, J. D., and, M. J. Caimano. 2008. The long strange trip of Borrelia burgdorferi outer-surface protein C. Mol. Microbiol. 69:14.
90. Raffatellu, M.,, D. Chesa,, R. P. Wilson,, C. Tiikel,, M. Akcelik, and, A. Bäumler. 2006. Capsule-mediated immune evasion: a new hypothesis explaining aspects of typhoid fever pathogenesis. Infect. Immun. 74:1927.
91. Ray, K.,, B. Marteyn,, P. J. Sansonetti, and, C. M. Tang. 2009. Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat. Rev. Microbiol. 7:333340.
92. Redpath, S.,, P. Ghazal, and, N. R. J. Gascoigne. 2001. Hijacking and exploitation of IL-10 by intracellular pathogens. Trends Microbiol. 9:8692.
93. Ricklin, D.,, S. K. Richlin-Lichtsteiner,, M. M. Markiewski,, B. V. Geisbrecht, and, J. D. Lambris. 2008. Cutting edge: members of the Staphylococcus aureus extracellular fibrinogen-binding protein family inhibit the interaction of C3d with complement receptor 2. J. Immunol. 181:74637467.
94. Rooijakkers,, S. H. M.,, M. Ruyken,, A. Roos,, M. R. Daha,, J. S. Presanis,, R. B. Sim,, W. J. B. van Wamel,, K. P. M. van Kessel, and, J. A. G. van Strijp. 2005. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat. Immunol. 6:920927.
95. Rosen,, D. A.,, T. M. Hooton,, W. E. Stamm,, P. A. Humphrey, and, S. J. Hultgren. 2007. Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med. 4:e329.
96. Schaefer, M.,, N. Reiling,, C. Fessler,, J. Stephani,, I. Taniuchi,, F. Hatam,, A. O. Yildirim,, H. Fehrenbach,, K. Walter,, J. Ruland,, H. Wagner,, S. Ehlers, and, T. Sparwasser. 2008. Decreased pathology and prolonged survival of human DC-SIGN transgenic mice during mycobacterial infection. J. Immunol. 180:68366845.
97. Schmees, C.,, C. Prinz,, T. Treptau,, R. Rad,, L. Hengst,, P. Voland,, S. Bauer,, L. Brenner,, R. M. Schmid, and, M. Gerhard. 2007. Inhibition of T-cell proliferation by Helicobacter pylori γ-glutamyl transferase. Gastroenterology 132:18201833.
98. Sewald, X.,, B. Gebert-Vogl,, S. Prassi,, I. Barwig,, E. Weiss,, M. Fabbri,, R. Osicka,, M. Schiemann,, D. H. Busch,, M. Semmrich,, B. Holzmann,, P. Sebo, and, R. Haas. 2008. Integrin subunit CD18 is the T-lymphocyte receptor for the Helicobacter pylori vacuolating cytotoxin. Cell Host Microbe 3:2029.
99. Singh, S. K., and, H. J. Girschick. 2004. Lyme borreliosis: from infection to autoimmunity. Clin. Microbiol. Infect. 10:598614.
100. Sow,, F. B.,, W. C. Florence,, A. R. Satoskar,, L. S. Schlesinger,, B. S. Zwilling, and, W. P. Lafuse. 2007. Expression and localization of hepcidin in macrophages: a role in host defense against tuberculosis. J. Leukoc. Biol. 82:934945.
101. Sundrud,, M. S.,, V. J. Torres,, D. Unutmaz, and, T. L. Cover. 2004. Inhibition of primary human T cell proliferation by Helicobacter pylori vacuolating toxin (VacA) is independent of VacA effects on IL-2 secretion. Proc. Natl. Acad. Sci. USA 101:77277732.
102. Tan,, S.,, L. S. Tompkins, and, M. R. Amieva. 2009. Helicobacter pylori usurps cell polarity to turn the cell surface into a replicative niche. PLoS Pathog. 5:e1000407.
103. Tsolis,, R. M.,, G. M. Young,, J. V. Solnick, and, A. J. Bäumler. 2008. From bench to bedside: stealth of enteroinvasive pathogens. Nat. Rev. Microbiol. 6:883892.
104. Vandal,, O. H.,, L. M. Pierini,, D. Schnappinger,, C. F. Nathan, and, S. Erht. 2008. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat. Med. 8:849854.
105. Vandal,, O. H.,, C. F. Nathan, and, S. Ehrt. 2009a. Acid resistance in Mycobacterium tuberculosis. J. Bacterial. 191:47144721.
106. Vandal,, O. H.,, J. A. Roberts,, T. Odaira,, D. Schnappinger,, C. F. Nathan, and, S. Ehrt. 2009b. Acid-susceptible mutants of Mycobacterium tuberculosis share hypersusceptibility to cell wall and oxidative stress and to the host environment. J. Bacteriol. 191:625631.
107. van der Woude,, M. W., and, A. J. Bäumler. 2004. Phase and antigenic variation in bacteria. Clin. Microbiol. Rev. 17:581611.
108. van Kooyk, Y., and, T. H. B. Geijtenbeek. 2003. DC-SIGN: escape mechanism for pathogens. Nat. Rev. Immunol. 3:697709.
109. Via,, L. E.,, R. A. Fratti,, M. McFalone,, E. Pagán-Ramos,, D. Deretic, and, V. Deretic. 1998. Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111:897905.
110. Vojtova, J.,, J. Kamanova, and, P. Sebo. 2006. Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr. Opin. Microbiol. 9:6975.
111. Walport, M. J. 2001a. Complement: first of two parts. N. Engl. J. Med. 344:10581066.
112. Walport, M. J. 2001b. Complement: second of two parts. N. Engl. J. Med. 344:11401144.
113. Wilson,, R. P.,, M. Raffatellu,, D. Chessa,, S. E. Winter,, C. Tükel, and, A. J. Bäumler. 2008. The Vi-capsule prevents Toll-like receptor 4 recognition of Salmonella. Cell. Microbiol. 10:876890.
114. Winter,, S. E.,, M. Raffatellu,, R. P. Wilson,, H. Rüssmann, and, A. J. Bäumler. 2008. The Salmonella enterica serotype Typhi regulator TviA reduces interleukin-8 production in intestinal epithelial cells by repressing flagellin secretion. Cell. Microbiol. 10:247261.
115. Wright, K. J.,, P. C. Seed, and, S. J. Hultgren. 2007. Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell. Microbiol. 9:22302241.
116. Xu, Q.,, K. McShan, and, F. T. Liang. 2008. Essential protective role attributed to the surface lipoproteins of Borrelia burgdorferi against innate defences. Mol. Microbiol. 69:1529.
117. Zähringer, U.,, B. Linder,, S. Inamura,, H. Heine, and, C. Alexander. 2008. TLR2–promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiol. 213:205224.

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