Contrasting persistence strategies in Salmonella and Mycobacterium

Current Opinion in Microbiology

Volumn 13, Issue 1, 2010, Pages 93-99

  Tischler, Anna D ^a   McKinney, John D ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOCYTE; REVIEW; SALMONELLA TYPHI; TUBERCULOSIS; TYPHOID FEVER;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; HUMANS; IMMUNE EVASION; MAMMALS; MYCOBACTERIUM TUBERCULOSIS; SALMONELLA TYPHI;

BACTERIA (MICROORGANISMS); MAMMALIA; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; NEGIBACTERIA; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI;

EID: 75449093245     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2009.12.007     Document Type: Review

References (53)

1. Young D., Hussell T., and Dougan G. Chronic bacterial infections: living with unwanted guests. Nat Immunol 3 (2002) 1026-1032
2. Monack D.M., Mueller A., and Falkow S. Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol 2 (2004) 747-765
3. Parry C.M., Hien T.T., Dougan G., White N., and Farrar J.J. Typhoid fever. N Engl J Med 347 (2002) 1770-1782
4. Lillebaek T., Dirksen A., Vynnycky E., Baess I., Thomsen V.Ø., and Andersen A.B. Stability of DNA patterns and evidence of Mycobacterium tuberculosis reactivation occurring decades after the initial infection. J Infect Dis 188 (2003) 1032-1039
5. Lillebaek T., Dirksen A., Baess I., Strunge B., Thomsen V.Ø., and Andersen A.B. Molecular evidence of endogenous reactivation of Mycobacterium tuberculosis after 33 years of latent infection. J Infect Dis 185 (2002) 401-404
6. Raffatellu M., Chesa D., Wilson R.P., Tükel C., Akcelik M., and Bäumler A. Capsule-mediated immune evasion: a new hypothesis explaining aspects of typhoid fever pathogenesis. Infect Immun 74 (2006) 19-27
7. Ibara J.A., and Steele-Mortimer O. Salmonella - the ultimate insider: Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 11 (2009) 1579-1586
8. Tsolis R.M., Young G.M., Solnick J.V., and Bäumler A.J. From bench to bedside: stealth of enteroinvasive pathogens. Nat Rev Microbiol 6 (2008) 883-892
9. Baker S., and Dougan G. The genome of Salmonella enterica serovar Typhi. Clin Infect Dis 45 (2007) S29-S33
10. Raffatellu M., Chessa D., Wilson R.P., Dusold R., Rubino S., and Bäumler A.J. The Vi-capsular antigen of Salmonella enterica serotype Typhi reduces Toll-like receptor-dependent IL-8 expression in the intestinal mucosa. Infect Immun 73 (2005) 3367-3374
11. Wilson R.P., Raffatellu M., Chessa D., Winter S.E., Tükel C., and Bäumler A.J. The Vi-capsule prevents Toll-like receptor 4 recognition of Salmonella. Cell Microbiol 10 (2008) 876-890. This paper demonstrated for the first time that ectopic expression of the Vi capsular polysaccharide by S. Typhimurium is sufficient to reduce the TLR4-dependent inflammatory response in murine infection models by 'masking' detection of lipopolysaccharide.
12. Winter S.E., Winter M.G., Thiennimitr P., Gerriets V.A., Nuccio S.-P., Rüssmann H., and Bäumler A.J. The TviA auxiliary protein renders the Salmonella enterica serotype Typhi RcsB regulon responsive to changes in osmolarity. Mol Microbiol 74 (2009) 175-193. This study revealed that osmolarity, an environmental signal that changes upon S. Typhi invasion of the intestinal mucosa, is integrated by the S. Typhi-specific transcription factor TviA to control expression of virulence factors. The authors demonstrate that TviA mediates the inverse regulation of the Vi capsule with flagellar motility and the invasion-associated T3SS in response to changes in osmolarity, and suggest that this inverse regulation is essential for the appropriate timing of virulence factor expression.
13. Tran Q.T., Gomez G., Khare S., Lawhon S.D., Raffatellu M., Bäumler A.J., Ajithdoss D., Dhavala S., and Adams L.G. The Salmonella enterica serotype Typhi Vi capsular antigen is expressed after the bacterium enters the ileal mucosa. Infect Immun 78 (2010) 527-535
14. Winter S.E., Raffatellu M., Wilson R.P., Rüssmann H., and Bäumler A.J. The Salmonella enterica serotype Typhi regulator TviA reduces interleukin-8 production in intestinal epithelial cells by repressing flagellin secretion. Cell Microbiol 10 (2008) 247-261
15. Begley M., Gahan C.G.M., and Hill C. The interaction between bacteria and bile. FEMS Microbiol Rev 29 (2005) 625-651
16. Langridge G.C., Phan M.-D., Turner D.J., Perkins T.T., Parts L., Haase J., Charles I., Maskell D.J., Peters S.E., Dougan G., et al. Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res 19 (2009) 2308-2316
17. Hall-Stoodley L., and Stoodley P. Evolving concepts in biofilm infections. Cell Microbiol 11 (2009) 1034-1043
18. Crawford R.W., Gibson D.L., Kay W.W., and Gunn J.S. Identification of a bile-induced exopolysaccharide required for Salmonella biofilm formation on gallstone surfaces. Infect Immun 76 (2008) 5341-5349
19. Menendez A., Arena E.T., Guttman J.A., Thorson L., Vallance B.A., Vogl W., and Finlay B.B. Salmonella infection of gallbladder epithelial cells drives local inflammation and injury in a model of acute typhoid fever. J Infect Dis 200 (2009) 1703-1713. Using a mouse model of S. Typhimurium infection, the authors demonstrate for the first time that Salmonella can invade and replicate within gallbladder epithelial cells, a potential site of persistence in chronic typhoid carriers.
20. Huynh K.K., and Grinstein S. Regulation of vacuolar pH and its modulation by some microbial species. Microbiol Mol Biol Rev 71 (2007) 452-462
21. Flannagan R.S., Cosîo G., and Grinstein S. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7 (2009) 355-366
22. Fang F.C. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2 (2004) 820-832
23. Purdy G.E. Lysosomal ubiquitin and the demise of Mycobacterium tuberculosis. Cell Microbiol 9 (2007) 2768-2774
24. Philips J.A. Mycobacterial manipulation of vacuolar sorting. Cell Microbiol 10 (2008) 2408-2415
25. Via Le, Fratti R.A., McFalone M., Pagán-Ramos E., Deretic D., and Deretic V. Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111 (1998) 897-905
26. Pethe K., Swenson D.L., Alonso S., Anderson J., Wang C., and Russell D.G. Isolation of Mycobacterium tuberculosis mutations defective in the arrest of phagosome maturation. Proc Natl Acad Sci U S A 101 (2004) 13642-13647
27. MacGurn J.A., and Cox J.S. A genetic screen for Mycobacterium tuberculosis mutants defective for phagosome maturation arrest identifies components of the ESX-1 secretion system. Infect Immun 75 (2007) 2668-2678
28. Ehrt S., and Schnappinger D. Mycobacterial survival strategies in the phagosome: defense against host stresses. Cell Microbiol 11 (2009) 1170-1178
29. Darwin K.H., Ehrt S., Gutierrez-Ramos J.C., Weich N., and Nathan C.F. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302 (2003) 1963-1966
30. Gandotra S., Schnappinger D., Monteleone M., Hillen W., and Ehrt S. In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat Med 13 (2007) 1515-1520. The authors use a conditional gene silencing technique to demonstrate that the core proteasome subunits, which are required for optimal growth of M. tuberculosis in vitro, are also required for persistence in the lungs of mice. This was the first time that conditional gene expression was successfully used to analyze the contribution of an M. tuberculosis gene to persistence in vivo.
31. Wang T., Li H., Lin G., Tang C., Li D., Nathan C., Darwin K.H., and Li H. Structural insights on the Mycobacterium tuberculosis proteasome ATPase Mpa. Structure 17 (2009) 1377-1385
32. Pearce M.J., Mintseris J., Ferreyra J., Gygi S.P., and Darwin K.H. Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322 (2008) 1104-1107. Using bacterial two-hybrid systems, the authors identified a prokaryotic ubiquitin-like protein (Pup) that modifies substrates of the mycobacterial proteasome. This was the first demonstration that a proteasome-containing prokaryote uses post-translational protein modification to target specific protein substrates for degradation.
33. Sutter M., Striebel F., Damberger F.F., Allain F.H., and Weber-Ban E. A distinct structural region of the prokaryotic ubiquitin-like protein (Pup) is recognized by the N-terminal domain of the proteasomal ATPase Mpa. FEBS Lett 583 (2009) 3151-3157
34. Striebel F., Imkamp F., Sutter M., Steiner M., Mamedov A., and Weber-Ban E. Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes. Nat Struct Mol Biol 16 (2009) 647-651
35. Darwin K.H. Prokaryotic ubiquitin-like protein (Pup), proteasomes and pathogenesis. Nat Rev Microbiol 7 (2009) 485-491
36. Vandal O.H., Roberts J.A., Odaira T., Schnappinger D., Nathan C.F., and Ehrt S. Acid-susceptible mutants of Mycobacterium tuberculosis share hypersusceptibility to cell wall and oxidative stress and to the host environment. J Bacteriol 191 (2009) 625-631
37. Vandal O.H., Pierini L.M., Schnappinger D., Nathan C.F., and Erht S. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 8 (2008) 849-854. The authors used a pH-sensitive GFP and fluorescence microscopy to make noninvasive measurements of intrabacterial pH on live M. tuberculosis. They demonstrate for the first time that a membrane-localized protease, Rv3671c, is required for the maintenance of neutral cytoplasmic pH in both acidified growth medium and in the acidified phagosomes of activated macrophages.
38. Vandal O.H., Nathan C.F., and Ehrt S. Acid resistance in Mycobacterium tuberculosis. J Bacteriol 191 (2009) 4714-4721
39. Liu P.T., Stenger S., Tang D.H., and Modlin R.L. Cutting edge: Vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J Immunol 179 (2007) 2060-2063
40. Sow F.B., Florence W.C., Satoskar A.R., Schlesinger L.S., Zwilling B.S., and Lafuse W.P. Expression and localization of hepcidin in macrophages: a role in host defense against tuberculosis. J Leukoc Biol 82 (2007) 934-945
41. Alonso S., Pethe K., Russell D.G., and Purdy G.E. Lysosomal killing of Mycobacterium tuberculosis mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc Natl Acad Sci U S A 104 (2007) 6031-6036
42. Peschel A., and Sahl H.-G. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 4 (2006) 529-536
43. Maloney E., Stankowska D., Zhang J., Fol M., Cheng Q.-J., Lun S., Bishai W.R., Rajagopalan M., Chatterjee D., and Madiraju M.V. The two-domain LysX protein of Mycobacterium tuberculosis is required for production of lysinylated phosphatidylglycerol and resistance to cationic antimicrobial peptides. PLoS Pathog 5 (2009) e1000534. The authors identify one component of the mycobacterial cell wall that is critical for resistance to cationic antimicrobial peptides and antibiotics and replication in animal models of infection. They demonstrate that the LysX enzyme modifies phosphatidylglycerol with positively charged lysine moieties, thereby increasing the net positive charge of the M. tuberculosis membrane.
44. Purdy G.E., Niederweis M., and Russell D.G. Decreased outer membrane permeability protects mycobacteria from killing by ubiquitin-derived peptides. Mol Microbiol 73 (2009) 844-857
45. +/+ mice and can be reactivated by IFNγ neutralization. J Exp Med 199 (2004) 231-241
46. Lawley T.D., Bouley D.M., Hoy Y.E., Gerke C., Relman D.A., and Monack D.M. Host transmission of Salmonella enterica serovar Typhimurium is controlled by virulence factors and indigenous intestinal microbiota. Infect Immun 76 (2008) 403-416
47. Lawley T.D., Chan K., Thompson L.J., Kim C.C., Govoni G.R., and Monack D.M. Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2 (2006) e11
48. McLaughlin L.M., Govoni G.R., Gerke C., Gopinath S., Peng K., Laidlaw G., Chien Y.-H., Jeong H.-W., Li Z., Brown M.D., et al. The Salmonella SPI2 effector SseI mediates long-term systemic infection by modulating host cell migration. PLoS Pathog 5 (2009) e1000671
49. Demangel C., Stinear T.P., and Cole S.T. Buruli ulcer: reductive evolution enhances pathogenicity of Mycobacterium ulcerans. Nat Rev Microbiol 10 (2009) 50-60. An excellent review on M. ulcerans pathogenesis highlighting its evolution from related mycobacteria and the immune suppressive properties of mycolactone.
50. Torrado E., Adusumilli S., Fraga A.G., Small P.L., Castro A.G., and Pedrosa J. Mycolactone-mediated inhibition of tumor necrosis factor production by macrophages infected with Mycobacterium ulcerans has implications for the control of infection. Infect Immun 75 (2007) 3979-3988
51. Coutanceau E., Decalf J., Martino A., Babon A., Winter N., Cole S.T., Albert M.L., and Demangel C. Selective immune suppression of dendritic cell functions by Mycobacterium ulcerans toxin mycolactone. J Exp Med 204 (2007) 1395-1403
52. Hong H., Coutanceau E., Leclerc M., Caleechurn L., Leadlay P.F., and Demangel C. Mycolactone diffuses from Mycobacterium ulcerans-infected tissues and targets mononuclear cells in peripheral blood and lymphoid organs. PLoS Negl Trop Dis 2 (2008) e325
53. En J., Goto M., Nakanaga K., Higashi M., Ishil N., Saito H., Yonezawa S., Hamada H., and Small P.L. Mycolactone is responsible for the painlessness of Mycobacterium ulcerans infection (buruli ulcer) in a murine study. Infect Immun 76 (2008) 2002-2007