The Vi Capsular Polysaccharide Enables Salmonella enterica Serovar Typhi to Evade Microbe-Guided Neutrophil Chemotaxis

PLoS Pathogens

Volumn 10, Issue 8, 2014, Pages

  Wangdi, Tamding ^a   Lee, Cheng Yuk ^b   Spees, Alanna M ^a   Yu, Chenzhou ^b   Kingsbury, Dawn D ^a   Winter, Sebastian E ^a   Hastey, Christine J ^b   Wilson, R Paul ^a   Heinrich, Volkmar ^b   Bäumler, Andreas J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A RECEPTOR; UNCLASSIFIED DRUG; VIRULENCE ASSOCIATED CAPSULAR POLYSACCHARIDE; VIRULENCE FACTOR; BACTERIAL POLYSACCHARIDE; CAPSULAR POLYSACCHARIDE, SALMONELLA;

ANIMAL MODEL; ARTICLE; BACTERIAL CAPSULE; BACTERIAL VIRULENCE; CELL MIGRATION; COMPLEMENT DEPENDENT CYTOTOXICITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FEMALE; FLOW CYTOMETRY; GENE DELETION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNE EVASION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENICITY ISLAND; SALMONELLA ENTERICA SEROVAR TYPHI; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SINGLE CELL ANALYSIS; TYPHOID FEVER; ANIMAL; IMMUNOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI; SALMONELLA TYPHI;

ANIMALS; CHEMOTAXIS, LEUKOCYTE; COMPLEMENT C5A; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMANS; MICE; NEUTROPHIL INFILTRATION; POLYSACCHARIDES, BACTERIAL; RECEPTOR, ANAPHYLATOXIN C5A; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; TYPHOID FEVER;

EID: 84918842275     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004306     Document Type: Article

References (55)

1. Nuccio S-P, Wangdi T, Winter SE, Baumler AJ (2013) Typhoid. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The Prokaryotes. 4th ed. Berlin Heidelberg: Springer-Verlag. pp. 353–374.
2. Zhang S, Kingsley RA, Santos RL, Andrews-Polymenis H, Raffatellu M, et al. (2003) Molecular pathogenesis of Salmonella enterica serotype typhimurium- induced diarrhea. Infect Immun 71: 1–12.
3. Spano S, Ugalde JE, Galan JE, (2008) Delivery of a Salmonella Typhi exotoxin from a host intracellular compartment. Cell Host Microbe 3: 30–38.
4. Song J, Gao X, Galan JE, (2013) Structure and function of the Salmonella Typhi chimaeric A(2)B(5) typhoid toxin. Nature 499: 350–354.
5. Winter SE, Raffatellu M, Wilson RP, Russmann H, Baumler AJ, (2008) The Salmonella enterica serotype Typhi regulator TviA reduces interleukin-8 production in intestinal epithelial cells by repressing flagellin secretion. Cell Microbiol 10: 247–261.
6. Winter SE, Winter MG, Godinez I, Yang H-J, Russmann H, et al. (2010) A Rapid Change in Virulence Gene Expression during the Transition from the Intestinal Lumen into Tissue Promotes Systemic Dissemination of Salmonella. PLoS Pathog 6: e1001060.
7. Atif SM, Winter SE, Winter MG, McSorley SJ, Baumler AJ, (2014) Salmonella enterica serovar Typhi impairs CD4 T cell responses by reducing antigen availability. Infect Immun 82: 2247–2254.
8. Tartera C, Metcalf ES, (1993) Osmolarity and growth phase overlap in regulation of Salmonella typhi adherence to and invasion of human intestinal cells. Infect Immun 61: 3084–3089.
9. Leclerc GJ, Tartera C, Metcalf ES, (1998) Environmental regulation of Salmonella typhi invasion-defective mutants. Infect Immun 66: 682–691.
10. Winter SE, Winter MG, Thiennimitr P, Gerriets VA, Nuccio SP, et al. (2009) The TviA auxiliary protein renders the Salmonella enterica serotype Typhi RcsB regulon responsive to changes in osmolarity. Mol Microbiol 74: 175–193.
11. Miller RM, Garbus J, Hornick RB, (1972) Lack of enhanced oxygen consumption by polymorphonuclear leukocytes on phagocytosis of virulent Salmonella typhi. Science 175: 1010–1011.
12. Looney RJ, Steigbigel RT, (1986) Role of the Vi antigen of Salmonella typhi in resistance to host defense in vitro. J Lab Clin Med 108: 506–516.
13. Hirose K, Ezaki T, Miyake M, Li T, Khan AQ, et al. (1997) Survival of Vi-capsulated and Vi-deleted Salmonella typhi strains in cultured macrophage expressing different levels of CD14 antigen. FEMS Microbiol Lett 147: 259–265.
14. Wilson RP, Raffatellu M, Chessa D, Winter SE, Tukel C, et al. (2008) The Vi-capsule prevents Toll-like receptor 4 recognition of Salmonella. Cell Microbiol 10: 876–890.
15. Haneda T, Winter SE, Butler BP, Wilson RP, Tukel C, et al. (2009) The capsule-encoding viaB locus reduces intestinal inflammation by a Salmonella pathogenicity island 1-independent mechanism. Infect Immun 77: 2932–2942.
16. Wilson RP, Winter SE, Spees AM, Winter MG, Nishimori JH, et al. (2011) The Vi capsular polysaccharide prevents complement receptor 3-mediated clearance of Salmonella enterica serotype Typhi. Infect Immun 79: 830–837.
17. Jansen AM, Hall LJ, Clare S, Goulding D, Holt KE, et al. (2011) A Salmonella Typhimurium-Typhi Genomic Chimera: A Model to Study Vi Polysaccharide Capsule Function In Vivo. PLoS Pathog 7: e1002131.
18. Spano S, Liu X, Galan JE, (2011) Proteolytic targeting of Rab29 by an effector protein distinguishes the intracellular compartments of human-adapted and broad-host Salmonella. Proc Natl Acad Sci U S A 108: 18418–18423.
19. Crawford RW, Wangdi T, Spees AM, Xavier MN, Tsolis RM, et al. (2013) Loss of very-long O-antigen chains optimizes capsule-mediated immune evasion by Salmonella enterica serovar Typhi. MBio 4: pii: e00232-13.
20. Noriega LM, Van der Auwera P, Daneau D, Meunier F, Aoun M, (1994) Salmonella infections in a cancer center. Support Care Cancer 2: 116–122.
21. Tumbarello M, Tacconelli E, Caponera S, Cauda R, Ortona L, (1995) The impact of bacteraemia on HIV infection. Nine years experience in a large Italian university hospital. J Infect 31: 123–131.
22. Cunnington AJ, Njie M, Correa S, Takem EN, Riley EM, et al. (2012) Prolonged neutrophil dysfunction after Plasmodium falciparum malaria is related to hemolysis and heme oxygenase-1 induction. J Immunol 189: 5336–5346.
23. Reddy EA, Shaw AV, Crump JA, (2010) Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. Lancet Infect Dis 10: 417–432.
24. Gotze O, Muller-Eberhard HJ, (1971) The c3-activator system: an alternate pathway of complement activation. J Exp Med 134: 90–108.
25. Law SK, Levine RP, (1977) Interaction between the third complement protein and cell surface macromolecules. Proc Natl Acad Sci U S A 74: 2701–2705.
26. Tack BF, Harrison RA, Janatova J, Thomas ML, Prahl JW, (1980) Evidence for presence of an internal thiolester bond in third component of human complement. Proc Natl Acad Sci U S A 77: 5764–5768.
27. Horwitz MA, (1982) Phagocytosis of microorganisms. Rev Infect Dis 4: 104–123.
28. Heinrich V, Lee CY, (2011) Blurred line between chemotactic chase and phagocytic consumption: an immunophysical single-cell perspective. J Cell Sci 124: 3041–3051.
29. Mankovich AR, Lee CY, Heinrich V, (2013) Differential effects of serum heat treatment on chemotaxis and phagocytosis by human neutrophils. PLoS One 8: e54735.
30. Schiffmann E, Corcoran BA, Wahl SM, (1975) N-formylmethionyl peptides as chemoattractants for leucocytes. Proc Natl Acad Sci U S A 72: 1059–1062.
31. Manthey HD, Woodruff TM, Taylor SM, Monk PN, (2009) Complement component 5a (C5a). Int J Biochem Cell Biol 41: 2114–2117.
32. Muller-Eberhard HJ, (1975) Complement. Annu Rev Biochem 44: 697–724.
33. Boyden S, (1962) The chemotactic effect of mixtures of antibody and antigen on polymorphonuclear leucocytes. J Exp Med 115: 453–466.
34. Ikari N, Sakai Y, Hitomi Y, Fujii S, (1983) New synthetic inhibitor to the alternative complement pathway. Immunology 49: 685–691.
35. Inagi R, Miyata T, Maeda K, Sugiyama S, Miyama A, et al. (1991) FUT-175 as a potent inhibitor of C5/C3 convertase activity for production of C5a and C3a. Immunol Lett 27: 49–52.
36. Felix A, Pitt RM, (1934) A new antigen of B. typhosus. Lancet 227: 186–191.
37. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, et al. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413: 848–852.
38. Virlogeux I, Waxin H, Ecobichon C, Popoff MY, (1995) Role of the viaB locus in synthesis, transport and expression of Salmonella typhi Vi antigen. Microbiology 141 (Pt 12) 3039–3047.
39. Fischer MB, Ma M, Goerg S, Zhou X, Xia J, et al. (1996) Regulation of the B cell response to T-dependent antigens by classical pathway complement. J Immunol 157: 549–556.
40. Hopken UE, Lu B, Gerard NP, Gerard C, (1996) The C5a chemoattractant receptor mediates mucosal defence to infection. Nature 383: 86–89.
41. Russo TA, Davidson BA, Topolnycky DM, Olson R, Morrill SA, et al. (2003) Human neutrophil chemotaxis is modulated by capsule and O antigen from an extraintestinal pathogenic Escherichia coli strain. Infect Immun 71: 6435–6445.
42. Melly MA, Thomison JB, Rogers DE, (1960) Fate of staphylococci within human leukocytes. J Exp Med 112: 1121–1130.
43. Smith CW, Hollers JC, Patrick RA, Hassett C, (1979) Motility and adhesiveness in human neutrophils. Effects of chemotactic factors. J Clin Invest 63: 221–229.
44. Zhelev DV, Alteraifi AM, Chodniewicz D, (2004) Controlled pseudopod extension of human neutrophils stimulated with different chemoattractants. Biophys J 87: 688–695.
45. Musher DM, Hague-Park M, Gyorkey F, Anderson DC, Baughn RE, (1983) The interaction between Treponema pallidum and human polymorphonuclear leukocytes. J Infect Dis 147: 77–86.
46. Densen P, MacKeen LA, Clark RA, (1982) Dissemination of gonococcal infection is associated with delayed stimulation of complement-dependent neutrophil chemotaxis in vitro. Infect Immun 38: 563–572.
47. Sordelli DO, Djafari M, Garcia VE, Fontan PA, Doring G, (1992) Age-dependent pulmonary clearance of Pseudomonas aeruginosa in a mouse model: diminished migration of polymorphonuclear leukocytes to N-formyl-methionyl-leucyl-phenylalanine. Infect Immun 60: 1724–1727.
48. Ijiri Y, Matsumoto K, Kamata R, Nishino N, Okamura R, et al. (1994) Suppression of polymorphonuclear leucocyte chemotaxis by Pseudomonas aeruginosa elastase in vitro: a study of the mechanisms and the correlation with ring abscess in pseudomonal keratitis. Int J Exp Pathol 75: 441–451.
49. Li Y, Loike JD, Ember JA, Cleary PP, Lu E, et al. (2002) The bacterial peptide N-formyl-Met-Leu-Phe inhibits killing of Staphylococcus epidermidis by human neutrophils in fibrin gels. J Immunol 168: 816–824.
50. Southgate EL, He RL, Gao JL, Murphy PM, Nanamori M, et al. (2008) Identification of formyl peptides from Listeria monocytogenes and Staphylococcus aureus as potent chemoattractants for mouse neutrophils. J Immunol 181: 1429–1437.
51. Murphy H, Cogan T, Humphrey T, (2011) Direction of neutrophil movements by Campylobacter-infected intestinal epithelium. Microbes Infect 13: 42–48.
52. Heyns K, Kiessling G, (1967) Strukturaufklarung des Vi-antigens aus Citrobacter freundii (E. coli) 5396/38. Carbohydrate Res 3: 340–353.
53. Laxalt KA, Kozel TR, (1979) Chemotaxigenesis and activation of the alternative complement pathway by encapsulated and non-encapsulated Cryptococcus neoformans. Infect Immun 26: 435–440.
54. Cummings LA, Wilkerson WD, Bergsbaken T, Cookson BT, (2006) In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted. Mol Microbiol 61: 795–809.
55. Raffatellu M, Santos RL, Chessa D, Wilson RP, Winter SE, et al. (2007) The capsule encoding the viaB locus reduces interleukin-17 expression and mucosal innate responses in the bovine intestinal mucosa during infection with Salmonella enterica serotype Typhi. Infect Immun 75: 4342–4350.