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

Infection and Immunity

Volumn 75, Issue 9, 2007, Pages 4342-4350

  Raffatellu, Manuela ^a   Santos, Renato L ^a   Chessa, Daniela ^a   Wilson, R Paul ^a   Winter, Sebastian E ^a   Rossetti, Carlos A ^b   Lawhon, Sara D ^b   Chu, Hiutung ^a   Lau, Tsang ^a   Bevins, Charles L ^a   Adams, L Garry ^b   Bäumler, Andreas J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 17; STREPTOMYCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL MEMBRANE; BACTERIUM MUTANT; CONTROLLED STUDY; COW; CYTOKINE RELEASE; DOWN REGULATION; GASTROENTERITIS; GENE EXPRESSION; GENE LOCUS; IMMUNE RESPONSE; INTESTINE MUCOSA; MALE; MOLECULAR CLONING; MOUSE; NONHUMAN; ONCOGENE; OPERON; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHI; SEROTYPE; UPREGULATION;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL CAPSULES; CATTLE; CELL MOVEMENT; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GENETIC MARKERS; IMMUNITY, MUCOSAL; INFLAMMATION MEDIATORS; INTERLEUKIN-17; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; NEUTROPHILS; OPERON; POLYSACCHARIDES, BACTERIAL; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHI;

EID: 34548490154     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01571-06     Document Type: Article

References (66)

1. Alves, G. E. S., S. M. Hartsfield, G. L. Carroll, R. L. Santos, S. Zhang, R. M. Tsolis, A. J. Bäumler, L. G. Adams, and R. L. Santos. 2003. Use of propofol, isoflurane and morphine for prolonged general anesthesia in calves. Arq. Bras. Med. Vet. Zoo. 55:411-420.
2. Arricau, N., D. Hermant, H. Waxin, C. Ecobichon, P. S. Duffey, and M. Y. Popoff. 1998. The RcsB-RcsC regulatory system of Salmonella typhi differentially modulates the expression of invasion proteins, flagellin and Vi antigen in response to osmolarity. Mol. Microbiol. 29:835-850.
3. Baron, L. S., D. J. Kopecko, S. M. McCowen, N. J. Snellings, E. M. Johnson, W. C. Reid, and C. A. Life. 1982. Genetic and molecular studies of the regulation of atypical citrate utilization and variable Vi antigen expression in enteric bacteria. Basic Life Sci. 19:175-194.
4. Barthel, M., S. Hapfelmeier, L. Quintanilla-Martinez, M. Kremer, M. Rohde, M. Hogardt, K. Pfeffer, H. Russmann, and W. D. Hardt. 2003. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71:2839-2858.
5. Bohnhoff, M., and C. P. Miller. 1962. Enhanced susceptibility to Salmonella infection in streptomycin-treated mice. J. Infect. Dis. 111:117-127.
6. Bozic, C. R., L. F. Kolakowski, Jr., N. P. Gerard, C. Garcia-Rodriguez, C. von Uexkull-Guldenband, M. J. Conklyn, R. Breslow, H. J. Showell, and C. Gerard. 1995. Expression and biologic characterization of the murine chemokine KC. J. Immunol. 154:6048-6057.
7. Coburn, B., Y. Li, D. Owen, B. A. Vallence, and B. B. Finlay. 2005. Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect. Immun. 73:3219-3227.
8. Collins, F. M., and P. B. Carter. 1978. Growth of salmonellae in orally infected germfree mice. Infect. Immun. 21:41-47.
9. Day, D. W., B. K. Mandal, and B. C. Morson. 1978. The rectal biopsy appearances in Salmonella colitis. Histopathology 2:117-131.
10. Frost, A. J., A. P. Bland, and T. S. Wallis. 1997. The early dynamic response of the calf ileal epithelium to Salmonella typhimurium. Vet. Pathol. 34:369-386.
11. Gaines, S., H. Sprinz, J. G. Tully, and W. D. Tigertt. 1968. Studies on infection and immunity in experimental typhoid fever. VII. The distribution of Salmonella typhi in chimpanzee tissue following oral challenge, and the relationship between the numbers of bacilli and morphologic lesions. J. Infect. Dis. 118:293-306.
12. Grant, S. G. N., J. Jessee, F. R. Bloom, and D. Hanahan. 1990. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc. Natl. Acad. Sci. USA 87:4645-4649.
13. Hapfelmeier, S., K. Ehrbar, B. Stecher, M. Barthel, M. Kremer, and W. D. Hardt. 2004. Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72:795-809.
14. Hapfelmeier, S., B. Stecher, M. Barthel, M. Kremer, A. J. Muller, M. Heikenwalder, T. Stallmach, M. Hensel, K. Pfeffer, S. Akira, and W. D. Hardt. 2005. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol. 174:1675-1685.
15. Happel, K. I., P. J. Dubin, M. Zheng, N. Ghilardi, C. Lockhart, L. J. Quinton, A. R. Odden, J. E. Shellito, G. J. Bagby, S. Nelson, and J. K. Kolls. 2005. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J Exp. Med. 202:761-769.
16. Happel, K. I., M. Zheng, E. Young, L. J. Quinton, E. Lockhart, A. J. Ramsay, J. E. Shellito, J. R. Schurr, G. J. Bagby, S. Nelson, and J. K. Kolls. 2003. Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. I. Immunol. 170:4432-4436.
17. Harris, J. C., H. L. Dupont, and R. B. Hornick. 1972. Fecal leukocytes in diarrheal illness. Ann. Intern. Med. 76:697-703.
18. Hashimoto, Y., T. Ezaki, N. Li, and H. Yamamoto. 1991. Molecular cloning of the ViaB region of Salmonella typhi. FEMS Microbiol. Lett. 69:53-56.
19. Hirose, K., T. Ezaki, M. Miyake, T. Li, A. Q. Khan, Y. Kawamura, H. Yokoyama, and T. Takami. 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.
20. Humphries, A. D., M. Raffatellu, S. Winter, E. H. Weening, R. A. Kingsley, R. Droleskey, S. Zhang, J. Figueiredo, S. Khare, J. Nunes, L. G. Adams, R. M. Tsolis, and A. J. Bäumler. 2003. The use of flow cytometry to detect expression of subunits encoded by 11 Salmonella enterica serotype Typhimurium fimbrial operons. Mol. Microbiol. 48:1357-1376.
21. Kao, C. Y., Y. Chen, P. Thai, S. Wachi, F. Huang, C. Kim, R. W. Harper, and R. Wu. 2004. IL-17 markedly up-regulates beta-defensin-2 expression in human airway epithelium via IAK and NF-kappaB signaling pathways. I. Immunol. 173:3482-3491.
22. Kolyva, S., H. Waxin, and M. Y. Popoff. 1992. The Vi antigen of Salmonella typhi: molecular analysis of the viaB locus. J Gen. Microbiol. 138:297-304.
23. Kraus, M. D., B. Amatya, and Y. Kimula. 1999. Histopathology of typhoid enteritis: morphologic and immunophenotypic findings. Mod. Pathol. 12:949-955.
24. Laan, M., Z. H. Cui, H. Hoshino, J. Lotvall, M. Sjostrand, D. C. Gruenert, B. E. Skoogh, and A. Linden. 1999. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J. Immunol. 162:2347-2352.
25. McCormick, B. A., S. I. Miller, D. Carnes, and J. L. Madara. 1995. Transepithelial signaling to neutrophils by salmonellae: a novel virulence mechanism for gastroenteritis. Infect. Immun. 63:2302-2309.
26. McGovern, V. J., and L. J. Slavutin. 1979. Pathology of salmonella colitis. Am. J. Surg. Pathol. 3:483-490.
27. Miyake, M., L. Zhao, T. Ezaki, K. Hirose, A. Q. Khan, Y. Kawamura, R. Shima, M. Kamijo, T. Masuzawa, and Y. Yanagihara. 1998. Vi-deficient and nonfimbriated mutants of Salmonella typhi agglutinate human blood type antigens and are hyperinvasive. FEMS Microbiol. Lett. 161:75-82.
28. Modi, W. S., M. R. Amarante, M. Hanson, J. E. Womack, and A. Chidambaram. 1998. Assignment of the mouse and cow CXC chemokine genes. Cytogenet. Cell Genet. 81:213-216.
29. Mukawi, T. J. 1978. Histopathological study of typhoid perforation of the small intestines. Southeast Asian J. Trop. Med. Public Health 9:252-255.
30. Nguyen, Q. C., P. Everest, T. K. Tran, D. House, S. Murch, C. Parry, P. Connerton, V. B. Phan, S. D. To, P. Mastroeni, N. J. White, T. H. Tran, V. H. Vo, G. Dougan, J. J. Farrar, and J. Wain. 2004. A clinical, microbiological, and pathological study of intestinal perforation associated with typhoid fever. Clin. Infect. Dis. 39:61-67.
31. Oquendo, P., J. Alberta, D. Z. Wen, J. L. Graycar, R. Derynck, and C. D. Stiles. 1989. The platelet-derived growth factor-inducible KC gene encodes a secretory protein related to platelet alpha-granule proteins. J. Biol. Chem. 264:4133-4137.
32. Parkhill, J., G. Dougan, K. D. James, N. R. Thomson, D. Pickard, J. Wain, C. Churcher, K. L. Mungall, S. D. Bentley, M. T. Holden, M. Sebaihia, S. Baker, D. Basham, K. Brooks, T. Chillingworth, P. Connerton, A. Cronin, P. Davis, R. M. Davies, L. Dowd, N. White, J. Farrar, T. Feltwell, N. Hamlin, A. Haque, T. T. Hien, S. Holroyd, K. Jagels, A. Krogh, T. S. Larsen, S. Leather, S. Moule, P. O'Gaora, C. Parry, M. Quail, K. Rutherford, M. Simmonds, J. Skelton, K. Stevens, S. Whitehead, and B. G. Barrell. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848-852.
33. Prentki, P., and H. M. Krisch. 1984. In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303-313.
34. Que, J. U., S. W. Casey, and D. J. Hentges. 1986. Factors responsible for increased susceptibility of mice to intestinal colonization after treatment with streptomycin. Infect. Immun. 53:116-123.
35. Raffatellu, M., D. Chessa, R. P. Wilson, R. Dusold, S. Rubino, and A. J. Baumler. 2005. The Vi capsular antigen of Salmonella enterica serotype Typhi reduces Toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect. Immun. 73:3367-3374.
36. Raffatellu, M., D. Chessa, R. P. Wilson, C. Tukel, M. Akcelik, and A. J. Baumler. 2006. Capsule-mediated immune evasion: a new hypothesis explaining aspects of typhoid fever pathogenesis. Infect. Immun. 74:19-27.
37. Raffatellu, M., Y. H. Sun, R. P. Wilson, Q. T. Tran, D. Chessa, H. L. Andrews-Polymenis, S. D. Lawhon, J. F. Figueiredo, R. M. Tsolis, L. G. Adams, and A. J. Baumler. 2005. Host restriction of Salmonella enterica serotype Typhi is not caused by functional alteration of SipA, SopB, or SopD. Infect. Immun. 73:7817-7826.
38. Raffatellu, M., R. P. Wilson, D. Chessa, H. Andrews-Polymenis, Q. T. Tran, S. Lawhon, S. Khare, L. G. Adams, and A. J. Baumler. 2005. SipA, SopA, SopB, SopD and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect. Immun. 73:146-154.
39. Santos, R. L., R. M. Tsolis, S. Zhang, T. A. Ficht, A. J. Baumler, and L. G. Adams. 2001. Salmonella-induced cell death is not required for enteritis in calves. Infect. Immun. 69:4610-4617.
40. Santos, R. L., S. Zhang, R. M. Tsolis, A. J. Baumler, and L. G. Adams. 2002. Morphologic and molecular characterization of Salmonella typhimurium infection in neonatal calves. Vet. Pathol. 39:200-215.
41. Santos, R. L., S. Zhang, R. M. Tsolis, R. A. Kingsley, L. G. Adams, and A. J. Baumler. 2001. Animal models of Salmonella infections: enteritis vs. typhoid fever. Microb. Infect. 3:1335-1344.
42. Schmitt, C. K., J. S. Ikeda, S. C. Darnell, P. R. Watson, J. Bispham, T. S. Wallis, D. L. Weinstein, E. S. Metcalf, and A. D. O'Brien. 2001. Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69:5619-5625.
43. Sharma, A., and A. Qadri. 2004. Vi polysaccharide of Salmonella typhi targets the prohibitin family of molecules in intestinal epithelial cells and suppresses early inflammatory responses. Proc. Natl. Acad. Sci. USA 101: 17492-17497.
44. Shirai, Y., K. Sunakawa, Y. Ichihashi, and H. Yamaguchi. 1979. A morphological study in germfree mice (Salmonella infection). Exp. Pathol. 17:158-166.
45. Song, F., K. Ito, T. L. Denning, D. Kuninger, J. Papaconstantinou, W. Gourley, G. Klimpel, E. Balish, J. Hokanson, and P. B. Ernst. 1999. Expression of the neutrophil chemokine KC in the colon of mice with enterocolitis and by intestinal epithelial cell lines: effects of flora and proinflammatory cytokines. J. Immunol. 162:2275-2280.
46. Sprinz, H., E. J. Gangarosa, M. Williams, R. B. Hornick, and T. E. Woodward. 1966. Histopathology of the upper small intestines in typhoid fever. Biopsy study of experimental disease in man. Am. J. Dig. Dis. 11:615-624.
47. Stecher, B., A. J. Macpherson, S. Hapfelmeier, M. Kremer, T. Stallmach, and W. D. Hardt. 2005. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect. Immun. 73:3228-3241.
48. Stojiljkovic, I., A. J. Bäumler, and F. Heffron. 1995. Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J. Bacteriol. 177:1357-1366.
49. Suar, M., J. Jantsch, S. Hapfelmeier, M. Kremer, T. Stallmach, P. A. Barrow, and W. D. Hardt. 2006. Virulence of broad- and narrow-host-range Salmonella enterica serovars in the streptomycin-pretreated mouse model. Infect. Immun. 74:632-644.
50. Tekamp-Olson, P., C. Gallegos, D. Bauer, J. McClain, B. Sherry, M. Fabre, S. van Deventer, and A. Cerami. 1990. Cloning and characterization of cDNAs for murine macrophage inflammatory protein 2 and its human homologues. J Exp. Med. 172:911-919.
51. Tsolis, R. M., L. G. Adams, T. A. Ficht, and A. J. Bäumler. 1999. Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect. Immun. 67:4879-4885.
52. Tükel, C., M. Raffatellu, A. D. Humphries, R. P. Wilson, H. L. Andrews-Polymenis, T. Gull, J. F. Figueiredo, M. Wong, K. S. Michelsen, M. Akcelik, L. G. Adams, and A. J. Bäumler. 2005. CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype Typhimurium that is recognized by Toll-like receptor 2. Mol. Microbiol. 58:289-304.
53. Wallis, T. S., M. Wood, P. Watson, S. Paulin, M. Jones, and E. Galyov. 1999. Sips, Sops, and SPIs but not stn influence Salmonella enteropathogenesis. Adv. Exp. Med. Biol. 473:275-280.
54. Wang, R. F., and S. R. Kushner. 1991. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.
55. Watson, P. R., A. Benmore, S. A. Khan, P. W. Jones, D. J. Maskell, and T. S. Wallis. 2000. Mutation of waaN reduces Salmonella enterica serovar Typhimurium-induced enteritis and net secretion of type III secretion system 1-dependent proteins. Infect. Immun. 68:3768-3771.
56. Watson, P. R., E. E. Galyov, S. M. Paulin, P. W. Jones, and T. S. Wallis. 1998. Mutation of invH, but not stn, reduces Salmonella-induced enteritis in cattle. Infect. Immun. 66:1432-1438.
57. Watson, P. R., S. M. Paulin, A. P. Bland, S. J. Libby, P. W. Jones, and T. S. Wallis. 1999. Differential regulation of enteric and systemic salmonellosis by slyA. Infect. Immun. 67:4950-4954.
58. Wolpe, S. D., and A. Cerami. 1989. Macrophage inflammatory proteins 1 and 2: members of a novel superfamily of cytokines. FASEB J. 3:2565-2573.
59. Wray, C., and W. J. Sojka. 1978. Experimental Salmonella typhimurium infection in calves. Res. Vet. Sci. 25:139-143.
60. Ye, P., P. B. Garvey, P. Zhang, S. Nelson, G. Bagby, W. R. Summer, P. Schwarzenberger, J. E. Shellito, and J. K. Kolls. 2001. Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am. J. Respir. Cell Mol. Biol. 25:335-340.
61. Ye, P., F. H. Rodriguez, S. Kanaly, K. L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, J. E. Shellito, G. J. Bagby, S. Nelson, K. Charrier, J. J. Peschon, and J. K. Kolls. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194:519-527.
62. Zeng, H., A. Q. Carlson, Y. Guo, Y. Yu, L. S. Collier-Hyams, J. L. Madara, A. T. Gewirtz, and A. S. Neish. 2003. Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J. Immunol. 171:3668-3674.
63. Zhang, S., L. G. Adams, J. Nunes, S. Khare, R. M. Tsolis, and A. J. Bäumler. 2003. Secreted effector proteins of Salmonella enterica serotype Typhimurium elicit host-specific chemokine profiles in animal models of typhoid fever and enterocolitis. Infect. Immun. 71:4795-4803.
64. Zhang, S., R. A. Kingsley, R. L. Santos, H. Andrews-Polymenis, M. Raffatellu, J. Figueiredo, J. Nunes, R. M. Tsolis, L. G. Adams, and A. J. Bäumler. 2003. Molecular pathogenesis of Salmonella enterica serotype Typhimurium-induced diarrhea. Infect. Immun. 71:1-12.
65. Zhang, S., R. L. Santos, R. M. Tsolis, S. Mirold, W.-D. Hardt, L. G. Adams, and A. J. Bäumler. 2002. Phage mediated horizontal transfer of the sopE1 gene increases enteropathogenicity of Salmonella enterica serotype Typhimurium for calves. FEMS Microbiol. Lett. 217:243-247.
66. Zhang, S., R. L. Santos, R. M. Tsolis, S. Stender, W.-D. Hardt, A. J. Bäumler, and L. G. Adams. 2002. SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves infected with Salmonella enterica serotype Typhimurium. Infect. Immun. 70:3843-3855.