From bench to bedside: Stealth of enteroinvasive pathogens

Nature Reviews Microbiology

Volumn 6, Issue 12, 2008, Pages 883-892

  Tsolis, Renée M ^a   Young, Glenn M ^b   Solnick, Jay V ^a   Bäumler, Andreas J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABDOMINAL PAIN; ACUTE PHASE RESPONSE; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BODY TEMPERATURE; BRUCELLA; BRUCELLOSIS; CLINICAL FEATURE; DIARRHEA; FEVER; GASTROENTERITIS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; INTESTINE INFECTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SALMONELLA; SIGNAL TRANSDUCTION; TYPHOID FEVER; VOMITING; YERSINIA; YERSINIOSIS;

ANIMALS; BACTEREMIA; BRUCELLA; BRUCELLOSIS; DIARRHEA; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTIONS; GENOMIC ISLANDS; HOST-PATHOGEN INTERACTIONS; HUMANS; SALMONELLA TYPHI; SYNDROME; TYPHOID FEVER; VIRULENCE; YERSINIA; YERSINIA INFECTIONS;

BACTERIA (MICROORGANISMS); BRUCELLA; SALMONELLA; YERSINIA;

EID: 56349170256     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2012     Document Type: Review

References (107)

1. Guerrant, R. L. in Principles and Practices of Infectious Diseases (eds Mandell, G. L., Bennett, J. E. & Dolin, R.) 945-962 (Churchill Livingstone, New York, 1995).
2. Harris, J. C., Dupont, H. L. & Hornick, R. B. Fecal leukocytes in diarrheal illness. Ann. Intern. Med. 76, 697-703 (1972).
3. Herrington, D. A. et al. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168, 1487-1492 (1988).
4. Evans, D. G., Satterwhite, T. K., Evans, D. J. Jr & DuPont, H. L. Differences in serological responses and excretion patterns of volunteers challenged with enterotoxigenic Escherichia coli with and without the colonization factor antigen. Infect. Immun. 19 883-888 (1978).
5. Tacket, C. O. et al. Role of EspB in experimental human enteropathogenic Escherichia coli infection. Infect. Immun. 68, 3689-3695 (2000).
6. Finkelstein, R. A. & LoSpalluto, J. J. Pathogenesis of experimental cholera. Preparation and isolation of choleragen and choleragenoid. J. Exp. Med. 130, 185-202 (1969).
7. Raffatellu, M. et al. Capsule-mediated immune evasion: A new hypothesis explaining aspects of typhoid fever pathogenesis. Infect. Immun. 74, 19-27 (2006).
8. Tsolis, R. M., Adams, L. G., Ficht, T. A. & Bäumler, A. J. Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect. Immun. 67, 4879-4885 (1999).
9. Parsot, C. Shigella spp. and enteroinvasive Escherichia coli pathogenicity factors. FEMS Microbiol. Lett. 252, 11-18 (2005).
10. Iwasaki, A. & Medzhitov, R. Toll-like receptor control of the adaptive immune responses. Nature Immunol. 5, 987-995 (2004).
11. Franchi, L. et al. Intracellular NOD-like receptors in innate immunity, infection and disease. Cell. Microbiol. 10, 1-8 (2008).
12. Hoebe, K., Janssen, E. & Beutler, B. The interface between innate and adaptive immunity. Nature Immunol. 5, 971-974 (2004).
13. McGovern, V. J. & Slavutin, L. J. Pathology of Salmonella colitis. Am. J. Surg. Pathol. 3, 483-490 (1979).
14. Murphy, T. F. & Gorbach, S. L. Salmonella colitis. NY State J. Med. 82, 1236-1238 (1982).
15. Day, D. W., Mandal, B. K. & Morson, B. C. The rectal biopsy appearances in Salmonella colitis. Histopathology 2, 117-131 (1978).
16. Alvarado, T. Faecal leucocytes in patients with infectious diarrhoea. Trans. R. Soc. Trop. Med. Hyg. 77, 316-320 (1983).
17. Guyot, J., Gonvers, J. J., Pyndiah, N. & Heitz, M. Value of fecal leukocyte studies in cases of acute diarrhea. Schweiz. Med. Wochenschr. 114, 634-636 (1984).
18. Rothwell, N. J. Mechanisms of the pyrogenic actions of cytokines. Eur. Cytokine Netw. 1, 211-213 (1990).
19. Young, E. J. in Brucellosis: Clinical and Laboratory Aspects (eds Young, E. J. & Corbel, M. J.) 97-126 (CRC, Boca Raton, 1989).
20. Shorter, N. A., Thompson, M. D., Mooney, D. P. & Modlin, J. F. Surgical aspects of an outbreak of Yersinia enterocolitis. Pediatr. Surg. Int. 13, 2-5 (1998).
21. Bitar, R. & Tarpley, J. Intestinal perforation and typhoid fever: A historical and state-of-the-art review. Rev. Infect. Dis. 7, 257 (1985).
22. Sprinz, H., Gangarosa, E. J., Williams, M., Hornick, R. B. & Woodward, T. E. Histopathology of the upper small intestines in typhoid fever. Biopsy study of experimental disease in man. Am. J. Dig. Dis. 11, 615-624 (1966).
23. Nguyen, Q. C. et al. A clinical, microbiological, and pathological study of intestinal perforation associated with typhoid fever. Clin. Infect. Dis. 39, 61-67 (2004).
24. Mukawi, T. J. Histopathological study of typhoid perforation of the small intestines. Southeast Asian J. Trop. Med. Public Health 9 252-255 (1978).
25. Kraus, M. D., Amatya, B. & Kimula, Y. Histopathology of typhoid enteritis: Morphologic and immunophenotypic findings. Mod. Pathol. 12, 949-955 (1999).
26. Koj, A. Initiation of acute phase response and synthesis of cytokines. Biochim. Biophys. Acta 1317, 84-94 (1996).
27. Tewari, A., Buhles, W. C. Jr & Starnes, H. F. Jr. Preliminary report: effects of interleukin-1 on platelet counts. Lancet 336, 712-714 (1990).
28. Fleisher, G. R. Management of children with occult bacteremia who are treated in the emergency department. Rev. Infect. Dis. 13 (Suppl 2), 156-159 (1991).
29. Abdool Gaffar, M. S., Seedat, Y. K., Coovadia, Y. M. & Khan, Q. The white cell count in typhoid fever. Trop. Geogr. Med. 44, 23-27 (1992).
30. Bondarev, L. S., Tseneva, G., Domashenko, O. N., Rastuntsev, L. P. & Lugovaia Iu, V. The mononuclear syndrome in yersiniosis and pseudotuberculosis. Lik Sprava Sep-Dec, 154-156 (1994).
31. Waage, A., Brandtzaeg, P., Espevik, T. & Halstensen, A. Current understanding of the pathogenesis of gram-negative shock. Infect. Dis. Clin. North Am. 5, 781-791 (1991).
32. Beutler, B. & Kruys, V. Lipopolysaccharide signal transduction, regulation of tumor necrosis factor biosynthesis, and signaling by tumor necrosis factor itself. J. Cardiovasc. Pharmacol. 25, S1-S8 (1995).
33. Galofre, J. et al. Analysis of factors influencing the outcome and development of septic metastasis or relapse in Salmonella bacteremia. Clin. Infect. Dis. 18, 873-878 (1994).
34. Khan, S. A. et al. A lethal role for lipid A in Salmonella infections. Mol. Microbiol. 29, 571-579 (1998).
35. Engelberts, I., von Asmuth, E. J., van der Linden, C. J. & Buurman, W. A. The interrelation between TNF, IL-6, and PAF secretion induced by LPS in an in vivo and in vitro murine model. Lymphokine Cytokine Res. 10, 127-131 (1991).
36. Wilson, R. P. et al. The Vi-capsule prevents Toll-like receptor 4 recognition of Salmonella. Cell. Microbiol. 10, 876-890 (2008).
37. Kilbourn, R. G. & Belloni, P. Endothelial cell production of nitrogen oxides in response to interferon γ in combination with tumor necrosis factor, interleukin-1, or endotoxin. J. Natl Cancer Inst. 82 772-776 (1990).
38. Petros, A., Bennett, D. & Vallance, P. Effect of nitric oxide synthase inhibitors on hypotension in patients with septic shock. Lancet 338, 1557-1558 (1991).
39. Kilbourn, R. G. et al. Reversal of endotoxin-mediated shock by NG-methyl-L-arginine, an inhibitor of nitric oxide synthesis. Biochem. Biophys. Res. Commun. 172, 1132-1138 (1990).
40. Conkling, P. R., Greenberg, C. S. & Weinberg, J. B. Tumor necrosis factor induces tissue factor-like activity in human leukemia cell line U937 and peripheral blood monocytes. Blood 72, 128-133 (1988).
41. Carlsen, E., Flatmark, A. & Prydz, H. Cytokine-induced procoagulant activity in monocytes and endothelial cells. Further enhancement by cyclosporine. Transplantation 46, 575-580 (1988).
42. Butler, T., Bell, W. R., Levin, J., Linh, N. N. & Arnold, K. Typhoid fever. Studies of blood coagulation, bacteremia, and endotoxemia. Arch. Intern. Med. 138, 407-410 (1978).
43. Cunha, B. A. Typhoid fever: The temporal relations of key clinical diagnostic points. Lancet Infect. Dis. 6, 318-320; author reply 320-321 (2006).
44. Connor, B. A. & Schwartz, E. Typhoid and paratyphoid fever in travellers. Lancet Infect. Dis. 5, 623-628 (2005).
45. Dharmana, E., Keuter, M., Netea, M. G., Verschueren, I. C. & Kullberg, B. J. Divergent effects of tumor necrosis factor-alpha and lymphotoxin-alpha on lethal endotoxemia and infection with live Salmonella typhimurium in mice. Eur. Cytokine Netw. 13, 104-109 (2002).
46. Bignold, L. P., Rogers, S. D., Siaw, T. M. & Bahnisch, J. Inhibition of chemotaxis of neutrophil leukocytes to interleukin-8 by endotoxins of various bacteria. Infect. Immun. 59, 4255-4258 (1991).
47. Hayashi, F. et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103 (2001).
48. Gewirtz, A. T., Navas, T. A., Lyons, S., Godowski, P. J. & Madara, J. L. Cutting edge: Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167, 1882-1885 (2001).
49. Zeng, H. et al. Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J. Immunol. 171, 3668-3674 (2003).
50. Winter, S. E., Raffatellu, M., Wilson, R. P., Russmann, H. & 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, 247-261 (2008).
51. Wyant, T. L., Tanner, M. K. & Sztein, M. B. Salmonella typhi flagella are potent inducers of proinflammatory cytokine secretion by human monocytes. Infect. Immun. 67, 3619-3624 (1999).
52. Parkhill, J. et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413, 848-852 (2001).
53. Hirose, K. et al. 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 (1997).
54. Sharma, A. & Qadri, A. 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 (2004).
55. Raffatellu, M. et al. 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 (2005).
56. Heyns, K. & Kiessling, G. Strukturaufklarung des Vi-antigens aus Citrobacter freundii (E. coli) 5396/38. Carbohydr. Res. 3 340-353 (1967).
57. Virlogeux, I., Waxin, H., Ecobichon, C. & Popoff, M. Y. Role of the viaB locus in synthesis, transport and expression of Salmonella typhi Vi antigen. Microbiology 141, 3039-3047 (1995).
58. Raffatellu, M. et al. 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 (2007).
59. Barquero-Calvo, E. et al. Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS ONE 2, e631 (2007).
60. Lapaque, N. et al. Differential inductions of TNF-α and IGTP, IIGP by structurally diverse classic and non-classic lipopolysaccharides. Cell. Microbiol. 8, 401-413 (2006).
61. Andersen-Nissen, E. et al. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl Acad. Sci. USA 102, 9247-9252 (2005).
62. + T cells. Int. Immunol. 5, 877-883 (1993).
63. Zhan, Y., Kelso, A. & Cheers, C. Cytokine production in the murine response to Brucella infection or immunization with antigenic extracts. Immunology 80, 458-464 (1993).
64. Roux, C. M. et al. Brucella requires a functional Type IV secretion system to elicit innate immune responses in mice. Cell. Microbiol. 9, 1851-1869 (2007).
65. Oellerich, M. F. et al. Yersinia enterocolitica infection of mice reveals clonal invasion and abscess formation. Infect. Immun. 75, 3802-3811 (2007).
66. Marceau, M. Transcriptional regulation in Yersinia: An update. Curr. Issues Mol. Biol. 7, 151-177 (2005).
67. Bottone, E. J. Yersinia enterocolitica: A panoramic view of a charismatic microorganism. CRC Crit. Rev. Microbiol. 5, 211-241 (1977).
68. Young, G. M., Smith, M. J., Minnich, S. A. & Miller, V. L. The Yersinia enterocolitica motility master regulatory operon, flhDC is required for flagellin production, swimming motility, and swarming motility. J. Bacteriol. 181, 2823-2833 (1999).
69. Horne, S. M. & Pruss, B. M. Global gene regulation in Yersinia enterocolitica: Effect of FliA on the expression levels of flagellar and plasmid-encoded virulence genes. Arch. Microbiol. 185, 115-126 (2006).
70. Kapatral, V., Olson, J. W., Pepe, J. C., Miller, V. L. & Minnich, S. A. Temperature-dependent regulation of Yersinia enterocolitica class III flagellar genes. Mol. Microbiol. 19, 1061-1071 (1996).
71. Kapatral, V. et al. Gene array analysis of Yersinia enterocolitica FlhD and FlhC: Regulation of enzymes affecting synthesis and degradation of carbamoylphosphate. Microbiology 150, 2289-2300 (2004).
72. Kapatral, V. & Minnich, S. A. Co-ordinate, temperature-sensitive regulation of the three Yersinia enterocolitica flagellin genes. Mol. Microbiol. 17, 49-56 (1995).
73. Minnich, S. A. & Rohde, H. N. A rationale for repression and/or loss of motility by pathogenic Yersinia in the mammalian host. Adv. Exp. Med. Biol. 603, 298-310 (2007).
74. Rebeil, R., Ernst, R. K., Gowen, B. B., Miller, S. I. & Hinnebusch, B. J. Variation in lipid A structure in the pathogenic yersiniae. Mol. Microbiol. 52, 1363-1373 (2004).
75. Guo, L. et al. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95, 189-198 (1998).
76. Oertelt, C., Lindner, B., Skurnik, M. & Holst, O. Isolation and structural characterization of an R-form lipopolysaccharide from Yersinia enterocolitica serotype O:8. Eur. J. Biochem. 268 554-564 (2001).
77. Kawahara, K., Tsukano, H., Watanabe, H., Lindner, B. & Matsuura, M. Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect. Immun. 70, 4092-4098 (2002).
78. Logsdon, L. K. & Mecsas, J. A non-invasive quantitative assay to measure murine intestinal inflammation using the neutrophil marker lactoferrin. J. Immunol. Methods 313, 183-190 (2006).
79. Carter, P. B. Pathogenicity of Yersinia enterocolitica for mice. Infect. Immun. 11, 164-170 (1975).
80. Rivano, M. T. et al. Histiocytic necrotizing lymphadenitis without granulocytic infiltration (Kikuchi's lymphadenitis). Morphological and immunohistochemical study of eight cases. Histopathology 11, 1013-1027 (1987).
81. Tipple, M. A. et al. Sepsis associated with transfusion of red cells contaminated with Yersinia enterocolitica. Transfusion 30 207-213 (1990).
82. Arduino, M. J. et al. Growth and endotoxin production of Yersinia enterocolitica and Enterobacter agglomerans in packed erythrocytes. J. Clin. Microbiol. 27, 1483-1485 (1989).
83. Schwalbe, B. et al. Fatal Yersinia infection after intraoperative transfusion. Anasthesiol. Intensivmed. Notfallmed. Schmerzther. 31, 658-660 (1996).
84. Bach, A., Bohrer, H. & Mathias, D. Transfusion-induced Yersinia infection. Dtsch. Med. Wochenschr. 115, 1232-1234 (1990).
85. Sansonetti, P. J., Arondel, J., Huerre, M., Harada, A. & Matsushima, K. Interleukin-8 controls bacterial transepithelial translocation at the cost of epithelial destruction in experimental shigellosis. Infect. Immun. 67, 1471-1480 (1999).
86. Raffatellu, M. et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nature Med. 14, 421-428 (2008).
87. Godinez, I. et al. T cells help to amplify inflammatory responses induced by Salmonella enterica serotype Typhimurium in the intestinal mucosa. Infect. Immun. 76, 2008-2017 (2008).
88. Bottone, E. J., Gullans, C. R. & Sierra, M. F. Disease spectrum of Yersinia enterocolitica serogroup 0:3, the predominant cause of human infection in New York City. Contrib. Microbiol. Immunol. 9, 56-60 (1987).
89. Shapiro, E. D. Yersinia enterocolitica septicemia in normal infants. Am. J. Dis. Child. 135, 477-478 (1981).
90. Piroth, L., Meyer, P., Bielefeld, P. & Besancenot, J. F. Yersinia bacteremia and iron overload. Rev. Med. Interne 18, 932-938 (1997).
91. Robins-Browne, R. M., Prpic, J. K. & Stuart, S. J. Yersiniae and iron. A study in host-parasite relationships. Contrib. Microbiol. Immunol. 9, 254-258 (1987).
92. Ku, C. L. et al. Selective predisposition to bacterial infections in IRAK-4-deficient children: IRAK-4-dependent TLRs are otherwise redundant in protective immunity. J. Exp. Med. 204, 2407-2422 (2007).
93. Knirel, Y. A. et al. Temperature-dependent variations and intraspecies diversity of the structure of the lipopolysaccharide of Yersinia pestis. Biochemistry 44, 1731-1743 (2005).
94. Montminy, S. W. et al. Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nature Immunol. 7, 1066-1073 (2006).
95. Finkelstein, R. A., Boesman, M., Neoh, S. H., LaRue, M. K. & Delaney, R. Dissociation and recombination of the subunits of the cholera enterotoxin (choleragen). J. Immunol. 113, 145-150 (1974).
96. Gill, D. M. The arrangement of subunits in cholera toxin. Biochemistry 15, 1242-1248 (1976).
97. King, C. A. & Van Heyningen, W. E. Deactivation of cholera toxin by a sialidase-resistant monosialosylganglioside. J. Infect. Dis. 127, 639-647 (1973).
98. van Heyningen, S. The subunits of cholera toxin: Structure, stoichiometry, and function. J. Infect. Dis. 133 (Suppl.), 5-13 (1976).
99. Cassel, D. & Selinger, Z. Mechanism of adenylate cyclase activation by cholera toxin: Inhibition of GTP hydrolysis at the regulatory site. Proc. Natl Acad. Sci. USA 74, 3307-3311 (1977).
100. Mekalanos, J. J., Collier, R. J. & Romig, W. R. Enzymic activity of cholera toxin. II. Relationships to proteolytic processing, disulfide bond reduction, and subunit composition. J. Biol. Chem. 254, 5855-5861 (1979).
101. Mekalanos, J. J., Collier, R. J. & Romig, W. R. Enzymic activity of cholera toxin. I. New method of assay and the mechanism of ADP-ribosyl transfer. J. Biol. Chem. 254, 5849-5854 (1979).
102. Gill, D. M. Mechanism of action of cholera toxin. Adv. Cyclic Nucleotide Res. 8, 85-118 (1977).
103. Cassel, D. & Pfeuffer, T. Mechanism of cholera toxin action: Covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc. Natl Acad. Sci. USA 75, 2669-2673 (1978).
104. Santos, R. L., Zhang, S., Tsolis, R. M., Bäumler, A. J. & Adams, L. G. Morphologic and molecular characterization of Salmonella typhimurium infection in neonatal calves. Vet. Pathol. 39 200-215 (2002).
105. Santos, R. L., Tsolis, R. M., Bäumler, A. J. & Adams, L. G. Dynamics of hematologic and blood chemical changes in Salmonella typhimurium infected calves. Am. J. Vet. Res. 63, 1145-1150 (2002).
106. Zhang, H., Zhou, Y., Bao, H. & Liu, H. W. Vi antigen biosynthesis in Salmonella typhi: Characterization of UDP-N-acetylglucosamine C-6 dehydrogenase (TviB) and UDP-N-acetylglucosaminuronic acid C-4 epimerase (TviC). Biochemistry 45, 8163-8173 (2006).
107. Ferguson, G. P. et al. Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. Proc. Natl Acad. Sci. USA 101, 5012-5017 (2004).