Salmonella Typhimurium diarrhea: Switching the mucosal epithelium from homeostasis to defense

Current Opinion in Immunology

Volumn 23, Issue 4, 2011, Pages 456-463

  Kaiser, Patrick ^a   Hardt, Wolf Dietrich ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 18; INTERLEUKIN 1BETA CONVERTING ENZYME; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN AVRA; PROTEIN SOPE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; BACTERIAL VIRULENCE; DIARRHEA; ENTEROPATHY; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; INNATE IMMUNITY; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE INFECTION; INTESTINE MUCOSA; MUCOSA INFLAMMATION; NONHUMAN; PROTEIN PROTEIN INTERACTION; REVIEW; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SIGNAL TRANSDUCTION;

ADAPTIVE IMMUNITY; ANIMALS; BACTERIAL PROTEINS; BYSTANDER EFFECT; CYTOKINES; DIARRHEA; EPITHELIAL CELLS; GASTROENTERITIS; GENE EXPRESSION REGULATION; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INFLAMMATION; INTESTINAL MUCOSA; METAGENOME; MICE; SALMONELLA INFECTIONS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; STREPTOMYCIN; VIRULENCE;

EID: 80052350106     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2011.06.004     Document Type: Review

References (97)

1. Turner J.R. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009, 9:799-809.
2. Brandl K., Plitas G., Schnabl B., DeMatteo R.P., Pamer E.G. MyD88-mediated signals induce the bactericidal lectin RegIII gamma and protect mice against intestinal Listeria monocytogenes infection. J Exp Med 2007, 204:1891-1900.
3. Flo T.H., Smith K.D., Sato S., Rodriguez D.J., Holmes M.A., Strong R.K., Akira S., Aderem A. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004, 432:917-921.
4. Hooper L.V., Macpherson A.J. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 2010, 10:159-169.
5. Vaishnava S., Behrendt C.L., Hooper L.V. Innate immune responses to commensal bacteria in the gut epithelium. J Pediatr Gastroenterol Nutr 2008, 46(Suppl. 1):E10-E11.
6. Vaishnava S., Behrendt C.L., Ismail A.S., Eckmann L., Hooper L.V. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci U S A 2008, 105:20858-20863.
7. Wells J.M., Rossi O., Meijerink M., van Baarlen P. Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci U S A 2011, 108(Suppl. 1):4607-4614.
8. Kobayashi K., Hernandez L.D., Galan J.E., Janeway C.A., Medzhitov R., Flavell R.A. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 2002, 110:191-202.
9. Nakagawa R., Naka T., Tsutsui H., Fujimoto M., Kimura A., Abe T., Seki E., Sato S., Takeuchi O., Takeda K., et al. SOCS-1 participates in negative regulation of LPS responses. Immunity 2002, 17:677-687.
10. Zaph C., Troy A.E., Taylor B.C., Berman-Booty L.D., Guild K.J., Du Y., Yost E.A., Gruber A.D., May M.J., Greten F.R., et al. Epithelial-cell-intrinsic IKK-beta expression regulates intestinal immune homeostasis. Nature 2007, 446:552-556.
11. Gribar S.C., Anand R.J., Sodhi C.P., Hackam D.J. The role of epithelial Toll-like receptor signaling in the pathogenesis of intestinal inflammation. J Leukoc Biol 2008, 83:493-498.
12. Chassin C., Kocur M., Pott J., Duerr C.U., Gutle D., Lotz M., Hornef M.W. miR-146a mediates protective innate immune tolerance in the neonate intestine. Cell Host Microbe 2010, 8:358-368.
13. Hornef M.W., Frisan T., Vandewalle A., Normark S., Richter-Dahlfors A. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 2002, 195:559-570.
14. Hornef M.W., Normark B.H., Vandewalle A., Normark S. Intracellular recognition of lipopolysaccharide by toll-like receptor 4 in intestinal epithelial cells. J Exp Med 2003, 198:1225-1235.
15. Lotz M., Gutle D., Walther S., Menard S., Bogdan C., Hornef M.W. Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J Exp Med 2006, 203:973-984.
16. Shibolet O., Podolsky D.K. TLRs in the Gut IV. Negative regulation of Toll-like receptors and intestinal homeostasis: addition by subtraction. Am J Physiol Gastrointest Liver Physiol 2007, 292:G1469-G1473.
17. Kobayashi K.S., Chamaillard M., Ogura Y., Henegariu O., Inohara N., Nunez G., Flavell R.A. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005, 307:731-734.
18. Schilling J.D., Martin S.M., Hung C.S., Lorenz R.G., Hultgren S.J. Toll-like receptor 4 on stromal and hematopoietic cells mediates innate resistance to uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 2003, 100:4203-4208.
19. Hansson G.C., Johansson M.E. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Gut Microbes 2010, 1:51-54.
20. Stecher B., Chaffron S., Kappeli R., Hapfelmeier S., Freedrich S., Weber T.C., Kirundi J., Suar M., McCoy K.D., von Mering C., et al. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 2010, 6:e1000711.
21. Girardin S.E., Boneca I.G., Carneiro L.A., Antignac A., Jehanno M., Viala J., Tedin K., Taha M.K., Labigne A., Zahringer U., et al. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 2003, 300:1584-1587.
22. Girardin S.E., Boneca I.G., Viala J., Chamaillard M., Labigne A., Thomas G., Philpott D.J., Sansonetti P.J. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 2003, 278:8869-8872.
23. Meylan E., Tschopp J., Karin M. Intracellular pattern recognition receptors in the host response. Nature 2006, 442:39-44.
24. Warren S.E., Mao D.P., Rodriguez A.E., Miao E.A., Aderem A. Multiple Nod-like receptors activate caspase 1 during Listeria monocytogenes infection. J Immunol 2008, 180:7558-7564.
25. Chen L.M., Hobbie S., Galan J.E. Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 1996, 274:2115-2118.
26. Eckmann L., Kagnoff M.F., Fierer J. Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun 1993, 61:4569-4574.
27. Fierer J., Eckmann L., Kagnoff M. IL-8 secreted by epithelial cells invaded by bacteria. Infect Agents Dis 1993, 2:255-258.
28. Jung H.C., Eckmann L., Yang S.K., Panja A., Fierer J., Morzycka-Wroblewska E., Kagnoff M.F. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 1995, 95:55-65.
29. Dolowschiak T., Chassin C., Ben Mkaddem S., Fuchs T.M., Weiss S., Vandewalle A., Hornef M.W. Potentiation of epithelial innate host responses by intercellular communication. PLoS Pathog 2010, 6:e1001194.
30. Hardt W.D. Infected cell in trouble: bystander cells ring the bell. Immunity 2010, 33:652-654.
31. Kasper C.A., Sorg I., Schmutz C., Tschon T., Wischnewski H., Kim M.L., Arrieumerlou C. Cell-cell propagation of NF-kappaB transcription factor and MAP kinase activation amplifies innate immunity against bacterial infection. Immunity 2010, 33:804-816.
32. Barthel M., Hapfelmeier S., Quintanilla-Martinez L., Kremer M., Rohde M., Hogardt M., Pfeffer K., Russmann H., Hardt W.D. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 2003, 71:2839-2858.
33. Stecher B., Hardt W.D. Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol 2010.
34. Altmeyer M., Barthel M., Eberhard M., Rehrauer H., Hardt W.D., Hottiger M.O. Absence of poly(ADP-ribose) polymerase 1 delays the onset of Salmonella enterica serovar Typhimurium-induced gut inflammation. Infect Immun 2010, 78:3420-3431.
35. Boyd J.F. Pathology of the alimentary tract in Salmonella typhimurium food poisoning. Gut 1985, 26:935-944.
36. Day D.W., Mandal B.K., Morson B.C. The rectal biopsy appearances in Salmonella colitis. Histopathology 1978, 2:117-131.
37. Hapfelmeier S., Hardt W.D. A mouse model for S. typhimurium-induced enterocolitis. Trends Microbiol 2005, 13:497-503.
38. Raffatellu M., Santos R.L., Chessa D., Wilson R.P., Winter S.E., Rossetti C.A., Lawhon S.D., Chu H., Lau T., Bevins C.L., 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 2007, 75:4342-4350.
39. Tsolis R.M., Kingsley R.A., Townsend S.M., Ficht T.A., Adams L.G., Baumler A.J. Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections. Adv Exp Med Biol 1999, 473:261-274.
40. Zhang S., Adams L.G., Nunes J., Khare S., Tsolis R.M., Baumler A.J. Secreted effector proteins of Salmonella enterica serotype typhimurium elicit host-specific chemokine profiles in animal models of typhoid fever and enterocolitis. Infect Immun 2003, 71:4795-4803.
41. Hapfelmeier S., Ehrbar K., Stecher B., Barthel M., Kremer M., Hardt W.D. 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 2004, 72:795-809.
42. Hapfelmeier S., Stecher B., Barthel M., Kremer M., Muller A.J., Heikenwalder M., Stallmach T., Hensel M., Pfeffer K., Akira S., et al. 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 2005, 174:1675-1685.
43. Raffatellu M., Wilson R.P., Chessa D., Andrews-Polymenis H., Tran Q.T., Lawhon S., Khare S., Adams L.G., Baumler A.J. SipA, SopA, SopB SopD, and SopE2 contribute to Salmonella enterica serotype typhimurium invasion of epithelial cells. Infect Immun 2005, 73:146-154.
44. Stecher B., Robbiani R., Walker A.W., Westendorf A.M., Barthel M., Kremer M., Chaffron S., Macpherson A.J., Buer J., Parkhill J., et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 2007, 5:2177-2189.
45. Raffatellu M., George M.D., Akiyama Y., Hornsby M.J., Nuccio S.P., Paixao T.A., Butler B.P., Chu H., Santos R.L., Berger T., et al. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 2009, 5:476-486.
46. Stecher B., Barthel M., Schlumberger M.C., Haberli L., Rabsch W., Kremer M., Hardt W.D. Motility allows S. Typhimurium to benefit from the mucosal defence. Cell Microbiol 2008, 10:1166-1180.
47. Winter S.E., Thiennimitr P., Winter M.G., Butler B.P., Huseby D.L., Crawford R.W., Russell J.M., Bevins C.L., Adams L.G., Tsolis R.M., et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 2010, 467:426-429.
48. Hapfelmeier S., Stecher B., Barthel M., Kremer M., Müller A., Heikenwalder M., Stallmach T., Hensel M., Pfeffer K., Akira S., et al. The Salmonella Pathogenicity Island (SPI)-1 and SPI-2 Type III secretion systems allow Salmonella Serovar Typhimurium to trigger Colitis via MyD88-dependent and MyD88-independent mechanisms. J Immunol 2005, 174:1675-1685.
49. Hapfelmeier S., Muller A.J., Stecher B., Kaiser P., Barthel M., Endt K., Eberhard M., Robbiani R., Jacobi C.A., Heikenwalder M., et al. Microbe sampling by mucosal dendritic cells is a discrete MyD88-independent step in DeltainvG S. Typhimurium colitis. J Exp Med 2008, 205:437-450.
50. Varol C., Zigmond E., Jung S. Securing the immune tightrope: mononuclear phagocytes in the intestinal lamina propria. Nat Rev Immunol 2010, 10:415-426.
51. Baumler A.J., Tsolis R.M., Heffron F. Contribution of fimbrial operons to attachment to and invasion of epithelial cell lines by Salmonella typhimurium. Infect Immun 1996, 64:1862-1865.
52. Gerlach R.G., Claudio N., Rohde M., Jackel D., Wagner C., Hensel M. Cooperation of Salmonella pathogenicity islands 1 and 4 is required to breach epithelial barriers. Cell Microbiol 2008, 10:2364-2376.
53. Gerlach R.G., Jackel D., Stecher B., Wagner C., Lupas A., Hardt W.D., Hensel M. Salmonella Pathogenicity Island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol 2007, 9:1834-1850.
54. Misselwitz B., Kreibich S.K., Rout S., Stecher B., Periaswamy B., Hardt W.D. Salmonella enterica serovar Typhimurium binds to HeLa cells via Fim-mediated reversible adhesion and irreversible type three secretion system 1-mediated docking. Infect Immun 2011, 79:330-341.
55. Muller A.J., Hoffmann C., Galle M., Van Den Broeke A., Heikenwalder M., Falter L., Misselwitz B., Kremer M., Beyaert R., Hardt W.D. The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe 2009, 6:125-136.
56. Hardt W.D., Chen L.M., Schuebel K.E., Bustelo X.R., Galan J.E. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 1998, 93:815-826.
57. Zhou D., Mooseker M.S., Galan J.E. Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 1999, 283:2092-2095.
58. Zhang S., Santos R.L., Tsolis R.M., Stender S., Hardt W.D., Baumler A.J., Adams L.G. The Salmonella enterica serotype Typhimurium effector proteins SipA, SopA, SopB SopD, and SopE2 Act in concert to induce diarrhea in calves. Infect Immun 2002, 70:3843-3855.
59. Akira S., Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004, 4:499-511.
60. Franchi L., Warner N., Viani K., Nunez G. Function of Nod-like receptors in microbial recognition and host defense. Immunol Rev 2009, 227:106-128.
61. Vijay-Kumar M., Aitken J.D., Gewirtz A.T. Toll like receptor-5: protecting the gut from enteric microbes. Semin Immunopathol 2008, 30:11-21.
62. Arpaia N., Godec J., Lau L., Sivick K.E., McLaughlin L.M., Jones M.B., Dracheva T., Peterson S.N., Monack D.M., Barton G.M. TLR signaling is required for Salmonella typhimurium virulence. Cell 2011, 144:675-688.
63. Geddes K., Rubino S., Streutker C., Cho J.H., Magalhaes J.G., Le Bourhis L., Selvanantham T., Girardin S.E., Philpott D.J. Nod1 and Nod2 regulation of inflammation in the Salmonella colitis model. Infect Immun 2010, 78:5107-5115.
64. Raupach B., Peuschel S.K., Monack D.M., Zychlinsky A. Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect Immun 2006, 74:4922-4926.
65. Bruno V.M., Hannemann S., Lara-Tejero M., Flavell R.A., Kleinstein S.H., Galan J.E. Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog 2009, 5:e1000538.
66. Li H., Xu H., Zhou Y., Zhang J., Long C., Li S., Chen S., Zhou J.M., Shao F. The phosphothreonine lyase activity of a bacterial type III effector family. Science 2007, 315:1000-1003.
67. Arbibe L., Kim D.W., Batsche E., Pedron T., Mateescu B., Muchardt C., Parsot C., Sansonetti P.J. An injected bacterial effector targets chromatin access for transcription factor NF-kappaB to alter transcription of host genes involved in immune responses. Nat Immunol 2007, 8:47-56.
68. Jones R.M., Wu H., Wentworth C., Luo L., Collier-Hyams L., Neish A.S. Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host Microbe 2008, 3:233-244.
69. Kim D.W., Lenzen G., Page A.L., Legrain P., Sansonetti P.J., Parsot C. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci U S A 2005, 102:14046-14051.
70. Du F., Galan J.E. Selective inhibition of type III secretion activated signaling by the Salmonella effector AvrA. PLoS Pathog 2009, 5:e1000595.
71. Wallis T.S., Galyov E.E. Molecular basis of Salmonella-induced enteritis. Mol Microbiol 2000, 36:997-1005.
72. Hoffmann C., Galle M., Dilling S., Kappeli R., Muller A.J., Songhet P., Beyaert R., Hardt W.D. In macrophages, caspase-1 activation by SopE and the type III secretion system-1 of S. typhimurium can proceed in the absence of flagellin. PLoS One 2010, 5:e12477.
73. Muller A.J., Hoffmann C., Hardt W.D. Caspase-1 activation via Rho GTPases: a common theme in mucosal infections?. PLoS Pathog 2010, 6:e1000795.
74. Huang Z., Sutton S.E., Wallenfang A.J., Orchard R.C., Wu X., Feng Y., Chai J., Alto N.M. Structural insights into host GTPase isoform selection by a family of bacterial GEF mimics. Nat Struct Mol Biol 2009, 16:853-860.
75. Lee C.A., Silva M., Siber A.M., Kelly A.J., Galyov E., McCormick B.A. A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc Natl Acad Sci U S A 2000, 97:12283-12288.
76. Tsolis R.M., Adams L.G., Hantman M.J., Scherer C.A., Kimbrough T., Kingsley R.A., Ficht T.A., Miller S.I., Baumler A.J. SspA is required for lethal Salmonella enterica serovar Typhimurium infections in calves but is not essential for diarrhea. Infect Immun 2000, 68:3158-3163.
77. Hayward R.D., Cain R.J., McGhie E.J., Phillips N., Garner M.J., Koronakis V. Cholesterol binding by the bacterial type III translocon is essential for virulence effector delivery into mammalian cells. Mol Microbiol 2005, 56:590-603.
78. Kaniga K., Tucker S., Trollinger D., Galan J.E. Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J Bacteriol 1995, 177:3965-3971.
79. Hayward R.D., Koronakis V. Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J 1999, 18:4926-4934.
80. Kaniga K., Trollinger D., Galan J.E. Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. J Bacteriol 1995, 177:7078-7085.
81. Tsolis R.M., Townsend S.M., Miao E.A., Miller S.I., Ficht T.A., Adams L.G., Baumler A.J. Identification of a putative Salmonella enterica serotype Typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect Immun 1999, 67:6385-6393.
82. Diao J., Zhang Y., Huibregtse J.M., Zhou D., Chen J. Crystal structure of SopA, a Salmonella effector protein mimicking a eukaryotic ubiquitin ligase. Nat Struct Mol Biol 2008, 15:65-70.
83. Wood M.W., Jones M.A., Watson P.R., Siber A.M., McCormick B.A., Hedges S., Rosquist R., Wallis T.S., Galyov E.E. The secreted effector protein of Salmonella dublin SopA, is translocated into eukaryotic cells and influences the induction of enteritidis. Cell Microbiol 2000, 2:293-303.
84. Zhang Y., Higashide W.M., McCormick B.A., Chen J., Zhou D. The inflammation-associated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol Microbiol 2006, 62:786-793.
85. Hernandez L.D., Hueffer K., Wenk M.R., Galan J.E. Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 2004, 304:1805-1807.
86. Norris F.A., Wilson M.P., Wallis T.S., Galyov E.E., Majerus P.W. SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci U S A 1998, 95:14057-14059.
87. Terebiznik M.R., Vieira O.V., Marcus S.L., Slade A., Yip C.M., Trimble W.S., Meyer T., Finlay B.B., Grinstein S. Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella. Nat Cell Biol 2002, 4:766-773.
88. Zhou D., Chen L.M., Hernandez L., Shears S.B., Galan J.E. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol 2001, 39:248-260.
89. Jiang X., Rossanese O.W., Brown N.F., Kujat-Choy S., Galan J.E., Finlay B.B., Brumell J.H. The related effector proteins SopD and SopD2 from Salmonella enterica serovar Typhimurium contribute to virulence during systemic infection of mice. Mol Microbiol 2004, 54:1186-1198.
90. Friebel A., Ilchmann H., Aelpfelbacher M., Ehrbar K., Machleidt W., Hardt W.D. SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J Biol Chem 2001, 276:34035-34040.
91. Stender S., Friebel A., Linder S., Rohde M., Mirold S., Hardt W.D. Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol Microbiol 2000, 36:1206-1221.
92. Fu Y., Galan J.E. A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 1999, 401:293-297.
93. Haraga A., Miller S.I. A Salmonella enterica serovar typhimurium translocated leucine-rich repeat effector protein inhibits NF-kappa B-dependent gene expression. Infect Immun 2003, 71:4052-4058.
94. Kaniga K., Uralil J., Bliska J.B., Galan J.E. A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurium. Mol Microbiol 1996, 21:633-641.
95. Murli S., Watson R.O., Galan J.E. Role of tyrosine kinases and the tyrosine phosphatase SptP in the interaction of Salmonella with host cells. Cell Microbiol 2001, 3:795-810.
96. Miao E.A., Scherer C.A., Tsolis R.M., Kingsley R.A., Adams L.G., Baumler A.J., Miller S.I. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol Microbiol 1999, 34:850-864.
97. Geddes K., Worley M., Niemann G., Heffron F. Identification of new secreted effectors in Salmonella enterica serovar Typhimurium. Infect Immun 2005, 73:6260-6271.