Chronic effects of a salmonella type III secretion effector protein AvrA in vivo

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Lu, Rong ^a   Wu, Shaoping ^a   Liu, Xingyin ^a   Xia, Yinglin ^b   Zhang, Yong Guo ^a   Sun, Jun ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GAMMA INTERFERON; INTERLEUKIN 12; PROTEIN AVRA; STREPTOMYCIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AUTACOID; AVRA PROTEIN, SALMONELLA TYPHIMURIUM; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; CYTOKINE RELEASE; ENTERITIS; GALLBLADDER; IN VIVO STUDY; LIVER ABSCESS; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN SYNTHESIS INHIBITION; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; TYPE III SECRETION SYSTEM; ANIMAL; ANTIBODY SPECIFICITY; CHRONIC DISEASE; DISEASE MODEL; DRUG EFFECT; INTESTINE; LIVER; METABOLISM; MICROBIOLOGY; MOVEMENT (PHYSIOLOGY); ORGAN SIZE; PATHOLOGY; SECRETION; SPLEEN; SURVIVAL; WEIGHT GAIN;

BACTERIA (MICROORGANISMS); MUS; SALMONELLA; SALMONELLA TYPHIMURIUM;

ANIMALS; BACTERIAL PROTEINS; CHRONIC DISEASE; CYTOKINES; DISEASE MODELS, ANIMAL; GALLBLADDER; INFLAMMATION MEDIATORS; INTESTINES; LIVER; MICE; MOVEMENT; ORGAN SIZE; ORGAN SPECIFICITY; SALMONELLA INFECTIONS; SPLEEN; STREPTOMYCIN; SURVIVAL ANALYSIS; WEIGHT GAIN;

EID: 77956281903     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010505     Document Type: Article

References (42)

1. Grassl GA, Valdez Y, Bergstrom KS, Vallance BA, Finlay BB (2008) Chronic enteric salmonella infection in mice leads to severe and persistent intestinal fibrosis. Gastroenterology 134: 768-780.
2. Gradel KO, Nielsen HL, Schonheyder HC, Ejlertsen T, Kristensen B, et al. (2009) Increased short- and long-term risk of inflammatory bowel disease after salmonella or campylobacter gastroenteritis. Gastroenterology 137: 495-501.
3. Kumar S (2006) Infection as a risk factor for gallbladder cancer. J Surg Oncol 93: 633-639.
4. Siccardi D, Mumy KL, Wall DM, Bien JD, McCormick BA (2008) Salmonella enterica serovar Typhimurium modulates P-glycoprotein in the intestinal epithelium. Am J Physiol Gastrointest Liver Physiol 294: G1392-1400.
5. Mager DL (2006) Bacteria and cancer: cause, coincidence or cure? A review. J Transl Med 4: 14.
6. Arrach N, Zhao M, Porwollik S, Hoffman RM, McClelland M (2008) Salmonella promoters preferentially activated inside tumors. Cancer Res 68: 4827-4832.
7. Zhao M, Yang M, Li XM, Jiang P, Baranov E, et al. (2005) Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. Proc Natl Acad Sci U S A 102: 755-760.
8. Zhao M, Geller J, Ma H, Yang M, Penman S, et al. (2007) Monotherapy with a tumor-targeting mutant of Salmonella typhimurium cures orthotopic metastatic mouse models of human prostate cancer. Proc Natl Acad Sci U S A 104: 10170-10174.
9. Hapfelmeier S, Ehrbar K, Stecher B, Barthel M, Kremer M, et al. (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.
10. Galan JE (2001) Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 17: 53-86.
11. Galan JE (2007) SnapShot: effector proteins of type III secretion systems. Cell 130: 192.
12. Schlumberger MC, Hardt WD (2006) Salmonella type III secretion effectors: pulling the host cell's strings. Curr Opin Microbiol 9: 46-54.
13. Knodler LA, Celli J, Hardt WD, Vallance BA, Yip C, et al. (2002) Salmonella effectors within a single pathogenicity island are differentially expressed and translocated by separate type III secretion systems. Mol Microbiol 43: 1089-1103.
14. Broberg CA, Orth K Tipping the balance by manipulating post-translational modifications. Curr Opin Microbiol 13: 34-40.
15. Ibarra JA, Steele-Mortimer O (2009) Salmonella--the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 11: 1579-1586.
16. Haraga A, Ohlson MB, Miller SI (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 6: 53-66.
17. Du F, Galan JE (2009) Selective inhibition of type III secretion activated signaling by the Salmonella effector AvrA. PLoS Pathog 5: e1000595.
18. Collier-Hyams LS, Zeng H, Sun J, Tomlinson AD, Bao ZQ, et al. (2002) Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, antiapoptotic NF-kappa B pathway. J Immunol 169: 2846-2850.
19. Hardt WD, Galan JE (1997) A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci U S A 94: 9887-9892.
20. Liao AP, Petrof EO, Kuppireddi S, Zhao Y, Xia Y, et al. (2008) Salmonella type III effector AvrA stabilizes cell tight junctions to inhibit inflammation in intestinal epithelial cells. PLoS ONE 3: e2369.
21. Sun J, Hobert ME, Rao AS, Neish AS, Madara JL (2004) Bacterial activation of beta-catenin signaling in human epithelia. Am J Physiol Gastrointest Liver Physiol 287: G220-227.
22. Ye Z, Petrof EO, Boone D, Claud EC, Sun J (2007) Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am J Pathol 171: 882-892.
23. Liu X, Lu R, Wu S, Sun J Salmonella regulation of intestinal stem cells through the Wnt/beta-catenin pathway. FEBS Lett 584: 911-916.
24. Sun J, Hobert ME, Duan Y, Rao AS, He TC, et al. (2005) Crosstalk between NF-kappaB and beta-catenin pathways in bacterial-colonized intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 289: G129-137.
25. Duan Y, Liao AP, Kuppireddi S, Ye Z, Ciancio MJ, et al. (2007) beta-Catenin activity negatively regulates bacteria-induced inflammation. Lab Invest 87: 613-624.
26. Neish AS, Gewirtz AT, Zeng H, Young AN, Hobert ME, et al. (2000) Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination. Science 289: 1560-1563.
27. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, et al. (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.
28. Woo H, Okamoto S, Guiney D, Gunn JS, Fierer J (2008) A model of Salmonella colitis with features of diarrhea in SLC11A1 wild-type mice. PLoS ONE 3: e1603.
29. Vidal JE, da Silva PR, Schiavon Nogueira R, Bonasser Filho F, Hernandez AV (2003) Liver abscess due to Salmonella enteritidis in a returned traveler with HIV infection: case report and review of the literature. Rev Inst Med Trop Sao Paulo 45: 115-117.
30. Okamura M, Kamijima Y, Miyamoto T, Tani H, Sasai K, et al. (2001) Differences among six Salmonella serovars in abilities to colonize reproductive organs and to contaminate eggs in laying hens. Avian Dis 45: 61-69.
31. Jimenez-Saenz M, Gomez-Rodriguez BJ, Carmona I, Rebollo J, Torres Y, et al. (2001) Salmonella dublin infection: a rare cause of spontaneous bacterial peritonitis and chronic colitis in alcoholic liver cirrhosis. Eur J Gastroenterol Hepatol 13: 587-589.
32. Menendez A, Arena ET, Guttman JA, Thorson L, Vallance BA, et al. (2009) Salmonella infection of gallbladder epithelial cells drives local inflammation and injury in a model of acute typhoid fever. J Infect Dis 200: 1703-1713.
33. Jeans AR, McKendrick MW (2007) Salmonella Paratyphi A liver abscess-- secondary infection of an amoebic liver abscess? Travel Med Infect Dis 5: 144-146.
34. Gast RK, Guard-Bouldin J, Holt PS (2004) Colonization of reproductive organs and internal contamination of eggs after experimental infection of laying hens with Salmonella heidelberg and Salmonella enteritidis. Avian Dis 48: 863-869.
35. Valdez Y, Diehl GE, Vallance BA, Grassl GA, Guttman JA, et al. (2008) Nramp1 expression by dendritic cells modulates inflammatory responses during Salmonella Typhimurium infection. Cell Microbiol 10: 1646-1661.
36. Darveau R (1999) Infection, inflammation, and cancer. Nat Biotechnol 17: 19.
37. Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, et al. (2009) A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 15: 1016-1022.
38. Rhee KJ, Wu S, Wu X, Huso DL, Karim B, et al. (2009) Induction of persistent colitis by a human commensal, enterotoxigenic Bacteroides fragilis, in wild-type C57BL/6 mice. Infect Immun 77: 1708-1718.
39. Miller SI, Mekalanos JJ (1990) Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol 172: 2485-2490.
40. McCormick BA, Colgan SP, Delp-Archer C, Miller SI, Madara JL (1993) Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 123: 895-907.
41. Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W, et al. (1998) Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 66: 5224-5231.
42. Zeger SL, Liang KY (1986) Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42: 121-130.