Bacterial protein AvrA stabilizes intestinal epithelial tight junctions via blockage of the C-Jun N-terminal kinase pathway

References

• Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009; 9:799-809; PMID:19855405; http://dx.doi.org/10.1038/nri2653
   PubMed Web of Science ®Google Scholar
• Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 2010; 10:131-44; PMID:20098461; http://dx.doi.org/10.1038/nri2707
   PubMed Web of Science ®Google Scholar
• Robinson A, Keely S, Karhausen J, Gerich ME, Furuta GT, Colgan SP. Mucosal protection by hypoxia-inducible factor prolyl hydroxylase inhibition. Gastroenterology 2008; 134:145-55; PMID:18166352; http://dx.doi.org/10.1053/j.gastro.2007.09.033
   PubMed Web of Science ®Google Scholar
• Mshvildadze M, Neu J. The infant intestinal microbiome: Friend or foe? Early Hum Dev 2010; 86(Suppl 1):67-71; PMID:20116944; http://dx.doi.org/10.1016/j.earlhumdev.2010.01.018
   PubMed Web of Science ®Google Scholar
• Hooper LV. Do symbiotic bacteria subvert host immunity? Nat Rev Microbiol 2009; 7:367-74; PMID:19369952; http://dx.doi.org/10.1038/nrmicro2114
   PubMed Web of Science ®Google Scholar
• Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002; 22:283-307; PMID:12055347; http://dx.doi.org/10.1146/annurev.nutr.22.011602.092259
   PubMed Web of Science ®Google Scholar
• Bates JM, Akerlund J, Mittge E, Guillemin K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2007; 2:371-82; PMID:18078689; http://dx.doi.org/10.1016/j.chom.2007.10.010
   PubMed Web of Science ®Google Scholar
• Preidis GA, Versalovic J. Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 2009; 136:2015-31; PMID: 19462507; http://dx.doi.org/10.1053/j.gastro.2009.01.072
   PubMed Web of Science ®Google Scholar
• Camp JG, Kanther M, Semova I, Rawls JF. Patterns and scales in gastrointestinal microbial ecology. Gastroenterology 2009; 136:1989-2002; PMID:19457423; http://dx.doi.org/10.1053/j.gastro.2009.02.075
   PubMed Web of Science ®Google Scholar
• Neish AS. Microbes in gastrointestinal health and disease. Gastroenterology 2009; 136:65-80; PMID:19026645; http://dx.doi.org/10.1053/j.gastro.2008.10.080
   PubMed Web of Science ®Google Scholar
• Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 2008; 8:411-20; PMID:18469830; http://dx.doi.org/10.1038/nri2316
   PubMed Web of Science ®Google Scholar
• Ngendahayo Mukiza C, Dubreuil JD. Escherichia coli heat-stable toxin b impairs intestinal epithelial barrier function by altering tight junction proteins. InfectImmun 2013; 81:2819-27; PMID:23716609; http://dx.doi.org/10.1128/IAI.00455-13
   PubMedGoogle Scholar
• Popoff MR, Geny B. Multifaceted role of Rho, Rac, Cdc42 and Ras in intercellular junctions, lessons from toxins. Biochim Biophys Acta 2009; 1788:797-812; PMID:19366594; http://dx.doi.org/10.1016/j.bbamem.2009.01.011
   PubMed Web of Science ®Google Scholar
• Berkes J, Viswanathan VK, Savkovic SD, Hecht G. Intestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation. Gut 2003; 52:439-51; PMID:12584232; http://dx.doi.org/10.1136/gut.52.3.439
   PubMed Web of Science ®Google Scholar
• Zhang YG, Wu S, Xia Y, Sun J. Salmonella infection upregulates the leaky protein claudin-2 in intestinal epithelial cells. PloS one 2013; 8:e58606; PMID:23505542; http://dx.doi.org/10.1371/journal.pone.0058606
   PubMed Web of Science ®Google Scholar
• Sousa S, Lecuit M, Cossart P. Microbial strategies to target, cross or disrupt epithelia. Curr Opin Cell Bio 2005; 17:489-98; PMID:16102958; http://dx.doi.org/10.1016/j.ceb.2005.08.013
   PubMed Web of Science ®Google Scholar
• Hollander D. Crohn's disease—a permeability disorder of the tight junction? Gut 1988; 29:1621-4; PMID:3065154; http://dx.doi.org/10.1136/gut.29.12.1621
   PubMed Web of Science ®Google Scholar
• Schulzke JD, Ploeger S, Amasheh M, Fromm A, Zeissig S, Troeger H, Richter J, Bojarski C, Schumann M, Fromm M. Epithelial tight junctions in intestinal inflammation. Ann N Y Acad Sci 2009; 1165:294-300; PMID:19538319; http://dx.doi.org/10.1111/j.1749-6632.2009.04062.x
   PubMed Web of Science ®Google Scholar
• Ivanov AI, Nusrat A, Parkos CA. The epithelium in inflammatory bowel disease: potential role of endocytosis of junctional proteins in barrier disruption. Novartis Found Symp 2004; 263:115-24; discussion 24-32, 211-8; PMID:15669638; http://dx.doi.org/10.1002/0470090480.ch9
   PubMedGoogle Scholar
• Weber CR, Nalle SC, Tretiakova M, Rubin DT, Turner JR. Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Invest 2008; 88:1110-20; PMID:18711353; http://dx.doi.org/10.1038/labinvest.2008.78
   PubMed Web of Science ®Google Scholar
• Zeissig S, Burgel N, Gunzel D, Richter J, Mankertz J, Wahnschaffe U, Kroesen AJ, Zeitz M, Fromm M, Schulzke JD. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 2007; 56:61-72; PMID:16822808; http://dx.doi.org/10.1136/gut.2006.094375
   PubMed Web of Science ®Google Scholar
• Arnott ID, Kingstone K, Ghosh S. Abnormal intestinal permeability predicts relapse in inactive Crohn disease. Scand J Gastroenterol 2000; 35:1163-9; PMID:11145287; http://dx.doi.org/10.1080/003655200750056637
   PubMed Web of Science ®Google Scholar
• Wyatt J, Vogelsang H, Hubl W, Waldhoer T, Lochs H. Intestinal permeability and the prediction of relapse in Crohn's disease. Lancet 1993; 341:1437-9; PMID:8099141; http://dx.doi.org/10.1016/0140-6736(93)90882-H
   PubMed Web of Science ®Google Scholar
• Katz KD, Hollander D, Vadheim CM, McElree C, Delahunty T, Dadufalza VD, Krugliak P, Rotter JI. Intestinal permeability in patients with Crohn's disease and their healthy relatives. Gastroenterology 1989; 97:927-31; PMID:2506103
   PubMed Web of Science ®Google Scholar
• Mota LJ, Journet L, Sorg I, Agrain C, Cornelis GR. Bacterial injectisomes: needle length does matter. Science 2005; 307:1278; PMID:15731447; http://dx.doi.org/10.1126/science.1107679
   PubMedGoogle Scholar
• Sun J. Pathogenic Bacterial Proteins and their Anti-Inflammatory Effects in the Eukaryotic Host. Antiinflamm Allergy Agents Med Chem 2009; 8:214-27; PMID:20090866
   PubMedGoogle Scholar
• Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr 2011; 141:769-76; PMID:21430248; http://dx.doi.org/10.3945/jn.110.135657
   PubMed Web of Science ®Google Scholar
• Bansal T, Alaniz RC, Wood TK, Jayaraman A. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc Natl Acad Sci U S A 2010; 107:228-33; PMID:19966295; http://dx.doi.org/10.1073/pnas.0906112107
   PubMed Web of Science ®Google Scholar
• Liao AP, Petrof EO, Kuppireddi S, Zhao Y, Xia Y, Claud EC, Sun J. Salmonella type III effector AvrA stabilizes cell tight junctions to inhibit inflammation in intestinal epithelial cells. PloS one 2008; 3:e2369; PMID:18523661; http://dx.doi.org/10.1371/journal.pone.0002369
   PubMed Web of Science ®Google Scholar
• Zhang S, Santos RL, Tsolis RM, Stender S, Hardt WD, Baumler AJ, et al. The Salmonella enterica serotype typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infec Immun 2002; 70:3843-55; PMID:12065528; http://dx.doi.org/10.1128/IAI.70.7.3843-3855.2002
   PubMed Web of Science ®Google Scholar
• Schesser K, Dukuzumuremyi JM, Cilio C, Borg S, Wallis TS, Pettersson S, Galyov EE. The Salmonella YopJ-homologue AvrA does not possess YopJ-like activity. Microb Pathog 2000; 28:59-70; PMID:10644492; http://dx.doi.org/10.1006/mpat.1999.0324
   PubMedGoogle Scholar
• Ma J, Zhang YG, Xia Y, Sun J. The inflammatory cytokine tumor necrosis factor modulates the expression of Salmonella typhimurium effector proteins. J Inflamm (Lond) 2010; 7:42; PMID:20704730; http://dx.doi.org/10.1186/1476-9255-7-42
   PubMed Web of Science ®Google Scholar
• Du F, Galan JE. Selective inhibition of type III secretion activated signaling by the Salmonella effector AvrA. PLoS Pathog 2009; 5:e1000595; PMID:19779561; http://dx.doi.org/10.1371/journal.ppat.1000595
   PubMedGoogle Scholar
• Jones RM, Wu H, Wentworth C, Luo L, Collier-Hyams L, Neish AS. Salmonella AvrA Coordinates Suppression of Host Immune and Apoptotic Defenses via JNK Pathway Blockade. Cell Host Microbe 2008; 3:233-44; PMID:18407067; http://dx.doi.org/10.1016/j.chom.2008.02.016
   PubMed Web of Science ®Google Scholar
• Naydenov NG, Hopkins AM, Ivanov AI. c-Jun N-terminal kinase mediates disassembly of apical junctions in model intestinal epithelia. Cell Cycle 2009; 8:2110-21; PMID:19502798; http://dx.doi.org/10.4161/cc.8.13.8928
   PubMed Web of Science ®Google Scholar
• Miller SI, Mekalanos JJ. Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. Journal of bacteriology 1990; 172:2485-90; PMID:2185222
   PubMed Web of Science ®Google Scholar
• Reed KA, Hobert ME, Kolenda CE, Sands KA, Rathman M, O'Connor M, Lyons S, Gewirtz AT, Sansonetti PJ, Madara JL. The Salmonella typhimurium flagellar basal body protein FliE is required for flagellin production and to induce a proinflammatory response in epithelial cells. J Biol Chem 2002; 277:13346-53; PMID:11821427; http://dx.doi.org/10.1074/jbc.M200149200
   PubMed Web of Science ®Google Scholar
• Sun J, Hobert ME, Rao AS, Neish AS, Madara JL. Bacterial activation of β-catenin signaling in human epithelia. Am J Physiol Gastrointest Liver Physiol 2004; 287:G220-7; PMID:14764450; http://dx.doi.org/10.1152/ajpgi.00498.2003
   PubMed Web of Science ®Google Scholar
• Liu X, Lu R, Wu S, Sun J. Salmonella regulation of intestinal stem cells through the Wnt/β-catenin pathway. FEBS Lett 2010; 584:911-6; PMID:20083111; http://dx.doi.org/10.1016/j.febslet.2010.01.024
   PubMed Web of Science ®Google Scholar
• Wu S, Ye Z, Liu X, Zhao Y, Xia Y, Steiner A, Petrof EO, Claud EC, Sun J. Salmonella typhimurium infection increases p53 acetylation in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2010; 298:G784-94; PMID:20224008; http://dx.doi.org/10.1152/ajpgi.00526.2009
   PubMedGoogle Scholar
• Ye Z, Petrof EO, Boone D, Claud EC, Sun J. Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am J Pathol 2007; 171:882-92; PMID:17690189; http://dx.doi.org/10.2353/ajpath.2007.070220
   PubMed Web of Science ®Google Scholar
• Duan Y, Liao AP, Kuppireddi S, Ye Z, Ciancio MJ, Sun J. β-Catenin activity negatively regulates bacteria-induced inflammation. Lab Invest 2007; 87:613-24; PMID:17384665; http://dx.doi.org/10.1038/labinvest.3700497
   PubMedGoogle Scholar
• Sweeney NJ, Laux DC, Cohen PS. Escherichia coli F-18 and E. coli K-12 eda mutants do not colonize the streptomycin-treated mouse large intestine. Infect Immun 1996; 64:3504-11; PMID:8751891
   PubMed Web of Science ®Google Scholar
• Liu X, Lu R, Wu S, Zhang YG, Xia Y, Sartor RB, et al. Wnt2 inhibits enteric bacterial-induced inflammation in intestinal epithelial cells. Inflamm Bowel Dis 2012; 18:418-29; PMID:21674728; http://dx.doi.org/10.1002/ibd.21788
   PubMed Web of Science ®Google Scholar
• Rui HL, Wang YY, Cheng H, Chen YP. JNK-dependent AP-1 activation is required for aristolochic acid-induced TGF-beta1 synthesis in human renal proximal epithelial cells. Am J Renal Physiol 2012; 302:F1569-75; PMID:22442213; http://dx.doi.org/10.1152/ajprenal.00560.2011
   PubMed Web of Science ®Google Scholar
• Das KC, Muniyappa H. c-Jun-NH2 terminal kinase (JNK)-mediates AP-1 activation by thioredoxin: phosphorylation of cJun, JunB, and Fra-1. Mol Cell Biochem 2010; 337:53-63; PMID:19859790; http://dx.doi.org/10.1007/s11010-009-0285-0
   PubMedGoogle Scholar
• Collier-Hyams LS, Zeng H, Sun J, Tomlinson AD, Bao ZQ, Chen H, Madara JL, Orth K, Neish AS. Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol 2002; 169:2846-50; PMID:12218096; http://dx.doi.org/10.4049/jimmunol.169.6.2846
   PubMedGoogle Scholar
• Steele-Mortimer O, Knodler LA, Marcus SL, Scheid MP, Goh B, Pfeifer CG, et al. Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J Biol Chem 2000; 275:37718-24; PMID:10978351; http://dx.doi.org/10.1074/jbc.M008187200
   PubMed Web of Science ®Google Scholar
• Friebel A, Ilchmann H, Aepfelbacher M, Ehrbar K, Machleidt W, Hardt WD. SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J Biol Chem 2001; 276:34035-40; PMID:11440999; http://dx.doi.org/10.1074/jbc.M100609200
   PubMed Web of Science ®Google Scholar
• Zhang S, Kingsley RA, Santos RL, Andrews-Polymenis H, Raffatellu M, Figueiredo J,Nunes J, Tsolis RM, Adams LG, Bäumler AJ. Molecular pathogenesis of salmonella enterica serotype typhimurium-induced diarrhea. Infect Immun 2003; 71:1-12; PMID:12496143; http://dx.doi.org/10.1128/IAI.71.1.1-12.2003
   PubMed Web of Science ®Google Scholar
• Huang FC, Werne A, Li Q, Galyov EE, Walker WA, Cherayil BJ. Cooperative interactions between flagellin and SopE2 in the epithelial interleukin-8 response to salmonella enterica serovar typhimurium infection. Infec Immun 2004; 72:5052-62; PMID:15321998; http://dx.doi.org/10.1128/IAI.72.9.5052-5062.2004
   PubMedGoogle Scholar
• Van Itallie CM, Colegio OR, Anderson JM. The cytoplasmic tails of claudins can influence tight junction barrier properties through effects on protein stability. J Membr Biol 2004; 199:29-38; PMID:15366421; http://dx.doi.org/10.1007/s00232-004-0673-z
   PubMed Web of Science ®Google Scholar
• Wilson BA, Ho M. Recent insights into Pasteurella multocida toxin and other G-protein-modulating bacterial toxins. Future Microbiol 2010; 5:1185-201; PMID:20722598; http://dx.doi.org/10.2217/fmb.10.91
   PubMedGoogle Scholar
• Yoon SS, Sun J. Probiotics, nuclear receptor signaling, and anti-inflammatory pathways. Gastroenterol Res Pract 2011; 2011:971938; PMID:21808643; http://dx.doi.org/10.1155/2011/971938
   PubMedGoogle Scholar
• Traweger A, Fang D, Liu YC, Stelzhammer W, Krizbai IA, Fresser F, Bauer HC, Bauer H. The tight junction-specific protein occludin is a functional target of the E3 ubiquitin-protein ligase itch. J Biol Chem 2002; 277:10201-8; PMID:11782481; http://dx.doi.org/10.1074/jbc.M111384200
   PubMed Web of Science ®Google Scholar