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

Tissue Barriers

Volumn 3, Issue 1, 2015, Pages

  Zhang, Yongguo ^a   Wu, Shaoping ^a   Ma, Jun ^a   Xia, Yinglin ^b   Ai, Xun ^c   Sun, Jun ^a  

^a RUSH UNIVERSITY   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

AvrA; C Jun; Epithelial cell; Inflammation; Intestine; JNK; Permeability; Salmonella; Tight junction; ZO 1

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL PROTEIN AVRA; LUCIFERASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN ZO1; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; COLITIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; INTESTINE EPITHELIUM CELL; INTRACELLULAR SIGNALING; LASER MICROSCOPY; MOUSE; MUTATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; RNA EXTRACTION; SALMONELLA; TIGHT JUNCTION; WESTERN BLOTTING;

EID: 84981288163     PISSN: 21688362     EISSN: 21688370     Source Type: Journal    
DOI: 10.4161/21688362.2014.972849     Document Type: Article

References (55)

1. 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.
2. 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.
3. 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.
4. Mshvildadze M, Neu J. The infant intestinalmicrobiome: 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.
5. Hooper LV. Do symbiotic bacteria subvert host immunity? Nat Rev Microbiol 2009; 7:367-74; PMID: 19369952; http://dx.doi.org/10.1038/nrmicro2114.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. Bansal T, Alaniz RC, Wood TK, Jayaraman A. The bacterial signal indole increases epithelial-cell tightjunction 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.
29. 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.
30. 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.
31. 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.
32. Ma J, ZhangYG, 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. Sun J, Hobert ME, Rao AS, Neish AS, Madara JL. Bacterial activation of b-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.
39. Liu X, Lu R, Wu S, Sun J. Salmonella regulation of intestinal stem cells through the Wnt/b-catenin pathway. FEBS Lett 2010; 584:911-6; PMID:20083111; http://dx.doi.org/10.1016/j.febslet.2010.01.024.
40. 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.
41. 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.
42. Duan Y, Liao AP, Kuppireddi S, Ye Z, Ciancio MJ, Sun J. b-Catenin activity negatively regulates bacteriainduced inflammation. Lab Invest 2007; 87:613-24; PMID:17384665; http://dx.doi.org/10.1038/labinvest. 3700497.
43. 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.
44. 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.
45. Rui HL, Wang YY, Cheng H, Chen YP. JNK-dependent AP-1 activation is required for aristolochic acidinduced 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. Zhang S, Kingsley RA, Santos RL, Andrews-Polymenis H, Raffatellu M, Figueiredo J,Nunes J, Tsolis RM, Adams LG, B€aumler 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. Traweger A, Fang D, Liu YC, Stelzhammer W, Krizbai IA, Fresser F, Bauer HC, Bauer H. The tight junctionspecific 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