Prolonged NF-κB activation by a macrophage inhibitory cytokine 1-linked signal in enteropathogenic Escherichia coli-infected epithelial cells

Infection and Immunity

Volumn 81, Issue 6, 2013, Pages 1860-1869

  Choi, Hye Jin ^a   Kim, Juil ^a   Do, Kee Hun ^a   Park, Seong Hwan ^a   Moon, Yuseok ^a  

^a Pusan National University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; GROWTH DIFFERENTIATION FACTOR 15; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SYNAPTOTAGMIN I;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INTESTINE CELL; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM;

ANIMALS; CELL LINE; CYCLIN D1; ENTEROPATHOGENIC ESCHERICHIA COLI; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, BACTERIAL; GROWTH DIFFERENTIATION FACTOR 15; HUMANS; INTERLEUKIN-8; INTESTINAL MUCOSA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; NF-KAPPA B; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA;

EID: 84877834756     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00162-13     Document Type: Article

References (52)

1. Imani Fooladi AA, Mousavi SF, Seghatoleslami S, Yazdani S, Nourani MR. 2011. Toll-like receptors: role of inflammation and commensal bacteria. Inflamm. Allergy Drug Targets 10:198-207.
2. Eckmann L, Neish AS. 2011. NF-κB and mucosal homeostasis. Curr. Top. Microbiol. Immunol. 349:145-158.
3. Swamy M, Jamora C, Havran W, Hayday A. 2010. Epithelial decision makers: in search of the "epimmunome." Nat. Immunol. 11:656-665.
4. Wullaert A, Bonnet MC, Pasparakis M. 2011. NF-κB in the regulation of epithelial homeostasis and inflammation. Cell Res. 21:146-158.
5. Robins-Browne RM. 1987. Traditional enteropathogenic Escherichia coli of infantile diarrhea. Rev. Infect. Dis. 9:28-53.
6. Kallinowski F, Wassmer A, Hofmann MA, Harmsen D, Heesemann J, Karch H, Herfarth C, Buhr HJ. 1998. Prevalence of enteropathogenic bacteria in surgically treated chronic inflammatory bowel disease. Hepatogastroenterology 45:1552-1558.
7. La Ferla K, Seegert D, Schreiber S. 2004. Activation of NF-κB in intestinal epithelial cells by E. coli strains isolated from the colonic mucosa of IBD patients. Int. J. Colorectal Dis. 19:334-342.
8. Maddocks OD, Short AJ, Donnenberg MS, Bader S, Harrison DJ. 2009. Attaching and effacing Escherichia coli downregulate DNA mismatch repair protein in vitro and are associated with colorectal adenocarcinomas in humans. PLoS One 4:e5517. doi:10.1371/journal.pone.0005517.
9. Weber P, Koch M, Heizmann WR, Scheurlen M, Jenss H, Hartmann F. 1992. Microbic superinfection in relapse of inflammatory bowel disease. J. Clin. Gastroenterol. 14:302-308.
10. Long-Krug SA, Weikel CS, Tiemens KT, Hewlett EL, Levine MM, Guerrant RL. 1984. Does enteropathogenic Escherichia coli produce heatlabile enterotoxin, heat-stable enterotoxins a or b, or cholera toxin A subunits? Infect. Immun. 46:612-614.
11. Robins-Browne RM, Levine MM, Rowe B, Gabriel EM. 1982. Failure to detect conventional enterotoxins in classical enteropathogenic (serotyped) Escherichia coli strains of proven pathogenicity. Infect. Immun. 38:798-801.
12. Edwards LA, Bajaj-Elliott M, Klein NJ, Murch SH, Phillips AD. 2011. Bacterial-epithelial contact is a key determinant of host innate immune responses to enteropathogenic and enteroaggregative Escherichia coli. PLoS One 6:e27030. doi:10.1371/journal.pone.0027030.
13. Ruchaud-Sparagano MH, Muhlen S, Dean P, Kenny B. 2011. The Enteropathogenic E. coli (EPEC) Tir effector inhibits NF-κB activity by targeting TNFβ receptor-associated factors. PLoS Pathog. 7:e1002414. doi:10.1371/journal.ppat.1002414.
14. Sham HP, Shames SR, Croxen MA, Ma C, Chan JM, Khan MA, Wickham ME, Deng W, Finlay BB, Vallance BA. 2011. Attaching and effacing bacterial effector NleC suppresses epithelial inflammatory responses by inhibiting NF-κB and p38 mitogen-activated protein kinase activation. Infect. Immun. 79:3552-3562.
15. Rothbaum R, McAdams AJ, Giannella R, Partin JC. 1982. A clinicopathologic study of enterocyte-adherent Escherichia coli: a cause of protracted diarrhea in infants. Gastroenterology 83:441-454.
16. Ulshen MH, Rollo JL. 1980. Pathogenesis of escherichia coli gastroenteritis in man-another mechanism. N. Engl. J. Med. 302:99-101.
17. Dean P, Maresca M, Schuller S, Phillips AD, Kenny B. 2006. Potent diarrheagenic mechanism mediated by the cooperative action of three enteropathogenic Escherichia coli-injected effector proteins. Proc. Natl. Acad. Sci. U. S. A. 103:1876-1881.
18. Sampaio SC, Gomes TA, Pichon C, du Merle L, Guadagnini S, Abe CM, Sampaio JL, Le Bouguenec C. 2009. The flagella of an atypical enteropathogenic Escherichia coli strain are required for efficient interaction with and stimulation of interleukin-8 production by enterocytes in vitro. Infect. Immun. 77:4406-4413.
19. Gao X, Wan F, Mateo K, Callegari E, Wang D, Deng W, Puente J, Li F, Chaussee MS, Finlay BB, Lenardo MJ, Hardwidge PR. 2009. Bacterial effector binding to ribosomal protein s3 subverts NF-κB function. PLoS Pathog. 5:e1000708. doi:10.1371/journal.ppat.1000708.
20. Royan SV, Jones RM, Koutsouris A, Roxas JL, Falzari K, Weflen AW, Kim A, Bellmeyer A, Turner JR, Neish AS, Rhee KJ, Viswanathan VK, Hecht GA. 2010. Enteropathogenic E. coli non-LEE encoded effectors NleH1 and NleH2 attenuate NF-κB activation. Mol. Microbiol. 78:1232-1245.
21. Fairlie WD, Moore AG, Bauskin AR, Russell PK, Zhang HP, Breit SN. 1999. MIC-1 is a novel TGF-β superfamily cytokine associated with macrophage activation. J. Leukoc. Biol. 65:2-5.
22. Bootcov MR, Bauskin AR, Valenzuela SM, Moore AG, Bansal M, He XY, Zhang HP, Donnellan M, Mahler S, Pryor K, Walsh BJ, Nicholson RC, Fairlie WD, Por SB, Robbins JM, Breit SN. 1997. MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-β superfamily. Proc. Natl. Acad. Sci. U. S. A. 94:11514-11519.
23. Whitman M. 1998. Smads and early developmental signaling by the TGFβ superfamily. Genes Dev. 12:2445-2462.
24. Bauskin AR, Brown DA, Kuffner T, Johnen H, Luo XW, Hunter M, Breit SN. 2006. Role of macrophage inhibitory cytokine-1 in tumorigenesis and diagnosis of cancer. Cancer Res. 66:4983-4986.
25. Bottner M, Suter-Crazzolara C, Schober A, Unsicker K. 1999. Expression of a novel member of the TGF-β superfamily, growth/differentiation factor-15/macrophage-inhibiting cytokine-1 (GDF-15/MIC-1) in adult rat tissues. Cell Tissue Res. 297:103-110.
26. Agarwal MK, Hastak K, Jackson MW, Breit SN, Stark GR, Agarwal ML. 2006. Macrophage inhibitory cytokine 1 mediates a p53-dependent protective arrest in S phase in response to starvation for DNA precursors. Proc. Natl. Acad. Sci. U. S. A. 103:16278-16283.
27. Brown DA, Ward RL, Buckhaults P, Liu T, Romans KE, Hawkins NJ, Bauskin AR, Kinzler KW, Vogelstein B, Breit SN. 2003. MIC-1 serum level and genotype: associations with progress and prognosis of colorectal carcinoma. Clin. Cancer Res. 9:2642-2650.
28. Lee DH, Yang Y, Lee SJ, Kim KY, Koo TH, Shin SM, Song KS, Lee YH, Kim YJ, Lee JJ, Choi I, Lee JH. 2003. Macrophage inhibitory cytokine-1 induces the invasiveness of gastric cancer cells by up-regulating the urokinase- type plasminogen activator system. Cancer Res. 63:4648-4655.
29. Tan M, Wang Y, Guan K, Sun Y. 2000. PTGF-β, a type beta transforming growth factor (TGF-β) superfamily member, is a p53 target gene that inhibits tumor cell growth via TGF-β signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 97:109-114.
30. Borenshtein D, McBee ME, Schauer DB. 2008. Utility of the Citrobacter rodentium infection model in laboratory mice. Curr. Opin. Gastroenterol. 24:32-37.
31. Garcia A, Marini RP, Feng Y, Vitsky A, Knox KA, Taylor NS, Schauer DB, Fox JG. 2002. A naturally occurring rabbit model of enterohemorrhagic Escherichia coli-induced disease. J. Infect. Dis. 186:1682-1686.
32. Calderon Toledo C, Arvidsson I, Karpman D. 2011. Cross-reactive protection against enterohemorrhagic Escherichia coli infection by enteropathogenic E. coli in a mouse model. Infect. Immun. 79:2224-2233.
33. Savkovic SD, Villanueva J, Turner JR, Matkowskyj KA, Hecht G. 2005. Mouse model of enteropathogenic Escherichia coli infection. Infect. Immun. 73:1161-1170.
34. Rhee KJ, Cheng H, Harris A, Morin C, Kaper JB, Hecht G. 2011. Determination of spatial and temporal colonization of enteropathogenic E. coli and enterohemorrhagic E. coli in mice using bioluminescent in vivo imaging. Gut Microbes 2:34-41.
35. Alcantara Warren C, Destura RV, Sevilleja JE, Barroso LF, Carvalho H, Barrett LJ, O'Brien AD, Guerrant RL. 2008. Detection of epithelial-cell injury, and quantification of infection, in the HCT-8 organoid model of cryptosporidiosis. J. Infect. Dis. 198:143-149.
36. Sifuentes LY, Di Giovanni GD. 2007. Aged HCT-8 cell monolayers support Cryptosporidium parvum infection. Appl. Environ. Microbiol. 73: 7548-7551.
37. Thebault S, Deniel N, Marion R, Charlionet R, Tron F, Cosquer D, Leprince J, Vaudry H, Ducrotte P, Dechelotte P. 2006. Proteomic analysis of glutamine-treated human intestinal epithelial HCT-8 cells under basal and inflammatory conditions. Proteomics 6:3926-3937.
38. Khan MA, Bouzari S, Ma C, Rosenberger CM, Bergstrom KS, Gibson DL, Steiner TS, Vallance BA. 2008. Flagellin-dependent and -independent inflammatory responses following infection by enteropathogenic Escherichia coli and Citrobacter rodentium. Infect. Immun. 76:1410-1422.
39. Ruchaud-Sparagano MH, Maresca M, Kenny B. 2007. Enteropathogenic Escherichia coli (EPEC) inactivate innate immune responses prior to compromising epithelial barrier function. Cell Microbiol. 9:1909-1921.
40. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE, Leaf IA, Aderem A. 2010. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl. Acad. Sci. U. S. A. 107:3076-3080.
41. Salazar-Gonzalez H, Navarro-Garcia F. 2011. Intimate adherence by enteropathogenic Escherichia coli modulates TLR5 localization and proinflammatory host response in intestinal epithelial cells. Scand. J. Immunol. 73:268-283.
42. Khan MA, Ma C, Knodler LA, Valdez Y, Rosenberger CM, Deng W, Finlay BB, Vallance BA. 2006. Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infect. Immun. 74:2522-2536.
43. Karrasch T, Jobin C. 2008. NF-κB and the intestine: friend or foe? Inflamm. Bowel Dis. 14:114-124.
44. Pasparakis M. 2009. Regulation of tissue homeostasis by NF-κB signalling: implications for inflammatory diseases. Nat. Rev. Immunol. 9:778-788.
45. Strauch ED, Yamaguchi J, Bass BL, Wang JY. 2003. Bile salts regulate intestinal epithelial cell migration by nuclear factor-kappa B-induced expression of transforming growth factor-beta. J. Am. Coll. Surg. 197: 974-984.
46. Chen LW, Egan L, Li ZW, Greten FR, Kagnoff MF, Karin M. 2003. The two faces of IKK and NF-κB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat. Med. 9:575-581.
47. Egan LJ, Eckmann L, Greten FR, Chae S, Li ZW, Myhre GM, Robine S, Karin M, Kagnoff MF. 2004. IκB-kinaseβ-dependent NF-κB activation provides radioprotection to the intestinal epithelium. Proc. Natl. Acad. Sci. U. S. A. 101:2452-2457.
48. Ma TY, Boivin MA, Ye D, Pedram A, Said HM. 2005. Mechanism of TNF-β modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression. Am. J. Physiol. Gastrointest Liver Physiol. 288:G422-430.
49. Yen H, Ooka T, Iguchi A, Hayashi T, Sugimoto N, Tobe T. 2010. NleC, a type III secretion protease, compromises NF-κB activation by targeting p65/RelA. PLoS Pathog. 6:e1001231. doi:10.1371/journal.ppat.1001231.
50. Lopez-Rovira T, Chalaux E, Rosa JL, Bartrons R, Ventura F. 2000. Interaction and functional cooperation of NF-κB with Smads. Transcriptional regulation of the junB promoter. J. Biol. Chem. 275:28937-28946.
51. Min/+ mice. J. Infect. Dis. 184:227-230.
52. Barthold SW, Jonas AM. 1977. Morphogenesis of early 1, 2-dimethylhydrazine- induced lesions and latent period reduction of colon carcinogenesis in mice by a variant of Citrobacter freundii. Cancer Res. 37:4352-4360.