Helicobacter pylori-induced disruption of monolayer permeability and proinflammatory cytokine secretion in polarized human gastric epithelial cells

Infection and Immunity

Volumn 81, Issue 3, 2013, Pages 876-883

  Fiorentino, Maria ^a,b   Ding, Hua ^b   Blanchard, Thomas G ^b   Czinn, Steven J ^b   Sztein, Marcelo B ^a,b   Fasanoa, Alessio ^a,b,c  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 1; FLUORESCEIN ISOTHIOCYANATE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; PROTEIN ZO1; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL MEMBRANE PERMEABILITY; CELL POLARITY; CELL VIABILITY; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DIFFUSION; ELECTRIC RESISTANCE; EPITHELIUM CELL; HELICOBACTER INFECTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; STOMACH EPITHELIUM; SUPERNATANT;

CELL LINE; CYTOKINES; ELECTRIC IMPEDANCE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HELICOBACTER PYLORI; HUMANS; INFLAMMATION; PERMEABILITY; STOMACH; TIGHT JUNCTION PROTEINS;

EID: 84874670567     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01406-12     Document Type: Article

References (38)

1. Turner JR. 2006. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am. J. Pathol. 169:1901-1909.
2. Marshall BJ, Warren JR. 1984. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet i:1311-1315.
3. Everhart JE. 2000. Recent developments in the epidemiology of Helicobacter pylori. Gastroenterol. Clin. North Am. 29:559-578.
4. NIH Consensus Conference. 1994. Helicobacter pylori in peptic ulcer disease. JAMA 272:65-69.
5. Parsonnet J, Hansen S, Rodriguez L, Gelb AB, Warnke RA, Jellum E, Orentreich N, Vogelman JH, Friedman GD. 1994. Helicobacter pylori infection and gastric lymphoma. N. Engl. J. Med. 330:1267-1271.
6. Peek RM, Jr, Blaser MJ. 2002. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2:28-37.
7. World Health Organization. 1994. Infection with Helicobacter pylori, p 177-241. In Schistosomes, liver flukes and Helicobacter pylori, vol 61. International Agency for Research on Cancer, Lyon, France.
8. Correa P. 1992. Human gastric carcinogenesis: a multistep and multifactorial process-First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res. 52:6735-6740.
9. Asahi M, Azuma T, Ito S, Ito Y, Suto H, Nagai Y, Tsubokawa M, Tohyama Y, Maeda S, Omata M, Suzuki T, Sasakawa C. 2000. Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J. Exp. Med. 191:593-602.
10. Backert S, Ziska E, Brinkmann V, Zimny-Arndt U, Fauconnier A, Jungblut PR, Naumann M, Meyer TF. 2000. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell. Microbiol. 2:155-164.
11. Odenbreit S, Puls J, Sedlmaier B, Gerland E, Fischer W, Haas R. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287:1497-1500.
12. Segal ED, Cha J, Lo J, Falkow S, Tompkins LS. 1999. Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc. Natl. Acad. Sci. U. S. A. 96:14559-14564.
13. Stein M, Rappuoli R, Covacci A. 2000. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc. Natl. Acad. Sci. U. S. A. 97:1263-1268.
14. Fischer W, Puls J, Buhrdorf R, Gebert B, Odenbreit S, Haas R. 2001. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol. Microbiol. 42:1337-1348.
15. Foryst-Ludwig A, Naumann M. 2000. p21-activated kinase 1 activates the nuclear factor kappa B (NF-kappa B)-inducing kinase-Ikappa B kinases NF-kappa B pathway and proinflammatory cytokines in Helicobacter pylori infection. J. Biol. Chem. 275:39779-39785.
16. Rieder G, Einsiedl W, Hatz RA, Stolte M, Enders GA, Walz A. 2001. Comparison of CXC chemokines ENA-78 and interleukin-8 expression in Helicobacter pylori-associated gastritis. Infect. Immun. 69:81-88.
17. Rieder G, Hatz RA, Moran AP, Walz A, Stolte M, Enders G. 1997. Role of adherence in interleukin-8 induction in Helicobacter pylori-associated gastritis. Infect. Immun. 65:3622-3630.
18. Jimenez-Soto LF, Kutter S, Sewald X, Ertl C, Weiss E, Kapp U, Rohde M, Pirch T, Jung K, Retta SF, Terradot L, Fischer W, Haas R. 2009. Helicobacter pylori type IV secretion apparatus exploits beta1 integrin in a novel RGD-independent manner. PLoS Pathog. 5:e1000684. doi:10.1371/journal.ppat.1000684.
19. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, Misselwitz R, Berger J, Sewald N, Konig W, Backert S. 2007. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449:862-866.
20. Saha A, Backert S, Hammond CE, Gooz M, Smolka AJ. 2010. Helicobacter pylori CagL activates ADAM17 to induce repression of the gastric H, K-ATPase alpha subunit. Gastroenterology 139:239-248.
21. Tegtmeyer N, Hartig R, Delahay RM, Rohde M, Brandt S, Conradi J, Takahashi S, Smolka AJ, Sewald N, Backert S. 2010. A small fibronectinmimicking protein from bacteria induces cell spreading and focal adhesion formation. J. Biol. Chem. 285:23515-23526.
22. Basque JR, Chenard M, Chailler P, Menard D. 2001. Gastric cancer cell lines as models to study human digestive functions. J. Cell. Biochem. 81: 241-251.
23. McGovern KJ, Blanchard TG, Gutierrez JA, Czinn SJ, Krakowka S, Youngman P. 2001. γ-Glutamyltransferase is a Helicobacter pylori virulence factor but is not essential for colonization. Infect. Immun. 69:4168-4173.
24. Chang YT, Wu MS, Chang YJ, Chen CC, Lin YS, Hsieh T, Yang PC, Lin JT. 2006. Distinct gene expression profiles in gastric epithelial cells induced by different clinical isolates of Helicobacter pylori-implication of bacteria and host interaction in gastric carcinogenesis. Hepatogastroenterology 53:484-490.
25. Moese S, Selbach M, Brinkmann V, Karlas A, Haimovich B, Backert S, Meyer TF. 2007. The Helicobacter pylori CagA protein disrupts matrix adhesion of gastric epithelial cells by dephosphorylation of vinculin. Cell. Microbiol. 9:1148-1161.
26. Oliveira MJ, Costa AC, Costa AM, Henriques L, Suriano G, Atherton JC, Machado JC, Carneiro F, Seruca R, Mareel M, Leroy A, Figueiredo C. 2006. Helicobacter pylori induces gastric epithelial cell invasion in a c-Met and type IV secretion system-dependent manner. J. Biol. Chem. 281:34888-34896.
27. Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, Athman R, Memet S, Huerre MR, Coyle AJ, DiStefano PS, Sansonetti PJ, Labigne A, Bertin J, Philpott DJ, Ferrero RL. 2004. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5:1166-1174.
28. Amieva MR, Vogelmann R, Covacci A, Tompkins LS, Nelson WJ, Falkow S. 2003. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 300:1430-1434.
29. Fedwick JP, Lapointe TK, Meddings JB, Sherman PM, Buret AG. 2005. Helicobacter pylori activates myosin light-chain kinase to disrupt claudin- 4 and claudin-5 and increase epithelial permeability. Infect. Immun. 73:7844-7852.
30. Wroblewski LE, Shen L, Ogden S, Romero-Gallo J, Lapierre LA, Israel DA, Turner JR, Peek RM, Jr. 2009. Helicobacter pylori dysregulation of gastric epithelial tight junctions by urease-mediated myosin II activation. Gastroenterology 136:236-246.
31. Jung YJ, Lee KL, Kim BK, Kim JW, Jeong JB, Kim SG, Kim JS, Jung HC, Song IS. 2006. Usefulness of NCI-N87 cell lines in Helicobacter pylori infected gastric mucosa model. Korean J. Gastroenterol. 47:357-362. (In Korean.).
32. Lapointe TK, O'Connor PM, Jones NL, Menard D, Buret AG. 2010. Interleukin-1 receptor phosphorylation activates Rho kinase to disrupt human gastric tight junctional claudin-4 during Helicobacter pylori infection. Cell. Microbiol. 12:692-703.
33. Chailler P, Menard D. 2005. Establishment of human gastric epithelial (HGE) cell lines exhibiting barrier function, progenitor, and prezymogenic characteristics. J. Cell. Physiol. 202:263-274.
34. Rad R, Ballhorn W, Voland P, Eisenacher K, Mages J, Rad L, Ferstl R, Lang R, Wagner H, Schmid RM, Bauer S, Prinz C, Kirschning CJ, Krug A. 2009. Extracellular and intracellular pattern recognition receptors cooperate in the recognition of Helicobacter pylori. Gastroenterology 136: 2247-2257.
35. Faherty C, Harper JM, Shea-Donohue T, Barry EM, Kaper JB, Fasano A, Nataro JP. 2012. Chromosomal and plasmid-encoded factors of shigella flexneri induce secretogenic activity ex vivo. PLoS One 7:e49980. doi:10.1371/journal.pone.0049980.
36. El Asmar R, Panigrahi P, Bamford P, Berti I, Not T, Coppa GV, Catassi C, Fasano A. 2002. Host-dependent zonulin secretion causes the impairment of the small intestine barrier function after bacterial exposure. Gastroenterology 123:1607-1615.
37. Boll EJ, Struve C, Sander A, Demma Z, Krogfelt KA, McCormick BA. 2012. Enteroaggregative Escherichia coli promotes transepithelial migration of neutrophils through a conserved 12-lipoxygenase pathway. Cell. Microbiol. 14:120-132.
38. Mumy KL, Bien JD, Pazos MA, Gronert K, Hurley BP, McCormick BA. 2008. Distinct isoforms of phospholipase A2 mediate the ability of Salmonella enterica serotype Typhimurium and Shigella flexneri to induce the transepithelial migration of neutrophils. Infect. Immun. 76:3614-3627.