Helicobacter pylori targets cancer-associated apical-junctional constituents in gastroids and gastric epithelial cells

Gut

Volumn 64, Issue 5, 2015, Pages 720-730

  Wroblewski, Lydia E ^a   Piazuelo, M Blanca ^a   Chaturvedi, Rupesh ^a   Schumacher, Michael ^b   Aihara, Eitaro ^b   Feng, Rui ^b   Noto, Jennifer M ^a   Delgado, Alberto ^a   Israel, Dawn A ^a   Zavros, Yana ^b   Montrose, Marshall H ^b   Shroyer, Noah ^c   Correa, Pelayo ^a   Wilson, Keith T ^a   Peek, Richard M ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CAGA PROTEIN; CLAUDIN 7; TRANSCRIPTION FACTOR SNAIL; CLAUDIN; CLDN7 PROTEIN, MOUSE; CTNNB1 PROTEIN, MOUSE; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM CELL; GASTROID; GENE ACTIVATION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STOMACH CANCER; STOMACH EPITHELIUM; ANIMAL; C57BL MOUSE; CELL CULTURE; COCULTURE; GASTRIC MUCOSA; HELICOBACTER INFECTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY;

ANIMALS; BETA CATENIN; CELL PROLIFERATION; CELLS, CULTURED; CLAUDINS; COCULTURE TECHNIQUES; EPITHELIAL CELLS; GASTRIC MUCOSA; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MICE, INBRED C57BL; TRANSCRIPTION FACTORS;

EID: 84929660818     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2014-307650     Document Type: Article

References (52)

1. Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010;23:713-39.
2. Polk DB, Peek RM Jr. Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer 2010;10:403-14.
3. Censini S, Lange C, Xiang Z, et al. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA 1996;93:14648-53.
4. Selbach M, Moese S, Hauck CR, et al. Src is the kinase of the Helicobacter pylori CagA protein in vitro and in vivo. J Biol Chem 2002;277:6775-8.
5. Backert S, Moese S, Selbach M, et al. Phosphorylation of tyrosine 972 of the Helicobacter pylori CagA protein is essential for induction of a scattering phenotype in gastric epithelial cells. Mol Microbiol 2001;42:631-44.
6. Tammer I, Brandt S, Hartig R, et al. Activation of Abl by Helicobacter pylori: a novel kinase for CagA and crucial mediator of host cell scattering. Gastroenterology 2007;132:1309-19.
7. Mueller D, Tegtmeyer N, Brandt S, et al. c-Src and c-Abl kinases control hierarchic phosphorylation and function of the CagA effector protein in Western and East Asian Helicobacter pylori strains. J Clin Invest 2012;122:1553-66.
8. Franco AT, Israel DA, Washington MK, et al. Activation of b-catenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci USA 2005;102:10646-51.
9. Murata-Kamiya N, Kurashima Y, Teishikata Y, et al. Helicobacter pylori CagA interacts with E-cadherin and deregulates the beta-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene 2007;26:4617-26.
10. Saadat I, Higashi H, Obuse C, et al. Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity. Nature 2007;447:330-3.
11. Tolwinski NS, Wieschaus E. Rethinking WNT signaling. Trends Genet 2004;20:177-81.
12. Nagy TA, Frey MR, Yan F, et al. Helicobacter pylori regulates cellular migration and apoptosis by activation of phosphatidylinositol 3-kinase signaling. J Infect Dis 2009;199:641-51.
13. Nagy TA, Wroblewski LE, Wang D, et al. beta-Catenin and p120 mediate PPARdelta-dependent proliferation induced by Helicobacter pylori in human and rodent epithelia. Gastroenterology 2011;141:553-64.
14. Ding L, Lu Z, Lu Q, et al. The claudin family of proteins in human malignancy: a clinical perspective. Cancer Manag Res 2013;5:367-75.
15. Amieva MR, Vogelmann R, Covacci A, et al. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 2003;300:1430-4.
16. Wroblewski LE, Shen L, Ogden S, et al. Helicobacter pylori dysregulation of gastric epithelial tight junctions by urease-mediated myosin II activation. Gastroenterology 2009;136:236-46.
17. Ding L, Lu Z, Foreman O, et al. Inflammation and disruption of the mucosal architecture in claudin-7-deficient mice. Gastroenterology 2012;142:305-15.
18. Carrozzino F, Soulie P, Huber D, et al. Inducible expression of Snail selectively increases paracellular ion permeability and differentially modulates tight junction proteins. Am J Physiol 2005;289:C1002-14.
19. Ikenouchi J, Matsuda M, Furuse M, et al. Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci 2003;116(Pt 10):1959-67.
20. Yin Y, Grabowska AM, Clarke PA, et al. Helicobacter pylori potentiates epithelial: mesenchymal transition in gastric cancer: links to soluble HB-EGF, gastrin and matrix metalloproteinase-7. Gut 2010;59:1037-45.
21. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994. IARC Monogr Eval Carcinog Risks Hum 1994;61:1-241.
22. Wroblewski LE, Noble PJ, Pagliocca A, et al. Stimulation of MMP-7 (matrilysin) by Helicobacter pylori in human gastric epithelial cells: role in epithelial cell migration. J Cell Sci 2003;116(Pt 14):3017-26.
23. Peek RM Jr, Blaser MJ, Mays DJ, et al. Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res 1999; 59:6124-31.
24. Cha0turvedi R, Asim M, Romero-Gallo J, et al. Spermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA. Gastroenterology 2011;141:1696-708. e1-2.
25. Noto JM, Khizanishvili T, Chaturvedi R, et al. Helicobacter pylori promotes the expression of Kruppel-like factor 5, a mediator of carcinogenesis, in vitro and in vivo. PLoS ONE 2013;8:e54344.
26. Piazuelo MB, Haque S, Delgado A, et al. Phenotypic differences between esophageal and gastric intestinal metaplasia. Mod Pathol 2004;17:62-74.
27. Barker N, Huch M, Kujala P, et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 2010;6:25-36.
28. de Martel C, Ferlay J, Franceschi S, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 2012;13:607-15.
29. Peek RM Jr, Fiske C, Wilson KT. Role of innate immunity in Helicobacter pylori-induced gastric malignancy. Physiol Rev 2010;90:831-58.
30. Peek RM Jr, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2002;2:28-37.
31. Chen Y, Blaser MJ. Inverse associations of Helicobacter pylori with asthma and allergy. Arch Intern Med 2007;167:821-7.
32. Tsukashita S, Kushima R, Bamba M, et al. Beta-catenin expression in intramucosal neoplastic lesions of the stomach. Comparative analysis of adenoma/dysplasia, adenocarcinoma and signet-ring cell carcinoma. Oncology 2003;64:251-8.
33. Ebert MP, Fei G, Kahmann S, et al. Increased beta-catenin mRNA levels and mutational alterations of the APC and beta-catenin gene are present in intestinal-type gastric cancer. Carcinogenesis 2002;23:87-91.
34. Clements WM, Wang J, Sarnaik A, et al. beta-Catenin mutation is a frequent cause of Wnt pathway activation in gastric cancer. Cancer Res 2002;62:3503-6.
35. Kim HS, Hong EK, Park SY, et al. Expression of beta-catenin and E-cadherin in the adenoma-carcinoma sequence of the stomach. Anticancer Res 2003;23:2863-8.
36. Cheng XX, Sun Y, Chen XY, et al. Frequent translocalization of beta-catenin in gastric cancers and its relevance to tumor progression. Oncol Rep 2004;11:1201-7.
37. Yoshizawa K, Nozaki S, Kato A, et al. Loss of claudin-7 is a negative prognostic factor for invasion and metastasis in oral squamous cell carcinoma. Oncol Rep 2013;29:445-50.
38. Lei Z, Maeda T, Tamura A, et al. EpCAM contributes to formation of functional tight junction in the intestinal epithelium by recruiting claudin proteins. Dev Biol 2012;371:136-45.
39. He H, Chen W, Wang X, et al. Snail is an independent prognostic predictor for progression and patient survival of gastric cancer. Cancer Sci 2012;103:1296-303.
40. Takaishi S, Wang TC. Gene expression profiling in a mouse model of Helicobacter-induced gastric cancer. Cancer Sci 2007;98:284-93.
41. Xiang Z, Censini S, Bayeli PF, et al. Analysis of expression of CagA and VacA virulence factors in 43 strains of Helicobacter pylori reveals that clinical isolates can be divided into two major types and that CagA is not necessary for expression of the vacuolating cytotoxin. Infect Immun 1995;63:94-8.
42. Cover TL, Peek RM Jr. Diet, microbial virulence and Helicobacter pylori-induced gastric cancer. Gut Microbes 2013;4:482-93.
43. Gaddy JA, Radin JN, Loh JT, et al. High dietary salt intake exacerbates Helicobacter pylori-induced gastric carcinogenesis. Infect Immun 2013;81:2258-67.
44. Nomura A, Chyou PH, Stemmermann GN. Association of serum ferritin levels with the risk of stomach cancer. Cancer Epidemiol Biomarkers Prev 1992;1:547-50.
45. Harrison LE, Zhang ZF, Karpeh MS, et al. The role of dietary factors in the intestinal and diffuse histologic subtypes of gastric adenocarcinoma: a case-control study in the U.S. Cancer 1997;80:1021-8.
46. Yuan W, Li Y, Yang K, et al. Iron deficiency anemia in Helicobacter pylori infection: meta-analysis of randomized controlled trials. Scand J Gastroenterol 2010;45:665-76.
47. Van Heyningen WE, Gladstone GP. The neurotoxin of Shigella shigae. III. The effect of iron on production of the toxin. Br J Exp Pathol 1953;34:221-9.
48. Calderwood SB, Mekalanos JJ. Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J Bacteriol 1987;169:4759-64.
49. Tai SP, Krafft AE, Nootheti P, et al. Coordinate regulation of siderophore and diphtheria toxin production by iron in Corynebacterium diphtheriae. Microb Pathog 1990;9:267-73.
50. Bjorn MJ, Iglewski BH, Ives SK, et al. Effect of iron on yields of exotoxin A in cultures of Pseudomonas aeruginosa PA-103. Infect Immun 1978;19:785-91.
51. Tan S, Noto JM, Romero-Gallo J, et al. Helicobacter pylori perturbs iron trafficking in the epithelium to grow on the cell surface. PLoS Pathog 2011; 7:e1002050.
52. Noto JM, Gaddy JA, Lee JY, et al. Iron deficiency accelerates Helicobacter pylori-induced carcinogenesis in rodents and humans. J Clin Invest 2013;123:479-92.