Helicobacter pylori urease and flagellin alter mucin gene expression in human gastric cancer cells

Gastric Cancer

Volumn 17, Issue 2, 2014, Pages 235-246

  Perrais, Michaël ^a   Rousseaux, Christel ^b   Ducourouble, Marie Paule ^a   Courcol, René ^b   Vincent, Pascal ^b   Jonckheere, Nicolas ^a   Van Seuningen, Isabelle ^a  

^a JEAN PIERRE AUBERT RESEARCH CENTER   (France)

^b INSERM   (France)

Author keywords

Helicobacter pylori; MUC5AC; Mucin; Stomach; Urease

Indexed keywords

CYTOKINE; FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MUCIN 5AC; UREASE;

GENE EXPRESSION REGULATION; GENETICS; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOMACH TUMOR; TUMOR CELL CULTURE; VIROLOGY; VIRULENCE; WESTERN BLOTTING;

BLOTTING, WESTERN; CYTOKINES; FLAGELLIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MUCIN 5AC; NF-KAPPA B; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STOMACH NEOPLASMS; TUMOR CELLS, CULTURED; UREASE; VIRULENCE;

EID: 84898814382     PISSN: 14363291     EISSN: 14363305     Source Type: Journal    
DOI: 10.1007/s10120-013-0267-5     Document Type: Article

References (49)

1. Correa P. Helicobacter pylori as a pathogen and carcinogen. J Physiol Pharmacol. 1997;48(suppl 4):19-24. (Pubitemid 127699206)
2. Dunn BE, Cohen H, Blaser MJ. Helicobacter pylori. Clin Microbiol Rev. 1997;10(4):720-41. (Pubitemid 27477732)
3. Peek RM Jr, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2002;2(1):28-37. (Pubitemid 37328805)
4. Barreto-Zuniga R, Maruyama M, Kato Y, Aizu K, Ohta H, Takekoshi T, et al. Significance of Helicobacter pylori infection as a risk factor in gastric cancer: serological and histological studies. J Gastroenterol. 1997;32(3):289-94. (Pubitemid 27254793)
5. Corfield AP, Carroll D, Myerscough N, Probert CS. Mucins in the gastrointestinal tract in health and disease. Front Biosci. 2001;6:D1321-57.
6. Hollingsworth MA, Swanson BJ. Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer. 2004;4(1):45-60. (Pubitemid 38082153)
7. Dekker J, Rossen JW, Buller HA, Einerhand AW. The MUC family: an obituary. Trends Biochem Sci. 2002;27(3):126-31. (Pubitemid 34219322)
8. Jonckheere N, Skrypek N, Frenois F, Van Seuningen I. Membrane-bound mucin modular domains: from structure to function. Biochimie 2013;95(6):1077-1086
9. Buisine MP, Devisme L, Maunoury V, Deschodt E, Gosselin B, Copin MC, et al. Developmental mucin gene expression in the gastroduodenal tract and accessory digestive glands. I. Stomach. A relationship to gastric carcinoma. J Histochem Cytochem. 2000;48(12):1657-66.
10. Teixeira A, David L, Reis CA, Costa J, Sobrinho-Simoes M. Expression of mucins (MUC1, MUC2, MUC5AC, and MUC6) and type 1 Lewis antigens in cases with and without Helicobacter pylori colonization in metaplastic glands of the human stomach. J Pathol. 2002;197(1):37-43. (Pubitemid 34450162)
11. Allen A, Newton J, Oliver L, Jordan N, Strugala V, Pearson JP, et al. Mucus and H. pylori. J Physiol Pharmacol. 1997;48(3):297-305. (Pubitemid 27421473)
12. Kocer B, Ulas M, Ustundag Y, Erdogan S, Karabeyoglu M, Yldrm O, et al. A confirmatory report for the close interaction of Helicobacter pylori with gastric epithelial MUC5AC expression. J Clin Gastroenterol. 2004;38(6):496-502. (Pubitemid 38808422)
13. Linden SK, Wickstrom C, Lindell G, Gilshenan K, Carlstedt I. Four modes of adhesion are used during Helicobacter pylori binding to human mucins in the oral and gastric niches. Helicobacter. 2008;13(2):81-93. (Pubitemid 351347660)
14. Van de Bovenkamp JH, Mahdavi J, Korteland-Van Male AM, Buller HA, Einerhand AW, Boren T, et al. The MUC5AC glycoprotein is the primary receptor for Helicobacter pylori in the human stomach. Helicobacter. 2003;8(5):521-32. (Pubitemid 37288100)
15. Magalhaes A, Reis CA. Helicobacter pylori adhesion to gastric epithelial cells is mediated by glycan receptors. Braz J Med Biol Res. 2010;43(7):611-8.
16. Byrd JC, Yan P, Sternberg L, Yunker CK, Scheiman JM, Bresalier RS. Aberrant expression of gland-type gastric mucin in the surface epithelium of Helicobacter pylori-infected patients. Gastroenterology. 1997;113(2):455-64. (Pubitemid 27351771)
17. Babu SD, Jayanthi V, Devaraj N, Reis CA, Devaraj H. Expression profile of mucins (MUC2, MUC5AC and MUC6) in Helicobacter pylori-infected pre-neoplastic and neoplastic human gastric epithelium. Mol Cancer. 2006;5:10.
18. Byrd JC, Yunker CK, Xu QS, Sternberg LR, Bresalier RS. Inhibition of gastric mucin synthesis by Helicobacter pylori. Gastroenterology. 2000;118(6):1072-9. (Pubitemid 30346984)
19. Morgenstern S, Koren R, Moss SF, Fraser G, Okon E, Niv Y. Does Helicobacter pylori affect gastric mucin expression? Relationship between gastric antral mucin expression and H. pylori colonization. Eur J Gastroenterol Hepatol. 2001;13(1):19-23. (Pubitemid 32099563)
20. Dunn BE, Phadnis SH. Structure, function and localization of Helicobacter pylori urease. Yale J Biol Med. 1998;71(2):63-73. (Pubitemid 29281910)
21. O'Toole PW, Lane MC, Porwollik S. Helicobacter pylori motility. Microbes Infect. 2000;2(10):1207-14.
22. Backert S, Ziska E, Brinkmann V, Zimny-Arndt U, Fauconnier A, Jungblut PR, et al. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell Microbiol. 2000;2(2):155-64. (Pubitemid 30368030)
23. Perrais M, Pigny P, Buisine MP, Porchet N, Aubert JP, Van Seuningen-Lempire I. Aberrant expression of human mucin gene MUC5B in gastric carcinoma and cancer cells. Identification and regulation of a distal promoter. J Biol Chem. 2001;276(18):15386-96.
24. Ferrero RL, Cussac V, Courcoux P, Labigne A. Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J Bacteriol. 1992;174(13):4212-7.
25. Suerbaum S, Josenhans C, Labigne A. Cloning and genetic characterization of the Helicobacter pylori and Helicobacter mustelae flaB flagellin genes and construction of H. pylori flaA- and flaB-negative mutants by electroporation-mediated allelic exchange. J Bacteriol. 1993;175(11):3278-88. (Pubitemid 23163369)
26. Chevalier C, Thiberge JM, Ferrero RL, Labigne A. Essential role of Helicobacter pylori gamma-glutamyltranspeptidase for the colonization of the gastric mucosa of mice. Mol Microbiol. 1999;31(5):1359-72. (Pubitemid 29110095)
27. Lee A, O'Rourke J, De Ungria MC, Robertson B, Daskalopoulos G, Dixon MF. A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology. 1997;112(4):1386-97. (Pubitemid 27157555)
28. Perrais M, Pigny P, Copin MC, Aubert JP, Van Seuningen I. Induction of MUC2 and MUC5AC mucins by factors of the epidermal growth factor (EGF) family is mediated by EGF receptor/Ras/Raf/extracellular signal-regulated kinase cascade and Sp1. J Biol Chem. 2002;277(35):32258-67. (Pubitemid 34969042)
29. Van Seuningen I, Perrais M, Pigny P, Porchet N, Aubert JP. Sequence of the 50 -flanking region and promoter activity of the human mucin gene MUC5B in different phenotypes of colon cancer cells. Biochem J. 2000;348(pt 3):675-86. (Pubitemid 30410259)
30. Kawano S, Tsujii M, Fusamoto H, Sato N, Kamada T. Chronic effect of intragastric ammonia on gastric mucosal structures in rats. Dig Dis Sci. 1991;36(1):33-8.
31. McNamara N, Khong A, McKemy D, Caterina M, Boyer J, Julius D, et al. ATP transduces signals from ASGM1, a glycolipid that functions as a bacterial receptor. Proc Natl Acad Sci USA. 2001;98(16):9086-91. (Pubitemid 32743873)
32. Meyer-ter-Vehn T, Covacci A, Kist M, Pahl HL. Helicobacter pylori activates mitogen-activated protein kinase cascades and induces expression of the proto-oncogenes c-fos and c-jun. J Biol Chem. 2000;275(21):16064-72. (Pubitemid 30366914)
33. Basbaum C, Lemjabbar H, Longphre M, Li D, Gensch E, McNamara N. Control of mucin transcription by diverse injury-induced signaling pathways. Am J Respir Crit Care Med. 1999;160(5 pt 2):S44-8.
34. Van Seuningen I, Pigny P, Perrais M, Porchet N, Aubert JP. Transcriptional regulation of the 11p15 mucin genes. Towards new biological tools in human therapy, in inflammatory diseases and cancer? Front Biosci. 2001;6:D1216-34.
35. Vincent A, Perrais M, Desseyn JL, Aubert JP, Pigny P, Van Seuningen I. Epigenetic regulation (DNA methylation, histone modifications) of the 11p15 mucin genes (MUC2, MUC5AC, MUC5B, MUC6) in epithelial cancer cells. Oncogene. 2007;26(45):6566-76. (Pubitemid 47530602)
36. Harris PR, Mobley HL, Perez-Perez GI, Blaser MJ, Smith PD. Helicobacter pylori urease is a potent stimulus of mononuclear phagocyte activation and inflammatory cytokine production. Gastroenterology. 1996;111(2):419-25. (Pubitemid 26256730)
37. Keates S, Hitti YS, Upton M, Kelly CP. Helicobacter pylori infection activates NF-kappa B in gastric epithelial cells. Gastroenterology. 1997;113(4):1099-109. (Pubitemid 27418963)
38. van Den Brink GR, ten Kate FJ, Ponsioen CY, Rive MM, Tytgat GN, van Deventer SJ, et al. Expression and activation of NF-kappa B in the antrum of the human stomach. J Immunol. 2000;164(6):3353-9. (Pubitemid 30149001)
39. Dohrman A, Miyata S, Gallup M, Li JD, Chapelin C, Coste A, et al. Mucin gene (MUC 2 and MUC 5AC) upregulation by gram-positive and gram-negative bacteria. Biochim Biophys Acta. 1998;1406(3):251-9. (Pubitemid 28269307)
40. Li JD, Feng W, Gallup M, Kim JH, Gum J, Kim Y, et al. Activation of NF-kappaB via a Src-dependent Ras-MAPK-pp 90rsk pathway is required for Pseudomonas aeruginosa-induced mucin overproduction in epithelial cells. Proc Natl Acad Sci USA. 1998;95(10):5718-23. (Pubitemid 28224162)
41. Li D, Gallup M, Fan N, Szymkowski DE, Basbaum CB. Cloning of the amino-terminal and 5′-flanking region of the human MUC5AC mucin gene and transcriptional up-regulation by bacterial exoproducts. J Biol Chem. 1998;273(12):6812-20. (Pubitemid 28160344)
42. Debailleul V, Laine A, Huet G, Mathon P, d'Hooghe MC, Aubert JP, et al. Human mucin genes MUC2, MUC3, MUC4, MUC5AC, MUC5B, and MUC6 express stable and extremely large mRNAs and exhibit a variable length polymorphism. An improved method to analyze large mRNAs. J Biol Chem. 1998;273(2):881-90. (Pubitemid 28049180)
43. Harris PR, Weber HC, Wilcox CM, Jensen RT, Smith PD. Cytokine gene profile in gastric mucosa in Helicobacter pylori infection and Zollinger-Ellison syndrome. Am J Gastroenterol. 2002;97(2):312-8. (Pubitemid 34160755)
44. Johansson ME, Sjovall H, Hansson GC. The gastrointestinal mucus system in health and disease. Nat Rev Gastroenterol Hepatol. 2013. doi:10.1038/nrgastro. 2013.35.
45. Fukuda M, Kawakubo M, Ito Y, Kobayashi M, Lee H, Nakayama J. Assay of human gastric mucin as a natural antibiotic against Helicobacter pylori. Methods Enzymol. 2006;415:164-79. (Pubitemid 44751097)
46. Kawakubo M, Ito Y, Okimura Y, Kobayashi M, Sakura K, Kasama S, et al. Natural antibiotic function of a human gastric mucin against Helicobacter pylori infection. Science. 2004;305(5686):1003-6. (Pubitemid 39071775)
47. Kobayashi M, Lee H, Nakayama J, Fukuda M. Roles of gastric mucin-type O-glycans in the pathogenesis of Helicobacter pylori infection. Glycobiology. 2009;19(5):453-61.
48. Matsuzwa M, Ota H, Hayama M, Zhang MX, Sano K, Honda T, et al. Helicobacter pylori infection up-regulates gland mucous cell-type mucins in gastric pyloric mucosa. Helicobacter. 2003;8(6):594-600. (Pubitemid 37553433)
49. Skoog EC, Sjoling A, Navabi N, Holgersson J, Lundin SB, Linden SK. Human gastric mucins differently regulate Helicobacter pylori proliferation, gene expression and interactions with host cells. PLoS ONE. 2012;7(5):e36378.