Upregulation of progranulin by Helicobacter pylori in human gastric epithelial cells via p38MAPK and MEK1/2 signaling pathway: Role in epithelial cell proliferation and migration

FEMS Immunology and Medical Microbiology

Volumn 63, Issue 1, 2011, Pages 82-92

  Wang, Hongyan ^a,b   Sun, Yundong ^a   Liu, Shili ^a   Yu, Han ^a   Li, Wenjuan ^a   Zeng, Jiping ^a   Chen, Chunyan ^a   Jia, Jihui ^a  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b WEIFANG MEDICAL UNIVERSITY   (China)

Author keywords

Gastric epithelial cells; Helicobacter pylori; Progranulin

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROGRANULIN;

ARTICLE; CELL MIGRATION; CELL PROLIFERATION; COLONY FORMING UNIT; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; GASTRITIS; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INHIBITION KINETICS; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STOMACH CANCER; STOMACH CARCINOGENESIS; STOMACH EPITHELIUM; UPREGULATION;

CELL MIGRATION ASSAYS; CELL MOVEMENT; CELL PROLIFERATION; COLONY-FORMING UNITS ASSAY; EPITHELIAL CELLS; GASTRIC MUCOSA; GENE EXPRESSION PROFILING; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 80052599271     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2011.00833.x     Document Type: Article

References (46)

1. Al-Ghoul L, Wessler S, Hundertmark T, Krüger S, Fischer W, Wunder C, Haas R, Roessner A & Naumann M (2004) Analysis of the type IV secretion system-dependent cell motility of Helicobacter pylori-infected epithelial cells. Biochem Bioph Res Co322: 860-866.
2. Bagnato A, Tecce R, Di Castro V & Catt KJ (1997) Activation of mitogenic signaling by endothelin 1 in ovarian carcinoma cells. Cancer Res57: 1306-1311.
3. Boncristiano M, Paccani SR, Barone S, Ulivieri C, Patrussi L, Ilver D, Amedei A, D'Elios MM, Telford JL & Baldari CT (2003) The Helicobacter pylori vacuolating toxin inhibits T cell activation by two independent mechanisms. J Exp Med198: 1887-1897.
4. Censini S, Lange C, Xiang Z, Crabtree JE, Ghiara P, Borodovsky M, Rappuoli R & Covacci A (1996) cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. P Natl Acad Sci USA93: 14648-14653.
5. Chang L & Karin M (2001) Mammalian MAP kinase signalling cascades. Nature410: 37-40.
6. Chen XY, Li JS, Liang QP, He DZ & Zhao J (2008) Expression of PC cell-derived growth factor and vascular endothelial growth factor in esophageal squamous cell carcinoma and their clinicopathologic significance. Chinese Med J121: 881-886.
7. Cheung ST, Wong SY, Leung KL, Chen X, So S, Ng IO & Fan ST (2004) Granulin-epithelin precursor overexpression promotes growth and invasion of hepatocellular carcinoma. Clin Cancer Res10: 7629-7636.
8. Chochi K, Ichikura T, Kinoshita Met al. (2008) Helicobacter pylori augments growth of gastric cancers via the lipopolysaccharide-Toll-like receptor 4 pathway whereas its lipopolysaccharide attenuates antitumor activities of human mononuclear cells. Clin Cancer Res14: 2909-2917.
9. Cover TL, Krishna US, Israel DA & Peek RMJr (2003) Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res63: 951-957.
10. Daniel R, He Z, Carmichael KP, Halper J & Bateman A (2000) Cellular localization of gene expression for progranulin. J Histochem Cytochem48: 999-1009.
11. Ding SZ, Smith MFJr & Goldberg JB (2008) Helicobacter pylori and mitogen-activated protein kinases regulate the cell cycle, proliferation and apoptosis in gastric epithelial cells. J Gastroenterol Hepatol23: e67-78.
12. Ernst PB, Peura DA & Crowe SE (2006) The translation of Helicobacter pylori basic research to patient care. Gastroenterology130: 188-206.
13. Fraser AG, Sim R, Sankey EA, Dhillon AP & Pounder RE (1994) Effect of eradication of Helicobacter pylori on gastric epithelial cell proliferation. Aliment Pharmacol Ther8: 167-173.
14. Fukazawa T, Maeda Y, Sladek FM & Owen-Schaub LB (2004) Development of a cancer-targeted tissue-specific promoter system. Cancer Res64: 363-369.
15. Guo W & Giancotti FG (2004) Integrin signalling during tumour progression. Nat Rev Mol Cell Bio5: 816-826.
16. Handa O, Naito Y & Yoshikawa T (2007) CagA protein of Helicobacter pylori: a hijacker of gastric epithelial cell signaling. Biochem Pharmacol 73: 1697-1702.
17. He Z, Ong CH, Halper J & Bateman A (2003) Progranulin is a mediator of the wound response. Nat Med9: 225-229.
18. Higashi H, Tsutsumi R, Muto S, Sugiyama T, Azuma T, Asaka M & Hatakeyama M (2002) SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science295: 683-686.
19. Huang JQ, Zheng GF, Sumanac K, Irvine EJ & Hunt RH (2003) Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology125: 1636-1644.
20. Houghton J & Wang TC (2005) Helicobacter pylori and gastric cancer: a new paradigm for inflammation-associated epithelial cancers. Gastroenterology 128: 1567-1578.
21. Israel DA & Peek RMJr (2006) The role of persistence in Helicobacter pylori pathogenesis. Curr Opin Gastroenterol22: 3-7.
22. Johnson GL & Lapadat R (2002) Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science298: 1911-1912.
23. Jones MB, Spooner M & Kohn EC (2003) The granulin epithelin precursor: a putative new growth factor for ovarian cancer. Gynecol Oncol 88: 136-139.
24. Keates AC, Tummala S, Peek RMJr, Csizmadia E, Kunzli B, Becker K & Correa P (2008) Helicobacter pylori infection stimulates plasminogen activator inhibitor 1 production by gastric epithelial cells. Infect Immun76: 3992-3999.
25. Krueger S, Kuester D, Bernhardt A, Wex T & Roessner A (2009) Regulation of cathepsin X overexpression in H. pylori-infected gastric epithelial cells and macrophages. J Pathol217: 581-588.
26. Linē A, Stengrēvics A, Slucka Z, Li G, Jankevics E & Rees RC (2002) Serological identification and expression analysis of gastric cancer-associated genes. Br J Cancer86: 1824-1830.
27. Lu R & Serrero G (2000) Inhibition of PC cell-derived growth factor (PCDGF, epithelin/granulin precursor) expression by antisense PCDGF cDNA transfection inhibits tumorigenicity of the human breast carcinoma cell line MDA-MB-468. Proc Natl Acad Sci USA97: 3993-3998.
28. Maeda S, Yoshida H, Mitsuno Y, Hirata Y, Ogura K, Shiratori Y & Omata M (2002) Analysis of apoptotic and antiapoptotic signalling pathways induced by Helicobacter pylori. Gut50: 771-778.
29. Matsumura N, Mandai M, Miyanishi M, Fukuhara K, Baba T, Higuchi T, Kariya M, Takakura K & Fujii S (2006) Oncogenic property of acrogranin in human uterine leiomyosarcoma: direct evidence of genetic contribution in in vivo tumorigenesis. Clin Cancer Res 12: 1402-1411.
30. Mauro L, Sisci D, Bartucci M, Salerno M, Kim J, Tam T, Guvakova MA, Ando S & Surmacz E (1999) SHC-alpha5beta1 integrin interactions regulate breast cancer cell adhesion and motility. Exp Cell Res252: 439-448.
31. +Helicobacter pylori induces homotypic aggregation of macrophage-like cells by upregulation and recruitment of intracellular adhesion molecule 1 to the cell surface. Infect Immun70: 4687-4691.
32. Monami G, Gonzalez EM, Hellman M, Gomella LG, Baffa R, Iozzo RV & Morrione A (2006) Proepithelin promotes migration and invasion of 5637 bladder cancer cells through the activation of ERK1/2 and the formation of a paxillin/FAK/ERK complex. Cancer Res66: 7103-7110.
33. Nagy TA, Frey MR, Yan F, Israel DA, Polk DB & Peek RMJr (2009) Helicobacter pylori regulates cellular migration and apoptosis by activation of phosphatidylinositol 3-kinase signaling. J Infect Dis199: 641-651.
34. Peek RM Jr & Blaser MJ (2002) Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer2: 28-37.
35. Peek RM Jr, Wirth HP, Moss SF, Yang M, Abdalla AM, Tham KT, Zhang T, Tang LH, Modlin IM & Blaser MJ (2000) Helicobacter pylori alters gastric epithelial cell cycle events and gastrin secretion in Mongolian gerbils. Gastroenterology118: 48-59.
36. Qin J, Díaz-Cueto L, Schwarze JE, Takahashi Y, Imai M, Isuzugawa K, Yamamoto S, Chang KT, Gerton GL & Imakawa K (2005) Effects of progranulin on blastocyst hatching and subsequent adhesion and outgrowth in the mouse. Biol Reprod73: 434-442.
37. Saha A, Hammond CE, Trojanowska M & Smolka AJ (2008) Helicobacter pylori-induced H, K-ATPase alpha-subunit gene repression is mediated by NF-kappaB p50 homodimer promoter binding. Am J Physiol Gastrointest Liver Physiol294: G795-807.
38. Take S, Mizuno M, Ishiki K, Nagahara Y, Yoshida Y, Yokota K, Oguma K, Okada H & Shiratori Y (2005) The effect of eradicating Helicobacter pylori on the development of gastric cancer in patients with peptic ulcer disease. Am J Gastroenterol100: 1037-1042.
39. Tangkeangsirisin W & Serrero G (2004) PC cell-derived growth factor (PCDGF/GP88, progranulin) stimulates migration, invasiveness and VEGF expression in breast cancer cells. Carcinogenesis25: 1587-1592.
40. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N & Schlemper RJ (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med345: 784-789.
41. Wilson KT & Crabtree JE (2007) Immunology of Helicobacter pylori: insights into the failure of the immune response and perspectives on vaccine studies. Gastroenterology 133: 288-308.
42. Wong BC, Lam SK, Wong WMet al. (2004) Helicobacter pylori eradication to prevent gastric cancer in a high risk region of China: a randomized controlled trial. JAMA 291: 187-194.
43. Wroblewski LE, Noble PJ, Pagliocca A, Pritchard DM, Hart CA, Campbell F, Dodson AR, Dockray GJ & Varro A (2003) Stimulation of MMP-7 (matrilysin) by Helicobacter pylori in human gastric epithelial cells: role in epithelial cell migration. J Cell Sci 116: 3017-3026.
44. Yokota S, Okabayashi T, Rehli M, Fujii N & Amano K (2010) Helicobacter pylori lipopolysaccharides upregulate Toll-like receptor 4 expression and proliferation of gastric epithelial cells via MEK1/2-ERK1/2 MAP mitogen-activated protein kinase pathway. Infect Immun78: 468-476.
45. Zanocco-Marani T, Bateman A, Romano G, Valentinis B, He ZH & Baserga R (1999) Biological activities and signaling pathways of the granulin/epithelin precursor. Cancer Res59: 5331-5340.
46. Zhang H & Serrero G (1998) Inhibition of tumorigenicity of the teratoma PC cell line by transfection with antisense cDNA for PC cell-derived growth factor (PCDGF, epithelin/granulin precursor). Proc Natl Acad Sci USA95: 14202-14207.