H. pylori-induced promoter hypermethylation downregulates USF1 and USF2 transcription factor gene expression

Cellular Microbiology

Volumn 12, Issue 8, 2010, Pages 1124-1133

  Bussière, Françoise I ^a   Michel, Valérie ^a   Mémet, Sylvie ^a,b   Avé, Patrick ^a   Vivas, José Ramos ^c   Huerre, Michel ^a   Touati, Eliette ^a  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c Hospital Santa Cruz de Liencres   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; UPSTREAM STIMULATORY FACTOR 1; UPSTREAM STIMULATORY FACTOR 2; UPSTREAM STIMULATORY FACTOR; USF1 PROTEIN, HUMAN; USF1 PROTEIN, MOUSE; USF2 PROTEIN, HUMAN; USF2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DNA BINDING; DNA METHYLATION; DOWN REGULATION; E BOX ELEMENT; GENE EXPRESSION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; STOMACH; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; EPITHELIUM CELL; GEL MOBILITY SHIFT ASSAY; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PATHOGENICITY;

ANIMALS; CELL LINE; DNA METHYLATION; DOWN-REGULATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPITHELIAL CELLS; GENE EXPRESSION; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; MALE; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; UPSTREAM STIMULATORY FACTORS;

HELICOBACTER PYLORI; MUS;

EID: 77957165327     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01457.x     Document Type: Article

References (39)

1. Atchley WR, Fitch WM. A natural classification of the basic helix-loop-helix class of transcription factors. Proc Natl Acad Sci USA 1997, 94:5172-5176.
2. Atherton JC. The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol 2006, 1:63-96.
3. Baylin SB, Ohm JE. Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 2006, 6:107-116.
4. Chan AO, Peng JZ, Lam SK, Lai KC, Yuen MF, Cheung HK. Eradication of Helicobacter pylori infection reverses E-cadherin promoter hypermethylation. Gut 2006, 55:463-468.
5. Chang JT, Yang HT, Wang TC, Cheng AJ. Upstream stimulatory factor (USF) as a transcriptional suppressor of human telomerase reverse transcriptase (hTERT) in oral cancer cells. Mol Carcinog 2005, 44:183-192.
6. Chen N, Szentirmay MN, Pawar SA, Sirito M, Wang J, Wang Z. Tumor-suppression function of transcription factor USF2 in prostate carcinogenesis. Oncogene 2006, 25:579-587.
7. Cheng Y, Chaturvedi R, Asim M, Bussiere FI, Scholz A, Xu H. Helicobacter pylori-induced macrophage apoptosis requires activation of ornithine decarboxylase by c-Myc. J Biol Chem 2005, 280:22492-22496.
8. Corre S, Galibert MD. Upstream stimulating factors: highly versatile stress-responsive transcription factors. Pigment Cell Res 2005, 18:337-348.
9. Correa P, Houghton J. Carcinogenesis of Helicobacter pylori. Gastroenterology 2007, 133:659-672.
10. Cox JM, Clayton CL, Tomita T, Wallace DM, Robinson PA, Crabtree JE. cDNA array analysis of cag pathogenicity island-associated Helicobacter pylori epithelial cell response genes. Infect Immun 2001, 69:6970-6980.
11. Farinha P, Gascoyne RD. Helicobacter pylori and MALT lymphoma. Gastroenterology 2005, 128:1579-1605.
12. Griswold MD, Kim JS. Site-specific methylation of the promoter alters deoxyribonucleic acid-protein interactions and prevents follicle-stimulating hormone receptor gene transcription. Biol Reprod 2001, 64:602-610.
13. Ismail PM, Lu T, Sawadogo M. Loss of USF transcriptional activity in breast cancer cell lines. Oncogene 1999, 18:5582-5591.
14. Israel DA, Salama N, Arnold CN, Moss SF, Ando T, Wirth HP. Helicobacter pylori strain-specific differences in genetic content, identified by microarray, influence host inflammatory responses. J Clin Invest 2001, 107:611-620.
15. Israel MA, Hernandez MC, Florio M, Andres-Barquin PJ, Mantani A, Carter JH, Julin CM. Id gene expression as a key mediator of tumor cell biology. Cancer Res 1999, 59:1726s-1730s.
16. Jaiswal AS, Narayan S. Upstream stimulating factor-1 (USF1) and USF2 bind to and activate the promoter of the adenomatous polyposis coli (APC) tumor suppressor gene. J Cell Biochem 2001, 81:262-277.
17. Juttner S, Cramer T, Wessler S, Walduck A, Gao F, Schmitz F. Helicobacter pylori stimulates host cyclooxygenase-2 gene transcription: critical importance of MEK/ERK-dependent activation of USF1/-2 and CREB transcription factors. Cell Microbiol 2003, 5:821-834.
18. Kaise M, Yamasaki T, Yonezawa J, Miwa J, Ohta Y, Tajiri H. CpG island hypermethylation of tumor-suppressor genes in H. pylori-infected non-neoplastic gastric mucosa is linked with gastric cancer risk. Helicobacter 2008, 13:35-41.
19. Kang GH, Shim YH, Jung HY, Kim WH, Ro JY, Rhyu MG. CpG island methylation in premalignant stages of gastric carcinoma. Cancer Res 2001, 61:2847-2851.
20. Kudo T, Lu H, Wu JY, Ohno T, Wu MJ, Genta RM. Pattern of transcription factor activation in Helicobacter pylori-infected Mongolian gerbils. Gastroenterology 2007, 132:1024-1038.
21. 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, 112:1386-1397.
22. Lehours P, Menard A, Dupouy S, Bergey B, Richy F, Zerbib F. Evaluation of the association of nine Helicobacter pylori virulence factors with strains involved in low-grade gastric mucosa-associated lymphoid tissue lymphoma. Infect Immun 2004, 72:880-888.
23. Luo X, Sawadogo M. Antiproliferative properties of the USF family of helix-loop-helix transcription factors. Proc Natl Acad Sci USA 1996, 93:1308-1313.
24. Maekita T, Nakazawa K, Mihara M, Nakajima T, Yanaoka K, Iguchi M. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin Cancer Res 2006, 12:989-995.
25. Manzo BA, Crabtree JE, Fiona Campbell M, Tweedle D, Potten CS, Bajaj-Elliott M. Helicobacter pylori regulates the expression of inhibitors of DNA binding (Id) proteins by gastric epithelial cells. Microbes Infect 2006, 8:1064-1074.
26. Nakajima T, Maekita T, Oda I, Gotoda T, Yamamoto S, Umemura S. Higher methylation levels in gastric mucosae significantly correlate with higher risk of gastric cancers. Cancer Epidemiol Biomarkers Prev 2006, 15:2317-2321.
27. Nardone G, Compare D. Epigenetic alterations due to diet and Helicobacter pylori infection in gastric carcinogenesis. Expert Rev Gastroenterol Hepatol 2008, 2:243-248.
28. Naumann M, Crabtree JE. Helicobacter pylori-induced epithelial cell signalling in gastric carcinogenesis. Trends Microbiol 2004, 12:29-36.
29. Parsonnet J, Isaacson PG. Bacterial infection and MALT lymphoma. N Engl J Med 2004, 350:213-215.
30. Prophet EB, Mills B, Arrington JB, Sobin LH. Laboratory methods in histotechnology. 1992, AFIP Washington D.C.
31. Sato F, Meltzer SJ. CpG island hypermethylation in progression of esophageal and gastric cancer. Cancer 2006, 106:483-493.
32. Sirito M, Lin Q, Maity T, Sawadogo M. Ubiquitous expression of the 43- and 44-kDa forms of transcription factor USF in mammalian cells. Nucleic Acids Res 1994, 22:427-433.
33. Takakura M, Kyo S, Kanaya T, Hirano H, Takeda J, Yutsudo M, Inoue M. Cloning of human telomerase catalytic subunit (hTERT) gene promoter and identification of proximal core promoter sequences essential for transcriptional activation in immortalized and cancer cells. Cancer Res 1999, 59:551-557.
34. Touati E, Michel V, Thiberge JM, Wuscher N, Huerre M, Labigne A. Chronic Helicobacter pylori infections induce gastric mutations in mice. Gastroenterology 2003, 124:1408-1419.
35. Umetani N, Takeuchi H, Fujimoto A, Shinozaki M, Bilchik AJ, Hoon DS. Epigenetic inactivation of ID4 in colorectal carcinomas correlates with poor differentiation and unfavorable prognosis. Clin Cancer Res 2004, 10:7475-7483.
36. Valinluck V, Sowers LC. Inflammation-mediated cytosine damage: a mechanistic link between inflammation and the epigenetic alterations in human cancers. Cancer Res 2007, 67:5583-5586.
37. Vivas JR, Regnault B, Michel V, Bussiere FI, Ave P, Huerre M. Interferon gamma-signature transcript profiling and IL-23 upregulation in response to Helicobacter pylori infection. Int J Immunopathol Pharmacol 2008, 21:515-526.
38. Wessler S, Hocker M, Fischer W, Wang TC, Rosewicz S, Haas R. Helicobacter pylori activates the histidine decarboxylase promoter through a mitogen-activated protein kinase pathway independent of pathogenicity island-encoded virulence factors. J Biol Chem 2000, 275:3629-3636.
39. Zhong G, Fan T, Liu L. Chlamydia inhibits interferon gamma-inducible major histocompatibility complex class II expression by degradation of upstream stimulatory factor 1. J Exp Med 1999, 189:1931-1938.