Mutagenic potency of Helicobacter pylori in the gastric mucosa of mice is determined by sex and duration of infection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 34, 2010, Pages 15217-15222

  Sheh, Alexander ^a   Lee, Chung Wei ^a,b   Masumura, Kenichi ^c   Rickman, Barry H ^b   Nohmi, Takehiko ^c   Wogan, Gerald N ^a   Fox, James G ^a,b   Schauer, David B ^a,b  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

Gpt delta mouse; Helicobacter; Inflammation; Mutagenesis; Sexual dimorphism

Indexed keywords

DNA; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; BACTERIUM ANTIBODY; CYTOKINE; ESCHERICHIA COLI PROTEIN; GLYCOSYLTRANSFERASE; GPT PROTEIN, E COLI; IMMUNOGLOBULIN G; INDUCIBLE NITRIC OXIDE SYNTHASE; NOS2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CONTROLLED STUDY; DNA DAMAGE; FEMALE; GENE DELETION; GENE EXPRESSION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; IMMUNE RESPONSE; MALE; MOUSE; MUTAGENESIS; NONHUMAN; OXIDATIVE STRESS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH LESION; STOMACH MUCOSA; ANIMAL; BLOOD; C57BL MOUSE; GASTRITIS; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PATHOLOGY; SEXUAL DEVELOPMENT; TIME; TRANSGENIC MOUSE;

HELICOBACTER; HELICOBACTER PYLORI; MUS;

ANIMALS; ANTIBODIES, BACTERIAL; CYTOKINES; ESCHERICHIA COLI PROTEINS; FEMALE; GASTRIC MUCOSA; GASTRITIS; GENE EXPRESSION; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; IMMUNOGLOBULIN G; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTAGENESIS; MUTATION; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PENTOSYLTRANSFERASES; SEX CHARACTERISTICS; TIME FACTORS;

EID: 77956992674     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1009017107     Document Type: Article

References (58)

1. Fox JG, Wang TC (2007) Inflammation, atrophy, and gastric cancer. J Clin Invest 117:60-69.
2. Suerbaum S, Michetti P (2002) Helicobacter pylori infection. N Engl J Med 347:1175-1186.
3. International Agency for Research on Cancer (1994) 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 61:1-241.
4. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860-867.
5. Obst B, Wagner S, Sewing KF, Beil W (2000) Helicobacter pylori causes DNA damage in gastric epithelial cells. Carcinogenesis 21:1111-1115.
6. Xu H, et al. (2004) Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: Implications for gastric carcinogenesis. Cancer Res 64:8521-8525.
7. Davies GR, et al. (1994) Relationship between infective load of Helicobacter pylori and reactive oxygen metabolite production in antral mucosa. Scand J Gastroenterol 29:419-424.
8. Davies GR, et al. (1994) Helicobacter pylori stimulates antral mucosal reactive oxygen metabolite production in vivo. Gut 35:179-185.
9. Mannick EE, et al. (1996) Inducible nitric oxide synthase, nitrotyrosine, and apoptosis in Helicobacter pylori gastritis: Effect of antibiotics and antioxidants. Cancer Res 56:3238-3243.
10. Meira LB, et al. (2008) DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice. J Clin Invest 118:2516-2525.
11. Nair J, et al. (2006) Increased etheno-DNA adducts in affected tissues of patients suffering from Crohn's disease, ulcerative colitis, and chronic pancreatitis. Antioxid Redox Signal 8:1003-1010. (Pubitemid 44036517)
12. Zhuang JC, Lin C, Lin D, Wogan GN (1998) Mutagenesis associated with nitric oxide production in macrophages. Proc Natl Acad Sci USA 95:8286-8291.
13. Sato Y, et al. (2006) IL-10 deficiency leads to somatic mutations in a model of IBD. Carcinogenesis 27:1068-1073.
14. Bartsch H, Nair J (2004) Oxidative stress and lipid peroxidation-derived DNA-lesions in inflammation driven carcinogenesis. Cancer Detect Prev 28:385-391.
15. Nair U, Bartsch H, Nair J (2007) Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: a review of published adduct types and levels in humans. Free Radic Biol Med 43:1109-1120. (Pubitemid 47374441)
16. Kang JM, Iovine NM, Blaser MJ (2006) A paradigm for direct stress-induced mutation in prokaryotes. FASEB J 20:2476-2485.
17. Crabtree JE, Ferrero RL, Kusters JG (2002) The mouse colonizing Helicobacter pylori strain SS1 may lack a functional cag pathogenicity island. Helicobacter 7:139-140, author reply 140-141.
18. Lee A, Mitchell H, O'Rourke J (2002) The mouse colonizing Helicobacter pylori strain SS1 may lack a functional cag pathogenicity island: Response. Helicobacter 7:140-141.
19. Miyazawa M, et al. (2003) Suppressed apoptosis in the inflamed gastric mucosa of Helicobacter pylori-colonized iNOS-knockout mice. Free Radic Biol Med 34:1621-1630.
20. Jang J, et al. (2003) Malgun (clear) cell change in Helicobacter pylori gastritis reflects epithelial genomic damage and repair. Am J Pathol 162:1203-1211. (Pubitemid 36350664)
21. Lee H, et al. (2000) "Malgun" (clear) cell change of gastric epithelium in chronic Helicobacter pylori gastritis. Pathol Res Pract 196:541-551.
22. Touati E, et al. (2003) Chronic Helicobacter pylori infections induce gastric mutations in mice. Gastroenterology 124:1408-1419.
23. Jenks PJ, Jeremy AH, Robinson PA, Walker MM, Crabtree JE (2003) Long-term infection with Helicobacter felis and inactivation of the tumour suppressor gene p53 cumulatively enhance the gastric mutation frequency in Big Blue transgenic mice. J Pathol 201:596-602.
24. Nohmi T, et al. (1996) A new transgenic mouse mutagenesis test system using Spi- and 6-thioguanine selections. Environ Mol Mutagen 28:465-470.
25. Ihrig M, Whary MT, Dangler CA, Fox JG (2005) Gastric helicobacter infection induces a Th2 phenotype but does not elevate serum cholesterol in mice lacking inducible nitric oxide synthase. Infect Immun 73:1664-1670. (Pubitemid 40470755)
26. Lee CW, et al. (2008) Helicobacter pylori eradication prevents progression of gastric cancer in hypergastrinemic INS-GAS mice. Cancer Res 68:3540-3548.
27. Fox JG, et al. (2000) Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy. Nat Med 6:536-542.
28. De Bont R, van Larebeke N (2004) Endogenous DNA damage in humans: A review of quantitative data. Mutagenesis 19:169-185.
29. Burney S, Caulfield JL, Niles JC, Wishnok JS, Tannenbaum SR (1999) The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat Res 424:37-49. (Pubitemid 29101606)
30. Kadlubar FF, et al. (1998) Comparison of DNA adduct levels associated with oxidative stress in human pancreas. Mutat Res 405:125-133.
31. Pandya GA, Moriya M (1996) 1, N6-ethenodeoxyadenosine, a DNA adduct highly mutagenic in mammalian cells. Biochemistry 35:11487-11492.
32. Ambs S, et al. (1999) Relationship between p53 mutations and inducible nitric oxide synthase expression in human colorectal cancer. J Natl Cancer Inst 91:86-88. (Pubitemid 29042448)
33. Kim MY, Wogan GN (2006) Mutagenesis of the supF gene of pSP189 replicating in AD293 cells cocultivated with activated macrophages: roles of nitric oxide and reactive oxygen species. Chem Res Toxicol 19:1483-1491.
34. Dedon PC, Plastaras JP, Rouzer CA, Marnett LJ (1998) Indirect mutagenesis by oxidative DNA damage: formation of the pyrimidopurinone adduct of deoxyguanosine by base propenal. Proc Natl Acad Sci USA 95:11113-11116.
35. Jackson AL, Loeb LA (2001) The contribution of endogenous sources of DNA damage to the multiple mutations in cancer. Mutat Res 477:7-21.
36. Wood ML, Esteve A, Morningstar ML, Kuziemko GM, Essigmann JM (1992) Genetic effects of oxidative DNA damage: comparative mutagenesis of 7,8-dihydro-8-oxoguanine and 7,8-dihydro-8-oxoadenine in Escherichia coli. Nucleic Acids Res 20:6023-6032.
37. Pang B, et al. (2007) Lipid peroxidation dominates the chemistry of DNA adduct formation in a mouse model of inflammation. Carcinogenesis 28:1807-1813.
38. Masumura K, et al. (2003) Low dose genotoxicity of 2-amino-3,8- dimethylimidazo[4,5-f]quinoxaline (MeIQx) in gpt delta transgenic mice. Mutat Res 541:91-102. (Pubitemid 38368662)
39. Masumura K, et al. (2000) Characterization of mutations induced by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine in the colon of gpt delta transgenic mouse: novel G:C deletions beside runs of identical bases. Carcinogenesis 21:2049-2056.
40. Balkwill F, Coussens LM (2004) Cancer: An inflammatory link. Nature 431:405-406.
41. Clevers H (2004) At the crossroads of inflammation and cancer. Cell 118:671-674.
42. Court M, Robinson PA, Dixon MF, Jeremy AH, Crabtree JE (2003) The effect of gender on Helicobacter felis-mediated gastritis, epithelial cell proliferation, and apoptosis in the mouse model. J Pathol 201:303-311.
43. Fox JG, et al. (2002) Germ-line p53-targeted disruption inhibits helicobacter-induced premalignant lesions and invasive gastric carcinoma through down-regulation of Th1 proinflammatory responses. Cancer Res 62:696-702.
44. Lee A, Fox JG, Otto G, Murphy J (1990) A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology 99:1315-1323. (Pubitemid 20381865)
45. Taylor NS, et al. (1995) Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fingerprinting. J Clin Microbiol 33:918-923.
46. Lemke LB, et al. (2009) Concurrent Helicobacter bilis infection in C57BL/6 mice attenuates proinflammatory H. pylori-induced gastric pathology. Infect Immun 77:2147-2158.
47. Crabtree JE, et al. (2004) Gastric mucosal cytokine and epithelial cell responses to Helicobacter pylori infection in Mongolian gerbils. J Pathol 202:197-207.
48. Fox JG, et al. (2003) Host and microbial constituents influence Helicobacter pylori-induced cancer in a murine model of hypergastrinemia. Gastroenterology 124:1879-1890.
49. Bamford KB, et al. (1998) Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 114:482-492.
50. Mohammadi M, Czinn S, Redline R, Nedrud J (1996) Helicobacter-specific cell-mediated immune responses display a predominant Th1 phenotype and promote a delayed-type hypersensitivity response in the stomachs of mice. J Immunol 156:4729-4738. (Pubitemid 26174457)
51. Sakagami T, et al. (1996) Atrophic gastric changes in both Helicobacter felis and Helicobacter pylori infected mice are host dependent and separate from antral gastritis. Gut 39:639-648.
52. Lee CW, et al. (2007) Wild-type and interleukin-10-deficient regulatory T cells reduce effector T-cell-mediated gastroduodenitis in Rag2-/- mice, but only wild-type regulatory T cells suppress Helicobacter pylori gastritis. Infect Immun 75:2699-2707.
53. Kao JY, et al. (2010) Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice. Gastroenterology 138:1046-1054.
54. Xu S, Cao X (2010) Interleukin-17 and its expanding biological functions. Cell Mol Immunol 7:164-174.
55. Rogers AB, et al. (2005) Helicobacter pylori but not high salt induces gastric intraepithelial neoplasia in B6129 mice. Cancer Res 65:10709-10715.
56. Masumura K, et al. (1999) Spectra of gpt mutations in ethylnitrosourea-treated and untreated transgenic mice. Environ Mol Mutagen 34:1-8. (Pubitemid 29420232)
57. Nüesch J, Schümperli D (1984) Structural and functional organization of the gpt gene region of Escherichia coli. Gene 32:243-249.
58. Kim MY, Dong M, Dedon PC, Wogan GN (2005) Effects of peroxynitrite dose and dose rate on DNA damage and mutation in the supF shuttle vector. Chem Res Toxicol 18:76-86.