Helicobacter pylori, inflammation, oxidative damage and gastric cancer: A morphological, biological and molecular pathway

European Journal of Cancer Prevention

Volumn 17, Issue 3, 2008, Pages 195-200

  Farinati, Fabio ^a,b   Cardin, Romilda ^a   Cassaro, Mauro ^a   Bortolami, Marina ^a   Nitti, Donato ^a   Tieppo, Chiara ^a   Zaninotto, Giovanni ^a   Rugge, Massimo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY HOSPITAL OF PADOVA   (Italy)

Author keywords

Gastric cancer; Helicobacter pylori; Oxidative DNA damage; Preneoplastic lesions

Indexed keywords

CELL ADHESION MOLECULE; DNA; GROWTH FACTOR; REACTIVE OXYGEN METABOLITE;

CANCER GROWTH; CARCINOGENESIS; CARCINOMA IN SITU; CELL CYCLE; CELL DIFFERENTIATION; DNA DAMAGE; DNA REPAIR; DYSPLASIA; EPIGENETICS; GASTROINTESTINAL ENDOSCOPY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; INFLAMMATION; ONCOGENE; OXIDATIVE STRESS; PRECANCER; PRIORITY JOURNAL; REVIEW; STOMACH ADENOCARCINOMA; STOMACH CANCER; STOMACH CARCINOMA; TUMOR SUPPRESSOR GENE;

ANIMALS; DNA DAMAGE; GASTRITIS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS;

EID: 42249100307     PISSN: 09598278     EISSN: None     Source Type: Journal    
DOI: 10.1097/CEJ.0b013e3282f0bff5     Document Type: Review

References (73)

1. Bai YQ, Yamamoto H, Akiyama Y, Tanaka H, Takizawa T, Koike M, et al. (2002). Ectopic expression of homeodomain protein CDX2 in intestinal metaplasia and carcinomas of the stomach. Cancer Lett 176:47-55.
2. Baik SC, Youn HS, Chung MH, Lee WK, Cho MJ, Ko GH, et al. (1996). Increased oxidative DNA damage in Helicobacter pylori infected human gastric mucosa. Cancer Res 56:1279-1282.
3. Becker KF, Atkinson MJ, Reich U, Becker I, Nekarda H, Siewert JR, Hofler H (1994). E-cadherin gene mutations provide clues to diffuse type gastric carcinomas. Cancer Res 54:3845-3852.
4. Berglund G, Hill MJ, Caygill CP, Farinati F, Giacosa A, De Koster E, et al. (1997). Consensus statement on diet and gastric cancer. Gastric Cancer Panel. Eur J Cancer Prev 6:404-407.
5. Chong JM, Fukayama M, Hayashi Y, Takizawa T, Koike M, Konishi M, et al. (1994). Microsatellite instability in the progression of gastric carcinoma. Cancer Res 54:4595-4597.
6. Conchillo JM, Houben G, de Bruine A, Stockbrugger R (2001). Is type III intestinal metaplsia an obligatory precancerous lesion in intestinal type gastric carcinoma? Eur J Cancer Prev 10:307-312.
7. Correa P (1988). A human model of gastric carcinogenesis. Cancer Res 48:3554-3560.
8. Correa P (1992). Human gastric carcinogenesis: a multistep and multifactorial process. First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 52:6735-6740.
9. Correa P (2004). The biological model of gastric carcinogenesis. IARC Sci Publ 157:301-310.
10. Correa P, Shiao YH (1994). Phenotypic and genotypic events in gastric carcinogenesis. Cancer Res 54:1941s-1943s.
11. Correa P, Fontham ET, Bravo JC, Bravo LE, Ruiz B, Zarama G, et al. (2000). Chemoprevention of gastric dysplasia: randomized trial of antioxidant supplements and anti-helicobacter pylori therapy. J Natl Cancer Inst 92: 1881-1888.
12. Danese S, Cremonini F, Armuzzi A, Candelli M, Papa A, Ojetti V, et al. (2001). Helicobacter pylori CagA-positive strains affect oxygen free radicals generation by gastric mucosa. Scand J Gastroenterol 36:247-250.
13. Dundon WG, de Bernard M, Montecucco C (2001). Virulence factors of Helicobacter pylori. Int J Med Microbiol 290:647-658.
14. ECP-IM Intervention Study Group (2001). ECP intestinal metaplasia intervention study. Eur J Cancer Prev 10:105.
15. El-Omar EM, Rabkin CS, Gammon MD, Vaughan T, Risch H, Schoenberg J, et al. (2003). Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 124: 1193-1201.
16. El-Rifai W, Powell SM (2002). Molecular biology of gastric cancer. Semin Radiat Oncol 12:128-140.
17. Eurogast Study Group (1993). An international association between Helicobacter pylori infection and gastric cancer. Lancet 341:1359-1362.
18. Farinati F, Cardin R, Della Libera G, Rugge M, Herszenyi L, Di Mario F, et al. (1995). Determinants for the development of chronic atrophic gastritis and intestinal metaplasma in the stomach. Eur J Cancer Prev 4:181-186.
19. Farinati F, Della Libera G, Cardin R, Molari A, Plebani M, Rugge M, et al. (1996). Gastric antioxidant, nitrites, and mucosal lipoperoxidation in chronic gastritis and Helicobacter pylori infection. J Clin Gastroenterol 22:275-281.
20. Farinati F, Cardin R, Degan P, Rugge M, Di Mario F, Bonvicini P, Naccarato R (1998a). Oxidative DNA damage accumulation in gastric carcinogenesis. Gut 42:351-356.
21. Farinati F, Foschia F, Di Mario F, Cassaro M, Rugge M (1998b). H. pylori eradication and gastric precancerous lesions. Gastroenterology 115: 512-514.
22. Farinati F, Cardin R, Russo VM, Busatto G, Franco M, Rugge M (2003). Helicobacter pylori CagA status, mucosal oxidative damage and gastritis phenotype: a potential pathway to cancer? Helicobacter 8:227-234.
23. Farinati F, Cardin R, Russo VM, Busatto G, Franco M, Falda A, et al. (2004). Differential effects of Helicobacter pylori eradication on oxidative DNA damage at the gastroesophageal junction and at the gastric antrum. Cancer Epidemiol Biomarkers Prev 13:1722-1728.
24. Farinati F, Cardin R, Bortolami M, Nitti D, Basso D, de Bernard M, et al. (2008). Oxidative DNA damage in gastric cancer: CagA status and OGG1 gene polymorphism. Int J Cancer (in press).
25. Fenoglio-Preiser C, Carneiro F, Correa P, Guilford P, Lambert R, Megraud F, et al. (2000). Gastric carcinoma. In: Hamilton SR, Aaltonen LA, editors. Pathology & Genetics, Tumors of the Digestive System. Lyon: IARC Press. pp. 39-52.
26. Fuccio L, Zagari RM, Minardi ME, Bazzoli F (2007). Systematic review: Helicobacter pylori eradication for the prevention of gastric cancer. Aliment Pharmacol Ther 25:133-141.
27. Graham DY, Yamaoka Y (2000). Disease-specific Helicobacter pylori virulence factors: the unfulfilled promise. Helicobacter 5:S27-S31.
28. Hatakeyama M (2006). The role of Helicobacter pylori CagA in gastric carcinogenesis. Int J Hematol 84:301-308.
29. Higashikawa K, Yokozaki H, Ue T, Taniyama K, Ishikawa T, Tarin D, Tahara E (1996). Evaluation of CD44 transcription variants in human digestive tract carcinomas and normal tissues. Int J Cancer 66:11-17.
30. Hironaka K, Factor VM, Calvisi DF, Conner EA, Thorgeirsson SS (2003). Dysregulation of DNA repair pathways in a transforming growth factor alpha/c-myc transgenic mouse model of accelerated hepatocarcinogenesis. Lab Invest 83:643-654.
31. Isogaki J, Shinmura K, Yin W, Arai T, Koda K, Kimura T, et al. (1999). Microsatellite instability and K-ras mutations in gastric adenomas, with reference to associated gastric cancers. Cancer Detect Prev 23:204-214.
32. Kim H (2005). Oxidative stress in Helicobacter pylori-induced gastric cell injury. Inflammopharmacology 13:63-74.
33. Kim SY, Lee YC, Kim HK, Blaser MJ (2006). Helicobacter pylori CagA transfection of gastric epithelial cells induces interleukin-8. Cell Microbiol 8:97-106.
34. Kohno T, Shinmura K, Tosaka M, Tani M, Kim SR, Sugimura H, et al. (1998). Genetic polymorphisms and alternative splicing of the hOGG1 gene, that is involved in the repair of 8-hydroxyguanine in damaged DNA. Oncogene 16:3219-3225.
35. Kuchino Y, Mori F, Kasai H, Inoue H, Iwai S, Miura K, et al. (1987). Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature 327:77-79.
36. Lee JH, Abraham SC, Kim HS, Nam JH, Choi C, Lee MC, et al. (2002). Inverse relationship between APC gene mutation in gastric adenomas and development of adenocarcinoma. Am J Pathol 161:611-618.
37. Lefebvre O, Chenard MP, Masson R, Linares J, Dierich A, LeMeur M, et al. (1996). Gastric mucosa abnormalities and tumorigenesis in mice lacking the pS2 trefoil protein. Science 274:259-262.
38. Liu TZ, Lee KT, Chern CL, Cheng JT, Stern A, Tsai LY (2001). Free radical-triggered hepatic injury of experimental obstructive jaundice of rats involves overproduction of proinflammatory cytokines and enhanced activation of nuclear factor kappaB. Ann Clin Lab Sci 31:383-390.
39. Lu H, Yamaoka Y, Graham DY (2005). Helicobacter pylori virulence factors: facts and fantasies. Curr Opin Gastroenterol 21:653-659.
40. Montecucco C, de Bernard M (2003). Molecular and cellular mechanisms of action of the vacuolating cytotoxin (VacA) and neutrophil-activating protein (HP-NAP) virulence factors of Helicobacter pylori. Microbes Infect 5: 715-721.
41. Morson BC, Sobin LH, Grundmann E, Johansen A, Nagayo T, Serck-Hanssen A (1980). Precancerous conditions and epithelial dysplasia in the stomach. J Clin Pathol 33:711-721.
42. Moss SF, Sordillo EM, Abdalla AM, Makarov V, Hanzely Z, Perez-Perez GI, et al. (2001). Increased gastric epithelial cell apoptosis associated with colonization with cagA+ Helicobacter pylori strains. Cancer Res 61: 1406-1411.
43. Nakabeppu Y, Sakumi K, Sakamoto K, Tsuchimoto D, Tsuzuki T, Nakatsu Y (2006). Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids. Biol Chem 387:373-379.
44. Nogueira C, Figueiredo C, Carneiro F, Gomes AT, Barreira R, Figueira P, et al. (2001). Helicobacter pylori genotypes may determine gastric histopathology. Am J Pathol 158:647-654.
45. Papa A, Danese S, Sgambato A, Ardito R, Zannoni G, Rinelli A, et al. (2002). Role of Helicobacter pylori CagA+ infection in determining oxidative DNA damage in gastric mucosa. Scand J Gastroenterol 37:409-413.
46. Parsonnet J, Friedmann GD, Vandersteen DP, Chang Y, Vogelman J, Orentreich N, Sibley RK (1991). Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 325:1127-1131.
47. Peek RM Jr. (2002). Helicobacter pylori strain-specific modulation of gastric mucosal cellular turnover: implications for carcinogenesis. J Gastroenterol 37 (Suppl 13):10-16.
48. Peek RM Jr, Blaser MJ, Mays DJ, Forsyth MH, Cover TL, Song SY, et al. (1999). Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res 59:6124-6131.
49. Pignatelli B, Bancel B, Plummer M, Toyokuni S, Patricot L-M, Ohshima H (2001). Helicobacter pylori eradication attenuates oxidative stress in human gastric mucosa. Am J Gastroenterol 96:1758-1766.
50. Rudi J, Kolb C, Maiwald M, Zuna I, von Herbay A, Galle PR, Stremmel W (1997). Serum antibodies against Helicobacter pylori proteins VacA and CagA are associated with increased risk for gastric adenocarcinoma. Dig Dis Sci 42:1652-1659.
51. Rugge M, Farinati F, Baffa R, Sonego F, Di Mario F, Leandro G, Valiante F (1994). Gastric epithelial dysplasia in the natural history of gastric cancer: a multicenter prospective follow-up study. Interdisciplinary group on gastric epithelial dysplasia. Gastroenterology 107:1288-1296.
52. Rugge M, Busatto G, Cassaro M, Shiao YH, Russo V, Leandro G, et al. (1999). Patients younger than 40 years with gastric carcinoma. Helicobacter pylori genotype and associated gastritis phenotype. Cancer 85: 2506-2511.
53. Rugge M, Correa P, Dixon MF, Hattori T, Leandro G, Lewin K, et al. (2000). Gastric dysplasia: the Padova international classification. Am J Surg Pathol 24:167-176.
54. Rugge M, Cassaro M, Di Mario F, Leo G, Leandro G, Russo VM, et al. (2003a). Interdisciplinary Group on Gastric Epithelial Dysplasia (IGGED). The long-term outcome of gastric non-invasive neoplasia. Gut 52:1111-1116.
55. Rugge M, Cassaro M, Pennelli G, Russo VM, Di Mario F, Farinati F (2003b). Pathology and cost effectiveness of endoscopic surveillance for premalignant gastric lesions. Gut 52:453-454.
56. Rugge M, Russo VM, Guido M (2003c). Review article: what have we learnt from gastric biopsy? Aliment Pharmacol Ther 17:68-74.
57. Rugge M, Ingravallo G, Farinati F, Russo VM, Zaninotto G, Alvisi V (2004). CDX2 Homeotic gene expression in gastric non-invasive neoplasia. Am J Surg Pathol 28:834-835.
58. Rugge M, Nitti D, Farinati F, Di Mario F, Genta RM (2005). Non-invasive neoplasia of the stomach. Eur J Gastroenterol Hepatol 17:1191-1196.
59. Sakurai S, Sano T, Nakajima T (1995). Clinicopathological and molecular biological studies of gastric adenomas with special reference to p53 abnormality. Pathol Int 45:51-57.
60. Semba S, Yokozaki H, Yamamoto S, Yasui W, Tahara E (1996). Microsatellite instability in precancerous lesions and adenocarcinomas of the stomach. Cancer 77:1620-1627.
61. Seruca R, Santos NR, David L, Constancia M, Barroca H, Carneiro F, et al. (1995). Sporadic gastric carcinomas with microsatellite instability display a particular clinicopathologic profile. Int J Cancer 64:32-36.
62. Shimoyama T, Fukuda S, Tanaka M, Mikami T, Saito Y, Munakata A (1997). High prevalence of the CagA-positive Helicobacter pylori strains in Japanese asymptomatic patients and gastric cancer patients. Scand J Gastroenterol 32:465-468.
63. Siomek A, Rytarowska A, Szaflarska-Poplawska A, Gackowski D, Rozalski R, Dziaman T, et al. (2006). Helicobacter pylori infection is associated with oxidatively damaged DNA in human leukocytes and decreased level of urinary 8-oxo-7,8-dihydroguanine. Carcinogenesis 27:405-408.
64. Tahara E, Yokozaki H, yasui W (1999). Stomach Genetic and epigenetic alterations of preneoplastic and neoplastic lesions. In: Srivastava S, Henson DE, Gazdar A, editors. Molecular pathology of early cancer. Amsterdam Berlin, Oxford, Tokyo, Washington, DC: AIOS-press Ohmsha.
65. Tamura G, Maesawa C, Suzuki Y, Tamada H, Satoh M, Ogasawara S, et al. (1994). Mutations of the APC gene occur during early stages of gastric adenoma development. Cancer Res 54:1149-1151.
66. Thorgeirsson SS, Factor VM, Snyderwine EG (2000). Transgenic mouse models in carcinogenesis research and testing. Toxicol Lett 112-113:553-555.
67. Tohdo H, Yokozaki H, Haruma K, Kajiyama G, Tahara E (1993). p53 gene mutations in gastric adenomas. Virchows Arch B Cell Pathol Incl Mol Pathol 63:191-195.
68. Toyokuni S (2006). Novel aspects of oxidative stress-associated carcinogenesis. Antioxidants & Redox Signaling 8:1373-1377.
69. Vermeulen K, Berneman ZN, Van Bockstaele DR (2003). Cell cycle and apoptosis. Cell Prolif 36:165-175.
70. Wang G, Conover RC, Olczak AA, Alamari P, Johnson MX, Maier RJ (2005). Oxidative stress defense mechanisms to counter iron-promoter DNA damage in Helicobacter pylori. Free Radic Res 39:1183-1191.
71. Xia HH, Kalantar JS, Talley NJ, Wyatt JM, Adams S, Chueng K, Mitchell HM (2000). Antral-type mucosa in the gastric incisura, body, and fundus (antralization): a link between Helicobacter pylori infection and intestinal metaplasia? Am J Gastroenterol 95:114-121.
72. You W, Brown L, Zhang L, Li J, Jin M, Chang Y, et al. (2006). Randomized double-blind factorial trial of three treatments to reduce the prevalence of precancerous gastric lesions. J Natl Cancer Inst 98:974-983.
73. Zambon CF, Basso D, Navaglia F, Falda A, Belluco C, Fogar P, Greco E, et al. (2004). Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 126:382-384.