Oxidative stress and DNA damage in human gastric carcinoma: 8-Oxo-7'8-dihydro-2'-deoxyguanosine (8-oxo-dG) as a possible tumor marker

International Journal of Molecular Sciences

Volumn 14, Issue 2, 2013, Pages 3467-3486

  Borrego, Silvia ^a,b   Vazquez, Antonio ^a   Dasí, Francisco ^c   Cerdá, Concha ^a,b   Iradi, Antonio ^d   Tormos, Carmen ^d   Sánchez, Julia M ^d   Bagán, Leticia ^d   Boix, Javier ^d   Zaragoza, Cristóbal ^a   Camps, Jordi ^e   Sáez, Guillermo ^a,b,d  

^a HOSPITAL GENERAL UNIVERSITARIO DE VALENCIA   (Spain)

^b Sociedad Espanola de Bioquimica Clinica y Patologia Molecular   (Spain)

^c Biomedical Research Institute Hospital Clinic de Valencia INCLIVA   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

^e HOSPITAL UNIVERSITARI SANT JOAN DE REUS   (Spain)

Author keywords

8 oxo dG; DNA repair enzymes; Gastric cancer; Oxidative stress; Tumor marker

Indexed keywords

8 OXO 7'8 DIHYDRO 2' DEOXYGUANOSINE; DNA GLYCOSYLASE MUTY; GLUTATHIONE; HOGG1 PROTEIN; MALONALDEHYDE; MTH1 PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RAD51 PROTEIN; TUMOR MARKER; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CANCER PATIENT; CANCER TISSUE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; FEMALE; GASTRECTOMY; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MUCOSA; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; STOMACH CARCINOMA; URINE;

EID: 84875093460     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14023467     Document Type: Article

References (80)

1. Halliwell, B.; Gutteridge, J.M.C. Free Radicals in Biology and Medicine; Oxford University Press: Oxford, UK, 2007.
2. Sies, H. Oxidative Stress; Academic Press Inc.: Orlando, FL, USA, 1985.
3. Cooke, M.S.; Evans, M.D.; Dizdaroglu, M.; Lunec, J. Oxidative DNA damage: Mechanisms, mutation and disease. FASEB J. 2003, 17, 1195-1214.
4. Gackowski, D.; Speina, E.; Zielinska, M.; Lowalewski, J.; Rozalski, R.; Siomek, A.; Paciorek, T.; Tudek, B.; Olinski, R. Products of oxidative DNA damage and repair as possible biomarkers of susceptibility to lung cancer. Cancer Res. 2003, 63, 4899-4902.
5. Andreoli, R.; Mutti, A.; Goldoni, M.; Manini, P.; Apostoli, P.; de Palma, G. Reference ranges of urinary biomarkers of oxidized guanine in (2-deoxy) ribonucleotides and nucleic acids. Free Radic. Biol. Med. 2011, 50, 254-261.
6. Blumberg, J. Use of biomarkers of oxidative stress in research studies. J. Nutr. 2004, 134, S3188-S3189.
7. Schisterman, E.F.; Faraggi, D.; Browne, R.; Freudenheim, J.; Dron, J.; Muti, P.; Armastrong, D.; Reiser, B.; Trevisan, M. Minimal and best linear combination of oxidative stress and antioxidant biomarkers to discriminate cardiovascular diseases. Nutri. Metab. Cardiovasc. Dis. 2002, 12, 259-266.
8. Gros, L.; Saparbaev, M.K.; Laval, J. Enzymology of the repair of free radical-induced DNA damage. Oncogene 2002, 21, 8905-8925.
9. Paz-Elizur, T.; Sevlya, Z.; Leitner-Dagan, Y.; Elinger, D.; Roisman, L.; Livneh Z. DNA repair of oxidative DNA damage in human carcinogenesis. Cancer Lett. 2008, 266, 60-72.
10. Faucher, F.; Doublié, S.; Jia, Z. 8-oxoguanine DNA glycosylases: One lesion, three subfamilies. Int. J. Mol. Sci. 2012, 13, 6711-6729.
11. Mo, J.-Y.; Maki, H.; Sekiguchi, M. Hydrolytic elimination of a mutagenic nucleotide, 8-oxo-dGTP, by human 18-kilodalton protein: Sanitization of nucleotide pool. Proc. Natl. Acad. Sci. USA 1992, 89, 11021-11025.
12. Ohtsube, T.; Nishioka, Y.; Imaiso, Y.; Iwai, S.; Shimokawa, H.; Oda, H.; Tujiwara, T.; Nakabeppu, Y. Identification of human MutY homolog (hMYH) as a repair enzyme for 2-hydroxyadenine in DNA and detection of multiple forms of hMYH located in nuclei and mitochondria. Nucleic Acids Res. 2000, 28, 1355-1364.
13. Thacker, J. The RAD51 family, genetic instability and cancer. Cancer Lett. 2005, 219, 125-135.
14. Kuchino, Y.; Mori, F.; Kasai, H.; Inoue, H.; Iwai, S.; Miura, K.; Ohtsuka, E.; Nishimura, S. Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature 1987, 327, 77-79.
15. Shibutani, S.; Takeshita, M.; Grollman, A.P. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxo-dG. Nature 1991, 349, 431-434.
16. Floyd, R.A. The role of 8-hydroxyguanine in carcinogenesis. Carcinogenesis 1990, 11, 1447-1450.
17. Due, M.-Q.; Carmichael, P.L.; Philips, D.H. Induction of activating mutation in the human C-Ha-ras-1 protooncogene by oxygen free radicals. Mol. Carcinog. 1994, 11, 170-175.
18. Hussain, F.; Aguilar, F.; Cerutti, P. Oxy-radicals induced mutagenesis of hotspot codons 248 and 249 of the human p53 gene. Oncogen 1994, 9, 2277-2281.
19. Oliva, M.R.; Ripoll, F.; Muñiz, P.; Iradi, A.; Trullenque, R.; Valls, V.; Drehmer, E.; Sáez, G.T. Genetic alterations and oxidative metabolisms in sporadic colorectal tumors from a Spanish community. Molecular Carcinog. 1997, 18, 232-243.
20. Oltra, A.M.; Carbonell, F.; Tormos, C.; Iradi, A.; Sáez, G.T. Antioxidant enzyme activities and the production of MDA and 8-oxo-dG in chronic lymphocytic leukemia. Free Radic. Biol. Med. 2001, 30, 1286-1292.
21. Sánchez, M.; Torres, J.V.; Tormos, C.; Iradi, A.; Muñiz, P.; Espinosa, O.; Salvador, A.; Rodriguez-Delgado, J.; Fandos, M.; Sáez, G.T. Impairment of antioxidant enzyme, lipid peroxidation and 8-oxo-2'-deoxyguanosine in advanced epithelial ovarian carcinoma from a Spanish community. Cancer Lett. 2006, 233, 28-35.
22. Collado, R.; Oliver, I.; Tormos, C.; Egea, M.; Miguel, A.; Cerdá, C.; Ivars, D.; Borrego, S.; Carbonell, F.; Sáez, G.T. Early ROS-mediated DNA damage and oxidative stress biomarkers in Monoclonal B Lymphocytosis. Cancer Lett. 2012, 317, 144-149.
23. Kuo, H.W.; Chou, S.Y.; Hu, T.W.; Wu, F.; Chen, D.J. Urinary 8-hydroxy-2'-deoxyguanosine (8-OHdG) and genetic polymorphisms in breast cancer patients. Mutation Res. 2007, 631, 62-68.
24. Räsänen, J.V.; Sihvo, E.I.; Ahotupa, M.O.; Farkkila, M.A.; Salo, J.A. The expression of 8-hydroxydeoxyguanosine in oesophageal tissues and tumors. Eur. J. Surg. Oncol. 2007, 33, 1164-1168.
25. Chen, J.H.; Yakes, F.M.; Srivastava, D.K.; Singhal, R.K.; Sobol, R.W.; Horton, J.K.; van Houten, B.; Wilson, S.H. Up-regulation of base excision repair correlates with enhanced protection against DNA damaging agent in mouse cell lines. Nucleic Acid Res.1998, 26, 2001-2007.
26. Tudek, B. Base excision repair modulation as a risk factor for human cancers. Mol. Aspects Med. 2007, 28, 258-275.
27. Jemal, A.; Siegal, R.; Ward, E.; Hao, Y.; Xu, J.; Thun, M.J. Cancer statistics 2009. CA Cancer J. Clin. 2009, 59, 225-249.
28. Loft, S.; Poulsen, H.E. Cancer risk and oxidative DNA damage in man. J. Mol. Med. 1996, 74, 297-312.
29. Ni, J.; Mei, M.; Sun, J. Oxidative DNA damage and repair in chronic gastritis and gastric cancer. Hepatogastroenterology. 2012, 59, 671-675.
30. Liu, R.; Yin, L.H.; Pu, Y.P. Reduced expression of human DNA genes in esophageal squamous-cell carcinoma in China. J. Toxicol. Environ. Health A 2007, 70, 956-963.
31. Poplawski, T.; Arabski, M.; Kozirowska, D.; Blasinska-Morawiec, M.; Morawiec, Z.; Morawiec-Bajda, A.; Klupińska, G.; Jeziorski, A.; Chojnacki, J.; Blasiak, J. DNA damage and repair in gastric cancer: A correlation with the hOGG1 and RAD51 genes polymorphisms. Mutat. Res. 2006, 601, 83-91.
32. Simic, M.G. DNA markers of oxidative processes in vivo. Relevance to carcinogenesis and anticarcinogenesis. Cancer Res. 1993, 54, S1918-S1923.
33. Kaynar, H.M.; Meral, M.; Turhan, H.; Keles, M.; Celik, G.; Akcay, F. Glutathione peroxidase, glutathione-S-transferase, catalase, xanthine oxidase, Cu-Zn superoxide dismutase activities, total glutathione, nitric oxide and malondialdehyde levels in erythrocytes of patients with small cell and non-small cell lung cancer. Cancer Lett. 2005, 227, 133-139.
34. Ferraris, A.M.; Rolfo, M.; Mangerini, R.; Gaetani, G.F. Increased glutathione in chronic lymphocytic leukemia lymphocytes. Am. J. Hematol. 1994, 47, 237-238.
35. Blume, K.G.; Paniker, N.V.; Beutler, E. Enzymes of glutathione synthesis in patients with myeloproliferative disorders. Clin. Chim. Acta 1973, 45, 281-285.
36. Ahmad, S.; Okine, L.; Le, B.; Najarian, P.; Vistica, D.T. Elevation of glutathione in phenylalanine mustard-resistant murine L1210 leukemia cells. J. Biol. Chem. 1987, 262, 15048-15053.
37. Toyokuni, S.; Okamoto, D.; Yodoy, J.; Hiai, H. Persistent oxidative stress in cancer. FEBS Lett. 1995, 358, 1-3.
38. Sun, Y. Free radicals, antioxidant enzymes and carcinogenesis. Free Radic. Biol. Med. 1990, 8, 583-599.
39. Szatrowski, T.P.; Nathan, C.F. Production of large amounts of hydrogen peroxide in human tumor cells. Cancer Res. 1991, 51, 794-798.
40. Kryston, T.B.; Georgiev, A.B.; Pissis, P.; Georgakilas, A.G. Role of oxidative stress and DNA damage in human carcinogenesis. Mutat. Res. 2011, 711, 193-201.
41. Evans, M.D.; Dizdaroglu, M.; Cooke, M.S. Oxidative DNA damage and disease: Induction, repair and significance. Mutat. Res. 2004, 567, 1-61.
42. Kondo, S.; Toyokuni, S.; Tanaka, T.; Hiai, H.; Onodera, H.; Kasai, H.; Imamura, M. Overexpression of the hOGG1 and high 8-hydroxy-2'-deoxy guanosine (8-OHdG) lyase activity in human colorectal carcinoma: Regulation mechanism of the 8-OHdG level in DNA. Clin. Cancer Res.2000, 6, 1394-1400.
43. Liguori, M.; Solinas, G.; Germano, G.; Mantovani, A.; Allavena, P. Tumor-associated macrophages as incessant builders and destroyers of the cancer stroma. Cancers 2011, 3, 3740-3761.
44. Reuter, S.; Gupta, S.C.; Chaturvedi, M.M.; Aggarwal, B.B. Oxidative stress, inflammation and cancer: How are they linked? Free Radic. Biol. Med. 2010, 49, 1603-1616.
45. Mantovani, A.; Allavena, P.; Sica, A.; Balkwill, F. Cancer-related inflammation. Nature 2004, 454, 436-444.
46. Redon, C.; Dickey, J.S.; Nakamura, A.; Kareva, I.; Naf, D.; Nowsheen, S.; Kryston, T.B.; Bonner, W.M.; Georgakilas, A.G.; Sedenikova, O.A. Tumors induce complex DNA damage in distant proliferative tissues in vivo. Proc. Natl. Acad. Sci. USA 2010, 107, 17992-17997.
47. Cooke, M.S.; Olinski, R.; Loft, S. Measurements and meaning of oxidatively modified DNA lesions in urine. Cancer Epidemiol. Biomarkers Prev. 2008, 17, 3-14.
48. Valavanidis, A.; Vlachogianni, T.; Flotakis C. 8-hydroxy-2'-deoxyguanosine (8-OHdG): A critical biomarker of oxidative stress and carcinogenesis. J. Environ Sci. Health. 2009, 27, 120-139.
49. Hoeijmakers, J.H. Genome maintenance mechanisms for preventing cancer. Nature 2001, 411, 366-374.
50. Bruner, S.D.; Norman, P.D.G.; Verdine, Y.L. Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature 2000, 403, 859-866.
51. Okamoto, K.; Toyokuni, S.; Kim, W.J.; Ogava, O.; Kakehi, Y.; Arao, S.; Hiai, H.; Yoshida, O. Overexpression of human mutT homologue gene messenger RNA in renal-cell carcinoma: Evidence of persistent oxidative stress in cancer. Int. J. Cancer 1995, 65, 437-441.
52. Kenny, C.H.; Pass, H.I.; Mitchell, J.B. Expression of human MutT homologue (hMTH1) protein in primary non-small-cell lung carcinomas and histologically normal surrounding tissue. Free Radic. Biol. Med. 2003, 34, 1447-1457.
53. Speina, E.; Arczewska, K.D.; Gackowski, D.; Zielinska, M.; Siomek, A.; Kawalewski, J.; Olinski, R.; Tudek, B.; Jusmierek, J.T. Contribution of hMTH1 to the maintenance of 8-oxoguanine levels in lung DNA of non-small-cell lung cancer patients. J. Natl. Cancer Inst. 2005, 97, 384-395.
54. Jewell, R.; Conway, C.; Mitra, A.; Randerson-Moor, J.; Lobo, S.; Nsengimana, J.; Harland, M.; Marples, M.; Edward, S.; Cook, M.; et al. Patterns of expression of DNA repair genes and relapse from melanoma. Clin. Cancer Res. 2010, 16, 5211-5221.
55. Mitra, A.; Jameson, C.; Barbachano, Y.; Sanchez, L.; Kote-Jarai, Z.; Peock, S.; Sodha, N.; Bancroft, E.; Fletcher, A.; Cooper, C.; et al. IMPACT Steering Committee and IMPACT and EMBRACE Collaborators, Eeles R, Foster CS. Overexpression of RAD51 occurs in aggressive prostatic cancer. Histopathology 2009, 55, 696-704.
56. Cooke, M.S.; Evans, M.D.; Dove, R.; Rozalski, R.; Gackowski, D.; Lunec, J.; Olinski, R. DNA repair is responsible for the presence of oxidatively damaged DNA lesions in urine. Mutat. Res. 2005, 574, 58-66.
57. Svoboda, P.; Kasai, H. Simultaneous HPLC analysis of 8-hydroy-deoxyguanosine and 7-methylguanine in urine from humans and rodents. Anal. Biochem. 2004, 334, 239-250.
58. Bogdanov, M.B.; Beal, M.F.; McCabe, D.R.; Griffin, R.M.; Matson, W.R. A carbon column-based liquid chromatography electrochemical approach to routine 8-hydroxy-2'-dexyguanosine measurements in urine and other biologic matrices: A one-year evaluation of the methods. Free Radic. Biol. Med. 1999, 27, 646-666.
59. Collins, A.R.; Gedik, C.; Wood, S.; White, A.; Dubois, J.; Duez, P.; Rees, J.-F.; Legal, R.; Degand, L.; Loft, S.; et al. Inter-laboratory validation of procedures for measuring 8-oxo-7,8-dihydroguanine/8-oxo-7,8-dhydro-2'-deoxyguanosine in DNA. Free Radic. Res. 2002, 36, 239-245.
60. Evans, M.D.; Olinski, R.; Loft, S.; Cooke, M.S. Toward consensus in the analysis of urinary 8-oxo-7,8-2'-deoxyguanosine as a noninvasive biomarker of oxidative stress. FASEB J. 2009, 24, 1249-1260.
61. Loft, S.; Pousen, H.E.; Vistisens, K.; Knudsen, L.E. Increased urinary excretion of 8-oxo-2'-deoxyguanosine, a biomarker of oxidative DNA damage, in urban bus drivers. Mutat. Res. 1999, 441, 11-19.
62. Lenger, C.; Schöh, G.; Topp, H. A high-performance liquid chromatographic method for the determination of 8-oxo-7,8-2'-deoxyguanosine in urine from man and rat. Anal. Biochem. 2000, 287, 65-72.
63. Weiman, A.; Belling, D.; Poulsen, H. Quantification of 8-oxo-guanine and guanosine as the nucleobase, nucleoside and deoxynucleoside forms in human urine by high-performance liquid chromatography-electrospray mas spectromety. Nucleic Acid. Res. 2002, 304, 4-8.
64. Foksinski, M.; Gackowski, D.; Rozalski, R.; Olinski, R. Cellular level of 8-oxo-2'-deoxyguanosine in DNA does not correlate with urinary excretion of the modified base/nucleoside. Acta Biochem. Pol. 2003, 50, 549-553.
65. Lunec, J.; Holloway, K.A.; Cooke, M.S.; Faux, S.; Griffiths, H.R.; Evans, M.D. Urinary 8-oxo-2'-deoxyguanosine: Redox regulation of DNA repair in vivo? Free Radic. Biol. Med. 2002, 33, 875-885.
66. Hayakwa, H.; Taketomi, A.; Sakimi, K.; Kuwano, M.; Sekiguchi, M. Generation and elimination of 8-oxo-7,8-dihidro-2'-deoxyguanosine 5'-triphophate, a mutagenic substrate for DNA synthesis, in human cells. Biochemistry 1995, 34, 89-95.
67. Cooke, M.S.; Henderson, P.T.; Evans, M.D. Sources of extracellular, oxidatively-modified DNA lesions: Implications for their measurement in urine. J. Clin. Nutr. 2009, 45, 255-270.
68. Carpelan-Holmström, M.; Louhimo, J.; Stenman, U.H.; Alfthan, H.; Haglund, C. CEA, CA19-9 and CA72-4 improve the diagnostic accuracy in gastrointestinal cancers. Anticancer Res. 2002, 22, 2311-2316.
69. Jass, J.R.; Sobin, L.H. Histological Typing of Intestinal Tumors (International Histological Classification of Tumors, WHO); Springer Verlag New York, Inc.: New York, NY, USA, 1989.
70. Ahn, S.; Lee, H.J.; Hahn, S.; Kim, W.H.; Lee, K.U.; Sano, T.; Edge, S.B.; Yang, H.K. Evaluation of the seventh American Joint Committee on Cancer/International Union Against Cancer Classification of gastric adenocarcinoma in comparison with the sixth classification. Cancer 2010, 116, 5592-5598.
71. Boyum, A. Isolation of mononuclear cells and granulocytes from human blood. Scan. J. Clin. Lab. Invest. 1968, 21, 77-89.
72. Navarro, J.; Obrador, E.; Pellicer, J.A.; Asensi, M.; Viña, J.; Estrela, J.M. Blood glutathione as an index of radiation-induced oxidative stress in mice and humans. Free Radic. Biol. Med. 1997, 22, 1203-1209.
73. Brigelius, R.; Muckel, C.; Akerboom, T.P.; Sies, H. Identification and quantitation of glutathione in hepatic protein mixed disulfides and its relationship to glutathione disulfide. Biochem. Pharmacol. 1983, 32, 2529-2534.
74. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
75. Gupta, R.C. Non random binding of the carcinogen N-hydroxy-2-acetylaminofluorene to repetitive sequences of rat liver DNA in vivo. Proc. Natl Acad. Sci. USA 1984, 81, 6943-6947.
76. Muñíz, P.; Valls, V.; Perez-Broseta, C.; Iradi, A.; Climent, J.V.; Oliva, M.R.; Sáez, G.T. The role of 8-hydroxy-2'-deoxyguanosine in rifamycin-induced DNA damage. Free Radic. Biol. Med. 1995, 18, 747-755.
77. Wei, H.; Frenkel, K. Suppression of tumor promoter-induced oxidative events and DNA damage in vivo by sarcophytol A: A possible mechanism of antipromotion. Cancer Res. 1992, 32, 2298-2303.
78. Brown, R.K.; McBurney, A.; Kelly, F.J. Oxidative damage to DNA in patients with cystic fibrosis. Free Radic. Biol. Med. 1995, 18, 801-806.
79. Espinosa, O.; Jiménez-Almazán, J.; Chaves, F.J.; Tormos, C.; Clapés, S.; Iradi, A.; Salvador, A.; Fandos, M.; Redón, J.; Sáez, G.T. Urinary 8-oxo-2'-deoxyguanosine (8-oxo-dG), a reliable oxidative stress marker in hypertension. Free Rad Res. 2007, 44, 546-554.
80. Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) method. Methods 2001, 25, 402-408.