The adaptive imbalance in base excision-repair enzymes generates microsatellite instability in chronic inflammation

Journal of Clinical Investigation

Volumn 112, Issue 12, 2003, Pages 1887-1894

  Hofseth, Lorne J ^a   Khan, Mohammed A ^a   Ambrose, Mark ^b   Nikolayeva, Olga ^b   Xu Welliver, Meng ^a   Kartalou, Maria ^b   Hussain, S Perwez ^a   Roth, Richard B ^b   Zhou, Xiaoling ^a   Mechanic, Leah E ^a   Zurer, Irit ^c   Rotter, Varda ^c   Samson, Leona D ^b   Harris, Curtis C ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CD68 ANTIGEN; DNA; DNA GLYCOSYLTRANSFERASE; ENDONUCLEASE; ENZYME; FREE RADICAL; PROTEIN;

ARTICLE; CHRONIC INFLAMMATION; DOSE RESPONSE; ENZYME ACTIVITY; EXCISION REPAIR; FRAMESHIFT MUTATION; GENE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MICROSATELLITE INSTABILITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ULCERATIVE COLITIS;

EID: 9144271661     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI19757     Document Type: Article

References (54)

1. Ekbom, A. Helmick, C., Zack, M., and Adami, H.O. 1990. Ulcerative colitis and colorectal cancer. A population-based study. N. Engl. J. Med. 323:1228-1233.
2. O'Sullivan, J.N., et al. 2002. Chromosomal instability in ulcerative colitis is related to telomere shortening. Nat. Genet. 32:280-284.
3. Loeb, K.R., and Loeb, L.A. 1999. Genetic instability and the mutator phenotype. Studies in ulcerative colitis. Am. J. Pathol. 154:1621-1626.
4. Brentnall, T.A. et al. 1996. Microsatellite instability in nonneoplastic mucosa from patients with chronic ulcerative colitis. Cancer Res. 56:1237-1240.
5. Chang, C.L., et al. 2002. Oxidative stress inactivates the human DNA mismatch repair system. Am. J. Physiol. Cell Physiol. 283:C148-C154.
6. Fleisher, A.S., et al. 2000. Microsatellite instability in inflammatory bowel disease-associated neoplastic lesions is associated with hypermethylation and diminished expression of the DNA mismatch repair gene, hMLH1. Cancer Res. 60:4864-4868.
7. Cawkwell, L., et al. 2000. Defective hMSH2/hMLH1 protein expression is seen infrequently in ulcerative colitis associated colorectal cancers. Gut. 46:367-369.
8. Noffsinger, A.E., et al. 1999. A germline hMSH2 alteration is unrelated to colonic microsatellite instability in patients with ulcerative colitis. Hum. Pathol. 30:8-12.
9. Ambs, S., et al. 1998. Frequent nitric oxide synthase-2 expression in human colon adenomas: implication for tumor angiogenesis and colon cancer progression. Cancer Res. 58:334-341.
10. 6-ethenoadenine removal by murine 3-methyladenine DNA glycosylase. Carcinogenesis. 21:901-908.
11. Engelward, B.P., et al. 1997. Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl. Acad. Sci. U. S. A. 94:13087-13092.
12. Bartsch, H., Nair, J., and Velic, I. 1997. Etheno-DNA base adducts as tools in human cancer aetiology and chemoprevention. Eur. J. Cancer. Prev. 6:529-534.
13. Bartsch, H. 2000. Studies on biomarkers in cancer etiology and prevention: a summary and challenge of 20 years of interdisciplinary research. Mutat. Res. 462:255-279.
14. Ohshima, H., and Bartsch, H. 1994. Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis. Mutat. Res 305:253-264.
15. Nair, J., et al. 1998. Lipid peroxidation-induced etheno-DNA adducts in the liver of patients with the genetic metal storage disorders Wilson's disease and primary hemochromatosis. Cancer Epidemiol. Biomarkers Prev. 7:435-440.
16. Nair, J., Barbin, A., Velic, I., and Bartsch, H. 1999. Etheno DNA-base adducts from endogenous reactive species. Mutat. Res. 424:59-69.
17. Holness, C.L., and Simmons, D.L. 1993. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 81:1607-1613.
18. Soini, Y., et al. 1996. An aflatoxin-associated mutational hotspot at codon 249 in the p53 tumor suppressor gene occurs in hepatocellular carcinomas from Mexico. Carcinogenesis. 17:1007-1012.
19. Burke, L., et al. 1998. Allelic deletion analysis of the FHIT gene predicts poor survival in non-small cell lung cancer. Cancer Res. 58:2533-2536.
20. Boland, C.R., et al. 1998. A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res. 58:5248-5257.
21. Markowitz, S., et al. 1995. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science 268:1336-1338.
22. Calin, G., et al. 2001. Somatic frameshift mutations in the Bloom syndrome BLM gene are frequent in sporadic gastric carcinomas with microsatellite mutator phenotype. BMC Genet. 2:14.
23. Glassner, B.J., Rasmussen, L.J., Najarian, M.T., Posnick, L.M., and Samson, L.D. 1998. Generation of a strong mutator phenotype in yeast by imbalanced base excision repair. Proc. Natl. Acad. Sci. U. S. A. 95:9997-10002.
24. Tran, H.T., Keen, J.D., Kricker, M., Resnick, M.A., and Gordenin, D.A. 1997. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol. Cell Biol. 17:2859-2865.
25. Goel, A., et al. 2003. Characterization of sporadic colon cancer by patterns of genomic instability. Cancer Res. 63:1608-1614.
26. Hoang, J.M., et al. 1997. BAT-26, an indicator of the replication error phenotype in colorectal cancers and cell lines. Cancer Res. 57:300-303.
27. Glassner, B.J., Posnick, L.M., and Samson, L.D. 1998. The influence of DNA glycosylases on spontaneous mutation. Mutat. Res. 400:33-44.
28. Xiao, W., and Samson, L. 1993. In vivo evidence for endogenous DNA alkylation damage as a source of spontaneous mutation in eukaryotic cells. Proc. Natl. Acad. Sci. U. S. A. 90:2117-2121.
29. Ames, B.N. 1989. Endogenous oxidative DNA damage, aging, and cancer. Free Radic. Res Commun. 7:121-128.
30. Hussain, S.P., Hofseth, L.J., and Harris, C.C. 2003. Radical causes of cancer. Nat. Rev. Cancer. 3:276-285.
31. Bohr, V.A. 2002. Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radic. Biol. Med. 32:804-812.
32. Xu, W., Liu, L., Smith, G.C., and Charles, I. 2000. Nitric oxide upregulates expression of DNA-PKcs to protect cells from DNA-damaging anti-tumour agents. Nat. Cell Biol. 2:339-345.
33. Akhand, A.A., et al. 1999. Nitric oxide controls src kinase activity through a sulfhydryl group modification-mediated Tyr-527-independent and Tyr-416-linked mechanism. J. Biol. Chem. 274:25821-25826.
34. Ramana, C.V., Boldogh, I., Izumi, T., and Mitra, S. 1998. Activation of apurinic/apyrimidmic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotoxicity of free radicals. Proc. Natl. Acad. Sci. U. S. A. 95:5061-5066.
35. Rusyn, I., et al. 2000. Expression of base excision repair enzymes in rat and mouse liver is induced by peroxisome proliferators and is dependent upon carcinogenic potency. Carcinogenesis. 21:2141-2145.
36. Hofseth, L.J., et al. 2003. Nitric oxide-induced cellular stress and p53 activation in chronic inflammation. Proc. Natl. Acad. Sci. U. S. A. 100:143-148.
37. Zurer, I., et al. 2003. The role of p53 in base excision repair following genotoxic stress. Carcinogenesis. In press.
38. Ho, E., and Ames, B.N. 2002. Low intracellular zinc induces oxidative DNA damage, disrupts p53, NFkappa B,and AP1 DNA binding, and affects DNA repair in a rat glioma cell line. Proc. Natl. Acad. Sci. U. S. A. 99:16770-16775.
39. Bouziane, M., et al. 2000. Promoter structure and cell cycle dependent expression of the human methylpurine-DNA glycosylase gene. Mutat. Res. 461:15-29.
40. Cerda, S.R., et al. 1999. Regulation of expression of N-methylpurine DNA glycosylase in human mammary epithelial cells: role of transcription factor AP-2. Chem. Res. Toxicol. 12:1098-1109.
41. Fung, H., Bennett, R.A., and Demple, B. 2001. Key role of a downstream specificity protein 1 site in cell cycle-regulated transcription of the AP endonuclease gene APE1/APEX in NIH3T3 cells. J. Biol. Chem. 276:42011-42017.
42. Harrison, L., et al. 1997. Comparison of the promoters of the mouse (APEX) and human (APE) apurinic endonuclease genes. Mutat. Res. 385:159-172.
43. Evans, A.R., Limp-Foster, M., and Kelley, M.R. 2000. Going APE over ref-1. Mutat. Res. 461:83-108.
44. Izumi, T., Henner, W.D., and Mitra, S. 1996. Negative regulation of the major human AP-endonuclease, a multifunctional protein. Biochemistry. 35:14679-14683.
45. Dantzer, F., Luna, L., Bjoras, M., and Seeberg, E. 2002. Human OGG1 undergoes serine phosphorylation and associates with the nuclear matrix and mitotic chromatin in vivo. Nucleic Acids Res 30:2349-2357.
46. Tini, M., et al. 2002. Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol. Cell. 9:265-277.
47. Hasan, S., et al. 2002. Acetylation regulates the DNA end-trimming activity of DNA polymerase β. Mol. Cell. 10:1213-1222.
48. Hasan, S., et al. 2001. Regulation of human flap endonuclease-1 activity by acetylation through the transcriptional coactivator p300. Mol. Cell. 7:1221-1231.
49. Yamada, N.A., and Farber, R.A. 2002. Induction of a low level of microsatellite instability by overexpression of DNA polymerase β. Cancer Res. 62:6061-6064.
50. Mori, Y., et al. 2001. Instabilotyping: comprehensive identification of frameshift mutations caused by coding region microsatellite instability. Cancer Res. 61:6046-6049.
51. Rampino, N., et al. 1997. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science. 275:967-969.
52. Gruber, S.B., et al. 2002. BLM heterozygosity and the risk of colorectal cancer. Science. 297:2013.
53. Goss, K.H., et al. 2002. Enhanced tumor formation in mice heterozygous for Blm mutation. Science. 297:2051-2053.
54. Berdal, K.G., Johansen, R.F., and Seeberg, E. 1998. Release of normal bases from intact DNA by a native DNA repair enzyme. EMBO J. 17:363-367.