Differential effects of reactive nitrogen species on DNA base excision repair initiated by the alkyladenine DNA glycosylase

Carcinogenesis

Volumn 30, Issue 12, 2009, Pages 2123-2129

  Jones Larry E , Jr ^a   Ying, Lei ^a   Hofseth, Anne B ^a   Jelezcova, Elena ^b   Sobol, Robert W ^b,c   Ambs, Stefan ^d   Harris, Curtis C ^d   Espey, Michael Graham ^e   Hofseth, Lorne J ^a   Wyatt, Michael D ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLADENINE DNA GLYCOSYLTRANSFERASE; CYSTEINE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA DIRECTED DNA POLYMERASE BETA; DNA GLYCOSYLTRANSFERASE; INDUCIBLE NITRIC OXIDE SYNTHASE; REACTIVE NITROGEN SPECIES; TYROSINE; UNCLASSIFIED DRUG; 3 METHYLADENINE DEOXYRIBONUCLEIC ACID GLYCOSYLASE; 3-METHYLADENINE-DNA GLYCOSYLASE; APEX1 PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; COLON ADENOCARCINOMA; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOPLASM; ENZYME ACTIVITY; EXCISION REPAIR; HUMAN; HUMAN TISSUE; MOUSE; NITRATION; NITROSATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; ADENOMA; ANIMAL; DNA REPAIR; ENZYME ACTIVE SITE; GENETICS; INTESTINE TUMOR; MALE; PROTEIN CONFORMATION; TRANSGENIC MOUSE; TUMOR CELL LINE;

ADENOMA; ANIMALS; CATALYTIC DOMAIN; CELL LINE, TUMOR; DNA GLYCOSYLASES; DNA POLYMERASE BETA; DNA REPAIR; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; HUMANS; INTESTINAL NEOPLASMS; MALE; MICE; MICE, TRANSGENIC; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; REACTIVE NITROGEN SPECIES;

EID: 73949135721     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgp256     Document Type: Article

References (55)

1. Lu,H. et al. (2006) Inflammation, a key event in cancer development. Mol. Cancer Res., 4, 221-233.
2. Dedon,P.C. et al. (2004) Reactive nitrogen species in the chemical biology of inflammation. Arch. Biochem. Biophys., 423, 12-22.
3. Ohshima,H. et al. (2003) Chemical basis of inflammation-induced carcinogenesis. Arch. Biochem. Biophys., 417, 3-11.
4. Dong,M. et al. (2006) Relatively small increases in the steady-state levels of nucleobase deamination products in DNA from human TK6 cells exposed to toxic levels of nitric oxide. Chem. Res. Toxicol., 19, 50-57.
5. Pang,B. et al. (2007) Lipid peroxidation dominates the chemistry of DNA adduct formation in a mouse model of inflammation. Carcinogenesis, 28, 1807-1813.
6. Bartsch,H. et al. (2005) Accumulation of lipid peroxidation-derived DNA lesions: potential lead markers for chemoprevention of inflammationdriven malignancies. Mutat. Res., 591, 34-44.
7. Almeida,K.H. et al. (2007) A unified view of base excision repair: lesiondependent protein complexes regulated by post-translational modification. DNA Repair (Amst), 6, 695-711.
8. Engelward,B.P. et al. (1997) Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl Acad. Sci. USA, 94, 13087-13092.
9. Hang,B. et al. (1997) Targeted deletion of alkylpurine-DNA-N-glycosylase in mice eliminates repair of 1, N6 ethenoadenine and hypoxanthine but not of 3, N4 ethenocytosine or 8-oxoguanine. Proc. Natl Acad. Sci. USA, 94, 12869-12874.
10. Hitchcock,T.M. et al. (2004) Oxanine DNA glycosylase activity from mammalian alkyladenine glycosylase. J. Biol. Chem., 279, 38177-38183.
11. Saparbaev,M.K. et al. (2002) 1, N2-Ethenoguanine, a mutagenic DNA adduct, is a substrate of Escherichia coli mismatch-specific uracil-DNA glycosylase and human alkylpurine-DNA-N glycosylase. J. Biol. Chem., 277, 26987-26993.
12. Wuenschell,G.E. et al. (2003) Stability, miscoding potential, and repair of 2-deoxyxanthosine in DNA: implications for nitric oxide-induced mutagenesis. Biochemistry, 42, 3608-3616.
13. Ringvoll,J. et al. (2008) AlkB homologue 2-mediated repair of ethenoadenine lesions in mammalian DNA. Cancer Res., 68, 4142-4149.
14. Meira,L.B. et al. (2008) DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice. J. Clin. Invest., 118, 2516-2525.
15. Schmid,K. et al. (2000) Increased levels of promutagenic etheno-DNA adducts in colonic polyps of FAP patients. Int. J. Cancer, 87, 1-4.
16. Hofseth,L.J. et al. (2003) The adaptive imbalance in base excision-repair enzymes generates microsatellite instability in chronic inflammation. J. Clin. Invest., 112, 1887-1894.
17. Benhar,M. et al. (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science, 320, 1050-1054.
18. Iyer,A.K. et al. (2008) Role of S-nitrosylation in apoptosis resistance and carcinogenesis. Nitric Oxide, 19, 146-151.
19. Szabo,C. et al. (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov., 6, 662-680.
20. Thomas,D.D. et al. (2008) The chemical biology of nitric oxide: implications in cellular signaling. Free Radic. Biol. Med., 45, 18-31.
21. Jaiswal,M. et al. (2001) Human Ogg1, a protein involved in the repair of 8-oxoguanine, is inhibited by nitric oxide. Cancer Res., 61, 6388-6393.
22. Qu,J. et al. (2007) Nitric oxide controls nuclear export of APE1/Ref-1 through S-nitrosation of cysteines 93 and 310. Nucleic Acids Res., 35, 2522-2532.
23. Pettersen,E.F. et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
24. Lau,A.Y. et al. (2000) Molecular basis for discriminating between normal and damaged bases by the human alkyladenine glycosylase, AAG. Proc. Natl Acad. Sci. USA, 97, 13573-13578.
25. Connor,E.E. et al. (2005) Effects of substrate specificity on initiating the base excision repair of N-methylpurines by variant human 3-methyladenine DNA glycosylases. Chem. Res. Toxicol., 18, 87-94.
26. Connor,E.E. et al. (2002) Active-site clashes prevent the human 3-methyladenine DNA glycosylase from improperly removing bases. Chem. Biol., 9, 1033-1041.
27. Lau,A. et al. (1998) Crystal structure of a human alkylbase-DNA repair enzyme complexed to DNA: mechanism for nucleotide flipping and base excision. Cell, 95, 249-258.
28. Adhikari,S. et al. (2007) N-terminal extension of N-methylpurine DNA glycosylase is required for turnover in hypoxanthine excision reaction. J. Biol. Chem., 282, 30078-30084.
29. Thomas,D.D. et al. (2002) Protein nitration is mediated by heme and free metals through Fenton-type chemistry: an alternative to the NO/O2-reaction. Proc. Natl Acad. Sci. USA, 99, 12691-12696.
30. 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.
31. Ying,L. et al. (2005) Chronic inflammation promotes retinoblastoma protein hyperphosphorylation and E2F1 activation. Cancer Res., 65, 9132-9136.
32. Roy,R. et al. (1996) The domains of mammalian base excision repair enzyme N-methylpurine-DNA glycosylase. Interaction, conformational change, and role in DNA binding and damage recognition. J. Biol. Chem., 271, 23690-23697.
33. Trivedi,R.N. et al. (2008) Human methyl purine DNA glycosylase and DNA polymerase {beta} expression collectively predict sensitivity to temozolomide. Mol. Pharmacol., 74, 505-516.
34. Kotakadi,V.S. et al. (2008) Ginkgo biloba extract EGb 761 has antiinflammatory properties and ameliorates colitis in mice by driving effector T cell apoptosis. Carcinogenesis, 29, 1799-1806.
35. Espey,M.G. et al. (2002) Direct real-time evaluation of nitration with green fluorescent protein in solution and within human cells reveals the impact of nitrogen dioxide vs. peroxynitrite mechanisms. Proc. Natl Acad. Sci. USA, 99, 3481-3486.
36. Vallur,A.C. et al. (2002) Effects of hydrogen bonding within a damaged base pair on the activity of wild-type and DNA-intercalating mutants of human alkyladenine DNA glycosylase. J. Biol. Chem., 277, 31673-31678.
37. Hogg,N. (2000) Biological chemistry and clinical potential of S-nitrosothiols. Free Radic. Biol. Med., 28, 1478-1486.
38. Espey,M.G. et al. (2001) Distinction between nitrosating mechanisms within human cells and aqueous solution. J. Biol. Chem., 276, 30085-30091.
39. Maragos,C.M. et al. (1991) Complexes of.NO with nucleophiles as agents for the controlled biological release of nitric oxide. Vasorelaxant effects. J. Med. Chem., 34, 3242-3247.
40. Luongo,C. et al. (1994) Loss of Apc+ in intestinal adenomas from Min mice. Cancer Res., 54, 5947-5952.
41. Espey,M.G. et al. (2000) Mechanisms of cell death governed by the balance between nitrosative and oxidative stress. Ann. N. Y. Acad. Sci., 899, 209-221.
42. Schopfer,F.J. et al. (2003) NO-dependent protein nitration: a cell signaling event or an oxidative inflammatory response? Trends Biochem. Sci., 28, 646-654.
43. Zhang,H. et al. (2005) Intramolecular electron transfer between tyrosyl radical and cysteine residue inhibits tyrosine nitration and induces thiyl radical formation in model peptides treated with myeloperoxidase, H2O2, and NO2-: EPR SPIN trapping studies. J. Biol. Chem., 280, 40684-40698.
44. Zhang,H. et al. (2009) The effect of neighboring methionine residue on tyrosine nitration and oxidation in peptides treated with MPO, H2O2, and NO2(-) or peroxynitrite and bicarbonate: role of intramolecular electron transfer mechanism? Arch. Biochem. Biophys., 484, 134-145.
45. Kojima,M. et al. (1999) Nitric oxide synthase expression and nitric oxide production in human colon carcinoma tissue. J. Surg. Oncol., 70, 222-229.
46. Seril,D.N. et al. (2002) Inhibition of chronic ulcerative colitis-associated colorectal adenocarcinoma development in a murine model by Nacetylcysteine. Carcinogenesis, 23, 993-1001.
47. Yerushalmi,H.F. et al. (2006) The role of NO synthases in argininedependent small intestinal and colonic carcinogenesis. Mol. Carcinog., 45, 93-105.
48. Burney,S. et al. (1999) The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat. Res., 424, 37-49.
49. Chen,C.Y. et al. (2008) Substrate binding pocket residues of human alkyladenine-DNA glycosylase critical for methylating agent survival. DNA Repair (Amst), 7, 1731-1745.
50. O'Brien,P.J. et al. (2004) Dissecting the broad substrate specificity of human 3-methyladenine-DNA glycosylase. J. Biol. Chem., 279, 9750-9757.
51. Wyatt,M.D. et al. (2006) Methylating agents and DNA repair responses: methylated bases and sources of strand breaks. Chem. Res. Toxicol., 19, 1580-1594.
52. Berdal,K.G. et al. (1998) Release of normal bases from intact DNA by a native DNA repair enzyme. EMBO J., 17, 363-367.
53. Glassner,B.J. et al. (1998) Generation of a strong mutator phenotype in yeast by imbalanced base excision repair. Proc. Natl Acad. Sci. USA, 95, 9997-10002.
54. Kakolyris,S. et al. (1997) Human apurinic endonuclease 1 expression in a colorectal adenoma-carcinoma sequence. Cancer Res., 57, 1794-1797.
55. Tell,G. et al. (2005) The intracellular localization of APE1/Ref-1: more than a passive phenomenon? Antioxid. Redox Signal., 7, 367-384.