Prereplicative repair of oxidized bases in the human genome is mediated by NEIL1 DNA glycosylase together with replication proteins

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

Volumn 110, Issue 33, 2013, Pages

  Hegde, Muralidhar L ^a   Hegde, Pavana M ^a   Bellot, Larry J ^a   Mandal, Santi M ^a   Hazra, Tapas K ^a   Li, Guo Min ^b   Boldogh, Istvan ^a   Tomkinson, Alan E ^c   Mitra, Sankar ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Genome damage repair; Oxidized base repair at DNA replication fork; Replication fork stalling

Indexed keywords

DNA GLYCOSYLTRANSFERASE; DNA POLYMERASE; HELICASE; OXYGEN DERIVATIVE; REPLICATION FACTOR A; SINGLE STRANDED DNA;

ARTICLE; CELL CYCLE S PHASE; CELL STRESS; CELL SYNCHRONIZATION; CONTROLLED STUDY; DEAMINATION; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; DNA TEMPLATE; EMBRYO; GENOME; HUMAN; HUMAN CELL; IN VITRO STUDY; OXIDATION; PRIORITY JOURNAL;

GENOME DAMAGE REPAIR; OXIDIZED BASE REPAIR AT DNA REPLICATION FORK; REPLICATION FORK STALLING;

BLOTTING, WESTERN; BROMODEOXYURIDINE; CHROMATIN IMMUNOPRECIPITATION; DNA GLYCOSYLASES; DNA POLYMERASE III; DNA REPAIR; DNA REPLICATION; GENOME, HUMAN; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; OXIDATIVE STRESS; RNA, SMALL INTERFERING;

EID: 84882342093     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1304231110     Document Type: Article

References (64)

1. Hegde ML, Hazra TK, Mitra S (2008) Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res 18(1):27-47.
2. Friedberg EC, et al. (2006) DNA repair: From molecular mechanism to human disease. DNA Repair (Amst) 5(8):986-996.
3. Charlet-Berguerand N, et al. (2006) RNA polymerase II bypass of oxidative DNA damage is regulated by transcription elongation factors. EMBO J 25(23):5481-5491.
4. Frederico LA, Kunkel TA, Shaw BR (1990) A sensitive genetic assay for the detection of cytosine deamination: Determination of rate constants and the activation energy. Biochemistry 29(10):2532-2537.
5. Hazra TK, et al. (2002) Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc Natl Acad Sci USA 99(6): 3523-3528.
6. Hazra TK, et al. (2002) Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions. J Biol Chem 277(34):30417-30420.
7. Liu M, et al. (2010) The mouse ortholog of NEIL3 is a functional DNA glycosylase in vitro and in vivo. Proc Natl Acad Sci USA 107(11):4925-4930.
8. Dou H, Mitra S, Hazra TK (2003) Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. J Biol Chem 278(50):49679-49684.
9. Das A, et al. (2007) The human Werner syndrome protein stimulates repair of oxidative DNA base damage by the DNA glycosylase NEIL1. J Biol Chem 282(36): 26591-26602.
10. Dou H, et al. (2008) Interaction of the human DNA glycosylase NEIL1 with proliferating cell nuclear antigen. The potential for replication-associated repair of oxidized bases in mammalian genomes. J Biol Chem 283(6):3130-3140.
11. Hegde ML, et al. (2008) Physical and functional interaction between human oxidized base-specific DNA glycosylase NEIL1 and flap endonuclease J Biol Chem 283(40): 27028-27037.
12. Hegde ML, et al. (2013) The disordered C-terminal domain of human DNA glycosylase NEIL1 contributes to its stability via intramolecular interactions. J Mol Biol 425(13): 2359-2371.
13. Theriot CA, Hegde ML, Hazra TK, Mitra S (2010) RPA physically interacts with the human DNA glycosylase NEIL1 to regulate excision of oxidative DNA base damage in primer-template structures. DNA Repair (Amst) 9(6):643-652.
14. Groth P, et al. (2010) Methylated DNA causes a physical block to replication forks independently of damage signalling, O(6)-methylguanine or DNA single-strand breaks and results in DNA damage. J Mol Biol 402(1):70-82.
15. Jackson DA, Pombo A (1998) Replicon clusters are stable units of chromosome structure: Evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 140(6):1285-1295.
16. Zhao X, Krishnamurthy N, Burrows CJ, David SS (2010) Mutation versus repair: NEIL1 removal of hydantoin lesions in single-stranded, bulge, bubble, and duplex DNA contexts. Biochemistry 49(8):1658-1666.
17. Tornaletti S, Maeda LS, Lloyd DR, Reines D, Hanawalt PC (2001) Effect of thymine glycol on transcription elongation by T7 RNA polymerase and mammalian RNA polymerase II. J Biol Chem 276(48):45367-45371.
18. Evans J, et al. (1993) Thymine ring saturation and fragmentation products: Lesion bypass, misinsertion and implications for mutagenesis. Mutat Res 299(3-4):147-156.
19. Nakamura H, Morita T, Sato C (1986) Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp Cell Res 165(2):291-297.
20. Mills AD, et al. (1989) Replication occurs at discrete foci spaced throughout nuclei replicating in vitro. J Cell Sci 94(pt 3):471-477.
21. Banerjee D, et al. (2011) Preferential repair of oxidized base damage in the transcribed genes of mammalian cells. J Biol Chem 286(8):6006-6016.
22. Harper JV (2005) Synchronization of cell populations in G1/S and G2/M phases of the cell cycle. Methods Mol Biol 296:157-166.
23. Johansson H, Svensson F, Runnberg R, Simonsson T, Simonsson S (2010) Phosphorylated nucleolin interacts with translationally controlled tumor protein during mitosis and with Oct4 during interphase in ES cells. PLoS ONE 5(10):e13678.
24. Fredriksson S, et al. (2002) Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol 20(5):473-477.
25. Mandal SM, et al. (2012) Role of human DNA glycosylase Nei-like 2 (NEIL2) and single strand break repair protein polynucleotide kinase 3′-phosphatase in maintenance of mitochondrial genome. J Biol Chem 287(4):2819-2829.
26. Wiederhold L, et al. (2004) AP endonuclease-independent DNA base excision repair in human cells. Mol Cell 15(2):209-220.
27. Matsumoto Y, et al. (1999) Reconstitution of proliferating cell nuclear antigendependent repair of apurinic/apyrimidinic sites with purified human proteins. J Biol Chem 274(47):33703-33708.
28. Frosina G, et al. (1996) Two pathways for base excision repair in mammalian cells. J Biol Chem 271(16):9573-9578.
29. Klungland A, Lindahl T (1997) Second pathway for completion of human DNA base excision-repair: Reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J 16(11):3341-3348.
30. Fortini P, Dogliotti E (2007) Base damage and single-strand break repair: Mechanisms and functional significance of short- and long-patch repair subpathways. DNA Repair (Amst) 6(4):398-409.
31. Das A, et al. (2006) NEIL2-initiated, APE-independent repair of oxidized bases in DNA: Evidence for a repair complex in human cells. DNA Repair (Amst) 5(12):1439-1448.
32. Hegde ML, et al. (2010) Specific inhibition of NEIL-initiated repair of oxidized base damage in human genome by copper and iron: Potential etiological linkage to neurodegenerative diseases. J Biol Chem 285(37):28812-28825.
33. Szczesny B, Tann AW, Longley MJ, Copeland WC, Mitra S (2008) Long patch base excision repair in mammalian mitochondrial genomes. J Biol Chem 283(39): 26349-26356.
34. OtterleiM, et al. (1999) Post-replicative base excision repair in replication foci. EMBO J 18(13):3834-3844.
35. Hayashi H, et al. (2002) Replication-associated repair of adenine:8-oxoguanine mispairs by MYH. Curr Biol 12(4):335-339.
36. Shibutani S, Takeshita M, Grollman AP (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349(6308):431-434.
37. Slupska MM, et al. (1996) Cloning and sequencing a human homolog (hMYH) of the Escherichia coli mutY gene whose function is required for the repair of oxidative DNA damage. J Bacteriol 178(13):3885-3892.
38. Krokan HE, Drabløs F, Slupphaug G (2002) Uracil in DNA - occurrence, consequences and repair. Oncogene 21(58):8935-8948.
39. Boldogh I, et al. (2001) hMYH cell cycle-dependent expression, subcellular localization and association with replication foci: Evidence suggesting replication-coupled repair of adenine:8-oxoguanine mispairs. Nucleic Acids Res 29(13):2802-2809.
40. Kavli B, et al. (2002) hUNG2 is the major repair enzyme for removal of uracil from U:A matches, U:G mismatches, and U in single-stranded DNA, with hSMUG1 as a broad specificity backup. J Biol Chem 277(42):39926-39936.
41. Parsons JL, Zharkov DO, Dianov GL (2005) NEIL1 excises 3′ end proximal oxidative DNA lesions resistant to cleavage by NTH1 and OGG1. Nucleic Acids Res 33(15):4849-4856.
42. Hazra TK, et al. (2007) Oxidative DNA damage repair in mammalian cells: A new perspective. DNA Repair (Amst) 6(4):470-480.
43. Rodríguez-López AM, et al. (2003) Characterisation of the interaction between WRN, the helicase/exonuclease defective in progeroid Werner's syndrome, and an essential replication factor, PCNA. Mech Ageing Dev 124(2):167-174.
44. Machwe A, Lozada E, Wold MS, Li GM, Orren DK (2011) Molecular cooperation between the Werner syndrome protein and replication protein A in relation to replication fork blockage. J Biol Chem 286(5):3497-3508.
45. Brosh RM, Jr., et al. (2001) Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity. EMBO J 20(20):5791-5801.
46. Sharma S, et al. (2005) The interaction site of Flap Endonuclease-1 with WRN helicase suggests a coordination of WRN and PCNA. Nucleic Acids Res 33(21):6769-6781.
47. Pichierri P, Franchitto A, Mosesso P, Palitti F (2001) Werner's syndrome protein is required for correct recovery after replication arrest and DNA damage induced in S-phase of cell cycle. Mol Biol Cell 12(8):2412-2421.
48. Machwe A, Xiao L, Groden J, Orren DK (2006) The Werner and Bloom syndrome proteins catalyze regression of a model replication fork. Biochemistry 45(47): 13939-13946.
49. Postow L, Woo EM, Chait BT, Funabiki H (2009) Identification of SMARCAL1 as a component of the DNA damage response. J Biol Chem 284(51):35951-35961.
50. Driscoll R, Cimprich KA (2009) HARPing on about the DNA damage response during replication. Genes Dev 23(20):2359-2365.
51. Neurauter CG, Luna L, Bjørås M (2012) Release from quiescence stimulates the expression of human NEIL3 under the control of the Ras dependent ERK-MAP kinase pathway. DNA Repair (Amst) 11(4):401-409.
52. Takao M, et al. (2002) A back-up glycosylase in Nth1 knock-out mice is a functional Nei (endonuclease VIII) homologue. J Biol Chem 277(44):42205-42213.
53. Vartanian V, et al. (2006) The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase. Proc Natl Acad Sci USA 103(6):1864-1869.
54. Klungland A, et al. (1999) Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc Natl Acad Sci USA 96(23): 13300-13305.
55. Minowa O, et al. (2000) Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice. Proc Natl Acad Sci USA 97(8):4156-4161.
56. Hegde ML, et al. (2012) Enhancement of NEIL1 protein-initiated oxidized DNA base excision repair by heterogeneous nuclear ribonucleoprotein U (hnRNP-U) via direct interaction. J Biol Chem 287(41):34202-34211.
57. Wang H, Hays JB (2003) Mismatch repair in human nuclear extracts: Effects of internal DNA-hairpin structures between mismatches and excision-initiation nicks on mismatch correction and mismatch-provoked excision. J Biol Chem 278(31):28686-28693.
58. Hill JW, Hazra TK, Izumi T, Mitra S (2001) Stimulation of human 8-Oxoguanine-DNA glycosylase by AP-endonuclease: Potential coordination of the initial steps in base excision repair. Nucleic Acids Res 29(2):430-438.
59. Taylor RM, Whitehouse CJ, Caldecott KW (2000) The DNA ligase III zinc finger stimulates binding to DNA secondary structure and promotes end joining. Nucleic Acids Res 28(18):3558-3563.
60. Prasad R, Beard WA, Strauss PR, Wilson SH (1998) Human DNA polymerase beta deoxyribose phosphate lyase. Substrate specificity and catalytic mechanism. J Biol Chem 273(24):15263-15270.
61. Chiu RW, Baril EF (1975) Nuclear DNA polymerases and the HeLa cell cycle. J Biol Chem 250(19):7951-7957.
62. Bresnahan WA, Boldogh I, Thompson EA, Albrecht T (1996) Human cytomegalovirus inhibits cellular DNA synthesis and arrests productively infected cells in late G1. Virology 224(1):150-160.
63. Kumar D, Ray A, Ray BK (2009) Transcriptional synergy mediated by SAF-1 and AP-1: Critical role of N-terminal polyalanine and two zinc finger domains of SAF-1. J Biol Chem 284(3):1853-1862.
64. Hegde ML, Hegde PM, Arijit D, Boldogh I, Mitra S (2012) Human DNA glycosylase NEIL1's interactions with downstream repair proteins is critical for efficient repair of oxidized DNA base damage and enhanced cell survival. Biomolecules 2(4): 564-578.