Endonuclease V: An unusual enzyme for repair of DNA deamination

Cellular and Molecular Life Sciences

Volumn 70, Issue 17, 2013, Pages 3145-3156

  Cao, Weiguo ^a  

^a CLEMSON UNIVERSITY   (United States)

Author keywords

Deamination; DNA repair; Endonuclease; Inosine; Mutagenesis; Oxanosine; Uridine; Xanthosine

Indexed keywords

ENDONUCLEASE; ENDONUCLEASE V; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARCHAEON; BACTERIUM; BIOTECHNOLOGY; CATALYSIS; DEAMINATION; DNA MODIFICATION; DNA REPAIR; ENZYME ACTIVITY; ENZYME STRUCTURE; EUKARYOTE; GENE SEQUENCE; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; DEAMINATION; DEOXYRIBONUCLEASE (PYRIMIDINE DIMER); DNA REPAIR; HUMANS;

ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA;

EID: 84882448985     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1222-z     Document Type: Review

References (93)

1. Burney S, Caulfield JL, Niles JC, Wishnok JS, Tannenbaum SR (1999) The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat Res 424:37-49
2. Dedon PC, Tannenbaum SR (2004) Reactive nitrogen species in the chemical biology of inflammation. Arch Biochem Biophys 423:12-22
3. Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709-715
4. Nguyen T, Brunson D, Crespi CL, Penman BW, Wishnok JS, Tannenbaum SR (1992) DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc Natl Acad Sci USA 89:3030-3034
5. Shapiro R (1981) Damage to DNA caused by hydrolysis. In: Seeberg E, Kleppe K (eds) Chromosome damage and repair. Plenum Press, New York, pp 3-18
6. Spencer JP, Whiteman M, Jenner A, Halliwell B (2000) Nitrite-induced deamination and hypochlorite-induced oxidation of DNA in intact human respiratory tract epithelial cells. Free Radic Biol Med 28:1039-1050
7. Wink DA, Kasprzak KS, Maragos CM, Elespuru RK, Misra M, Dunams TM, Cebula TA, Koch WH, Andrews AW, Allen JS et al (1991) DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254:1001-1003
8. Suzuki T, Yamaoka R, Nishi M, Ide H, Makino K (1996) Isolation and characterization of a novel product, 2′-deoxyoxanosine, from 2′-deoxyguanosine, oligodeoxynucleotide and calf thymus DNA treated by nitrous-acid and nitric-oxide. J Am Chem Soc 118:2515-2516
9. Parikh SS, Putnam CD, Tainer JA (2000) Lessons learned from structural results on uracil-DNA glycosylase. Mutat Res 460:183-199
10. Pearl LH (2000) Structure and function in the uracil-DNA glycosylase superfamily. Mutat Res 460:165-181
11. Mi R, Dong L, Kaulgud T, Hackett KW, Dominy BN, Cao W (2009) Insights from xanthine and uracil DNA glycosylase activities of bacterial and human SMUG1: switching SMUG1 to UDG. J Mol Biol 385:761-778
12. Lee HW, Brice AR, Wright CB, Dominy BN, Cao W (2010) Identification of Escherichia coli mismatch-specific uracil DNA glycosylase as a robust xanthine DNA glycosylase. J Biol Chem 285:41483-41490
13. Lee HW, Dominy BN, Cao W (2011) New family of deamination repair enzymes in uracil-DNA glycosylase superfamily. J Biol Chem 286:31282-31287
14. Dong L, Meira LB, Hazra TK, Samson LD, Cao W (2008) Oxanine DNA glycosylase activities in mammalian systems. DNA Repair 7:128-134
15. Dong L, Mi R, Glass RA, Barry JN, Cao W (2008) Repair of deaminated base damage by Schizosaccharomyces pombe thymine DNA glycosylase. DNA Repair 7:1962-1972
16. Hitchcock TM, Dong L, Connor EE, Meira LB, Samson LD, Wyatt MD, Cao W (2004) Oxanine DNA glycosylase activity from mammalian alkyladenine glycosylase. J Biol Chem 279:38177-38183
17. Saparbaev M, Laval J (1994) Excision of hypoxanthine from DNA containing dIMP residues by the Escherichia coli, yeast, rat, and human alkylpurine DNA glycosylases. Proc Natl Acad Sci USA 91:5873-5877
18. Terato H, Masaoka A, Asagoshi K, Honsho A, Ohyama Y, Suzuki T, Yamada M, Makino K, Yamamoto K, Ide H (2002) Novel repair activities of AlkA (3-methyladenine DNA glycosylase II) and endonuclease VIII for xanthine and oxanine, guanine lesions induced by nitric oxide and nitrous acid. Nucleic Acids Res 30:4975-4984
19. Cortazar D, Kunz C, Saito Y, Steinacher R, Schar P (2007) The enigmatic thymine DNA glycosylase. DNA Repair 6:489-504
20. Kow YW (2002) Repair of deaminated bases in DNA. Free Radic Biol Med 33:886-893
21. Krokan HE, Drablos F, Slupphaug G (2002) Uracil in DNA - occurrence, consequences and repair. Oncogene 21:8935-8948
22. Dalhus B, Laerdahl JK, Backe PH, Bjoras M (2009) DNA base repair-recognition and initiation of catalysis. FEMS Microbiol Rev 33:1044-1078
23. Barnes DE, Lindahl T (2004) Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu Rev Genet 38:445-476
24. Stivers JT, Jiang YL (2003) A mechanistic perspective on the chemistry of DNA repair glycosylases. Chem Rev 103:2729-2759
25. Gates FT 3rd, Linn S (1977) Endonuclease V of Escherichia coli. J Biol Chem 252:1647-1653
26. Linn S (2012) Life in the serendipitous lane: excitement and gratification in studying DNA repair. DNA Repair 11:595-605
27. Demple B, Linn S (1982) On the recognition and cleavage mechanism of Escherichia coli endodeoxyribonuclease V, a possible DNA repair enzyme. J Biol Chem 257:2848-2855
28. Harosh I, Sperling J (1988) Hypoxanthine-DNA glycosylase from Escherichia coli. Partial purification and properties. J Biol Chem 263:3328-3334
29. Karran P, Lindahl T (1978) Enzymatic excision of free hypoxanthine from polydeoxynucleotides and DNA containing deoxyinosine monophosphate residues. J Biol Chem 253:5877-5879
30. Yao M, Hatahet Z, Melamede RJ, Kow YW (1994) Purification and characterization of a novel deoxyinosine-specific enzyme, deoxyinosine 3′ endonuclease, from Escherichia coli. J Biol Chem 269:16260-16268
31. Yao M, Kow YW (1994) Strand-specific cleavage of mismatch-containing DNA by deoxyinosine 3′-endonuclease from Escherichia coli. J Biol Chem 269:31390-31396
32. Yao M, Kow YW (1995) Interaction of deoxyinosine 3′-endonuclease from Escherichia coli with DNA containing deoxyinosine. J Biol Chem 270:28609-28616
33. Yao M, Kow YW (1996) Cleavage of insertion/deletion mismatches, flap and pseudo-Y DNA structures by deoxyinosine 3′-endonuclease from Escherichia coli. J Biol Chem 271:30672-30676
34. Yao M, Kow YW (1997) Further characterization of Escherichia coli endonuclease V. J Biol Chem 272:30774-30779
35. Demple B, Gates FT, 3rd, Linn S (1980) Purification and properties of Escherichia coli endodeoxyribonuclease V. Methods Enzymol 65:224-231
36. Guo G, Ding Y, Weiss B (1997) nfi, the gene for endonuclease V in Escherichia coli K-12. J Bacteriol 179:310-316
37. Dianov G, Lindahl T (1991) Preferential recognition of I.T base-pairs in the initiation of excision-repair by hypoxanthine-DNA glycosylase. Nucleic Acids Res 19:3829-3833
38. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2006) DNA repair and mutagenesis, 2nd edn. ASM Press, Washington, DC
39. Sekiguchi M (2012) My path toward DNA repair. DNA Repair 11:606-615
40. Yasuda S, Sekiguchi M (1970) T4 endonuclease involved in repair of DNA. Proc Natl Acad Sci USA 67:1839-1845
41. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290-301
42. Aravind L, Walker DR, Koonin EV (1999) Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res 27:1223-1242
43. Van Houten B, Croteau DL, DellaVecchia MJ, Wang H, Kisker C (2005) 'Close-fitting sleeves': DNA damage recognition by the UvrABC nuclease system. Mutat Res 577:92-117
44. Nowotny M (2009) Retroviral integrase superfamily: the structural perspective. EMBO Rep 10:144-151
45. Haren L, Ton-Hoang B, Chandler M (1999) Integrating DNA: transposases and retroviral integrases. Annu Rev Microbiol 53:245-281
46. Rand TA, Ginalski K, Grishin NV, Wang X (2004) Biochemical identification of Argonaute 2 as the sole protein required for RNA-induced silencing complex activity. Proc Natl Acad Sci USA 101:14385-14389
47. Song JJ, Smith SK, Hannon GJ, Joshua-Tor L (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305:1434-1437
48. Majorek KA, Bujnicki JM (2009) Modeling of Escherichia coli endonuclease V structure in complex with DNA. J Mol Model 15:173-182
49. Dalhus B, Arvai AS, Rosnes I, Olsen OE, Backe PH, Alseth I, Gao H, Cao W, Tainer JA, Bjoras M (2009) Structures of endonuclease V with DNA reveal initiation of deaminated adenine repair. Nat Struct Mol Biol 16:138-143
50. Huffman JL, Sundheim O, Tainer JA (2005) DNA base damage recognition and removal: new twists and grooves. Mutat Res 577:55-76
51. Roberts RJ, Cheng X (1998) Base flipping. Annu Rev Biochem 67:181-198
52. Scharer OD, Campbell AJ (2009) Wedging out DNA damage. Nat Struct Mol Biol 16:102-104
53. Huang J, Lu J, Barany F, Cao W (2001) Multiple cleavage activities of endonuclease V from Thermotoga maritima: recognition and strand nicking mechanism. Biochemistry 40:8738-8748
54. Feng H, Dong L, Klutz AM, Aghaebrahim N, Cao W (2005) Defining amino acid residues involved in DNA-protein interactions and revelation of 3′-exonuclease activity in endonuclease V. Biochemistry 44:11486-11495
55. Huang J, Lu J, Barany F, Cao W (2002) Mutational analysis of endonuclease V from Thermotoga maritima. Biochemistry 41:8342-8350
56. Feng H, Dong L, Cao W (2006) Catalytic mechanism of endonuclease v: a catalytic and regulatory two-metal model. Biochemistry 45:10251-10259
57. Mi R, Alford-Zappala M, Kow YW, Cunningham RP, Cao W (2012) Human endonuclease V as a repair enzyme for DNA deamination. Mutat Res 735:12-18
58. 2+ ions reveals two divalent metals bound in the active site. J Biol Chem 276:7266-7271
59. Hitchcock TM, Gao H, Cao W (2004) Cleavage of deoxyoxanosine-containing oligodeoxyribonucleotides by bacterial endonuclease V. Nucleic Acids Res 32:4071-4080
60. Horton NC, Perona JJ (2004) DNA cleavage by EcoRV endonuclease: two metal ions in three metal ion binding sites. Biochemistry 43:6841-6857
61. 2+ binding to the active site of EcoRV endonuclease: a crystallographic study of complexes with substrate and product DNA at 2 A resolution. Biochemistry 34:683-696
62. Vipond IB, Baldwin GS, Halford SE (1995) Divalent metal ions at the active sites of the EcoRV and EcoRI restriction endonucleases. Biochemistry 34:697-704
63. Nowotny M, Gaidamakov SA, Crouch RJ, Yang W (2005) Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell 121:1005-1016
64. Pingoud V, Wende W, Friedhoff P, Reuter M, Alves J, Jeltsch A, Mones L, Fuxreiter M, Pingoud A (2009) On the divalent metal ion dependence of DNA cleavage by restriction endonucleases of the EcoRI family. J Mol Biol 393:140-160
65. Noble CG, Maxwell A (2002) The role of GyrB in the DNA cleavage-religation reaction of DNA gyrase: a proposed two metal-ion mechanism. J Mol Biol 318:361-371
66. 2+ binding sites in regulation of murine flap endonuclease-1 activities. Biochemistry 41:10323-10331
67. Dupureur CM (2010) One is enough: insights into the two-metal ion nuclease mechanism from global analysis and computational studies. Metallomics: integrated biometal science 2:609-620
68. Yang W (2011) Nucleases: diversity of structure, function and mechanism. Q Rev Biophys 44:1-93
69. He B, Qing H, Kow YW (2000) Deoxyxanthosine in DNA is repaired by Escherichia coli endonuclease V. Mutat Res 459:109-114
70. Feng H, Klutz AM, Cao W (2005) Active site plasticity of endonuclease V from Salmonella typhimurium. Biochemistry 44:675-683
71. Guo G, Weiss B (1998) Endonuclease V (nfi) mutant of Escherichia coli K-12. J Bacteriol 180:46-51
72. Lin J, Gao H, Schallhorn KA, Harris RM, Cao W, Ke PC (2007) Lesion recognition and cleavage by endonuclease V: a single-molecule study. Biochemistry 46:7132-7137
73. Mi R, Abole AK, Cao W (2011) Dissecting endonuclease and exonuclease activities in endonuclease V from Thermotoga maritima. Nucleic Acids Res 39:536-544
74. Liu J, He B, Qing H, Kow YW (2000) A deoxyinosine specific endonuclease from hyperthermophile. Archaeoglobus fulgidus: a homolog of Escherichia coli endonuclease V. Mutat Res 461:169-177
75. 6-alkylguanine- DNA alkyltransferase and endonuclease V activities. Proc Natl Acad Sci USA 102:3617-3622
76. Emptage K, O'Neill R, Solovyova A, Connolly BA (2008) Interplay between DNA polymerase and proliferating cell nuclear antigen switches off base excision repair of uracil and hypoxanthine during replication in archaea. J Mol Biol 383:762-771
77. Moe A, Ringvoll J, Nordstrand LM, Eide L, Bjoras M, Seeberg E, Rognes T, Klungland A (2003) Incision at hypoxanthine residues in DNA by a mammalian homologue of the Escherichia coli antimutator enzyme endonuclease V. Nucleic Acids Res 31:3893-3900
78. Schouten KA, Weiss B (1999) Endonuclease V protects Escherichia coli against specific mutations caused by nitrous acid. Mutat Res 435:245-254
79. Weiss B (2001) Endonuclease V of Escherichia coli prevents mutations from nitrosative deamination during nitrate/nitrite respiration. Mutat Res 461:301-309
80. Burgis NE, Brucker JJ, Cunningham RP (2003) Repair system for noncanonical purines in Escherichia coli. J Bacteriol 185:3101-3110
81. Lopez-Olmos K, Hernandez MP, Contreras-Garduno JA, Robleto EA, Setlow P, Yasbin RE, Pedraza-Reyes M (2012) Roles of endonuclease V, uracil-DNA glycosylase, and mismatch repair in Bacillus subtilis DNA base-deamination- induced mutagenesis. J Bacteriol 194:243-252
82. Bradshaw JS, Kuzminov A (2003) RdgB acts to avoid chromosome fragmentation in Escherichia coli. Mol Microbiol 48:1711-1725
83. Lee CC, Yang YC, Goodman SD, Yu YH, Lin SB, Kao JT, Tsai KS, Fang WH (2010) Endonuclease V-mediated deoxyinosine excision repair in vitro. DNA Repair 9:1073-1079
84. Weiss B (2008) Removal of deoxyinosine from the Escherichia coli chromosome as studied by oligonucleotide transformation. DNA Repair 7:205-212
85. Bazar L, Collier G, Vanek P, Siles B, Kow Y, Doetsch P, Cunningham R, Chirikjian J (1999) Mutation identification DNA analysis system (MIDAS) for detection of known mutations. Electrophoresis 20:1141-1148
86. Huang J, Kirk B, Favis R, Soussi T, Paty P, Cao W, Barany F (2002) An endonuclease/ligase based mutation scanning method especially suited for analysis of neoplastic tissue. Oncogene 21:1909-1921
87. Pincas H, Pingle MR, Huang J, Lao K, Paty PB, Friedman AM, Barany F (2004) High sensitivity EndoV mutation scanning through real-time ligase proofreading. Nucleic Acids Res 32:e148
88. Gao H, Huang J, Barany F, Cao W (2007) Switching base preferences of mismatch cleavage in endonuclease V: an improved method for scanning point mutations. Nucleic Acids Res 35:e2
89. Turner DJ, Pingle MR, Barany F (2006) Harnessing asymmetrical substrate recognition by thermostable EndoV to achieve balanced linear amplification in multiplexed SNP typing. Biochem Cell Biol (Biochimie et biologie cellulaire) 84:232-242
90. Miyazaki K (2002) Random DNA fragmentation with endonuclease V: application to DNA shuffling. Nucleic Acids Res 30:e139
91. Stemmer WP (1994) DNA shuffling by random fragmentation and reassembly: in vitro recombination for molecular evolution. Proc Natl Acad Sci USA 91:10747-10751
92. Stemmer WP (1994) Rapid evolution of a protein in vitro by DNA shuffling. Nature 370:389-391
93. Wang Z, Wang HY, Feng H (2012) A simple and reproducible method for directed evolution: combination of random mutation with dITP and DNA fragmentation with endonuclease V. Mol Biotechnol. doi: 10.1007/s12033-012-9516- 9