The HSV-1 Exonuclease, UL12, Stimulates Recombination by a Single Strand Annealing Mechanism

PLoS Pathogens

Volumn 8, Issue 8, 2012, Pages

  Schumacher, April J ^a   Mohni, Kareem N ^a   Kan, Yinan ^b   Hendrickson, Eric A ^b   Stark, Jeremy M ^c   Weller, Sandra K ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXONUCLEASE; INFECTED CELL PROTEIN 8; RAD52 PROTEIN; SINGLE STRAND ANNEALING PROTEIN; UL12 PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE LAMBDA; BACTERIOPHAGE T4; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA PACKAGING; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; GENE TARGETING; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SINGLE STRAND ANNEALING; VIRUS GENOME; VIRUS MUTANT;

DEOXYRIBONUCLEASES; DNA REPLICATION; DNA, SINGLE-STRANDED; DNA, VIRAL; DNA-BINDING PROTEINS; HEK293 CELLS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HOMOLOGOUS RECOMBINATION; HUMANS; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; VIRAL PROTEINS;

EUKARYOTA; HUMAN HERPESVIRUS 1; SIMPLEXVIRUS;

EID: 84866057096     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002862     Document Type: Article

References (106)

1. Brown SM, Ritchie DA, Subak-Sharpe JH, (1973) Genetic studies with herpes simplex virus type 1. The isolation of temperature-sensitive mutants, their arrangement into complementation groups and recombination analysis leading to a linkage map. J Gen Virol 18: 329-346.
2. Hayward GS, Jacob RJ, Wadsworth SC, Roizman B, (1975) Anatomy of herpes simplex virus DNA: evidence for four populations of molecules that differ in the relative orientations of their long and short components. Proc Natl Acad Sci U S A 72: 4243-4247.
3. Schaffer PA, Tevethia MJ, Benyesh-Melnick M, (1974) Recombination between temperature-sensitive mutants of herpes simplex virus type 1. Virology 58: 219-228.
4. Sheldrick P, Berthelot N, (1975) Inverted repetitions in the chromosome of herpes simplex virus. Cold Spring Harb Symp Quant Biol 39 Pt 2: 667-678.
5. Zhang X, Efstathiou S, Simmons A, (1994) Identification of novel herpes simplex virus replicative intermediates by field inversion gel electrophoresis: implications for viral DNA amplification strategies. Virology 202: 530-539.
6. Delius H, Clements JB, (1976) A partial denaturation map of herpes simplex virus type 1 DNA: evidence for inversions of the unique DNA regions. J Gen Virol 33: 125-133.
7. Dutch RE, Bianchi V, Lehman IR, (1995) Herpes simplex virus type 1 DNA replication is specifically required for high-frequency homologous recombination between repeated sequences. J Virol 69: 3084-3089.
8. Fu X, Wang H, Zhang X, (2002) High-frequency intermolecular homologous recombination during herpes simplex virus-mediated plasmid DNA replication. J Virol 76: 5866-5874.
9. Reuven NB, Staire AE, Myers RS, Weller SK, (2003) The herpes simplex virus type 1 alkaline nuclease and single-stranded DNA binding protein mediate strand exchange in vitro. J Virol 77: 7425-7433.
10. Reuven NB, Willcox S, Griffith JD, Weller SK, (2004) Catalysis of strand exchange by the HSV-1 UL12 and ICP8 proteins: potent ICP8 recombinase activity is revealed upon resection of dsDNA substrate by nuclease. J Mol Biol 342: 57-71.
11. Ellis HM, Yu D, DiTizio T, Court DL, (2001) High efficiency mutagenesis, repair, and engineering of chromosomal DNA using single-stranded oligonucleotides. Proc Natl Acad Sci U S A 98: 6742-6746.
12. Murphy KC, (1998) Use of bacteriophage lambda recombination functions to promote gene replacement in Escherichia coli. J Bacteriol 180: 2063-2071.
13. Court DL, Sawitzke JA, Thomason LC, (2002) Genetic engineering using homologous recombination. Annu Rev Genet 36: 361-388.
14. Muyrers JP, Zhang Y, Testa G, Stewart AF, (1999) Rapid modification of bacterial artificial chromosomes by ET-recombination. Nucleic Acids Res 27: 1555-1557.
15. Zhang Y, Buchholz F, Muyrers JP, Stewart AF, (1998) A new logic for DNA engineering using recombination in Escherichia coli. Nat Genet 20: 123-128.
16. Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, et al. (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci U S A 97: 5978-5983.
17. Szczepanska AK, (2009) Bacteriophage-encoded functions engaged in initiation of homologous recombination events. Crit Rev Microbiol 35: 197-220.
18. Lo Piano A, Martinez-Jimenez MI, Zecchi L, Ayora S, (2011) Recombination-dependent concatemeric viral DNA replication. Virus Res 160: 1-14.
19. Kuzminov A, (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63: 751-813 table of contents.
20. Wilkinson DE, Weller SK, (2003) The role of DNA recombination in herpes simplex virus DNA replication. IUBMB Life 55: 451-458.
21. Kass EM, Jasin M, (2010) Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett 584: 3703-3708.
22. Wyman C, Kanaar R, (2006) DNA double-strand break repair: all's well that ends well. Annu Rev Genet 40: 363-383.
23. Iyer LM, Koonin EV, Aravind L, (2002) Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52. BMC Genomics 3: 8.
24. Kawabata M, Kawabata T, Nishibori M, (2005) Role of recA/RAD51 family proteins in mammals. Acta Med Okayama 59: 1-9.
25. Singleton MR, Wentzell LM, Liu Y, West SC, Wigley DB, (2002) Structure of the single-strand annealing domain of human RAD52 protein. Proc Natl Acad Sci U S A 99: 13492-13497.
26. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M, (2004) Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol Cell Biol 24: 9305-9316.
27. Branzei D, Foiani M, (2008) Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol 9: 297-308.
28. Shrivastav M, De Haro LP, Nickoloff JA, (2008) Regulation of DNA double-strand break repair pathway choice. Cell Res 18: 134-147.
29. Harper JW, Elledge SJ, (2007) The DNA damage response: ten years after. Mol Cell 28: 739-745.
30. Lavin MF, Kozlov S, (2007) DNA damage-induced signalling in ataxia-telangiectasia and related syndromes. Radiother Oncol 83: 231-237.
31. DeFazio LG, Stansel RM, Griffith JD, Chu G, (2002) Synapsis of DNA ends by DNA-dependent protein kinase. EMBO J 21: 3192-3200.
32. Spagnolo L, Rivera-Calzada A, Pearl LH, Llorca O, (2006) Three-dimensional structure of the human DNA-PKcs/Ku70/Ku80 complex assembled on DNA and its implications for DNA DSB repair. Mol Cell 22: 511-519.
33. Valerie K, Povirk LF, (2003) Regulation and mechanisms of mammalian double-strand break repair. Oncogene 22: 5792-5812.
34. Mohni KN, Livingston CM, Cortez D, Weller SK, (2010) ATR and ATRIP are recruited to herpes simplex virus type 1 replication compartments even though ATR signaling is disabled. J Virol 84: 12152-12164.
35. Mohni KN, Mastrocola AS, Bai P, Weller SK, Heinen CD, (2011) DNA mismatch repair proteins are required for efficient herpes simplex virus 1 replication. J Virol 85: 12241-12253.
36. Gregory DA, Bachenheimer SL, (2008) Characterization of mre11 loss following HSV-1 infection. Virology 373: 124-136.
37. Lees-Miller SP, Long MC, Kilvert MA, Lam V, Rice SA, et al. (1996) Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0. J Virol 70: 7471-7477.
38. Lilley CE, Carson CT, Muotri AR, Gage FH, Weitzman MD, (2005) DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc Natl Acad Sci U S A 102: 5844-5849.
39. Taylor TJ, Knipe DM, (2004) Proteomics of herpes simplex virus replication compartments: association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J Virol 78: 5856-5866.
40. Wilcock D, Lane DP, (1991) Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells. Nature 349: 429-431.
41. Wilkinson DE, Weller SK, (2004) Recruitment of cellular recombination and repair proteins to sites of herpes simplex virus type 1 DNA replication is dependent on the composition of viral proteins within prereplicative sites and correlates with the induction of the DNA damage response. J Virol 78: 4783-4796.
42. Lilley CE, Chaurushiya MS, Boutell C, Everett RD, Weitzman MD, (2011) The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0. PLoS Pathog 7: e1002084.
43. Lilley CE, Chaurushiya MS, Boutell C, Landry S, Suh J, et al. (2010) A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J 29: 943-955.
44. Parkinson J, Lees-Miller SP, Everett RD, (1999) Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J Virol 73: 650-657.
45. Shirata N, Kudoh A, Daikoku T, Tatsumi Y, Fujita M, et al. (2005) Activation of ataxia telangiectasia-mutated DNA damage checkpoint signal transduction elicited by herpes simplex virus infection. J Biol Chem 280: 30336-30341.
46. Muylaert I, Elias P, (2007) Knockdown of DNA ligase IV/XRCC4 by RNA interference inhibits herpes simplex virus type I DNA replication. J Biol Chem 282: 10865-10872.
47. Pierce AJ, Johnson RD, Thompson LH, Jasin M, (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 13: 2633-2638.
48. Bennardo N, Cheng A, Huang N, Stark JM, (2008) Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 4: e1000110.
49. Severini A, Morgan AR, Tovell DR, Tyrrell DL, (1994) Study of the structure of replicative intermediates of HSV-1 DNA by pulsed-field gel electrophoresis. Virology 200: 428-435.
50. Goldstein DJ, Weller SK, (1988) lacZ insertional mutagen is used to demonstrate that the UL52 gene of herpes simplex virus type 1 is required for virus growth and DNA synthesis. J Virol 62: 2970-2977.
51. Lamberti C, Weller SK, (1998) The herpes simplex virus type 1 cleavage/packaging protein, UL32, is involved in efficient localization of capsids to replication compartments. J Virol 72: 2463-2473.
52. Lim SI, Min BE, Jung GY, (2008) Lagging strand-biased initiation of red recombination by linear double-stranded DNAs. J Mol Biol 384: 1098-1105.
53. Poteete AR, (2008) Involvement of DNA replication in phage lambda Red-mediated homologous recombination. Mol Microbiol 68: 66-74.
54. Stahl FW, McMilin KD, Stahl MM, Crasemann JM, Lam S, (1974) The distribution of crossovers along unreplicated lambda bacteriophage chromosomes. Genetics 77: 395-408.
55. Li Z, Karakousis G, Chiu SK, Reddy G, Radding CM, (1998) The beta protein of phage lambda promotes strand exchange. J Mol Biol 276: 733-744.
56. Muniyappa K, Radding CM, (1986) The homologous recombination system of phage lambda. Pairing activities of beta protein. J Biol Chem 261: 7472-7478.
57. Stahl MM, Thomason L, Poteete AR, Tarkowski T, Kuzminov A, et al. (1997) Annealing vs. invasion in phage lambda recombination. Genetics 147: 961-977.
58. Gao M, Knipe DM, (1989) Genetic evidence for multiple nuclear functions of the herpes simplex virus ICP8 DNA-binding protein. J Virol 63: 5258-5267.
59. Weller SK, Seghatoleslami MR, Shao L, Rowse D, Carmichael EP, (1990) The herpes simplex virus type 1 alkaline nuclease is not essential for viral DNA synthesis: isolation and characterization of a lacZ insertion mutant. J Gen Virol 71 (Pt 12): 2941-2952.
60. Nimonkar AV, Boehmer PE, (2002) In vitro strand exchange promoted by the herpes simplex virus type-1 single strand DNA-binding protein (ICP8) and DNA helicase-primase. J Biol Chem 277: 15182-15189.
61. Nimonkar AV, Boehmer PE, (2003) On the mechanism of strand assimilation by the herpes simplex virus type-1 single-strand DNA-binding protein (ICP8). Nucleic Acids Res 31: 5275-5281.
62. Balasubramanian N, Bai P, Buchek G, Korza G, Weller SK, (2010) Physical interaction between the herpes simplex virus type 1 exonuclease, UL12, and the DNA double-strand break-sensing MRN complex. J Virol 84: 12504-12514.
63. Thomas MS, Gao M, Knipe DM, Powell KL, (1992) Association between the herpes simplex virus major DNA-binding protein and alkaline nuclease. J Virol 66: 1152-1161.
64. Antrobus R, Grant K, Gangadharan B, Chittenden D, Everett RD, et al. (2009) Proteomic analysis of cells in the early stages of herpes simplex virus type-1 infection reveals widespread changes in the host cell proteome. Proteomics 9: 3913-3927.
65. Stark JM, Hu P, Pierce AJ, Moynahan ME, Ellis N, et al. (2002) ATP hydrolysis by mammalian RAD51 has a key role during homology-directed DNA repair. J Biol Chem 277: 20185-20194.
66. Goldstein JN, Weller SK, (1998) The exonuclease activity of HSV-1 UL12 is required for in vivo function. Virology 244: 442-457.
67. Shirasawa S, Furuse M, Yokoyama N, Sasazuki T, (1993) Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 260: 85-88.
68. Koi M, Umar A, Chauhan DP, Cherian SP, Carethers JM, et al. (1994) Human chromosome 3 corrects mismatch repair deficiency and microsatellite instability and reduces N-methyl-N′-nitro-N-nitrosoguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation. Cancer Res 54: 4308-4312.
69. Gunn A, Bennardo N, Cheng A, Stark JM, (2011) Correct End Use during End Joining of Multiple Chromosomal Double Strand Breaks Is Influenced by Repair Protein RAD50, DNA-dependent Protein Kinase DNA-PKcs, and Transcription Context. J Biol Chem 286: 42470-42482.
70. Brooks K, Clark AJ, (1967) Behavior of lambda bacteriophage in a recombination deficienct strain of Escherichia coli. J Virol 1: 283-293.
71. Echolas H, Gingery R, (1968) Mutants of bacteriophage lambda defective in vegetative genetic recombination. J Mol Biol 34: 239-249.
72. Franklin NC, (1967) Deletions and functions of the center of the phi80-lambda phage genome. Evidence for a phage function promoting genetic recombination. Genetics 57: 301-318.
73. Shulman MJ, Hallick LM, Echols H, Signer ER, (1970) Properties of recombination-deficient mutants of bacteriophage lambda. J Mol Biol 52: 501-520.
74. Signer ER, Weil J, (1968) Recombination in bacteriophage lambda. I. Mutants deficient in general recombination. J Mol Biol 34: 261-271.
75. van de Putte P, Zwenk H, Rorsch A, (1966) Properties of four mutants of Escherichia coli defective in genetic recombination. Mutat Res 3: 381-392.
76. Kulkarni AS, Fortunato EA, (2011) Stimulation of homology-directed repair at I-SceI-induced DNA breaks during the permissive life cycle of human cytomegalovirus. J Virol 85: 6049-6054.
77. Mimitou EP, Symington LS, (2009) DNA end resection: many nucleases make light work. DNA Repair (Amst) 8: 983-995.
78. Nimonkar AV, Genschel J, Kinoshita E, Polaczek P, Campbell JL, et al. (2011) BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev 25: 350-362.
79. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, et al. (2007) Human CtIP promotes DNA end resection. Nature 450: 509-514.
80. de Wind N, Dekker M, Berns A, Radman M, te Riele H, (1995) Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell 82: 321-330.
81. Lyndaker AM, Alani E, (2009) A tale of tails: insights into the coordination of 3′ end processing during homologous recombination. Bioessays 31: 315-321.
82. Sugawara N, Paques F, Colaiacovo M, Haber JE, (1997) Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination. Proc Natl Acad Sci U S A 94: 9214-9219.
83. Jacob RJ, Roizman B, (1977) Anatomy of herpes simplex virus DNA VIII. Properties of the replicating DNA. J Virol 23: 394-411.
84. RW HY, Oakes JE, Kudler L, (1977) In vitro repair of the preexisting nicks and gaps in herpes simplex virus DNA. Virology 76: 286-294.
85. Bataille D, Epstein A, (1994) Herpes simplex virus replicative concatemers contain L components in inverted orientation. Virology 203: 384-388.
86. Bataille D, Epstein AL, (1997) Equimolar generation of the four possible arrangements of adjacent L components in herpes simplex virus type 1 replicative intermediates. J Virol 71: 7736-7743.
87. Sarisky RT, Weber PC, (1994) Requirement for double-strand breaks but not for specific DNA sequences in herpes simplex virus type 1 genome isomerization events. J Virol 68: 34-47.
88. Rybalchenko N, Golub EI, Bi B, Radding CM, (2004) Strand invasion promoted by recombination protein beta of coliphage lambda. Proc Natl Acad Sci U S A 101: 17056-17060.
89. Maresca M, Erler A, Fu J, Friedrich A, Zhang Y, et al. (2010) Single-stranded heteroduplex intermediates in lambda Red homologous recombination. BMC Mol Biol 11: 54.
90. Mosberg JA, Lajoie MJ, Church GM, (2010) Lambda red recombineering in Escherichia coli occurs through a fully single-stranded intermediate. Genetics 186: 791-799.
91. Bujnicki JM, Rychlewski L, (2001) The herpesvirus alkaline exonuclease belongs to the restriction endonuclease PD-(D/E)XK superfamily: insight from molecular modeling and phylogenetic analysis. Virus Genes 22: 219-230.
92. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
93. Murphy KC, Campellone KG, Poteete AR, (2000) PCR-mediated gene replacement in Escherichia coli. Gene 246: 321-330.
94. Muyrers JP, Zhang Y, Stewart AF, (2001) Techniques: Recombinogenic engineering-new options for cloning and manipulating DNA. Trends Biochem Sci 26: 325-331.
95. Campbell A, (1994) Comparative molecular biology of lambdoid phages. Annu Rev Microbiol 48: 193-222.
96. Bowden R, Sakaoka H, Donnelly P, Ward R, (2004) High recombination rate in herpes simplex virus type 1 natural populations suggests significant co-infection. Infect Genet Evol 4: 115-123.
97. Muylkens B, Farnir F, Meurens F, Schynts F, Vanderplasschen A, et al. (2009) Coinfection with two closely related alphaherpesviruses results in a highly diversified recombination mosaic displaying negative genetic interference. J Virol 83: 3127-3137.
98. Thiry E, Meurens F, Muylkens B, McVoy M, Gogev S, et al. (2005) Recombination in alphaherpesviruses. Rev Med Virol 15: 89-103.
99. Norberg P, Kasubi MJ, Haarr L, Bergstrom T, Liljeqvist JA, (2007) Divergence and recombination of clinical herpes simplex virus type 2 isolates. J Virol 81: 13158-13167.
100. Topaloglu O, Hurley PJ, Yildirim O, Civin CI, Bunz F, (2005) Improved methods for the generation of human gene knockout and knockin cell lines. Nucleic Acids Res 33: e158.
101. Goldstein JN, Weller SK, (1998) In vitro processing of herpes simplex virus type 1 DNA replication intermediates by the viral alkaline nuclease, UL12. J Virol 72: 8772-8781.
102. Reuven NB, Antoku S, Weller SK, (2004) The UL12.5 gene product of herpes simplex virus type 1 exhibits nuclease and strand exchange activities but does not localize to the nucleus. J Virol 78: 4599-4608.
103. Richardson C, Moynahan ME, Jasin M, (1998) Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev 12: 3831-3842.
104. Fattah F, Lee EH, Weisensel N, Wang Y, Lichter N, et al. (2010) Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells. PLoS Genet 6: e1000855.
105. Heilbronn R, zur Hausen H, (1989) A subset of herpes simplex virus replication genes induces DNA amplification within the host cell genome. J Virol 63: 3683-3692.
106. Livingston CM, DeLuca NA, Wilkinson DE, Weller SK, (2008) Oligomerization of ICP4 and rearrangement of heat shock proteins may be important for herpes simplex virus type 1 prereplicative site formation. J Virol 82: 6324-6336.