1932

Abstract

Helicases are enzymes that move, manage, and manipulate nucleic acids. They can be subdivided into six super families and are required for all aspects of nucleic acid metabolism. In general, all helicases function by converting the chemical energy stored in the bond between the gamma and beta phosphates of adenosine triphosphate into mechanical work, which results in the unidirectional movement of the helicase protein along one strand of a nucleic acid. The results of this translocation activity can range from separation of strands within duplex nucleic acids to the physical remodeling or removal of nucleoprotein complexes. In this review, we focus on describing key helicases from the model organism that contribute to the regulation of homologous recombination, which is an essential DNA repair pathway for fixing damaged chromosomes.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-052118-115418
2019-05-06
2024-06-17
Loading full text...

Full text loading...

/deliver/fulltext/biophys/48/1/annurev-biophys-052118-115418.html?itemId=/content/journals/10.1146/annurev-biophys-052118-115418&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Aguilera A, Klein HL 1988. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic characterization of hyper-recombination mutations. Genetics 119:779–90
    [Google Scholar]
  2. 2.
    Alexeev A, Mazin A, Kowalczykowski SC 2003. Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat. Struct. Mol. Biol. 10:182–86
    [Google Scholar]
  3. 3.
    Alexiadis V, Kadonaga JT 2002. Strand pairing by Rad54 and Rad51 is enhanced by chromatin. Genes Dev 16:2767–71
    [Google Scholar]
  4. 4.
    Amitani I, Baskin RJ, Kowalczykowski SC 2006. Visualization of Rad54, a chromatin remodeling protein, translocating on single DNA molecules. Mol. Cell 23:143–48
    [Google Scholar]
  5. 5.
    Antony E, Tomko EJ, Xiao Q, Krejci L, Lohman TM, Ellenberger T 2009. Srs2 disassembles Rad51 filaments by a protein-protein interaction triggering ATP turnover and dissociation of Rad51 from DNA. Mol. Cell 35:105–15
    [Google Scholar]
  6. 6.
    Arora H, Chacon AH, Choudhary S, McLeod MP, Meshkov L et al. 2014. Bloom syndrome. Int. J. Dermatol. 53:798–802
    [Google Scholar]
  7. 7.
    Banerjee S, Smith S, Oum JH, Liaw HJ, Hwang JY et al. 2008. Mph1p promotes gross chromosomal rearrangement through partial inhibition of homologous recombination. J. Cell Biol. 181:1083–93
    [Google Scholar]
  8. 8.
    Bell JC, Plank JL, Dombrowski CC, Kowalczykowski SC 2012. Direct imaging of RecA nucleation and growth on single molecules of SSB-coated ssDNA. Nature 491:274–78
    [Google Scholar]
  9. 9.
    Bennett RJ, Keck JL, Wang JC 1999. Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J. Mol. Biol 289:235–48
    [Google Scholar]
  10. 10.
    Bennett RJ, Sharp JA, Wang JC 1998. Purification and characterization of the Sgs1 DNA helicase activity of Saccharomyces cerevisiae. J. Biol. Chem 273:9644–50
    [Google Scholar]
  11. 11.
    Bernstein KA, Gangloff S, Rothstein R 2010. The RecQ DNA helicases in DNA repair. Annu. Rev. Genet. 44:393–417
    [Google Scholar]
  12. 12.
    Bernstein KA, Reid RJ, Sunjevaric I, Demuth K, Burgess RC, Rothstein R 2011. The Shu complex, which contains Rad51 paralogues, promotes DNA repair through inhibition of the Srs2 anti-recombinase. Mol. Biol. Cell 22:1599–607
    [Google Scholar]
  13. 13.
    Bianco PR, Tracy RB, Kowalczykowski SC 1998. DNA strand exchange proteins: a biochemical and physical comparison. Front. Biosci. 3:D570–603
    [Google Scholar]
  14. 14.
    Bizard AH, Hickson ID 2014. The dissolution of double Holliday junctions. Cold Spring Harb. Perspect. Biol. 6:a016477
    [Google Scholar]
  15. 15.
    Bloom D 1954. Congenital telangiectatic erythema resembling lupus erythematosus in dwarfs. Probably a syndrome entity. AMA Am. J. Dis. Child 88:754–58
    [Google Scholar]
  16. 16.
    Bogliolo M, Surralles J 2015. Fanconi anemia: a model disease for studies on human genetics and advanced therapeutics. Curr. Opin. Genet. Dev. 33:32–40
    [Google Scholar]
  17. 17.
    Branzei D, Foiani M 2007. RecQ helicases queuing with Srs2 to disrupt Rad51 filaments and suppress recombination. Genes Dev 21:3019–26
    [Google Scholar]
  18. 18.
    Branzei D, Szakal B 2017. Building up and breaking down: mechanisms controlling recombination during replication. Crit. Rev. Biochem. Mol. Biol. 52:381–94
    [Google Scholar]
  19. 19.
    Brosh RM Jr 2013. DNA helicases involved in DNA repair and their roles in cancer. Nat. Rev. Cancer 13:542–58
    [Google Scholar]
  20. 20.
    Brosh RM Jr, Bohr VA 2007. Human premature aging, DNA repair and RecQ helicases. Nucleic Acids Res 35:7527–44
    [Google Scholar]
  21. 21.
    Brown MS, Bishop DK 2014. DNA strand exchange and RecA homologs in meiosis. Cold Spring Harb. Perspect. Biol. 7:a016659
    [Google Scholar]
  22. 22.
    Bugreev DV, Brosh RM Jr, Mazin AV 2008. RECQ1 possesses DNA branch migration activity. J. Biol. Chem. 283:20231–42
    [Google Scholar]
  23. 23.
    Bugreev DV, Hanaoka F, Mazin AV 2007. Rad54 dissociates homologous recombination intermediates by branch migration. Nat. Struct. Mol. Biol. 14:746–53
    [Google Scholar]
  24. 24.
    Bugreev DV, Mazina OM, Mazin AV 2006. Rad54 protein promotes branch migration of Holliday junctions. Nature 442:590–93
    [Google Scholar]
  25. 25.
    Burgess RC, Lisby M, Altmannova V, Krejci L, Sung P, Rothstein R 2009. Localization of recombination proteins and Srs2 reveals anti-recombinase function in vivo. J. Cell Biol. 185:969–81
    [Google Scholar]
  26. 26.
    Busygina V, Saro D, Williams G, Leung WK, Say AF et al. 2012. Novel attributes of Hed1 affect dynamics and activity of the Rad51 presynaptic filament during meiotic recombination. J. Biol. Chem. 287:1566–75
    [Google Scholar]
  27. 27.
    Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, Sung P 2008. Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev 22:786–95
    [Google Scholar]
  28. 28.
    Campbell MB, Campbell WC, Rogers J, Rogers N, Rogers Z et al. 2018. Bloom syndrome: research and data priorities for the development of precision medicine as identified by some affected families. Cold Spring Harb. Mol. Case Stud. 4:a002816
    [Google Scholar]
  29. 29.
    Ceballos SJ, Heyer WD 2011. Functions of the Snf2/Swi2 family Rad54 motor protein in homologous recombination. Biochim. Biophys. Acta 1809:509–23
    [Google Scholar]
  30. 30.
    Cejka P, Cannavo E, Polaczek P, Masuda-Sasa T, Pokharel S et al. 2010. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467:112–16
    [Google Scholar]
  31. 31.
    Cejka P, Kowalczykowski SC 2010. The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds Holliday junctions. J. Biol. Chem. 285:8290–301
    [Google Scholar]
  32. 32.
    Chen R, Wold MS 2014. Replication protein A: single-stranded DNA's first responder: dynamic DNA-interactions allow replication protein A to direct single-strand DNA intermediates into different pathways for synthesis or repair. BioEssays 36:1156–61
    [Google Scholar]
  33. 33.
    Chester N, Kuo F, Kozak C, O'Hara CD, Leder P 1998. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev 12:3382–93
    [Google Scholar]
  34. 34.
    Chi P, Kwon Y, Seong C, Epshtein A, Lam I et al. 2006. Yeast recombination factor Rdh54 functionally interacts with the Rad51 recombinase and catalyzes Rad51 removal from DNA. J. Biol. Chem. 281:26268–79
    [Google Scholar]
  35. 35.
    Chu WK, Hickson ID 2009. RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer 9:644–54
    [Google Scholar]
  36. 36.
    Constantinou A, Tarsounas M, Karow JK, Brosh RM, Bohr VA et al. 2000. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep 1:80–84
    [Google Scholar]
  37. 37.
    Crickard JB, Kaniecki K, Kwon Y, Sung P, Greene EC 2018. Meiosis-specific recombinase Dmc1 is a potent inhibitor of the Srs2 antirecombinase. PNAS 115:E10041–48
    [Google Scholar]
  38. 38.
    Crickard JB, Kaniecki K, Kwon Y, Sung P, Lisby M, Greene EC 2018. Regulation of Hed1 and Rad54 binding during maturation of the meiosis-specific presynaptic complex. EMBO J 37:e98728
    [Google Scholar]
  39. 39.
    Croteau DL, Popuri V, Opresko PL, Bohr VA 2014. Human RecQ helicases in DNA repair, recombination, and replication. Annu. Rev. Biochem. 83:519–52
    [Google Scholar]
  40. 40.
    Daley JM, Niu H, Miller AS, Sung P 2015. Biochemical mechanism of DSB end resection and its regulation. DNA Repair 32:66–74
    [Google Scholar]
  41. 41.
    De Tullio L, Kaniecki K, Kwon Y, Crickard JB, Sung P, Greene EC 2017. Yeast Srs2 helicase promotes redistribution of single-stranded DNA-bound RPA and Rad52 in homologous recombination regulation. Cell Rep 21:570–77
    [Google Scholar]
  42. 42.
    Deans B, Griffin CS, Maconochie M, Thacker J 2000. Xrcc2 is required for genetic stability, embryonic neurogenesis and viability in mice. EMBO J 19:6675–85
    [Google Scholar]
  43. 43.
    Elango R, Sheng Z, Jackson J, DeCata J, Ibrahim Y et al. 2017. Break-induced replication promotes formation of lethal joint molecules dissolved by Srs2. Nat. Commun. 8:1790
    [Google Scholar]
  44. 44.
    Ellis NA, Groden J, Ye TZ, Straughen J, Lennon DJ et al. 1995. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83:655–66
    [Google Scholar]
  45. 45.
    Feng Z, Scott SP, Bussen W, Sharma GG, Guo G et al. 2011. Rad52 inactivation is synthetically lethal with BRCA2 deficiency. PNAS 108:686–91
    [Google Scholar]
  46. 46.
    Fortin GS, Symington LS 2002. Mutations in yeast Rad51 that partially bypass the requirement for Rad55 and Rad57 in DNA repair by increasing the stability of Rad51-DNA complexes. EMBO J 21:3160–70
    [Google Scholar]
  47. 47.
    Fung CW, Fortin GS, Peterson SE, Symington LS 2006. The rad51-K191R ATPase-defective mutant is impaired for presynaptic filament formation. Mol. Cell. Biol. 26:9544–54
    [Google Scholar]
  48. 48.
    Galletto R, Amitani I, Baskin RJ, Kowalczykowski SC 2006. Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443:875–78
    [Google Scholar]
  49. 49.
    German J 1997. Bloom's syndrome. XX. The first 100 cancers. Cancer Genet. Cytogenet. 93:100–6
    [Google Scholar]
  50. 50.
    German J, Archibald R, Bloom D 1965. Chromosomal breakage in a rare and probably genetically determined syndrome of man. Science 148:506–7
    [Google Scholar]
  51. 51.
    German J, Sanz MM, Ciocci S, Ye TZ, Ellis NA 2007. Syndrome-causing mutations of the BLM gene in persons in the Bloom's Syndrome Registry. Hum. Mutat. 28:743–53
    [Google Scholar]
  52. 52.
    Gibb B, Ye LF, Gergoudis SC, Kwon Y, Niu H et al. 2014. Concentration-dependent exchange of replication protein A on single-stranded DNA revealed by single-molecule imaging. PLOS ONE 9:e87922
    [Google Scholar]
  53. 53.
    Gibb B, Ye LF, Kwon Y, Niu H, Sung P, Greene EC 2014. Protein dynamics during presynaptic-complex assembly on individual single-stranded DNA molecules. Nat. Struct. Mol. Biol. 21:893–900
    [Google Scholar]
  54. 54.
    Godin S, Wier A, Kabbinavar F, Bratton-Palmer DS, Ghodke H et al. 2013. The Shu complex interacts with Rad51 through the Rad51 paralogues Rad55-Rad57 to mediate error-free recombination. Nucleic Acids Res 41:4525–34
    [Google Scholar]
  55. 55.
    Ha T, Kozlov AG, Lohman TM 2012. Single-molecule views of protein movement on single-stranded DNA. Annu. Rev. Biophys. 41:295–319
    [Google Scholar]
  56. 56.
    Heyer WD, Li X, Rolfsmeier M, Zhang XP 2006. Rad54: the Swiss Army knife of homologous recombination?. Nucleic Acids Res 34:4115–25
    [Google Scholar]
  57. 57.
    Holzen TM, Shah PP, Olivares HA, Bishop DK 2006. Tid1/Rdh54 promotes dissociation of Dmc1 from nonrecombinogenic sites on meiotic chromatin. Genes Dev 20:2593–604
    [Google Scholar]
  58. 58.
    Hunter N 2015. Meiotic recombination: the essence of heredity. Cold Spring Harb. Perspect. Biol. 7:a016618
    [Google Scholar]
  59. 59.
    Ira G, Malkova A, Liberi G, Foiani M, Haber JE 2003. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115:401–11
    [Google Scholar]
  60. 60.
    Jasin M, Rothstein R 2013. Repair of strand breaks by homologous recombination. Cold Spring Harb. Perspect. Biol. 5:a012740
    [Google Scholar]
  61. 61.
    Johnson DS, Bai L, Smith BY, Patel SS, Wang MD 2007. Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase. Cell 129:1299–309
    [Google Scholar]
  62. 62.
    Kang YH, Munashingha PR, Lee CH, Nguyen TA, Seo YS 2012. Biochemical studies of the Saccharomyces cerevisiae Mph1 helicase on junction-containing DNA structures. Nucleic Acids Res 40:2089–106
    [Google Scholar]
  63. 63.
    Kaniecki K, De Tullio L, Gibb B, Kwon Y, Sung P, Greene EC 2017. Dissociation of Rad51 presynaptic complexes and heteroduplex DNA joints by tandem assemblies of Srs2. Cell Rep 21:3166–77
    [Google Scholar]
  64. 64.
    Karow JK, Constantinou A, Li JL, West SC, Hickson ID 2000. The Bloom's syndrome gene product promotes branch migration of Holliday junctions. PNAS 97:6504–8
    [Google Scholar]
  65. 65.
    Kass EM, Moynahan ME, Jasin M 2016. When genome maintenance goes badly awry. Mol. Cell 62:777–87
    [Google Scholar]
  66. 66.
    Keeney S, Lange J, Mohibullah N 2014. Self-organization of meiotic recombination initiation: general principles and molecular pathways. Annu. Rev. Genet. 48:187–214
    [Google Scholar]
  67. 67.
    Kowalczykowski SC 2015. An overview of the molecular mechanisms of recombinational DNA repair. Cold Spring Harb. Perspect. Biol. 7:016410
    [Google Scholar]
  68. 68.
    Krejci L, Van Komen S, Li Y, Villemain J, Reddy MS et al. 2003. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305–9
    [Google Scholar]
  69. 69.
    Kuznetsov SG, Haines DC, Martin BK, Sharan SK 2009. Loss of Rad51c leads to embryonic lethality and modulation of Trp53-dependent tumorigenesis in mice. Cancer Res 69:863–72
    [Google Scholar]
  70. 70.
    Kwon Y, Seong C, Chi P, Greene EC, Klein H, Sung P 2008. ATP-dependent chromatin remodeling by the Saccharomyces cerevisiae homologous recombination factor Rdh54. J. Biol. Chem. 283:10445–52
    [Google Scholar]
  71. 71.
    Larsen NB, Hickson ID 2013. RecQ helicases: conserved guardians of genomic integrity. Adv. Exp. Med. Biol. 767:161–84
    [Google Scholar]
  72. 72.
    Lee JY, Yang W 2006. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127:1349–60
    [Google Scholar]
  73. 73.
    Liberi G, Maffioletti G, Lucca C, Chiolo I, Baryshnikova A et al. 2005. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev 19:339–50
    [Google Scholar]
  74. 74.
    Lim DS, Hasty P 1996. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16:7133–43
    [Google Scholar]
  75. 75.
    Lindsley JE, Cox MM 1989. Dissociation pathway for recA nucleoprotein filaments formed on linear duplex DNA. J. Mol. Biol. 205:695–711
    [Google Scholar]
  76. 76.
    Liu J, Renault L, Veaute X, Fabre F, Stahlberg H, Heyer WD 2011. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 479:245–48
    [Google Scholar]
  77. 77.
    Lohman TM, Tomko EJ, Wu CG 2008. Non-hexameric DNA helicases and translocases: mechanisms and regulation. Nat. Rev. Mol. Cell Biol. 9:391–401
    [Google Scholar]
  78. 78.
    Lok BH, Carley AC, Tchang B, Powell SN 2013. RAD52 inactivation is synthetically lethal with deficiencies in BRCA1 and PALB2 in addition to BRCA2 through RAD51-mediated homologous recombination. Oncogene 32:3552–58
    [Google Scholar]
  79. 79.
    Lorenz A 2017. Modulation of meiotic homologous recombination by DNA helicases. Yeast 34:195–203
    [Google Scholar]
  80. 80.
    Marini V, Krejci L 2010. Srs2: the “Odd-Job Man” in DNA repair. DNA Repair 9:268–75
    [Google Scholar]
  81. 81.
    Martino J, Bernstein KA 2016. The Shu complex is a conserved regulator of homologous recombination. FEMS Yeast Res 16:fow073
    [Google Scholar]
  82. 82.
    Mason JM, Dusad K, Wright WD, Grubb J, Budke B et al. 2015. RAD54 family translocases counter genotoxic effects of RAD51 in human tumor cells. Nucleic Acids Res 43:3180–96
    [Google Scholar]
  83. 83.
    Mazin AV, Alexeev AA, Kowalczykowski SC 2003. A novel function of Rad54 protein. Stabilization of the Rad51 nucleoprotein filament. J. Biol. Chem. 278:14029–36
    [Google Scholar]
  84. 84.
    Mazin AV, Bornarth CJ, Solinger JA, Heyer WD, Kowalczykowski SC 2000. Rad54 protein is targeted to pairing loci by the Rad51 nucleoprotein filament. Mol. Cell 6:583–92
    [Google Scholar]
  85. 85.
    Mazin AV, Mazina OM, Bugreev DV, Rossi MJ 2010. Rad54, the motor of homologous recombination. DNA Repair 9:286–302
    [Google Scholar]
  86. 86.
    McCarthy EE, Celebi JT, Baer R, Ludwig T 2003. Loss of Bard1, the heterodimeric partner of the Brca1 tumor suppressor, results in early embryonic lethality and chromosomal instability. Mol. Cell. Biol. 23:5056–63
    [Google Scholar]
  87. 87.
    Mehta A, Haber JE 2014. Sources of DNA double-strand breaks and models of recombinational DNA repair. Cold Spring Harb. Perspect. Biol. 6:a016428
    [Google Scholar]
  88. 88.
    Menetski JP, Kowalczykowski SC 1985. Interaction of recA protein with single-stranded DNA. Quantitative aspects of binding affinity modulation by nucleotide cofactors. J. Mol. Biol. 181:281–95
    [Google Scholar]
  89. 89.
    Morrical SW 2015. DNA-pairing and annealing processes in homologous recombination and homology-directed repair. Cold Spring Harb. Perspect. Biol. 7:a016444
    [Google Scholar]
  90. 90.
    Morrison C, Shinohara A, Sonoda E, Yamaguchi-Iwai Y, Takata M et al. 1999. The essential functions of human Rad51 are independent of ATP hydrolysis. Mol. Cell. Biol. 19:6891–97
    [Google Scholar]
  91. 91.
    Myong S, Bruno MM, Pyle AM, Ha T 2007. Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase. Science 317:513–16
    [Google Scholar]
  92. 92.
    Myong S, Cui S, Cornish PV, Kirchhofer A, Gack MU et al. 2009. Cytosolic viral sensor RIG-I is a 5′-triphosphate-dependent translocase on double-stranded RNA. Science 323:1070–74
    [Google Scholar]
  93. 93.
    Myong S, Rasnik I, Joo C, Lohman TM, Ha T 2005. Repetitive shuttling of a motor protein on DNA. Nature 437:1321–25
    [Google Scholar]
  94. 94.
    Neale MJ, Keeney S 2006. Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442:153–58
    [Google Scholar]
  95. 95.
    Nimonkar AV, Amitani I, Baskin RJ, Kowalczykowski SC 2007. Single molecule imaging of Tid1/Rdh54, a Rad54 homolog that translocates on duplex DNA and can disrupt joint molecules. J. Biol. Chem. 282:30776–84
    [Google Scholar]
  96. 96.
    Nimonkar AV, Dombrowski CC, Siino JS, Stasiak AZ, Stasiak A, Kowalczykowski SC 2012. Saccharomyces cerevisiae Dmc1 and Rad51 proteins preferentially function with Tid1 and Rad54 proteins, respectively, to promote DNA strand invasion during genetic recombination. J. Biol. Chem. 287:28727–37
    [Google Scholar]
  97. 97.
    Niu H, Chung WH, Zhu Z, Kwon Y, Zhao W et al. 2010. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. . Nature 467:108–11
    [Google Scholar]
  98. 98.
    Niu H, Klein HL 2017. Multifunctional roles of Saccharomyces cerevisiae Srs2 protein in replication, recombination and repair. FEMS Yeast Res 17:fow111
    [Google Scholar]
  99. 99.
    Niu H, Wan L, Busygina V, Kwon Y, Allen JA et al. 2009. Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol. Cell 36:393–404
    [Google Scholar]
  100. 100.
    Palladino F, Klein HL 1992. Analysis of mitotic and meiotic defects in Saccharomyces cerevisiae SRS2 DNA helicase mutants. Genetics 132:23–37
    [Google Scholar]
  101. 101.
    Paques F, Haber JE 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev 63:349–404
    [Google Scholar]
  102. 102.
    Park J, Myong S, Niedziela-Majka A, Lee KS, Yu J et al. 2010. PcrA helicase dismantles RecA filaments by reeling in DNA in uniform steps. Cell 142:544–55
    [Google Scholar]
  103. 103.
    Piazza A, Wright WD, Heyer WD 2017. Multi-invasions are recombination byproducts that induce chromosomal rearrangements. Cell 170:760–73.e15
    [Google Scholar]
  104. 104.
    Pittman DL, Schimenti JC 2000. Midgestation lethality in mice deficient for the RecA-related gene, Rad51d/Rad51l3. Genesis 26:167–73
    [Google Scholar]
  105. 105.
    Prakash R, Krejci L, Van Komen S, Anke Schurer K, Kramer W, Sung P 2005. Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 3′ to 5′ DNA helicase. J. Biol. Chem. 280:7854–60
    [Google Scholar]
  106. 106.
    Prakash R, Satory D, Dray E, Papusha A, Scheller J et al. 2009. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev 23:67–79
    [Google Scholar]
  107. 107.
    Prakash R, Zhang Y, Feng W, Jasin M 2015. Homologous recombination and human health: the roles of BRCA1, BRCA2, and associated proteins. Cold Spring Harb. Perspect. Biol. 7:a016600
    [Google Scholar]
  108. 108.
    Prasad TK, Robertson RB, Visnapuu ML, Chi P, Sung P, Greene EC 2007. A DNA-translocating Snf2 molecular motor: Saccharomyces cerevisiae Rdh54 displays processive translocation and extrudes DNA loops. J. Mol. Biol. 369:940–53
    [Google Scholar]
  109. 109.
    Pyle AM 2008. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu. Rev. Biophys. 37:317–36
    [Google Scholar]
  110. 110.
    Qiu Y, Antony E, Doganay S, Koh HR, Lohman TM, Myong S 2013. Srs2 prevents Rad51 filament formation by repetitive motion on DNA. Nat. Commun. 4:2281
    [Google Scholar]
  111. 111.
    Ristic D, Wyman C, Paulusma C, Kanaar R 2001. The architecture of the human Rad54-DNA complex provides evidence for protein translocation along DNA. PNAS 98:8454–60
    [Google Scholar]
  112. 112.
    Rong L, Klein HL 1993. Purification and characterization of the SRS2 DNA helicase of the yeast Saccharomyces cerevisiae. J. Biol. Chem 268:1252–59
    [Google Scholar]
  113. 113.
    Rong L, Palladino F, Aguilera A, Klein HL 1991. The hyper-gene conversion hpr5-1 mutation of Saccharomyces cerevisiae is an allele of the SRS2/RADH gene. Genetics 127:75–85
    [Google Scholar]
  114. 114.
    Sasanuma H, Furihata Y, Shinohara M, Shinohara A 2013. Remodeling of the Rad51 DNA strand-exchange protein by the Srs2 helicase. Genetics 194:859–72
    [Google Scholar]
  115. 115.
    Scheller J, Schurer A, Rudolph C, Hettwer S, Kramer W 2000. MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics 155:1069–81
    [Google Scholar]
  116. 116.
    Seki M, Otsuki M, Ishii Y, Tada S, Enomoto T 2008. RecQ family helicases in genome stability: lessons from gene disruption studies in DT40 cells. Cell Cycle 7:2472–78
    [Google Scholar]
  117. 117.
    Shah PP, Zheng X, Epshtein A, Carey JN, Bishop DK, Klein HL 2010. Swi2/Snf2-related translocases prevent accumulation of toxic Rad51 complexes during mitotic growth. Mol. Cell 39:862–72
    [Google Scholar]
  118. 118.
    Sharan SK, Morimatsu M, Albrecht U, Lim DS, Regel E et al. 1997. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. . Nature 386:804–10
    [Google Scholar]
  119. 119.
    Shu Z, Smith S, Wang L, Rice MC, Kmiec EB 1999. Disruption of muREC2/RAD51L1 in mice results in early embryonic lethality which can be partially rescued in a p53−/− background. Mol. Cell. Biol. 19:8686–93
    [Google Scholar]
  120. 120.
    Singleton MR, Dillingham MS, Wigley DB 2007. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76:23–50
    [Google Scholar]
  121. 121.
    Singleton MR, Wigley DB 2002. Modularity and specialization in superfamily 1 and 2 helicases. J. Bacteriol. 184:1819–26
    [Google Scholar]
  122. 122.
    Sonoda E, Sasaki MS, Buerstedde JM, Bezzubova O, Shinohara A et al. 1998. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J 17:598–608
    [Google Scholar]
  123. 123.
    Soultanas P, Wigley DB 2000. DNA helicases: ‘inching forward. .’ Curr. Opin. Struct. Biol. 10:124–28
    [Google Scholar]
  124. 124.
    Sung P, Stratton SA 1996. Yeast Rad51 recombinase mediates polar DNA strand exchange in the absence of ATP hydrolysis. J. Biol. Chem. 271:27983–86
    [Google Scholar]
  125. 125.
    Symington LS 2014. End resection at double-strand breaks: mechanism and regulation. Cold Spring Harb. Perspect. Biol. 6:a016436
    [Google Scholar]
  126. 126.
    Symington LS, Gautier J 2011. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45:247–71
    [Google Scholar]
  127. 127.
    Symington LS, Rothstein R, Lisby M 2014. Mechanisms and regulation of mitotic recombination in Saccharomyces cerevisiae. . Genetics 198:795–835
    [Google Scholar]
  128. 128.
    Tan TL, Kanaar R, Wyman C 2003. Rad54, a Jack of all trades in homologous recombination. DNA Repair 2:787–94
    [Google Scholar]
  129. 129.
    Tomko EJ, Jia H, Park J, Maluf NK, Ha T, Lohman TM 2010. 5′-Single-stranded/duplex DNA junctions are loading sites for E. coli UvrD translocase. EMBO J 29:3826–39
    [Google Scholar]
  130. 130.
    Tsubouchi H, Roeder GS 2006. Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev 20:1766–75
    [Google Scholar]
  131. 131.
    Tsuzuki T, Fujii Y, Sakumi K, Tominaga Y, Nakao K et al. 1996. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. PNAS 93:6236–40
    [Google Scholar]
  132. 132.
    Van Komen S, Reddy MS, Krejci L, Klein H, Sung P 2003. ATPase and DNA helicase activities of the Saccharomyces cerevisiae anti-recombinase Srs2. J. Biol. Chem. 278:44331–37
    [Google Scholar]
  133. 133.
    van Mameren J, Modesti M, Kanaar R, Wyman C, Peterman EJ, Wuite GJ 2009. Counting RAD51 proteins disassembling from nucleoprotein filaments under tension. Nature 457:745–48
    [Google Scholar]
  134. 134.
    Veaute X, Jeusset J, Soustelle C, Kowalczykowski SC, Le Cam E, Fabre F 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309–12
    [Google Scholar]
  135. 135.
    Velankar SS, Soultanas P, Dillingham MS, Subramanya HS, Wigley DB 1999. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97:75–84
    [Google Scholar]
  136. 136.
    West SC, Blanco MG, Chan YW, Matos J, Sarbajna S, Wyatt HD 2015. Resolution of recombination intermediates: mechanisms and regulation. Cold Spring Harb. Symp. Quant. Biol. 80:103–9
    [Google Scholar]
  137. 137.
    Whitby MC 2010. The FANCM family of DNA helicases/translocases. DNA Repair 9:224–36
    [Google Scholar]
  138. 138.
    White RR, Vijg J 2016. Do DNA double-strand breaks drive aging. ? Mol. Cell 63:729–38
    [Google Scholar]
  139. 139.
    Wold MS 1997. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66:61–92
    [Google Scholar]
  140. 140.
    Wright WD, Heyer WD 2014. Rad54 functions as a heteroduplex DNA pump modulated by its DNA substrates and Rad51 during D loop formation. Mol. Cell 53:420–32
    [Google Scholar]
  141. 141.
    Wyatt HD, West SC 2014. Holliday junction resolvases. Cold Spring Harb. Perspect. Biol. 6:a023192
    [Google Scholar]
  142. 142.
    Xue X, Sung P, Zhao X 2015. Functions and regulation of the multitasking FANCM family of DNA motor proteins. Genes Dev 29:1777–88
    [Google Scholar]
  143. 143.
    Yang W 2010. Lessons learned from UvrD helicase: mechanism for directional movement. Annu. Rev. Biophys. 39:367–85
    [Google Scholar]
  144. 144.
    Yodh JG, Stevens BC, Kanagaraj R, Janscak P, Ha T 2009. BLM helicase measures DNA unwound before switching strands and hRPA promotes unwinding reinitiation. EMBO J 28:405–16
    [Google Scholar]
  145. 145.
    Zhang Z, Fan HY, Goldman JA, Kingston RE 2007. Homology-driven chromatin remodeling by human RAD54. Nat. Struct. Mol. Biol. 14:397–405
    [Google Scholar]
  146. 146.
    Zheng XF, Prakash R, Saro D, Longerich S, Niu H, Sung P 2011. Processing of DNA structures via DNA unwinding and branch migration by the S. cerevisiae Mph1 protein. DNA Repair 10:1034–43
    [Google Scholar]
  147. 147.
    Zhu Z, Chung WH, Shim EY, Lee SE, Ira G 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981–94
    [Google Scholar]
  148. 148.
    Zickler D, Kleckner N 2015. Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harb. Perspect. Biol. 7:a016626
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-052118-115418
Loading
/content/journals/10.1146/annurev-biophys-052118-115418
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error