MEIOB Targets Single-Strand DNA and Is Necessary for Meiotic Recombination

English version České info

Meiotic recombination is a mandatory process for sexual reproduction. We identified a protein specifically implicated in meiotic homologous recombination that we named: meiosis specific with OB domain (MEIOB). This protein is conserved among metazoan species and contains single-strand DNA binding sites similar to those of RPA1. Our studies in vitro revealed that both recombinant and endogenous MEIOB can be retained on single-strand DNA. Those in vivo demonstrated the specific expression of Meiob in early meiotic germ cells and the co-localization of MEIOB protein with RPA on chromosome axes. MEIOB localization in Dmc1^−/− spermatocytes indicated that it accumulates on resected DNA. Homologous Meiob deletion in mice caused infertility in both sexes, due to a meiotic arrest at a zygotene/pachytene-like stage. DNA double strand break repair and homologous chromosome synapsis were impaired in Meiob^−/− meiocytes. Interestingly MEIOB appeared to be dispensable for the initial loading of recombinases but was required to maintain a proper number of RAD51 and DMC1 foci beyond the zygotene stage. In light of these findings, we propose that RPA and this new single-strand DNA binding protein MEIOB, are essential to ensure the proper stabilization of recombinases which is required for successful homology search and meiotic recombination.

Vyšlo v časopise: MEIOB Targets Single-Strand DNA and Is Necessary for Meiotic Recombination. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003784
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003784

Souhrn

Zdroje

1. Bascom-SlackCA, RossLO, DawsonDS (1997) Chiasmata, crossovers, and meiotic chromosome segregation. Adv Genet 35: 253–284.

2. SchwachaA, KlecknerN (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51–63.

3. AndersenSL, SekelskyJ (2010) Meiotic versus mitotic recombination: two different routes for double-strand break repair: the different functions of meiotic versus mitotic DSB repair are reflected in different pathway usage and different outcomes. Bioessays 32: 1058–1066.

4. KeeneyS, GirouxCN, KlecknerN (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375–384.

5. BaudatF, ManovaK, YuenJP, JasinM, KeeneyS (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6: 989–998.

6. RomanienkoPJ, Camerini-OteroRD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6: 975–987.

7. SunH, TrecoD, SzostakJW (1991) Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell 64: 1155–1161.

8. BishopDK, ZicklerD (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9–15.

9. WoldMS, KellyT (1988) Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA. Proc Natl Acad Sci U S A 85: 2523–2527.

10. BochkarevaE, KorolevS, Lees-MillerSP, BochkarevA (2002) Structure of the RPA trimerization core and its role in the multistep DNA-binding mechanism of RPA. EMBO J 21: 1855–1863.

11. NealeMJ, KeeneyS (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442: 153–158.

12. SharanSK, PyleA, CoppolaV, BabusJ, SwaminathanS, et al. (2004) BRCA2 deficiency in mice leads to meiotic impairment and infertility. Development 131: 131–142.

13. HollomanWK (2011) Unraveling the mechanism of BRCA2 in homologous recombination. Nat Struct Mol Biol 18: 748–754.

14. SiaudN, DrayE, GyI, GerardE, TakvorianN, et al. (2004) Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO J 23: 1392–1401.

15. CloudV, ChanYL, GrubbJ, BudkeB, BishopDK (2012) Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337: 1222–1225.

16. KurzbauerMT, UanschouC, ChenD, SchlogelhoferP (2012) The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell 24: 2058–2070.

17. TsubouchiH, RoederGS (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev 20: 1766–1775.

18. ZicklerD, KlecknerN (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603–754.

19. FrauneJ, SchrammS, AlsheimerM, BenaventeR (2012) The mammalian synaptonemal complex: protein components, assembly and role in meiotic recombination. Exp Cell Res 318: 1340–1346.

20. PageSL, HawleyRS (2003) Chromosome choreography: the meiotic ballet. Science 301: 785–789.

21. KouznetsovaA, BenaventeR, PastinkA, HoogC (2011) Meiosis in mice without a synaptonemal complex. PLoS One 6: e28255.

22. JoyceEF, TannetiSN, McKimKS (2009) Drosophila hold'em is required for a subset of meiotic crossovers and interacts with the dna repair endonuclease complex subunits MEI-9 and ERCC1. Genetics 181: 335–340.

23. CorpetF (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16: 10881–10890.

24. KogoH, Kowa-SugiyamaH, YamadaK, BolorH, TsutsumiM, et al. (2010) Screening of genes involved in chromosome segregation during meiosis I: toward the identification of genes responsible for infertility in humans. J Hum Genet 55: 293–299.

25. BishopDK, ParkD, XuL, KlecknerN (1992) DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69: 439–456.

26. PittmanDL, CobbJ, SchimentiKJ, WilsonLA, CooperDM, et al. (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1: 697–705.

27. YoshidaK, KondohG, MatsudaY, HabuT, NishimuneY, et al. (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell 1: 707–718.

28. CimprichKA, CortezD (2008) ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 9: 616–627.

29. RogakouEP, PilchDR, OrrAH, IvanovaVS, BonnerWM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858–5868.

30. CelesteA, PetersenS, RomanienkoPJ, Fernandez-CapetilloO, ChenHT, et al. (2002) Genomic instability in mice lacking histone H2AX. Science 296: 922–927.

31. de VriesFA, de BoerE, van den BoschM, BaarendsWM, OomsM, et al. (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19: 1376–1389.

32. GuillonH, BaudatF, GreyC, LiskayRM, de MassyB (2005) Crossover and noncrossover pathways in mouse meiosis. Mol Cell 20: 563–573.

33. HerranY, Gutierrez-CaballeroC, Sanchez-MartinM, HernandezT, VieraA, et al. (2011) The cohesin subunit RAD21L functions in meiotic synapsis and exhibits sexual dimorphism in fertility. EMBO J 30: 3091–3105.

34. HakemR, de la PompaJL, EliaA, PotterJ, MakTW (1997) Partial rescue of Brca1 (5–6) early embryonic lethality by p53 or p21 null mutation. Nat Genet 16: 298–302.

35. YangF, EckardtS, LeuNA, McLaughlinKJ, WangPJ (2008) Mouse TEX15 is essential for DNA double-strand break repair and chromosomal synapsis during male meiosis. J Cell Biol 180: 673–679.

36. FanningE, KlimovichV, NagerAR (2006) A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res 34: 4126–4137.

37. AlaniE, ThresherR, GriffithJD, KolodnerRD (1992) Characterization of DNA-binding and strand-exchange stimulation properties of y-RPA, a yeast single-strand-DNA-binding protein. J Mol Biol 227: 54–71.

38. MoensPB, KolasNK, TarsounasM, MarconE, CohenPE, et al. (2002) The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci 115: 1611–1622.

39. IchijimaY, IchijimaM, LouZ, NussenzweigA, Camerini-OteroRD, et al. (2011) MDC1 directs chromosome-wide silencing of the sex chromosomes in male germ cells. Genes Dev 25: 959–971.

40. BishopDK (2012) Rad51, the lead in mitotic recombinational DNA repair, plays a supporting role in budding yeast meiosis. Cell Cycle 11: 4105–06.

41. SiaudN, BarberaMA, EgashiraA, LamI, ChristN, et al. (2011) Plasticity of BRCA2 function in homologous recombination: genetic interactions of the PALB2 and DNA binding domains. PLoS Genet 7: e1002409.

42. ChiP, San FilippoJ, SehornMG, PetukhovaGV, SungP (2007) Bipartite stimulatory action of the Hop2-Mnd1 complex on the Rad51 recombinase. Genes Dev 21: 1747–1757.

43. MazinAV, AlexeevAA, KowalczykowskiSC (2003) A novel function of Rad54 protein. Stabilization of the Rad51 nucleoprotein filament. J Biol Chem 278: 14029–14036.

44. YuanJ, ChenJ (2011) The role of the human SWI5-MEI5 complex in homologous recombination repair. J Biol Chem 286: 9888–9893.

45. WesolyJ, AgarwalS, SigurdssonS, BussenW, Van KomenS, et al. (2006) Differential contributions of mammalian Rad54 paralogs to recombination, DNA damage repair, and meiosis. Mol Cell Biol 26: 976–989.

46. PetukhovaGV, RomanienkoPJ, Camerini-OteroRD (2003) The Hop2 protein has a direct role in promoting interhomolog interactions during mouse meiosis. Dev Cell 5: 927–936.

47. AkamatsuY, JasinM (2010) Role for the mammalian Swi5-Sfr1 complex in DNA strand break repair through homologous recombination. PLoS Genet 6: e1001160.

48. HayaseA, TakagiM, MiyazakiT, OshiumiH, ShinoharaM, et al. (2004) A protein complex containing Mei5 and Sae3 promotes the assembly of the meiosis-specific RecA homolog Dmc1. Cell 119: 927–940.

49. TsaiSP, SuGC, LinSW, ChungCI, XueX, et al. (2012) Rad51 presynaptic filament stabilization function of the mouse Swi5-Sfr1 heterodimeric complex. Nucleic Acids Res 40: 6558–6569.

50. SayAF, LedfordLL, SharmaD, SinghAK, LeungWK, et al. (2011) The budding yeast Mei5-Sae3 complex interacts with Rad51 and preferentially binds a DNA fork structure. DNA Repair (Amst) 10: 586–594.

51. FerrariSR, GrubbJ, BishopDK (2009) The Mei5-Sae3 protein complex mediates Dmc1 activity in Saccharomyces cerevisiae. J Biol Chem 284: 11766–11770.

52. La VolpeA, BarchiM (2012) Meiotic double strand breaks repair in sexually reproducing eukaryotes: we are not all equal. Exp Cell Res 318: 1333–1339.

53. IshibashiT, KimuraS, FurukawaT, HatanakaM, HashimotoJ, et al. (2001) Two types of replication protein A 70 kDa subunit in rice, Oryza sativa: molecular cloning, characterization, and cellular & tissue distribution. Gene 272: 335–343.

54. ShultzRW, TatineniVM, Hanley-BowdoinL, ThompsonWF (2007) Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice. Plant Physiol 144: 1697–1714.

55. ChangY, GongL, YuanW, LiX, ChenG, et al. (2009) Replication protein A (RPA1a) is required for meiotic and somatic DNA repair but is dispensable for DNA replication and homologous recombination in rice. Plant Physiol 151: 2162–2173.

56. HsiaKT, MillarMR, KingS, SelfridgeJ, RedheadNJ, et al. (2003) DNA repair gene Ercc1 is essential for normal spermatogenesis and oogenesis and for functional integrity of germ cell DNA in the mouse. Development 130: 369–378.

57. BurgoynePS, MahadevaiahSK, TurnerJM (2007) The management of DNA double-strand breaks in mitotic G2, and in mammalian meiosis viewed from a mitotic G2 perspective. Bioessays 29: 974–986.

58. LiveraG, DelbesG, PairaultC, Rouiller-FabreV, HabertR (2006) Organotypic culture, a powerful model for studying rat and mouse fetal testis development. Cell Tissue Res 324: 507–521.

59. GuerquinMJ, DuquenneC, LahayeJB, TourpinS, HabertR, et al. (2010) New testicular mechanisms involved in the prevention of fetal meiotic initiation in mice. Dev Biol 346: 320–330.

60. BernexF, De SepulvedaP, KressC, ElbazC, DelouisC, et al. (1996) Spatial and temporal patterns of c-kit-expressing cells in WlacZ/+ and WlacZ/WlacZ mouse embryos. Development 122: 3023–3033.

61. YoshimizuT, SugiyamaN, De FeliceM, YeomYI, OhboK, et al. (1999) Germline-specific expression of the Oct-4/green fluorescent protein (GFP) transgene in mice. Dev Growth Differ 41: 675–684.

62. Le BouffantR, SouquetB, DuvalN, DuquenneC, HerveR, et al. (2011) Msx1 and Msx2 promote meiosis initiation. Development 138: 5393–5402.

63. BastosH, LassalleB, ChicheporticheA, RiouL, TestartJ, et al. (2005) Flow cytometric characterization of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis. Cytometry A 65: 40–49.

64. SouquetB, TourpinS, MessiaenS, MoisonD, HabertR, et al. (2012) Nodal signaling regulates the entry into meiosis in fetal germ cells. Endocrinology 153: 2466–2473.

65. SchneiderCA, RasbandWS, EliceiriKW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675.

66. PetersAH, PlugAW, van VugtMJ, de BoerP (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5: 66–68.

67. ChicheporticheA, Bernardino-SgherriJ, de MassyB, DutrillauxB (2007) Characterization of Spo11-dependent and independent phospho-H2AX foci during meiotic prophase I in the male mouse. J Cell Sci 120: 1733–1742.

68. WojtaszL, DanielK, RoigI, Bolcun-FilasE, XuH, et al. (2009) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet 5: e1000702.

69. ColeF, KauppiL, LangeJ, RoigI, WangR, et al. (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 14: 424–430.