Meiotic Chromosome Pairing Is Promoted by Telomere-Led Chromosome Movements Independent of Bouquet Formation

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Chromosome pairing in meiotic prophase is a prerequisite for the high fidelity of chromosome segregation that haploidizes the genome prior to gamete formation. In the budding yeast Saccharomyces cerevisiae, as in most multicellular eukaryotes, homologous pairing at the cytological level reflects the contemporaneous search for homology at the molecular level, where DNA double-strand broken ends find and interact with templates for repair on homologous chromosomes. Synapsis (synaptonemal complex formation) stabilizes pairing and supports DNA repair. The bouquet stage, where telomeres have formed a transient single cluster early in meiotic prophase, and telomere-promoted rapid meiotic prophase chromosome movements (RPMs) are prominent temporal correlates of pairing and synapsis. The bouquet has long been thought to contribute to the kinetics of pairing, but the individual roles of bouquet and RPMs are difficult to assess because of common dependencies. For example, in budding yeast RPMs and bouquet both require the broadly conserved SUN protein Mps3 as well as Ndj1 and Csm4, which link telomeres to the cytoskeleton through the intact nuclear envelope. We find that mutants in these genes provide a graded series of RPM activity: wild-type>mps3-dCC>mps3-dAR>ndj1Δ>mps3-dNT = csm4Δ. Pairing rates are directly correlated with RPM activity even though only wild-type forms a bouquet, suggesting that RPMs promote homologous pairing directly while the bouquet plays at most a minor role in Saccharomyces cerevisiae. A new collision trap assay demonstrates that RPMs generate homologous and heterologous chromosome collisions in or before the earliest stages of prophase, suggesting that RPMs contribute to pairing by stirring the nuclear contents to aid the recombination-mediated homology search.

Vyšlo v časopise: Meiotic Chromosome Pairing Is Promoted by Telomere-Led Chromosome Movements Independent of Bouquet Formation. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002730
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002730

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1. MaguireMP 1974 A new model for homologous chromosome pairing. Caryologia 27 349 357

2. RickardsGK 1975 Prophase chromosome movements in living house cricket spermatocytes and their relationship to prometaphase, anaphase and granule movements. Chromosoma 49 407 455

3. ParvinenMSoderstromKO 1976 Chromosome rotation and formation of synapsis. Nature 260 534 535

4. ChikashigeYDingDQFunabikiHHaraguchiTMashikoS 1994 Telomere-led premeiotic chromosome movement in fission yeast. Science 264 270 273

5. ScherthanHWangHAdelfalkCWhiteEJCowanC 2007 Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104 16934 16939

6. PenknerAMFridkinAGloggnitzerJBaudrimontAMachacekT 2009 Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139 920 933

7. SatoAIsaacBPhillipsCMRilloRCarltonPM 2009 Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139 907 919

8. ChikashigeYTsutsumiCYamaneMOkamasaKHaraguchiT 2006 Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125 59 69

9. ConradMNLeeCYWilkersonJLDresserME 2007 MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104 8863 8868

10. FridkinAPenknerAJantschVGruenbaumY 2009 SUN-domain and KASH-domain proteins during development, meiosis and disease. Cell Mol Life Sci 66 1518 1533

11. HiraokaYDernburgAF 2009 The SUN rises on meiotic chromosome dynamics. Dev Cell 17 598 605

12. KoszulRKlecknerN 2009 Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 19 716 724

13. BaudrimontAPenknerAWoglarAMachacekTWegrostekC 2010 Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans. PLoS Genet 6 e1001219 doi:10.1371/journal.pgen.1001219

14. JiangXZYangMGHuangLHLiCQXingXW 2011 SPAG4L, a novel nuclear envelope protein involved in the meiotic stage of spermatogenesis. DNA Cell Biol 30 875 882

15. RaoHBShinoharaMShinoharaA 2011 Mps3 SUN domain is important for chromosome motion and juxtaposition of homologous chromosomes during meiosis. Genes Cells 16 1081 1096

16. WynneDJRogOCarltonPMDernburgAF 2012 Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. J Cell Biol 196 47 64

17. MosesMJ 1968 Synaptonemal complex. Annu Rev Genet 2 363 412

18. ZicklerDKlecknerN 1998 The leptotene-zygotene transition of meiosis. Annu Rev Genet 32:619-97 619 697

19. ScherthanH 2001 A bouquet makes ends meet. Nat Rev Mol Cell Biol 2 621 627

20. ZicklerD 2006 From early homologue recognition to synaptonemal complex formation. Chromosoma 115 158 174

21. MacQueenAJPhillipsCMBhallaNWeiserPVilleneuveAM 2005 Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123 1037 1050

22. DingDQYamamotoAHaraguchiTHiraokaY 2004 Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 6 329 341

23. StorlazziATesseSGarganoSJamesFKlecknerN 2003 Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev 17 2675 2687

24. TankimanovaMHultenMATeaseC 2004 The initiation of homologous chromosome synapsis in mouse fetal oocytes is not directly driven by centromere and telomere clustering in the bouquet. Cytogenet Genome Res 105 172 181

25. PfeiferCScherthanHThomsenPD 2003 Sex-specific telomere redistribution and synapsis initiation in cattle oogenesis. Dev Biol 255 206 215

26. Trelles-StickenEDresserMEScherthanH 2000 Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 151 95 106

27. ConradMNLeeCYChaoGShinoharaMKosakaH 2008 Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3 and CSM4 and is modulated by recombination. Cell 133 1175 1187

28. KosakaHShinoharaMShinoharaA 2008 Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination. PLoS Genet 4 e1000196 doi:10.1371/journal.pgen.1000196

29. WanatJJKimKPKoszulRZandersSWeinerB 2008 Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis. PLoS Genet 4 e1000188 doi:10.1371/journal.pgen.1000188

30. Sonntag BrownMZandersSAlaniE 2011 Sustained and rapid chromosome movements are critical for chromosome pairing and meiotic progression in budding yeast. Genetics 188 21 32

31. KoszulRKimKPPrentissMKlecknerNKameokaS 2008 Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133 1188 1201

32. JaspersenSLGiddingsTHJrWineyM 2002 Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J Cell Biol 159 945 956

33. NishikawaSTerazawaYNakayamaTHirataAMakioT 2003 Nep98p is a component of the yeast spindle pole body and essential for nuclear division and fusion. J Biol Chem 278 9938 9943

34. WangQDuXCaiZGreeneMI 2006 Characterization of the structures involved in localization of the SUN proteins to the nuclear envelope and the centrosome. DNA Cell Biol 25 554 562

35. BuppJMMartinAEStensrudESJaspersenSL 2007 Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3. J Cell Biol 179 845 854

36. AntoniacciLMKennaMASkibbensRV 2007 The nuclear envelope and spindle pole body-associated Mps3 protein bind telomere regulators and function in telomere clustering. Cell Cycle 6 75 79

37. OzaPJaspersenSLMieleADekkerJPetersonCL 2009 Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev 23 912 927

38. SchoberHFerreiraHKalckVGehlenLRGasserSM 2009 Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev 23 928 938

39. KalocsayMHillerNJJentschS 2009 Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell 33 335 343

40. WitkinKLFriederichsJMCohen-FixOJaspersenSL 2010 Changes in the nuclear envelope environment affect spindle pole body duplication in Saccharomyces cerevisiae. Genetics 186 867 883

41. ChanJNPoonBPSalviJOlsenJBEmiliA 2011 Perinuclear cohibin complexes maintain replicative life span via roles at distinct silent chromatin domains. Dev Cell 20 867 879

42. HorigomeCOkadaTShimazuKGasserSMMizutaK 2011 Ribosome biogenesis factors bind a nuclear envelope SUN domain protein to cluster yeast telomeres. EMBO J 30 3799 3811

43. StraightAFBelmontASRobinettCCMurrayAW 1996 GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol 6 1599 1608

44. WeinerBMKlecknerN 1994 Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77 977 991

45. BornerGVKlecknerNHunterN 2004 Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117 29 45

46. ConchelloJADresserME 2007 Extended depth-of-focus microscopy via constrained deconvolution. J Biomed Opt 12 064026

47. BergHC 1993 Random Walks in Biology Princeton University Press

48. Trelles-StickenEAdelfalkCLoidlJScherthanH 2005 Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J Cell Biol 170 213 223

49. LacefieldSMurrayAW 2007 The spindle checkpoint rescues the meiotic segregation of chromosomes whose crossovers are far from the centromere. Nat Genet 39 1273 1277

50. PeoplesTLDeanEGonzalezOLambourneLBurgessSM 2002 Close, stable homolog juxtaposition during meiosis in budding yeast is dependent on meiotic recombination, occurs independently of synapsis, and is distinct from DSB-independent pairing contacts. Genes Dev 16 1682 1695

51. KeeneySGirouxCNKlecknerN 1997 Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88 375 384

52. GirouxCNDresserMETianoHF 1989 Genetic control of chromosome synapsis in yeast meiosis. Genome 31 88 94

53. Peoples-HolstTLBurgessSM 2005 Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast. Genes Dev 19 863 874

54. GoldmanASLichtenM 2000 Restriction of ectopic recombination by interhomolog interactions during Saccharomyces cerevisiae meiosis. Proc Natl Acad Sci U S A 97 9537 9542

55. SchlechtHBLichtenMGoldmanAS 2004 Compartmentalization of the yeast meiotic nucleus revealed by analysis of ectopic recombination. Genetics 168 1189 1203

56. JinQTrelles-StickenEScherthanHLoidlJ 1998 Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J Cell Biol 141 21 29

57. HayashiAOgawaHKohnoKGasserSMHiraokaY 1998 Meiotic behaviours of chromosomes and microtubules in budding yeast: relocalization of centromeres and telomeres during meiotic prophase. Genes Cells 3 587 601

58. KleinFLarocheTCardenasMEHofmannJFSchweizerD 1992 Localization of RAP1 and topoisomerase II in nuclei and meiotic chromosomes of yeast. J Cell Biol 117 935 948

59. PalladinoFLarocheTGilsonEAxelrodAPillusL 1993 SIR3 and SIR4 proteins are required for the positioning and integrity of yeast telomeres. Cell 75 543 555

60. ConradMNDominguezAMDresserME 1997 Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. Science 276 1252 1255

61. ChuaPRRoederGS 1997 Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev 11 1786 1800

62. RockmillBSymMScherthanHRoederGS 1995 Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev 9 2684 2695

63. ScherthanHSchonbornI 2001 Asynchronous chromosome pairing in male meiosis of the rat (Rattus norvegicus). Chromosome Res 9 273 282

64. WuHYBurgessSM 2006 Ndj1, a telomere-associated protein, promotes meiotic recombination in budding yeast. Mol Cell Biol 26 3683 3694

65. ChenSYTsubouchiTRockmillBSandlerJSRichardsDR 2008 Global analysis of the meiotic crossover landscape. Dev Cell 15 401 415

66. RockmillBRoederGS 1998 Telomere-mediated chromosome pairing during meiosis in budding yeast. Genes Dev 12 2574 2586

67. TomitaKCooperJP 2007 The telomere bouquet controls the meiotic spindle. Cell 130 113 126

68. BullardSAKimSGalbraithAMMaloneRE 1996 Double strand breaks at the HIS2 recombination hot spot in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 93 13054 13059

69. KeeneySKlecknerN 1996 Communication between homologous chromosomes: genetic alterations at a nuclease-hypersensitive site can alter mitotic chromatin structure at that site both in cis and in trans. Genes Cells 1 475 489

70. KatenevaAVKonovchenkoAAGuacciVDresserME 2005 Recombination protein Tid1p controls resolution of cohesin-dependent linkages in meiosis in Saccharomyces cerevisiae. J Cell Biol 171 241 253

71. DresserME 2009 Time-Lapse fluorescence microscopy of Saccharomyces cerevisiae. KeeneyS Methods in Molecular Biology, Vol. 558, Meiosis, Volume 2: Cytological Methods Ottowa Humana Press

72. DresserMEGirouxCN 1988 Meiotic chromosome behavior in spread preparations of yeast. J Cell Biol 106 567 573