#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Interplay between Synaptonemal Complex, Homologous Recombination, and Centromeres during Mammalian Meiosis


The intimate synapsis of homologous chromosome pairs (homologs) by synaptonemal complexes (SCs) is an essential feature of meiosis. In many organisms, synapsis and homologous recombination are interdependent: recombination promotes SC formation and SCs are required for crossing-over. Moreover, several studies indicate that initiation of SC assembly occurs at sites where crossovers will subsequently form. However, recent analyses in budding yeast and fruit fly imply a special role for centromeres in the initiation of SC formation. In addition, in budding yeast, persistent SC–dependent centromere-association facilitates the disjunction of chromosomes that have failed to become connected by crossovers. Here, we examine the interplay between SCs, recombination, and centromeres in a mammal. In mouse spermatocytes, centromeres do not serve as SC initiation sites and are invariably the last regions to synapse. However, centromeres are refractory to de-synapsis during diplonema and remain associated by short SC fragments. Since SC–dependent centromere association is lost before diakinesis, a direct role in homolog segregation seems unlikely. However, post–SC disassembly, we find evidence of inter-centromeric connections that could play a more direct role in promoting homolog biorientation and disjunction. A second class of persistent SC fragments is shown to be crossover-dependent. Super-resolution structured-illumination microscopy (SIM) reveals that these structures initially connect separate homolog axes and progressively diminish as chiasmata form. Thus, DNA crossing-over (which occurs during pachynema) and axis remodeling appear to be temporally distinct aspects of chiasma formation. SIM analysis of the synapsis and crossover-defective mutant Sycp1−/− implies that SCs prevent unregulated fusion of homolog axes. We propose that SC fragments retained during diplonema stabilize nascent bivalents and help orchestrate local chromosome reorganization that promotes centromere and chiasma function.


Vyšlo v časopise: Interplay between Synaptonemal Complex, Homologous Recombination, and Centromeres during Mammalian Meiosis. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002790
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002790

Souhrn

The intimate synapsis of homologous chromosome pairs (homologs) by synaptonemal complexes (SCs) is an essential feature of meiosis. In many organisms, synapsis and homologous recombination are interdependent: recombination promotes SC formation and SCs are required for crossing-over. Moreover, several studies indicate that initiation of SC assembly occurs at sites where crossovers will subsequently form. However, recent analyses in budding yeast and fruit fly imply a special role for centromeres in the initiation of SC formation. In addition, in budding yeast, persistent SC–dependent centromere-association facilitates the disjunction of chromosomes that have failed to become connected by crossovers. Here, we examine the interplay between SCs, recombination, and centromeres in a mammal. In mouse spermatocytes, centromeres do not serve as SC initiation sites and are invariably the last regions to synapse. However, centromeres are refractory to de-synapsis during diplonema and remain associated by short SC fragments. Since SC–dependent centromere association is lost before diakinesis, a direct role in homolog segregation seems unlikely. However, post–SC disassembly, we find evidence of inter-centromeric connections that could play a more direct role in promoting homolog biorientation and disjunction. A second class of persistent SC fragments is shown to be crossover-dependent. Super-resolution structured-illumination microscopy (SIM) reveals that these structures initially connect separate homolog axes and progressively diminish as chiasmata form. Thus, DNA crossing-over (which occurs during pachynema) and axis remodeling appear to be temporally distinct aspects of chiasma formation. SIM analysis of the synapsis and crossover-defective mutant Sycp1−/− implies that SCs prevent unregulated fusion of homolog axes. We propose that SC fragments retained during diplonema stabilize nascent bivalents and help orchestrate local chromosome reorganization that promotes centromere and chiasma function.


Zdroje

1. HunterN 2004 Lennarz WaLM Meiosis San Diego Elsevier Press

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

3. BhallaNDernburgAF 2008 Prelude to a division. Annu Rev Cell Dev Biol 24 397 424

4. von WettsteinDRasmussenSWHolmPB 1984 The synaptonemal complex in genetic segregation. Annu Rev Genet 18 331 413

5. PageSLHawleyRS 2004 The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20 525 558

6. ZicklerDKlecknerN 1999 Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33 603 754

7. CostaYCookeHJ 2007 Dissecting the mammalian synaptonemal complex using targeted mutations. Chromosome Res 15 579 589

8. YangFWangPJ 2009 The Mammalian synaptonemal complex: a scaffold and beyond. Genome Dyn 5 69 80

9. PelttariJHojaMRYuanLLiuJGBrundellE 2001 A meiotic chromosomal core consisting of cohesin complex proteins recruits DNA recombination proteins and promotes synapsis in the absence of an axial element in mammalian meiotic cells. Mol Cell Biol 21 5667 5677

10. KouznetsovaANovakIJessbergerRHoogC 2005 SYCP2 and SYCP3 are required for cohesin core integrity at diplotene but not for centromere cohesion at the first meiotic division. J Cell Sci 118 2271 2278

11. HendersonKAKeeneyS 2005 Synaptonemal complex formation: where does it start? Bioessays 27 995 998

12. HunterN 2006 Meiotic Recombination. AguileraARothsteinR Molecular Genetics of Recombination Heidelberg Springer-Verlag 381 442

13. TsaiJHMcKeeBD 2011 Homologous pairing and the role of pairing centers in meiosis. J Cell Sci 124 1955 1963

14. JonesGH 1987 Chiasmata. MoensPB Meiosis Orlando Academic Press 213 244

15. SakunoTTanakaKHaufSWatanabeY 2011 Repositioning of aurora B promoted by chiasmata ensures sister chromatid mono-orientation in meiosis I. Dev Cell 21 534 545

16. HiroseYSuzukiROhbaTHinoharaYMatsuharaH 2011 Chiasmata promote monopolar attachment of sister chromatids and their co-segregation toward the proper pole during meiosis I. PLoS Genet 7 e1001329 doi:10.1371/journal.pgen.1001329

17. de VriesFAde BoerEvan den BoschMBaarendsWMOomsM 2005 Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19 1376 1389

18. SymMEngebrechtJARoederGS 1993 ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72 365 378

19. SubramanianVVHochwagenA 2011 Centromere clustering: where synapsis begins. Curr Biol 21 R920 922

20. StewartMNDawsonDS 2008 Changing partners: moving from non-homologous to homologous centromere pairing in meiosis. Trends Genet 24 564 573

21. KempBBoumilRMStewartMNDawsonDS 2004 A role for centromere pairing in meiotic chromosome segregation. Genes Dev 18 1946 1951

22. TsubouchiTRoederGS 2005 A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308 870 873

23. FalkJEChanACHoffmannEHochwagenA 2010 A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 19 599 611

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

25. ObesoDDawsonDS 2010 Temporal characterization of homology-independent centromere coupling in meiotic prophase. PLoS ONE 5 e10336 doi:10.1371/journal.pone.0010336

26. HassoldTHallHHuntP 2007 The origin of human aneuploidy: where we have been, where we are going. Hum Mol Genet 16 Spec No. 2 R203 208

27. RockmillBVoelkel-MeimanKRoederGS 2006 Centromere-proximal crossovers are associated with precocious separation of sister chromatids during meiosis in Saccharomyces cerevisiae. Genetics 174 1745 1754

28. TsubouchiTMacqueenAJRoederGS 2008 Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22 3217 3226

29. MacqueenAJRoederGS 2009 Fpr3 and Zip3 ensure that initiation of meiotic recombination precedes chromosome synapsis in budding yeast. Curr Biol 19 1519 1526

30. TakeoSLakeCMMorais-de-SaESunkelCEHawleyRS 2011 Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr Biol 21 1845 1851

31. TannetiNSLandyKJoyceEFMcKimKS 2011 A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr Biol 21 1852 1857

32. NewnhamLJordanPRockmillBRoederGSHoffmannE 2010 The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis I. Proc Natl Acad Sci U S A 107 781 785

33. CheslockPSKempBJBoumilRMDawsonDS 2005 The roles of MAD1, MAD2 and MAD3 in meiotic progression and the segregation of nonexchange chromosomes. Nat Genet 37 756 760

34. HawleyRSTheurkaufWE 1993 Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet 9 310 317

35. PageJBerriosSRufasJSParraMTSujaJA 2003 The pairing of X and Y chromosomes during meiotic prophase in the marsupial species Thylamys elegans is maintained by a dense plate developed from their axial elements. J Cell Sci 116 551 560

36. PageJVieraAParraMTde la FuenteRSujaJA 2006 Involvement of synaptonemal complex proteins in sex chromosome segregation during marsupial male meiosis. PLoS Genet 2 e136 doi:10.1371/journal.pgen.0020136

37. de la FuenteRParraMTVieraACalventeAGomezR 2007 Meiotic pairing and segregation of achiasmate sex chromosomes in eutherian mammals: the role of SYCP3 protein. PLoS Genet 3 e198 doi:10.1371/journal.pgen.0030198

38. SolariAJ 1974 The behavior of the XY pair in mammals. Int Rev Cytol 38 273 317

39. BurgoynePS 1982 Genetic homology and crossing over in the X and Y chromosomes of Mammals. Hum Genet 61 85 90

40. OttoSPPannellJRPeichelCLAshmanTLCharlesworthD 2011 About PAR: the distinct evolutionary dynamics of the pseudoautosomal region. Trends Genet 27 358 367

41. EarnshawWCRothfieldN 1985 Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91 313 321

42. de BoerEHeytingC 2006 The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115 220 234

43. LeeJHiranoT 2011 RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol 192 263 276

44. HerranYGutierrez-CaballeroCSanchez-MartinMHernandezTVieraA 2011 The cohesin subunit RAD21L functions in meiotic synapsis and exhibits sexual dimorphism in fertility. Embo J 30 3091 3105

45. IshiguroKKimJFujiyama-NakamuraSKatoSWatanabeY 2011 A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep 12 267 275

46. LukasJLukasCBartekJ 2011 More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 13 1161 1169

47. ParraMTVieraAGomezRPageJBenaventeR 2004 Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J Cell Sci 117 1221 1234

48. BisigCGGuiraldelliMFKouznetsovaAScherthanAHHöögC 2012 Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes. PLoS Genet 8 doi:10.1371/journal.pgen.1002701 e1002701

49. ZicklerDMoreauPJHuynhADSlezecAM 1992 Correlation between pairing initiation sites, recombination nodules and meiotic recombination in Sordaria macrospora. Genetics 132 135 148

50. ZicklerD 1977 Development of the synaptonemal complex and the “recombination nodules” during meiotic prophase in the seven bivalents of the fungus Sordaria macrospora Auersw. Chromosoma 61 289 316

51. RoigIDowdleJATothAde RooijDGJasinM 2010 Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLoS Genet 6 e1001062 doi.org/10.1371/journal.pgen.1001062

52. HolmPBRasmussenSWZicklerDLuBCSageJ 1981 Chromosome pairing, recombination nodules and chiasma formation in the basidiomycete Coprinus cinereus. Carlsberg Res Commun 46 305 346

53. BrownPWJudisLChanERSchwartzSSeftelA 2005 Meiotic synapsis proceeds from a limited number of subtelomeric sites in the human male. Am J Hum Genet 77 556 566

54. PerryJPalmerSGabrielAAshworthA 2001 A short pseudoautosomal region in laboratory mice. Genome Res 11 1826 1832

55. AgarwalSRoederGS 2000 Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102 245 255

56. ChengCHLoYHLiangSSTiSCLinFM 2006 SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20 2067 2081

57. PerryJKlecknerNBornerGV 2005 Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci U S A 102 17594 17599

58. KongAThorleifssonGStefanssonHMassonGHelgasonA 2008 Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319 1398 1401

59. Bolcun-FilasEHallESpeedRTaggartMGreyC 2009 Mutation of the mouse Syce1 gene disrupts synapsis and suggests a link between synaptonemal complex structural components and DNA repair. PLoS Genet 5 e1000393 doi:10.1371/journal.pgen.1000393

60. Bolcun-FilasECostaYSpeedRTaggartMBenaventeR 2007 SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J Cell Biol 176 741 747

61. HamerGWangHBolcun-FilasECookeHJBenaventeR 2008 Progression of meiotic recombination requires structural maturation of the central element of the synaptonemal complex. J Cell Sci 121 2445 2451

62. HolmPBRasmussenSW 1983 Human meiosis. VII. Chiasma formation in human spermatocytes. Carlsberg Res Coinrnitn 48 415 456

63. WangCJCarltonPMGolubovskayaINCandeWZ 2009 Interlock formation and coiling of meiotic chromosome axes during synapsis. Genetics 183 905 915

64. CarltonPM 2008 Three-dimensional structured illumination microscopy and its application to chromosome structure. Chromosome Res 16 351 365

65. GuillonHBaudatFGreyCLiskayRMde MassyB 2005 Crossover and noncrossover pathways in mouse meiosis. Mol Cell 20 563 573

66. GuillonHde MassyB 2002 An initiation site for meiotic crossing-over and gene conversion in the mouse. Nat Genet 32 296 299

67. HughesSEGillilandWDCotittaJLTakeoSCollinsKA 2009 Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genet 5 e1000348 doi:10.1371/journal.pgen.1000348

68. MoensPBSpyropoulosB 1995 Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis. Chromosoma 104 175 182

69. DobsonMJPearlmanREKaraiskakisASpyropoulosBMoensPB 1994 Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci 107 Pt 10 2749 2760

70. ScherthanHWeichSSchweglerHHeytingCHarleM 1996 Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134 1109 1125

71. MosesMJDresserMEPoormanPA 1984 Composition and role of the synaptonemal complex. EvansCWDickinsonHG Controlling Events in Meiosis 245 270

72. WojtaszLDanielKRoigIBolcun-FilasEXuH 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 doi:10.1371/journal.pgen.1000702

73. AndersonLKStackSM 2005 Recombination nodules in plants. Cytogenet Genome Res 109 198 204

74. BlackBEJansenLEFoltzDRClevelandDW 2010 Centromere identity, function, and epigenetic propagation across cell divisions. Cold Spring Harb Symp Quant Biol 75 403 418

75. HassoldTHuntP 2001 To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2 280 291

76. ResnickTDDejKJXiangYHawleyRSAhnC 2009 Mutations in the chromosomal passenger complex and the condensin complex differentially affect synaptonemal complex disassembly and metaphase I configuration in Drosophila female meiosis. Genetics 181 875 887

77. NabeshimaKVilleneuveAMColaiacovoMP 2005 Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J Cell Biol 168 683 689

78. Martinez-PerezESchvarzsteinMBarrosoCLightfootJDernburgAF 2008 Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev 22 2886 2901

79. KlecknerNZicklerDJonesGHDekkerJPadmoreR 2004 A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 101 12592 12597

80. RuchaudSCarmenaMEarnshawWC 2007 Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8 798 812

81. MalmancheNOwenSGegickSSteffensenSTomkielJE 2007 Drosophila BubR1 is essential for meiotic sister-chromatid cohesion and maintenance of synaptonemal complex. Curr Biol 17 1489 1497

82. JordanPCopseyANewnhamLKolarELichtenM 2009 Ipl1/Aurora B kinase coordinates synaptonemal complex disassembly with cell cycle progression and crossover formation in budding yeast meiosis. Genes Dev 23 2237 2251

83. ParraMTGomezRVieraALlanoEPendasAM 2009 Sequential assembly of centromeric proteins in male mouse meiosis. PLoS Genet 5 e1000417 doi:10.1371/journal.pgen.1000417

84. ParraMTVieraAGomezRPageJCarmenaM 2003 Dynamic relocalization of the chromosomal passenger complex proteins inner centromere protein (INCENP) and aurora-B kinase during male mouse meiosis. J Cell Sci 116 961 974

85. La SalleSSunFZhangXDMatunisMJHandelMA 2008 Developmental control of sumoylation pathway proteins in mouse male germ cells. Dev Biol 321 227 237

86. EijpeMOffenbergHJessbergerRRevenkovaEHeytingC 2003 Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3. J Cell Biol 160 657 670

87. AshleyTWalpitaDde RooijDG 2001 Localization of two mammalian cyclin dependent kinases during mammalian meiosis. J Cell Sci 114 685 693

88. DernburgAFSedatJWHawleyRS 1996 Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86 135 146

89. KarpenGHLeMHLeH 1996 Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273 118 122

90. HawleyRSIrickHZitronAEHaddoxDALoheA 1992 There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology. Dev Genet 13 440 467

91. BaudatFManovaKYuenJPJasinMKeeneyS 2000 Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6 989 998

92. HollowayJKBoothJEdelmannWMcGowanCHCohenPE 2008 MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLoS Genet 4 e1000186 doi:10.1371/journal.pgen.1000186

93. QiaoHLohmillerLAndersonL 2011 Cohesin proteins load sequentially during prophase I in tomato primary microsporocytes. Chromosome Research 19 193 207

94. MeuwissenRLOffenbergHHDietrichAJRiesewijkAvan IerselM 1992 A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. Embo J 11 5091 5100

95. CostaYSpeedROllingerRAlsheimerMSempleCA 2005 Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J Cell Sci 118 2755 2762

96. HamerGGellKKouznetsovaANovakIBenaventeR 2006 Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J Cell Sci 119 4025 4032

97. RomanienkoPJCamerini-OteroRD 2000 The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6 975 987

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 6
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#