Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (2024)

Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (1) https://doi.org/10.3390/genes8030105 · Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (2) Повний текст

Видання: Genes, 2017, №3, с.105

Видавець: MDPI AG

Автори: Blanca Gómez-Escoda, Pei-Yun Wu

Анотація

Cells reproduce using two types of divisions: mitosis, which generates two daughter cells each with the same genomic content as the mother cell, and meiosis, which reduces the number of chromosomes of the parent cell by half and gives rise to four gametes. The mechanisms that promote the proper progression of the mitotic and meiotic cycles are highly conserved and controlled. They require the activities of two types of serine-threonine kinases, the cyclin-dependent kinases (CDKs) and the Dbf4-dependent kinase (DDK). CDK and DDK are essential for genome duplication and maintenance in both mitotic and meiotic divisions. In this review, we aim to highlight how these kinases cooperate to orchestrate diverse processes during cellular reproduction, focusing on meiosis-specific adaptions of their regulation and functions in DNA metabolism.

Джерела фінансування

  1. Centre National de la Recherche Scientifique
  2. Seventh Framework Programme

Список літератури

  1. Kleckner, Meiosis: How could it work?, Proc. Natl. Acad. Sci. USA, № 93, с. 8167
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (3) https://doi.org/10.1073/pnas.93.16.8167
  2. Lam, Mechanism and regulation of meiotic recombination initiation, Cold Spring Harb. Perspect. Biol., № 7, с. a016634
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (4) https://doi.org/10.1101/cshperspect.a016634
  3. Labib, How do Cdc7 and cyclin-dependent kinases trigger the initiation of chromosome replication in eukaryotic cells?, Genes Dev., № 24, с. 1208
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (5) https://doi.org/10.1101/gad.1933010
  4. Zegerman, Evolutionary conservation of the CDK targets in eukaryotic DNA replication initiation, Chromosoma, № 124, с. 309
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (6) https://doi.org/10.1007/s00412-014-0500-y
  5. Morgan, Cyclin-dependent kinases: Engines, clocks, and microprocessors, Annu. Rev. Cell Dev. Biol., № 13, с. 261
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (7) https://doi.org/10.1146/annurev.cellbio.13.1.261
  6. Yata, Dual role of CDKs in DNA repair: To be, or not to be, DNA Repair, № 8, с. 6
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (8) https://doi.org/10.1016/j.dnarep.2008.09.002
  7. Lim, Cdks, cyclins and CKIs: Roles beyond cell cycle regulation, Development, № 140, с. 3079
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (9) https://doi.org/10.1242/dev.091744
  8. Bailis, Hsk1-Dfp1 is required for heterochromatin-mediated cohesion at centromeres, Nat. Cell Biol., № 5, с. 1111
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (10) https://doi.org/10.1038/ncb1069
  9. Tsuji, The role of Dbf4/Drf1-dependent kinase Cdc7 in DNA-damage checkpoint control, Mol. Cell, № 32, с. 862
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (11) https://doi.org/10.1016/j.molcel.2008.12.005
  10. Takahashi, Cdc7-Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts, Genes Dev., № 22, с. 1894
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (12) https://doi.org/10.1101/gad.1683308
  11. Furuya, DDK phosphorylates checkpoint clamp component Rad9 and promotes its release from damaged chromatin, Mol. Cell, № 40, с. 606
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (13) https://doi.org/10.1016/j.molcel.2010.10.026
  12. Lee, Dbf4 is direct downstream target of ataxia telangiectasia mutated (ATM) and ataxia telangiectasia and Rad3-related (ATR) protein to regulate intra-S-phase checkpoint, J. Biol. Chem., № 287, с. 2531
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (14) https://doi.org/10.1074/jbc.M111.291104
  13. Ogino, Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast, Proc. Natl. Acad. Sci. USA, № 103, с. 8131
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (15) https://doi.org/10.1073/pnas.0602498103
  14. Wan, Chemical inactivation of cdc7 kinase in budding yeast results in a reversible arrest that allows efficient cell synchronization prior to meiotic recombination, Genetics, № 174, с. 1767
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (16) https://doi.org/10.1534/genetics.106.064303
  15. Lo, Cdc7-Dbf4 regulates NDT80 transcription as well as reductional segregation during budding yeast meiosis, Mol. Biol. Cell, № 19, с. 4956
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (17) https://doi.org/10.1091/mbc.e08-07-0755
  16. Matos, Dbf4-dependent CDC7 kinase links DNA replication to the segregation of hom*ologous chromosomes in meiosis I, Cell, № 135, с. 662
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (18) https://doi.org/10.1016/j.cell.2008.10.026
  17. Sasanuma, Cdc7-dependent phosphorylation of Mer2 facilitates initiation of yeast meiotic recombination, Genes Dev., № 22, с. 398
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (19) https://doi.org/10.1101/gad.1626608
  18. Wan, Cdc28-Clb5 (CDK-S) and Cdc7-Dbf4 (DDK) collaborate to initiate meiotic recombination in yeast, Genes Dev., № 22, с. 386
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (20) https://doi.org/10.1101/gad.1626408
  19. Masai, Human Cdc7-related kinase complex. In vitro phosphorylation of MCM by concerted actions of Cdks and Cdc7 and that of a criticial threonine residue of Cdc7 bY Cdks, J. Biol. Chem., № 275, с. 29042
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (21) https://doi.org/10.1074/jbc.M002713200
  20. Seta, Hierarchy of S-phase-promoting factors: Yeast Dbf4-Cdc7 kinase requires prior S-phase cyclin-dependent kinase activation, Mol. Cell. Biol., № 20, с. 3795
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (22) https://doi.org/10.1128/MCB.20.11.3795-3806.2000
  21. Devault, Interplay between S-cyclin-dependent kinase and Dbf4-dependent kinase in controlling DNA replication through phosphorylation of yeast Mcm4 N-terminal domain, Mol. Biol. Cell, № 19, с. 2267
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (23) https://doi.org/10.1091/mbc.e07-06-0614
  22. Sheu, The Dbf4-Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4, Nature, № 463, с. 113
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (24) https://doi.org/10.1038/nature08647
  23. Larasati, Mechanisms Governing DDK Regulation of the Initiation of DNA Replication, Genes, № 8, с. 3
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (25) https://doi.org/10.3390/genes8010003
  24. Kitada, Temperature-sensitive Cdc7 mutations of Saccharomyces cerevisiae are suppressed by the DBF4 gene, which is required for the G1/S cell cycle transition, Genetics, № 131, с. 21
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (26) https://doi.org/10.1093/genetics/131.1.21
  25. Jackson, Cell cycle regulation of the yeast Cdc7 protein kinase by association with the Dbf4 protein, Mol. Cell. Biol., № 13, с. 2899
  26. Montagnoli, Drf1, a novel regulatory subunit for human Cdc7 kinase, EMBO J., № 21, с. 3171
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (27) https://doi.org/10.1093/emboj/cdf290
  27. Takahashi, Cdc7-Drf1 is a developmentally regulated protein kinase required for the initiation of vertebrate DNA replication, Genes Dev., № 19, с. 2295
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (28) https://doi.org/10.1101/gad.1339805
  28. Fisher, A single fission yeast mitotic cyclin B p34cdc2 kinase promotes both S-phase and mitosis in the absence of G1 cyclins, EMBO J., № 15, с. 850
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (29) https://doi.org/10.1002/j.1460-2075.1996.tb00420.x
  29. Stern, A quantitative model for the cdc2 control of S phase and mitosis in fission yeast, Trends Genet., № 12, с. 345
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (30) https://doi.org/10.1016/S0168-9525(96)80016-3
  30. Donaldson, CLB5-dependent activation of late replication origins in S. cerevisiae, Mol. Cell, № 2, с. 173
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (31) https://doi.org/10.1016/S1097-2765(00)80127-6
  31. Hu, Swe1 regulation and transcriptional control restrict the activity of mitotic cyclins toward replication proteins in Saccharomyces cerevisiae, Proc. Natl. Acad. Sci. USA, № 102, с. 8910
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (32) https://doi.org/10.1073/pnas.0406987102
  32. Moore, Unmasking the S-phase-promoting potential of cyclin B1, Science, № 300, с. 987
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (33) https://doi.org/10.1126/science.1081418
  33. Kozar, Mouse development and cell proliferation in the absence of D-cyclins, Cell, № 118, с. 477
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (34) https://doi.org/10.1016/j.cell.2004.07.025
  34. Cerqueira, Cdk1 is sufficient to drive the mammalian cell cycle, Nature, № 448, с. 811
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (35) https://doi.org/10.1038/nature06046
  35. Coudreuse, Driving the cell cycle with a minimal CDK control network, Nature, № 468, с. 1074
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (36) https://doi.org/10.1038/nature09543
  36. Johnson, Mammalian cell fusion: Induction of premature chromosome condensation in interphase nuclei, Nature, № 226, с. 717
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (37) https://doi.org/10.1038/226717a0
  37. Banyai, Cdk1 activity acts as a quantitative platform for coordinating cell cycle progression with periodic transcription, Nat. Commun., № 7, с. 11161
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (38) https://doi.org/10.1038/ncomms11161
  38. Rahi, The CDK-APC/C Oscillator Predominantly Entrains Periodic Cell-Cycle Transcription, Cell, № 165, с. 475
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (39) https://doi.org/10.1016/j.cell.2016.02.060
  39. Swaffer, CDK Substrate Phosphorylation and Ordering the Cell Cycle, Cell, № 167, с. 1750
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (40) https://doi.org/10.1016/j.cell.2016.11.034
  40. Brown, Cell cycle regulation of Dfp1, an activator of the Hsk1 protein kinase, Proc. Natl. Acad. Sci. USA, № 96, с. 8443
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (41) https://doi.org/10.1073/pnas.96.15.8443
  41. Oshiro, Cell cycle control of Cdc7p kinase activity through regulation of Dbf4p stability, Mol. Cell. Biol., № 19, с. 4888
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (42) https://doi.org/10.1128/MCB.19.7.4888
  42. Takeda, A fission yeast gene, him1+/dfp1+, encoding a regulatory subunit for Hsk1 kinase, plays essential roles in S-phase initiation as well as in S-phase checkpoint control and recovery from DNA damage, Mol. Cell. Biol., № 19, с. 5535
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (43) https://doi.org/10.1128/MCB.19.8.5535
  43. Ferreira, Dbf4p, an essential S phase-promoting factor, is targeted for degradation by the anaphase-promoting complex, Mol. Cell. Biol., № 20, с. 242
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (44) https://doi.org/10.1128/MCB.20.1.242-248.2000
  44. Sclafani, Differential regulation of the yeast CDC7 gene during mitosis and meiosis, Mol. Cell. Biol., № 8, с. 293
  45. Patel, The Hsk1(Cdc7) replication kinase regulates origin efficiency, Mol. Biol. Cell, № 19, с. 5550
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (45) https://doi.org/10.1091/mbc.e08-06-0645
  46. Wu, Establishing the program of origin firing during S phase in fission Yeast, Cell, № 136, с. 852
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (46) https://doi.org/10.1016/j.cell.2009.01.017
  47. Mantiero, Limiting replication initiation factors execute the temporal programme of origin firing in budding yeast, EMBO J., № 30, с. 4805
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (47) https://doi.org/10.1038/emboj.2011.404
  48. Grandin, Differential function and expression of Saccharomyces cerevisiae B-type cyclins in mitosis and meiosis, Mol. Cell. Biol., № 13, с. 2113
  49. Chu, Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80, Mol. Cell, № 1, с. 685
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (48) https://doi.org/10.1016/S1097-2765(00)80068-4
  50. Dahmann, Specialization of B-type cyclins for mitosis or meiosis in S. cerevisiae, Genetics, № 140, с. 957
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (49) https://doi.org/10.1093/genetics/140.3.957
  51. Carlile, Meiosis I is established through division-specific translational control of a cyclin, Cell, № 133, с. 280
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (50) https://doi.org/10.1016/j.cell.2008.02.032
  52. Schwob, CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae, Genes Dev., № 7, с. 1160
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (51) https://doi.org/10.1101/gad.7.7a.1160
  53. Dirick, Regulation of meiotic S phase by Ime2 and a Clb5,6-associated kinase in Saccharomyces cerevisiae, Science, № 281, с. 1854
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (52) https://doi.org/10.1126/science.281.5384.1854
  54. Stuart, CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint, Genes Dev., № 12, с. 2698
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (53) https://doi.org/10.1101/gad.12.17.2698
  55. DeCesare, Among B-type cyclins only CLB5 and CLB6 promote premeiotic S phase in Saccharomyces cerevisiae, Genetics, № 190, с. 1001
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (54) https://doi.org/10.1534/genetics.111.134684
  56. Smith, B-type cyclins CLB5 and CLB6 control the initiation of recombination and synaptonemal complex formation in yeast meiosis, Current Biology, № 11, с. 88
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (55) https://doi.org/10.1016/S0960-9822(01)00026-4
  57. Nurse, A single cyclin-CDK complex is sufficient for both mitotic and meiotic progression in fission yeast, Nat. Commun., № 6, с. 6871
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (56) https://doi.org/10.1038/ncomms7871
  58. Malapeira, A meiosis-specific cyclin regulated by splicing is required for proper progression through meiosis, Mol. Cell. Biol., № 25, с. 6330
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (57) https://doi.org/10.1128/MCB.25.15.6330-6337.2005
  59. Geng, Cyclin E ablation in the mouse, Cell, № 114, с. 431
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (58) https://doi.org/10.1016/S0092-8674(03)00645-7
  60. Liu, Cyclin A1 is required for meiosis in the male mouse, Nat. Genet., № 20, с. 377
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (59) https://doi.org/10.1038/3855
  61. Benjamin, Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2, Genes Dev., № 17, с. 1524
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (60) https://doi.org/10.1101/gad.1101503
  62. Schindler, Phosphorylation of Ime2 regulates meiotic progression in Saccharomyces cerevisiae, J. Biol. Chem., № 281, с. 18307
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (61) https://doi.org/10.1074/jbc.M602349200
  63. Sagee, Human Cdk2 is a functional hom*olog of budding yeast Ime2, the meiosis-specific Cdk-like kinase, Cell Cycle, № 8, с. 647
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (62) https://doi.org/10.4161/cc.8.4.7843
  64. Honigberg, Ime2p and Cdc28p: Co-pilots driving meiotic development, J. Cell. Biochem., № 92, с. 1025
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (63) https://doi.org/10.1002/jcb.20131
  65. Averbeck, Negative control contributes to an extensive program of meiotic splicing in fission yeast, Mol. Cell, № 18, с. 491
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (64) https://doi.org/10.1016/j.molcel.2005.04.007
  66. Borgne, The G1/S Cyclin Cig2p during Meiosis in Fission Yeast, Mol. Biol. Cell, № 13, с. 2080
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (65) https://doi.org/10.1091/mbc.01-10-0507
  67. Schild, Meiotic effects of DNA-defective cell division cycle mutations of Saccharomyces cerevisiae, Chromosoma, № 70, с. 109
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (66) https://doi.org/10.1007/BF00292220
  68. Hollingsworth, Yeast pre-meiotic DNA replication utilizes mitotic origin ARS1 independently of CDC7 function, Chromosoma, № 102, с. 415
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (67) https://doi.org/10.1007/BF00360406
  69. Nakamura, Novel Fission Yeast Cdc7-Dbf4-Like Kinase Complex Required for the Initiation and Progression of Meiotic Second Division, Mol. Cell. Biol., № 22, с. 309
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (68) https://doi.org/10.1128/MCB.22.1.309-320.2002
  70. Kovacikova, A knockout screen for protein kinases required for the proper meiotic segregation of chromosomes in the fission yeast Schizosaccharomyces pombe, Cell Cycle, № 12, с. 618
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (69) https://doi.org/10.4161/cc.23513
  71. Donaldson, Molecular evolution allows bypass of the requirement for activation loop phosphorylation of the Cdc28 cyclin-dependent kinase, Mol. Cell. Biol., № 18, с. 2923
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (70) https://doi.org/10.1128/MCB.18.5.2923
  72. Kaldis, Localization and regulation of the cdk-activating kinase (Cak1p) from budding yeast, J. Cell Sci., № 111, с. 3585
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (71) https://doi.org/10.1242/jcs.111.24.3585
  73. Schwob, The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae, Cell, № 79, с. 233
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (72) https://doi.org/10.1016/0092-8674(94)90193-7
  74. Verma, Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase, Science, № 278, с. 455
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (73) https://doi.org/10.1126/science.278.5337.455
  75. Schindler, The Cdk-Activating Kinase Cak1p Promotes Meiotic S Phase through Ime2p, Mol. Cell. Biol., № 23, с. 8718
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (74) https://doi.org/10.1128/MCB.23.23.8718-8728.2003
  76. Murakami, Regulation of premeiotic S phase and recombination-related double-strand DNA breaks during meiosis in fission yeast, Nat. Genet., № 28, с. 290
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (75) https://doi.org/10.1038/90142
  77. Lindner, Essential role of MCM proteins in premeiotic DNA replication, Mol. Biol. Cell, № 13, с. 435
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (76) https://doi.org/10.1091/mbc.01-11-0537
  78. Ofir, The role and regulation of the preRC component Cdc6 in the initiation of premeiotic DNA replication, Mol. Biol. Cell, № 15, с. 2230
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (77) https://doi.org/10.1091/mbc.e03-08-0617
  79. Williamson, The timing of the S phase and other nuclear events in yeast meiosis, Exp. Cell Res., № 145, с. 209
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (78) https://doi.org/10.1016/S0014-4827(83)80022-6
  80. Cha, Progression of meiotic DNA replication is modulated by interchromosomal interaction proteins, negatively by Spo11p and positively by Rec8p, Genes Dev., № 14, с. 493
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (79) https://doi.org/10.1101/gad.14.4.493
  81. Heichinger, Genome-wide characterization of fission yeast DNA replication origins, EMBO J., № 25, с. 5171
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (80) https://doi.org/10.1038/sj.emboj.7601390
  82. Blitzblau, H.G., Chan, C.S., Hochwagen, A., and Bell, S.P. (2012). Separation of DNA replication from the assembly of break-competent meiotic chromosomes. PLoS Genet., 8.
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (81) https://doi.org/10.1371/journal.pgen.1002643
  83. Wu, Replication origin selection regulates the distribution of meiotic recombination, Mol. Cell, № 53, с. 655
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (82) https://doi.org/10.1016/j.molcel.2014.01.022
  84. Holm, The premeiotic DNA replication of euchromatin and heterochromatin in Lilium longiflorum (Thunb.), Carlsberg Res. Commun., № 42, с. 249
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (83) https://doi.org/10.1007/BF02910453
  85. Cho, CDC7 kinase phosphorylates serine residues adjacent to acidic amino acids in the minichromosome maintenance 2 protein, Proc. Natl. Acad. Sci. USA, № 103, с. 11521
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (84) https://doi.org/10.1073/pnas.0604990103
  86. Zegerman, Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast, Nature, № 445, с. 281
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (85) https://doi.org/10.1038/nature05432
  87. Tanaka, CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast, Nature, № 445, с. 328
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (86) https://doi.org/10.1038/nature05465
  88. Heller, Eukaryotic origin-dependent DNA replication in vitro reveals sequential action of DDK and S-CDK kinases, Cell, № 146, с. 80
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (87) https://doi.org/10.1016/j.cell.2011.06.012
  89. Yeeles, Regulated eukaryotic DNA replication origin firing with purified proteins, Nature, № 519, с. 431
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (88) https://doi.org/10.1038/nature14285
  90. Fragkos, DNA replication origin activation in space and time, Nat. Rev. Mol. Cell Biol., № 16, с. 360
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (89) https://doi.org/10.1038/nrm4002
  91. Picard, Newly assembled cyclin B-cdc2 kinase is required to suppress DNA replication between meiosis I and meiosis II in starfish oocytes, EMBO J., № 15, с. 3590
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (90) https://doi.org/10.1002/j.1460-2075.1996.tb00728.x
  92. Iwabuchi, Residual Cdc2 activity remaining at meiosis I exit is essential for meiotic M-M transition in Xenopus oocyte extracts, EMBO J., № 19, с. 4513
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (91) https://doi.org/10.1093/emboj/19.17.4513
  93. Nakajo, Absence of Wee1 ensures the meiotic cell cycle in Xenopus oocytes, Genes Dev., № 14, с. 328
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (92) https://doi.org/10.1101/gad.14.3.328
  94. Pesin, Regulation of APC/C activators in mitosis and meiosis, Annu. Rev. Cell Dev. Biol., № 24, с. 475
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (93) https://doi.org/10.1146/annurev.cellbio.041408.115949
  95. Cooper, Meiotic control of the APC/C: Similarities & differences from mitosis, Cell Div, № 6, с. 16
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (94) https://doi.org/10.1186/1747-1028-6-16
  96. Furuno, Suppression of DNA replication via Mos function during meiotic divisions in Xenopus oocytes, EMBO J., № 13, с. 2399
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (95) https://doi.org/10.1002/j.1460-2075.1994.tb06524.x
  97. Tachibana, c-Mos forces the mitotic cell cycle to undergo meiosis II to produce haploid gametes, Proc. Natl. Acad. Sci. USA, № 97, с. 14301
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (96) https://doi.org/10.1073/pnas.97.26.14301
  98. Hua, Sequential steps in DNA replication are inhibited to ensure reduction of ploidy in meiosis, Mol. Biol. Cell, № 24, с. 578
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (97) https://doi.org/10.1091/mbc.e12-11-0825
  99. Knockleby, Cdk1-mediated phosphorylation of Cdc7 suppresses DNA re-replication, Cell Cycle, № 15, с. 1494
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (98) https://doi.org/10.1080/15384101.2016.1176658
  100. Whitmire, Cdc6 synthesis regulates replication competence in Xenopus oocytes, Nature, № 419, с. 722
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (99) https://doi.org/10.1038/nature01032
  101. Murakami, Regulating the formation of DNA double-strand breaks in meiosis, Genes Dev., № 22, с. 286
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (100) https://doi.org/10.1101/gad.1642308
  102. Hochwagen, The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity, Cell, № 122, с. 861
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (101) https://doi.org/10.1016/j.cell.2005.07.010
  103. Tonami, A checkpoint control linking meiotic S phase and recombination initiation in fission yeast, Proc. Natl. Acad. Sci. USA, № 102, с. 5797
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (102) https://doi.org/10.1073/pnas.0407236102
  104. Ogino, Rad3-Cds1 mediates coupling of initiation of meiotic recombination with DNA replication. Mei4-dependent transcription as a potential target of meiotic checkpoint, J. Biol. Chem., № 281, с. 1338
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (103) https://doi.org/10.1074/jbc.M505767200
  105. Borde, Direct coupling between meiotic DNA replication and recombination initiation, Science, № 290, с. 806
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (104) https://doi.org/10.1126/science.290.5492.806
  106. Murakami, Correlation between premeiotic DNA replication and chromatin transition at yeast recombination initiation sites, Nucleic Acids Res., № 31, с. 4085
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (105) https://doi.org/10.1093/nar/gkg441
  107. Henderson, Cyclin-dependent kinase directly regulates initiation of meiotic recombination, Cell, № 125, с. 1321
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (106) https://doi.org/10.1016/j.cell.2006.04.039
  108. Matsumoto, Hsk1-Dfp1/Him1, the Cdc7-Dbf4 kinase in Schizosaccharomyces pombe, associates with Swi1, a component of the replication fork protection complex, J. Biol. Chem., № 280, с. 42536
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (107) https://doi.org/10.1074/jbc.M510575200
  109. Murakami, Temporospatial coordination of meiotic DNA replication and recombination via DDK recruitment to replisomes, Cell, № 158, с. 861
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (108) https://doi.org/10.1016/j.cell.2014.06.028
  110. Ceccaldi, Repair Pathway Choices and Consequences at the Double-Strand Break, Trends Cell Biol., № 26, с. 52
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (109) https://doi.org/10.1016/j.tcb.2015.07.009
  111. Lindner, Genome destabilization by hom*ologous recombination in the germ line, Nat. Rev. Mol. Cell Biol., № 11, с. 182
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (110) https://doi.org/10.1038/nrm2849
  112. Aylon, The CDK regulates repair of double-strand breaks by hom*ologous recombination during the cell cycle, EMBO J., № 23, с. 4868
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (111) https://doi.org/10.1038/sj.emboj.7600469
  113. Ira, DNA end resection, hom*ologous recombination and DNA damage checkpoint activation require CDK1, Nature, № 431, с. 1011
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (112) https://doi.org/10.1038/nature02964
  114. Ferreira, Two modes of DNA double-strand break repair are reciprocally regulated through the fission yeast cell cycle, Genes Dev., № 18, с. 2249
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (113) https://doi.org/10.1101/gad.315804
  115. Hentges, Cdk1 restrains NHEJ through phosphorylation of XRCC4-like factor Xlf1, Cell Rep., № 9, с. 2011
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (114) https://doi.org/10.1016/j.celrep.2014.11.044
  116. Heyer, Regulation of hom*ologous recombination in eukaryotes, Annu. Rev. Genet., № 44, с. 113
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (115) https://doi.org/10.1146/annurev-genet-051710-150955
  117. Ferretti, Controlling DNA-end resection: A new task for CDKs, Front. Genet., № 4, с. 99
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (116) https://doi.org/10.3389/fgene.2013.00099
  118. Huertas, CDK targets Sae2 to control DNA-end resection and hom*ologous recombination, Nature, № 455, с. 689
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (117) https://doi.org/10.1038/nature07215
  119. Huertas, Human CtIP mediates cell cycle control of DNA end resection and double strand break repair, J. Biol. Chem., № 284, с. 9558
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (118) https://doi.org/10.1074/jbc.M808906200
  120. Yun, CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle, Nature, № 459, с. 460
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (119) https://doi.org/10.1038/nature07955
  121. Matos, Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis, Cell, № 147, с. 158
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (120) https://doi.org/10.1016/j.cell.2011.08.032
  122. Saugar, Cell cycle-dependent regulation of the nuclease activity of Mus81-Eme1/Mms4, Nucleic Acids Res., № 40, с. 8325
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (121) https://doi.org/10.1093/nar/gks599
  123. Szakal, Premature Cdk1/Cdc5/Mus81 pathway activation induces aberrant replication and deleterious crossover, EMBO J., № 32, с. 1155
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (122) https://doi.org/10.1038/emboj.2013.67
  124. Clerici, The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends, J. Biol. Chem., № 280, с. 38631
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (123) https://doi.org/10.1074/jbc.M508339200
  125. Princz, Dbf4-dependent kinase and the Rtt107 scaffold promote Mus81-Mms4 resolvase activation during mitosis, EMBO J., № 36, с. 664
    Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (124) https://doi.org/10.15252/embj.201694831

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Roles of CDK and DDK in Genome Duplication and Maintenance: Meiotic Singularities (2024)

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