Casein Kinase 1 and Phosphorylation of Cohesin Subunit Rec11 (SA3) Promote Meiotic Recombination through Linear Element Formation

English version České info

The formation of haploid gametes (sex cells, such as eggs and sperm) from diploid precursor cells involves two nuclear divisions but one round of chromosomal replication. In the unique first meiotic division, centromeres of sister chromatids remain connected and homologous chromosomes (homologs) segregate from each other. In most species proper homolog segregation requires that crossover recombination occur between homologs to impart tension between homologs as they move apart. A protein kinase (casein kinase 1) has long been known to regulate proper sister centromere connections by phosphorylating Rec8, a meiosis-specific sister chromatid cohesin subunit. We report here that in fission yeast this kinase has a second critical role—to mediate phosphorylation of another meiosis-specific cohesin subunit Rec11. Phosphorylation of Rec11 enhances loading of two meiosis-specific components of linear elements, which are related to the synaptonemal complex and help pair homologs. These linear element proteins lead to high-level DNA breakage and crossovers between homologs. Thus, casein kinase regulates two crucial but separate events in meiosis. The mammalian functional homolog of Rec11, called STAG3, is also phosphorylated during meiosis and appears to be required for fertility in human females. These observations suggest wide-spread conservation of the roles of casein kinase 1 and Rec11 in ensuring proper meiotic chromosome segregation and sexual reproduction.

Vyšlo v časopise: Casein Kinase 1 and Phosphorylation of Cohesin Subunit Rec11 (SA3) Promote Meiotic Recombination through Linear Element Formation. PLoS Genet 11(5): e32767. doi:10.1371/journal.pgen.1005225
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005225

Souhrn

Zdroje

1. Phadnis N, Hyppa RW, Smith GR (2011) New and old ways to control meiotic recombination. Trends Genet 27: 411–421. doi: 10.1016/j.tig.2011.06.007 21782271

2. Li YF, Numata M, Wahls WP, Smith GR (1997) Region-specific meiotic recombination in S. pombe: the rec11 gene. Molecular Microbiology 23: 869–878. 9076725

3. Lin Y, Larson KL, Dorer R, Smith GR (1992) Meiotically induced rec7 and rec8 genes from Schizosaccharomyces pombe. Genetics 132: 75–85. 1339382

4. Nasmyth K, Haering CH (2005) The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74: 595–648. 15952899

5. Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y (2003) Distinct cohesin complexes organize meiotic chromosome domains. Science 300: 1152–1155. 12750522

6. Klein F, Mahr P, Galova M, Buonomo SBC, Michaelis C, et al. (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98: 91–103. 10412984

7. Howard-Till RA, Lukaszewicz A, Novatchkova M, Loidl J (2013) A single cohesin complex performs mitotic and meiotic functions in the protist tetrahymena. PLoS Genet 9: e1003418. doi: 10.1371/journal.pgen.1003418 23555314

8. Uhlmann F, Nasmyth K (1998) Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8: 1095–1101. 9778527

9. Gruber S, Haering CH, Nasmyth K (2003) Chromosomal cohesin forms a ring. Cell 112: 765–777. 12654244

10. Buonomo SB, Clyne RK, Fuchs J, Loidl J, Uhlmann F, et al. (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell 103: 387–398. 11081626

11. Brar GA, Kiburz BM, Zhang Y, Kim JE, White F, et al. (2006) Rec8 phosphorylation and recombination promote the step-wise loss of cohesins in meiosis. Nature 441: 532–536. 16672979

12. Ishiguro T, Tanaka K, Sakuno T, Watanabe Y (2010) Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase. Nat Cell Biol 12: 500–506. doi: 10.1038/ncb2052 20383139

13. Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400: 461–464. 10440376

14. Fowler KR, Gutiérrez-Velasco S, Martín-Castellanos C, Smith GR (2013) Protein determinants of meiotic DNA break hotspots. Molecular Cell 49: 983–996. doi: 10.1016/j.molcel.2013.01.008 23395004

15. Ponticelli AS, Smith GR (1989) Meiotic recombination-deficient mutants of Schizosaccharomyces pombe. Genetics 123: 45–54. 2806887

16. Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375–384. 9039264

17. Cromie GA, Smith GR (2008) Meiotic recombination in Schizosaccharomyces pombe: A paradigm for genetic and molecular analysis. In: Egel R, Lankenau D-H, editors. Recombination and meiosis: Models, means, and evolution. Berlin: Springer-Verlag. pp. 195–230.

18. Ellermeier C, Smith GR (2005) Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe. Proceedings of the National Academy of Sciences of the United States of America 102: 10952–10957. 16043696

19. Davis L, Rozalén AE, Moreno S, Smith GR, Martin-Castellanos C (2008) Rec25 and Rec27, novel components of meiotic linear elements, link cohesin to DNA breakage and recombination in fission yeast. Current Biology 18: 849–854. doi: 10.1016/j.cub.2008.05.025 18514516

20. Lorenz A, Wells JL, Pryce DW, Novatchkova FE, Eisenhaber F, et al. (2004) S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J Cell Sci 117: 3343–3351. 15226405

21. Estreicher A, Lorenz A, Loidl J (2012) Mug20, a novel protein associated with linear elements in fission yeast meiosis. Current Genetics 58: 119–127. doi: 10.1007/s00294-012-0369-3 22362333

22. Molnar M, Doll E, Yamamoto A, Hiraoka Y, Kohli J (2003) Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing. J Cell Sci 116: 1719–1731. 12665553

23. Rumpf C, Cipak L, Dudas A, Benko Z, Pozgajova M, et al. (2010) Casein kinase 1 is required for efficient removal of Rec8 during meiosis I. Cell Cycle 9: 2657–2662. doi: 10.4161/cc.9.13.12146 20581463

24. Krawchuk MD, DeVeaux LC, Wahls WP (1999) Meiotic chromosome dynamics dependent upon the rec8+, rec10+ and rec11+ genes of the fission yeast Schizosaccharomyces pombe. Genetics 153: 57–68. 10471700

25. DeVeaux LC, Smith GR (1994) Region-specific activators of meiotic recombination in Schizosaccharomyces pombe. Genes Development 8: 203–210. 8299939

26. Dhillon N, Hoekstra MF (1994) Characterization of two protein kinases from Schizosaccharomyces pombe involved in the regulation of DNA repair. EMBO Journal 13: 2777–2788. 8026462

27. Kearney PH, Ebert M, Kuret J (1994) Molecular cloning and sequence analysis of two novel fission yeast casein kinase-1 isoforms. Biochemical and Biophysical Research Communications 203: 231–236. 8074660

28. Gregan J, Zhang C, Rumpf C, Cipak L, Li Z, et al. (2007) Construction of conditional analog-sensitive kinase alleles in the fission yeast Schizosaccharomyces pombe. Nat Protoc 2: 2996–3000. 18007635

29. Bishop AC, Ubersax JA, Petsch DT, Matheos DP, Gray NS, et al. (2000) A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407: 395–401. 11014197

30. Davis L, Smith GR (2005) Dynein promotes achiasmate segregation in Schizosaccharomyces pombe. Genetics 170: 581–590. 15802518

31. Davis L, Smith GR (2003) Non-random homolog segregation at meiosis I in Schizosaccharomyces pombe mutants lacking recombination. Genetics 163: 857–874. 12663528

32. Rumpf C, Cipak L, Dudas A, Benko Z, Pozgajova M, et al. (2010) Casein kinase 1 is required for efficient removal of Rec8 during meiosis I. Cell Cycle 9: 2657–2662. doi: 10.4161/cc.9.13.12146 20581463

33. Farah JA, Cromie GA, Smith GR (2009) Ctp1 and Exonuclease 1, alternative nucleases regulated by the MRN complex, are required for efficient meiotic DNA repair and recombination. Proceedings of the National Academy of Sciences of the United States of America 106: 9356–9361. doi: 10.1073/pnas.0902793106 19470480

34. Cromie GA, Hyppa RW, Cam HP, Farah JA, Grewal SI, et al. (2007) A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLoS Genet 3: e141. 17722984

35. Young JA, Schreckhise RW, Steiner WW, Smith GR (2002) Meiotic recombination remote from prominent DNA break sites in S. pombe. Mol Cell 9: 253–263. 11864600

36. Brar GA, Hochwagen A, Ee LS, Amon A (2009) The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. Mol Biol Cell 20: 1030–1047. doi: 10.1091/mbc.E08-06-0637 19073884

37. Johnson AE, Chen JS, Gould KL (2013) CK1 is required for a mitotic checkpoint that delays cytokinesis. Current biology 23: 1920–1926. doi: 10.1016/j.cub.2013.07.077 24055157

38. 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. doi: 10.1016/j.molcel.2009.09.029 19917248

39. Tsukahara T, Tanno Y, Watanabe Y (2010) Phosphorylation of the CPC by Cdk1 promotes chromosome bi-orientation. Nature 467: 719–723. doi: 10.1038/nature09390 20739936

40. Rumpf C, Cipak L, Dudas A, Benko Z, Pozgajova M, et al. (2010) Casein kinase 1 is required for efficient removal of Rec8 during meiosis I. Cell Cycle 9 2657–62. doi: 10.4161/cc.9.13.12146 20581463.

41. Kitajima TS, Miyazaki Y, Yamamoto M, Watanabe Y (2003) Rec8 cleavage by separase is required for meiotic nuclear divisions in fission yeast. Embo J 22: 5643–5653. 14532136

42. Ding DQ, Sakurai N, Katou Y, Itoh T, Shirahige K, et al. (2006) Meiotic cohesins modulate chromosome compaction during meiotic prophase in fission yeast. J Cell Biol 174: 499–508. 16893973

43. Sakuno T, Watanabe Y (2015) Phosphorylation of cohesin Rec11/SA3 by casein kinase 1 promotes homologous recombination by assembling the meiotic chromosome axis. Dev Cell 32: 220–230. doi: 10.1016/j.devcel.2014.11.033 25579976

44. Stern B, Nurse P (1996) A quantitative model for the cdc2 control of S phase and mitosis in fission yeast. Trends Genet 12: 345–350. 8855663

45. Henderson KA, Kee K, Maleki S, Santini PA, Keeney S (2006) Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125: 1321–1332. 16814718

46. Mata J, Lyne R, Burns G, Bahler J (2002) The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32: 143–147. 12161753

47. Fowler KR, Sasaki M, Milman N, Keeney S, Smith GR (2014) Evolutionarily diverse determinants of meiotic DNA break and recombination landscapes across the genome. Genome Research 24 1650–1664. doi: 10.1101/gr.172122.114 25024163

48. Wood AJ, Severson AF, Meyer BJ (2010) Condensin and cohesin complexity: the expanding repertoire of functions. Nat Rev Genet 11: 391–404. doi: 10.1038/nrg2794 20442714

49. Petronczki M, Siomos MF, Nasmyth K (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112: 423–440. 12600308

50. Winters T, McNicoll F, Jessberger R (2014) Meiotic cohesin STAG3 is required for chromosome axis formation and sister chromatid cohesion. EMBO J 33: 1256–1270. doi: 10.1002/embj.201387330 24797474

51. Fukuda T, Fukuda N, Agostinho A, Hernandez-Hernandez A, Kouznetsova A, et al. (2014) STAG3-mediated stabilization of REC8 cohesin complexes promotes chromosome synapsis during meiosis. EMBO J 33: 1243–1255. doi: 10.1002/embj.201387329 24797475

52. Prieto I, Suja JA, Pezzi N, Kremer L, Martinez AC, et al. (2001) Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nature Cell Biology 3: 761–766. 11483963

53. Fukuda T, Pratto F, Schimenti JC, Turner JM, Camerini-Otero RD, et al. (2012) Phosphorylation of chromosome core components may serve as axis marks for the status of chromosomal events during mammalian meiosis. PLoS Genet 8: e1002485. doi: 10.1371/journal.pgen.1002485 22346761

54. Hopkins J, Hwang G, Jacob J, Sapp N, Bedigian R, et al. (2014) Meiosis-specific cohesin component, Stag3 is essential for maintaining centromere chromatid cohesion, and required for DNA repair and synapsis between homologous chromosomes. PLoS Genet 10: e1004413. doi: 10.1371/journal.pgen.1004413 24992337

55. Llano E, Gomez HL, Garcia-Tunon I, Sanchez-Martin M, Caburet S, et al. (2014) STAG3 is a strong candidate gene for male infertility. Hum Mol Genet 23: 3421–3431. doi: 10.1093/hmg/ddu051 24608227

56. Caburet S, Arboleda VA, Llano E, Overbeek PA, Barbero JL, et al. (2014) Mutant cohesin in premature ovarian failure. N Engl J Med 370: 943–949. doi: 10.1056/NEJMoa1309635 24597867

57. Smith GR (2009) Genetic analysis of meiotic recombination in Schizosaccharomyces pombe. In: Keeney S, editor. Meiosis. Totowa, NJ: Humana Press. pp. 65–76.

58. Hyppa RW, Smith GR (2009) Using Schizosaccharomyces pombe meiosis to analyze DNA recombination intermediates. In: Keeney S, editor. Meiosis. Totowa, NJ: Humana Press. pp. 235–252.

59. Cipak L, Spirek M, Novatchkova M, Chen Z, Rumpf C, et al. (2009) An improved strategy for tandem affinity purification-tagging of Schizosaccharomyces pombe genes. Proteomics 9: 4825–4828. doi: 10.1002/pmic.200800948 19750511

60. Young JA, Schreckhise RW, Steiner WW, Smith GR (2002) Meiotic recombination remote from prominent DNA break sites in S. pombe. Molecular Cell 9: 253–263. 11864600

61. Steiner WW, Schreckhise RW, Smith GR (2002) Meiotic DNA breaks at the S. pombe recombination hotspot M26. Molecular Cell 9: 847–855 11983175

62. Grishchuk AL, Kohli J (2003) Five RecA-like proteins of Schizosaccharomyces pombe are involved in meiotic recombination. Genetics 165: 1031–1043. 14668362

63. Farah JA, Cromie G, Davis L, Steiner WW, Smith GR (2005) Activation of an alternative, Rec12 (Spo11)-independent pathway of fission yeast meiotic recombination in the absence of a DNA flap endonuclease. Genetics 171: 1499–1511. 16118186

64. Lin Y, Smith GR (1994) Transient meiosis-induced expression of the rec6 and rec12 genes of Schizosaccharomyces pombe. Genetics 136: 769–779. 8005432