Abstract
During meiosis, a single round of genome duplication is followed by two sequential rounds of chromosome segregation. Through this process, a diploid parent cell generates gametes with a haploid set of chromosomes. A characteristic of meiotic chromosome segregation is a stepwise loss of sister chromatid cohesion along chromosomal arms and at centromeres. Whereas arm cohesion plays an important role in ensuring homologue disjunction at meiosis I, persisting cohesion at pericentromeric regions throughout meiosis I is essential for the faithful equational segregation of sisters in the following meiosis II, similar to mitosis. A widely conserved pericentromeric protein called shugoshin, which associates with protein phosphatase 2A (PP2A), plays a critical role in this protection of cohesin. Another key aspect of meiosis I is the establishment of monopolar attachment of sister kinetochores to spindle microtubules. Cohesion or physical linkage at the core centromeres, where kinetochores assemble, may conjoin sister kinetochores, leading to monopolar attachment. A meiosis-specific kinetochore factor such as fission yeast Moa1 or budding yeast monopolin contributes to this regulation. We propose that cohesion at the core centromere and pericentromeric regions plays distinct roles, especially in defining the orientation of kinetochores.
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Abbreviations
- CK1δ/ɛ:
-
casein kinase 1 δ/ɛ
- HP1:
-
heterochromatin protein 1
- MCAK:
-
mitotic centromere-associated kinesin
- MEF:
-
mouse embryonic fibroblast
- PP2A:
-
protein phosphatase 2A
- SMC:
-
structural maintenance of chromosome
References
Bernard P, Maure JF, Javerzat JP (2001) Fission yeast Bub1 is essential in setting up the meiotic pattern of chromosome segregation. Nat Cell Biol 3:522–526
Brar GA, Kiburz BM, Zhang Y, Kim JE, White F, Amon A (2006) Rec8 phosphorylation and recombination promote the step-wise loss of cohesins in meiosis. Nature 441:532–536
Chelysheva L, Diallo S, Vezon D et al (2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118:4621–4632
Clyne RK, Katis VL, Jessop L et al (2003) Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat Cell Biol 5:480–485
Davis BK (1971) Genetic analysis of a meiotic mutant resulting in precocious sister-centromere separation in Drosophila melanogaster. Mol Gen Genet 113:251–272
DeVeaux LC, Smith GR (1994) Region-specific activators of meiotic recombination in Schizosaccharomyces pombe. Genes Dev 8:203–210
Gandhi R, Gillespie PJ, Hirano T (2006) Human Wapl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase. Curr Biol 16:2406–2417
Goldstein LS (1981) Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. Cell 25:591–602
Gregan J, Riedel CG, Pidoux AL et al (2007) The kinetochore proteins Pcs1 and Mde4 and heterochromatin are required to prevent merotelic orientation. Curr Biol 17:1190–1200
Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K (2008) The cohesin ring concatenates sister DNA molecules. Nature 454:297–301
Hauf S, Waizenegger IC, Peters JM (2001) Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 293:1320–1323
Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, Peters JM (2005) Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. Plos Biol 3:e69
Hauf S, Biswas A, Langegger M, Kawashima SA, Tsukahara T, Watanabe Y (2007) Aurora controls sister kinetochore mono-orientation and homolog bi-orientation in meiosis-I. EMBO J 26:4475–4486
Huang H, Feng J, Famulski J et al (2007) Tripin/hSgo2 recruits MCAK to the inner centromere to correct defective kinetochore attachments. J Cell Biol 177:413–424
Indjeian VB, Stern BM, Murray AW (2005) The centromeric protein Sgo1 is required to sense lack of tension on mitotic chromosomes. Science 307:130–133
Kawashima SA, Tsukahara T, Langegger M, Hauf S, Kitajima TS, Watanabe Y (2007) Shugoshin enables tension-generating attachment of kinetochores by loading Aurora to centromeres. Genes Dev 21:420–435
Kerrebrock AW, Miyazaki WY, Birnby D, Orr-Weaver TL (1992) The Drosophila mei-S332 gene promotes sister-chromatid cohesion in meiosis following kinetochore differentiation. Genetics 130:827–841
Kerrebrock AW, Moore DP, Wu JS, Orr-Weaver TL (1995) MEI-S332, a Drosophila protein required for sister-chromatid cohesion, can localize to meiotic centromere regions. Cell 83:247–256
Kiburz BM, Reynolds DB, Megee PC et al (2005) The core centromere and Sgo1 establish a 50-kb cohesin-protected domain around centromeres during meiosis I. Genes Dev 19:3017–3030
Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427:510–517
Kitajima TS, Hauf S, Ohsugi M, Yamamoto T, Watanabe Y (2005) Human Bub1 defines the persistent cohesion site along the mitotic chromosome by affecting Shugoshin localization. Curr Biol 15:353–359
Kitajima TS, Sakuno T, Ishiguro K et al (2006) Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441:46–52
Klein F, Mahr P, Galova M et al (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, recombination during yeast meiosis. Cell 98:91–103
Kueng S, Hegemann B, Peters BH et al (2006) Wapl controls the dynamic association of cohesin with chromatin. Cell 127:955–967
Lee BH, Amon A (2003) Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation. Science 300:482–486
Lee J, Miyano T, Dai Y, Wooding P, Yen TJ, Moor RM (2000) Specific regulation of CENP-E and kinetochores during meiosis I/meiosis II transition in pig oocytes. Mol Rep Dev 56:51–62
Lee J, Kitajima TS, Tanno Y et al (2008) Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol 10:42–52
Llano E, Gomez R, Gutierrez-Caballero C et al (2008) Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice. Genes Dev 22:2400–2413
Lorenz A, Wells JL, Pryce DW et al (2004) S pombe meiotic linear elements contain proteins related to synaptonemal complex components. J Cell Sci 117:3343–3351
Losada A, Hirano M, Hirano T (2002) Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev 16:3004–3016
Mailhes JB, Hilliard C, Fuseler JW, London SN (2003) Okadaic acid, an inhibitor of protein phosphatase 1 and 2A, induces premature separation of sister chromatids during meiosis I and aneuploidy in mouse oocytes in vitro. Chromosome Res 11:619–631
Marston AL, Tham WH, Shah H, Amon A (2004) A genome-wide screen identifies genes required for centromeric cohesion. Science 303:1367–1370
McGuinness BE, Hirota T, Kudo NR, Peters JM, Nasmyth K (2005) Shugoshin prevents dissociation of cohesin from centromeres during mitosis in vertebrate cells. Plos Biol 3:e86
Monje-Casas F, Prabhu VR, Lee BH, Boselli M, Amon A (2007) Kinetochore orientation during meiosis is controlled by Aurora B and the monopolin complex. Cell 128:477–490
Moore DP, Orr-Weaver TL (1998) Chromosome segregation during meiosis: building an unambivalent bivalent. Curr Top Dev Biol 37:263–299
Nasmyth K (2001) Disseminating the genome: joining, resolving, separating sister chromatids during mitosis and meiosis. Annu Rev Genet 35:673–745
Nicklas RB (1997) How cells get the right chromosomes. Science 275:632–637
Parisi S, McKay MJ, Molnar M et al (1999) Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol 19:3515–3528
Parra MT, Viera A, Gomez R et al (2004) Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J Cell Sci 117:1221–1234
Petronczki M, Matos J, Mori S et al (2006) Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 126:1049–1064
Rabitsch KP, Petronczki M, Javerzat JP et al (2003) Kinetochore recruitment of two nucleolar proteins is required for homolog segregation in meiosis I. Dev Cell 4:535–548
Rabitsch KP, Gregan J, Schleiffer A, Javerzat JP, Eisenhaber F, Nasmyth K (2004) Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II. Curr Biol 14:287–301
Riedel CG, Katis VL, Katou Y et al (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441:53–61
Sumara I, Vorlaufer E, Stukenberg PT et al (2002) The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol Cell 9:515–525
Tanaka TU (2002) Bi-orienting chromosomes on the mitotic spindle. Curr Opni Cell Biol 14:365–371
Tang Z, Sun Y, Harley SE, Zou H, Yu H (2004) Human Bub1 protects centromeric sister-chromatid cohesion through Shugoshin during mitosis. Proc Natl Acad Sci U S A 101:18012–18017
Tang Z, Shu H, Qi W, Mahmood NA, Mumby MC, Yu H (2006) PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation. Dev Cell 10:575–585
Toth A, Rabitsch KP, Galova M, Schleiffer A, Buonomo SB, Nasmyth K (2000) Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis I. Cell 103:1155–1168
Uhlmann F (2003) Chromosome cohesion and separation: from men and molecules. Curr Biol 13:R104–114
Watanabe Y (2006) A one-sided view of kinetochore attachment in meiosis. Cell 126:1030–1032
Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464
Winey M, Morgan GP, Straight PD, Giddings TH Jr, Mastronarde DN (2005) Three-dimensional ultrastructure of Saccharomyces cerevisiae meiotic spindles. Mol Biol Cell 16:1178–1188
Yamagishi Y, Sakuno T, Shimura M, Watanabe Y (2008) Heterochromatin links to centromeric protection by recruiting shugoshin. Nature 455:251–255
Yokobayashi S, Watanabe Y (2005) The kinetochore protein Moa1 enables cohesion-mediated monopolar attachment at meiosis I. Cell 123:803–817
Yokobayashi S, Yamamoto M, Watanabe Y (2003) Cohesins determine the attachment manner of kinetochores to spindle microtubules at meiosis I in fission yeast. Mol Cell Biol 23:3965–3973
Yu HG, Dawe RK (2000) Functional redundancy in the maize meiotic kinetochore. J Cell Biol 151:131–142
Acknowledgements
We apologize to those researchers whose work was not cited or discussed owing to space limitations. This work was supported in part by a Special Coordination Funds for Promoting Science and Technology (to T.S.) and a Grant-in-Aid for Specially Promoted Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to Y.W.).
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Sakuno, T., Watanabe, Y. Studies of meiosis disclose distinct roles of cohesion in the core centromere and pericentromeric regions. Chromosome Res 17, 239–249 (2009). https://doi.org/10.1007/s10577-008-9013-y
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DOI: https://doi.org/10.1007/s10577-008-9013-y