Abstract
Meiosis is a specialised cell division process for generating gametes. In contrast to mitosis, meiosis involves recombination followed by two consecutive rounds of cell division, meiosis I and II. A vast field of research has been devoted to understanding the differences between mitotic and meiotic cell divisions from the viewpoint of chromosome behaviour. For faithful inheritance of paternal and maternal genetic information to offspring, two events are indispensable: meiotic recombination, which generates a physical link between homologous chromosomes, and reductional segregation, in which homologous chromosomes move towards opposite poles, thereby halving the ploidy. The cytoskeleton and its regulators play specialised roles in meiosis to accomplish these divisions. Recent studies have shown that microtubule-associated proteins (MAPs), including tumour overexpressed gene (TOG), play unique roles during meiosis. Furthermore, the conserved mitotic protein kinase Polo modulates MAP localisation in meiosis I. As Polo is a well-known regulator of reductional segregation in meiosis, the evidence suggests that Polo constitutes a plausible link between meiosis-specific MAP functions and reductional segregation. Here, we review the latest findings on how the localisation and regulation of MAPs in meiosis differ from those in mitosis, and we discuss conservation of the system between yeast and higher eukaryotes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Al-Bassam J, Chang F (2011) Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol 21:604–614. doi:10.1016/j.tcb.2011.06.007
Amelina H, Subramaniam S, Moiseeva V, Armstrong CA, Pearson SR, Tomita K (2015) Telomere protein Rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation. BMC Biol 13:37. doi:10.1186/s12915-015-0149-x
Aoki K, Nakaseko Y, Kinoshita K, Goshima G, Yanagida M (2006) Cdc2 phosphorylation of the fission yeast Dis1 ensures accurate chromosome segregation. Curr Biol 16:1627–1635. doi:10.1016/j.cub.2006.06.065
Asakawa H, Hayashi A, Haraguchi T, Hiraoka Y (2005) Dissociation of the Nuf2-Ndc80 complex releases centromeres from the spindle-pole body during meiotic prophase in fission yeast. Mol Biol Cell 16:2325–2338. doi:10.1091/mbc.E04-11-0996
Bähler J, Steever AB, Wheatley S, Wang Y, Pringle JR, Gould KL, McCollum D (1998) Role of polo kinase and Mid1p in determining the site of cell division in fission yeast. J Cell Biol 143:1603–1616. doi:10.1083/jcb.143.6.1603
Brouhard GJ et al (2008) XMAP215 is a processive microtubule polymerase. Cell 132:79–88. doi:10.1016/j.cell.2007.11.043
Bucciarelli E, Pellacani C, Naim V, Palena A, Gatti M, Somma MP (2009) Drosophila Dgt6 interacts with Ndc80, Msps/XMAP215, and gamma-tubulin to promote kinetochore-driven MT formation. Curr Biol 19:1839–1845. doi:10.1016/j.cub.2009.09.043
Buttrick GJ, Lancaster TC, Meadows JC, Millar JB (2012) Plo1 phosphorylates Dam1 to promote chromosome bi-orientation in fission yeast. J Cell Sci 125:1645–1651. doi:10.1242/jcs.096826
Cao L, Alani E, Kleckner N (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61:1089–1101
Chan YW, Jeyaprakash AA, Nigg EA, Santamaria A (2012) Aurora B controls kinetochore-microtubule attachments by inhibiting Ska complex-KMN network interaction. J Cell Biol 196:563–571. doi:10.1083/jcb.201109001
Cheeseman IM et al (2002) Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111:163–172
Cheeseman IM et al (2001) Implication of a novel multiprotein Dam1p complex in outer kinetochore function. J Cell Biol 155:1137–1145. doi:10.1083/jcb.200109063
Chikashige Y, Ding DQ, Funabiki H, Haraguchi T, Mashiko S, Yanagida M, Hiraoka Y (1994) Telomere-led premeiotic chromosome movement in fission yeast. Science 264:270–273
Chikashige Y, Tsutsumi C, Yamane M, Okamasa K, Haraguchi T, Hiraoka Y (2006) Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125:59–69. doi:10.1016/j.cell.2006.01.048
Clyne RK, Katis VL, Jessop L, Benjamin KR, Herskowitz I, Lichten M, Nasmyth K (2003) Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat Cell Biol 5:480–485. doi:10.1038/ncb977
Colombie N, Gluszek AA, Meireles AM, Ohkura H (2013) Meiosis-specific stable binding of augmin to acentrosomal spindle poles promotes biased microtubule assembly in oocytes. PLoS Genet 9:e1003562. doi:10.1371/journal.pgen.1003562
Conrad MN et al (2008) Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133:1175–1187. doi:10.1016/j.cell.2008.04.047
Cullen CF, Ohkura H (2001) Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nat Cell Biol 3:637–642. doi:10.1038/35083025
Elowe S, Hummer S, Uldschmid A, Li X, Nigg EA (2007) Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev 21:2205–2219. doi:10.1101/gad.436007
Enquist-Newman M, Cheeseman IM, Van Goor D, Drubin DG, Meluh PB, Barnes G (2001) Dad1p, third component of the Duo1p/Dam1p complex involved in kinetochore function and mitotic spindle integrity. Mol Biol Cell 12:2601–2613
Franco A, Meadows JC, Millar JB (2007) The Dam1/DASH complex is required for the retrieval of unclustered kinetochores in fission yeast. J Cell Sci 120:3345–3351. doi:10.1242/jcs.013698
Fujita I et al (2012) Telomere-nuclear envelope dissociation promoted by Rap1 phosphorylation ensures faithful chromosome segregation. Curr Biol 22:1932–1937. doi:10.1016/j.cub.2012.08.019
Funabiki H, Hagan I, Uzawa S, Yanagida M (1993) Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J Cell Biol 121:961–976
Funaya C et al (2012) Transient structure associated with the spindle pole body directs meiotic microtubule reorganization in S. pombe. Curr Biol 22:562–574. doi:10.1016/j.cub.2012.02.042
Gachet Y, Reyes C, Courtheoux T, Goldstone S, Gay G, Serrurier C, Tournier S (2008) Sister kinetochore recapture in fission yeast occurs by two distinct mechanisms, both requiring Dam1 and Klp2. Mol Biol Cell 19:1646–1662. doi:10.1091/mbc.E07-09-0910
Garcia MA, Vardy L, Koonrugsa N, Toda T (2001) Fission yeast ch-TOG/XMAP215 homologue Alp14 connects mitotic spindles with the kinetochore and is a component of the Mad2-dependent spindle checkpoint. EMBO J 20:3389–3401
Gergely F, Draviam VM, Raff JW (2003) The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 17:336–341. doi:10.1101/gad.245603
Giroux CN, Dresser ME, Tiano HF (1989) Genetic control of chromosome synapsis in yeast meiosis. Genome 31:88–94
Glover DM, Hagan IM, Tavares AA (1998) Polo-like kinases: a team that plays throughout mitosis. Genes Dev 12:3777–3787
Goshima G, Mayer M, Zhang N, Stuurman N, Vale RD (2008) Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J Cell Biol 181:421–429. doi:10.1083/jcb.200711053
Hanisch A, Sillje HH, Nigg EA (2006) Timely anaphase onset requires a novel spindle and kinetochore complex comprising Ska1 and Ska2. Embo J 25:5504–5515. doi:10.1038/sj.emboj.7601426
Hayashi A, Asakawa H, Haraguchi T, Hiraoka Y (2006) Reconstruction of the kinetochore during meiosis in fission yeast Schizosaccharomyces pombe. Mol Biol Cell 17:5173–5184. doi:10.1091/mbc.E06-05-0388
Hayashi A, Ogawa H, Kohno K, Gasser SM, Hiraoka Y (1998) Meiotic behaviours of chromosomes and microtubules in budding yeast: relocalization of centromeres and telomeres during meiotic prophase. Genes Cells 3:587–601
Hofmann C, Cheeseman IM, Goode BL, McDonald KL, Barnes G, Drubin DG (1998) Saccharomyces cerevisiae Duo1p and Dam1p, novel proteins involved in mitotic spindle function. J Cell Biol 143:1029–1040
Hou H et al (2012) Csi1 links centromeres to the nuclear envelope for centromere clustering. J Cell Biol 199:735–744. doi:10.1083/jcb.201208001
Hsu KS, Toda T (2011) Ndc80 internal loop interacts with Dis1/TOG to ensure proper kinetochore-spindle attachment in fission yeast. Curr Biol 21:214–220. doi:10.1016/j.cub.2010.12.048
Hughes SE et al (2011) Gamma-tubulin is required for bipolar spindle assembly and for proper kinetochore microtubule attachments during prometaphase I in Drosophila oocytes. PLoS Genet 7, e1002209. doi:10.1371/journal.pgen.1002209
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
Jin Q, Trelles-Sticken E, Scherthan H, Loidl J (1998) Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J Cell Biol 141:21–29
Jin QW, Fuchs J, Loidl J (2000) Centromere clustering is a major determinant of yeast interphase nuclear organization. J Cell Sci 113(Pt 11):1903–1912
Kakui Y, Sato M, Okada N, Toda T, Yamamoto M (2013) Microtubules and Alp7-Alp14 (TACC-TOG) reposition chromosomes before meiotic segregation. Nat Cell Biol 15:786–796. doi:10.1038/ncb2782
Kalantzaki M, Kitamura E, Zhang T, Mino A, Novak B, Tanaka TU (2015) Kinetochore-microtubule error correction is driven by differentially regulated interaction modes. Nat Cell Biol doi:10.1038/ncb3128
Katis VL, Matos J, Mori S, Shirahige K, Zachariae W, Nasmyth K (2004) Spo13 facilitates monopolin recruitment to kinetochores and regulates maintenance of centromeric cohesion during yeast meiosis. Curr Biol 14:2183–2196. doi:10.1016/j.cub.2004.12.020
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
Kim J et al (2015) Meikin is a conserved regulator of meiosis-I-specific kinetochore function. Nature 517:466–471. doi:10.1038/nature14097
Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427:510–517. doi:10.1038/nature02312
Kitajima TS, Ohsugi M, Ellenberg J (2011) Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 146:568–581. doi:10.1016/j.cell.2011.07.031
Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, Watanabe Y (2006) Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441:46–52. doi:10.1038/nature04663
Kitamura E, Tanaka K, Komoto S, Kitamura Y, Antony C, Tanaka TU (2010) Kinetochores generate microtubules with distal plus ends: their roles and limited lifetime in mitosis. Dev Cell 18:248–259. doi:10.1016/j.devcel.2009.12.018
Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98:91–103. doi:10.1016/S0092-8674(00)80609-1
Krapp A, Collin P, Cokoja A, Dischinger S, Cano E, Simanis V (2006) The Schizosaccharomyces pombe septation initiation network (SIN) is required for spore formation in meiosis. J Cell Sci 119:2882–2891. doi:10.1242/jcs.03025
Lacefield S, Lau DT, Murray AW (2009) Recruiting a microtubule-binding complex to DNA directs chromosome segregation in budding yeast. Nat Cell Biol 11:1116–1120. doi:10.1038/ncb1925
Lacefield S, Murray AW (2007) The spindle checkpoint rescues the meiotic segregation of chromosomes whose crossovers are far from the centromere. Nat Genet 39:1273–1277. doi:10.1038/ng2120
Lam I, Keeney S (2015) Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb Perspect Biol 7:a016634. doi:10.1101/cshperspect.a016634
Lee BH, Kiburz BM, Amon A (2004) Spo13 maintains centromeric cohesion and kinetochore coorientation during meiosis I. Curr Biol 14:2168–2182. doi:10.1016/j.cub.2004.12.033
Lee J et al (2008) Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol 10:42–52. doi:10.1038/ncb1667
Lee MJ, Gergely F, Jeffers K, Peak-Chew SY, Raff JW (2001) Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nat Cell Biol 3:643–649. doi:10.1038/35083033
Li Y, Bachant J, Alcasabas AA, Wang Y, Qin J, Elledge SJ (2002) The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev 16:183–197. doi:10.1101/gad.959402
Llano E 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. doi:10.1101/gad.475308
Magidson V, O’Connell CB, Loncarek J, Paul R, Mogilner A, Khodjakov A (2011) The spatial arrangement of chromosomes during prometaphase facilitates spindle assembly. Cell 146:555–567. doi:10.1016/j.cell.2011.07.012
Maure JF et al (2011) The Ndc80 loop region facilitates formation of kinetochore attachment to the dynamic microtubule plus end. Curr Biol 21:207–213. doi:10.1016/j.cub.2010.12.050
Meyer RE, Kim S, Obeso D, Straight PD, Winey M, Dawson DS (2013) Mps1 and Ipl1/Aurora B act sequentially to correctly orient chromosomes on the meiotic spindle of budding yeast. Science 339:1071–1074. doi:10.1126/science.1232518
Miller MP, Amon A, Unal E (2013) Meiosis I: when chromosomes undergo extreme makeover. Curr Opin Cell Biol 25:687–696. doi:10.1016/j.ceb.2013.07.009
Morimoto A, Shibuya H, Zhu X, Kim J, Ishiguro K, Han M, Watanabe Y (2012) A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J Cell Biol 198:165–172. doi:10.1083/jcb.201204085
Mulvihill DP, Petersen J, Ohkura H, Glover DM, Hagan IM (1999) Plo1 kinase recruitment to the spindle pole body and its role in cell division in Schizosaccharomyces pombe. Mol Biol Cell 10:2771–2785. doi:10.1091/mbc.10.8.2771
Nakaseko Y, Goshima G, Morishita J, Yanagida M (2001) M phase-specific kinetochore proteins in fission yeast: microtubule-associating Dis1 and Mtc1 display rapid separation and segregation during anaphase. Curr Biol 11:537–549
Nigg EA (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2:21–32. doi:10.1038/35048096
Ohkura H, Garcia MA, Toda T (2001) Dis1/TOG universal microtubule adaptors—one MAP for all? J Cell Sci 114:3805–3812
Okada N, Toda T, Yamamoto M, Sato M (2014) CDK-dependent phosphorylation of Alp7-Alp14 (TACC-TOG) promotes its nuclear accumulation and spindle microtubule assembly. Mol Biol Cell 25(13):1969–1982. doi:10.1091/mbc.E13-11-0679
Peset I, Seiler J, Sardon T, Bejarano LA, Rybina S, Vernos I (2005) Function and regulation of Maskin, a TACC family protein, in microtubule growth during mitosis. J Cell Biol 170:1057–1066
Peset I, Vernos I (2008) The TACC proteins: TACC-ling microtubule dynamics and centrosome function. Trends Cell Biol 18:379–388. doi:10.1016/j.tcb.2008.06.005
Petronczki M, Siomos MF, Nasmyth K (2003) Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–440
Rabl C (1885) über Zellteilung. Morphol Jahrbuch 10:214–330
Riedel CG et al (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441:53–61. doi:10.1038/nature04664
Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975–987
Roque H, Ward JJ, Murrells L, Brunner D, Antony C (2010) The fission yeast XMAP215 homolog Dis1p is involved in microtubule bundle organization. PLoS One 5, e14201. doi:10.1371/journal.pone.0014201
Saito TT, Tougan T, Okuzaki D, Kasama T, Nojima H (2005) Mcp6, a meiosis-specific coiled-coil protein of Schizosaccharomyces pombe, localizes to the spindle pole body and is required for horsetail movement and recombination. J Cell Sci 118:447–459. doi:10.1242/jcs.01629
Sakuno T, Tanaka K, Hauf S, Watanabe Y (2011) Repositioning of aurora B promoted by chiasmata ensures sister chromatid mono-orientation in meiosis I. Dev Cell 21:534–545. doi:10.1016/j.devcel.2011.08.012
Sanchez-Perez I et al (2005) The DASH complex and Klp5/Klp6 kinesin coordinate bipolar chromosome attachment in fission yeast. EMBO J 24:2931–2943. doi:10.1038/sj.emboj.7600761
Sato M, Okada N, Kakui Y, Yamamoto M, Yoshida M, Toda T (2009) Nucleocytoplasmic transport of Alp7/TACC organizes spatiotemporal microtubule formation in fission yeast. EMBO Rep 10:1161–1167. doi:10.1038/embor.2009.158
Sato M, Toda T (2007) Alp7/TACC is a crucial target in Ran-GTPase-dependent spindle formation in fission yeast. Nature 447:334–337. doi:10.1038/nature05773
Sato M, Vardy L, Garcia MA, Koonrugsa N, Toda T (2004) Interdependency of fission yeast Alp14/TOG and coiled coil protein Alp7 in microtubule localization and bipolar spindle formation. Mol Biol Cell 15:1609–1622
Savoian MS, Glover DM (2014) Differing requirements for Augmin in male meiotic and mitotic spindle formation in Drosophila. Open Biol 4:140047. doi:10.1098/rsob.140047
Schatten G (1994) The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 165:299–335. doi:10.1006/dbio.1994.1256
Scherthan H (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2:621–627. doi:10.1038/35085086
Schmidt JC et al (2012) The kinetochore-bound Ska1 complex tracks depolymerizing microtubules and binds to curved protofilaments. Dev Cell 23:968–980. doi:10.1016/j.devcel.2012.09.012
Schuh M, Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130:484–498. doi:10.1016/j.cell.2007.06.025
Sharif WD, Glick GG, Davidson MK, Wahls WP (2002) Distinct functions of S. pombe Rec12 (Spo11) protein and Rec12-dependent crossover recombination (chiasmata) in meiosis I; and a requirement for Rec12 in meiosis II. Cell Chromosome 1:1
Shibuya H, Ishiguro K, Watanabe Y (2014) The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis. Nat Cell Biol 16:145–156. doi:10.1038/ncb2896
Solc P et al (2015) Multiple requirements of PLK1 during mouse oocyte maturation. PLoS One 10:e0116783. doi:10.1371/journal.pone.0116783
Tanaka K, Kitamura E, Kitamura Y, Tanaka TU (2007) Molecular mechanisms of microtubule-dependent kinetochore transport toward spindle poles. J Cell Biol 178:269–281. doi:10.1083/jcb.200702141
Tanaka K, Kohda T, Yamashita A, Nonaka N, Yamamoto M (2005a) Hrs1p/Mcp6p on the meiotic SPB organizes astral microtubule arrays for oscillatory nuclear movement. Curr Biol 15:1479–1486. doi:10.1016/j.cub.2005.07.058
Tanaka K et al (2005b) Molecular mechanisms of kinetochore capture by spindle microtubules. Nature 434:987–994
Tanaka TU, Stark MJ, Tanaka K (2005c) Kinetochore capture and bi-orientation on the mitotic spindle. Nat Rev Mol Cell Biol 6:929–942. doi:10.1038/nrm1764
Tang NH, Takada H, Hsu KS, Toda T (2013) The internal loop of fission yeast Ndc80 binds Alp7/TACC-Alp14/TOG and ensures proper chromosome attachment. Mol Biol Cell 24:1122–1133. doi:10.1091/mbc.E12-11-0817
Tang NH, Toda T (2015) Alp7/TACC recruits kinesin-8-PP1 to the Ndc80 kinetochore protein for timely mitotic progression and chromosome movement. J Cell Sci 128:354–363. doi:10.1242/jcs.160036
Tien JF et al (2010) Cooperation of the Dam1 and Ndc80 kinetochore complexes enhances microtubule coupling and is regulated by aurora B. J Cell Biol 189:713–723. doi:10.1083/jcb.200910142
Tomita K, Cooper JP (2007) The telomere bouquet controls the meiotic spindle. Cell 130:113–126. doi:10.1016/j.cell.2007.05.024
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
Tournebize R et al (2000) Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat Cell Biol 2:13–19. doi:10.1038/71330
Wang HW et al (2007) Architecture of the Dam1 kinetochore ring complex and implications for microtubule-driven assembly and force-coupling mechanisms. Nat Struct Mol Biol 14:721–726. doi:10.1038/nsmb1274
Watanabe Y (2012) Geometry and force behind kinetochore orientation: lessons from meiosis. Nat Rev Mol Cell Biol 13:370–382. doi:10.1038/nrm3349
Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464. doi:10.1038/22774
Welburn JP, Grishchuk EL, Backer CB, Wilson-Kubalek EM, Yates JR 3rd, Cheeseman IM (2009) The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev Cell 16:374–385. doi:10.1016/j.devcel.2009.01.011
Westermann S et al (2005) Formation of a dynamic kinetochore-microtubule interface through assembly of the Dam1 ring complex. Mol Cell 17:277–290. doi:10.1016/j.molcel.2004.12.019
Westermann S, Wang HW, Avila-Sakar A, Drubin DG, Nogales E, Barnes G (2006) The Dam1 kinetochore ring complex moves processively on depolymerizing microtubule ends. Nature 440:565–569. doi:10.1038/nature04409
Yamamoto A, Hiraoka Y (2003) Monopolar spindle attachment of sister chromatids is ensured by two distinct mechanisms at the first meiotic division in fission yeast. EMBO J 22:2284–2296. doi:10.1093/emboj/cdg222
Yamashita A, Yamamoto M (2006) Fission yeast Num1p is a cortical factor anchoring dynein and is essential for the horse-tail nuclear movement during meiotic prophase. Genetics 173:1187–1196. doi:10.1534/genetics.105.050062
Yokobayashi S, Watanabe Y (2005) The kinetochore protein Moa1 enables cohesion-mediated monopolar attachment at meiosis I. Cell 123:803–817
Yoshida M et al (2013) Microtubule-organizing center formation at telomeres induces meiotic telomere clustering. J Cell Biol 200:385–395. doi:10.1083/jcb.201207168
Zhang G, Kelstrup CD, Hu XW, Kaas Hansen MJ, Singleton MR, Olsen JV, Nilsson J (2012) The Ndc80 internal loop is required for recruitment of the Ska complex to establish end-on microtubule attachment to kinetochores. J Cell Sci 125:3243–3253. doi:10.1242/jcs.104208
Acknowledgments
We thank Frank Uhlmann, Takashi Toda and Masayuki Yamamoto for the support.
Funding
M.S. is supported by Grants-in-Aid for Scientific Research (B) from the Japan Society for Promotion of Science (JSPS), by the Naito Foundation, by the Kato Memorial Bioscience Foundation, by the Sumitomo Foundation and by Waseda University Grants for Special Research Projects (2014K-6168, 2014B-318 and 2015A-057). Y.K. is supported by JSPS Postdoctoral Fellowships for Research Abroad.
Compliance with ethical standards
ᅟ
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Author information
Authors and Affiliations
Corresponding authors
Additional information
This article is part of a Special Issue on "Recent advances in meiotic chromosome structure, recombination and segregation” edited by Marco Barchi, Paula Cohen and Scott Keeney.
Rights and permissions
About this article
Cite this article
Kakui, Y., Sato, M. Differentiating the roles of microtubule-associated proteins at meiotic kinetochores during chromosome segregation. Chromosoma 125, 309–320 (2016). https://doi.org/10.1007/s00412-015-0541-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-015-0541-x