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Gathering up meiotic telomeres: a novel function of the microtubule-organizing center

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Abstract

During meiosis, telomeres cluster and promote homologous chromosome pairing. Telomere clustering depends on conserved SUN and KASH domain nuclear membrane proteins, which form a complex called the linker of nucleoskeleton and cytoskeleton (LINC) and connect telomeres with the cytoskeleton. It has been thought that LINC-mediated cytoskeletal forces induce telomere clustering. However, how cytoskeletal forces induce telomere clustering is not fully understood. Recent study of fission yeast has shown that the LINC complex forms the microtubule-organizing center (MTOC) at the telomere, which has been designated as the “telocentrosome”, and that microtubule motors gather telomeres via telocentrosome-nucleated microtubules. This MTOC-dependent telomere clustering might be conserved in other eukaryotes. Furthermore, the MTOC-dependent clustering mechanism appears to function in various other biological events. This review presents an overview of the current understanding of the mechanism of meiotic telomere clustering and discusses the universality of the MTOC-dependent clustering mechanism.

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Abbreviations

DHC:

Dynein heavy chain

DLC:

Dynein light chain

LINC:

Linker of nucleoskeleton and cytoskeleton

MTOC:

Microtubule-organizing center

PC:

Pairing center

SPB:

Spindle pole body

γ-TuC:

γ-Tubulin complex

References

  1. Scherthan H (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2(8):621–627

    Article  CAS  PubMed  Google Scholar 

  2. Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32:619–697. doi:10.1146/annurev.genet.32.1.619

    Article  CAS  PubMed  Google Scholar 

  3. Fridkin A, Penkner A, Jantsch V, Gruenbaum Y (2009) SUN-domain and KASH-domain proteins during development, meiosis and disease. Cellular Mol Life Sci: CMLS 66(9):1518–1533. doi:10.1007/s00018-008-8713-y

    Article  CAS  PubMed  Google Scholar 

  4. Hiraoka Y, Dernburg AF (2009) The SUN rises on meiotic chromosome dynamics. Dev Cell 17(5):598–605. doi:10.1016/j.devcel.2009.10.014

    Article  CAS  PubMed  Google Scholar 

  5. Razafsky D, Hodzic D (2009) Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J Cell Biol 186(4):461–472. doi:10.1083/jcb.200906068

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D (2006) Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172(1):41–53. doi:10.1083/jcb.200509124

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Yoshida M, Katsuyama S, Tateho K, Nakamura H, Miyoshi J, Ohba T, Matsuhara H, Miki F, Okazaki K, Haraguchi T, Niwa O, Hiraoka Y, Yamamoto A (2013) Microtubule-organizing center formation at telomeres induces meiotic telomere clustering. J Cell Biol 200(4):385–395. doi:10.1083/jcb.201207168

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Yamamoto A, Hiraoka Y (2001) How do meiotic chromosomes meet their homologous partners? Lessons from fission yeast. Bioessays 23(6):526–533. doi:10.1002/bies.1072

    Article  CAS  PubMed  Google Scholar 

  9. Harper L, Golubovskaya I, Cande WZ (2004) A bouquet of chromosomes. J Cell Sci 117(Pt 18):4025–4032. doi:10.1242/jcs.01363

    Article  CAS  PubMed  Google Scholar 

  10. Koszul R, Kleckner N (2009) Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 19(12):716–724. doi:10.1016/j.tcb.2009.09.007

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Yamamoto M, Imai Y, Watanabe Y (1997) Mating and sporulation in Schizosaccharomyces pombe. In: Pringle JR, Broach JR, Jones EW (eds) The molecular and cellular biology of the yeast Saccharomyces; cell cycle and cell biology, vol 3. Cold Spring Harbor Laboratory Press, New York, pp 1037–1106

    Google Scholar 

  12. 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(5156):270–273

    Article  CAS  PubMed  Google Scholar 

  13. Ding DQ, Chikashige Y, Haraguchi T, Hiraoka Y (1998) Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells. J Cell Sci 111(Pt 6):701–712

    CAS  PubMed  Google Scholar 

  14. Yamamoto A, West RR, McIntosh JR, Hiraoka Y (1999) A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J Cell Biol 145(6):1233–1249

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Yamamoto A, Tsutsumi C, Kojima H, Oiwa K, Hiraoka Y (2001) Dynamic behavior of microtubules during dynein-dependent nuclear migrations of meiotic prophase in fission yeast. Mol Biol Cell 12(12):3933–3946

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Yamamoto A, Hiraoka Y (2003) Cytoplasmic dynein in fungi: insights from nuclear migration. J Cell Sci 116(Pt 22):4501–4512. doi:10.1242/jcs.00835

    Article  CAS  PubMed  Google Scholar 

  17. Ananthanarayanan V, Schattat M, Vogel SK, Krull A, Pavin N, Tolic-Norrelykke IM (2013) Dynein motion switches from diffusive to directed upon cortical anchoring. Cell 153(7):1526–1536. doi:10.1016/j.cell.2013.05.020

    Article  CAS  PubMed  Google Scholar 

  18. Vogel SK, Pavin N, Maghelli N, Julicher F, Tolic-Norrelykke IM (2009) Self-organization of dynein motors generates meiotic nuclear oscillations. PLoS Biol 7(4):e1000087. doi:10.1371/journal.pbio.1000087

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  19. Ding DQ, Yamamoto A, Haraguchi T, Hiraoka Y (2004) Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 6(3):329–341

    Article  CAS  PubMed  Google Scholar 

  20. Miki F, Okazaki K, Shimanuki M, Yamamoto A, Hiraoka Y, Niwa O (2002) The 14-kDa dynein light chain-family protein Dlc1 is required for regular oscillatory nuclear movement and efficient recombination during meiotic prophase in fission yeast. Mol Biol Cell 13(3):930–946. doi:10.1091/mbc.01-11-0543

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Shimanuki M, Miki F, Ding DQ, Chikashige Y, Hiraoka Y, Horio T, Niwa O (1997) A novel fission yeast gene, kms1+, is required for the formation of meiotic prophase-specific nuclear architecture. Mol Gen Genet: MGG 254(3):238–249

    Article  CAS  PubMed  Google Scholar 

  22. Nimmo ER, Pidoux AL, Perry PE, Allshire RC (1998) Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 392(6678):825–828. doi:10.1038/33941

    Article  CAS  PubMed  Google Scholar 

  23. Cooper JP, Watanabe Y, Nurse P (1998) Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination. Nature 392(6678):828–831. doi:10.1038/33947

    Article  CAS  PubMed  Google Scholar 

  24. Tuzon CT, Borgstrom B, Weilguny D, Egel R, Cooper JP, Nielsen O (2004) The fission yeast heterochromatin protein Rik1 is required for telomere clustering during meiosis. J Cell Biol 165(6):759–765. doi:10.1083/jcb.200312061

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Chikashige Y, Hiraoka Y (2001) Telomere binding of the Rap1 protein is required for meiosis in fission yeast. Curr Biol 11(20):1618–1623

    Article  CAS  PubMed  Google Scholar 

  26. Kanoh J, Ishikawa F (2001) spRap1 and spRif1, recruited to telomeres by Taz1, are essential for telomere function in fission yeast. Curr Biol 11(20):1624–1630

    Article  CAS  PubMed  Google Scholar 

  27. Niwa O, Shimanuki M, Miki F (2000) Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis. EMBO J 19(14):3831–3840. doi:10.1093/emboj/19.14.3831

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Trelles-Sticken E, Dresser ME, Scherthan H (2000) Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 151(1):95–106

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Trelles-Sticken E, Adelfalk C, Loidl J, Scherthan H (2005) Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J Cell Biol 170(2):213–223

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Conrad MN, Lee CY, Chao G, Shinohara M, Kosaka H, Shinohara A, Conchello JA, Dresser ME (2008) Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133(7):1175–1187

    Article  CAS  PubMed  Google Scholar 

  31. Koszul R, Kim KP, Prentiss M, Kleckner N, Kameoka S (2008) Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133(7):1188–1201

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Scherthan H, Wang H, Adelfalk C, White EJ, Cowan C, Cande WZ, Kaback DB (2007) Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 104(43):16934–16939

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Conrad MN, Dominguez AM, Dresser ME (1997) Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. Science 276(5316):1252–1255

    Article  CAS  PubMed  Google Scholar 

  34. Chua PR, Roeder GS (1997) Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev 11(14):1786–1800

    Article  CAS  PubMed  Google Scholar 

  35. Rockmill B, Roeder GS (1998) Telomere-mediated chromosome pairing during meiosis in budding yeast. Genes Dev 12(16):2574–2586

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Goldman AS, Lichten M (2000) Restriction of ectopic recombination by interhomolog interactions during Saccharomyces cerevisiae meiosis. Proc Natl Acad Sci USA 97(17):9537–9542

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Schlecht HB, Lichten M, Goldman AS (2004) Compartmentalization of the yeast meiotic nucleus revealed by analysis of ectopic recombination. Genetics 168(3):1189–1203. doi:10.1534/genetics.104.029157

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123(6):1037–1050

    Article  CAS  PubMed  Google Scholar 

  39. Phillips CM, Wong C, Bhalla N, Carlton PM, Weiser P, Meneely PM, Dernburg AF (2005) HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123(6):1051–1063

    Article  CAS  PubMed  Google Scholar 

  40. Penkner AM, Fridkin A, Gloggnitzer J, Baudrimont A, Machacek T, Woglar A, Csaszar E, Pasierbek P, Ammerer G, Gruenbaum Y, Jantsch V (2009) Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139(5):920–933. doi:10.1016/j.cell.2009.10.045

    Article  CAS  PubMed  Google Scholar 

  41. Baudrimont A, Penkner A, Woglar A, Machacek T, Wegrostek C, Gloggnitzer J, Fridkin A, Klein F, Gruenbaum Y, Pasierbek P, Jantsch V (2010) Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans. PLoS Genet 6(11):e1001219. doi:10.1371/journal.pgen.1001219

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  42. Wynne DJ, Rog O, Carlton PM, Dernburg AF (2012) Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. J Cell Biol 196(1):47–64. doi:10.1083/jcb.201106022

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Sato A, Isaac B, Phillips CM, Rillo R, Carlton PM, Wynne DJ, Kasad RA, Dernburg AF (2009) Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139(5):907–919. doi:10.1016/j.cell.2009.10.039

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Scherthan H, Weich S, Schwegler H, Heyting C, Harle M, Cremer T (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(5):1109–1125

    Article  CAS  PubMed  Google Scholar 

  45. 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(2):165–172. doi:10.1083/jcb.201204085

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Bass HW, Marshall WF, Sedat JW, Agard DA, Cande WZ (1997) Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J Cell Biol 137(1):5–18

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Carlton PM, Cande WZ (2002) Telomeres act autonomously in maize to organize the meiotic bouquet from a semipolarized chromosome orientation. J Cell Biol 157(2):231–242. doi:10.1083/jcb.200110126

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Bass HW, Riera-Lizarazu O, Ananiev EV, Bordoli SJ, Rines HW, Phillips RL, Sedat JW, Agard DA, Cande WZ (2000) Evidence for the coincident initiation of homolog pairing and synapsis during the telomere-clustering (bouquet) stage of meiotic prophase. J Cell Sci 113(Pt 6):1033–1042

    CAS  PubMed  Google Scholar 

  49. Sosa BA, Rothballer A, Kutay U, Schwartz TU (2012) LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins. Cell 149(5):1035–1047. doi:10.1016/j.cell.2012.03.046

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Zhou Z, Du X, Cai Z, Song X, Zhang H, Mizuno T, Suzuki E, Yee MR, Berezov A, Murali R, Wu SL, Karger BL, Greene MI, Wang Q (2012) Structure of Sad1-UNC84 homology (SUN) domain defines features of molecular bridge in nuclear envelope. J Biol Chem 287(8):5317–5326. doi:10.1074/jbc.M111.304543

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Starr DA, Han M (2003) ANChors away: an actin based mechanism of nuclear positioning. J Cell Sci 116(Pt 2):211–216

    Article  CAS  PubMed  Google Scholar 

  52. Starr DA, Fischer JA (2005) KASH ‘n Karry: the KASH domain family of cargo-specific cytoskeletal adaptor proteins. Bioessays 27(11):1136–1146. doi:10.1002/bies.20312

    Article  CAS  PubMed  Google Scholar 

  53. Wilhelmsen K, Ketema M, Truong H, Sonnenberg A (2006) KASH-domain proteins in nuclear migration, anchorage and other processes. J Cell Sci 119(Pt 24):5021–5029

    Article  CAS  PubMed  Google Scholar 

  54. Patterson K, Molofsky AB, Robinson C, Acosta S, Cater C, Fischer JA (2004) The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye. Mol Biol Cell 15(2):600–610. doi:10.1091/mbc.E03-06-0374

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM, Fry AM, Trembath RC, Shackleton S (2006) SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 26(10):3738–3751. doi:10.1128/MCB.26.10.3738-3751.2006

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Libotte T, Zaim H, Abraham S, Padmakumar VC, Schneider M, Lu W, Munck M, Hutchison C, Wehnert M, Fahrenkrog B, Sauder U, Aebi U, Noegel AA, Karakesisoglou I (2005) Lamin A/C-dependent localization of Nesprin-2, a giant scaffolder at the nuclear envelope. Mol Biol Cell 16(7):3411–3424. doi:10.1091/mbc.E04-11-1009

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Mislow JM, Kim MS, Davis DB, McNally EM (2002) Myne-1, a spectrin repeat transmembrane protein of the myocyte inner nuclear membrane, interacts with lamin A/C. J Cell Sci 115(Pt 1):61–70

    CAS  PubMed  Google Scholar 

  58. Zhang Q, Ragnauth CD, Skepper JN, Worth NF, Warren DT, Roberts RG, Weissberg PL, Ellis JA, Shanahan CM (2005) Nesprin-2 is a multi-isomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle. J Cell Sci 118(Pt 4):673–687. doi:10.1242/jcs.01642

    Article  CAS  PubMed  Google Scholar 

  59. Lee KK, Starr D, Cohen M, Liu J, Han M, Wilson KL, Gruenbaum Y (2002) Lamin-dependent localization of UNC-84, a protein required for nuclear migration in Caenorhabditis elegans. Mol Biol Cell 13(3):892–901. doi:10.1091/mbc.01-06-0294

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Emery AE (1989) Emery-Dreifuss syndrome. J Med Genet 26(10):637–641

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Bione S, Maestrini E, Rivella S, Mancini M, Regis S, Romeo G, Toniolo D (1994) Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat Genet 8(4):323–327. doi:10.1038/ng1294-323

    Article  CAS  PubMed  Google Scholar 

  62. Yadlapalli S, Yamashita YM (2013) Chromosome-specific nonrandom sister chromatid segregation during stem-cell division. Nature 498(7453):251–254. doi:10.1038/Nature12106

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Yamashita YM (2013) Nonrandom sister chromatid segregation of sex chromosomes in Drosophila male germline stem cells. Chromosome Res 21(3):243–254. doi:10.1007/S10577-013-9353-0

    Article  CAS  PubMed  Google Scholar 

  64. Hagan I, Yanagida M (1995) The product of the spindle formation gene sad1+ associates with the fission yeast spindle pole body and is essential for viability. J Cell Biol 129(4):1033–1047

    Article  CAS  PubMed  Google Scholar 

  65. 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(1):59–69

    Article  CAS  PubMed  Google Scholar 

  66. Chikashige Y, Yamane M, Okamasa K, Tsutsumi C, Kojidani T, Sato M, Haraguchi T, Hiraoka Y (2009) Membrane proteins Bqt3 and -4 anchor telomeres to the nuclear envelope to ensure chromosomal bouquet formation. J Cell Biol 187(3):413–427. doi:10.1083/jcb.200902122

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. Tang X, Jin Y, Cande WZ (2006) Bqt2p is essential for initiating telomere clustering upon pheromone sensing in fission yeast. J Cell Biol 173(6):845–851. doi:10.1083/jcb.200602152

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Conrad MN, Lee CY, Wilkerson JL, Dresser ME (2007) MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 104(21):8863–8868

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Rao HB, Shinohara M, Shinohara A (2011) Mps3 SUN domain is important for chromosome motion and juxtaposition of homologous chromosomes during meiosis. Genes Cells 16(11):1081–1096. doi:10.1111/j.1365-2443.2011.01554.x

    Article  CAS  PubMed  Google Scholar 

  70. Penkner A, Tang L, Novatchkova M, Ladurner M, Fridkin A, Gruenbaum Y, Schweizer D, Loidl J, Jantsch V (2007) The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell 12(6):873–885

    Article  CAS  PubMed  Google Scholar 

  71. Labella S, Woglar A, Jantsch V, Zetka M (2011) Polo kinases establish links between meiotic chromosomes and cytoskeletal forces essential for homolog pairing. Dev Cell 21(5):948–958. doi:10.1016/j.devcel.2011.07.011

    Article  CAS  PubMed  Google Scholar 

  72. Harper NC, Rillo R, Jover-Gil S, Assaf ZJ, Bhalla N, Dernburg AF (2011) Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev Cell 21(5):934–947. doi:10.1016/j.devcel.2011.09.001

    Article  CAS  PubMed  Google Scholar 

  73. Woglar A, Daryabeigi A, Adamo A, Habacher C, Machacek T, La Volpe A, Jantsch V (2013) Matefin/SUN-1 phosphorylation is part of a surveillance mechanism to coordinate chromosome synapsis and recombination with meiotic progression and chromosome movement. PLoS Genet 9(3):e1003335. doi:10.1371/journal.pgen.1003335

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Ding X, Xu R, Yu J, Xu T, Zhuang Y, Han M (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12(6):863–872

    Article  CAS  PubMed  Google Scholar 

  75. Schmitt J, Benavente R, Hodzic D, Hoog C, Stewart CL, Alsheimer M (2007) Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope. Proc Natl Acad Sci USA 104(18):7426–7431. doi:10.1073/pnas.0609198104

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. Horn HF, Kim DI, Wright GD, Wong ES, Stewart CL, Burke B, Roux KJ (2013) A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J Cell Biol 202:1023–1039. doi:10.1083/jcb.201304004

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Fridolfsson HN, Ly N, Meyerzon M, Starr DA (2010) UNC-83 coordinates kinesin-1 and dynein activities at the nuclear envelope during nuclear migration. Dev Biol 338(2):237–250. doi:10.1016/j.ydbio.2009.12.004

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Fridolfsson HN, Starr DA (2010) Kinesin-1 and dynein at the nuclear envelope mediate the bidirectional migrations of nuclei. J Cell Biol 191(1):115–128. doi:10.1083/jcb.201004118

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  79. Meyerzon M, Fridolfsson HN, Ly N, McNally FJ, Starr DA (2009) UNC-83 is a nuclear-specific cargo adaptor for kinesin-1-mediated nuclear migration. Development 136(16):2725–2733. doi:10.1242/dev.038596

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. Whited JL, Cassell A, Brouillette M, Garrity PA (2004) Dynactin is required to maintain nuclear position within postmitotic Drosophila photoreceptor neurons. Development 131(19):4677–4686. doi:10.1242/dev.01366

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  81. Wilson MH, Holzbaur EL (2012) Opposing microtubule motors drive robust nuclear dynamics in developing muscle cells. J Cell Sci 125(Pt 17):4158–4169. doi:10.1242/jcs.108688

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  82. Cowan CR, Cande WZ (2002) Meiotic telomere clustering is inhibited by colchicine but does not require cytoplasmic microtubules. J Cell Sci 115(Pt 19):3747–3756

    Article  CAS  PubMed  Google Scholar 

  83. Trelles-Sticken E, Loidl J, Scherthan H (2003) Increased ploidy and KAR3 and SIR3 disruption alter the dynamics of meiotic chromosomes and telomeres. J Cell Sci 116(Pt 12):2431–2442. doi:10.1242/jcs.00453

    Article  CAS  PubMed  Google Scholar 

  84. Drummond DR, Cross RA (2000) Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr Biol 10(13):766–775

    Article  CAS  PubMed  Google Scholar 

  85. Tran PT, Marsh L, Doye V, Inoue S, Chang F (2001) A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153(2):397–411

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  86. Sagolla MJ, Uzawa S, Cande WZ (2003) Individual microtubule dynamics contribute to the function of mitotic and cytoplasmic arrays in fission yeast. J Cell Sci 116(Pt 24):4891–4903. doi:10.1242/jcs.00796

    Article  CAS  PubMed  Google Scholar 

  87. Horio T, Uzawa S, Jung MK, Oakley BR, Tanaka K, Yanagida M (1991) The fission yeast gamma-tubulin is essential for mitosis and is localized at microtubule organizing centers. J Cell Sci 99(Pt 4):693–700

    CAS  PubMed  Google Scholar 

  88. Funaya C, Samarasinghe S, Pruggnaller S, Ohta M, Connolly Y, Muller J, Murakami H, Grallert A, Yamamoto M, Smith D, Antony C, Tanaka K (2012) Transient structure associated with the spindle pole body directs meiotic microtubule reorganization in S. pombe. Curr Biol 22(7):562–574. doi:10.1016/j.cub.2012.02.042

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  89. Sawin KE, Tran PT (2006) Cytoplasmic microtubule organization in fission yeast. Yeast 23(13):1001–1014. doi:10.1002/yea.1404

    Article  CAS  PubMed  Google Scholar 

  90. Sawin KE, Lourenco PC, Snaith HA (2004) Microtubule nucleation at non-spindle pole body microtubule-organizing centers requires fission yeast centrosomin-related protein mod20p. Curr Biol 14(9):763–775. doi:10.1016/j.cub.2004.03.042

    Article  CAS  PubMed  Google Scholar 

  91. Venkatram S, Tasto JJ, Feoktistova A, Jennings JL, Link AJ, Gould KL (2004) Identification and characterization of two novel proteins affecting fission yeast gamma-tubulin complex function. Mol Biol Cell 15(5):2287–2301. doi:10.1091/mbc.E03-10-0728

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  92. Tanaka K, Kohda T, Yamashita A, Nonaka N, Yamamoto M (2005) Hrs1p/Mcp6p on the meiotic SPB organizes astral microtubule arrays for oscillatory nuclear movement. Curr Biol 15(16):1479–1486. doi:10.1016/j.cub.2005.07.058

    Article  CAS  PubMed  Google Scholar 

  93. Samejima I, Miller VJ, Rincon SA, Sawin KE (2010) Fission yeast Mto1 regulates diversity of cytoplasmic microtubule organizing centers. Curr Biol 20(21):1959–1965. doi:10.1016/j.cub.2010.10.006

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  94. Manandhar G, Schatten H, Sutovsky P (2005) Centrosome reduction during gametogenesis and its significance. Biol Reprod 72(1):2–13. doi:10.1095/biolreprod.104.031245

    Article  CAS  PubMed  Google Scholar 

  95. Schatten H, Sun QY (2009) The functional significance of centrosomes in mammalian meiosis, fertilization, development, nuclear transfer, and stem cell differentiation. Environ Mol Mutagen 50(8):620–636. doi:10.1002/em.20493

    Article  CAS  PubMed  Google Scholar 

  96. Schuh M, Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130(3):484–498. doi:10.1016/j.cell.2007.06.025

    Article  CAS  PubMed  Google Scholar 

  97. Khodjakov A, Cole RW, Oakley BR, Rieder CL (2000) Centrosome-independent mitotic spindle formation in vertebrates. Curr Biol 10(2):59–67

    Article  CAS  PubMed  Google Scholar 

  98. Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, Hyman A, Karsenti E (1996) Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382(6590):420–425. doi:10.1038/382420a0

    Article  CAS  PubMed  Google Scholar 

  99. Heald R, Tournebize R, Habermann A, Karsenti E, Hyman A (1997) Spindle assembly in Xenopus egg extracts: respective roles of centrosomes and microtubule self-organization. J Cell Biol 138(3):615–628

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  100. Jaspersen SL, Giddings TH Jr, Winey M (2002) Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J Cell Biol 159(6):945–956. doi:10.1083/jcb.200208169

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  101. Tomita K, Cooper JP (2007) The telomere bouquet controls the meiotic spindle. Cell 130(1):113–126. doi:10.1016/j.cell.2007.05.024

    Article  CAS  PubMed  Google Scholar 

  102. Mitchison TJ, Kirschner MW (1985) Properties of the kinetochore in vitro. I. Microtubule nucleation and tubulin binding. J Cell Biol 101(3):755–765

    Article  CAS  PubMed  Google Scholar 

  103. Khodjakov A, Copenagle L, Gordon MB, Compton DA, Kapoor TM (2003) Minus-end capture of preformed kinetochore fibers contributes to spindle morphogenesis. J Cell Biol 160(5):671–683. doi:10.1083/jcb.200208143

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  104. Maiato H, Rieder CL, Khodjakov A (2004) Kinetochore-driven formation of kinetochore fibers contributes to spindle assembly during animal mitosis. J Cell Biol 167(5):831–840. doi:10.1083/jcb.200407090

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  105. 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(2):248–259. doi:10.1016/j.devcel.2009.12.018

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  106. Mishra RK, Chakraborty P, Arnaoutov A, Fontoura BM, Dasso M (2010) The Nup107-160 complex and gamma-TuRC regulate microtubule polymerization at kinetochores. Nat Cell Biol 12(2):164–169. doi:10.1038/ncb2016

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  107. Torosantucci L, De Luca M, Guarguaglini G, Lavia P, Degrassi F (2008) Localized RanGTP accumulation promotes microtubule nucleation at kinetochores in somatic mammalian cells. Mol Biol Cell 19(5):1873–1882. doi:10.1091/mbc.E07-10-1050

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  108. Salina D, Enarson P, Rattner JB, Burke B (2003) Nup358 integrates nuclear envelope breakdown with kinetochore assembly. J Cell Biol 162(6):991–1001. doi:10.1083/jcb.200304080

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  109. Joseph J, Liu ST, Jablonski SA, Yen TJ, Dasso M (2004) The RanGAP1-RanBP2 complex is essential for microtubule-kinetochore interactions in vivo. Curr Biol 14(7):611–617. doi:10.1016/j.cub.2004.03.031

    Article  CAS  PubMed  Google Scholar 

  110. Zuccolo M, Alves A, Galy V, Bolhy S, Formstecher E, Racine V, Sibarita JB, Fukagawa T, Shiekhattar R, Yen T, Doye V (2007) The human Nup107-160 nuclear pore subcomplex contributes to proper kinetochore functions. EMBO J 26(7):1853–1864. doi:10.1038/sj.emboj.7601642

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  111. Feng J, Huang H, Yen TJ (2006) CENP-F is a novel microtubule-binding protein that is essential for kinetochore attachments and affects the duration of the mitotic checkpoint delay. Chromosoma 115(4):320–329. doi:10.1007/s00412-006-0049-5

    Article  CAS  PubMed  Google Scholar 

  112. Vergnolle MA, Taylor SS (2007) Cenp-F links kinetochores to Ndel1/Nde1/Lis1/dynein microtubule motor complexes. Curr Biol 17(13):1173–1179. doi:10.1016/j.cub.2007.05.077

    Article  CAS  PubMed  Google Scholar 

  113. Moynihan KL, Pooley R, Miller PM, Kaverina I, Bader DM (2009) Murine CENP-F regulates centrosomal microtubule nucleation and interacts with Hook2 at the centrosome. Mol Biol Cell 20(22):4790–4803. doi:10.1091/mbc.E09-07-0560

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  114. Chen JS, Lu LX, Ohi MD, Creamer KM, English C, Partridge JF, Ohi R, Gould KL (2011) Cdk1 phosphorylation of the kinetochore protein Nsk1 prevents error-prone chromosome segregation. J Cell Biol 195(4):583–593. doi:10.1083/jcb.201105074

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  115. Buttrick GJ, Meadows JC, Lancaster TC, Vanoosthuyse V, Shepperd LA, Hoe KL, Kim DU, Park HO, Hardwick KG, Millar JB (2011) Nsk1 ensures accurate chromosome segregation by promoting association of kinetochores to spindle poles during anaphase B. Mol Biol Cell 22(23):4486–4502. doi:10.1091/mbc.E11-07-0608

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  116. Allan VJ, Thompson HM, McNiven MA (2002) Motoring around the Golgi. Nat Cell Biol 4(10):E236–E242. doi:10.1038/ncb1002-e236

    Article  CAS  PubMed  Google Scholar 

  117. Rogalski AA, Singer SJ (1984) Associations of elements of the Golgi apparatus with microtubules. J Cell Biol 99(3):1092–1100

    Article  CAS  PubMed  Google Scholar 

  118. Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB (1997) Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol 139(2):469–484

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  119. Corthesy-Theulaz I, Pauloin A, Pfeffer SR (1992) Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J Cell Biol 118(6):1333–1345

    Article  CAS  PubMed  Google Scholar 

  120. Harada A, Takei Y, Kanai Y, Tanaka Y, Nonaka S, Hirokawa N (1998) Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J Cell Biol 141(1):51–59

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  121. Fath KR, Trimbur GM, Burgess DR (1994) Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J Cell Biol 126(3):661–675

    Article  CAS  PubMed  Google Scholar 

  122. Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM, Andreyeva N, Gleeson P, Galjart N, Maia AR, McLeod IX, Yates JR 3rd, Maiato H, Khodjakov A, Akhmanova A, Kaverina I (2007) Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev Cell 12(6):917–930. doi:10.1016/j.devcel.2007.04.002

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  123. Chabin-Brion K, Marceiller J, Perez F, Settegrana C, Drechou A, Durand G, Pous C (2001) The Golgi complex is a microtubule-organizing organelle. Mol Biol Cell 12(7):2047–2060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  124. Rios RM, Sanchis A, Tassin AM, Fedriani C, Bornens M (2004) GMAP-210 recruits gamma-tubulin complexes to cis-Golgi membranes and is required for Golgi ribbon formation. Cell 118(3):323–335. doi:10.1016/j.cell.2004.07.012

    Article  CAS  PubMed  Google Scholar 

  125. Verde I, Pahlke G, Salanova M, Zhang G, Wang S, Coletti D, Onuffer J, Jin SL, Conti M (2001) Myomegalin is a novel protein of the Golgi/centrosome that interacts with a cyclic nucleotide phosphodiesterase. J Biol Chem 276(14):11189–11198. doi:10.1074/jbc.M006546200

    Article  CAS  PubMed  Google Scholar 

  126. Ho WC, Allan VJ, van Meer G, Berger EG, Kreis TE (1989) Reclustering of scattered Golgi elements occurs along microtubules. Eur J Cell Biol 48(2):250–263

    CAS  PubMed  Google Scholar 

  127. Reinsch S, Gonczy P (1998) Mechanisms of nuclear positioning. J Cell Sci 111(Pt 16):2283–2295

    CAS  PubMed  Google Scholar 

  128. Salina D, Bodoor K, Eckley DM, Schroer TA, Rattner JB, Burke B (2002) Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108(1):97–107

    Article  CAS  PubMed  Google Scholar 

  129. Hebbar S, Mesngon MT, Guillotte AM, Desai B, Ayala R, Smith DS (2008) Lis1 and Ndel1 influence the timing of nuclear envelope breakdown in neural stem cells. J Cell Biol 182(6):1063–1071. doi:10.1083/jcb.200803071

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  130. Burke B, Roux KJ (2009) Nuclei take a position: managing nuclear location. Dev Cell 17(5):587–597. doi:10.1016/j.devcel.2009.10.018

    Article  CAS  PubMed  Google Scholar 

  131. Mejat A, Misteli T (2010) LINC complexes in health and disease. Nucleus Austin 1(1):40–52. doi:10.4161/Nucl.1.1.10530

    Google Scholar 

  132. Rothballer A, Schwartz TU, Kutay U (2013) LINCing complex functions at the nuclear envelope: what the molecular architecture of the LINC complex can reveal about its function. Nucleus 4(1):29–36. doi:10.4161/nucl.23387

    Article  PubMed Central  PubMed  Google Scholar 

  133. Tapley EC, Starr DA (2013) Connecting the nucleus to the cytoskeleton by SUN-KASH bridges across the nuclear envelope. Curr Opin Cell Biol 25(1):57–62. doi:10.1016/j.ceb.2012.10.014

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  134. Malone CJ, Misner L, Le Bot N, Tsai MC, Campbell JM, Ahringer J, White JG (2003) The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115(7):825–836

    Article  CAS  PubMed  Google Scholar 

  135. Kracklauer MP, Banks SM, Xie X, Wu Y, Fischer JA (2007) Drosophila klaroid encodes a SUN domain protein required for Klarsicht localization to the nuclear envelope and nuclear migration in the eye. Fly 1(2):75–85

    PubMed  Google Scholar 

  136. Anderson MA, Jodoin JN, Lee E, Hales KG, Hays TS, Lee LA (2009) Asunder is a critical regulator of dynein-dynactin localization during Drosophila spermatogenesis. Mol Biol Cell 20(11):2709–2721. doi:10.1091/mbc.E08-12-1165

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  137. Sitaram P, Anderson MA, Jodoin JN, Lee E, Lee LA (2012) Regulation of dynein localization and centrosome positioning by Lis-1 and asunder during Drosophila spermatogenesis. Development 139(16):2945–2954. doi:10.1242/dev.077511

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  138. Jodoin JN, Shboul M, Sitaram P, Zein-Sabatto H, Reversade B, Lee E, Lee LA (2012) Human Asunder promotes dynein recruitment and centrosomal tethering to the nucleus at mitotic entry. Mol Biol Cell 23(24):4713–4724. doi:10.1091/mbc.E12-07-0558

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  139. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, Xu R, Han M (2009) SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64(2):173–187. doi:10.1016/j.neuron.2009.08.018

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  140. Bolhy S, Bouhlel I, Dultz E, Nayak T, Zuccolo M, Gatti X, Vallee R, Ellenberg J, Doye V (2011) A Nup133-dependent NPC-anchored network tethers centrosomes to the nuclear envelope in prophase. J Cell Biol 192(5):855–871. doi:10.1083/jcb.201007118

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  141. Splinter D, Tanenbaum ME, Lindqvist A, Jaarsma D, Flotho A, Yu KL, Grigoriev I, Engelsma D, Haasdijk ED, Keijzer N, Demmers J, Fornerod M, Melchior F, Hoogenraad CC, Medema RH, Akhmanova A (2010) Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol 8(4):e1000350. doi:10.1371/journal.pbio.1000350

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  142. Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG (2004) Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165(5):709–721. doi:10.1083/jcb.200309025

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  143. Erhardt M, Stoppin-Mellet V, Campagne S, Canaday J, Mutterer J, Fabian T, Sauter M, Muller T, Peter C, Lambert AM, Schmit AC (2002) The plant Spc98p homologue colocalizes with gamma-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J Cell Sci 115(Pt 11):2423–2431

    CAS  PubMed  Google Scholar 

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Acknowledgments

I thank Akira Shinohara, Kayoko Tanaka, Takashi Ushimaru, and Masahiro Uritani for critical reading of the manuscript and helpful comments. This work was supported by Grants-in-aid for Scientific Research (C) to A. Y. and the Cooperative Research Program of the Institute for Protein Research, Osaka University.

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  1. Department of Chemistry, Graduate School of Science, Shizuoka University, 836 Ohya, Suruga-ku, Sizuoka, 422-8529, Japan

    Ayumu Yamamoto

  2. Department of Bioscience, Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Sizuoka, 422-8529, Japan

    Ayumu Yamamoto

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Yamamoto, A. Gathering up meiotic telomeres: a novel function of the microtubule-organizing center. Cell. Mol. Life Sci. 71, 2119–2134 (2014). https://doi.org/10.1007/s00018-013-1548-1

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