Meiotic spindle, spindle checkpoint and embryonic aneuploidy

Frontiers in Bioscience

Volumn 11, Issue 1 P.447-888, 2006, Pages 620-636

  Wang, Wei Hua ^a   Sun, Qing Yuan ^b  

^a Tomball Regional Hospital   (United States)

^b INSTITUTE OF ZOOLOGY   (China)

Author keywords

Embryonic Aneuploidy; Meiosis; Oocytes; Review; Spindle; Spindle Checkpoint

Indexed keywords

MAMMALIA; SACCHAROMYCETALES;

EID: 32944462998     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/1822     Document Type: Review

References (148)

1. Hassold T. & P. Hunt: To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2, 280-291 (2001)
2. Jallepalli P.V. & C. Lengauer: Chromosome segregation and cancer: cutting through the mystery. Nat Rev Cancer 1, 109-117 (2001)
3. Matsuura S., E. Ito, H. Tauchi, K. Komatsu, T. Ikeuchi & T. Kajii: Chromosomal instability syndrome of total premature chromatid separation with mosaic variegated aneuploidy is defective in mitotic-spindle checkpoint. Am J Hum Genet 67, 483-486 (2000)
4. Bharadwaj R. & H. Yu: The spindle checkpoint, aneuploidy, and cancer. Oncogene 23, 2016-2027 (2004)
5. Mailhes J.B., D. Young & S.N. London: Postovulatory ageing of mouse oocytes in vitro and premature centromere separation and aneuploidy. Biol Reprod 58, 1206-1210 (1998)
6. Zenzes M.T. & R.F. Casper: Cytogenetics of human oocytes, zygotes and embryos after in vitro fertilization. Hum Genetics 88, 367-375 (1992)
7. Cowchock F.S., Z. Gibas & L.G. Jackson: Chromosome errors as a cause of spontaneous abortion: the relative importance of maternal age and obstetric history. Fertil Steril 59, 1011-1014 (1993)
8. Hassold T., M. Abruzzo, K. Adkins, D. Griffin, M. Merrill, E. Millie, D. Saker, J. Shen & M. Zaragoza: Human aneuploidy: Incidence, origin, and etiology. Environ Mol Mutagen 28, 167-175 (1996)
9. Balton V.N., S.M. Hawes, C.T. Taylor & J.H. Parsons: Development of spare human implantation embryos in vitro: an analysis of the correlations among gross morphology, cleavage rates, and development to blastocyst. J In Vitro Fertil Embryo Transfer 6, 30-35 (1989)
10. Petroza J.C. & B. O'Brien: Early pregnancy loss. E-Medicine 10, 2002 (2002)
11. Rubio C., C. Simon & T. Vida: Chromosomal abnormalities and embryo development in recurrent miscarriage couples Hum Reprod 18, 182-188 (2003)
12. Robinson W.P., D.E. Mcfadden, M.D. Stephenson: The origin of abnormalities in recurrent aneuploidy/polyploidy. Am J Med Gene 69, 1245-1254 (2001)
13. Bruyere H., R. Rupps & B.D. Kuchinka: Recurrent trisomy 21 in a couple with a child presenting trisomy 21 mosaicism and maternal uniparatal disomy for chromosome 21 in the euploid cell line. Ame J Hum Gene 94, 35-41 (2000)
14. Tseng L.H., S.M. Chung, T.Y. Lee & T.M. Ko: Recurrent Down's syndrome due to maternal ovarian trisomy 21 mosaicism. Arch Gyn Ob 255, 213-216 (1994)
15. Amon A.: The spindle checkpoint. Curr Opin Cell Biol 9, 69-75 (1999).
16. Nicklas R.B.: How cells get the right chromosomes. Science 275, 632-637 (1997)
17. Hoyt M.A.: A new view of the spindle checkpoint. J Cell Biol 154, 909-911 (2001)
18. Li R. & A.W. Murray: Feedback control of mitosis in budding yeast. Cell 66, 519-531 (1991)
19. Hoyt M.A., L. Totis & B.T. Roberts: S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66, 507-517 (1991)
20. Weiss E. and M. Winey: The S. cerevisiae SPB duplication gene MPS1 is part of a mitotic checkpoint. J Cell Biol 132, lll-123 (1996)
21. Chen R.H., J.C. Waters, E.D. Salmon & A.W. Murray: Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science 274, 242-246 (1996)
22. Chen R.H., A. Shevchenko, M. Mann, & A.W. Murray: Spindle checkpoint protein Xmad1 recruits Xmad2 to unattached kinetochores. J Cell Biol 143, 283-295 (1998)
23. Taylor S.S. & F. McKeon: Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage. Cell 89, 727-735 (1997)
24. Taylor S.S., E. Ha & F. McKeon: The human homologue of Bub3 is required for kinetochore localization and a Mad3/Bub1-related protein kinase. J Cell Biol 142, 1-11 (1998)
25. Taylor S.S., D. Hussein, Y. Wang, S. Elderkin & C.J. Morrow: Kinetochore localisation and phosphorylation of the mitotic checkpoint components Bub1 and BubR1 are differentially regulated by spindle events in human cells. J Cell Sci 114, 4385-4395 (2001)
26. Kallio M., J. Weinstein, J.R. Daum, D.J. Burke & G.J. Gorbsky: Mammalian p55CDC mediate association of the spindle checkpoint protein Mad2 with the cyclosme/anaphase-promoting complex, and is involved in regulating anaphase onset and late mitotic events. J Cell Biol 141, 1393-1406 (1998)
27. Maney T., L.M. Ginkel, A.W. Hunter & L. Wordeman: The kinetochore of higher eucaryotes: a molecular view. Int Rev Cytol 194, 67-132 (1999)
28. Sudakin V., G.K. Chan & T.J. Yen: Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J Cell Biol 154, 909-911 (2001)
29. Chen R.H.: BubR1 is essential for kinetochore localization of other spindle checkpoint proteins and its phosphorylation requires Mad1. J Cell Biol 158, 487-496 (2002)
30. Sharp-Baker H., & R.H. Chen: Spindle checkpoint protein Bub1 is required for kinetochore localization of Mad1, Mad2, Bub3, and CENP-E, independently of its kinase activity. J Cell Biol 153, 1239-1250 (2001)
31. Fraschini R., A. Beretta, L. Sironi, A. Musacchio, G. Lucchini & S. Piatti: Bub3 interaction with Mad2, Mad3 and Cdc20 is mediated by WD40 repeats and does not require intact kinetochores. EMBO J 20, 6648-6659 (2001)
32. Vigneron S., S. Prieto, C. Bernis, J.C. Labbe, A. Castro & T. Lorca: Kinetochore localization of spindle checkpoint proteins: Who controls whom. Mol Biol Cell 15, 4584-4596 (2004)
33. Fraschini R., E. Formenti, G. Lucchini & S. Piatti: Budding yeast Bub2 is localized at spindle pole bodies and activates the mitotic checkpoint via a different pathway from Mad2. J Cell Biol 145, 979-991 (1999)
34. Fesquet D., P.J. Fitzpatrick, A.L. Johnson, K.M. Kramer, J.H. Tony & L.H. Johnston: A Bub2p-dependent spindle checkpoint pathway regulates the Dbf2p kinase in budding yeast. EMBO J 18, 2424-2434 (1999)
35. Alexandru G., W. Zachariae, A. Schleidder & K. Nasmyth: Sister chromatid separation and chromosome reduplication are regulated by different mechanisms in response to spindle damage. EMBO J 18, 2707-2721 (1999)
36. Kallio M., J.E. Eriksson & G.J. Gorbsky: Differences in spindle association of the mitotic checkpoint protein Mad2 in mammalian spermatogenesis and oogenesis. Dev Biol 225, 112-123 (2000)
37. Wassmann K., T. Niault & B. Maro: Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol 13, 1596-1608 (2003)
38. Brunet S., G. Pahlavan, S. Taylor & B. Maro: Functionality of the spindle checkpoint during the first meiotic division of mammalian oocytes. Reproduction 126, 443-450 (2003)
39. Zhang D., M. Li, W. Ma, Y. Hou, Y.H. Li, S.W. Li, Q.Y. Sun & W.H. Wang: Localization of MAD1 in mouse oocytes during the first meiosis and its functions as a spindle checkpoint protein. Biol Reprod 72, 58-68 (2005)
40. Zhang D., W. Ma, Y.H. Li, Y. Hou, S.W. Li, X.Q. Meng, X.F. Sun, Q.Y. Sun & W.H. Wang: Intra-oocyte localization of MAD2 and its relationship with kinetochores, microtubules and chromosomes in rat oocytes during meiosis. Biol Reprod 71, 740-748 (2004)
41. Ma W., D. Zhang, Y. Hou, Y.H., Q.Y. Sun, X.F. Sun & W.H. Wang: Reduced expression of MAD2, Bcl-2 and MAP kinase activity in pig oocytes after In vitro ageing are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation. Biol Reprod 72, 373-383 (2005)
42. Homer H.A., A. McDougall, M. Levasseur, K. Yallop, A.P. Murdoch & M. Herbert: Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes Dev 19, 202-207 (2005)
43. Brunet S., A.S. Maria, P. Guillaud, D. Dujardin, J.Z. Kubiak & B. Maro: Kinetochor fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M phase. J Cell Biol 146, 1-11 (1999)
44. Vernos I. & E. Karsenti: Chromosomes take the lead in spindle assembly. Trends Cell Biol 5, 297-301 (1995)
45. Vernos I. & E. Karsenti: The mitotic spindle: A self-made machine Science 294, 543-549 (2001)
46. Pennisi E.: Cell division gatekeepers identified. Science 279, 477-478 (1998)
47. Rieder C.L. & E.D. Salmon: The vertebrate cell kinetochore and its roles during mitosis. Trends Cell Biol 8, 310-318 (1998)
48. Li G.P., Y. Liu, T.D. Bunch, K.L. White & K.I. Aston: Asymmetric division of spindle microtubules and microfilaments during bovine meiosis from metaphase I to metaphase III. Mol Reprod Dev 71, 220-226 (2005)
49. Sun X.F., W.H. Zhang, X.J. Chen, G.H. Xiao, W.Y. Mai & W.H. Wang: Spindle dynamics in living mouse oocytes during meiotic maturation, ageing, cooling and overheating: a study by polarized light microscopy. Zygote 12, 1-9 (2004)
50. Heald R., R. Tournebize, A. Habermann, E. Karsenti & A. Hyman: Spindle assembly in Xenopus egg extracts: Respective roles of centrosomes and microtubule self-organization. J Cell Biol 138, 615-628 (1997)
51. Fan H.Y. & Q.Y. Sun: Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod 70, 535-547 (2004)
52. Dujardin D., U.I. Wacker, A. Moreau, T.A. Schroer & J.E. Rickard: Evidence for a role of CLIP-170 in the establishment of metaphase chromosome alignment. J Cell Biol 141, 849-862 (1998)
53. Sticker S.A.: Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211, 157-176 (1999)
54. Brenner S., D. Pepper, M.W. Burns, E. Tan & B.R. Brinkly: Kinetochore structure, duplication and distribution in mammalian cells: Analysis by human autoantibodies from scleroderma patients J Cell Biol 91, 95-102 (1981)
55. Moroi Y., C. Peebles, M.J. Fritzler & E.M. Tan: Autoantibody to centromere (kinetochore) in scleroderma sera. Proc Natl Acad Sci USA 77, 1627-1631 (1980)
56. Moroi Y., A.L. Hartman, P.K. Nakane & E.M. Tan: Distribution of kinetochore (centromere) antigen in mammalian cell nuclei. J Cell Biol 90, 254-259 (1981)
57. Warburton P.E., C.A. Cooke, S. Bourassa, O. Vafa, B.A. Sullivan, G. Stetten, G. Gimelli, D. Warburton, C. Tyler-Smith, K.F. Sullivan, G.G. Poirier & W.C. Earnshaw: Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres Curr Biol 1, 901-904 (1997)
58. Hudson D.F., K.J. Fowler, E. Earle, R. Saffery, P. Kalitsis, H. Trowell, J. Hill, N.G. Wreford, D.M. de Kretser, M.R. Cancilla, E. Howman, L. Hii, S.M. Cutts, D.V. Irvine & K.H.A. Choo: Centromere protein B null mice are mitotically and meiotically normal but have lower body and testis weights. J Cell Biol 141, 309-319 (1998)
59. Craig J.M., W.C. Earnshaw & P. Vagnarelli: Mammalian centromeres: DNA sequence, protein composition and role in cell cycle progression Exp Cell Res 246, 249-262 (1999)
60. Simerly C., R. Balczon, B.R. Brinkley & G. Schatten: Microinjected kinetochore antibodies interfere with chromosome movement in meiotic and mitotic mouse oocytes. J Cell Biol 111, 1491-1504 (1990)
61. Ma W., Y. Hou, Q.Y. Sun, X.F. Sun & W.H. Wang: Localization of centromere proteins and their association with chromosomes and microtubules during meiotic maturation in porcine oocytes. Reproduction 126, 731-738 (2004)
62. Yen T.J., D.A. Compton, D. Wise, R.P. Zinkowski, B.R. Brinkley, W.C. Earnshaw & D.W. Cleveland: CENP-E, a novel human centromere-associated protein required for progression from metaphase to anaphase. EMBO J 10, 1245-1254 (1991)
63. Tomascik-Cheeseman L., F. Marchetti, X. Lowe, F.L. Shamanski, J. Nath, R.A. Pedersen & A.J. Wyrobek: CENP-B is not critical for meiotic chromosome segregation in male mice. Mutation Res 513, 197-203 (2002)
64. Bernat R.L., G.G. Borisy, N.F. Rothfield & W.C. Earnshaw: Injection of anticentromere antibodies in interphase disrupts events required for chromosome movement in mitosis. J Cell Biol 111, 1519-1533 (1990)
65. Bernat R.L., M.R. Delannoy, N.F. Rothfield & W.C. Earnshaw: Disruption of centromere assembly during interphase inhibits kinetochore morphogenesis and function in mitosis. Cell 66, 1229-1238 (1991)
66. Cimini D., B. Howell, P. Maddox, A. Khodjakov, F. Degrassi & E.D. Salmon: Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells J Cell Biol 153, 517-527 (2001)
67. Polanski Z., E. Ledan, S. Brunet, S. Louvet, J.Z. Kubiak, M.H. Verlhac & B. Maro: Cyclin synthesis controls the progression of meiotic maturation in mouse oocytes. Development 125, 4989-4997 (1998)
68. Jablonski S.A., G.K. Chan, C.A. Cooke, W.C. Eamshwa & T.J. Yen: The hBUB1 and hBUBR1 kineses sequentially assemble onto kinetochores during prophase with hBUBR1 concentrating at the kinetochore plates in mitosis. Chromosoma 107, 386-396 (1998)
69. Abrieu A., L. Magnaghi-Jaulin, J.A. Kahana, M. Peter, A. Castro, S. Vignero, T. Lorca, D.W. Clevland & J.C. Labbe: Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell 106, 83-93 (2001)
70. Adams R.R., H. Maiato, W.C. Earnshaw & M. Carmena: Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histon H3 phosporylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J Cell Biol 153, 865-880 (2001)
71. Kallio M.J., M.L. McCleland, P.T. Stukenburg & G.J. Gorbsky: Inhibition of aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis. Curr Biol 12, 900-905 (2002)
72. Murata-Hori M. & Y. Wang: The kinase activity of Aurora B is required for kinetochore-microtubule interactions during mitosis. Curr Biol 12, 894-899 (2002)
73. Ditchfield C., V.L. Johnson, A. Tighe, R. Ellston, C. Haworth, T. Johnson, A. Mortlock, N. Keen & S.S. Taylor: Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2 and CENP-E to kinetochores. J Cell Biol 161, 267-280 (2003)
74. Johnson V.L., M.I.F. Scott, S.V. Holt, D. Hussein & S.S. Taylor: Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp_F and mad2 and chromosome congression. J Cell Sci 117, 1577-1589 (2004)
75. Liu ST., G.K. Chan, J.C. Hittle, G. Fujii, E. Lees & T.J. Yen: Human MPS1 kinase is required for mitotic arrest induced by the loss of CENP-E from kinetochores. Mol Biol Cell 14, 1638-1651 (2003)
76. Yen T.J., G. Li, B.T. Schaar, I. Szilak & D.W. Cleveland: CENP-E is a putative kinetochore motor that accumulate just before mitosis. Nature 359, 536-539 (1992)
77. Cooke C.A., B. Schaar, T.J. Yen & W.C. Earnshaw: Localization of CENP-E in the fibrous corona and outer plate of mammalian kinetochore from prometaphase through anaphase. Chromosoma 106, 446-455 (1997)
78. Wood K.W., R. Sakowcz, L.S.B. Goldstein & D.W. Cleveland: CENP-E is a plus end-directed kinetochore motor required for metaphase chromosome alignment. Cell 91, 357-366 (1997)
79. Lombillo V.A., C. Nislow, T.J. Yen, V.I. Gelfand & J.R. McIntosh: Antibodies to the kinesin motor domain and CENP-E inhibit microtubule depolymerization-dependent motion of chromosomes in vitro. J Cell Biol 128, 107-115 (1995)
80. Chan G.K., B.T. Schaar & T.J. Yen: Characterization of the kinetochore binding domain of CENP-E reveals interactions with the kinetochore proteins CENP-F and hBUBR1. J Cell Biol 143, 49-63 (1998)
81. Chan G.K., S.A. Jablonski, V. Sudakin, J.C. Hittle & T.J. Yen: Human BUBR1 is a mitotic checkpoint kinase that monitors CENP-E functions at kinetochores and binds the cyclosome/APC. J Cell Biol 146, 941-954 (1999)
82. Yao X., K.L. Anderson & D.W. Cleveland: The microtubule-dependent motor centromere-associated protein E (CENP-E) is an integral component of kinetochore corona fibers that link centromeres to spindle microtubules. J Cell Biol 139, 435-447 (1997)
83. Yao X., A. Abrieu, Y. Zhang, K.F. Sullivan & D.W. Cleveland: CENP-E forms a link between attachment of spindle microtubules to kinetochores and the mitotic checkpoint. Nat Cell Biol 2, 484-491 (2000)
84. Mao Y.A., A. Abrieu & D.W. Cleveland: Activating and silencing the mitotic checkpoint through CENP-E dependent activation/inactivation of BubR1. Cell 114, 87-98 (2003)
85. Weaver B.A.A., Z.O. Bonday, F.B. Putkey, G.J.P.L. Kops, A.D. Silk & D.W. Cleveland: Centromere-associated protein-E is essential for the mammalian mitotic checkpoint to prevent aneuploidy due to signal chromosome loss. J Cell Biol 162, 551-563 (2003)
86. Martinez-Exposito M. J., K.B. Kaplan, J. Copeland & P.K. Sorger: Retention of the BUB3 checkpoint protein on lagging chromosomes. Proc Natl Acad Sci USA 96, 8493-8498 (1999)
87. Fang G.: Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol Biol Cell 13, 755-766 (2002)
88. Wu H., Z. Lan, W. Li, S. Wu, J. Weinstein, K.M. Sakamoto & W. Dai: p55CDC/hCDC20 is associated with BUBR1 and may be a downstream target of the spindle checkpoint kinase. Oncogene 19, 4557-4562 (2000)
89. Chen R.H., D.M. Brady, D. Smith, A.W. Murray & K.G. Hardwick: The spindle checkpoint of budding yeast depends on a tight complex between the Mad1 and Mad2 proteins. Mol Biol Cell 10, 2607-2618 (1999)
90. Sironi L., M. Mapelli, S. Knapp, A. De Antoni, K.T. Jeang & A. Musacchio: Crystal structure of the tetrameric Mad1-Mad2 core complex: implications of a 'safety belt' binding mechanism for the spindle checkpoint. EMBO J 21, 2496-2506 (2002)
91. Chung E. & R.H. Chen: Spindle checkpoint requires Mad1-bound and Mad1-free Mad2. Mol Biol Cell 13, 1501-1511 (2002)
92. Nasmyth K.: Segregating sister genomes: The molecular biology of chromosome separation. Science 297, 559-565 (2002)
93. Uhlmann F.: Chromosome cohesion and separation: from men to molecules. Curr Biol 13, 104-114 (2003)
94. Uhlmann F.: Separase regulation during mitosis. Biochem Soc Symp 70, 243-251 (2003)
95. Page S.L. & R.S. Hawley: Chromosome choreography: the meiotic ballet. Science 301, 785-789 (2003)
96. Tang Z., R. Bharadwaj, B. Li & H. Yu: Mad2-independent inhibition of APCCdc20 by the mitotic checkpoint protein BubR1. Dev Cell 1, 227-237 (2001)
97. Fang G., H. Yu & M.W. Kirschner: The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev 12, 1871-1883 (1998)
98. Howell B.J., B.F. McEwen, J.C. Canman, D.B. Hoffman, E.M. Farrar, C.L. Rieder & E.D. Salmon: Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J Cell Biol 155, 1159-1172 (2001)
99. Pfarr C.M., M. Coue, P.M. Grissom, T.S. Hays, M.E. Porter & J.R. McIntosh: Cytoplasmic dynein is localized to kinetochores during mitosis. Nature 345, 263-265 (1990)
100. Escheverri C.J., B.M. Paschal, K.T. Vaughan & R.B. Vallee: Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J Cell Biol 132, 617-633 (1996)
101. King J.M., T.S. Hays & R.B. Nicklas: Dynein is a transient kinetochore component whose binding is regulated by microtubule attachment, not tension. J Cell Biol 151, 739-748 (2000)
102. Basto R., R. Gomes & R.E. Karess: Rough deal and Zw10 are required for the metaphase checkpoint in Drosophila. Nat Cell Biol 2, 939-943 (2000)
103. Starr D.A., B.C. Williams, T.S. Hays & M.L. Goldberg: ZW10 helps recruit dynactin and dynein to the kinetochore. J Cell Biol 142, 763-774 (1998)
104. Chan G.K., S.A. Jablonski, D.A. Starr, M.L. Goldberg & T.J. Yen: Human Zw10 and ROD are mitotic checkpoint proteins that bind to kinetochores. Nat Cell Biol 2, 944-947 (2000)
105. Scaerou F., I. Aguilera, R. Saunders, N. Kane, L. Blottiere & R. Karess: The rough deal protein is a new kinetochore component required for accurate chromosome segregation in Drosophila. J Cell Sci 112, 3757-3768 (1999)
106. Basu J., E. Logarinho, S. Herrmann, H. Bousbaa, Z. Li, G.K. Chan, T.J. Yen, C.E. Sunkel, & M.L. Goldberg: Localization of the Drosophila checkpoint control protein Bub3 to the kinetochore requires Bub1 but not Zw10 or Rod. Chromosoma 107, 376-385 (1998)
107. Hardwick K.G. & A.W. Murray: Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast. J Cell Biol 131, 709-720 (1995)
108. Campbell M.S., G.K. Chan & T.J. Yen: Mitotic checkpoint proteins HsMAD1 and HsMAD2 are associated with nuclear pore complexes in interphase. J Cell Sci 114, 953-963 (2001)
109. Chung E. & R.H. Chen: Spindle checkpoint requires Mad1-bound and Mad1-free Mad2. Mol Biol Cell 13, 1501-1511 (2002)
110. Pickering S.J., P.R. Braude, M.H. Johnson, A. Cant & J. Currie: Transient cooling to room temperature can cause irreversible disruption the meiotic spindle in the human oocytes. Fertil Steril 54, 102-108 (1990)
111. Wang W.H., L. Meng, R.J. Hackett, R. Oldenbourg & D.L. Keefe: Limited recovery of meiotic spindles in living human oocytes after cooling-rewarming observed using polarized light microscopy. Hum Reprod 16, 2374-2378 (2001)
112. Pickering S.J. & M.H. Johnson: The influence of cooling on the organization of the meiotic spindle of the mouse oocytes. Hum Reprod 2, 207-216 (1987)
113. Liu R.H., Q.Y. Sun, Y.H. LI, L.H. Jiao & W.H. Wang: Effects of cooling on meiotic spindle structure and chromosome alignment within in vitro matured porcine oocytes. Mol Reprod Dev 65, 212-218 (2003)
114. Gorbsky G.J., R.H. Chen & A. Murray: Microinjection of antibody to Mad2 protein into mammalian cells in mitosis induces premature anaphase. J Cell Biol 141, 1193-1205 (1998)
115. Dobles M., V. Liberal, L. Martin, M. Benezra & P.K. Sorger: Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101, 635-645 (2000)
116. Michel L.S., V. Liberal, A. Chatterjee, R. Kirchwegger, B. Pasche, W. Gerald, M. Dobles, P.K. Sorger, V.V. Murty & R. Benezra: MAD2 haploinsufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409, 355-359 (2001)
117. Howell, B.J., D.B. Hoffman, G. Fang, A.W. Murray & E.D. Salmon: Visualization of Mad2 dynamics at kinetochores, along spindle fibers, and at spindle poles in living cells. J Cell Biol 150, 1233-1250 (2000)
118. Skoufias D.A., P.R. Andreassen, F.B. Lacroix, L. Wilson & R.L. Margolis: Mammalian Mad2 and Bub1/BubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints. Proc Natl Acad Sci USA 98, 4492-4497 (2001)
119. Waters J.C., R.H. Chen, A.W. Murray & E.D. Salmon: Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J Cell Biol 141, 1181-1191 (1998)
120. Battaglia D.G., P. Goodwin, N.A. Klein & M.R. Soules: Influence of maternal age on meiotic spindle in oocytes from naturally cycling women. Hum Reprod 11, 2217-2222 (1996)
121. Kallio M., T. Mustalahti, T.J. Yen & J. Lahdetie: Immunolocalization of alpha-tubulin, gamma-tubulin, and CENP-E in male rat and male mouse meiotic division: pathway of meiosis I spindle formation in mammalian spermatocytes. Dev Biol 195, 29-37 (1998)
122. Duesbery N.S., T. Choi, K.D. Brown, K.W. Wood, J. Resau, K. Fukasawa, D.W. Cleveland & G.F. Vande Woude: CENP-E is an essential kinetochore motor in maturing oocytes and is masked during mos-dependent, cell cycle arrest at metaphase II. Proc Natl Acad Sci USA 94, 9165-9170 (1997)
123. Lee J., T. Miyano, Y. Dai, P. Wooding, T.J. Yen, R.M Moor: Specific regulation of CENP-E and kinetochores during meiosis I/meiosis II transition in pig oocytes. Mol Reprod Dev 56, 51-62 (2000)
124. Minshull J., H. Sun, N.K. Tonks & A.W. Murray: A MAP kinase-dependent spindle assembly checkpoint in Xenopus egg extract. Cell 79, 475-486 (1994)
125. Takenaka K., Y. Gotoh & E. Nishida: Map kinase is required for the spindle assembly checkpoint but is dispensable for the normal M phase entry and exit in Xenopus egg cell cycle extracts. J Cell Biol 136, 1091-1097 (1997)
126. Wang X.M., Y. Zhai & J.J. Ferrell: A role for mitogen-activated protein kinase in the spindle assembly checkpoint in XTC cells. J Cell Biol 137, 433-443 (1997)
127. Zecevic M., A.D. Catling, S.T. Eblen, L. Renzi, J.C. Hittle, T.J. Yen, G.J. Gorbsky & M.J. Weber: Active MAP kinase in mitosis: Localization at kinetochores and association with the motor protein CENP-E. J Cell Biol 142, 1547-1558 (1998)
128. Gordo A., C.L. He, S. Smith & R.A. Fissore: Mitogen-activated protein kinase plays a significant role in metaphase II arrest, spindle morphology and maintenance of maturation promoting factor activity in bovine oocytes. Mol Reprod Dev 59, 106-114 (2001)
129. Inoue M., K. Maito, T. Nakayama & E. Sato: Mitogen-activated protein kinase translocates into the germinal vesicle and induces germinal vesicle breakdown in porcine oocytes. Biol Reprod 58, 130-136 (1998)
130. Verlhac M.H., H.D. Pennart, B. Maro, M.H. Cobb & H.J. Clarke: Map kinase becomes stable activated at metaphase and in associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev Biol 158, 330-340 (1993)
131. Lee J., T. Miyano & R.M. Moor: Localization of phosphorylated MAP kinase during transition from meiosis I to meiosis II in pig oocytes. Zygote 8, 119-125 (2000)
132. Vaisberg E.A., M.P. Koonce & J.R. Mcintosh: Cytoplasmic dynein plays a role in mammalian spindle formation. J Cell Biol 123, 849-858 (1993)
133. van Kooij R.J., C.W. Looman, J.D. Habbema, M. Dorland & E.R. te Velde: Age-dependent decrease in embryo implantation rate after in vitro fertilization. Fertil Steril 66, 769-775 (1966)
134. Navot D., A.B. Bergh, M. A. Williams, G.J. Garrisi, I. Guzman, B. Sandler & B. Grundeld: Poor oocyte quality rather than implantation failure as a cause of age related decline in female infertility. Lancet 337, 1375-1377 (1991)
135. Munne S., M. Alikani, G. Tomkin, J. Grifo & J. Cohen: Embryo morphology, developmental rates and maternal age are correlated with chromosome abnormalities. Fertil Steril 64, 382-391 (1995)
136. Benadiva C.A., I. Kligman & S. Munne: Aneuploidy 16 in human embryos increases significantly with maternal age. Fertil Steril 66, 248-255 (1996)
137. Hassold T. & D. Chiu: Maternal age specofic rates of numerical chromosome abnormalities with special reference to trisomy. Hum Genet 70, 11-17 (1985)
138. Verlinsky Y., J. Cieslak & A. Kuliev: High frequency of meiosis II aneuploidies in in vitro fertilization patients of advanced maternal age. Reprod Tech 10, 314-317 (2001)
139. Tarin J.J. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol Hum Reprod 2, 717-724 (1996)
140. Keefe D.L., T. Niven-Fairchild, S. Powell & S. Buradagunta: Mictochondria dexoxyribonucleic acid deletions in oocytes and reproductive aging in women. Fertil Steril 64, 577-583 (1995)
141. Keefe D.L., S. Franco, L. Liu, J. Trimarchi, B. Cao, S. Weitzen, S. Agarwal & M.A. Blasco: Telomere length predicts embryo fragmentation after in vitro fertilization in women - toward a telomere theory of reproductive aging in women. Am J Obstet Gynecol 192, 1256-1260 (2005)
142. Wang W.H., L. Meng, R.J. Hackett & D.L. Keefe: Developmental ability of human oocytes with or without birefringent spindle imaged by Polscope before insemination. Hum Reprod 146, 4-8 (2001)
143. Wang W.H., L. Meng, R.J. Hackett, R. Oldenbourg & D.L. Keefe: Rigorous thermal control during intracytoplasmic sperm injection stabilizes the meiotic spindle and improves fertilization and pregnancy rates. Fertil Steril 77, 1274-1277 (2002)
144. Yoon P.W., S.B. Freeman & S.L. Sherman: Advanced maternal age and the risk of Down syndrome characterized by the meiotic stage of chromosomal error: a population-based study. Ame J Hum Gnet 58, 628-633 (1996)
145. Giorlandino C., G. Calugi & L. Laconianni: Spermatozoa with chromosomal abnormalities may result in a higher rate of recurrent abortion. Fertil Steril 70, 576-577 (1998)
146. Bernardini L.M., M. Cosata, C. Bottazzi, L. Gianaroli, M.C. Magli, P.L. Venturini, R. Francisco, N. Conte and N. Ragni: Sperm aneuploid and recurrent pregnancy loss. Reprod Biomed Online 9, 312-320 (2004)
147. Verlinsky Y., J. Cieslak & V. Ivakhenenko: Preimplantation diagnosis of common aneuploidies by the first and second polar body FISH analysis. J Assis Reprod Genet 15, 285-289 (1998)
148. Munne S.: Preimplantation genetic diagnosis of numerical and structural chromosome abnormalities. Reprod Biomed Online 4, 183-196 (2002)