Inherent Instability of Correct Kinetochore-Microtubule Attachments during Meiosis I in Oocytes

Developmental Cell

Volumn 33, Issue 5, 2015, Pages 589-602

  Yoshida, Shuhei ^a   Kaido, Masako ^a   Kitajima, Tomoya S ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; AURORA C KINASE; BUB1 SPINDLE CHECKPOINT PROTEIN; BUB1B PROTEIN, MOUSE; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE 1; PHOSPHOPROTEIN PHOSPHATASE 2; PPP2R5A PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL FUSION; CHROMOSOME SEGREGATION; COLD TREATMENT; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; FLUORESCENCE; IN VITRO STUDY; KINETOCHORE MICROTUBULE; MEIOSIS; METAPHASE; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROMETAPHASE; TIME LAPSE IMAGING; ANIMAL; CENTROMERE; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE PROCESSING; METABOLISM; MICROTUBULE; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; AURORA KINASE B; AURORA KINASE C; CDC2 PROTEIN KINASE; CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE PROCESSING, COMPUTER-ASSISTED; KINETOCHORES; MEIOSIS; MICE; MICROTUBULES; OOCYTES; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; PROTEIN-SERINE-THREONINE KINASES;

EID: 84930575863     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.04.020     Document Type: Article

References (63)

1. Akiyoshi B., Sarangapani K.K., Powers A.F., Nelson C.R., Reichow S.L., Arellano-Santoyo H., Gonen T., Ranish J.A., Asbury C.L., Biggins S. Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 2010, 468:576-579.
2. Balboula A.Z., Schindler K. Selective disruption of aurora C kinase reveals distinct functions from aurora B kinase during meiosis in mouse oocytes. PLoS Genet. 2014, 10:e1004194.
3. Brunet S., Maria A.S., Guillaud P., Dujardin D., Kubiak J.Z., Maro B. Kinetochore 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. 1999, 146:1-12.
4. Campbell C.S., Desai A. Tension sensing by Aurora B kinase is independent of survivin-based centromere localization. Nature 2013, 497:118-121.
5. Carninci P., Kasukawa T., Katayama S., Gough J., Frith M.C., Maeda N., Oyama R., Ravasi T., Lenhard B., Wells C., et al. The transcriptional landscape of the mammalian genome. Science 2005, 309:1559-1563. FANTOM Consortium, RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group)RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group).
6. Cheerambathur D.K., Desai A. Linked in: formation and regulation of microtubule attachments during chromosome segregation. Curr. Opin. Cell Biol. 2014, 26:113-122.
7. Cheeseman I.M., Chappie J.S., Wilson-Kubalek E.M., Desai A. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 2006, 127:983-997.
8. Choi T., Aoki F., Mori M., Yamashita M., Nagahama Y., Kohmoto K. Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 1991, 113:789-795.
9. Davydenko O., Schultz R.M., Lampson M.A. Increased CDK1 activity determines the timing of kinetochore-microtubule attachments in meiosis I. J.Cell Biol. 2013, 202:221-229.
10. DeLuca J.G., Gall W.E., Ciferri C., Cimini D., Musacchio A., Salmon E.D. Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 2006, 127:969-982.
11. DeLuca K.F., Lens S.M., DeLuca J.G. Temporal changes in Hec1 phosphorylation control kinetochore-microtubule attachment stability during mitosis. J.Cell Sci. 2011, 124:622-634.
12. Diaz-Rodríguez E., Sotillo R., Schvartzman J.-M.M., Benezra R. Hec1 overexpression hyperactivates the mitotic checkpoint and induces tumor formation invivo. Proc. Natl. Acad. Sci. USA 2008, 105:16719-16724.
13. Elowe S., Dulla K., Uldschmid A., Li X., Dou Z., Nigg E.A. Uncoupling of the spindle-checkpoint and chromosome-congression functions of BubR1. J.Cell Sci. 2010, 123:84-94.
14. Foley E.A., Kapoor T.M. Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell Biol. 2013, 14:25-37.
15. Foley E.A., Maldonado M., Kapoor T.M. Formation of stable attachments between kinetochores and microtubules depends on the B56-PP2A phosphatase. Nat. Cell Biol. 2011, 13:1265-1271.
16. Fuller B.G., Lampson M.A., Foley E.A., Rosasco-Nitcher S., Le K.V., Tobelmann P., Brautigan D.L., Stukenberg P.T., Kapoor T.M. Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient. Nature 2008, 453:1132-1136.
17. Gavin A.C., Cavadore J.C., Schorderet-Slatkine S. Histone H1 kinase activity, germinal vesicle breakdown and M phase entry in mouse oocytes. J.Cell Sci. 1994, 107:275-283.
18. Gui L., Homer H. Spindle assembly checkpoint signalling is uncoupled from chromosomal position in mouse oocytes. Development 2012, 139:1941-1946.
19. Holt J.E., Jones K.T. Control of homologous chromosome division in the mammalian oocyte. Mol. Hum. Reprod. 2009, 15:139-147.
20. Huang H., Hittle J., Zappacosta F., Annan R.S., Hershko A., Yen T.J. Phosphorylation sites in BubR1 that regulate kinetochore attachment, tension, and mitotic exit. J.Cell Biol. 2008, 183:667-680.
21. Ishiguro K., Kim J., Fujiyama-Nakamura S., Kato S., Watanabe Y. A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep. 2011, 12:267-275.
22. Jones K.T., Lane S.I. Molecular causes of aneuploidy in mammalian eggs. Development 2013, 140:3719-3730.
23. Kabeche L., Compton D.A. Cyclin A regulates kinetochore microtubules to promote faithful chromosome segregation. Nature 2013, 502:110-113.
24. King J.M., Nicklas R.B. Tension on chromosomes increases the number of kinetochore microtubules but only within limits. J.Cell Sci. 2000, 113:3815-3823.
25. Kitajima T.S., Ohsugi M., Ellenberg J. Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 2011, 146:568-581.
26. Kiyomitsu T., Obuse C., Yanagida M. Human Blinkin/AF15q14 is required for chromosome alignment and the mitotic checkpoint through direct interaction with Bub1 and BubR1. Dev. Cell 2007, 13:663-676.
27. Kolano A., Brunet S., Silk A.D., Cleveland D.W., Verlhac M.-H.H. Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. Proc. Natl. Acad. Sci. USA 2012, 109:E1858-E1867.
28. Kouznetsova A., Lister L., Nordenskjöld M., Herbert M., Höög C. Bi-orientation of achiasmatic chromosomes in meiosis I oocytes contributes to aneuploidy in mice. Nat. Genet. 2007, 39:966-968.
29. Kruse T., Zhang G., Larsen M.S., Lischetti T., Streicher W., Kragh Nielsen T., Bjørn S.P., Nilsson J. Direct binding between BubR1 and B56-PP2A phosphatase complexes regulate mitotic progression. J.Cell Sci. 2013, 126:1086-1092.
30. Lampson M.A., Cheeseman I.M. Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends Cell Biol. 2011, 21:133-140.
31. Lane S.I., Jones K.T. Non-canonical function of spindle assembly checkpoint proteins after APC activation reduces aneuploidy in mouse oocytes. Nat. Commun. 2014, 5:3444.
32. Lane S.I., Chang H.-Y.Y., Jennings P.C., Jones K.T. The Aurora kinase inhibitor ZM447439 accelerates first meiosis in mouse oocytes by overriding the spindle assembly checkpoint. Reproduction 2010, 140:521-530.
33. Lane S.I., Yun Y., Jones K.T. Timing of anaphase-promoting complex activation in mouse oocytes is predicted by microtubule-kinetochore attachment but not by bivalent alignment or tension. Development 2012, 139:1947-1955.
34. LeMaire-Adkins R., Radke K., Hunt P.A. Lack of checkpoint control at the metaphase/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females. J.Cell Biol. 1997, 139:1611-1619.
35. Li X., Sakashita G., Matsuzaki H., Sugimoto K., Kimura K., Hanaoka F., Taniguchi H., Furukawa K., Urano T. Direct association with inner centromere protein (INCENP) activates the novel chromosomal passenger protein, Aurora-C. J.Biol. Chem. 2004, 279:47201-47211.
36. Liu D., Vader G., Vromans M.J., Lampson M.A., Lens S.M. Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 2009, 323:1350-1353.
37. Maresca T.J., Salmon E.D. Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J.Cell Biol. 2009, 184:373-381.
38. Nagaoka S.I., Hodges C.A., Albertini D.F., Hunt P.A. Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr. Biol. 2011, 21:651-657.
39. Nezi L., Musacchio A. Sister chromatid tension and the spindle assembly checkpoint. Curr. Opin. Cell Biol. 2009, 21:785-795.
40. Polanski Z., Ledan E., Brunet S., Louvet S., Verlhac M.H., Kubiak J.Z., Maro B. Cyclin synthesis controls the progression of meiotic maturation in mouse oocytes. Development 1998, 125:4989-4997.
41. Rabut G., Ellenberg J. Automatic real-time three-dimensional cell tracking by fluorescence microscopy. J.Microsc. 2004, 216:131-137.
42. Rattani A., Wolna M., Ploquin M., Helmhart W., Morrone S., Mayer B., Godwin J., Xu W., Stemmann O., Pendas A., Nasmyth K. Sgol2 provides a regulatory platform that coordinates essential cell cycle processes during meiosis I in oocytes. eLife 2013, 2:e01133.
43. Renshaw M.J., Ward J.J., Kanemaki M., Natsume K., Nédélec F.J., Tanaka T.U. Condensins promote chromosome recoiling during early anaphase to complete sister chromatid separation. Dev. Cell 2010, 19:232-244.
44. Sakuno T., Tada K., Watanabe Y. Kinetochore geometry defined by cohesion within the centromere. Nature 2009, 458:852-858.
45. Sakuno T., Tanaka K., Hauf S., Watanabe Y. Repositioning of aurora B promoted by chiasmata ensures sister chromatid mono-orientation in meiosis I. Dev. Cell 2011, 21:534-545.
46. Sarangapani K.K., Asbury C.L. Catch and release: how do kinetochores hook the right microtubules during mitosis?. Trends Genet. 2014, 30:150-159.
47. Sasai K., Katayama H., Stenoien D.L., Fujii S., Honda R., Kimura M., Okano Y., Tatsuka M., Suzuki F., Nigg E.A., et al. Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil. Cytoskeleton 2004, 59:249-263.
48. Sayaka W., Satoshi K., Van Thuan N., Hiroshi O., Takafusa H., Eiji M., Thuy B.H., Masashi M., Teruhiko W. Effect of volume of oocyte cytoplasm on embryo development after parthenogenetic activation, intracytoplasmic sperm injection, or somatic cell nuclear transfer. Zygote 2008, 16:211-222.
49. Schindler K., Davydenko O., Fram B., Lampson M.A., Schultz R.M. Maternally recruited Aurora C kinase is more stable than Aurora B to support mouse oocyte maturation and early development. Proc. Natl. Acad. Sci. USA 2012, 109:E2215-E2222.
50. Schuh M., Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 2007, 130:484-498.
51. Sebestova J., Danylevska A., Novakova L., Kubelka M., Anger M. Lack of response to unaligned chromosomes in mammalian female gametes. Cell Cycle 2012, 11:3011-3018.
52. Solc P., Kitajima T.S., Yoshida S., Brzakova A., Kaido M., Baran V., Mayer A., Samalova P., Motlik J., Ellenberg J. Multiple requirements of PLK1 during mouse oocyte maturation. PLoS ONE 2015, 10:e0116783.
53. Suijkerbuijk S.J., Vleugel M., Teixeira A., Kops G.J. Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochore-microtubule attachments. Dev. Cell 2012, 23:745-755.
54. Suzuki A., Badger B.L., Wan X., DeLuca J.G., Salmon E.D. The architecture of CCAN proteins creates a structural integrity to resist spindle forces and achieve proper Intrakinetochore stretch. Dev. Cell 2014, 30:717-730.
55. Tada K., Susumu H., Sakuno T., Watanabe Y. Condensin association with histone H2A shapes mitotic chromosomes. Nature 2011, 474:477-483.
56. Tanaka T.U. Kinetochore-microtubule interactions: steps towards bi-orientation. EMBO J. 2010, 29:4070-4082.
57. Tseng T.C., Chen S.H., Hsu Y.P., Tang T. Protein kinase profile of sperm and eggs: cloning and characterization of two novel testis-specific protein kinases (AIE1, AIE2) related to yeast and fly chromosome segregation regulators. DNA Cell Biol. 1998, 10:823-833.
58. Uchida K.S., Takagaki K., Kumada K., Hirayama Y., Noda T., Hirota T. Kinetochore stretching inactivates the spindle assembly checkpoint. J.Cell Biol. 2009, 184:383-390.
59. Wassmann K., Niault T., Maro B. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr. Biol. 2003, 13:1596-1608.
60. Watanabe Y. Geometry and force behind kinetochore orientation: lessons from meiosis. Nat. Rev. Mol. Cell Biol. 2012, 13:370-382.
61. Welburn J.P., Vleugel M., Liu D., Yates J.R., Lampson M.A., Fukagawa T., Cheeseman I.M. Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol. Cell 2010, 38:383-392.
62. Yang K.-T.T., Li S.-K.K., Chang C.-C.C., Tang C.-J.C.J., Lin Y.-N.N., Lee S.-C.C., Tang T.K. Aurora-C kinase deficiency causes cytokinesis failure in meiosis I and production of large polyploid oocytes in mice. Mol. Biol. Cell 2010, 21:2371-2383.
63. Yue Z., Carvalho A., Xu Z., Yuan X., Cardinale S., Ribeiro S., Lai F., Ogawa H., Gudmundsdottir E., Gassmann R., et al. Deconstructing Survivin: comprehensive genetic analysis of Survivin function by conditional knockout in a vertebrate cell line. J.Cell Biol. 2008, 183:279-296.