Dual-mode regulation of the APC/C by CDK1 and MAPK controls meiosis I progression and fidelity

Journal of Cell Biology

Volumn 204, Issue 6, 2014, Pages 891-900

  Nabti, Ibtissem ^a   Marangos, Petros ^a,c   Bormann, Jenny ^a   Kudo, Nobuaki R ^d   Carroll, John ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF IOANNINA   (Greece)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CYCLIN DEPENDENT KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN MAD2; SECURIN;

ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CENTROMERE; CHROMOSOME NUMBER; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; M PHASE CELL CYCLE CHECKPOINT; MEIOSIS; METAPHASE; MICROTUBULE; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; ANIMALS; CDC2 PROTEIN KINASE; CELLS, CULTURED; CHROMATIDS; CHROMOSOME SEGREGATION; FEMALE; KINETOCHORES; M PHASE CELL CYCLE CHECKPOINTS; MAD2 PROTEINS; MEIOTIC PROPHASE I; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASES; OOCYTES; PROMETAPHASE; SECURIN;

EID: 84896266290     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201305049     Document Type: Article

References (63)

1. Angell, R.R. 1991. Predivision in human oocytes at meiosis I: a mechanism for trisomy formation in man. Hum. Genet. 86:383-387. http://dx.doi.org/10 .1007/BF00201839
2. Angell, R. 1997. First-meiotic-division nondisjunction in human oocytes. Am. J. Hum. Genet. 61:23-32. http://dx.doi.org/10.1086/513890
3. Chambon, J.P., S.A. Touati, S. Berneau, D. Cladière, C. Hebras, R. Groeme, A. McDougall, and K. Wassmann. 2013. The PP2A inhibitor I2PP2A is essential for sister chromatid segregation in oocyte meiosis II. Curr. Biol. 23:485-490. http://dx.doi.org/10.1016/j.cub.2013.02.004
4. Chung, E.N., and R.H. Chen. 2003. Phosphorylation of Cdc20 is required for its inhibition by the spindle checkpoint. Nat. Cell Biol. 5:748-753. http:// dx.doi.org/10.1038/ncb1022
5. Ciosk, R., W. Zachariae, C. Michaelis, A. Shevchenko, M. Mann, and K. Nasmyth. 1998. An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell. 93:1067-1076. http://dx.doi.org/10.1016/S0092-8674(00)81211-8
6. Clute, P., and J. Pines. 1999. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1:82-87. http://dx.doi.org/10.1038/10049
7. Conti, M., M. Hsieh, A.M. Zamah, and J.S. Oh. 2012. Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol. Cell. Endocrinol. 356:65-73. http://dx.doi.org/10.1016/j.mce.2011.11.002
8. Coonrod, S.A., L.C. Bolling, P.W. Wright, P.E. Visconti, and J.C. Herr. 2001. A morpholino phenocopy of the mouse mos mutation. Genesis. 30:198-200. http://dx.doi.org/10.1002/gene.1065
9. D'Angiolella, V., C. Mari, D. Nocera, L. Rametti, and D. Grieco. 2003. The spindle checkpoint requires cyclin-dependent kinase activity. Genes Dev. 17:2520-2525. http://dx.doi.org/10.1101/gad.267603
10. Davydenko, O., R.M. Schultz, and M.A. Lampson. 2013. Increased CDK1 activity determines the timing of kinetochore-microtubule attachments in meiosis I. J. Cell Biol. 202:221-229. http://dx.doi.org/10.1083/jcb.201303019
11. Duncan, F.E., T. Chiang, R.M. Schultz, and M.A. Lampson. 2009. Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs. Biol. Reprod. 81:768-776. http://dx.doi.org/10.1095/biolreprod.109.077909
12. Favata, M.F., K.Y. Horiuchi, E.J. Manos, A.J. Daulerio, D.A. Stradley, W.S. Feeser, D.E. Van Dyk, W.J. Pitts, R.A. Earl, F. Hobbs, et al. 1998. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273:18623-18632. http://dx.doi.org/10.1074/jbc.273.29.18623
13. Gavet, O., and J. Pines. 2010. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev. Cell. 18:533-543. http://dx.doi.org/10.1016/j .devcel.2010.02.013
14. Gorr, I.H., A. Reis, D. Boos, M. Wühr, S. Madgwick, K.T. Jones, and O. Stemmann. 2006. Essential CDK1-inhibitory role for separase during meiosis I in vertebrate oocytes. Nat. Cell Biol. 8:1035-1037. http://dx .doi.org/10.1038/ncb1467
15. Hached, K., S.Z. Xie, E. Buffin, D. Cladière, C. Rachez, M. Sacras, P.K. Sorger, and K. Wassmann. 2011. Mps1 at kinetochores is essential for female mouse meiosis I. Development. 138:2261-2271. http://dx.doi.org/10 .1242/dev.061317
16. Hashimoto, N., and T. Kishimoto. 1988. Regulation of meiotic metaphase by a cytoplasmic maturation-promoting factor during mouse oocyte maturation. Dev. Biol. 126:242-252. http://dx.doi.org/10.1016/0012-1606(88)90135-2
17. Herbert, M., M. Levasseur, H. Homer, K. Yallop, A. Murdoch, and A. McDougall. 2003. Homologue disjunction in mouse oocytes requires proteolysis of securin and cyclin B1. Nat. Cell Biol. 5:1023-1025. http://dx.doi.org/10 .1038/ncb1062
18. Hershko, A., D. Ganoth, V. Sudakin, A. Dahan, L.H. Cohen, F.C. Luca, J.V. Ruderman, and E. Eytan. 1994. Components of a system that ligates cyclin to ubiquitin and their regulation by the protein kinase cdc2. J. Biol. Chem. 269:4940-4946.
19. Hewitt, L., A. Tighe, S. Santaguida, A.M. White, C.D. Jones, A. Musacchio, S. Green, and S.S. Taylor. 2010. Sustained Mps1 activity is required in mitosis to recruit O-Mad2 to the Mad1-C-Mad2 core complex. J. Cell Biol. 190:25-34. http://dx.doi.org/10.1083/jcb.201002133
20. Hoffmann, S., B. Maro, J.Z. Kubiak, and Z. Polanski. 2011. A single bivalent efficiently inhibits cyclin B1 degradation and polar body extrusion in mouse oocytes indicating robust SAC during female meiosis I. PLoS ONE. 6: e27143. http://dx.doi.org/10.1371/journal.pone.0027143
21. Holt, J.E., S.I.R. Lane, P. Jennings, I. García-Higuera, S. Moreno, and K.T. Jones. 2012. APC(FZR1) prevents nondisjunction in mouse oocytes by controlling meiotic spindle assembly timing. Mol. Biol. Cell. 23:3970-3981. http://dx.doi.org/10.1091/mbc.E12-05-0352
22. Homer, H. 2013. The APC/C in female mammalian meiosis I. Reproduction. 146:R61-R71. http://dx.doi.org/10.1530/REP-13-0163
23. Homer, H.A., A. McDougall, M. Levasseur, A.P. Murdoch, and M. Herbert. 2005a. Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction. 130:829-843. http://dx.doi.org/10.1530/rep.1.00856
24. Homer, H.A., A. McDougall, M. Levasseur, K. Yallop, A.P. Murdoch, and M. Herbert. 2005b. Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes Dev. 19:202-207. http://dx.doi.org/10.1101/gad.328105
25. Homer, H., L. Gui, and J. Carroll. 2009. A spindle assembly checkpoint protein functions in prophase I arrest and prometaphase progression. Science. 326:991-994. http://dx.doi.org/10.1126/science.1175326
26. Illingworth, C., N. Pirmadjid, P. Serhal, K. Howe, and G. Fitzharris. 2010. MCAK regulates chromosome alignment but is not necessary for preventing aneuploidy in mouse oocyte meiosis I. Development. 137:2133-2138. http://dx.doi.org/10.1242/dev.048306
27. Inoue, D., M. Ohe, Y. Kanemori, T. Nobui, and N. Sagata. 2007. A direct link of the Mos-MAPK pathway to Erp1/Emi2 in meiotic arrest of Xenopus laevis eggs. Nature. 446:1100-1104. http://dx.doi.org/10.1038/nature05688
28. Jaspersen, S.L., J.F. Charles, and D.O. Morgan. 1999. Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr. Biol. 9:227-236. http://dx.doi.org/10.1016/ S0960-9822(99)80111-0
29. Jones, K.T. 2008. Meiosis in oocytes: predisposition to aneuploidy and its increased incidence with age. Hum. Reprod. Update. 14:143-158. http:// dx.doi.org/10.1093/humupd/dmm043
30. Kim, S., H.B. Sun, H.L. Ball, K. Wassmann, X.L. Luo, and H.T. Yu. 2010. Phosphorylation of the spindle checkpoint protein Mad2 regulates its conformational transition. Proc. Natl. Acad. Sci. USA. 107:19772-19777. http://dx.doi.org/10.1073/pnas.1009000107
31. Kotani, S., S. Tugendreich, M. Fujii, P.M. Jorgensen, N. Watanabe, C. Hoog, P. Hieter, and K. Todokoro. 1998. PKA and MPF-activated polo-like kinase regulate anaphase-promoting complex activity and mitosis progression. Mol. Cell. 1:371-380. http://dx.doi.org/10.1016/S1097-2765 (00)80037-4
32. Kraft, C., F. Herzog, C. Gieffers, K. Mechtler, A. Hagting, J. Pines, and J.M. Peters. 2003. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22:6598-6609. http://dx.doi.org/10 .1093/emboj/cdg627
33. Ledan, E., Z. Polanski, M.E. Terret, and B. Maro. 2001. Meiotic maturation of the mouse oocyte requires an equilibrium between cyclin B synthesis and degradation. Dev. Biol. 232:400-413. http://dx.doi.org/10.1006/dbio .2001.0188
34. Madgwick, S., V.L. Nixon, H.Y. Chang, M. Herbert, M. Levasseur, and K.T. Jones. 2004. Maintenance of sister chromatid attachment in mouse eggs through maturation-promoting factor activity. Dev. Biol. 275:68-81. http:// dx.doi.org/10.1016/j.ydbio.2004.07.024
35. McGarry, T.J., and M.W. Kirschner. 1998. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell. 93:1043-1053. http://dx.doi.org/ 10.1016/S0092-8674(00)81209-X
36. McGuinness, B.E., M. Anger, A. Kouznetsova, A.M. Gil-Bernabé, W. Helmhart, N.R. Kudo, A. Wuensche, S. Taylor, C. Hoog, B. Novak, and K. Nasmyth. 2009. Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr. Biol. 19:369-380. http://dx.doi.org/ 10.1016/j.cub.2009.01.064
37. Meijer, L., A. Borgne, O. Mulner, J.P. Chong, J.J. Blow, N. Inagaki, M. Inagaki, J.G. Delcros, and J.P. Moulinoux. 1997. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur. J. Biochem. 243:527-536. http://dx.doi .org/10.1111/j.1432-1033.1997.t01-2-00527.x
38. Morin, V., S. Prieto, S. Melines, S. Hem, M. Rossignol, T. Lorca, J. Espeut, N. Morin, and A. Abrieu. 2012. CDK-dependent potentiation of MPS1 kinase activity is essential to the mitotic checkpoint. Curr. Biol. 22:289-295. http://dx.doi.org/10.1016/j.cub.2011.12.048
39. Musacchio, A., and E.D. Salmon. 2007. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8:379-393. http://dx.doi.org/10 .1038/nrm2163
40. Nabti, I., A. Reis, M. Levasseur, O. Stemmann, and K.T. Jones. 2008. Securin and not CDK1/cyclin B1 regulates sister chromatid disjunction during meiosis II in mouse eggs. Dev. Biol. 321:379-386. http://dx.doi.org/10 .1016/j.ydbio.2008.06.036
41. Nagaoka, S.I., T.J. Hassold, and P.A. Hunt. 2012. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Rev. Genet. 13:493-504. http://dx.doi.org/10.1038/nrg3245
42. Nishiyama, T., K. Ohsumi, and T. Kishimoto. 2007. Phosphorylation of Erp1 by p90rsk is required for cytostatic factor arrest in Xenopus laevis eggs. Nature. 446:1096-1099. http://dx.doi.org/10.1038/nature05696
43. Peters, J.M. 2002. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell. 9:931-943. http://dx.doi.org/10.1016/S1097-2765 (02)00540-3
44. Peters, J.M. 2006. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 7:644-656. http://dx.doi.org/ 10.1038/nrm1988
45. -/- parthenogenotes. Dev. Biol. 247:210-223. http://dx.doi.org/10.1006/ dbio.2002.0680
46. Pines, J. 2011. Cubism and the cell cycle: the many faces of the APC/C. Nat. Rev. Mol. Cell Biol. 12:427-438. http://dx.doi.org/10.1038/nrm3132
47. Polanski, Z., E. Ledan, S. Brunet, S. Louvet, M.H. Verlhac, J.Z. Kubiak, and B. Maro. 1998. Cyclin synthesis controls the progression of meiotic maturation in mouse oocytes. Development. 125:4989-4997.
48. Potapova, T.A., J.R. Daum, B.D. Pittman, J.R. Hudson, T.N. Jones, D.L. Satinover, P.T. Stukenberg, and G.J. Gorbsky. 2006. The reversibility of mitotic exit in vertebrate cells. Nature. 440:954-958. http://dx.doi.org/10 .1038/nature04652
49. Reis, A., S. Madgwick, H.Y. Chang, I. Nabti, M. Levasseur, and K.T. Jones. 2007. Prometaphase APCcdh1 activity prevents non-disjunction in mammalian oocytes. Nat. Cell Biol. 9:1192-1198. http://dx.doi.org/10.1038/ncb1640
50. Schwab, M.S., B.T. Roberts, S.D. Gross, B.J. Tunquist, F.E. Taieb, A.L. Lewellyn, and J.L. Maller. 2001. Bub1 is activated by the protein kinase p90(Rsk) during Xenopus oocyte maturation. Curr. Biol. 11:141-150. http://dx.doi.org/10.1016/S0960-9822(01)00045-8
51. Shoji, S., N. Yoshida, M. Amanai, M. Ohgishi, T. Fukui, S. Fujimoto, Y. Nakano, E. Kajikawa, and A.C.F. Perry. 2006. Mammalian Emi2 mediates cytostatic arrest and transduces the signal for meiotic exit via Cdc20. EMBO J. 25:834-845. http://dx.doi.org/10.1038/sj.emboj.7600953
52. Terret, M.E., K. Wassmann, I. Waizenegger, B. Maro, J.M. Peters, and M.H. Verlhac. 2003. The meiosis I-to-meiosis II transition in mouse oocytes requires separase activity. Curr. Biol. 13:1797-1802. http://dx.doi.org/10 .1016/j.cub.2003.09.032
53. Tung, J.J., D.V. Hansen, K.H. Ban, A.V. Loktev, M.K. Summers, J.R. Adler III, and P.K. Jackson. 2005. A role for the anaphase-promoting complex inhibitor Emi2/XErp1, a homolog of early mitotic inhibitor 1, in cytostatic factor arrest of Xenopus eggs. Proc. Natl. Acad. Sci. USA. 102:4318-4323. http://dx.doi.org/10.1073/pnas.0501108102
54. Visintin, R., S. Prinz, and A. Amon. 1997. CDC20 and CDH1: a family of substratespecific activators of APC-dependent proteolysis. Science. 278:460-463. http://dx.doi.org/10.1126/science.278.5337.460
55. Wassmann, K., V. Liberal, and R. Benezra. 2003a. Mad2 phosphorylation regulates its association with Mad1 and the APC/C. EMBO J. 22:797-806. http://dx.doi.org/10.1093/emboj/cdg071
56. Wassmann, K., T. Niault, and B. Maro. 2003b. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr. Biol. 13:1596-1608. http://dx.doi.org/10.1016/j.cub.2003.08.052
57. Waters, J.C., R.H. Chen, A.W. Murray, and E.D. Salmon. 1998. Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J. Cell Biol. 141:1181-1191. http://dx.doi.org/10.1083/jcb.141.5.1181
58. Wu, J.Q., D.V. Hansen, Y.X. Guo, M.Z. Wang, W.L. Tang, C.D. Freel, J.J. Tung, P.K. Jackson, and S. Kornbluth. 2007. Control of Emi2 activity and stability through Mos-mediated recruitment of PP2A. Proc. Natl. Acad. Sci. USA. 104:16564-16569. http://dx.doi.org/10.1073/pnas.0707537104
59. Yamamoto, A., V. Guacci, and D. Koshland. 1996. Pds1p is required for faithful execution of anaphase in the yeast, Saccharomyces cerevisiae. J. Cell Biol. 133:85-97. http://dx.doi.org/10.1083/jcb.133.1.85
60. Yu, L.Z., B. Xiong, W.X. Gao, C.M. Wang, Z.S. Zhong, L.J. Huo, Q. Wang, Y. Hou, K. Liu, X.J. Liu, et al. 2007. MEK1/2 regulates microtubule organization, spindle pole tethering and asymmetric division during mouse oocyte meiotic maturation. Cell Cycle. 6:330-338. http://dx.doi.org/10.4161/ cc.6.3.3805
61. Zachariae, W., M. Schwab, K. Nasmyth, and W. Seufert. 1998. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science. 282:1721-1724. http://dx.doi.org/10.1126/science .282.5394.1721
62. Zhao, Y., and R.H. Chen. 2006. Mps1 phosphorylation by MAP kinase is required for kinetochore localization of spindle-checkpoint proteins. Curr. Biol. 16:1764-1769. http://dx.doi.org/10.1016/j.cub.2006.07.058
63. Zur, A., and M. Brandeis. 2001. Securin degradation is mediated by fzy and fzr, and is required for complete chromatid separation but not for cytokinesis. EMBO J. 20:792-801. http://dx.doi.org/10.1093/emboj/20.4.792