The APC/C in female mammalian meiosis i

Reproduction

Volumn 146, Issue 2, 2013, Pages

  Homer, Hayden ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Institute for Women's Health   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIN A1; CYCLIN A2; CYCLIN B1; CYCLIN B2; CYCLIN DEPENDENT KINASE 1;

ANAPHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CENTROSOME; MEIOSIS; MITOSIS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROMETAPHASE; PROPHASE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW; UBIQUITINATION;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; ANIMALS; CYCLIN A2; CYCLIN B1; CYCLIN B2; FEMALE; HUMANS; MEIOSIS; MODELS, BIOLOGICAL; OOCYTES; OOGENESIS; PROTEIN TRANSPORT; PROTEOLYSIS;

EID: 84880553345     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-13-0163     Document Type: Review

References (72)

1. Bellanger S, de Gramont A & Sobczak-Thepot J 2007 Cyclin B2 suppresses mitotic failure and DNA re-replication in human somatic cells knocked down for both cyclins B1 and B2. Oncogene 26 7175-7184. (doi:10.1038/sj.onc. 1210539)
2. Brandeis M, Rosewell I, Carrington M, Crompton T, Jacobs MA, Kirk J, Gannon J & Hunt T 1998 Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. PNAS 95 4344-4349. (doi:10.1073/pnas.95.8.4344)
3. Breuer M, Kolano A, Kwon M, Li CC, Tsai TF, Pellman D, Brunet S & Verlhac MH 2010 HURP permits MTOC, sorting for robust meiotic spindle bipolarity, similar to extra centrosome clustering in cancer cells. Journal of Cell Biology 191 1251-1260. (doi:10.1083/jcb.201005065)
4. Brunet S, Dumont J, Lee KW, Kinoshita K, Hikal P, Gruss OJ, Maro B & Verlhac MH 2008 Meiotic regulation of TPX2 protein levels governs cell cycle progression in mouse oocytes. PLoS ONE 3 e3338. (doi:10.1371/ journal.pone.0003338)
5. Campbell CS & Desai A 2013 What the Hec is up with mouse oocyte meiosis? Developmental Cell 25 3-4. (doi:10.1016/j.devcel.2013.03.018)
6. Chapman DL & Wolgemuth DJ 1993 Isolation of the murine cyclin B2 cDNA and characterization of the lineage and temporal specificity of expression of the B1 and B2 cyclins during oogenesis, spermatogenesis and early embryogenesis. Development 118 229-240.
7. Di Fiore B & Pines J 2010 How cyclin A destruction escapes the spindle assembly checkpoint. Journal of Cell Biology 190 501-509. (doi:10.1083/jcb.201001083)
8. DoreeM& Hunt T 2002 From Cdc2 to Cdk1: when did the cell cycle kinase join its cyclin partner? Journal of Cell Science 115 2461-2464.
9. Dumont J & Desai A 2012 Acentrosomal spindle assembly and chromosome segregation during oocyte meiosis. Trends in Cell Biology 22 241-249. (doi:10.1016/j.tcb.2012.02.007)
10. Eichenlaub-Ritter U 2012 Oocyte ageing and its cellular basis. International Journal of Developmental Biology 56 841-852. (doi:10.1387/ijdb. 120141ue)
11. den Elzen N & Pines J 2001 Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. Journal of Cell Biology 153 121-136. (doi:10.1083/jcb.153.1.121)
12. Foley EA & Kapoor TM 2013 Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nature Reviews. Molecular Cell Biology 14 25-37. (doi:10.1038/nrm3494)
13. Fung TK, Ma HT & Poon RY 2007 Specialized roles of the two mitotic cyclins in somatic cells: cyclin A as an activator of M phase-promoting factor. Molecular Biology of the Cell 18 1861-1873. (doi:10.1091/mbc.E06-12-1092)
14. Gautier J, Minshull J, Lohka M, Glotzer M, Hunt T & Maller JL 1990 Cyclin is a component of maturation-promoting factor from Xenopus. Cell 60 487-494. (doi:10.1016/0092-8674(90)90599-A)
15. Geley S, Kramer E, Gieffers C, Gannon J, Peters JM & Hunt T 2001 APC/C-dependent proteolysis of human cyclin A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. Journal of Cell Biology 153 137-148. (doi:10.1083/jcb.153.1.137)
16. Gong D, Pomerening JR, Myers JW, Gustavsson C, Jones JT, Hahn AT, Meyer T & Ferrell JE 2007 Cyclin A2 regulates nuclear-envelope breakdown and the nuclear accumulation of cyclin B1. Current Biology 17 85-91. (doi:10.1016/j.cub.2006.11.066)
17. Gui L & Homer H 2012 Spindle assembly checkpoint signalling is uncoupled from chromosomal position in mouse oocytes. Development 139 1941-1946. (doi:10.1242/dev.078352)
18. Gui L & Homer H 2013 Hec1-dependent cyclin B2 stabilization regulates the G2-M transition and early prometaphase in mouse oocytes. Developmental Cell 25 43-54. (doi:10.1016/j.devcel.2013.02.008)
19. Hached K, Xie SZ, Buffin E, CladiFre D, Rachez C, Sacras M, Sorger PK & Wassmann K 2011 Mps1 at kinetochores is essential for female mouse meiosis I. Development 138 2261-2271. (doi:10.1242/dev.061317)
20. Hagting A, Karlsson C, Clute P, Jackman M & Pines J 1998 MPF localization is controlled by nuclear export. EMBO Journal 17 4127-4138. (doi:10.1093/emboj/17.14.4127)
21. Han SJ, Chen R, Paronetto MP & Conti M 2005 Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Current Biology 15 1670-1676. (doi:10.1016/j.cub.2005.07.056)
22. Herbert M, Levasseur M, Homer H, Yallop K, Murdoch A & McDougall A 2003 Homologue disjunction in mouse oocytes requires proteolysis of securin and cyclin B1. Nature Cell Biology 5 1023-1025. (doi:10.1038/ ncb1062)
23. Holt JE, Weaver J & Jones KT 2010 Spatial regulation of APCCdh1-induced cyclin B1 degradation maintains G2 arrest in mouse oocytes. Development 137 1297-1304. (doi:10.1242/dev.047555)
24. Holt JE, Tran SM, Stewart JL, Minahan K, Garcia-Higuera I, Moreno S & Jones KT 2011 The APC/C activator FZR1 coordinates the timing of meiotic resumption during prophase I arrest in mammalian oocytes. Development 138 905-913. (doi:10.1242/dev.059022)
25. Holt JE, Lane SI, Jennings P, Garcia-Higuera I, Moreno S & Jones KT 2012 APC(FZR1) prevents nondisjunction in mouse oocytes by controlling meiotic spindle assembly timing. Molecular Biology of the Cell 23 3970-3981. (doi:10.1091/mbc.E12-05-0352)
26. Homer H 2007 Ageing, aneuploidy and meiosis: eggs in a race against time. In The Yearbook of Obstetrics and Gynaecology, vol 12, pp 139-158. Ed T Hillard. London: RCOG Press.
27. Homer H 2011 New insights into the genetic regulation of homologue disjunction in mammalian oocytes. Cytogenetic and Genome Research 133 209-222. (doi:10.1159/000324118)
28. Homer H, McDougall A, Levasseur M & Herbert M 2005a Restaging the spindle assembly checkpoint in female mammalian meiosis I. Cell Cycle 4 650-653. (doi:10.4161/cc.4.5.1677)
29. Homer H, McDougall A, Levasseur M, Murdoch A & Herbert M 2005b Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction 130 829-843. (doi:10.1530/rep.1.00856)
30. Homer H, McDougall A, Levasseur M, Yallop K, Murdoch A & Herbert M 2005c Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes and Development 19 202-207. (doi:10.1101/gad.328105)
31. Homer H, Gui L & Carroll J 2009 A spindle assembly checkpoint protein functions in prophase I arrest and prometaphase progression. Science 326 991-994. (doi:10.1126/science.1175326)
32. Hwang LH, Lau LF, Smith DL, Mistrot CA, Hardwick KG, Hwang ES, Amon A & Murray AW 1998 Budding yeast Cdc20: a target of the spindle checkpoint. Science 279 1041-1044. (doi:10.1126/science.279.5353.1041)
33. Jin F, Hamada M, Malureanu L, Jeganathan KB, ZhouW, Morbeck DE & van Deursen JM 2010 Cdc20 is critical for meiosis I and fertility of female mice. PLoS Genetics 6 e1001147. (doi:10.1371/journal.pgen.1001147)
34. Kitajima TS, Ohsugi M & Ellenberg J 2011 Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 146 568-581. (doi:10.1016/j.cell.2011.07.031)
35. Kolano A, Brunet S, Silk AD, Cleveland DW & Verlhac MH 2012 Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. PNAS 109 E1858-E1867. (doi:10.1073/pnas.1204686109)
36. Kramer ER, Scheuringer N, Podtelejnikov AV, Mann M & Peters JM 2000 Mitotic regulation of the APC activator proteins CDC20 and CDH1. Molecular Biology of the Cell 11 1555-1569.
37. Labbe J-C, Capony JP, Caput D, Cavadore JC, Derancourt J, Kaghad M, Lelias JM, Picard A & Doree M 1989 MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO Journal 8 3053-3058.
38. LampsonM& Kapoor T 2005 The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nature Cell Biology 7 93-98. (doi:10.1038/ncb1208)
39. Lane SI, Yun Y & Jones KT 2012 Timing of anaphase-promoting complex activation in mouse oocytes is predicted by microtubule-kinetochore attachment but not by bivalent alignment or tension. Development 139 1947-1955. (doi:10.1242/dev.077040)
40. Ledan E, Polanski Z, Terret M-E & Maro B 2001 Meiotic maturation of the mouse oocyte requires an equilibrium between cyclin B synthesis and degradation. Developmental Biology 232 400-413. (doi:10.1006/dbio.2001.0188)
41. Leland S, Nagarajan P, Polyzos A, Thomas S, Samaan G, Donnell R, Marchetti F & Venkatachalam S 2009 Heterozygosity for a Bub1 mutation causes female-specific germ cell aneuploidy in mice. PNAS 106 12776-12781. (doi:10.1073/pnas.0903075106)
42. Li M, Li S, Yuan J, Wang ZB, Sun SC, Schatten H & Sun QY 2009 Bub3 is a spindle assembly checkpoint protein regulating chromosome segregation during mouse oocyte meiosis. PLoS ONE 4 e7701. (doi:10.1371/ journal.pone.0007701)
43. Li L, Zhou Y, Wang GF, Liao SC, Ke YB, Wu W, Li XH, Zhang RL & Fu YC 2011 Anaphase-promoting complex/cyclosome controls HEC1 stability. Cell Proliferation 44 1-9. (doi:10.1111/j.1365-2184.2010.00712.x)
44. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P & Wolgemuth DJ 1998 Cyclin A1 is required for meiosis in the male mouse. Nature Genetics 20 377-380. (doi:10.1038/3855)
45. Madgwick S, Hansen D, Levasseur M, Jackson P & Jones K 2006 Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. Journal of Cell Biology 174 791-801. (doi:10.1083/jcb.200604140)
46. Marangos P & Carroll J 2008 Securin regulates entry into M-phase by modulating the stability of cyclin B. Nature Cell Biology 10 445-451. (doi:10.1038/ncb1707)
47. Marangos P, Verschuren E, Chen R, Jackson P & Carroll J 2007 Prophase I arrest and progression to metaphase I in mouse oocytes are controlled by Emi1-dependent regulation of APCCdh1. Journal of Cell Biology 176 65-75. (doi:10.1083/jcb.200607070)
48. McGuinness BE, Anger M, Kouznetsova A, Gil-Bernabq AM, Helmhart W, Kudo NR, Wuensche A, Taylor S, Hoog C, Novak B et al. 2009 Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Current Biology 19 369-380. (doi:10.1016/j.cub.2009.01.064)
49. Miller JJ, Summers MK, Hansen DV, Nachury MV, Lehman NL, Loktev A & Jackson PK 2006 Emi1 stably binds and inhibits the anaphase-promoting complex/cyclosome as a pseudosubstrate inhibitor. Genes and Development 20 2410-2420. (doi:10.1101/gad.1454006)
50. Mondal G, Sengupta S, Panda CK, Gollin SM, Saunders WS & Roychoudhury S 2007 Overexpression of Cdc20 leads to impairment of the spindle assembly checkpoint and aneuploidization in oral cancer. Carcinogenesis 28 81-92. (doi:10.1093/carcin/bgl100)
51. MurphyM, Stinnakre MG, Senamaud-Beaufort C, Winston NJ, Sweeney C, Kubelka M, Carrington M, Brechot C & Sobczak-Thepot J 1997 Delayed early embryonic lethality following disruption of the murine cyclin A2 gene. Nature Genetics 15 83-86. (doi:10.1038/ng0197-83)
52. Nagaoka SI, Hodges CA, Albertini DF & Hunt PA 2011 Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Current Biology 21 651-657. (doi:10.1016/j.cub.2011.03.003)
53. Nagaoka SI, Hassold TJ & Hunt PA 2012 Human aneuploidy: mechanisms and new insights into an age-old problem. Nature Reviews. Genetics 13 493-504. (doi:10.1038/nrg3245)
54. Niault T, Hached K, Sotillo R, Sorger PK,Maro B, Benezra R &Wassmann K 2007 Changing Mad2 levels affects chromosome segregation and spindle assembly checkpoint control in female mouse meiosis I. PLoS ONE 2 e1165. (doi:10.1371/journal.pone.0001165)
55. Oh JS, Han SJ & Conti M 2010 Wee1B, Myt1, and Cdc25 function in distinct compartments of the mouse oocyte to control meiotic resumption. Journal of Cell Biology 188 199-207. (doi:10.1083/jcb.200907161)
56. Pines J 2011 Cubism and the cell cycle: the many faces of the APC/C. Nature Reviews. Molecular Cell Biology 12 427-438. (doi:10.1038/ nrm3132)
57. Pirino G, Wescott MP & Donovan PJ 2009 Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes. Cell Cycle 8 665-670. (doi:10.4161/cc.8.4.7846)
58. Polanski Z, Homer H & Kubiak JZ 2012 Cyclin B in mouse oocytes and embryos: importance for human reproduction and aneuploidy. Results and Problems in Cell Differentiation 55 69-91. (doi:10.1007/978-3-642- 30406-4-4)
59. Reis A, Chang H, Levasseur M & Jones K 2006 APCcdh1 activity in mouse oocytes prevents entry into the first meiotic division. Nature Cell Biology 8 539-540. (doi:10.1038/ncb1406)
60. Reis A, Madgwick S, Chang HY, Nabti I, Levasseur M & Jones KT 2007 Prometaphase APCcdh1 activity prevents non-disjunction in mammalian oocytes. Nature Cell Biology 9 1192-1198. (doi:10.1038/ ncb1640)
61. Satyanarayana A & Kaldis P 2009 Mammalian cell-cycle regulation: several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 28 2925-2939. (doi:10.1038/onc.2009.170)
62. Schindler K & Schultz RM 2009a The CDC14A phosphatase regulates oocyte maturation in mouse. Cell Cycle 8 1090-1098. (doi:10.4161/ cc.8.7.8144)
63. Schindler K & Schultz RM 2009b CDC14B acts through FZR1 (CDH1) to prevent meiotic maturation of mouse oocytes. Biology of Reproduction 80 795-803. (doi:10.1095/biolreprod.108.074906)
64. Schuh M & Ellenberg J 2007 Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130 484-498. (doi:10.1016/j.cell4.2007.06.025)
65. Solc P, Schultz RM & Motlik J 2010 Prophase I arrest and progression to metaphase I in mouse oocytes: comparison of resumption of meiosis and recovery from G2-arrest in somatic cells. Molecular Human Reproduction 16 654-664. (doi:10.1093/molehr/gaq034)
66. Sun SC & Kim NH 2012 Spindle assembly checkpoint and its regulators in meiosis. Human Reproduction Update 18 60-72. (doi:10.1093/humupd/ dmr044)
67. Tooley J & Stukenberg PT 2011 The Ndc80 complex: integrating the kinetochore's many movements. Chromosome Research 19 377-391. (doi:10.1007/s10577-010-9180-5)
68. Touati SA, Cladiere D, Lister LM, Leontiou I, Chambon JP, Rattani A, Bottger F, Stemmann O, Nasmyth K, Herbert M et al. 2012 Cyclin A2 is required for sister chromatid segregation, but not separase control, in mouse oocyte meiosis. Cell Reports 2 1077-1087. (doi:10.1016/j.celrep.2012.10.002)
69. Wassmann K, Niault T & Maro B 2003 Metaphase I arrest upon activation of the MAD2-dependent spindle checkpoint in mouse oocytes. Current Biology 13 1596-1608. (doi:10.1016/j.cub.2003.08.052)
70. Wei L, Liang XW, Zhang QH, Li M, Yuan J, Li S, Sun SC, Ouyang YC, Schatten H & Sun QY 2010 BubR1 is a spindle assembly checkpoint protein regulating meiotic cell cycle progression of mouse oocyte. Cell Cycle 9 1112-1121. (doi:10.4161/cc.9.6.10957)
71. Wolthuis R, Clay-Farrace L, van Zon W, Yekezare M, Koop L, Ogink J, Medema R & Pines J 2008 Cdc20 and Cks direct the spindle checkpointindependent destruction of cyclin A. Molecular Cell 30 290-302. (doi:10.1016/j.molcel.2008.02.027)
72. Yin S, Wang Q, Liu JH, Ai JS, Liang CG, Hou Y, Chen DY, Schatten H & Sun QY 2006 Bub1 prevents chromosome misalignment and precocious anaphase during mouse oocyte meiosis. Cell Cycle 5 2130-2137. (doi:10.4161/cc.5.18.3170)