Prophase I arrest and progression to metaphase I in mouse oocytes are controlled by Emi1-dependent regulation of APCCdh1

Journal of Cell Biology

Volumn 176, Issue 1, 2007, Pages 65-75

  Marangos, Petros ^a   Verschuren, Emmy W ^b   Chen, Ruby ^c   Jackson, Peter K ^b   Carroll, John ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b School of Medicine

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CYCLIN B; MATURATION PROMOTING FACTOR; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL DIVISION; CONTROLLED STUDY; GERMINAL VESICLE; MEIOSIS; METAPHASE; MITOSIS INHIBITION; MITOSIS SPINDLE; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROPHASE;

3T3 CELLS; ANIMALS; CELL CYCLE PROTEINS; CYCLIN B; EMBRYO; F-BOX PROTEINS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MEIOSIS; MEIOTIC PROPHASE I; METAPHASE; MICE; MITOTIC SPINDLE APPARATUS; OOCYTES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; RNA, MESSENGER; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

MAMMALIA;

EID: 33845994023     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200607070     Document Type: Article

References (57)

1. Brunet, S., and B. Maro. 2005. Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction. 130:801-811.
2. Chang, H.Y., M. Levasseur, and K.T. Jones. 2004. Degradation of APCcdc20 and APCcdh1 substrates during the second meiotic division in mouse eggs. J. Cell Sci. 117:6289-6296.
3. Choi, T., F. Aoki, M. Mori, M. Yamashita, Y. Nagahama, and K. Kohmoto. 1991. Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development. 113:789-795.
4. Cleveland, D.W., Y. Mao, and K.F. Sullivan. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell. 112:407-421.
5. Davis, M., A. Hatzubai, J.S. Andersen, E. Ben-Shushan, G.Z. Fisher, A. Yaron, A. Bauskin, F. Mercurio, M. Mann, and Y. Ben-Neriah. 2002. Pseudosubstrate regulation of the SCF(beta-TrCP) ubiquitin ligase by hnRNP-U. Genes Dev. 16:439-451.
6. Draetta, G., F. Luca, J. Westendorf, L. Brizuela, J. Ruderman, and D. Beach. 1989. Cdc2 protein kinase is complexed with both cyclin A and B: evidence for proteolytic inactivation of MPF. Cell. 56:829-838.
7. Fang, G. 2002. Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol. Biol. Cell. 13:755-766.
8. Fang, G., H. Yu, and M.W. Kirschner. 1998. 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.
9. Fang, G., H. Yu, and M.W. Kirschner. 1999. Control of mitotic transitions by the anaphase-promoting complex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354:1583-1590.
10. Felix, M.A., J.C. Labbe, M. Doree, T. Hunt, and E. Karsenti. 1990. Triggering of cyclin degradation in interphase extracts of amphibian eggs by cdc2 kinase. Nature. 346:379-382.
11. Gautier, J., J. Minshull, M. Lohka, M. Glotzer, T. Hunt, and J.L. Maller. 1990. Cyclin is a component of maturation-promoting factor from Xenopus. Cell. 60:487-494.
12. Glotzer, M., A.W. Murray, and M.W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature. 349:132-138.
13. Golan, A., Y. Yudkovsky, and A. Hershko. 2002. The cyclin-ubiquitin ligase activity of cyclosome/APC is jointly activated by protein kinases Cdk1-cyclin B and Plk. J. Biol. Chem. 277:15552-15557.
14. Grosskortenhaus, R., and F. Sprenger. 2002. Rca1 inhibits APC-Cdh1(Fzr) and is required to prevent cyclin degradation in G2. Dev. Cell. 2:29-40.
15. Guardavaccaro, D., Y. Kudo, J. Boulaire, M. Barchi, L. Busino, M. Donzelli, F. Margottin-Goguet, P.K. Jackson, L. Yamasaki, and M. Pagano. 2003. Control of meiotic and mitotic progression by the F box protein beta-Trcp1 in vivo. Dev. Cell. 4:799-812.
16. Hansen, D.V., A.V. Loktev, K.H. Ban, and P.K. Jackson. 2004. Plk1 regulates activation of the anaphase promoting complex by phosphorylating and triggering SCFbetaTrCP-dependent destruction of the APC inhibitor Emi1. Mol. Biol. Cell. 15:5623-5634.
17. Hansen, D.V., J.J. Tung, and P.K. Jackson. 2006. CaMKII and polo-like kinase 1 sequentially phosphorylate the cytostatic factor Emi2/XErp1 to trigger its destruction and meiotic exit. Proc. Natl. Acad. Sci. USA. 103:608-613.
18. Hashimoto, N., and T. Kishimoto. 1986. Cell cycle dynamics of maturation-promoting factor during mouse oocyte maturation. Tokai J. Exp. Clin. Med. 11:471-477.
19. 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.
20. Homer, H.A., A. McDougall, M. Levasseur, K. Yallop, A.P. Murdoch, and M. Herbert. 2005. Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes Dev. 19:202-207.
21. Hsu, J.Y., J.D. Reimann, C.S. Sorensen, J. Lukas, and P.K. Jackson. 2002. E2F-dependent accumulation of hEmi1 regulates S phase entry by inhibiting APC(Cdh1). Nat. Cell Biol. 4:358-366.
22. King, R.W., R.J. Deshaies, J.M. Peters, and M.W. Kirschner. 1996. How proteolysis drives the cell cycle. Science. 274:1652-1659.
23. Kramer, E.R., C. Gieffers, G. Holzl, M. Hengstschlager, and J.M. Peters. 1998. Activation of the human anaphase-promoting complex by proteins of the CDC20/Fizzy family. Curr. Biol. 8:1207-1210.
24. Kubiak, J.Z., M. Weber, H. de Pennart, N.J. Winston, and B. Maro. 1993. The metaphase II arrest in mouse oocytes is controlled through microtubule-dependent destruction of cyclin B in the presence of CSF. EMBO J. 12:3773-3778.
25. Labbe, J.C., J.P. Capony, D. Caput, J.C. Cavadore, J. Derancourt, M. Kaghad, J.M. Lelias, A. Picard, and M. Doree. 1989. MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO J. 8:3053-3058.
26. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
27. Lawitts, J.A., and J.D. Biggers. 1993. Culture of preimplantation embryos. Methods Enzymol. 225:153-164.
28. 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.
29. Li, X., and R.B. Nicklas. 1995. Mitotic forces control a cell-cycle checkpoint. Nature. 373:630-632.
30. Liu, J., and J.L. Maller. 2005. Calcium elevation at fertilization coordinates phosphorylation of XErp1/Emi2 by Plx1 and CaMK II to release metaphase arrest by cytostatic factor. Curr. Biol. 15:1458-1468.
31. Lorca, T., A. Castro, A.M. Martinez, S. Vigneron, N. Morin, S. Sigrist, C. Lehner, M. Doree, and J.C. Labbe. 1998. Fizzy is required for activation of the APC/cyclosome in Xenopus egg extracts. EMBO J. 17:3565-3575.
32. Madgwick, S., D.V. Hansen, M. Levasseur, P.K. Jackson, and K.T. Jones. 2006. Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J. Cell Biol. 174:791-801.
33. Marangos, P., and J. Carroll. 2004a. Fertilization and InsP3-induced Ca2+ release stimulate a persistent increase in the rate of degradation of cyclin B1 specifically in mature mouse oocytes. Dev. Biol. 272:26-38.
34. Marangos, P., and J. Carroll. 2004b. The dynamics of cyclin B1 distribution during meiosis I in mouse oocytes. Reproduction. 128:153-162.
35. Marangos, P., G. Fitzharris, and J. Carroll. 2003. Ca2+ oscillations at fertilization in mammals are regulated by the formation of pronuclei. Development. 130:1461-1472.
36. Margottin-Goguet, F., J.Y. Hsu, A. Loktev, H.M. Hsieh, J.D. Reimann, and P.K. Jackson. 2003. Prophase destruction of Emi1 by the SCF(betaTrCP/Slimb) ubiquitin ligase activates the anaphase promoting complex to allow progression beyond prometaphase. Dev. Cell. 4:813-826.
37. Masui, Y., and C.L. Markert. 1971. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 177:129-145.
38. Moshe, Y., J. Boulaire, M. Pagano, and A. Hershko. 2004. Role of Polo-like kinase in the degradation of early mitotic inhibitor 1, a regulator of the anaphase promoting complex/cyclosome. Proc. Natl. Acad. Sci. USA. 101:7937-7942.
39. Ohsumi, K., A. Koyanagi, T.M. Yamamoto, T. Gotoh, and T. Kishimoto. 2004. Emi1-mediated M-phase arrest in Xenopus eggs is distinct from cytostatic factor arrest. Proc. Natl. Acad. Sci. USA. 101:12531-12536.
40. Paronetto, M.P., E. Giorda, R. Carsetti, P. Rossi, R. Geremia, and C. Sette. 2004. Functional interaction between p90Rsk2 and Emi1 contributes to the metaphase arrest of mouse oocytes. EMBO J. 23:4649-4659.
41. Peter, M., A. Castro, T. Lorca, C. Le Peuch, L. Magnaghi-Jaulin, M. Doree, and J.C. Labbe. 2001. The APC is dispensable for first meiotic anaphase in Xenopus oocytes. Nat. Cell Biol. 3:83-87.
42. Peters, J.M. 2002. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell. 9:931-943.
43. 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.
44. Raff, J.W., K. Jeffers, and J.Y. Huang. 2002. The roles of Fzy/Cdc20 and Fzr/Cdh1 in regulating the destruction of cyclin B in space and time. J. Cell Biol. 157:1139-1149.
45. Rauh, N.R., A. Schmidt, J. Bormann, E.A. Nigg, and T.U. Mayer. 2005. Calcium triggers exit from meiosis II by targeting the APC/C inhibitor XErp1 for degradation. Nature. 437:1048-1052.
46. Reimann, J.D., and P.K. Jackson. 2002. Emi1 is required for cytostatic factor arrest in vertebrate eggs. Nature. 416:850-854.
47. Reimann, J.D., E. Freed, J.Y. Hsu, E.R. Kramer, J.M. Peters, and P.K. Jackson. 2001a. Emi1 is a mitotic regulator that interacts with Cdc20 and inhibits the anaphase promoting complex. Cell. 105:645-655.
48. Reimann, J.D., B.E. Gardner, F. Margottin-Goguet, and P.K. Jackson. 2001b. Emi1 regulates the anaphase-promoting complex by a different mechanism than Mad2 proteins. Genes Dev. 15:3278-3285.
49. Reis, A., H.Y. Chang, M. Levasseur, and K.T. Jones. 2006. APCcdh1 activity in mouse oocytes prevents entry into the first meiotic division. Nat. Cell Biol. 8:539-540.
50. Shoji, S., N. Yoshida, M. Amanai, M. Ohgishi, T. Fukui, S. Fujimoto, Y. Nakano, E. Kajikawa, and A.C. Perry. 2006. Mammalian Emi2 mediates cytostatic arrest and transduces the signal for meiotic exit via Cdc20. EMBO J. 25:834-845.
51. Tay, J., R. Hodgman, and J.D. Richter. 2000. The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev. Biol. 221:1-9.
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.
53. Tung, J.J., and P.K. Jackson. 2005. Emi1 class of proteins regulate entry into meiosis and the meiosis I to meiosis II transition in Xenopus oocytes. Cell Cycle. 4:478-482.
54. 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.
55. Tunquist, B.J., and J.L. Maller. 2003. Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev. 17:683-710.
56. Wassmann, K., T. Niault, and B. Maro. 2003. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr. Biol. 13:1596-1608.
57. Zachariae, W., and K. Nasmyth. 1999. Whose end is destruction: cell division and the anaphase-promoting complex. Genes Dev. 13:2039-2058.