Phosphorylation of ARPP19 by protein kinase A prevents meiosis resumption in Xenopus oocytes

Nature Communications

Volumn 5, Issue , 2014, Pages

  Dupré, Aude ^a,b   Daldello, Enrico M ^a,b   Nairn, Angus C ^c   Jessus, Catherine ^a,b   Haccard, Olivier ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP-REGULATED PHOSPHOPROTEIN 19; PHOSPHOPROTEIN;

ANIMAL; MEIOSIS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; XENOPUS;

ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; MEIOSIS; PHOSPHOPROTEINS; PHOSPHORYLATION; XENOPUS;

EID: 84894046705     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4318     Document Type: Article

References (62)

1. Taylor, S. S., Ilouz, R., Zhang, P. & Kornev, A. P. Assembly of allosteric macromolecular switches: Lessons from PKA. Nat. Rev. Mol. Cell. Biol. 13, 646-658 (2012
2. Grieco, D., Avvedimento, E. V. & Gottesman, M. E. A role for cAMPdependent protein kinase in early embryonic divisions. Proc. Natl Acad. Sci. USA 91, 9896-9900 (1994 (Pubitemid 24311915)
3. Grieco, D., Porcellini, A., Avvedimento, E. V. & Gottesman, M. E. Requirement for cAMP-PKA pathway activation by M phase-promoting factor in the transition from mitosis to interphase. Science 271, 1718-1723 (1996 (Pubitemid 26102818)
4. Fernandez, A., Cavadore, J. C., Demaille, J. & Lamb, N. Implications for cAMPdependent protein kinase in the maintenance of the interphase state. Prog. Cell. Cycle Res. 1, 241-253 (1995
5. Jaffe, L. A. & Norris, R. P. Initiation of the meiotic prophase-To-metaphase transition in mammalian oocytes. In: Oogenesis (eds Verlhac, M. H.& Villeneuve, A.) (John Wiley & Sons, Ltd, 2010
6. Karaiskou, A., Dupre, A., Haccard, O. & Jessus, C. From progesterone to active Cdc2 in Xenopus oocytes: A puzzling signalling pathway. Biol. Cell 93, 35-46 (2001 (Pubitemid 33040858)
7. Ozon, R., Belle, R., Huchon, D. & Mulner, O. Roles of cyclic AMP and calcium in maturation of Xenopus laevis oocytes. J. Steroid. Biochem. 11, 709-713 (1979 (Pubitemid 9249084)
8. Smith, L. D. The induction of oocyte maturation: Transmembrane signaling events and regulation of the cell cycle. Development 107, 685-699 (1989 (Pubitemid 20017218)
9. Wang, J. & Liu, X. J. Progesterone inhibits protein kinase A (PKA) in Xenopus oocytes: Demonstration of endogenous PKA activities using an expressed substrate. J. Cell. Sci. 117, 5107-5116 (2004 (Pubitemid 39517526)
10. Maller, J. L., Butcher, F. R. & Krebs, E. G. Early effect of progesterone on levels of cyclic adenosine 3:5-monophosphate in Xenopus oocytes. J. Biol. Chem. 254, 579-582 (1979 (Pubitemid 9145921)
11. Conti, M. et al. Role of cyclic nucleotide signaling in oocyte maturation. Mol. Cell Endocrinol. 187, 153-159 (2002 (Pubitemid 34436944)
12. Masciarelli, S. et al. Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J. Clin. Invest. 114, 196-205 (2004 (Pubitemid 39071624)
13. Maller, J. L. & Krebs, E. G. Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3:5-monophosphate-dependent protein kinase. J. Biol. Chem. 252, 1712-1718 (1977 (Pubitemid 8062370)
14. Huchon, D., Ozon, R., Fischer, E. H. & Demaille, J. G. The pure inhibitor of cAMP-dependent protein kinase initiates Xenopus laevis meiotic maturation. A 4-step scheme for meiotic maturation. Mol. Cell Endocrinol. 22, 211-222 (1981 (Pubitemid 11109007)
15. Rime, H., Haccard, O. & Ozon, R. Activation of P34cdc2 kinase by cyclin is negatively regulated by cyclic amp-dependent protein-kinase in xenopusoocytes. Dev. Biol. 151, 105-110 (1992
16. Daar, I., Yew, N. & Vande Woude, G. F. Inhibition of mos-induced oocyte maturation by protein kinase A. J. Cell Biol. 120, 1197-1202 (1993 (Pubitemid 23064174)
17. Duckworth, B. C., Weaver, J. S. & Ruderman, J. V. G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. Proc. Natl Acad. Sci. USA 99, 16794-16799 (2002 (Pubitemid 36034052)
18. Wang, R. et al. Direct roles of the signaling kinase RSK2 in Cdc25C activation during Xenopus oocyte maturation. Proc. Natl Acad. Sci. USA 107, 19885-19890 (2010
19. Palmer, A., Gavin, A. C. & Nebreda, A. R. A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: P90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase myt1. EMBO J. 17, 5037-5047 (1998 (Pubitemid 28408469)
20. Haccard, O. & Jessus, C. Redundant pathways for Cdc2 activation in Xenopus oocyte: Either cyclin B or Mos synthesis. EMBO Rep. 7, 321-325 (2006
21. Dupre, A., Jessus, C., Ozon, R. & Haccard, O. Mos is not required for the initiation of meiotic maturation in Xenopus oocytes. EMBO J. 21, 4026-4036 (2002 (Pubitemid 34857435)
22. Inoue, D. & Sagata, N. The polo-like kinase Plx1 interacts with and inhibits Myt1 after fertilization of Xenopus eggs. EMBO J. 24, 1057-1067 (2005 (Pubitemid 40470153)
23. Frank-Vaillant, M., Jessus, C., Ozon, R., Maller, J. L. & Haccard, O. Two distinct mechanisms control the accumulation of cyclin B1 and Mos in Xenopus oocytes in response to progesterone. Mol. Biol. Cell 10, 3279-3288 (1999 (Pubitemid 29489561)
24. Gaffre, M. et al. A critical balance between cyclin B synthesis and Myt1 activity controls meiosis entry in Xenopus oocytes. Development 138, 3735-3744 (2011
25. Haccard, O. & Jessus, C. Oocyte maturation, Mos and cyclins-A matter of synthesis: Two functionally redundant ways to induce meiotic maturation. Cell Cycle 5, 1152-1159 (2006
26. Abrieu, A. et al. The polo-like kinase Plx1 is a component of the MPF amplification loop at the G2/M-phase transition of the cell cycle in Xenopus eggs. J. Cell Sci. 111, 1751-1757 (1998 (Pubitemid 28330561)
27. Karaiskou, A., Jessus, C., Brassac, T. & Ozon, R. Phosphatase 2A and polo kinase, two antagonistic regulators of cdc25 activation and MPF autoamplification. J. Cell Sci. 112(Pt 21): 3747-3756 (1999
28. Haccard, O., Lewellyn, A., Hartley, R. S., Erikson, E. & Maller, J. L. Induction of Xenopus oocyte meiotic maturation by MAP kinase. Dev. Biol. 168, 677-682 (1995
29. Peter, M., Labbe, J. C., Doree, M. & Mandart, E. A new role for Mos in Xenopus oocyte maturation: Targeting Myt1 independently of MAPK. Development 129, 2129-2139 (2002 (Pubitemid 34874227)
30. Sagata, N., Daar, I., Oskarsson, M., Showalter, S. D. & Vandewoude, G. F. The product of the Mos proto-oncogene as a candidate initiator for oocyte maturation. Science 245, 643-646 (1989 (Pubitemid 19213342)
31. Hara, M. et al. Greatwall kinase and cyclin B-Cdk1 are both critical constituents of M-phase-promoting factor. Nat. Commun. 3, 1059 (2012
32. Dupre, A., Buffin, E., Roustan, C., Nairn, A. C., Jessus, C. & Haccard, O. The phosphorylation of ARPP19 by Greatwall renders the auto-Amplification of MPF independently of PKA in Xenopus oocytes. J. Cell Sci. 126, 3916-3926 (2013
33. Zhao, Y. et al. Roles of Greatwall kinase in the regulation of cdc25 phosphatase. Mol. Biol. Cell 19, 1317-1327 (2008 (Pubitemid 351805087)
34. Li, Y. H. et al. Greatwall kinase is required for meiotic maturation in porcine oocytes. Biol. Reprod. 89, 53 (2013
35. Dulubova, I. et al. ARPP-16/ARPP-19: A highly conserved family of cAMPregulated phosphoproteins. J. Neurochem. 77, 229-238 (2001 (Pubitemid 32245097)
36. Gharbi-Ayachi, A et al. The substrate of Greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. Science 330, 1673-1677 (2010
37. Juanes, M. A. et al. Budding yeast greatwall and endosulfines control activity and spatial regulation of PP2A(Cdc55) for timely mitotic progression. PLoS Genet. 9, e1003575 (2013
38. Mochida, S., Maslen, S. L., Skehel, M. & Hunt, T. Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. Science 330, 1670-1673 (2010
39. Masui, Y. & Markert, C. L. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 177, 129-145 (1971
40. Eyers, P. A. et al. Regulation of the G(2)/M transition in Xenopus oocytes by the cAMP-dependent protein kinase. J. Biol. Chem. 280, 24339-24346 (2005 (Pubitemid 40934516)
41. Horiuchi, A., Williams, K. R., Kurihara, T., Nairn, A. C. & Greengard, P. Purification and cDNA cloning of ARPP-16, a cAMP-regulated phosphoprotein enriched in basal ganglia, and of a related phosphoprotein, ARPP-19. J. Biol. Chem. 265, 9476-9484 (1990
42. Boyer, J., Asselin, J., Belle, R. & Ozon, R. Progesterone and cAMP-dependent protein kinase regulate in vivo the level of phosphorylation of two proteins (Mr 20,000 and Mr 32,000) in Xenopus oocytes. Dev. Biol. 113, 420-428 (1986 (Pubitemid 16074692)
43. Wasserman, W. J. & Masui, Y. Effects of cycloheximide on a cytoplasmic factor initiating meiotic maturation in xenopus oocytes. Exp. Cell Res. 91, 381-388 (1975
44. Matten, W. & Daar, I. Woude GFV. Protein-kinase a acts at multiple points to inhibit xenopus-oocyte maturation. Mol. Cell Biol. 14, 4419-4426 (1994 (Pubitemid 24196790)
45. Rime, H. et al. Microinjection of Cdc25 protein phosphatase into xenopus prophase oocyte activates MPF and arrests meiosis at metaphase-I. Biol. Cell 82, 11-22 (1994
46. Mulner, O., Huchon, D., Thibier, C. & Ozon, R. Cyclic AMP synthesis in Xenopus laevis oocytes: Inhibition by progesterone. Biochim. Biophys. Acta. 582, 179-184 (1979 (Pubitemid 9065597)
47. Huchon, D. & Ozon, R. Effects of 3-isobutyl-methylxanthine (IBMX) and of cholera toxin on maturation induced by the injection of maturation promoting factor (MPF) in oocyte of Xenopus laevis. Biol. Cell 35, 15-20 (1979 (Pubitemid 10229498)
48. Goris, J., Hermann, J., Hendrix, P., Ozon, R. & Merlevede, W. Okadaic acid, a specific protein phosphatase inhibitor, induces maturation and MPF formation in Xenopus laevis oocytes. FEBS Lett. 245, 91-94 (1989 (Pubitemid 19076209)
49. Rime, H. et al. Characterization of MPF activation by okadaic acid in Xenopus oocyte. Cell Differ. Dev. 29, 47-58 (1990 (Pubitemid 20048280)
50. Han, S. J., Chen, R., Paronetto, M. P. & Conti, M. Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr. Biol. 15, 1670-1676 (2005 (Pubitemid 41323746)
51. Nakajo, N. et al. Absence of Wee1 ensures the meiotic cell cycle in Xenopus oocytes. Genes Dev. 14, 328-338 (2000 (Pubitemid 30106487)
52. Morgan, D. O. Principles of CDK regulation. Nature 374, 131-134 (1995
53. Bontron, Set al. Yeast endosulfines control entry into quiescence and chronological life span by inhibiting protein phosphatase 2A. Cell Rep. 3, 16-22 (2013
54. Talarek, N. et al. Initiation of the TORC1-regulated G0 program requires Igo1/2, which license specific mRNAs to evade degradation via the 50-30 mRNA decay pathway. Mol. Cell 38, 345-355 (2010
55. Sheppard, J. R. & Prescott, D. M. Cyclic AMP levels in synchronized mammalian cells. Exp. Cell Res. 75, 293-296 (1972
56. Kurokawa, K. & Kato, J. Cyclic AMP delays G2 progression and prevents efficient accumulation of cyclin B1 proteins in mouse macrophage cells. Cell Struct. Funct. 23, 357-365 (1998 (Pubitemid 29084157)
57. Stambrook, P. J. & Velez, C. Reversible arrest of Chinese hamster V79 cells in G2 by dibutytyl AMP. Exp. Cell Res. 99, 57-62 (1976
58. Laemmli, UK. Cleavage of structural proteins during theassembly of the head of bacteriophage T4. Nature 227, 680-685 (1970
59. Schagger, H. Tricine-SDS-PAGE. Nat. Protoc. 1, 16-22 (2006
60. Studier, F. W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207-234 (2005
61. Thomas, J. et al. Expression in Escherichia coli and characterization of the heatstable inhibitor of the cAMP-dependent protein kinase. J. Biol. Chem. 266, 10906-10911 (1991 (Pubitemid 21906890)
62. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976