Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation

EMBO Journal

Volumn 25, Issue 24, 2006, Pages 5716-5725

  Han, Seung Jin ^a   Vaccari, Sergio ^a   Nedachi, Taku ^b   Andersen, Carsten B ^c   Kovacina, Kristina S ^a   Roth, Richard A ^a   Conti, Marco ^a  

^a STANFORD UNIVERSITY   (United States)

^b TOHOKU UNIVERSITY   (Japan)

^c GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

Author keywords

Oocyte maturation; PDE3A; Phosphorylation; PKB Akt

Indexed keywords

ALANINE; CYCLIC AMP; INSULIN; MESSENGER RNA; PHOSPHODIESTERASE 3A; PHOSPHODIESTERASE III; PROTEIN KINASE B; PROTEIN SUBUNIT; SERINE;

ANIMAL CELL; ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FEMALE; MAMMAL CELL; MEIOSIS; MICROINJECTION; MOUSE; NONHUMAN; OOCYTE; OOCYTE MATURATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; XENOPUS;

3',5'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASE; AMINO ACID SEQUENCE; ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; FEMALE; HUMANS; INSULIN; ISOENZYMES; MATURATION-PROMOTING FACTOR; MICE; MOLECULAR SEQUENCE DATA; OOCYTES; OOGENESIS; PHENOTYPE; PHOSPHORYLATION; PHOSPHOSERINE; PROTO-ONCOGENE PROTEINS C-AKT; XENOPUS;

MAMMALIA;

EID: 33845708060     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601431     Document Type: Article

References (51)

1. Alliston TN, Gonzalez-Robayna IJ, Buse P, Firestone GL, Richards JS (2000) Expression and localization of serum/glucocorticoid-induced kinase in the rat ovary: relation to follicular growth and differentiation. Endocrinology 141: 385-395
2. Andersen CB, Roth RA, Conti M (1998) Protein kinase B/Akt induces resumption of meiosis in Xenopus oocytes. J Biol Chem 273: 18705-18708
3. Andersen CB, Sakaue H, Nedachi T, Kovacina KS, Clayberger C, Conti M, Roth RA (2003) Protein kinase B/Akt is essential for the insulin- but not progesterone-stimulated resumption of meiosis in Xenopus oocytes. Biochem J 369: 227-238
4. Conti M, Andersen CB, Richard F, Mehats C, Chun SY, Horner K, Jin C, Tsafriri A (2002) Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol 187: 153-159
5. Conti M, Andersen CB, Richard FJ, Shitsukawa K, Tsafriri A (1998) Role of cyclic nucleotide phosphodiesterases in resumption of meiosis. Mol Cell Endocrinol 145: 9-14
6. Conti M, Hsieh M, Park JY, Su YQ (2005) Role of the EGF network in ovarian follicles. Mol Endocrinol 20: 715-723
7. Deuter-Reinhard M, Apell G, Pot D, Klippel A, Williams LT, Kavanaugh WM (1997) SIP/SHIP inhibits Xenopus oocyte maturation induced by insulin and phosphatidylinositol 3-kinase. Mol Cell Biol 17: 2559-2565
8. Downward J (2004) PI 3-kinase, Akt and cell survival. Semin Cell Dev Biol 15: 177-182
9. El-Etr M, Schorderet-Slatkine S, Baulieu EE (1979) Meiotic maturation in Xenopus laevis oocytes initiated by insulin. Science 205: 1397-1399
10. Goud PT, Goud AP, Qian C, Laverge H, Van der Elst J, De Sutter P, Dhont M (1998) In-vitro maturation of human germinal vesicle stage oocytes: role of cumulus cells and epidermal growth factor in the culture medium. Hum Reprod 13: 1638-1644
11. Grant PG, Mannarino AF, Colman RW (1988) cAMP-mediated phosphorylation of the low-Km cAMP phosphodiesterase markedly stimulates its catalytic activity. Proc Natl Acad Sci USA 85: 9071-9075
12. 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. Curr Biol 15: 1670-1676
13. Hoshino Y, Yokoo M, Yoshida N, Sasada H, Matsumoto H, Sato E (2004) Phosphatidylinositol 3-kinase and Akt participate in the FSH-induced meiotic maturation of mouse oocytes. Mol Reprod Dev 69: 77-86
14. Kalous J, Solc P, Baran V, Kubelka M, Schultz RM, Motlik J (2006) PKB/AKT is involved in resumption of meiosis in mouse oocytes. Biol Cell 98: 111-123
15. Kenan Y, Murata T, Shakur Y, Degerman E, Manganiello VC (2000) Functions of the N-terminal region of cyclic nucleotide phosphodiesterase 3 (PDE 3) isoforms. J Biol Chem 275: 12331-12338
16. Kim S, Jee K, Kim D, Koh H, Chung J (2001) Cyclic AMP inhibits Akt activity by blocking the membrane localization of PDK1. J Biol Chem 276: 12864-12870
17. Kitamura T, Kitamura Y, Kuroda S, Hino Y, Ando M, Kotani K, Konishi H, Matsuzaki H, Kikkawa U, Ogawa W, Kasuga M (1999) Insulin-induced phosphorylation and activation of cyclic nucleotide phosphodiesterase 3B by the serine-threonine kinase Akt. Mol Cell Biol 19: 6286-6296
18. Kohn AD, Takeuchi F, Roth RA (1996) Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation. J Biol Chem 271: 21920-21926
19. Liu H, Maurice DH (1998) Expression of cyclic GMP-inhibited phosphodiesterases 3A and 3B (PDE3A and PDE3B) in rat tissues: differential subcellular localization and regulated expression by cyclic AMP. Br J Pharmacol 125: 1501-1510
20. Liu XJ, Sorisky A, Zhu L, Pawson T (1995) Molecular cloning of an amphibian insulin receptor substrate 1-like cDNA and involvement of phosphatidylinositol 3-kinase in insulin-induced Xenopus oocyte maturation. Mol Cell Biol 15: 3563-3570
21. Macphee CH, Reifsnyder DH, Moore TA, Lerea KM, Beavo JA (1988) Phosphorylation results in activation of a cAMP phosphodiesterase in human platelets. J Biol Chem 263: 10353-10358
22. Maller JL, Koontz JW (1981) A study of the induction of cell division in amphibian oocytes by insulin. Dev Biol 85: 309-316
23. Maller JL, Krebs EG (1977) 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
24. Masciarelli S, Horner K, Liu C, Park SH, Hinckley M, Hockman S, Nedachi T, Jin C, Conti M, Manganiello V (2004) Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest 114: 196-205
25. Meijer L, Dostmann W, Genieser HG, Butt E, Jastorff B (1989) Starfish oocyte maturation: evidence for a cyclic AMP-dependent inhibitory pathway. Dev Biol 133: 58-66
26. Movsesian MA (2002) PDE3 cyclic nucleotide phosphodiesterases and the compartmentation of cyclic nucleotide-mediated signalling in cardiac myocytes. Basic Res Cardiol 97 (Suppl 1): I83-I90
27. Murray JT, Cummings LA, Bloomberg GB, Cohen P (2005) Identification of different specificity requirements between SGK1 and PKBalpha. FEBS Lett 579: 991-994
28. Murthy KS, Zhou H, Makhlouf GM (2002) PKA-dependent activation of PDE3A and PDE4 and inhibition of adenylyl cyclase V/VI in smooth muscle. Am J Physiol Cell Physiol 282: C508-C517
29. Newhall KJ, Criniti AR, Cheah CS, Smith KC, Kafer KE, Burkart AD, McKnight GS (2006) Dynamic anchoring of PKA is essential during oocyte maturation. Curr Biol 16: 321-327
30. Oki N, Takahashi SI, Hidaka H, Conti M (2000) Short term feedback regulation of cAMP in FRTL-5 thyroid cells. Role of PDE4D3 phosphodiesterase activation. J Biol Chem 275: 10831-10837
31. Okumura E, Fukuhara T, Yoshida H, Hanada Si S, Kozutsumi R, Mori M, Tachibana K, Kishimoto T (2002) Akt inhibits Myt1 in the signalling pathway that leads to meiotic G2/M-phase transition. Nat Cell Biol 4: 111-116
32. Onuma H, Osawa H, Yamada K, Ogura T, Tanabe F, Granner DK, Makino H (2002) Identification of the insulin-regulated interaction of phosphodiesterase 3B with 14-3-3 beta protein. Diabetes 51: 3362-3367
33. Park J, Leong ML, Buse P, Maiyar AC, Firestone GL, Hemmings BA (1999) Serum and glucocorticoid-inducible kinase (SGK) is a target of the PI 3-kinase-stimulated signaling pathway. EMBO J 18: 3024-3033
34. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M (2004) EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303: 682-684
35. Pozuelo Rubio M, Campbell DG, Morrice NA, Mackintosh C (2005) Phosphodiesterase 3A binds to 14-3-3 proteins in response to PMA-induced phosphorylation of Ser428. Biochem J 392: 163-172
36. Richard FJ, Tsafriri A, Conti M (2001) Role of phosphodiesterase type 3A in rat oocyte maturation. Biol Reprod 65: 1444-1451
37. Rondinone CM, Carvalho E, Rahn T, Manganiello VC, Degerman E, Smith UP (2000) Phosphorylation of PDE3B by phosphatidylinositol 3-kinase associated with the insulin receptor. J Biol Chem 275: 10093-10098
38. Sadler SE (1991) Type III phosphodiesterase plays a necessary role in the growth-promoting actions of insulin, insulin-like growth factor-I, and Ha p21ras in Xenopus laevis oocytes. Mol Endocrinol 5: 1939-1946
39. Scheid MP, Woodgett JR (2001) PKB/AKT: functional insights from genetic models. Nat Rev Mol Cell Biol 2: 760-768
40. Sette C, Conti M (1996) Phosphorylation and activation of a cAMP-specific phosphodiesterase by the cAMP-dependent protein kinase. Involvement of serine 54 in the enzyme activation. J Biol Chem 271: 16526-16534
41. Shakur Y, Takeda K, Kenan Y, Yu ZX, Rena G, Brandt D, Houslay MD, Degerman E, Ferrans VJ, Manganiello VC (2000) Membrane localization of cyclic nucleotide phosphodiesterase 3 (PDE3). Two N-terminal domains are required for the efficient targeting to, and association of, PDE3 with endoplasmic reticulum. J Biol Chem 275: 38749-38761
42. Shitsukawa K, Andersen CB, Richard FJ, Horner AK, Wiersma A, van Duin M, Conti M (2001) Cloning and characterization of the cyclic guanosine monophosphate-inhibited phosphodiesterase PDE3A expressed in mouse oocyte. Biol Reprod 65: 188-196
43. Smitz J, Cortvrindt R, Hu Y (1998) Epidermal growth factor combined with recombinant human chorionic gonadotrophin improves meiotic progression in mouse follicle-enclosed oocyte culture. Hum Reprod 13: 664-669
44. Svoboda P, Stein P, Schultz RM (2001) RNAi in mouse oocytes and preimplantation embryos: effectiveness of hairpin dsRNA. Biochem Biophys Res Commun 287: 1099-1104
45. Thompson WJ, Terasaki WL, Epstein PM, Strada SJ (1979) Assay of cyclic nucleotide phosphodiesterase and resolution of multiple molecular forms of the enzyme. Adv Cyclic Nucleotide Res 10: 69-92
46. Toker A, Newton AC (2000) Cellular signaling: pivoting around PDK-1. Cell 103: 185-188
47. Tsafriri A, Chun SY, Zhang R, Hsueh AJ, Conti M (1996) Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev Biol 178: 393-402
48. Webster MK, Goya L, Ge Y, Maiyar AC, Firestone GL (1993) Characterization of sgk, a novel member of the serine/threonine protein kinase gene family which is transcriptionally induced by glucocorticoids and serum. Mol Cell Biol 13: 2031-2040
49. Wechsler J, Choi YH, Krall J, Ahmad F, Manganiello VC, Movsesian MA (2002) Isoforms of cyclic nucleotide phosphodiesterase PDE3A in cardiac myocytes. J Biol Chem 277: 38072-38078
50. Wijkander J, Landstrom TR, Manganiello V, Belfrage P, Degerman E (1998) Insulin-induced phosphorylation and activation of phosphodiesterase 3B in rat adipocytes: possible role for protein kinase B but not mitogen-activated protein kinase or p70 S6 kinase. Endocrinology 139: 219-227
51. Wiley LM, Wu JX, Harari I, Adamson ED (1992) Epidermal growth factor receptor mRNA and protein increase after the four-cell preimplantation stage in murine development. Dev Biol 149: 247-260