Abstract
Oocytes stimulated to reinitiate meiosis produce an intracytoplasmic maturation promoting factor (MPF). MPF can trigger maturation of recipient prophase-arrested oocytes even after a number of serial microinjection transfers performed in the presence of protein synthesis inhibitors. This indicates that arrested oocytes contain a stockpile of MPF precursor molecules which are posttranslationally activated following MPF seed microinjection and accounts for MPF amplification.
In Patella and the starfish, MPF activity has been shown to be associated with protein phosphorylation. Emetine treatment does not preclude the initiation of protein phosphorylation and MPF formation, which results in nuclear breakdown, chromosome condensation and first maturation spindle formation. Under these conditions, however, dephosphorylation soon occurs, which induces spindle destruction and the precocious formation of interphase-type resting nuclei. The same cytological effects were promoted by the without affecting protein synthesis. Similar results were obtained with sea urchins, amphibians and mammals.
We conclude that (1) newly formed short lived proteins are required for maintaining metaphase 1 conditions in Patella or for driving the next cycle; (2) these proteins can only act if they are further activated directly or indirectly via a phosphorylation dependent process.
Presently, even when major advances have been made in our understanding of the molecular and genetic factors which drive the cell cycle, a number of questions remain to be answered. These will be soon resolved provided that one can choose, for each one, the appropriate key and the best available model.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
Similar content being viewed by others
Literature Cited
Arion D, Meijer L, Brizuela L, Beach D (1988) cdc2 is a component fo the M-phase specific histone H1-kinase: evidence for identity with MPF. Cell 55: 371–378
Clarke HJ, Masui Y (1983) The induction of reversible and irreversible chromosome condensation by protein synthesis inhibition during meiotic maturation of mouse oocytes. Dev Biol 97: 291–301
Cyert MS, Kirschner MW (1988) Regulation of MPF activity in vitro. Cell 53: 185–195
Dorée M, Guerrier P (1975) Site of action of 1-methylademine in inducing oocyte maturation in starfish: kinetic evidence for receptors localized on the cell membrane. Exp Cell Res 96: 296–300
Dorée M, Peaucellier G, Picard A (1983) Activity of the maturation promoting factor and the extent of the protein phosphorylation oscillate simultaneously during meiotic maturation of starfish oocytes. Dev Biol 99: 489–501
Draetta G, Piwnica-Worms H, Morrison D, Druker B, Roberts T, Beach D (1988) Human cdc2 protein kinase is a major cell-cycle regulated tyrosine kinase substrate. Nature 336: 738–744
Dumphy WG, Newport JW (1988) Mitosis-inducing factors are present in a latent form during interphase in the Xenopus embryo. J Cell Biol 106: 2047–2056
Dumphy WG, Newport JW (1989) Fission yeast p13 blocks mitotic activation and tyrosine dephosphorylation of the Xenopus cdc 2 protein kinase. Cell 58: 181–191
Fortune JE, Concannon PW, Hansel W (1975) Ovarian progesterone level during in vitro oocyte maturation and ovulation in Xenopus laevis. Biol Reprod 13: 561–567
Gautier J, Matsukanva T, Nurse P, Maller J (1989) Dephosphorylation and activation of Xenopus p34 cdc2 protein kinase during the cell cycle. Nature 339: 626–629
Goris J, Hermann J, Hendrix P, Ozon R, Merlevede W (1989) Okadaic acid, a non-TPA tumor promotor, inhibits specifically protein phophatases, induces maturation and MPF formation in Xenopus laevis oocytes. Adv Prot Phosphatases 5: 579–592
Guerrier P, Dorée M (1975) Hormonal control of reinitiation of meiosis in starfish. The requirement of 1- methyladenine during nuclear maturation. Dev Biol 47: 341–348
Guerrier P, Moreau M, Meijer L, Mazzei G, Vilain JP, Dubé F (1982) The role of calcium in meiosis reinitiation. Progress in clinical and Biological Research 91: 139–155
Guerrier P, Brassart M, David C, Moreau M (1986 a) Sequential control of meiosis reinitiation by pH and Ca2+ in the prosobranch mollusk Patella vulgata. Dev Biol 114: 315–324
Guerrier P, Guerrier C, Néant I, Moreau M (1986 b) Germinal vesicle nucleoplasm and intracellular pH requirements for cytoplasmic maturity in oocytes of the prosobranch mollusk Patella vulgata. Dev Biol 116: 92–99
Guerrier P, Néant I (1986) Metabolic cooperation following fusion of starfish ootid and primary oocyte restores meiotic phase-promoting activity. Proc Natl Acad Sci USA 83: 4814–4818
Hirai S, Kanatani H (1971) Site of production of meiosis-inducing substance in ovary of starfish. Exp Cell Res 67: 224–227
Kanatani H (1964) Spawning of starfish: action of gamete-shedding substances obtained from radial nerves. Science 146: 1177–1179
Kanatani H, Shirai H, Nakanishi K, Kurokawa T (1969) Isolation and identification of meiosis-inducing substance in starfish Asterias amurensis. Nature 221: 273–274
Kanatani H, Shirai H (1972) On the maturation-inducing substance produced in starfish gonad by neural substance. Gen Comp Endocrinol Suppl 3: 571–579
Kanatani H, Hiramoto Y (1970) Site of action of 1-methyladenine in inducing oocyte maturation in starfish. Exp Cell Res 61: 280–284
Kishimoto T, Yamazaki K, Kato Y, Koide S, Kanatani H (1984) Induction of starfish oocyte maturation by maturation promoting factor of mouse and surf clam oocytes. J Exp Zool 231: 293–295
Labbé JC, Lee MG, Nurse P, Picard A, Dorée M (1988) Activation at M- phase of a protein kinase encoded by à starfish hormologue of the cell cycle controgene cdc2+. Nature 335: 251–254
Labbé JC, Picard A, Peaucellier G, Cavadore JC, Nurse P, Dorée M (1989) Purification of MPF from starfish: identification as the H1 histone kinase p34 cdc2 and a possible mechanism for its periodic activation. Cell 57: 253–263
Masui Y, Clarke HJ (1979) Oocyte maturation. Int Rev Cytol 57: 185–282
Masui Y, Markert CL (1971) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177: 129–146
Masui Y, Meyerhof PG, Ziegler DH (1979) Control of chromosome behavior during progesterone induced maturation in amphibian oocytes. J Steroid Biochem 11: 715–722
Meijer L, Guerrier P (1984) Maturation and fertilization in starfish oocytes. Int Rev Cytol 86: 129–196
Moria AO, Draetta G, Beach D, Wang JYJ (1989) Reversible tyrosine phosphorilation of cdc2: dephosphorylation accompanies activation during entry into mitosis. Cell 58: 193–203
Néant I, Guerrier P (1988 a) Meiosis réinitiation in the mollusc Patella vulgata. Regulation of MPF, CSF and chromosome condensation activity by intracellular pH, protein synthesis and phosphorylation. Development 102: 505–516
Néant I, Guerrier P (1988 b) 6- dimethylaminopurine blocks starfish oocyte maturation by inhibiting a relevant protein kinase. Exp Cell Res 176: 68–79
Néant I, Charbonneau M, Guerrier P (1989) A requirement for protein phosphorylation in regulating the meiotic and mitotic, cell cycles in echinoderms. Dev Biol 132: 304–314
Picard A, Labbé JC, Peaucellier G, Le Bouffant F, Le Peuch C, Dorée M (1987) Changes in the activity of the maturation promoting factor are correlated with those of a major cyclin AMP and calcium-independent protein kinase during the first meiotic cell cycles in the early starfish embryo. Develop Growth Differ 29: 93–103
Rebhun LL, White D, Sander G, Ivy N (1973) Cleavage inhibition in marine eggs by puromycin and 6-dimethylaminopurine. Exp Cell Res 77: 312–318
Reynhout JK, Smith LD (1974) Studies of the appearance and nature of a maturation inducing factor in the cytoplasm of amphibian oocytes exposed to progesterone. Dev Biol 38: 394–400
Rime H, Néant I, Guerrier P, Ozon R (1989) 6- Dimethylaminopurine (6 DMAP), a reversible inhibitor of the transition to metaphase during the first meiotic cell division of the mouse oocyte. Dev Biol 133: 164–179
Sano K, Kanatani H (1983) Effect of various protease inhibitors on starfish oocyte maturation. Biomed Res 4: 139–146
Sawada MT, Someno T, Hoshi M, Sawada H (1989) Inhibition of starfish oocyte maturation by leupeptin analogs, potent trypsin inhibitors. Dev Biol 133: 609–612
Shirai H, Néant I, Guerrier P (1987) Induction of oocyte maturation by a ganglion extract in Patella vulgata. Develop Growth Differ 29: 398
Smith LD, Ecker RE (1969) Role of the oocyte nucleus in physiological maturation in Rana pipiens. Dev Biol 19: 281–309
Smith LD, Ecker RE (1971) The interaction of steroids with Rana pipieus oocytes in the induction of maturation. Dev Biol 25: 232–247
Standart N, Minshull J, Pines J, Hunt T (1987) Cyclin synthesis, modification and destruction during meiotic maturation of the starfish oocyte. Dev Biol 124: 248–258
Sunkara PS, Wright DA, Rao PN (1979) Mitotic factors from mammalian cells induce germinal vesicle breakdown and chromosome condensation in amphibian oocytes. Proc natl Acad Sci USA 76: 2799–2802
Weintraub H, Buscaglia M, Ferrez M, Weiller S, Boulet A, Fabre F, Baulieu EE (1982) Mise en évidence d’une activité MPF chez Saccharomyces cerevisiae. CR hebd Seanc Acad Sci Paris: 295: 787–790
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1990 Springer-Verlag Berlin Heidelberg
About this paper
Cite this paper
Guerrier, P., Néant, I., Colas, P., Dufresne, L., Pierre, J.S., Dubé, F. (1990). Protein Synthesis and Protein Phosphorylation as Regulators of MPF Activity. In: Dale, B. (eds) Mechanism of Fertilization: Plants to Humans. NATO ASI Series, vol 45. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-83965-8_7
Download citation
DOI: https://doi.org/10.1007/978-3-642-83965-8_7
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-83967-2
Online ISBN: 978-3-642-83965-8
eBook Packages: Springer Book Archive