Home LiteratureArticle Details
PMID: 206889 Published · ppublish English Journal Article

Amphibian oocyte maturation and protein synthesis: related inhibition by cyclic AMP, theophylline, and papaverine.

Bravo R, Otero C, Allende CC, Allende JE

Abstract

Two inhibitors of cyclic AMP phosphodiesterase (3':5'-cyclic-AMP 5'-nucleotidohydrolase, EC 3.1.4.17), theophylline and papaverine, inhibit the maturation of Xenopus laevis oocytes induced by four different stimuli: human chorionic gonadotropin, progesterone, testosterone, and lanthanum ions. Addition of 1 mM cyclic AMP to the medium delays maturation by approximately 2 hr. Papaverine, theophylline, and cyclic AMP inhibit amino acid incorporation into oocyte proteins by 50% or more but do not inhibit amino acid uptake. The capacity of theophylline to block maturation and protein synthesis is reversed in a parallel fashion by addition of 1-5 mM calcium ion to the medium. Addition of papaverine, theophylline, and cycloheximide to oocytes at different times after hormonal treatment shows that the step sensitive to blockage by the three drugs is coincident and precedes germinal vesicle breakdown by about 1.5 hr. Theophylline and papaverine do not increase endogenous cyclic AMP levels in oocytes but do block the decrease of cyclic AMP levels observed 3 hr after progesterone treatment. Both drugs inhibit oocyte cyclic AMP phosphodiesterase measured in vivo and severely inhibit the stimulus of calcium uptake caused by progesterone and human chorionic gonadotropin. These results suggest that cyclic AMP, theophylline, and papaverine may block oocyte maturation by inhibiting protein synthesis, possibly via a cyclic AMP-dependent protein kinase as shown in reticulocytes [Datta, A., De Haro, C., Sierra, J. & Ochoa, S. (1977) Proc. Natl. Acad. Sci., USA 74, 1463-1467].

MeSH Terms
Animals Calcium/metabolism Chorionic Gonadotropin/antagonists & inhibitors Cyclic AMP/pharmacology Cycloheximide/pharmacology Egg Proteins/biosynthesis Female Lanthanum/antagonists & inhibitors Oocytes/metabolism Oogenesis/drug effects Papaverine/pharmacology Progesterone/antagonists & inhibitors Testosterone/antagonists & inhibitors Theophylline/pharmacology Xenopus
Chemicals
Chorionic Gonadotropin Egg Proteins Testosterone Progesterone Lanthanum Cycloheximide Theophylline Papaverine Cyclic AMP Calcium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Bravo R
Otero C
Allende C C
Allende J E
References (19)
19 references, click to expand
  1. Compartmentalization of adenosine 3':5'-monophosphate and adenosine 3':5'-monophosphate-dependent protein kinase in heart tissue.
    J Biol Chem. 1977 Jun 10;252(11):3854-61 PMID: 16921
  2. Cyclic nucleotide fluctuations during steroid induced meiotic maturation of frog oocytes.
    Nature. 1977 Jun 30;267(5614):848-50 PMID: 197413
  3. Comparison of in vivo and in vitro properties of cyclic adenosine 3':5'-monophosphate phosphodiesterase of amphibian oocytes.
    J Biol Chem. 1977 Jul 10;252(13):4662-6 PMID: 194890
  4. 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. 1977 Mar 10;252(5):1712-8 PMID: 190238
  5. Role of 3':5'-cyclic-AMP-dependent protein kinase in regulation of protein synthesis in reticulocyte lysates.
    Proc Natl Acad Sci U S A. 1977 Apr;74(4):1463-7 PMID: 193101
  6. Changes in protein phosphorylation accompanying maturation of Xenopus laevis oocytes.
    Dev Biol. 1977 Jul 15;58(2):295-312 PMID: 885290
  7. Induction of meiosis by injection of heterologous protein kinase and phosphorylase kinase in Xenopus laevis oocytes.
    J Exp Zool. 1976 Sep;197(3):435-42 PMID: 965920
  8. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals.
    J Morphol. 1972 Feb;136(2):153-79 PMID: 4109871
  9. Cyclic 3',5'-nucleotide phosphodiesterase. Evidence for and properties of a protein activator.
    J Biol Chem. 1971 May 10;246(9):2859-69 PMID: 4324340
  10. A protein binding assay for adenosine 3':5'-cyclic monophosphate.
    Proc Natl Acad Sci U S A. 1970 Sep;67(1):305-12 PMID: 4318781
  11. Induction of maturation (meiosis) in Xenopus laevis oocytes by three organomercurials.
    Proc Natl Acad Sci U S A. 1975 Apr;72(4):1574-8 PMID: 1055428
  12. Conditions affecting protein synthesis in amphibian oocytes.
    Arch Biochem Biophys. 1976 Feb;172(2):648-53 PMID: 4024
  13. Induction of maturation (meiosis) in small Xenopus laevis oocytes by injection of maturation promoting factor.
    Proc Natl Acad Sci U S A. 1976 Jun;73(6):2028-32 PMID: 1064873
  14. Initiation of meiotic maturation in Xenopus laevis oocytes by lanthanum.
    Nature. 1976 Jul 22;262(5566):289-90 PMID: 986558
  15. Progesterone-induced maturational events in oocytes of Xenopus laevis. II. Change in intracellular calcium and magnesium distribution at germinal vesicle breakdown.
    Exp Cell Res. 1971 Sep;68(1):81-7 PMID: 5113963
  16. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes.
    J Exp Zool. 1971 Jun;177(2):129-45 PMID: 5106340
  17. The interaction of steroids with Rana pipiens Oocytes in the induction of maturation.
    Dev Biol. 1971 Jun;25(2):232-47 PMID: 5562852
  18. Action of hormones on germinal vesicle breakdown in frog (Rana pipiens) oocytes.
    J Exp Zool. 1967 Dec;166(3):347-54 PMID: 5625910
  19. Inhibition of oocyte maturation by theophylline: possible mechanism of action.
    Dev Biol. 1976 Sep;52(2):318-22 PMID: 12194441
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1978-03-00
Pages
1242-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC411446
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]