Home LiteratureArticle Details
PMID: 1321032 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The 'second-codon rule' and autophosphorylation govern the stability and activity of Mos during the meiotic cell cycle in Xenopus oocytes.

The EMBO journal ·Vol. 11 ·No. 7 ·1992-07-00 ·Pages 2433-46

Nishizawa M, Okazaki K, Furuno N, Watanabe N, Sagata N

Abstract

The c-mos proto-oncogene product, Mos, functions in both early (germinal vesicle breakdown) and late (metaphase II arrest) steps during meiotic maturation in Xenopus oocytes. In the early step, Mos is only partially phosphorylated and metabolically unstable, while in the late step it is fully phosphorylated and highly stable. Using a number of Mos mutants expressed in oocytes, we show here that the instability of Mos in the early step is determined primarily by its penultimate N-terminal residue, or by a rule referred to here as the 'second-codon rule'. We demonstrate that unstable Mos is degraded by the ubiquitin-dependent pathway. In the late step, on the other hand, Mos is stabilized by autophosphorylation at Ser3, which probably acts to prevent the N-terminus of Mos from being recognized by a ubiquitin-protein ligase. Moreover, we show that Ser3 phosphorylation is essential for Mos to exert its full cytostatic factor (CSF) activity in fully mature oocytes. Thus, a few N-terminal amino acids are primary determinants of both the metabolic stability and physiological activity of Mos during the meiotic cell cycle.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Codon DNA Electrophoresis, Polyacrylamide Gel Humans Meiosis Molecular Sequence Data Ovum/cytology Peptide Mapping Phosphorylation Phosphotransferases/metabolism Precipitin Tests Protein-Tyrosine Kinases/genetics,metabolism Proto-Oncogene Mas Proto-Oncogene Proteins/genetics,metabolism Proto-Oncogene Proteins c-mos Serine/metabolism Ubiquitins/metabolism Xenopus
Chemicals
Codon MAS1 protein, human Proto-Oncogene Mas Proto-Oncogene Proteins Ubiquitins Serine DNA Phosphotransferases Protein-Tyrosine Kinases Proto-Oncogene Proteins c-mos
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Nishizawa M
Division of Molecular Genetics, Kurume University, Fukuoka, Japan.
Okazaki K
Furuno N
Watanabe N
Sagata N
References (77)
77 references, click to expand
  1. Involvement of the proteasome in various degradative processes in mammalian cells.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2597-601 PMID: 2539595
  2. Specific proteolysis of the c-mos proto-oncogene product by calpain on fertilization of Xenopus eggs.
    Nature. 1989 Nov 30;342(6249):505-11 PMID: 2555717
  3. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells.
    Cell. 1987 Nov 6;51(3):503-12 PMID: 2822260
  4. Ubiquitin-mediated pathways for intracellular proteolysis.
    Annu Rev Cell Biol. 1987;3:1-30 PMID: 2825735
  5. Expression of c-mos RNA in germ cells of male and female mice.
    Proc Natl Acad Sci U S A. 1987 Jul;84(13):4509-13 PMID: 2955407
  6. Cyclin is degraded by the ubiquitin pathway.
    Nature. 1991 Jan 10;349(6305):132-8 PMID: 1846030
  7. Definition of a consensus sequence for peptide substrate recognition by p44mpk, the meiosis-activated myelin basic protein kinase.
    J Biol Chem. 1991 Aug 15;266(23):15180-4 PMID: 1907971
  8. Regulation of rhodopsin kinase by autophosphorylation.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2568-72 PMID: 2006192
  9. Universal control mechanism regulating onset of M-phase.
    Nature. 1990 Apr 5;344(6266):503-8 PMID: 2138713
  10. Activation of cell growth by binding of Friend spleen focus-forming virus gp55 glycoprotein to the erythropoietin receptor.
    Nature. 1990 Feb 22;343(6260):762-4 PMID: 2154701
  11. The multicatalytic proteinase complex, a major extralysosomal proteolytic system.
    Biochemistry. 1990 Nov 13;29(45):10289-97 PMID: 2175651
  12. Substrates for p34cdc2: in vivo veritas?
    Cell. 1990 May 18;61(4):549-51 PMID: 2188729
  13. Microinjection of antisense c-mos oligonucleotides prevents meiosis II in the maturing mouse egg.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):7038-42 PMID: 2476810
  14. Expression of c-mos proto-oncogene transcripts in mouse tissues.
    Nature. 1985 Jun 6-12;315(6019):516-8 PMID: 4000280
  15. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals.
    J Morphol. 1972 Feb;136(2):153-79 PMID: 4109871
  16. The use of Xenopus oocytes for the expression of cloned genes.
    Methods Enzymol. 1983;101:370-86 PMID: 6193395
  17. Hemin inhibits ATP-dependent ubiquitin-dependent proteolysis: role of hemin in regulating ubiquitin conjugate degradation.
    Proc Natl Acad Sci U S A. 1981 Nov;78(11):6845-8 PMID: 6273891
  18. Conjugation of ubiquitin to denatured hemoglobin is proportional to the rate of hemoglobin degradation in HeLa cells.
    Proc Natl Acad Sci U S A. 1982 Oct;79(19):5857-61 PMID: 6310549
  19. Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs.
    J Cell Biol. 1984 Apr;98(4):1247-55 PMID: 6425302
  20. Red light-induced formation of ubiquitin-phytochrome conjugates: Identification of possible intermediates of phytochrome degradation.
    Proc Natl Acad Sci U S A. 1987 Jan;84(2):359-63 PMID: 16593800
  21. Properties of a cytostatic factor from Xenopus laevis eggs.
    Dev Biol. 1979 Sep;72(1):182-7 PMID: 315899
  22. Acetylation of Protein N-terminal amino groups structural observations on alpha-amino acetylated proteins.
    J Theor Biol. 1975 Nov;55(1):1-12 PMID: 1207150
  23. Progression from meiosis I to meiosis II in Xenopus oocytes requires de novo translation of the mosxe protooncogene.
    Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5794-8 PMID: 1648231
  24. Natural substrates of the ubiquitin proteolytic pathway.
    Cell. 1991 Aug 23;66(4):615-8 PMID: 1652366
  25. Ability of the c-mos product to associate with and phosphorylate tubulin.
    Science. 1991 Feb 8;251(4994):671-5 PMID: 1825142
  26. A characterization of cytostatic factor activity from Xenopus eggs and c-mos-transformed cells.
    J Cell Biol. 1991 Jul;114(2):329-35 PMID: 1830055
  27. Oocyte maturation.
    Int Rev Cytol. 1979;57:185-282 PMID: 385540
  28. Differential occurrence of CSF-like activity and transforming activity of Mos during the cell cycle in fibroblasts.
    EMBO J. 1992 Jul;11(7):2447-56 PMID: 1385775
  29. The short-lived MAT alpha 2 transcriptional regulator is ubiquitinated in vivo.
    Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4606-10 PMID: 1647011
  30. Pro-Leu-Ser/Thr-Pro is a consensus primary sequence for substrate protein phosphorylation. Characterization of the phosphorylation of c-myc and c-jun proteins by an epidermal growth factor receptor threonine 669 protein kinase.
    J Biol Chem. 1991 Aug 15;266(23):15277-85 PMID: 1651323
  31. In vitro effects on microtubule dynamics of purified Xenopus M phase-activated MAP kinase.
    Nature. 1991 Jan 17;349(6306):251-4 PMID: 1702878
  32. Degradation of the proto-oncogene product p39mos is not necessary for cyclin proteolysis and exit from meiotic metaphase: requirement for a Ca(2+)-calmodulin dependent event.
    EMBO J. 1991 Aug;10(8):2087-93 PMID: 1829675
  33. Independent inactivation of MPF and cytostatic factor (Mos) upon fertilization of Xenopus eggs.
    Nature. 1991 Jul 18;352(6332):247-8 PMID: 1830371
  34. Degradation of nuclear oncoproteins by the ubiquitin system in vitro.
    Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):139-43 PMID: 1846034
  35. Sindbis virus RNA polymerase is degraded by the N-end rule pathway.
    Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):8967-71 PMID: 1924357
  36. The N-end rule in bacteria.
    Science. 1991 Nov 29;254(5036):1374-7 PMID: 1962196
  37. Mouse Mos protooncogene product is present and functions during oogenesis.
    Proc Natl Acad Sci U S A. 1989 Jul;86(14):5395-9 PMID: 2526337
  38. The degradation signal in a short-lived protein.
    Cell. 1989 Mar 24;56(6):1019-32 PMID: 2538246
  39. Dephosphorylation and activation of Xenopus p34cdc2 protein kinase during the cell cycle.
    Nature. 1989 Jun 22;339(6226):626-9 PMID: 2543932
  40. The scanning model for translation: an update.
    J Cell Biol. 1989 Feb;108(2):229-41 PMID: 2645293
  41. Ubiquitin-mediated protein degradation.
    J Biol Chem. 1988 Oct 25;263(30):15237-40 PMID: 2844803
  42. Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes.
    Nature. 1988 Oct 6;335(6190):519-25 PMID: 2971141
  43. Lysine residue 121 in the proposed ATP-binding site of the v-mos protein is required for transformation.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):7894-8 PMID: 2999782
  44. The protein substrate binding site of the ubiquitin-protein ligase system.
    J Biol Chem. 1986 Sep 15;261(26):11992-9 PMID: 3017957
  45. Growth factor receptor tyrosine kinases.
    Annu Rev Biochem. 1988;57:443-78 PMID: 3052279
  46. Sequence determinants of cytosolic N-terminal protein processing.
    Eur J Biochem. 1986 Jan 2;154(1):193-6 PMID: 3080313
  47. Stabilization and enhancement of primary cytostatic factor (CSF) by ATP and NaF in amphibian egg cytosols.
    Dev Biol. 1988 Sep;129(1):253-64 PMID: 3261698
  48. Specificity of cotranslational amino-terminal processing of proteins in yeast.
    Biochemistry. 1987 Dec 15;26(25):8242-6 PMID: 3327521
  49. Developmental regulation of ovarian-specific Mos expression.
    Oncogene. 1988 Mar;2(3):235-40 PMID: 3353114
  50. Altered turnover of allelic variants of hypoxanthine phosphoribosyltransferase is associated with N-terminal amino acid sequence variation.
    J Biol Chem. 1988 Jul 5;263(19):9079-82 PMID: 3379061
  51. Interaction of protein kinase C with membranes is regulated by Ca2+, phorbol esters, and ATP.
    J Biol Chem. 1985 Dec 15;260(29):15718-22 PMID: 4066694
  52. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes.
    J Exp Zool. 1971 Jun;177(2):129-45 PMID: 5106340
  53. Immunochemical analysis of the turnover of ubiquitin-protein conjugates in intact cells. Relationship to the breakdown of abnormal proteins.
    J Biol Chem. 1982 Dec 10;257(23):13964-70 PMID: 6292216
  54. Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutant ts85.
    Cell. 1984 May;37(1):43-55 PMID: 6327059
  55. Interconversion of metaphase and interphase microtubule arrays, as studied by the injection of centrosomes and nuclei into Xenopus eggs.
    J Cell Biol. 1984 May;98(5):1730-45 PMID: 6725396
  56. Amino-terminal processing of mutant forms of yeast iso-1-cytochrome c. The specificities of methionine aminopeptidase and acetyltransferase.
    J Biol Chem. 1985 May 10;260(9):5382-91 PMID: 2985590
  57. Serine kinase activity associated with Maloney murine sarcoma virus-124-encoded p37mos.
    Virology. 1985 May;143(1):321-33 PMID: 2998008
  58. The rapid generation of oligonucleotide-directed mutations at high frequency using phosphorothioate-modified DNA.
    Nucleic Acids Res. 1985 Dec 20;13(24):8765-85 PMID: 3001650
  59. In vivo half-life of a protein is a function of its amino-terminal residue.
    Science. 1986 Oct 10;234(4773):179-86 PMID: 3018930
  60. Cotranslational processing and protein turnover in eukaryotic cells.
    Biochemistry. 1988 Oct 18;27(21):7979-84 PMID: 3069123
  61. Differential cytolocalization of prosomes in axolotl during oogenesis and meiotic maturation.
    J Cell Sci. 1988 Aug;90 ( Pt 4):543-53 PMID: 3075616
  62. Proteasomes (multi-protease complexes) as 20 S ring-shaped particles in a variety of eukaryotic cells.
    J Biol Chem. 1988 Nov 5;263(31):16209-17 PMID: 3141402
  63. The Xenopus cdc2 protein is a component of MPF, a cytoplasmic regulator of mitosis.
    Cell. 1988 Jul 29;54(3):423-31 PMID: 3293802
  64. Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2+.
    Cell. 1988 Jul 29;54(3):433-9 PMID: 3293803
  65. Specificity of binding of NH2-terminal residue of proteins to ubiquitin-protein ligase. Use of amino acid derivatives to characterize specific binding sites.
    J Biol Chem. 1988 Feb 25;263(6):2693-8 PMID: 3343227
  66. Cotranslational amino-terminal processing of cytosolic proteins. Cell-free expression of site-directed mutants of human hemoglobin.
    J Biol Chem. 1988 Jun 15;263(17):8443-9 PMID: 3372535
  67. Distinct developmental patterns of c-mos protooncogene expression in female and male mouse germ cells.
    Proc Natl Acad Sci U S A. 1987 Aug;84(15):5301-5 PMID: 3474657
  68. Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis.
    Science. 1990 May 11;248(4956):742-5 PMID: 2110383
  69. The cyclin B2 component of MPF is a substrate for the c-mos(xe) proto-oncogene product.
    Cell. 1990 Jun 1;61(5):825-31 PMID: 2140529
  70. Ha-rasVal-12,Thr-59 activates S6 kinase and p34cdc2 kinase in Xenopus oocytes: evidence for c-mosxe-dependent and -independent pathways.
    Mol Cell Biol. 1990 Jan;10(1):310-5 PMID: 2152963
  71. Evidence for involvement of the protein kinase C pathway in the activation of p37v-mos protein kinase.
    Oncogene. 1990 Aug;5(8):1251-7 PMID: 2168030
  72. Requirement of the c-mos protein kinase for murine meiotic maturation.
    Oncogene. 1990 Nov;5(11):1727-30 PMID: 2176285
  73. Regulation of an enzyme by phosphorylation at the active site.
    Science. 1990 Aug 31;249(4972):1012-6 PMID: 2204109
  74. The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation.
    Science. 1989 Aug 11;245(4918):643-6 PMID: 2474853
  75. Universality and structure of the N-end rule.
    J Biol Chem. 1989 Oct 5;264(28):16700-12 PMID: 2506181
  76. Xenopus homolog of the mos protooncogene transforms mammalian fibroblasts and induces maturation of Xenopus oocytes.
    Proc Natl Acad Sci U S A. 1989 Aug;86(15):5805-9 PMID: 2527365
  77. The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs.
    Nature. 1989 Nov 30;342(6249):512-8 PMID: 2531292
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1992-07-00
Pages
2433-46
Language
English
Region
England
NLM ID
8208664
PMCID
PMC556718
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: product@genelibs.com