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. 1986 Dec 20;5(13):3571–3577. doi: 10.1002/j.1460-2075.1986.tb04684.x

C-myc expression is dissociated from DNA synthesis and cell division in Xenopus oocyte and early embryonic development.

F Godeau, H Persson, H E Gray, A B Pardee
PMCID: PMC1167395  PMID: 3549281

Abstract

The combined use of a human c-myc probe and of an antibody raised against the human c-myc gene product demonstrated that the Xenopus cells contained a 2.5-kb c-myc transcript and synthesized a c-myc immunoreactive 65-kd polypeptide. In full-grown oocytes, p65c-myc was predominantly located in the nucleus. In non-dividing Xenopus oocytes c-myc mRNA was present at a steady-state level 10(4) times higher than that of growing somatic A6 cells. This very high level of c-myc transcript was reached early in oogenesis and remained constant thereafter. The rate of p65c-myc synthesis also reached high levels, but only in vitellogenic oocytes, suggesting a post-transcriptional control. Although the cell cycle is resumed at a very fast pace in developing embryos, no further increase in total embryonic content of c-myc RNA could be demonstrated up to the swimming tadpole stage. Furthermore, in embryos the rate of synthesis of p65c-myc decreased to a level markedly lower than that of cell cycle-arrested vitellogenic oocytes. This observation suggests that the function of the c-myc gene in the cell cycle may not be implicated directly in sustaining DNA synthesis or mitosis.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Armelin H. A., Armelin M. C., Kelly K., Stewart T., Leder P., Cochran B. H., Stiles C. D. Functional role for c-myc in mitogenic response to platelet-derived growth factor. Nature. 1984 Aug 23;310(5979):655–660. doi: 10.1038/310655a0. [DOI] [PubMed] [Google Scholar]
  2. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BROWN D. D., GURDON J. B. ABSENCE OF RIBOSOMAL RNA SYNTHESIS IN THE ANUCLEOLATE MUTANT OF XENOPUS LAEVIS. Proc Natl Acad Sci U S A. 1964 Jan;51:139–146. doi: 10.1073/pnas.51.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BROWN D. D., LITTNA E. VARIATIONS IN THE SYNTHESIS OF STABLE RNA'S DURING OOGENESIS AND DEVELOPMENT OF XENOPUS LAEVIS. J Mol Biol. 1964 May;8:688–695. doi: 10.1016/s0022-2836(64)80117-0. [DOI] [PubMed] [Google Scholar]
  5. Battey J., Moulding C., Taub R., Murphy W., Stewart T., Potter H., Lenoir G., Leder P. The human c-myc oncogene: structural consequences of translocation into the IgH locus in Burkitt lymphoma. Cell. 1983 Oct;34(3):779–787. doi: 10.1016/0092-8674(83)90534-2. [DOI] [PubMed] [Google Scholar]
  6. Bienz M., Gurdon J. B. The heat-shock response in Xenopus oocytes is controlled at the translational level. Cell. 1982 Jul;29(3):811–819. doi: 10.1016/0092-8674(82)90443-3. [DOI] [PubMed] [Google Scholar]
  7. Bishop J. M. Viral oncogenes. Cell. 1985 Aug;42(1):23–38. doi: 10.1016/s0092-8674(85)80098-2. [DOI] [PubMed] [Google Scholar]
  8. Blin N., Stafford D. W. A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res. 1976 Sep;3(9):2303–2308. doi: 10.1093/nar/3.9.2303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Campisi J., Gray H. E., Pardee A. B., Dean M., Sonenshein G. E. Cell-cycle control of c-myc but not c-ras expression is lost following chemical transformation. Cell. 1984 Feb;36(2):241–247. doi: 10.1016/0092-8674(84)90217-4. [DOI] [PubMed] [Google Scholar]
  10. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  11. Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
  12. Eisenman R. N., Tachibana C. Y., Abrams H. D., Hann S. R. V-myc- and c-myc-encoded proteins are associated with the nuclear matrix. Mol Cell Biol. 1985 Jan;5(1):114–126. doi: 10.1128/mcb.5.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Elliott S. G., McLaughlin C. S. Rate of macromolecular synthesis through the cell cycle of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4384–4388. doi: 10.1073/pnas.75.9.4384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ford P. J. Non-coordinated accumulation and synthesis of 5S ribonucleic acid by ovaries of Xenopus laevis. Nature. 1971 Oct 22;233(5321):561–564. doi: 10.1038/233561a0. [DOI] [PubMed] [Google Scholar]
  15. Golden L., Schafer U., Rosbash M. Accumulation of individual pA+ RNAs during oogenesis of Xenopus laevis. Cell. 1980 Dec;22(3):835–844. doi: 10.1016/0092-8674(80)90560-7. [DOI] [PubMed] [Google Scholar]
  16. Gurdon J. B., Wickens M. P. The use of Xenopus oocytes for the expression of cloned genes. Methods Enzymol. 1983;101:370–386. doi: 10.1016/0076-6879(83)01028-9. [DOI] [PubMed] [Google Scholar]
  17. Hann S. R., Thompson C. B., Eisenman R. N. c-myc oncogene protein synthesis is independent of the cell cycle in human and avian cells. 1985 Mar 28-Apr 3Nature. 314(6009):366–369. doi: 10.1038/314366a0. [DOI] [PubMed] [Google Scholar]
  18. Hausen P., Wang Y. H., Dreyer C., Stick R. Distribution of nuclear proteins during maturation of the Xenopus oocyte. J Embryol Exp Morphol. 1985 Nov;89 (Suppl):17–34. [PubMed] [Google Scholar]
  19. Hayward W. S., Neel B. G., Astrin S. M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. doi: 10.1038/290475a0. [DOI] [PubMed] [Google Scholar]
  20. Kelly K., Cochran B. H., Stiles C. D., Leder P. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell. 1983 Dec;35(3 Pt 2):603–610. doi: 10.1016/0092-8674(83)90092-2. [DOI] [PubMed] [Google Scholar]
  21. Klein G., Klein E. Evolution of tumours and the impact of molecular oncology. Nature. 1985 May 16;315(6016):190–195. doi: 10.1038/315190a0. [DOI] [PubMed] [Google Scholar]
  22. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  23. Land H., Parada L. F., Weinberg R. A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature. 1983 Aug 18;304(5927):596–602. doi: 10.1038/304596a0. [DOI] [PubMed] [Google Scholar]
  24. Lee G., Hynes R., Kirschner M. Temporal and spatial regulation of fibronectin in early Xenopus development. Cell. 1984 Mar;36(3):729–740. doi: 10.1016/0092-8674(84)90353-2. [DOI] [PubMed] [Google Scholar]
  25. Mauck J. C., Green H. Regulation of RNA synthesis in fibroblasts during transition from resting to growing state. Proc Natl Acad Sci U S A. 1973 Oct;70(10):2819–2822. doi: 10.1073/pnas.70.10.2819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mills A. D., Laskey R. A., Black P., De Robertis E. M. An acidic protein which assembles nucleosomes in vitro is the most abundant protein in Xenopus oocyte nuclei. J Mol Biol. 1980 May 25;139(3):561–568. doi: 10.1016/0022-2836(80)90148-5. [DOI] [PubMed] [Google Scholar]
  27. Mougneau E., Lemieux L., Rassoulzadegan M., Cuzin F. Biological activities of v-myc and rearranged c-myc oncogenes in rat fibroblast cells in culture. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5758–5762. doi: 10.1073/pnas.81.18.5758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Moya M., Dautry-Varsat A., Goud B., Louvard D., Boquet P. Inhibition of coated pit formation in Hep2 cells blocks the cytotoxicity of diphtheria toxin but not that of ricin toxin. J Cell Biol. 1985 Aug;101(2):548–559. doi: 10.1083/jcb.101.2.548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell. 1982 Oct;30(3):675–686. doi: 10.1016/0092-8674(82)90272-0. [DOI] [PubMed] [Google Scholar]
  30. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell. 1982 Oct;30(3):687–696. doi: 10.1016/0092-8674(82)90273-2. [DOI] [PubMed] [Google Scholar]
  31. Persson H., Gray H. E., Godeau F., Braunhut S., Bellvé A. R. Multiple growth-associated nuclear proteins immunoprecipitated by antisera raised against human c-myc peptide antigens. Mol Cell Biol. 1986 Mar;6(3):942–949. doi: 10.1128/mcb.6.3.942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Persson H., Gray H. E., Godeau F. Growth-dependent synthesis of c-myc-encoded proteins: early stimulation by serum factors in synchronized mouse 3T3 cells. Mol Cell Biol. 1985 Nov;5(11):2903–2912. doi: 10.1128/mcb.5.11.2903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Persson H., Hennighausen L., Taub R., DeGrado W., Leder P. Antibodies to human c-myc oncogene product: evidence of an evolutionarily conserved protein induced during cell proliferation. Science. 1984 Aug 17;225(4663):687–693. doi: 10.1126/science.6431612. [DOI] [PubMed] [Google Scholar]
  34. Persson H., Leder P. Nuclear localization and DNA binding properties of a protein expressed by human c-myc oncogene. Science. 1984 Aug 17;225(4663):718–721. doi: 10.1126/science.6463648. [DOI] [PubMed] [Google Scholar]
  35. Pierandrei-Amaldi P., Campioni N., Beccari E., Bozzoni I., Amaldi F. Expression of ribosomal-protein genes in Xenopus laevis development. Cell. 1982 Aug;30(1):163–171. doi: 10.1016/0092-8674(82)90022-8. [DOI] [PubMed] [Google Scholar]
  36. Rabbitts P. H., Watson J. V., Lamond A., Forster A., Stinson M. A., Evan G., Fischer W., Atherton E., Sheppard R., Rabbitts T. H. Metabolism of c-myc gene products: c-myc mRNA and protein expression in the cell cycle. EMBO J. 1985 Aug;4(8):2009–2015. doi: 10.1002/j.1460-2075.1985.tb03885.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rebagliati M. R., Weeks D. L., Harvey R. P., Melton D. A. Identification and cloning of localized maternal RNAs from Xenopus eggs. Cell. 1985 Oct;42(3):769–777. doi: 10.1016/0092-8674(85)90273-9. [DOI] [PubMed] [Google Scholar]
  38. Roeder R. G. Multiple forms of deoxyribonucleic acid-dependent ribonucleic acid polymerase in Xenopus laevis. Levels of activity during oocyte and embryonic development. J Biol Chem. 1974 Jan 10;249(1):249–256. [PubMed] [Google Scholar]
  39. Rosbash M. Polyadenylic acid-containing RNA in Xenopus laevis oocytes. J Mol Biol. 1974 May 5;85(1):87–101. doi: 10.1016/0022-2836(74)90131-4. [DOI] [PubMed] [Google Scholar]
  40. Ruderman J. V., Woodland H. R., Sturgess E. A. Modulations of histone messenger RNA during the early development of Xenopus laevis. Dev Biol. 1979 Jul;71(1):71–82. doi: 10.1016/0012-1606(79)90083-6. [DOI] [PubMed] [Google Scholar]
  41. Scharff M. D., Robbins E. Synthesis of ribosomal RNA in synchronized HeLa cells. Nature. 1965 Oct 30;208(5009):464–466. doi: 10.1038/208464a0. [DOI] [PubMed] [Google Scholar]
  42. Scheer U. Nuclear pore flow rate of ribosomal RNA and chain growth rate of its precursor during oogenesis of Xenopus laevis. Dev Biol. 1973 Jan;30(1):13–28. doi: 10.1016/0012-1606(73)90044-4. [DOI] [PubMed] [Google Scholar]
  43. Stewart T. A., Bellvé A. R., Leder P. Transcription and promoter usage of the myc gene in normal somatic and spermatogenic cells. Science. 1984 Nov 9;226(4675):707–710. doi: 10.1126/science.6494906. [DOI] [PubMed] [Google Scholar]
  44. Stewart T. A., Pattengale P. K., Leder P. Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell. 1984 Oct;38(3):627–637. doi: 10.1016/0092-8674(84)90257-5. [DOI] [PubMed] [Google Scholar]
  45. Thompson C. B., Challoner P. B., Neiman P. E., Groudine M. Levels of c-myc oncogene mRNA are invariant throughout the cell cycle. 1985 Mar 28-Apr 3Nature. 314(6009):363–366. doi: 10.1038/314363a0. [DOI] [PubMed] [Google Scholar]
  46. Woodland H. R., Adamson E. D. The synthesis and storage of histones during the oogenesis of Xenopus laevis. Dev Biol. 1977 May;57(1):118–135. doi: 10.1016/0012-1606(77)90359-1. [DOI] [PubMed] [Google Scholar]
  47. Woodland H. The translational control phase of early development. Biosci Rep. 1982 Jul;2(7):471–491. doi: 10.1007/BF01115246. [DOI] [PubMed] [Google Scholar]

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