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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- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- Bishop J. M. Viral oncogenes. Cell. 1985 Aug;42(1):23–38. doi: 10.1016/s0092-8674(85)80098-2. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]