Skip to main content
PMC home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1985 Mar;5(3):538–544. doi: 10.1128/mcb.5.3.538

myc and src oncogenes have complementary effects on cell proliferation and expression of specific extracellular matrix components in definitive chondroblasts.

S Alema, F Tato, D Boettiger
PMCID: PMC366746  PMID: 2985957

Abstract

The effects of the avian viral oncogenes src and myc were compared for their ability to alter the differentiated phenotype and the proliferative capacity of definitive chondroblasts. As previously demonstrated, viruses carrying the src oncogene suppressed the synthesis of the chondroblast-specific products, type II collagen and cartilage-specific sulfated proteoglycan. In contrast, infection with MC29 and HB1 viruses, which carry the myc oncogene, did not suppress the synthesis of these normal differentiated cell products, but the infected cells exhibited an increased proliferative potential. The MH2 virus, which carries both the myc and mil oncogenes, both induced the suppression of these chondroblast-specific products and increased cell proliferation. The implications of these results for cooperation between oncogenes and the multi-oncogene models for neoplastic transformation are discussed.

Full text

PDF
541

Images in this article

539Image
on p.539
540Image
on p.540
541Image
on p.541
542Image
on p.542

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. Boettiger D., Durban E. M. Progenitor-cell populations can be infected by RNA tumor viruses, but transformation is dependent on the expression of specific differentiated functions. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):1249–1254. doi: 10.1101/sqb.1980.044.01.135. [DOI] [PubMed] [Google Scholar]
  3. Bunte T., Greiser-Wilke I., Moelling K. The transforming protein of the MC29-related virus CMII is a nuclear DNA-binding protein whereas MH2 codes for a cytoplasmic RNA-DNA binding polyprotein. EMBO J. 1983;2(7):1087–1092. doi: 10.1002/j.1460-2075.1983.tb01550.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chacko S., Abbott J., Holtzer S., Holtzer H. The loss of phenotypic traits by differentiated cells. VI. Behavior of the progeny of a single chondrocyte. J Exp Med. 1969 Aug 1;130(2):417–442. doi: 10.1084/jem.130.2.417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dessau W., Sasse J., Timpl R., Jilek F., von der Mark K. Synthesis and extracellular deposition of fibronectin in chondrocyte cultures. Response to the removal of extracellular cartilage matrix. J Cell Biol. 1978 Nov;79(2 Pt 1):342–355. doi: 10.1083/jcb.79.2.342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Donner P., Greiser-Wilke I., Moelling K. Nuclear localization and DNA binding of the transforming gene product of avian myelocytomatosis virus. Nature. 1982 Mar 18;296(5854):262–269. doi: 10.1038/296262a0. [DOI] [PubMed] [Google Scholar]
  7. Durban E. M., Boettiger D. Differential effects of transforming avian RNA tumor viruses on avian macrophages. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3600–3604. doi: 10.1073/pnas.78.6.3600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Enrietto P. J., Payne L. N., Hayman M. J. A recovered avian myelocytomatosis virus that induces lymphomas in chickens: pathogenic properties and their molecular basis. Cell. 1983 Dec;35(2 Pt 1):369–379. doi: 10.1016/0092-8674(83)90170-8. [DOI] [PubMed] [Google Scholar]
  9. Gionti E., Capasso O., Cancedda R. The culture of chick embryo chondrocytes and the control of their differentiated functions in vitro. Transformation by rous sarcoma virus induces a switch in the collagen type synthesis and enhances fibronectin expression. J Biol Chem. 1983 Jun 10;258(11):7190–7194. [PubMed] [Google Scholar]
  10. Hann S. R., Abrams H. D., Rohrschneider L. R., Eisenman R. N. Proteins encoded by v-myc and c-myc oncogenes: identification and localization in acute leukemia virus transformants and bursal lymphoma cell lines. Cell. 1983 Oct;34(3):789–798. doi: 10.1016/0092-8674(83)90535-4. [DOI] [PubMed] [Google Scholar]
  11. Jansen H. W., Rückert B., Lurz R., Bister K. Two unrelated cell-derived sequences in the genome of avian leukemia and carcinoma inducing retrovirus MH2. EMBO J. 1983;2(11):1969–1975. doi: 10.1002/j.1460-2075.1983.tb01686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Linial M. Two retroviruses with similar transforming genes exhibit differences in transforming potential. Virology. 1982 Jun;119(2):382–391. doi: 10.1016/0042-6822(82)90097-6. [DOI] [PubMed] [Google Scholar]
  14. Menko A. S., Toyama Y., Boettiger D., Holtzer H. Altered cell spreading in cytochalasin B: a possible role for intermediate filaments. Mol Cell Biol. 1983 Jan;3(1):113–125. doi: 10.1128/mcb.3.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Pachl C., Biegalke B., Linial M. RNA and protein encoded by MH2 virus: evidence for subgenomic expression of v-myc. J Virol. 1983 Jan;45(1):133–139. doi: 10.1128/jvi.45.1.133-139.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pacifici M., Boettiger D., Roby K., Holtzer H. Transformation of chondroblasts by Rous sarcoma virus and synthesis of the sulfated proteoglycan matrix. Cell. 1977 Aug;11(4):891–899. doi: 10.1016/0092-8674(77)90300-2. [DOI] [PubMed] [Google Scholar]
  17. Pacifici M., Soltesz R., Thal G., Shanley D. J., Boettiger D., Holtzer H. Immunological characterization of the major chick cartilage proteoglycan and its intracellular localization in cultured chondroblasts: a comparison with Type II procollagen. J Cell Biol. 1983 Dec;97(6):1724–1736. doi: 10.1083/jcb.97.6.1724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Palmieri S., Kahn P., Graf T. Quail embryo fibroblasts transformed by four v-myc-containing virus isolates show enhanced proliferation but are non tumorigenic. EMBO J. 1983;2(12):2385–2389. doi: 10.1002/j.1460-2075.1983.tb01750.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pawlowski P. J., Brierley G. T., Lukens L. N. Changes in the type II and type I collagen messenger RNA population during growth of chondrocytes in 5-bromo-2-deoxyuridine. J Biol Chem. 1981 Aug 10;256(15):7695–7698. [PubMed] [Google Scholar]
  20. Pfeifer-Ohlsson S., Goustin A. S., Rydnert J., Wahlström T., Bjersing L., Stehelin D., Ohlsson R. Spatial and temporal pattern of cellular myc oncogene expression in developing human placenta: implications for embryonic cell proliferation. Cell. 1984 Sep;38(2):585–596. doi: 10.1016/0092-8674(84)90513-0. [DOI] [PubMed] [Google Scholar]
  21. Prywes R., Foulkes J. G., Rosenberg N., Baltimore D. Sequences of the A-MuLV protein needed for fibroblast and lymphoid cell transformation. Cell. 1983 Sep;34(2):569–579. doi: 10.1016/0092-8674(83)90389-6. [DOI] [PubMed] [Google Scholar]
  22. Ramsay G. M., Enrietto P. J., Graf T., Hayman M. J. Recovery of myc-specific sequences by a partially transformation-defective mutant of avian myelocytomatosis virus, MC29, correlates with the restoration of transforming activity. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6885–6889. doi: 10.1073/pnas.79.22.6885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ramsay G., Graf T., Hayman M. J. Mutants of avian myelocytomatosis virus with smaller gag gene-related proteins have an altered transforming ability. Nature. 1980 Nov 13;288(5787):170–172. doi: 10.1038/288170a0. [DOI] [PubMed] [Google Scholar]
  24. West C. M., Boettiger D. Selective effect of Rous sarcoma virus src gene expression on contractile protein synthesis in chick embryo myotubes. Cancer Res. 1983 May;43(5):2042–2046. [PubMed] [Google Scholar]
  25. Wyke J. A., Linial M. Temperature-sensitive avian sarcoma viruses: a physiological comparison of twenty mutants. Virology. 1973 May;53(1):152–161. doi: 10.1016/0042-6822(73)90474-1. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES