Skip to main content
SpringerLink
Log in
Book cover

Gene Expression in Normal and Transformed Cells pp 315–348Cite as

The Reversible Modulation of the Synthesis of Matrix Components in Definitive Chondroblasts Transformed by a ts-Rous Sarcoma Virus Mutant

  • Chapter

Abstract

The differentiation program of several types of terminally-differentiated embryonic cells can be reversibly altered by transformation with RNA tumour vi ruses. For example, definitive chondroblasts isolated from chick embryo vertebral cartilage and infected with a temperature sensitive (ts)-mutant of Rous sarcoma virus (ts-RSV) lose their characteristic polygonal morphology and become bipolar in shape when maintained at the permissive temperature for transformation (36°C). Concurrently with their morphological alteration, the transformed chondroblasts lose the ability to synthesize two major intercellular matrix components, the Type IV sulphated proteoglycan and Type II collagen (1,2). These morphological and biosynthetic alterations induced by viral transformation are fully reversible; within 1–2 days following a shift to the non-permissive temperature for transformation (41°C), the infected chondroblast display the characteristic polygonal-epithelioid appearance and reinitiate the synthesis of Type IV proteoglycan and Type II collagen.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. PACIFICI, M., BOETTIGER, D., ROBY, K. and HOLTZER, H. (1977). Transformation of chondroblasts by Rous sarcoma virus and synthesis of the sulphated proteoglycan matrix. Cell, 11, 891.

    Article  PubMed  CAS  Google Scholar 

  2. ADAMS, S.L., BOETTIGER, D., FOCHT, R.J., HOLTZER, H., and PACIFICI, M. (1982). Regulation of the synthesis of extracellular matrix components in chondroblasts transformed by a temperature sensitive mutant of Rous sarcoma virus. Cell, 30, 373.

    Article  PubMed  CAS  Google Scholar 

  3. DURBAN, E.M. and BOETTIGER, D. (1981). Differential effects of transforming avian RNA tumour viruses on avian macrophages. Proc. Natl. Acad. Sci. USA, 78, 3600.

    Article  PubMed  CAS  Google Scholar 

  4. BOETTIGER, D., ROBY, K., BRUMBAUGH, J., BIEHL, J. and HOLTZER, H. (1977). Transformation of chicken embryo retinal melano-blasts by a temperature sensitive mutant of Rous sarcoma virus. Cell, 11, 881.

    Article  PubMed  CAS  Google Scholar 

  5. ROUSLAHTI, E., ENGVALL, E. and HAYMAN, E.G. (1981). Fibronec-tin: Current concepts of its structure and functions. Collagen and Related Res., 1, 95.

    Google Scholar 

  6. BORNSTEIN, P. and SAGE, H. (1980). Structurally distinct collagen types. Ann. Rev. Biochem., 49, 957.

    Article  PubMed  CAS  Google Scholar 

  7. LEVINSON, W., BHATNAGAR, R.S. and LIU, T. (1975). Loss of ability to synthesize collagen in fibroblasts transformed by Rous sarcoma virus. J. Natl. Cancer Inst., 55, 807.

    PubMed  CAS  Google Scholar 

  8. OLDEN, K. and YAMADA, K.M. (1977). Mechanism of the decrease in the major cell surface protein of chick embryo fibroblasts after transformation. Cell, 11, 957.

    Article  PubMed  CAS  Google Scholar 

  9. ADAMS, S.L., SOBEL, M.E., HOWARD, B.H., OLDEN, K., YAMADA, K.M., PASTAN, I. and DE CROMBRUGGHE, B. (1977), Levels of translatable mRNAs for cell surface protein, collagen precursors, and two membrane proteins are altered in Rous sarcoma virus-transformed chick embryo fibroblasts. Proc. Natl. Acad. Sci. USA, 74, 3399.

    Article  PubMed  CAS  Google Scholar 

  10. ROWE, D.W., MOEN, R.C., DAVIDSON, J.M., BYERS, P.H., BORNSTEIN, P. and PALMITER, R.D. (1978). Correlation of procollagen mRNA levels in normal and transformed chick embryo fibroblasts with different rates of procollagen synthesis. Biochemistry, 17, 1581.

    Article  PubMed  CAS  Google Scholar 

  11. ADAMS, S.L., ALWINE, J.C., DE CROMBRUGGHE, B. and PASTAN, I. (1979). Use of recombinant plasmids to characterize collagen RNAs in normal and transformed chick embryo fibroblasts. J. Biol. Chem. 254, 4935.

    PubMed  CAS  Google Scholar 

  12. SandMEYER, S. and BORNSTEIN, P. (1979). Declining procollagen mRNA sequences in chick embryo fibroblasts infected with Rous sarcoma virus. J. Biol. Chem., 254, 4950.

    PubMed  CAS  Google Scholar 

  13. FAGAN, J., PASTAN, I. and DE CROMBRUGGGE, B. (1980). Sequence rearrangement and duplication of double stranded fibronectin cDNA probably occurring during cDNA synthesis by AMV reverse transcriptase and E. coli DNA polymerase I. Nucl. Acids Res., 8, 3055.

    Article  PubMed  CAS  Google Scholar 

  14. SandMEYER, S., GALLIS, B., and BORNSTEIN, P. (1981). Coordinate transcriptional regulation of Type I procollagen genes by Rous sarcoma virus. J. Biol. Chem. 256, 5022.

    PubMed  CAS  Google Scholar 

  15. OKAYAMA, M., PACIFICI, M. and HOLTZER, H. (1976). Differences among sulphated proteoglycans synthesized in nonchondrogenic cells, presumptive chondroblasts, and chondroblasts. Proc. Natl. Acad. Sci. USA, 73, 3224.

    Article  PubMed  CAS  Google Scholar 

  16. DE LUCA, S., HEINEGARD, D.K., HASCALL, V.C., KIMURA, J.H. and CAPLAN, A.I. (1977). Chemical and physical changes in proteoglycand during development of chick limb bud chondrocytes grown in vitro. J. Biol. Chem. 252, 6600.

    PubMed  Google Scholar 

  17. HEINEGARD, D.K. and AXELSSON, I. (1977). Distribution of keratan sulphate in proteoglycans. J. Biol. Chem., 252, 1971.

    PubMed  CAS  Google Scholar 

  18. DE LUCA, S., LOHMandER, L.S., NILSSON, B., HASCALL, V.C. and CAPLAN, A.I. (1980). Proteoglycans from chick limb bud chondrocyte cultures: Keratan sulphate and oligosaccharides which contain mannose and sialic acid. J. Biol. Chem., 255, 6077.

    PubMed  Google Scholar 

  19. HASCALL, V.C. and HASCALL, G.K. (1981). Proteoglycans. In; Cell biology of extracellular matrix (ed., E.D. Hay), p. 39, Plenum Press, New York.

    Chapter  Google Scholar 

  20. LOHMandER, L.S., DE LUCA, S., NILSSON, B., HASCALL, V.C., CAPUTO, C.B., KIMURA, J.H. and HEINEGARD, D. (1980). Oligosaccharides on proteoglycans from the Swarm rat chondrosarcoma. J. Biol. Chem., 255, 6084.

    PubMed  CAS  Google Scholar 

  21. LOHMandER, L.S., NILSSON, B., DE LUCA, S. and HASCALL, V.C. (1981). Structures of N- and O-linked oligosaccharides from chondrosarcoma proteoglycan. Seminars in Arthritis and Rheumatism 11 (Supplement), 12.

    Article  CAS  Google Scholar 

  22. HEINEGARD, D.K. and HASCAL, V.C. (1979). The effect of dansylation and acetylation on the interaction between hyaluronic acid and the hyaluronic binding region of cartilage proteoglycans. J. Biol. Chem., 254, 912.

    Google Scholar 

  23. LOWE, M.E., PACIFICI, M. and HOLTZER, H. (1978). Effects of phorbol-12-myristate-13-acetate on the phenotypic program of cultured chondroblasts and fibroblasts. Cancer Res., 38, 2350.

    PubMed  CAS  Google Scholar 

  24. PACIFICI, M. and HOLTZER, H. (1980). 12–0-Tedradecanoylphor-bol-13-acetate-induced changes in sulphated proteoglycan synthesis in cultured chondroblasts. Cancer Res. 40, 2461.

    PubMed  CAS  Google Scholar 

  25. PACIFICI, M. and MOLINARO, M. (1980). Developmental changes in glycosaminoglyeans during skeletal muscle cell differentiation in culture. Exp. Cell Res., 126, 143.

    Article  PubMed  CAS  Google Scholar 

  26. CARLSTEDT, I., COSTER, L. and MALMSTROM, A. (1981). Isolation and characterization of dermatan sulphate and heparan sulphate proteoglycans from fibroblast cultures. Biochem. J., 197, 217.

    PubMed  CAS  Google Scholar 

  27. BLOBEL, G. (1978). Mechanisms for the intracellular compartment of newly synthesized proteins. FEBS (Fed. Eur. Biochem. Soc.) Proc. Meet., 43 (A2), 99.

    Google Scholar 

  28. PROCKOP, D.J., KIVIRIKKO, K.J., TUDERMAN, L. and GUZMAN, N.A. (1979). The biosynthesis of collagen and its disorders. NI. Eng. J. Med., 301, 13 and 77.

    Article  CAS  Google Scholar 

  29. NIST, C., VON DER MARK, K., HAY, E.D., OLSEN, B.R., BORNSTEIN, P., ROSS, R. and DEHM, P. (1975). Localization of procollagen in chick corneal and tendon fibroblasts with ferritin-conjugated antibodies. J. Cell Biol. 65, 75.

    Article  PubMed  CAS  Google Scholar 

  30. HEINEGARD, D.K. (1972). Hyaluronidase digestion and alkaline treatment of bovine tracheal cartilage proteoglycans. Isolation and characterization of different keratan sulphate proteins. Biochem. Biophys. Acta, 285, 193.

    Article  PubMed  CAS  Google Scholar 

  31. MOSKALEWSKI, S., THYBERG, J., LOHMandER, S. and FRIBERG, U. (1975). Influence of colchicine and vinblastine on the Golgi complex and matrix deposition in chondrocyte aggregates. Exp. Cell Res., 95, 440.

    Article  PubMed  CAS  Google Scholar 

  32. KIMURA, J.H., THONAR, E.J.-M., HASCALL, V.C., REINER, A. and POOLE, A.R. (1981). Identification of core protein, and intermediate in proteoglycan biosynthesis in cultured chondrocytes from the swarm rat chondrosarcoma. J. Biol. Chem. 256, 7890.

    PubMed  CAS  Google Scholar 

  33. CHACKO, S., ABBOTT, J., HOLTZER, S. and HOLTZER, H. (1969). The loss of phenytypic traits by differentiating cells. VI. Behaviour of the progeny of a single chondrocyte. J. Exp. Med. 130, 417.

    Article  PubMed  CAS  Google Scholar 

  34. REESE, C.A. and MAYNE, R. (1981). Minor collagen of chicken hyaline cartilage. Biochemistry, 20, 5443.

    Article  PubMed  CAS  Google Scholar 

  35. TOWBIN, H., STAEHELIN, T. and GORDON, J. (1979). Electropho-retic transfer of proteins from Polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. USA, 76, 4350.

    Article  PubMed  CAS  Google Scholar 

  36. BAKER, J.R. and CATERSON, B. (1979). The isolation and characterization of the link proteins from proteoglycan aggregates of bovine nasal cartilage. J. Biol. Chem., 254, 2387.

    PubMed  CAS  Google Scholar 

  37. TANG, L. H., ROSENBERG, L., REINER, A., POOLE, A.R. (1979). Proteoglycans from bovine nasal cartilage. Properties of a soluble form of link protein. J. Biol. Chem., 254, 10523.

    PubMed  CAS  Google Scholar 

  38. DESSAU, W., SASSE, J., TIMPL, R., JILEK, F. and VON DER MARK, K. (1978). Synthesis and extracellular deposition of fibro-nectin in chondrocyte cultures. J. Cell Biol., 79, 342.

    Article  PubMed  CAS  Google Scholar 

  39. UPHOLT, W.B., VERTEL, B.M. and DORFMAN, A. (1979). Translation and characterization of mRNAs in differentiation of chicken cartilage. Proc. Natl Acad. Sci. USA, 76, 4847.

    Article  PubMed  CAS  Google Scholar 

  40. CHEAH, K.S.E., GRANT, M.E. and JACKSON, D.S. (1979). Translation of Type II procollagen mRNA and hydroxylation of the cell-free product. Biochem. Biophys. Res. Commun. 91, 1025.

    Article  PubMed  CAS  Google Scholar 

  41. PAGLIA, L.M., WIESTNER, M., DUCHENE, M., QUELLETTE, L.A., HORLEIN, D., MARTIN, G.R. and MULLER, P.K. (1981). Effects of procollagen peptides on the translation of Type II collagen mRNA and on collagen biosynthesis in chondrocytes. Biochemistry 20, 3523.

    Article  PubMed  CAS  Google Scholar 

  42. PAWLOWSKI, P.J., BRIERLEY, G.T. and LUKENS, L.N. (1981). Changes in the Type II and Type I collagen messenger RNA population during growth of chondrocytes in 5-bromo-2-deoxy-uridine. J. Biol. Chem. 256, 7695.

    PubMed  CAS  Google Scholar 

  43. YOSHIMURA, M., JIMENEZ, S.A. and KAJI, A. (1981). Effects of viral transformation on synthesis and secretion of collagen and fibronectin-like molecules by embryonic chick chondrocytes in culture. J. Biol. Chem., 256, 9111.

    PubMed  CAS  Google Scholar 

  44. HOWARD, B.H., ADAMS, S.L., SOBEL, M.E., PASTAN, I. and DE CROMBRUGGHE, B. (1978). Decreased levels of collagen mRNA in Rous sarcoma virus-transformed chick embryo fibroblasts. J. Biol. Chem., 253, 5869.

    PubMed  CAS  Google Scholar 

  45. FAGAN, J.B., SOBEL, M.E., YAMADA, K.M., DE CROMBRUGGHE, B. and PASTAN, I. (1981). Effects of transformation on fibro-nectin gene expression using cloned fibronectin cDNA. J. Biol. Chem., 256, 520.

    PubMed  CAS  Google Scholar 

  46. HYNES, R.O. (1976). Cell surface proteins and malignant transformation. Biochim. Biophys. Acta, 458, 73.

    PubMed  CAS  Google Scholar 

  47. VERTEL, B.M. and DORMAN, A. (1979). Simultaneous localization of Type II collagen and core protein of chondroitin sulphate proteoglycan in individual chondrocytes. Proc. Natl Acad. Sci. USA, 76, 1261.

    Article  PubMed  CAS  Google Scholar 

  48. KITAMURA, K. and YAMAGATA, T. (1976). The occurrence of a new type of proteochondroitin sulphate in the developing chick embryo. FEBS Lett., 71, 337.

    Article  PubMed  CAS  Google Scholar 

  49. DURBAN, E.M. and BOETTIGER, D. (1980). Progenitor-cell populations can be infected by RNA tumour viruses, but transformation is dependent on the expression of specific differentiated functions. Cold Spring Harbor Symposium on Quant. Biol., 44, 1249.

    Article  Google Scholar 

  50. GAZZOLO, L., SAMARUT, J., BOUABDELLI, M. and BLANCKET, J.P. (1980). Early precursors in the eythroid lineage are the specific target cells of avian erythroblastosis virus in vitro. Cell, 22, 683.

    Article  PubMed  CAS  Google Scholar 

  51. ABBOTT, J. and HOLTZER, H. (1968). The loss of phenotypic traits by differentiated cells. V. The effect of 5-bromode-oxyuridine on cloned chondrocytes. Proc. Natl Acad. Sci. USA, 59, 1144.

    Article  PubMed  CAS  Google Scholar 

  52. SCHILTZ, J.R., MAYNE, R. and HOLTZER, H. (1973). The synthesis of collagen and glycosaminoglycans by dedifferentiated chon-droblasts in culture. Differentiation, 1, 97.

    Article  CAS  Google Scholar 

  53. MAYNE, R., VAIL, M.S. and MILLER, E.J. (1975). Analysis of changes in collagen biosynthesis that occur when chick chondrocytes are grown in 5-bromo-2′-deoxyurdine. Proc. Natl. Acad. Sci. USA, 72, 4511.

    Article  PubMed  CAS  Google Scholar 

  54. PACIFICI, M. and HOLTZER, H. (1977) Effects of tumour-promoting agents on chondrogenesis. Am. J. Anat., 150, 207.

    Article  PubMed  CAS  Google Scholar 

  55. TOLSTOSHEV, P., HABER, R., TRAPNELL, B.C. and CRYSTAL, R.G. (1981). Procollagen mRNA levels, activity and collagen synthesis during the fetal development of sheep lung, tendon, and skin. J. Biol. Chem. 256, 9672.

    PubMed  CAS  Google Scholar 

  56. PAGLIA, L., WILCZEK, J., DIAZ DE LEON, L., MARTIN, G.R., HORLEIN, D. and MULLER, P. (1979). Inhibition of procollagen cell-free synthesis by aminoterminal extension peptides. Biochemistry, 18, 5030.

    Article  PubMed  CAS  Google Scholar 

  57. WIESTNER, M., KRIEG, T., HORLEIN, D., GLANVILLE, R.W., FIETZEK, P. and MULLER, P.K. (1979). Inhibiting effect of procollagen peptides on collagen biosynthesis in fibroblast cultures. J. Biol. Chem. 254, 7016.

    PubMed  CAS  Google Scholar 

  58. HORLEIN, D., MCPHERSON, J., GOH, S.H. and BORNSTEIN, P. (1981). Regulation of protein synthesis: translational control by procollagen-derived fragments. Proc. Natl. Acad. Sci. USA, 78, 6163.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Anatomy, Human Genetics and Microbiology School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, 19104, USA

    M. Pacifici, S. L. Adams, H. Holtzer & D. Boettiger

Authors
  1. M. Pacifici
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. L. Adams
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Holtzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. Boettiger
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Aarhus University, Aarhus, Denmark

    J. E. Celis

  2. EMBL Laboratory, Heidelberg, Federal Republic of Germany

    R. Bravo

Rights and permissions

Reprints and permissions

Copyright information

© 1983 Plenum Press, New York

About this chapter

Cite this chapter

Pacifici, M., Adams, S.L., Holtzer, H., Boettiger, D. (1983). The Reversible Modulation of the Synthesis of Matrix Components in Definitive Chondroblasts Transformed by a ts-Rous Sarcoma Virus Mutant. In: Celis, J.E., Bravo, R. (eds) Gene Expression in Normal and Transformed Cells. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-4541-1_15

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-4541-1_15

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-4543-5

  • Online ISBN: 978-1-4684-4541-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation