Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1984 May;3(5):921–928. doi: 10.1002/j.1460-2075.1984.tb01908.x

The c-sis gene encodes a precursor of the B chain of platelet-derived growth factor.

A Johnsson, C H Heldin, A Wasteson, B Westermark, T F Deuel, J S Huang, P H Seeburg, A Gray, A Ullrich, G Scrace, et al.
PMCID: PMC557452  PMID: 6329745

Abstract

The relationship between platelet-derived growth factor (PDGF) and the proto-oncogene c-sis has been determined by amino acid sequence analysis of PDGF and nucleotide sequence analysis of c-sis genomic clones. The nucleotide sequences of five regions of the human c-sis gene which are homologous to sequences of the transforming region (v-sis) of simian sarcoma virus (SSV) were determined. By alignment of the c-sis and v-sis nucleotide sequences the predicted amino acid sequence of a polypeptide homologous to the putative transforming protein p28sis of SSV was deduced. Both predicted sequences use the same termination codon and additional coding sequences may lie 5' to the homologous regions. Amino acid sequence analysis of the PDGF B chain shows identity to the amino acid sequence predicted from the c-sis sequences over 109 amino acid residues. Polymorphism may exist at two amino acid residues. These results suggest that c-sis encodes a polypeptide precursor of the B chain. A partial amino acid sequence of the PDGF A chain is also described. This chain is 60% homologous to the B chain and cannot be encoded by that part of c-sis which has been sequenced but could be encoded by sequences which lie 5' to the five regions of v-sis homology in c-sis, or at a separate locus.

Full text

PDF
921

Images in this article

924Fig. 2.
on p.924

Selected References

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

  1. Antoniades H. N. Human platelet-derived growth factor (PDGF): purification of PDGF-I and PDGF-II and separation of their reduced subunits. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7314–7317. doi: 10.1073/pnas.78.12.7314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Antoniades H. N., Hunkapiller M. W. Human platelet-derived growth factor (PDGF): amino-terminal amino acid sequence. Science. 1983 May 27;220(4600):963–965. doi: 10.1126/science.6844921. [DOI] [PubMed] [Google Scholar]
  3. Betsholtz C., Heldin C. H., Nister M., Ek B., Wasteson A., Westermark B. Synthesis of a PDGF-like growth factor in human glioma and sarcoma cells suggests the expression of the cellular homologue to the transforming protein of simian sarcoma virus. Biochem Biophys Res Commun. 1983 Nov 30;117(1):176–182. doi: 10.1016/0006-291x(83)91557-7. [DOI] [PubMed] [Google Scholar]
  4. Blobel G., Dobberstein B. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol. 1975 Dec;67(3):835–851. doi: 10.1083/jcb.67.3.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bourne H. R., Rozengurt E. An 18,000 molecular weight polypeptide induces early events and stimulates DNA synthesis in cultured cells. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4555–4559. doi: 10.1073/pnas.73.12.4555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bürk R. R. Induction of cell proliferation by a migration factor released from a transformed cell line. Exp Cell Res. 1976 Sep;101(2):293–298. doi: 10.1016/0014-4827(76)90380-3. [DOI] [PubMed] [Google Scholar]
  7. Dalla-Favera R., Gallo R. C., Giallongo A., Croce C. M. Chromosomal localization of the human homolog (c-sis) of the simian sarcoma virus onc gene. Science. 1982 Nov 12;218(4573):686–688. doi: 10.1126/science.6291150. [DOI] [PubMed] [Google Scholar]
  8. Dalla-Favera R., Gelmann E. P., Gallo R. C., Wong-Staal F. A human onc gene homologous to the transforming gene (v-sis) of simian sarcoma virus. Nature. 1981 Jul 2;292(5818):31–35. doi: 10.1038/292031a0. [DOI] [PubMed] [Google Scholar]
  9. Deuel T. F., Huang J. S., Huang S. S., Stroobant P., Waterfield M. D. Expression of a platelet-derived growth factor-like protein in simian sarcoma virus transformed cells. Science. 1983 Sep 30;221(4618):1348–1350. doi: 10.1126/science.6310754. [DOI] [PubMed] [Google Scholar]
  10. Deuel T. F., Huang J. S. Platelet-derived growth factor: purification, properties, and biological activities. Prog Hematol. 1983;13:201–221. [PubMed] [Google Scholar]
  11. Deuel T. F., Huang J. S., Proffitt R. T., Baenziger J. U., Chang D., Kennedy B. B. Human platelet-derived growth factor. Purification and resolution into two active protein fractions. J Biol Chem. 1981 Sep 10;256(17):8896–8899. [PubMed] [Google Scholar]
  12. Devare S. G., Reddy E. P., Law J. D., Robbins K. C., Aaronson S. A. Nucleotide sequence of the simian sarcoma virus genome: demonstration that its acquired cellular sequences encode the transforming gene product p28sis. Proc Natl Acad Sci U S A. 1983 Feb;80(3):731–735. doi: 10.1073/pnas.80.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dicker P., Pohjanpelto P., Pettican P., Rozengurt E. Similarities between fibroblast-derived growth factor and platelet-derived growth factor. Exp Cell Res. 1981 Sep;135(1):221–227. doi: 10.1016/0014-4827(81)90314-1. [DOI] [PubMed] [Google Scholar]
  14. Doolittle R. F., Hunkapiller M. W., Hood L. E., Devare S. G., Robbins K. C., Aaronson S. A., Antoniades H. N. Simian sarcoma virus onc gene, v-sis, is derived from the gene (or genes) encoding a platelet-derived growth factor. Science. 1983 Jul 15;221(4607):275–277. doi: 10.1126/science.6304883. [DOI] [PubMed] [Google Scholar]
  15. Eva A., Robbins K. C., Andersen P. R., Srinivasan A., Tronick S. R., Reddy E. P., Ellmore N. W., Galen A. T., Lautenberger J. A., Papas T. S. Cellular genes analogous to retroviral onc genes are transcribed in human tumour cells. Nature. 1982 Jan 14;295(5845):116–119. doi: 10.1038/295116a0. [DOI] [PubMed] [Google Scholar]
  16. Heldin C. H., Westermark B., Wasteson A. Chemical and biological properties of a growth factor from human-cultured osteosarcoma cells: resemblance with platelet-derived growth factor. J Cell Physiol. 1980 Nov;105(2):235–246. doi: 10.1002/jcp.1041050207. [DOI] [PubMed] [Google Scholar]
  17. Heldin C. H., Westermark B., Wasteson A. Platelet-derived growth factor. Isolation by a large-scale procedure and analysis of subunit composition. Biochem J. 1981 Mar 1;193(3):907–913. doi: 10.1042/bj1930907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Heldin C. H., Westermark B., Wasteson A. Platelet-derived growth factor: purification and partial characterization. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3722–3726. doi: 10.1073/pnas.76.8.3722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hewick R. M., Hunkapiller M. W., Hood L. E., Dreyer W. J. A gas-liquid solid phase peptide and protein sequenator. J Biol Chem. 1981 Aug 10;256(15):7990–7997. [PubMed] [Google Scholar]
  20. Johnsson A., Heldin C. H., Westermark B., Wasteson A. Platelet-derived growth factor: identification of constituent polypeptide chains. Biochem Biophys Res Commun. 1982 Jan 15;104(1):66–74. doi: 10.1016/0006-291x(82)91941-6. [DOI] [PubMed] [Google Scholar]
  21. Josephs S. F., Dalla-Favera R., Gelmann E. P., Gallo R. C., Wong-Staal F. 5' viral and human cellular sequences corresponding to the transforming gene of simian sarcoma virus. Science. 1983 Feb 4;219(4584):503–505. doi: 10.1126/science.6297002. [DOI] [PubMed] [Google Scholar]
  22. Josephs S. F., Guo C., Ratner L., Wong-Staal F. Human-proto-oncogene nucleotide sequences corresponding to the transforming region of simian sarcoma virus. Science. 1984 Feb 3;223(4635):487–491. doi: 10.1126/science.6318322. [DOI] [PubMed] [Google Scholar]
  23. Morrissey J. H. Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem. 1981 Nov 1;117(2):307–310. doi: 10.1016/0003-2697(81)90783-1. [DOI] [PubMed] [Google Scholar]
  24. Nistér M., Heldin C. H., Wasteson A., Westermark B. A glioma-derived analog to platelet-derived growth factor: demonstration of receptor competing activity and immunological crossreactivity. Proc Natl Acad Sci U S A. 1984 Feb;81(3):926–930. doi: 10.1073/pnas.81.3.926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Raines E. W., Ross R. Platelet-derived growth factor. I. High yield purification and evidence for multiple forms. J Biol Chem. 1982 May 10;257(9):5154–5160. [PubMed] [Google Scholar]
  26. Robbins K. C., Antoniades H. N., Devare S. G., Hunkapiller M. W., Aaronson S. A. Structural and immunological similarities between simian sarcoma virus gene product(s) and human platelet-derived growth factor. Nature. 1983 Oct 13;305(5935):605–608. doi: 10.1038/305605a0. [DOI] [PubMed] [Google Scholar]
  27. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Skehel J. J., Waterfield M. D. Studies on the primary structure of the influenza virus hemagglutinin. Proc Natl Acad Sci U S A. 1975 Jan;72(1):93–97. doi: 10.1073/pnas.72.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Swan D. C., McBride O. W., Robbins K. C., Keithley D. A., Reddy E. P., Aaronson S. A. Chromosomal mapping of the simian sarcoma virus onc gene analogue in human cells. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4691–4695. doi: 10.1073/pnas.79.15.4691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ui N. Rapid estimation of the molecular weights of protein polypeptide chains using high-pressure liquid chromatography in 6 M guanidine hydrochloride. Anal Biochem. 1979 Aug;97(1):65–71. doi: 10.1016/0003-2697(79)90328-2. [DOI] [PubMed] [Google Scholar]
  31. Ullrich A., Berman C. H., Dull T. J., Gray A., Lee J. M. Isolation of the human insulin-like growth factor I gene using a single synthetic DNA probe. EMBO J. 1984 Feb;3(2):361–364. doi: 10.1002/j.1460-2075.1984.tb01812.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Waterfield M. D., Scrace G. T., Whittle N., Stroobant P., Johnsson A., Wasteson A., Westermark B., Heldin C. H., Huang J. S., Deuel T. F. Platelet-derived growth factor is structurally related to the putative transforming protein p28sis of simian sarcoma virus. Nature. 1983 Jul 7;304(5921):35–39. doi: 10.1038/304035a0. [DOI] [PubMed] [Google Scholar]
  33. Westermark B., Wasteson A. The response of cultured human normal glial cells to growth factors. Adv Metab Disord. 1975;8:85–100. doi: 10.1016/b978-0-12-027308-9.50012-3. [DOI] [PubMed] [Google Scholar]
  34. Wong-Staal F., Dalla-Favera R., Franchini G., Gelmann E. P., Gallo R. C. Three distinct genes in human DNA related to the transforming genes of mammalian sarcoma retroviruses. Science. 1981 Jul 10;213(4504):226–228. doi: 10.1126/science.6264598. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES