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. 1988 Oct;7(10):2977–2982. doi: 10.1002/j.1460-2075.1988.tb03160.x

Tenascin: cDNA cloning and induction by TGF-beta.

C A Pearson 1, D Pearson 1, S Shibahara 1, J Hofsteenge 1, R Chiquet-Ehrismann 1
PMCID: PMC454679  PMID: 2460335

Abstract

cDNA clones coding for tenascin, an extracellular matrix glycoprotein with a restricted tissue distribution, were isolated from a chicken fibroblast cDNA expression library using a specific tenascin antiserum. Antibodies eluted from the cDNA-encoded fusion proteins reacted exclusively with tenascin. Limited trypsin treatment of purified tenascin resulted in a peptide which confirmed the deduced protein sequences. The largest clone encoding 632 amino acids showed a cysteine-rich region containing 13 consecutive epidermal growth factor-like repeats of unusual uniformity. Northern blot analysis revealed 8- to 9-kb messages. Tenascin is shown to be induced in vitro by fetal calf serum as well as by transforming growth factor beta (TGF-beta). A 4-fold increase in tenascin secretion by chick embryo fibroblasts was seen after TGF-beta treatment. The induction of tenascin protein synthesis was preceded by an increase of tenascin mRNA as determined by Northern blot analysis. The induction of tenascin was compared with fibronectin. The accumulation of the two extracellular matrix proteins in the medium was differentially affected by fetal calf serum and TGF-beta and the increase was in both cases higher for tenascin.

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Selected References

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

  1. Appella E., Weber I. T., Blasi F. Structure and function of epidermal growth factor-like regions in proteins. FEBS Lett. 1988 Apr 11;231(1):1–4. doi: 10.1016/0014-5793(88)80690-2. [DOI] [PubMed] [Google Scholar]
  2. Aufderheide E., Chiquet-Ehrismann R., Ekblom P. Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme. J Cell Biol. 1987 Jul;105(1):599–608. doi: 10.1083/jcb.105.1.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bourdon M. A., Matthews T. J., Pizzo S. V., Bigner D. D. Immunochemical and biochemical characterization of a glioma-associated extracellular matrix glycoprotein. J Cell Biochem. 1985;28(3):183–195. doi: 10.1002/jcb.240280302. [DOI] [PubMed] [Google Scholar]
  4. Bourdon M. A., Wikstrand C. J., Furthmayr H., Matthews T. J., Bigner D. D. Human glioma-mesenchymal extracellular matrix antigen defined by monoclonal antibody. Cancer Res. 1983 Jun;43(6):2796–2805. [PubMed] [Google Scholar]
  5. Carpenter G., Cohen S. Epidermal growth factor. Annu Rev Biochem. 1979;48:193–216. doi: 10.1146/annurev.bi.48.070179.001205. [DOI] [PubMed] [Google Scholar]
  6. Childs C. B., Proper J. A., Tucker R. F., Moses H. L. Serum contains a platelet-derived transforming growth factor. Proc Natl Acad Sci U S A. 1982 Sep;79(17):5312–5316. doi: 10.1073/pnas.79.17.5312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chiquet-Ehrismann R., Kalla P., Pearson C. A., Beck K., Chiquet M. Tenascin interferes with fibronectin action. Cell. 1988 May 6;53(3):383–390. doi: 10.1016/0092-8674(88)90158-4. [DOI] [PubMed] [Google Scholar]
  8. Chiquet-Ehrismann R., Mackie E. J., Pearson C. A., Sakakura T. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell. 1986 Oct 10;47(1):131–139. doi: 10.1016/0092-8674(86)90374-0. [DOI] [PubMed] [Google Scholar]
  9. Chiquet M., Fambrough D. M. Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol. 1984 Jun;98(6):1926–1936. doi: 10.1083/jcb.98.6.1926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chiquet M., Fambrough D. M. Chick myotendinous antigen. II. A novel extracellular glycoprotein complex consisting of large disulfide-linked subunits. J Cell Biol. 1984 Jun;98(6):1937–1946. doi: 10.1083/jcb.98.6.1937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  13. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ehrismann R., Chiquet M., Turner D. C. Mode of action of fibronectin in promoting chicken myoblast attachment. Mr = 60,000 gelatin-binding fragment binds native fibronectin. J Biol Chem. 1981 Apr 25;256(8):4056–4062. [PubMed] [Google Scholar]
  15. Endo T., Nakanishi M., Furukawa S., Joubert F. J., Tamiya N., Hayashi K. Stopped-flow fluorescence studies on binding kinetics of neurotoxins with acetylcholine receptor. Biochemistry. 1986 Jan 28;25(2):395–404. doi: 10.1021/bi00350a019. [DOI] [PubMed] [Google Scholar]
  16. Engvall E. Enzyme immunoassay ELISA and EMIT. Methods Enzymol. 1980;70(A):419–439. doi: 10.1016/s0076-6879(80)70067-8. [DOI] [PubMed] [Google Scholar]
  17. Erickson H. P., Inglesias J. L. A six-armed oligomer isolated from cell surface fibronectin preparations. Nature. 1984 Sep 20;311(5983):267–269. doi: 10.1038/311267a0. [DOI] [PubMed] [Google Scholar]
  18. Erickson H. P., Taylor H. C. Hexabrachion proteins in embryonic chicken tissues and human tumors. J Cell Biol. 1987 Sep;105(3):1387–1394. doi: 10.1083/jcb.105.3.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Faissner A., Kruse J., Chiquet-Ehrismann R., Mackie E. The high-molecular-weight J1 glycoproteins are immunochemically related to tenascin. Differentiation. 1988;37(2):104–114. doi: 10.1111/j.1432-0436.1988.tb00802.x. [DOI] [PubMed] [Google Scholar]
  20. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  21. Grumet M., Hoffman S., Crossin K. L., Edelman G. M. Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8075–8079. doi: 10.1073/pnas.82.23.8075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Heine U., Munoz E. F., Flanders K. C., Ellingsworth L. R., Lam H. Y., Thompson N. L., Roberts A. B., Sporn M. B. Role of transforming growth factor-beta in the development of the mouse embryo. J Cell Biol. 1987 Dec;105(6 Pt 2):2861–2876. doi: 10.1083/jcb.105.6.2861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hoffman S., Crossin K. L., Edelman G. M. Molecular forms, binding functions, and developmental expression patterns of cytotactin and cytotactin-binding proteoglycan, an interactive pair of extracellular matrix molecules. J Cell Biol. 1988 Feb;106(2):519–532. doi: 10.1083/jcb.106.2.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hofsteenge J., Stone S. R. The effect of thrombomodulin on the cleavage of fibrinogen and fibrinogen fragments by thrombin. Eur J Biochem. 1987 Oct 1;168(1):49–56. doi: 10.1111/j.1432-1033.1987.tb13385.x. [DOI] [PubMed] [Google Scholar]
  25. Hursh D. A., Andrews M. E., Raff R. A. A sea urchin gene encodes a polypeptide homologous to epidermal growth factor. Science. 1987 Sep 18;237(4821):1487–1490. doi: 10.1126/science.3498216. [DOI] [PubMed] [Google Scholar]
  26. Ignotz R. A., Endo T., Massagué J. Regulation of fibronectin and type I collagen mRNA levels by transforming growth factor-beta. J Biol Chem. 1987 May 15;262(14):6443–6446. [PubMed] [Google Scholar]
  27. Ignotz R. A., Massagué J. Cell adhesion protein receptors as targets for transforming growth factor-beta action. Cell. 1987 Oct 23;51(2):189–197. doi: 10.1016/0092-8674(87)90146-2. [DOI] [PubMed] [Google Scholar]
  28. Ignotz R. A., Massagué J. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J Biol Chem. 1986 Mar 25;261(9):4337–4345. [PubMed] [Google Scholar]
  29. Jones F. S., Burgoon M. P., Hoffman S., Crossin K. L., Cunningham B. A., Edelman G. M. A cDNA clone for cytotactin contains sequences similar to epidermal growth factor-like repeats and segments of fibronectin and fibrinogen. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2186–2190. doi: 10.1073/pnas.85.7.2186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kornblihtt A. R., Umezawa K., Vibe-Pedersen K., Baralle F. E. Primary structure of human fibronectin: differential splicing may generate at least 10 polypeptides from a single gene. EMBO J. 1985 Jul;4(7):1755–1759. doi: 10.1002/j.1460-2075.1985.tb03847.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kruse J., Keilhauer G., Faissner A., Timpl R., Schachner M. The J1 glycoprotein--a novel nervous system cell adhesion molecule of the L2/HNK-1 family. Nature. 1985 Jul 11;316(6024):146–148. doi: 10.1038/316146a0. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Lewis S. A., Villasante A., Sherline P., Cowan N. J. Brain-specific expression of MAP2 detected using a cloned cDNA probe. J Cell Biol. 1986 Jun;102(6):2098–2105. doi: 10.1083/jcb.102.6.2098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
  35. Lizardi P. M., Engelberg A. Rapid isolation of RNA using proteinase K and sodium perchlorate. Anal Biochem. 1979 Sep 15;98(1):116–122. doi: 10.1016/0003-2697(79)90714-0. [DOI] [PubMed] [Google Scholar]
  36. Mackie E. J., Thesleff I., Chiquet-Ehrismann R. Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol. 1987 Dec;105(6 Pt 1):2569–2579. doi: 10.1083/jcb.105.6.2569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Mercola M., Stiles C. D. Growth factor superfamilies and mammalian embryogenesis. Development. 1988 Mar;102(3):451–460. doi: 10.1242/dev.102.3.451. [DOI] [PubMed] [Google Scholar]
  38. Mustoe T. A., Pierce G. F., Thomason A., Gramates P., Sporn M. B., Deuel T. F. Accelerated healing of incisional wounds in rats induced by transforming growth factor-beta. Science. 1987 Sep 11;237(4820):1333–1336. doi: 10.1126/science.2442813. [DOI] [PubMed] [Google Scholar]
  39. Padgett R. A., Grabowski P. J., Konarska M. M., Seiler S., Sharp P. A. Splicing of messenger RNA precursors. Annu Rev Biochem. 1986;55:1119–1150. doi: 10.1146/annurev.bi.55.070186.005351. [DOI] [PubMed] [Google Scholar]
  40. Penttinen R. P., Kobayashi S., Bornstein P. Transforming growth factor beta increases mRNA for matrix proteins both in the presence and in the absence of changes in mRNA stability. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1105–1108. doi: 10.1073/pnas.85.4.1105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rossi P., Karsenty G., Roberts A. B., Roche N. S., Sporn M. B., de Crombrugghe B. A nuclear factor 1 binding site mediates the transcriptional activation of a type I collagen promoter by transforming growth factor-beta. Cell. 1988 Feb 12;52(3):405–414. doi: 10.1016/s0092-8674(88)80033-3. [DOI] [PubMed] [Google Scholar]
  42. Sasaki M., Kato S., Kohno K., Martin G. R., Yamada Y. Sequence of the cDNA encoding the laminin B1 chain reveals a multidomain protein containing cysteine-rich repeats. Proc Natl Acad Sci U S A. 1987 Feb;84(4):935–939. doi: 10.1073/pnas.84.4.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Seyedin S. M., Segarini P. R., Rosen D. M., Thompson A. Y., Bentz H., Graycar J. Cartilage-inducing factor-B is a unique protein structurally and functionally related to transforming growth factor-beta. J Biol Chem. 1987 Feb 15;262(5):1946–1949. [PubMed] [Google Scholar]
  44. Shibahara S., Müller R., Taguchi H., Yoshida T. Cloning and expression of cDNA for rat heme oxygenase. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7865–7869. doi: 10.1073/pnas.82.23.7865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sidman K. E., George D. G., Barker W. C., Hunt L. T. The protein identification resource (PIR). Nucleic Acids Res. 1988 Mar 11;16(5):1869–1871. doi: 10.1093/nar/16.5.1869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sporn M. B., Roberts A. B., Wakefield L. M., de Crombrugghe B. Some recent advances in the chemistry and biology of transforming growth factor-beta. J Cell Biol. 1987 Sep;105(3):1039–1045. doi: 10.1083/jcb.105.3.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Takanami M. RNA polymerase nascent product analysis. Methods Enzymol. 1980;65(1):497–499. doi: 10.1016/s0076-6879(80)65058-7. [DOI] [PubMed] [Google Scholar]
  48. Thesleff I., Mackie E., Vainio S., Chiquet-Ehrismann R. Changes in the distribution of tenascin during tooth development. Development. 1987 Oct;101(2):289–296. doi: 10.1242/dev.101.2.289. [DOI] [PubMed] [Google Scholar]
  49. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Vaughan L., Huber S., Chiquet M., Winterhalter K. H. A major, six-armed glycoprotein from embryonic cartilage. EMBO J. 1987 Feb;6(2):349–353. doi: 10.1002/j.1460-2075.1987.tb04761.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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