Abstract
We used a subclone of a rabbit genomic clone for collagenase that cross-hybridizes with human synovial cell messenger RNA (mRNA) to identify a human collagenase complementary DNA (cDNA) clone. The human cDNA clone is 2.1 kilobases (kb) and selects a mRNA transcript of approximately the same size from primary cultures of rheumatoid synovial cells that produce collagenase, but no mRNA is selected from control (nonproducing) synovial fibroblasts. Restriction enzyme analysis and DNA sequence data indicate that our cDNA clone is full length and that it is identical to that recently described for human skin fibroblast collagenase. The cDNA clone identified a single collagenase gene of approximately 17 kb from blots of human genomic DNA. The identity of human skin and synovial cell collagenase and the ubiquity of this enzyme and of its substrates, the interstitial collagens types I, II, and III, imply that common mechanisms controlling collagenolysis throughout the human body may be operative in both normal and disease states.
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- Aldridge J., Kunkel L., Bruns G., Tantravahi U., Lalande M., Brewster T., Moreau E., Wilson M., Bromley W., Roderick T. A strategy to reveal high-frequency RFLPs along the human X chromosome. Am J Hum Genet. 1984 May;36(3):546–564. [PMC free article] [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]
- Bauer E. A., Seltzer J. L., Eisen A. Z. Inhibition of collagen degradative enzymes by retinoic acid in vitro. J Am Acad Dermatol. 1982 Apr;6(4 Pt 2 Suppl):603–607. doi: 10.1016/s0190-9622(82)70049-0. [DOI] [PubMed] [Google Scholar]
- Brinckerhoff C. E., Benoit M. C., Culp W. J. Autoregulation of collagenase production by a protein synthesized and secreted by synovial fibroblasts: cellular mechanism for control of collagen degradation. Proc Natl Acad Sci U S A. 1985 Apr;82(7):1916–1920. doi: 10.1073/pnas.82.7.1916. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brinckerhoff C. E., Harris E. D., Jr Collagen production by cultures containing multinucleated cells derived from synovial fibroblasts. Arthritis Rheum. 1978 Sep-Oct;21(7):745–753. doi: 10.1002/art.1780210702. [DOI] [PubMed] [Google Scholar]
- Brinckerhoff C. E., Harris E. D., Jr Modulation by retinoic acid and corticosteroids of collagenase production by rabbit synovial fibroblasts treated with phorbol myristate acetate or poly(ethylene glycol). Biochim Biophys Acta. 1981 Nov 5;677(3-4):424–432. doi: 10.1016/0304-4165(81)90256-7. [DOI] [PubMed] [Google Scholar]
- Brinckerhoff C. E., McMillan R. M., Dayer J. M., Harris E. D., Jr Inhibition by retinoic acid of collagenase production in rheumatoid synovial cells. N Engl J Med. 1980 Aug 21;303(8):432–436. doi: 10.1056/NEJM198008213030805. [DOI] [PubMed] [Google Scholar]
- Brinckerhoff C. E., Plucinska I. M., Sheldon L. A., O'Connor G. T. Half-life of synovial cell collagenase mRNA is modulated by phorbol myristate acetate but not by all-trans-retinoic acid or dexamethasone. Biochemistry. 1986 Oct 21;25(21):6378–6384. doi: 10.1021/bi00369a006. [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]
- Dayer J. M., Krane S. M., Russell R. G., Robinson D. R. Production of collagenase and prostaglandins by isolated adherent rheumatoid synovial cells. Proc Natl Acad Sci U S A. 1976 Mar;73(3):945–949. doi: 10.1073/pnas.73.3.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dayer J. M., de Rochemonteix B., Burrus B., Demczuk S., Dinarello C. A. Human recombinant interleukin 1 stimulates collagenase and prostaglandin E2 production by human synovial cells. J Clin Invest. 1986 Feb;77(2):645–648. doi: 10.1172/JCI112350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
- Fini M. E., Austin S. D., Holt P. T., Ruby P. L., Gross R. H., White H. D., Brinckerhoff C. E. Homology between exon-containing portions of rabbit genomic clones for synovial cell collagenase and human foreskin and synovial cell mRNAs. Coll Relat Res. 1986 Jul;6(3):239–248. doi: 10.1016/s0174-173x(86)80009-7. [DOI] [PubMed] [Google Scholar]
- Fyrberg E. A., Mahaffey J. W., Bond B. J., Davidson N. Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell. 1983 May;33(1):115–123. doi: 10.1016/0092-8674(83)90340-9. [DOI] [PubMed] [Google Scholar]
- GLIMCHER M. J., FRANCOIS C. J., RICHARDS L., KRANE S. M. THE PRESENCE OF ORGANIC PHOSPHORUS IN COLLAGENS AND GELATINS. Biochim Biophys Acta. 1964 Dec 9;93:585–602. doi: 10.1016/0304-4165(64)90342-3. [DOI] [PubMed] [Google Scholar]
- Gisslow M. T., McBride B. C. A rapid sensitive collagenase assay. Anal Biochem. 1975 Sep;68(1):70–78. doi: 10.1016/0003-2697(75)90680-6. [DOI] [PubMed] [Google Scholar]
- Goldberg G. I., Wilhelm S. M., Kronberger A., Bauer E. A., Grant G. A., Eisen A. Z. Human fibroblast collagenase. Complete primary structure and homology to an oncogene transformation-induced rat protein. J Biol Chem. 1986 May 15;261(14):6600–6605. [PubMed] [Google Scholar]
- Golub L. M., Lee H. M., Lehrer G., Nemiroff A., McNamara T. F., Kaplan R., Ramamurthy N. S. Minocycline reduces gingival collagenolytic activity during diabetes. Preliminary observations and a proposed new mechanism of action. J Periodontal Res. 1983 Sep;18(5):516–526. doi: 10.1111/j.1600-0765.1983.tb00388.x. [DOI] [PubMed] [Google Scholar]
- Gross R. H. A DNA sequence analysis program for the Apple Macintosh. Nucleic Acids Res. 1986 Jan 10;14(1):591–596. doi: 10.1093/nar/14.1.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
- Harris E. D., Jr, DiBona D. R., Krane S. M. Collagenases in human synovial fluid. J Clin Invest. 1969 Nov;48(11):2104–2113. doi: 10.1172/JCI106177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harris E. D., Jr, Welgus H. G., Krane S. M. Regulation of the mammalian collagenases. Coll Relat Res. 1984 Dec;4(6):493–512. doi: 10.1016/s0174-173x(84)80015-1. [DOI] [PubMed] [Google Scholar]
- Hasselbacher P., McMillan R. M., Vater C. A., Hahn J., Harris E. D., Jr Stimulation of secretion of collagenase and prostaglandin E2 by synovial fibroblasts in response to crystals of monosodium urate monohydrate: a model for joint destruction in gout. Trans Assoc Am Physicians. 1981;94:243–252. [PubMed] [Google Scholar]
- Hasty K. A., Hibbs M. S., Kang A. H., Mainardi C. L. Heterogeneity among human collagenases demonstrated by monoclonal antibody that selectively recognizes and inhibits human neutrophil collagenase. J Exp Med. 1984 May 1;159(5):1455–1463. doi: 10.1084/jem.159.5.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herron G. S., Werb Z., Dwyer K., Banda M. J. Secretion of metalloproteinases by stimulated capillary endothelial cells. I. Production of procollagenase and prostromelysin exceeds expression of proteolytic activity. J Biol Chem. 1986 Feb 25;261(6):2810–2813. [PubMed] [Google Scholar]
- Johnson-Wint B., Gross J. Regulation of connective tissue collagenase production: stimulators from adult and fetal epidermal cells. J Cell Biol. 1984 Jan;98(1):90–96. doi: 10.1083/jcb.98.1.90. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Korn J. H., Brinckerhoff C. E., Edwards R. L. Synthesis of PGE2, collagenase and tissue factor by fibroblast substrains: substrains are differentially activated for different metabolic products. Coll Relat Res. 1985 Nov;5(5):437–447. doi: 10.1016/s0174-173x(85)80031-5. [DOI] [PubMed] [Google Scholar]
- Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 1986 Jan 31;44(2):283–292. doi: 10.1016/0092-8674(86)90762-2. [DOI] [PubMed] [Google Scholar]
- Kronberger A., Valle K. J., Eisen A. Z., Bauer E. A. Enhanced cell-free translation of human skin collagenase in recessive dystrophic epidermolysis bullosa. J Invest Dermatol. 1982 Sep;79(3):208–211. doi: 10.1111/1523-1747.ep12500059. [DOI] [PubMed] [Google Scholar]
- Matrisian L. M., Leroy P., Ruhlmann C., Gesnel M. C., Breathnach R. Isolation of the oncogene and epidermal growth factor-induced transin gene: complex control in rat fibroblasts. Mol Cell Biol. 1986 May;6(5):1679–1686. doi: 10.1128/mcb.6.5.1679. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McCroskery P. A., Arai S., Amento E. P., Krane S. M. Stimulation of procollagenase synthesis in human rheumatoid synovial fibroblasts by mononuclear cell factor/interleukin 1. FEBS Lett. 1985 Oct 21;191(1):7–12. doi: 10.1016/0014-5793(85)80983-2. [DOI] [PubMed] [Google Scholar]
- Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
- Mizel S. B., Dayer J. M., Krane S. M., Mergenhagen S. E. Stimulation of rheumatoid synovial cell collagenase and prostaglandin production by partially purified lymphocyte-activating factor (interleukin 1). Proc Natl Acad Sci U S A. 1981 Apr;78(4):2474–2477. doi: 10.1073/pnas.78.4.2474. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moscatelli D. A., Rifkin D. B., Jaffe E. A. Production of latent collagenase by human umbilical vein endothelial cells in response to angiogenic preparations. Exp Cell Res. 1985 Feb;156(2):379–390. doi: 10.1016/0014-4827(85)90545-2. [DOI] [PubMed] [Google Scholar]
- Okada Y., Nagase H., Harris E. D., Jr A metalloproteinase from human rheumatoid synovial fibroblasts that digests connective tissue matrix components. Purification and characterization. J Biol Chem. 1986 Oct 25;261(30):14245–14255. [PubMed] [Google Scholar]
- Richards R. I., Shine J., Ullrich A., Wells J. R., Goodman H. M. Molecular cloning and sequence analysis of adult chicken betal globin cDNA. Nucleic Acids Res. 1979 Nov 10;7(5):1137–1146. doi: 10.1093/nar/7.5.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roswit W. T., Halme J., Jeffrey J. J. Purification and properties of rat uterine procollagenase. Arch Biochem Biophys. 1983 Aug;225(1):285–295. doi: 10.1016/0003-9861(83)90032-2. [DOI] [PubMed] [Google Scholar]
- Salo T., Liotta L. A., Tryggvason K. Purification and characterization of a murine basement membrane collagen-degrading enzyme secreted by metastatic tumor cells. J Biol Chem. 1983 Mar 10;258(5):3058–3063. [PubMed] [Google Scholar]
- 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]
- Vater C. A., Nagase H., Harris E. D., Jr Proactivator-dependent activation of procollagenase induced by treatment with EGTA. Biochem J. 1986 Aug 1;237(3):853–858. doi: 10.1042/bj2370853. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vater C. A., Nagase H., Harris E. D., Jr Purification of an endogenous activator of procollagenase from rabbit synovial fibroblast culture medium. J Biol Chem. 1983 Aug 10;258(15):9374–9382. [PubMed] [Google Scholar]
- Welgus H. G., Grant G. A., Sacchettini J. C., Roswit W. T., Jeffrey J. J. The gelatinolytic activity of rat uterus collagenase. J Biol Chem. 1985 Nov 5;260(25):13601–13606. [PubMed] [Google Scholar]
- Werb Z., Reynolds J. J. Stimulation by endocytosis of the secretion of collagenase and neutral proteinase from rabbit synovial fibroblasts. J Exp Med. 1974 Dec 1;140(6):1482–1497. doi: 10.1084/jem.140.6.1482. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilhelm S. M., Eisen A. Z., Teter M., Clark S. D., Kronberger A., Goldberg G. Human fibroblast collagenase: glycosylation and tissue-specific levels of enzyme synthesis. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3756–3760. doi: 10.1073/pnas.83.11.3756. [DOI] [PMC free article] [PubMed] [Google Scholar]





