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An Essay on Biological Degradation of Collagen

  • Chapter
Cell Biology of Extracellular Matrix

Abstract

The limitations of language very often tend to confuse concepts. We are intuitively led to believe that the cleavage of a molecule is a “degradative” or catabolic activity. However, enzymatic removal of portions of molecules serves the purpose of activating them if they are enzymes or altering their behavior so that they may now form a highly ordered superstructure, as in the case of the fibrinogen—fibrin conversion or procollagen—collagen transformation in fibril-logenesis. The inactive precursor molecules are “degraded” to shorter sizes that permit their participation in the process for which they were designed. In the case of morphogenesis at the tissue level, total destruction of the extensive collagenous lamellae of the tadpole tail during metamorphosis involves highly synchronized and selective removal of collagen fibrils, the function of this process being to prepare the animal for its transition from an aqueous to a terrestrial environment. On another level during embryonic development, highly localized and in some cases massive programmed death of cells is an important phase of morphogenesis (e.g., limbs and nervous system). From the viewpoint of the dismantled structural or cellular element, it is undergoing degradation, but viewed from the higher level of the tissue or the organism as a whole, the process is merely a phase of essential remodeling to facilitate overall function.

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References

  • Banerjee, S. D., Cohn, R. H., and Bernfield, M. R., 1977, The basal lamina of embryonic salivary epithelium and role in maintaining lobular morphology, J. Cell Biol. 73:445–463.

    Article  Google Scholar 

  • Bauer, E. A., Gordon, J. M., Reddick, M. E., and Eisen, A. Z., 1977, Quantitation and immunocytochemical localization of human skin collagenase in basal cell carcinoma, J. Invest. Dermatol. 69:363–367.

    Article  Google Scholar 

  • Berman, M., and Dohlman, C., 1975, Collagenase inhibitors, Arch. Ophtalmol. 35:95–103.

    Google Scholar 

  • Birkedal-Hansen, H., Cobb, C., Taylor, R., and Fullmer, H., 1976, Activation of fibroblast procollagenase by mast cell proteases, Biochim. Biophys. Acta 438:273–286.

    Google Scholar 

  • Biswas, C., and Dayer, J.-M., 1979, Stimulation of collagenase production by collagen in mammalian cell culture, Cell 18:1035–1041.

    Article  Google Scholar 

  • Biswas, C., Moran, W. B., Bloch, K. J., and Gross, J., 1978, Collagenolytic activity of rabbit V2-carcinoma growing at multiple sites, Biochem. Biophys. Res. Commun. 80:33–38.

    Article  Google Scholar 

  • Bloom, W., and Fawcett, D. W., 1975, A Textbook of Histology, Saunders, Philadelphia.

    Google Scholar 

  • Brinckerhoff, C. E., McMillan, R. M., Fahey, J. C., and Harris, E. D., Jr., 1979, Collagenase production by synovial fibroblasts treated with phorbol myristic acetate, Arthritis Rheum. 22:1109–1116.

    Article  Google Scholar 

  • Brinckerhoff, C. E., McMillan, R. M., Dayer, J.-M., and Harris, E. D., Jr., 1980, Inhibition by retinoic acid of collagenase production in rheumatoid synovial cells, N. Engl. J. Med. 303:432–436.

    Article  Google Scholar 

  • Burleigh, P. M. C., 1977, Degradation of collagen by non-specific proteases, in: Proteinases in Mammalian Cells and Tissues (A. J. Barrett, ed.), pp. 285–309, North-Holland, Amsterdam.

    Google Scholar 

  • Davison, P., and Schmitt, F. O., 1968, The enzymatic dissection of tropocollagen, Hoppe.Seyler’s Z. Physiol. Chem. 349:119–124.

    Article  Google Scholar 

  • Dayer, J.-M., Krane, S. M., Russell, R. G. G., and Robinson, D. R., 1976, Production of collagenase and prostaglandins by isolated adherent rheumatoid synovial cells, Proc. Natl. Acad. Sci. USA 73:945–949.

    Article  Google Scholar 

  • Dayer, J.-M., Russell, R. G. G., and Krane, S. M., 1977, Collagenase production by rheumatoid synovial cells: Stimulation by a human lymphocyte factor, Science 195:181–183.

    Article  Google Scholar 

  • Dayer, J.-M., Goldring, S. R., Robinson, D. R., and Krane, S. M., 1980, Cell-cell interactions and collagenase production, in: Collagenase in Normal and Pathological Connective Tissues (D. E. Woolley and J. M. Evanson, eds,), pp. 83–104, Wiley, New York.

    Google Scholar 

  • Dixit, S. N., Mainardi, C. L., Sever, J. M., and Kang, A. H., 1979, Covalent structure of collagen: Amino acid sequence of α2-CB5 of chick skin collagen containing the animal collagen cleavage site, Biochemistry 18:5416–5422.

    Article  Google Scholar 

  • Dresden, M. H., 1971, Search for products of degradation giving clues to the function of collagenase in vivo, Nature, New Biol. 231:55–57.

    Article  Google Scholar 

  • Eisen, A. Z., and Gross, J., 1965, The role of epithelium and mesenchyme in the production of a collagenolytic enzyme and a hyaluronidase in the anuran tadpole, Dev. Biol. 12:408–418.

    Article  Google Scholar 

  • Engvall, E., and Ruoslahti, E., 1977, Binding of soluble form of fibroblast surface protein, fibronectin to collagen, Int. J. Cancer 20:1–5.

    Article  Google Scholar 

  • Gadek, J. E., Fells, G. A., Wright, D. G., and Crystal, R. G., 1980, Human neutrophil elastase functions as a type III collagen “collagenase”, Biochem. Biophys. Res. Comm. 95:1815–1822.

    Article  Google Scholar 

  • Gimbrone, M. A., Jr., Cotran, R. S., Leapman, S. B., and Folkman, J., 1974, Tumor growth and neovascularization: An experimental model using rabbit cornea, J. Natl. Cancer Inst. 52:413–427.

    Google Scholar 

  • Gordon, J. M., Bauer, E. A., and Eisen, A. Z., 1980, Collagenase in human cornea: Immunologic localization, Arch. Ophthalmol. 98:341–345.

    Google Scholar 

  • Grillo, H. C., and Gross, J., 1967, Collagenolytic activity during mammalian wound repair, Dev. Biol. 15:300–317.

    Article  Google Scholar 

  • Gross, J., 1953, Evaluation of structural and chemical changes in connective tissue, Ann. N.Y. Acad. Sci. 56:674–683.

    Article  Google Scholar 

  • Gross, J., 1964, Thermal denaturation of collagen in the dispersed and solid state, Science 143:960–961.

    Article  Google Scholar 

  • Gross, J., 1969, Some aspects of collagen metabolism, in: Thule International Symposia. Aging of Connective and Skeletal Tissue (A. Engel and T. Larsson, eds.), pp. 33–44, Nordiska Bokhandelns Forlag, Stockholm.

    Google Scholar 

  • Gross, J., 1970, The animal collagenases, in: Chemical and Molecular Biology of the Intercellular Matrix (E. A. Balazs, ed.), pp. 1623–1636, Academic Press, New York.

    Google Scholar 

  • Gross, J., 1974, Collagen biology, structure, degradation and disease, in: The Harvey Lectures Series, Series 86, pp. 351–432, Academic Press, New York.

    Google Scholar 

  • Gross, J., 1976, Aspects of the animal collagenases, in: Biochemistry of Collagen (R. N. Ramachandran and A. H. Reddi, eds.), pp. 275–317, Plenum Press, New York.

    Google Scholar 

  • Gross, J., and Bruschi, A. B., 1971, The pattern of collagen degradation in cultured tadpole tissues, Dev. Biol. 26:36–41.

    Article  Google Scholar 

  • Gross, J., and Lapiere, C. M., 1962, Collagenolytic activity in amphibian tissues: A tissue culture assay, Proc. Natl. Acad. Sci. USA 48:1014–1022.

    Article  Google Scholar 

  • Gross, J., and Nagai, Y., 1965, Specific degradation of the collagen molecule by tadpole collagenolytic enzyme, Biochemistry 54:1197–1204.

    Google Scholar 

  • Gross, J., Highberger, J. H., Johnson-Wint, B., and Biswas, C., 1980, Mode of action and regulation of tissue collagens, in: Collagenase in Normal and Pathological Connective Tissues (D. E. Woolley and J. M. Evanson, eds.), pp. 11–35, Wiley, New York.

    Google Scholar 

  • Gross, J., Azizkhan, R. G., Biswas, C., Bruns, R. R., Hsieh, D. S.-T., and Folkman, J., 1981, Inhibition of tumor growth, vascularization and collagenolysis in the rabbit cornea by medroxyprogesterone, Proc. Natl. Acad. Sci. USA, 78:1176–1180.

    Article  Google Scholar 

  • Harkness, R. D., Marko, A. N., Muir, H. M., and Neuberger, A., 1954, The metabolism of collagen and other proteins of the skin of rabbits, Biochem. J. 56:558–569.

    Google Scholar 

  • Harper, E., and Gross, J., 1972, Collagenase, procollagenase and activator relationships in tadpole tissue culture, Biochem. Biophys. Res. Commun. 48:1147–1153.

    Article  Google Scholar 

  • Harper, E., Bloch, K. J., and Gross, J., 1971, The zymogen of tadpole collagenase, Biochemistry 10:3033–3040.

    Article  Google Scholar 

  • Harris, E. D., Jr., and Cartwright, E. C., 1977, Mammalian collagenases, in: Proteinases in Mammalian Cells and Tissues (A. J. Barrett, ed.), pp. 249–283, North-Holland, Amsterdam.

    Google Scholar 

  • Harris, E. D., Jr., and Farrell, M. E., 1972, Resistance to collagenase: A characteristic of collagen fibrils cross-linked by formaldehyde, Biochim. Biophys. Acta 278:133–141.

    Google Scholar 

  • Harris, E. D., Jr., and Krane, S. M., 1974, Collagenases, N. Engl. J. Med. 291:557–563, 605–609, 652–661.

    Article  Google Scholar 

  • Harris, E. D., Jr., Reynolds, J. J., and Werb, Z., 1975, Cytochalasin B increases collagenase production by cells in vitro, Nature (London) 257:243–244.

    Article  Google Scholar 

  • Horwitz, A. L., Hance, A. J., and Crystal, R. G., 1977, Granulocyte collagenase: Selective digestion of type I relative to type III collagen, Proc. Natl. Acad. Sci. USA 74:897–901.

    Article  Google Scholar 

  • Hashimoto, K., Yamanishi, Y., and Dabbous, M. K., 1972, Electron microscopic observations of collagenolytic activity of basal cell epithelioma of the skin in vivo and in vitro, Cancer Res. 32:2561–2567.

    Google Scholar 

  • Highberger, J. H., Corbett, C., and Gross, J., 1979, Isolation and characterization of a peptide containing the site of the cleavage of the chick skin collagen α1 chain by animal collagenases, Biochem. Biophys. Res. Commun. 89:202–208.

    Article  Google Scholar 

  • Hutchins, G. M., and Sheldon, W. H., 1973, pH of inflammatory exudates in granulocytopenic rabbits, Proc. Soc. Exp. Biol. Med. 14:1014–1017.

    Google Scholar 

  • Jackson, D. S., and Bentley, J. P., 1960, On the significance of the extractable collagens, J. Biophys. Biochem. Cytol. 7:37–42.

    Article  Google Scholar 

  • Jeffrey, J. J., Koob, T. J., and Eisen, A. Z., 1975, Hormonal regulation of mammalian collagenases, in: Dynamics of Connective Tissue Macromolecules (P. M. C. Burleigh and A. R. Poole, eds.), pp. 147–156, North-Holland, Amsterdam.

    Google Scholar 

  • Johnson-Muller, B., and Gross, J., 1978, Regulation of corneal collagenase production: Epithelial-stromal cell interactions, Proc. Natl. Acad. Sci. USA 75:4417–4421.

    Article  Google Scholar 

  • Johnson-Wint, B., 1980, Regulation of stromal cell collagenase production in the adult rabbit cornea. In vitro stimulation and inhibition by epithelial cell products, Proc. Natl. Acad. Sci. USA 77:5331–5335.

    Article  Google Scholar 

  • Koob, T. J., and Jeffrey, J. J., 1974, Hormonal regulation of collagen degradation in the uterus: Inhibition of collagenase expression by progesterone and cyclic AMP, Biochim. Biophys. Acta 354:61–70.

    Google Scholar 

  • Kuboki, Y., Shimokawa, H., Ono, T., and Sasaki, S., 1973, Detection of collagen degradation products in bone, Calcif. Tissue Res. 12:303–312.

    Article  Google Scholar 

  • Lapiere, C. M., and Gross, J., 1963, Animal collagenase and collagen metabolism, in: Mechanisms of Hard Tissue Destruction (R. F. Sognnaes, ed.), pp. 663–694, American Association for the Advancement of Science, Washington, D. C.

    Google Scholar 

  • Lapiere, C. M., Bruschi, A., Tanzer, M. L., and Gross, J., 1964, Metabolic behavior of the collagen in steady state and in remodelling tissues, in: Proceedings of the Second European Symposium on Calcified Tissues, Liege, Belgium, pp. 275–284.

    Google Scholar 

  • Leibovich, S. J., and Weiss, J. B., 1971, Failure of human rheumatoid synovial collagenase to degrade either normal or rheumatoid arthritis polymeric collagen, Biochim. Biophys. Acta 251:109–118.

    Google Scholar 

  • Linsenmayer, T. F., and Toole, B. P., 1977, Biosynthesis of different collagens and glycosaminoglycans during limb development, in: Morphogenesis and Malformations of the Limb (D. Bergsma and W. Lenz, eds.), pp. 19–35, Liss, New York.

    Google Scholar 

  • Liotta, L. A., Abe, S., Robey, P. G., and Martin, G. R., 1979, Preferential digestion of basement membrane collagen by an enzyme derived from a metastatic murine tumor, Proc. Natl. Acad. Sci. USA 76:2268–2272.

    Article  Google Scholar 

  • Liotta, L. A., Tryggvason, K., Garbisa, S., Hart, I., Foltz, C. M., and Shafie, S., 1980, Metastatic potential correlates with enzymatic degradation of basement membrane collagens, Nature (London) 284:67–68.

    Article  Google Scholar 

  • Liotta, L. A., Tryggvason, K., Garbisa, S., Robey, P. G., and Abe, S., 1981a, Partial purification and characterization of a neutral protease which cleaves type IV collagen, Biochemistry 20:100–104.

    Article  Google Scholar 

  • Liotta, L. A., Lauzer, W. L., and Garbisa, S., 1981b, Identification of a type V specific collagenolytic enzyme. Biochem. Biophys. Res. Comm. 98:184–190.

    Article  Google Scholar 

  • McCroskery, P. A., Wood, S., and Harris, E. D., Jr., 1973, Gelatin: A poor substrate for a mammalian collagenase, Science 182:70–71.

    Article  Google Scholar 

  • McCroskery, P. A., Richards, J. F., and Harris, E. D., Jr., 1975, Purification and characterization of collagenase extracted from rabbit tumors, Biochem. J. 152:131–142.

    Google Scholar 

  • Mainardi, C. L., Dixit, S. N., and Kang, A. H., 1980, Degradation of type IV (basement membrane) collagen by a proteinase isolated from human polymorphonuclear leukocyte granules, J. Biol. Chem. 255:5435–5441.

    Google Scholar 

  • Martinez-Hernandez, A., Fink, L. M., and Pierce, G. B., 1976, Removal of basement membrane in the involuting breast, Lab. Invest. 34:455–462.

    Google Scholar 

  • Masui, Y., Takemoto, T., Sakakibara, S., Hon, H., and Nagai, Y., 1977, Synthetic substrates for vertebrate collagenase, Biochem. Med. 17:215–221.

    Article  Google Scholar 

  • Merrilees, M. J., and Scott, L., 1980, Interaction of epithelial cells and fibroblasts in culture: Effect on glycosaminoglycan levels, Dev. Biol. 76:396–409.

    Article  Google Scholar 

  • Miller, J., Finch, E. D., Chung, E., and Butler, W., 1976, Specific cleavage of the native type III collagen molecule with trypsin, Arch. Biochem. Biophys. 173:631–637.

    Article  Google Scholar 

  • Montfort, I., and Perez-Tamayo, R., 1975, The distribution of collagenase in the rat uterus during postpartum involution. An immunohistochemical study, Connect. Tissue Res. 3:245–252.

    Article  Google Scholar 

  • Morris, J. E., and Moscona, A. A., 1971, The induction of glutamine synthetase in cell aggregates of embryonic neural retina: Correlations with differentiation and multicellular organization, Dev. Biol. 25:420–444.

    Article  Google Scholar 

  • Murphy, G., and Sellers, A., 1980, The extracellular regulation of collagenase activity, in: Collagenase in Normal and Pathological Connective Tissues (D. E. Woolley and J. M. Evanson, eds.), pp. 65–81, Wiley, New York.

    Google Scholar 

  • Nagai, Y., Shinkai, H., and Ninomiya, Y., 1978, The release of collagenase inhibitors from procollagen additional peptides by pepsin treatment, Proc. Jpn. Acad. Ser. B 54:140–144.

    Article  Google Scholar 

  • Newsome, D. A., and Gross, J., 1977, Prevention by medroxyprogesterone of perforation in alkali-burned rabbit cornea: Inhibition of collagenolytic activity, Invest. Ophthalmol. 16:21–31.

    Google Scholar 

  • Newsome, D. A., and Gross, J., 1979, Cellular regulation of corneal collagenase: Stimulation of serially passaged stroma cells by blood mononuclear cells, Cell 16:895–900.

    Article  Google Scholar 

  • Olsen, B. R., 1964, Electron microscope studies on collagen. III. Tryptic digestion of tropocollagen molecules, Z. Zellforsch. Mikrosk. Anat. 61:913–917.

    Article  Google Scholar 

  • Parakkal, P., 1969, Involvement of macrophages in collagen resorption, J. Cell Biol. 41:345–354.

    Article  Google Scholar 

  • Paranjpe, M., Engel, L., Young, N., and Liotta, L. A., 1980, Activation of human breast carcinoma collagenase by plasminogen activator, Life Sci. 28:1223–1231.

    Article  Google Scholar 

  • Perez-Tamayo, R., 1973, Collagen degradation and resorption: Physiology and pathology, in: Molecular Pathology of Connective Tissues (R. Perez-Tamayo and M. Rojkind, eds.), pp. 229–322, Dekker, New York.

    Google Scholar 

  • Piez, K. A., and Sherman, M. R., 1970, Characterization of the product formed by renaturation, α1-CB2, a small peptide from collagen. Biochemistry 9:4129–4133.

    Article  Google Scholar 

  • Reich, E., 1978, Activation of plasminogen: A general mechanism for producing localized extracellular proteolysis, in: Molecular Basis of Biological Degradation Processes (R. D. Beslin, H. Hermann, I. H. Lepow, and M. L. Tanzer, eds.), pp. 155–169, Academic Press, New York.

    Google Scholar 

  • Sage, H., Woodbury, R. C., and Bornstein, P., 1979, Structural studies on human type IV collagen, J. Biol Chem. 254:9893–9900.

    Google Scholar 

  • Sakai, T., and Gross, J., 1967, Some properties of the products of reaction of tadpole collagenase with collagen, Biochemistry 6:518–529.

    Article  Google Scholar 

  • Sakamoto, S., Goldhaber, P., and Glimcher, M. J., 1973, Mouse bone collagenase. The effect of heparin on the amount of enzyme released in tissue culture and on the activity of the enzyme, Calcif. Tissue Res. 12:247–258.

    Article  Google Scholar 

  • Sakamoto, S., Sakamoto, M., Goldhaber, P., and Glimcher, M. J., 1975, Studies on the interaction between heparin and mouse bone collagenase, Biochim. Biophys. Acta 385:41–50.

    Google Scholar 

  • Sakamoto, S., Sakamoto, M., Goldhaber, P., and Glimcher, M. J., 1978, Mouse bone collagenase. Purification of the enzyme by heparin-substituted Sepharose 4B affinity chromatography and preparation of specific antibody to the enzyme, Arch. Biochem. Biophys. 188:438–449.

    Article  Google Scholar 

  • Salpeter, M. M., and Singer, M., 1960, Differentiation of the submicroscopic adepidermal membrane during limb regeneration in adult Triturus, including a note on the use of the term basement membrane, Anat. Rec. 136:27–40.

    Article  Google Scholar 

  • Sellers, A., Cartwright, E., Murphy, G., and Reynolds, J. J., 1977, Evidence that latent collagenases are enzyme-inhibitor complexes, Biochem. J. 163:303–307.

    Google Scholar 

  • Seltzer, J. L., Weglus, H. G., Jeffrey, J. J., and Eisen, A. Z., 1976, The function of calcium in the action of mammalian collagenase, Arch. Biochem. Biophys. 173:355–361.

    Article  Google Scholar 

  • Seltzer, J. L., Eisen, A. Z., Jeffrey, J. J., and Feder, J., 1978, A component of normal human serum which enhances the activity of vertebrate collagenase, Biochem. Biophys. Res. Commun. 80:637–645.

    Article  Google Scholar 

  • Slavkin, H. C., and Bringas, P., Jr., 1976, Epithelial-mesenchymal interactions in dontogenesis, Dev. Biol. 50:428–442.

    Article  Google Scholar 

  • Stricklin, G. P., Eisen, A. Z., Bauer, E. A., and Jeffrey, J. J., 1977, Human skin collagenase: Isolation of precursor and active forms from both fibroblast and organ cultures, Biochemistry 16:1607–1615.

    Article  Google Scholar 

  • Stricklin, G. P., Eisen, A. Z., Bauer, E. A., and Jeffrey, J. J., 1978, Human skin fibroblast collagenase: Chemical properties of precursor and active forms, Biochemistry 17:2331–2337.

    Article  Google Scholar 

  • Ten Cate, A. R., and Deporter, D. A., 1974, The degradative role of the fibroblast in the remodelling and turnover of collagen in soft connective tissue, Anat. Rec. 182:1–14.

    Article  Google Scholar 

  • Thompson, R. C., and Ballou, L. E., 1956, Studies of metabolic turnover with tritium as a tracer, J. Biol. Chem. 223:795–809.

    Google Scholar 

  • Timpl, R., Rohde, H., Robey, P. G., Rennard, S. I., Foidart, J.-M., and Martin, G. R., 1979, Laminin—A glycoprotein from basement membranes, J. Biol. Chem. 254:9933–9937.

    Google Scholar 

  • Traub, W., and Piez, K. A., 1971, The chemistry and structure of collagen, Adv. Protein Chem. 25:243–289.

    Article  Google Scholar 

  • Trelstad, R. L., and Hayashi, K., 1979, Tendon fibrillogenesis: Intracellular collagen subassemblies and cell surface changes associated with fibril growth, Dev. Biol. 71:228–242.

    Article  Google Scholar 

  • Uitto, V. J., Schwartz, D., and Veis, A., 1980, Degradation of basement-membrane collagen by neutral proteases from human leukocytes, Eur. J. Biochem. 105:409–417.

    Article  Google Scholar 

  • Usuku, G., and Gross, J., 1965, Morphologic studies of connective tissue resorption in the tail fin of metamorphosing bullfrog tadpole, Dev. Biol. 11:352–370.

    Article  Google Scholar 

  • Vaes, G., 1972, Multiple steps in the activation of the inactive precursor of bone collagenase by trypsin, FEBS Lett. 28:198–200.

    Article  Google Scholar 

  • Vaes, G., 1980, Collagenase lysosomes and osteoclastic bone resorption, in: Collagenase in Normal and Pathological ConnectiveTissues (D. E. Woolley and J. M. Evanson, eds.), pp. 185–207, Wiley, New York.

    Google Scholar 

  • Valle, K.-J., and Bauer, E. A., 1979, Biosynthesis of collagenase by human skin fibroblasts in monolayer culture, J. Biol. Chem. 254:10115–10122.

    Google Scholar 

  • Vater, C. A., Mainardi, C. L., and Harris, E. D., Jr., 1978, Binding of latent rheumatoid synovial collagenase to collagen fibrils, Biochim. Biophys. Acta 539:238–247.

    Google Scholar 

  • Vater, C. A., Harris, E. D., Jr., and Siegel, R. C., 1979, Native cross-links in collagen fibrils induce resistance to human synovial collagenase, Biochem. J. 181:639–645.

    Google Scholar 

  • Wahl, L. M., Wahl, S. M., Mergenhagen, S. E., and Martin, G. R., 1974, Collagenase production by endotoxin-activated macrophages, Proc. Natl. Acad. Sci. USA 71:3598–3601.

    Article  Google Scholar 

  • Wahl, L. M., Wahl, S. M., Mergenhagen, S. E., and Martin, G. R., 1975, Collagenase production by lymphokine-activated macrophages, Science 187:261–263.

    Article  Google Scholar 

  • Wahl, L. M., Olsen, C. E., Sandberg, A. L., and Mergenhagen, S. E., 1977, Prostaglandin regulation of macrophage collagenase production, Proc. Natl. Acad. Sci. USA 74:4955–4958.

    Article  Google Scholar 

  • Wang, H. M., Chan, J., Pettigrew, D. W., and Sodek, J., 1978, Cleavage of native type III collagen in collagenase-susceptible region by thermolysin, Biochim. Biophys. Acta 533:270–275.

    Google Scholar 

  • Weiss, J. B., 1976, Enzymatic degradation of collagen, in: International Review of Connective Tissue Research, Vol. 7 (D. A. Hall and D. S. Jackson, eds.), pp. 101–157, Academic Press, New York.

    Google Scholar 

  • Welgus, H. G., Jeffrey, J. J., Stricklin, G. P., Roswit, W. T., and Eisen, A. Z., 1980, Characteristics of the action of human skin fibroblast collagenase on fibrillar collagen, J. Biol. Chem. 255:6806–6813.

    Google Scholar 

  • Werb, Z., and Aggeler, J., 1978, Proteases induce secretion of collagenase and plasminogen activator by fibroblasts, Proc. Natl Acad. Sci. USA 75:1839–1843.

    Article  Google Scholar 

  • Werb, Z., and Reynolds, J. J., 1974, Stimulation by endocytosis of secretion of collagenase and neutral proteinase from rabbit synovial fibroblasts, J. Exp. Med. 140:1482–1497.

    Article  Google Scholar 

  • Werb, Z., Mainardi, C. L., Vater, C. A., and Harris, E. D., Jr., 1977, Endogenous activation of latent collagenase by rheumatoid synovial cells, N. Engl. J. Med. 296:1017–1023.

    Article  Google Scholar 

  • Werb, Z., Foley, R., and Munck, A., 1978, Glucocorticoid receptors and glucocorticoid sensitive secretion of neutral proteinases in a macrophage line, J. Immunol. 121:115–121.

    Google Scholar 

  • Woolley, D. E., and Evanson, J. M., 1977, Effect of cartilage proteoglycans on human collagenase activities, Biochim. Biophys. Acta 497:144–150.

    Google Scholar 

  • Woolley, D. E., and Evanson, J. M., (eds.), 1980, Collagenase in Normal and Pathological Connective Tissues, Wiley, New York.

    Google Scholar 

  • Woolley, D. E., Lindberg, K. A., Glanville, R. W., and Evanson, J. M., 1975, Action of rheumatoid synovial collagenase on cartilage collagen. Different susceptibilities of cartilage and tendon collagen to collagenase attack, Eur. J. Biochem. 50:427–444.

    Article  Google Scholar 

  • Woolley, D. E., Glanville, R. W., Crossley, M. J., and Evanson, J. M., 1975, Purification of rheumatoid synovial collagenase and its action on soluble and insoluble collagen, Eur. J. Biochem. 54:611–622.

    Article  Google Scholar 

  • Woolley, D. E., Brinckerhoff, C. L., Mainardi, C. L., Vater, C. A., Evanson, J. M., and Harris, E. D., Jr., 1979, Collagenase production by rheumatoid synovial cells: Morphologic and immunohistochemical studies of the dendritic cell, Ann. Rheum. Dis. 38:262–270.

    Article  Google Scholar 

  • Woolley, D. E., Harris, E. D., Jr., Mainardi, C. L., and Brinckerhoff, C. E., 1978, Collagenase immunolocalization in cultures of rheumatoid synovial cells, Science 200:773–775.

    Article  Google Scholar 

  • Woolley, D. E., Tetlow, L. C., and Evanson, J. M., 1980, Collagenase immunolocalization studies of rheumatoid and malignant tissues, in: Collagenase in Normal and Pathological Connective Tissues (D. E. Woolley and J. M. Evanson, eds.), pp. 105–125, Wiley, New York.

    Google Scholar 

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Gross, J. (1981). An Essay on Biological Degradation of Collagen. In: Hay, E.D. (eds) Cell Biology of Extracellular Matrix. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0881-2_9

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  • DOI: https://doi.org/10.1007/978-1-4613-0881-2_9

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-8226-6

  • Online ISBN: 978-1-4613-0881-2

  • eBook Packages: Springer Book Archive

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