Production of matrix metalloproteinases and tissue inhibitor of metalloproteinases-1 by human brain tumors

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  • 1 Department of Neurosurgery, Fukui Medical School, Fukui; Department of Biochemistry, School of Dentistry, Aichi-Gakuin University, Nagoya; and Department of Pathology, School of Medicine, Kanazawa University, Kanazawa, Japan
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✓ The role of matrix metalloproteinases (MMP's) and their inhibitor, tissue inhibitor of metalloproteinases-1 (TIMP-1), in human brain tumor invasion was investigated. Gelatinolytic activity was assayed via gelatin zymography, and four MMP's (MMP-1, MMP-2, MMP-3, and MMP-9) and TIMP-1 were immunolocalized in human brain tumors and in normal brain tissues using monoclonal antibodies. The tissue was surgically removed from 44 patients: glioblastoma (five cases), anaplastic astrocytoma (six cases), astrocytoma (four cases), metastatic tumor (six cases), neurinoma (10 cases), meningioma (10 cases), and normal brain tissue (three cases). Glioblastomas, anaplastic astrocytomas, and metastatic tumors showed high gelatinolytic activity and positive immunostaining for MMP's; TIMP-1 was also expressed in these tumors, but some tumor cells were negative for the antibody. Astrocytomas had low gelatinolytic activity and the tumor cells showed no immunoreactivity for MMP's and TIMP-1. Although neurinomas and meningiomas had only moderate proteinase activity and exhibited positive immunoreactivity for MMP-9, intense expression of TIMP-1 was simultaneously observed in these tumor cells. These findings suggest that MMP's play an important role in human brain tumor invasion, probably due to an imbalance between the production of MMP's and TIMP-1 by the tumor cells.

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Contributor Notes

Address for Dr. Hayakawa: Department of Biochemistry, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan.Address for Dr. Okada: Department of Pathology, School of Medicine, Kanazawa University, Kanazawa, Japan.Address reprint requests to: Takao Nakagawa, M.D., Department of Neurosurgery, Fukui Medical School, Matsuoka, Fukui 910–11, Japan.
  • 1.

    Apodaca G, , Rutka JT, & Bouhana K, et al: Expression of metalloproteinases and metalloproteinase inhibitors by fetal astrocytes and glioma cells. Cancer Res 50:23222329, 1990 Apodaca G, Rutka JT, Bouhana K, et al: Expression of metalloproteinases and metalloproteinase inhibitors by fetal astrocytes and glioma cells. Cancer Res 50:2322–2329, 1990

    • Search Google Scholar
    • Export Citation
  • 2.

    Barsky SH, , Togo S, & Garbisa S, et al: Type IV collagenase immunoreactivity in invasive breast carcinoma. Lancer I:296297, 1983 Barsky SH, Togo S, Garbisa S, et al: Type IV collagenase immunoreactivity in invasive breast carcinoma. Lancer I:296–297, 1983

    • Search Google Scholar
    • Export Citation
  • 3.

    Bellon G, , Caulet T, & Cam Y, et al: Immunohistochemical localisation of macromolecules of the basement membrane and extracellular matrix of human gliomas and meingiomas. Acta Neuropathol 66:245252, 1985 Bellon G, Caulet T, Cam Y, et al: Immunohistochemical localisation of macromolecules of the basement membrane and extracellular matrix of human gliomas and meingiomas. Acta Neuropathol 66:245–252, 1985

    • Search Google Scholar
    • Export Citation
  • 4.

    Brown PD, , Levy AT, & Margulies IMK, et al: Independent expression and cellular processing of Mr 72,000 type IV collagenase and interstitial collagenase in human tumorigenic cell lines. Cancer Res 50:61846191, 1990 Brown PD, Levy AT, Margulies IMK, et al: Independent expression and cellular processing of Mr 72,000 type IV collagenase and interstitial collagenase in human tumorigenic cell lines. Cancer Res 50:6184–6191, 1990

    • Search Google Scholar
    • Export Citation
  • 5.

    Caccamo DV, & McKeever PE: Plasminogen activators and inhibitors in gliomas: an immunohistochemical study. J Neuropathol Exp Neurol 51:332, 1992 (Abstract) Caccamo DV, McKeever PE: Plasminogen activators and inhibitors in gliomas: an immunohistochemical study. J Neuropathol Exp Neurol 51:332, 1992 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 6.

    DeClerck YA, , Perez N, & Shimada H, et al: Inhibition of invasion and metastasis in cells transfected with an inhibitor of metalloproteinases. Cancer Res 52:701708, 1992 DeClerck YA, Perez N, Shimada H, et al: Inhibition of invasion and metastasis in cells transfected with an inhibitor of metalloproteinases. Cancer Res 52:701–708, 1992

    • Search Google Scholar
    • Export Citation
  • 7.

    DeClerck YA, , Yean TD, & Chan D, et al: Inhibition of tumor invasion of smooth muscle cell layers by recombinant human metalloproteinsae inhibitor. Cancer Res 51:21512157, 1991 DeClerck YA, Yean TD, Chan D, et al: Inhibition of tumor invasion of smooth muscle cell layers by recombinant human metalloproteinsae inhibitor. Cancer Res 51:2151–2157, 1991

    • Search Google Scholar
    • Export Citation
  • 8.

    D'Errico A, , Garbisa S, & Liotta LA, et al: Augmentation of type IV collagenase, laminin receptor, and Ki67 proliferation antigen associated with human colon, gastric, and breast carcinoma progression. Mod Pathol 4:239246, 1991 D'Errico A, Garbisa S, Liotta LA, et al: Augmentation of type IV collagenase, laminin receptor, and Ki67 proliferation antigen associated with human colon, gastric, and breast carcinoma progression. Mod Pathol 4:239–246, 1991

    • Search Google Scholar
    • Export Citation
  • 9.

    Desrochers PE, , Jeffrey JJ, & Weiss SJ: Interstitial collagenase (Matrix metalloproteinase-1) expresses serpinase activity. J Clin Invest 87:22582265, 1991 Desrochers PE, Jeffrey JJ, Weiss SJ: Interstitial collagenase (Matrix metalloproteinase-1) expresses serpinase activity. J Clin Invest 87:2258–2265, 1991

    • Search Google Scholar
    • Export Citation
  • 10.

    Docherty AJP, , Lyons A, & Smith BJ, et al: Sequence of human tissue inhibitor of metalloproteinase and its identity to erythroid-potentiating activity. Nature 318:6669, 1985 (Letter) Docherty AJP, Lyons A, Smith BJ, et al: Sequence of human tissue inhibitor of metalloproteinase and its identity to erythroid-potentiating activity. Nature 318:66–69, 1985 (Letter)

    • Search Google Scholar
    • Export Citation
  • 11.

    Franks AJ, & Ellis E: Immunohistochemical localisation of tissue plasminogen activator in human brain tumours. Br J Cancer 59:462466, 1989 Franks AJ, Ellis E: Immunohistochemical localisation of tissue plasminogen activator in human brain tumours. Br J Cancer 59:462–466, 1989

    • Search Google Scholar
    • Export Citation
  • 12.

    Fujimoto N, , Mouri N, & Iwata K, et al: A one-step sandwich enzyme immunoassay for human matrix metalloproteinase 2(72-kDa gelatinase/type IV collagenase) using monoclonal antibodies. Clin Chim Acta 221:91103, 1993 Fujimoto N, Mouri N, Iwata K, et al: A one-step sandwich enzyme immunoassay for human matrix metalloproteinase 2(72-kDa gelatinase/type IV collagenase) using monoclonal antibodies. Clin Chim Acta 221:91–103, 1993

    • Search Google Scholar
    • Export Citation
  • 13.

    Fukuda Y, , Imoto M, & Koyama Y, et al: Immunohistochemical study on tissue inhibitors of metalloproteinases in normal and pathological human livers. Gastroenterol Jpn 26:3741, 1991 Fukuda Y, Imoto M, Koyama Y, et al: Immunohistochemical study on tissue inhibitors of metalloproteinases in normal and pathological human livers. Gastroenterol Jpn 26:37–41, 1991

    • Search Google Scholar
    • Export Citation
  • 14.

    Goldberg GI, , Strongin A, & Collier IE, et al: Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin. J Biol Chem 267:45834591, 1992 Goldberg GI, Strongin A, Collier IE, et al: Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin. J Biol Chem 267:4583–4591, 1992

    • Search Google Scholar
    • Export Citation
  • 15.

    Halaka AN, , Bunning RAD, & Bird CC, et al: Production of collagenase and inhibitor (TIMP) by intracranial tumors and dura in vitro. J Neurosurg 59:461466, 1983 Halaka AN, Bunning RAD, Bird CC, et al: Production of collagenase and inhibitor (TIMP) by intracranial tumors and dura in vitro. J Neurosurg 59:461–466, 1983

    • Search Google Scholar
    • Export Citation
  • 16.

    Herron GS, , Banda MJ, & Clark EJ, et al: Secretion of metalloproteinases by stimulated capillary endothelial cells. II. Expression of collagenase and stromelysin activities is regulated by endogenous inhibitors. J Biol Chem 261:28142818, 1986 Herron GS, Banda MJ, Clark EJ, et al: Secretion of metalloproteinases by stimulated capillary endothelial cells. II. Expression of collagenase and stromelysin activities is regulated by endogenous inhibitors. J Biol Chem 261:2814–2818, 1986

    • Search Google Scholar
    • Export Citation
  • 17.

    Herron GS, , Werb Z, & Dwyer K, et al: Secretion of metalloproteinases by stimulated capillary endothelial cells. I. Production of procollagenase and prostromelysin exceeds expression of proteolytic activity. J Biol Chem 261:28102813, 1986 Herron GS, Werb Z, Dwyer K, et al: Secretion of metalloproteinases by stimulated capillary endothelial cells. I. Production of procollagenase and prostromelysin exceeds expression of proteolytic activity. J Biol Chem 261:2810–2813, 1986

    • Search Google Scholar
    • Export Citation
  • 18.

    Hibbs MS, , Hasty KA, & Seyer JM, et al: Biochemical and immunological characterization of the secreted forms of human neutrophil gelatinase. J Biol Chem 260:24932500, 1985 Hibbs MS, Hasty KA, Seyer JM, et al: Biochemical and immunological characterization of the secreted forms of human neutrophil gelatinase. J Biol Chem 260:2493–2500, 1985

    • Search Google Scholar
    • Export Citation
  • 19.

    Hibbs MS, , Hoidal JR, & Kang AH: Expression of a metalloproteinase that degrades native type V collagen and denatured collagens by cultured human alveolar macrophages. J Clin Invest 80:16441650, 1987 Hibbs MS, Hoidal JR, Kang AH: Expression of a metalloproteinase that degrades native type V collagen and denatured collagens by cultured human alveolar macrophages. J Clin Invest 80:1644–1650, 1987

    • Search Google Scholar
    • Export Citation
  • 20.

    Hicks NJ, , Ward RV, & Reynolds JJ: A fibrosarcoma model derived from mouse embryo cells: growth properties and secretion of collagenase and metalloproteinase inhibitor (TIMP) by tumour cell lines. Int J Cancer 33:835844, 1984 Hicks NJ, Ward RV, Reynolds JJ: A fibrosarcoma model derived from mouse embryo cells: growth properties and secretion of collagenase and metalloproteinase inhibitor (TIMP) by tumour cell lines. Int J Cancer 33:835–844, 1984

    • Search Google Scholar
    • Export Citation
  • 21.

    Kalebic T, , Garbisa S, & Glaser B, et al: Basement membrane collagen: degradation by migrating endothelial cells. Science 221:281283, 1983 Kalebic T, Garbisa S, Glaser B, et al: Basement membrane collagen: degradation by migrating endothelial cells. Science 221:281–283, 1983

    • Search Google Scholar
    • Export Citation
  • 22.

    Keohane ME, , Hall SW, & VandenBerg SR, et al: Secretion of α 2-macroglobulin, α 2-antiplasmin, and plasminogen activator inhibitor-1 by glioblastoma multiforme in primary organ culture. J Neurosurg 73:234241, 1990 Keohane ME, Hall SW, VandenBerg SR, et al: Secretion of α 2-macroglobulin, α 2-antiplasmin, and plasminogen activator inhibitor-1 by glioblastoma multiforme in primary organ culture. J Neurosurg 73:234–241, 1990

    • Search Google Scholar
    • Export Citation
  • 23.

    Kubota T, , Nakagawa T, & Hosotani K, et al: Immunohistochemical study of extracellular matrix in schwannomas: in vivo and in vitro observations. Brain Tumor Pathol 9:2331, 1992 Kubota T, Nakagawa T, Hosotani K, et al: Immunohistochemical study of extracellular matrix in schwannomas: in vivo and in vitro observations. Brain Tumor Pathol 9:23–31, 1992

    • Search Google Scholar
    • Export Citation
  • 24.

    Liotta LA, , Steeg PS, & Stetler-Stevenson WG: Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 64:327336, 1991 Liotta LA, Steeg PS, Stetler-Stevenson WG: Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 64:327–336, 1991

    • Search Google Scholar
    • Export Citation
  • 25.

    Liotta LA, , Tryggvason K, & Garbisa S, et al: Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284:6768, 1980 Liotta LA, Tryggvason K, Garbisa S, et al: Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284:67–68, 1980

    • Search Google Scholar
    • Export Citation
  • 26.

    Lund-Johansen M, , Rucklidge GJ, & Milne G, et al: A metalloproteinase, capable of destroying cultured brain tissue isolated from rat glioma cells. Anticancer Res 11:10011006, 1991 Lund-Johansen M, Rucklidge GJ, Milne G, et al: A metalloproteinase, capable of destroying cultured brain tissue isolated from rat glioma cells. Anticancer Res 11:1001–1006, 1991

    • Search Google Scholar
    • Export Citation
  • 27.

    Mast AE, , Enghild JJ, & Nagase H, et al: Kinetics and physiologic relevance of the inactivation of αl-proteinase inhibitor, α1-antichymotrypsin, and antithrombin III by matrix metalloproteinases-1 (tissue collagenase), -2 (72-kDa gelatinase/type IV collagenase), and -3 (stromelysin). J Biol Chem 266:1581015816, 1991 Mast AE, Enghild JJ, Nagase H, et al: Kinetics and physiologic relevance of the inactivation of αl-proteinase inhibitor, α1-antichymotrypsin, and antithrombin III by matrix metalloproteinases-1 (tissue collagenase), -2 (72-kDa gelatinase/type IV collagenase), and -3 (stromelysin). J Biol Chem 266:15810–15816, 1991

    • Search Google Scholar
    • Export Citation
  • 28.

    Mignatti P, , Robbins E, & Rifkin DB: Tumor invasion through the human amniotic membrane: requirement for a proteinase cascade. Cell 47:487498, 1986 Mignatti P, Robbins E, Rifkin DB: Tumor invasion through the human amniotic membrane: requirement for a proteinase cascade. Cell 47:487–498, 1986

    • Search Google Scholar
    • Export Citation
  • 29.

    Moll UM, , Youngleib GL, & Rosinski KB, et al: Tumor promoter-stimulated Mr 92,000 gelatinase secreted by normal and malignant human cells: isolation and characterization of the enzyme from HT1080 tumor cells. Cancer Res 50:61626170, 1990 Moll UM, Youngleib GL, Rosinski KB, et al: Tumor promoter-stimulated Mr 92,000 gelatinase secreted by normal and malignant human cells: isolation and characterization of the enzyme from HT1080 tumor cells. Cancer Res 50:6162–6170, 1990

    • Search Google Scholar
    • Export Citation
  • 30.

    Monteagudo C, , Merino MJ, & San-Juan J, et al: Immunohistochemical distribution of type IV collagenase in normal, benign, and malignant breast tissue. Am J Pathol 136:585592, 1990 Monteagudo C, Merino MJ, San-Juan J, et al: Immunohistochemical distribution of type IV collagenase in normal, benign, and malignant breast tissue. Am J Pathol 136:585–592, 1990

    • Search Google Scholar
    • Export Citation
  • 31.

    Nagase H, , Barrett AJ, & Woessner JF Jr: Nomenclature and glossary of the matrix metalloproteinases. Matrix Suppl 1:421424, 1992 Nagase H, Barrett AJ, Woessner JF Jr: Nomenclature and glossary of the matrix metalloproteinases. Matrix Suppl 1:421–424, 1992

    • Search Google Scholar
    • Export Citation
  • 32.

    Obata K, , Iwata K, & Okada Y, et al: A one-step sandwich enzyme immunoassay for human matrix metalloproteinase 3 (stromelysin-1) using monoclonal antibodies. Clin Chim Acta 211:5972, 1992 Obata K, Iwata K, Okada Y, et al: A one-step sandwich enzyme immunoassay for human matrix metalloproteinase 3 (stromelysin-1) using monoclonal antibodies. Clin Chim Acta 211:59–72, 1992

    • Search Google Scholar
    • Export Citation
  • 33.

    Okada Y, , Gonoji Y, & Naka K, et al: Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT 1080 human fibrosarcoma cells. Purification and activation of the precursor and enzymic properties. J Biol Chem 267:2171221729, 1992 Okada Y, Gonoji Y, Naka K, et al: Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT 1080 human fibrosarcoma cells. Purification and activation of the precursor and enzymic properties. J Biol Chem 267:21712–21729, 1992

    • Search Google Scholar
    • Export Citation
  • 34.

    Okada Y, , Harris ED Jr, & Nagase H: The precursor of a metalloendopeptidase from human rheumatoid synovial fibroblasts. Purification and mechanisms of activation by endopeptidases and 4-aminophenylmercuric acetate. Biochem J 254:731741, 1988 Okada Y, Harris ED Jr, Nagase H: The precursor of a metalloendopeptidase from human rheumatoid synovial fibroblasts. Purification and mechanisms of activation by endopeptidases and 4-aminophenylmercuric acetate. Biochem J 254:731–741, 1988

    • Search Google Scholar
    • Export Citation
  • 35.

    Paganetti PA, , Caroni P, & Schwab ME: Glioblastoma infiltration into central nervous system tissue in vitro: involvement of a metalloprotease. J Cell Biol 107:22812291, 1988 Paganetti PA, Caroni P, Schwab ME: Glioblastoma infiltration into central nervous system tissue in vitro: involvement of a metalloprotease. J Cell Biol 107:2281–2291, 1988

    • Search Google Scholar
    • Export Citation
  • 36.

    Ponton A, , Coulombe B, & Skup D: Decreased expression of tissue inhibitor of metalloproteinases in metastatic tumor cells leading to increased levels of collagenase activity. Cancer Res 51:21382143, 1991 Ponton A, Coulombe B, Skup D: Decreased expression of tissue inhibitor of metalloproteinases in metastatic tumor cells leading to increased levels of collagenase activity. Cancer Res 51:2138–2143, 1991

    • Search Google Scholar
    • Export Citation
  • 37.

    Reich R, , Thompson EW, & Iwamoto Y, et al: Effects of inhibitors of plasminogen activator, serine proteinases, and collagenase IV on the invasion of basement membranes by metastatic cells. Cancer Res 48:33073312, 1988 Reich R, Thompson EW, Iwamoto Y, et al: Effects of inhibitors of plasminogen activator, serine proteinases, and collagenase IV on the invasion of basement membranes by metastatic cells. Cancer Res 48:3307–3312, 1988

    • Search Google Scholar
    • Export Citation
  • 38.

    Reith A, & Rucklidge GJ: Invasion of brain tissue by primary glioma: evidence for the involvement of urokinase-type plasminogen activator as an activator of type IV collagenase. Biochem Biophys Res Commun 186:348354, 1992 Reith A, Rucklidge GJ: Invasion of brain tissue by primary glioma: evidence for the involvement of urokinase-type plasminogen activator as an activator of type IV collagenase. Biochem Biophys Res Commun 186:348–354, 1992

    • Search Google Scholar
    • Export Citation
  • 39.

    Russell DS, & Rubinstein LJ: Pathology of Tumours of the Nervous System, ed 5. Baltimore: Williams & Wilkins, 1989, pp 834837 Russell DS, Rubinstein LJ: Pathology of Tumours of the Nervous System, ed 5. Baltimore: Williams & Wilkins, 1989, pp 834–837

    • Search Google Scholar
    • Export Citation
  • 40.

    Sawaya R, & Highsmith R: Plasminogen activator activity and molecular weight patterns in human brain tumors. J Neurosurg 68:7379, 1988 Sawaya R, Highsmith R: Plasminogen activator activity and molecular weight patterns in human brain tumors. J Neurosurg 68:73–79, 1988

    • Search Google Scholar
    • Export Citation
  • 41.

    Sawaya R, , Rämö J, & Shi ML, et al: Biological significance of tissue plasminogen activator content in brain tumors. J Neurosurg 74:480486, 1991 Sawaya R, Rämö J, Shi ML, et al: Biological significance of tissue plasminogen activator content in brain tumors. J Neurosurg 74:480–486, 1991

    • Search Google Scholar
    • Export Citation
  • 42.

    Sawaya R, , Zuccarello M, & Highsmith R: Alpha-1-antitrypsin in human brain tumors. J Neurosurg 67:258262, 1987 Sawaya R, Zuccarello M, Highsmith R: Alpha-1-antitrypsin in human brain tumors. J Neurosurg 67:258–262, 1987

    • Search Google Scholar
    • Export Citation
  • 43.

    Schultz RM, , Silberman S, & Persky B, et al: Inhibition by human recombinant tissue inhibitor of metalloproteinases of human amnion invasion and lung colonization by murine B16-F10 melanoma cells. Cancer Res 48:55395545, 1988 Schultz RM, Silberman S, Persky B, et al: Inhibition by human recombinant tissue inhibitor of metalloproteinases of human amnion invasion and lung colonization by murine B16-F10 melanoma cells. Cancer Res 48:5539–5545, 1988

    • Search Google Scholar
    • Export Citation
  • 44.

    Stetler-Stevenson WG, , Krutzsch HC, & Liotta LA: Tissue inhibitor of metalloproteinase (TIMP-2). A new member of the metalloproteinase inhibitor family. J Biol Chem 264:1737417378, 1989 Stetler-Stevenson WG, Krutzsch HC, Liotta LA: Tissue inhibitor of metalloproteinase (TIMP-2). A new member of the metalloproteinase inhibitor family. J Biol Chem 264:17374–17378, 1989

    • Search Google Scholar
    • Export Citation
  • 45.

    Suzuki K, , Enghild JJ, & Morodomi T, et al: Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin). Biochemistry 29:1026110270, 1990 Suzuki K, Enghild JJ, Morodomi T, et al: Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin). Biochemistry 29:10261–10270, 1990

    • Search Google Scholar
    • Export Citation
  • 46.

    Tsuchiya Y, , Endo Y, & Sato H, et al: Expression of type IV collagenases in human tumor cell lines that can form liver colonies in chick embryos. Int J Cancer 56:4651, 1994 Tsuchiya Y, Endo Y, Sato H, et al: Expression of type IV collagenases in human tumor cell lines that can form liver colonies in chick embryos. Int J Cancer 56:46–51, 1994

    • Search Google Scholar
    • Export Citation
  • 47.

    Vaithilingam IS, , McDonald W, & Brown NK, et al: Serum proteolytic activity during the growth of C6 astrocytoma. J Neurosurg 77:595600, 1992 Vaithilingam IS, McDonald W, Brown NK, et al: Serum proteolytic activity during the growth of C6 astrocytoma. J Neurosurg 77:595–600, 1992

    • Search Google Scholar
    • Export Citation
  • 48.

    Woessner JF Jr: Matrix metalloproteinase and their inhibitors in connective tissue remodeling. FASEB J 5:21452154, 1991 Woessner JF Jr: Matrix metalloproteinase and their inhibitors in connective tissue remodeling. FASEB J 5:2145–2154, 1991

    • Search Google Scholar
    • Export Citation
  • 49.

    Yamagata S, , Ito Y, & Tanaka R, et al: Gelatinases of metastatic cell lines of murine colonic carcinoma as detected by substrate-gel electrophoresis. Biochem Biophys Res Commun 151:158162, 1988 Yamagata S, Ito Y, Tanaka R, et al: Gelatinases of metastatic cell lines of murine colonic carcinoma as detected by substrate-gel electrophoresis. Biochem Biophys Res Commun 151:158–162, 1988

    • Search Google Scholar
    • Export Citation
  • 50.

    Zhang J, , Fujimoto N, & Iwata K, et al: A one step sandwich enzyme immunoassay for human matrix metalloproteinase 1 (interstitial collagenase) using monoclonal antibodies. Clin Chim Acta 219:114, 1993 Zhang J, Fujimoto N, Iwata K, et al: A one step sandwich enzyme immunoassay for human matrix metalloproteinase 1 (interstitial collagenase) using monoclonal antibodies. Clin Chim Acta 219:1–14, 1993

    • Search Google Scholar
    • Export Citation

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