Extracellular matrix 6: Role of matrix metalloproteinases in tumor invasion and metastasis

Tumor invasion and metastasis formation are major obstacles for successful cancer therapy. Metastasis is a complex multistep process that requires sequential interactions between the invasive cell and the extracellular matrix. A model system for tumor invasion of extracellular matrix barriers has been developed, and application of this model has facilitated our understanding of the molecular mechanisms of metastasis formation. This model consists of three steps: tumor cell adhesion, extracellular matrix proteolysis, and cell migration. The role of the matrix metalloprotease enzymes in tumor cell‐mediated extracellular matrix proteolysis is well established. We review the functional domain structure of the matrix metalloprotease enzymes in general and specifically the interaction of metastasis‐associated gelatinase A (72‐kDa type IV collagenase) with the tissue inhibitor of metalloproteases‐2 (TIMP‐2). We also discuss the physiologic activation of the matrix metalloprotease enzymes and the specific cellular mechanism of action of gelatinase A.— Stetler‐Stevenson, W. G., Liotta, L. A., Kleiner, D. E., Jr. Extracellular matrix 6: role of matrix metalloproteinases in tumor invasion and metastasis. FASEB J. 7: 1434‐1441; 1993.

[1]  H K Chan,et al.  Human fibroblast stromelysin catalytic domain: expression, purification, and characterization of a C-terminally truncated form. , 1991, Biochemistry.

[2]  Kerbel Rs Expression of multi-cytokine resistance and multi-growth factor independence in advanced stage metastatic cancer. Malignant melanoma as a paradigm. , 1992 .

[3]  J. Foidart,et al.  Tumor cell surface-associated binding site for the M(r) 72,000 type IV collagenase. , 1992, Cancer research.

[4]  I. Fidler,et al.  Genetic control of cancer metastasis. , 1990, Journal of the National Cancer Institute.

[5]  H. Kleinman,et al.  Enhanced tumor growth of both primary and established human and murine tumor cells in athymic mice after coinjection with Matrigel. , 1991, Journal of the National Cancer Institute.

[6]  H. Kleinman,et al.  Malignant transformation of NIH‐3T3 cells after subcutaneous co‐injection with a reconstituted basement membrane (matrigel) , 1992, International journal of cancer.

[7]  Tumor invasion and metastasis. , 1982 .

[8]  H. Morris,et al.  Disulphide bond assignment in human tissue inhibitor of metalloproteinases (TIMP). , 1990, The Biochemical journal.

[9]  N. Pavloff,et al.  A new inhibitor of metalloproteinases from chicken: ChIMP-3. A third member of the TIMP family. , 1992, The Journal of biological chemistry.

[10]  T M Grogan,et al.  Expression of the metalloproteinase matrilysin in DU-145 cells increases their invasive potential in severe combined immunodeficient mice. , 1993, Cancer research.

[11]  M. Cockett,et al.  The C-terminal domain of 72 kDa gelatinase A is not required for catalysis, but is essential for membrane activation and modulates interactions with tissue inhibitors of metalloproteinases. , 1992, The Biochemical journal.

[12]  A. Kossakowska,et al.  Expression of metalloproteinases and their inhibitors in primary pulmonary carcinomas. , 1992, British Journal of Cancer.

[13]  L. Chow,et al.  Complete structure of the human gene for 92-kDa type IV collagenase. Divergent regulation of expression for the 92- and 72-kilodalton enzyme genes in HT-1080 cells. , 1991, The Journal of biological chemistry.

[14]  W. Stetler-Stevenson,et al.  Inhibition of tumor cell invasion by a highly conserved peptide sequence from the matrix metalloproteinase enzyme prosegment. , 1992, Cancer research.

[15]  J. Keski‐Oja,et al.  Proteolytic processing of the 72,000-Da type IV collagenase by urokinase plasminogen activator. , 1992, Experimental cell research.

[16]  E. Thompson,et al.  Collagen-induced activation of the M(r) 72,000 type IV collagenase in normal and malignant human fibroblastoid cells. , 1992, Cancer research.

[17]  L. Liotta,et al.  The activation of human type IV collagenase proenzyme. Sequence identification of the major conversion product following organomercurial activation. , 1989, The Journal of biological chemistry.

[18]  D. Rifkin,et al.  Bimodal relationship between invasion of the amniotic membrane and plasminogen activator activity , 1990, International journal of cancer.

[19]  R. Williamson,et al.  Site-directed mutations that alter the inhibitory activity of the tissue inhibitor of metalloproteinases-1: importance of the N-terminal region between cysteine 3 and cysteine 13. , 1992, Biochemistry.

[20]  L. Orci,et al.  Increased proteolytic activity is responsible for the aberrant morphogenetic behavior of endothelial cells expressing the middle T oncogene , 1990, Cell.

[21]  W. Stetler-Stevenson,et al.  Higher-order complex formation between the 72-kilodalton type IV collagenase and tissue inhibitor of metalloproteinases-2. , 1992, Biochemistry.

[22]  C. Harris,et al.  Invasive and metastatic potential of a v-Ha-ras-transformed human bronchial epithelial cell line. , 1989, Journal of the National Cancer Institute.

[23]  I. Clark,et al.  Large inhibitor of metalloproteinases (LIMP) contains tissue inhibitor of metalloproteinases (TIMP)-2 bound to 72,000-M(r) progelatinase. , 1992, Biochemical Journal.

[24]  S. Weitzman,et al.  Culture of normal and malignant primary human mammary epithelial cells in a physiological manner simulates in vivo growth patterns and allows discrimination of cell type. , 1993, Cancer research.

[25]  H. Birkedal‐Hansen,et al.  Multiple modes of activation of latent human fibroblast collagenase: evidence for the role of a Cys73 active-site zinc complex in latency and a "cysteine switch" mechanism for activation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[26]  K. Suzuki,et al.  Stepwise activation mechanisms of the precursor of matrix metalloproteinase 3 (stromelysin) by proteinases and (4-aminophenyl)mercuric acetate. , 1990, Biochemistry.

[27]  W. Stetler-Stevenson,et al.  Cellular activation of the 72 kDa type IV procollagenase/TIMP-2 complex. , 1993, Kidney international.

[28]  L. Liotta,et al.  Distribution of the 72-kd type IV collagenase in nonneoplastic and neoplastic thyroid tissue. , 1992, Human pathology.

[29]  J. Hermes,et al.  Characterization of zinc-binding sites in human stromelysin-1: stoichiometry of the catalytic domain and identification of a cysteine ligand in the proenzyme. , 1992, Biochemistry.

[30]  R. Pozzatti,et al.  Expression of matrix metalloproteinase genes in transformed rat cell lines of high and low metastatic potential. , 1992, Cancer research.

[31]  R Poulsom,et al.  Stromal expression of 72 kda type IV collagenase (MMP-2) and TIMP-2 mRNAs in colorectal neoplasia. , 1992, The American journal of pathology.

[32]  L. Liotta,et al.  Secretion of basement membrane collagen degrading enzyme and plasminogen activator by transformed cells – role in metastasis , 1982, International journal of cancer.

[33]  W. Stetler-Stevenson,et al.  Growth factors specifically alter hair follicle cell proliferation and collagenolytic activity alone or in combination. , 1990, Differentiation; research in biological diversity.

[34]  M. Stearns,et al.  Type IV collagenase (M(r) 72,000) expression in human prostate: benign and malignant tissue. , 1993, Cancer research.

[35]  D. Gerhard,et al.  On the structure and chromosome location of the 72- and 92-kDa human type IV collagenase genes. , 1991, Genomics.

[36]  D. Rifkin,et al.  Biology and biochemistry of proteinases in tumor invasion. , 1993, Physiological reviews.

[37]  L. Liotta,et al.  Tissue inhibitor of metalloproteinase (TIMP-2). A new member of the metalloproteinase inhibitor family. , 1989, The Journal of biological chemistry.

[38]  H. Birkedal‐Hansen,et al.  Matrix metalloproteinases: a review. , 1993, Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists.

[39]  W. Noack,et al.  The complex between a tissue inhibitor of metalloproteinases (TIMP-2) and 72-kDa progelatinase is a metalloproteinase inhibitor. , 1991, European journal of biochemistry.

[40]  R. Hembry,et al.  The purification of tissue inhibitor of metalloproteinases-2 from its 72 kDa progelatinase complex. Demonstration of the biochemical similarities of tissue inhibitor of metalloproteinases-2 and tissue inhibitor of metalloproteinases-1. , 1991, The Biochemical journal.

[41]  C. Clavel,et al.  Immunolocalization of matrix metallo-proteinases and their tissue inhibitor in human mammary pathology. , 1992, Bulletin du cancer.

[42]  B. Pauli,et al.  Mediation of lung metastasis of murine melanomas by a lung-specific endothelial cell adhesion molecule. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[43]  N. Suzuki,et al.  Stereo‐specific inhibition of sea urchin envelysin (hatching enzyme) by a synthetic autoinhibitor peptide with a cysteine‐switch consensus sequence , 1993, FEBS letters.

[44]  M. Hendrix,et al.  Role of the alpha v beta 3 integrin in human melanoma cell invasion. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Bissell,et al.  Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. Stephens,et al.  Sequence of human tissue inhibitor of metalloproteinases and its identity to erythroid-potentiating activity , 1985, Nature.

[47]  L. Liotta,et al.  Inhibition of human type IV collagenase by a highly conserved peptide sequence derived from its prosegment. , 1991, The American journal of the medical sciences.

[48]  T. Hamilton,et al.  Effects of synthetic peptides and protease inhibitors on the interaction of a human ovarian cancer cell line (NIH:OVCAR-3) with a reconstituted basement membrane (Matrigel). , 1991, Invasion & metastasis.

[49]  L. Liotta,et al.  Independent expression and cellular processing of Mr 72,000 type IV collagenase and interstitial collagenase in human tumorigenic cell lines. , 1990, Cancer research.

[50]  Z. Werb,et al.  Role of zinc-binding- and hemopexin domain-encoded sequences in the substrate specificity of collagenase and stromelysin-2 as revealed by chimeric proteins. , 1993, The Journal of biological chemistry.

[51]  L. Liotta,et al.  Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation , 1991, Cell.

[52]  L. Liotta,et al.  Evaluation of Basement Membrane Components and the 72 kDa Type IV Collagenase in Serous Tumors of the Ovary , 1992, The American journal of surgical pathology.

[53]  P. Chambon,et al.  A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas , 1990, Nature.

[54]  W. Stetler-Stevenson,et al.  Stability analysis of latent and active 72-kDa type IV collagenase: the role of tissue inhibitor of metalloproteinases-2 (TIMP-2). , 1993, Biochemistry.

[55]  S. Albelda,et al.  Role of integrins and other cell adhesion molecules in tumor progression and metastasis. , 1993, Laboratory investigation; a journal of technical methods and pathology.

[56]  L. Liotta,et al.  Domain structure of human 72-kDa gelatinase/type IV collagenase. Characterization of proteolytic activity and identification of the tissue inhibitor of metalloproteinase-2 (TIMP-2) binding regions. , 1992, The Journal of biological chemistry.

[57]  J. Woessner,et al.  Nomenclature and glossary of the matrix metalloproteinases. , 1992, Matrix (Stuttgart, Germany). Supplement.

[58]  R. Williamson,et al.  The N-terminal domain of tissue inhibitor of metalloproteinases retains metalloproteinase inhibitory activity. , 1991, Biochemistry.

[59]  Y. DeClerck,et al.  Characterization of the functional domain of tissue inhibitor of metalloproteinases-2 (TIMP-2). , 1993, The Biochemical journal.

[60]  H. Lu,et al.  Purification and characterization of two related but distinct metalloproteinase inhibitors secreted by bovine aortic endothelial cells. , 1989, The Journal of biological chemistry.

[61]  H. Tschesche,et al.  The recombinant catalytic domain of human neutrophil collagenase lacks type I collagen substrate specificity. , 1993, Biochemical and Biophysical Research Communications - BBRC.

[62]  J. Reynolds,et al.  Cell-mediated degradation of type IV collagen and gelatin films is dependent on the activation of matrix metalloproteinases. , 1992, The Biochemical journal.

[63]  Y. Kato,et al.  Induction of 103-kDa gelatinase/type IV collagenase by acidic culture conditions in mouse metastatic melanoma cell lines. , 1992, The Journal of biological chemistry.

[64]  J. O'Connell,et al.  The role of the C-terminal domain in collagenase and stromelysin specificity. , 1992, The Journal of biological chemistry.

[65]  C. Bucana,et al.  Influence of organ environment on extracellular matrix degradative activity and metastasis of human colon carcinoma cells. , 1990, Journal of the National Cancer Institute.

[66]  A. Eisen,et al.  Human 72-kilodalton type IV collagenase forms a complex with a tissue inhibitor of metalloproteases designated TIMP-2. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[67]  A. Eisen,et al.  SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages. , 1989, The Journal of biological chemistry.

[68]  A. Strongin,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. , 1992, The Journal of biological chemistry.

[69]  H. Nagase,et al.  Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) is induced in rabbit articular chondrocytes by cotreatment with interleukin 1 beta and a protein kinase C activator. , 1992, Experimental cell research.

[70]  A Yasui,et al.  Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. , 1990, European journal of biochemistry.

[71]  L. Matrisian,et al.  Mutational analysis of the transin (rat stromelysin) autoinhibitor region demonstrates a role for residues surrounding the "cysteine switch". , 1991, The Journal of biological chemistry.

[72]  J. Woessner,et al.  Matrix metalloproteinases and their inhibitors in connective tissue remodeling , 1991, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.