Independent Expression and Cellular Processing of Mr 72,000 Type IV Collagenase and Interstitial Collagenase in Human Tumorigenic Cell Lines

Cancer Research

Volumn 50, Issue 19, 1990, Pages 6184-6191

  Brown, Peter D ^a   Levy, Anna T ^a   Margulies, Inger M K ^a   Liotta, Lance A ^a   Stetler Stevenson, William G ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE; MESSENGER RNA; PHORBOL ESTER;

ARTICLE; CARCINOGENICITY; CELL CULTURE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TUMOR CELL LINE;

BLOTTING, WESTERN; CULTURE MEDIA; ENZYME PRECURSORS; EXTRACELLULAR SPACE; FIBROSARCOMA; HUMAN; MELANOMA; MICROBIAL COLLAGENASE; MOLECULAR WEIGHT; RNA, MESSENGER; RNA, NEOPLASM; TETRADECANOYLPHORBOL ACETATE; TUMOR CELLS, CULTURED;

EID: 0025035989     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Goldberg, G. I., Wilhelm, S. M., Kronberger, A., Bauer, E. A., Grant, G. A., and Eisen, A. Z. Human fibroblast collagenase: complete primary structure and homology to an oncogene transformation-induced rat protein. J. Biol. Chem., 261:6600–6605, 1986.
2. Fini, M. E., Plucinska, I. M., Mayer, A. S., Gross, R. H., and Brinckerhoff, C. E. A gene for rabbit synovial cell collagenase: member of a family of metalloproteinases that degrade the connective tissue matrix. Biochemistry, 26:6156–6165, 1987.
3. Whitham, S. E., Murphy, G., Angel, P., Rahmsdorf, H.J., Smith, B. J., Lyons, A., Harris, T. J. R., Reynolds, J. J., Herrlich, P., and Docherty, A. J. P. Comparison of human stromelysin and collagenase by cloning and sequence analysis. Biochem. J., 240:913–916, 1986.
4. Wilhelm, S. R., Collier, I. E., Kronberger, A., Eisen, A. Z., Manner, B. L., Grant, G. A., Bauer, E. A., and Goldberg, G. I. Human skin fibroblast stromelysin: structure, glycosylation, substrate specificity, and differential expression in normal and tumorigenic cells. Proc. Natl. Acad. Sci. USA, 84: 6725–6729, 1987.
5. Collier, I. E., Wilhelm, S. M., Eisen, A. Z., Marnier, B. L., Grant, G. A., Seltzer, J. L., Kronberger, A., He, C., Bauer, E. A., and Goldberg, G. I. H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloproteinase capable of degrading basement membrane collagen. J. Biol. Chem., 263: 6579–6587, 1988.
6. Muller, D., Quantin, B., Gesnel, M.-C., MilIon-Collard, R., Abecassis, J., and Breathnach, R. The collagenase gene family consists of at least four members. Biochem. J., 253:187–192, 1988.
7. Murphy, G., Nagase, H., and Brinckerhoft, C. E. Relationship of procolla-genase activator, stromelysin, and matrix metalloproteinase 3. Collagen Relat. Res., 8:389–391, 1988.
8. Matrisian, L. M., Glaichenhaus, N., Gesnel, M.-C., and Breathnach, R. Epidermal growth factor and oncogenes induce transcription of the same cellular mRNA in rat fibroblasts. EMBO J., 4:1435–1440, 1985.
9. Matrisian, L. M., Leroy, P., Ruhlmann, C., Gesnel, M.-C., and Breathnach, R. Isolation of the oncogene and epidermal growth factor-induced transin gene: complex control in rat fibroblasts. Mol. Cell. Biol., 6: 1679–1686, 1986.
10. Quantin, B., Murphy, G., and Breathnach, R. Pump-1 cDNA codes for a protein with characteristics similar to those of classical collagenase family members. Biochemistry, 28: 5327–5334, 1989.
11. Liotta, L. A., Tryggvason, K., Garbisa, S., Gehron-Robey, P., and Abe, S. Partial purification and characterization of a neutral proteinase which cleaves type IV collagen. Biochemistry, 20: 100–104, 1981.
12. Salo, T., Liotta, L. A., and Tryggvason, K. Purification and characterization of a murine basement membrane collagen-degrading enzyme secreted by metastatic tumor cells. J. Biol. Chem., 258:3058–3063, 1983.
13. Wilhelm, S. M., Collier, I. E., Maimer, B. L., Eisen, A. Z., Grant, G.A., and Goldberg, G. I. SV40-transformed human lung fibroblasts secrete a 92-kDa type-IV collagenase which is identical to that secreted by normal human macrophages. J. Biol. Chem., 264: 17213–17221, 1989.
14. Stetler-Stevenson, W. G., Krutzsch, H. C., Wacher, M. P., Margulies, I. M. K., and Liotta, L. A. The activation of human type IV collagenase proenzyme. Sequence identification of the major conversion product following organ-omercurial activation. J. Biol. Chem., 264: 1353–1356, 1989.
15. Welgus, H. G., Stricklin, G. P., Eisen, A. Z., Bauer, E. A., Cooney, R. V., and Jeffrey, J. J. A specific inhibitor of vertebrate collagenase produced by human skin fibroblasts. J. Biol. Chem., 254: 1938–1943, 1979.
16. Stricklin, G. P., and Welgus, H. G. Human skin fibroblast collagenase inhibitor purification and biochemical characterization. J. Biol. Chem., 258: 12252–12258, 1983.
17. Stetler-Stevenson, W. G., Krutzsch, H. C., and Liotta, L. A. Tissue inhibitor of metalloproteinase (TIMP-2): a new member of the metalloproteinase inhibitor family. J. Biol. Chem., 264: 17374–17378, 1989.
18. Declerck, Y. A., Yean, T. D., Ratzkin, B. J., Lu, H. S., and Langley, K. E. Purification and characterization of two related but distinct metalloproteinase inhibitors secreted by bovine aortic endothelial cells. J. Biol. Chem., 264: 17445–17453, 1989.
19. Goldberg, G. I., Marnier, B. L., Grant, G. A., Eisen, A. Z., Wilhelm, S., and He, C. Human 72-kilodalton type IV collagenase forms a complex with a tissue inhibitor of metalloproteases designated TIMP-2. Proc. Natl. Acad. Sci. USA, 86:8207–8211, 1989.
20. Woolley, D. E., and Evanson, J. M. Collagenase in Normal and Pathological Connective Tissues, 292 pp. New York: John Wiley & Sons, 1980.
21. Chin, J. R., Murphy, G., and Werb, Z. Stromelysin, a connective tissue-degrading metalloendopeptidase secreted by stimulated rabbit synovial fibroblasts in parallel with collagenase. Biosynthesis, isolation, characterization, and substrates. J. Biol. Chem., 260: 12367–12376, 1985.
22. Werb, Z., Hembry, R. M., Murphy, G., and Aggeler, J. Commitment to expression of the metalloendopeptidases, collagenase, and stromelysin: relationship of inducing events to changes in cytoskeletal architecture. J. Cell Biol., 702:697–702, 1986.
23. Frisch, S. M., Clark, E. J., and Werb, Z. Coordinate regulation of stromelysin and collagenase genes determined with cDNA probes. Proc. Natl. Acad. Sci. USA, 84:2600–2604, 1987.
24. Edwards, D. R., Murphy, G., Reynolds, J. J., Whitham, S. E., Docherty, A. J. P., Angel, P., and Heath, J. K. Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. EMBO J., 6: 1899–1904, 1987.
25. Vance, B. A., Kowalski, C. G., and Brinckerhoft, C. E. Heat shock of rabbit synovial fibroblasts increases expression of mRNAs for two metalloprotei-nases, collagenase and stromelysin, J. Cell Biol., 108:2037–2043, 1989.
26. Werb, Z., and Clark, E. J. Phorbol diesters regulate expression of the membrane neutral metalloendopeptidase (EC 3.4.24.11) in rabbit synovial fibroblasts and mammary epithelial cells. J. Biol. Chem., 264: 9111–9113, 1989.
27. Overall, C. M., Wrana, J. L., and Sodek, J. Independent regulation of collagenase, 72-kDa progelatinase, and metalloproteinase inhibitor expression in human fibroblasts by transforming growth factor-0. J. Biol. Chem., 264:1860–1869, 1989.
28. He, C., Wilhelm, S. M., Pentland, A. P., Marnier, B. L., Grant, G. A., Eisen, A. Z., and Goldberg, G. I. Tissue cooperation in a proteolytic cascade activating human interstitial collagenase. Proc. Natl. Acad. Sci. USA, 86: 2632–2636, 1989.
29. Murphy, G., Cockett, M. I., Stephens, P. E., Smith, B. J., and Docherty, A. J. P. Stromelysin is an activator of procollagenase; a study with natural and recombinant enzymes. Biochem. J., 248:265–268, 1987.
30. Murphy, G., Reynolds, J. J., and Hembry, R. M. Metalloproteinases and cancer invasion and metastasis. Int. J. Cancer, 44: 757–760, 1989.
31. Fridman, R., Lascal, J. C., Reich, R., Bonfil, D. R., and Ahn, C-H. Differential effects of phorbol ester on the in vitro invasiveness of malignant and nonmalignant human fibroblast cells. J. Cell. Physiol., 142: 55–60, 1990.
32. Kumkumian, G. K., Lafyatis, R., Remmers, E. F., Case, J. P., Kim, S. J., and Wilder, R. L. Platelet-derived growth factor and IL-1 interactions in rheumatoid arthritis. J. Immunol., 143:833–837, 1989.
33. Postlethwaite, A. E., Raghow, R., Stricklin, G. P., Poppleton, H., Sever, J. M., and Kang, A. H. Modulation of fibroblast functions by interleukin 1: increased steady-state accumulation of type I procollagen messenger RNAs and stimulation of other functions but not chemotaxis by human recombinant interleukin la and 0. J. Cell Biol., 106:311–318, 1988.
34. Brinckerhoff, C. E., Plucinska, I. M., Sheldon, L. A., and O'Connor, G. T. Half-life of synovial cell collagenase mRNA is modulated by phorbol myris-tate acetate but not by all-trans-retinoic acid or dexamethasone. Biochemistry, 25:6378–6384, 1986.
35. Aggeler, J., Frisch, S. M., and Werb, Z. Changes in cell shape correlate with collagenase gene expression in rabbit synovial fibroblasts. J. Cell Biol., 98: 1662–1671, 1984.
36. Clark, S. D., Wilhelm, S. M., Stricklin, G. P., and Welgus, H. G. Coregula-tion of collagenase and collagenase inhibitor production by phorbol myristate acetate in human skin fibroblasts. Arch. Biochem. Biophys., 214: 36–44, 1985.
37. Wilhelm, S. M., Eisen, A. Z., Teter, M., Clark, S. D., Kronberger, A., and Goldberg, G. I. Human fibroblast collagenase: glycosylation and tissue-specific levels of enzyme synthesis. Proc. Natl. Acad. Sci. USA, 83: 3756–3760, 1986.
38. Welgus, H. G., Connolly, N. L., and Senion, R. M. 12–0-Tetradecanoyl-phorbol-13-acetate-differentiated U937 cells express a macrophage-like profile of neutral proteinases. J. Clin. Invest., 77: 1675–1681, 1986.
39. Clark, S. D., Kobayashi, D. K., and Welgus, H. G. Regulation of the expression of tissue inhibitor of metalloproteinases and collagenase by retinoids and glucocorticoids in human fibroblasts. J. Clin. Invest., 80: 1280–1288, 1987.
40. Todaro, G. J., Fryling, C., and De Largo, J. E. Transforming growth factors produced by certain human cells: polypeptides that interact with epidermal growth factor receptors. Proc. Natl. Acad. Sci. USA, 77: 5258–5262, 1980.
41. Ito, A., Goshowaki, H., Sato, T., Mori, Y., Yamashita, K., Hayakawa, T., and Nagase, H. Human recombinant interleukin-la-mediated stimulation of procollagenase production and suppression of biosynthesis of tissue inhibitor of metalloproteinases in rabbit uterine cervical fibroblasts. FEBS Lett., 234: 326–330, 1988.
42. Gough, N. M. Rapid and quantitative preparation of cytoplasmic RNA from small numbers of cells. Anal. Biochem., 173:93–95, 1988.
43. Maniatis, T., Fritsch, E. F., and Sambrook, J. Molecular Cloning, a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1982.
44. Church, G., and Gilbert, W. Genomic sequencing. Proc. Natl. Acad. Sci. USA,81: 1991–1995, 1984.
45. Fort, P., Marty, L., Piechaczyk, M., Sabrouty, S. E., Dani, C., Jeanteur, P., and Blanchard, J. M. Various rat adult tissues express only one major raRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res., 13:1431–1441, 1985.
46. Heussen, C., and Dowdle, E. B. Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal. Biochem., 102:196–202, 1980.
47. Hoyhtya, M., Turpeenniemi-Hujanen, T., Stetler-Stevenson, W. G., Krutzsch, H. C., Tryggvason, K., and Liotta, L. A. Monoclonal antibodies to type IV collagenase recognize a protein with limited sequence homology to interstitial collagenase and stromelysin. FEBS Lett., 233:109–113, 1988.
48. Herron, G. S., Banda, M. J., Clark, E. J., Gavrilovic, J., and Werb, Z. 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.
49. Nakajima, M., Lotan, D., Baig, M. M., Carralero, R. M., Wood, W. R., Hendrix, M. J. C., and Lotan, R. Inhibition of retinoic acid of type IV collagenolysis and invasion through reconstituted basement membrane by metastatic rat mammary adenocarcinoma cells. Cancer Res., 49:1698–1706, 1989.
50. Huhtala, P., Chow, L. T., and Tryggvason, K. Structure of the human type IV collagenase gene. J. Biol. Chem., 265: 11077–11082, 1990.
51. Angel, P., Baumann, I., Stein, B., Delius, H., Rahmsdorf, H. J., and Herrlich, P. 12–0-Tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5’-flanking region. Mol. Cell. Biol., 7: 2256–2266, 1987.
52. Ignotz, R. A., and Massague, J. Transforming growth factor-β stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem., 261:4337–4345, 1986.
53. Roberts, A. B., Sporn, M. B., Assoian, R. K., Smith, J. M., Roche, N. S., Wakefield, L. M., Heine, U. I., Liotta, L. A., Falanga, V., Kehrl, J. H., and Fauci, A. S. Transforming growth factor type β: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc. Natl. Acad. Sci. USA, 83:4167–4171, 1986.
54. Heino, J., Ignotz, R. A., Helmer, M. E., Crouse, C., and Massague, J. Regulation of cell adhesion receptors by transforming growth factor-β. Concomitant regulation of integrins that share a common f}t subunit. J. Biol. Chem., 264:380–388, 1989.
55. Keski-Oja, J., Blasi, F., Leof, E. B., and Moses, H. L. Regulation of the synthesis and activity of urokinase plasminogen activator in A549 human lung carcinoma cells by transforming growth factor-β. J. Cell Biol., 106: 451–459, 1988.
56. Reich, R., Thompson, E. W., Iwamoto, Y., Martin, G. R., Deason, J. R., Fuller, G. C., and Miskin, R. 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.
57. Sato, Y., and Riflcin, D. B. Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-β 1-like molecule by plasmin during co-culture. J. Cell Biol., 109:309–315, 1989.
58. Albini, A., Iwamoto, Y., Kleinman, H. K., Martin, G. R., Aaronson, S. A., Kozlowski, J. M., and McEwan, R. N. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res., 47:3239–3245, 1987.