Overexpression of the matrix metalloproteinase matrilysin results in premature mammary gland differentiation and male infertility

Molecular Biology of the Cell

Volumn 9, Issue 2, 1998, Pages 421-435

  Rudolph Owen, Laura A ^a   Cannon, Paul ^b   Matrisian, Lynn M ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ROCHE BIOSCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CASEIN; MATRILYSIN; MATRIX METALLOPROTEINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; BREAST DISEASE; BREAST EPITHELIUM; CELL DESTRUCTION; CELL DIFFERENTIATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MALE; MALE GENITAL SYSTEM; MALE INFERTILITY; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

ANIMALIA; MAMMARY TUMOR ONCOVIRUS; MAMMARY TUMOR VIRUS; MOUSE MAMMARY TUMOR VIRUS; MURINAE; MURINE MAMMARY TUMOR VIRUS; MUS MUSCULUS; ONCOVIRINAE; TUMOR VIRUS;

EID: 0031930620     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.2.421     Document Type: Article

References (62)

1. Birkedal-Hansen, H., Moore, W.G.I., Bodden, M.K., Windsor, L.J., Birkedal-Hansen, B., DeCarlo, A., Engler, J.A. (1993). Matrix metalloproteinases: a review. Crit. Rev. Oral Biol. Med. 4, 197-250.
2. Boudreau, N., Sympson, C.J., Werb, A., Bissell, M.J. (1995). Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267, 891-893.
3. Brannstrom, M., Woessner, J.F., Jr., Koos, R.D., Sear, C.H., LeMaire, W.J. (1988). Inhibitors of mammalian tissue collagenase and metalloproteinase suppress ovulation in the perfused rat ovary. Endocrinology 122, 1715-1721.
4. Breathnach, R., Harris, B.A. (1983). Plasmids for the cloning and expression of full-length double-stranded cDNAs under control of the SV40 early or late gene promoter. Nucleic Acids Res. 11, 7119-7136.
5. Burkhardt, H., Hartmann, F., Schwingel, M.F. (1986). Activation of latent collagenase from polymorphonuclear leukocytes by oxygen radicals. Enzyme 36, 221-231.
6. Butler, T.A., Zhu, C., Mueller, R.A., Fuller, G.C., Lemaire, W.J., Woessner, J.F., Jr. (1991). Inhibition of ovulation in the perfused rat ovary by the synthetic collagenase inhibitor SC 44463. Biol. Reprod. 44, 1183-1188.
7. Cardiff, R.D., Muller, W.J. (1993). Transgenic mouse models of mammary tumorigenesis. Cancer Surv. 16, 97-113.
8. Choi, Y., Henrard, D., Lee, I., Ross, S.R. (1987). The mouse mammary tumor virus long terminal repeat directs expression in epithelial and lymphoid cells of different tissues in transgenic mice. J. Virol. 61, 3013-3019.
9. Chomczynski, P., Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
10. Cossins, J., Dudgeon, T.J., Catlin, G., Gearing, A.J., Clements, J.M. (1996). Identification of MMP-18, a putative novel human matrix metalloproteinase. Biochem. Biophys. Res. Commun. 228, 494-498.
11. Danielson, P., Forss-Petter, S., Brow, M., Calavetta, L., Douglass, J., Milner, R., Sutcliffe, J. (1988). p1B15: A clone of the rat mRNA encoding cyclophilin. DNA 7, 261-267.
12. D'Armiento, J., Dalal, S.S., Okada, Y., Berg, R.A., Chada, K. (1992). Collagenase expression in the lungs of transgenic mice causes pulmonary emphysema. Cell 71, 955-961.
13. Eeckhout, Y., Vaes, G. (1977). Further studies on the activation of procollagenase, the latent precursor of bone collagenase: Effects of lysosomal cathepsin B, plasmin and kallikrein, and spontaneous activation. Biochem. J. 166, 21-29.
14. Gavrieli, Y., Sherman, Y., Ben-Sasson, S.A. (1992). Identification of programmed cell death in situvia specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
15. Grant, G.A., Eisen, A.Z., Marmer, B.L., Roswit, W.T., Goldberg, G.I. (1987). The activation of human skin fibroblast procollagenase. J. Biol. Chem. 262, 5886-5889.
16. Griswold, M.D. (1988). Protein secretions of Sertoli cells. Int. Rev. Cytol. 110, 133-156.
17. Gunsalus, G.L., Bardin, C.W. (1991), Sertoli-germ cell interactions as determinants of bidirectional secretion of androgen-binding protein. Ann. NY Acad. Sci. 637, 322-326.
18. Gunzburg, W.H., Salmons, B. (1992). Factors controlling the expression of mouse mammary tumour virus. Biochem. J. 283, 625-632.
19. Heppner, K.J., Matrisian, L.M., Jensen, R.A., Rodgers, W.H. (1996). Expression of most matrix metalloproteinase family members in breast cancer represents a tumor-induced host response. Am. J. Pathol. 149, 273-282.
20. Hogan, B., Beddington, R., Costantini, F., Lacy, E. (1995). Production of transgenic mice. In: Manipulating the Mouse Embryo, A Laboratory Manual. 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 217-253.
21. Hulboy, D.L., Rudolph, L.A., Matrisian, L.M. (1997). Matrix metalloprotienases as mediators of reproductive function. Mol. Hum. Reprod. 3, 27-45.
22. Imai, K., Kusakabe, M., Sakakura, T., Nakanishi, I, Okada, Y. (1994). Susceptibility of tenascin to degradation by matrix metalloproteinases and serine proteinases, FEBS Lett. 352, 216-218.
23. Imai, K., Yokohama, Y., Nakanishi, I., Ohuchi, E., Fujii, Y., Nakai, N., Okada, Y. (1995). Matrix metalloproteinase 7 (matrilysin) from human rectal carcinoma cells. Activation of the precursor, interaction with other matrix metalloproteinases and enzymic properties. J. Biol. Chem. 270, 6691-6697.
24. Johnson, M.H., Everitt, B.J. (1995). Testicular function. In: Essential Reproduction. Cambridge, UK: Blackwell Science, Ltd., 45-59.
25. Kessler, O., Chasin, L.A. (1996). Effects of nonsense mutation on nuclear and cytoplasmic adenine phosphoribosyltransferase RNA. Mol. Cell. Biol. 16, 4426-4435.
26. Liu, X., Wu, H., Byrne, M., Jeffrey, J., Krane, S., Jaenisch, R. (1995). A targeted mutation at the known collagenase cleavage site in mouse type I collagen impairs tissue remodeling. J. Cell. Biol. 730, 227-237.
27. Marbaix, E., Kokorine, I., Moulin, P., Donnez, J., Eeckhout, Y., Courtoy, P.J. (1996). Menstrual breakdown of human endometrium can be mimicked in vitro and is selectively and reversibly blocked by inhibitors of matrix metalloproteinases. Proc. Natl. Acad. Sci. USA 93, 9120-9125.
28. Matsui, Y., Halter, S.A., Holt, J.T., Hogan, B.L.M., Coffey, R.J. (1990). Development of mammary hyperplasia and neoplasia in MMTV-TGFa transgenic mice. Cell 61, 1147-1155.
29. McDonnell, S., Navre, M., Coffey, R.J., Matrisian, L.M. (1991). Expression and localization of the matrix metalloproteinase pump-1 (MMP-7) in human gastric and colon carcinomas. Mol. Carcinog. 4, 527-533.
30. Medina, D. (1973). Preneoplastic lesions in mouse mammary tumorigenesis. In: Methods in Cancer Research, ed. H. Busch, New York: Academic Press, 3-53.
31. Muller, D., Quantin, B., Gesnel, M., Millon-Collard, R., Abecassis, J., Breathnach, R. (1988). The collagenase gene family in humans consists of at least four members. Biochem. J. 253, 187-192.
32. Murphy, G., Cockett, M.I., Ward, R.V., Docherty, A.J.P. (1991). Matrix metalloproteinase degradation of elastin, type IV collagen, and proteoglycan: A quantitative comparison of the activities of 95 kDa and 72 kDa gelatinases, stromelysins-1 and -2 and punctuated metalloproteinase (PUMP). Biochem. J. 277, 277-279.
33. Nagase, H., Enghild, J.J., Salvesen, G. (1990). Stepwise activation mechanisms of the proecursor of matrix metalloproteinase-3 (stromelysin) by proteinases and (4-aminophenyl) mercuric acetate. Biochemistry 29, 5783-5789.
34. Okada, Y., Nakanishi, I. (1989). Activation of matrix metalloproteinase 3 (stromelysin) and matrix metalloproteinase 2 ("gelatinase") by human neutrophil elastase and cathepsin G. FEBS Lett. 249, 353-356.
35. Park, A.J., Matrisian, L.M., Kells, A.F., Pearson, R., Yuan, Z., Navre, M. (1991). Mutational analysis of the transin (rat stromelysin) autoinhibitor region demonstrates a role for residues surrounding the "cysteine switch". J. Biol. Chem. 266, 1584-1590.
36. Powell, W.C., Matrisian, L.M. (1996). Complex roles of matrix metalloproteinases in tumor progression. In: Attempts to Understand Metastasis Formation I: Metastasis-Related Molecules, ed. U. Gunthert and W. Birchmeier, Berlin: Springer-Ver lag, 1-21.
37. Puente, X.S., Pendas, A.M., Llano, E., Velasco, G., Lopez-Otin, C. (1996). Molecular cloning of a novel membrane-type matrix metalloproteinase from human breast carcinoma. Cancer Res. 56, 944-949.
38. Rajagopalan, S., Meng, X.P., Ramasamy, S., Harrison, D.G., Galis, Z.S. (1996). Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J. Clin. Invest. 98, 2572-2579.
39. Ringold, G.M. (1983). Regulation of mouse mammary tumor virus gene expression by glucocorticoid hormones. Curr. Top. Microbiol. Immunol. 106, 79-103.
40. Robinson, S.D., Roberts, A.B., Daniel, C.W. (1993). TGF-beta supresses casein synthesis in mouse mammary expiants and may play a role in controlling milk levels during pregnancy. J. Cell Biol. 120, 245-251.
41. Ross, S.R., Hsu, C.L.L., Choi, Y., Mok, E., Dudley, J.P. (1990). Negative regulation in correct tissue-specific expression of mouse mammary tumor virus in transgenic mice. Mol. Cell. Biol. 20, 5822-5829.
42. Rudolph-Owen, L.A., Hulboy, D.L., Wilson, C.L., Mudgert, J., Matrisian, L.M. (1997). Coordinate expression of matrix metalloproteinase family members in the uterus of normal, matrilysin-deficient, and stromelysin-1-deficient mice. Endocrinology 138, 4902-4911.
43. Saari, H., Suomalainen, K., Lindy, O., Konttinen, Y.T., Sorsa, T. (1990). Activation of latent human neutrophil collagenase by reactive oxygen species and serine proteases. Biochem. Biophys. Res. Commun. 171, 979-987.
44. Saarialho-Kere, U.K., Crouch, E.C., Parks, W.C. (1995). The matrix metalloproteinase matrilysin is constitutively expressed in adult human exocrine epithelium. J. Invest. Dermatol. 105,190-196.
45. Sanchez-Lopez, R., Nicholson, R., Gesnel, M.-C, Matrisian, L.M., Breathnach, R. (1988). Structure-function relationships in the collagenase family member transin. J. Biol. Chem. 263, 11892-11899.
46. Sang, Q-X., Dym, M, Byers, S.W. (1990a). Secreted metalloprotienases in testicular cell culture. Biol. Reprod. 43, 946-955.
47. Sang, Q-X., Stetler-Stevenson, W.G., Liotta, L.A., Byers, S.W. (1990b). Identification of type IV collagenase in rat testicular cell culture: Influence of peritubular-Sertoli cell interactions. Biol. Reprod. 43, 956-964.
48. Sires, U.I., Griffin, G.L., Broekelmann, T.J., Mecham, R.P., Murphy, G., Chung, A.E., Welgus, H.G., Senior, R.M. (1993). Degradation of entactin by matrix metalloproteinases. Susceptibility to matrilysin and identification of cleavage sites. J. Biol. Chem. 268, 2069-2074.
49. Siri, A., Knauper, V., Veirana, N., Caocci, F., Murphy, G., Zaradi, L. (1995). Different susceptibility of small and large human tenascin-c isoforms to degradation by matrix metalloproteinases. J. Biol. Chem. 270, 8650-8654.
50. Snedeker, S.M., Brown, C.F., DiAugustine, R.P. (1991). Expression and functional properties of transforming growth factor alpha and epidermal growth factor during mouse mammary gland ductal morphogenesis. Proc. Natl. Acad. Sci. USA 88, 276-280.
51. Sympson, C.J., Talhouk, R.S., Alexander, C.M., Chin, J.R., Clift, S.M., Bissell, M.J., Werb, Z. (1994). Targeted expression of stromelysin-1 in mammary gland provides evidence for a role of proteinases in branching morphogenesis and the requirement for an intact basement membrane for tissue-specific gene expression. J. Cell Biol. 125, 681-693.
52. Talhouk, R.S., Bissell, M.J., Werb, Z. (1992). Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution, J. Cell Biol. 118, 1271-1282.
53. Ulisse, S., Farina, A.R., Piersanti, D., Tiberio, A., Cappabianca, L., D'Orazi, G., Jannini, E.A., Malykh, O., Stetler-Stevenson, W.G., D'Armiento, M., Gulino, A., Mackay, A.R. (1994). Follicle-stim- | ulating hormone increases the expression of tissue inhibitors of metalloproteinases TIMP-1 and TIMP-2 and induces TIMP-1 AP-1 site binding complex(es) in prepubertal rat Sertoli cells. Endocrinology 135, 2479-2487.
54. Van Wart, H.E., Birkedal-Hansen, H. (1990). The cysteine switch: A principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc. Natl. Acad. Sci. USA 87, 5578-5582.
55. Waseem, N.H., Lane, D.P. (1990). Monoclonal antibody analysis of the proliferating cell nuclear antigen (PCNA). Structural conservation and the detection of a nucleolar form. J. Cell Sci. 96, 121-129.
56. Wilson, C.L., Heppner, K.J., Rudolph, L.A., Matrisian, L.M. (1995). The metalloproteinase matrilysin is preferentially expressed by epithelial cells in a tissue-restricted pattern in the mouse. Mol. Biol. Cell 6, 851-869.
57. Wilson, C.L., Matrisian, L.M. (1996). Matrilysin: An epithelial matrix metalloproteinase with potentially novel functions. Int. J. Biochem. Cell Biol. 28, 123-136.
58. Wilson, C.L., Heppner, K.J., Labosky, P.A., Hogan, B.L.M., Matrisian, L.M. (1997). Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc. Natl. Acad. Sci. USA 64, 1402-1407.
59. Witty, J.P., Lempka, T., Coffey, R.J., Jr., Matrisian, L.M. (1995a). Decreased tumor formation in 7,12-dimethylbenzanthracenetreated stromelysin-1 transgenic mice is associated with alterations in mammary epithelial cell apoptosis. Cancer Res. 55, 1401-1406.
60. Witty, J.P., McDonnell, S., Newell, K.J., Cannon P., Navre.M., Tressler, R.J., Matrisian, L.M. (1994). Modulation of matrilysin levels in colon carcinoma cell lines affects tumorigenicity in vivo. Cancer Res. 54, 4805-4812.
61. Witty, J.P., Wright, J., Matrisian, L.M. (1995b). Matrix metalloproteinases are expressed during ductal and alveolar mammary morphogenesis, and misregulation of stromelysin-1 in transgenic mice induces unscheduled alveolar development. Mol. Biol. Cell 6, M287-1303.
62. Wolfsberg, T.G., Bazan, J.F., Blobel, CF., Myles, D.G., Primakoff, P., White, J.M. (1993). The precursor region of a protein active in sperm-egg fusion contains a metalloproteinase and a disintegrin domain: structural, functional, and evolutionary implications. Proc. Natl. Acad. Sci. USA 90, 10783-10787.