Epithelial cells up-regulate matrix metalloproteinases in cells within the same mammary carcinoma that have undergone an epithelial-mesenchymal transition

Cancer Research

Volumn 58, Issue 21, 1998, Pages 4970-4979

  Martorana, Anna M ^a,b   Zheng, Guoping ^a   Crowe, Timothy C ^a   O'Grady, Robert L ^b   Lyons, J Guy ^a  

^a ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE; GELATINASE B; MATRIX METALLOPROTEINASE; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE;

ANIMAL CELL; ARTICLE; BREAST CARCINOMA; CELL DIFFERENTIATION; CELL SUBPOPULATION; CELL TRANSFORMATION; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; EPITHELIUM CELL; GENETIC HETEROGENEITY; MESENCHYME CELL; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; RAT;

ANIMALS; COLLAGEN; COLLAGENASES; EPITHELIAL CELLS; FEMALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE 9; NEOPLASM METASTASIS; RATS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE INHIBITOR OF METALLOPROTEINASE-2; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 0032211308     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Birkedal-Hansen, H., Moore, W. G. I., Bodden, M. K., Windsor, L. J., Birkedal-Hansen, B., DeCarlo, A., and Engler, J. A. Matrix metalloproteinases: a review. Crit. Rev. Oral Biol. Med., 4: 197-250, 1993.
2. Stetler-Stevenson, W. G., Liotta, L. A., and Kleiner, D. E. Extracellular matrix 6: role of matrix metalloproteinases in tumor invasion and metastasis. FASEB J., 7: 1434-1441, 1993.
3. Grabowska, M. Collagen content of normal connective tissue, of tissue surrounding a tumour and of growing sarcoma. Nature (Lond.), 183: 1186-1187, 1959.
4. Stetler-Stevenson, W. G., Aznavoorian, S., and Liotta, L. A. Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu. Rev. Cell Biol., 9: 541-573, 1993.
5. Kossakowska, A. E., Huchcroft, S. A., Urbanski, S. J., and Edwards, D. R. Comparative analysis of the expression patterns of metalloproteinases and their inhibitors in breast neoplasia, sporadic colorectal neoplasia, pulmonary carcinomas and malignant non-Hodgkin's lymphomas in humans. Br. J. Cancer, 73: 1401-1408, 1996.
6. Freije, J. M. P., Diez-Itza, I., Balbin, M., Sanchez, L. M., Blasco, R., Tolivia, J., and Lopez-Otin, C. Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J. Biol. Chem., 269: 16766-16773, 1994.
7. Basset, P., Bellocq, J. P., Wolf, C., Stoll, I., Hutin, P., Limacher, J. M., Podhajcer, O. L., Chenard, M. P., Rio, M. C., and Chambon, P. A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature (Lond.), 348: 699-704, 1990.
8. Wright, J. H., McDonnell, S., Portella, G., Bowden, G. T., Balmain, A., and Matrisian, L. M. A switch from stromal to tumor cell expression of stromelysin-1 mRNA associated with the conversion of squamous to spindle carcinomas during mouse skin tumor progression. Mol. Carcinog., 10: 207-215, 1994.
9. Heppner, K. J., Matrisian, L. M., Jensen, R. A., and Rodgers, W. H. Expression of most matrix metalloproteinase family members in breast cancer represents a tumour-induced host response. Am. J. Pathol., 149: 273-282, 1996.
10. Witty, J. P., Lempka, T., Coffey, R. J., and Matrisian, L. M. Decreased tumor formation in 7,12-dimethylbenzanthracene-treated stromelysin-1 transgenic mice is associated with alterations in mammary epithelial cell apoptosis. Cancer Res., 55: 1401-1406, 1995.
11. Sympson, C. J., Talhouk, R. S., Alexander, C. M., Chin, J. R., Clift, S. M., Bissell, M. J., and Werb, Z. 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, 1994.
12. 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.
13. Wasylyk, C., Gutman, A., Nicholson, R., and Wasylyk, B. The c-Ets oncoprotein activates the stromelysin promoter through the same elements as several non-nuclear oncoproteins. EMBO J., 10: 1127-1134, 1991.
14. r 95,000 type IV collagenase/gelatinase and interstitial fibroblast-type collagenase by rat mucosal keratinocytes. J. Biol. Chem., 268: 19143-19151, 1993.
15. Wargotz, E. S., Deos, P. H., and Norris, H. J. Metaplastic carcinomas of the breast. II. Spindle cell carcinoma. Hum. Pathol., 20: 732-740, 1989.
16. Wargotz, E. S., and Norris, H. J. Metaplastic carcinomas of the breast. III. Carcinosarcoma. Cancer (Phila.), 64: 1490-1499, 1989.
17. Lee, C., Lapin, V., Oyasu, R., and Battifora, H. Effect of ovariectomy on serially transplanted rat mammary tumors induced by 7,12-dimethylbenz[a]anthracene. Eur. J. Cancer Clin. Oncol., 17: 801-808, 1981.
18. Sommers, C. L., Walker-Jones, D., Heckford, S. E., Worland, P., Valverius, E., Clark, R., McCormick, F., Stampfer, M., Abularach, S., and Gelmann, E. P. Vimentin rather than keratin expression in some hormone-independent breast cancer cell lines and in oncogene-transformed mammary epithelial cells. Cancer Res., 49: 4258-4263, 1989.
19. Sommers, C. L., Heckford, S. E., Skerter, J. M., Worland, P., Torri, J. A., Thompson, E. W., Byers, S. W., and Gelmann, E. P. Loss of epithelial markers and acquisition of vimentin expression in Adriamycin- and vinblastine-resistant human breast cancer cell lines. Cancer Res., 52: 5190-5197, 1992.
20. Nakanishi, H., Taylor, R. M., Chrest, F. J., Masui, T., Utsumi, K., Tatamatsu, M., and Passaniti, A. Progression of hormone-dependent adenocarcinoma cells to hormone-independent spindle carcinoma cells in vitro in a clonal spontaneous rat mammary tumor cell line. Cancer Res., 55: 399-407, 1995.
21. Lyons, J. G., Siew, K., and O'Grady, R. L. Cellular interactions determining the production of collagenase by a rat mammary carcinoma cell line. Int. J. Cancer, 43: 119-125, 1989.
22. Stevenson, G. A., Lyons, J. G., Cameron, D. A., and O'Grady, R. L. Rat carcinoma cells in long-term, serum-free culture provide a continuing supply of collagenase. Biosci. Rep., 5: 1071-1077, 1985.
23. Nethery, A., Lyons, J. G., and O'Grady, R. L. A spectrophotometric collagenase assay. Anal. Biochem., 159: 390-395, 1986.
24. Chomczynski, P., and Sacchi, N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162: 156-159, 1987.
25. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.), 227: 680-685, 1970.
26. Lyons, J. G., Birkedal-Hansen, B., Moore, W. G. I., O'Grady. R. L., and Birkedal-Hansen, H. Characteristics of a 95kDa matrix metalloproteinase produced by mammary carcinoma cells. Biochemistry, 30: 1449-1456, 1991.
27. Sanchez-Lopez, R., Nicholson, R., Gesnel, M-C., Matrisian, L. M., and Breathnach, R. Structure-function relationships in the collagenase family member transin. J. Biol. Chem., 263: 11892-11899, 1988.
28. Birchmeier, C., Birchmeier, W., and Brand-Saberi, B. Epithelial-mesenchymal transitions in cancer progression. Acta Anat., 156: 217-226, 1996.
29. Zhang, L., Zhou, W., Velculescu, V. E., Kern, S. E., Hruban, R. H., Hamilton, S. R., Vogelstein, B., and Kinzler, K. W. Gene expression profiles in normal and cancer cells. Science (Washington DC), 276: 1268-1272, 1997.
30. Nagase, H., Enghild, J. J., Suzuki, K., and Salvesen, G. Stepwise activation mechanisms of the precursor of matrix metalloproteinase 3 (stromelysin) by proteinases and (4-aminophenyl)mercuric acetate. Biochemistry, 29: 5783-5789, 1990.
31. O'Grady, R. L., Upfold, L. I., and Stephens, R. W. Rat mammary carcinoma cells secrete active collagenase and activate latent enzyme in the stroma via plasminogen activator. Int. J. Cancer, 28: 509-515, 1981.
32. Lyons, J. G., Nethery, A., Harrop, P. J., and O'Grady, R. L. The collagenase produced by neoplastic rat epithelial cells: modulation of secretion, molecular weight characteristics and purification. Matrix, 9: 7-16, 1989.
33. Uría, J. A., Stahle-Bäckdahl, M., Seiki, M., Fueyo, A., and López-Otín, C. Regulation of collagenase-3 expression in human breast carcinomas is mediated by stromal-epithelial cell interactions. Cancer Res., 57: 4882-4888, 1997.
34. Ito, A., Nakajima, S., Sasaguri, Y., Nagase, H., and Mori, Y. Co-culture of human breast adenocarcinoma MCF-7 cells and human dermal fibroblasts enhances the production of matrix metalloproteinases 1, 2 and 3 in fibroblasts. Br. J. Cancer, 71: 1039-1045, 1995.
35. Newell, K. J., Witty, J. P., Rodgers, W. H., and Matrisian, L. M. Expression and localization of matrix-degrading metalloproteinases during colorectal tumorigenesis. Mol. Carcinog., 10: 199-206, 1994.
36. Matrisian, L. M., Bowden, G. T., Krieg, P., Furstenberger, G., Briand, J. P., LeRoy, P., and Breathnach, R. The mRNA coding for the secreted protease transin is expressed more abundantly in malignant than benign tumours. Proc. Natl Acad. Sci. USA, 83: 9413-9417, 1986.
37. Paine, M. L., Gibbins, J. R., Chew, K. E., Demetriou, A., and Kefford, R. F. Loss of keratin expression in anaplastic carcinoma cells due to posttranscriptional down-regulation acting in trans. Cancer Res., 52: 6603-6611, 1992.
38. Paine, M. L., Gibbins, J. R., Whitelock, J. M., O'Grady, R. L., and Kefford, R. F. Unregulated and independent expression of collagenase and transin related to tumor progression. J. Natl. Cancer Inst., 85: 1425-1427, 1993.
39. Li, F., Strange, R., Friis, R. R., Djonov, V., Altermatt, H. J., Saurer, S., Niemann, H., and Andres, A. C. Expression of stromelysin-1 and TIMP-1 in the involuting mammary gland and in early invasive tumors of the mouse. Int. J. Cancer, 59: 560-568, 1994.
40. Nicholson, R. C., Murphy, G., and Breathnach, R. Human and rat malignant tumour-associated mRNAs encode stromelysin-like metalloproteinases. Biochemistry, 28: 5195-5203, 1989.
41. Muller, D., Quantin, B., Gesnel, M-C., Millom-Collard, R., Abecassis, J., and Breathnach, R. The collagenase gene family in humans consists of at least four members. Biochem. J., 253: 187-192, 1988.
42. Breathnach, R., Matrisian, L. M., Gesnel, M. C., Staub, A., and Leroy, P. Sequences coding for part of oncogene-induced transin are highly conserved in a related rat gene. Nucleic Acids Res., 15: 1139-1151, 1987.
43. Windsor, L. J., Grenett, H., Birkedal-Hansen, B., Bodden, M. K., Engler, J. A., and Birkedal-Hansen, H. Cell type-specific regulation of SL-1 and SL-2 genes. J. Biol. Chem., 268: 17341-17347, 1993.
44. Bernhard, E. J., Gruber, S. B., and Muschel, R. J. Direct evidence linking expression of matrix metalloproteinase 9 (92-kDa gelatinase/collagenase) to the metastatic phenotype in transformed rat embryo cells. Proc. Natl. Acad. Sci. USA, 91: 4293-4297, 1994.
45. Alessandro, R., Minafra, S., Pucci-Minafra, I., Onisto, M., Garbisa, S., Melchiori, A., Tetlow, L., and Woolley, D. E. Metalloproteinase, and TIMP expression by the human breast carcinoma cell line 8701-BC. Int. J. Cancer, 55: 250-255, 1993.
46. Nakajima, M., Lotan, D., Baig, M. M., Carralero, R. M., Wood, W. R., Hendrix, M. J., and Lotan, R. Inhibition by retinoic acid of type IV collagenolysis and invasion through reconstituted basement membrane by metastatic rat mammary adenocarcinoma cells. Cancer Res., 49: 1698-1706, 1989.
47. Iwata, H., Kobayashi, S., Iwase, H., Masaoka, A., Fujimoto, N., and Okada, Y. Production of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human breast carcinomas. Jap. J. Cancer Res., 87: 602-611, 1996.
48. Visscher, D. W., Hoyhtya, M., Ottosen, S. K., Liang, C. M., Sarkar, F. H., Crissman, J. D., and Fridman, R. Enhanced expression of tissue inhibitor of metalloproteinase-2 (TIMP-2) in the stroma of breast carcinomas correlates with tumor recurrence. Int. J. Cancer, 59: 339-344, 1994.
49. Soini, Y., Hurskainen, T., Hoyhtya, M., Oikarinen, A., and Autio-Harmainen, H. 72KD and 92KD type IV collagenase, type IV collagen, and laminin mRNAs in breast cancer: a study by in situ hybridization. J. Histochem. Cytochem., 42: 945-951, 1994.
50. Stetler-Stevenson, W. G., Brown, P. D., Onisto, M., Levy, A. T., and Liotta, L. A. Tissue inhibitor of metalloproteinases-2 (TIMP-2) mRNA expression in tumor cell lines and human tumor tissues. J. Biol. Chem., 265: 13933-13938, 1990.
51. Khokha, R., Waterhouse, P., Yagel, S., Lala, P. K., Overall, C. M., Norton, G., and Denhardt, D. T. Antisense RNA-induced reduction in murine TIMP levels confers oncogenicity on Swiss 3T3 cells. Science (Washington DC), 243: 947-950, 1989.
52. Strongin, A. Y., Marmer, B. L., Grant, G. A., and Goldberg, G. I. Plasma membrane-dependent activation of the 72-kDa type IV collagenase is prevented by complex formation with TIMP-2. J. Biol. Chem., 268: 14033-14039, 1993.
53. Murphy, G., Willenbrock, F., Ward, R. V., Cockett, M. I., Eaton, D., and Docherty, A. J. 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. Biochem. J., 283: 637-641, 1992.
54. O'Grady, R. L., and Cameron, D. A. Osteoclasts and the resorption of bone by transformed mammary carcinoma in rats. Br. J. Cancer, 51: 767-774, 1985.
55. Whitelock, J. M., O'Grady, R. L., and Gibbins, J. R. Interstitial collagenase (matrix metalloproteinase 1) associated with the plasma membrane of both neoplastic and nonneoplastic cells. Invasion Metastasis, 11: 139-148, 1991.
56. Vogelstein, B., and Kinzler, K. W. The multistep nature of cancer. Trends Genet., 9: 138-141, 1993.
57. Sonnenberg, A., van Balen, P., Hilgers, J., Schuuring, E., and Nusse, R. Oncogene expression during progression of mouse mammary tumor cells: activity of a proviral enhancer and the resulting expression of int-2 is influenced by the state of differentiation. EMBO J., 6: 121-125, 1987.
58. Bennett, D. C., Peachey, L. A., Durbin, H., and Rudland, P. S. A possible mammary stem cell line. Cell, 15: 283-298, 1978.
59. Whitehead, R. H., Bertoncello, I., Webber, L. M., and Pederson, J. S. A new human breast carcinoma cell line (PMC42) with stem cell characteristics. I. Morphologic characterization. J. Natl. Cancer Inst., 70: 649-661, 1983.
60. Heppner, G. H., Miller, B. E., and Miller, F. R. Tumor subpopulation interactions in neoplasms. Biochim. Biophys. Acta, 695: 215-226, 1983.
61. Pitts, W. C., Rojas, V. A., Gaffey, M. J., Rouse, R. V., Esteban, J., Frierson, H. F., Kempson, R. L., and Weiss, L. M. Carcinomas with metaplasia and sarcomas of the breast. Am. J. Clin. Pathol., 95: 623-632, 1991.
62. Sonnenberg, A., Daams, H., Calafat, J., and Hilgers, J. In vitro differentiation and progression of mouse mammary tumor cells. Cancer Res., 46: 5913-5922, 1986.
63. Gilles, C., Polette, M., Seiki, M., Birembaut, P., and Thompson, E. W. Implication of collagen type I-induced membrane-type 1-matrix metalloproteinase expression and matrix metalloproteinase-2 activation in the metastatic progression of breast carcinoma. Lab. Invest., 76: 651-660, 1997.
64. Gilles, C., Polette, M., Piette, J., Birembaut, P., and Foidart, J. M. Epithelial-to-mesenchymal transition in HPV-33-transfected cervical keratinocytes is associated with increased invasiveness and expression of gelatinase A. Int. J. Cancer, 59: 661-666, 1994.
65. Kataoka, H., DeCastro, R., Zucker, S., and Biswas, C. Tumor cell-derived collagenase-stimulatory factor increases expression of interstitial collagenase, stromelysin, and 72-kDa gelatinase. Cancer Res., 53: 3154-3158, 1993.