Expression of collagenases-1 and -3 and their inhibitors TIMP-1 and -3 correlates with the level of invasion in malignant melanomas

Abstract

Since proteolysis of the dermal collagenous matrix and basement membranes is required for local invasive growth and early metastasis formation of cutaneous melanomas, we have analysed the activities/expression levels of certain metalloproteinases in melanomas and cultured melanoma cells by in situ hybridization and Northern analysis. In addition to collagenases-1 and -3 that have been implicated in invasive growth behaviour of various malignant tumours, we analysed the levels of 72-kDa gelatinase and its activators MT1-MMP and TIMP-2 in cultured melanoma cells. The lesions examined included three cases of lentigo maligna and 28 cases of Clark grade I-V melanomas. The premalignant as well as the grade I tumours were consistently negative for collagenase-1 and -3 and TIMP-1 and -3. The collagenases were predominantly expressed in the cancer cells of Clark grade III and IV tumours. TIMP-1 and -3 were abundantly expressed in the cancer and/or stromal cells of grade III and IV melanomas, while TIMP-2 protein was detected also in melanomas representing lower invasive potential. Northern analysis of seven melanoma cell lines showed that the expression of collagenase-1 and TIMPs-1 and -3 was associated with 72-kDa gelatinase positivity. All melanoma cell lines were positive for MT1-MMP and TIMP-2 mRNAs. Our results suggest that overexpression of collagenases-1 and -3 and TIMPs-1 and -3 is induced during melanoma progression. Expression of TIMPs may reflect host response to tumour invasion in an effort to control MMP activity and preserve extracellular matrix integrity.

References 54

1. 1.

   Ahonen M., Baker A. H., Kähäri V. M. Adenovirus-mediated gene delivery of tissue inhibitor of metalloproteinases-3 inhibits invasion and induces apoptosis in melanoma cells. Cancer Res. 1998;58(11):2310-2315.

   Not in our library

2. 2.

   Airola K., Ahonen M., Johansson N., Heikkilä P., Kere J., Kähäri V. M., Saarialho-Kere U. K. Human TIMP-3 is expressed during fetal development, hair growth cycle, and cancer progression. J Histochem Cytochem. 1998;46(4):437-447.

   Not in our library10.1177/002215549804600403

3. 3.

   Airola K., Johansson N., Kariniemi A. L., Kähäri V. M., Saarialho-Kere U. K. Human collagenase-3 is expressed in malignant squamous epithelium of the skin. J Invest Dermatol. 1997;109(2):225-231.

   Not in our library10.1111/1523-1747.ep12319441

4. 4.

   Anand-Apte B., Bao L., Smith R., Iwata K., Olsen B. R., Zetter B., Apte S. S. A review of tissue inhibitor of metalloproteinases-3 (TIMP-3) and experimental analysis of its effect on primary tumor growth. Biochem Cell Biol. 1996;74(6):853-862.

   Not in our library10.1139/o96-090

5. 5.

   Anand-Apte B., Pepper M. S., Voest E., Montesano R., Olsen B., Murphy G., Apte S. S., Zetter B. Inhibition of angiogenesis by tissue inhibitor of metalloproteinase-3. Invest Ophthalmol Vis Sci. 1997;38(5):817-823.

   Not in our library

6. 6.

   Birkedal-Hansen H., Moore W. G., Bodden M. K., Windsor L. J., Birkedal-Hansen B., DeCarlo A., Engler J. A. Matrix metalloproteinases: a review. Crit Rev Oral Biol Med. 1993;4(2):197-250.

   Not in our library10.1177/10454411930040020401

7. 7.

   Breslow A. Thickness, cross-sectional areas and depth of invasion in the prognosis of cutaneous melanoma. Ann Surg. 1970;172(5):902-908.

   Not in our library10.1097/00000658-197011000-00017

8. 8.

   Brooks P. C., Strömblad S., Sanders L. C., von Schalscha T. L., Aimes R. T., Stetler-Stevenson W. G., Quigley J. P., Cheresh D. A. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell. 1996;85(5):683-693.

   Not in our library10.1016/s0092-8674(00)81235-0

9. 9.

   Brown P. D., Levy A. T., Margulies I. M., Liotta L. A., Stetler-Stevenson W. G. Independent expression and cellular processing of Mr 72,000 type IV collagenase and interstitial collagenase in human tumorigenic cell lines. Cancer Res. 1990;50(19):6184-6191.

   Not in our library

10. 10.

    Butler G. S., Butler M. J., Atkinson S. J., Will H., Tamura T., Schade van Westrum S., Crabbe T., Clements J., d'Ortho M. P., Murphy G. The TIMP2 membrane type 1 metalloproteinase "receptor" regulates the concentration and efficient activation of progelatinase A. A kinetic study. J Biol Chem. 1998;273(2):871-880.

    Not in our library10.1074/jbc.273.2.871

11. 11.

    Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162(1):156-159.

    Not in our library10.1006/abio.1987.9999

12. 12.

    Clark W. H., From L., Bernardino E. A., Mihm M. C. The histogenesis and biologic behavior of primary human malignant melanomas of the skin. Cancer Res. 1969;29(3):705-727.

    Not in our library

13. 13.

    Collier I. E., Wilhelm S. M., Eisen A. Z., Marmer B. L., Grant G. A., Seltzer J. L., Kronberger A., He C. S., Bauer E. A., Goldberg G. I. H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen. J Biol Chem. 1988;263(14):6579-6587.

    Not in our library

14. 14.

    Deryugina E. I., Luo G. X., Reisfeld R. A., Bourdon M. A., Strongin A. Tumor cell invasion through matrigel is regulated by activated matrix metalloproteinase-2. Anticancer Res. 1997;17(5A):3201-3210.

    Not in our library

15. 15.

    Durko M., Navab R., Shibata H. R., Brodt P. Suppression of basement membrane type IV collagen degradation and cell invasion in human melanoma cells expressing an antisense RNA for MMP-1. Biochim Biophys Acta. 1997;1356(3):271-280.

    Not in our library10.1016/s0167-4889(97)00004-9

16. 16.

    Fong K. M., Kida Y., Zimmerman P. V., Smith P. J. TIMP1 and adverse prognosis in non-small cell lung cancer. Clin Cancer Res. 1996;2(8):1369-1372.

    Not in our library

17. 17.

    Fort P., Marty L., Piechaczyk M., el Sabrouty S., Dani C., Jeanteur P., Blanchard J. M. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res. 1985;13(5):1431-1442.

    Not in our library10.1093/nar/13.5.1431

18. 18.

    Freije J. M., Díez-Itza I., Balbín M., Sánchez L. M., Blasco R., Tolivia J., López-Otín C. Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem. 1994;269(24):16766-16773.

    Not in our library

19. 19.

    Gomez D. E., Alonso D. F., Yoshiji H., Thorgeirsson U. P. Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol. 1997;74(2):111-122.

    Not in our library

20. 20.

    Herlyn M., Balaban G., Bennicelli J., Guerry D., Halaban R., Herlyn D., Elder D. E., Maul G. G., Steplewski Z., Nowell P. C. Primary melanoma cells of the vertical growth phase: similarities to metastatic cells. J Natl Cancer Inst. 1985;74(2):283-289.

    Not in our library

21. 21.

    Herlyn M., Thurin J., Balaban G., Bennicelli J. L., Herlyn D., Elder D. E., Bondi E., Guerry D., Nowell P., Clark W. H. Characteristics of cultured human melanocytes isolated from different stages of tumor progression. Cancer Res. 1985;45(11 Pt 2):5670-5676.

    Not in our library

22. 22.

    Höyhtyä M., Hujanen E., Turpeenniemi-Hujanen T., Thorgeirsson U., Liotta L. A., Tryggvason K. Modulation of type-IV collagenase activity and invasive behavior of metastatic human melanoma (A2058) cells in vitro by monoclonal antibodies to type-IV collagenase. Int J Cancer. 1990;46(2):282-286.

    Not in our library10.1002/ijc.2910460224

23. 23.

    Iliopoulos D., Ernst C., Steplewski Z., Jambrosic J. A., Rodeck U., Herlyn M., Clark W. H., Koprowski H., Herlyn D. Inhibition of metastases of a human melanoma xenograft by monoclonal antibody to the GD2/GD3 gangliosides. J Natl Cancer Inst. 1989;81(6):440-444.

    Not in our library10.1093/jnci/81.6.440

24. 24.

    Johansson N., Airola K., Grénman R., Kariniemi A. L., Saarialho-Kere U., Kähäri V. M. Expression of collagenase-3 (matrix metalloproteinase-13) in squamous cell carcinomas of the head and neck. Am J Pathol. 1997;151(2):499-508.

    Not in our library

25. 25.

    Johnson M. D., Kim H. R., Chesler L., Tsao-Wu G., Bouck N., Polverini P. J. Inhibition of angiogenesis by tissue inhibitor of metalloproteinase. J Cell Physiol. 1994;160(1):194-202.

    Not in our library10.1002/jcp.1041600122

26. 26.

    Khokha R. Suppression of the tumorigenic and metastatic abilities of murine B16-F10 melanoma cells in vivo by the overexpression of the tissue inhibitor of the metalloproteinases-1. J Natl Cancer Inst. 1994;86(4):299-304.

    Not in our library10.1093/jnci/86.4.299

27. 27.

    Knäuper V., Cowell S., Smith B., López-Otin C., O'Shea M., Morris H., Zardi L., Murphy G. The role of the C-terminal domain of human collagenase-3 (MMP-13) in the activation of procollagenase-3, substrate specificity, and tissue inhibitor of metalloproteinase interaction. J Biol Chem. 1997;272(12):7608-7616.

    Not in our library10.1074/jbc.272.12.7608

28. 28.

    Knäuper V., López-Otin C., Smith B., Knight G., Murphy G. Biochemical characterization of human collagenase-3. J Biol Chem. 1996;271(3):1544-1550.

    Not in our library10.1074/jbc.271.3.1544

29. 29.

    Kähäri V. M., Saarialho-Kere U. Matrix metalloproteinases in skin. Exp Dermatol. 1997;6(5):199-213.

    Not in our library10.1111/j.1600-0625.1997.tb00164.x

30. 30.

    Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680-685.

    Not in our library10.1038/227680a0

31. 31.

    Lehti K., Lohi J., Valtanen H., Keski-Oja J. Proteolytic processing of membrane-type-1 matrix metalloproteinase is associated with gelatinase A activation at the cell surface. Biochem J. 1998;334(Pt 2):345-353.

    Not in our library10.1042/bj3340345

32. 32.

    Llano E., Pendás A. M., Knäuper V., Sorsa T., Salo T., Salido E., Murphy G., Simmer J. P., Bartlett J. D., López-Otín C. Identification and structural and functional characterization of human enamelysin (MMP-20). Biochemistry. 1997;36(49):15101-15108.

    Not in our library10.1021/bi972120y

33. 33.

    Lohi J., Harvima I., Keski-Oja J. Pericellular substrates of human mast cell tryptase: 72,000 dalton gelatinase and fibronectin. J Cell Biochem. 1992;50(4):337-349.

    Not in our library10.1002/jcb.240500402

34. 34.

    Lohi J., Keski-Oja J. Calcium ionophores decrease pericellular gelatinolytic activity via inhibition of 92-kDa gelatinase expression and decrease of 72-kDa gelatinase activation. J Biol Chem. 1995;270(29):17602-17609.

    Not in our library10.1074/jbc.270.29.17602

35. 35.

    Lohi J., Lehti K., Westermarck J., Kähäri V. M., Keski-Oja J. Regulation of membrane-type matrix metalloproteinase-1 expression by growth factors and phorbol 12-myristate 13-acetate. Eur J Biochem. 1996;239(2):239-247.

    Not in our library10.1111/j.1432-1033.1996.0239u.x

36. 36.

    MacDougall J. R., Bani M. R., Lin Y., Rak J., Kerbel R. S. The 92-kDa gelatinase B is expressed by advanced stage melanoma cells: suppression by somatic cell hybridization with early stage melanoma cells. Cancer Res. 1995;55(18):4174-4181.

    Not in our library

37. 37.

    Mimori K., Mori M., Shiraishi T., Fujie T., Baba K., Haraguchi M., Abe R., Ueo H., Akiyoshi T. Clinical significance of tissue inhibitor of metalloproteinase expression in gastric carcinoma. Br J Cancer. 1997;76(4):531-536.

    Not in our library10.1038/bjc.1997.420

38. 38.

    Montgomery A. M., De Clerck Y. A., Langley K. E., Reisfeld R. A., Mueller B. M. Melanoma-mediated dissolution of extracellular matrix: contribution of urokinase-dependent and metalloproteinase-dependent proteolytic pathways. Cancer Res. 1993;53(3):693-700.

    Not in our library

39. 39.

    Mueller B. M. Different roles for plasminogen activators and metalloproteinases in melanoma metastasis. Curr Top Microbiol Immunol. 1996;213(Pt 1):65-80.

    Not in our library10.1007/978-3-642-61107-0_5

40. 40.

    Murphy G., Knäuper V. Relating matrix metalloproteinase structure to function: why the "hemopexin" domain? Matrix Biol. 1997;15(8-9):511-518.

    Not in our library10.1016/s0945-053x(97)90025-1

Cited by papers we hold 1

• Tumor-derived matrix metalloproteinase-13 (MMP-13) correlates with poor prognosis of invasive breast cancer · 2008
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