[en] The basement membrane (BM) is the first barrier encountered by tumor cells when they become invasive. Moreover, some invasive tumor clusters are surrounded by a remnant or neosynthetized BM material. We have previously reported the presence of a particular alpha chain of type IV collagen, the alpha3(IV) chain, in bronchopulmonary carcinomas. This chain was not detected in the normal bronchial epithelium, but was found around some invasive tumor cluster BM. In the present study, we examined the effects of the alpha3(IV) chain on the invasive properties of bronchial tumor cell lines, with special emphasis on their expression of matrix metalloproteinase-2 (MMP-2) and its activator, membrane type 1-matrix metalloproteinase (MT1-MMP), which is largely involved in tumor progression. Two epithelial bronchial cell lines (16HBE14o- and BZR), showing different invasive abilities, were evaluated. Using the Boyden chamber invasion assay, we demonstrated that the alpha3(IV) chain inhibits the invasive properties of BZR cells and modifies their morphology by inducing an epithelial cell shape. In the presence of the recombinant NC1 domain of the alpha3(IV) chain, the expression of MMP-2 and tissue inhibitor of metalloproteinase-2 (TIMP-2) was not modified in either cell line. The NC1 alpha3(IV) domain did not modulate the MT1-MMP expression of noninvasive 16HBE14o- cells, whereas a 50% decrease of MT1-MMP mRNA was observed in invasive BZR cells. Accordingly, Western blot analyses showed a disappearance of the 45-kd MT1-MMP form when BZR cells were treated with the recombinant NC1 alpha3(IV) domain. These findings suggest that the alpha3 chain of type IV collagen may play a role in tumor invasion, at least by decreasing the expression and synthesis of MT1-MMP.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Martinella-Catusse, C.
Polette, M.
Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme
Gilles, Christine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Dehan, Pierre ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques
Munaut, Carine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Colige, Alain ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Laboratoire de biologie des tissus conjonctifs
Volders, Laure ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique - Labo de biologie des tumeurs et du développement
Birembaut, P.
Language :
English
Title :
Down-Regulation of MT1-MMP expression by the alpha3 chain of type IV collagen inhibits bronchial tumor cell line invasion
Publication date :
2001
Journal title :
Laboratory Investigation
ISSN :
0023-6837
eISSN :
1530-0307
Publisher :
Lippincott Williams & Wilkins, Hagerstown, United States - Maryland
Butkowski R.J., Langeveld J.P., Wieslander J., Hamilton J., Hudson B.G. (1987) Localization of the Goodpasture epitope to a novel chain of basement membrane collagen. J Biol Chem 262:7874-7877.
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. (1998) The TIMP2 membrane type I metalloproteinase receptor regulates the concentration and efficient activation of gelatinase A. A kinetic study. J Biol Chem 273:871-880.
Catusse C., Polette M., Coraux C., Burlet H., Birembaut P. (2000) Modified basement membrane composition during bronchopulmonary tumor progression. J Histochem Cytochem 48:663-669.
Chelberg M.K., Tsilibary E.C., Hauser A.R., McCarthy J.B. (1989) Type IV collagen-mediated melanoma cell adhesion and migration: Involvement of multiple, distinct domains of the collagen molecule. Cancer Res 49:4796-4802.
Cosgrove D., Samuelson G., Meehan D.T., Miller C., McGee J., Walsh E., Siegel M. (1998) Ultrastructural, physiological, and molecular defects in the inner ear of a gene-knockout mouse model for autosomal Alport syndrome. Hear Res 121:84-98.
Dehan P., Weber M., Zhang Xu., Reeders S.T., Foidart J.M., Tryggvason K. (1996) Sera from patients with anti-GBM nephritis including Goodpasture syndrome show heterogenous reactivity to recombinant NC1 domain of type IV collagen α chains. Nephrol Dial Transplant 11:2215-2222.
Fridman R., Kibbey M.C., Royce L.S., Zain M., Sweeney T.M. (1991) Enhanced tumor growth of both primary and established human and murine tumor cells in athymic mice after coinjection with Matrigel. J Natl Cancer Inst 83:769-774.
Gilles C., Bassuk J.A., Pulyaeva H., Sage E.H., Foidart J.M., Thompson E.W. (1998) Sparc/octeonectin induces matrix metalloproteinase 2 activation in human breast cancer cell lines. Cancer Res 58:5529-5536.
Gilles C., Polette M., Piette J., Munaut C., Thompson E.W., Birembaut P., Foidart J.M. (1996) High level of MT-MMP expression is associated with invasiveness of cervical cancer cells. Int J Cancer 65:209-213.
Gilles C., Polette M., Seiki M., Birembaut P., Thompson E.W. (1997) Implication of collagen type I-induced membrane-type 1-metalloproteinase expression and matrix metalloproteinase-2 activation in the metastatic progression of breast carcinoma. Lab Invest 76:651-660.
Han J., Ohno N., Pasco S., Monboisse J.C., Borel J.P., Kefalides N.A. (1997) A cell binding domain from the α3 chain of type IV collagen inhibits proliferation of melanoma cells. J Biol Chem 272:20395-20401.
Hostikka S.L., Eddy R.L., Byers M.G., Hoyhtya M., Shows T.B., Tryggvason K. (1990) Identification of a distinct type IV collagen α chain with restricted kidney distribution and assignment of its gene to the locus of X chromosome-linked Alport syndrome. Proc Natl Acad Sci USA 87:1606-1610.
Imai K., Ohuchi E., Aoki T., Nomura H., Fujii Y., Sato H., Seiki M., Okada Y. (1996) Membrane type matrix metalloproteinase 1 is a gelatinolytic enzyme and is secreted in a complex with tissue inhibitor of metalloproteinase 2. Cancer Res 56:2707-2710.
Kim W.H., Jun S.H., Kibbey M.C., Thompson E.W., Kleiman H.K. (1994) Expression of β1 integrin in lamin-adhesion-selected human colon cancer cell lines of varying tumorigenicity. Invasion Metastasis 14:147-155.
Koshikawa N., Gianelli G., Cirulli V., Miyazaki K., Quaranta V. (2000) Role of cell surface MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 148:615-624.
Kurschat P., Zigrino P., Nischt R., Breitkopf K., Steurer P., Klein C.E., Krieg T., Mauch C. (1999) Tissue inhibitor of matrix metalloproteinase-2 regulates matrix metalloproteinase-2 activation by modulation of membrane-type 1 matrix metalloproteinase activity in high and low invasive melanoma cell lines. J Biol Chem 274:21056-21062.
Li C., McCarthy J.B., Furcht L.T., Fields G.B. (1997) An all-D amino acid peptide model of α1(IV)531-543 from type IV collagen binds the α3β1 integrin and mediates tumor cell adhesion, spreading and motility. Biochemistry 36:15404-15410.
Lohi J., Lehti K., Westermarck J., Kahari V.M., Keski-Oja J. (1996) Regulation of membrane-type matrix metalloproteinase-1 expression by growth factors and phorbol 12-myristate 13-acetate. Eur J Biochem 239:239-247.
Miner J.H., Saus J.R. (1994) Collagen α3, α4 and α5 chains in rodent BL: Sequence, distribution, association with laminins and developmental switches. J Cell Biol 121:879-891.
Miner J.H., Saus J.R. (1996) Molecular and functional defects in Kidneys of mice lacking collagen α3(IV): Implication for Alport syndrome. J Cell Biol 135:1403-1413.
Monboisse J.C., Garnotel R., Bellon G., Ohno N., Perreau C., Borel J.P., Kefalides N.A. (1994) The α3 chain of type IV collagen prevents activation of human polymorphonuclear leukocytes. J Biol Chem 269:25475-25482.
Nawrocki B., Polette M., Marchand V., Monteau M., Gillery P., Tournier J.M., Birembaut P. (1997) Expression of matrix metalloproteinases and their inhibitors in human bronchopulmonary carcinomas: Quantitative and morphological analyses. Int J Cancer 72:556-564.
Ninomiya Y., Kagawa M., Iyama K.I., Naito I., Kishiro Y., Seyer J., Sugimoto M., Oohashi T., Sado Y. (1995) Differential expression of two basement membrane collagen genes COL4A6 and COL4A5, demonstrated by immunofluorescence staining using peptide-specific monoclonal antibodies. J Cell Biol 130:1219-1229.
Ohuchi E., Imai K., Fujii Y., Sato H., Seiki M., Okada Y. (1997) Membrane type matrix metalloproteinase digests interstitial collagen and other extracellular matrix macromolecules. J Biol Chem 272:2446-2451.
Pasco S., Han J., Gillery P., Bellon G., Maquart F.X., Borel J.P., Kefalides N.A., Monboisse J.C. (2000) A specific sequence of the noncollagenous domain of the α3 (IV) chain of type IV collagen inhibits expression and activation of matrix metalloproteinases by tumor cells. Cancer Res 60:467-473.
Pei D., Weiss S.J. (1996) Transmembrane-deletion mutants of the membrane type matrix metalloproteinase-1 process progelatinase A and express intrinsic matrix-degrading activity. J Biol Chem 271:9135-9140.
Petitclerc E., Boutaud A., Prestayko A., Xu J., Sado Y., Ninomiya Y., Sarras M.P., Hudson B.G., Brooks P.C. (2000) New functions for non-collagenous domains of human collagen type IV. J Biol Chem 275:8051-8061.
Polette M., Gilles C., De Bentzmann S., Gruenert D., Tournier J.M., Birembaut P. (1998) Association of fibroblastoid features with the invasive phenotype in human bronchial cancer cell lines. Clin Exp Metastasis 16:105-112.
Polette M., Thiblet J., Ploton D., Buisson A.C., Monboisse J.C., Tournier J.M., Birembaut P. (1997) Distribution of α1(IV) and α3 (IV) chains of type IV collagen in lung tumours. J Pathol 182:185-191.
Sato H., Kinoshita T., Takino T., Nakayama K., Seiki M. (1996) Activation of a recombinant membrane type 1-matrix metalloproteinase (MT1-MMP) by furin and its interaction with tissue inhibitor of metalloproteinases (TIMP-2). FEBS Lett 393:101-104.
Sato H., Takino T., Okada Y., Cao J., Shinagawa A., Yamamoto E., Seiki M. (1994) A matrix metalloproteinase expressed on the surface of invasive tumor cells. Nature 370:61-65.
Smith D.B., Johnson K.S. (1988) Single-step purification of polypeptides expressed in Escherichia coli in fusions with glutathione S-transferase. Gene 67:31-40.
Stanton H., Gavrilovic J., Atkinson S.T., D'Ortho M.P., Yamada K.M., Zardi L., Murphy G. (1998) The activation of proMMP-2 (gelatinase A) by HT1080 fibrosarcoma cells is promoted by culture on a fibronectin substrate and is concomitant with an increase in processing of MT1-MMT (MMP-14) to a 45 kDa form. J Cell Sci 111:2789-2798.
Strongin A.Y., Colloer I., Bannikov G., Marmer B.L., Grant G.A., Goldberg G.I. (1995) Mechanism of cell surface activation of 72-Kda type IV collagenase. J Biol Chem 270:5331-5338.
Terranova V.P., Williams J.E., Liotta L.A., Martin G.R. (1984) Modulation of the metastatic activity of melanoma cells by laminin and fibronectin. Science 226:982-985.
