[en] Cell spreading and migration associated with the expression of the 92-kD gelatinase (matrix metalloproteinase 9 or MMP-9) are important mechanisms involved in the repair of the respiratory epithelium. We investigated the location of MMP-9 and its potential role in migrating human bronchial epithelial cells (HBEC). In vivo and in vitro, MMP-9 accumulated in migrating HBEC located at the leading edge of a wound and MMP-9 expression paralleled cell migration speed. MMP-9 accumulated through an actin-dependent pathway in the advancing lamellipodia of migrating cells and was subsequently found active in the extracellular matrix (ECM). Lamellipodia became anchored through primordial contacts established with type IV collagen. MMP-9 became amassed behind collagen IV where there were fewer cell-ECM contacts. Both collagen IV and MMP-9 were involved in cell migration because when cell-collagen IV interaction was blocked, cells spread slightly but did not migrate; and when MMP-9 activation was prevented, cells remained fixed on primordial contacts and did not advance at all. These observations suggest that MMP-9 controls the migration of repairing HBEC by remodeling the provisional ECM implicated in primordial contacts.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Legrand, C.
Gilles, Christine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Zahm, J. M.
Polette, M.
Buisson, A. C.
Kaplan, H.
Birembaut, P.
Tournier, J. L.
Language :
English
Title :
Airway epithelial cell migration dynamics. MMP-9 role in cell-extracellular matrix remodeling
Publication date :
1999
Journal title :
Journal of Cell Biology
ISSN :
0021-9525
eISSN :
1540-8140
Publisher :
Rockefeller University Press, New York, United States - New York
Abercombie, M., J.E.M. Heaysman, and S.M. Pegrum. 1970. The locomotion of fibroblasts in culture. Exp. Cell Res. 67:359-367.
Ågren, M.S. 1994. Gelatinase activity during wound healing. Br. J. Dermatol. 131:634-640.
Bendeck, M.P., N. Zempo, A.W. Clowes, R.E. Galardy, and M.A. Reidy. 1994. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ. Res. 75:539-545.
Brezillon, S., F. Dupuit, J. Hinnrasky, V. Marchand, N. Kälin, B. Tümmler, and E. Puchelle. 1995. Decreased expression of the CFTR protein in remodeled human nasal epithelium from non-cystic fibrosis patients. Lab. Invest. 72: 191-200.
Buisson, A.C., J.M. Zahm, M. Polette, D. Pierrot, G. Bellon, E. Puchelle, P. Birembaut, and J.M. Tournier. 1996a. Gelatinase B is involved in the in vitro wound repair of human respiratory epithelium. J. Cell. Physiol. 166:413-426.
Buisson, A.C., C. Gilles, M. Polette, J.M. Zahm, P. Birembaut, and J.M. Tournier. 1996b. Wound repair-induced expression of stromelysins is associated with the acquisition of a mesenchymal phenotype in human respiratory epithelial cells. Lab. Invest. 74:658-669.
Chambers, A.F., and L.M. Matrisian. 1997. Changing views of the role of matrix metalloproteinases in metastasis. J. Natl. Cancer Inst. 89:1260-1269.
Chintala, S.K., R. Sawaya, B.B. Aggarwal, S. Majumder, D.K. Giri, A.P. Kyritsis, Z.L. Gokaslan, and J.S. Rao. 1998. Induction of matrix metalloproteinase-9 requires a polymerized actin cytoskeleton in human malignant glioma cells. J. Biol. Chem. 273:13545-13551.
Delclaux, C., C. Delacourt, M.P. d'Ortho, V. Boyer, C. Lafuma, and A. Harf. 1996. Role of gelatinase B and elastase in human polymorphonuclear neutrophil migration across basement membrane. Am. J. Respir. Cell Mol. Biol. 14:288-295.
Erjefält, J.S., I. Erjefält, F. Sundler, and C.G.A. Persson. 1995. In vivo restitution of airway epithelium. Cell Tissue Res. 281:305-316.
Green, H., O. Kehinde, and J. Thomas. 1979. Growth of cultured human epidermal cells into multiple epithelia suitable for grafting. Proc. Natl. Acad. Sci. USA. 76:5665-5668.
Hérard, A.L., D. Pierrot, J. Hinnrasky, H. Kaplan, D. Sheppard, E. Puchelle, and J.M. Zahm. 1996a. Fibronectin and its α5β1-integrin receptor are involved in the wound-repair process of airway epithelium. Am. J. Physiol. 271:L726-L733.
Hérard, A.L., J.M. Zahm, D. Pierrot, J. Hinnrasky, C. Fuchey, and E. Puchelle. 1996b. Epithelial barrier integrity during in vitro wound repair of the airway epithelium. Am. J. Respir. Cell Mol. Biol. 15:624-632.
Jockusch, B.M., P. Bubeck, K. Giehl, M. Kroemker, J. Moshner, M. Rothkegel, M. Rüdiger, K. Schlüter, G. Stanke, and J. Winkler. 1995. The molecular architecture of focal adhesions. Annu. Rev. Cell Dev. Biol. 11:379-416.
Keenan, K.P., J.W. Combs, and E.M. McDowell. 1982. Regeneration of hamster tracheal epithelium after mechanical injury. I. Focal lesions: quantitative morphologic study of cell proliferation. Virchows Arch. B. 41:193-214.
Kelly, T., Y. Yan, R.L. Osborne, A.B. Athota, T.L. Rozypal, J.C. Colclasure, and W.S. Chu. 1998. Proteolysis of extracellular matrix by invadopodia facilitates human breast cancer cell invasion and is mediated by matrix metalloproteinases. Clin. Exp. Metastasis. 16:501-512.
Lane, B.P., and R. Gordon. 1974. Regeneration of rat tracheal epithelium after mechanical injury. The relationship between mitotic activity and cellular differentiation. Proc. Soc. Exp. Biol. Med. 145:1139-1144.
Lee, J., A. Ishihara, and K. Jacobson. 1993. How do cells move along surfaces? Trends Cell Biol. 3:366-370.
Leppert, D., E. Waubant, R. Galardy, N.W. Bunnett, and S.L. Hauser. 1995. T cell gelatinases mediate basement membrane transmigration in vitro. J. Immunol. 154:4379-4389.
Man, S.F.P., and W.C. Hulbert. 1988. Airway repair and adaptation to inhalation injury. In Pathophysiology and Treatment of Inhalation Injuries. Lung Biology in Health and Disease. J. Loke, editor. Marcel Dekker, New York. 1-47.
Matsubara, M., M.T. Girard, C.L. Kublin, C. Cintron, and M.E. Fini. 1991. Differential roles for two gelatinolytic enzymes of the matrix metalloproteinase family in the remodeling cornea. Dev. Biol. 147:425-439.
McCawley, L.J., P. O'Brien, and L.G. Hudson. 1998. Epidermal growth factor (EGF)- and scatter factor/hepatocyte growth factor (SF/HGF)-mediated keratinocyte migration is coincident with induction of matrix metalloproteinase (MMP-9). J. Cell. Physiol. 176:255-265.
McDowell, E.M., P.J. Becci, W. Schurch, and B.F. Trump. 1979. The respiratory epithelium. VII. Epidermoid metaplasia of hamster tracheal epithelium during regeneration following mechanical injury. J. Natl. Cancer Inst. 62: 995-1008.
Nguyen, M., J. Arkell, and C.J. Jackson. 1998. Active and tissue inhibitor of matrix metalloproteinase-free gelatinase B accumulates within human microvascular endothelial vesicles. J. Biol. Chem. 273:5400-5404.
Nikula, K.J., D.W. Wilson, S.N. Giri, C.G. Plopper, and D.L. Dungworth. 1988. The response of the rat tracheal epithelium to ozone exposure: injury, adaptation and repair. Am. J. Pathol. 131:373-384.
Nordin, U., B. Engström, B. Jansson, and C.E. Lindholm. 1977. Surface structure and vascular anatomy of the tracheal wall under normal conditions and after intubation. Acta Anaesthesiol. Scand. 345(Suppl.):35-56.
Oikarinen, A., M. Kylmäniemi, H. Autio-Harmainen, P. Autio, and T. Salo. 1993. Demonstration of 72-kDa and 92-kDa forms of type IV collagenase in human skin: variable expression in various blistering diseases, induction during re-epithelialization, and decrease by topical glucocorticoids. J. Invest. Dermatol. 101:205-210.
Okada, S., H. Kita, J. George, G.J. Gleich, and K. Leiferman. 1997. Migration of eosinophils through basement membrane components in vitro: role of matrix metalloproteinase-9. Am. J. Respir. Cell Mol. Biol. 17:519-528.
Partridge, C.A., P.G. Phillips, M.J. Niedbala, and J.J. Jeffrey. 1997. Localization and activation of type IV collagenase/gelatinase at endothelial focal contacts. Am. J. Physiol. 272:L813-L822.
Pluznik, D.H., R. Fridman, and R. Reich. 1992. Correlation in the expression of type IV collagenase and the invasive and chemotactic abilities of myelomonocytic cells differentiation into macrophages. Exp. Hematol. 20:57-63.
Ramos-DeSimone, N., U.M. Moll, J.P. Quigley, and D.L. French. 1993. Inhibition of matrix metalloproteinase 9 activation by a specific monoclonal antibody. Hybridoma. 12:349-363.
Roger, P., E. Puchelle, O. Bajolet-Laudinat, J.-M. Tournier, C. Debordeaux, M.-C. Plotkowski, J.H.M. Cohen, D. Sheppard, and S. de Bentzmann. 1999. Fibronectin and the α5β1 integrin mediate binding of Pseudomonas aeruginosa to repairing airway epithelium. Eur. Respir. J. In press.
Saarialho-Kere, U.K., S.O. Kovacs, A.P. Pentland, J.E. Olerud, H.G. Welgus, and W.C. Parks. 1993. Cell-matrix interactions modulate interstitial collagenase expression by human keratinocytes actively involved in wound healing. J. Clin. Invest. 92:2858-2866.
Salo, T., M. Mäkelä, M. Kylmäniemi, H. Autio-Harmainen, and H. Larjava. 1994. Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab. Invest. 70:176-182.
Small, J.V., K. Anderson, and K. Rottner. 1996. Actin and the coordination of protrusion, attachment and retraction in cell crawling. Biosci. Rep. 16:351-368.
Starkey, J.R., H.L. Hosick, D.R. Stanford, and H.D. Liggitt. 1984. Interaction of metastatic tumor cells with bovine lens capsule basement membrane. Cancer Res. 44:1585-1594.
Stricklin, G.P., L. Li, and L.B. Nanney. 1994. Localization of mRNAs representing interstitial collagenase, 72-kDa gelatinase, and TIMP in healing porcine burn wounds. J. Invest. Dermatol. 103:352-358.
Uhm, J.H., N.P. Dooley, L.Y.S. Oh, and V.W. Yong. 1998. Oligodendrocytes utilize a matrix metalloproteinase. MMP-9, to extend processes along an astrocyte extracellular matrix. Glia. 22:53-63.
Vu, T.H., and Z. Werb. 1998. Gelatinase B: structure, regulation and function. In Matrix Metalloproteinases (Biology of Extracellular Matrix Series). W.C. Parks and R.P. Mecham, editors. Academic Press, New York. 115-148.
Wilhelm, D.L. 1953. Regeneration of tracheal epithelium. J. Pathol. Bacteriol. 5025:543-550.
Woessner, J.F. 1998. The matrix metalloproteinase family. In Matrix Metalloproteinases (Biology of Extracellular Matrix Series). W.C. Parks and R.P. Mecham, editors. Academic Press, New York. 1-14.
Yao, P.M., C. Delclaux, M.P. d'Ortho, B. Maitre, A. Harf, and C. Lafuma. 1998. Cell-matrix interactions modulate 92-kD gelatinase expression by human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 18:813-822.
Zahm, J.M., M. Chevillard, and E. Puchelle. 1991. Wound repair of human surface respiratory epithelium. Am. J. Respir. Cell Mol. Biol. 5:242-248.
Zahm, J.M., H. Kaplan, A.L. Hérard, F. Doriot, D. Pierrot, P. Somelette, and E. Puchelle. 1997. Cell migration and proliferation during the in vitro wound repair of the respiratory epithelium. Cell Motil. Cytoskelet. 37:33-43.
