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J Biol Chem, Vol. 273, Issue 17, 10672-10681, April 24, 1998

High Affinity Binding of Latent Matrix Metalloproteinase-9 to the 2(IV) Chain of Collagen IV

Matthew W. Olson, Marta Toth, David C. Gervasi, Yoshikazu Sado^¶, Yoshifumi Ninomiya, and Rafael Fridman

From the  Department of Pathology and the Karmanos Cancer Institute, Wayne State University, Detroit, Michigan 48201, the ^¶ Division of Immunology Shigei Medical Research Institute 2117 Yamada, Okayama 701-02, Japan, and the  Department of Molecular Biology and Biochemistry, Okayama University Medical School, Shikata-cho, Okayama 700, Japan

Association of matrix metalloproteinases (MMPs) with the cell surface and with areas of cell-matrix contacts is critical for extracellular matrix degradation. Previously, we showed the surface association of pro-MMP-9 in human breast epithelial MCF10A cells. Here, we have characterized the binding parameters of pro-MMP-9 and show that the enzyme binds with high affinity (K_d ~22 nM) to MCF10A cells and other cell lines. Binding of pro-MMP-9 to MCF10A cells does not result in zymogen activation and is not followed by ligand internalization, even after complex formation with tissue inhibitor of metalloproteinase-1 (TIMP-1). A 190-kDa cell surface protein was identified by ligand blot analysis and affinity purification with immobilized pro-MMP-9. Microsequencing and immunoblot analysis revealed that the 190-kDa protein is the 2(IV) chain of collagen IV. Specific pro-MMP-9 surface binding was competed with purified 2(IV) and was significantly reduced after treatment of the cells with active MMP-9 before the binding assay since 2(IV) is hydrolyzed by MMP-9. A pro-MMP-9·TIMP-1 complex and MMP-9 bind to 2(IV), suggesting that neither the C-terminal nor the N-terminal domain of the enzyme is directly involved in 2(IV) binding. The closely related pro-MMP-2 exhibits a weaker affinity for 2(IV) compared with that of pro-MMP-9, suggesting that sites other than the gelatin-binding domain may be involved in the binding of 2(IV) to pro-MMP-9. Although pro-MMP-9 forms a complex with 2(IV), the proenzyme does not bind to triple-helical collagen IV. These studies suggest a unique interaction between pro-MMP-9 and 2(IV) that may play a role in targeting the zymogen to cell-matrix contacts and in the degradation of the collagen IV network.

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