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Papers In Press, published online ahead of print August 2, 2004
Oral Biological and Medical Sciences, University of British Columbia, Vancouver, BC V6T 1Z3
Corresponding Author: chris.overall{at}ubc.ca
Matrix metalloproteinase-2 (MMP-2, gelatinase A) and membrane type (MT)1-MMP (MMP-14) are cooperative dynamic components of a cell surface proteolysis apparatus involved in regulating the cellular signaling environment and pericellular collagen homeostasis. We have shown that the linker/hemopexin C domain (LCD) of MT1-MMP, but not MMP-2, binds native type I collagen, and that the native and denatured collagen binding properties of MMP-2 reside in the fibronectin type II modules, accordingly termed the collagen binding domain (CBD). Whereas MT1-MMP exhibits type I collagenolytic but poor gelatinolytic activities, MMP-2 is a potent gelatinase with weak type I collagenolytic behavior. Upon binding collagen, recombinant MT1-LCD competes for and blocks MT1-MMP collagenolytic activity. Circular dichroism spectroscopy of native type I collagen showed that upon addition of MT1-LCD, an increase in the wavelength of maximal circular dichroism absorption occurred, which together with a drop in ellipticity, indicated structural perturbation of the triple helix. These changes were reflected by enhanced cleavage of the MT1-LCD–bound collagen by the soluble collagenases, MMP-1 and MMP-8. Similarly, recombinant MMP-2 CBD, but not the MMP-2 LCD, changed the circular dichroism spectra and also stimulated an increase in MMP-1 and -8 cleavage of native collagen. However, recombinant CBD reduced gelatin and collagen cleavage by MMP-2 as did CBD23, comprised of the 2nd and 3rd fibronectin type II modules, but not the CBD23 mutant W316A/W374A, which neither binds gelatin nor collagen. This indicates that MMP-2 and MT1-MMP bind collagen at a different site than the soluble collagenases, MMP-1 and MMP-8. Thus, MMP-2 utilizes the CBD for collagen binding and triple helicase activity that compensates for the lack of collagen binding by the MMP-2 hemopexin C domain. Hence, the MMP family has evolved at least 2 distinct mechanisms for the complex process of collagen triple helicase activity and cleavage using 2 structurally distinct domains.
J. Biol. Chem, 10.1074/jbc.M407186200
Submitted on June 28, 2004
Revised on July 26, 2004
Accepted on August 2, 2004
Characterization of the distinct collagen binding and cleavage mechanisms of matrix metalloproteinase 2 and 14 (gelatinase A and MT1-MMP): The differential roles of the MMP hemopexin C domains and the MMP-2 fibronectin type II modules in collagen triple helicase activities
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