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J. Biol. Chem., Vol. 282, Issue 36, 26035-26045, September 7, 2007

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In Vitro Modeling of Matrix Vesicle Nucleation

SYNERGISTIC STIMULATION OF MINERAL FORMATION BY ANNEXIN A5 AND PHOSPHATIDYLSERINE^*

From the Department of Chemistry and Biochemistry, Graduate Science Research Center, University of South Carolina, Columbia, South Carolina 29208

Annexins A5, A2, and A6 (Anx-A5, -A2, and -A6) are quantitatively major proteins of the matrix vesicle nucleational core that is responsible for mineral formation. Anx-A5 significantly activated the induction and propagation of mineral formation when incorporated into synthetic nucleation complexes made of amorphous calcium phosphate (ACP) and Anx-A5 or of phosphatidylserine (PS) plus ACP (PS-CPLX) and Anx-A5. Incorporation of Anx-A5 markedly shortened the induction time, greatly increasing the rate and overall amount of mineral formed when incubated in synthetic cartilage lymph. Constructed by the addition of Ca²⁺ to PS, emulsions prepared in an intracellular phosphate buffer matched in ionic composition to the intracellular fluid of growth plate chondrocytes, these biomimetic PS-CPLX nucleators had little nucleational activity. However, incorporation of Anx-A5 transformed them into potent nucleators, with significantly greater activity than those made from ACP without PS. The ability of Anx-A5 to enhance the nucleation and growth of mineral appears to stem from its ability to form two-dimensional crystalline arrays on PS-containing monolayers. However, some stimulatory effect also may result from its ability to exclude Mg²⁺ and HCO^–₃ from nucleation sites. Comparing the various annexins for their ability to activate PS-CPLX nucleation yields the following: avian cartilage Anx-A5 > human placental Anx-A5 > avian liver Anx-A5 avian cartilage Anx-A6 >> cartilage Anx-A2. The stimulatory effect of human placental Anx-A5 and avian cartilage Anx-A6 depended on the presence of PS, since in its absence they either had no effect or actually inhibited the nucleation activity of ACP. Anx-A2 did not significantly enhance mineralization.

Received for publication, February 5, 2007 , and in revised form, July 5, 2007.

^* This work was supported by Department of Defense, Office of Naval Research, Grant N00014-97-1-0806 (to B. R. G.) and NIAMS, National Institutes of Health, Grants AR42359 (to L. N. Y. W.) and AR18983 (to R. E. W.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed: Dept. of Chemistry and Biochemistry, University of South Carolina, 631 Sumter St., Graduate Science Research Center, Columbia, SC 29208. Tel.: 803-777-6626; Fax: 803-777-9521; E-mail: wuthier{at}mail.chem.sc.edu.

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