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J. Biol. Chem., Vol. 279, Issue 24, 25455-25463, June 11, 2004

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Extracellular Bone Acidic Glycoprotein-75 Defines Condensed Mesenchyme Regions to be Mineralized and Localizes with Bone Sialoprotein during Intramembranous Bone Formation^*

Jeff P. Gorski||, Aimin Wang¶, Dinah Lovitch||, Douglas Law**, Kimerly Powell¶, and Ronald J. Midura¶

From the ^||Division of Biochemistry and Molecular Biology, School of Biological Sciences, and Department of Oral Biology, School of Dentistry, University of Missouri-Kansas City, Kansas City, Missouri 64108, the ^¶Orthopaedic Research Center and Department of Biomedical Engineering, Cleveland Clinic and Foundation, Cleveland, Ohio 44195, and the ^**Division of Cell Biology and Biophysics, School of Biological Sciences, University of Missouri-Kansas City, Kansas City, Missouri 64110

Bone acidic glycoprotein-75 is expressed very early during in vivo models of intramembranous bone formation, highly enriched in condensing osteogenic mesenchyme after marrow ablation and the osteoprogenitor layer of tibial periosteum. Bone sialoprotein accumulates within bone acidic glycoprotein-75-enriched matrix areas at a later stage in both models. Decalcification of initial sites of mineralization consistently revealed focal immunostaining for bone acidic glycoprotein-75 underneath these sites suggesting that mineralization occurs within bone acidic glycoprotein-75-enriched matrix areas. Ultrastructural immunolocalization of bone acidic glycoprotein-75 does not support a direct association with banded collagen fibrils, but rather suggests it is a component of a separate, amorphous scaffold occupying interfibrillar spaces. Double immunogold labeling demonstrated that a sizeable proportion of bone sialoprotein particles were located within a 50-nm radius of bone acidic glycoprotein-75. These results define bone acidic glycoprotein-75 as the earliest bone-restricted, extracellular marker of osteogenic mesenchyme. Based on this early bone-restricted expression pattern and a previously documented propensity of bone acidic glycoprotein-75 to form supramolecular complexes through self-association, bone acidic glycoprotein-75 may serve a key structural role in setting boundary limits of condensing osteogenic mesenchyme.

Received for publication, November 12, 2003 , and in revised form, March 5, 2004.

^* This work was supported by National Institutes of Health Grants DE-14619 and DE-11197 and the University of Missouri Research Board (to J. P. G.) and National Institutes of Health Grant AR-45171 (to R. J. M.) and The Lerner Research Institute of The Cleveland Clinic Foundation. A preliminary account of this material was presented at the annual meeting of the American Society for Bone and Mineral Research, September 19–23, 2003, in Minneapolis, MN (64). 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.

To whom correspondence should be addressed: Dept. of Oral Biology, Bone Biology Research Program, School of Dentistry, University of Missouri, 650 East 25th St., Kansas City, MO 64108. Tel.: 816-235-2537; Fax: 816-235-5524; E-mail: Gorskij{at}umkc.edu.

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