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J. Biol. Chem., Vol. 281, Issue 48, 36905-36914, December 1, 2006

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The Structure, Location, and Function of Perlecan, a Prominent Pericellular Proteoglycan of Fetal, Postnatal, and Mature Hyaline Cartilages^*

James Melrose¹, Peter Roughley, Sarah Knox^¶, Susan Smith, Megan Lord^¶, and John Whitelock^¶

From the The Raymond Purves Research Laboratories, Institute of Bone and Joint Research and Kolling Institute of Medical Research, University of Sydney at the Royal North Shore Hospital of Sydney, St. Leonards, New South Wales 2065, Australia, the Genetics Unit, Shriners Hospital for Children, Montreal, Quebec H3G 1A6, Canada, and the ^¶Graduate School of Biomedical Engineering, University of New South Wales, Kensington, New South Wales 2052, Australia

The aim of this study was to immunolocalize perlecan in human fetal, postnatal, and mature hyaline cartilages and to determine information on the structure and function of chondrocyte perlecan. Perlecan is a prominent component of human fetal (12-14 week) finger, toe, knee, and elbow cartilages; it was localized diffusely in the interterritorial extracellular matrix, densely in the pericellular matrix around chondrocytes, and to small blood vessels in the joint capsules and perichondrium. Aggrecan had a more intense distribution in the marginal regions of the joint rudiments and in para-articular structures. Perlecan also had a strong pericellular localization pattern in postnatal (2-7 month) and mature (55-64 year) femoral cartilages, whereas aggrecan had a prominent extracellular matrix distribution in these tissues. Western blotting identified multiple perlecan core protein species in extracts of the postnatal and mature cartilages, some of which were substituted with heparan sulfate and/or chondroitin sulfate and some were devoid of glycosaminoglycan substitution. Some perlecan core proteins were smaller than intact perlecan, suggesting that proteolytic processing or alternative splicing had occurred. Surface plasmon resonance and quartz crystal microbalance with dissipation experiments demonstrated that chondrocyte perlecan bound fibroblast growth factor (FGF)-1 and -9 less efficiently than endothelial cell perlecan. The latter perlecan supported the proliferation of Baf-32 cells transfected with FGFR3c equally well with FGF-1 and -9, whereas chondrocyte perlecan only supported Baf-32 cell proliferation with FGF-9. The function of perlecan therefore may not be universal but may vary with its cellular origin and presumably its structure.

Received for publication, September 5, 2006

^* This work was supported by National Health and Medical Research Council of Australia Grant 211266, the Shriners of North America, seed grants from the Australian Arthritis Foundation, Rebecca Cooper Medical Research Foundation (to J. M.), and University of New South Wales and Australian Research Council Faculty of Engineering Infrastructure Research Grants LP0455407 and DP0557863 (to J. 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: Level 5, The University Clinic, Bldg. B26, The Royal North Shore Hospital, St. Leonards, NSW 2065 Australia. Tel.: 61-2-9926-6535; Fax: 61-2-9926-6539; E-mail: jmelrose{at}med.usyd.edu.au.

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