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J. Biol. Chem., Vol. 282, Issue 14, 10814-10825, April 6, 2007

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Formation of Hyaluronan- and Versican-rich Pericellular Matrix by Prostate Cancer Cells Promotes Cell Motility^*

Carmela Ricciardelli¹, Darryl L. Russell, Miranda P. Ween, Keiko Mayne, Supaporn Suwiwat, Sharon Byers^¶, Villis R. Marshall^||, Wayne D. Tilley, and David J. Horsfall

From the Dame Roma Mitchell Cancer Research Laboratories, Hanson Institute, University of Adelaide, Box 14 Rundle Mall, Adelaide, South Australia 5001, Australia, the Discipline of Obstetrics and Gynaecology & Centre for Reproductive Health, University of Adelaide, Frome Rd, South Australia 5005, Australia, the ^¶Matrix Biology Unit, Department of Genetic Medicine, Women's and Children's Hospital, North Adelaide, South Australia 5006, Australia, and the ^||Surgical Speciality Services, Royal Adelaide Hospital, Adelaide, South Australia 5000, Australia

Previous studies have demonstrated that high levels of hyaluronan (HA) and the chondroitin sulfate proteoglycan, versican in the peritumoral stroma are associated with metastatic spread of clinical prostate cancer. In vitro integration of HA and versican into a pericellular sheath is a prerequisite for proliferation and migration of vascular smooth muscle cells. In this study, a particle exclusion assay was used to determine whether human prostate cancer cell lines are capable of assembling a pericellular sheath following treatment with versican-containing medium and whether formation of a pericellular sheath modulated cell motility. PC3 and DU145, but not LNCaP cells formed prominent polarized pericellular sheaths following treatment with prostate fibroblast-conditioned medium. The capacity to assemble a pericellular sheath correlated with the ability to express membranous HA receptor, CD44. HA and versican histochemical staining were observed surrounding PC3 and DU145 cells following treatment with prostatic fibroblast-conditioned medium. The dependence on HA for integrity of the pericellular sheath was demonstrated by its removal following treatment with hyaluronidase. Purified versican or conditioned medium from Chinese hamster ovary K1 cells overexpressing versican V1, but not conditioned medium from parental cells, promoted pericellular sheath formation and motility of PC3 cells. Using time lapse microscopy, motile PC3 cells treated with versican but not non-motile cells exhibited a polar pericellular sheath. Polar pericellular sheath was particularly evident at the trailing edge but was excluded from the leading edge of PC3 cells. These studies indicate that prostate cancer cells recruit stromal components to remodel their pericellular environment and promote their motility.

Received for publication, July 24, 2006 , and in revised form, February 8, 2007.

^* This work was supported by the Cancer Council of South Australia. 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.

The on-line version of this article (available at http://www.jbc.org) contains a supplemental movie.

¹ To whom correspondence should be addressed: Discipline of Obstetrics and Gynaecology, Research Centre for Reproductive Health, University of Adelaide, Frome Rd, 5005 South Australia, Australia. Tel.: 618-8303-8255; Fax: 618-8303-4099; E-mail: carmela.ricciardelli{at}adelaide.edu.au.

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