A role for versican in the development of leiomyosarcoma

J Biol Chem. 2014 Dec 5;289(49):34089-103. doi: 10.1074/jbc.M114.607168. Epub 2014 Oct 15.

Abstract

Leiomyosarcoma (LMS) is a mesenchymal cancer that occurs throughout the body. Although LMS is easily recognized histopathologically, the cause of the disease remains unknown. Versican, an extracellular matrix proteoglycan, increases in LMS. Microarray analyses of 80 LMSs and 24 leiomyomas showed a significant elevated expression of versican in human LMS versus benign leiomyomas. To explore the importance of versican in this smooth muscle cell tumor, we used versican-directed siRNA to knock down versican expression in a LMS human cell line, SK-LMS-1. Decreased versican expression was accompanied by slower rates of LMS cell proliferation and migration, increased adhesion, and decreased accumulation of the extracellular matrix macromolecule hyaluronan. Addition of purified versican to cells expressing versican siRNA restored cell proliferation to the level of LMS controls, increased the pericellular coat and the retention of hyaluronan, and decreased cell adhesion in a dose-dependent manner. The presence of versican was not only synergistic with hyaluronan in increasing cell proliferation, but the depletion of versican decreased hyaluronan synthase expression and decreased the retention of hyaluronan. When LMS cells stably expressing versican siRNA were injected into nude mice, the resulting tumors displayed significantly less versican and hyaluronan staining, had lower volumes, and had reduced levels of mitosis as compared with controls. Collectively, these results suggest a role for using versican as a point of control in the management and treatment of LMS.

Keywords: Cell Migration; Cell Proliferation; Extracellular Matrix; Hyaluronan; Leiomyosarcoma; Small Interfering RNA (siRNA); Tumor Growth; Versican.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Cell Adhesion / drug effects
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Cell Proliferation / drug effects
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic*
  • Glucuronosyltransferase / genetics
  • Glucuronosyltransferase / metabolism
  • Humans
  • Hyaluronan Synthases
  • Hyaluronic Acid / metabolism*
  • Leiomyosarcoma / genetics*
  • Leiomyosarcoma / metabolism
  • Leiomyosarcoma / pathology
  • Mice
  • Mice, Nude
  • Muscle Neoplasms / genetics*
  • Muscle Neoplasms / metabolism
  • Muscle Neoplasms / pathology
  • Muscle, Smooth / metabolism
  • Muscle, Smooth / pathology
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Signal Transduction
  • Tissue Array Analysis
  • Versicans / antagonists & inhibitors
  • Versicans / genetics*
  • Versicans / metabolism
  • Versicans / pharmacology

Substances

  • RNA, Small Interfering
  • Versicans
  • Hyaluronic Acid
  • Glucuronosyltransferase
  • Hyaluronan Synthases