Lactate promotes glioma migration by TGF-beta2-dependent regulation of matrix metalloproteinase-2

Neuro Oncol. 2009 Aug;11(4):368-80. doi: 10.1215/15228517-2008-106. Epub 2008 Nov 25.

Abstract

Lactate dehydrogenase type A (LDH-A) is a key metabolic enzyme catalyzing pyruvate into lactate and is excessively expressed by tumor cells. Transforming growth factor-beta2 (TGF-beta2) is a key regulator of invasion in high-grade gliomas, partially by inducing a mesenchymal phenotype and by remodeling the extracellular matrix. In this study, we tested the hypothesis that lactate metabolism regulates TGF-beta2-mediated migration of glioma cells. Small interfering RNA directed against LDH-A (siLDH-A) suppresses, and lactate induces, TGF-beta2 expression, suggesting that lactate metabolism is strongly associated with TGF-beta2 in glioma cells. Here we demonstrate that TGF-beta2 enhances expression, secretion, and activation of matrix metalloproteinase-2 (MMP-2) and induces the cell surface expression of integrin alpha(v)beta(3) receptors. In spheroid and Boyden chamber migration assays, inhibition of MMP-2 activity using a specific MMP-2 inhibitor and blocking of integrin alpha(v)beta(3) abrogated glioma cell migration stimulated by TGF-beta2. Furthermore, siLDH-A inhibited MMP2 activity, leading to inhibition of glioma migration. Taken together, we define an LDH-A-induced and TGF-beta2-coordinated regulatory cascade of transcriptional regulation of MMP-2 and integrin alpha(v)beta(3). This novel interaction between lactate metabolism and TGF-beta2 might constitute a crucial mechanism for glioma migration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology*
  • Cell Movement*
  • Enzyme-Linked Immunosorbent Assay
  • Flow Cytometry
  • Gene Expression Regulation, Neoplastic
  • Glioma / metabolism
  • Glioma / pathology*
  • Glucose / analysis
  • Humans
  • Integrin alphaVbeta3 / antagonists & inhibitors
  • Integrin alphaVbeta3 / metabolism*
  • Isoenzymes / physiology
  • L-Lactate Dehydrogenase / physiology*
  • Lactate Dehydrogenase 5
  • Matrix Metalloproteinase 2 / metabolism*
  • Matrix Metalloproteinase Inhibitors
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / pharmacology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Transforming Growth Factor beta2 / metabolism*
  • Tumor Cells, Cultured

Substances

  • Integrin alphaVbeta3
  • Isoenzymes
  • Matrix Metalloproteinase Inhibitors
  • RNA, Messenger
  • RNA, Small Interfering
  • TGFB2 protein, human
  • Transforming Growth Factor beta2
  • L-Lactate Dehydrogenase
  • Lactate Dehydrogenase 5
  • Matrix Metalloproteinase 2
  • Glucose