CD44 stimulation by fragmented hyaluronic acid induces upregulation of urokinase-type plasminogen activator and its receptor and subsequently facilitates invasion of human chondrosarcoma cells

Int J Cancer. 2002 Dec 1;102(4):379-89. doi: 10.1002/ijc.10710.

Abstract

It has been established that fragmented hyaluronic acid (HA), but not native high molecular weight HA, can induce angiogenesis, cell proliferation and migration. We have studied the outside-in signal transduction pathways responsible for fragmented HA-mediated cancer cell invasion. In our study, we have studied the effects of CD44 stimulation by ligation with HA upon the expression of matrix metalloproteinases (MMPs)-2 and -9 as well as urokinase-type plasminogen activator (uPA), its receptor (uPAR) and its inhibitor (PAI-1) and the subsequent induction of invasion of human chondrosarcoma cell line HCS-2/8. Our study indicates that (i) CD44 stimulation by fragmented HA upregulates expression of uPA and uPAR mRNA and protein but does not affect MMPs secretion or PAI-1 mRNA expression; (ii) the effects of HA fragments are critically HA size dependent: high molecular weight HA is inactive, but lower molecular weight fragmented HA (Mr 3.5 kDa) is active; (iii) cells can bind avidly Mr 3.5 kDa fragmented HA through a CD44 molecule, whereas cells do not effectively bind higher Mr HA; (iv) a fragmented HA induces phosphorylation of MAP kinase proteins (MEK1/2, ERK1/2 and c-Jun) within 30 min; (v) CD44 is critical for the response (activation of MAP kinase and upregulation of uPA and uPAR expression); and (vi) cell invasion induced by CD44 stimulation with a fragmented HA is inhibited by anti-CD44 mAb, MAP kinase inhibitors, neutralizing anti-uPAR pAb, anti-catalytic anti-uPA mAb or amiloride. Therefore, our study represents the first report that CD44 stimulation induced by a fragmented HA results in activation of MAP kinase and, subsequently, enhances uPA and uPAR expression and facilitates invasion of human chondrosarcoma cells.

MeSH terms

  • Adjuvants, Immunologic / metabolism*
  • Adjuvants, Immunologic / pharmacology
  • Bone Neoplasms / drug therapy
  • Bone Neoplasms / genetics
  • Bone Neoplasms / metabolism*
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism
  • Chondrosarcoma / drug therapy
  • Chondrosarcoma / genetics
  • Chondrosarcoma / metabolism*
  • Enzyme Inhibitors / pharmacology
  • Gene Expression Regulation
  • Humans
  • Hyaluronan Receptors / metabolism*
  • Hyaluronic Acid / pharmacology*
  • MAP Kinase Signaling System / physiology
  • Matrix Metalloproteinases / metabolism
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases / metabolism
  • Neoplasm Invasiveness
  • Phosphorylation
  • Plasminogen Activator Inhibitor 1 / metabolism
  • RNA, Messenger / metabolism
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Receptors, Urokinase Plasminogen Activator
  • Signal Transduction / drug effects
  • Tumor Cells, Cultured / drug effects
  • Tyrosine / metabolism*
  • Up-Regulation
  • Urokinase-Type Plasminogen Activator / genetics
  • Urokinase-Type Plasminogen Activator / metabolism*

Substances

  • Adjuvants, Immunologic
  • Enzyme Inhibitors
  • Hyaluronan Receptors
  • PLAUR protein, human
  • Plasminogen Activator Inhibitor 1
  • RNA, Messenger
  • Receptors, Cell Surface
  • Receptors, Urokinase Plasminogen Activator
  • Tyrosine
  • Hyaluronic Acid
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases
  • Urokinase-Type Plasminogen Activator
  • Matrix Metalloproteinases