Modulation of invasive properties of CD133+ glioblastoma stem cells: a role for MT1-MMP in bioactive lysophospholipid signaling

Mol Carcinog. 2009 Oct;48(10):910-9. doi: 10.1002/mc.20541.

Abstract

Future breakthroughs in cancer therapy must accompany targeted agents that will neutralize cancer stem cells response to circulating growth factors. Since the brain tissue microenvironmental niche is a prerequisite for expression of the stem cell marker CD133 antigen in brain tumors, we investigated the invasion mechanisms specific to CD133(+) U87 glioblastoma cells in response to lysophosphatidic acid (LPA) and sphingosine 1-phosphate (S1P), two circulating bioactive lysophospholipids and potent inducers of cancer. A CD133(+) U87 glioma cell population was isolated from parental U87 glioblastoma cells using magnetic cell sorting technology. The CD133(+)-enriched cell population grew as neurospheres and showed enhanced maximal response to both LPA (approximately 5.0-fold) and S1P (approximately 2.5-fold) at 1 microM when compared to parental U87 cells. The increased response to LPA in CD133(+) cells, reflected by increased levels of phosphorylated ERK, was found independent of the cooperative functions of the membrane-type-1 matrix metalloproteinase (MT1-MMP), while this cooperativity was essential to the S1P response. Quantitative RT-PCR was performed and we found higher gene expression levels of the S1P receptors S1P1 and S1P2, and of the LPA receptor LPA1 in CD133(+) cells than in their parental U87 cells. These increased levels reflected those observed from in vivo experimental U87 tumor implants. Our data suggest that the CD133(+) cell subpopulation evokes most of the lysophospholipid response within brain tumors through a combined regulation of S1P/LPA cell surface receptors signaling and by MT1-MMP. The emergence of lead compounds targeting the stem cell niche and S1P/LPA signaling in CD133(+) cancer cells is warranted.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AC133 Antigen
  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / metabolism*
  • Blotting, Western
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology*
  • Cell Line, Tumor
  • Female
  • Flow Cytometry
  • Glioblastoma / metabolism
  • Glioblastoma / pathology*
  • Glycoproteins / genetics
  • Glycoproteins / metabolism*
  • Humans
  • Lysophospholipids / genetics
  • Lysophospholipids / metabolism*
  • Matrix Metalloproteinase 14 / physiology*
  • Mice
  • Mice, Nude
  • Neoplasm Invasiveness
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology*
  • Peptides / genetics
  • Peptides / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / pharmacology
  • Receptors, Lysosphingolipid / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / physiology
  • Sphingosine / analogs & derivatives
  • Sphingosine / genetics
  • Xenograft Model Antitumor Assays

Substances

  • AC133 Antigen
  • Antigens, CD
  • Glycoproteins
  • Lysophospholipids
  • PROM1 protein, human
  • Peptides
  • Prom1 protein, mouse
  • RNA, Messenger
  • RNA, Small Interfering
  • Receptors, Lysosphingolipid
  • sphingosine 1-phosphate
  • Matrix Metalloproteinase 14
  • Sphingosine