Platelet-derived growth factor mediates survival of leukemic large granular lymphocytes via an autocrine regulatory pathway

Blood. 2010 Jan 7;115(1):51-60. doi: 10.1182/blood-2009-06-223719. Epub 2009 Oct 30.

Abstract

Large granular lymphocyte (LGL) leukemia results from chronic expansion of cytotoxic T cells or natural killer (NK) cells. Apoptotic resistance resulting from constitutive activation of survival signaling pathways is a fundamental pathogenic mechanism. Recent network modeling analyses identified platelet-derived growth factor (PDGF) as a key master switch in controlling these survival pathways in T-cell LGL leukemia. Here we show that an autocrine PDGF regulatory loop mediates survival of leukemic LGLs of both T- and NK-cell origin. We found high levels of circulating PDGF-BB in platelet-poor plasma samples from LGL leukemia patients. Production of PDGF-BB by leukemic LGLs was demonstrated by immunocytochemical staining. Leukemic cells expressed much higher levels of PDGFR-beta transcripts than purified normal CD8(+) T cells or NK cells. We observed that phosphatidylinositol-3-kinase (PI3 kinase), Src family kinase (SFK), and downstream protein kinase B (PKB)/AKT pathways were constitutively activated in both T- and NK-LGL leukemia. Pharmacologic blockade of these pathways led to apoptosis of leukemic LGLs. Neutralizing antibody to PDGF-BB inhibited PKB/AKT phosphorylation induced by LGL leukemia sera. These results suggest that targeting of PDGF-BB, a pivotal regulator for the long-term survival of leukemic LGLs, may be an important therapeutic strategy.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Antibodies, Neutralizing / pharmacology
  • Apoptosis / drug effects
  • Autocrine Communication* / drug effects
  • Becaplermin
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Enzyme-Linked Immunosorbent Assay
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Gene Expression Regulation, Leukemic / drug effects
  • Humans
  • Immunohistochemistry
  • Leukemia, Large Granular Lymphocytic / blood
  • Leukemia, Large Granular Lymphocytic / enzymology
  • Leukemia, Large Granular Lymphocytic / genetics
  • Leukemia, Large Granular Lymphocytic / pathology*
  • Lymphocytes / drug effects
  • Lymphocytes / enzymology
  • Lymphocytes / pathology
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation / drug effects
  • Platelet-Derived Growth Factor / genetics
  • Platelet-Derived Growth Factor / metabolism*
  • Platelet-Derived Growth Factor / pharmacology
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins c-sis
  • Receptor, Platelet-Derived Growth Factor beta / genetics
  • Receptor, Platelet-Derived Growth Factor beta / metabolism
  • Signal Transduction* / drug effects
  • Staining and Labeling
  • src-Family Kinases / antagonists & inhibitors

Substances

  • Antibodies, Neutralizing
  • Phosphoinositide-3 Kinase Inhibitors
  • Platelet-Derived Growth Factor
  • Proto-Oncogene Proteins c-sis
  • Becaplermin
  • Receptor, Platelet-Derived Growth Factor beta
  • src-Family Kinases
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases