Resistance to cytarabine induces the up-regulation of NKG2D ligands and enhances natural killer cell lysis of leukemic cells

Neoplasia. 2008 Dec;10(12):1402-10. doi: 10.1593/neo.08972.

Abstract

Prolonged treatment of leukemic cells with chemotherapeutic agents frequently results in development of drug resistance. Moreover, selection of drug-resistant cell populations may be associated with changes in malignant properties such as proliferation rate, invasiveness, and immunogenicity. In the present study, the sensitivity of cytarabine (1-beta-D-arabinofuranosylcytosine, araC)-resistant and parental human leukemic cell lines (T-lymphoid H9 and acute T-lymphoblastic leukemia Molt-4) to natural killer (NK) cell-mediated killing was investigated. The results obtained demonstrate that araC-resistant H9 and Molt-4 (H9(r)ARAC(100) and Molt-4(r)ARAC(100)) cell lines are more sensitive to NK cell-mediated lysis than their respective parental cell lines. This increased sensitivity was associated with a higher surface expression of ligands for the NK cell-activating receptor NKG2D, notably UL16 binding protein-2 (ULBP-2) and ULBP-3 in H9(r)ARAC(100) and Molt-4(r)ARAC(100) cell lines. Blocking ULBP-2 and ULBP-3 or NKG2D with monoclonal antibody completely abrogated NK cell lysis. Constitutive phosphorylated extracellular signal-regulated kinase (ERK) but not pAKT was higher in araC-resistant cells than in parental cell lines. Inhibition of ERK using ERK inhibitor PD98059 decreased both ULBP-2/ULBP-3 expression and NK cell cytotoxicity. Furthermore, overexpression of constitutively active ERK in H9 parental cells resulted in increased ULBP-2/ULBP-3 expression and enhanced NK cell lysis. These results demonstrate that increased sensitivity of araC-resistant leukemic cells to NK cell lysis is caused by higher NKG2D ligand expression, resulting from more active ERK signaling pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antimetabolites, Antineoplastic / pharmacology
  • Cell Line, Tumor
  • Cell Survival
  • Cytarabine / pharmacology*
  • Drug Resistance
  • Drug Resistance, Neoplasm*
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Humans
  • Interferon-gamma / metabolism
  • Killer Cells, Natural / metabolism*
  • Leukemia / drug therapy*
  • Leukemia / metabolism*
  • Ligands
  • NK Cell Lectin-Like Receptor Subfamily K / biosynthesis*
  • Phosphorylation
  • Up-Regulation*

Substances

  • Antimetabolites, Antineoplastic
  • KLRK1 protein, human
  • Ligands
  • NK Cell Lectin-Like Receptor Subfamily K
  • Cytarabine
  • Interferon-gamma
  • Extracellular Signal-Regulated MAP Kinases