Direct and immune-mediated cytotoxicity of interleukin-21 contributes to antitumor effects in mantle cell lymphoma

Blood. 2015 Sep 24;126(13):1555-64. doi: 10.1182/blood-2015-01-624585. Epub 2015 Jul 20.

Abstract

Mantle cell lymphoma (MCL) is a distinct subtype of non-Hodgkin lymphoma characterized by overexpression of cyclin D1 in 95% of patients. MCL patients experience frequent relapses resulting in median survival of 3 to 5 years, requiring more efficient therapeutic regimens. Interleukin (IL)-21, a member of the IL-2 cytokine family, possesses potent antitumor activity against a variety of cancers not expressing the IL-21 receptor (IL-21R) through immune activation. Previously, we established that IL-21 exerts direct cytotoxicity on IL-21R-expressing diffuse large B-cell lymphoma cells. Herein, we demonstrate that IL-21 possesses potent cytotoxicity against MCL cell lines and primary tumors. We identify that IL-21-induced direct cytotoxicity is mediated through signal transducer and activator of transcription 3-dependent cMyc upregulation, resulting in activation of Bax and inhibition of Bcl-2 and Bcl-XL. IL-21-mediated cMyc upregulation is only observed in IL-21-sensitive cells. Further, we demonstrate that IL-21 leads to natural killer (NK)-cell-dependent lysis of MCL cell lines that were resistant to direct cytotoxicity. In vivo treatment with IL-21 results in complete FC-muMCL1 tumor regression in syngeneic mice via NK- and T-cell-dependent mechanisms. Together, these data indicate that IL-21 has potent antitumor activity against MCL cells via direct cytotoxic and indirect, immune-mediated effects.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • CD4-Positive T-Lymphocytes / immunology
  • Cell Line, Tumor
  • Female
  • Humans
  • Immunologic Factors / immunology*
  • Immunologic Factors / therapeutic use*
  • Immunotherapy
  • Interleukins / immunology*
  • Interleukins / therapeutic use*
  • Killer Cells, Natural / immunology
  • Lymphoma, Mantle-Cell / immunology*
  • Lymphoma, Mantle-Cell / pathology
  • Lymphoma, Mantle-Cell / therapy*
  • Mice, Inbred C57BL
  • Proto-Oncogene Proteins c-myc / immunology
  • Receptors, Interleukin-21 / immunology
  • STAT3 Transcription Factor / immunology
  • Signal Transduction / drug effects
  • bcl-2-Associated X Protein / immunology

Substances

  • Immunologic Factors
  • Interleukins
  • Proto-Oncogene Proteins c-myc
  • Receptors, Interleukin-21
  • STAT3 Transcription Factor
  • bcl-2-Associated X Protein
  • interleukin-21