miR-155 augments CD8+ T-cell antitumor activity in lymphoreplete hosts by enhancing responsiveness to homeostatic γc cytokines

Proc Natl Acad Sci U S A. 2015 Jan 13;112(2):476-81. doi: 10.1073/pnas.1422916112. Epub 2014 Dec 29.

Abstract

Lymphodepleting regimens are used before adoptive immunotherapy to augment the antitumor efficacy of transferred T cells by removing endogenous homeostatic "cytokine sinks." These conditioning modalities, however, are often associated with severe toxicities. We found that microRNA-155 (miR-155) enabled tumor-specific CD8(+) T cells to mediate profound antitumor responses in lymphoreplete hosts that were not potentiated by immune-ablation. miR-155 enhanced T-cell responsiveness to limited amounts of homeostatic γc cytokines, resulting in delayed cellular contraction and sustained cytokine production. miR-155 restrained the expression of the inositol 5-phosphatase Ship1, an inhibitor of the serine-threonine protein kinase Akt, and multiple negative regulators of signal transducer and activator of transcription 5 (Stat5), including suppressor of cytokine signaling 1 (Socs1) and the protein tyrosine phosphatase Ptpn2. Expression of constitutively active Stat5a recapitulated the survival advantages conferred by miR-155, whereas constitutive Akt activation promoted sustained effector functions. Our results indicate that overexpression of miR-155 in tumor-specific T cells can be used to increase the effectiveness of adoptive immunotherapies in a cell-intrinsic manner without the need for life-threatening, lymphodepleting maneuvers.

Keywords: adoptive immunotherapy; homeostatic cytokines; lymphodepletion; microRNA-155.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • CD8-Positive T-Lymphocytes / immunology*
  • Cell Line, Tumor
  • Cytokines / biosynthesis
  • Cytokines / immunology*
  • HEK293 Cells
  • Humans
  • Immunotherapy, Adoptive
  • Melanoma, Experimental / genetics
  • Melanoma, Experimental / immunology
  • Melanoma, Experimental / therapy
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • MicroRNAs / genetics*
  • MicroRNAs / immunology*
  • MicroRNAs / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • STAT5 Transcription Factor / metabolism
  • Signal Transduction
  • gp100 Melanoma Antigen / genetics
  • gp100 Melanoma Antigen / immunology

Substances

  • Cytokines
  • MicroRNAs
  • Mirn155 microRNA, mouse
  • STAT5 Transcription Factor
  • Stat5a protein, mouse
  • gp100 Melanoma Antigen
  • Proto-Oncogene Proteins c-akt