Robust tumor immunity to melanoma mediated by interleukin-9-producing T cells

Nat Med. 2012 Aug;18(8):1248-53. doi: 10.1038/nm.2856. Epub 2012 Jul 8.

Abstract

Interleukin-9 (IL-9) is a T cell cytokine that acts through a γC-family receptor on target cells and is associated with inflammation and allergy. We determined that T cells from mice deficient in the T helper type 17 (T(H)17) pathway genes encoding retinoid-related orphan receptor γ (ROR-γ) and IL-23 receptor (IL-23R) produced abundant IL-9, and we found substantial growth inhibition of B16F10 melanoma in these mice. IL-9-blocking antibodies reversed this tumor growth inhibition and enhanced tumor growth in wild-type (WT) mice. Il9r(-/-) mice showed accelerated tumor growth, and administration of recombinant IL-9 (rIL-9) to tumor-bearing WT and Rag1(-/-) mice inhibited melanoma as well as lung carcinoma growth. Adoptive transfer of tumor-antigen-specific T(H)9 cells into both WT and Rag1(-/-) mice suppressed melanoma growth; this effect was abrogated by treatment with neutralizing antibodies to IL-9. Exogenous rIL-9 inhibited tumor growth in Rag1(-/-) mice but not in mast-cell-deficient mice, suggesting that the targets of IL-9 in this setting include mast cells but not T or B cells. In addition, we found higher numbers of T(H)9 cells in normal human skin and blood compared to metastatic lesions of subjects with progressive stage IV melanoma. These results suggest a role for IL-9 in tumor immunity and offer insight into potential therapeutic strategies.

Publication types

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

MeSH terms

  • Animals
  • Cancer Vaccines
  • Carcinoma, Lewis Lung / immunology
  • Carcinoma, Lewis Lung / pathology
  • Disease Progression
  • Gene Expression Profiling
  • Homeodomain Proteins / genetics
  • Humans
  • Immunotherapy, Adoptive
  • Interleukin-9 / analysis
  • Interleukin-9 / biosynthesis*
  • Interleukin-9 / genetics
  • Interleukin-9 / physiology
  • Lymphatic Metastasis
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Mast Cells / drug effects
  • Mast Cells / immunology
  • Melanoma / chemistry
  • Melanoma / immunology*
  • Melanoma / pathology
  • Melanoma / secondary
  • Melanoma, Experimental / immunology
  • Melanoma, Experimental / pathology
  • Melanoma, Experimental / therapy
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasm Proteins / analysis
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / physiology*
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / deficiency
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / genetics
  • Radiation Chimera
  • Receptors, Interleukin / deficiency
  • Receptors, Interleukin / genetics
  • Recombinant Fusion Proteins / physiology
  • Skin / immunology
  • Skin Neoplasms / chemistry
  • Skin Neoplasms / immunology*
  • Skin Neoplasms / pathology
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / metabolism
  • Tumor Burden
  • Vaccination

Substances

  • Cancer Vaccines
  • Homeodomain Proteins
  • IL9 protein, human
  • Interleukin-9
  • Neoplasm Proteins
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • Receptors, Interleukin
  • Recombinant Fusion Proteins
  • Rorc protein, mouse
  • interleukin-23 receptor, mouse
  • RAG-1 protein