Host IL11 Signaling Suppresses CD4+ T cell-Mediated Antitumor Responses to Colon Cancer in Mice

Cancer Immunol Res. 2021 Jul;9(7):735-747. doi: 10.1158/2326-6066.CIR-19-1023. Epub 2021 Apr 27.

Abstract

IL11 is a member of the IL6 family of cytokines and signals through its cognate receptor subunits, IL11RA and glycoprotein 130 (GP130), to elicit biological responses via the JAK/STAT signaling pathway. IL11 contributes to cancer progression by promoting the survival and proliferation of cancer cells, but the potential immunomodulatory properties of IL11 signaling during tumor development have thus far remained unexplored. Here, we have characterized a role for IL11 in regulating CD4+ T cell-mediated antitumor responses. Absence of IL11 signaling impaired tumor growth in a sporadic mouse model of colon cancer and syngeneic allograft models of colon cancer. Adoptive bone marrow transfer experiments and in vivo depletion studies demonstrated that the tumor-promoting activity of IL11 was mediated through its suppressive effect on host CD4+ T cells in the tumor microenvironment. Indeed, when compared with Il11ra-proficient CD4+ T cells associated with MC38 tumors, their Il11ra-deficient counterparts displayed elevated expression of mRNA encoding the antitumor mediators IFNγ and TNFα. Likewise, IL11 potently suppressed the production of proinflammatory cytokines (IFNγ, TNFα, IL6, and IL12p70) by CD4+ T cells in vitro, which we corroborated by RNAscope analysis of human colorectal cancers, where IL11RAhigh tumors showed less IFNG and CD4 expression than IL11RAlow tumors. Therefore, our results ascribe a tumor cell-extrinsic immunomodulatory role to IL11 during colon cancer development that could be amenable to an anticytokine-based therapy.See related Spotlight by van der Burg, p. 724.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4 Antigens / analysis
  • CD4 Antigens / metabolism
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • Cell Line, Tumor
  • Colon / immunology
  • Colon / pathology
  • Colonic Neoplasms / immunology*
  • Colonic Neoplasms / pathology
  • Datasets as Topic
  • Disease Models, Animal
  • Gene Expression Profiling
  • Humans
  • Interferon-gamma / analysis
  • Interferon-gamma / metabolism
  • Interleukin-11 / metabolism*
  • Interleukin-11 Receptor alpha Subunit / analysis
  • Interleukin-11 Receptor alpha Subunit / genetics
  • Interleukin-11 Receptor alpha Subunit / metabolism*
  • Mice
  • Mice, Knockout
  • Neoplasms, Bone Tissue
  • Receptors, Interleukin-11 / metabolism
  • Tumor Microenvironment / immunology

Substances

  • CD4 Antigens
  • IFNG protein, human
  • Interleukin-11
  • Interleukin-11 Receptor alpha Subunit
  • Receptors, Interleukin-11
  • Interferon-gamma