NLRC4 suppresses melanoma tumor progression independently of inflammasome activation

J Clin Invest. 2016 Oct 3;126(10):3917-3928. doi: 10.1172/JCI86953. Epub 2016 Sep 12.

Abstract

Members of the NLR family can assemble inflammasome complexes with the adaptor protein ASC and caspase-1 that result in the activation of caspase-1 and the release of IL-1β and IL-18. Although the NLRC4 inflammasome is known to have a protective role in tumorigenesis, there is an increased appreciation for the inflammasome-independent actions of NLRC4. Here, we utilized a syngeneic subcutaneous murine model of B16F10 melanoma to explore the role of NLRC4 in tumor suppression. We found that NLRC4-deficient mice exhibited enhanced tumor growth that was independent of the inflammasome components ASC and caspase-1. Nlrc4 expression was critical for cytokine and chemokine production in tumor-associated macrophages and was necessary for the generation of protective IFN-γ-producing CD4+ and CD8+ T cells. Tumor progression was diminished when WT or caspase-1-deficient, but not NLRC4-deficient, macrophages were coinjected with B16F10 tumor cells in NLRC4-deficient mice. Finally, examination of human primary melanomas revealed the extensive presence of NLRC4+ tumor-associated macrophages. In contrast, there was a paucity of NLRC4+ tumor-associated macrophages observed in human metastatic melanoma, supporting the concept that NLRC4 expression controls tumor growth. These results reveal a critical role for NLRC4 in suppressing tumor growth in an inflammasome-independent manner.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins / physiology*
  • Calcium-Binding Proteins / physiology*
  • Caspase 1 / metabolism
  • Chemokines / metabolism
  • Disease Progression
  • Female
  • Humans
  • Inflammasomes / metabolism
  • Lymphocytes, Tumor-Infiltrating / metabolism
  • MAP Kinase Signaling System
  • Macrophages / metabolism
  • Melanoma, Experimental / immunology
  • Melanoma, Experimental / metabolism*
  • Melanoma, Experimental / pathology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasm Transplantation
  • STAT3 Transcription Factor / metabolism
  • Tumor Burden
  • Tumor Microenvironment

Substances

  • Apoptosis Regulatory Proteins
  • Calcium-Binding Proteins
  • Chemokines
  • Inflammasomes
  • Ipaf protein, mouse
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Caspase 1