NLRP3 signaling drives macrophage-induced adaptive immune suppression in pancreatic carcinoma

J Exp Med. 2017 Jun 5;214(6):1711-1724. doi: 10.1084/jem.20161707. Epub 2017 Apr 25.

Abstract

The tumor microenvironment (TME) in pancreatic ductal adenocarcinoma (PDA) is characterized by immune tolerance, which enables disease to progress unabated by adaptive immunity. However, the drivers of this tolerogenic program are incompletely defined. In this study, we found that NLRP3 promotes expansion of immune-suppressive macrophages in PDA. NLRP3 signaling in macrophages drives the differentiation of CD4+ T cells into tumor-promoting T helper type 2 cell (Th2 cell), Th17 cell, and regulatory T cell populations while suppressing Th1 cell polarization and cytotoxic CD8+ T cell activation. The suppressive effects of NLRP3 signaling were IL-10 dependent. Pharmacological inhibition or deletion of NLRP3, ASC (apoptosis-associated speck-like protein containing a CARD complex), or caspase-1 protected against PDA and was associated with immunogenic reprogramming of innate and adaptive immunity within the TME. Similarly, transfer of PDA-entrained macrophages or T cells from NLRP3-/- hosts was protective. These data suggest that targeting NLRP3 holds the promise for the immunotherapy of PDA.

MeSH terms

  • Adaptive Immunity*
  • Animals
  • Apoptosis Regulatory Proteins / deficiency
  • Apoptosis Regulatory Proteins / metabolism
  • CARD Signaling Adaptor Proteins
  • Carcinoma, Pancreatic Ductal / metabolism
  • Carcinoma, Pancreatic Ductal / pathology
  • Caspase 1 / deficiency
  • Caspase 1 / metabolism
  • Cell Differentiation
  • Cell Proliferation
  • Cellular Reprogramming
  • Gene Deletion
  • Humans
  • Immunosuppression Therapy
  • Macrophages / metabolism*
  • Mice, Inbred C57BL
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Nod2 Signaling Adaptor Protein / metabolism
  • Pancreatic Neoplasms / metabolism*
  • Pancreatic Neoplasms / pathology*
  • Pancreatic Stellate Cells / metabolism
  • Pancreatic Stellate Cells / pathology
  • Signal Transduction*
  • T-Lymphocytes / immunology
  • Tumor Microenvironment

Substances

  • Apoptosis Regulatory Proteins
  • CARD Signaling Adaptor Proteins
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Nlrp3 protein, mouse
  • Nod2 Signaling Adaptor Protein
  • Nod2 protein, mouse
  • Pycard protein, mouse
  • Caspase 1