Germline NLRP1 Mutations Cause Skin Inflammatory and Cancer Susceptibility Syndromes via Inflammasome Activation

Cell. 2016 Sep 22;167(1):187-202.e17. doi: 10.1016/j.cell.2016.09.001.

Abstract

Inflammasome complexes function as key innate immune effectors that trigger inflammation in response to pathogen- and danger-associated signals. Here, we report that germline mutations in the inflammasome sensor NLRP1 cause two overlapping skin disorders: multiple self-healing palmoplantar carcinoma (MSPC) and familial keratosis lichenoides chronica (FKLC). We find that NLRP1 is the most prominent inflammasome sensor in human skin, and all pathogenic NLRP1 mutations are gain-of-function alleles that predispose to inflammasome activation. Mechanistically, NLRP1 mutations lead to increased self-oligomerization by disrupting the PYD and LRR domains, which are essential in maintaining NLRP1 as an inactive monomer. Primary keratinocytes from patients experience spontaneous inflammasome activation and paracrine IL-1 signaling, which is sufficient to cause skin inflammation and epidermal hyperplasia. Our findings establish a group of non-fever inflammasome disorders, uncover an unexpected auto-inhibitory function for the pyrin domain, and provide the first genetic evidence linking NLRP1 to skin inflammatory syndromes and skin cancer predisposition.

Keywords: ASC; IL-1; MSPC; MSSE; NLRP1; cancer; gain-of-function; genodermatosis; germline; inflammasome; keratinocytes; keratosis lichenoides chronica; multiple self-healing squamous cell carcinoma; skin inflammation.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / chemistry
  • Adaptor Proteins, Signal Transducing / genetics*
  • Amino Acid Sequence
  • Apoptosis Regulatory Proteins / chemistry
  • Apoptosis Regulatory Proteins / genetics*
  • Carcinoma / genetics*
  • Carcinoma / pathology
  • Chromosomes, Human, Pair 17 / genetics
  • Epidermis / pathology
  • Genetic Predisposition to Disease*
  • Germ-Line Mutation
  • Humans
  • Hyperplasia / genetics
  • Hyperplasia / pathology
  • Inflammasomes / genetics
  • Inflammasomes / metabolism*
  • Interleukin-1 / metabolism
  • Keratosis / genetics*
  • Keratosis / pathology
  • NLR Proteins
  • Paracrine Communication
  • Pedigree
  • Protein Domains
  • Pyrin / chemistry
  • Signal Transduction
  • Skin Neoplasms / genetics*
  • Skin Neoplasms / pathology
  • Syndrome

Substances

  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • Inflammasomes
  • Interleukin-1
  • NLR Proteins
  • NLRP1 protein, human
  • Pyrin