Germline Mutation of PLCD1 Contributes to Human Multiple Pilomatricomas through Protein Kinase D/Extracellular Signal-Regulated Kinase1/2 Cascade and TRPV6

J Invest Dermatol. 2021 Mar;141(3):533-544. doi: 10.1016/j.jid.2020.05.121. Epub 2020 Aug 11.

Abstract

Pilomatricoma, a benign skin appendage tumor, also known as calcifying epithelioma, consists of islands of epithelial cells histologically that contain anucleated cells in the center surrounded by basophilic cells and partial calcification. Sporadic pilomatricomas commonly have somatic mutations in the gene CTNNB1, but causative genes from germline and the underlying pathophysiology are unclear. In this study, we identified a germline missense variant of PLCD1 encoding PLCδ1, c.1186G>A (p.Glu396Lys), in a large Chinese family with autosomal dominant multiple pilomatricomas. Phospholipase C, a key enzyme playing critical roles in intracellular signal transduction, is essential for epidermal barrier integrity. The p.Glu396Lys variant increased the enzymatic activity of PLCδ1, leading to protein kinase C/protein kinase D/extracellular signal-regulated kinase1/2 pathway activation and TPRV6 channel closure, which not only resulted in excessive proliferation of keratinocytes in vitro and in vivo but also induced local accumulation of calcium in the pilomatricoma-like tumor that developed spontaneously in the skin of Plcd1E396K/E396K mice. Our results implicate this p.Glu396Lys variant of PLCD1 from germline leading to gain-of-function of PLCδ1 as a causative genetic defect in familial multiple pilomatricomas.

Publication types

  • Observational Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium Channels / metabolism*
  • DNA Mutational Analysis
  • Disease Models, Animal
  • Female
  • Germ-Line Mutation
  • Hair Diseases / genetics*
  • Hair Diseases / pathology
  • Humans
  • MAP Kinase Signaling System / genetics
  • Male
  • Mice, Transgenic
  • Middle Aged
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Mutation, Missense
  • Pedigree
  • Phospholipase C delta / genetics*
  • Pilomatrixoma / genetics*
  • Pilomatrixoma / pathology
  • Protein Kinase C / metabolism
  • Skin / pathology
  • Skin Neoplasms / genetics*
  • Skin Neoplasms / pathology
  • TRPV Cation Channels / metabolism*

Substances

  • Calcium Channels
  • TRPV Cation Channels
  • TRPV6 protein, human
  • protein kinase D
  • Protein Kinase C
  • MAPK1 protein, human
  • MAPK3 protein, human
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • PLCD1 protein, human
  • Phospholipase C delta
  • Plcd1 protein, mouse