ANKRD1 is a mesenchymal-specific driver of cancer-associated fibroblast activation bridging androgen receptor loss to AP-1 activation

Nat Commun. 2024 Feb 3;15(1):1038. doi: 10.1038/s41467-024-45308-w.

Abstract

There are significant commonalities among several pathologies involving fibroblasts, ranging from auto-immune diseases to fibrosis and cancer. Early steps in cancer development and progression are closely linked to fibroblast senescence and transformation into tumor-promoting cancer-associated fibroblasts (CAFs), suppressed by the androgen receptor (AR). Here, we identify ANKRD1 as a mesenchymal-specific transcriptional coregulator under direct AR negative control in human dermal fibroblasts (HDFs) and a key driver of CAF conversion, independent of cellular senescence. ANKRD1 expression in CAFs is associated with poor survival in HNSCC, lung, and cervical SCC patients, and controls a specific gene expression program of myofibroblast CAFs (my-CAFs). ANKRD1 binds to the regulatory region of my-CAF effector genes in concert with AP-1 transcription factors, and promotes c-JUN and FOS association. Targeting ANKRD1 disrupts AP-1 complex formation, reverses CAF activation, and blocks the pro-tumorigenic properties of CAFs in an orthotopic skin cancer model. ANKRD1 thus represents a target for fibroblast-directed therapy in cancer and potentially beyond.

MeSH terms

  • Cancer-Associated Fibroblasts* / metabolism
  • Fibroblasts / metabolism
  • Humans
  • Muscle Proteins / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Receptors, Androgen / genetics
  • Receptors, Androgen / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Skin Neoplasms* / pathology
  • Transcription Factor AP-1 / genetics
  • Transcription Factor AP-1 / metabolism
  • Tumor Microenvironment

Substances

  • ANKRD1 protein, human
  • Muscle Proteins
  • Nuclear Proteins
  • Receptors, Androgen
  • Repressor Proteins
  • Transcription Factor AP-1
  • AR protein, human
  • JUN protein, human