Human basal cell carcinoma: the induction of anagen hair follicle differentiation

Clin Exp Dermatol. 2020 Apr;45(3):309-317. doi: 10.1111/ced.14108. Epub 2019 Oct 22.

Abstract

Background: Consistent with cancer stem cell driven pattern of growth, human basal cell carcinomas (BCCs) demonstrate differentiation along hair follicle (HF) lineages.

Aim: To define the pattern of differentiation and therapeutic targets that promote BCC differentiation and therefore BCC cancer stem cell exhaustion.

Methods: An alkaline phosphatase substrate kit was used to determine dermal papilla cells within the BCC stroma. Autonomous HF cycle-dependent gene expression was identified by analysis of the human homologues of a murine gene set (total 2289 genes) that is differentially expressed in hair cycle phases. The findings were validated by quantitative real-time PCR and immunofluorescence, as well as in vitro transforming growth factor (TGF)-β2 stimulation of BCC cancer stem cell colonies.

Results: As in the HF, keratin expression in the inner root sheath and matrix in BCC correlated with proliferative index and was tightly regulated, despite the absence of dermal papilla cells. Cross-species microarray analysis comparing human BCC and murine synchronous HF growth cycle datasets revealed 74% concordance with telogen differentiation compared with anagen (23%, P < 0.01) and catagen (49%; P < 0.01). Incomplete anagen differentiation within BCC was characterized by reduced expression of the anagen master regulator DLX3 (-5.5-fold), and increased expression of telogen-associated genes: AEBP1 (2.2-fold), DEFB8 (35.3-fold), MMP3 (106.0-fold) and MMP12 (12.9-fold). Restoration of dermal papilla signals by in vitro addition of TGF-β2 enhanced anagen differentiation.

Conclusion: Our findings show that BCC cells differentiate along HF lineages and may be susceptible to exogenous HF cycle modulators.

MeSH terms

  • Animals
  • Carcinoma, Basal Cell / pathology*
  • Carcinoma, Basal Cell / physiopathology
  • Cell Differentiation / physiology*
  • Cell Transformation, Neoplastic
  • Fluorescent Antibody Technique
  • Gene Expression
  • Hair Follicle / cytology*
  • Hair Follicle / growth & development
  • Hair Follicle / metabolism
  • Humans
  • Keratins / metabolism
  • Mice
  • Oligonucleotide Array Sequence Analysis
  • Real-Time Polymerase Chain Reaction
  • Skin Neoplasms / pathology*
  • Skin Neoplasms / physiopathology

Substances

  • Keratins