Shh and p50/Bcl3 signaling crosstalk drives pathogenesis of BCCs in Gorlin syndrome

Oncotarget. 2015 Nov 3;6(34):36789-814. doi: 10.18632/oncotarget.5103.

Abstract

Nevoid basal cell carcinoma syndrome (NBCCS) is a rare autosomal dominant disorder that is due, in large measure, to aberrant Shh signaling driven by mutations in the tumor suppressor gene Ptch1. Here, we describe the development of Ptch1+/-/ SKH-1 mice as a novel model of this disease. These animals manifest many features of NBCCS, including developmental anomalies and are remarkably sensitive to both ultraviolet (UVB) and ionizing radiation that drive the development of multiple BCCs. Just as in patients with NBCCS, Ptch1+/-/SKH-1 also spontaneously develops BCCs and other neoplasms such as rhabdomyomas/rhabdomyosarcomas. Administration of smoothened inhibitors (vismodegib/itraconazole/cyclopamine) or non-steroidal anti-inflammatory drug (sulindac/sulfasalazine) each result in partial resolution of BCCs in these animals. However, combined administration of these agents inhibits the growth of UVB-induced BCCs by >90%. Employing small molecule- and decoy-peptide-based approaches we further affirm that complete remission of BCCs could only be achieved by combined inhibition of p50-NFκB/Bcl3 and Shh signaling. We posit that Ptch1+/-/SKH-1 mice are a novel and relevant animal model for NBCCS. Understanding mechanisms that govern genetic predisposition to BCCs should facilitate our ability to identify and treat NBCCS gene carriers, including those at risk for sporadic BCCs while accelerating development of novel therapeutic modalities for these patients.

Keywords: Bcl3; NBCCS; Shh; basal cell carcinoma; murine model.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • B-Cell Lymphoma 3 Protein
  • Basal Cell Nevus Syndrome / genetics
  • Basal Cell Nevus Syndrome / metabolism*
  • Basal Cell Nevus Syndrome / pathology
  • Disease Models, Animal
  • Female
  • Hedgehog Proteins / genetics
  • Hedgehog Proteins / metabolism*
  • Humans
  • Male
  • Mice
  • Mice, Hairless
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • NF-kappa B p50 Subunit / genetics
  • NF-kappa B p50 Subunit / metabolism*
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism*
  • Signal Transduction
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism*
  • Skin Neoplasms / pathology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • B-Cell Lymphoma 3 Protein
  • BCL3 protein, human
  • Bcl3 protein, mouse
  • Hedgehog Proteins
  • NF-kappa B p50 Subunit
  • Proto-Oncogene Proteins
  • SHH protein, human
  • Shh protein, mouse
  • Transcription Factors