Distinct cellular origin and genetic requirement of Hedgehog-Gli in postnatal rhabdomyosarcoma genesis

Oncogene. 2014 Nov 13;33(46):5370-8. doi: 10.1038/onc.2013.480. Epub 2013 Nov 25.

Abstract

Dysregulation of the Hedgehog (Hh)-Gli signaling pathway is implicated in a variety of human cancers, including basal cell carcinoma (BCC), medulloblastoma (MB) and embryonal rhabdhomyosarcoma (eRMS), three principle tumors associated with human Gorlin syndrome. However, the cells of origin of these tumors, including eRMS, remain poorly understood. In this study, we explore the cell populations that give rise to Hh-related tumors by specifically activating Smoothened (Smo) in both Hh-producing and -responsive cell lineages in postnatal mice. Interestingly, we find that unlike BCC and MB, eRMS originates from the stem/progenitor populations that do not normally receive active Hh signaling. Furthermore, we find that the myogenic lineage in postnatal mice is largely Hh quiescent and that Pax7-expressing muscle satellite cells are not able to give rise to eRMS upon Smo or Gli1/2 overactivation in vivo, suggesting that Hh-induced skeletal muscle eRMS arises from Hh/Gli quiescent non-myogenic cells. In addition, using the Gli1 null allele and a Gli3 repressor allele, we reveal a specific genetic requirement for Gli proteins in Hh-induced eRMS formation and provide molecular evidence for the involvement of Sox4/11 in eRMS cell survival and differentiation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Lineage / genetics*
  • Cells, Cultured
  • Gene Expression Regulation, Neoplastic
  • Hedgehog Proteins / genetics*
  • Hedgehog Proteins / metabolism
  • Humans
  • Immunoblotting
  • Kruppel-Like Transcription Factors / genetics*
  • Kruppel-Like Transcription Factors / metabolism
  • Mice, 129 Strain
  • Mice, Knockout
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • PAX7 Transcription Factor / genetics
  • PAX7 Transcription Factor / metabolism
  • RNA Interference
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Rhabdomyosarcoma / genetics*
  • Rhabdomyosarcoma / metabolism
  • Rhabdomyosarcoma / pathology
  • SOXC Transcription Factors / genetics
  • SOXC Transcription Factors / metabolism
  • Satellite Cells, Skeletal Muscle / metabolism
  • Satellite Cells, Skeletal Muscle / pathology
  • Smoothened Receptor
  • Tumor Cells, Cultured
  • Zinc Finger Protein GLI1
  • Zinc Finger Protein Gli2
  • Zinc Finger Protein Gli3

Substances

  • Gli1 protein, mouse
  • Gli2 protein, mouse
  • Gli3 protein, mouse
  • Hedgehog Proteins
  • Kruppel-Like Transcription Factors
  • Nerve Tissue Proteins
  • PAX7 Transcription Factor
  • Pax7 protein, mouse
  • Receptors, G-Protein-Coupled
  • SOXC Transcription Factors
  • Smo protein, mouse
  • Smoothened Receptor
  • Sox11 protein, mouse
  • Sox4 protein, mouse
  • Zinc Finger Protein GLI1
  • Zinc Finger Protein Gli2
  • Zinc Finger Protein Gli3