Identification and characterization of KCASH2 and KCASH3, 2 novel Cullin3 adaptors suppressing histone deacetylase and Hedgehog activity in medulloblastoma

Neoplasia. 2011 Apr;13(4):374-85. doi: 10.1593/neo.101630.

Abstract

Medulloblastoma is the most common pediatric malignant brain tumor, arising from aberrant cerebellar precursors' development, a process mainly controlled by Hedgehog (Hh) signaling pathway. Histone deacetylase HDAC1 has been recently shown to modulate Hh signaling, deacetylating its effectors Gli1/2 and enhancing their transcriptional activity. Therefore, HDAC may represent a potential therapeutic target for Hh-dependent tumors, but still little information is available on the physiological mechanisms of HDAC regulation. The putative tumor suppressor REN(KCTD11) acts through ubiquitination-dependent degradation of HDAC1, thereby affecting Hh activity and medulloblastoma growth. We identify and characterize here two REN(KCTD11) homologues, defining a new family of proteins named KCASH, as "KCTD containing, Cullin3 adaptor, suppressor of Hedgehog." Indeed, the novel genes (KCASH2(KCTD21) and KCASH3(KCTD6)) share with REN(KCTD11) a number of features, such as a BTB domain required for the formation of a Cullin3 ubiquitin ligase complex and HDAC1 ubiquitination and degradation capability, suppressing the acetylation-dependent Hh/Gli signaling. Expression of KCASH2 and -3 is observed in cerebellum, whereas epigenetic silencing and allelic deletion are observed in human medulloblastoma. Rescuing KCASHs expression reduces the Hedgehog-dependent medulloblastoma growth, suggesting that loss of members of this novel family of native HDAC inhibitors is crucial in sustaining Hh pathway-mediated tumorigenesis. Accordingly, they might represent a promising class of endogenous "agents" through which this pathway may be targeted.

MeSH terms

  • Adaptor Proteins, Signal Transducing / chemistry
  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Adaptor Proteins, Signal Transducing / physiology*
  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Cell Cycle Proteins
  • Cells, Cultured
  • Cerebellar Neoplasms / genetics*
  • Cerebellar Neoplasms / metabolism
  • Cerebellar Neoplasms / pathology
  • Cloning, Molecular
  • Cullin Proteins / metabolism
  • Female
  • Gestational Age
  • Hedgehog Proteins / antagonists & inhibitors*
  • Hedgehog Proteins / metabolism
  • Histone Deacetylase Inhibitors / metabolism
  • Histone Deacetylases / metabolism
  • Humans
  • Medulloblastoma / genetics*
  • Medulloblastoma / metabolism
  • Medulloblastoma / pathology
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Models, Biological
  • Potassium Channels / chemistry
  • Pregnancy
  • Sequence Homology, Amino Acid
  • Transferases
  • Young Adult

Substances

  • Adaptor Proteins, Signal Transducing
  • CUL3 protein, human
  • Cell Cycle Proteins
  • Cullin Proteins
  • Hedgehog Proteins
  • Histone Deacetylase Inhibitors
  • KCTD21 protein, human
  • KCTD6 proetin, human
  • Potassium Channels
  • KCTD11 protein, human
  • Transferases
  • Histone Deacetylases