AF4 is a critical regulator of the IGF-1 signaling pathway during Purkinje cell development

J Neurosci. 2009 Dec 9;29(49):15366-74. doi: 10.1523/JNEUROSCI.5188-09.2009.

Abstract

Deregulation of the insulin-like growth factor 1 (IGF-1) signaling pathway is a recurrent finding in mouse models and human patients with cerebellar ataxia and thus represents a common pathological cascade in neuronal cell death that may be targeted for therapy. We have previously identified a point mutation in AF4, a transcription cofactor of RNA polymerase II elongation and chromatin remodeling, that causes progressive and highly specific Purkinje cell (PC) death in the ataxic mouse mutant robotic, leading to the accumulation of AF4 in PCs. Here we confirm that the spatiotemporal pattern of PC degeneration in the robotic cerebellum correlates with the specific profile of AF4 upregulation. To identify the underlying molecular pathways, we performed microarray gene expression analysis of PCs obtained by laser capture microdissection (LCM) at the onset of degeneration. Igf-1 was significantly downregulated in robotic PCs compared with wild-type controls before and throughout the degenerative process. Consistently, we observed a decrease in the activation of downstream signaling molecules including type 1 IGF receptor (IGF-1R) and the extracellular signal-regulated kinase (ERK) 1 and ERK2. Chromatin immunoprecipitation confirmed that Igf-1 is a direct and the first validated target of the AF4 transcriptional regulatory complex, and treatment of presymptomatic robotic mice with IGF-1 indeed markedly delayed the progression of PC death. This study demonstrates that small changes in the levels of a single transcriptional cofactor can deleteriously affect normal cerebellum function and opens new avenues of research for the manipulation of the IGF-1 pathway in the treatment of cerebellar ataxia in humans.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Death / genetics
  • Cell Death / physiology
  • Cerebellar Diseases / genetics
  • Cerebellar Diseases / metabolism
  • Cerebellum / growth & development*
  • Cerebellum / metabolism*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Gene Expression
  • Insulin-Like Growth Factor I / metabolism*
  • Mice
  • Mice, Mutant Strains
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Nerve Degeneration / genetics
  • Nerve Degeneration / metabolism
  • Neurodegenerative Diseases / genetics
  • Neurodegenerative Diseases / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Purkinje Cells / metabolism*
  • Receptor, IGF Type 1 / metabolism
  • Signal Transduction

Substances

  • Aff1 protein, mouse
  • DNA-Binding Proteins
  • Nuclear Proteins
  • insulin-like growth factor-1, mouse
  • Insulin-Like Growth Factor I
  • Receptor, IGF Type 1
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3