Reelin is a target of polyglutamine expanded ataxin-7 in human spinocerebellar ataxia type 7 (SCA7) astrocytes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 52, 2012, Pages 21319-21324

  McCullough, Shaun D ^a   Xu, Xiaojiang ^a   Dent, Sharon Y R ^b   Bekiranov, Stefan ^a   Roeder, Robert G ^c   Grant, Patrick A ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Chromatin; Histone modification; SAGA complex

Indexed keywords

ATAXIN 7; HISTONE DEACETYLASE INHIBITOR; POLYGLUTAMINE; REELIN; TRICHOSTATIN A;

ARTICLE; ASTROCYTE; CELL CULTURE; CELL MATURATION; CEREBELLUM; EMBRYO; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL;

ASTROCYTES; CELL ADHESION MOLECULES, NEURONAL; EXTRACELLULAR MATRIX PROTEINS; HEK293 CELLS; HISTONE DEACETYLASE INHIBITORS; HISTONES; HUMANS; HYDROXAMIC ACIDS; INTRANUCLEAR INCLUSION BODIES; LENTIVIRUS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; PEPTIDES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECOMBINATION, GENETIC; RNA, MESSENGER; SERINE ENDOPEPTIDASES; SPINOCEREBELLAR ATAXIAS; TRANSCRIPTION, GENETIC; TRINUCLEOTIDE REPEAT EXPANSION; UBIQUITINATION;

EID: 84871823260     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1218331110     Document Type: Article

References (49)

1. David G, et al. (1997) Cloning of the SCA7 gene reveals a highly unstable CAG repeat expansion. Nat Genet 17(1):65-70. (Pubitemid 27377533)
2. Custer SK, et al. (2006) Bergmann glia expression of polyglutamine- expanded ataxin-7 produces neurodegeneration by impairing glutamate transport. Nat Neurosci 9(10):1302-1311. (Pubitemid 44454272)
3. Yvert G, et al. (2000) Expanded polyglutamines induce neurodegeneration and transneuronal alterations in cerebellum and retina of SCA7 transgenic mice. Hum Mol Genet 9(17):2491-2506.
4. Garden GA, et al. (2002) Polyglutamine-expanded ataxin-7 promotes non-cell-autonomous Purkinje cell degeneration and displays proteolytic cleavage in ataxic transgenic mice. J Neurosci 22(12):4897-4905. (Pubitemid 37465605)
5. Yoo SY, et al. (2003) SCA7 knockin mice model human SCA7 and reveal gradual accumulation of mutant ataxin-7 in neurons and abnormalities in short-term plasticity. Neuron 37(3):383-401.
6. Lobsiger CS, Cleveland DW (2007) Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nat Neurosci 10(11):1355-1360. (Pubitemid 350014678)
7. Bradford J, et al. (2009) Expression of mutant huntingtin in mouse brain astrocytes causes age-dependent neurological symptoms. Proc Natl Acad Sci USA 106(52):22480-22485.
8. Brenner M, Kisseberth WC, Su Y, Besnard F, Messing A (1994) GFAP promoter directs astrocyte-specific expression in transgenic mice. J Neurosci 14(3 pt 1):1030-1037. (Pubitemid 24081901)
9. Eroglu C, Barres BA (2010) Regulation of synaptic connectivity by glia. Nature 468(7321):223-231.
10. Barres BA (2008) The mystery and magic of glia: A perspective on their roles in health and disease. Neuron 60(3):430-440.
11. Haydon PG (2001) GLIA: listening and talking to the synapse. Nat Rev Neurosci 2(3):185-193.
12. McMahon SJ, Pray-Grant MG, Schieltz D, Yates JR, 3rd, Grant PA (2005) Polyglutamine-expanded spinocerebellar ataxia-7 protein disrupts normal SAGA and SLIK histone acetyltransferase activity. Proc Natl Acad Sci USA 102(24):8478-8482. (Pubitemid 40862761)
13. Palhan VB, et al. (2005) Polyglutamine-expanded ataxin-7 inhibits STAGA histone acetyltransferase activity to produce retinal degeneration. Proc Natl Acad Sci USA 102 (24):8472-8477. (Pubitemid 40862760)
14. D'Arcangelo G, et al. (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719-723.
15. Hong SE, et al. (2000) Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 26(1):93-96.
16. Miyata T, et al. (2010) Migration, early axonogenesis, and Reelin-dependent layer-forming behavior of early/posterior-born Purkinje cells in the developing mouse lateral cerebellum. Neural Dev 5:23.
17. Sonoda Y, et al. (2001) Formation of intracranial tumors by genetically modified human astrocytes defines four pathways critical in the development of human anaplastic astrocytoma. Cancer Res 61(13):4956-4960. (Pubitemid 32681517)
18. Orr HT, Zoghbi HY (2007) Trinucleotide repeat disorders. Annu Rev Neurosci 30:575-621. (Pubitemid 47218768)
19. Yvert G, et al. (2001) SCA7 mouse models show selective stabilization of mutant ataxin-7 and similar cellular responses in different neuronal cell types. Hum Mol Genet 10(16):1679-1692. (Pubitemid 32776298)
20. Grant PA, et al. (1997) Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: Characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev 11(13):1640-1650. (Pubitemid 27300590)
21. Martinez E, Kundu TK, Fu J, Roeder RG (1998) A human SPT3-TAFII31-GCN5-L acetylase complex distinct from transcription factor IID. J Biol Chem 273(37):23781-23785. (Pubitemid 28435711)
22. Daniel JA, et al. (2004) Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription. J Biol Chem 279(3):1867-1871. (Pubitemid 38084455)
23. Zhao Y, et al. (2008) A TFTC/STAGA module mediates histone H2A and H2B deubiquitination, coactivates nuclear receptors, and counteracts heterochromatin silencing. Mol Cell 29(1):92-101.
24. Wyce A, et al. (2007) H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGA-related complex. Mol Cell 27(2):275-288. (Pubitemid 47058302)
25. Lee KK, Swanson SK, Florens L, Washburn MP, Workman JL (2009) Yeast Sgf73/Ataxin-7 serves to anchor the deubiquitination module into both SAGA and Slik(SALSA) HAT complexes. Epigenetics Chromatin 2(1):2.
26. Helmlinger D, et al. (2004) Ataxin-7 is a subunit of GCN5 histone acetyltransferase-containing complexes. Hum Mol Genet 13(12):1257-1265. (Pubitemid 38877879)
27. Giunti P, et al. (1999) Molecular and clinical study of 18 families with ADCA type II: Evidence for genetic heterogeneity and de novo mutation. Am J Hum Genet 64(6):1594-1603. (Pubitemid 30481511)
28. Curran T, D'Arcangelo G (1998) Role of reelin in the control of brain development. Brain Res Brain Res Rev 26(2-3):285-294. (Pubitemid 28318083)
29. Förster E, et al. (2006) Recent progress in understanding the role of Reelin in radial neuronal migration, with specific emphasis on the dentate gyrus. Eur J Neurosci 23(4):901-909. (Pubitemid 43344685)
30. Rice DS, et al. (2001) The reelin pathway modulates the structure and function of retinal synaptic circuitry. Neuron 31(6):929-941. (Pubitemid 32925280)
31. Qiu S, Zhao LF, Korwek KM, Weeber EJ (2006) Differential reelin-induced enhancement of NMDA and AMPA receptor activity in the adult hippocampus. J Neurosci 26(50):12943-12955. (Pubitemid 44954613)
32. Rice DS, Curran T (2001) Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24:1005-1039. (Pubitemid 32695252)
33. Herz J, Chen Y (2006) Reelin lipoprotein receptors and synaptic plasticity. Nat Rev Neurosci 7:850-859. (Pubitemid 44624177)
34. Shukla A, Bajwa P, Bhaumik SR (2006) SAGA-associated Sgf73p facilitates formation of the preinitiation complex assembly at the promoters either in a HAT-dependent or independent manner in vivo. Nucleic Acids Res 34(21):6225-6232. (Pubitemid 44942743)
35. Chen Y, Sharma RP, Costa RH, Costa E, Grayson DR (2002) On the epigenetic regulation of the human reelin promoter. Nucleic Acids Res 30(13):2930-2939. (Pubitemid 34778154)
36. Köhler A, Schneider M, Cabal GG, Nehrbass U, Hurt E (2008) Yeast Ataxin-7 links histone deubiquitination with gene gating and mRNA export. Nat Cell Biol 10(6):707-715. (Pubitemid 351772936)
37. Chen YC, et al. (2012) Gcn5 loss-of-function accelerates cerebellar and retinal degeneration in a SCA7 mouse model. Hum Mol Genet 21(2):394-405.
38. Mitchell CP, Chen Y, Kundakovic M, Costa E, Grayson DR (2005) Histone deacetylase inhibitors decrease reelin promoter methylation in vitro. J Neurochem 93(2):483-492. (Pubitemid 40547505)
39. Mookerjee S, et al. (2009) Posttranslational modification of ataxin-7 at lysine 257 prevents autophagy-mediated turnover of an N-terminal caspase-7 cleavage fragment. J Neurosci 29(48):15134-15144.
40. Steffan JS, et al. (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413(6857):739-743. (Pubitemid 33009952)
41. Hathorn T, Snyder-Keller A, Messer A (2011) Nicotinamide improves motor deficits and upregulates PGC-1α and BDNF gene expression in a mouse model of Huntington's disease. Neurobiol Dis 41(1):43-50.
42. Chou AH, Chen SY, Yeh TH, Weng YH, Wang HL (2011) HDAC inhibitor sodium butyrate reverses transcriptional downregulation and ameliorates ataxic symptoms in a transgenic mouse model of SCA3. Neurobiol Dis 41(2):481-488.
43. Arrasate M, Mitra S, Schweitzer ES, Segal MR, Finkbeiner S (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431(7010):805-810. (Pubitemid 39434070)
44. Bowman AB, Yoo SY, Dantuma NP, Zoghbi HY (2005) Neuronal dysfunction in a polyglutamine disease model occurs in the absence of ubiquitin-proteasome system impairment and inversely correlates with the degree of nuclear inclusion formation. Hum Mol Genet 14(5):679-691. (Pubitemid 40309593)
45. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680-685.
46. Gentleman RC, et al. (2004) Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 5(10):R80.
47. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Δ Δ C(T)) Method. Methods 25(4):402-408. (Pubitemid 34164012)
48. Aparicio O, et al. (2001) Chromatin Immunoprecipitation for Determining the Association of Proteins with Specific Genomic Sequences in Vivo (Wiley, New York).
49. Miller SA, Johnson ML, Stukenberg PT (2008) Kinetochore attachments require an interaction between unstructured tails on microtubules and Ndc80(Hec1). Curr Biol 18(22):1785-1791.