RE1 silencing transcription factor is involved in regulating neuron-specific expression of α-internexin and neurofilament genes

Journal of Neurochemistry

Volumn 109, Issue 6, 2009, Pages 1610-1623

  Ching, Gee Y ^a   Liem, Ronald K H ^a  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

internexin; Histone modification; Neurofilament; Neuronal intermediate filament; RE1 silencing transcription factor; Transcription

Indexed keywords

ALPHA INTERNEXIN; HISTONE DEACETYLASE 1; METHYL CPG BINDING PROTEIN 2; NEUROFILAMENT H PROTEIN; NEUROFILAMENT M PROTEIN; NEUROFILAMENT PROTEIN; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR SIN3A; TRICHOSTATIN A; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA FLANKING REGION; GENE REPRESSION; GENETIC TRANSFECTION; METHYLATION; MOUSE; NEUROFILAMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HUMANS; INTERMEDIATE FILAMENT PROTEINS; METHYL-CPG-BINDING PROTEIN 2; MICE; NERVE TISSUE PROTEINS; NEUROFILAMENT PROTEINS; NEURONS; NIH 3T3 CELLS; RATS; REPRESSOR PROTEINS; TRANSFECTION;

EID: 65949105943     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06052.x     Document Type: Article

References (76)

1. Abderrahmani A., Steinmann M., Plaisance V., Niederhauser G., Haefliger J. A., Mooser V., Bonny C., Nicod P. Waeber G. (2001) The transcriptional repressor REST determines the cell-specific expression of the human MAPK8IP1 gene encoding IB1 (JIP-1). Mol. Cell. Biol. 21, 7256 7267. (Pubitemid 32953479)
2. Andres M. E., Burger C., Peral-Rubio M. J., Battaglioli E., Anderson M. E., Grimes J., Dallman J., Ballas N. Mandel G. (1999) CoREST: a functional corepressor required for regulation of neural-specific gene expression. Proc. Natl Acad. Sci. USA 96, 9873 9878. (Pubitemid 29398825)
3. Ballas N., Battaglioli E., Atouf F. et al. (2001) Regulation of neuronal traits by a novel transcriptional complex. Neuron 31, 353 365. (Pubitemid 32778556)
4. Ballas N., Grunseich C., Lu D. D., Speh J. C. Mandel G. (2005) REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121, 645 657. (Pubitemid 40720016)
5. Battaglioli E., Andres M. E., Rose D. W., Chenoweth J. G., Rosenfeld M. G., Anderson M. E. Mandel G. (2002) REST repression of neuronal genes requires components of the hSWI.SNF complex. J. Biol. Chem. 277, 41038 41045. (Pubitemid 35215694)
6. Beaudet L., Charron G., Houle D., Tretjakoff I., Peterson A. Julien J. P. (1992) Intragenic regulatory elements contribute to transcriptional control of the neurofilament light gene. Gene 116, 205 214.
7. Bernstein B. E., Kamal M., Lindblad-Toh K. et al. (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120, 169 181. (Pubitemid 40174761)
8. Bingham A. J., Ooi L., Kozera L., White E. Wood I. C. (2007) The repressor element 1-silencing transcription factor regulates heart-specific gene expression using multiple chromatin-modifying complexes. Mol. Cell. Biol. 27, 4082 4092. (Pubitemid 47011005)
9. Bruce A. W., Donaldson I. J., Wood I. C., Yerbury S. A., Sadowski M. I., Chapman M., Gottgens B. Buckley N. J. (2004) Genome-wide analysis of repressor element 1 silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) target genes. Proc. Natl Acad. Sci. USA 101, 10458 10463. (Pubitemid 38924947)
10. Calderone A., Jover T., Noh K. M. et al. (2003) Ischemic insults derepress the gene silencer REST in neurons destined to die. J. Neurosci. 23, 2112 2121. (Pubitemid 36368899)
11. Ching G. Y. Liem R. K. (1993) Assembly of type IV neuronal intermediate filaments in nonneuronal cells in the absence of preexisting cytoplasmic intermediate filaments. J. Cell Biol. 122, 1323 1335. (Pubitemid 23277301)
12. Ching G. Y. Liem R. K. (1998) Roles of head and tail domains in alpha-internexin's self-assembly and coassembly with the neurofilament triplet proteins. J. Cell Sci. 111, 321 333. (Pubitemid 28097259)
13. Ching G. Y. Liem R. K. H. (2006) Neuronal Intermediate Filaments and Neurodegenerative Diseases: Intermediate Filaments, pp. 35 51, Landes Biosciences, Austin, TX.
14. Ching G. Y., Chien C. L., Flores R. Liem R. K. (1999) Overexpression of alpha-internexin causes abnormal neurofilamentous accumulations and motor coordination deficits in transgenic mice. J. Neurosci. 19, 2974 2986. (Pubitemid 29173994)
15. Chomczynski P. Sacchi N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156 159. (Pubitemid 17064313)
16. Chong J. A., Tapia-Ramirez J., Kim S. et al. (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80, 949 957.
17. Dion M. F., Altschuler S. J., Wu L. F. Rando O. J. (2005) Genomic characterization reveals a simple histone H4 acetylation code. Proc. Natl Acad. Sci. USA 102, 5501 5506. (Pubitemid 40530287)
18. DiProspero N. A., Chen E. Y., Charles V., Plomann M., Kordower J. H. Tagle D. A. (2004) Early changes in Huntington's disease patient brains involve alterations in cytoskeletal and synaptic elements. J. Neurocytol. 33, 517 533. (Pubitemid 40768575)
19. Dou Y., Milne T. A., Tackett A. J. et al. (2005) Physical association and coordinate function of the H3K4 methyltransferase MLL1 and the H4K16 acetyltransferase MOF. Cell 121, 873 885. (Pubitemid 40806419)
20. Duan Z., Zarebski A., Montoya-Durango D., Grimes H. L. Horwitz M. (2005) Gfi1 coordinates epigenetic repression of p21Cip/WAF1 by recruitment of histone lysine methyltransferase G9a and histone deacetylase 1. Mol. Cell. Biol. 25, 10338 10351. (Pubitemid 41681959)
21. Fang S., Miao J., Xiang L., Ponugoti B., Treuter E. Kemper J. K. (2007) Coordinated recruitment of histone methyltransferase G9a and other chromatin-modifying enzymes in SHP-mediated regulation of hepatic bile acid metabolism. Mol. Cell. Biol. 27, 1407 1424. (Pubitemid 46239822)
22. Ferrante R. J., Kubilus J. K., Lee J. et al. (2003) Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington's disease mice. J. Neurosci. 23, 9418 9427. (Pubitemid 37323042)
23. Fliegner K. H. Liem R. K. (1991) Cellular and molecular biology of neuronal intermediate filaments. Int. Rev. Cytol. 131, 109 167.
24. Fliegner K. H., Kaplan M. P., Wood T. L., Pintar J. E. Liem R. K. (1994) Expression of the gene for the neuronal intermediate filament protein alpha-internexin coincides with the onset of neuronal differentiation in the developing rat nervous system. J. Comp. Neurol. 342, 161 173. (Pubitemid 24100124)
25. Forneris F., Binda C., Vanoni M. A., Battaglioli E. Mattevi A. (2005) Human histone demethylase LSD1 reads the histone code. J. Biol. Chem. 280, 41360 41365. (Pubitemid 41832193)
26. Gardian G., Browne S. E., Choi D. K. et al. (2005) Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington's disease. J. Biol. Chem. 280, 556 563. (Pubitemid 40165021)
27. Greenway D. J., Street M., Jeffries A. Buckley N. J. (2007) RE1 Silencing transcription factor maintains a repressive chromatin environment in embryonic hippocampal neural stem cells. Stem Cells 25, 354 363. (Pubitemid 46232789)
28. Grimes J. A., Nielsen S. J., Battaglioli E. et al. (2000) The co-repressor mSin3A is a functional component of the REST-CoREST repressor complex. J. Biol. Chem. 275, 9461 9467. (Pubitemid 30185174)
29. Huang Y., Myers S. J. Dingledine R. (1999) Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nat. Neurosci. 2, 867 872. (Pubitemid 30602598)
30. Jacomy H., Zhu Q., Couillard-Despres S., Beaulieu J. M. Julien J. P. (1999) Disruption of type IV intermediate filament network in mice lacking the neurofilament medium and heavy subunits. J. Neurochem. 73, 972 984. (Pubitemid 29395453)
31. Kaplan M. P., Chin S. S., Fliegner K. H. Liem R. K. (1990) Alpha-internexin, a novel neuronal intermediate filament protein, precedes the low molecular weight neurofilament protein (NF-L) in the developing rat brain. J. Neurosci. 10, 2735 2748.
32. Kurdistani S. K., Tavazoie S. Grunstein M. (2004) Mapping global histone acetylation patterns to gene expression. Cell 117, 721 733. (Pubitemid 38748889)
33. Leconte L., Semonin O., Zvara A., Boisseau S., Poujeol C., Julien J. P. Simonneau M. (1994) Both upstream and intragenic sequences of the human neurofilament light gene direct expression of lacZ in neurons of transgenic mouse embryos. J. Mol. Neurosci. 5, 273 295.
34. Lee M. K., Xu Z., Wong P. C. Cleveland D. W. (1993) Neurofilaments are obligate heteropolymers in vivo. J. Cell Biol. 122, 1337 1350. (Pubitemid 23277302)
35. Lee M. G., Wynder C., Cooch N. Shiekhattar R. (2005) An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437, 432 435. (Pubitemid 41613507)
36. Lee M. G., Wynder C., Bochar D. A., Hakimi M. A., Cooch N. Shiekhattar R. (2006) Functional interplay between histone demethylase and deacetylase enzymes. Mol. Cell. Biol. 26, 6395 6402. (Pubitemid 44277880)
37. Lemonde S., Rogaeva A. Albert P. R. (2004) Cell type-dependent recruitment of trichostatin A-sensitive repression of the human 5-HT1A receptor gene. J. Neurochem. 88, 857 868. (Pubitemid 38199306)
38. Li B., Carey M. Workman J. L. (2007) The role of chromatin during transcription. Cell 128, 707 719. (Pubitemid 46273570)
39. Litt M. D., Simpson M., Gaszner M., Allis C. D. Felsenfeld G. (2001) Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science 293, 2453 2455. (Pubitemid 32917326)
40. Livak K. J. Schmittgen T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402 408. (Pubitemid 34164012)
41. Lunyak V. V., Burgess R., Prefontaine G. G. et al. (2002) Corepressor-dependent silencing of chromosomal regions encoding neuronal genes. Science 298, 1747 1752. (Pubitemid 35404110)
42. McGraw T. S., Mickle J. P., Shaw G. Streit W. J. (2002) Axonally transported peripheral signals regulate alpha-internexin expression in regenerating motoneurons. J. Neurosci. 22, 4955 4963. (Pubitemid 37465610)
43. Milne T. A., Briggs S. D., Brock H. W., Martin M. E., Gibbs D., Allis C. D. Hess J. L. (2002) MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10, 1107 1117. (Pubitemid 35453828)
44. Nakahira K., Ikenaka K., Wada K., Tamura T., Furuichi T. Mikoshiba K. (1990) Structure of the 68-kDa neurofilament gene and regulation of its expression. J. Biol. Chem. 265, 19786 19791. (Pubitemid 120013931)
45. Nakamura T., Mori T., Tada S. et al. (2002) ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol. Cell 10, 1119 1128. (Pubitemid 35453829)
46. Naruse Y., Aoki T., Kojima T. Mori N. (1999) Neural restrictive silencer factor recruits mSin3 and histone deacetylase complex to repress neuron-specific target genes. Proc. Natl Acad. Sci. USA 96, 13691 13696.
47. Nightingale K. P., Gendreizig S., White D. A., Bradbury C., Hollfelder F. Turner B. M. (2007) Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J. Biol. Chem. 282, 4408 4416. (Pubitemid 47100929)
48. Nihei K. Kowall N. W. (1992) Neurofilament and neural cell adhesion molecule immunocytochemistry of Huntington's disease striatum. Ann. Neurol. 31, 59 63.
49. Ooi L., Belyaev N. D., Miyake K., Wood I. C. Buckley N. J. (2006) BRG1 chromatin remodeling activity is required for efficient chromatin binding by repressor element 1-silencing transcription factor (REST) and facilitates REST-mediated repression. J. Biol. Chem. 281, 38974 38980. (Pubitemid 46041857)
50. Otto S. J., McCorkle S. R., Hover J. et al. (2007) A new binding motif for the transcriptional repressor REST uncovers large gene networks devoted to neuronal functions. J. Neurosci. 27, 6729 6739. (Pubitemid 46983428)
51. Palm K., Belluardo N., Metsis M. Timmusk T. (1998) Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene. J. Neurosci. 18, 1280 1296. (Pubitemid 28082414)
52. Qi Y., Wang J. K., McMillian M. Chikaraishi D. M. (1997) Characterization of a CNS cell line, CAD, in which morphological differentiation is initiated by serum deprivation. J. Neurosci. 17, 1217 1225. (Pubitemid 27073725)
53. Rao M. V., Campbell J., Yuan A., Kumar A., Gotow T., Uchiyama Y. Nixon R. A. (2003) The neurofilament middle molecular mass subunit carboxyl-terminal tail domains is essential for the radial growth and cytoskeletal architecture of axons but not for regulating neurofilament transport rate. J. Cell Biol. 163, 1021 1031. (Pubitemid 37541878)
54. Roopra A., Sharling L., Wood I. C., Briggs T., Bachfischer U., Paquette A. J. Buckley N. J. (2000) Transcriptional repression by neuron-restrictive silencer factor is mediated via the Sin3-histone deacetylase complex. Mol. Cell. Biol. 20, 2147 2157. (Pubitemid 30123830)
55. Roopra A., Qazi R., Schoenike B., Daley T. J. Morrison J. F. (2004) Localized domains of G9a-mediated histone methylation are required for silencing of neuronal genes. Mol. Cell 14, 727 738. (Pubitemid 38780847)
56. Schoenherr C. J. Anderson D. J. (1995) The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267, 1360 1363.
57. Schoenherr C. J., Paquette A. J. Anderson D. J. (1996) Identification of potential target genes for the neuron-restrictive silencer factor. Proc. Natl Acad. Sci. USA 93, 9881 9886. (Pubitemid 26296703)
58. Schubeler D., MacAlpine D. M., Scalzo D. et al. (2004) The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18, 1263 1271. (Pubitemid 38720594)
59. Shahbazian M. D. Grunstein M. (2007) Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76, 75 100.
60. Shi Y., Sawada J., Sui G. et al. (2003) Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422, 735 738. (Pubitemid 36514114)
61. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J. R., Cole P. A., Casero R. A. Shi Y. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941 953. (Pubitemid 40037608)
62. Shi Y. J., Matson C., Lan F., Iwase S., Baba T. Shi Y. (2005) Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell 19, 857 864. (Pubitemid 41316679)
63. Slomiany B. A., Kelly M. M. Kurtz D. T. (2000) Extraction of nuclear proteins with increased DNA binding activity. BioTechniques 28, 938 942. (Pubitemid 30263010)
64. Sun Y. M., Greenway D. J., Johnson R., Street M., Belyaev N. D., Deuchars J., Bee T., Wilde S. Buckley N. J. (2005) Distinct profiles of REST interactions with its target genes at different stages of neuronal development. Mol. Biol. Cell 16, 5630 5638. (Pubitemid 41752213)
65. Tahiliani M., Mei P., Fang R., Leonor T., Rutenberg M., Shimizu F., Li J., Rao A. Shi Y. (2007) The histone H3K4 demethylase SMCX links REST target genes to X-linked mental retardation. Nature 447, 601 605. (Pubitemid 46868038)
66. Tapia-Ramirez J., Eggen B. J., Peral-Rubio M. J., Toledo-Aral J. J. Mandel G. (1997) A single zinc finger motif in the silencing factor REST represses the neural-specific type II sodium channel promoter. Proc. Natl Acad. Sci. USA 94, 1177 1182. (Pubitemid 27087824)
67. Vakoc C. R., Sachdeva M. M., Wang H. Blobel G. A. (2006) Profile of histone lysine methylation across transcribed mammalian chromatin. Mol. Cell. Biol. 26, 9185 9195.
68. Westbrook T. F., Hu G., Ang X. L. et al. (2008) SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 452, 370 374.
69. Xu Z., Marszalek J. R., Lee M. K., Wong P. C., Folmer J., Crawford T. O., Hsieh S. T., Griffin J. W. Cleveland D. W. (1996) Subunit composition of neurofilaments specifies axonal diameter. J. Cell Biol. 133, 1061 1069. (Pubitemid 26172511)
70. Yazdanbakhsh K., Fraser P., Kioussis D., Vidal M., Grosveld F. Lindenbaum M. (1993) Functional analysis of the human neurofilament light chain gene promoter. Nucleic Acids Res. 21, 455 461. (Pubitemid 23155531)
71. Yoshida M. Horinouchi S. (1999) Trichostatin and leptomycin. Inhibition of histone deacetylation and signal-dependent nuclear export. Ann. NY Acad. Sci. 886, 23 36. (Pubitemid 30042419)
72. Yuan A., Rao M. V., Sasaki T. et al. (2006) Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS. J. Neurosci. 26, 10006 10019. (Pubitemid 44477162)
73. Zala D., Benchoua A., Brouillet E., Perrin V., Gaillard M. C., Zurn A. D., Aebischer P. Deglon N. (2005) Progressive and selective striatal degeneration in primary neuronal cultures using lentiviral vector coding for a mutant huntingtin fragment. Neurobiol. Dis. 20, 785 798. (Pubitemid 41622214)
74. Zhang K., Siino J. S., Jones P. R., Yau P. M. Bradbury E. M. (2004) A mass spectrometric "Western blot" to evaluate the correlations between histone methylation and histone acetylation. Proteomics 4, 3765 3775. (Pubitemid 39657454)
75. Zuccato C., Tartari M., Crotti A. et al. (2003) Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat. Genet. 35, 76 83. (Pubitemid 37048599)
76. Zuccato C., Belyaev N., Conforti P. et al. (2007) Widespread disruption of repressor element-1 silencing transcription factor/neuron-restrictive silencer factor occupancy at its target genes in Huntington's disease. J. Neurosci. 27, 6972 6983. (Pubitemid 47015906)