The Repressor Element 1-Silencing Transcription Factor Regulates Heart-Specific Gene Expression Using Multiple Chromatin-Modifying Complexes

REFERENCES

• Agalioti, T., G. Chen, and D. Thanos. 2002. Deciphering the transcriptional histone acetylation code for a human gene. Cell 111:381–392.
   PubMed Web of Science ®Google Scholar
• Andres, M. E., C. Burger, M. J. Peral-Rubio, E. Battaglioli, M. E. Anderson, J. Grimes, J. Dallman, N. Ballas, and G. Mandel. 1999. CoREST: a functional corepressor required for regulation of neural-specific gene expression. Proc. Natl. Acad. Sci. USA 96:9873–9878.
   PubMed Web of Science ®Google Scholar
• Andrews, N. C., and D. V. Faller. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19:2499.
   PubMed Web of Science ®Google Scholar
• Ballas, N., E. Battaglioli, F. Atouf, M. E. Andres, J. Chenoweth, M. E. Anderson, C. Burger, M. Moniwa, J. R. Davie, W. J. Bowers, H. J. Federoff, D. W. Rose, M. G. Rosenfeld, P. Brehm, and G. Mandel. 2001. Regulation of neuronal traits by a novel transcriptional complex. Neuron 31:353–365.
   PubMed Web of Science ®Google Scholar
• Ballas, N., C. Grunseich, D. D. Lu, J. C. Speh, and G. Mandel. 2005. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121:645–657.
   PubMed Web of Science ®Google Scholar
• Belyaev, N. D., I. C. Wood, A. W. Bruce, M. Street, J. B. Trinh, and N. J. Buckley. 2004. Distinct RE-1 silencing transcription factor-containing complexes interact with different target genes. J. Biol. Chem. 279:556–561.
   PubMedGoogle Scholar
• Bruce, A. W., I. J. Donaldson, I. C. Wood, S. A. Yerbury, M. I. Sadowski, M. Chapman, B. Gottgens, and N. J. Buckley. 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.
   PubMedGoogle Scholar
• Burnett, J. C., Jr., P. C. Kao, D. C. Hu, D. W. Heser, D. Heublein, J. P. Granger, T. J. Opgenorth, and G. S. Reeder. 1986. Atrial natriuretic peptide elevation in congestive heart failure in the human. Science 231:1145–1147.
   PubMed Web of Science ®Google Scholar
• Calderone, A., T. Jover, K. M. Noh, H. Tanaka, H. Yokota, Y. Lin, S. Y. Grooms, R. Regis, M. V. Bennett, and R. S. Zukin. 2003. Ischemic insults derepress the gene silencer REST in neurons destined to die. J. Neurosci. 23:2112–2121.
   PubMed Web of Science ®Google Scholar
• Chen, Z. F., A. J. Paquette, and D. J. Anderson. 1998. NRSF/REST is required in vivo for repression of multiple neuronal target genes during embryogenesis. Nat. Genet. 20:136–142.
   PubMedGoogle Scholar
• Cheong, A., A. J. Bingham, J. Li, B. Kumar, P. Sukumar, C. Munsch, N. J. Buckley, C. B. Neylon, K. E. Porter, D. J. Beech, and I. C. Wood. 2005. Downregulated REST transcription factor is a switch enabling critical potassium channel expression and cell proliferation. Mol. Cell 20:45–52.
   PubMedGoogle Scholar
• Chong, J. A., J. Tapia-Ramirez, S. Kim, J. J. Toledo-Aral, Y. Zheng, M. C. Boutros, Y. M. Altshuller, M. A. Frohman, S. D. Kraner, and G. Mandel. 1995. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80:949–957.
   PubMed Web of Science ®Google Scholar
• Durocher, D., C. Grepin, and M. Nemer. 1998. Regulation of gene expression in the endocrine heart. Recent Prog. Horm. Res. 53:7–23.
   PubMedGoogle Scholar
• Gill, G., and M. Ptashne. 1988. Negative effect of the transcriptional activator GAL4. Nature 334:721–724.
   PubMed Web of Science ®Google Scholar
• Grimes, J. A., S. J. Nielsen, E. Battaglioli, E. A. Miska, J. C. Speh, D. L. Berry, F. Atouf, B. C. Holdener, G. Mandel, and T. Kouzarides. 2000. The co-repressor mSin3A is a functional component of the REST-CoREST repressor complex. J. Biol. Chem. 275:9461–9467.
   PubMed Web of Science ®Google Scholar
• Hakimi, M. A., D. A. Bochar, J. Chenoweth, W. S. Lane, G. Mandel, and R. Shiekhattar. 2002. A core-BRAF35 complex containing histone deacetylase mediates repression of neuronal-specific genes. Proc. Natl. Acad. Sci. USA 99:7420–7425.
   PubMed Web of Science ®Google Scholar
• Harrison, S. M., E. McCall, and M. R. Boyett. 1992. The relationship between contraction and intracellular sodium in rat and guinea-pig ventricular myocytes. J. Physiol. 449:517–550.
   PubMedGoogle Scholar
• He, Q., M. Mendez, and M. C. LaPointe. 2002. Regulation of the human brain natriuretic peptide gene by GATA-4. Am. J. Physiol. Endocrinol. Metab. 283:E50–E57.
   PubMedGoogle Scholar
• He, T. C., S. Zhou, L. T. da Costa, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509–2514.
   PubMed Web of Science ®Google Scholar
• Houweling, A. C., M. M. van Borren, A. F. Moorman, and V. M. Christoffels. 2005. Expression and regulation of the atrial natriuretic factor encoding gene Nppa during development and disease. Cardiovasc. Res. 67:583–593.
   PubMedGoogle Scholar
• Huang, Y., S. J. Myers, and R. Dingledine. 1999. Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nat. Neurosci. 2:867–872.
   PubMedGoogle Scholar
• Humphrey, G. W., Y. Wang, V. R. Russanova, T. Hirai, J. Qin, Y. Nakatani, and B. H. Howard. 2001. Stable histone deacetylase complexes distinguished by the presence of SANT domain proteins CoREST/kiaa0071 and Mta-L1. J. Biol. Chem. 276:6817–6824.
   PubMed Web of Science ®Google Scholar
• Johnson, R., R. J. Gamblin, L. Ooi, A. W. Bruce, I. J. Donaldson, D. R. Westhead, I. C. Wood, R. M. Jackson, and N. J. Buckley. 2006. Identification of the REST regulon reveals extensive transposable element-mediated binding site duplication. Nucleic Acids Res. 34:3862–3877.
   PubMed Web of Science ®Google Scholar
• Kim, T. G., J. Chen, J. Sadoshima, and Y. Lee. 2004. Jumonji represses atrial natriuretic factor gene expression by inhibiting transcriptional activities of cardiac transcription factors. Mol. Cell. Biol. 24:10151–10160.
   PubMed Web of Science ®Google Scholar
• Kimes, B. W., and B. L. Brandt. 1976. Properties of a clonal muscle cell line from rat heart. Exp. Cell Res. 98:367–381.
   PubMed Web of Science ®Google Scholar
• Kuratomi, S., A. Kuratomi, K. Kuwahara, T. M. Ishii, K. Nakao, Y. Saito, and M. Takano. 2007. NRSF regulates the developmental and hypertrophic changes of HCN4 transcription in rat cardiac myocytes. Biochem. Biophys. Res. Commun. 353:67–73.
   PubMedGoogle Scholar
• Kuwahara, K., Y. Saito, E. Ogawa, N. Takahashi, Y. Nakagawa, Y. Naruse, M. Harada, I. Hamanaka, T. Izumi, Y. Miyamoto, I. Kishimoto, R. Kawakami, M. Nakanishi, N. Mori, and K. Nakao. 2001. The neuron-restrictive silencer element-neuron-restrictive silencer factor system regulates basal and endothelin 1-inducible atrial natriuretic peptide gene expression in ventricular myocytes. Mol. Cell. Biol. 21:2085–2097.
   PubMedGoogle Scholar
• Kuwahara, K., Y. Saito, M. Takano, Y. Arai, S. Yasuno, Y. Nakagawa, N. Takahashi, Y. Adachi, G. Takemura, M. Horie, Y. Miyamoto, T. Morisaki, S. Kuratomi, A. Noma, H. Fujiwara, Y. Yoshimasa, H. Kinoshita, R. Kawakami, I. Kishimoto, M. Nakanishi, S. Usami, M. Harada, and K. Nakao. 2003. NRSF regulates the fetal cardiac gene program and maintains normal cardiac structure and function. EMBO J. 22:6310–6321.
   PubMedGoogle Scholar
• Langenickel, T., I. Pagel, K. Hohnel, R. Dietz, and R. Willenbrock. 2000. Differential regulation of cardiac ANP and BNP mRNA in different stages of experimental heart failure. Am. J. Physiol. Heart Circ. Physiol. 278:H1500–H1506.
   PubMed Web of Science ®Google Scholar
• Lee, M. G., C. Wynder, D. A. Bochar, M. A. Hakimi, N. Cooch, and R. Shiekhattar. 2006. Functional interplay between histone demethylase and deacetylase enzymes. Mol. Cell. Biol. 26:6395–6402.
   PubMed Web of Science ®Google Scholar
• Lee, Y., A. J. Song, R. Baker, B. Micales, S. J. Conway, and G. E. Lyons. 2000. Jumonji, a nuclear protein that is necessary for normal heart development. Circ. Res. 86:932–938.
   PubMedGoogle Scholar
• Leichter, M., and G. Thiel. 1999. Transcriptional repression by the zinc finger protein REST is mediated by titratable nuclear factors. Eur. J. Neurosci. 11:1937–1946.
   PubMedGoogle Scholar
• Lu, J. R., T. A. McKinsey, H. Xu, D. Z. Wang, J. A. Richardson, and E. N. Olson. 1999. FOG-2, a heart- and brain-enriched cofactor for GATA transcription factors. Mol. Cell. Biol. 19:4495–4502.
   PubMedGoogle Scholar
• Lunyak, V. V., R. Burgess, G. G. Prefontaine, C. Nelson, S. H. Sze, J. Chenoweth, P. Schwartz, P. A. Pevzner, C. Glass, G. Mandel, and M. G. Rosenfeld. 2002. Corepressor-dependent silencing of chromosomal regions encoding neuronal genes. Science 298:1747–1752.
   PubMed Web of Science ®Google Scholar
• Ma, K. K., K. Banas, and A. J. de Bold. 2005. Determinants of inducible brain natriuretic peptide promoter activity. Regul. Pept. 128:169–176.
   PubMedGoogle Scholar
• McBride, K., and M. Nemer. 2001. Regulation of the ANF and BNP promoters by GATA factors: lessons learned for cardiac transcription. Can. J. Physiol. Pharmacol. 79:673–681.
   PubMedGoogle Scholar
• Milne, T. A., S. D. Briggs, H. W. Brock, M. E. Martin, D. Gibbs, C. D. Allis, and J. L. Hess. 2002. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10:1107–1117.
   PubMed Web of Science ®Google Scholar
• Mukoyama, M., K. Nakao, K. Obata, M. Jougasaki, M. Yoshimura, E. Morita, K. Hosoda, S. Suga, Y. Ogawa, H. Yasue, et al. 1991. Augmented secretion of brain natriuretic peptide in acute myocardial infarction. Biochem. Biophys. Res. Commun. 180:431–436.
   PubMed Web of Science ®Google Scholar
• Nadeau, H., and H. A. Lester. 2002. NRSF causes cAMP-sensitive suppression of sodium current in cultured hippocampal neurons. J. Neurophysiol. 88:409–421.
   PubMedGoogle Scholar
• Nakagawa, Y., K. Kuwahara, M. Harada, N. Takahashi, S. Yasuno, Y. Adachi, R. Kawakami, M. Nakanishi, K. Tanimoto, S. Usami, H. Kinoshita, Y. Saito, and K. Nakao. 2006. Class II HDACs mediate CaMK-dependent signaling to NRSF in ventricular myocytes. J. Mol. Cell. Cardiol. 41:1010–1022.
   PubMed Web of Science ®Google Scholar
• Nakamura, T., T. Mori, S. Tada, W. Krajewski, T. Rozovskaia, R. Wassell, G. Dubois, A. Mazo, C. M. Croce, and E. Canaani. 2002. ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol. Cell 10:1119–1128.
   PubMed Web of Science ®Google Scholar
• Naruse, Y., T. Aoki, T. Kojima, and N. Mori. 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.
   PubMedGoogle Scholar
• Ogawa, E., Y. Saito, K. Kuwahara, M. Harada, Y. Miyamoto, I. Hamanaka, N. Kajiyama, N. Takahashi, T. Izumi, R. Kawakami, I. Kishimoto, Y. Naruse, N. Mori, and K. Nakao. 2002. Fibronectin signaling stimulates BNP gene transcription by inhibiting neuron-restrictive silencer element-dependent repression. Cardiovasc. Res. 53:451–459.
   PubMed Web of Science ®Google Scholar
• Ooi, L., N. D. Belyaev, K. Miyake, I. C. Wood, and N. J. Buckley. 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.
   PubMedGoogle Scholar
• Paquette, A. J., S. E. Perez, and D. J. Anderson. 2000. Constitutive expression of the neuron-restrictive silencer factor (NRSF)/REST in differentiating neurons disrupts neuronal gene expression and causes axon pathfinding errors in vivo. Proc. Natl. Acad. Sci. USA 97:12318–12323.
   PubMed Web of Science ®Google Scholar
• Pikkarainen, S., H. Tokola, R. Kerkela, T. Majalahti-Palviainen, O. Vuolteenaho, and H. Ruskoaho. 2003. Endothelin-1-specific activation of B-type natriuretic peptide gene via p38 mitogen-activated protein kinase and nuclear ETS factors. J. Biol. Chem. 278:3969–3975.
   PubMedGoogle Scholar
• Rivard, A., N. Principe, and V. Andres. 2000. Age-dependent increase in c-fos activity and cyclin A expression in vascular smooth muscle cells. A potential link between aging, smooth muscle cell proliferation and atherosclerosis. Cardiovasc. Res. 45:1026–1034.
   PubMedGoogle Scholar
• Roopra, A., R. Qazi, B. Schoenike, T. J. Daley, and J. F. Morrison. 2004. Localized domains of g9a-mediated histone methylation are required for silencing of neuronal genes. Mol. Cell 14:727–738.
   PubMedGoogle Scholar
• Roopra, A., L. Sharling, I. C. Wood, T. Briggs, U. Bachfischer, A. J. Paquette, and N. J. Buckley. 2000. Transcriptional repression by neuron-restrictive silencer factor is mediated via the Sin3-histone deacetylase complex. Mol. Cell. Biol. 20:2147–2157.
   PubMed Web of Science ®Google Scholar
• Rosati, B., F. Grau, and D. McKinnon. 2006. Regional variation in mRNA transcript abundance within the ventricular wall. J. Mol. Cell. Cardiol. 40:295–302.
   PubMedGoogle Scholar
• Rosenzweig, A., T. D. Halazonetis, J. G. Seidman, and C. E. Seidman. 1991. Proximal regulatory domains of rat atrial natriuretic factor gene. Circulation 84:1256–1265.
   PubMedGoogle Scholar
• Saito, Y., K. Nakao, H. Arai, K. Nishimura, K. Okumura, K. Obata, G. Takemura, H. Fujiwara, A. Sugawara, T. Yamada, et al. 1989. Augmented expression of atrial natriuretic polypeptide gene in ventricle of human failing heart. J. Clin. Investig. 83:298–305.
   PubMedGoogle Scholar
• Schoenherr, C. J., and D. J. Anderson. 1995. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267:1360–1363.
   PubMed Web of Science ®Google Scholar
• Shi, Y., F. Lan, C. Matson, P. Mulligan, J. R. Whetstine, P. A. Cole, R. A. Casero, and Y. Shi. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953.
   PubMed Web of Science ®Google Scholar
• Shin, C. H., Z. P. Liu, R. Passier, C. L. Zhang, D. Z. Wang, T. M. Harris, H. Yamagishi, J. A. Richardson, G. Childs, and E. N. Olson. 2002. Modulation of cardiac growth and development by HOP, an unusual homeodomain protein. Cell 110:725–735.
   PubMedGoogle Scholar
• Shiojima, I., I. Komuro, T. Oka, Y. Hiroi, T. Mizuno, E. Takimoto, K. Monzen, R. Aikawa, H. Akazawa, T. Yamazaki, S. Kudoh, and Y. Yazaki. 1999. Context-dependent transcriptional cooperation mediated by cardiac transcription factors Csx/Nkx-2.5 and GATA-4. J. Biol. Chem. 274:8231–8239.
   PubMedGoogle Scholar
• Spicer, D. B., J. Rhee, W. L. Cheung, and A. B. Lassar. 1996. Inhibition of myogenic bHLH and MEF2 transcription factors by the bHLH protein Twist. Science 272:1476–1480.
   PubMed Web of Science ®Google Scholar
• Tachibana, M., K. Sugimoto, T. Fukushima, and Y. Shinkai. 2001. Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J. Biol. Chem. 276:25309–25317.
   PubMed Web of Science ®Google Scholar
• Tapia-Ramirez, J., B. J. Eggen, M. J. Peral-Rubio, J. J. Toledo-Aral, and G. Mandel. 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.
   PubMed Web of Science ®Google Scholar
• Thuerauf, D. J., D. S. Hanford, and C. C. Glembotski. 1994. Regulation of rat brain natriuretic peptide transcription. A potential role for GATA-related transcription factors in myocardial cell gene expression. J. Biol. Chem. 269:17772–17775.
   PubMedGoogle Scholar
• Wei, C. M., P. C. Kao, J. T. Lin, D. M. Heublein, H. V. Schaff, and J. C. Burnett, Jr. 1993. Circulating beta-atrial natriuretic factor in congestive heart failure in humans. Circulation 88:1016–1020.
   PubMedGoogle Scholar
• Wood, I. C., N. D. Belyaev, A. W. Bruce, C. Jones, M. Mistry, A. Roopra, and N. J. Buckley. 2003. Interaction of the repressor element 1-silencing transcription factor (REST) with target genes. J. Mol. Biol. 334:863–874.
   PubMedGoogle Scholar
• Wynder, C., M. A. Hakimi, J. A. Epstein, A. Shilatifard, and R. Shiekhattar. 2005. Recruitment of MLL by HMG-domain protein iBRAF promotes neural differentiation. Nat. Cell Biol. 7:1113–1117.
   PubMed Web of Science ®Google Scholar
• Yeo, M., S. K. Lee, B. Lee, E. C. Ruiz, S. L. Pfaff, and G. N. Gill. 2005. Small CTD phosphatases function in silencing neuronal gene expression. Science 307:596–600.
   PubMed Web of Science ®Google Scholar
• You, A., J. K. Tong, C. M. Grozinger, and S. L. Schreiber. 2001. CoREST is an integral component of the CoREST-human histone deacetylase complex. Proc. Natl. Acad. Sci. USA 98:1454–1458.
   PubMed Web of Science ®Google Scholar
• Zang, M. X., Y. Li, L. X. Xue, H. T. Jia, and H. Jing. 2004. Cooperative activation of atrial naturetic peptide promoter by dHAND and MEF2C. J. Cell. Biochem. 93:1255–1266.
   PubMedGoogle Scholar
• Zuccato, C., M. Tartari, A. Crotti, D. Goffredo, M. Valenza, L. Conti, T. Cataudella, B. R. Leavitt, M. R. Hayden, T. Timmusk, D. Rigamonti, and E. Cattaneo. 2003. Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat. Genet. 35:76–83.
   PubMed Web of Science ®Google Scholar