miRNA-132 orchestrates chromatin remodeling and translational control of the circadian clock

Human Molecular Genetics

Volumn 20, Issue 4, 2011, Pages 731-751

  Alvarez Saavedra, Matías ^a,d   Antoun, Ghadi ^a   Yanagiya, Akiko ^b   Oliva Hernandez, Reynaldo ^a   Cornejo Palma, Daniel ^a   Perez Iratxeta, Carolina ^c   Sonenberg, Nahum ^b   Cheng, Hai Ying M ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^d Medical University of Vienna   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MIRNA 132; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MODULATION; MOUSE; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PRIORITY JOURNAL; PROMOTER REGION; SUPRACHIASMATIC NUCLEUS; TRANSLATION REGULATION;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CIRCADIAN RHYTHM; COMPUTATIONAL BIOLOGY; E1A-ASSOCIATED P300 PROTEIN; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; IMMEDIATE-EARLY PROTEINS; LIGHT; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; NIH 3T3 CELLS; PERIOD CIRCADIAN PROTEINS; RETINOBLASTOMA-BINDING PROTEIN 2; RNA STABILITY; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA;

EID: 78751686549     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq519     Document Type: Article

References (65)

1. Reppert, S.M. and Weaver, D.R. (2002) Coordination of circadian timing in mammals. Nature, 418, 935-941.
2. Toh, K.L., Jones, C.R., He, Y., Eide, E.J., Hinz, W.A., Virshup, D.M., Ptácek, L.J. and Fu, Y.H. (2001) An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science, 291, 1040-1043.
3. Xu, Y., Padiath, Q.S., Shapiro, R.E., Jones, C.R., Wu, S.C., Saigoh, N., Saigoh, K., Ptácek, L.J. and Fu, Y.H. (2005) Functional consequences of a CKIdelta mutation causing familial advanced sleep phase syndrome. Nature, 434, 640-644.
4. Ebisawa, T., Uchiyama, M., Kajimura, N., Mishima, K., Kamei, Y., Katoh, M., Watanabe, T., Sekimoto, M., Shibui, K., Kim, K. et al. (2001) Association of structural polymorphisms in the human period3 gene with delayed sleep phase syndrome. EMBO Rep., 2, 342-346.
5. Panda, S., Antoch, M.P., Miller, B.H., Su, A.I., Schook, A.B., Straume, M., Schultz, P.G., Kay, S.A., Takahashi, J.S. and Hogenesch, J.B. (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell, 109, 307-220.
6. Etchegaray, J.P., Lee, C., Wade, P.A. and Reppert, S.M. (2003) Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature, 421, 177-182.
7. Doi, M., Hirayama, J. and Sassone-Corsi, P. (2006) Circadian regulator CLOCK is a histone acetyltransferase. Cell, 125, 497-508.
8. Asher, G., Gatfield, D., Stratmann, M., Reinke, H., Dibner, C., Kreppel, F., Mostoslavsky, R., Alt, F.W. and Schibler, U. (2008) SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell, 134, 317-328.
9. +-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell, 134, 329-340.
10. Etchegaray, J.P., Yang, X., DeBruyne, J.P., Peters, A.H., Weaver, D.R., Jenuwein, T. and Reppert, S.M. (2006) The polycomb group protein EZH2 is required for mammalian circadian clock function. J. Biol. Chem., 281, 21209-21215.
11. Chen, S.T., Choo, K.B., Hou, M.F., Yeh, K.T., Kuo, S.J. and Chang, J.G. (2005) Deregulated expression of the PER1, PER2 and PER3 genes in breast cancers. Carcinogenesis, 26, 1241-1246.
12. Price, J.L., Blau, J., Rothenfluh, A., Abodeely, M., Kloss, B. and Young, M.W. (1998) double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell, 94, 83-95.
13. Shirogane, T., Jin, J., Ang, X.L. and Harper, J.W. (2005) SCFbeta-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein. J. Biol. Chem., 280, 26863-26872.
14. Busino, L., Bassermann, F., Maiolica, A., Lee, C., Nolan, P.M., Godinho, S.I., Draetta, G.F. and Pagano, M. (2007) SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science, 316, 900-904.
15. Siepka, S.M., Yoo, S.H., Park, J., Song, W., Kumar, V., Hu, Y., Lee, C. and Takahashi, J.S. (2007) Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression. Cell, 129, 1011-1023.
16. Baggs, J.E. and Green, C.B. (2003) Nocturnin, a deadenylase in Xenopus laevis retina: a mechanism for posttranscriptional control of circadian-related mRNA. Curr. Biol., 13, 189-198.
17. Cao, R., Lee, B., Cho, H.Y., Saklayen, S. and Obrietan, K. (2008) Photic regulation of the mTOR signaling pathway in the suprachiasmatic circadian clock. Mol. Cell. Neurosci., 38, 312-324.
18. Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
19. Cheng, H.-Y.M., Papp, J.W., Varlamova, O., Dziema, H., Russell, B., Curfman, J.P., Nakazawa, T., Shimizu, K., Okamura, H., Impey, S. and Obrietan, K. (2007) microRNA modulation of circadian-clock period and entrainment. Neuron, 54, 813-829.
20. Yang, M., Lee, J.E., Padgett, R.W. and Edery, I. (2008) Circadian regulation of a limited set of conserved microRNAs in Drosophila. BMC Genomics, 9, 83.
21. Gatfield, D., Le Martelot, G., Vejnar, C.E., Gerlach, D., Schaad, O., Fleury-Olela, F., Ruskeepää, A.L., Oresic, M., Esau, C.C., Zdobnov, E.M. and Schibler, U. (2009) Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev., 23, 1313-1326.
22. Kadener, S., Menet, J.S., Sugino, K., Horwich, M.D., Weissbein, U., Nawathean, P., Vagin, V.V., Zamore, P.D., Nelson, S.B. and Rosbash, M. (2009) A role for microRNAs in the Drosophila circadian clock. Genes Dev., 23, 2179-2191.
23. Lim, L.P., Lau, N.C., Garrett-Engele, P., Grimson, A., Schelter, J.M., Castle, J., Bartel, D.P., Linsley, P.S. and Johnson, J.M. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature, 433, 769-773.
24. Iliopoulos, D., Hirsch, H.A. and Struhl, K. (2009) An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell, 139, 693-706.
25. Valastyan, S., Reinhardt, F., Benaich, N., Calogrias, D., Szász, A.M., Wang, Z.C., Brock, J.E., Richardson, A.L. and Weinberg, R.A. (2009) A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell, 137, 1032-1046.
26. Xu, N., Papagiannakopoulos, T., Pan, G., Thomson, J.A. and Kosik, K.S. (2009) MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell, 137, 647-658.
27. Lewis, B.P., Burge, C.B. and Bartel, D.P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell, 120, 15-20.
28. Zhou, Z., Hong, E.J., Cohen, S., Zhao, W.N., Ho, H.Y., Schmidt, L., Chen, W.G., Lin, Y., Savner, E., Griffith, E.C. et al. (2006) Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron, 52, 255-269.
29. Porterfield, V.M. and Mintz, E.M. (2009) Temporal patterns of light-induced immediate-early gene expression in the suprachiasmatic nucleus. Neurosci. Lett., 463, 70-73.
30. Chahrour, M., Jung, S.Y., Shaw, C., Zhou, X., Wong, S.T., Qin, J. and Zoghbi, H.Y. (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science, 320, 1224-1229.
31. Ripperger, J.A. and Schibler, U. (2006) Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat. Genet., 38, 369-374.
32. Mayford, M., Bach, M.E., Huang, Y.Y., Wang, L., Hawkins, R.D. and Kandel, E.R. (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science, 274, 1678-1683.
33. Klose, R.J., Yan, Q., Tothova, Z., Yamane, K., Erdjument-Bromage, H., Tempst, P., Gilliland, D.G., Zhang, Y. and Kaelin, W.G. Jr. (2007) The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell, 128, 889-900.
34. Jenuwein, T. and Allis, C.D. (2001) Translating the histone code. Science, 293, 1074-1080.
35. Vo, N. and Goodman, R.H. (2001) CREB-binding protein and p300 in transcriptional regulation. J. Biol. Chem., 276, 13505-13508.
36. Nan, X., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N. and Bird, A. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature, 393, 386-389.
37. Young, J.I., Hong, E.P., Castle, J.C., Crespo-Barreto, J., Bowman, A.B., Rose, M.F., Kang, D., Richman, R., Johnson, J.M., Berget, S. et al. (2005) Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc. Natl Acad. Sci. USA, 102, 17551-17558.
38. Piazza, C.C., Fisher, W., Kiesewetter, K., Bowman, L. and Moser, H. (1990) Aberrant sleep patterns in children with the Rett syndrome. Brain Dev., 12, 488-493.
39. Mauxion, F., Faux, C. and Séraphin, B. (2008) The BTG2 protein is a general activator of mRNA deadenylation. EMBO J., 27, 1039-1048.
40. Woo, K.C., Kim, T.D., Lee, K.H., Kim, D.Y., Kim, W., Lee, K.Y. and Kim, K.T. (2009) Mouse period 2 mRNA circadian oscillation is modulated by PTB-mediated rhythmic mRNA degradation. Nucleic Acids Res., 37, 26-37.
41. Imataka, H., Gradi, A. and Sonenberg, N. (1998) A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J., 17, 7480-7489.
42. Khaleghpour, K., Svitkin, Y.V., Craig, A.W., DeMaria, C.T., Deo, R.C., Burley, S.K. and Sonenberg, N. (2001) Translational repression by a novel partner of human poly(A) binding protein, Paip2. Mol. Cell, 7, 205-216.
43. Ueda, H.R., Chen, W., Adachi, A., Wakamatsu, H., Hayashi, S., Takasugi, T., Nagano, M., Nakahama, K., Suzuki, Y., Sugano, S. et al. (2002) A transcription factor response element for gene expression during circadian night. Nature, 418, 534-539.
44. Klein, M.E., Lioy, D.T., Ma, L., Impey, S., Mandel, G. and Goodman, R.H. (2007) Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat. Neurosci., 10, 1513-1514.
45. Lagos, D., Pollara, G., Henderson, S., Gratrix, F., Fabani, M., Milne, R.S., Gotch, F. and Boshoff, C. (2010) miR-132 regulates antiviral innate immunity through suppression of the p300 transcriptional co-activator. Nat. Cell Biol., 12, 513-519.
46. Bruce, K., Myers, F.A., Mantouvalou, E., Lefevre, P., Greaves, I., Bonifer, C., Tremethick, D.J., Thorne, A.W. and Crane-Robinson, C. (2005) The replacement histone H2A.Z in a hyperacetylated form is a feature of active genes in the chicken. Nucleic Acids Res., 33, 5633-5639.
47. Shigeyoshi, Y., Taguchi, K., Yamamoto, S., Takekida, S., Yan, L., Tei, H., Moriya, T., Shibata, S., Loros, J.J., Dunlap, J.C. et al. (1997) Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell, 91, 1043-1053.
48. Takumi, T., Matsubara, C., Shigeyoshi, Y., Taguchi, K., Yagita, K., Maebayashi, Y., Sakakida, Y., Okumura, K., Takashima, N. and Okamura, H. (1998) A new mammalian period gene predominantly expressed in the suprachiasmatic nucleus. Genes Cells, 3, 167-176.
49. Yan, L. and Silver, R. (2004) Resetting the brain clock: time course and localization of mPER1 and mPER2 protein expression in suprachiasmatic nuclei during phase shifts. Eur. J. Neurosci., 19, 1105-1109.
50. Obrietan, K., Impey, S. and Storm, D.R. (1998) Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat. Neurosci., 1, 693-700.
51. Curtis, A.M., Seo, S.B., Westgate, E.J., Rudic, R.D., Smyth, E.M., Chakravarti, D., FitzGerald, G.A. and McNamara, P. (2004) Histone acetyltransferase-dependent chromatin remodeling and the vascular clock. J. Biol. Chem., 279, 7091-7097.
52. Jones, P.L., Veenstra, G.J., Wade, P.A., Vermaak, D., Kass, S.U., Landsberger, N., Strouboulis, J. and Wolffe, A.P. (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet., 19, 187-191.
53. Yasui, D.H., Peddada, S., Bieda, M.C., Vallero, R.O., Hogart, A., Nagarajan, R.P., Thatcher, K.N., Farnham, P.J. and Lasalle, J.M. (2007) Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl Acad. Sci. USA, 104, 19416-19421.
54. Mnatzakanian, G.N., Lohi, H., Munteanu, I., Alfred, S.E., Yamada, T., MacLeod, P.J., Jones, J.R., Scherer, S.W., Schanen, N.C., Friez, M.J. et al. (2004) A previously unidentified MECP2 open reading frame defines a new protein isoform relevant to Rett syndrome. Nat. Genet., 36, 339-341.
55. Dragich, J.M., Kim, Y.H., Arnold, A.P. and Schanen, N.C. (2007) Differential distribution of the MeCP2 splice variants in the postnatal mouse brain. J. Comp. Neurol., 501, 526-542.
56. Yamaguchi, S., Mitsui, S., Miyake, S., Yan, L., Onishi, H., Yagita, K., Suzuki, M., Shibata, S., Kobayashi, M. and Okamura, H. (2000) The 5′ upstream region of mPer1 gene contains two promoters and is responsible for circadian oscillation. Curr. Biol., 10, 873-876.
57. Yoo, S.H., Ko, C.H., Lowrey, P.L., Buhr, E.D., Song, E.J., Chang, S., Yoo, O.J., Yamazaki, S., Lee, C. and Takahashi, J.S. (2005) A noncanonical E-box enhancer drives mouse Period2 circadian oscillations in vivo. Proc. Natl Acad. Sci. USA, 102, 2608-2613.
58. Walton, K.M., Rehfuss, R.P., Chrivia, J.C., Lochner, J.E. and Goodman, R.H. (1992) A dominant repressor of cyclic adenosine 3′,5′-monophosphate (cAMP)-regulated enhancer-binding protein activity inhibits the cAMP-mediated induction of the somatostatin promoter in vivo. Mol. Endocrinol., 6, 647-655.
59. Yanagiya, A., Delbes, G., Svitkin, Y.V., Robaire, B. and Sonenberg, N. (2010) The poly(A)-binding protein partner Paip2a controls translation during late spermiogenesis in mice. J. Clin. Invest., 120, 3389-3400.
60. Goldstrohm, A.C. and Wickens, M. (2008) Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell. Biol., 9, 337-344.
61. Wormington, M., Searfoss, A.M. and Hurney, C.A. (1996) Overexpression of poly(A) binding protein prevents maturation-specific deadenylation and translational inactivation in Xenopus oocytes. EMBO J., 15, 900-909.
62. Walters, R.W., Bradrick, S.S. and Gromeier, M. (2010) Poly(A)-binding protein modulates mRNA susceptibility to cap-dependent miRNA-mediated repression. RNA, 16, 239-250.
63. 2+/cAMP response element-binding protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the suprachiasmatic nucleus circadian clock. J. Biol. Chem., 278, 718-723.
64. Cheng, H.-Y.M., Alvarez-Saavedra, M., Dziema, H., Choi, Y.S., Li, A. and Obrietan, K. (2009) Segregation of expression of mPeriod gene homologs in neurons and glia: possible divergent roles of mPeriod1 and mPeriod2 in the brain. Hum. Mol. Genet., 18, 3110-3124.
65. Cheng, H.-Y.M., Dziema, H., Papp, J., Mathur, D.P., Koletar, M., Ralph, M.R., Penninger, J.M. and Obrietan, K. (2006) The molecular gatekeeper Dexras1 sculpts the photic responsiveness of the mammalian circadian clock. J. Neurosci., 26, 12984-12995.