Ribonucleoprotein complexes that control circadian clocks

International Journal of Molecular Sciences

Volumn 14, Issue 5, 2013, Pages 9018-9036

  Wang, Dongni ^a   Liang, Xiaodi ^a   Chen, Xianyun ^a   Guo, Jinhu ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Circadian clock; Post transcription; Ribonucleoprotein; Transcription; Translation

Indexed keywords

CRYPTOCHROME 1; CRYPTOCHROME 2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MESSENGER RNA; MICRORNA; PER1 PROTEIN; PER2 PROTEIN; PROTEIN BMAL1; RETINOID RELATED ORPHAN RECEPTOR ALPHA; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; SIRTUIN 1; TRANSCRIPTION FACTOR CLOCK; MULTIPROTEIN COMPLEX;

3' UNTRANSLATED REGION; AU RICH ELEMENT; CIRCADIAN RHYTHM; GENE EXPRESSION REGULATION; HUMAN; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PERIODICITY; POLYADENYLATION; POSTTRANSCRIPTIONAL CONTROL; REVIEW; RIBOSOME; RNA CAPPING; RNA PROCESSING; RNA SPLICING; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; ACTIVE TRANSPORT; ALTERNATIVE RNA SPLICING; ANIMAL; GENETICS; METABOLISM;

ACTIVE TRANSPORT, CELL NUCLEUS; ALTERNATIVE SPLICING; ANIMALS; CIRCADIAN CLOCKS; HUMANS; MULTIPROTEIN COMPLEXES; POLYADENYLATION; RIBONUCLEOPROTEINS; RNA, MESSENGER;

EID: 84876894390     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14059018     Document Type: Review

References (128)

1. Duguay, D.; Cermakian, N. The crosstalk between physiology and circadian clock proteins. Chronobiol. Int. 2009, 26, 1479-1513.
2. Dunlap, J.C.; Loros, J.J. The neurospora circadian system. J. Biol. Rhythms. 2004, 19, 414-424.
3. Nagel, D.H.; Kay, S.A. Complexity in the wiring and regulation of plant circadian networks. Curr. Biol. 2012, 22, R648-R657.
4. Ozkaya, O.; Rosato, E. The circadian clock of the fly: A neurogenetics journey through time. Adv. Genet. 2012, 77, 79-123.
5. Albrecht, U.; Eichele, G. The mammalian circadian clock. Curr. Opin. Genet. Dev. 2003, 13, 271-277.
6. Bell-Pedersen, D.; Cassone, V.M.; Earnest, D.J.; Golden, S.S.; Hardin, P.E.; Thomas, T.L.; Zoran, M.J. Circadian rhythms from multiple oscillators: Lessons from diverse organisms. Nat. Rev. Genet. 2005, 6, 544-556.
7. Shoguchi, E.; Tanaka, M.; Shinzato, C.; Kawashima, T.; Satoh, N. A genome-wide survey of photoreceptor and circadian genes in the coral, Acropora digitifera. Gene 2013, 515, 426-431.
8. Chabot, J.R.; Pedraza, J.M.; Luitel, P.; van Oudenaarden, A. Stochastic gene expression out-of-steady-state in the cyanobacterial circadian clock. Nature 2007, 450, 1249-1252.
9. Feng, D.; Lazar, M.A. Clocks, metabolism, and the epigenome. Mol. Cell 2012, 47, 158-167.
10. Kawazoe, R.; Mahan, K.M.; Venghaus, B.E.; Carter, M.L.; Herrin, D.L. Circadian regulation of chloroplast transcription in Chlamydomonas is accompanied by little or no fluctuation in RPOD levels or core RNAP activity. Mol. Biol. Rep. 2012, 39, 10565-10571.
11. Lowrey, P.L.; Takahashi, J.S. Mammalian circadian biology: Elucidating genome-wide levels of temporal organization. Annu. Rev. Genomics Hum. Genet. 2004, 5, 407-441.
12. Zwiebel, L.J.; Hardin, P.E.; Liu, X.; Hall, J.C.; Rosbash, M. A post-transcriptional mechanism contributes to circadian cycling of a per-beta-galactosidase fusion protein. Proc. Natl. Acad. Sci. USA 1991, 88, 3882-3886.
13. So, W.V.; Rosbash, M. Post-transcriptional regulation contributes to Drosophila clock gene mRNA cycling. EMBO J. 1997, 16, 7146-7155.
14. Zhang, L.; Weng, W.; Guo, J. Posttranscriptional mechanisms in controlling eukaryotic circadian rhythms. FEBS Lett. 2011, 585, 1400-1405.
15. Koike, N.; Yoo, S.H.; Huang, H.C.; Kumar, V.; Lee, C.; Kim, T.K.; Takahashi, J.S. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 2012, 338, 349-354.
16. Menet, J.S.; Rodriguez, J.; Abruzzi, K.C.; Rosbash, M. Nascent-Seq reveals novel features of mouse circadian transcriptional regulation. ELife Sci. 2012, 1, e00011.
17. Dreyfuss, G.; Kim, V.N.; Kataoka, N. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell. Biol. 2002, 3, 195-205.
18. Glisovic, T.; Bachorik, J.L.; Yong, J.; Dreyfuss, G. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 2008, 582, 1977-1986.
19. Gao, F.B. Understanding fragile X syndrome: Insights from retarded flies. Neuron 2002, 34, 859-862.
20. Harms, E.; Kivimae, S.; Young, M.W.; Saez, L. Posttranscriptional and posttranslational regulation of clock genes. J. Biol. Rhythms 2004, 19, 361-373.
21. Cibois, M.; Gautier-Courteille, C.; Legagneux, V.; Paillard, L. Post-transcriptional controls-Adding a new layer of regulation to clock gene expression. Trends Cell Biol. 2010, 20, 533-541.
22. Kojima, S.; Shingle, D.L.; Green, C.B. Post-transcriptional control of circadian rhythms. J. Cell Sci. 2011, 124, 311-320.
23. Staiger, D.; Green, R. RNA-based regulation in the plant circadian clock. Trends Plant Sci. 2011, 16, 517-523.
24. Staiger, D.; Koster, T. Spotlight on post-transcriptional control in the circadian system. Cell. Mol. Life Sci. 2011, 68, 71-83.
25. Kojima, S.; Sher-Chen, E.L.; Green, C.B. Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev. 2012, 26, 2724-2736.
26. Wahl, M.C.; Will, C.L.; Luhrmann, R. The spliceosome: Design principles of a dynamic RNP machine. Cell 2009, 136, 701-718.
27. Majercak, J.; Chen, W.F.; Edery, I. Splicing of the period gene 3'-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol. Cell. Biol. 2004, 24, 3359-3372.
28. Low, K.H.; Chen, W.F.; Yildirim, E.; Edery, I. Natural Variation in the Drosophila melanogaster Clock Gene Period Modulates Splicing of Its 3'-Terminal Intron and Mid-Day Siesta. PLoS One 2012, 7, e49536.
29. Liu, Y.; Garceau, N.Y.; Loros, J.J.; Dunlap, J.C. Thermally regulated translational control of FRQ mediates aspects of temperature responses in the neurospora circadian clock. Cell 1997, 89, 477-486.
30. Liu, Y.; Merrow, M.; Loros, J.J.; Dunlap, J.C. How temperature changes reset a circadian oscillator. Science 1998, 281, 825-829.
31. Neiss, A.; Schafmeier, T.; Brunner; M. Transcriptional regulation and function of the Neurospora clock gene white collar 2 and its isoforms. EMBO Rep. 2008, 9, 788-794.
32. Diernfellner, A.; Colot, H.V.; Dintsis, O.; Loros, J.J.; Dunlap, J.C.; Brunner, M. Long and short isoforms of Neurospora clock protein FRQ support temperature-compensated circadian rhythms. FEBS Lett. 2007, 581, 5759-5764.
33. Collett, M.A.; Dunlap, J.C.; Loros, J.J. Circadian clock-specific roles for the light response protein WHITE COLLAR-2. Mol. Cell. Biol. 2001, 21, 2619-2628.
34. Diernfellner, A.C.; Schafmeier, T.; Merrow, M.W.; Brunner, M. Molecular mechanism of temperature sensing by the circadian clock of Neurospora crassa. Genes Dev. 2005, 19, 1968-1973.
35. Kaldi, K.; Gonzalez, B.H.; Brunner, M. Transcriptional regulation of the Neurospora circadian clock gene wc-1 affects the phase of circadian output. EMBO Rep. 2006, 7, 199-204.
36. Baker, C.L.; Loros, J.J.; Dunlap, J.C. The circadian clock of Neurospora crassa. FEMS Microbiol. Rev. 2012, 36, 95-110.
37. Colot, H.V.; Loros, J.J.; Dunlap, J.C. Temperature-modulated alternative splicing and promoter use in the Circadian clock gene frequency. Mol. Biol. Cell 2005, 16, 5563-5571.
38. Park, M.J.; Seo, P.J.; Park, C.M. CCA1 alternative splicing as a way of linking the circadian clock to temperature response in Arabidopsis. Plant Signal. Behav. 2012, 7, 1194-1196.
39. Wang, X.; Wu, F.; Xie, Q.; Wang, H.; Wang, Y.; Yue, Y.; Gahura, O.; Ma, S.; Liu, L.; Cao, Y.; et al. SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 2012, 24, 3278-3295.
40. Jones, M.A.; Williams, B.A.; McNicol, J.; Simpson, C.G.; Brown, J.W.; Harmer, S.L. Mutation of Arabidopsis SPLICEOSOMAL TIMEKEEPER LOCUS1 Causes Circadian Clock Defects. Plant Cell 2012, 24, 4066-4082.
41. Sanchez, S.E.; Petrillo, E.; Beckwith, E.J.; Zhang, X.; Rugnone, M.L.; Hernando, C.E.; Cuevas, J.C.; Godoy Herz, M.A.; Depetris-Chauvin, A.; Simpson, C.G.; et al. A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 2010, 468, 112-116.
42. Hong, S.; Song, H.R.; Lutz, K.; Kerstetter, R.A.; Michael, T.P.; McClung, C.R. Type II protein arginine methyltransferase 5 (PRMT5) is required for circadian period determination in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2010, 107, 21211-21216.
43. Shav-Tal, Y.; Zipori, D. PSF and p54nrb/NonO-Multi-functional nuclear proteins. FEBS Lett. 2002, 531, 109-114.
44. Guillaumond, F.; Boyer, B.; Becquet, D.; Guillen, S.; Kuhn, L.; Garin, J.; Belghazi, M.; Bosler, O.; Franc, J.L.; Francois-Bellan, A.M. Chromatin remodeling as a mechanism for circadian prolactin transcription: Rhythmic NONO and SFPQ recruitment to HLTF. FASEB J. 2011, 25, 2740-2756.
45. Peng, R.; Dye, B.T.; Perez, I.; Barnard, D.C.; Thompson, A.B.; Patton, J.G. PSF and p54nrb bind a conserved stem in U5 snRNA. RNA 2002, 8, 1334-1347.
46. Brown, S.A.; Ripperger, J.; Kadener, S.; Fleury-Olela, F.; Vilbois, F.; Rosbash, M.; Schibler, U. PERIOD1-associated proteins modulate the negative limb of the mammalian circadian oscillator. Science 2005, 308, 693-696.
47. Passon, D.M.; Lee, M.; Rackham, O.; Stanley, W.A.; Sadowska, A.; Filipovska, A.; Fox, A.H.; Bond, C.S. Structure of the heterodimer of human NONO and paraspeckle protein component 1 and analysis of its role in subnuclear body formation. Proc. Natl. Acad. Sci. USA 2012, 109, 4846-4850.
48. Kowalska, E.; Ripperger, J.A.; Hoegger, D.C.; Bruegger, P.; Buch, T.; Birchler, T.; Mueller, A.; Albrecht, U.; Contaldo, C.; Brown, S.A. NONO couples the circadian clock to the cell cycle. Proc. Natl. Acad. Sci. USA 2012, 110, 1592-1599.
49. Jacobson, A.; Peltz, S.W. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 1996, 65, 693-739.
50. Lin, C.L.; Evans, V.; Shen, S.; Xing, Y.; Richter, J.D. The nuclear experience of CPEB: Implications for RNA processing and translational control. RNA 2010, 16, 338-348.
51. Kowalska, E.; Ripperger, J.A.; Muheim, C.; Maier, B.; Kurihara, Y.; Fox, A.H.; Kramer, A.; Brown, S.A. Distinct Roles of DBHS Family Members in the Circadian Transcriptional Feedback Loop. Mol. Cell. Biol. 2012, 32, 4585-4594.
52. Green, C.B.; Besharse, J.C. Identification of a novel vertebrate circadian clock-regulated gene encoding the protein nocturnin. Proc. Natl. Acad. Sci. USA 1996, 93, 14884-14888.
53. Baggs, J.E.; Green, C.B. Nocturnin, a deadenylase in Xenopus laevis retina: A mechanism for posttranscriptional control of circadian-related mRNA. Curr. Biol. 2003, 13, 189-198.
54. Wang, Y.; Osterbur, D.L.; Megaw, P.L.; Tosini, G.; Fukuhara, C.; Green, C.B.; Besharse, J.C. Rhythmic expression of Nocturnin mRNA in multiple tissues of the mouse. BMC Dev. Biol. 2001, 1, doi:10.1186/1471-213X-1-9.
55. Oishi, K.; Miyazaki, K.; Kadota, K.; Kikuno, R.; Nagase, T.; Atsumi, G.; Ohkura, N.; Azama, T.; Mesaki, M.; Yukimasa, S.; et al. Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J. Biol. Chem. 2003, 278, 41519-41527.
56. Liu, X.; Green, C.B. A novel promoter element, photoreceptor conserved element II, directs photoreceptor-specific expression of nocturnin in Xenopus laevis. J. Biol. Chem. 2001, 276, 15146-15154.
57. Li, R.; Yue, J.; Zhang, Y.; Zhou, L.; Hao, W.; Yuan, J.; Qiang, B.; Ding, J.M.; Peng, X.; Cao, J.M. CLOCK/BMAL1 regulates human nocturnin transcription through binding to the E-box of nocturnin promoter. Mol. Cell. Biochem. 2008, 317, 169-177.
58. Hussain, M.M.; Pan, X. Clock regulation of dietary lipid absorption. Curr. Opin. Clin. Nutr. Metab. Care 2012, 15, 336-341.
59. Muller, W.E.; Wang, X.; Grebenjuk, V.A.; Korzhev, M.; Wiens, M.; Schlossmacher, U.; Schroder, H.C. Nocturnin in the demosponge Suberites domuncula: A potential circadian clock protein controlling glycogenin synthesis in sponges. Biochem. J. 2012, 448, 233-242.
60. Aktan, F. iNOS-mediated nitric oxide production and its regulation. Life Sci. 2004, 75, 639-653.
61. Niu, S.; Shingle, D.L.; Garbarino-Pico, E.; Kojima, S.; Gilbert, M.; Green, C.B. The circadian deadenylase Nocturnin is necessary for stabilization of the iNOS mRNA in mice. PLoS One 2011, 6, e26954.
62. Cheng, P.; He, Q.; He, Q.; Wang, L.; Liu, Y. Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev. 2005, 19, 234-241.
63. Guo, J.; Cheng, P.; Yuan, H.; Liu, Y. The Exosome regulates circadian gene expression in a posttranscriptional negative feedback loop. Cell 2009, 138, 1236-1246.
64. Guo, J.; Cheng, P.; Liu, Y. Functional significance of FRH in regulating the phosphorylation and stability of Neurospora circadian clock protein FRQ. J. Biol. Chem. 2010, 285, 11508-11515.
65. Hunt, S.M.; Thompson, S.; Elvin, M.; Heintzen, C. VIVID interacts with the WHITE COLLAR complex and FREQUENCY-interacting RNA helicase to alter light and clock responses in Neurospora. Proc. Natl. Acad. Sci. USA 2010, 107, 16709-16714.
66. Hunt, S.; Elvin, M.; Heintzen, C. Temperature-sensitive and circadian oscillators of Neurospora crassa share components. Genetics 2012, 191, 119-131.
67. Shi, M.; Collett, M.; Loros, J.J.; Dunlap, J.C. FRQ-interacting RNA helicase mediates negative and positive feedback in the Neurospora circadian clock. Genetics 2010, 184, 351-361.
68. Belden, W.J.; Lewis, Z.A.; Selker, E.U.; Loros, J.J.; Dunlap, J.C. CHD1 remodels chromatin and influences transient DNA methylation at the clock gene frequency. PLoS Genet. 2011, 7, e1002166.
69. Van Hoof, A.; Lennertz, P.; Parker, R. Yeast exosome mutants accumulate 3'-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol. Cell. Biol. 2000, 20, 441-452.
70. LaCava, J.; Houseley, J.; Saveanu, C.; Petfalski, E.; Thompson, E.; Jacquier, A.; Tollervey, D. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 2005, 121, 713-724.
71. Holub, P.; Lalakova, J.; Cerna, H.; Pasulka, J.; Sarazova, M.; Hrazdilova, K.; Arce, M.S.; Hobor, F.; Stefl, R.; Vanacova, S. Air2p is critical for the assembly and RNA-binding of the TRAMP complex and the KOW domain of Mtr4p is crucial for exosome activation. Nucleic Acids Res. 2012, 40, 5679-5693.
72. Fasken, M.B.; Leung, S.W.; Banerjee, A.; Kodani, M.O.; Chavez, R.; Bowman, E.A.; Purohit, M.K.; Rubinson, M.E.; Rubinson, E.H.; Corbett, A.H. Air1 zinc knuckles 4 and 5 and a conserved IWRXY motif are critical for the function and integrity of the Trf4/5-Air1/2-Mtr4 polyadenylation (TRAMP) RNA quality control complex. J. Biol. Chem. 2011, 286, 37429-37445.
73. Sadoff, B.U.; Heath-Pagliuso, S.; Castano, I.B.; Zhu, Y.; Kieff, F.S.; Christman, M.F. Isolation of mutants of Saccharomyces cerevisiae requiring DNA topoisomerase I. Genetics 1995, 141, 465-479.
74. Haracska, L.; Johnson, R.E.; Prakash, L.; Prakash, S. Trf4 and Trf5 proteins of Saccharomyces cerevisiae exhibit poly(A) RNA polymerase activity but no DNA polymerase activity. Mol. Cell. Biol. 2005, 25, 10183-10189.
75. Wagner, E.; Lykke-Andersen, J. mRNA surveillance: The perfect persist. J. Cell Sci. 2002, 115, 3033-3038.
76. Doma, M.K.; Parker, R. RNA quality control in eukaryotes. Cell 2007, 131, 660-668.
77. He, F.; Li, X.; Spatrick, P.; Casillo, R.; Dong, S.; Jacobson, A. Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5' to 3' mRNA decay pathways in yeast. Mol. Cell 2003, 12, 1439-1452.
78. Rehwinkel, J.; Letunic, I.; Raes, J.; Bork, P.; Izaurralde, E. Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA 2005, 11, 1530-1544.
79. Chang, Y.F.; Imam, J.S.; Wilkinson, M.F. The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 2007, 76, 51-74.
80. Metzstein, M.M.; Krasnow, M.A. Functions of the nonsense-mediated mRNA decay pathway in Drosophila development. PLoS Genet. 2006, 2, e180.
81. Rebbapragada, I.; Lykke-Andersen, J. Execution of nonsense-mediated mRNA decay: What defines a substrate? Curr. Opin. Cell. Biol. 2009, 21, 394-402.
82. Morgan, L.W.; Feldman, J.F. Isolation and characterization of a temperature-sensitive circadian clock mutant of Neurospora crassa. Genetics 1997, 146, 525-530.
83. Jeong, H.J.; Kim, Y.J.; Kim, S.H.; Kim, Y.H.; Lee, I.J.; Kim, Y.K.; Shin, J.S. Nonsense-mediated mRNA decay factors, UPF1 and UPF3, contribute to plant defense. Plant Cell Physiol. 2011, 52, 2147-2156.
84. Shi, C.; Baldwin, I.T.; Wu, J. Arabidopsis plants having defects in nonsense-mediated mRNA decay factors UPF1, UPF2, and UPF3 show photoperiod-dependent phenotypes in development and stress responses. J. Integr. Plant Biol. 2012, 54, 99-114.
85. Heintzen, C.; Nater, M.; Apel, K.; Staiger, D. AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 1997, 94, 8515-8120.
86. Schoning, J.C.; Streitner, C.; Page, D.R.; Hennig, S.; Uchida, K.; Wolf, E.; Furuya, M.; Staiger, D. Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation. Plant J. 2007, 52, 1119-1130.
87. Staiger, D.; Zecca, L.; Wieczorek Kirk, D.A.; Apel, K.; Eckstein, L. The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J. 2003, 33, 361-371.
88. Kim, J.S.; Jung, H.J.; Lee, H.J.; Kim, K.A.; Goh, C.H.; Woo, Y.; Oh, S.H.; Han, Y.S.; Kang, H. Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J. 2008, 55, 455-466.
89. Streitner, C.; Hennig, L.; Korneli, C.; Staiger, D. Global transcript profiling of transgenic plants constitutively overexpressing the RNA-binding protein AtGRP7. BMC Plant Biol. 2010, 10, doi:10.1186/1471-2229-10-221.
90. Kelly, S.M.; Corbett, A.H. Messenger RNA export from the nucleus: A series of molecular wardrobe changes. Traffic 2009, 10, 1199-1208.
91. Morf, J.; Rey, G.; Schneider, K.; Stratmann, M.; Fujita, J.; Naef, F.; Schibler, U. Cold-inducible RNA-binding protein modulates circadian gene expression posttranscriptionally. Science 2012, 338, 379-383.
92. Xia, Z.P.; Zheng, X.M.; Zheng, H.; Liu, X.J.; Liu, G.Y.; Wang, X.H. Downregulation of cold-inducible RNA-binding protein activates mitogen-activated protein kinases and impairs spermatogenic function in mouse testes. Asian J. Androl. 2012, 14, 884-889.
93. Inoue, S.; Shimoda, M.; Nishinokubi, I.; Siomi, M.C.; Okamura, M.; Nakamura, A.; Kobayashi, S.; Ishida, N.; Siomi, H. A role for the Drosophila fragile X-related gene in circadian output. Curr. Biol. 2002, 12, 1331-1335.
94. Dockendorff, T.C.; Su, H.S.; McBride, S.M.; Yang, Z.; Choi, C.H.; Siwicki, K.K.; Sehgal, A.; Jongens, T.A. Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron 2002, 34, 973-984.
95. Zhang, J.; Fang, Z.; Jud, C.; Vansteensel, M.J.; Kaasik, K.; Lee, C.C.; Albrecht, U.; Tamanini, F.; Meijer, J.H.; Oostra, B.A.; et al. Fragile X-related proteins regulate mammalian circadian behavioral rhythms. Am. J. Hum. Genet. 2008, 83, 43-52.
96. Liang, S.; Hitomi, M.; Hu, Y.H.; Liu, Y.; Tartakoff, A.M. A DEAD-box-family protein is required for nucleocytoplasmic transport of yeast mRNA. Mol. Cell. Biol. 1996, 16, 5139-5146.
97. Reddy, A.B.; Karp, N.A.; Maywood, E.S.; Sage, E.A.; Deery, M.; O'Neill, J.S.; Wong, G.K.; Chesham, J.; Odell, M.; Lilley, K.S.; et al. Circadian orchestration of the hepatic proteome. Curr. Biol. 2006, 16, 1107-1115.
98. Jouffe, C.; Cretenet, G.; Symul, L.; Martin, E.; Atger, F.; Naef, F.; Gachon, F. The circadian clock coordinates ribosome biogenesis. PLoS Biol. 2013, 11, e1001455.
99. Newby, L.M.; Jackson, F.R. Regulation of a specific circadian clock output pathway by lark, a putative RNA-binding protein with repressor activity. J. Neurobiol. 1996, 31, 117-128.
100. Sofola, O.; Sundram, V.; Ng, F.; Kleyner, Y.; Morales, J.; Botas, J.; Jackson, F.R.; Nelson, D.L. The Drosophila FMRP and LARK RNA-binding proteins function together to regulate eye development and circadian behavior. J. Neurosci. 2008, 28, 10200-10205.
101. Kojima, S.; Matsumoto, K.; Hirose, M.; Shimada, M.; Nagano, M.; Shigeyoshi, Y.; Hoshino, S.; Ui-Tei, K.; Saigo, K.; Green, C.B.; et al. LARK activates posttranscriptional expression of an essential mammalian clock protein, PERIOD1. Proc. Natl. Acad. Sci. USA 2007, 104, 1859-1864.
102. Kim, D.Y.; Woo, K.C.; Lee, K.H.; Kim, T.D.; Kim, K.T. hnRNP Q and PTB modulate the circadian oscillation of mouse Rev-erb alpha via IRES-mediated translation. Nucleic Acids Res. 2010, 38, 7068-7078.
103. Kim, T.D.; Woo, K.C.; Cho, S.; Ha, D.C.; Jang, S.K.; Kim, K.T. Rhythmic control of AANAT translation by hnRNP Q in circadian melatonin production. Genes Dev. 2007, 21, 797-810.
104. Lee, K.H.; Woo, K.C.; Kim, D.Y.; Kim, T.D.; Shin, J.; Park, S.M.; Jang, S.K.; Kim, K.T. Rhythmic Interaction between Period1 mRNA and hnRNP Q Leads to Circadian Time-Dependent Translation. Mol. Cell. Biol. 2012, 32, 717-728.
105. Morse, D.; Milos, P.M.; Roux, E.; Hastings, J.W. Circadian regulation of bioluminescence in Gonyaulax involves translational control. Proc. Natl. Acad. Sci. USA 1989, 86, 172-176.
106. Mittag, M.; Lee, D.H.; Hastings, J.W. Circadian expression of the luciferin-binding protein correlates with the binding of a protein to the 3' untranslated region of its mRNA. Proc. Natl. Acad. Sci. USA 1994, 91, 5257-5261.
107. Mittag, M.; Waltenberger, H. In vitro mutagenesis of binding site elements for the clock-controlled proteins CCTR and Chlamy 1. Biol. Chem. 1997, 378, 1167-1170.
108. Kimchi-Sarfaty, C.; Oh, J.M.; Kim, I.W.; Sauna, Z.E.; Calcagno, A.M.; Ambudkar, S.V.; Gottesman, M.M. A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science 2007, 315, 525-528.
109. Zhou, M.; Guo, J.; Cha, J.; Chase, M.; Chen, S.; Barral, J.M.; Sachs, M.S.; Liu, Y. Non-optimal codon usage determines the expression, structure and function of a circadian clock protein. Nature 2013, 495, 111-115.
110. Xu, Y.; Ma, P.; Shah, P.; Rokas, A.; Liu, Y.; Johnson, C.H. Non-optimal codon usage is a mechanism to achieve circadian clock conditionality. Nature 2013, 495, 116-120.
111. Carpen, J.D.; von Schantz, M.; Smits, M.; Skene, D.J.; Archer, S.N. A silent polymorphism in the PER1 gene associates with extreme diurnal preference in humans. J. Hum. Genet. 2006, 51, 1122-1125.
112. Parker, R.; Song, H. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 2004, 11, 121-127.
113. Dziembowski, A.; Lorentzen, E.; Conti, E.; Seraphin, B. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat. Struct. Mol. Biol. 2007, 14, 15-22.
114. Hartung, S.; Hopfner, K.P. Lessons from structural and biochemical studies on the archaeal exosome. Biochem. Soc. Trans. 2009, 37, 83-87.
115. Chen, C.Y.; Shyu, A.B. AU-rich elements: Characterization and importance in mRNA degradation. Trends Biochem. Sci. 1995, 20, 465-470.
116. Benjamin, D.; Schmidlin, M.; Min, L.; Gross, B.; Moroni, C. BRF1 protein turnover and mRNA decay activity are regulated by protein kinase B at the same phosphorylation sites. Mol. Cell. Biol. 2006, 26, 9497-9507.
117. Kim, T.D.; Kim, J.S.; Kim, J.H.; Myung, J.; Chae, H.D.; Woo, K.C.; Jang, S.K.; Koh, D.S.; Kim, K.T. Rhythmic Serotonin N-Acetyltransferase mRNA degradation is essential for the maintenance of its circadian oscillation. Mol. Cell. Biol. 2005, 25, 3232-3246.
118. Kim, D.Y.; Kwak, E.; Kim, S.H.; Lee, K.H.; Woo, K.C.; Kim, K.T. hnRNP Q mediates a phase-dependent translation-coupled mRNA decay of mouse Period3. Nucleic Acids Res. 2011, 39, 8901-8914.
119. Bartel, D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004, 116, 281-297.
120. Hammond, S.M. Dicing and slicing: The core machinery of the RNA interference pathway. FEBS Lett. 2005, 579, 5822-5829.
121. Jaskiewicz, L.; Filipowicz, W. Role of Dicer in posttranscriptional RNA silencing. Curr. Top. Microbiol. Immunol. 2008, 320, 77-97.
122. Cheng, H.Y.; Papp, J.W.; Varlamova, O.; Dziema, H.; Russell, B.; Curfman, J.P.; Nakazawa, T.; Shimizu, K.; Okamura, H; Impey, S.; et al. microRNA modulation of circadian-clock period and entrainment. Neuron 2007, 54, 813-829.
123. Gatfield, D.; le Martelot, G.; Vejnar, C.E.; Gerlach, D.; Schaad, O.; Fleury-Olela, F.; Ruskeepaa, A.L.; Oresic, M.; Esau, C.C.; Zdobnov, E.M.; et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev. 2009, 23, 1313-1326.
124. Kadener, S.; Menet, J.S.; Sugino, K.; Horwich, M.D.; Weissbein, U.; Nawathean, P.; Vagin, V.V.; Zamore, P.D.; Nelson, S.B.; Rosbash, M. A role for microRNAs in the Drosophila circadian clock. Genes Dev. 2009, 23, 2179-2191.
125. Pegoraro, M.; Tauber, E. The role of microRNAs (miRNA) in circadian rhythmicity. J. Genet. 2008, 87, 505-511.
126. Saus, E.; Soria, V.; Escaramis, G.; Vivarelli, F.; Crespo, J.M.; Kagerbauer, B.; Menchon, J.M.; Urretavizcaya, M.; Gratacos, M.; Estivill, X. Genetic variants and abnormal processing of pre-miR-182, a circadian clock modulator, in major depression patients with late insomnia. Hum. Mol. Genet. 2010, 19, 4017-4025.
127. Xu, S.; Witmer, P.D.; Lumayag, S.; Kovacs, B.; Valle, D. MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J. Biol. Chem. 2007, 282, 25053-25066.
128. Zhou, W.; Li, Y.; Wang, X.; Wu, L.; Wang, Y. MiR-206-mediated dynamic mechanism of the mammalian circadian clock. BMC Syst. Biol. 2011, 5, 141.