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Spotlight on post-transcriptional control in the circadian system

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Abstract

An endogenous timing mechanism, the circadian clock, causes rhythmic expression of a considerable fraction of the genome of most organisms to optimally align physiology and behavior with their environment. Circadian clocks are self-sustained oscillators primarily based on transcriptional feedback loops and post-translational modification of clock proteins. It is increasingly becoming clear that regulation at the RNA level strongly impacts the cellular circadian transcriptome and proteome as well as the oscillator mechanism itself. This review focuses on posttranscriptional events, discussing RNA-binding proteins that, by influencing the timing of pre-mRNA splicing, polyadenylation and RNA decay, shape rhythmic expression profiles. Furthermore, recent findings on the contribution of microRNAs to orchestrating circadian rhythms are summarized.

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Abbreviations

AANAT:

Serotonin N-acetyltransferase

AGO1:

ARGONAUTE1

ARE:

AU-rich element

AS:

Alternative splicing

bHLH:

Basic helix-loop-helix

CCA1:

CIRCADIAN CLOCK ASSOCIATED1

CIRP:

Cold-inducible RNA-binding protein

CLK:

CLOCK

CRY:

CRYPTHOCHROME

CYC:

CYCLE

FLC:

FLOWERING LOCUS C

FMRP:

Fragile X mental retardation protein

FRH:

FRQ-interacting helicase

FRQ:

FREQUENCY

GI:

GIGANTEA

hnRNP:

Heterogenous nuclear ribonucleoprotein

IRES:

Internal ribosome entry sites

KH:

K homology

LHY:

LATE ELONGATED HYPOCOTYL

NAT:

Natural antisense transcripts

NMD:

Nonsense-mediated decay

PABP:

Poly(A) binding protein

PDP:

PAR DOMAIN PROTEIN

PER:

PERIOD

PRR:

PSEUDO RESPONSE REGULATOR

PTB:

Polypyrimidine tract-binding protein

PTC:

Premature termination codon

RBM:

RNA binding motif protein

RBP:

RNA-binding protein

RRM:

RNA recognition motif

SCN:

Suprachiasmatic nuclei

TF:

Transcription factor

TIM:

TIMELESS

TOC1:

TIMING OF CAB EXPRESSION 1

UTR:

Untranslated region

VRI:

VRILLE

WC:

WHITE COLLAR

WCC:

WHITE COLLAR Complex

References

  1. Gachon F, Nagoshi E, Brown SA, Ripperger J, Schibler U (2004) The mammalian circadian timing system: from gene expression to physiology. Chromosoma 113:103–112

    PubMed  Google Scholar 

  2. Mas P (2008) Circadian clock function in Arabidopsis thaliana: time beyond transcription. Trends Cell Biol 18:273–281

    CAS  PubMed  Google Scholar 

  3. Schöning JC, Staiger D (2005) At the pulse of time: protein interactions determine the pace of circadian clocks. FEBS Lett 579:3246–3252

    PubMed  Google Scholar 

  4. Gallego M, Virshup DM (2007) Post-translational modifications regulate the ticking of the circadian clock. Nat Rev Mol Cell Biol 8:139–148

    CAS  PubMed  Google Scholar 

  5. Mehra A, Baker CL, Loros JJ, Dunlap JC (2009) Post-translational modifications in circadian rhythms. Trends Biochem Sci 34:483–490

    CAS  PubMed  Google Scholar 

  6. Edery I (1999) Role of post-transcriptional regulation in circadian clocks: lessons from Drosophila. Chronobiol Int 16:377–414

    CAS  PubMed  Google Scholar 

  7. Harms E, Kivimae S, Young MW, Saez L (2004) Post-transcriptional and post-translational regulation of clock genes. J Biol Rhythms 19:361–373

    CAS  PubMed  Google Scholar 

  8. Staiger D, Streitner C, Rudolf F, Huang X (2006) Multiple and slave oscillators, In: Hall A, McWatters H (eds) Endogenous plant rhythms. Blackwell, Oxford, pp 57–83

  9. Glisovic T, Bachorik JL, Yong J, Dreyfuss G (2008) RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett 582:1977–1986

    CAS  PubMed  Google Scholar 

  10. Moore MJ (2005) From birth to death: the complex lives of eukaryotic mRNAs. Science 309:1514–1548

    CAS  PubMed  Google Scholar 

  11. Keene JD, Tenenbaum SA (2002) Eukaryotic mRNPs may represent post-transcriptional operons. Mol Cell 9:1161–1167

    CAS  PubMed  Google Scholar 

  12. Tenenbaum SA, Carson CC, Lager PJ, Keene JD (2000) Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc Natl Acad Sci USA 97:14085–14090

    CAS  PubMed  Google Scholar 

  13. Keene JD (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8:533–543

    CAS  PubMed  Google Scholar 

  14. Keene JD (2007) Biological clocks and the coordination theory of RNA operons and regulons. Cold Spring Harb Symp Quant Biol 72:157–165

    CAS  PubMed  Google Scholar 

  15. Staiger D (2001) RNA-binding proteins and circadian rhythms in Arabidopsis thaliana. Philos Trans R Soc Lond B 356:1755–1759

    CAS  Google Scholar 

  16. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78–83

    CAS  PubMed  Google Scholar 

  17. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi H, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by circadian clock. Cell 109:307–320

    CAS  PubMed  Google Scholar 

  18. Pilgrim ML, Caspar T, Quail PH, McClung CR (1993) Circadian and light-regulated expression of nitrate reductase in Arabidopsis. Plant Mol Biol 23:349–364

    CAS  PubMed  Google Scholar 

  19. Dibner C, Sage D, Unser M, Bauer C, d’Esmond T, Naef F, Schibler U (2009) Circadian gene expression is resilient to large fluctuations in overall transcription rates. EMBO J 28:123–134

    Google Scholar 

  20. Reddy AB, Karp NA, Maywood ES, Sage EA, Deery M, O’Neill JS, Wong GK, Chesham J, Odell M, Lilley KS, Kyriacou CP, Hastings MH (2006) Circadian orchestration of the hepatic proteome. Curr Biol 16:1107–1115

    CAS  PubMed  Google Scholar 

  21. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271–290

    CAS  PubMed  Google Scholar 

  22. Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, Zoran MJ (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet 6:544–556

    CAS  PubMed  Google Scholar 

  23. Allada R, Chung BY (2010) Circadian organization of behavior and physiology in Drosophila. Annu Rev Physiol 72:605–624

    CAS  PubMed  Google Scholar 

  24. Hardin PE (2005) The circadian timekeeping system of Drosophila. Curr Biol 15:R714–R722

    CAS  PubMed  Google Scholar 

  25. Cyran SA, Buchsbaum AM, Reddy KL, Lin MC, Glossop NR, Hardin PE, Young MW, Storti RV, Blau J (2003) vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112:329–341

    CAS  PubMed  Google Scholar 

  26. Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72:517–549

    CAS  PubMed  Google Scholar 

  27. Ukai H, Ueda HR (2010) Systems biology of mammalian circadian clocks. Annu Rev Physiol 72:579–603

    CAS  PubMed  Google Scholar 

  28. Sato TK, Yamada RG, Ukai H, Baggs JE, Miraglia LJ, Kobayashi TJ, Welsh DK, Kay SA, Ueda HR, Hogenesch JB (2006) Feedback repression is required for mammalian circadian clock function. Nat Genet 38:312–319

    CAS  PubMed  Google Scholar 

  29. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, Schibler U (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110:251–260

    CAS  PubMed  Google Scholar 

  30. Ueda HR, Chen W, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, Nagano M, Nakahama K-I, Suzuki Y, Sugano S, Masamitsu I, Shigeyoshi Y, Hashimoto S (2002) A transcription factor response element for gene expression during circadian night. Nature 418:534–539

    CAS  PubMed  Google Scholar 

  31. Brunner M, Kaldi K (2008) Interlocked feedback loops of the circadian clock of Neurospora crassa. Mol Microbiol 68:255–262

    CAS  PubMed  Google Scholar 

  32. Locke JCW, Kozma-Bognar L, Gould PD, Feher B, Kevei E, Nagy F, Turner MS, Hall A, Millar AJ (2006) Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol Syst Biol 2:59

    PubMed  Google Scholar 

  33. Iliev D, Voytsekh O, Schmidt EM, Fiedler M, Nykytenko A, Mittag M (2006) A heteromeric RNA-binding protein is involved in maintaining acrophase and period of the circadian clock. Plant Physiol 142:797–806

    CAS  PubMed  Google Scholar 

  34. Schulze T, Prager K, Dathe H, Kelm J, Kiessling P, Mittag M (2010) How the green alga Chlamydomonas reinhardtii keeps time. Protoplasma. doi:10.1007/s00709-010-0113-0

  35. Wuarin J, Falvey E, Lavery D, Talbot D, Schmidt E, Ossipow V, Fonjallaz P (1992) The role of the transcriptional activator protein DBP in circadian liver gene expression. J Cell Sci 16:123–127

    CAS  Google Scholar 

  36. Jacobshagen S, Kessler B, Rinehart CA (2008) At least four distinct circadian regulatory mechanisms are required for all phases of rhythms in mRNA amount. J Biol Rhythms 23:511–524

    CAS  PubMed  Google Scholar 

  37. So WV, Rosbash M (1997) Post-transcriptional regulation contributes to Drosophila clock gene mRNA cycling. EMBO J 16:7146–7155

    CAS  PubMed  Google Scholar 

  38. Frisch B, Hardin PE, Hamblen-Coyle MJ, Rosbash M, Hall JC (1994) A promoterless period gene mediates behavioral rhythmicity and cyclical per expression in a restricted subset of the Drosophila nervous system. Neuron 12:555–570

    CAS  PubMed  Google Scholar 

  39. Stanewsky R, Jamison CF, Plautz JD, Kay SA, Hall JC (1997) Multiple circadian-regulated elements contribute to cycling period gene expression in Drosophila. EMBO J 16:5006–5018

    CAS  PubMed  Google Scholar 

  40. Mitchell P, Tollervey D (2000) mRNA stability in eukaryotes. Curr Opin Genet Dev 10:193–198

    CAS  PubMed  Google Scholar 

  41. Woo KC, Kim TD, Lee KH, Kim DY, Kim W, Lee KY, Kim KT (2009) Mouse period 2 mRNA circadian oscillation is modulated by PTB-mediated rhythmic mRNA degradation. Nucleic Acids Res 37:26–37

    CAS  PubMed  Google Scholar 

  42. Kwak E, Kim TD, Kim KT (2006) Essential role of 3′-untranslated region-mediated mRNA decay in circadian oscillations of mouse Period3 mRNA. J Biol Chem 281:19100–19106

    CAS  PubMed  Google Scholar 

  43. Woo KC, Ha DC, Lee KH, Kim DY, Kim TD, Kim KT (2010) Circadian amplitude of cryptochrome 1 is modulated by mRNA stability regulation via cytoplasmic hnRNP D oscillation. Mol Cell Biol 30:197–205

    CAS  PubMed  Google Scholar 

  44. Kim TD, Kim JS, Kim JH, Myung J, Chae HD, Woo KC, Jang SK, Koh DS, Kim KT (2005) Rhythmic serotonin N-acetyltransferase mRNA degradation is essential for the maintenance of its circadian oscillation. Mol Cell Biol 25:3232–3246

    CAS  PubMed  Google Scholar 

  45. Kim TD, Woo K-C, Cho S, Ha D-C, Jang SK, Kim K-T (2007) Rhythmic control of AANAT translation by hnRNP Q in circadian melatonin production. Genes Dev 21:797–810

    CAS  PubMed  Google Scholar 

  46. Benjamin D, Schmidlin M, Min L, Gross B, Moroni C (2006) BRF1 protein turnover and mRNA decay activity are regulated by protein kinase B at the same phosphorylation sites. Mol Cell Biol 26:9497–9507

    CAS  PubMed  Google Scholar 

  47. Cheng P, He Q, Wang L, Liu Y (2005) Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev 19:234–241

    CAS  PubMed  Google Scholar 

  48. Guo J, Cheng P, Yuan H, Liu Y (2009) The exosome regulates circadian gene expression in a post-transcriptional negative feedback loop. Cell 138:1236–1246

    CAS  PubMed  Google Scholar 

  49. Gutierrez RA, Ewing RM, Cherry JM, Green PJ (2002) Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch- and specific clock-controlled genes. Proc Natl Acad Sci USA 99:11513–11518

    CAS  PubMed  Google Scholar 

  50. Lidder P, Gutierrez RA, Salome PA, McClung CR, Green PJ (2005) Circadian control of messenger RNA stability. Association with a sequence-specific messenger RNA decay pathway. Plant Physiol 138:2374–2385

    CAS  PubMed  Google Scholar 

  51. Yakir E, Hilman D, Hassidim M, Green RM (2007) CCA1 transcript stability and the entrainment of the circadian clock in Arabidopsis. Plant Physiol 145:925–932

    CAS  PubMed  Google Scholar 

  52. Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11:113–127

    CAS  PubMed  Google Scholar 

  53. Robinson BG, Frim DM, Schwartz WJ, Majzoub JA (1988) Vasopressin mRNA in the suprachiasmatic nuclei: daily regulation of polyadenylate tail length. Science 241:342–344

    CAS  PubMed  Google Scholar 

  54. Wang Y, Osterbur DL, Megaw PL, Tosini G, Fukuhara C, Green CB, Besharse JC (2001) Rhythmic expression of Nocturnin mRNA in multiple tissues of the mouse. BMC Dev Biol 1:9

    CAS  PubMed  Google Scholar 

  55. Green CB, Douris N, Kojima S, Strayer CA, Fogerty J, Lourim D, Keller SR, Besharse JC (2007) Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity. Proc Natl Acad Sci USA 104:9888–9893

    CAS  PubMed  Google Scholar 

  56. Cheng Y, Gvakharia B, Hardin PE (1998) Two alternatively spliced transcripts from the Drosophila period gene rescue rhythms having different molecular and behavioral characteristics. Mol Cell Biol 18:6505–6514

    CAS  PubMed  Google Scholar 

  57. Collins BH, Rosato E, Kyriacou CP (2004) Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc Natl Acad Sci USA 101:1945–1950

    CAS  PubMed  Google Scholar 

  58. Majercak J, Sidote D, Hardin PE, Edery I (1999) How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24:219–230

    CAS  PubMed  Google Scholar 

  59. Majercak J, Chen WF, Edery I (2004) Splicing of the period gene 3′-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol Cell Biol 24:3359–3372

    CAS  PubMed  Google Scholar 

  60. Low KH, Lim C, Ko HW, Edery I (2008) Natural variation in the splice site strength of a clock gene and species-specific thermal adaptation. Neuron 60:1054–1067

    CAS  PubMed  Google Scholar 

  61. Liu Y, Garceau NY, Loros JJ, Dunlap JC (1997) Thermally regulated translational control of FRQ mediates aspects of temperature responses in the Neurospora circadian clock. Cell 89:477–486

    CAS  PubMed  Google Scholar 

  62. Colot HV, Loros JJ, Dunlap JC (2005) Temperature-modulated alternative splicing and promoter use in the circadian clock gene frequency. Mol Biol Cell 16:5563–5571

    CAS  PubMed  Google Scholar 

  63. Heintzen C, Melzer S, Fischer R, Kappeler S, Apel K, Staiger D (1994) A light- and temperature-entrained circadian clock controls expression of transcripts encoding nuclear proteins with homology to RNA-binding proteins in meristematic tissue. Plant J 5:799–813

    CAS  PubMed  Google Scholar 

  64. Carpenter CD, Kreps JA, Simon AE (1994) Genes encoding glycine-rich Arabidopsis thaliana proteins with RNA-binding motifs are influenced by cold treatment and an endogenous circadian rhythm. Plant Physiol 104:1015–1025

    CAS  PubMed  Google Scholar 

  65. Staiger D, Apel K (1999) Circadian clock-regulated expression of an RNA-binding protein in Arabidopsis: characterisation of a minimal promoter element. Mol Gen Genet 261:811–819

    CAS  PubMed  Google Scholar 

  66. Heintzen C, Nater M, Apel K, Staiger D (1997) AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:8515–8520

    CAS  PubMed  Google Scholar 

  67. Staiger D, Zecca L, Wieczorek Kirk DA, Apel K, Eckstein L (2003) The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J 33:361–371

    CAS  PubMed  Google Scholar 

  68. Schöning JC, Streitner C, Page DR, Hennig S, Uchida K, Wolf E, Furuya M, Staiger D (2007) Autoregulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation. Plant J 52:1119–1130

    PubMed  Google Scholar 

  69. Schüttpelz M, Schöning JC, Doose S, Neuweiler H, Peters E, Staiger D, Sauer M (2008) Changes of conformational dynamics of mRNA upon AtGRP7 binding studied by fluorescence correlation spectroscopy. J Am Chem Soc 130:9507–9513

    PubMed  Google Scholar 

  70. Schöning JC, Streitner C, Meyer IM, Gao Y, Staiger D (2008) Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis. Nucleic Acids Res 36:6977–6987

    PubMed  Google Scholar 

  71. McGlincy NJ, Smith CW (2008) Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense? Trends Biochem Sci 33:385–393

    CAS  PubMed  Google Scholar 

  72. Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447:284–288

    CAS  PubMed  Google Scholar 

  73. Kim JS, Jung HJ, Lee HJ, Kim KA, Goh C-H, Woo Y, Oh SH, Han YS, Kang H (2008) Glycine-rich RNA-binding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J 55:455–466

    CAS  PubMed  Google Scholar 

  74. Schmidt F, Marnef A, Cheung M-K, Wilson I, Hancock J, Staiger D, Ladomery M (2010) A proteomic analysis of oligo(dT)-bound mRNP containing oxidative stress-induced Arabidopsis thaliana RNA-binding proteins ATGRP7 and ATGRP8. Mol Biol Rep 37:839–845

    CAS  PubMed  Google Scholar 

  75. Fujita J (1999) Cold shock response in mammalian cells. J Mol Microbiol Biotechnol 1:243–255

    CAS  PubMed  Google Scholar 

  76. Nishiyama H, Xue JH, Sato T, Fukuyama H, Mizuno N, Houtani T, Sugimoto T, Fujita J (1998) Diurnal change of the cold-inducible RNA-binding protein (Cirp) expression in mouse brain. Biochem Biophys Res Commun 245:534–538

    CAS  PubMed  Google Scholar 

  77. Kornmann B, Schaad O, Bujard H, Takahashi JS, Schibler U (2007) System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol 5:e34

    PubMed  Google Scholar 

  78. Hazen SP, Naef F, Quisel T, Gendron JM, Chen H, Ecker JR, Borevitz JO, Kay SA (2009) Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays. Genome Biol 10:R17

    PubMed  Google Scholar 

  79. Ner-Gaon H, Halachmi R, Savaldi-Goldstein S, Rubin E, Ophir R, Fluhr R (2004) Intron retention is a major phenomenon in alternative splicing in Arabidopsis. Plant J 39:877–885

    CAS  PubMed  Google Scholar 

  80. Newby LM, Jackson FR (1996) Regulation of a specific circadian clock output pathway by lark, a putative RNA-binding protein with repressor activity. J Neurobiol 31:117–128

    CAS  PubMed  Google Scholar 

  81. Huang Y, Genova G, Roberts M, Jackson FR (2007) The LARK RNA-binding protein selectively regulates the circadian eclosion rhythm by controlling E74 protein expression. PLoS ONE 2:e1107

    PubMed  Google Scholar 

  82. Sofola O, Sundram V, Ng F, Kleyner Y, Morales J, Botas J, Jackson FR, Nelson DL (2008) The Drosophila FMRP and LARK RNA-binding proteins function together to regulate eye development and circadian behavior. J Neurosci 28:10200–10205

    CAS  PubMed  Google Scholar 

  83. Zhang J, Fang Z, Jud C, Vansteensel MJ, Kaasik K, Lee CC, Albrecht U, Tamanini F, Meijer JH, Oostra BA, Nelson DL (2008) Fragile X-related proteins regulate mammalian circadian behavioral rhythms. Am J Hum Genet 83:43–52

    CAS  PubMed  Google Scholar 

  84. Kojima S, Matsumoto K, Hirose M, Shimada M, Nagano M, Shigeyoshi Y, Hoshino S, Ui-Tei K, Saigo K, Green CB, Sakaki Y, Tei H (2007) LARK activates post-transcriptional expression of an essential mammalian clock protein, PERIOD1. Proc Natl Acad Sci USA 104:1859–1864

    CAS  PubMed  Google Scholar 

  85. Höck J, Weinmann L, Ender C, Rudel S, Kremmer E, Raabe M, Urlaub H, Meister G (2007) Proteomic and functional analysis of argonaute-containing mRNA-protein complexes in human cells. EMBO Rep 8:1052–1060

    PubMed  Google Scholar 

  86. Zhao B, Schneid C, Iliev D, Schmidt EM, Wagner V, Wollnik F, Mittag M (2004) The circadian RNA-binding protein CHLAMY 1 represents a novel type heteromer of RNA recognition motif and lysine homology domain-containing subunits. Eukaryot Cell 3:815–825

    CAS  PubMed  Google Scholar 

  87. Waltenberger H, Schneid C, Grosch JO, Bareiss A, Mittag M (2001) Identification of target mRNAs for the clock-controlled RNA-binding protein Chlamy 1 from Chlamydomonas reinhardtii. Mol Genet Genomics 265:180–188

    CAS  PubMed  Google Scholar 

  88. Kiaulehn S, Voytsekh O, Fuhrmann M, Mittag M (2007) The presence of UG-repeat sequences in the 3′-UTRs of reporter luciferase mRNAs mediates circadian expression and can determine acrophase in Chlamydomonas reinhardtii. J Biol Rhythms 22:275–277

    CAS  PubMed  Google Scholar 

  89. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP (2008) The impact of microRNAs on protein output. Nature 455:64–71

    CAS  PubMed  Google Scholar 

  90. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9:102–114

    CAS  PubMed  Google Scholar 

  91. Zdanowicz A, Thermann R, Kowalska J, Jemielity J, Duncan K, Preiss T, Darzynkiewicz E, Hentze MW (2009) Drosophila miR2 primarily targets the m7GpppN cap structure for translational repression. Mol Cell 35:881–888

    CAS  PubMed  Google Scholar 

  92. Brodersen P, Voinnet O (2009) Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 10:141–148

    CAS  PubMed  Google Scholar 

  93. Yang M, Lee JE, Padgett RW, Edery I (2008) Circadian regulation of a limited set of conserved microRNAs in Drosophila. BMC Genomics 9:83

    PubMed  Google Scholar 

  94. Kadener S, Menet JS, Sugino K, Horwich MD, Weissbein U, Nawathean P, Vagin VV, Zamore PD, Nelson SB, Rosbash M (2009) A role for microRNAs in the Drosophila circadian clock. Genes Dev 23:2179–2191

    CAS  PubMed  Google Scholar 

  95. Hipfner DR, Weigmann K, Cohen SM (2002) The bantam gene regulates Drosophila growth. Genetics 161:1527–1537

    CAS  PubMed  Google Scholar 

  96. Cheng HY, Papp JW, Varlamova O, Dziema H, Russell B, Curfman JP, Nakazawa T, Shimizu K, Okamura H, Impey S, Obrietan K (2007) microRNA modulation of circadian-clock period and entrainment. Neuron 54:813–829

    CAS  PubMed  Google Scholar 

  97. Xu S, Witmer PD, Lumayag S, Kovacs B, Valle D (2007) MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J Biol Chem 282:25053–25066

    CAS  PubMed  Google Scholar 

  98. Gatfield D, Le Martelot G, Vejnar CE, Gerlach D, Schaad O, Fleury-Olela F, Ruskeepaa AL, Oresic M, Esau CC, Zdobnov EM, Schibler U (2009) Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev 23:1313–1326

    CAS  PubMed  Google Scholar 

  99. Sire C, Moreno AB, Garcia-Chapa M, Lopez-Moya JJ, Segundo BS (2009) Diurnal oscillation in the accumulation of Arabidopsis microRNAs, miR167, miR168, miR171 and miR398. FEBS Lett 583:1039–1044

    CAS  PubMed  Google Scholar 

  100. Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM (2007) The GIGANTEA-regulated microRNA172 mediates photoperiodic Flowering independent of CONSTANS in Arabidopsis. Plant Cell 19:2736–2748

    CAS  PubMed  Google Scholar 

  101. Kramer C, Loros JJ, Dunlap JC, Crosthwaite SK (2003) Role for antisense RNA in regulating circadian clock function in Neurospora crassa. Nature 421:948–952

    CAS  PubMed  Google Scholar 

  102. Edwards KD, Anderson PE, Hall A, Salathia NS, Locke JC, Lynn JR, Straume M, Smith JQ, Millar AJ (2006) FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18:639–650

    CAS  PubMed  Google Scholar 

  103. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C (2010) Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327:94–97

    CAS  PubMed  Google Scholar 

  104. Zhang EE, Liu AC, Hirota T, Miraglia LJ, Welch G, Pongsawakul PY, Liu X, Atwood A, Huss JW 3rd, Janes J, Su AI, Hogenesch JB, Kay SA (2009) A genome-wide RNAi screen for modifiers of the circadian clock in human cells. Cell 139:199–210

    CAS  PubMed  Google Scholar 

  105. Brown JW, Birmingham A, Griffiths PE, Jossinet F, Kachouri-Lafond R, Knight R, Lang BF, Leontis N, Steger G, Stombaugh J, Westhof E (2009) The RNA structure alignment ontology. RNA 15:1623–1631

    CAS  PubMed  Google Scholar 

  106. Zong Q, Schummer M, Hood L, Morris DR (1999) Messenger RNA translation state: the second dimension of high-throughput expression screening. Proc Natl Acad Sci USA 96:10632–10636

    CAS  PubMed  Google Scholar 

  107. Nandi A, Vaz C, Bhattacharya A, Ramaswamy R (2009) miRNA-regulated dynamics in circadian oscillator models. BMC Syst Biol 3:45

    PubMed  Google Scholar 

  108. Eiring AM, Harb JG, Neviani P, Garton C, Oaks JJ, Spizzo R, Liu S, Schwind S, Santhanam R, Hickey CJ, Becker H, Chandler JC, Andino R, Cortes J, Hokland P, Huettner CS, Bhatia R, Roy DC, Liebhaber SA, Caligiuri MA, Marcucci G, Garzon R, Croce CM, Calin GA, Perrotti D (2010) miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 140:652–665

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Jay Dunlap for communication of results prior to publication, Stefan Janssen for help in preparing the figures and the anonymous reviewers for their suggestions on the manuscript. Tino Köster is a fellow of the German National Academic Foundation. Work in our laboratory is supported by the German Research Foundation through Grant STA 653/2 and the SFB 613.

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  1. Molecular Cell Physiology, Bielefeld University, 33501, Bielefeld, Germany

    Dorothee Staiger & Tino Köster

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  1. Dorothee Staiger
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  2. Tino Köster
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Correspondence to Dorothee Staiger.

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Staiger, D., Köster, T. Spotlight on post-transcriptional control in the circadian system. Cell. Mol. Life Sci. 68, 71–83 (2011). https://doi.org/10.1007/s00018-010-0513-5

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  • DOI: https://doi.org/10.1007/s00018-010-0513-5

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