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Systematic Identification of Rhythmic Genes Reveals as a New Element in the Circadian Clockwork


A wide variety of biochemical, physiological, and molecular processes are known to have daily rhythms driven by an endogenous circadian clock. While extensive research has greatly improved our understanding of the molecular mechanisms that constitute the circadian clock, the links between this clock and dependent processes have remained elusive. To address this gap in our knowledge, we have used RNA sequencing (RNA–seq) and DNA microarrays to systematically identify clock-controlled genes in the zebrafish pineal gland. In addition to a comprehensive view of the expression pattern of known clock components within this master clock tissue, this approach has revealed novel potential elements of the circadian timing system. We have implicated one rhythmically expressed gene, camk1gb, in connecting the clock with downstream physiology of the pineal gland. Remarkably, knockdown of camk1gb disrupts locomotor activity in the whole larva, even though it is predominantly expressed within the pineal gland. Therefore, it appears that camk1gb plays a role in linking the pineal master clock with the periphery.


Vyšlo v časopise: Systematic Identification of Rhythmic Genes Reveals as a New Element in the Circadian Clockwork. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003116
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003116

Souhrn

A wide variety of biochemical, physiological, and molecular processes are known to have daily rhythms driven by an endogenous circadian clock. While extensive research has greatly improved our understanding of the molecular mechanisms that constitute the circadian clock, the links between this clock and dependent processes have remained elusive. To address this gap in our knowledge, we have used RNA sequencing (RNA–seq) and DNA microarrays to systematically identify clock-controlled genes in the zebrafish pineal gland. In addition to a comprehensive view of the expression pattern of known clock components within this master clock tissue, this approach has revealed novel potential elements of the circadian timing system. We have implicated one rhythmically expressed gene, camk1gb, in connecting the clock with downstream physiology of the pineal gland. Remarkably, knockdown of camk1gb disrupts locomotor activity in the whole larva, even though it is predominantly expressed within the pineal gland. Therefore, it appears that camk1gb plays a role in linking the pineal master clock with the periphery.


Zdroje

1. PandaS, HogeneschJB, KaySA (2002) Circadian rhythms from flies to human. Nature 417: 329–335.

2. KoCH, TakahashiJS (2006) Molecular components of the mammalian circadian clock. Hum Mol Genet 15: R271–277.

3. ChoH, ZhaoX, HatoriM, YuRT, BarishGD, et al. (2012) Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 485: 123–127.

4. SoltLA, WangY, BanerjeeS, HughesT, KojetinDJ, et al. (2012) Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 485: 62–68.

5. GachonF, OlelaFF, SchaadO, DescombesP, SchiblerU (2006) The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metabolism 4: 25–36.

6. CahillGM (1996) Circadian regulation of melatonin production in cultured zebrafish pineal and retina. Brain Res 708: 177–181.

7. FalcónJ, BesseauL, FuentèsM, SauzetS, MagnanouE, et al. (2009) Structural and functional evolution of the pineal melatonin system in vertebrates. Ann N Y Acad Sci 1163: 101–111.

8. YáñezJ, BuschJ, AnadónR, MeisslH (2009) Pineal projections in the zebrafish (Danio rerio): overlap with retinal and cerebellar projections. Neuroscience 164: 1712–1720.

9. Ekström P, Meissl H (2010) Pineal photoreception and temporal physiology in fish. In: Kulczykowska E, Popek W, Kapoor B, editors. Biological clock in fish. Science Publishers. pp. 35–70.

10. VatineG, ValloneD, GothilfY, FoulkesNS (2011) It's time to swim! Zebrafish and the circadian clock. FEBS Letters 585: 1485–1494.

11. ZivL, GothilfY (2006) Circadian time-keeping during early stages of development. Proc Natl Acad Sci USA 103: 4146–4151.

12. VatineG, ValloneD, AppelbaumL, MracekP, Ben-MosheZ, et al. (2009) Light directs zebrafish period2 expression via conserved D and E boxes. PLoS Biol 7: e1000223 doi: 10.1371/journal.pbio.1000223.

13. GamseJT, ShenYC, ThisseC, ThisseB, RaymondPA, et al. (2001) Otx5 regulates genes that show circadian expression in the zebrafish pineal complex. Nature Genetics 30: 117–121.

14. DuffieldGE (2003) DNA microarray analyses of circadian timing: the genomic basis of biological time. Journal of Neuroendocrinology 15: 991–1002.

15. BaileyMJ, BeremandPD, HammerR, Bell-PedersenD, ThomasTL, et al. (2003) Transcriptional profiling of the chick pineal gland, a photoreceptive circadian oscillator and pacemaker. Mol Endocrinol 17: 2084–2095.

16. BaileyMJ, CoonSL, CarterDA, HumphriesA, KimJS, et al. (2009) Night/day changes in pineal expression of >600 genes: central role of adrenergic/cAMP signaling. J Biol Chem 284: 7606–7622.

17. ToyamaR, ChenX, JhawarN, AamarE, EpsteinJ, et al. (2009) Transcriptome analysis of the zebrafish pineal gland. Dev Dyn 238: 1813–1826.

18. KeeganKP, PradhanS, WangJP, AlladaR (2007) Meta-analysis of drosophila circadian microarray studies identifies a novel set of rhythmically expressed genes. PLoS Comput Biol 3: e208 doi:10.1371/journal.pcbi.0030208.

19. RovsingL, ClokieS, BustosDM, RohdeK, CoonSL, et al. (2011) Crx broadly modulates the pineal transcriptome. J Neurochem 119: 262–274.

20. DraghiciS, KhatriP, EklundAC, SzallasiZ (2006) Reliability and reproducibility issues in DNA microarray measurements. Trends in Genetics 22: 101–109.

21. MarioniJC, MasonCE, ManeSM, StephensM, GiladY (2008) RNA-Seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18: 1509–1517.

22. HaydenEC (2012) RNA studies under fire. Nature 484: 428.

23. LevyO, KaniewskaP, AlonS, EisenbergE, Karako-LampertS, et al. (2011) Complex diel cycles of gene expression in coral-algal symbiosis. Science 331: 175–175.

24. 't HoenPAC, AriyurekY, ThygesenHH, VreugdenhilE, VossenRHAM, et al. (2008) Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucl Acids Res 36: e141–e141.

25. AlonS, EisenbergE, Jacob-HirschJ, RechaviG, VatineG, et al. (2009) A new cis-acting regulatory element driving gene expression in the zebrafish pineal gland. Bioinformatics 25: 559–562.

26. BradfordY, ConlinT, DunnN, FashenaD, FrazerK, et al. (2011) ZFIN: enhancements and updates to the zebrafish model organism database. Nucleic Acids Res 39: D822–829.

27. ZivL, LevkovitzS, ToyamaR, FalconJ, GothilfY (2005) Functional development of the zebrafish pineal gland: light‐induced expression of period2 is required for onset of the circadian clock. Journal of Neuroendocrinology 17: 314–320.

28. HuangDW, ShermanBT, LempickiRA (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4: 44–57.

29. GothilfY, CoonSL, ToyamaR, ChitnisA, NamboodiriMA, et al. (1999) Zebrafish serotonin N-acetyltransferase-2: marker for development of pineal photoreceptors and circadian clock function. Endocrinology 140: 4895–4903.

30. Takemoto-KimuraS, TeraiH, TakamotoM, OhmaeS, KikumuraS, et al. (2003) Molecular cloning and characterization of CLICK-III/CaMKIgamma, a novel membrane-anchored neuronal Ca2+/calmodulin-dependent protein kinase (CaMK). J Biol Chem 278: 18597–18605.

31. NishimuraH, SakagamiH, UezuA, FukunagaK, WatanabeM, et al. (2003) Cloning, characterization and expression of two alternatively splicing isoforms of Ca2+/calmodulin‐dependent protein kinase Iγ in the rat brain. Journal of Neurochemistry 85: 1216–1227.

32. CahillGM (2007) Automated video image analysis of larval zebrafish locomotor rhythms. Methods Mol Biol 362: 83–94.

33. HurdMW, CahillGM (2002) Entraining signals initiate behavioral circadian rhythmicity in larval zebrafish. J Biol Rhythms 17: 307–314.

34. BurgessHA, GranatoM (2007) Modulation of locomotor activity in larval zebrafish during light adaptation. J Exp Biol 210: 2526–2539.

35. KleinDC (2007) Arylalkylamine N-acetyltransferase: “the Timezyme.”. J Biol Chem 282: 4233–4237.

36. BégayV, FalcónJ, CahillGM, KleinDC, CoonSL (1998) Transcripts encoding two melatonin synthesis enzymes in the teleost pineal organ: circadian regulation in pike and zebrafish, but not in trout. Endocrinology 139: 905–912.

37. FalcÓn J, Besseau L, Boeuf G (2006) Molecular and cellular regulation of pineal organ responses. Sensory Systems Neuroscience. Academic Press. pp. 243–306.

38. YangY, ChengP, ZhiG, LiuY (2001) Identification of a calcium/calmodulin-dependent protein kinase that phosphorylates the Neurospora circadian clock protein FREQUENCY. J Biol Chem 276: 41064–41072.

39. WeberF, HungH-C, MaurerC, KaySA (2006) Second messenger and Ras/MAPK signalling pathways regulate CLOCK/CYCLE-dependent transcription. J Neurochem 98: 248–257.

40. AgostinoPV, FerreyraGA, MuradAD, WatanabeY, GolombekDA (2004) Diurnal, circadian and photic regulation of calcium/calmodulin-dependent kinase II and neuronal nitric oxide synthase in the hamster suprachiasmatic nuclei. Neurochem Int 44: 617–625.

41. FukushimaT, ShimazoeT, ShibataS, WatanabeA, OnoM, et al. (1997) The involvement of calmodulin and Ca2+/calmodulin-dependent protein kinase II in the circadian rhythms controlled by the suprachiasmatic nucleus. Neurosci Lett 227: 45–48.

42. DohertyCJ, KaySA (2010) Circadian control of global gene expression patterns. Annu Rev Genet 44: 419–444.

43. HansenKD, BrennerSE, DudoitS (2010) Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucl Acids Res 38: e131.

44. CheungMS, DownTA, LatorreI, AhringerJ (2011) Systematic bias in high-throughput sequencing data and its correction by BEADS. Nucl Acids Res 39: e103.

45. SchwartzS, OrenR, AstG (2011) Detection and removal of biases in the analysis of next-generation sequencing reads. PLoS ONE 6: e16685 doi:10.1371/journal.pone.0016685.

46. RobertsA, TrapnellC, DonagheyJ, RinnJL, PachterL (2011) Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biology 12: R22.

47. FullerPM, GooleyJJ, SaperCB (2006) Neurobiology of the sleep-wake cycle: sleep architecture, circadian regulation, and regulatory feedback. J Biol Rhythms 21: 482–493.

48. ZhdanovaIV (2006) Sleep in Zebrafish. Zebrafish 3: 215–226.

49. DavareMA, FortinDA, SaneyoshiT, NygaardS, KaechS, et al. (2009) Transient receptor potential canonical 5 channels activate Ca2+/calmodulin kinase Igamma to promote axon formation in hippocampal neurons. J Neurosci 29: 9794–9808.

50. Takemoto-KimuraS, Ageta-IshiharaN, NonakaM, Adachi-MorishimaA, ManoT, et al. (2007) Regulation of dendritogenesis via a lipid-raft-associated Ca2+/calmodulin-dependent protein kinase CLICK-III/CaMKIgamma. Neuron 54: 755–770.

51. WaymanGA, ImpeyS, MarksD, SaneyoshiT, GrantWF, et al. (2006) Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50: 897–909.

52. RoseboomPH, CoonSL, BalerR, McCuneSK, WellerJL, et al. (1996) Melatonin synthesis: analysis of the more than 150-fold nocturnal increase in serotonin N-acetyltransferase messenger ribonucleic acid in the rat pineal gland. Endocrinology 137: 3033–3045.

53. BalerR, CovingtonS, KleinDC (1997) The rat arylalkylamine N-acetyltransferase gene promoter. cAMP activation via a cAMP-responsive element-CCAAT complex. J Biol Chem 272: 6979–6985.

54. YinL, WuN, CurtinJC, QatananiM, SzwergoldNR, et al. (2007) Rev-erbalpha, a heme sensor that coordinates metabolic and circadian pathways. Science 318: 1786–1789.

55. FroyO (2009) Cytochrome P450 and the biological clock in mammals. Curr Drug Metab 10: 104–115.

56. HirayamaJ, ChoS, Sassone-CorsiP (2007) Circadian control by the reduction/oxidation pathway: catalase represses light-dependent clock gene expression in the zebrafish. Proc Natl Acad Sci USA 104: 15747–15752.

57. DibnerC, SchiblerU, AlbrechtU (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72: 517–549.

58. DeBruyneJ, HurdMW, GutiérrezL, KanekoM, TanY, et al. (2004) Isolation and phenogenetics of a novel circadian rhythm mutant in zebrafish. J Neurogenet 18: 403–428.

59. BolstadBM, IrizarryRA, AstrandM, SpeedTP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185–193.

60. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.

61. LevinJZ, YassourM, AdiconisX, NusbaumC, ThompsonDA, et al. (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 7: 709–715.

62. AshburnerM, BallCA, BlakeJA, BotsteinD, ButlerH, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25–29.

63. KanehisaM, GotoS (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27–30.

64. CavallariN, FrigatoE, ValloneD, FröhlichN, Lopez-OlmedaJF, et al. (2011) A blind circadian clock in cavefish reveals that opsins mediate peripheral clock photoreception. PLoS Biol 9: e1001142 doi:10.1371/journal.pbio.1001142.

65. Machluf Y, Levkowitz G (2011) Visualization of mRNA expression in the zebrafish embryo. In: Gerst JE, editor. RNA detection and visualization. Methods in Molecular Biology. Humana Press. pp. 83–102.

66. AbeT, IshikawaT, MasudaT, MizusawaK, TsukamotoT, et al. (2006) Molecular analysis of Dec1 and Dec2 in the peripheral circadian clock of zebrafish photosensitive cells. Biochem Biophys Res Commun 351: 1072–1077.

67. CermakianN, WhitmoreD, FoulkesNS, Sassone-CorsiP (2000) Asynchronous oscillations of two zebrafish CLOCK partners reveal differential clock control and function. Proc Natl Acad Sci USA 97: 4339–4344.

68. MoserM, YuQ, BodeC, XiongJW, PattersonC (2007) BMPER is a conserved regulator of hematopoietic and vascular development in zebrafish. Journal of Molecular and Cellular Cardiology 43: 243–253.

69. RentzschF, ZhangJ, KramerC, SebaldW, HammerschmidtM (2006) Crossveinless 2 is an essential positive feedback regulator of Bmp signaling during zebrafish gastrulation. Development 133: 801–811.

70. KobayashiY, IshikawaT, HirayamaJ, DaiyasuH, KanaiS, et al. (2000) Molecular analysis of zebrafish photolyase/cryptochrome family: two types of cryptochromes present in zebrafish. Genes Cells 5: 725–738.

71. Ben-MosheZ, VatineG, AlonS, TovinA, MracekP, et al. (2010) Multiple PAR and E4BP4 bZIP transcription factors in zebrafish: diverse spatial and temporal expression patterns. Chronobiol Int 27: 1509–1531.

72. AmaralIPG, JohnstonIA (2012) Circadian expression of clock and putative clock-controlled genes in skeletal muscle of the zebrafish. Am J Physiol Regul Integr Comp Physiol 302: R193–R206.

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