In-Vivo Quantitative Proteomics Reveals a Key Contribution of Post-Transcriptional Mechanisms to the Circadian Regulation of Liver Metabolism

English version České info

Circadian clocks are endogenous oscillators that drive the rhythmic expression of a broad array of genes, orchestrating metabolism and physiology. Recent evidence indicates that post-transcriptional and post-translational mechanisms play essential roles in modulating temporal gene expression for proper circadian function, particularly for the molecular mechanism of the clock. Due to technical limitations in large-scale, quantitative protein measurements, it remains unresolved to what extent the circadian clock regulates metabolism by driving rhythms of protein abundance. Therefore, we aimed to identify global circadian oscillations of the proteome in the mouse liver by applying in vivo SILAC mouse technology in combination with state of the art mass spectrometry. Among the 3000 proteins accurately quantified across two consecutive cycles, 6% showed circadian oscillations with a defined phase of expression. Interestingly, daily rhythms of one fifth of the liver proteins were not accompanied by changes at the transcript level. The oscillations of almost half of the cycling proteome were delayed by more than six hours with respect to the corresponding, rhythmic mRNA. Strikingly we observed that the length of the time lag between mRNA and protein cycles varies across the day. Our analysis revealed a high temporal coordination in the abundance of proteins involved in the same metabolic process, such as xenobiotic detoxification. Apart from liver specific metabolic pathways, we identified many other essential cellular processes in which protein levels are under circadian control, for instance vesicle trafficking and protein folding. Our large-scale proteomic analysis reveals thus that circadian post-transcriptional and post-translational mechanisms play a key role in the temporal orchestration of liver metabolism and physiology.

Vyšlo v časopise: In-Vivo Quantitative Proteomics Reveals a Key Contribution of Post-Transcriptional Mechanisms to the Circadian Regulation of Liver Metabolism. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004047
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004047

Souhrn

Zdroje

1. Eckel-MahanK, Sassone-CorsiP (2009) Metabolism control by the circadian clock and vice versa. Nat Struct Mol Biol 16 : 462–467.

2. TakahashiJS, HongHK, KoCH, McDearmonEL (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 9 : 764–775.

3. HughesME, DiTacchioL, HayesKR, VollmersC, PulivarthyS, et al. (2009) Harmonics of circadian gene transcription in mammals. PLoS Genet 5: e1000442.

4. MillerBH, McDearmonEL, PandaS, HayesKR, ZhangJ, et al. (2007) Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci U S A 104 : 3342–3347.

5. PandaS, AntochMP, MillerBH, SuAI, SchookAB, et al. (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109 : 307–320.

6. StorchKF, LipanO, LeykinI, ViswanathanN, DavisFC, et al. (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417 : 78–83.

7. UedaHR, ChenW, AdachiA, WakamatsuH, HayashiS, et al. (2002) A transcription factor response element for gene expression during circadian night. Nature 418 : 534–539.

8. LamiaKA, StorchKF, WeitzCJ (2008) Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci U S A 105 : 15172–15177.

9. Le MartelotG, ClaudelT, GatfieldD, SchaadO, KornmannB, et al. (2009) REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biol 7: e1000181.

10. Eckel-MahanKL, PatelVR, MohneyRP, VignolaKS, BaldiP, et al. (2012) Coordination of the transcriptome and metabolome by the circadian clock. Proc Natl Acad Sci U S A 109 : 5541–5546.

11. FustinJM, DoiM, YamadaH, KomatsuR, ShimbaS, et al. (2012) Rhythmic nucleotide synthesis in the liver: temporal segregation of metabolites. Cell Rep 1 : 341–349.

12. DallmannR, ViolaAU, TarokhL, CajochenC, BrownSA (2012) The human circadian metabolome. Proc Natl Acad Sci U S A 109 : 2625–2629.

13. ReddyAB, KarpNA, MaywoodES, SageEA, DeeryM, et al. (2006) Circadian orchestration of the hepatic proteome. Curr Biol 16 : 1107–1115.

14. GachonF, BonnefontX (2010) Circadian clock-coordinated hepatic lipid metabolism: only transcriptional regulation? Aging (Albany NY) 2 : 101–106.

15. JouffeC, CretenetG, SymulL, MartinE, AtgerF, et al. (2013) The circadian clock coordinates ribosome biogenesis. PLoS Biol 11: e1001455.

16. KoikeN, YooSH, HuangHC, KumarV, LeeC, et al. (2012) Transcriptional Architecture and Chromatin Landscape of the Core Circadian Clock in Mammals. Science 338 : 349–354.

17. KojimaS, ShingleDL, GreenCB (2011) Post-transcriptional control of circadian rhythms. J Cell Sci 124 : 311–320.

18. MorfJ, ReyG, SchneiderK, StratmannM, FujitaJ, et al. (2012) Cold-Inducible RNA-Binding Protein Modulates Circadian Gene Expression Posttranscriptionally. Science 338 : 379–383.

19. AebersoldR, MannM (2003) Mass spectrometry-based proteomics. Nature 422 : 198–207.

20. MallickP, KusterB (2010) Proteomics: a pragmatic perspective. Nat Biotechnol 28 : 695–709.

21. GeigerT, CoxJ, OstasiewiczP, WisniewskiJR, MannM (2010) Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat Methods 7 : 383–385.

22. GouwJW, KrijgsveldJ, HeckAJ (2010) Quantitative proteomics by metabolic labeling of model organisms. Mol Cell Proteomics 9 : 11–24.

23. KrugerM, MoserM, UssarS, ThievessenI, LuberCA, et al. (2008) SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function. Cell 134 : 353–364.

24. ZanivanS, KruegerM, MannM (2012) In vivo quantitative proteomics: the SILAC mouse. Methods Mol Biol 757 : 435–450.

25. CoxJ, MannM (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26 : 1367–1372.

26. PossidenteB, StephanFK (1988) Circadian period in mice: analysis of genetic and maternal contributions to inbred strain differences. Behav Genet 18 : 109–117.

27. HughesME, HogeneschJB, KornackerK (2010) JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J Biol Rhythms 25 : 372–380.

28. CoxJ, MannM (2012) 1D and 2D annotation enrichment: a statistical method integrating quantitative proteomics with complementary high-throughput data. BMC Bioinformatics 13 Suppl 16: S12.

29. ReyG, CesbronF, RougemontJ, ReinkeH, BrunnerM, et al. (2011) Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLoS Biol 9: e1000595.

30. KojimaS, Sher-ChenEL, GreenCB (2012) Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev 26 : 2724–2736.

31. Le MartelotG, CanellaD, SymulL, MigliavaccaE, GilardiF, et al. (2012) Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. PLoS Biol 10: e1001442.

32. MenetJS, RodriguezJ, AbruzziKC, RosbashM (2012) Nascent-Seq reveals novel features of mouse circadian transcriptional regulation. Elife 1: e00011.

33. ReinkeH, SainiC, Fleury-OlelaF, DibnerC, BenjaminIJ, et al. (2008) Differential display of DNA-binding proteins reveals heat-shock factor 1 as a circadian transcription factor. Genes Dev 22 : 331–345.

34. SchwanhausserB, BusseD, LiN, DittmarG, SchuchhardtJ, et al. (2011) Global quantification of mammalian gene expression control. Nature 473 : 337–342.

35. SzklarczykD, FranceschiniA, KuhnM, SimonovicM, RothA, et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39: D561–568.

36. ClaudelT, CretenetG, SaumetA, GachonF (2007) Crosstalk between xenobiotics metabolism and circadian clock. FEBS Lett 581 : 3626–3633.

37. 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 Metab 4 : 25–36.

38. HowellSR, KlaassenC (1991) Circadian variation of hepatic UDP-glucuronic acid and the glucuronidation of xenobiotics in mice. Toxicol Lett 57 : 73–79.

39. BertolucciC, CavallariN, ColognesiI, AguzziJ, ChenZ, et al. (2008) Evidence for an overlapping role of CLOCK and NPAS2 transcription factors in liver circadian oscillators. Mol Cell Biol 28 : 3070–3075.

40. BertolucciC, PinottiM, ColognesiI, FoaA, BernardiF, et al. (2005) Circadian rhythms in mouse blood coagulation. J Biol Rhythms 20 : 219–224.

41. OhkuraN, OishiK, SakataT, KadotaK, KasamatsuM, et al. (2007) Circadian variations in coagulation and fibrinolytic factors among four different strains of mice. Chronobiol Int 24 : 651–669.

42. MullerOM, GerberHB (1985) Circadian changes of the rat pancreas acinar cell. A quantitative morphological investigation. Scand J Gastroenterol Suppl 112 : 12–19.

43. DecoususH, BoissierC, PerpointB, PageY, MismettiP, et al. (1991) Circadian dynamics of coagulation and chronopathology of cardiovascular and cerebrovascular events. Future therapeutic implications for the treatment of these disorders? Ann N Y Acad Sci 618 : 159–165.

44. KurnikPB (1996) Practical implications of circadian variations in thrombolytic and antithrombotic activities. Cardiol Clin 14 : 251–262.

45. MontagnanaM, SalvagnoGL, LippiG (2009) Circadian variation within hemostasis: an underrecognized link between biology and disease? Semin Thromb Hemost 35 : 23–33.

46. StenmarkH (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10 : 513–525.

47. MatsuokaK, OrciL, AmherdtM, BednarekSY, HamamotoS, et al. (1998) COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93 : 263–275.

48. PopoffV, LangerJD, ReckmannI, HellwigA, KahnRA, et al. (2011) Several ADP-ribosylation factor (Arf) isoforms support COPI vesicle formation. J Biol Chem 286 : 35634–35642.

49. BeckR, RawetM, WielandFT, CasselD (2009) The COPI system: molecular mechanisms and function. FEBS Lett 583 : 2701–2709.

50. BalasubramaniamS, SzantoA, RoachPD (1994) Circadian rhythm in hepatic low-density-lipoprotein (LDL)-receptor expression and plasma LDL levels. Biochem J 298 (Pt 1) 39–43.

51. LeeYJ, HanDH, PakYK, ChoSH (2012) Circadian regulation of low density lipoprotein receptor promoter activity by CLOCK/BMAL1, Hes1 and Hes6. Exp Mol Med 44 : 642–652.

52. PanX, HussainMM (2007) Diurnal regulation of microsomal triglyceride transfer protein and plasma lipid levels. J Biol Chem 282 : 24707–24719.

53. RezenT, RozmanD, PascussiJM, MonostoryK (2011) Interplay between cholesterol and drug metabolism. Biochim Biophys Acta 1814 : 146–160.

54. ChedidA, NairV (1972) Diurnal rhythm in endoplasmic reticulum of rat liver: electron microscopic study. Science 175 : 176–179.

55. CretenetG, Le ClechM, GachonF (2010) Circadian clock-coordinated 12 Hr period rhythmic activation of the IRE1alpha pathway controls lipid metabolism in mouse liver. Cell Metab 11 : 47–57.

56. WisniewskiJR, NagarajN, ZougmanA, GnadF, MannM (2010) Brain phosphoproteome obtained by a FASP-based method reveals plasma membrane protein topology. J Proteome Res 9 : 3280–3289.

57. WisniewskiJR, ZougmanA, MannM (2009) Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J Proteome Res 8 : 5674–5678.

58. CoxJ, NeuhauserN, MichalskiA, ScheltemaRA, OlsenJV, et al. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10 : 1794–1805.

59. TusherVG, TibshiraniR, ChuG (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98 : 5116–5121.

60. VizcainoJA, et al. The Proteomics Identifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 2013 Jan 1;41 (D1) D1063–9.