Rhythmic degradation explains and unifies circadian transcriptome and proteome data

Cell Reports

Volumn 9, Issue 2, 2014, Pages 741-751

  Lück, Sarah ^a   Thurley, Kevin ^a   Thaben, Paul F ^a   Westermark, Pål O ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLD INDUCED RNA BINDING PROTEIN; E3 LIGASE FBXO6; MESSENGER RNA; PROTEOME; RNA BINDING PROTEIN; TRANSCRIPTOME; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ABSOLUTE AMPLITUDE; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DEGRADATION; DROSOPHILA; ENZYME ACTIVITY; GENETIC PARAMETERS; HALF LIFE TIME; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PHASE VECTOR MODEL; POLY(A) TAIL LENGTH; POLYADENYLATION; PREDICTIVE VALUE; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN RNA BINDING; PROTEIN SYNTHESIS; PROTEOMICS; RELATIVE AMPLITUDE; RHYTHMIC DEGRADATION; RHYTHMIC POSTTRANSCRIPTIONAL REGULATION; RNA DEGRADATION; RNA SEQUENCE; RNA SYNTHESIS; SIGNAL PROCESSING; THEORY; TIME SERIES ANALYSIS; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANIMAL; BIOLOGICAL MODEL; GENETICS; METABOLISM; RNA PROCESSING; RNA STABILITY;

MAMMALIA;

ANIMALS; CIRCADIAN RHYTHM; DROSOPHILA; MICE; MODELS, BIOLOGICAL; PROTEOME; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; TRANSCRIPTOME;

EID: 84919650135     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.09.021     Document Type: Article

References (53)

1. Asher, G., and Schibler, U. (2011). Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab. 13, 125-137.
2. 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.
3. Bass, J., and Takahashi, J.S. (2010). Circadian integration of metabolism and energetics. Science 330, 1349-1354.
4. Benjamini, Y., and Hochberg, Y. (2000). On the adaptive control of the false discovery rate in multiple testing with independent statistics. J. Educ. Behav. Stat. 25, 60-83.
5. Clague, M.J., and Urbé, S. (2010). Ubiquitin: same molecule, different degradation pathways. Cell 143, 682-685.
6. Cookson, N.A., Mather, W.H., Danino, T., Mondragón-Palomino, O., Williams, R.J., Tsimring, L.S., and Hasty, J. (2011). Queueing up for enzymatic processing: correlated signaling through coupled degradation. Mol. Syst. Biol. 7, 561.
7. de Bie, P., and Ciechanover, A. (2011). Ubiquitination of E3 ligases: self-regulation of the ubiquitin system via proteolytic and non-proteolytic mechanisms. Cell Death Differ. 18, 1393-1402.
8. Doherty, C.J., and Kay, S.A. (2010). Circadian control of global gene expression patterns. Annu. Rev. Genet. 44, 419-444.
9. Doherty, C.J., and Kay, S.A. (2012). Circadian surprise-it's not all about transcription. Science 338, 338-340.
10. Eden, E., Geva-Zatorsky, N., Issaeva, I., Cohen, A., Dekel, E., Danon, T., Cohen, L., Mayo, A., and Alon, U. (2011). Proteome half-life dynamics in living human cells. Science 331, 764-768.
11. Friedel, C.C., Dölken, L., Ruzsics, Z., Koszinowski, U.H., and Zimmer, R. (2009). Conserved principles of mammalian transcriptional regulation revealed by RNA half-life. Nucleic Acids Res. 37, e115.
12. Friedman, N., Cai, L., and Xie, X.S. (2006). Linking stochastic dynamics to population distribution: an analytical framework of gene expression. Phys. Rev. Lett. 97, 168302.
13. Garneau, N.L., Wilusz, J., and Wilusz, C.J. (2007). The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8, 113-126.
14. Gutu, A., and O'Shea, E.K. (2013). Two antagonistic clock-regulated histidine kinases time the activation of circadian gene expression. Mol. Cell 50, 288-294.
15. Hargrove, J.L., and Schmidt, F.H. (1989). The role of mRNA and protein stability in gene expression. FASEB J. 3, 2360-2370.
16. Hausser, J., Syed, A.P., Selevsek, N., van Nimwegen, E., Jaskiewicz, L., Aebersold, R., and Zavolan, M. (2013). Timescales and bottlenecks in miRNA-dependent gene regulation. Mol. Syst. Biol. 9, 711.
17. Hogenesch, J.B., and Ueda, H.R. (2011). Understanding systems-level properties: timely stories from the study of clocks. Nat. Rev. Genet. 12, 407-416.
18. Hsu, S.-D., Tseng, Y.-T., Shrestha, S., Lin, Y.-L., Khaleel, A., Chou, C.-H., Chu, C.-F., Huang, H.-Y., Lin, C.-M., Ho, S.-Y., et al. (2014). miRTarBase update 2014: an information resource for experimentally validated miRNA-target interactions. Nucleic Acids Res. 42, D78-D85.
19. Hughes, M.E., DiTacchio, L., Hayes, K.R., Vollmers, C., Pulivarthy, S., Baggs, J.E., Panda, S., and Hogenesch, J.B. (2009). Harmonics of circadian gene transcription in mammals. PLoS Genet. 5, e1000442.
20. Hughes, M.E., Hogenesch, J.B., and Kornacker, K. (2010). JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J. Biol. Rhythms 25, 372-380.
21. Jouffe, C., Cretenet, G., Symul, L., Martin, E., Atger, F., Naef, F., and Gachon, F. (2013). The circadian clock coordinates ribosome biogenesis. PLoS Biol. 11, e1001455.
22. Koike, N., Yoo, S.-H., Huang, H.-C., Kumar, V., Lee, C., Kim, T.-K., and Takahashi, J.S. (2012). Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338, 349-354.
23. Kojima, S., Shingle, D.L., and Green, C.B. (2011). Post-transcriptional control of circadian rhythms. J. Cell Sci. 124, 311-320.
24. Kojima, S., Sher-Chen, E.L., and Green, C.B. (2012). Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev. 26, 2724-2736.
25. Lamia, K.A., Sachdeva, U.M., DiTacchio, L., Williams, E.C., Alvarez, J.G., Egan, D.F., Vasquez, D.S., Juguilon, H., Panda, S., Shaw, R.J., et al. (2009). AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326, 437-440.
26. Le Martelot, G., Canella, D., Symul, L., Migliavacca, E., Gilardi, F., Liechti, R., Martin, O., Harshman, K., Delorenzi, M., Desvergne, B., et al.; CycliX Consortium (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.
27. Lim, W.A., Lee, C.M., and Tang, C. (2013). Design principles of regulatory networks: searching for the molecular algorithms of the cell. Mol. Cell 49, 202-212.
28. Liu, B., Zheng, Y., Wang, T.-D., Xu, H.-Z., Xia, L., Zhang, J., Wu, Y.-L., Chen, G.Q., and Wang, L.-S. (2012). Proteomic identification of common SCF ubiquitin ligase FBXO6-interacting glycoproteins in three kinds of cells. J. Proteome Res. 11, 1773-1781.
29. Liu, Y., Hu, W., Murakawa, Y., Yin, J., Wang, G., Landthaler, M., and Yan, J. (2013). Cold-induced RNA-binding proteins regulate circadian gene expression by controlling alternative polyadenylation. Sci. Rep. 3, 2054.
30. Ma, D., Panda, S., and Lin, J.D. (2011). Temporal orchestration of circadian autophagy rhythm by C/EBPb. EMBO J. 30, 4642-4651.
31. Matsuo, T., Yamaguchi, S., Mitsui, S., Emi, A., Shimoda, F., and Okamura, H. (2003). Control mechanism of the circadian clock for timing of cell division in vivo. Science 302, 255-259.
32. Mauvoisin, D., Wang, J., Jouffe, C., Martin, E., Atger, F., Waridel, P., Quadroni, M., Gachon, F., and Naef, F. (2014). Circadian clock-dependent and-independent rhythmic proteomes implement distinct diurnal functions in mouse liver. Proc. Natl. Acad. Sci. USA 111, 167-172.
33. Menet, J.S., Rodriguez, J., Abruzzi, K.C., and Rosbash, M. (2012). Nascent-Seq reveals novel features of mouse circadian transcriptional regulation. eLife 1, e00011.
34. Milo, R., Shen-Orr, S., Itzkovitz, S., Kashtan, N., Chklovskii, D., and Alon, U. (2002). Network motifs: simple building blocks of complex networks. Science 298, 824-827.
35. Morf, J., Rey, G., Schneider, K., Stratmann, M., Fujita, J., Naef, F., and Schibler, U. (2012). Cold-inducible RNA-binding protein modulates circadian gene expression posttranscriptionally. Science 338, 379-383.
36. 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. (2006). Circadian orchestration of the hepatic proteome. Curr. Biol. 16, 1107-1115.
37. Robinson, B.G., Frim, D.M., Schwartz, W.J., and Majzoub, J.A. (1988). Vasopressin mRNA in the suprachiasmatic nuclei: daily regulation of polyadenylate tail length. Science 241, 342-344.
38. Robles, M.S., Cox, J., and Mann, M. (2014). In-vivo quantitative proteomics reveals a key contribution of post-transcriptional mechanisms to the circadian regulation of liver metabolism. PLoS Genet. 10, e1004047.
39. Rodriguez, J., Tang, C.-H.A., Khodor, Y.L., Vodala, S., Menet, J.S., and Rosbash, M. (2013). Nascent-Seq analysis of Drosophila cycling gene expression. Proc. Natl. Acad. Sci. USA 110, E275-E284.
40. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011). Global quantification of mammalian gene expression control. Nature 473, 337-342.
41. Stubblefield, J.J., Terrien, J., and Green, C.B. (2012). Nocturnin: at the crossroads of clocks and metabolism. Trends Endocrinol. Metab. 23, 326-333.
42. Thattai, M., and van Oudenaarden, A. (2001). Intrinsic noise in gene regulatory networks. Proc. Natl. Acad. Sci. USA 98, 8614-8619.
43. Thomsen, S., Anders, S., Janga, S.C., Huber, W., and Alonso, C.R. (2010). Genome-wide analysis of mRNA decay patterns during early Drosophila development. Genome Biol. 11, R93.
44. Tippmann, S.C., Ivanek, R., Gaidatzis, D., Schöler, A., Hoerner, L., van Nimwegen, E., Stadler, P.F., Stadler, M.B., and Schübeler, D. (2012). Chromatin measurements reveal contributions of synthesis and decay to steady-state mRNA levels. Mol. Syst. Biol. 8, 593.
45. Ukai-Tadenuma, M., Yamada, R.G., Xu, H., Ripperger, J.A., Liu, A.C., and Ueda, H.R. (2011). Delay in feedback repression by cryptochrome 1 is required for circadian clock function. Cell 144, 268-281.
46. Vinciguerra, M., Musaro, A., and Rosenthal, N. (2010). Regulation of muscle atrophy in aging and disease. Adv. Exp. Med. Biol. 694, 211-233.
47. Vollmers, C., Schmitz, R.J., Nathanson, J., Yeo, G., Ecker, J.R., and Panda, S. (2012). Circadian oscillations of protein-coding and regulatory RNAs in a highly dynamic mammalian liver epigenome. Cell Metab. 16, 833-845.
48. Westermark, P.O., and Herzel, H. (2013). Mechanism for 12 hr rhythm generation by the circadian clock. Cell Reports 3, 1228-1238.
49. Woo, K.-C., Ha, D.-C., Lee, K.-H., Kim, D.-Y., Kim, T.-D., and Kim, K.-T. (2010). Circadian amplitude of cryptochrome 1 is modulated by mRNA stability regulation via cytoplasmic hnRNP D oscillation. Mol. Cell. Biol. 30, 197-205.
50. Yamazaki, S., Straume, M., Tei, H., Sakaki, Y., Menaker, M., and Block, G.D. (2002). Effects of aging on central and peripheral mammalian clocks. Proc. Natl. Acad. Sci. USA 99, 10801-10806.
51. Yin, L., Joshi, S., Wu, N., Tong, X., and Lazar, M.A. (2010). E3 ligases Arf-bp1 and Pam mediate lithium-stimulated degradation of the circadian heme receptor Rev-erb alpha. Proc. Natl. Acad. Sci. USA 107, 11614-11619.
52. Yoo, S.-H., Mohawk, J.A., Siepka, S.M., Shan, Y., Huh, S.K., Hong, H.-K., Kornblum, I., Kumar, V., Koike, N., Xu, M., et al. (2013). Competing E3 ubiquitin ligases govern circadian periodicity by degradation of CRY in nucleus and cytoplasm. Cell 152, 1091-1105.
53. Zhang, E.E., and Kay, S.A. (2010). Clocks not winding down: unravelling circadian networks. Nat. Rev. Mol. Cell Biol. 11, 764-776.