Competing E3 ubiquitin ligases govern circadian periodicity by degradation of CRY in nucleus and cytoplasm

Cell

Volumn 152, Issue 5, 2013, Pages 1091-1105

  Yoo, Seung Hee ^a,b   Mohawk, Jennifer A ^a,b   Siepka, Sandra M ^c   Shan, Yongli ^a   Huh, Seong Kwon ^a   Hong, Hee Kyung ^c   Kornblum, Izabela ^b   Kumar, Vivek ^a,b   Koike, Nobuya ^a   Xu, Ming ^b   Nussbaum, Justin ^d   Liu, Xinran ^a   Chen, Zheng ^e   Chen, Zhijian J ^b   Green, Carla B ^a,d   Takahashi, Joseph S ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

^e UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME; F BOX PROTEIN; GLUTAMIC ACID; GLYCINE; PROTEIN FBXL 21; PROTEIN FBXL 3; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL COMPARTMENTALIZATION; CELL NUCLEUS; CIRCADIAN RHYTHM; CLONING; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; LOSS OF FUNCTION MUTATION; MISSENSE MUTATION; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; UBIQUITINATION;

EID: 84874768419     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.01.055     Document Type: Article

References (49)

1. J. Bass, and J.S. Takahashi Circadian integration of metabolism and energetics Science 330 2010 1349 1354
2. L. Busino, F. Bassermann, A. Maiolica, C. Lee, P.M. Nolan, S.I. Godinho, G.F. Draetta, and M. Pagano SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins Science 316 2007 900 904
3. A. Catic, C. Collins, G.M. Church, and H.L. Ploegh Preferred in vivo ubiquitination sites Bioinformatics 20 2004 3302 3307
4. C. Cenciarelli, D.S. Chiaur, D. Guardavaccaro, W. Parks, M. Vidal, and M. Pagano Identification of a family of human F-box proteins Curr. Biol. 9 1999 1177 1179
5. H. Cho, X. Zhao, M. Hatori, R.T. Yu, G.D. Barish, M.T. Lam, L.-W. Chong, L. DiTacchio, A.R. Atkins, and C.K. Glass Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β Nature 485 2012 123 127
6. C. Dai, and W. Gu p53 post-translational modification: deregulated in tumorigenesis Trends Mol. Med. 16 2010 528 536
7. H. Dardente, J. Mendoza, J.M. Fustin, E. Challet, and D.G. Hazlerigg Implication of the F-Box Protein FBXL21 in circadian pacemaker function in mammals PLoS ONE 3 2008 e3530
8. M. Gallego, and D.M. Virshup Post-translational modifications regulate the ticking of the circadian clock Nat. Rev. Mol. Cell Biol. 8 2007 139 148
9. N. Gekakis, D. Staknis, H.B. Nguyen, F.C. Davis, L.D. Wilsbacher, D.P. King, J.S. Takahashi, and C.J. Weitz Role of the CLOCK protein in the mammalian circadian mechanism Science 280 1998 1564 1569
10. S.I. Godinho, E.S. Maywood, L. Shaw, V. Tucci, A.R. Barnard, L. Busino, M. Pagano, R. Kendall, M.M. Quwailid, and M.R. Romero The after-hours mutant reveals a role for Fbxl3 in determining mammalian circadian period Science 316 2007 897 900
11. A. Hirano, K. Yumimoto, R. Tsunematsu, M. Matsumoto, M. Oyama, H. Kozuka-Hata, T. Nakagawa, D. Lanjakornsiripan, K.I. Nakayama, and Y. Fukada FBXL21 regulates oscillation of the circadian clock through ubiquitination and stabilization of cryptochromes Cell 152 2013 1106 1118 this issue
12. H.-K. Hong, J.L. Chong, W. Song, E.J. Song, A.A. Jyawook, A.C. Schook, C.H. Ko, and J.S. Takahashi Inducible and reversible Clock gene expression in brain using the tTA system for the study of circadian behavior PLoS Genet. 3 2007 e33
13. J. Jin, T. Cardozo, R.C. Lovering, S.J. Elledge, M. Pagano, and J.W. Harper Systematic analysis and nomenclature of mammalian F-box proteins Genes Dev. 18 2004 2573 2580
14. T.K. Kerppola Visualization of molecular interactions by fluorescence complementation Nat. Rev. Mol. Cell Biol. 7 2006 449 456
15. S.K. Khan, H. Xu, M. Ukai-Tadenuma, B. Burton, Y. Wang, H.R. Ueda, and A.C. Liu Identification of a novel cryptochrome differentiating domain required for feedback repression in circadian clock function J. Biol. Chem. 287 2012 25917 25926
16. D.P. King, Y. Zhao, A.M. Sangoram, L.D. Wilsbacher, M. Tanaka, M.P. Antoch, T.D. Steeves, M.H. Vitaterna, J.M. Kornhauser, and P.L. Lowrey Positional cloning of the mouse circadian clock gene Cell 89 1997 641 653
17. R.V. Kondratov, M.V. Chernov, A.A. Kondratova, V.Y. Gorbacheva, A.V. Gudkov, and M.P. Antoch BMAL1-dependent circadian oscillation of nuclear CLOCK: posttranslational events induced by dimerization of transcriptional activators of the mammalian clock system Genes Dev. 17 2003 1921 1932
18. K.A. Lamia, U.M. Sachdeva, L. DiTacchio, E.C. Williams, J.G. Alvarez, D.F. Egan, D.S. Vasquez, H. Juguilon, S. Panda, and R.J. Shaw AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation Science 326 2009 437 440
19. C. Lee, J.P. Etchegaray, F.R. Cagampang, A.S. Loudon, and S.M. Reppert Posttranslational mechanisms regulate the mammalian circadian clock Cell 107 2001 855 867
20. P.L. Lowrey, and J.S. Takahashi Genetics of circadian rhythms in Mammalian model organisms Adv. Genet. 74 2011 175 230
21. E.S. Maywood, J.E. Chesham, Q.J. Meng, P.M. Nolan, A.S. Loudon, and M.H. Hastings Tuning the period of the mammalian circadian clock: additive and independent effects of CK1εTau and Fbxl3Afh mutations on mouse circadian behavior and molecular pacemaking J. Neurosci. 31 2011 1539 1544
22. Q.J. Meng, L. Logunova, E.S. Maywood, M. Gallego, J. Lebiecki, T.M. Brown, M. Sládek, A.S. Semikhodskii, N.R. Glossop, and H.D. Piggins Setting clock speed in mammals: the CK1 epsilon tau mutation in mice accelerates circadian pacemakers by selectively destabilizing PERIOD proteins Neuron 58 2008 78 88
23. J.A. Mohawk, C.B. Green, and J.S. Takahashi Central and peripheral circadian clocks in mammals Annu. Rev. Neurosci. 35 2012 445 462
24. J. Pines Cubism and the cell cycle: the many faces of the APC/C Nat. Rev. Mol. Cell Biol. 12 2011 427 438
25. J. Pines, and C. Lindon Proteolysis: anytime, any place, anywhere? Nat. Cell Biol. 7 2005 731 735
26. N. Popov, C. Schülein, L.A. Jaenicke, and M. Eilers Ubiquitylation of the amino terminus of Myc by SCF(β-TrCP) antagonizes SCF(Fbw7)-mediated turnover Nat. Cell Biol. 12 2010 973 981
27. N. Preitner, F. Damiola, L. Lopez-Molina, J. Zakany, D. Duboule, U. Albrecht, and U. Schibler The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator Cell 110 2002 251 260
28. S.I. Reed Ratchets and clocks: the cell cycle, ubiquitylation and protein turnover Nat. Rev. Mol. Cell Biol. 4 2003 855 864
29. S.M. Siepka, S.H. Yoo, J. Park, W. Song, V. Kumar, Y. Hu, C. Lee, and J.S. Takahashi Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression Cell 129 2007 1011 1023
30. X. Tong, K. Buelow, A. Guha, R. Rausch, and L. Yin USP2a protein deubiquitinates and stabilizes the circadian protein CRY1 in response to inflammatory signals J. Biol. Chem. 287 2012 25280 25291
31. M. Ukai-Tadenuma, R.G. Yamada, H. Xu, J.A. Ripperger, A.C. Liu, and H.R. Ueda Delay in feedback repression by cryptochrome 1 is required for circadian clock function Cell 144 2011 268 281
32. G.T. van der Horst, M. Muijtjens, K. Kobayashi, R. Takano, S. Kanno, M. Takao, J. de Wit, A. Verkerk, A.P. Eker, and D. van Leenen Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms Nature 398 1999 627 630
33. M.H. Vitaterna, C.P. Selby, T. Todo, H. Niwa, C. Thompson, E.M. Fruechte, K. Hitomi, R.J. Thresher, T. Ishikawa, and J. Miyazaki Differential regulation of mammalian period genes and circadian rhythmicity by cryptochromes 1 and 2 Proc. Natl. Acad. Sci. USA 96 1999 12114 12119
34. M. Xu, B. Skaug, W. Zeng, and Z.J. Chen A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta Mol. Cell 36 2009 302 314
35. K. Yagita, F. Tamanini, M. Yasuda, J.H. Hoeijmakers, G.T. van der Horst, and H. Okamura Nucleocytoplasmic shuttling and mCRY-dependent inhibition of ubiquitylation of the mPER2 clock protein EMBO J. 21 2002 1301 1314
36. S.H. Yoo, S. Yamazaki, P.L. Lowrey, K. Shimomura, C.H. Ko, E.D. Buhr, S.M. Siepka, H.K. Hong, W.J. Oh, and O.J. Yoo PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues Proc. Natl. Acad. Sci. USA 101 2004 5339 5346
37. S.H. Yoo, C.H. Ko, P.L. Lowrey, E.D. Buhr, E.J. Song, S. Chang, O.J. Yoo, S. Yamazaki, C. Lee, and J.S. Takahashi A noncanonical E-box enhancer drives mouse Period2 circadian oscillations in vivo Proc. Natl. Acad. Sci. USA 102 2005 2608 2613
38. X. Zheng, and A. Sehgal Speed control: cogs and gears that drive the circadian clock Trends Neurosci. 35 2012 574 585
39. H.-K. Hong, J.L. Chong, W. Song, E.J. Song, A.A. Jyawook, A.C. Schook, C.H. Ko, and J.S. Takahashi Inducible and reversible Clock gene expression in brain using the tTA system for the study of circadian behavior PLoS Genet. 3 2007 e33
40. C.D. Hu, and T.K. Kerppola Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis Nat. Biotechnol. 21 2003 539 545
41. C.D. Hu, Y. Chinenov, and T.K. Kerppola Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation Mol. Cell 9 2002 789 798
42. Y. Li, W. Yu, Y. Liang, and X. Zhu Kinetochore dynein generates a poleward pulling force to facilitate congression and full chromosome alignment Cell Res. 17 2007 701 712
43. P. Meyer, L. Saez, and M.W. Young PER-TIM interactions in living Drosophila cells: an interval timer for the circadian clock Science 311 2006 226 229
44. J.L. Moran, A.D. Bolton, P.V. Tran, A. Brown, N.D. Dwyer, D.K. Manning, B.C. Bjork, C. Li, K. Montgomery, and S.M. Siepka Utilization of a whole genome SNP panel for efficient genetic mapping in the mouse Genome Res. 16 2006 436 440
45. S.M. Siepka, and J.S. Takahashi Forward genetic screens to identify circadian rhythm mutants in mice Methods Enzymol. 393 2005 219 229
46. S.M. Siepka, and J.S. Takahashi Methods to record circadian rhythm wheel running activity in mice Methods Enzymol. 393 2005 230 239
47. S.M. Siepka, S.H. Yoo, J. Park, W. Song, V. Kumar, Y. Hu, C. Lee, and J.S. Takahashi Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression Cell 129 2007 1011 1023
48. M. Xu, B. Skaug, W. Zeng, and Z.J. Chen A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta Mol. Cell 36 2009 302 314
49. S.H. Yoo, S. Yamazaki, P.L. Lowrey, K. Shimomura, C.H. Ko, E.D. Buhr, S.M. Siepka, H.K. Hong, W.J. Oh, and O.J. Yoo PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues Proc. Natl. Acad. Sci. USA 101 2004 5339 5346