USP2 regulates the intracellular localization of PER1 and circadian gene expression

Journal of Biological Rhythms

Volumn 29, Issue 4, 2014, Pages 243-256

  Yang, Yaoming ^a   Duguay, David ^b,c   Fahrenkrug, Jan ^d   Cermakian, Nicolas ^b,c   Wing, Simon S ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

circadian clock; clock controlled genes; deubiquitination; intracellular localization; PER1; USP2

Indexed keywords

CIRCADIAN RHYTHM SIGNALING PROTEIN; DEUBIQUITINASE; MESSENGER RNA; NUCLEAR PROTEIN; PER1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTOME; USP2 PROTEIN, MOUSE;

ANIMAL; C57BL MOUSE; CELL LINE; CELL NUCLEUS; CIRCADIAN RHYTHM; FEMALE; FIBROBLAST; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; MOUSE;

ANIMALS; CELL LINE; CELL NUCLEUS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CLOCK PROTEINS; FEMALE; FIBROBLASTS; GENE EXPRESSION; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR PROTEINS; PERIOD CIRCADIAN PROTEINS; RNA, MESSENGER; TRANSCRIPTOME; UBIQUITIN-SPECIFIC PROTEASES;

EID: 84905698438     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730414544741     Document Type: Article

References (62)

1. Ausabel FM, Brent R, Kingston DD, Moore DD, Seidman JG, Smith JA, and Struhl K (1993) Current Protocols in Molecular Biology. New York: John Wiley.
2. Balsalobre A, Damiola F, and Schibler U (1998) A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93:929-937.
3. Bass J (2012) Circadian topology of metabolism. Nature 491:348-356.
4. Bedard N, Yang Y, Gregory M, Cyr DG, Suzuki J, Yu X, Chian RC, Hermo L, O'Flaherty C, Smith CE, et al. (2011) Mice lacking the USP2 deubiquitinating enzyme have severe male subfertility associated with defects in fertilization and sperm motility. Biol Reprod 85:594-604.
5. Busino L, Bassermann F, Maiolica A, Lee C, Nolan PM, Godinho SI, Draetta GF, and Pagano M (2007) SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science 316:900-904.
6. Chopin-Delannoy S, Thenot S, Delaunay F, Buisine E, Begue A, Duterque-Coquillaud M, and Laudet V (2003) A specific and unusual nuclear localization signal in the DNA binding domain of the Rev-erb orphan receptors. J Mol Endocrinol 30:197-211.
7. Cuninkova L and Brown SA (2008) Peripheral circadian oscillators: Interesting mechanisms and powerful tools. Ann N Y Acad Sci 1129:358-370.
8. Dardente H, Fortier EE, Martineau V, and Cermakian N (2007) Cryptochromes impair phosphorylation of transcriptional activators in the clock: A general mechanism for circadian repression. Biochem J 402:525-536.
9. Dardente H, Mendoza J, Fustin JM, Challet E, and Hazlerigg DG (2008) Implication of the F-box protein FBXL21 in circadian pacemaker function in mammals. PLoS One 3:e3530.
10. Doi M, Nakajima Y, Okano T, and Fukada Y (2001) Light-induced phase-delay of the chicken pineal circadian clock is associated with the induction of cE4bp4, a potential transcriptional repressor of cPer2 gene. Proc Natl Acad Sci U S A 98:8089-8094.
11. Doi M, Okano T, Yujnovsky I, Sassone-Corsi P, and Fukada Y (2004) Negative control of circadian clock regulator E4BP4 by casein kinase Iepsilon-mediated phosphorylation. Curr Biol 14:975-980.
12. Duguay D and Cermakian N (2009) The crosstalk between physiology and circadian clock proteins. Chronobiol Int 26:1479-1513.
13. Eide EJ, Woolf MF, Kang H, Woolf P, Hurst W, Camacho F, Vielhaber EL, Giovanni A, and Virshup DM (2005) Control of mammalian circadian rhythm by CKIepsilon-regulated proteasome-mediated PER2 degradation. Mol Cell Biol 25:2795-2807.
14. Fahrenkrug J, Georg B, Hannibal J, Hindersson P, and Gras S (2006) Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. Endocrinology 147:3769-3776.
15. Feng D and Lazar MA (2012) Clocks, metabolism, and the epigenome. Mol Cell 47:158-167.
16. Field MD, Maywood ES, O'Brien JA, Weaver DR, Reppert SM, and Hastings MH (2000) Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of the circadian clockwork and resetting mechanisms. Neuron 25:437-447.
17. Gery S and Koeffler HP (2010) Circadian rhythms and cancer. Cell Cycle 9:1097-1103.
18. Glickman MH and Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol Rev 82:373-428.
19. Godinho SI, Maywood ES, Shaw L, Tucci V, Barnard AR, Busino L, Pagano M, Kendall R, Quwailid MM, Romero MR, et al. (2007) The after-hours mutant reveals a role for Fbxl3 in determining mammalian circadian period. Science 316:897-900.
20. Grima B, Lamouroux A, Chelot E, Papin C, Limbourg-Bouchon B, and Rouyer F (2002) The F-box protein slimb controls the levels of clock proteins period and timeless. Nature 420:178-182.
21. Hirano A, Yumimoto K, Tsunematsu R, Matsumoto M, Oyama M, Kozuka-Hata H, Nakagawa T, Lanjakornsiripan D, Nakayama KI, and Fukada Y (2013) FBXL21 regulates oscillation of the circadian clock through ubiquitination and stabilization of cryptochromes. Cell 152:1106-1118.
22. Kita Y, Shiozawa M, Jin W, Majewski RR, Besharse JC, Greene AS, and Jacob HJ (2002) Implications of circadian gene expression in kidney, liver and the effects of fasting on pharmacogenomic studies. Pharmacogenetics 12:55-65.
23. Kivimaki M, Virtanen M, Elovainio M, Vaananen A, Keltikangas-Jarvinen L, and Vahtera J (2006) Prevalent cardiovascular disease, risk factors and selection out of shift work. Scand J Work Environ Health 32:204-208.
24. Komander D, Clague MJ, and Urbe S (2009) Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10:550-563.
25. Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, Jin X, Maywood ES, Hastings MH, and Reppert SM (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98:193-205.
26. Kurabayashi N, Hirota T, Sakai M, Sanada K, and Fukada Y (2010) DYRK1A and glycogen synthase kinase 3beta, a dual-kinase mechanism directing proteasomal degradation of CRY2 for circadian timekeeping. Mol Cell Biol 30:1757-1768.
27. Kwon I, Lee J, Chang SH, Jung NC, Lee BJ, Son GH, Kim K, and Lee KH (2006) BMAL1 shuttling controls transactivation and degradation of the CLOCK/BMAL1 heterodimer. Mol Cell Biol 26:7318-7330.
28. Lee J, Lee Y, Lee MJ, Park E, Kang SH, Chung CH, Lee KH, and Kim K (2008) Dual modification of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex. Mol Cell Biol 28:6056-6065.
29. Lin H, Keriel A, Morales CR, Bedard N, Zhao Q, Hingamp P, Lefrancois S, Combaret L, and Wing SS (2000) Divergent N-terminal sequences target an inducible testis deubiquitinating enzyme to distinct subcellular structures. Mol Cell Biol 20:6568-6578.
30. Lin H, Yin L, Reid J, Wilkinson KD, and Wing SS (2001) Divergent N-terminal sequences of a deubiquitinating enzyme modulate substrate specificity. J Biol Chem 276:20357-20363.
31. Liu Z and Chu G (2013) Chronobiology in mammalian health. Mol Biol Rep 40:2491-2501.
32. Livak KJ and Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
33. McCarthy JJ, Andrews JL, McDearmon EL, Campbell KS, Barber BK, Miller BH, Walker JR, Hogenesch JB, Takahashi JS, and Esser KA (2007) Identification of the circadian transcriptome in adult mouse skeletal muscle. Physiol Genomics 31:86-95.
34. Mitsui S, Yamaguchi S, Matsuo T, Ishida Y, and Okamura H (2001) Antagonistic role of E4BP4 and PAR proteins in the circadian oscillatory mechanism. Genes Dev 15:995-1006.
35. Miyazaki K, Mesaki M, and Ishida N (2001) Nuclear entry mechanism of rat PER2 (rPER2): Role of rPER2 in nuclear localization of CRY protein. Mol Cell Biol 21:6651-6659.
36. Morikawa Y, Nakagawa H, Miura K, Soyama Y, Ishizaki M, Kido T, Naruse Y, Suwazono Y, and Nogawa K (2005) Shift work and the risk of diabetes mellitus among Japanese male factory workers. Scand J Work Environ Health 31:179-183.
37. Ohsaki K, Oishi K, Kozono Y, Nakayama K, Nakayama KI, and Ishida N (2008) The role of β-TrCP1 and β-TrCP2 in circadian rhythm generation by mediating degradation of clock protein PER2. J Biochem 144:609-618.
38. Oishi K, Amagai N, Shirai H, Kadota K, Ohkura N, and Ishida N (2005) Genome-wide expression analysis reveals 100 adrenal gland-dependent circadian genes in the mouse liver. DNA Res 12:191-202.
39. Okamura H (2007) Suprachiasmatic nucleus clock time in the mammalian circadian system. Cold Spring Harb Symp Quant Biol 72:551-556.
40. Reischl S, Vanselow K, Westermark PO, Thierfelder N, Maier B, Herzel H, and Kramer A (2007) Beta-TrCP1-mediated degradation of PERIOD2 is essential for circadian dynamics. J Biol Rhythms 22:375-386.
41. Sahar S and Sassone-Corsi P (2009) Metabolism and cancer: the circadian clock connection. Nat Rev Cancer 9:886-896.
42. Scoma HD, Humby M, Yadav G, Zhang Q, Fogerty J, and Besharse JC (2011) The de-ubiquitinylating enzyme, USP2, is associated with the circadian clockwork and regulates its sensitivity to light. PLoS One 6:e25382.
43. Shirogane T, Jin J, Ang XL, and Harper JW (2005) SCFbeta-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein. J Biol Chem 280:26863-26872.
44. Siepka SM, Yoo SH, Park J, Song W, Kumar V, Hu Y, Lee C, and Takahashi JS (2007) Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression. Cell 129:1011-1023.
45. Sowa ME, Bennett EJ, Gygi SP, and Harper JW (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138:389-403.
46. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, and Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78-83.
47. Takano A, Isojima Y, and Nagai K (2004) Identification of mPer1 phosphorylation sites responsible for the nuclear entry. J Biol Chem 279:32578-32585.
48. Tamanini F, Yagita K, Okamura H, and van der Horst GT (2005) Nucleocytoplasmic shuttling of clock proteins. Methods Enzymol 393:418-435.
49. Tamaru T, Isojima Y, van der Horst GT, Takei K, Nagai K, and Takamatsu K (2003) Nucleocytoplasmic shuttling and phosphorylation of BMAL1 are regulated by circadian clock in cultured fibroblasts. Genes Cells 8:973-983.
50. Tong X, Buelow K, Guha A, Rausch R, and Yin L (2012) USP2a protein deubiquitinates and stabilizes the circadian protein CRY1 in response to inflammatory signals. J Biol Chem 287:25280-25291.
51. Travnickova-Bendova Z, Cermakian N, Reppert SM, and Sassone-Corsi P (2002) Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity. Proc Natl Acad Sci U S A 99:7728-7733.
52. Ueda HR, Hayashi S, Chen W, Sano M, Machida M, Shigeyoshi Y, Iino M, and Hashimoto S (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 37:187-192.
53. Vielhaber EL, Duricka D, Ullman KS, and Virshup DM (2001) Nuclear export of mammalian PERIOD proteins. J Biol Chem 276:45921-45927.
54. Virshup DM, Eide EJ, Forger DB, Gallego M, and Harnish EV (2007) Reversible protein phosphorylation regulates circadian rhythms. Cold Spring Harb Symp Quant Biol 72:413-420.
55. Yagita K, Tamanini F, Yasuda M, Hoeijmakers JH, van der Horst GT, and Okamura H (2002) Nucleocytoplasmic shuttling and mCRY-dependent inhibition of ubiquitylation of the mPER2 clock protein. EMBO J 21:1301-1314.
56. Yagita K, Yamaguchi S, Tamanini F, van Der Horst GT, Hoeijmakers JH, Yasui A, Loros JJ, Dunlap JC, and Okamura H (2000) Dimerization and nuclear entry of mPER proteins in mammalian cells. Genes Dev 14:1353-1363.
57. Yamaguchi S, Mitsui S, Yan L, Yagita K, Miyake S, and Okamura H (2000) Role of DBP in the circadian oscillatory mechanism. Mol Cell Biol 20:4773-4781.
58. Yan J, Wang H, Liu Y, and Shao C (2008) Analysis of gene regulatory networks in the mammalian circadian rhythm. PLoS Comp Biol 4:e1000193.
59. Yang Y, Duguay D, Bedard N, Rachalski A, Baquiran G, Na CH, Fahrenkrug J, Storch KF, Peng J, Wing SS, et al. (2012) Regulation of behavioral circadian rhythms and clock protein PER1 by the deubiquitinating enzyme USP2. Biol Open 1:789-801.
60. Yin L, Joshi S, Wu N, Tong X, and Lazar MA (2010) E3 ligases Arf-bp1 and Pam mediate lithium-stimulated degradation of the circadian heme receptor Rev-erb alpha. Proc Natl Acad Sci U S A 107:11614-11619.
61. Yoo SH, Mohawk JA, Siepka SM, Shan Y, Huh SK, Hong HK, 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.
62. Yu EA and Weaver DR (2011) Disrupting the circadian clock: Gene-specific effects on aging, cancer, and other phenotypes. Aging 3:479-493.