USP2a protein deubiquitinates and stabilizes the circadian protein CRY1 in response to inflammatory signals

Journal of Biological Chemistry

Volumn 287, Issue 30, 2012, Pages 25280-25291

  Tong, Xin ^a   Buelow, Katie ^a   Guha, Anirvan ^a   Rausch, Rebecca ^a   Yin, Lei ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCADIAN CLOCK; CRYPTOCHROMES; CYTOKINES; DEUBIQUITINATING ENZYMES; DYNAMIC CONTROLS; ENVIRONMENTAL CUES; LARGE GROUPS; MAMMALIAN CLOCK; MOUSE LIVER; OPTIMAL ADAPTATION; OSCILLATION AMPLITUDE; PHYSIOLOGICAL ACTIVITY; PROMOTER ACTIVITIES; PROTEASOMES; PROTEIN LEVEL; PROTEIN STABILITY; UBIQUITINATION;

CLOCKS; DEGRADATION; ENZYME ACTIVITY; GENE EXPRESSION; MAMMALS;

PROTEINS;

CRYPTOCHROME 1; CYSTEINE PROTEINASE; PER2 PROTEIN; PROTEIN USP2A; SHORT HAIRPIN RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; EMBRYO; GENE; GENE EXPRESSION REGULATION; GENE REPRESSION; INFLAMMATION; LIVER; MALE; MOUSE; NONHUMAN; PER2 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN DEUBIQUITINATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UBIQUITINATION;

ANIMALS; CIRCADIAN CLOCKS; CRYPTOCHROMES; ENDOPEPTIDASES; GENE EXPRESSION REGULATION; HEP G2 CELLS; HUMANS; INFLAMMATION; LIVER; MICE; NIH 3T3 CELLS; PERIOD CIRCADIAN PROTEINS; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; PROTEOLYSIS; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITINATION;

MAMMALIA;

EID: 84864089093     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.340786     Document Type: Article

References (77)

1. Bass, J., and Takahashi, J. S. (2010) Circadian integration of metabolism and energetics. Science 330, 1349-1354
2. Green, C. B., Takahashi, J. S., and Bass, J. (2008) The meter of metabolism. Cell 134, 728-742
3. Takahashi, J. S., Hong, H. K., Ko, C. H., and McDearmon, E. L. (2008) The genetics of mammalian circadian order and disorder. Implications for physiology and disease. Nat. Rev. Genet. 9, 764-775
4. Baggs, J. E., and Hogenesch, J. B. (2010) Genomics and systems approaches in the mammalian circadian clock. Curr. Opin. Genet. Dev. 20, 581-587
5. Dibner, C., Schibler, U., and Albrecht, U. (2010) The mammalian circadian timing system. Organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517-549
6. Paschos, G. K., Baggs, J. E., Hogenesch, J. B., and FitzGerald, G. A. (2010) The role of clock genes in pharmacology. Annu. Rev. Pharmacol. Toxicol. 50, 187-214
7. Reppert, S. M., and Weaver, D. R. (2001) Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 63, 647-676 (Pubitemid 32304333)
8. 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 α. Proc. Natl. Acad. Sci. U.S.A. 107, 11614-11619
9. Zhang, E. E., Liu, A. C., Hirota, T., Miraglia, L. J., Welch, G., Pongsawakul, P. Y., Liu, X., Atwood, A., Huss, J. W., 3rd, Janes, J., Su, A. I., Hogenesch, J. B., and Kay, S. A. (2009) A genome-wide RNAi screen for modifiers of the circadian clock in human cells. Cell 139, 199-210
10. Asher, G., Gatfield, D., Stratmann, M., Reinke, H., Dibner, C., Kreppel, F., Mostoslavsky, R., Alt, F. W., and Schibler, U. (2008) SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134, 317-328 (Pubitemid 352024391)
11. Asher, G., Reinke, H., Altmeyer, M., Gutierrez-Arcelus, M., Hottiger, M. O., and Schibler, U. (2010) Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell 142, 943-953
12. Lee, C., Etchegaray, J. P., Cagampang, F. R., Loudon, A. S., and Reppert, S. M. (2001) Post-translational mechanisms regulate the mammalian circadian clock. Cell 107, 855-867 (Pubitemid 34084977)
13. Busino, L., Bassermann, F., Maiolica, A., Lee, C., Nolan, P. M., Godinho, S. I., Draetta, G. F., and Pagano, M. (2007) SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science 316, 900-904 (Pubitemid 46764282)
14. Godinho, S. I., Maywood, E. S., Shaw, L., Tucci, V., Barnard, A. R., Busino, L., Pagano, M., Kendall, R., Quwailid, M. M., Romero, M. R., O'neill, J., Chesham, J. E., Brooker, D., Lalanne, Z., Hastings, M. H., and Nolan, P. M. (2007) The after-hours mutant reveals a role for Fbxl3 in determining mammalian circadian period. Science 316, 897-900 (Pubitemid 46764281)
15. 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., Thompson, C. B., and Evans, R. M. (2009) AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326, 437-440
16. Siepka, S. M., Yoo, S. H., Park, J., Song, W., Kumar, V., Hu, Y., Lee, C., and Takahashi, J. S. (2007) Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression. Cell 129, 1011-1023 (Pubitemid 46802705)
17. Harada, Y., Sakai, M., Kurabayashi, N., Hirota, T., and Fukada, Y. (2005) Ser-557-phosphorylated mCRY2 is degraded upon synergistic phosphorylation by glycogen synthase kinase-3β. J. Biol. Chem. 280, 31714-31721 (Pubitemid 41291919)
18. Kurabayashi, N., Hirota, T., Sakai, M., Sanada, K., and Fukada, Y. (2010) DYRK1A and glycogen synthase kinase 3β, a dual-kinase mechanism directing proteasomal degradation of CRY2 for circadian timekeeping. Mol. Cell. Biol. 30, 1757-1768
19. van der Horst, G. T., Muijtjens, M., Kobayashi, K., Takano, R., Kanno, S., Takao, M., de Wit, J., Verkerk, A., Eker, A. P., van Leenen, D., Buijs, R., Bootsma, D., Hoeijmakers, J. H., and Yasui, A. (1999) Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398, 627-630 (Pubitemid 29183691)
20. Baggs, J. E., Price, T. S., DiTacchio, L., Panda, S., Fitzgerald, G. A., and Hogenesch, J. B. (2009) Network features of the mammalian circadian clock. PLoS Biol. 7, e52
21. Vollmers, C., Panda, S., and DiTacchio, L. (2008) A high-throughput assay for siRNA-based circadian screens in human U2OS cells. PLoS One 3, e3457
22. Hashiramoto, A., Yamane, T., Tsumiyama, K., Yoshida, K., Komai, K., Yamada, H., Yamazaki, F., Doi, M., Okamura, H., and Shiozawa, S. (2010) Mammalian clock gene Cryptochrome regulates arthritis via proinflammatory cytokine TNF-α. J. Immunol. 184, 1560-1565
23. Zhang, E. E., Liu, Y., Dentin, R., Pongsawakul, P. Y., Liu, A. C., Hirota, T., Nusinow, D. A., Sun, X., Landais, S., Kodama, Y., Brenner, D. A., Montminy, M., and Kay, S. A. (2010) Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis. Nat. Med. 16, 1152-1156
24. Doi, M., Takahashi, Y., Komatsu, R., Yamazaki, F., Yamada, H., Haraguchi, S., Emoto, N., Okuno, Y., Tsujimoto, G., Kanematsu, A., Ogawa, O., Todo, T., Tsutsui, K., van der Horst, G. T., and Okamura, H. (2010) Salt-sensitive hypertension in circadian clock-deficient Cry-null mice involves dysregulated adrenal Hsd3b6. Nat. Med. 16, 67-74
25. Katz, E. J., Isasa, M., and Crosas, B. (2010) A new map to understand deubiquitination. Biochem. Soc. Trans. 38, 21-28
26. Reyes-Turcu, F. E., Ventii, K. H., and Wilkinson, K. D. (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 78, 363-397
27. Sowa, M. E., Bennett, E. J., Gygi, S. P., and Harper, J. W. (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403
28. Sheng, Y., Saridakis, V., Sarkari, F., Duan, S., Wu, T., Arrowsmith, C. H., and Frappier, L. (2006) Molecular recognition of p53 and MDM2 by USP7/HAUSP. Nat. Struct. Mol. Biol. 13, 285-291 (Pubitemid 43348516)
29. van der Horst, A., de Vries-Smits, A. M., Brenkman, A. B., van Triest, M. H., van den Broek, N., Colland, F., Maurice, M. M., and Burgering, B. M. (2006) FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat. Cell Biol. 8, 1064-1073 (Pubitemid 44473601)
30. Mukai, A., Yamamoto-Hino, M., Awano, W., Watanabe, W., Komada, M., and Goto, S. (2010) Balanced ubiquitylation and deubiquitylation of Frizzled regulate cellular responsiveness to Wg/Wnt.EMBOJ. 29, 2114-2125
31. Ramakrishna, S., Suresh, B., and Baek, K. H. (2011) The role of deubiquitinating enzymes in apoptosis. Cell. Mol. Life Sci. 68, 15-26
32. Tauriello, D. V., Haegebarth, A., Kuper, I., Edelmann, M. J., Henraat, M., Canninga-van Dijk, M. R., Kessler, B. M., Clevers, H., and Maurice, M. M. (2010) Loss of the tumor suppressor CYLD enhances Wnt/β-catenin signaling through K63-linked ubiquitination of Dvl. Mol. Cell 37, 607-619
33. Zhao, B., Schlesiger, C., Masucci, M. G., and Lindsten, K. (2009) The ubiquitin-specific protease 4 (USP4) is a new player in the Wnt signaling pathway. J. Cell. Mol. Med. 13, 1886-1895
34. Stevenson, L. F., Sparks, A., Allende-Vega, N., Xirodimas, D. P., Lane, D. P., and Saville, M. K. (2007) The deubiquitinating enzyme USP2a regulates the p53 pathway by targeting Mdm2. EMBO J. 26, 976-986
35. Graner, E., Tang, D., Rossi, S., Baron, A., Migita, T., Weinstein, L. J., Lechpammer, M., Huesken, D., Zimmermann, J., Signoretti, S., and Loda, M. (2004) The isopeptidase USP2a regulates the stability of fatty acid synthase in prostate cancer. Cancer Cell 5, 253-261 (Pubitemid 38402117)
36. Shan, J., Zhao, W., and Gu, W. (2009) Suppression of cancer cell growth by promoting cyclin D1 degradation. Mol. Cell 36, 469-476
37. Allende-Vega, N., Sparks, A., Lane, D. P., and Saville, M. K. (2010) MdmX is a substrate for the deubiquitinating enzyme USP2a. Oncogene 29, 432-441
38. Gousseva, N., and Baker, R. T. (2003) Gene structure, alternate splicing, tissue distribution, cellular localization, and developmental expression pattern of mouse deubiquitinating enzyme isoforms Usp2-45 and Usp2-69. Gene Expr. 11, 163-179 (Pubitemid 37516649)
39. Wang, S., Wu, H., Liu, Y., Sun, J., Zhao, Z., Chen, Q., Guo, M., Ma, D., and Zhang, Z. (2010) Expression of USP2-69 in mesangial cells in vivo and in vitro. Pathol. Int. 60, 184-192
40. Haimerl, F., Erhardt, A., Sass, G., and Tiegs, G. (2009) Down-regulation of the deubiquitinating enzyme ubiquitin-specific protease 2 contributes to tumor necrosis factor-α-induced hepatocyte survival. J. Biol. Chem. 284, 495-504
41. Treeck, O., Lattrich, C., Juhasz-Boess, I., Buchholz, S., Pfeiler, G., and Ortmann, O. (2008) Adiponectin differentially affects gene expression in human mammary epithelial and breast cancer cells. Br. J. Cancer 99, 1246-1250
42. Sacco, J. J., Coulson, J. M., Clague, M. J., and Urbé, S. (2010) Emerging roles of deubiquitinases in cancer-associated pathways. IUBMB Life 62, 140-157
43. Priolo, C., Tang, D., Brahamandan, M., Benassi, B., Sicinska, E., Ogino, S., Farsetti, A., Porrello, A., Finn, S., Zimmermann, J., Febbo, P., and Loda, M. (2006) The isopeptidase USP2a protects human prostate cancer from apoptosis. Cancer Res. 66, 8625-8632 (Pubitemid 44449177)
44. Yang, Y., Hou, J. Q., Qu, L. Y., Wang, G. Q., Ju, H. W., Zhao, Z. W., Yu, Z. H., and Yang, H. J. (2007) Differential expression of USP2, USP14, and UBE4A between ovarian serous cystadenocarcinoma and adjacent normal tissues]. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 23, 504-506
45. 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
46. Oishi, K., Miyazaki, K., Kadota, K., Kikuno, R., Nagase, T., Atsumi, G., Ohkura, N., Azama, T., Mesaki, M., Yukimasa, S., Kobayashi, H., Iitaka, C., Umehara, T., Horikoshi, M., Kudo, T., Shimizu, Y., Yano, M., Monden, M., Machida, K., Matsuda, J., Horie, S., Todo, T., and Ishida, N. (2003) Genome- wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J. Biol. Chem. 278, 41519-41527 (Pubitemid 37280981)
47. Scoma, H. D., Humby, M., Yadav, G., Zhang, Q., Fogerty, J., and Besharse, J. C. (2011) The deubiquitinylating enzyme, USP2, is associated with the circadian clockwork and regulates its sensitivity to light. PLoS One 6, e25382
48. Balsalobre, A., Damiola, F., and Schibler, U. (1998) A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93, 929-937 (Pubitemid 28280787)
49. Tamanini, F. (2007) Manipulation of mammalian cell lines for circadian studies. Methods Mol. Biol. 362, 443-453
50. Yin, L., Wang, J., Klein, P. S., and Lazar, M. A. (2006) Nuclear receptor Rev-erbα is a critical lithium-sensitive component of the circadian clock. Science 311, 1002-1005 (Pubitemid 43271727)
51. Ruffieux-Daidié, D., Poirot, O., Boulkroun, S., Verrey, F., Kellenberger, S., and Staub, O. (2008) Deubiquitylation regulates activation and proteolytic cleavage of ENaC. J. Am. Soc. Nephrol. 19, 2170-2180
52. Shi, Y., Solomon, L. R., Pereda-Lopez, A., Giranda, V. L., Luo, Y., Johnson, E. F., Shoemaker, A. R., Leverson, J., and Liu, X. (2011) Ubiquitin-specific cysteine protease 2a (USP2a) regulates the stability of Aurora-A. J. Biol. Chem. 286, 38960-38968
53. Mahul-Mellier, A. L., Pazarentzos, E., Datler, C., Iwasawa, R., AbuAli, G., Lin, B., and Grimm, S. (2012) Deubiquitinating protease USP2a targets RIP1 and TRAF2 to mediate cell death by TNF. Cell Death Differ. 19, 891-899
54. Eide, E. J., Woolf, M. F., Kang, H., Woolf, P., Hurst, W., Camacho, F., Vielhaber, E. L., Giovanni, A., and Virshup, D. M. (2005) Control of mammalian circadian rhythm by CKIε-regulated proteasome-mediated PER2 degradation. Mol. Cell. Biol. 25, 2795-2807 (Pubitemid 40381641)
55. Sahar, S., Zocchi, L., Kinoshita, C., Borrelli, E., and Sassone-Corsi, P. (2010) Regulation of BMAL1 protein stability and circadian function by GSK3β-mediated phosphorylation. PLoS One 5, e8561
56. Shirogane, T., Jin, J., Ang, X. L., and Harper, J. W. (2005) SCFβ-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein. J. Biol. Chem. 280, 26863-26872 (Pubitemid 41040720)
57. Shearman, L. P., Zylka, M. J., Weaver, D. R., Kolakowski, L. F., Jr., and Reppert, S. M. (1997) Two period homologs. Circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron 19, 1261-1269 (Pubitemid 28030545)
58. Yagita, K., Tamanini, F., Yasuda, M., Hoeijmakers, J. H., van der Horst, G. T., and Okamura, H. (2002) Nucleocytoplasmic shuttling and mCRYdependent inhibition of ubiquitylation of the mPER2 clock protein.EMBO J. 21, 1301-1314 (Pubitemid 34246509)
59. Vitaterna, M. H., Selby, C. P., Todo, T., Niwa, H., Thompson, C., Fruechte, E. M., Hitomi, K., Thresher, R. J., Ishikawa, T., Miyazaki, J., Takahashi, J. S., and Sancar, A. (1999) Differential regulation of mammalian period genes and circadian rhythmicity by cryptochromes 1 and 2. Proc. Natl. Acad. Sci. U.S.A. 96, 12114-12119 (Pubitemid 29502867)
60. Chaves, I., Nijman, R. M., Biernat, M. A., Bajek, M. I., Brand, K., da Silva, A. C., Saito, S., Yagita, K., Eker, A. P., and van der Horst, G. T. (2011) The Potorous CPD photolyase rescues a cryptochrome-deficient mammalian circadian clock. PLoS One 6, e23447
61. Castanon-Cervantes, O., Wu, M., Ehlen, J. C., Paul, K., Gamble, K. L., Johnson, R. L., Besing, R. C., Menaker, M., Gewirtz, A. T., and Davidson, A. J. (2010) Dysregulation of inflammatory responses by chronic circadian disruption. J. Immunol. 185, 5796-5805
62. Cutolo, M., and Straub, R. H. (2008) Circadian rhythms in arthritis. Hormonal effects on the immune/inflammatory reaction. Autoimmun. Rev. 7, 223-228
63. Keller, M., Mazuch, J., Abraham, U., Eom, G. D., Herzog, E. D., Volk, H. D., Kramer, A., and Maier, B. (2009) A circadian clock in macrophages controls inflammatory immune responses. Proc. Natl. Acad. Sci. U.S.A. 106, 21407-21412
64. Sun, Y., Yang, Z., Niu, Z., Peng, J., Li, Q., Xiong, W., Langnas, A. N., Ma, M. Y., and Zhao, Y. (2006) MOP3, a component of the molecular clock, regulates the development of B cells. Immunology 119, 451-460 (Pubitemid 44722207)
65. Sun, Y., Yang, Z., Niu, Z., Wang, W., Peng, J., Li, Q., Ma, M. Y., and Zhao, Y. (2006) The mortality of MOP3-deficient mice with a systemic functional failure. J. Biomed. Sci. 13, 845-851 (Pubitemid 44900656)
66. Arjona, A., Boyadjieva, N., and Sarkar, D. K. (2004) Circadian rhythms of granzyme B, perforin, IFN-γ and NK cell cytolytic activity in the spleen. Effects of chronic ethanol. J. Immunol. 172, 2811-2817 (Pubitemid 38263665)
67. Arjona, A., and Sarkar, D. K. (2005) Circadian oscillations of clock genes, cytolytic factors, and cytokines in rat NK cells. J. Immunol. 174, 7618-7624 (Pubitemid 40806266)
68. Arjona, A., and Sarkar, D. K. (2006) Evidence supporting a circadian control of natural killer cell function. Brain Behav. Immun. 20, 469-476 (Pubitemid 44177763)
69. Cavadini, G., Petrzilka, S., Kohler, P., Jud, C., Tobler, I., Birchler, T., and Fontana, A. (2007) TNF-α suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc. Natl. Acad. Sci. U.S.A. 104, 12843-12848 (Pubitemid 47255242)
70. Petrzilka, S., Taraborrelli, C., Cavadini, G., Fontana, A., and Birchler, T. (2009) Clock gene modulation by TNF-α depends on calcium and p38 MAP kinase signaling. J. Biol. Rhythms 24, 283-294
71. Gallego, M., and Virshup, D. M. (2007) Post-translational modifications regulate the ticking of the circadian clock. Nat. Rev. Mol. Cell Biol. 8, 139-148 (Pubitemid 46432533)
72. Preitner, N., Damiola, F., Lopez-Molina, L., Zakany, J., Duboule, D., Albrecht, U., and Schibler, U. (2002) The orphan nuclear receptor REVERB α controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110, 251-260 (Pubitemid 34876552)
73. Ozturk, N., Selby, C. P., Annayev, Y., Zhong, D., and Sancar, A. (2011) Reaction mechanism of Drosophila cryptochrome. Proc. Natl. Acad. Sci. U.S.A. 108, 516-521
74. Metzig, M., Nickles, D., Falschlehner, C., Lehmann-Koch, J., Straub, B. K., Roth, W., and Boutros, M. (2011) An RNAi screen identifies USP2 as a factor required for TNF-α-induced NF-κB signaling. Int. J. Cancer 129, 607-618
75. Ando, H., Kumazaki, M., Motosugi, Y., Ushijima, K., Maekawa, T., Ishikawa, E., and Fujimura, A. (2011) Impairment of peripheral circadian clocks precedes metabolic abnormalities in ob/ob mice. Endocrinology 152, 1347-1354
76. Kaneko, K., Yamada, T., Tsukita, S., Takahashi, K., Ishigaki, Y., Oka, Y., and Katagiri, H. (2009) Obesity alters circadian expressions of molecular clock genes in the brainstem. Brain Res. 1263, 58-68
77. Kohsaka, A., Laposky, A. D., Ramsey, K. M., Estrada, C., Joshu, C., Kobayashi, Y., Turek, F. W., and Bass, J. (2007) High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 6, 414-421 (Pubitemid 350011997)