Phosphorylation of the cryptochrome 1 C-terminal tail regulates circadian period length

Journal of Biological Chemistry

Volumn 288, Issue 49, 2013, Pages 35277-35286

  Gao, Peng ^a   Yoo, Seung Hee ^a,b   Lee, Kyung Jong ^a   Rosensweig, Clark ^a   Takahashi, Joseph S ^a   Chen, Benjamin P ^a   Green, Carla B ^a  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL TAIL; CIRCADIAN CLOCK; CRITICAL COMPONENT; DNA-DEPENDENT PROTEIN KINASE; DNA-REPAIR ENZYMES; PERIOD LENGTH; PHOSPHORYLATION SITES; TRANSCRIPTIONAL REPRESSORS;

ENZYMES;

PHOSPHORYLATION;

CRYPTOCHROME 1; DNA DEPENDENT PROTEIN KINASE; F BOX PROTEIN; PROTEIN BMAL1; PROTEIN FBXL3; SERINE; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCADIAN RHYTHM; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; STRUCTURE ACTIVITY RELATION;

CIRCADIAN CLOCK; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STABILITY; TRANSCRIPTION REPRESSOR;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; CIRCADIAN CLOCKS; CRYPTOCHROMES; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; GENE KNOCKOUT TECHNIQUES; HEK293 CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SERINE;

EID: 84890287542     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.509604     Document Type: Article

References (69)

1. Mohawk, J. A., Green, C. B., and Takahashi, J. S. (2012) Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35, 445-462
2. Lowrey, P. L., and Takahashi, J. S. (2011) Genetics of circadian rhythms in Mammalian model organisms. Adv. Genet. 74, 175-230
3. 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
4. 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
5. Zhu, H., Conte, F., and Green, C. B. (2003) Nuclear localization and transcriptional repression are confined to separable domains in the circadian protein CRYPTOCHROME. Curr. Biol. 13, 1653-1658
6. Khan, S. K., Xu, H., Ukai-Tadenuma, M., Burton, B., Wang, Y., Ueda, H. R., and Liu, A. C. (2012) Identification of a novel cryptochrome differentiating domain required for feedback repression in circadian clock function. J. Biol. Chem. 287, 25917-25926
7. Chaves, I., Yagita, K., Barnhoorn, S., Okamura, H., van der Horst, G. T., and Tamanini, F. (2006) Functional evolution of the photolyase/cryptochrome protein family. Importance of the C terminus of mammalian CRY1 for circadian core oscillator performance. Mol. Cell. Biol. 26, 1743-1753
8. Czarna, A., Breitkreuz, H., Mahrenholz, C. C., Arens, J., Strauss, H. M., and Wolf, E. (2011) Quantitative analyses of cryptochrome-mBMAL1 interactions. Mechanistic insights into the transcriptional regulation of the mammalian circadian clock. J. Biol. Chem. 286, 22414-22425
9. Kurabayashi, N., Hirota, T., Sakai, M., Sanada, K., and Fukada, Y. (2010) DYRK1A and glycogen synthase kinase 3-, a dual-kinase mechanism directing proteasomal degradation of CRY2 for circadian timekeeping. Mol. Cell. Biol. 30, 1757-1768
10. 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-3-. J. Biol. Chem. 280, 31714-31721
11. Dissel, S., Codd, V., Fedic, R., Garner, K. J., Costa, R., Kyriacou, C. P., and Rosato, E. (2004) A constitutively active cryptochrome in Drosophila melanogaster. Nat. Neurosci. 7, 834-840
12. Rosato, E., Codd, V., Mazzotta, G., Piccin, A., Zordan, M., Costa, R., and Kyriacou, C. P. (2001) Light-dependent interaction between Drosophila CRY and the clock protein PER mediated by the carboxy terminus of CRY. Curr. Biol. 11, 909-917
13. Czarna, A., Berndt, A., Singh, H. R., Grudziecki, A., Ladurner, A. G., Timinszky, G., Kramer, A., and Wolf, E. (2013) Structures of Drosophila cryptochrome and mouse cryptochrome1 provide insight into circadian function. Cell 153, 1394-1405
14. Levy, C., Zoltowski, B. D., Jones, A. R., Vaidya, A. T., Top, D., Widom, J., Young, M. W., Scrutton, N. S., Crane, B. R., and Leys, D. (2013) Updated structure of Drosophila cryptochrome. Nature 495, E3-E4
15. Zoltowski, B. D., Vaidya, A. T., Top, D., Widom, J., Young, M. W., and Crane, B. R. (2011) Structure of full-length Drosophila cryptochrome. Nature 480, 396-399
16. Xing, W., Busino, L., Hinds, T. R., Marionni, S. T., Saifee, N. H., Bush, M. F., Pagano, M., and Zheng, N. (2013) SCF(FBXL3) ubiquitin ligase targets cryptochromes at their cofactor pocket. Nature 496, 64-68
17. 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
18. 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., Nussbaum, J., Liu, X., Chen, Z., Chen, Z. J., Green, C. B., and Takahashi, J. S. (2013) Competing E3 ubiquitin ligases govern circadian periodicity by degradation of CRY in nucleus and cytoplasm. Cell 152, 1091-1105
19. 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
20. 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
21. Hirano, A., Yumimoto, K., Tsunematsu, R., Matsumoto, M., Oyama, M., Kozuka-Hata, H., Nakagawa, T., Lanjakornsiripan, D., Nakayama, K. I., and Fukada, Y. (2013) FBXL21 regulates oscillation of the circadian clock through ubiquitination and stabilization of cryptochromes. Cell 152, 1106-1118
22. 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
23. 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
24. Yoo, S. H., Ko, C. H., Lowrey, P. L., Buhr, E. D., Song, E. J., Chang, S., Yoo, O. J., Yamazaki, S., Lee, C., and Takahashi, J. S. (2005) A noncanonical E-box enhancer drives mouse Period2 circadian oscillations in vivo. Proc. Natl. Acad. Sci. U.S.A. 102, 2608-2613
25. Chen, Z., Yoo, S. H., Park, Y. S., Kim, K. H., Wei, S., Buhr, E., Ye, Z. Y., Pan, H. L., and Takahashi, J. S. (2012) Identification of diverse modulators of central and peripheral circadian clocks by high-throughput chemical screening. Proc. Natl. Acad. Sci. U.S.A. 109, 101-106
26. Yamazaki, S., and Takahashi, J. S. (2005) Real-time luminescence reporting of circadian gene expression in mammals. Methods Enzymol. 393, 288-301
27. McCarthy, E. V., Baggs, J. E., Geskes, J. M., Hogenesch, J. B., and Green, C. B. (2009) Generation of a novel allelic series of cryptochrome mutants via mutagenesis reveals residues involved in protein-protein interaction and CRY2-specific repression. Mol. Cell. Biol. 29, 5465-5476
28. Peng, Y., Zhang, Q., Nagasawa, H., Okayasu, R., Liber, H. L., and Bedford, J. S. (2002) Silencing expression of the catalytic subunit of DNA-dependent protein kinase by small interfering RNA sensitizes human cells for radiation-induced chromosome damage, cell killing, and mutation. Cancer Res. 62, 6400-6404
29. Lavery, D. J., and Schibler, U. (1993) Circadian transcription of the cholesterol 7a hydroxylase gene may involve the liver-enriched bZIP protein DBP. Genes Dev. 7, 1871-1884
30. 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
31. Davis, A. J., Lee, K. J., and Chen, D. J. (2013) The N-terminal region of the DNA-dependent protein kinase catalytic subunit is required for its DNA double-stranded break-mediated activation. J. Biol. Chem. 288, 7037-7046
32. 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
33. Sun, Z. S., Albrecht, U., Zhuchenko, O., Bailey, J., Eichele, G., and Lee, C. C. (1997) RIGUI, a putative mammalian ortholog of the Drosophila period gene. Cell 90, 1003-1011
34. Robles, M. S., Boyault, C., Knutti, D., Padmanabhan, K., and Weitz, C. J. (2010) Identification of RACK1 and protein kinase C- as integral components of the mammalian circadian clock. Science 327, 463-466
35. Tei, H., Okamura, H., Shigeyoshi, Y., Fukuhara, C., Ozawa, R., Hirose, M., and Sakaki, Y. (1997) Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 389, 512-516
36. Kume, K., Zylka, M. J., Sriram, S., Shearman, L. P., Weaver, D. R., Jin, X., Maywood, E. S., Hastings, M. H., and Reppert, S. M. (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98, 193-205
37. Abraham, R. T. (2004) PI 3-kinase related kinases. "Big" players in stressinduced signaling pathways. DNA Repair 3, 883-887
38. Weterings, E., and Chen, D. J. (2008) The endless tale of non-homologous end-joining. Cell Res. 18, 114-124
39. Wong, R. H., Chang, I., Hudak, C. S., Hyun, S., Kwan, H. Y., and Sul, H. S. (2009) A role of DNA-PK for the metabolic gene regulation in response to insulin. Cell 136, 1056-1072
40. Liiv, I., Rebane, A., Org, T., Saare, M., Maslovskaja, J., Kisand, K., Juronen, E., Valmu, L., Bottomley, M. J., Kalkkinen, N., and Peterson, P. (2008) DNA-PK contributes to the phosphorylation of AIRE. Importance in transcriptional activity. Biochim. Biophys. Acta 1783, 74-83
41. Lai, J. S., and Herr, W. (1992) Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc. Natl. Acad. Sci. U.S.A. 89, 6958-6962
42. Leahy, J. J., Golding, B. T., Griffin, R. J., Hardcastle, I. R., Richardson, C., Rigoreau, L., and Smith, G. C. (2004) Identification of a highly potent and selective DNA-dependent protein kinase (DNA-PK) inhibitor (NU7441) by screening of chromenone libraries. Bioorg. Med. Chem. Lett. 14, 6083-6087
43. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R., 3rd, Hurov, K. E., Luo, J., Bakalarski, C. E., Zhao, Z., Solimini, N., Lerenthal, Y., Shiloh, Y., Gygi, S. P., and Elledge, S. J. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166
44. Harms, E., Kivimäe, S., Young, M. W., and Saez, L. (2004) Posttranscriptional and posttranslational regulation of clock genes. J. Biol. Rhythms 19, 361-373
45. Mehra, A., Baker, C. L., Loros, J. J., and Dunlap, J. C. (2009) Post-translational modifications in circadian rhythms. Trends Biochem. Sci. 34, 483-490
46. Vanselow, K., Vanselow, J. T., Westermark, P. O., Reischl, S., Maier, B., Korte, T., Herrmann, A., Herzel, H., Schlosser, A., and Kramer, A. (2006) Differential effects of PER2 phosphorylation. Molecular basis for the human familial advanced sleep phase syndrome (FASPS). Genes Dev. 20, 2660-2672
47. Huang, G., Chen, S., Li, S., Cha, J., Long, C., Li, L., He, Q., and Liu, Y. (2007) Protein kinase A and casein kinases mediate sequential phosphorylation events in the circadian negative feedback loop. Genes Dev. 21, 3283-3295
48. Bauer, P. M., Fulton, D., Boo, Y. C., Sorescu, G. P., Kemp, B. E., Jo, H., and Sessa, W. C. (2003) Compensatory phosphorylation and protein-protein interactions revealed by loss of function and gain of function mutants of multiple serine phosphorylation sites in endothelial nitric-oxide synthase. J. Biol. Chem. 278, 14841-14849
49. Zheng, Y. L., Li, B. S., Rudrabhatla, P., Shukla, V., Amin, N. D., Maric, D., Kesavapany, S., Kanungo, J., Pareek, T. K., Takahashi, S., Grant, P., Kulkarni, A. B., and Pant, H. C. (2010) Phosphorylation of p27Kip1 at Thr187 by cyclin-dependent kinase 5 modulates neural stem cell differentiation. Mol. Biol. Cell 21, 3601-3614
50. Schwarz, E. M., Van Antwerp, D., and Verma, I. M. (1996) Constitutive phosphorylation of I-B- by casein kinase II occurs preferentially at serine 293. Requirement for degradation of free I-B-. Mol. Cell. Biol. 16, 3554-3559
51. Preuss, F., Fan, J. Y., Kalive, M., Bao, S., Schuenemann, E., Bjes, E. S., and Price, J. L. (2004) Drosophila doubletime mutations which either shorten or lengthen the period of circadian rhythms decrease the protein kinase activity of casein kinase I. Mol. Cell. Biol. 24, 886-898
52. Fan, J. Y., Preuss, F., Muskus, M. J., Bjes, E. S., and Price, J. L. (2009) Drosophila and vertebrate casein kinase I- exhibits evolutionary conservation of circadian function. Genetics 181, 139-152
53. Douglas, P., Zhong, J., Ye, R., Moorhead, G. B., Xu, X., and Lees-Miller, S. P. (2010) Protein phosphatase 6 interacts with the DNA-dependent protein kinase catalytic subunit and dephosphorylates -H2AX. Mol. Cell. Biol. 30, 1368-1381
54. Mi, J., Dziegielewski, J., Bolesta, E., Brautigan, D. L., and Larner, J. M. (2009) Activation of DNA-PK by ionizing radiation is mediated by protein phosphatase PLoS One 4, e4395
55. Wechsler, T., Chen, B. P., Harper, R., Morotomi-Yano, K., Huang, B. C., Meek, K., Cleaver, J. E., Chen, D. J., and Wabl, M. (2004) DNA-PKcs function regulated specifically by protein phosphatase Proc. Natl. Acad. Sci. U.S.A. 101, 1247-1252
56. Partch, C. L., Shields, K. F., Thompson, C. L., Selby, C. P., and Sancar, A. (2006) Posttranslational regulation of the mammalian circadian clock by cryptochrome and protein phosphatase 5. Proc. Natl. Acad. Sci. U.S.A. 103, 10467-10472
57. Zhao, S., and Sancar, A. (1997) Human blue-light photoreceptor hCRY2 specifically interacts with protein serine/threonine phosphatase 5 and modulates its activity. Photochem. Photobiol. 66, 727-731
58. Lee, H. M., Chen, R., Kim, H., Etchegaray, J. P., Weaver, D. R., and Lee, C. (2011) The period of the circadian oscillator is primarily determined by the balance between casein kinase 1 and protein phosphatase 1. Proc. Natl. Acad. Sci. U.S.A. 108, 16451-16456
59. Amatya, P. N., Kim, H. B., Park, S. J., Youn, C. K., Hyun, J. W., Chang, I. Y., Lee, J. H., and You, H. J. (2012) A role of DNA-dependent protein kinase for the activation of AMP-activated protein kinase in response to glucose deprivation. Biochim. Biophys. Acta 1823, 2099-2108
60. Ruis, B. L., Fattah, K. R., and Hendrickson, E. A. (2008) The catalytic subunit of DNA-dependent protein kinase regulates proliferation, telomere length, and genomic stability in human somatic cells. Mol. Cell. Biol. 28, 6182-6195
61. Brumbaugh, K. M., Otterness, D. M., Geisen, C., Oliveira, V., Brognard, J., Li, X., Lejeune, F., Tibbetts, R. S., Maquat, L. E., and Abraham, R. T. (2004) The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells. Mol. Cell 14, 585-598
62. Gehring, W., and Rosbash, M. (2003) The coevolution of blue-light photoreception and circadian rhythms. J. Mol. Evol. 57, S286-S289
63. Gorbacheva, V. Y., Kondratov, R. V., Zhang, R., Cherukuri, S., Gudkov, A. V., Takahashi, J. S., and Antoch, M. P. (2005) Circadian sensitivity to the chemotherapeutic agent cyclophosphamide depends on the functional status of the CLOCK/BMAL1 transactivation complex. Proc. Natl. Acad. Sci. U.S.A. 102, 3407-3412
64. Fu, L., Pelicano, H., Liu, J., Huang, P., and Lee, C. (2002) The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 111, 41-50
65. Gery, S., Komatsu, N., Baldjyan, L., Yu, A., Koo, D., and Koeffler, H. P. (2006) The circadian gene per1 plays an important role in cell growth and DNA damage control in human cancer cells. Mol. Cell 22, 375-382
66. Cotta-Ramusino, C., McDonald, E. R., 3rd, Hurov, K., Sowa, M. E., Harper, J. W., and Elledge, S. J. (2011) A DNA damage response screen identifies RHINO, a 9-1-1 and TopBP1 interacting protein required for ATR signaling. Science 332, 1313-1317
67. Oklejewicz, M., Destici, E., Tamanini, F., Hut, R. A., Janssens, R., and van der Horst, G. T. (2008) Phase resetting of the mammalian circadian clock by DNA damage. Curr. Biol. 18, 286-291
68. Tamanini, F., Chaves, I., Bajek, M. I., and van der Horst, G. T. (2007) Structure function analysis of mammalian cryptochromes. Cold Spring Harb. Symp. Quant. Biol. 72, 133-139
69. 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