Interaction of circadian clock proteins CRY1 and PER2 is modulated by zinc binding and disulfide bond formation

Cell

Volumn 157, Issue 5, 2014, Pages 1203-1215

  Schmalen, Ira ^a   Reischl, Silke ^c   Wallach, Thomas ^c   Klemz, Roman ^c   Grudziecki, Astrid ^c   Prabu, J Rajan ^a   Benda, Christian ^a   Kramer, Achim ^c   Wolf, Eva ^a,b  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME 1; DISULFIDE; PER2 PROTEIN; PROTEIN BMAL1; TRANSCRIPTION FACTOR CLOCK; ZINC BINDING PROTEIN; ZINC ION; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; PROTEIN FBXL3; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL LYSATE; CELL METABOLISM; CIRCADIAN RHYTHM; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; HUMAN; HUMAN CELL; HYDROGEN BOND; IN VITRO STUDY; METABOLIC REGULATION; METAL BINDING; OXIDATION REDUCTION STATE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; U2OS CELL LINE; MOUSE; NONHUMAN; TRANSACTIVATION;

AMINO ACID SEQUENCE; ANIMALS; CRYPTOCHROMES; CRYSTALLOGRAPHY, X-RAY; F-BOX PROTEINS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PERIOD CIRCADIAN PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; ZINC;

EID: 84901358563     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.03.057     Document Type: Article

References (61)

1. D.S. Auld Zinc coordination sphere in biochemical zinc sites Biometals 14 2001 271 313 (Pubitemid 34066634)
2. J.L. Barclay, A. Shostak, A. Leliavski, A.H. Tsang, O. Jöhren, H. Müller-Fielitz, D. Landgraf, N. Naujokat, G.T.J. van der Horst, and H. Oster High-fat diet-induced hyperinsulinemia and tissue-specific insulin resistance in Cry-deficient mice Am. J. Physiol. Endocrinol. Metab. 304 2013 E1053 E1063
3. I. Chaves, K. Yagita, S. Barnhoorn, H. Okamura, G.T.J. van der Horst, and F. Tamanini 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 2006 1743 1753
4. A. Czarna, H. Breitkreuz, C.C. Mahrenholz, J. Arens, H.M. Strauss, and E. Wolf Quantitative analyses of cryptochrome-mBMAL1 interactions: mechanistic insights into the transcriptional regulation of the mammalian circadian clock J. Biol. Chem. 286 2011 22414 22425
5. A. Czarna, A. Berndt, H.R. Singh, A. Grudziecki, A.G. Ladurner, G. Timinszky, A. Kramer, and E. Wolf Structures of Drosophila cryptochrome and mouse cryptochrome1 provide insight into circadian function Cell 153 2013 1394 1405
6. K. Eckel-Mahan, and P. Sassone-Corsi Metabolism control by the circadian clock and vice versa Nat. Struct. Mol. Biol. 16 2009 462 467
7. R.S. Edgar, E.W. Green, Y. Zhao, G. van Ooijen, M. Olmedo, X. Qin, Y. Xu, M. Pan, U.K. Valekunja, and K.A. Feeney et al. Peroxiredoxins are conserved markers of circadian rhythms Nature 485 2012 459 464
8. E.J. Eide, E.L. Vielhaber, W.A. Hinz, and D.M. Virshup The circadian regulatory proteins BMAL1 and cryptochromes are substrates of casein kinase Iepsilon J. Biol. Chem. 277 2002 17248 17254 (Pubitemid 34967759)
9. J.C. Evans, D.P. Huddler, J. Jiracek, C. Castro, N.S. Millian, T.A. Garrow, and M.L. Ludwig Betaine-homocysteine methyltransferase: zinc in a distorted barrel Structure 10 2002 1159 1171 (Pubitemid 35254005)
10. D. Gatfield, and U. Schibler Physiology. Proteasomes keep the circadian clock ticking Science 316 2007 1135 1136 (Pubitemid 46880958)
11. E.A. Griffin Jr., D. Staknis, and C.J. Weitz Light-independent role of CRY1 and CRY2 in the mammalian circadian clock Science 286 1999 768 771
12. 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
13. T. Hirota, J.W. Lee, P.C. St John, M. Sawa, K. Iwaisako, T. Noguchi, P.Y. Pongsawakul, T. Sonntag, D.K. Welsh, and D.A. Brenner et al. Identification of small molecule activators of cryptochrome Science 337 2012 1094 1097
14. K. Hitomi, L. DiTacchio, A.S. Arvai, J. Yamamoto, S.-T. Kim, T. Todo, J.A. Tainer, S. Iwai, S. Panda, and E.D. Getzoff Functional motifs in the (6-4) photolyase crystal structure make a comparative framework for DNA repair photolyases and clock cryptochromes Proc. Natl. Acad. Sci. USA 106 2009 6962 6967
15. N. Huang, Y. Chelliah, Y. Shan, C.A. Taylor, S.-H. Yoo, C. Partch, C.B. Green, H. Zhang, and J.S. Takahashi Crystal structure of the heterodimeric CLOCK:BMAL1 transcriptional activator complex Science 337 2012 189 194
16. M. Ilbert, P.C. Graf, and U. Jakob Zinc center as redox switch - new function for an old motif Antioxid. Redox Signal. 8 2006 835 846 (Pubitemid 44036501)
17. D.P. King, M.H. Vitaterna, A.M. Chang, W.F. Dove, L.H. Pinto, F.W. Turek, and J.S. Takahashi The mouse Clock mutation behaves as an antimorph and maps within the W19H deletion, distal of Kit Genetics 146 1997 1049 1060 (Pubitemid 27290987)
18. N. Koike, S.-H. Yoo, H.-C. Huang, V. Kumar, C. Lee, T.-K. Kim, and J.S. Takahashi Transcriptional architecture and chromatin landscape of the core circadian clock in mammals Science 338 2012 349 354
19. N. Kucera, I. Schmalen, S. Hennig, R. Öllinger, H.M. Strauss, A. Grudziecki, C. Wieczorek, A. Kramer, and E. Wolf Unwinding the differences of the mammalian PERIOD clock proteins from crystal structure to cellular function Proc. Natl. Acad. Sci. USA 109 2012 3311 3316
20. K. Kume, M.J. Zylka, S. Sriram, L.P. Shearman, D.R. Weaver, X. Jin, E.S. Maywood, M.H. Hastings, and S.M. Reppert mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop Cell 98 1999 193 205 (Pubitemid 29344907)
21. 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 et al. AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation Science 326 2009 437 440
22. K.A. Lamia, S.J. Papp, R.T. Yu, G.D. Barish, N.H. Uhlenhaut, J.W. Jonker, M. Downes, and R.M. Evans Cryptochromes mediate rhythmic repression of the glucocorticoid receptor Nature 480 2011 552 556
23. B. Marcheva, K.M. Ramsey, E.D. Buhr, Y. Kobayashi, H. Su, C.H. Ko, G. Ivanova, C. Omura, S. Mo, and M.H. Vitaterna et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes Nature 466 2010 627 631
24. W. Maret New perspectives of zinc coordination environments in proteins J. Inorg. Biochem. 111 2012 110 116
25. K. Miyazaki, M. Mesaki, and N. Ishida Nuclear entry mechanism of rat PER2 (rPER2): role of rPER2 in nuclear localization of CRY protein Mol. Cell. Biol. 21 2001 6651 6659 (Pubitemid 32927431)
26. M. Müller, and T. Carell Structural biology of DNA photolyases and cryptochromes Curr. Opin. Struct. Biol. 19 2009 277 285
27. J.S. O'Neill, and A.B. Reddy Circadian clocks in human red blood cells Nature 469 2011 498 503
28. J.S. O'Neill, G. van Ooijen, L.E. Dixon, C. Troein, F. Corellou, F.-Y. Bouget, A.B. Reddy, and A.J. Millar Circadian rhythms persist without transcription in a eukaryote Nature 469 2011 554 558
29. S. Okano, M. Akashi, K. Hayasaka, and O. Nakajima Unusual circadian locomotor activity and pathophysiology in mutant CRY1 transgenic mice Neurosci. Lett. 451 2009 246 251
30. S. Okano, K. Hayasaka, M. Igarashi, H. Iwai, Y. Togashi, and O. Nakajima Non-obese early onset diabetes mellitus in mutant cryptochrome1 transgenic mice Eur. J. Clin. Invest. 40 2010 1011 1017
31. S. Okano, K. Hayasaka, M. Igarashi, Y. Togashi, and O. Nakajima Characterization of age-associated alterations of islet function and structure in diabetic mutant cryptochrome 1 transgenic mice J. Diabetes Investigation 4 2013 428 435
32. P.I. Oteiza Zinc and the modulation of redox homeostasis Free Radic. Biol. Med. 53 2012 1748 1759
33. N. Ozber, I. Baris, G. Tatlici, I. Gur, S. Kilinc, E.B. Unal, and I.H. Kavakli Identification of two amino acids in the C-terminal domain of mouse CRY2 essential for PER2 interaction BMC Mol. Biol. 11 2010 69
34. D.J. Templeton, M.-S. Aye, J. Rady, F. Xu, and J.V. Cross Purification of reversibly oxidized proteins (PROP) reveals a redox switch controlling p38 MAP kinase activity PLoS ONE 5 2010 e15012
35. T. Tomita, K. Miyazaki, Y. Onishi, S. Honda, N. Ishida, and K. Oishi Conserved amino acid residues in C-terminus of PERIOD 2 are involved in interaction with CRYPTOCHROME 1 Biochim. Biophys. Acta 1803 2010 492 498
36. 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 et al. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms Nature 398 1999 627 630 (Pubitemid 29183691)
37. T.A. Wang, Y.V. Yu, G. Govindaiah, X. Ye, L. Artinian, T.P. Coleman, J.V. Sweedler, C.L. Cox, and M.U. Gillette Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons Science 337 2012 839 842
38. J.R. Weir, F. Bonneau, J. Hentschel, and E. Conti Structural analysis reveals the characteristic features of Mtr4, a DExH helicase involved in nuclear RNA processing and surveillance Proc. Natl. Acad. Sci. USA 107 2010 12139 12144
39. H.H. Wu, J.A. Thomas, and J. Momand p53 protein oxidation in cultured cells in response to pyrrolidine dithiocarbamate: a novel method for relating the amount of p53 oxidation in vivo to the regulation of p53-responsive genes Biochem. J. 351 2000 87 93
40. W. Xing, L. Busino, T.R. Hinds, S.T. Marionni, N.H. Saifee, M.F. Bush, M. Pagano, and N. Zheng SCF(FBXL3) ubiquitin ligase targets cryptochromes at their cofactor pocket Nature 496 2013 64 68
41. K. Yagita, F. Tamanini, M. Yasuda, J.H.J. Hoeijmakers, G.T.J. 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 (Pubitemid 34246509)
42. R. Ye, C.P. Selby, N. Ozturk, Y. Annayev, and A. Sancar Biochemical analysis of the canonical model for the mammalian circadian clock J. Biol. Chem. 286 2011 25891 25902
43. S.-H. Yoo, J.A. Mohawk, S.M. Siepka, Y. Shan, S.K. Huh, H.-K. Hong, I. Kornblum, V. Kumar, N. Koike, and M. Xu et al. Competing E3 ubiquitin ligases govern circadian periodicity by degradation of CRY in nucleus and cytoplasm Cell 152 2013 1091 1105
44. M.W. Young, and S.A. Kay Time zones: a comparative genetics of circadian clocks Nat. Rev. Genet. 2 2001 702 715 (Pubitemid 33674792)
45. E.E. Zhang, Y. Liu, R. Dentin, P.Y. Pongsawakul, A.C. Liu, T. Hirota, D.A. Nusinow, X. Sun, S. Landais, and Y. Kodama et al. Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis Nat. Med. 16 2010 1152 1156
46. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
47. T.M. Bergfors Protein Crystallization: Techniques, Strategies, and Tips Second Edition 2009 International University Line La Jolla, CA
48. K. Cowtan The Buccaneer software for automated model building. 1. Tracing protein chains Acta Crystallogr. D Biol. Crystallogr. 62 2006 1002 1011 (Pubitemid 44337374)
49. J.J.R.F. da Silva, and R.J.P. Williams The Biological Chemistry of the Elements 2001 Oxford University Press Oxford
50. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
51. M. Goujon, H. McWilliam, W. Li, F. Valentin, S. Squizzato, J. Paern, and R. Lopez A new bioinformatics analysis tools framework at EMBL-EBI Nucleic Acids Res. 38 Web Server issue 2010 W695 W699
52. W. Kabsch Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Cryst. 26 1993 795 800
53. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797 (Pubitemid 47321791)
54. B. Maier, S. Wendt, J.T. Vanselow, T. Wallach, S. Reischl, S. Oehmke, A. Schlosser, and A. Kramer A large-scale functional RNAi screen reveals a role for CK2 in the mammalian circadian clock Genes Dev. 23 2009 708 718
55. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674 (Pubitemid 47080256)
56. R.D. Palmiter, and S.D. Findley Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc EMBO J. 14 1995 639 649
57. S.E. Pattison, and R.J. Cousins Kinetics of zinc uptake and exchange by primary cultures of rat hepatocytes Am. J. Physiol. 250 1986 E677 E685
58. S.W. Provencher, and J. Glöckner Estimation of globular protein secondary structure from circular dichroism Biochemistry 20 1981 33 37
59. F. Sievers, A. Wilm, D. Dineen, T.J. Gibson, K. Karplus, W. Li, R. Lopez, H. McWilliam, M. Remmert, and J. Söding et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega Mol. Syst. Biol. 7 2011 539
60. T.C. Terwilliger, P.D. Adams, R.J. Read, A.J. McCoy, N.W. Moriarty, R.W. Grosse-Kunstleve, P.V. Afonine, P.H. Zwart, and L.W. Hung Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard Acta Crystallogr. D Biol. Crystallogr. 65 2009 582 601
61. A.M. Waterhouse, J.B. Procter, D.M.A. Martin, M. Clamp, and G.J. Barton Jalview Version 2 - a multiple sequence alignment editor and analysis workbench Bioinformatics 25 2009 1189 1191