Role of structural plasticity in signal transduction by the cryptochrome blue-light photoreceptor

Biochemistry

Volumn 44, Issue 10, 2005, Pages 3795-3805

  Partch, Carrie L ^a   Clarkson, Michael W ^a,c   Özgür, Sezgin ^a   Lee, Andrew L ^a,b   Sancar, Aziz ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROMES; PHOTOLYASES; PHOTORECEPTORS; PHOTOTRANSDUCTION;

AMINO ACIDS; DNA; ENZYMES; PLASTICITY; PROTEINS; REDOX REACTIONS;

CHROMOSOMES;

ARABIDOPSIS PROTEIN; CRYPTOCHROME; CRYPTOCHROME 1; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; VEGETABLE PROTEIN;

ARTICLE; BLUE LIGHT; CHEMICAL ANALYSIS; LIGHT EXPOSURE; NONHUMAN; PHOTORECEPTOR; PHOTOTRANSDUCTION; PLASTICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS PROTEINS; CIRCULAR DICHROISM; COMPUTATIONAL BIOLOGY; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DROSOPHILA PROTEINS; FLAVOPROTEINS; HUMANS; HYDROLYSIS; LIGHT; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PHOTORECEPTORS, VERTEBRATE; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP; TRYPSIN;

ANIMALIA; ARABIDOPSIS;

EID: 14844355899     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047545g     Document Type: Article

References (71)

1. Nikaido, S. S., and Johnson, C. H. (2000) Daily and circadian variation in survival from ultraviolet radiation in Chlamydomonas reinhardtii, Photochem. Photobiol. 71, 758-65.
2. DeCoursey, P. J., Krulas, J. R., Mele, G., and Holley, D. C. (1997) Circadian performance of suprachiasmatic nuclei (SCN)-lesioned antelope ground squirrels in a desert enclosure, Physiol. Behav. 62, 1099-108.
3. DeCoursey, P. J., and Krulas, J. R. (1998) Behavior of SCN-lesioned chipmunks in natural habitat: a pilot study, J. Biol. Rhythms 13, 229-44.
4. Mitsui, A., Kumazawa, S., Takahashi, A., Ikemoto, H., and Arai, T. (1986) Strategy by which nitrogen-fixing unicellular cyanobacteria can grow photo-autotrophically, Nature 323, 720-722.
5. Gehring, W., and Rosbash, M. (2003) The coevolution of blue-light photoreception and circadian rhythms, J. Mol. Evol. 57 (Suppl. 1), S286-9.
6. Ragni, M. a. R. D. A., M. (2004) Light as an information carrier underwater, J. Plankton Res. 26, 433-443.
7. van der Horst, M. A., and Hellingwerf, K. J. (2004) Photoreceptor proteins, "star actors of modern times": a review of the functional dynamics in the structure of representative members of six different photoreceptor families, Acc. Chem. Res. 37, 13-20.
8. Ahmad, M., and Cashmore, A. R. (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor, Nature 366, 162-6.
9. Lin, C., Robertson, D. E., Ahmad, M., Raibekas, A. A., Jorns, M. S., Dutton, P. L., and Cashmore, A. R. (1995) Association of flavin adenine dinucleotide with the Arabidopsis blue light receptor CRY1, Science 269, 968-70.
10. Malhotra, K., Kim, S. T., Batschauer, A., Dawut, L., and Sancar, A. (1995) Putative blue-light photoreceptors from Arabidopsis thaliana and Sinapis alba with a high degree of sequence homology to DNA photolyase contain the two photolyase cofactors but lack DNA repair activity, Biochemistry 34, 6892-9.
11. Hsu, D. S., Zhao, X., Zhao, S., Kazantsev, A., Wang, R. P., Todo, T., Wei, Y. F., and Sancar, A. (1996) Putative human blue-light photoreceptors hCRY1 and hCRY2 are flavoproteins, Biochemistry 35, 13871-7.
12. Cashmore, A. R. (2003) Cryptochromes: enabling plants and animals to determine circadian time, Cell 114, 537-43.
13. Sancar, A. (2003) Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors, Chem. Rev. 103, 2203-37.
14. Park, H. W., Kim, S. T., Sancar, A., and Deisenhofer, J. (1995) Crystal structure of DNA photolyase from Escherichia coli, Science 268, 1866-72.
15. Tamada, T., Kitadokoro, K., Higuchi, Y., Inaka, K., Yasui, A., de Ruiter, P. E., Eker, A. P., and Miki, K. (1997) Crystal structure of DNA photolyase from Anacystis nidulans, Nat. Struct. Biol. 4, 887-91.
16. Komori, H., Masui, R., Kuramitsu, S., Yokoyama, S., Shibata, T., Inoue, Y., and Miki, K. (2001) Crystal structure of thermostable DNA photolyase: pyrimidine-dimer recognition mechanism, Proc. Natl. Acad. Sci. U.S.A. 98, 13560-5.
17. Brudler, R., Hitomi, K., Daiyasu, H., Toh, H., Kucho, K., Ishiura, M., Kanehisa, M., Roberts, V. A., Todo, T., Tainer, J. A., and Getzoff, E. D. (2003) Identification of a new cryptochrome class. Structure, function, and evolution, Mol. Cell 11, 59-67.
18. Brautigam, C. A., Smith, B. S., Ma, Z., Palnitkar, M., Tomchick, D. R., Machius, M., and Deisenhofer, J. (2004) Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana, Proc. Natl. Acad. Sci. U.S.A. 101, 12142-7.
19. Lin, C., and Shalitin, D. (2003) Cryptochrome Structure and Signal Transduction, Annu. Rev. Plant Physiol. Plant Mol. Biol. 54, 469-496.
20. Yang, H. Q., Wu, Y. J., Tang, R. H., Liu, D., Liu, Y., and Cashmore, A. R. (2000) The C termini of Arabidopsis cryptochromes mediate a constitutive light response, Cell 103, 815-27.
21. Wang, H., Ma, L. G., Li, J. M., Zhao, H. Y., and Deng, X. W. (2001) Direct interaction of Arabidopsis cryptochromes with COP1 in light control development, Science 294, 154-8.
22. Yang, H. Q., Tang, R. H., and Cashmore, A. R. (2001) The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1, Plant Cell 13, 2573-87.
23. Lin, F. J., Song, W., Meyer-Bernstein, E., Naidoo, N., and Sehgal, A. (2001) Photic signaling by cryptochrome in the Drosophila circadian system. Mol. Cell. Biol. 21, 7287-94.
24. 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, 909-17.
25. Busza, A., Emery-Le, M., Rosbash, M., and Emery, P. (2004) Roles of the two Drosophila CRYPTOCHROME structural domains in circadian photoreception, Science 304, 1503-6.
26. 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, 834-40.
27. Özgür, S., and Sancar, A. (2003) Purification and properties of human blue-light photoreceptor cryptochrome 2, Biochemistry 42, 2926-32.
28. Farrow, N. A., Muhandiram, R., Singer, A. U., Pascal, S. M., Kay, C. M., Gish, G., Shoelson, S. E., Pawson, T., Forman-Kay, J. D., and Kay, L. E. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation, Biochemistry 33, 5984-6003.
29. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-93.
30. Johnson, B. A., and Blevins, R. A. (1994) NMRView: A computer program for the visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
31. Thompson, C. L., Rickman, C. B., Shaw, S. J., Ebright, J. N., Kelly, U., Sancar, A., and Rickman, D. W. (2003) Expression of the blue-light receptor cryptochrome in the human retina, Invest. Ophthalmol. Visual Sci. 44, 4515-21.
32. Vihinen, M., Torkkila, E., and Riikonen, P. (1994) Accuracy of protein flexibility predictions, Proteins 19, 141-9.
33. Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J., and Dunker, A. K. (2001) Sequence complexity of disordered protein, Proteins 42, 38-48.
34. Romero, P., Obradovic, Z., and Dunker, A. K. (1999) Folding minimal sequences: the lower bound for sequence complexity of globular proteins, FEBS Lett. 462, 363-7.
35. Linding, R., Jensen, L. J., Diella, F., Bork, P., Gibson, T. J., and Russell, R. B. (2003) Protein disorder prediction: implications for structural proteomics, Structure (London) 11, 1453-9.
36. Dunker, A. K., Obradovic, Z., Romero, P., Garner, E. C., and Brown, C. J. (2000) Intrinsic protein disorder in complete genomes, Genome Inf. Ser. Workshop Genome Inf. 11, 161-71.
37. Fuxreiter, M., Simon, I., Friedrich, P., and Tompa, P. (2004) Preformed structural elements feature in partner recognition by intrinsically unstructured proteins, J. Mol. Biol. 338, 1015-26.
38. Dedmon, M. M., Patel, C. N., Young, G. B., and Pielak, G. J. (2002) FlgM gains structure in living cells, Proc. Natl. Acad. Sci. U.S.A. 99, 12681-4.
39. Davis-Searles, P. R., Saunders, A. J., Erie, D. A., Winzor, D. J., and Pielak, G. J. (2001) Interpreting the effects of small uncharged solutes on protein-folding equilibria, Annu. Rev. Biophys. Biomol. Struct. 30, 271-306.
40. Qu, Y., Bolen, C. L., and Bolen, D. W. (1998) Osmolyte-driven contraction of a random coil protein, Proc. Natl. Acad. Sci. U.S.A. 95, 9268-73.
41. Wishart, D. S., and Sykes, B. D. (1994) Chemical shifts as a tool for structure determination, Methods Enzymol. 239, 363-92.
42. Cho, H. S., Liu, C. W., Damberger, F. F., Pelton, J. G., Nelson, H. C., and Wemmer, D. E. (1996) Yeast heat shock transcription factor N-terminal activation domains are unstructured as probed by heteronuclear NMR spectroscopy, Protein Sci. 5, 262-9.
43. Donne, D. G., Viles, J. H., Groth, D., Mehlhorn, I., James, T. L., Cohen, F. E., Prusiner, S. B., Wright, P. E., and Dyson, H. J. (1997) Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible, Proc. Natl. Acad. Sci. U.S.A. 94, 13452-7.
44. Farrow, N. A., Zhang, O., Forman-Kay, J. D., and Kay, L. E. (1997) Characterization of the backbone dynamics of folded and denatured states of an SH3 domain, Biochemistry 36, 2390-402.
45. Fontana, A., De Laureto, P. P., Spolaore, B., Frare, E., Picotti, P., and Zambonin, M. (2004) Probing protein structure by limited proteolysis, Acta Biochim. Pol. 51, 299-321.
46. Dyson, H. J., and Wright, P. E. (2002) Coupling of folding and binding for unstructured proteins, Curr. Opin. Struct. Biol. 12, 54-60.
47. Bouly, J. P., Giovani, B., Djamei, A., Mueller, M., Zeugner, A., Dudkin, E. A., Batschauer, A., and Ahmad, M. (2003) Novel ATP-binding and autophosphorylation activity associated with Arabidopsis and human cryptochrome-1, Eur. J. Biochem. 270, 2921-8.
48. Shalitin, D., Yu, X., Maymon, M., Mockler, T., and Lin, C. (2003) Blue light-dependent in vivo and in vitro phosphorylation of Arabidopsis cryptochrome 1, Plant Cell 15, 2421-9.
49. Shalitin, D., Yang, H., Mockler, T. C., Maymon, M., Guo, H., Whitelam, G. C., and Lin, C. (2002) Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation, Nature 417, 763-7.
50. Iakoucheva, L. M., Brown, C. J., Lawson, J. D., Obradovic, Z., and Dunker, A. K. (2002) Intrinsic disorder in cell-signaling and cancer-associated proteins, J. Mol. Biol. 323, 573-84.
51. Bell, S., Klein, C., Muller, L., Hansen, S., and Buchner, J. (2002) p53 contains large unstructured regions in its native state, J. Mol. Biol. 322, 917-27.
52. Esteve, V., Canela, N., Rodriguez-Vilarrupla, A., Aligue, R., Agell, N., Mingarro, I., Bachs, O., and Perez-Paya, E. (2003) The structural plasticity of the C terminus of p21Cip1 is a determinant for target protein recognition, ChemBioChem 4, 863-9.
53. DiGiammarino, E. L., Filippov, I., and Weber, J. D., Bothner, B., and Kriwacki, R. W. (2001) Solution structure of the p53 regulatory domain of the p19Arf tumor suppressor protein, Biochemistry 40, 2379-86.
54. Matthews, J. R., Nicholson, J., Jaffray, E., Kelly, S. M., Price, N. C., and Hay, R. T. (1995) Conformational changes induced by DNA binding of NF-kappa B, Nucleic Acids Res. 23, 3393-402.
55. Shoemaker, B. A., Portman, J. J., and Wolynes, P. G. (2000) Speeding molecular recognition by using the folding funnel: the fly-casting mechanism, Proc. Natl. Acad. Sci. U.S.A. 97, 8868-73.
56. Meador, W. E., Means, A. R., and Quiocho, F. A. (1992) Target enzyme recognition by calmodulin: 2.4 A structure of a calmodulin-peptide complex, Science 257, 1251-5.
57. Schulz, G. E. (1979) in Nucleotide binding proteins (Balaban, M., Ed.) pp 79-94, Elsevier/North-Holland Biomedical Press, New York.
58. Spolar, R. S., and Record, M. T., Jr. (1994) Coupling of local folding to site-specific binding of proteins to DNA, Science 263, 777-84.
59. Rosenfeld, R., Vajda, S., and DeLisi, C. (1995) Flexible docking and design, Annu. Rev. Biophys. Biomol. Struct. 24, 677-700.
60. Salghetti, S. E., Caudy, A. A., Chenoweth, J. G., and Tansey, W. P. (2001) Regulation of transcriptional activation domain function by ubiquitin, Science 293, 1651-3.
61. Prakash, S., Tian, L., Ratliff, K. S., Lehotzky, R. E., and Matouschek, A. (2004) An unstructured initiation site is required for efficient proteasome-mediated degradation, Nat. Struct. Mol. Biol. 11, 830-7.
62. Ahmad, M., Jarillo, J. A., and Cashmore, A. R. (1998) Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability, Plant Cell 10, 197-207.
63. Iakoucheva, L. M., Radivojac, P., Brown, C. J., O'Connor, T. R., Sikes, J. G., Obradovic, Z., and Dunker, A. K. (2004) The importance of intrinsic disorder for protein phosphorylation, Nucleic Acids Res. 32, 1037-49.
64. Osterlund, M. T., Hardtke, C. S., Wei, N., and Deng, X. W. (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis, Nature 405, 462-6.
65. Holm, M., Hardtke, C. S., Gaudet, R., and Deng, X. W. (2001) Identification of a structural motif that confers specific interaction with the WD40 repeat domain of Arabidopsis COP1, EMBO J. 20, 118-27.
66. Tu, D. C., Batten, M. L., Palczewski, K., and Van Gelder, R. N. (2004) Nonvisual photoreception in the chick iris, Science 306, 129-31.
67. Hirayama, J., Nakamura, H., Ishikawa, T., Kobayashi, Y., and Todo, T. (2003) Functional and structural analyses of cryptochrome. Vertebrate CRY regions responsible for interaction with the CLOCK:BMAL1 heterodimer and its nuclear localization, J. Biol. Chem. 278, 35620-8.
68. 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, 1653-8.
69. Giovani, B., Byrdin, M., Ahmad, M., and Brettel, K. (2003) Light-induced electron transfer in a cryptochrome blue-light photoreceptor, Nat. Struct. Biol. 10, 489-90.
70. Li, Y. F., Heelis, P. F., and Sancar, A. (1991) Active site of DNA photolyase: tryptophan-306 is the intrinsic hydrogen atom donor essential for flavin radical photoreduction and DNA repair in vitro, Biochemistry 30, 6322-9.
71. Kavakli, I. H., and Sancar, A. (2004) Analysis of the role of intraprotein electron transfer in photoreduction by DNA photolyase in vivo, Biochemistry 43, 15103-15110.