Structure of a light-activated LOV protein dimer that regulates transcription

Science Signaling

Volumn 4, Issue 184, 2011, Pages

  Vaidya, Anand T ^a   Chen, Chen Hui ^b   Dunlap, Jay C ^b   Loros, Jennifer J ^b   Crane, Brian R ^a  

^a Department of Obstetrics Gynecology   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; FUNGAL PROTEIN; OLIGOMER; VVD PROTEIN, NEUROSPORA CRASSA;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; HYDROGEN BOND; LIGHT ADAPTATION; NEUROSPORA CRASSA; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TRANSCRIPTION REGULATION; CHEMISTRY; CIRCADIAN RHYTHM; GENETIC TRANSCRIPTION; GENETICS; LIGHT; METABOLISM; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; RADIATION EXPOSURE; X RAY CRYSTALLOGRAPHY;

FUNGI; NEUROSPORA; NEUROSPORA CRASSA; PROTISTA;

CIRCADIAN RHYTHM; CRYSTALLOGRAPHY, X-RAY; FUNGAL PROTEINS; HYDROGEN BONDING; LIGHT; NEUROSPORA CRASSA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION, GENETIC;

EID: 79961215646     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2001945     Document Type: Article

References (43)

1. B. L. Taylor, I. B. Zhulin, PAS domains: Internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63, 479-506 (1999).
2. R. A. Ayers, K. Moffat, Changes in quaternary structure in the signaling mechanisms of PAS domains. Biochemistry 47, 12078-12086 (2008).
3. A. Möglich, R. A. Ayers, K. Moffat, Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17, 1282-1294 (2009).
4. S. Crosson, K. Moffat, Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch. Plant Cell 14, 1067-1075 (2002).
5. J. M. Christie, Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58, 21-45 (2007).
6. B. D. Zoltowski, K. H. Gardner, Tripping the light fantastic: Blue-light photoreceptors as examples of environmentally modulated protein-protein interactions. Biochemistry 50, 4-16 (2011).
7. C. Heintzen, J. J. Loros, J. C. Dunlap, The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 104, 453-464 (2001).
8. J. C. Dunlap, J. J. Loros, The Neurospora circadian system. J. Biol. Rhythms 19, 414-424 (2004).
9. C. Heintzen, Y. Liu, The Neurospora crassa circadian clock. Adv. Genet. 58, 25-66 (2007).
10. U. Krauss, B. Q. Minh, A. Losi, W. Gartner, T. Eggert, A. von Haeseler, K. E. Jaeger, Distribution and phylogeny of light-oxygen-voltage-blue-light- signaling proteins in the three kingdoms of life. J. Bacteriol. 191, 7234-7242 (2009).
11. J. C. Dunlap, J. J. Loros, How fungi keep time: Circadian system in Neurospora and other fungi. Curr. Opin. Microbiol. 9, 579-587 (2006).
12. Q. He, P. Cheng, Y. Yang, L. Wang, K. H. Gardner, Y. Liu, White collar-1, a DNA binding transcription factor and a light sensor. Science 297, 840-843 (2002).
13. A. C. Froehlich, Y. Liu, J. J. Loros, J. C. Dunlap, White collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297, 815-819 (2002).
14. Y. Liu, Q. He, P. Cheng, Photoreception in Neurospora: A tale of two White Collar proteins. Cell. Mol. Life Sci. 60, 2131-2138 (2003).
15. Q. He, Y. Liu, Molecular mechanism of light responses in Neurospora: From light-induced transcription to photoadaptation. Genes Dev. 19, 2888-2899 (2005).
16. C. H. Chen, C. S. Ringelberg, R. H. Gross, J. C. Dunlap, J. J. Loros, Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J. 28, 1029-1042 (2009).
17. C. Schwerdtfeger, H. Linden, Blue light adaptation and desensitization of light signal transduction in Neurospora crassa. Mol. Microbiol. 39, 1080-1087 (2001).
18. P. Cheng, Q. He, Y. Yang, L. Wang, Y. Liu, Functional conservation of light, oxygen, or voltage domains in light sensing. Proc. Natl. Acad. Sci. U.S.A. 100, 5938-5943 (2003).
19. E. Malzahn, S. Ciprianidis, K. Káldi, T. Schafmeier, M. Brunner, Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 142, 762-772 (2010).
20. S. M. Hunt, S. Thompson, M. Elvin, C. Heintzen, VIVID interacts with theWHITE COLLAR complex and FREQUENCY-interacting RNA helicase to alter light and clock responses in Neurospora. Proc. Natl. Acad. Sci. U.S.A. 107, 16709-16714 (2010).
21. C. H. Chen, B. S. DeMay, A. S. Gladfelter, J. C. Dunlap, J. J. Loros, Physical interaction between VIVID and white collar complex regulates photoadaptation in Neurospora. Proc. Natl. Acad. Sci. U.S.A. 107, 16715-16720 (2010).
22. B. D. Zoltowski, C. Schwerdtfeger, J. Widom, J. J. Loros, A. M. Bilwes, J. C. Dunlap, B. R. Crane, Conformational switching in the fungal light sensor vivid. Science 316, 1054-1057 (2007).
23. A. Möglich, K. Moffat, Structural basis for light-dependent signaling in the dimeric LOV domain of the photosensor YtvA. J. Mol. Biol. 373, 112-126 (2007).
24. A. S. Halavaty, K. Moffat, N- and C-terminal flanking regions modulate light-induced signal transduction in the LOV2 domain of the blue light sensor phototropin 1 from Avena sativa. Biochemistry 46, 14001-14009 (2007).
25. S. M. Harper, L. C. Neil, K. H. Gardner, Structural basis of a phototropin light switch. Science 301, 1541-1544 (2003).
26. S. M. Harper, J. M. Christie, K. H. Gardner, Disruption of the LOV-J a helix interaction activates phototropin kinase activity. Biochemistry 43, 16184-16192 (2004).
27. E. B. Purcell, C. A. McDonald, B. A. Palfey, S. Crosson, An analysis of the solution structure and signaling mechanism of LovK, a sensor histidine kinase integrating light and redox signals. Biochemistry 49, 6761-6770 (2010).
28. B. D. Zoltowski, B. R. Crane, Light activation of the LOV protein Vivid generates a rapidly exchanging dimer. Biochemistry 47, 7012-7019 (2008).
29. J. S. Lamb, B. D. Zoltowski, S. A. Pabit, B. R. Crane, L. Pollack, Time-resolved dimerization of a PAS-LOV protein measured with photocoupled small angle X-ray scattering. J. Am. Chem. Soc. 130, 12226-12227 (2008).
30. J. S. Lamb, B. D. Zoltowski, S. A. Pabit, L. Li, B. R. Crane, L. Pollack, Illuminating solution responses of a LOV domain protein with photocoupled small-angle X-ray scattering. J. Mol. Biol. 393, 909-919 (2009).
31. B. D. Zoltowski, B. Vaccaro, B. R. Crane, Mechanism-based tuning of a LOV domain photoreceptor. Nat. Chem. Biol. 5, 827-834 (2009).
32. C.Chothia, A. M. Lesk, Helixmovements in proteins. TrendsBiochem.Sci. 10, 116-118 (1985).
33. E. Krissinel, K. Henrick, Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (2007).
34. P. Cheng, Y. Yang, L. Wang, Q. He, Y. Liu, WHITE COLLAR-1, a multifunctional Neurospora protein involved in the circadian feedback loops, light sensing, and transcription repression of wc-2. J. Biol. Chem. 278, 3801-3808 (2003).
35. Z. Otwinowski, W. Minor, Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
36. A. J. McCoy, R. W. Grosse-Kunstleve, P. D. Adams, M. D. Winn, L. C. Storoni, R. J. Read, Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
37. D. E. McRee, XtalView Xfit - A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125, 156-165 (1999).
38. A. T. Brunger, Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2, 2728-2733 (2007).
39. R. Fedorov, I. Schlichting, E. Hartmann, T. Domratcheva, M. Fuhrmann, P. Hegemann, Crystal structures and molecular mechanism of a light-induced signaling switch: The Phot-LOV1 domain from Chlamydomonas reinhardtii. Biophys. J. 84, 2474-2482 (2003).
40. F. Plewniak, L. Bianchetti, Y. Brelivet, A. Carles, F. Chalmel, O. Lecompte, T. Mochel, L. Moulinier, A. Muller, J. Muller, V. Prigent, R. Ripp, J. C. Thierry, J. D. Thompson, N. Wicker, O. Poch, PipeAlign: A new toolkit for protein family analysis. Nucleic Acids Res. 31, 3829-3832 (2003).
41. H. V. Colot, G. Park, G. E. Turner, C. Ringelberg, C. M. Crew, L. Litvinkova, R. L. Weiss, K. A. Borkovich, J. C. Dunlap, A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U.S.A. 103, 10352-10357 (2006).
42. N. Bardiya, P. K. Shiu, Cyclosporin A-resistance based gene placement system for Neurospora crassa. Fungal Genet. Biol. 44, 307-314 (2007).
43. Acknowledgments: We thank B. Zoltowski and J. Widom for important discussions and experimental assistance, J. Schuermann for help with synchrotron data collection, B. Dzikovski for help with the electron spin resonance spectrum, and the Northeastern Collaborative Access Team (NE-CAT) at the APS for access to data collection facilities. We are grateful to the Fungal Genetics Stock Center at the University of Missouri for supporting our work with Neurospora. Funding: Supported by grants from NIH (GM079879 to B.R.C., GM08336 to J.J.L., and GM34985 and GM068087 to J.C.D.). Author contributions: B.R.C., A.T.V., C.-H.C., J.C.D., and J.J.L. generated the general ideas for this manuscript; A.T.V. mutated, expressed, purified, and obtained the size exclusion profiles of the proteins used; A.T.V. crystallized the protein and collected diffraction data; A.T.V. and B.R.C. determined the structure; C.-H.C., J.C.D., and J.J.L. performed and described the N. crassa coloration studies and al-3 repression analysis; and A.T.V. and B.R.C. wrote the manuscript and all authors provided editorial input. Competing interests: The authors declare that they have no competing interests. Data availability: Structure coordinates for the LSD of VVD are deposited in the PDB (http://www.pdb.org) as 3RH8.