Dynamics at the serine loop underlie differential affinity of cryptochromes for CLOCK:BMAL1 to control circadian timing
Abstract
Mammalian circadian rhythms are generated by a transcription-based feedback loop in which CLOCK:BMAL1 drives transcription of its repressors (PER1/2, CRY1/2), which ultimately interact with CLOCK:BMAL1 to close the feedback loop with ~24 hr periodicity. Here we pinpoint a key difference between CRY1 and CRY2 that underlies their differential strengths as transcriptional repressors. Both cryptochromes bind the BMAL1 transactivation domain similarly to sequester it from coactivators and repress CLOCK:BMAL1 activity. However, we find that CRY1 is recruited with much higher affinity to the PAS domain core of CLOCK:BMAL1, allowing it to serve as a stronger repressor that lengthens circadian period. We discovered a dynamic serine-rich loop adjacent to the secondary pocket in the photolyase homology region (PHR) domain that regulates differential binding of cryptochromes to the PAS domain core of CLOCK:BMAL1. Notably, binding of the co-repressor PER2 remodels the serine loop of CRY2, making it more CRY1-like and enhancing its affinity for CLOCK:BMAL1.
- Authors:
-
- Univ. of California, Santa Cruz, CA (United States)
- Nagoya Univ. (Japan)
- The Scripps Research Inst., La Jolla, CA (United States)
- Univ. of Washington, Seattle, WA (United States)
- Kyoto Univ. (Japan)
- Univ. of Washington, Seattle, WA (United States); Howard Hughes Medical Inst., Seattle, WA (United States)
- Nagoya Univ. (Japan); RIKEN Center for Computational Science, Kobe (Japan)
- Univ. of California, Santa Cruz, CA (United States); Univ. of California, San Diego, CA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH); Cancer Research Coordinating Committee
- OSTI Identifier:
- 1644118
- Grant/Contract Number:
- R01 GM107069; DP2 EB020402; F31 CA189660; S10 OD021634; CRN-15–380548
- Resource Type:
- Accepted Manuscript
- Journal Name:
- eLife
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 02, 2020; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Fribourgh, Jennifer L., Srivastava, Ashutosh, Sandate, Colby R., Michael, Alicia K., Hsu, Peter L., Rakers, Christin, Nguyen, Leslee T., Torgrimson, Megan R., Parico, Gian Carlo G., Tripathi, Sarvind, Zheng, Ning, Lander, Gabriel C., Hirota, Tsuyoshi, Tama, Florence, and Partch, Carrie L. Dynamics at the serine loop underlie differential affinity of cryptochromes for CLOCK:BMAL1 to control circadian timing. United States: N. p., 2020.
Web. doi:10.7554/elife.55275.
Fribourgh, Jennifer L., Srivastava, Ashutosh, Sandate, Colby R., Michael, Alicia K., Hsu, Peter L., Rakers, Christin, Nguyen, Leslee T., Torgrimson, Megan R., Parico, Gian Carlo G., Tripathi, Sarvind, Zheng, Ning, Lander, Gabriel C., Hirota, Tsuyoshi, Tama, Florence, & Partch, Carrie L. Dynamics at the serine loop underlie differential affinity of cryptochromes for CLOCK:BMAL1 to control circadian timing. United States. https://doi.org/10.7554/elife.55275
Fribourgh, Jennifer L., Srivastava, Ashutosh, Sandate, Colby R., Michael, Alicia K., Hsu, Peter L., Rakers, Christin, Nguyen, Leslee T., Torgrimson, Megan R., Parico, Gian Carlo G., Tripathi, Sarvind, Zheng, Ning, Lander, Gabriel C., Hirota, Tsuyoshi, Tama, Florence, and Partch, Carrie L. Wed .
"Dynamics at the serine loop underlie differential affinity of cryptochromes for CLOCK:BMAL1 to control circadian timing". United States. https://doi.org/10.7554/elife.55275. https://www.osti.gov/servlets/purl/1644118.
@article{osti_1644118,
title = {Dynamics at the serine loop underlie differential affinity of cryptochromes for CLOCK:BMAL1 to control circadian timing},
author = {Fribourgh, Jennifer L. and Srivastava, Ashutosh and Sandate, Colby R. and Michael, Alicia K. and Hsu, Peter L. and Rakers, Christin and Nguyen, Leslee T. and Torgrimson, Megan R. and Parico, Gian Carlo G. and Tripathi, Sarvind and Zheng, Ning and Lander, Gabriel C. and Hirota, Tsuyoshi and Tama, Florence and Partch, Carrie L.},
abstractNote = {Mammalian circadian rhythms are generated by a transcription-based feedback loop in which CLOCK:BMAL1 drives transcription of its repressors (PER1/2, CRY1/2), which ultimately interact with CLOCK:BMAL1 to close the feedback loop with ~24 hr periodicity. Here we pinpoint a key difference between CRY1 and CRY2 that underlies their differential strengths as transcriptional repressors. Both cryptochromes bind the BMAL1 transactivation domain similarly to sequester it from coactivators and repress CLOCK:BMAL1 activity. However, we find that CRY1 is recruited with much higher affinity to the PAS domain core of CLOCK:BMAL1, allowing it to serve as a stronger repressor that lengthens circadian period. We discovered a dynamic serine-rich loop adjacent to the secondary pocket in the photolyase homology region (PHR) domain that regulates differential binding of cryptochromes to the PAS domain core of CLOCK:BMAL1. Notably, binding of the co-repressor PER2 remodels the serine loop of CRY2, making it more CRY1-like and enhancing its affinity for CLOCK:BMAL1.},
doi = {10.7554/elife.55275},
journal = {eLife},
number = 02, 2020,
volume = 9,
place = {United States},
year = {Wed Feb 26 00:00:00 EST 2020},
month = {Wed Feb 26 00:00:00 EST 2020}
}
Web of Science
Works referenced in this record:
Macromolecular Assemblies of the Mammalian Circadian Clock
journal, September 2017
- Aryal, Rajindra P.; Kwak, Pieter Bas; Tamayo, Alfred G.
- Molecular Cell, Vol. 67, Issue 5
Rhythmic expression of cryptochrome induces the circadian clock of arrhythmic suprachiasmatic nuclei through arginine vasopressin signaling
journal, February 2016
- Edwards, Mathew D.; Brancaccio, Marco; Chesham, Johanna E.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 10
Differential regulation of mammalian Period genes and circadian rhythmicity by cryptochromes 1 and 2
journal, October 1999
- Vitaterna, M. H.; Selby, C. P.; Todo, T.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 21
The BMAL1 C terminus regulates the circadian transcription feedback loop
journal, June 2006
- Kiyohara, Y. B.; Tagao, S.; Tamanini, F.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 26
Transcriptional Architecture and Chromatin Landscape of the Core Circadian Clock in Mammals
journal, August 2012
- Koike, N.; Yoo, S. -H.; Huang, H. -C.
- Science, Vol. 338, Issue 6105
Overview of the CCP 4 suite and current developments
journal, March 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
Intercellular Coupling Confers Robustness against Mutations in the SCN Circadian Clock Network
journal, May 2007
- Liu, Andrew C.; Welsh, David K.; Ko, Caroline H.
- Cell, Vol. 129, Issue 3
Cryptochrome 1 regulates the circadian clock through dynamic interactions with the BMAL1 C terminus
journal, May 2015
- Xu, Haiyan; Gustafson, Chelsea L.; Sammons, Patrick J.
- Nature Structural & Molecular Biology, Vol. 22, Issue 6
Functional motifs in the (6-4) photolyase crystal structure make a comparative framework for DNA repair photolyases and clock cryptochromes
journal, April 2009
- Hitomi, Kenichi; DiTacchio, Luciano; Arvai, Andrew S.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 17
DoG Picker and TiltPicker: Software tools to facilitate particle selection in single particle electron microscopy
journal, May 2009
- Voss, N. R.; Yoshioka, C. K.; Radermacher, M.
- Journal of Structural Biology, Vol. 166, Issue 2
Improved side-chain torsion potentials for the Amber ff99SB protein force field
journal, January 2010
- Lindorff-Larsen, Kresten; Piana, Stefano; Palmo, Kim
- Proteins: Structure, Function, and Bioinformatics
Automated molecular microscopy: The new Leginon system
journal, July 2005
- Suloway, Christian; Pulokas, James; Fellmann, Denis
- Journal of Structural Biology, Vol. 151, Issue 1
The role of tyrosine sulfation in the dimerization of the CXCR4:SDF-1 complex: Tyrosine Sulfation in the CXCR4:SDF-1 Complex
journal, June 2013
- Rapp, Chaya; Snow, Sara; Laufer, Talya
- Protein Science, Vol. 22, Issue 8
Site-Specific Biotinylation of Purified Proteins Using BirA
book, December 2014
- Fairhead, Michael; Howarth, Mark
- Site-Specific Protein Labeling
GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers
journal, September 2015
- Abraham, Mark James; Murtola, Teemu; Schulz, Roland
- SoftwareX, Vol. 1-2
A Slow Conformational Switch in the BMAL1 Transactivation Domain Modulates Circadian Rhythms
journal, May 2017
- Gustafson, Chelsea L.; Parsley, Nicole C.; Asimgil, Hande
- Molecular Cell, Vol. 66, Issue 4
The ratio of intracellular CRY proteins determines the clock period length
journal, April 2016
- Li, Yang; Xiong, Wei; Zhang, Eric Erquan
- Biochemical and Biophysical Research Communications, Vol. 472, Issue 3
Knockout-Rescue Embryonic Stem Cell-Derived Mouse Reveals Circadian-Period Control by Quality and Quantity of CRY1
journal, January 2017
- Ode, Koji L.; Ukai, Hideki; Susaki, Etsuo A.
- Molecular Cell, Vol. 65, Issue 1
Crystal Structure of the Heterodimeric CLOCK:BMAL1 Transcriptional Activator Complex
journal, May 2012
- Huang, N.; Chelliah, Y.; Shan, Y.
- Science, Vol. 337, Issue 6091
Updated structure of Drosophila cryptochrome
journal, March 2013
- Levy, Colin; Zoltowski, Brian D.; Jones, Alex R.
- Nature, Vol. 495, Issue 7441
Structure and Function of DNA Photolyase and Cryptochrome Blue-Light Photoreceptors
journal, June 2003
- Sancar, Aziz
- Chemical Reviews, Vol. 103, Issue 6
α-helix stabilization by alanine relative to glycine: Roles of polar and apolar solvent exposures and of backbone entropy
journal, June 2006
- López-Llano, J.; Campos, L. A.; Sancho, J.
- Proteins: Structure, Function, and Bioinformatics, Vol. 64, Issue 3
Scaling and assessment of data quality
journal, December 2005
- Evans, Philip
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82
Animal Cryptochromes: Divergent Roles in Light Perception, Circadian Timekeeping and Beyond
journal, January 2017
- Michael, Alicia K.; Fribourgh, Jennifer L.; Van Gelder, Russell N.
- Photochemistry and Photobiology, Vol. 93, Issue 1
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Crystal structure of DNA photolyase from Escherichia coli
journal, June 1995
- Park, H.; Kim, S.; Sancar, A.
- Science, Vol. 268, Issue 5219
MDTraj: A Modern Open Library for the Analysis of Molecular Dynamics Trajectories
journal, October 2015
- McGibbon, Robert T.; Beauchamp, Kyle A.; Harrigan, Matthew P.
- Biophysical Journal, Vol. 109, Issue 8
Role of Structural Plasticity in Signal Transduction by the Cryptochrome Blue-Light Photoreceptor †
journal, March 2005
- Partch, Carrie L.; Clarkson, Michael W.; Özgür, Sezgin
- Biochemistry, Vol. 44, Issue 10
Role of the CLOCK Protein in the Mammalian Circadian Mechanism
journal, June 1998
- Gekakis, N.
- Science, Vol. 280, Issue 5369
Allosteric Control of a Plant Receptor Kinase through S-Glutathionylation
journal, December 2017
- Moffett, Alexander S.; Bender, Kyle W.; Huber, Steven C.
- Biophysical Journal, Vol. 113, Issue 11
Vertebrate-like CRYPTOCHROME 2 from monarch regulates circadian transcription via independent repression of CLOCK and BMAL1 activity
journal, August 2017
- Zhang, Ying; Markert, Matthew J.; Groves, Shayna C.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 36
Quantitative Analyses of Cryptochrome-mBMAL1 Interactions: MECHANISTIC INSIGHTS INTO THE TRANSCRIPTIONAL REGULATION OF THE MAMMALIAN CIRCADIAN CLOCK
journal, April 2011
- Czarna, Anna; Breitkreuz, Helena; Mahrenholz, Carsten C.
- Journal of Biological Chemistry, Vol. 286, Issue 25
Formation of a repressive complex in the mammalian circadian clock is mediated by the secondary pocket of CRY1
journal, January 2017
- Michael, Alicia K.; Fribourgh, Jennifer L.; Chelliah, Yogarany
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 7
Phosphorylation Regulating the Ratio of Intracellular CRY1 Protein Determines the Circadian Period
journal, September 2016
- Liu, Na; Zhang, Eric Erquan
- Frontiers in Neurology, Vol. 7
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM
journal, March 2011
- Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
Malleable machines take shape in eukaryotic transcriptional regulation
journal, November 2008
- Fuxreiter, Monika; Tompa, Peter; Simon, István
- Nature Chemical Biology, Vol. 4, Issue 12
Canonical sampling through velocity rescaling
journal, January 2007
- Bussi, Giovanni; Donadio, Davide; Parrinello, Michele
- The Journal of Chemical Physics, Vol. 126, Issue 1
An evolutionary hotspot defines functional differences between CRYPTOCHROMES
journal, March 2018
- Rosensweig, Clark; Reynolds, Kimberly A.; Gao, Peng
- Nature Communications, Vol. 9, Issue 1
SCFFBXL3 ubiquitin ligase targets cryptochromes at their cofactor pocket
journal, March 2013
- Xing, Weiman; Busino, Luca; Hinds, Thomas R.
- Nature, Vol. 496, Issue 7443
Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana
journal, August 2004
- Brautigam, C. A.; Smith, B. S.; Ma, Z.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 33
Molecular dynamics with coupling to an external bath
journal, October 1984
- Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.
- The Journal of Chemical Physics, Vol. 81, Issue 8
Features and development of Coot
journal, March 2010
- Emsley, P.; Lohkamp, B.; Scott, W. G.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
Molecular architecture of the mammalian circadian clock
journal, February 2014
- Partch, Carrie L.; Green, Carla B.; Takahashi, Joseph S.
- Trends in Cell Biology, Vol. 24, Issue 2
RELION: Implementation of a Bayesian approach to cryo-EM structure determination
journal, December 2012
- Scheres, Sjors H. W.
- Journal of Structural Biology, Vol. 180, Issue 3, p. 519-530
Interaction of Circadian Clock Proteins CRY1 and PER2 Is Modulated by Zinc Binding and Disulfide Bond Formation
journal, May 2014
- Schmalen, Ira; Reischl, Silke; Wallach, Thomas
- Cell, Vol. 157, Issue 5
A Novel Bmal1 Mutant Mouse Reveals Essential Roles of the C-Terminal Domain on Circadian Rhythms
journal, September 2015
- Park, Noheon; Kim, Hee-Dae; Cheon, Solmi
- PLOS ONE, Vol. 10, Issue 9
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Posttranslational Mechanisms Regulate the Mammalian Circadian Clock
journal, December 2001
- Lee, Choogon; Etchegaray, Jean-Pierre; Cagampang, Felino R. A.
- Cell, Vol. 107, Issue 7
Polymorphic transitions in single crystals: A new molecular dynamics method
journal, December 1981
- Parrinello, M.; Rahman, A.
- Journal of Applied Physics, Vol. 52, Issue 12
A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation
journal, January 1999
- Beckett, Dorothy; Kovaleva, Elena; Schatz, Peter J.
- Protein Science, Vol. 8, Issue 4
Identification of Small Molecule Activators of Cryptochrome
journal, July 2012
- Hirota, T.; Lee, J. W.; St. John, P. C.
- Science, Vol. 337, Issue 6098
The HADDOCK2.2 Web Server: User-Friendly Integrative Modeling of Biomolecular Complexes
journal, February 2016
- van Zundert, G. C. P.; Rodrigues, J. P. G. L. M.; Trellet, M.
- Journal of Molecular Biology, Vol. 428, Issue 4
Transcriptional architecture of the mammalian circadian clock
journal, December 2016
- Takahashi, Joseph S.
- Nature Reviews Genetics, Vol. 18, Issue 3
Mutation of the Human Circadian Clock Gene CRY1 in Familial Delayed Sleep Phase Disorder
journal, April 2017
- Patke, Alina; Murphy, Patricia J.; Onat, Onur Emre
- Cell, Vol. 169, Issue 2
Delay in Feedback Repression by Cryptochrome 1 Is Required for Circadian Clock Function
journal, January 2011
- Ukai-Tadenuma, Maki; Yamada, Rikuhiro G.; Xu, Haiyan
- Cell, Vol. 144, Issue 2
Structures of Drosophila Cryptochrome and Mouse Cryptochrome1 Provide Insight into Circadian Function
journal, June 2013
- Czarna, Anna; Berndt, Alex; Singh, Hari Raj
- Cell, Vol. 153, Issue 6
Feedback repression is required for mammalian circadian clock function
journal, February 2006
- Sato, Trey K.; Yamada, Rikuhiro G.; Ukai, Hideki
- Nature Genetics, Vol. 38, Issue 3
Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms
journal, April 1999
- Horst, Gijsbertus T. J. van der; Muijtjens, Manja; Kobayashi, Kumiko
- Nature, Vol. 398, Issue 6728
Nucleocytoplasmic shuttling and mCRY-dependent inhibition of ubiquitylation of the mPER2 clock protein
journal, March 2002
- Yagita, Kazuhiro; Tamanini, Filippo; Yasuda, Maya
- The EMBO Journal, Vol. 21, Issue 6
The two CRYs of the butterfly
journal, December 2005
- Zhu, Haisun; Yuan, Quan; Froy, Oren
- Current Biology, Vol. 15, Issue 23
Light-Independent Role of CRY1 and CRY2 in the Mammalian Circadian Clock
journal, October 1999
- Griffin Jr., E. A.
- Science, Vol. 286, Issue 5440
POVME 3.0: Software for Mapping Binding Pocket Flexibility
journal, August 2017
- Wagner, Jeffrey R.; Sørensen, Jesper; Hensley, Nathan
- Journal of Chemical Theory and Computation, Vol. 13, Issue 9
EMAN: Semiautomated Software for High-Resolution Single-Particle Reconstructions
journal, December 1999
- Ludtke, Steven J.; Baldwin, Philip R.; Chiu, Wah
- Journal of Structural Biology, Vol. 128, Issue 1
Comparing Conformational Ensembles Using the Kullback–Leibler Divergence Expansion
journal, May 2012
- McClendon, Christopher L.; Hua, Lan; Barreiro, Gabriela
- Journal of Chemical Theory and Computation, Vol. 8, Issue 6
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome
journal, December 2019
- Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman
- Nature Communications, Vol. 10, Issue 1
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation
journal, February 2021
- Tillu, Vikas A.; Rae, James; Gao, Ya
- Nature Communications, Vol. 12, Issue 1
Rational identification and characterisation of peptide ligands for targeting polysialic acid
journal, May 2020
- Shastry, Divya G.; Irudayanathan, Flaviyan Jerome; Williams, Asher
- Scientific Reports, Vol. 10, Issue 1
Overview of the CCP4 suite and current developments.
text, January 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Apollo - University of Cambridge Repository
Differential regulation of mammalian Period genes and circadian rhythmicity by cryptochromes 1 and 2
text, January 1999
- J., Miyazaki,; H., Niwa,; T., Todo,
- The University of North Carolina at Chapel Hill University Libraries
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
The two CRYs of the butterfly
journal, April 2006
- Zhu, Haisun; Yuan, Quan; Briscoe, Adriana D.
- Current Biology, Vol. 16, Issue 7
α-helix stabilization by alanine relative to glycine: Roles of polar and apolar solvent exposures and of backbone entropy
journal, June 2006
- López-Llano, J.; Campos, L. A.; Sancho, J.
- Proteins: Structure, Function, and Bioinformatics, Vol. 64, Issue 3
EMAN: Semiautomated Software for High-Resolution Single-Particle Reconstructions
journal, December 1999
- Ludtke, Steven J.; Baldwin, Philip R.; Chiu, Wah
- Journal of Structural Biology, Vol. 128, Issue 1
Site-Specific Biotinylation of Purified Proteins Using BirA
book, December 2014
- Fairhead, Michael; Howarth, Mark
- Site-Specific Protein Labeling
The ratio of intracellular CRY proteins determines the clock period length
journal, April 2016
- Li, Yang; Xiong, Wei; Zhang, Eric Erquan
- Biochemical and Biophysical Research Communications, Vol. 472, Issue 3
MDTraj: A Modern Open Library for the Analysis of Molecular Dynamics Trajectories
journal, October 2015
- McGibbon, Robert T.; Beauchamp, Kyle A.; Harrigan, Matthew P.
- Biophysical Journal, Vol. 109, Issue 8
Allosteric Control of a Plant Receptor Kinase through S-Glutathionylation
journal, December 2017
- Moffett, Alexander S.; Bender, Kyle W.; Huber, Steven C.
- Biophysical Journal, Vol. 113, Issue 11
Intercellular Coupling Confers Robustness against Mutations in the SCN Circadian Clock Network
journal, May 2007
- Liu, Andrew C.; Welsh, David K.; Ko, Caroline H.
- Cell, Vol. 129, Issue 3
Delay in Feedback Repression by Cryptochrome 1 Is Required for Circadian Clock Function
journal, January 2011
- Ukai-Tadenuma, Maki; Yamada, Rikuhiro G.; Xu, Haiyan
- Cell, Vol. 144, Issue 2
Interaction of Circadian Clock Proteins CRY1 and PER2 Is Modulated by Zinc Binding and Disulfide Bond Formation
journal, May 2014
- Schmalen, Ira; Reischl, Silke; Wallach, Thomas
- Cell, Vol. 157, Issue 5
Mutation of the Human Circadian Clock Gene CRY1 in Familial Delayed Sleep Phase Disorder
journal, April 2017
- Patke, Alina; Murphy, Patricia J.; Onat, Onur Emre
- Cell, Vol. 169, Issue 2
The two CRYs of the butterfly
journal, April 2006
- Zhu, Haisun; Yuan, Quan; Briscoe, Adriana D.
- Current Biology, Vol. 16, Issue 7
The HADDOCK2.2 Web Server: User-Friendly Integrative Modeling of Biomolecular Complexes
journal, February 2016
- van Zundert, G. C. P.; Rodrigues, J. P. G. L. M.; Trellet, M.
- Journal of Molecular Biology, Vol. 428, Issue 4
Automated molecular microscopy: The new Leginon system
journal, July 2005
- Suloway, Christian; Pulokas, James; Fellmann, Denis
- Journal of Structural Biology, Vol. 151, Issue 1
Macromolecular Assemblies of the Mammalian Circadian Clock
journal, September 2017
- Aryal, Rajindra P.; Kwak, Pieter Bas; Tamayo, Alfred G.
- Molecular Cell, Vol. 67, Issue 5
Molecular architecture of the mammalian circadian clock
journal, February 2014
- Partch, Carrie L.; Green, Carla B.; Takahashi, Joseph S.
- Trends in Cell Biology, Vol. 24, Issue 2
POVME 3.0: Software for Mapping Binding Pocket Flexibility
journal, August 2017
- Wagner, Jeffrey R.; Sørensen, Jesper; Hensley, Nathan
- Journal of Chemical Theory and Computation, Vol. 13, Issue 9
Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms
journal, April 1999
- Horst, Gijsbertus T. J. van der; Muijtjens, Manja; Kobayashi, Kumiko
- Nature, Vol. 398, Issue 6728
Updated structure of Drosophila cryptochrome
journal, March 2013
- Levy, Colin; Zoltowski, Brian D.; Jones, Alex R.
- Nature, Vol. 495, Issue 7441
Malleable machines take shape in eukaryotic transcriptional regulation
journal, November 2008
- Fuxreiter, Monika; Tompa, Peter; Simon, István
- Nature Chemical Biology, Vol. 4, Issue 12
Feedback repression is required for mammalian circadian clock function
journal, February 2006
- Sato, Trey K.; Yamada, Rikuhiro G.; Ukai, Hideki
- Nature Genetics, Vol. 38, Issue 3
Cryptochrome 1 regulates the circadian clock through dynamic interactions with the BMAL1 C terminus
journal, May 2015
- Xu, Haiyan; Gustafson, Chelsea L.; Sammons, Patrick J.
- Nature Structural & Molecular Biology, Vol. 22, Issue 6
An evolutionary hotspot defines functional differences between CRYPTOCHROMES
journal, March 2018
- Rosensweig, Clark; Reynolds, Kimberly A.; Gao, Peng
- Nature Communications, Vol. 9, Issue 1
Molecular basis for assembly of the shieldin complex and its implications for NHEJ
journal, April 2020
- Liang, Ling; Feng, Jiawen; Zuo, Peng
- Nature Communications, Vol. 11, Issue 1
Structural basis for the transition from translation initiation to elongation by an 80S-eIF5B complex
journal, October 2020
- Wang, Jinfan; Wang, Jing; Shin, Byung-Sik
- Nature Communications, Vol. 11, Issue 1
Syndecan-4 tunes cell mechanics by activating the kindlin-integrin-RhoA pathway
journal, January 2020
- Chronopoulos, Antonios; Thorpe, Stephen D.; Cortes, Ernesto
- Nature Materials, Vol. 19, Issue 6
Molecular dynamics with coupling to an external bath
journal, October 1984
- Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.
- The Journal of Chemical Physics, Vol. 81, Issue 8
Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana
journal, August 2004
- Brautigam, C. A.; Smith, B. S.; Ma, Z.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 33
Formation of a repressive complex in the mammalian circadian clock is mediated by the secondary pocket of CRY1
journal, January 2017
- Michael, Alicia K.; Fribourgh, Jennifer L.; Chelliah, Yogarany
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 7
Vertebrate-like CRYPTOCHROME 2 from monarch regulates circadian transcription via independent repression of CLOCK and BMAL1 activity
journal, August 2017
- Zhang, Ying; Markert, Matthew J.; Groves, Shayna C.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 36
Differential regulation of mammalian Period genes and circadian rhythmicity by cryptochromes 1 and 2
journal, October 1999
- Vitaterna, M. H.; Selby, C. P.; Todo, T.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 21
Identification of a Novel Cryptochrome Differentiating Domain Required for Feedback Repression in Circadian Clock Function
journal, June 2012
- Khan, Sanjoy K.; Xu, Haiyan; Ukai-Tadenuma, Maki
- Journal of Biological Chemistry, Vol. 287, Issue 31
Phosphorylation of the Cryptochrome 1 C-terminal Tail Regulates Circadian Period Length
journal, October 2013
- Gao, Peng; Yoo, Seung-Hee; Lee, Kyung-Jong
- Journal of Biological Chemistry, Vol. 288, Issue 49
A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation
journal, January 1999
- Beckett, Dorothy; Kovaleva, Elena; Schatz, Peter J.
- Protein Science, Vol. 8, Issue 4
Crystal Structure of the Heterodimeric CLOCK:BMAL1 Transcriptional Activator Complex
journal, May 2012
- Huang, N.; Chelliah, Y.; Shan, Y.
- Science, Vol. 337, Issue 6091
Transcriptional Architecture and Chromatin Landscape of the Core Circadian Clock in Mammals
journal, August 2012
- Koike, N.; Yoo, S. -H.; Huang, H. -C.
- Science, Vol. 338, Issue 6105
Role of the CLOCK Protein in the Mammalian Circadian Mechanism
journal, June 1998
- Gekakis, N.
- Science, Vol. 280, Issue 5369
Light-Independent Role of CRY1 and CRY2 in the Mammalian Circadian Clock
journal, October 1999
- Griffin Jr., E. A.
- Science, Vol. 286, Issue 5440
Crystal structure of DNA photolyase from Escherichia coli
journal, June 1995
- Park, H.; Kim, S.; Sancar, A.
- Science, Vol. 268, Issue 5219
Nuclear Entry Mechanism of Rat PER2 (rPER2): Role of rPER2 in Nuclear Localization of CRY Protein
journal, October 2001
- Miyazaki, Koyomi; Mesaki, Miho; Ishida, Norio
- Molecular and Cellular Biology, Vol. 21, Issue 19
Distinct and Separable Roles for Endogenous CRY1 and CRY2 within the Circadian Molecular Clockwork of the Suprachiasmatic Nucleus, as Revealed by the Fbxl3Afh Mutation
journal, April 2013
- Anand, S. N.; Maywood, E. S.; Chesham, J. E.
- Journal of Neuroscience, Vol. 33, Issue 17
Macroscopic conductivity of aqueous electrolyte solutions scales with ultrafast microscopic ion motions
text, January 2020
- Balos, Vasileios; Imoto, Sho; Netz, Roland R.
- Freie Universität Berlin
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
Phosphorylation Regulating the Ratio of Intracellular CRY1 Protein Determines the Circadian Period
journal, September 2016
- Liu, Na; Zhang, Eric Erquan
- Frontiers in Neurology, Vol. 7
Molecular assembly of the period-cryptochrome circadian transcriptional repressor complex
journal, August 2014
- Nangle, Shannon N.; Rosensweig, Clark; Koike, Nobuya
- eLife, Vol. 3