Coupling of distant ATPase domains in the circadian clock protein KaiC.
Journal
Nature structural & molecular biology
ISSN: 1545-9985
Titre abrégé: Nat Struct Mol Biol
Pays: United States
ID NLM: 101186374
Informations de publication
Date de publication:
08 2022
08 2022
Historique:
received:
20
10
2021
accepted:
06
06
2022
pubmed:
22
7
2022
medline:
16
8
2022
entrez:
21
7
2022
Statut:
ppublish
Résumé
The AAA
Identifiants
pubmed: 35864165
doi: 10.1038/s41594-022-00803-w
pii: 10.1038/s41594-022-00803-w
pmc: PMC9495280
mid: NIHMS1833232
doi:
Substances chimiques
Bacterial Proteins
0
Circadian Rhythm Signaling Peptides and Proteins
0
CLOCK Proteins
EC 2.3.1.48
Adenosine Triphosphatases
EC 3.6.1.-
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
759-766Subventions
Organisme : NIGMS NIH HHS
ID : F32 GM130070
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS095892
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM121507
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM107521
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM141849
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM118290
Pays : United States
Organisme : NIGMS NIH HHS
ID : R21 GM142196
Pays : United States
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
Ishiura, M. et al. Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281, 1519–1523 (1998).
pubmed: 9727980
doi: 10.1126/science.281.5382.1519
Diamond, S., Jun, D., Rubin, B. E. & Golden, S. S. The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth. Proc. Natl Acad. Sci. USA 112, E1916–E1925 (2015).
pubmed: 25825710
pmcid: 4403147
doi: 10.1073/pnas.1504576112
Pattanayak, G. K., Phong, C. & Rust, M. J. Rhythms in energy storage control the ability of the cyanobacterial circadian clock to reset. Curr. Biol. 24, 1934–1938 (2014).
pubmed: 25127221
pmcid: 4477845
doi: 10.1016/j.cub.2014.07.022
Hayashi, F. et al. Roles of two ATPase-motif-containing domains in cyanobacterial circadian clock protein KaiC. J. Biol. Chem. 279, 52331–52337 (2004).
pubmed: 15377674
doi: 10.1074/jbc.M406604200
Rust, M. J., Markson, J. S., Lane, W. S., Fisher, D. S. & O’Shea, E. K. Ordered phosphorylation governs oscillation of a three-protein circadian clock. Science 318, 809–812 (2007).
pubmed: 17916691
pmcid: 2427396
doi: 10.1126/science.1148596
Nishiwaki, T. et al. A sequential program of dual phosphorylation of KaiC as a basis for circadian rhythm in cyanobacteria. EMBO J. 26, 4029–4037 (2007).
pubmed: 17717528
pmcid: 1994132
doi: 10.1038/sj.emboj.7601832
Kim, Y. I., Dong, G., Carruthers, C. W. Jr., Golden, S. S. & LiWang, A. The day/night switch in KaiC, a central oscillator component of the circadian clock of cyanobacteria. Proc. Natl Acad. Sci. USA 105, 12825–12830 (2008).
pubmed: 18728181
pmcid: 2529086
doi: 10.1073/pnas.0800526105
Chang, Y. G., Tseng, R., Kuo, N. W. & LiWang, A. Rhythmic ring-ring stacking drives the circadian oscillator clockwise. Proc. Natl Acad. Sci. USA 109, 16847–16851 (2012).
pubmed: 22967510
pmcid: 3479483
doi: 10.1073/pnas.1211508109
Snijder, J. et al. Insight into cyanobacterial circadian timing from structural details of the KaiB-KaiC interaction. Proc. Natl Acad. Sci. USA 111, 1379–1384 (2014).
pubmed: 24474762
pmcid: 3910634
doi: 10.1073/pnas.1314326111
Murakami, R. et al. Cooperative binding of KaiB to the KaiC Hexamer ensures accurate circadian clock oscillation in cyanobacteria. Int. J. Mol. Sci. https://doi.org/10.3390/ijms20184550 (2019).
Chavan, A. G. et al. Reconstitution of an intact clock reveals mechanisms of circadian timekeeping. Science 374, eabd4453 (2021).
pubmed: 34618577
pmcid: 8686788
doi: 10.1126/science.abd4453
Chow, G. K. et al. A night-time edge site intermediate in the cyanobacterial circadian clock identified by EPR spectroscopy. J. Am. Chem. Soc. 144, 184–194 (2022).
pubmed: 34979080
doi: 10.1021/jacs.1c08103
Tseng, R. et al. Structural basis of the day-night transition in a bacterial circadian clock. Science 355, 1174–1180 (2017).
pubmed: 28302851
pmcid: 5441561
doi: 10.1126/science.aag2516
Chang, Y. G. et al. Circadian rhythms. A protein fold switch joins the circadian oscillator to clock output in cyanobacteria. Science 349, 324–328 (2015).
pubmed: 26113641
pmcid: 4506712
doi: 10.1126/science.1260031
Chang, Y. G., Kuo, N. W., Tseng, R. & LiWang, A. Flexibility of the C-terminal, or CII, ring of KaiC governs the rhythm of the circadian clock of cyanobacteria. Proc. Natl Acad. Sci. USA 108, 14431–14436 (2011).
pubmed: 21788479
pmcid: 3167551
doi: 10.1073/pnas.1104221108
Tseng, R. et al. Cooperative KaiA-KaiB-KaiC interactions affect KaiB/SasA competition in the circadian clock of cyanobacteria. J. Mol. Biol. 426, 389–402 (2014).
pubmed: 24112939
doi: 10.1016/j.jmb.2013.09.040
Snijder, J. et al. Structures of the cyanobacterial circadian oscillator frozen in a fully assembled state. Science 355, 1181–1184 (2017).
pubmed: 28302852
doi: 10.1126/science.aag3218
Phong, C., Markson, J. S., Wilhoite, C. M. & Rust, M. J. Robust and tunable circadian rhythms from differentially sensitive catalytic domains. Proc. Natl Acad. Sci. USA 110, 1124–1129 (2013).
pubmed: 23277568
doi: 10.1073/pnas.1212113110
Terauchi, K. et al. ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria. Proc. Natl Acad. Sci. USA 104, 16377–16381 (2007).
pubmed: 17901204
pmcid: 2042214
doi: 10.1073/pnas.0706292104
Ito-Miwa, K., Furuike, Y., Akiyama, S. & Kondo, T. Tuning the circadian period of cyanobacteria up to 6.6 days by the single amino acid substitutions in KaiC. Proc. Natl Acad. Sci. USA 117, 20926–20931 (2020).
pubmed: 32747571
pmcid: 7456120
doi: 10.1073/pnas.2005496117
Pattanayek, R., Xu, Y., Lamichhane, A., Johnson, C. H. & Egli, M. An arginine tetrad as mediator of input-dependent and input-independent ATPases in the clock protein KaiC. Acta Crystallogr. D. Biol. Crystallogr. 70, 1375–1390 (2014).
pubmed: 24816106
pmcid: 4722857
doi: 10.1107/S1399004714003228
Dong, G. et al. Elevated ATPase activity of KaiC applies a circadian checkpoint on cell division in Synechococcus elongatus. Cell 140, 529–539 (2010).
pubmed: 20178745
pmcid: 3031423
doi: 10.1016/j.cell.2009.12.042
Murakami, R. et al. The roles of the dimeric and tetrameric structures of the clock protein KaiB in the generation of circadian oscillations in cyanobacteria. J. Biol. Chem. 287, 29506–29515 (2012).
pubmed: 22722936
pmcid: 3436200
doi: 10.1074/jbc.M112.349092
Murayama, Y. et al. Tracking and visualizing the circadian ticking of the cyanobacterial clock protein KaiC in solution. EMBO J. 30, 68–78 (2011).
pubmed: 21113137
doi: 10.1038/emboj.2010.298
Mukaiyama, A. et al. Conformational rearrangements of the C1 ring in KaiC measure the timing of assembly with KaiB. Sci. Rep. 8, 8803 (2018).
pubmed: 29892030
pmcid: 5995851
doi: 10.1038/s41598-018-27131-8
Oyama, K., Azai, C., Matsuyama, J. & Terauchi, K. Phosphorylation at Thr432 induces structural destabilization of the CII ring in the circadian oscillator KaiC. FEBS Lett. 592, 36–45 (2018).
pubmed: 29265368
doi: 10.1002/1873-3468.12945
Pattanayek, R. et al. Structures of KaiC circadian clock mutant proteins: a new phosphorylation site at T426 and mechanisms of kinase, ATPase and phosphatase. PLoS ONE 4, e7529 (2009).
pubmed: 19956664
pmcid: 2777353
doi: 10.1371/journal.pone.0007529
Ito, H. et al. Autonomous synchronization of the circadian KaiC phosphorylation rhythm. Nat. Struct. Mol. Biol. 14, 1084–1088 (2007).
pubmed: 17965725
doi: 10.1038/nsmb1312
Hong, L., Vani, B. P., Thiede, E. H., Rust, M. J. & Dinner, A. R. Molecular dynamics simulations of nucleotide release from the circadian clock protein KaiC reveal atomic-resolution functional insights. Proc. Natl Acad. Sci. USA 115, E11475–E11484 (2018).
pubmed: 30442665
pmcid: 6298084
Oyama, K., Azai, C., Nakamura, K., Tanaka, S. & Terauchi, K. Conversion between two conformational states of KaiC is induced by ATP hydrolysis as a trigger for cyanobacterial circadian oscillation. Sci. Rep. 6, 32443 (2016).
pubmed: 27580682
pmcid: 5007536
doi: 10.1038/srep32443
Efremov, R. G., Leitner, A., Aebersold, R. & Raunser, S. Architecture and conformational switch mechanism of the ryanodine receptor. Nature 517, 39–43 (2015).
pubmed: 25470059
doi: 10.1038/nature13916
Pattanayek, R. et al. Visualizing a circadian clock protein: crystal structure of KaiC and functional insights. Mol. Cell 15, 375–388 (2004).
pubmed: 15304218
doi: 10.1016/j.molcel.2004.07.013
Nishiwaki, T. & Kondo, T. Circadian autodephosphorylation of cyanobacterial clock protein KaiC occurs via formation of ATP as intermediate. J. Biol. Chem. 287, 18030–18035 (2012).
pubmed: 22493509
pmcid: 3365771
doi: 10.1074/jbc.M112.350660
Nishiwaki-Ohkawa, T., Kitayama, Y., Ochiai, E. & Kondo, T. Exchange of ADP with ATP in the CII ATPase domain promotes autophosphorylation of cyanobacterial clock protein KaiC. Proc. Natl Acad. Sci. USA 111, 4455–4460 (2014).
pubmed: 24616498
pmcid: 3970490
doi: 10.1073/pnas.1319353111
Leypunskiy, E. et al. The cyanobacterial circadian clock follows midday in vivo and in vitro. eLife https://doi.org/10.7554/eLife.23539 (2017).
Jessop, M. et al. Structural insights into ATP hydrolysis by the MoxR ATPase RavA and the LdcI-RavA cage-like complex. Commun. Biol. 3, 46 (2020).
pubmed: 31992852
pmcid: 6987120
doi: 10.1038/s42003-020-0772-0
Ye, Q. Z. et al. TRIP13 is a protein-remodeling AAA plus ATPase that catalyzes MAD2 conformation switching. eLife 4, e0736710.7554/eLife.07367 (2015).
Glynn, S. E., Nager, A. R., Baker, T. A. & Sauer, R. T. Dynamic and static components power unfolding in topologically closed rings of a AAA
pubmed: 22562135
pmcid: 3372766
doi: 10.1038/nsmb.2288
Nakajima, M., Ito, H. & Kondo, T. In vitro regulation of circadian phosphorylation rhythm of cyanobacterial clock protein KaiC by KaiA and KaiB. FEBS Lett. 584, 898–902 (2010).
pubmed: 20079736
doi: 10.1016/j.febslet.2010.01.016
Abe, J. et al. Circadian rhythms. Atomic-scale origins of slowness in the cyanobacterial circadian clock. Science 349, 312–316 (2015).
pubmed: 26113637
doi: 10.1126/science.1261040
Erzberger, J. P. & Berger, J. M. Evolutionary relationships and structural mechanisms of AAA
pubmed: 16689629
doi: 10.1146/annurev.biophys.35.040405.101933
Puri, N. et al. The molecular coupling between substrate recognition and ATP turnover in a AAA
Gutu, A. & O’Shea, E. K. Two antagonistic clock-regulated histidine kinases time the activation of circadian gene expression. Mol. Cell 50, 288–294 (2013).
pubmed: 23541768
pmcid: 3674810
doi: 10.1016/j.molcel.2013.02.022
Kitayama, Y., Iwasaki, H., Nishiwaki, T. & Kondo, T. KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial circadian clock system. EMBO J. 22, 2127–2134 (2003).
pubmed: 12727879
pmcid: 156084
doi: 10.1093/emboj/cdg212
Cohen, S. E. et al. Dynamic localization of the cyanobacterial circadian clock proteins. Curr. Biol. 24, 1836–1844 (2014).
pubmed: 25127213
pmcid: 4139467
doi: 10.1016/j.cub.2014.07.036
Ouyang, D. et al. Development and optimization of expression, purification, and ATPase assay of KaiC for medium-throughput screening of circadian clock mutants in cyanobacteria. Int. J. Mol. Sci. https://doi.org/10.3390/ijms20112789 (2019).
Liu, H. & Naismith, J. H. An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol. 8, 91 (2008).
pubmed: 19055817
pmcid: 2629768
doi: 10.1186/1472-6750-8-91
Naydenova, K., Peet, M. J. & Russo, C. J. Multifunctional graphene supports for electron cryomicroscopy. Proc. Natl Acad. Sci. USA 116, 11718–11724 (2019).
pubmed: 31127045
pmcid: 6575631
doi: 10.1073/pnas.1904766116
Han, Y. et al. High-yield monolayer graphene grids for near-atomic resolution cryoelectron microscopy. Proc. Natl Acad. Sci. USA 117, 1009–1014 (2020).
pubmed: 31879346
doi: 10.1073/pnas.1919114117
Carragher, B. et al. Leginon: an automated system for acquisition of images from vitreous ice specimens. J. Struct. Biol. 132, 33–45 (2000).
pubmed: 11121305
doi: 10.1006/jsbi.2000.4314
Lander, G. C. et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol. 166, 95–102 (2009).
pubmed: 19263523
pmcid: 2775544
doi: 10.1016/j.jsb.2009.01.002
Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).
pubmed: 23000701
pmcid: 3690530
doi: 10.1016/j.jsb.2012.09.006
Tan, Y. Z. et al. Addressing preferred specimen orientation in single-particle cryo-EM through tilting. Nat. Methods 14, 793–796 (2017).
pubmed: 28671674
pmcid: 5533649
doi: 10.1038/nmeth.4347
Voss, N. R., Yoshioka, C. K., Radermacher, M., Potter, C. S. & Carragher, B. DoG Picker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J. Struct. Biol. 166, 205–213 (2009).
pubmed: 19374019
pmcid: 2768396
doi: 10.1016/j.jsb.2009.01.004
Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. https://doi.org/10.1016/j.jsb.2015.11.003 (2016).
Roseman, A. M. FindEM–a fast, efficient program for automatic selection of particles from electron micrographs. J. Struct. Biol. 145, 91–99 (2004).
pubmed: 15065677
doi: 10.1016/j.jsb.2003.11.007
Pettersen, E. F. et al. UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
doi: 10.1002/jcc.20084
Nicholls, R. A., Fischer, M., McNicholas, S. & Murshudov, G. N. Conformation-independent structural comparison of macromolecules with ProSMART. Acta Crystallogr. D. Biol. Crystallogr. 70, 2487–2499 (2014).
pubmed: 25195761
pmcid: 4157452
doi: 10.1107/S1399004714016241
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr. 60, 2126–2132 (2004).
pubmed: 15572765
doi: 10.1107/S0907444904019158
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D. Biol. Crystallogr. 66, 213–221 (2010).
pubmed: 20124702
pmcid: 2815670
doi: 10.1107/S0907444909052925
Croll, T. I. ISOLDE: a physically realistic environment for model building into low-resolution electron-density maps. Acta Crystallogr. D. Struct. Biol. 74, 519–530 (2018).
pubmed: 29872003
pmcid: 6096486
doi: 10.1107/S2059798318002425
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D. Biol. Crystallogr. 66, 12–21 (2010).
pubmed: 20057044
doi: 10.1107/S0907444909042073
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
pubmed: 22930834
pmcid: 5554542
doi: 10.1038/nmeth.2089
UniProt, C. UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res. 49, D480–D489 (2021).
doi: 10.1093/nar/gkaa1100
Sievers, F. & Higgins, D. G. The clustal omega multiple alignment package. Methods Mol. Biol. 2231, 3–16 (2021).
pubmed: 33289883
doi: 10.1007/978-1-0716-1036-7_1
Hayashi, F. et al. ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. Genes Cells 8, 287–296 (2003).
pubmed: 12622725
doi: 10.1046/j.1365-2443.2003.00633.x
Bagshaw, C. R. Biomolecular Kinetics: A Step-By-Step Guide (CRC Press, Taylor & Francis Group, 2017).
Heisler, J., Chavan, A., Chang, Y. G. & LiWang, A. Real-time in vitro fluorescence anisotropy of the cyanobacterial circadian clock. Methods Protoc. https://doi.org/10.3390/mps2020042 (2019).
Ungerer, J. & Pakrasi, H. B. Cpf1 is a versatile tool for CRISPR genome editing across diverse species of cyanobacteria. Sci. Rep. 6, 39681 (2016).
pubmed: 28000776
pmcid: 5175191
doi: 10.1038/srep39681
Mackey, S. R. & Golden, S. S. Winding up the cyanobacterial circadian clock. Trends Microbiol. 15, 381–388 (2007).
pubmed: 17804240
doi: 10.1016/j.tim.2007.08.005