Elucidating the ticking of an in vitro circadian clockwork

PLoS Biology

Volumn 5, Issue 4, 2007, Pages 841-853

  Mori, Tetsuya ^a   Williams, Dewight R ^b   Byrne, Mark O ^a   Qin, Ximing ^a   Egli, Martin ^a   Mchaourab, Hassane S ^b   Stewart, Phoebe L ^b   Johnson, Carl Hirschie ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN KAIA; PROTEIN KAIB; PROTEIN KAIC; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG;

ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; CYANOBACTERIUM; ELECTRON MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEL ELECTROPHORESIS; GENE INTERACTION; MODEL; NONHUMAN; OSCILLATOR; PERIODICITY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; TEMPERATURE; BINDING SITE; CHEMISTRY; IN VITRO STUDY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SYNECHOCOCCUS; ULTRASTRUCTURE;

KAIA;

BACTERIAL PROTEINS; BINDING SITES; CIRCADIAN RHYTHM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENCE RESONANCE ENERGY TRANSFER; MICROSCOPY, ELECTRON; PHOSPHORYLATION; SYNECHOCOCCUS;

EID: 34247232450     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0050093     Document Type: Article

References (41)

1. Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y, et al. (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308: 414-415. doi:10.1126/science.1108451
2. Ishiura M, Kutsuna S, Aoki S, Iwasaki H, Andersson CR, et al. (1998) Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281: 1519-1523. doi:10.1126/science.281.5382.1519
3. Iwasaki H, Taniguchi Y, Ishiura M, Kondo T (1999) Physical interactions among circadian clock proteins KaiA, KaiB and KaiC in cyanobacteria. EMBO J 18: 1137-1145. doi:10.1093/emboj/18.5.1137
4. Xu Y, Piston DW, Johnson CH (1999) A bioluminescence resonance energy transfer (BRET) system: Application to interacting circadian clock proteins. Proc Natl Acad Sci U S A 96: 151-156. Available: http://www.pnas.org/cgi/ content/full/96/1/151. Accessed 11 February 11, 2007.
5. Taniguchi Y, Yamaguchi A, Hijikata A, Iwasaki H, Kamagata K, et al. (2006) Two KaiA-binding domains of cyanobacterial circadian clock protein KaiC. FEBS Lett 496: 86-90. doi:10.1016/S0014-5793(01)02408-5
6. Nishiwaki T, Iwasaki H, Ishiura M, Kondo T (2000) Nucleotide binding and autophosphorylation of the clock protein KaiC as a circadian timing process of cyanobacteria. Proc Natl Acad Sci U S A 97: 495-499. Available: http://www.pnas.org/cgi/content/full/97/1/495. Accessed 11 February 2007.
7. Iwasaki H, Nishiwaki T, Kitayama Y, Nakajima M, Kondo T (2002) KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria. Proc Natl Acad Sci U S A 99: 15788-15793. Available: http://www.pnas.org/cgi/ content/full/99/24/15788. Accessed 11 February 2007.
8. Xu Y, Mori T, Johnson CH (2003) Cyanobacterial circadian clockwork: Roles of KaiA, KaiB and the kaiBC promoter in regulating KaiC. EMBO J 22: 2117-2126. Available: http://www.nature.com/emboj/journal/v22/n9/full/ 7590600a.html. Accessed 11 February 2007.
9. Williams SB, Vakonakis I, Golden SS, LiWang AC (2002) Structure and function from the circadian clock protein KaiA of Synechococcus elongatus: A potential clock input mechanism. Proc Natl Acad Sci U S A 99: 15357-15362. Available: http://www.pnas.org/cgi/content/full/99/24/15357. Accessed: 11 February 2007.
10. Kitayama Y, Iwasaki H, Nishiwaki T, Kondo T (2003) KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial circadian clock system. EMBO J 22: 2127-2134. Available: http://www.nature.com/emboj/journal/v22/n9/ full/7590622a.html. Accessed 11 February 2007.
11. Pattanayek R, Wang J, Mori T, Xu Y, Johnson CH, et al. (2004) Visualizing a circadian clock protein: Crystal structure of KaiC and functional insights. Mol Cell 15: 375-388. doi:10.1016/j.molcel.2004.07.013
12. Garces RG, Wu N, Gillon W, Pai EF (2004) Anabaena circadian clock proteins KaiA and KaiB reveal a potential common binding site to their partner KaiC. EMBO J 23: 1688-1698. Available: http://www.nature.com/emboj/journal/v23/ n8/full/7600190a.html. Accessed 11 February 2007.
13. Vakonakis I, Sun J, Wu T, Holzenburg A, Golden SS, et al. (2004) NMR structure of the KaiC-interacting C-terminal domain of KaiA, a circadian clock protein: Implications for KaiA-KaiC interaction. Proc Natl Acad Sci U S A 101: 1479-1484. Available: http://www.pnas.org/cgi/content/full/101/6/ 1479. Accessed 11 February 2007.
14. Ye S, Vakonakis I, Ioerger TR, LiWang AC, Sacchettini JC (2004) Crystal structure of circadian clock protein KaiA from Synechococcus elongatus. J Biol Chem 279: 20511-20518. Available: http://www.jbc.org/cgi/content/full/279/ 19/20511. Accessed 11 February 2007.
15. Vakonakis I, LiWang AC (2004) Structure of the C-terminal domain of the clock protein KaiA in complex with a KaiC-derived peptide: Implications for KaiC regulation. Proc Natl Acad Sci U S A 101: 10925-10930. Available: http://www.pnas.org/cgi/content/full/101/30/10925. Accessed 11 February 2007.
16. Pattanayek R, Williams DR, Pattanayek S, Xu Y, Mori T, et al. (2006) Analysis of KaiA-KaiC protein interactions in the cyanobacterial circadian clock using hybrid structural methods. EMBO J 25: 2017-2028. doi:10.1038/sj.emboj. 7601086
17. Xu Y, Mori T, Pattanayek R, Pattanayek S, Egli M, et al. (2004) Identification of key phosphorylation sites in the circadian clock protein KaiC by crystallographic and mutagenetic analyses. Proc Natl Acad Sci U S A 101:13933-13938. Available: http://www.pnas.org/cgi/content/full/101/38/13933. Accessed 11 February 2007.
18. Hitomi K, Oyama T, Han S, Arvai AS, Getzoff ED (2005) Tetrameric architecture of the circadian clock protein KaiB. A novel interface for intermolecular interactions and its impact on the circadian rhythm. J Biol Chem 280: 19127-19135. Available: http://www.jbc.org/cgi/content/full/280/ 19/19127. Accessed 11 February 2007.
19. Mori T, Saveliev SV, Xu Y, Stafford WF, Cox MM, et al. (2002) Circadian clock protein KaiC forms ATP-dependent hexameric rings and binds DNA. Proc Natl Acad Sci U S A 99: 17203-17208. Available: http://www.pnas.org/cgi/content/full/ 99/26/17203. Accessed 12 February 2007.
20. Tomita J, Nakajima M, Kondo T, Iwasaki H (2005) No transcription- translation feedback in circadian rhythm of KaiC phosphorylation. Science 307: 251-254. doi:10.1126/science.1102540
21. Kageyama H, Nishiwaki T, Nakajima M, Iwasaki H, Oyama T, et al. (2006) Cyanobacterial circadian pacemaker: Kai protein complex dynamics in the KaiC phosphorylation cycle in vitro. Mol Cell 23: 161-171. doi:10.1016/j.molcel.2006. 05.039
22. Schä gger H, Cramer WA, von Jagow G (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal Biochem 217: 220-230. doi:10.1006/abio.1994.1112
23. Farmery MR, Tjernberg LO, Pursglove SE, Bergman A, Winblad B, et al. (2003) Partial purification and characterization of γ-secretase from postmortem human brain. J Biol Chem 278: 24277-24284. Available: http://www.jbc.org/cgi/content/full/278/27/24277. Accessed 12 February 2007.
24. Camacho-Carvajal MM, Wollscheid B, Aebersold R, Steimle V, Schamel WW (2004) Two-dimensional Blue native/SDS gel electrophoresis of multiprotein complexes from whole cellular lysates: a proteomics approach. Mol Cell Proteomics 3: 176-182. Available: http://www.mcponline.org/cgi/content/full/3/2/ 176. Accessed 12 February 2007.
25. Wittig I, Braun HP, Schägger H (2006) Blue native PAGE. Nature Protocols 1: 418-428. Available: http://www.nature.com/nprot/journal/v1/n1/full/ nprot. 2006.62.html. Accessed 12 February 2007.
26. Swamy M, Siegers GM, Minguet S, Wollscheid B, Schamel WW (2006) Blue native polyacrylamide gel electrophoresis (BN-PAGE) for the identification and analysis of multiprotein complexes. Sci STKE 2006: p 14. doi:10.1126/stke. 3452006p14
27. Clegg RM (1995) Fluorescence resonance energy transfer. Curr Opin Biotechnol 6: 103-110. doi:10.1016/0958-1669(95)80016-6
28. Bova MP, Huang Q, Ding L, Horwitz J (2002) Subunit exchange, conformational stability, and chaperone-like function of the small heat shock protein 16.5 from Methanococcus jannaschii. J Biol Chem 277: 38468-38475. Available: http://www.jbc.org/cgi/content/full/277/41/38468. Accessed 12 February 2007.
29. Emberly E, Wingreen NS (2006) Hourglass model for a protein-based circadian oscillator. Phys Rev Lett 96: 038303. doi:10.1103/PhysRevLett.96. 038303
30. Aschoff J (1965) Response curves in circadian periodicity. In: Aschoff J, editor. Circadian clocks. Amsterdam: North-Holland Publishing. pp. 95-111.
31. Johnson CH (1990) An atlas of phase response curves for circadian and circatidal rhythms. Nashville: Department of Biology, Vanderbilt University. 715 p.Available: http://www.cas.vanderbilt.edu/johnsonlab/prcatlas/ index.html. Accessed 18 November 2006.
32. Liu Y, Merrow M, Loros JJ, Dunlap JC (1998) How temperature changes reset a circadian oscillator. Science 281: 825-829. doi:10.1126/science.281.5378.825
33. Liu Y, Tsinoremas NF, Johnson CH, Lebedeva NV, Golden SS, Ishiura M, Kondo T (1995) Circadian orchestration of gene expression in cyanobacteria. Genes Dev 9: 1469-1478.
34. Xu Y, Mori T, Johnson CH (2000) Circadian clock-protein expression in cyanobacteria: rhythms and phase-setting. EMBO J 19: 3349-3357. Available: http://www.nature.com/emboj/journal/v19/n13/full/7593154a. html. Accessed 12 February 2007.
35. Woelfle MA, Johnson CH (2006) No promoter left behind: Global circadian gene expression in cyanobacteria. J Biol Rhythms 21: 419-431. Available: http://jbr.sagepub.com/cgi/reprint/21/6/419. Accessed 12 February 2007.
36. Smith RA, Williams SB (2006) Circadian rhythms of gene transcription imparted by chromosome compaction in the cyanobacterium Synechococcus elongatus. Proc Natl Acad Sci U S A 103: 8564-8569. Available: http://www.pnas.org/cgi/content/full/103/22/8564. Accessed 12 February 2007.
37. Takai N, Nakajima M, Oyama T, Kito R, Sugita C, et al. (2006) A KaiC-associating SasA-RpaA two-component regulatory system as a major circadian timing mediator in cyanobacteria. Proc Natl Acad Sci U S A 103: 12109-12114. Available: http://www.pnas.org/cgi/content/full/103/32/ 12109. Accessed 12 February 2007.
38. Nishiwaki T, Satomi Y, Nakajima M, Lee C, Kiyohara R, et al. (2004) Role of KaiC phosphorylation in the circadian clock system of Synechococcus elongatus PCC 7942. Proc Natl Acad Sci U S A 101: 13927-13932. Available: http://www.pnas.org/cgi/content/full/101/38/13927.
39. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: Semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97. doi:10.1006/jsbi.1999.4174
40. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116: 17-24. doi:10.1006/jsbi.1996.0004
41. Gillespie DT (1976) A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J Comput Phys 22: 403-444.