Abstract
The KaiABC circadian clock in the cyanobacterium Synechococcus elongatus can be reconstituted in vitro from three proteins in the presence of ATP. This oscillator displays the pertinent features of circadian rhythms including a self-sustained 24-h period and temperature compensation. At every phase of the cycle there is a mixture of types of Kai complexes and the proportions of the various types are oscillating. The KaiC protein is an auto-kinase and auto-phosphatase whose phosphorylation levels oscillate over the daily period whereby KaiA and KaiB interact with KaiC to increase and decrease its phosphorylation, respectively. This chapter provides an overview of the three-dimensional (3D) structural characterization of Kai proteins and the understanding of the KaiA–KaiC interaction gained by NMR and 3D electron microscopy (EM). Despite impressive advances in the structural realm, many open questions remain regarding the control of KaiC phosphorylation by KaiA and KaiB and conformational changes accompanying the transition between the hypo- and hyper-phosphorylated states of KaiC.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 Å resolution of F1 ATPase from bovine heart mitochondria. Nature 370:621–628
Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242
Egli M, Pattanayek R, Pattanayek S (2007) Protein–protein interactions in the cyanobacterial KaiABC circadian clock. In: Boeyens JCA, Ogilvie JF (eds) Models, mysteries, and magic of molecules; proceedings of the INDABA-5 conference, Kruger National Park, South Africa, August 20–25, 2006. Springer, Dordrecht, pp 287–303
Garces RG, Wu N, Gillon W, Pai EF (2004) Anabaena circadian clock proteins KaiA and KaiB reveal potential common binding site to their partner KaiC. EMBO J 23:1688–1698
Golden SS (2004) Meshing the gears of the cyanobacterial circadian clock. Proc Natl Acad Sci USA 101:13697–13698
Golden SS, Cassone VM, LiWang A (2007) Shifting nanoscopic clock gears. Nat Struct Mol Biol 14:362–363
Hayashi F, Suzuki H, Iwase R, Uzumaki T, Miyake A, Shen J-R, Imada K, Furukawa Y, Yonekura K, Namba K, Ishiura M (2003) ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. Genes Cells 8:287–296
Hayashi F, Itoh N, Uzumaki T, Iwase R, Tsuchiya Y, Yamakawa H, Morishita M, Onai K, Itoh S, Ishiura M (2004a) Roles of two ATPase-motif-containing domains in cyanobacterial circadian clock protein KaiC. J Biol Chem 50:52331–52337
Hayashi F, Ito H, Fujita M, Iwase R, Uzumaki T, Ishiura M (2004b) Stoichiometric interactions between cyanobacterial clock proteins KaiA and KaiC. Biochem Biophys Res Comm 316:195–202
Hayashi F, Iwase R, Uzumaki T, Ishiura M (2006) Hexamerization by the N-terminal domain and intersubunit phosphorylation by the C-terminal domain of cyanobacterial circadian clock protein KaiC. Biochem Biophys Res Comm 318:864–872
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 cir-cadian rhythm. J Biol Chem 280:18643–18650
Ishiura M, Kutsuna S, Aoki S, Iwasaki H, Andersson CR, Tanabe A, Golden SS, Johnson CH, Kondo T (1998) Expression of a gene cluster kaiABC as a circadian feedback process in cyano-bacteria. Science 281:1519–1523
Ito H, Kageyama H, Mutsuda M, Nakajima M, Oyama T, Kondo T (2007) Autonomous synchronization of the circadian KaiC phosphorylation rhythm. Nat Struct Mol Biol 14:1084–1088
Iwasaki H, Williams SB, Kitayama, Y, Ishiura M, Golden SS, Kondo T (2000) A KaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobac-teria. Cell 101:223–233
Iwasaki H, Nishiwaki T, Kitayama Y, Nakajima M, Kondo T (2002) KaiA-stimulated KaiC phospho-rylation in circadian timing loops in cyanobacteria. Proc Natl Acad Sci USA 99:15788–15793
Iwase R, Imada K, Hayashi F, Uzumaki T, Morishita M, Onai K, Furukawa Y, Namba K, Ishiura M (2005) Functionally important substructures of circadian clock protein KaiB in a unique tetramer complex. J Biol Chem 280:43141–43149
Johnson CH, Egli M (2004) Visualizing a biological clockwork's cogs. Nat Struct Mol Biol 11:584–585
Kageyama H, Nishiwaki T, Nakajima M, Iwasaki H, Oyama T, Kondo T (2006) Cyanobacterial circadian pacemaker: Kai protein complex dynamics in the KaiC phosphorylation cycle in vitro. Mol Cell 23:161–171
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 22:1–8
Leipe DD, Aravind L, Grishin N V, Koonin EV (2000) The bacterial replicative helicase DnaB evolved from a RecA duplication. Genome Res 10:5–16
Mori T, Johnson CH (2001) Circadian programming in cyanobacteria. Semin Cell Dev Biol 12:271–278
Mori T, Saveliev SV, Xu Y, Stafford WF, Cox MM, Inman RB, Johnson CH (2002) Circadian clock protein KaiC forms ATP-dependent hexameric rings and binds DNA. Proc Natl Acad Sci USA 99:17203–17208
Mori T, Williams DR, Byrne M, Qin X, Egli M, Mchaourab H, Stewart PL, Johnson CH (2007) Elucidating the ticking of an in vitro circadian clockwork. PLoS Biol 5:841–853
Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y, Iwasaki H, Oyama T, Kondo T (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308:414–415
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 USA 97:495–499
Nishiwaki T, Satomi Y, Nakajima M, Lee C, Kiyohara R, Kageyama H, Kitayama Y, Temamoto M, Yamaguchi A, Hijikata A, Go M, Iwasaki H, Takao T, Kondo T (2004) Role of KaiC phos-phorylation in the circadian clock system of Synechococcus elongatus PCC 7942. Proc Natl Acad Sci USA 101:13927–13932
Nishiwaki T, Satomi Y, Kitayama Y, Terauchi K, Kiyohara R, Takao T, Kondo T (2007) A sequential program of dual phosphorylation of KaiC as a basis for circadian rhythm in cyanobacteria. EMBO J 26:4029–4037
Pattanayek R, Wang J, Mori T, Xu Y, Johnson CH, Egli M (2004) Visualizing a circadian clock protein: crystal structure of KaiC and functional insights. Mol Cell 15:375–388
Pattanayek R, Williams DR, Pattanayek S, Xu Y, Mori T, Johnson CH, Stewart PL, Egli M (2006) Analysis of KaiA–KaiC protein interactions in the cyanobacterial circadian clock using hybrid structural methods. EMBO J 25:2017–2038
Pattanayek R, Williams DR, Pattanayek S, Mori T, Johnson CH, Stewart PL, Egli M (2008) Structural model of the circadian clock KaiB-KaiC complex and mechanism for modulation of KaiC phosphorylation. EMBO J 27:1767–1778
Pettersen EF (2004) UCSF chimera – a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612
Rust MJ, Markson JS, Lane WS, Fisher DS, O'Shea EK (2007) Ordered phosphorylation governs oscillation of a three-protein circadian clock. Science 318:809–812
Schmitz O, Katayama M, Williams SB, Kondo T, and Golden SS (2000) CikA, a bacteriophyto-chrome that resets the cyanobacterial circadian clock. Science 289:765–768
Taniguchi Y, Yamaguchi A, Hijikata A, Iwasaki H, Kamagata K, Ishiura M, Go M, Kondo T (2001) Two KaiA-binding domains of cyanobacterial circadian clock protein KaiC. FEBS Lett 496:86–90
Terauchi K, Kitayama Y, Nishiwaki T, Miwa K, Murayama Y, Oyama T, Kondo T (2007) The ATPase activity of KaiC determines the basic timing for circadian clock in cyanobacteria. Proc Natl Acad Sci USA 104:16377–16381
Tomita J, Nakajima M, Kondo T, Iwasaki H (2005) Circadian rhythm of KaiC phosphorylation without transcription-translation feedback. Science 307:251–254
Uzumaki T, Fujita M, Nakatsu T, Hayashi F, Shibata H, Itoh N, Kato H, Ishiura M (2004) Crystal structure of the C-terminal clock-oscillator domain of the cyanobacterial KaiA protein. Nat Struct Mol Biol 11:623–631
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 USA 101:10925–10930
Vakonakis I, Sun J, Wu T, Holzenburg A, Golden SS, LiWang AC (2004a) NMR structure of the KaiC-interacting C-terminal domain of KaiA, a circadian clock protein: Implications for the KaiA–KaiC Interaction. Proc Natl Acad Sci USA 101:1479–1484
Vakonakis I, Klewer DA, Williams SB, Golden SS, LiWang AC (2004b) Structure of the N-termi-nal domain of the circadian clock-associated histidine kinase SasA. J Mol Biol 342:9–17
Wang J (2005) Recent cyanobacterial Kai protein structures suggest a rotary clock. Structure 13:735–741
Williams SB, Vakonakis I, Golden SS, LiWang AC (2002) Structure and function from the circa-dian clock protein KaiA of Synechococcus elongatus: a potential clock input mechanism. Proc Natl Acad Sci USA 99:15357–15362
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
Xu Y, Mori T, Pattanayek R, Pattanayek S, Egli M, Johnson CH (2004) Identification of key phosphorylation sites in the circadian clock protein KaiC by crystallographic and mutagenetic analyses. Proc Natl Acad Sci USA 101:13933–13938
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
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Egli, M., Stewart, P.L. (2009). Structural Aspects of the Cyanobacterial KaiABC Circadian Clock. In: Ditty, J.L., Mackey, S.R., Johnson, C.H. (eds) Bacterial Circadian Programs. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-88431-6_7
Download citation
DOI: https://doi.org/10.1007/978-3-540-88431-6_7
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-88430-9
Online ISBN: 978-3-540-88431-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)