Insight into cyanobacterial circadian timing from structural details of the KaiB-KaiC interaction

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 4, 2014, Pages 1379-1384

  Snijder, Joost ^a,b   Burnley, Rebecca J ^a,b   Wiegard, Anika ^c   Melquiond, Adrien S J ^d   Bonvin, Alexandre M J J ^d   Axmann, Ilka M ^c   Heck, Albert J R ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; DIMER; MONOMER; PROTEIN KAIB; PROTEIN KAIC; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; CIRCADIAN RHYTHM; COMPLEX FORMATION; CYANOBACTERIUM; ENZYME ACTIVITY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ION MOBILITY SPECTROMETRY; NATIVE MS; PROTEIN-PROTEIN DOCKING;

BACTERIAL PROTEINS; CIRCADIAN RHYTHM; CIRCADIAN RHYTHM SIGNALING PEPTIDES AND PROTEINS; CYANOBACTERIA; MASS SPECTROMETRY; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84893370016     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1314326111     Document Type: Article

References (55)

1. Dong G, Kim YI, Golden SS (2010) Simplicity and complexity in the cyanobacterial circadian clock mechanism. Curr Opin Genet Dev 20(6):619-625.
2. Tomita J, Nakajima M, Kondo T, Iwasaki H (2005) No transcription- translation feedback in circadian rhythm of KaiC phosphorylation. Science 307(5707):251-254.
3. Xu Y, Mori T, Johnson CH (2003) Cyanobacterial circadian clockwork: Roles of KaiA, KaiB and the kaiBC promoter in regulating KaiC. EMBO J 22(9):2117-2126.
4. Xu Y, et al. (2004) Identification of key phosphorylation sites in the circadian clock protein KaiC by crystallographic and mutagenetic analyses. Proc Natl Acad Sci USA 101(38):13933-13938.
5. Ishiura M, et al. (1998) Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281(5382):1519-1523.
6. Taniguchi Y, Takai N, Katayama M, Kondo T, Oyama T (2010) Three major output pathways from the KaiABC-based oscillator cooperate to generate robust circadian kaiBC expression in cyanobacteria. Proc Natl Acad Sci USA 107(7):3263-3268.
7. Ito H, et al. (2009) Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. Proc Natl Acad Sci USA 106(33):14168-14173.
8. Hertel S, Brettschneider C, Axmann IM (2013) Revealing a two-loop transcriptional feedback mechanism in the cyanobacterial circadian clock. PLOS Comput Biol 9(3): e1002966.
9. NakajimaM, et al. (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308(5720):414-415.
10. Yoshida T, Murayama Y, Ito H, Kageyama H, Kondo T (2009) Nonparametric entrainment of the in vitro circadian phosphorylation rhythm of cyanobacterial KaiC by temperature cycle. Proc Natl Acad Sci USA 106(5):1648-1653.
11. Rust MJ, Golden SS, O'Shea EK (2011) Light-driven changes in energy metabolism directly entrain the cyanobacterial circadian oscillator. Science 331(6014):220-223.
12. Mori T, et al. (2007) Elucidating the ticking of an in vitro circadian clockwork. PLoS Biol 5(4):e93.
13. 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 Commun 348(3):864-872.
14. Hayashi F, et al. (2003) ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. Genes Cells 8(3):287-296.
15. Mori T, et al. (2002) Circadian clock protein KaiC forms ATP-dependent hexameric rings and binds DNA. Proc Natl Acad Sci USA 99(26):17203-17208.
16. Nishiwaki T, et al. (2007) A sequential program of dual phosphorylation of KaiC as a basis for circadian rhythm in cyanobacteria. EMBO J 26(17):4029-4037.
17. Rust MJ, Markson JS, Lane WS, Fisher DS, O'Shea EK (2007) Ordered phosphorylation governs oscillation of a three-protein circadian clock. Science 318(5851):809-812.
18. Kageyama H, et al. (2006) Cyanobacterial circadian pacemaker: Kai protein complex dynamics in the KaiC phosphorylation cycle in vitro. Mol Cell 23(2):161-171.
19. Kim YI, Dong G, Carruthers CW, Jr., Golden SS, LiWang A (2008) The day/night switch in KaiC, a central oscillator component of the circadian clock of cyanobacteria. Proc Natl Acad Sci USA 105(35):12825-12830.
20. Egli M, et al. (2012) Dephosphorylation of the core clock protein KaiC in the cyanobacterial KaiABC circadian oscillator proceeds via an ATP synthase mechanism. Biochemistry 51(8):1547-1558.
21. Nishiwaki T, Kondo T (2012) Circadian autodephosphorylation of cyanobacterial clock protein KaiC occurs via formation of ATP as intermediate. J Biol Chem 287(22): 18030-18035.
22. Brettschneider C, et al. (2010) A sequestration feedback determines dynamics and temperature entrainment of the KaiABC circadian clock. Mol Syst Biol 6:389.
23. Clodong S, et al. (2007) Functioning and robustness of a bacterial circadian clock. Mol Syst Biol 3:90.
24. Qin X, et al. (2010) Intermolecular associations determine the dynamics of the circadian KaiABC oscillator. Proc Natl Acad Sci USA 107(33):14805-14810.
25. Pattanayek R, et al. (2006) Analysis of KaiA-KaiC protein interactions in the cyanobacterial circadian clock using hybrid structural methods. EMBO J 25(9):2017-2028.
26. Pattanayek R, et al. (2004) Visualizing a circadian clock protein: Crystal structure of KaiC and functional insights. Mol Cell 15(3):375-388.
27. Pattanayek R, et al. (2008) Structural model of the circadian clock KaiB-KaiC complex and mechanism for modulation of KaiC phosphorylation. EMBO J 27(12):1767-1778.
28. Murakami R, et al. (2012) 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(35):29506-29515.
29. Iwase R, et al. (2005) Functionally important substructures of circadian clock protein KaiB in a unique tetramer complex. J Biol Chem 280(52):43141-43149.
30. 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(8): 1688-1698.
31. 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(19):19127-19135.
32. Villarreal SA, et al. (2013) CryoEM and molecular dynamics of the circadian KaiB-KaiC complex indicates that KaiB monomers interact with KaiC and block ATP binding clefts. J Mol Biol 425(18):3311-3324.
33. Akiyama S, Nohara A, Ito K, Maéda Y (2008) Assembly and disassembly dynamics of the cyanobacterial periodosome. Mol Cell 29(6):703-716.
34. Pattanayek R, et al. (2011) Combined SAXS/EM based models of the S. elongatus posttranslational circadian oscillator and its interactions with the output His-kinase SasA. PLoS ONE 6(8):e23697.
35. Pattanayek R, Yadagiri KK, Ohi MD, Egli M (2013) Nature of KaiB-KaiC binding in the cyanobacterial circadian oscillator. Cell Cycle 12(5):810-817.
36. Chang YG, Tseng R, Kuo NW, LiWang A (2012) Rhythmic ring-ring stacking drives the circadian oscillator clockwise. Proc Natl Acad Sci USA 109(42):16847-16851.
37. de Vries SJ, van Dijk M, Bonvin AM (2010) The HADDOCK web server for data-driven biomolecular docking. Nat Protoc 5(5):883-897.
38. Dominguez C, Boelens R, Bonvin AMJJ (2003) HADDOCK: A protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125(7): 1731-1737.
39. Uetrecht C, Rose RJ, van Duijn E, Lorenzen K, Heck AJR (2010) Ion mobility mass spectrometry of proteins and protein assemblies. Chem Soc Rev 39(5):1633-1655.
40. Heck AJR (2008) Native mass spectrometry: A bridge between interactomics and structural biology. Nat Methods 5(11):927-933.
41. Benesch JLP (2009) Collisional activation of protein complexes: Picking up the pieces. J Am Soc Mass Spectrom 20(3):341-348.
42. Xu Y, et al. (2009) Intramolecular regulation of phosphorylation status of the circadian clock protein KaiC. PLoS ONE 4(11):e7509.
43. Chang YG, Kuo NW, Tseng R, LiWang A (2011) 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(35):14431-14436.
44. Konermann L, Pan J, Liu YH (2011) Hydrogen exchange mass spectrometry for studying protein structure and dynamics. Chem Soc Rev 40(3):1224-1234.
45. Nakajima M, Ito H, Kondo T (2010) In vitro regulation of circadian phosphorylation rhythm of cyanobacterial clock protein KaiC by KaiA and KaiB. FEBS Lett 584(5): 898-902.
46. 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(9): 2127-2134.
47. Tseng R, et al. (2013) KaiA assists the KaiB-KaiC interaction and KaiB/SasA competition in the circadian clock of cyanobacteria. J Mol Biol, 10.1016/j.jmb.2013.09.040.
48. Terauchi K, et al. (2007) ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria. Proc Natl Acad Sci USA 104(41):16377-16381.
49. Dong G, et al. (2010) Elevated ATPase activity of KaiC applies a circadian checkpoint on cell division in Synechococcus elongatus. Cell 140(4):529-539.
50. Phong C, Markson JS, Wilhoite CM, Rust MJ (2013) Robust and tunable circadian rhythms from differentially sensitive catalytic domains. Proc Natl Acad Sci USA 110(3): 1124-1129.
51. Murayama Y, et al. (2011) Tracking and visualizing the circadian ticking of the cyanobacterial clock protein KaiC in solution. EMBO J 30(1):68-78.
52. Tahallah N, Pinkse M, Maier CS, Heck AJR (2001) The effect of the source pressure on the abundance of ions of noncovalent protein assemblies in an electrospray ionization orthogonal time-of-flight instrument. Rapid Commun Mass Spectrom 15(8): 596-601.
53. Ruotolo BT, Benesch JLP, Sandercock AM, Hyung SJ, Robinson CV (2008) Ion mobilitymass spectrometry analysis of large protein complexes. Nat Protoc 3(7):1139-1152.
54. Bush MF, et al. (2010) Collision cross sections of proteins and their complexes: A calibration framework and database for gas-phase structural biology. Anal Chem 82(22):9557-9565.
55. de Vries SJ, et al. (2007) HADDOCK versus HADDOCK: New features and performance of HADDOCK2.0 on the CAPRI targets. Proteins 69(4):726-733.