Abstract
The transcription–translation feedback model has had a huge impact on the study of biological clocks. The study of the cyanobacterial circadian system has defied this influential model and set a milestone in chronobiology with the establishment of the in vitro reconstituted oscillator system. As a researcher who had the good fortune to witness this turning point, I would like to review the process from a very personal perspective. I have been strongly influenced by science studies, especially the history and philosophy of science: indeed, my main reason for choosing the biological clock as my research topic in the first place was my interest in its scientific-philosophical and cultural-historical implications. History is always destined to be recorded by those who remain and is always subject to bias. If this same topic was recalled by, e.g., Takao Kondo, Carl Johnson, or anyone else who was engaged in the same events, it would probably be described completely differently. I would appreciate it if you read this chapter with that perspective in mind.
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References
Antoch MP, Song EJ, Chang AM, Vitaterna MH, Zhao Y, Wilsbacher LD, Sangoram AM, King DP, Pinto LH, Takahashi JS (1997) Functional identification of the mouse circadian Clock gene by transgenic BAC rescue. Cell 89:655–657
Aronson BD, Johnson KA, Loros JJ, Dunlap JC (1994) Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science 263:1578–1584
Crosthwaite SK, Loros JJ, Dunlap JC (1995) Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell 81:1003–1012
Dunlap JC (1998) Common threads in eukaryotic circadian systems. Curr Opin Genet Dev 8:400–406
Elowitz MB, Leibler S (2000) A synthetic oscillatory network of transcriptional regulators. Nature 403:335–338
Goodwin BC (1963) Temporal organization in cells; a dynamic theory of cellular control processes. Academic, London
Hardin PE, Hall JC, Rosbash M (1990) Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343:536–540
Helfrich C, Engelmann W (1987) Evidences for circadian rhythmicity in the per0 mutant of Drosophila melanogaster. Z Naturforsch C J Biosci 42:1335–1338
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 cyanobacteria. Science 281:1519–1523
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
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 cyanobacteria. Cell 101:223–233
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
Jacob F, Monod J (1961) On the regulation of gene activity. Cold Spring Harb Symp Quant Biol 26:193–211
Johnson CH, Roeber JF, Hastings JW (1984) Circadian changes in enzyme concentration account for rhythm of enzyme activity in Gonyaulax. Science 223:1428–1430
King DP, Zhao Y, Sangoram AM, Wilsbacher LD, Tanaka M, Antoch MP, Steeves TD, Vitaterna MH, Kornhauser JM, Lowrey PL, Turek FW, Takahashi JS (1997) Positional cloning of the mouse circadian clock gene. Cell 89:641–653
Lakin-Thomas P (1998) Choline depletion, frq mutations, and temperature compensation of the circadian rhythm in Neurospora crassa. J Biol Rhythm 13:268–277
Lakin-Thomas PL, Brody S (2000) Circadian rhythms in Neurospora crassa: lipid deficiencies restore robust rhythmicity to null frequency and white-collar mutants. Proc Natl Acad Sci U S A 97:256–261
Matsumoto A (2002) Temperature-dependent circadian locomotion rhythm in the per0 mutant of Drosophila melanogaster. J Jpn Soc Chronobiol 8:11–15. (in Japanese)
Mergenhagen D, Schweiger HG (1975) The effect of different inhibitors of transcription and translation on the expression and control of circadian rhythm in individual cells of Acetabularia. Exp Cell Res 94:321–326
Merrow M, Brunner M, Roenneberg T (1999) Assignment of circadian function for the Neurospora clock gene frequency. Nature 399:584–586. https://doi.org/10.1038/21190
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 U S A 99:17203–17208
Nakahira Y, Katayama M, Miyashita H, Kutsuna S, Iwasaki H, Oyama T, Kondo T (2004) Global gene repression by KaiC as a master process of prokaryotic circadian system. Proc Natl Acad Sci U S A 101:881–885
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(5720):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 U S A 97:495–499
Pokhilko A, Fernández AP, Edwards KD, Sounthern MM, Halliday KJ, Millar AJ (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol 8:574
Sweeney BM, Haxo FT (1961) Persistence of a photosynthetic rhythm in enucleated Acetabularia. Science 134:1361
Sweeney BM, Tuffli CF, Rubin RH (1967) The circadian rhythm in photosynthesis in Acetabularia in the presence of actinomycin D, puromycin, and chloramphenicol. J Gen Physiol 50:647–659
Takano S, Tomita J, Sonoike K, Iwasaki H (2015) The initiation of nocturnal dormancy in Synechococcus as an active process. BMC Biol 13:36
Tomita J, Nakajima M, Kondo T, Iwasaki H (2005) No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307(5707):251–254
Ukai-Tadenuma M, Yamada RG, Xu H, Ripperger JA, Liu AC, Ueda HR (2011) Delay in feedback repression by Cryptochrome 1 is required for circadian clock function. Cell 144:268–281
Xu Y, Mori T, Johnson CH (2000) Circadian clock-protein expression in cyanobacteria: rhythms and phase setting. EMBO J 19:3349–3357
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
Yang Z, Sehgal A (2001) Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 29:453–467
Acknowledgments
There are many colleagues and collaborators to whom I owe a debt of gratitude, but I would like to thank initially Takao Kondo, Masahiro Ishiura, Carl Johnson, and Susan Golden for pioneering the field and guiding me in the early days. Until around 2003, there was active interaction among these groups, especially among students, and we had a habit of showing each other manuscripts before they were submitted. When I think about it now, it was an honor for me to have my first manuscript very carefully corrected by Susan even though she was not an author. Without the friendly collaboration with Takao Kondo, Shinsuke Kutsuna, Taeko Nishiwaki, Jun Tomita, Masato Nakajima, Yohko Kitayama, Keiko Imai, Hakuto Kageyama, Hiroshi Ito, Kazuki Terauchi, and other excellent teammates, the results I have described here would not have been possible. Also, Tetsuya Mori, Akira Matsumoto, Till Roenneberg, Martha Merrow, Pat Lakin-Thomas, and Hiroki Ueda, with whom I discussed possibilities outside of the TTFL, were my few comrades at the time. I would like to thank them for their support. I thank Taeko and Jun for kindly providing copies of their valuable notebook for this chapter. Finally, I thank Carl for reading the manuscript carefully with valuable comments, and Taeko for providing detailed information on the process of in vitro reconstitution studies.
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Iwasaki, H. (2021). A Retrospective: On Disproving the Transcription–Translation Feedback Loop Model in Cyanobacteria. In: Johnson, C.H., Rust, M.J. (eds) Circadian Rhythms in Bacteria and Microbiomes. Springer, Cham. https://doi.org/10.1007/978-3-030-72158-9_3
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DOI: https://doi.org/10.1007/978-3-030-72158-9_3
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