ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC

Fumio Hayashi, Hirofumi Suzuki, Ryo Iwase, Tatsuya Uzumaki, Asako Miyake, Jian-Ren Shen, Katsumi Imada, Yukio Furukawa, Koji Yonekura, Keiichi Namba, Masahiro Ishiura

Research output: Contribution to journalArticle

92 Citations (Scopus)

Abstract

Background: KaiA, KaiB and KaiC are cyanobacterial circadian clock proteins. KaiC contains two ATP/GTP-binding Walker's motif As, and mutations in these regions affect the clock oscillations. Results: ATP induced the hexamerization of KaiC. The Km value for the ATP for the hexamerization was 1.9 μM. Triphosphate nucleotides bound to the two Walker's motif As, and their binding functioned cooperatively for the hexamerization. An unhydrolysable substrate, 5′-adenylylimidodiphosphate (AMPPNP), also induced the hexamerization, indicating that nucleotide binding, but not its hydrolysis, is essential for the hexamerization. Mutations in each of the two Walker's motif As that affect the clock phenotype increased the Km value for ATP and inhibited the hexamerization. Thus, the KaiC hexamerization seems to be necessary for its clock function. The KaiC hexamer has the shape of a hexagonal pot with a diameter and height of approximately 100 Å and with a relatively large cavity (73 Å deep and 18-34 Å wide) inside. This pot-shaped structure suggests that KaiC functions in a similar manner to F1-ATPase, helicase or ATP-dependent protease/chaperon, all of which have dynamic activities inside the central cavity of their hexameric rings. Conclusion: ATP-induced KaiC hexamerization is necessary for the clock function of KaiC.

Original languageEnglish
Pages (from-to)287-296
Number of pages10
JournalGenes to Cells
Volume8
Issue number3
DOIs
Publication statusPublished - Mar 1 2003
Externally publishedYes

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Circadian Clocks
Adenosine Triphosphate
Adenylyl Imidodiphosphate
Proteins
Nucleotides
ATP-Dependent Proteases
Mutation
Proton-Translocating ATPases
Guanosine Triphosphate
Hydrolysis
Phenotype

ASJC Scopus subject areas

  • Genetics
  • Cell Biology

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ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. / Hayashi, Fumio; Suzuki, Hirofumi; Iwase, Ryo; Uzumaki, Tatsuya; Miyake, Asako; Shen, Jian-Ren; Imada, Katsumi; Furukawa, Yukio; Yonekura, Koji; Namba, Keiichi; Ishiura, Masahiro.

In: Genes to Cells, Vol. 8, No. 3, 01.03.2003, p. 287-296.

Research output: Contribution to journalArticle

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 to Cells, vol. 8, no. 3, pp. 287-296. https://doi.org/10.1046/j.1365-2443.2003.00633.x
Hayashi, Fumio ; Suzuki, Hirofumi ; Iwase, Ryo ; Uzumaki, Tatsuya ; Miyake, Asako ; Shen, Jian-Ren ; Imada, Katsumi ; Furukawa, Yukio ; Yonekura, Koji ; Namba, Keiichi ; Ishiura, Masahiro. / ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. In: Genes to Cells. 2003 ; Vol. 8, No. 3. pp. 287-296.
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abstract = "Background: KaiA, KaiB and KaiC are cyanobacterial circadian clock proteins. KaiC contains two ATP/GTP-binding Walker's motif As, and mutations in these regions affect the clock oscillations. Results: ATP induced the hexamerization of KaiC. The Km value for the ATP for the hexamerization was 1.9 μM. Triphosphate nucleotides bound to the two Walker's motif As, and their binding functioned cooperatively for the hexamerization. An unhydrolysable substrate, 5′-adenylylimidodiphosphate (AMPPNP), also induced the hexamerization, indicating that nucleotide binding, but not its hydrolysis, is essential for the hexamerization. Mutations in each of the two Walker's motif As that affect the clock phenotype increased the Km value for ATP and inhibited the hexamerization. Thus, the KaiC hexamerization seems to be necessary for its clock function. The KaiC hexamer has the shape of a hexagonal pot with a diameter and height of approximately 100 {\AA} and with a relatively large cavity (73 {\AA} deep and 18-34 {\AA} wide) inside. This pot-shaped structure suggests that KaiC functions in a similar manner to F1-ATPase, helicase or ATP-dependent protease/chaperon, all of which have dynamic activities inside the central cavity of their hexameric rings. Conclusion: ATP-induced KaiC hexamerization is necessary for the clock function of KaiC.",
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AB - Background: KaiA, KaiB and KaiC are cyanobacterial circadian clock proteins. KaiC contains two ATP/GTP-binding Walker's motif As, and mutations in these regions affect the clock oscillations. Results: ATP induced the hexamerization of KaiC. The Km value for the ATP for the hexamerization was 1.9 μM. Triphosphate nucleotides bound to the two Walker's motif As, and their binding functioned cooperatively for the hexamerization. An unhydrolysable substrate, 5′-adenylylimidodiphosphate (AMPPNP), also induced the hexamerization, indicating that nucleotide binding, but not its hydrolysis, is essential for the hexamerization. Mutations in each of the two Walker's motif As that affect the clock phenotype increased the Km value for ATP and inhibited the hexamerization. Thus, the KaiC hexamerization seems to be necessary for its clock function. The KaiC hexamer has the shape of a hexagonal pot with a diameter and height of approximately 100 Å and with a relatively large cavity (73 Å deep and 18-34 Å wide) inside. This pot-shaped structure suggests that KaiC functions in a similar manner to F1-ATPase, helicase or ATP-dependent protease/chaperon, all of which have dynamic activities inside the central cavity of their hexameric rings. Conclusion: ATP-induced KaiC hexamerization is necessary for the clock function of KaiC.

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