Versatile properties of dynein molecules underlying regulation in flagellar oscillation
Abstract Dynein is a minus-end-directed motor that generates oscillatory motion in eukaryotic flagella. Cyclic beating, which is the most significant feature of a flagellum, occurs by sliding spatiotemporal regulation by dynein along microtubules. To elucidate oscillation generated by dynein in flag...
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| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-06-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-37242-6 |
| _version_ | 1797789800422440960 |
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| author | Takashi Fujiwara Chikako Shingyoji Hideo Higuchi |
| author_facet | Takashi Fujiwara Chikako Shingyoji Hideo Higuchi |
| author_sort | Takashi Fujiwara |
| collection | DOAJ |
| description | Abstract Dynein is a minus-end-directed motor that generates oscillatory motion in eukaryotic flagella. Cyclic beating, which is the most significant feature of a flagellum, occurs by sliding spatiotemporal regulation by dynein along microtubules. To elucidate oscillation generated by dynein in flagellar beating, we examined its mechanochemical properties under three different axonemal dissection stages. By starting from the intact 9 + 2 structure, we reduced the number of interacting doublets and determined three parameters, namely, the duty ratio, dwell time and step size, of the generated oscillatory forces at each stage. Intact dynein molecules in the axoneme, doublet bundle and single doublet were used to measure the force with optical tweezers. The mean forces per dynein determined under three axonemal conditions were smaller than the previously reported stall forces of axonemal dynein; this phenomenon suggests that the duty ratio is lower than previously thought. This possibility was further confirmed by an in vitro motility assay with purified dynein. The dwell time and step size estimated from the measured force were similar. The similarity in these parameters suggests that the essential properties of dynein oscillation are inherent to the molecule and independent of the axonemal architecture, composing the functional basis of flagellar beating. |
| first_indexed | 2024-03-13T01:55:48Z |
| format | Article |
| id | doaj.art-c645c68b44524f10addd7a5413f7b69f |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-13T01:55:48Z |
| publishDate | 2023-06-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-c645c68b44524f10addd7a5413f7b69f2023-07-02T11:15:38ZengNature PortfolioScientific Reports2045-23222023-06-0113111510.1038/s41598-023-37242-6Versatile properties of dynein molecules underlying regulation in flagellar oscillationTakashi Fujiwara0Chikako Shingyoji1Hideo Higuchi2Department of Biological Sciences, Graduate School of Science, The University of TokyoDepartment of Biological Sciences, Graduate School of Science, The University of TokyoDepartment of Physics, Graduate School of Science, The University of TokyoAbstract Dynein is a minus-end-directed motor that generates oscillatory motion in eukaryotic flagella. Cyclic beating, which is the most significant feature of a flagellum, occurs by sliding spatiotemporal regulation by dynein along microtubules. To elucidate oscillation generated by dynein in flagellar beating, we examined its mechanochemical properties under three different axonemal dissection stages. By starting from the intact 9 + 2 structure, we reduced the number of interacting doublets and determined three parameters, namely, the duty ratio, dwell time and step size, of the generated oscillatory forces at each stage. Intact dynein molecules in the axoneme, doublet bundle and single doublet were used to measure the force with optical tweezers. The mean forces per dynein determined under three axonemal conditions were smaller than the previously reported stall forces of axonemal dynein; this phenomenon suggests that the duty ratio is lower than previously thought. This possibility was further confirmed by an in vitro motility assay with purified dynein. The dwell time and step size estimated from the measured force were similar. The similarity in these parameters suggests that the essential properties of dynein oscillation are inherent to the molecule and independent of the axonemal architecture, composing the functional basis of flagellar beating.https://doi.org/10.1038/s41598-023-37242-6 |
| spellingShingle | Takashi Fujiwara Chikako Shingyoji Hideo Higuchi Versatile properties of dynein molecules underlying regulation in flagellar oscillation Scientific Reports |
| title | Versatile properties of dynein molecules underlying regulation in flagellar oscillation |
| title_full | Versatile properties of dynein molecules underlying regulation in flagellar oscillation |
| title_fullStr | Versatile properties of dynein molecules underlying regulation in flagellar oscillation |
| title_full_unstemmed | Versatile properties of dynein molecules underlying regulation in flagellar oscillation |
| title_short | Versatile properties of dynein molecules underlying regulation in flagellar oscillation |
| title_sort | versatile properties of dynein molecules underlying regulation in flagellar oscillation |
| url | https://doi.org/10.1038/s41598-023-37242-6 |
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