DOI: 10.1073/pnas.94.9.4378. Dynamic electron microscopy of ATP-induced myosin head movement in living muscle thick filaments

Dynamic electron microscopy of ATP-induced myosin head movement in living muscle thick filaments

10.1073/pnas.94.9.4378

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

Although muscle contraction is known to result from movement of the myosin heads on the thick filaments while attached to the thin filaments, the myosin head movement coupled with ATP hydrolysis still remains to be investigated. Using a gas environmental (hydration) chamber, in which biological specimens can be kept in wet state, we succeeded in recording images of living muscle thick filaments with gold position markers attached to the myosin heads. The position of individual myosin heads did not change appreciably with time in the absence of ATP, indicating stability of the myosin head mean position. On application of ATP, the position of individual myosin heads was found to move by ≈20 nm along the filament axis, whereas no appreciable movement of the filaments was detected. The ATP-induced myosin head movement was not observed in filaments in which ATPase activity of the myosin heads was eliminated. Application of ADP produced no appreciable myosin head movement. These results show that the ATP-induced myosin head movement takes place in the absence of the thin filaments. Because ATP reacts rapidly with the myosin head (M) to form the complex (M⋅ADP⋅P i ) with an average lifetime of >10 s, the observed myosin head movement may be mostly associated with reaction, M + ATP → M⋅ADP⋅P i . This work will open a new research field to study dynamic structural changes of individual biomolecules, which are kept in a living state in an electron microscope.

Bibliography

Sugi, H., Akimoto, T., Sutoh, K., Chaen, S., Oishi, N., & Suzuki, S. (1997). Dynamic electron microscopy of ATP-induced myosin head movement in living muscle thickâfilaments. Proceedings of the National Academy of Sciences, 94(9), 4378â4382.

Authors 6

Haruo Sugi (first)
Tsuyoshi Akimoto (additional)
Kazuo Sutoh (additional)
Shigeru Chaen (additional)
Noboru Oishi (additional)
Suechika Suzuki (additional)

References 23 Referenced 42

10.1016/S0096-4174(18)30128-8
10.1126/science.164.3886.1356
H Sugi Muscle Contraction and Cell Motility: Molecular and Cellular Aspects, ed H Sugi (Springer, Heidelberg), pp. 132–171 (1992). (10.1007/978-3-642-76927-6_5) / Muscle Contraction and Cell Motility: Molecular and Cellular Aspects by Sugi H (1992)
10.1146/annurev.ph.58.030196.000245
E P Butler, K F Hale Dynamic Experiments in the Electron Microscope (North Holland, Amsterdam, 1981). / Dynamic Experiments in the Electron Microscope by Butler E P (1981)
K Fukushima, A Ishikawa, A Fukami, S Suzuki, H Sugi, S Murakami 11th Int Congr Electron Microsc 1, 329–330 (1986). / 11th Int Congr Electron Microsc by Fukushima K (1986)
H Suda, A Ishikawa, A Fukami J Electron Microsc 41, 223–229 (1992). / J Electron Microsc by Suda H (1992)
K Fukushima, A Ishikawa, A Fukami J Electron Microsc 34, 47–51 (1985). / J Electron Microsc by Fukushima K (1985)
10.1007/978-1-4612-4428-8_36
K Fukushima Ph.D. Thesis (Nihon University, Tokyo, (in Japanese). (1988). / Ph.D. Thesis by Fukushima K (1988)
10.1016/0022-2836(74)90494-X
10.1016/0022-2836(89)90485-3
10.1126/science.3496662
10.1113/jphysiol.1991.sp018623
10.1093/oxfordjournals.jbchem.a124134
10.1021/bi00801a004
J S Wray J Muscle Res Cell Motil 8, 62, (abstr.). (1987). / J Muscle Res Cell Motil by Wray J S (1987)
10.1038/368113a0
10.1006/bbrc.1994.1336
10.1021/bi00785a033
10.1016/S0021-9258(18)67067-X
10.1073/pnas.85.6.1849
10.1073/pnas.89.13.6134

Dates

Type	When
Created	23 years ago (July 26, 2002, 10:31 a.m.)
Deposited	3 years, 4 months ago (April 13, 2022, 3:58 p.m.)
Indexed	4 months ago (April 17, 2025, 1:04 p.m.)
Issued	28 years, 3 months ago (April 29, 1997)
Published	28 years, 3 months ago (April 29, 1997)
Published Online	28 years, 3 months ago (April 29, 1997)
Published Print	28 years, 3 months ago (April 29, 1997)

Funders 0

None

BibTeX

@article{Sugi_1997, title={Dynamic electron microscopy of ATP-induced myosin head movement in living muscle thick filaments}, volume={94}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.94.9.4378}, DOI={10.1073/pnas.94.9.4378}, number={9}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Sugi, Haruo and Akimoto, Tsuyoshi and Sutoh, Kazuo and Chaen, Shigeru and Oishi, Noboru and Suzuki, Suechika}, year={1997}, month=apr, pages={4378–4382} }

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