Elongation and Contraction of Scallop Sarcoplasmic Reticulum (SR): ATP Stabilizes Ca2+-ATPase Crystalline Array Elongation of SR Vesicles

Nakamura, Jun; Maruyama, Yuusuke; Tajima, Genichi; Suwa, Makiko; Sato, Chikara

doi:10.3390/ijms23063311

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Elongation and Contraction of Scallop Sarcoplasmic Reticulum (SR): ATP Stabilizes Ca²⁺-ATPase Crystalline Array Elongation of SR Vesicles

by

Jun Nakamura

^1,*,

Yuusuke Maruyama

¹,

Genichi Tajima

²,

Makiko Suwa

³ and

Chikara Sato

^1,*

¹

Health and Medical Institute, National Institute of Advanced Industrial Science and Technology (AIST), Central 6, 1-1-4 Umezono, Tsukuba 305-8568, Ibaraki, Japan

²

Institute for Excellence in Higher Education, Tohoku University, 41 Kawauchi, Aoba-ku, Sendai 980-8576, Miyagi, Japan

³

Biological Science Course, Graduate School of Science and Engineering, Aoyama Gakuin University, 5-10-1 Fuchinobe, Chuou-ku, Sagamihara 252-5258, Kanagawa, Japan

^*

Authors to whom correspondence should be addressed.

Int. J. Mol. Sci. 2022, 23(6), 3311; https://doi.org/10.3390/ijms23063311

Submission received: 31 December 2021 / Revised: 7 March 2022 / Accepted: 10 March 2022 / Published: 18 March 2022

(This article belongs to the Special Issue Electron Microscopy for Hydrophilic Specimen and Related Measurements)

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Abstract

The Ca²⁺-ATPase is an integral transmembrane Ca²⁺ pump of the sarcoplasmic reticulum (SR). Crystallization of the cytoplasmic surface ATPase molecules of isolated scallop SR vesicles was studied at various calcium concentrations by negative stain electron microscopy. In the absence of ATP, round SR vesicles displaying an assembly of small crystalline patches of ATPase molecules were observed at 18 µM [Ca²⁺]. These partly transformed into tightly elongated vesicles containing ATPase crystalline arrays at low [Ca²⁺] (≤1.3 µM). The arrays were classified as ‘’tetramer’’, “two-rail” (like a railroad) and ‘’monomer’’. Their crystallinity was low, and they were unstable. In the presence of ATP (5 mM) at a low [Ca²⁺] of ~0.002 µM, “two-rail” arrays of high crystallinity appeared more frequently in the tightly elongated vesicles and the distinct tetramer arrays disappeared. During prolonged (~2.5 h) incubation, ATP was consumed and tetramer arrays reappeared. A specific ATPase inhibitor, thapsigargin, prevented both crystal formation and vesicle elongation in the presence of ATP. Together with the second part of this study, these data suggest that the ATPase forms tetramer units and longer tetramer crystalline arrays to elongate SR vesicles, and that the arrays transform into more stable “two-rail” forms in the presence of ATP at low [Ca²⁺].

Keywords: scallop; sarcoplasmic reticulum; Ca²⁺-ATPase; two-dimensional crystallization; ATP; membrane endoskeleton; transmission microscopy; cell morphology; cell dynamics; thapsigargin

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MDPI and ACS Style

Nakamura, J.; Maruyama, Y.; Tajima, G.; Suwa, M.; Sato, C. Elongation and Contraction of Scallop Sarcoplasmic Reticulum (SR): ATP Stabilizes Ca²⁺-ATPase Crystalline Array Elongation of SR Vesicles. Int. J. Mol. Sci. 2022, 23, 3311. https://doi.org/10.3390/ijms23063311

AMA Style

Nakamura J, Maruyama Y, Tajima G, Suwa M, Sato C. Elongation and Contraction of Scallop Sarcoplasmic Reticulum (SR): ATP Stabilizes Ca²⁺-ATPase Crystalline Array Elongation of SR Vesicles. International Journal of Molecular Sciences. 2022; 23(6):3311. https://doi.org/10.3390/ijms23063311

Chicago/Turabian Style

Nakamura, Jun, Yuusuke Maruyama, Genichi Tajima, Makiko Suwa, and Chikara Sato. 2022. "Elongation and Contraction of Scallop Sarcoplasmic Reticulum (SR): ATP Stabilizes Ca²⁺-ATPase Crystalline Array Elongation of SR Vesicles" International Journal of Molecular Sciences 23, no. 6: 3311. https://doi.org/10.3390/ijms23063311

APA Style

Nakamura, J., Maruyama, Y., Tajima, G., Suwa, M., & Sato, C. (2022). Elongation and Contraction of Scallop Sarcoplasmic Reticulum (SR): ATP Stabilizes Ca²⁺-ATPase Crystalline Array Elongation of SR Vesicles. International Journal of Molecular Sciences, 23(6), 3311. https://doi.org/10.3390/ijms23063311

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Elongation and Contraction of Scallop Sarcoplasmic Reticulum (SR): ATP Stabilizes Ca²⁺-ATPase Crystalline Array Elongation of SR Vesicles

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