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Electrostatic and bending energies predict staggering and splaying in nonmuscle myosin II minifilaments.
PLoS Comput Biol. 2020 Jul; 16(7):e1007801.PC

Abstract

Recent experiments with super-resolution live cell microscopy revealed that nonmuscle myosin II minifilaments are much more dynamic than formerly appreciated, often showing plastic processes such as splitting, concatenation and stacking. Here we combine sequence information, electrostatics and elasticity theory to demonstrate that the parallel staggers at 14.3, 43.2 and 72 nm have a strong tendency to splay their heads away from the minifilament, thus potentially initiating the diverse processes seen in live cells. In contrast, the straight antiparallel stagger with an overlap of 43 nm is very stable and likely initiates minifilament nucleation. Using stochastic dynamics in a newly defined energy landscape, we predict that the optimal parallel staggers between the myosin rods are obtained by a trial-and-error process in which two rods attach and re-attach at different staggers by rolling and zipping motion. The experimentally observed staggers emerge as the configurations with the largest contact times. We find that contact times increase from isoforms C to B to A, that A-B-heterodimers are surprisingly stable and that myosin 18A should incorporate into mixed filaments with a small stagger. Our findings suggest that nonmuscle myosin II minifilaments in the cell are first formed by isoform A and then convert to mixed A-B-filaments, as observed experimentally.

Authors+Show Affiliations

Institute for Theoretical Physics and BioQuant, Heidelberg University, Heidelberg, Germany.Institute for Theoretical Physics and BioQuant, Heidelberg University, Heidelberg, Germany.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

32628657

Citation

Kaufmann, Tom L., and Ulrich S. Schwarz. "Electrostatic and Bending Energies Predict Staggering and Splaying in Nonmuscle Myosin II Minifilaments." PLoS Computational Biology, vol. 16, no. 7, 2020, pp. e1007801.
Kaufmann TL, Schwarz US. Electrostatic and bending energies predict staggering and splaying in nonmuscle myosin II minifilaments. PLoS Comput Biol. 2020;16(7):e1007801.
Kaufmann, T. L., & Schwarz, U. S. (2020). Electrostatic and bending energies predict staggering and splaying in nonmuscle myosin II minifilaments. PLoS Computational Biology, 16(7), e1007801. https://doi.org/10.1371/journal.pcbi.1007801
Kaufmann TL, Schwarz US. Electrostatic and Bending Energies Predict Staggering and Splaying in Nonmuscle Myosin II Minifilaments. PLoS Comput Biol. 2020;16(7):e1007801. PubMed PMID: 32628657.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Electrostatic and bending energies predict staggering and splaying in nonmuscle myosin II minifilaments. AU - Kaufmann,Tom L, AU - Schwarz,Ulrich S, Y1 - 2020/07/06/ PY - 2020/03/12/received PY - 2020/05/28/accepted PY - 2020/07/16/revised PY - 2020/7/7/pubmed PY - 2020/7/7/medline PY - 2020/7/7/entrez SP - e1007801 EP - e1007801 JF - PLoS computational biology JO - PLoS Comput. Biol. VL - 16 IS - 7 N2 - Recent experiments with super-resolution live cell microscopy revealed that nonmuscle myosin II minifilaments are much more dynamic than formerly appreciated, often showing plastic processes such as splitting, concatenation and stacking. Here we combine sequence information, electrostatics and elasticity theory to demonstrate that the parallel staggers at 14.3, 43.2 and 72 nm have a strong tendency to splay their heads away from the minifilament, thus potentially initiating the diverse processes seen in live cells. In contrast, the straight antiparallel stagger with an overlap of 43 nm is very stable and likely initiates minifilament nucleation. Using stochastic dynamics in a newly defined energy landscape, we predict that the optimal parallel staggers between the myosin rods are obtained by a trial-and-error process in which two rods attach and re-attach at different staggers by rolling and zipping motion. The experimentally observed staggers emerge as the configurations with the largest contact times. We find that contact times increase from isoforms C to B to A, that A-B-heterodimers are surprisingly stable and that myosin 18A should incorporate into mixed filaments with a small stagger. Our findings suggest that nonmuscle myosin II minifilaments in the cell are first formed by isoform A and then convert to mixed A-B-filaments, as observed experimentally. SN - 1553-7358 UR - https://www.unboundmedicine.com/medline/citation/32628657/Electrostatic_and_bending_energies_predict_staggering_and_splaying_in_nonmuscle_myosin_II_minifilaments L2 - https://dx.plos.org/10.1371/journal.pcbi.1007801 DB - PRIME DP - Unbound Medicine ER -
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