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Lessons from a tarantula: new insights into muscle thick filament and myosin interacting-heads motif structure and function

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Abstract

The tarantula skeletal muscle X-ray diffraction pattern suggested that the myosin heads were helically arranged on the thick filaments. Electron microscopy (EM) of negatively stained relaxed tarantula thick filaments revealed four helices of heads allowing a helical 3D reconstruction. Due to its low resolution (5.0 nm), the unambiguous interpretation of densities of both heads was not possible. A resolution increase up to 2.5 nm, achieved by cryo-EM of frozen-hydrated relaxed thick filaments and an iterative helical real space reconstruction, allowed the resolving of both heads. The two heads, “free” and “blocked”, formed an asymmetric structure named the “interacting-heads motif” (IHM) which explained relaxation by self-inhibition of both heads ATPases. This finding made tarantula an exemplar system for thick filament structure and function studies. Heads were shown to be released and disordered by Ca2+-activation through myosin regulatory light chain phosphorylation, leading to EM, small angle X-ray diffraction and scattering, and spectroscopic and biochemical studies of the IHM structure and function. The results from these studies have consequent implications for understanding and explaining myosin super-relaxed state and thick filament activation and regulation. A cooperative phosphorylation mechanism for activation in tarantula skeletal muscle, involving swaying constitutively Ser35 mono-phosphorylated free heads, explains super-relaxation, force potentiation and post-tetanic potentiation through Ser45 mono-phosphorylated blocked heads. Based on this mechanism, we propose a swaying-swinging, tilting crossbridge-sliding filament for tarantula muscle contraction.

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Acknowledgements

We thank Dr. John Wray for permission to reproduce unpublished tarantula diffraction patterns, and Drs. Guidenn Sulbarán, Jesús Mavárez and Gustavo Márquez for help with the manuscript. Molecular graphics images were produced using the UCSF Chimera package (Pettersen et al. 2004) from the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco (supported by the National Institutes of Health grant P41 RR-01081). This work was supported in part by Centro de Biología Estructural del Mercosur (www.cebem-lat.org) (to R.P.), Russian Foundation for Basic Research (15-04-02174 to N.K., 16-04-00693 to A.T.), Cornell High Energy Synchrotron Source (CHESS) is supported by the NSF & NIH/NIGMS via NSF award DMR-1332208, and the MacCHESS resources are supported by NIGMS award GM-103485 (to R.E.G.) and the Howard Hughes Medical Institute (to R.P.).

We dedicate this paper to the memory of Dr. Hugh E. Huxley.

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Authors and Affiliations

  1. Centro de Biología Estructural “Humberto Fernández-Morán”, Instituto Venezolano de Investigaciones Científicas (IVIC), Apdo. 20632, Caracas, 1020A, Venezuela

    Lorenzo Alamo, Antonio Pinto & Raúl Padrón

  2. Institute of Mechanics, Moscow State University, Mitchurinsky prosp. 1, Moscow, 119992, Russia

    Natalia Koubassova & Andrey Tsaturyan

  3. Macromolecular Diffraction Facility, Cornell High Energy Synchrotron Source, Ithaca, NY, USA

    Richard Gillilan

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  1. Lorenzo Alamo
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  2. Natalia Koubassova
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  3. Antonio Pinto
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  4. Richard Gillilan
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  5. Andrey Tsaturyan
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  6. Raúl Padrón
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Correspondence to Raúl Padrón.

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Lorenzo Alamo declares that he has no conflicts of interest. Natalia Koubassova declares that she has no conflicts of interest. Antonio Pinto declares that he has no conflicts of interest. Richard Gillilan declares that he has no conflicts of interest. Andrey Tsaturyan declares that he has no conflicts of interest. Raúl Padrón declares that he has no conflicts of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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This article is part of a Special Issue on ‘Latin America’ edited by Pietro Ciancaglini and Rosangela Itri.

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Alamo, L., Koubassova, N., Pinto, A. et al. Lessons from a tarantula: new insights into muscle thick filament and myosin interacting-heads motif structure and function. Biophys Rev 9, 461–480 (2017). https://doi.org/10.1007/s12551-017-0295-1

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