Growing Old Too Early: Skeletal Muscle Single Fiber Biomechanics in Ageing R349P Desmin Knock-in Mice Using the MyoRobot Technology

Pollmann, Charlotte; Haug, Michael; Reischl, Barbara; Prölß, Gerhard; Pöschel, Thorsten; Rupitsch, Stefan J; Clemen, Christoph S; Schröder, Rolf; Friedrich, Oliver

doi:10.3390/ijms21155501

Open AccessArticle

Growing Old Too Early: Skeletal Muscle Single Fiber Biomechanics in Ageing R349P Desmin Knock-in Mice Using the MyoRobot Technology

by

Charlotte Pollmann

^1,†,

Michael Haug

^1,2,3,*,†

,

Barbara Reischl

¹,

Gerhard Prölß

¹,

Thorsten Pöschel

⁴,

Stefan J Rupitsch

⁵,

Christoph S Clemen

^6,7,8,

Rolf Schröder

^7,9 and

Oliver Friedrich

^{1,2,3,9,10,11}

¹

Institute of Medical Biotechnology, Friedrich-Alexander-University Erlangen-Nürnberg, Paul-Gordan-Str. 3, 91052 Erlangen, Bavaria, Germany

²

Graduate School in Advanced Optical Technologies, Paul-Gordan-Str. 6, 91052 Erlangen, Bavaria, Germany

³

School of Medical Sciences, University of New South Wales, Wallace Wurth Building, 18 High St, Sydney, NSW 2052, Australia

⁴

Institute of Multi Scale Simulation of Particulate Systems, Friedrich-Alexander-University Erlangen-Nürnberg, Nägelbachstr. 49b, 91052 Erlangen, Bavaria, Germany

⁵

Institute of Sensor Technology, Friedrich-Alexander-University Erlangen-Nürnberg, Paul-Gordan-Str. 3/5, 91052 Erlangen, Bavaria, Germany

⁶

German Aerospace Center (DLR), Institute of Aerospace Medicine, Linder Höhe, 51147 Cologne, North Rhine-Westphalia, Germany

⁷

Institute of Neuropathology, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nürnberg, Schwabachanlage 6, 91054 Erlangen, Bavaria, Germany

⁸

Insitute of Vegetative Physiology, Medical Faculty, University of Cologne, Center of Physiology and Pathophysiology, Robert-Koch-Street 39, 50931 Cologne, North Rhine-Westphalia, Germany

⁹

Muscle Research Center Erlangen (MURCE), Friedrich-Alexander-University Erlangen-Nürnberg, 91054 Erlangen, Bavaria, Germany

¹⁰

Victor Chang Cardiac Research Institute, Lowy Packer Building, 405 Liverpool St, Sydney, NSW 2010, Australia

¹¹

Optical Imaging Centre Erlangen OICE, Cauerstr. 3, 91058 Erlangen, Bavaria, Germany

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^*

Author to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Int. J. Mol. Sci. 2020, 21(15), 5501; https://doi.org/10.3390/ijms21155501

Submission received: 2 July 2020 / Revised: 21 July 2020 / Accepted: 28 July 2020 / Published: 31 July 2020

(This article belongs to the Section Molecular Pathology, Diagnostics, and Therapeutics)

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Abstract

Muscle biomechanics relies on active motor protein assembly and passive strain transmission through cytoskeletal structures. The desmin filament network aligns myofibrils at the z-discs, provides nuclear–sarcolemmal anchorage and may also serve as memory for muscle repositioning following large strains. Our previous analyses of R349P desmin knock-in mice, an animal model for the human R350P desminopathy, already depicted pre-clinical changes in myofibrillar arrangement and increased fiber bundle stiffness. As the effect of R349P desmin on axial biomechanics in fully differentiated single muscle fibers is unknown, we used our MyoRobot to compare passive visco-elasticity and active contractile biomechanics in single fibers from fast- and slow-twitch muscles from adult to senile mice, hetero- or homozygous for the R349P desmin mutation with wild type littermates. We demonstrate that R349P desmin presence predominantly increased axial stiffness in both muscle types with a pre-aged phenotype over wild type fibers. Axial viscosity and Ca

^{2 +}

-mediated force were largely unaffected. Mutant single fibers showed tendencies towards faster unloaded shortening over wild type fibers. Effects of aging seen in the wild type appeared earlier in the mutant desmin fibers. Our single-fiber experiments, free of extracellular matrix, suggest that compromised muscle biomechanics is not exclusively attributed to fibrosis but also originates from an impaired intermediate filament network.

Keywords: biomechatronics; desminopathy; R349P desmin; single fibers; skeletal muscle

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MDPI and ACS Style

Pollmann, C.; Haug, M.; Reischl, B.; Prölß, G.; Pöschel, T.; Rupitsch, S.J.; Clemen, C.S.; Schröder, R.; Friedrich, O. Growing Old Too Early: Skeletal Muscle Single Fiber Biomechanics in Ageing R349P Desmin Knock-in Mice Using the MyoRobot Technology. Int. J. Mol. Sci. 2020, 21, 5501. https://doi.org/10.3390/ijms21155501

AMA Style

Pollmann C, Haug M, Reischl B, Prölß G, Pöschel T, Rupitsch SJ, Clemen CS, Schröder R, Friedrich O. Growing Old Too Early: Skeletal Muscle Single Fiber Biomechanics in Ageing R349P Desmin Knock-in Mice Using the MyoRobot Technology. International Journal of Molecular Sciences. 2020; 21(15):5501. https://doi.org/10.3390/ijms21155501

Chicago/Turabian Style

Pollmann, Charlotte, Michael Haug, Barbara Reischl, Gerhard Prölß, Thorsten Pöschel, Stefan J Rupitsch, Christoph S Clemen, Rolf Schröder, and Oliver Friedrich. 2020. "Growing Old Too Early: Skeletal Muscle Single Fiber Biomechanics in Ageing R349P Desmin Knock-in Mice Using the MyoRobot Technology" International Journal of Molecular Sciences 21, no. 15: 5501. https://doi.org/10.3390/ijms21155501

APA Style

Pollmann, C., Haug, M., Reischl, B., Prölß, G., Pöschel, T., Rupitsch, S. J., Clemen, C. S., Schröder, R., & Friedrich, O. (2020). Growing Old Too Early: Skeletal Muscle Single Fiber Biomechanics in Ageing R349P Desmin Knock-in Mice Using the MyoRobot Technology. International Journal of Molecular Sciences, 21(15), 5501. https://doi.org/10.3390/ijms21155501

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Growing Old Too Early: Skeletal Muscle Single Fiber Biomechanics in Ageing R349P Desmin Knock-in Mice Using the MyoRobot Technology

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