Optical prediction of single muscle fiber force production using a combined biomechatronics and second harmonic generation imaging approach

Dominik Schneidereit; Stefanie Nübler; Gerhard Prölß; Barbara Reischl; Sebastian Schürmann; Oliver J Müller; Oliver Friedrich

doi:10.1038/s41377-018-0080-3

Go to Nature Website

Your Location：

Home >

Browse articles >

Optical prediction of single muscle fiber force production using a combined biomechatronics and second harmonic generation imaging approach

Original Articles

- Optical prediction of single muscle fiber force production using a combined biomechatronics and second harmonic generation imaging approach
- Light: Science & Applications Vol. 7, Issue 6, Pages: 797-810(2018)
- Affiliations：
  
  1.Institute of Medical Biotechnology, Friedrich-Alexander-University (FAU) Erlangen-Nürnberg, Paul-Gordan-Str. 3, 91052, Erlangen, Germany
  2.Erlangen Graduate School in Advanced Optical Technologies (SAOT), FAU Erlangen-Nürnberg, Paul-Gordan-Str. 7, 91052, Erlangen, Germany
  3.Muscle Research Center Erlangen (MURCE), Friedrich-Alexander-University Erlangen-Nürnberg, Erlangen, Germany
  4.Department of Internal Medicine Ⅲ, University of Kiel, Arnold-Heller-Str. 3, 24105, Kiel, Germany
  5.DZHK (German Center for Cardiovascular Research) Partner Site Hamburg/Kiel/Lübeck, Kiel, Germany
- Author bio：
  
  Oliver Friedrich (oliver.friedrich@mbt.uni-erlangen.de)
- Funds：
- DOI：10.1038/s41377-018-0080-3
  CLC：
Scan for full text
Schneidereit, D. et al. Optical prediction of single muscle fiber force production using a combined biomechatronics and second harmonic generation imaging approach. Light: Science & Applications, 6, 797-810 (2018).
DOI：

Schneidereit, D. et al. Optical prediction of single muscle fiber force production using a combined biomechatronics and second harmonic generation imaging approach. Light: Science & Applications, 6, 797-810 (2018). DOI： 10.1038/s41377-018-0080-3.

摘要

Abstract

Skeletal muscle is an archetypal organ whose structure is tuned to match function. The magnitude of order in muscle fibers and myofibrils containing motor protein polymers determines the directed force output of the summed force vectors and, therefore, the muscle's power performance on the structural level. Structure and function can change dramatically during disease states involving chronic remodeling. Cellular remodeling of the cytoarchitecture has been pursued using noninvasive and label-free multiphoton second harmonic generation (SHG) microscopy. Hereby, structure parameters can be extracted as a measure of myofibrillar order and thus are suggestive of the force output that a remodeled structure can still achieve. However, to date, the parameters have only been an indirect measure, and a precise calibration of optical SHG assessment for an exerted force has been elusive as no technology in existence correlates these factors. We engineered a novel, automated, high-precision biomechatronics system into a multiphoton microscope allows simultaneous isometric Ca,2+,-graded force or passive viscoelasticity measurements and SHG recordings. Using this ,MechaMorph, system, we studied force and SHG in single EDL muscle fibers from wt and ,mdx, mice; the latter serves as a model for compromised force and abnormal myofibrillar structure. We present Ca,2+,-graded isometric force, pCa-force curves, passive viscoelastic parameters and 3D structure in the same fiber for the first time. Furthermore, we provide a direct calibration of isometric force to morphology, which allows noninvasive prediction of the force output of single fibers from only multiphoton images, suggesting a potential application in the diagnosis of myopathies.

关键词

Keywords

references

Clark, K. A., McElhinny, A. S., Beckerle, M. C. & Gregorio, C. C. Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell. Dev. Biol. 18, 637–706 (2002).

Goldfarb, L. G. & Dalakas, M. C. Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J. Clin. Invest. 119, 1806–1813 (2009).

Both, M. et al. Second harmonic imaging of intrinsic signals in muscle fibers in situ. J. Biomed. Opt. 9, 882–892 (2004).

Rode, C., Siebert, T., Tomalka, A. & Blickhan, R. Myosin filament sliding through the Z-disc relates striated muscle fibre structure to function. Proc. Biol. Sci. 283, 20153030 (2016).

Berchtold, M. W., Brinkmeier, H. & Müntener, M. Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol. Rev. 80, 1215–1265 (2000).

Matsakas, A. & Patel, K. Skeletal muscle fibre plasticity in response to selected environmental and physiological stimuli. Histol. Histopathol. 24, 611–629 (2009).

Abmayr, S. M. & Pavlath, G. K. Myoblast fusion: lessons from flies and mice. Development 139, 641–656 (2012).

Loell, I. et al. Effects on muscle tissue remodeling and lipid metabolism in muscle tissue from adult patients with polymyositis or dermatomyositis treated with immunosuppressive agents. Arthritis Res. Ther. 18, 136 (2016).

Devine, R. D., Bicer, S., Reiser, P. J., Velten, M. & Wold, L. E. Metalloproteinase expression is altered in cardiac and skeletal muscle in cancer cachexia. Am. J. Physiol. -Heart Circ. Physiol. 309, H685–H691 (2015).

Dadgar, S. et al. Asynchronous remodeling is a driver of failed regeneration in Duchenne muscular dystrophy. J. Cell. Biol. 207, 139–158 (2014).

Brocca, L. et al. Structure and function of human muscle fibres and muscle proteome in physically active older men. J. Physiol. 595, 4823–4844 (2017).

Head, S. I. Branched fibres in old dystrophic mdx muscle are associated with mechanical weakening of the sarcolemma, abnormal Ca2+ transients and a breakdown of Ca2+ homeostasis during fatigue. Exp. Physiol. 95, 641–656 (2010).

Head, S. I., Stephenson, D. G. & Williams, D. A. Properties of enzymatically isolated skeletal fibres from mice with muscular dystrophy. J. Physiol. 422, 351–367 (1990).

Friedrich, O. et al. Microarchitecture is severely compromised but motor protein function is preserved in dystrophic mdx skeletal muscle. Biophys. J. 98, 606–616 (2010).

Ho, K. W. et al. Skeletal muscle fiber splitting with weight‐lifting exercise in rats.Am. J. Anat. 157, 433–440 (1980).

Head, S. I., Houweling, P. J., Chan, S., Chen, G. & Hardeman, E. C. Properties of regenerated mouse extensor digitorum longus muscle following notexin injury. Exp. Physiol. 99, 664–674 (2014).

Lynch, G. S., Hinkle, R. T., Chamberlain, J. S., Brooks, S. V. & Faulkner, J. A. Force and power output of fast and slow skeletal muscles from mdx mice 6‐28 months old. J. Physiol. 535, 591–600 (2001).

Lovering, R. M., Michaelson, L. & Ward, C. W. Malformed mdx myofibers have normal cytoskeletal architecture yet altered EC coupling and stress-induced Ca2+ signaling. Am. J. Physio 297, C571–C580 (2009).

Hernández-Ochoa, E. O., Pratt, S. J. P., Garcia-Pelagio, K. P., Schneider, M. F. & Lovering, R. M. Disruption of action potential and calcium signaling properties in malformed myofibers from dystrophin-deficient mice. Physiol. Rep. 3, e12366 (2015).

Plotnikov, S. V. et al. Measurement of muscle disease by quantitative second-harmonic generation imaging. J. Biomed. Opt. 13, 044018 (2008).

Rehberg, M., Krombach, F., Pohl, U. & Dietzel, S. Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy. PLoS ONE 6, e28237 (2011).

Paesen, R. et al. Fully automated muscle quality assessment by Gabor filtering of second harmonic generation images. J. Biomed. Opt. 21, 026003 (2016).

Garbe, C. S., Buttgereit, A., Schürmann, S. & Friedrich, O. Automated multiscale morphometry of muscle disease from second harmonic generation microscopy using tensor-based image processing. Ieee. Trans. Biomed. Eng. 59, 39–44 (2012).

Buttgereit, A., Weber, C., Garbe, C. S. & Friedrich, O. From chaos to split-ups - SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle. J. Pathol. 229, 477–485 (2013).

Buttgereit, A., Weber, C. & Friedrich, O. A novel quantitative morphometry approach to assess regeneration in dystrophic skeletal muscle. Neuromuscul. Disord. 24, 596–603 (2014).

Diermeier, S. et al. Preaged remodeling of myofibrillar cytoarchitecture in skeletal muscle expressing R349P mutant desmin. Neurobiol. Aging 58, 77–87 (2017).

Diermeier, S. et al. Early signs of architectural and biomechanical failure in isolated myofibers and immortalized myoblasts from desmin-mutant knock-in mice. Sci. Rep. 7, 1391 (2017).

Moss, R. L. Sarcomere length‐tension relations of frog skinned muscle fibres during calcium activation at short lengths. J. Physiol. 292, 177–192 (1979).

de Souza Leite, F., Minozzo, F. C., Altman, D. & Rassier, D. E. Microfluidic perfusion shows intersarcomere dynamics within single skeletal muscle myofibrils. Proc.. Natl. Acad. Sci. U. S. A. 114, 8794 (2017).

Horowits, R. Passive force generation and titin isoforms in mammalian skeletal muscle. Biophys. J. 61, 392–398 (1992).

Anderson, J., Li, Z. & Goubel, F. Models of skeletal muscle to explain the increase in passive stiffness in desmin knockout muscle. J. Biomech. 35, 1315–1324 (2002).

Haug, M. et al. The MyoRobot: A novel automated biomechatronics system to assess voltage/Ca2+ biosensors and active/passive biomechanics in muscle and biomaterials. Biosens. Bioelectron. 102, 589–599 (2018).

Plotnikov, S. V., Millard, A. C., Campagnola, P. J. & Mohler, W. A. Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres. Biophys. J. 90, 693–703 (2006).

Schürmann, S., von Wegner, F., Fink, R. H. A., Friedrich, O. & Vogel, M. Second harmonic generation microscopy probes different states of motor protein interaction in myofibrils. Biophys. J. 99, 1842–1851 (2010).

Nucciotti, V. et al. Probing myosin structural conformation in vivo by second-harmonic generation microscopy. Proc. Natl Acad. Sci. USA 107, 7763–7768 (2010).

Ralston, E. et al. Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence. J. Struct. Biol. 162, 500–508 (2008).

Feeney, E. J. et al. The value of muscle biopsies in Pompe disease: identifying lipofuscin inclusions in juvenile- and adult-onset patients. Acta Neuropathol. Commun. 2, 2 (2014).

Liu, W. H., Ralston, E. & Raben, N. Quantitative evaluation of skeletal muscle defects in second harmonic generation images. J. Biomed. Opt. 18, 026005 (2013).

Mohler, W., Millard, A. C. & Campagnola, P. J. Second harmonic generation imaging of endogenous structural proteins. Methods 29, 97–109 (2003).

Légaré, F., Pfeffer, C. & Olsen, B. R. The role of backscattering in SHG tissue imaging. Biophys. J. 93, 1312–1320 (2007).

Nadiarnykh, O., LaComb, R., Campagnola, P. J. & Mohler, W. A. Coherent and incoherent SHG in fibrillar cellulose matrices. Opt. Express 15, 3348–3360 (2007).

Mazumder, N. et al. Stokes vector based polarization resolved second harmonic microscopy of starch granules. Biomed. Opt. Express 4, 538–547 (2013).

Golaraei, A. et al. Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy. Biomed. Opt. Express 5, 3562–3567 (2014).

Hayes, A. & Williams, D. A. Contractile function and low-intensity exercise effects of old dystrophic ( mdx) mice. Am. J. Physiol. 274, C1138–C1144 (1998).

Hakim, C. H. & Duan, D. S. Gender differences in contractile and passive properties of mdx extensor digitorum longus muscle. Muscle Nerve 45, 250–256 (2011).

Sosa, H., Popp, D., Ouyang, G. & Huxley, H. E. Ultrastructure of skeletal muscle fibers studied by a plunge quick freezing method: myofilament lengths. Biophys. J. 67, 283–292 (1994).

Moo, E. K., Leonard, T. R. & Herzog, W. In vivo sarcomere lengths become more non-uniform upon activation in intact whole muscle. Front. Physiol. 8, 1015 (2017).

Wood, D. S., Sorenson, M. M., Eastwood, A. B., Charash, W. E. & Reuben, J. P. Duchenne dystrophy: abnormal generation of tension and Ca++ regulation in single skinned fibers. Neurology 28, 447 (1978).

Williams, D. A., Head, S. I., Lynch, G. S. & Stephenson, D. G. Contractile properties of skinned muscle fibres from young and adult normal and dystrophic ( mdx) mice. J. Physiol. 460, 51–67 (1993).

Schertzer, J. D., van der Poel, C., Shavlakadze, T., Grounds, M. D. & Lynch, G. S. Muscle-specific overexpression of IGF-I improves E-C coupling in skeletal muscle fibers from dystrophic mdx mice. Am. J. Physiol. 294, C161–C168 (2008).

Horowits, R., Dalakas, M. C. & Podolsky, R. J. Single skinned muscle fibers in duchenne muscular dystrophy generate normal force. Ann. Neurol. 27, 636–641 (1990).

Rehorn, M. R., Schroer, A. K. & Blemker, S. S. The passive properties of muscle fibers are velocity dependent. J. Biomech. 47, 687–693 (2014).

Wolff, A. V. et al. Passive mechanical properties of maturing extensor digitorum longus are not affected by lack of dystrophin.Muscle Nerve 34, 304–312 (2006).

Bobet, J., Mooney, R. F. & Gordon, T. Force and stiffness of old dystrophic (mdx) mouse skeletal muscles. Muscle Nerve 21, 536–539 (1998).

Hakim, C. H., Grange, R. W. & Duan, D. S. The passive mechanical properties of the extensor digitorum longus muscle are compromised in 2- to 20-mo-old mdx mice. J. Appl. Physiol. 110, 1656–1663 (2011).

Smith, L. R. & Barton, E. R. Collagen content does not alter the passive mechanical properties of fibrotic skeletal muscle in mdx mice. Am. J. Physiol. 306, C889–C898 (2014).

Vogel, A., Noack, J., Hüttman, G. & Paltauf, G. Mechanisms of femtosecond laser nanosurgery of cells and tissues. Appl. Phys. B 81, 1015–1047 (2005).

Meldrum, R. A., Botchway, S. W., Wharton, C. W. & Hirst, G. J. Nanoscale spatial induction of ultraviolet photoproducts in cellular DNA by three-photon near-infrared absorption. EMBO Rep. 4, 1144–1149 (2003).

Kong, X. D. et al. Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells. Nucleic Acids Res. 37, e68 (2009).

Von Wegner, F., Both, M., Fink, R. H. A. & Friedrich, O. Fast XYT imaging of elementary calcium release events in muscle with multifocal multiphoton microscopy and wavelet denoising and detection. IEEE Trans. Med. Imaging 26, 925–934 (2007).

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

No data

Related Author

No data

Related Institution

No data

⁰