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The Effect of Experimental Hyperthyroidism on Characteristics of Actin–Myosin Interaction in Fast and Slow Skeletal Muscles

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Abstract

The molecular mechanism of the failure of contractile function of skeletal muscles caused by oxidative damage to myosin in hyperthyroidism is not fully understood. Using an in vitro motility assay, we studied the effect of myosin damage caused by oxidative stress in experimental hyperthyroidism on the actin–myosin interaction and its regulation by calcium. We found that hyperthyroidism-induced oxidation of myosin is accompanied by a decrease in the sliding velocity of the regulated thin filaments in the in vitro motility assay, and this effect is increased with the duration of the pathological process.

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Abbreviations

FT3:

free triiodothyronine

FT4:

free thyroxine

h :

Hill cooperativity coefficient

MHC:

myosin heavy chains

MLC:

myosin light chains

pCa:

negative decimal logarithm of the calcium concentration

pCa50 :

calcium concentration at which half-maximal sliding velocity of thin filaments is achieved (the calcium sensitivity)

V max :

the maximal sliding velocity of thin filaments

References

  1. Pette, D., and Staron, R. S. (2000) Myosin isoforms, muscle fiber types, and transitions, Microsc. Res. Tech., 50, 500–509.

    Article  PubMed  CAS  Google Scholar 

  2. Schiaffino, S., and Reggiani, C. (2011) Fiber types in mammalian skeletal muscles, Physiol. Rev., 91, 1447–1531.

    Article  PubMed  CAS  Google Scholar 

  3. Galler, S., Schmitt, T. L., and Pette, D. (1994) Stretch acti-vation, unloaded shortening velocity, and myosin heavy chain isoforms of rat skeletal muscle fibres, J. Physiol., 478, 513–521.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Nwoye, L., Mommaerts, W. F., Simpson, D. R., Seraydarian, K., and Marusich, M. (1982) Evidence for a direct action of thyroid hormone in specifying muscle properties, Am. J. Physiol., 242, 401–408.

    Google Scholar 

  5. Diffee, G. M., Haddad, F., Herrick, R. E., and Baldwin, K. M. (1991) Control of myosin heavy chain expression: inter-action of hypothyroidism and hindlimb suspension, Am. J. Physiol., 261, 1099–1106.

    Article  Google Scholar 

  6. Larsson, L., Li, X., Teresi, A., and Salviati, G. (1994) Effects of thyroid hormone on fast-and slow-twitch skele-tal muscles in young and old rats, J. Physiol., 481, 149–161.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Caiozzo, V. J., Herrick, R. E., and Baldwin, K. M. (1991) Influence of hyperthyroidism on maximal shortening velocity and myosin isoform distribution in skeletal mus-cles, Am. J. Physiol., 261, 285–295.

    Article  Google Scholar 

  8. Caiozzo, V. J., Herrick, R. E., and Baldwin, K. M. (1992) Response of slow and fast muscle to hypothyroidism: max-imal shortening velocity and myosin isoforms, Am. J. Physiol., 263, 86–94.

    Article  Google Scholar 

  9. Ramsay, I. D. (1966) Muscle dysfunction in hyperthy-roidism, Lancet, 2, 931–934.

    Article  PubMed  CAS  Google Scholar 

  10. Nшrrelund, H., Hove, K. Y., Brems-Dalgaard, E., Jurik, A. G., Nielsen, L. P., Nielsen, S., Jorgensen, J. O., Weeke, J., and Moller, N. (1999) Muscle mass and function in thyro-toxic patients before and during medical treatment, Clin. Endocrinol. (Oxf.), 51, 693–699.

    Article  Google Scholar 

  11. Yamada, T., and Wada, M. (2004) Effects of thyroid hor-mone on sarcoplasmic reticulum Ca2+ uptake and contrac-tile properties in rat soleus muscle, Jpn. J. Phys. Fitness Sports Med., 53, 509–518.

    Article  Google Scholar 

  12. Yamada, T., Mishima, T., Sakamoto, M., Sugiyama, M., Matsunaga, S., and Wada, M. (2006) Oxidation of myosin heavy chain in force production in hyperthyroid rat soleus, J. Appl. Physiol., 100, 1520–1526.

    Article  PubMed  CAS  Google Scholar 

  13. Yamada, T., Mishima, T., Sakamoto, M., Sugiyama, M., Matsunga, S., and Wada, M. (2007) Myofibrillar oxidation and contractile dysfunction in hyperthyroid rat diaphragm, J. Appl. Physiol., 102, 1850–1855.

    Article  PubMed  CAS  Google Scholar 

  14. Venditti, P., and Di Meo, S. (2006) Thyroid hormone-induced oxidative stress, Cell. Mol. Life Sci., 63, 414–434.

    Article  PubMed  CAS  Google Scholar 

  15. Reid, M. B. (2001) Redox modulation of skeletal muscle contraction: what we know and what we don’t, J. Appl. Physiol., 90, 724–731.

    Article  PubMed  CAS  Google Scholar 

  16. Asayama, K., and Kato, K. (1990) Oxidative muscular injury and its relevance to hyperthyroidism, Free Radic. Biol. Med., 8, 293–303.

    Article  PubMed  CAS  Google Scholar 

  17. Andrade, F. H., Reid, M. B., Allen, D. G., and Westerblad, H. (1998) Effect of hydrogen peroxide and dithiothreitol on contractile function of single skeletal muscle fibres from the mouse, J. Physiol., 509, 565–575.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Plant, D. R., Lynch, G. S., and Williams, D. A. (2000) Hydrogen peroxide modulates Ca2+-activation of single permeabilized fibres from fast-and slow-twitch skeletal muscles of rats, J. Muscle Res. Cell Motil., 21, 747–752.

    Article  PubMed  CAS  Google Scholar 

  19. Murphy, R. M., Dutka, T. L., and Lamb, G. D. (2008) Hydroxyl radical and glutathione interactions alter calci-um sensitivity and maximum force of the contractile appa-ratus in rat skeletal muscle fibres, J. Physiol., 586, 2203–2216.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Prochniewicz, E., Lowe, D. A., Spakowicz, D. J., Higgins, L., O’Conor, K., Thompson, L. V., Ferrington, D. A., and Thomas, D. D. (2008) Functional, structural, and chemi-cal changes in myosin associated with hydrogen peroxide treatment of skeletal muscle fibers, Am. J. Physiol. Cell Physiol., 294, 613–626.

    Article  CAS  Google Scholar 

  21. Lamb, G. D., and Westerblad, H. (2011) Acute effects of reactive oxygen and nitrogen species on the contractile function of skeletal muscle, J. Physiol., 589, 2119–2127.

    Article  PubMed  CAS  Google Scholar 

  22. Dutka, T. L., Verburg, E., Larkins, N., Hortemo, K. H., Lunde, P. K., Sejersted, O. M., and Lamb, G. D. (2012) ROS-mediated decline in maximum Ca2+-activated force in rat skeletal muscle fibers following in vitro and in vivo stimulation, PLoS One, 7, e35226.

    Google Scholar 

  23. Zergeroglu, M. A., McKenzie, M. J., Shanely, R. A., Van Gammeren, D., DeRuisseau, K. C., and Powers, S. K. (2003) Mechanical ventilation-induced oxidative stress in the diaphragm, J. Appl. Physiol., 95, 1116–1124.

    Article  PubMed  CAS  Google Scholar 

  24. Dalle-Donne, I., Rossi, R., Giustarini, D., Milzani, A., and Colombo, R. (2003) Protein carbonyl groups as bio-markers of oxidative stress, Clin. Chim. Acta, 329, 23–38.

    Article  PubMed  CAS  Google Scholar 

  25. Stadtman, E. R., and Levine, R. L. (2003) Free radical-mediated oxidation of free amino acids and amino acid residues in proteins, Amino Acids, 25, 207–218.

    Article  PubMed  CAS  Google Scholar 

  26. Noguchi, T., Camp, P., Jr., Alix, S. L., Gorga, J. A., Begin, K. J., Leavitt, B. J., Ittleman, F. P., Alpert, N. R., LeWinter, M. M., and Van’Buren, P. (2003) Myosin from failing and non-failing human ventricles exhibit similar contractile properties, J. Mol. Cell. Cardiol., 35, 91–97.

    Article  PubMed  CAS  Google Scholar 

  27. Harrison, A. R., Lee, M. S., and McLoon, L. K. (2010) Effects of elevated thyroid hormone on adult rabbit extraocular muscles, Invest. Ophthalmol. Vis. Sci., 51, 183–191.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Margossian, S. S., and Lowey, S. (1982) Preparation of myosin and its subfragments from rabbit skeletal muscle, Methods Enzymol., 85, 55–71.

    Article  PubMed  CAS  Google Scholar 

  29. Talmadge, R. J., and Roy, R. R. (1993) Electrophoretic separation of rat skeletal muscle myosin heavy chain iso-forms, J. Appl. Physiol., 75, 2337–2340.

    Article  PubMed  CAS  Google Scholar 

  30. Laemmli, U. K. (1970) Cleavage of structural proteins dur-ing the assembly of the head of bacteriophage T4, Nature, 227, 680–685.

    Article  PubMed  CAS  Google Scholar 

  31. Pardee, J. D., and Spudich, J. A. (1982) Purification of muscle actin, Methods Enzymol., 85, 164–179.

    Article  PubMed  CAS  Google Scholar 

  32. Potter, J. D. (1982) Preparation of troponin and its sub-units, Methods Enzymol., 85, 241–263.

    Article  PubMed  CAS  Google Scholar 

  33. Smillie, L. B. (1982) Preparation and identification of alpha-and beta-tropomyosins, Methods Enzymol., 85, 234–241.

    Article  PubMed  CAS  Google Scholar 

  34. Araujo, A. S., Ribeiro, M. F., Enzveiler, A., Schenkel, P., Fernandes, T. R., Partata, W. A., Irigoyen, M. C., Llesuy, S., and Bello-Klein, A. (2006) Myocardial antioxidant enzyme activities and concentration and glutathione metabolism in experimental hyperthyroidism, Mol. Cell. Endocrinol., 249, 133–139.

    Article  PubMed  CAS  Google Scholar 

  35. Araujo, A. S., Schenkel, P., Enzveiler, A. T., Fernandes, T. R., Partata, W. A., Llesuy, S., Ribeiro, M. F., Khaper, N., Singal, P. K., and Bello-Klein, A. (2008) The role of redox signaling in cardiac hypertrophy induced by experimental hyperthyroidism, J. Mol. Endocrinol., 41, 423–430.

    Article  PubMed  CAS  Google Scholar 

  36. Reznick, A. Z., and Packer, L. (1994) Carbonyl assay for determination of oxidatively modified proteins, Meth. Enzymol., 233, 357–363.

    Article  CAS  Google Scholar 

  37. Matyushenko, A. M., Shchepkin, D. V., Kopylova, G. V., Popruga, K. E., Artemova, N. V., Pivovarova, A. V., Bershitsky, S. Y., and Levitsky, D. I. (2017) Structural and functional effects of cardiomyopathy-causing mutations in the troponin T-binding region of cardiac tropomyosin, Biochemistry, 56, 250–259.

    Article  PubMed  CAS  Google Scholar 

  38. Mashanov, G. I., and Molloy, J. E. (2007) Automatic detec-tion of single fluorophores in live cells, Biophys. J., 92, 2199–2211.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Penheiter, A. R., Bogoger, M., Ellison, P. A., Oswald, B., Perkins, W. J., Jones, K. A., and Cremo, C. R. (2007) H2O2-induced kinetic and chemical modifications of smooth muscle myosin: correlation to effects of H2O2 on airway smooth muscle, J. Biol. Chem., 282, 4336–4344.

    Article  PubMed  CAS  Google Scholar 

  40. Tiago, T., Simao, S., Aureliano, M., Martнn-Romero, F. J., and Gutierrez-Merino, C. (2006) Inhibition of skeletal muscle S1-myosin ATPase by peroxynitrite, Biochemistry, 45, 3794–3804.

    Article  PubMed  CAS  Google Scholar 

  41. Klein, J. C., Moen, R. J., Smith, E. A., Titus, M. A., and Thomas, D. D. (2011) Structural and functional impact of site-directed methionine oxidation in myosin, Biochemistry, 50, 10318–10327.

    Article  PubMed  CAS  Google Scholar 

  42. Moen, R. J., Cornea, S., Oseid, D. E., Binder, B. P., Klein, J. C., and Thomas, D. D. (2014) Redox-sensitive residue in the actin-binding interface of myosin, Biochem. Biophys. Res. Commun., 453, 345–349.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Gordon, A. M., Homsher, E., and Regnier, M. (2000) Regulation of contraction in striated muscle, Physiol. Rev., 80, 853–924.

    Article  PubMed  CAS  Google Scholar 

  44. Andrade, F. H., Reid, M. B., and Westerblad, H. (2001) Contractile response of skeletal muscle to low peroxide concentrations: myofibrillar calcium sensitivity as a likely target for redox-modulation, FASEB J., 15, 309–311.

    Article  PubMed  CAS  Google Scholar 

  45. Bruton, J. D., Place, N., Yamada, T., Silva, J. P., Andrade, F. H., Dahlstedt, A. J., Zhang, S. J., Katz, A., Larsson, N. G., and Westerblad, H. (2008) Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 overex-pressing mice, J. Physiol., 586, 175–184.

    Article  PubMed  CAS  Google Scholar 

  46. Lamb, G. D., and Posterino, G. S. (2003) Effects of oxida-tion and reduction on contractile function in skeletal mus-cle fibres of the rat, J. Physiol., 546, 149–163.

    Article  PubMed  CAS  Google Scholar 

  47. Snook, J. H., Li, J., Helmke, B. P., and Guilford, W. H. (2008) Peroxynitrite inhibits myofibrillar protein function in an in vitro assay of motility, Free Radic. Biol. Med., 44, 14–23.

    Article  PubMed  CAS  Google Scholar 

  48. Gross, S. M., and Lehman, S. L. (2013) Accessibility of myofilament cysteines and effects on ATPase depend on the activation state during exposure to oxidants, PLoS One, 8, e69110.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Correspondence to G. V. Kopylova.

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Published in Russian in Biokhimiya, 2018, Vol. 83, No. 5, pp. 695–702.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM17-426, March 5, 2018.

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Kopylova, G.V., Shchepkin, D.V. & Bershitsky, S.Y. The Effect of Experimental Hyperthyroidism on Characteristics of Actin–Myosin Interaction in Fast and Slow Skeletal Muscles. Biochemistry Moscow 83, 527–533 (2018). https://doi.org/10.1134/S000629791805005X

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  • DOI: https://doi.org/10.1134/S000629791805005X

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