Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 6792694, 15 pages
https://doi.org/10.1155/2017/6792694
Research Article

Antioxidant Treatment Reduces Formation of Structural Cores and Improves Muscle Function in RYR1Y522S/WT Mice

1Center for Research on Aging and Translational Medicine (CeSI-MeT), University G. d'Annunzio of Chieti, 66100 Chieti, Italy
2Department of Neuroscience, Imaging, and Clinical Sciences (DNICS), University G. d'Annunzio of Chieti, 66100 Chieti, Italy
3Department of General Pathology, University Estadual de Londrina, 86057-970 Londrina, PR, Brazil
4Department of Medicine and Aging Science (DMSI), University G. d'Annunzio of Chieti, 66100 Chieti, Italy

Correspondence should be addressed to Simona Boncompagni; ti.hcinu@ingapmocnob.anomis

Received 6 April 2017; Accepted 13 June 2017; Published 10 September 2017

Academic Editor: Marko D. Prokić

Copyright © 2017 Antonio Michelucci et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. R. Magee and G. M. Shy, “A new congenital non-progressive myopathy,” Brain, vol. 79, no. 4, pp. 610–621, 1956. View at Google Scholar
  2. H. Jungbluth, “Central core disease,” Orphanet Journal of Rare Diseases, vol. 2, p. 25, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. V. Dubowitz and A. G. Pearse, “Oxidative enzymes and phosphorylase in central-core disease of muscle,” Lancet, vol. 2, no. 7140, pp. 23-24, 1960. View at Google Scholar
  4. K. Hayashi, R. G. Miller, and A. K. Brownell, “Central core disease: ultrastructure of the sarcoplasmic reticulum and T-tubules,” Muscle & Nerve, vol. 12, no. 2, pp. 95–102, 1989. View at Publisher · View at Google Scholar · View at Scopus
  5. D. H. Maclennan and E. Zvaritch, “Mechanistic models for muscle diseases and disorders originating in the sarcoplasmic reticulum,” Biochimica et Biophysica Acta, vol. 1813, no. 5, pp. 948–964, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Franzini-Armstrong and F. Protasi, “Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions,” Physiological Reviews, vol. 77, no. 3, pp. 699–729, 1997. View at Google Scholar
  7. M. F. Schneider, “Control of calcium release in functioning skeletal muscle fibers,” Annual Review of Physiology, vol. 56, pp. 463–484, 1994. View at Publisher · View at Google Scholar
  8. M. A. Denborough, K. C. Hopkinson, and D. G. Banney, “Firefighting and malignant hyperthermia,” British Medical Journal (Clinical Research Edition), vol. 296, no. 6634, pp. 1442-1443, 1988. View at Google Scholar
  9. D. H. MacLennan, K. Otsu, J. Fujii et al., “The role of the skeletal muscle ryanodine receptor gene in malignant hyperthermia,” Symposia of the Society for Experimental Biology, vol. 46, pp. 189–201, 1992. View at Google Scholar
  10. K. A. Quane, J. M. Healy, K. E. Keating et al., “Mutations in the ryanodine receptor gene in central core disease and malignant hyperthermia,” Nature Genetics, vol. 5, no. 1, pp. 51–55, 1993. View at Publisher · View at Google Scholar · View at Scopus
  11. M. A. Denborough, X. Dennett, and R. M. Anderson, “Central-core disease and malignant hyperpyrexia,” British Medical Journal, vol. 1, no. 5848, pp. 272-273, 1973. View at Google Scholar
  12. G. D. Eng, B. S. Epstein, W. K. Engel, D. W. McKay, and R. McKay, “Malignant hyperthermia and central core disease in a child with congenital dislocating hips,” Archives of Neurology, vol. 35, no. 4, pp. 189–197, 1978. View at Google Scholar
  13. G. B. Frank, “The current view of the source of trigger calcium in excitation-contraction coupling in vertebrate skeletal muscle,” Biochemical Pharmacology, vol. 29, no. 18, pp. 2399–2406, 1980. View at Google Scholar
  14. A. Shuaib, R. T. Paasuke, and K. W. Brownell, “Central core disease. Clinical features in 13 patients,” Medicine (Baltimore), vol. 66, no. 5, pp. 389–396, 1987. View at Google Scholar
  15. M. G. Chelu, S. A. Goonasekera, W. J. Durham et al., “Heat- and anesthesia-induced malignant hyperthermia in an RyR1 knock-in mouse,” The FASEB Journal, vol. 20, no. 2, pp. 329-330, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. W. J. Durham, P. Aracena-Parks, C. Long et al., “RyR1 S-nitrosylation underlies environmental heat stroke and sudden death in Y522S RyR1 knockin mice,” Cell, vol. 133, no. 1, pp. 53–65, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Boncompagni, A. E. Rossi, M. Micaroni et al., “Characterization and temporal development of cores in a mouse model of malignant hyperthermia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 51, pp. 21996–22001, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Wei, G. Salahura, S. Boncompagni et al., “Mitochondrial superoxide flashes: metabolic biomarkers of skeletal muscle activity and disease,” The FASEB Journal, vol. 25, no. 9, pp. 3068–3078, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Michelucci, C. Paolini, M. Canato et al., “Antioxidants protect calsequestrin-1 knockout mice from halothane- and heat-induced sudden death,” Anesthesiology, vol. 123, no. 3, pp. 603–617, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Boncompagni, A. E. Rossi, M. Micaroni et al., “Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures,” Molecular Biology of the Cell, vol. 20, no. 3, pp. 1058–1067, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. B. A. Mobley and B. R. Eisenberg, “Sizes of components in frog skeletal muscle measured by methods of stereology,” The Journal of General Physiology, vol. 66, no. 1, pp. 31–45, 1975. View at Google Scholar
  22. A. V. Loud, “A method for the quantitative estimation of cytoplasmic structures,” The Journal of Cell Biology, vol. 15, no. 3, pp. 481–487, 1962. View at Google Scholar
  23. L. Pietrangelo, A. D'Incecco, A. Ainbinder et al., “Age-dependent uncoupling of mitochondria from Ca2+ release units in skeletal muscle,” Oncotarget, vol. 6, no. 34, pp. 35358–35371, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. D. E. Goll, V. F. Thompson, H. Li, W. Wei, and J. Cong, “The calpain system,” Physiological Reviews, vol. 83, no. 3, pp. 731–801, 2003. View at Publisher · View at Google Scholar
  25. A. Z. Reznick and L. Packer, “Oxidative damage to proteins: spectrophotometric method for carbonyl assay,” Methods in Enzymology, vol. 233, pp. 357–363, 1994. View at Google Scholar
  26. D. Weber, M. J. Davies, and T. Grune, “Determination of protein carbonyls in plasma, cell extracts, tissue homogenates, isolated proteins: focus on sample preparation and derivatization conditions,” Redox Biology, vol. 5, pp. 367–380, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. A. M. Connolly, R. M. Keeling, S. Mehta, A. Pestronk, and J. R. Sanes, “Three mouse models of muscular dystrophy: the natural history of strength and fatigue in dystrophin-, dystrophin/utrophin-, and laminin alpha2-deficient mice,” Neuromuscular Disorders, vol. 11, no. 8, pp. 703–712, 2001. View at Google Scholar
  28. P. Brancaccio, G. Lippi, and N. Maffulli, “Biochemical markers of muscular damage,” Clinical Chemistry and Laboratory Medicine, vol. 48, no. 6, pp. 757–767, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Huang and N. E. Forsberg, “Role of calpain in skeletal-muscle protein degradation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 21, pp. 12100–12105, 1998. View at Google Scholar
  30. J. Huang and X. Zhu, “The molecular mechanisms of calpains action on skeletal muscle atrophy,” Physiological Research, vol. 65, no. 4, pp. 547–560, 2016. View at Google Scholar
  31. K. Ogino and D. H. Wang, “Biomarkers of oxidative/nitrosative stress: an approach to disease prevention,” Acta Medica Okayama, vol. 61, no. 4, pp. 181–189, 2007. View at Google Scholar
  32. T. Grune, K. Merker, T. Jung, N. Sitte, and K. J. Davies, “Protein oxidation and degradation during postmitotic senescence,” Free Radical Biology & Medicine, vol. 39, no. 9, pp. 1208–1215, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Jung, M. Engels, B. Kaiser, D. Poppek, and T. Grune, “Intracellular distribution of oxidized proteins and proteasome in HT22 cells during oxidative stress,” Free Radical Biology & Medicine, vol. 40, no. 8, pp. 1303–1312, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. S. K. Powers, J. Duarte, A. N. Kavazis, and E. E. Talbert, “Reactive oxygen species are signalling molecules for skeletal muscle adaptation,” Experimental Physiology, vol. 95, no. 1, pp. 1–9, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. J. M. McCord and I. Fridovich, “The utility of superoxide dismutase in studying free radical reactions. I. Radicals generated by the interaction of sulfite, dimethyl sulfoxide, and oxygen,” The Journal of Biological Chemistry, vol. 244, no. 22, pp. 6056–6063, 1969. View at Google Scholar
  36. S. Marklund and G. Marklund, “Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase,” European Journal of Biochemistry, vol. 47, no. 3, pp. 469–474, 1974. View at Google Scholar
  37. I. Fridovich, “Superoxide anion radical (O2-), superoxide dismutases, and related matters,” The Journal of Biological Chemistry, vol. 272, no. 30, pp. 18515–18517, 1997. View at Google Scholar
  38. C. Paolini, M. Quarta, A. Nori et al., “Reorganized stores and impaired calcium handling in skeletal muscle of mice lacking calsequestrin-1,” The Journal of Physiology, vol. 583, Part 2, pp. 767–784, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Paolini, M. Quarta, L. Wei-LaPierre et al., “Oxidative stress, mitochondrial damage, and cores in muscle from calsequestrin-1 knockout mice,” Skeletal Muscle, vol. 5, p. 10, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Dainese, M. Quarta, A. D. Lyfenko et al., “Anesthetic- and heat-induced sudden death in calsequestrin-1-knockout mice,” The FASEB Journal, vol. 23, no. 6, pp. 1710–1720, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Protasi, C. Paolini, and M. Dainese, “Calsequestrin-1: a new candidate gene for malignant hyperthermia and exertional/environmental heat stroke,” The Journal of Physiology, vol. 587, Part 13, pp. 3095–3100, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. F. A. Guarnier, A. L. Cecchini, A. A. Suzukawa et al., “Time course of skeletal muscle loss and oxidative stress in rats with Walker 256 solid tumor,” Muscle & Nerve, vol. 42, no. 6, pp. 950–958, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. J. M. Gutteridge and B. Halliwell, Radicals in Biology and Medicine, Oxford University Press, Oxford, Fourth edition, 2007.
  44. M. H. Disatnik, J. Dhawan, Y. Yu et al., “Evidence of oxidative stress in mdx mouse muscle: studies of the pre-necrotic state,” Journal of the Neurological Sciences, vol. 161, no. 1, pp. 77–84, 1998. View at Google Scholar
  45. J. M. Lawler, W. Song, and S. R. Demaree, “Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle,” Free Radical Biology & Medicine, vol. 35, no. 1, pp. 9–16, 2003. View at Google Scholar
  46. P. M. Abruzzo, S. di Tullio, C. Marchionni et al., “Oxidative stress in the denervated muscle,” Free Radical Research, vol. 44, no. 5, pp. 563–576, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. R. M. Denton and J. G. McCormack, “The calcium sensitive dehydrogenases of vertebrate mitochondria,” Cell Calcium, vol. 7, no. 5-6, pp. 377–386, 1986. View at Google Scholar
  48. P. R. Territo, S. A. French, and R. S. Balaban, “Simulation of cardiac work transitions, in vitro: effects of simultaneous Ca2+ and ATPase additions on isolated porcine heart mitochondria,” Cell Calcium, vol. 30, no. 1, pp. 19–27, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. S. K. Powers and M. J. Jackson, “Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production,” Physiological Reviews, vol. 88, no. 4, pp. 1243–1276, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. Q. Chen, Y. C. Chai, S. Mazumder et al., “The late increase in intracellular free radical oxygen species during apoptosis is associated with cytochrome c release, caspase activation, and mitochondrial dysfunction,” Cell Death and Differentiation, vol. 10, no. 3, pp. 323–334, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. W. Wang, H. Fang, L. Groom et al., “Superoxide flashes in single mitochondria,” Cell, vol. 134, no. 2, pp. 279–290, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. R. Rudolf, M. Mongillo, P. J. Magalhaes, and T. Pozzan, “In vivo monitoring of Ca2+ uptake into mitochondria of mouse skeletal muscle during contraction,” The Journal of Cell Biology, vol. 166, no. 4, pp. 527–536, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Caputo and P. Bolanos, “Effect of mitochondria poisoning by FCCP on Ca2+ signaling in mouse skeletal muscle fibers,” Pflügers Archiv, vol. 455, no. 4, pp. 733–743, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. A. E. Rossi, S. Boncompagni, and R. T. Dirksen, “Sarcoplasmic reticulum-mitochondrial symbiosis: bidirectional signaling in skeletal muscle,” Exercise and Sport Sciences Reviews, vol. 37, no. 1, pp. 29–35, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. A. E. Rossi, S. Boncompagni, L. Wei, F. Protasi, and R. T. Dirksen, “Differential impact of mitochondrial positioning on mitochondrial Ca2+ uptake and Ca2+ spark suppression in skeletal muscle,” American Journal of Physiology. Cell Physiology, vol. 301, no. 5, pp. C1128–C1139, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Franzini-Armstrong and S. Boncompagni, “The evolution of the mitochondria-to-calcium release units relationship in vertebrate skeletal muscles,” Journal of Biomedicine & Biotechnology, vol. 2011, Article ID 830573, 9 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. C. J. Duncan, “Role of intracellular calcium in promoting muscle damage: a strategy for controlling the dystrophic condition,” Experientia, vol. 34, no. 12, pp. 1531–1535, 1978. View at Google Scholar
  58. D. G. Allen, N. P. Whitehead, and E. W. Yeung, “Mechanisms of stretch-induced muscle damage in normal and dystrophic muscle: role of ionic changes,” The Journal of Physiology, vol. 567, no. 3, pp. 723–735, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. A. R. Burr and J. D. Molkentin, “Genetic evidence in the mouse solidifies the calcium hypothesis of myofiber death in muscular dystrophy,” Cell Death and Differentiation, vol. 22, no. 9, pp. 1402–1412, 2015. View at Publisher · View at Google Scholar · View at Scopus
  60. D. E. Croall and G. N. DeMartino, “Calcium-activated neutral protease (calpain) system: structure, function, and regulation,” Physiological Reviews, vol. 71, no. 3, pp. 813–847, 1991. View at Google Scholar
  61. P. Costelli, P. Reffo, F. Penna, R. Autelli, G. Bonelli, and F. M. Baccino, “Ca2+-dependent proteolysis in muscle wasting,” The International Journal of Biochemistry & Cell Biology, vol. 37, no. 10, pp. 2134–2146, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Gissel, “The role of Ca2+ in muscle cell damage,” Annals of the New York Academy of Sciences, vol. 1066, pp. 166–180, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. A. J. Smuder, A. N. Kavazis, M. B. Hudson, W. B. Nelson, and S. K. Powers, “Oxidation enhances myofibrillar protein degradation via calpain and caspase-3,” Free Radical Biology & Medicine, vol. 49, no. 7, pp. 1152–1160, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. E. Dargelos, C. Brule, P. Stuelsatz et al., “Up-regulation of calcium-dependent proteolysis in human myoblasts under acute oxidative stress,” Experimental Cell Research, vol. 316, no. 1, pp. 115–125, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. T. Tiago, P. S. Palma, C. Gutierrez-Merino, and M. Aureliano, “Peroxynitrite-mediated oxidative modifications of myosin and implications on structure and function,” Free Radical Research, vol. 44, no. 11, pp. 1317–1327, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Fedorova, N. Kuleva, and R. Hoffmann, “Identification, quantification, and functional aspects of skeletal muscle protein-carbonylation in vivo during acute oxidative stress,” Journal of Proteome Research, vol. 9, no. 5, pp. 2516–2526, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Michelucci, C. Paolini, S. Boncompagni, M. Canato, C. Reggiani, and F. Protasi, “Strenuous exercise triggers a life-threatening response in mice susceptible to malignant hyperthermia,” The FASEB Journal, 2017. View at Publisher · View at Google Scholar