About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2011 (2011), Article ID 830573, 9 pages
http://dx.doi.org/10.1155/2011/830573
Review Article

The Evolution of the Mitochondria-to-Calcium Release Units Relationship in Vertebrate Skeletal Muscles

1Department of Cell and Developmental Biology, School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
2Center for Research on Ageing and Department of Neuroscience and Imaging, Università Gabriele d'Annunzio, 66100 Chieti, Italy

Received 5 July 2011; Accepted 10 August 2011

Academic Editor: Aikaterini Kontrogianni-Konstantopoulos

Copyright © 2011 Clara Franzini-Armstrong and Simona Boncompagni. 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. C. S. Rossi and A. L. Lehninger, “Stoichiometry of respiratory stimulation, accumulation oF Ca++ and phosphate, and oxidative phosphorylation in rat liver mitochondria,” The Journal of Biological hemistry, vol. 239, pp. 3971–3980, 1964.
  2. R. S. Balaban, “Cardiac energy metabolism homeostasis: role of cytosolic calcium,” Journal of Molecular and Cellular Cardiology, vol. 34, no. 10, pp. 1259–1271, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. P. S. Brookes, Y. Yoon, J. L. Robotham, M. W. Anders, and S. S. Sheu, “Calcium, ATP, and ROS: a mitochondrial love-hate triangle,” American Journal of Physiology—Cell Physiology, vol. 287, no. 4, pp. C817–C833, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Rizzuto, A. W. M. Simpson, M. Brini, and T. Pozzan, “Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin,” Nature, vol. 358, no. 6384, pp. 325–327, 1992. View at Publisher · View at Google Scholar · View at Scopus
  5. G. Hajnoczky, L. D. Robb-Gaspers, M. B. Seitz, and A. P. Thomas, “Decoding of cytosolic calcium oscillations in the mitochondria,” Cell, vol. 82, no. 3, pp. 415–424, 1995. View at Scopus
  6. B. Chance, G. R. Williams, W. F. Holmes, and J. Higgins, “Respiratory enzymes in oxidative phosphorylation. V. A mechanism for oxidative phosphorylation,” The Journal of Biological Chemistry, vol. 217, no. 1, pp. 439–451, 1955. View at Scopus
  7. E. Carafoli, C. S. Rossi, and A. L. Lehninger, “Uptake of Adenine Nucleotides by Respiring Mitochondria During Active Accumulation of Ca++ and Phosphate,” The Journal of Biological Chemistry, vol. 240, pp. 2254–2261, 1965.
  8. A. Scarpa and P. Graziotti, “Mechanisms for intracellular calcium regulation in heart. I. Stopped flow measurements of Ca++ uptake by cardiac mitochondria,” Journal of General Physiology, vol. 62, no. 6, pp. 756–772, 1973. View at Scopus
  9. R. Rizzuto, M. Brini, M. Murgia, and T. Pozzan, “Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria,” Science, vol. 262, no. 5134, pp. 744–747, 1993. View at Scopus
  10. R. Rizzuto, P. Pinton, W. Carrington et al., “Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses,” Science, vol. 280, no. 5370, pp. 1763–1766, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Rizzuto and T. Pozzan, “Microdomains of intracellular Ca2+: molecular determinants and functional consequences,” Physiological Reviews, vol. 86, no. 1, pp. 369–408, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. G. Csordás, P. Várnai, T. Golenár et al., “Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface,” Molecular Cell, vol. 39, no. 1, pp. 121–132, 2010. View at Publisher · View at Google Scholar
  13. C. A. Mannella, K. Buttle, B. K. Rath, and M. Marko, “Electron microscopic tomography of rat-liver mitochondria and their interactions with the endoplasmic reticulum,” BioFactors, vol. 8, no. 3-4, pp. 225–228, 1998. View at Scopus
  14. G. C. Shore and J. R. Tata, “Two fractions of rough endoplasmic reticulum from rat liver. I. Recovery of rapidly sedimenting endoplasmic reticulum in association with mitochondria,” Journal of Cell Biology, vol. 72, no. 3, pp. 714–725, 1977. View at Scopus
  15. C. García-Pérez, G. Hajnóczky, and G. Csordás, “Physical coupling supports the local Ca2+ transfer between sarcoplasmic reticulum subdomains and the mitochondria in heart muscle,” Journal of Biological Chemistry, vol. 283, no. 47, pp. 32771–32780, 2008. View at Publisher · View at Google Scholar
  16. G. Szabadkai, K. Bianchi, P. Várnai et al., “Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels,” Journal of Cell Biology, vol. 175, no. 6, pp. 901–911, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Rudolf, M. Mongillo, P. J. Magalhäes, and T. Pozzan, “In vivo monitoring of Ca2+ uptake into mitochondria of mouse skeletal muscle during contraction,” Journal of Cell Biology, vol. 166, no. 4, pp. 527–536, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. V. K. Sharma, V. Ramesh, C. Franzini-Armstrong, and S. S. Sheu, “Transport of Ca2+ from sarcoplasmic reticulum to mitochondria in rat ventricular myocytes,” Journal of Bioenergetics and Biomembranes, vol. 32, no. 1, pp. 97–104, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. J. M. Gillis, “Inhibition of mitochondrial calcium uptake slows down relaxation in mitochondria-rich skeletal muscles,” Journal of Muscle Research and Cell Motility, vol. 18, no. 4, pp. 473–483, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. E. V. Isaeva and N. Shirokova, “Metabolic regulation of Ca2+ release in permeabilized mammalian skeletal muscle fibres,” Journal of Physiology, vol. 547, part 2, pp. 453–462, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Ogata and Y. Yamasaki, “Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers,” Anatomical Record, vol. 248, no. 2, pp. 214–223, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. 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
  23. V. M. Shkryl and N. Shirokova, “Transfer and tunneling of Ca2+ from sarcoplasmic reticulum to mitochondria in skeletal muscle,” Journal of Biological Chemistry, vol. 281, no. 3, pp. 1547–1554, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Rambourg and D. Segretain, “Three-dimensional electron microscopy of mitochondria and endoplasmic reticulum in the red muscle fiber of the rat diaphragm,” Anatomical Record, vol. 197, no. 1, pp. 33–48, 1980. View at Scopus
  25. T. Ogata and Y. Yamasaki, “Scanning electron-microscopic studies on the three-dimensional structure of mitochondria in the mammalian red, white and intermediate muscle fibers,” Cell and Tissue Research, vol. 241, no. 2, pp. 251–256, 1985. View at Scopus
  26. 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
  27. T. M. Williams, G. P. Dobson, O. Mathieu-Costello, D. Morsbach, M. B. Worley, and J. A. Phillips, “Skeletal muscle histology and biochemistry of an elite sprinter, the African cheetah,” Journal of Comparative Physiology, B, vol. 167, no. 8, pp. 527–535, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Boncompagni, H. Kern, K. Rossini et al., “Structural differentiation of skeletal muscle fibers in the absence of innervation in humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 49, pp. 19339–19344, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. B. R. Eisenberg, A. M. Kuda, and J. B. Peter, “Stereological analysis of mammalian skeletal muscle. I. Soleus muscle of the adult guinea pig,” Journal of Cell Biology, vol. 60, no. 3, pp. 732–754, 1974. View at Scopus
  30. A. G. Engel and B. Q. Banker, “Ultrastructural changes in diseased muscle,” in Myology, A. G. Engel and C. Franzini-Armstrong, Eds., vol. 1, chapter 31, pp. 749–888, McGraw–Hill, 3rd edition, 2004.
  31. S. Boncompagni, L. d'Amelio, S. Fulle, G. Fanò, and F. Protasi, “Progressive disorganization of the excitation-contraction coupling apparatus in aging human skeletal muscle as revealed by electron microscopy: a possible role in the decline of muscle performance,” Journals of Gerontology, Series A, vol. 61, no. 10, pp. 995–1008, 2006. View at Scopus
  32. O. Mathieu-Costello, S. Morales, J. Savolainen, and M. Vornanen, “Fiber capillarization relative to mitochondrial volume in diaphragm of shrew,” Journal of Applied Physiology, vol. 93, no. 1, pp. 346–353, 2002. View at Scopus
  33. J. P. Revel, “The sarcoplasmic reticulum of the bat cricothroid muscle,” The Journal of cell biology, vol. 12, pp. 571–588, 1962. View at Scopus
  34. A. F. Howatson, “The structure of pigeon breast muscle mitochondria,” The Journal of Biophysical and Biochemical Cytology, vol. 2, supplement 4, pp. 363–368, 1956.
  35. S. G. Page, “Structure and some contractile properties of fast and slow muscles of the chicken,” Journal of Physiology, vol. 205, no. 1, pp. 131–145, 1969. View at Scopus
  36. I. Grinyer and J. C. George, “Some observations on the ultrastructure of the hummingbird pectoral muscles,” Canadian Journal of Zoology, vol. 47, no. 5, pp. 771–773, 1969. View at Scopus
  37. R. K. Suarez, J. R. B. Lighton, G. S. Brown, and O. Mathieu-Costello, “Mitochondrial respiration in hummingbird flight muscles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 11, pp. 4870–4873, 1991. View at Scopus
  38. S. G. Page, “Fine structure of tortoise skeletal muscle,” Journal of Physiology, vol. 197, no. 3, pp. 709–715, 1968. View at Scopus
  39. K. E. Conley and S. L. Lindstedt, “Minimal cost per twitch in rattlesnake tall muscle,” Nature, vol. 383, no. 6595, pp. 71–72, 1996. View at Publisher · View at Google Scholar · View at Scopus
  40. B. R. Moon, J. J. Hopp, and K. E. Conley, “Mechanical trade-offs explain how performance increases without increasing cost in rattlesnake tailshaker muscle,” Journal of Experimental Biology, vol. 205, part 5, pp. 667–675, 2002. View at Scopus
  41. L. C. Rome, D. A. Syme, S. Hollingworth, S. L. Lindstedt, and S. M. Baylor, “The whistle and the rattle: the design of sound producing muscles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 15, pp. 8095–8100, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. P. J. Schaeffer, K. E. Conley, and S. L. Lindstedt, “Structural correlates of speed and endurance in skeletal muscle: the rattlesnake tailshaker muscle,” Journal of Experimental Biology, vol. 199, part 2, pp. 351–358, 1996. View at Scopus
  43. C. Franzini-Armstrong, “Studies of the triad. 3. Structure of the junction in fast twitch fibers,” Tissue and Cell, vol. 47, no. 2, pp. 488–499, 1970. View at Scopus
  44. C. Franzini-Armstrong, “Studies of the triad. IV. Structure of the junction in frog slow fibers,” Journal of Cell Biology, vol. 56, no. 1, pp. 120–128, 1973. View at Scopus
  45. I. Sato, K. Konishi, M. Sunohara, and A. Mikami, “Enzyme activities and morphology of Japanese brown frog (Rana japonica) mitochondria in the tibialis anterior muscle during hibernation and active life,” Canadian Journal of Zoology, vol. 79, no. 7, pp. 1316–1321, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Ogata and Y. Yamasaki, “High-resolution scanning electron-microscopic studies on the three-dimensional structure of mitochondria and sarcoplasmic reticulum in the different twitch muscle fibers of the frog,” Cell and Tissue Research, vol. 250, no. 3, pp. 489–497, 1987. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Franzini-Armstrong and K. R. Porter, “Sarcolemmal invaginations constituting the T system in fish muscle fibers,” Journal of Cell Biology, vol. 22, pp. 675–696, 1964.
  48. C. Franzini-Armstrong, W. F. Gilly, E. Aladjem, and D. Appelt, “Golgi stain identifies three types of fibres in fish muscle,” Journal of Muscle Research and Cell Motility, vol. 8, no. 5, pp. 418–427, 1987. View at Publisher · View at Google Scholar · View at Scopus
  49. V. Di Biase and C. Franzini-Armstrong, “Evolution of skeletal type e-c coupling: a novel means of controlling calcium delivery,” Journal of Cell Biology, vol. 171, no. 4, pp. 695–704, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Schredelseker, V. Di Biase, G. J. Obermair et al., “The β1a subunit is essential for the assembly of dihydropyridine-receptor arrays in skeletal muscle,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 47, pp. 17219–17224, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. M. A. Freadman, “Role partitioning of swimming musculature of striped Bass Morone saxatilis Walbaum and Bluefish, Pomatomus saltatrix L.,” Journal of Fish Biology, vol. 15, no. 4, pp. 417–423, 1979.
  52. S. Egginton and B. D. Sidell, “Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle,” American Journal of Physiology, vol. 256, no. 1, part 2, pp. R1–R9, 1989. View at Scopus
  53. K. M. O'Brien, C. Skilbeck, B. D. Sidell, and S. Egginton, “Muscle fine structure may maintain the function of oxidative fibres in haemoglobinless Antarctic fishes,” Journal of Experimental Biology, vol. 206, part 2, pp. 411–421, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. I. A. Johnston, J. Calvo, H. Guderley, D. Fernandez, and L. Palmer, “Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes,” Journal of Experimental Biology, vol. 201, part 1, pp. 1–12, 1998. View at Scopus
  55. K. E. Loesser, J. Rafi, and M. L. Fine, “Embryonic, juvenile, and adult development of the toadfish sonic muscle,” Anatomical Record, vol. 249, no. 4, pp. 469–477, 1997. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Appelt, V. Shen, and C. Franzini-Armstrong, “Quantitation of Ca ATPase, feet and mitochondria in superfast muscle fibres from the toadfish, Opsanus tau,” Journal of Muscle Research and Cell Motility, vol. 12, no. 6, pp. 543–552, 1991. View at Scopus
  57. M. K. Lewis, P. C. Nahirney, V. Chen et al., “Concentric intermediate filament lattice links to specialized Z-band junctional complexes in sonic muscle fibers of the type I male midshipman fish,” Journal of Structural Biology, vol. 143, no. 1, pp. 56–71, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. L. C. Rome and S. L. Lindstedt, “The quest for speed: muscles built for high-frequency contractions,” News in Physiological Sciences, vol. 13, no. 6, pp. 261–268, 1998. View at Scopus
  59. M. Yi, D. Weaver, and G. Hajnóczky, “Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit,” Journal of Cell Biology, vol. 167, no. 4, pp. 661–672, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. L. Wei, G. Salahura, S. Boncompagni et al., “Mitochondrial superoxide flashes: metabolic biomarkers of skeletal muscle activity and disease,” FASEB Journal, vol. 25, pp. 3068–3078, 2011. View at Publisher · View at Google Scholar
  61. 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