- About this Journal
- Abstracting and Indexing
- Aims and Scope
- Annual Issues
- Article Processing Charges
- Articles in Press
- Author Guidelines
- Bibliographic Information
- Citations to this Journal
- Contact Information
- Editorial Board
- Editorial Workflow
- Free eTOC Alerts
- Publication Ethics
- Reviewers Acknowledgment
- Submit a Manuscript
- Subscription Information
- Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2011 (2011), Article ID 830573, 9 pages
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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- R. Rizzuto and T. Pozzan, “Microdomains of intracellular Ca2+: molecular determinants and functional consequences,” Physiological Reviews, vol. 86, no. 1, pp. 369–408, 2006.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- J. P. Revel, “The sarcoplasmic reticulum of the bat cricothroid muscle,” The Journal of cell biology, vol. 12, pp. 571–588, 1962.
- 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.
- 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.
- 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.
- 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.
- S. G. Page, “Fine structure of tortoise skeletal muscle,” Journal of Physiology, vol. 197, no. 3, pp. 709–715, 1968.
- K. E. Conley and S. L. Lindstedt, “Minimal cost per twitch in rattlesnake tall muscle,” Nature, vol. 383, no. 6595, pp. 71–72, 1996.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.