Different fibre populations distinguished by their calcium transient characteristics in enzymatically dissociated murine flexor digitorum brevis and soleus muscles

  • Juan C. Calderón
  • Pura Bolaños
  • Sonia H. Torres
  • Greta Rodríguez-Arroyo
  • Carlo Caputo
Original Paper

Abstract

Enzymatically dissociated flexor digitorum brevis (FDB) and soleus fibres from mouse were used to compare the kinetics of electrically elicited Ca2+ transients of slow and fast skeletal muscle fibres, using the fast Ca2+ dye MagFluo4-AM, at 20–22°C. For FDB two Ca2+ transient morphologies, types I (MT-I, 11 fibres, 19%) and II (MT-II, 47 fibres, 81%), were found, the kinetic parameters (amplitude, rise time, half width, decay time, and time constants of decay) being statistically different. For soleus (n = 20) only MT-I was found, with characteristics similar to MT-I from FDB. Correlations with histochemically determined mATPase, reduced nicotinamide adenine dinucleotide diaphorase and α-glycerophosphate dehydrogenase activities, as well as immunostaining and myosin heavy chain electrophoretic analysis of both muscles suggest that signals classified as MT-I may correspond to slow type I and fast IIA fibres while those classified as MT-II may correspond to fast IIX/D fibres. The results point to the importance of Ca2+ signaling for characterization of muscle fibres, but also to its possible role in determining fibre function.

Keywords

Fibre types Calcium transients Flexor digitorum brevis Soleus Myosin adenosine triphosphatase activity 

Notes

Acknowledgments

Grant support was provided by FONACIT projects G-2001000637 and G-2005000372. We wish to thank Lic. Meyerling Betancourt, for helping with myosin heavy chain electrophoresis, and Lic. Víctor Salazar for helping with images.

References

  1. Allen D, Duty S, Westerblad H (1993) Metabolic changes in muscle during exercise: their effects on muscle function. Proc Aust Physiol Pharmacol Soc 24:65–75Google Scholar
  2. Asmussen G, Maréchal G (1989) Maximal shortening velocities, isomyosins and fibre types in soleus muscle of mice, rats and guinea pigs. J Physiol 416:245–254PubMedGoogle Scholar
  3. Bär A, Pette D (1988) Three fast myosin heavy chains in adult rat skeletal muscle. FEBS Lett 235(1, 2):153–155PubMedCrossRefGoogle Scholar
  4. Barnard R, Edgerton V, Furukawa T, Peter J (1971) Histochemical, biochemical, and contractile properties of red, white, and intermediate fibers. Am J Physiol 220:410–414PubMedGoogle Scholar
  5. Baylor S, Hollingworth S (2003) Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol 551:125–138. doi: 10.1113/jphysiol.2003.041608 PubMedCrossRefGoogle Scholar
  6. Bekoff A, Betz W (1977) Physiological properties of dissociated muscle fibres obtained from innervated and denervated adult rat muscle. J Physiol 271:25–40PubMedGoogle Scholar
  7. Blough E, Rennie E, Zhang F, Reiser P (1996) Enhanced electrophoretic separation and resolution of myosin heavy chains in mammalian and avian skeletal muscles. Anal Biochem 233:31–35. doi: 10.1006/abio.1996.0003 PubMedCrossRefGoogle Scholar
  8. Bolaños P, Guillén A, Rojas H, Boncompagni S, Caputo C (2008) The use of calcium-orange-5 N as a specific marker of mitochondrial Ca2+ in mouse skeletal muscle fibers. Pflugers Arch 455:721–731. doi: 10.1007/s00424-007-0312-5 PubMedCrossRefGoogle Scholar
  9. Bottinelli R, Reggiani C (2000) Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol 73:195–262. doi: 10.1016/S0079-6107(00)00006-7 PubMedCrossRefGoogle Scholar
  10. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72:248–254. doi: 10.1016/0003-2697(76)90527-3 PubMedCrossRefGoogle Scholar
  11. Brooke M, Kaiser K (1969) Some comments on the hitochemical characterization of muscle adenosine triphosphatase. J Histochem Cytochem 17:431–432PubMedGoogle Scholar
  12. Brooke M, Kaiser K (1970) Three “myosin adenosine triphosphatase” systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18(9):670–672PubMedGoogle Scholar
  13. Burke R, Levine D, Zajac F (1971) Mammalian motor units: physiological-histochemical correlation in three types in cat gastrocnemius. Science 174:709–712. doi: 10.1126/science.174.4010.709 PubMedCrossRefGoogle Scholar
  14. Calderón-Vélez J, Bolaños P, Caputo C (2009) Functional identification of fiber types in enzymatically dissociated murine flexor digitorum brevis and soleus muscles. Biophys J 96(3-S1):233aCrossRefGoogle Scholar
  15. Capote J, Bolaños P, Schuhmeier R, Caputo C (2005) Calcium transients in developing mouse skeletal muscle fibres. J Physiol 564(2):451–464. doi: 10.1113/jphysiol.2004.081034 PubMedCrossRefGoogle Scholar
  16. Carroll S, Klein M, Schneider M (1995) Calcium transients in intact rat skeletal muscle fibers in agarosa gel. Am J Physiol 269:C28–C34PubMedGoogle Scholar
  17. Carroll S, Klein M, Schneider M (1997) Decay of calcium transients after electrical stimulation in rat fast- and slow-twitch skeletal muscle fibres. J Physiol 501(3):573–588. doi: 10.1111/j.1469-7793.1997.573bm.x PubMedCrossRefGoogle Scholar
  18. Celio M, Heizmann C (1982) Calcium-binding protein parvalbumin is associated with fast contracting muscle fibres. Nature 297:504–506. doi: 10.1038/297504a0 PubMedCrossRefGoogle Scholar
  19. Cheung A, Dantzig J, Hollingworth S, Baylor S, Goldman Y, Mitchison T et al (2002) A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4:83–89. doi: 10.1038/ncb734 PubMedCrossRefGoogle Scholar
  20. Close R (1972) Dynamic properties of mammalian skeletal muscles. Physiol Rev 52(1):129–197PubMedGoogle Scholar
  21. Delp M, Duan C (1996) Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J Appl Physiol 80(1):261–270PubMedGoogle Scholar
  22. DiFranco M, Novo D, Vergara JL (2002) Characterization of the calcium release domains during excitation–contraction coupling in skeletal muscle fibers. Pflugers Arch 443:508–519. doi: 10.1007/s004240100719 PubMedCrossRefGoogle Scholar
  23. Dubowitz V (1985) Muscle biopsy: a practical approach, 2nd edn. Bailliere Tindall, LondonGoogle Scholar
  24. Dubowitz V, Pearse A (1960) A comparative histochemical study of oxidative enzyme and phophorylase activity in skeletal muscle. Histochemie 2:105–117. doi: 10.1007/BF00744575 PubMedCrossRefGoogle Scholar
  25. Dulhunty A, Banyard M, Medveczky C (1987) Distribution of calcium ATPase in the sarcoplasmic reticulum of fast- and slow-twitch muscles determined with monoclonal antibodies. J Membr Biol 99:79–92. doi: 10.1007/BF01871228 PubMedCrossRefGoogle Scholar
  26. Ecob-Prince M, Leberer E (1989) Parvalbumin in mouse muscle in vivo and in vitro. Differentiation 40:10–16. doi: 10.1111/j.1432-0436.1989.tb00808.x PubMedCrossRefGoogle Scholar
  27. Engel W (1962) The essentiality of histo- and cytochemical studies of skeletal muscle in the investigation of neuromuscular disease. Neurology 12:778–794Google Scholar
  28. Eusebi F, Miledi R, Takahashi T (1980) Calcium transients in mammalian muscles. Nature 284:560–561. doi: 10.1038/284560a0 PubMedCrossRefGoogle Scholar
  29. Ferguson D, Franzini-Armstrong C (1988) The Ca2+ ATPase content of slow and fast twitch fibers of guinea pig. Muscle Nerve 11:561–570. doi: 10.1002/mus.880110607 PubMedCrossRefGoogle Scholar
  30. Franzini-Armstrong C, Ferguson D, Champ C (1988) Discrimination between fast- and slow-twitch fibres of guinea pig skeletal muscle using the relative surface density of junctional transverse tubule membrane. J Muscle Res Cell Motil 9:403–414. doi: 10.1007/BF01774067 PubMedCrossRefGoogle Scholar
  31. Füchtbauer E, Rowlerson A, Gotz K, Friedrich G, Mabuchi K, Gergely J et al (1991) Direct correlation of parvalbumin levels with myosin isoforms and succinate dehydrogenase activity on frozen sections of rodent muscle. J Histochem Cytochem 39(3):355–361PubMedGoogle Scholar
  32. Gillis J, Thomason D, Lefévre J, Kretsinger R (1982) Parvalbumins and muscle relaxation: a computer simulation study. J Muscle Res Cell Motil 3:377–398. doi: 10.1007/BF00712090 PubMedCrossRefGoogle Scholar
  33. González E, Messi M, Zheng Z, Delbono O (2003) Insulin-like growth factor-1 prevents age-related decrease in specific force and intracellular Ca2+ in single intact muscle fibres from transgenic mouse. J Physiol 552:833–844. doi: 10.1113/jphysiol.2003.048165 PubMedCrossRefGoogle Scholar
  34. Guth L, Samaha F (1969) Qualitative differences between actomyosin ATPase of slow and fast mammalian muscle. Exp Neurol 25:138–152. doi: 10.1016/0014-4886(69)90077-6 PubMedCrossRefGoogle Scholar
  35. Hämäläinen N, Pette D (1995) Patterns of myosin isoforms in mammalian skeletal muscle fibres. Microsc Res Tech 30:381–389. doi: 10.1002/jemt.1070300505 PubMedCrossRefGoogle Scholar
  36. Hasselbach W (1998) The Ca2+-ATPase of the sarcoplasmic reticulum in skeletal and cardiac muscle. Ann N Y Acad Sci 853:1–8. doi: 10.1111/j.1749-6632.1998.tb08251.x PubMedCrossRefGoogle Scholar
  37. Heizmann C, Berchtold M, Rowlerson A (1982) Correlation of parvalbumin concentration with relaxation speed in mammalian muscle. Proc Natl Acad Sci USA 79:7243–7247. doi: 10.1073/pnas.79.23.7243 PubMedCrossRefGoogle Scholar
  38. Hollingworth S, Marshall M (1981) A comparative study of charge movement in rat and frog skeletal muscle fibres. J Physiol 321:583–602PubMedGoogle Scholar
  39. Jiang Y, Johnson J, Rall J (1996) Parvalbumin relaxes frog skeletal muscle when sarcoplasmic reticulum Ca2+-ATPase is inhibited. Am J Physiol 270:C411–C417PubMedGoogle Scholar
  40. Leberer E, Pette D (1986) Immunochemical quantification of sarcoplasmic reticulum Ca-ATPase, of calsequestrin and of parvalbumin in rabbit skeletal muscles. Eur J Biochem 156:489–496. doi: 10.1111/j.1432-1033.1986.tb09607.x PubMedCrossRefGoogle Scholar
  41. Leberer E, Härtner K, Pette D (1988) Postnatal development of Ca2+-sequestration by the sarcoplasmic reticulum of fast and slow muscles in normal and dystrophic mice. Eur J Biochem 174:247–253. doi: 10.1111/j.1432-1033.1988.tb14090.x PubMedCrossRefGoogle Scholar
  42. Maréchal G, Beckers-Bleukx G (1993) Force-velocity relation and isomyosins in soleus muscles from two strains of mice (C57 and NMRI). Pflugers Arch 424:478–487. doi: 10.1007/BF00374911 PubMedCrossRefGoogle Scholar
  43. Novikoff A, Woo-yung S, Drucker J (1961) Mitochondrial localization of oxidative enzymes: staining results with two tetrazolium salts. J Biophys Biochem Cytol 9:47–61PubMedCrossRefGoogle Scholar
  44. Padykula H, Herman E (1955a) Factors affecting the activity of adenosine triphospahatase and other phosphatases as measured by histochemical techniques. J Histochem Cytochem 3:161–170PubMedGoogle Scholar
  45. Padykula H, Herman E (1955b) The specificity of the histochemical method for adenosine triphosphatase. J Histochem Cytochem 3:170–195PubMedGoogle Scholar
  46. Periasamy M, Kalyanasundaram A (2007) Serca pump isoforms: their role in calcium transport and disease. Muscle Nerve 35:430–442. doi: 10.1002/mus.20745 PubMedCrossRefGoogle Scholar
  47. Peter J, Barnard R, Edgerton V, Gillespie C, Stempel K (1972) Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11(14):2627–2633. doi: 10.1021/bi00764a013 PubMedCrossRefGoogle Scholar
  48. Ranvier L (1873) Propriétés et structures différentes des muscles rouges et des muscles blancs, chez les Lapins et chez les Raies. Compt Rend 77:1030–1034Google Scholar
  49. Sartorius C, Lu B, Acakpo-Satchivi L, Jacobsen R, Byrnes W, Leinwand L (1998) Myosin heavy chains IIa and IId are functionally distinct in the mouse. J Cell Biol 141(4):943–953. doi: 10.1083/jcb.141.4.943 PubMedCrossRefGoogle Scholar
  50. Schiaffino S, Ausoni S, Saggin L, Gundersen K, Lomo T (1988) Myosin heavy chain isoforms and velocity of shortening of type 2 skeletal muscle fibres. Acta Physiol Scand 134:575–576. doi: 10.1111/j.1748-1716.1998.tb08539.x PubMedCrossRefGoogle Scholar
  51. Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M et al (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10:197–205. doi: 10.1007/BF01739810 PubMedCrossRefGoogle Scholar
  52. Schmitt T, Pette D (1991) Fiber type-specific distribution of parvalbumin in rabbit skeletal muscle. Histochemistry 96:459–465. doi: 10.1007/BF00267071 PubMedCrossRefGoogle Scholar
  53. Shaw M, Ostap E, Goldman Y (2003) Mechanism of inhibition of skeletal muscle actomyosin by N-benzyl-p-toluenesulfonamide. Biochemistry 42:6128–6135. doi: 10.1021/bi026964f PubMedCrossRefGoogle Scholar
  54. Staron R (1991) Correlation between myofibrillar ATPase activity and myosin heavy chain composition in single human muscle fibers. Histochemistry 96:21–24. doi: 10.1007/BF00266756 PubMedCrossRefGoogle Scholar
  55. Stein J, Padykula H (1962) Histochemical classification of individual skeletal muscle fibers of the rat. Am J Anat 110:103–123. doi: 10.1002/aja.1001100203 PubMedCrossRefGoogle Scholar
  56. Szent-Györgyi A (1953) Chemical physiology of contraction in body and heart muscle. Academic Press, New YorkGoogle Scholar
  57. Talmadge R, Roy R (1993) Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J Appl Physiol 75(5):2337–2340PubMedGoogle Scholar
  58. Watemberg L, Leong L (1960) Effects of coenzyme Q10 and menadione on succinic dehydrogenase activity as measured by tetrazolium salt reduction. J Histochem Cytochem 8:296–303Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Juan C. Calderón
    • 1
    • 2
  • Pura Bolaños
    • 1
  • Sonia H. Torres
    • 3
  • Greta Rodríguez-Arroyo
    • 4
  • Carlo Caputo
    • 1
  1. 1.Laboratorio de Fisiología Celular, Centro de Biofísica y BioquímicaInstituto Venezolano de Investigaciones Científicas (IVIC)CaracasVenezuela
  2. 2.Departamento de Fisiología y Bioquímica, Grupo de Fisiología del EjercicioUniversidad de AntioquiaMedellínColombia
  3. 3.Instituto de Medicina Experimental, Sección para el Estudio de la Adaptación MuscularUniversidad Central de VenezuelaCaracasVenezuela
  4. 4.Laboratorio de Genética Humana, Centro de Medicina ExperimentalInstituto Venezolano de Investigaciones Científicas (IVIC)CaracasVenezuela

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