Sarcoplasmic reticulum Ca 2+ permeation explored from the lumen side in mdx muscle fibers under voltage control

Journal of General Physiology

Volumn 139, Issue 3, 2012, Pages 209-218

  Robin, Gaëlle ^a,b   Berthier, Christine ^a,b   Allard, Bruno ^a,b  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); FLUORESCENT DYE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; C57BL MOUSE; CALCIUM SIGNALING; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; CONFOCAL MICROSCOPY; CYTOSOL; DISEASE MODEL; DRUG ANTAGONISM; DUCHENNE MUSCULAR DYSTROPHY; ELECTROPHYSIOLOGY; GENETICS; IN VITRO STUDY; MALE; METABOLISM; MOUSE; PHYSIOLOGY; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; CALCIUM SIGNALING; CALCIUM-TRANSPORTING ATPASES; CELL MEMBRANE PERMEABILITY; CYTOSOL; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGICAL PHENOMENA; FLUORESCENT DYES; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MUSCLE FIBERS, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; SARCOPLASMIC RETICULUM;

EID: 84858126592     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201110738     Document Type: Article

References (36)

1. Allard, B. 2006. Sarcolemmal ion channels in dystrophin-deficient skeletal muscle fibres. J. Muscle Res. Cell Motil. 27:367-373. http://dx.doi.org/10.1007/s10974-006-9083-4
2. Allen, D.G., O.L. Gervasio, E.W. Yeung, and N.P. Whitehead. 2010. Calcium and the damage pathways in muscular dystrophy. Can. J. Physiol. Pharmacol. 88:83-91. http://dx.doi.org/10.1139/Y09-058
3. Bellinger, A.M., S. Reiken, C. Carlson, M. Mongillo, X. Liu, L. Rothman, S. Matecki, A. Lacampagne, and A.R. Marks. 2009. Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat. Med. 15:325-330. http://dx.doi.org/10.1038/nm.1916
4. Berbey, C., and B. Allard. 2009. Electrically silent divalent cation entries in resting and active voltage-controlled muscle fibers. Biophys. J. 96:2648-2657. http://dx.doi.org/10.1016/j.bpj.2009.01.008
5. Berbey, C., N. Weiss, C. Legrand, and B. Allard. 2009. Transient receptor potential canonical type 1 (TRPC1) operates as a sarcoplasmic reticulum calcium leak channel in skeletal muscle. J. Biol. Chem. 284:36387-36394. http://dx.doi.org/10.1074/jbc.M109.073221
6. Blake, D.J., A. Weir, S.E. Newey, and K.E. Davies. 2002. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev. 82:291-329.
7. 2+ entry in dystrophic skeletal muscle fibers. J. Cell Sci. 119:3733-3742. http://dx.doi.org/10.1242/jcs.03184
8. Camello, C., R. Lomax, O.H. Petersen, and A.V. Tepikin. 2002. Calcium leak from intracellular stores-the enigma of calcium signalling. Cell Calcium. 32:355-361. http://dx.doi.org/10.1016/S0143416002001926
9. Collet, C., B. Allard, Y. Tourneur, and V. Jacquemond. 1999. Intracellular calcium signals measured with indo-1 in isolated skeletal muscle fibres from control and mdx mice. J. Physiol. 520:417-429. http://dx.doi.org/10.1111/j.1469-7793.1999.00417.x
10. DiFranco, M., C.E. Woods, J. Capote, and J.L. Vergara. 2008. Dystrophic skeletal muscle fibers display alterations at the level of calcium microdomains. Proc. Natl. Acad. Sci. USA. 105:14698-14703. http://dx.doi.org/10.1073/pnas.0802217105
11. Divet, A., and C. Huchet-Cadiou. 2002. Sarcoplasmic reticulum function in slow- and fast-twitch skeletal muscles from mdx mice. Pflugers Arch. 444:634-643. http://dx.doi.org/10.1007/s00424-002-0854-5
12. 2+ entry in dystrophic mdx mouse muscle. Am. J. Physiol. Cell Physiol. 299:C42-C50. http://dx.doi.org/10.1152/ajpcell.00524.2009
13. Eltit, J.M., H. Li, C.W. Ward, T. Molinski, I.N. Pessah, P.D. Allen, and J.R. Lopez. 2011. Orthograde dihydropyridine receptor signal regulates ryanodine receptor passive leak. Proc. Natl. Acad. Sci. USA. 108:7046-7051. http://dx.doi.org/10.1073/pnas.1018380108
14. Fong, P.Y., P.R. Turner, W.F. Denetclaw, and R.A. Steinhardt. 1990. Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science. 250:673-676. http://dx.doi.org/10.1126/science.2173137
15. Franco, A. Jr., and J.B. Lansman. 1990. Calcium entry through stretchinactivated ion channels in mdx myotubes. Nature. 344:670-673. http://dx.doi.org/10.1038/344670a0
16. Gailly, P. 2002. New aspects of calcium signaling in skeletal muscle cells: implications in Duchenne muscular dystrophy. Biochim. Biophys. Acta. 1600:38-44.
17. Gervásio, O.L., N.P. Whitehead, E.W. Yeung, W.D. Phillips, and D.G. Allen. 2008. TRPC1 binds to caveolin-3 and is regulated by Src kinase - role in Duchenne muscular dystrophy. J. Cell Sci. 121:2246-2255. http://dx.doi.org/10.1242/jcs.032003
18. 2+ pool. Cell Calcium. 48:143-149. http://dx.doi.org/10.1016/j.ceca.2010.08.001
19. Hollingworth, S., U. Zeiger, and S.M. Baylor. 2008. Comparison of the myoplasmic calcium transient elicited by an action potential in intact fibres of mdx and normal mice. J. Physiol. 586:5063-5075. http://dx.doi.org/10.1113/jphysiol.2008.160507
20. 2+ depletion in adult skeletal muscle fibres measured with the biosensor D1ER. Pflugers Arch. 459:725-735. http://dx.doi.org/10.1007/s00424-009-0778-4
21. Kabbara, A.A., and D.G. Allen. 2001. The use of the indicator fluo-5N to measure sarcoplasmic reticulum calcium in single muscle fibres of the cane toad. J. Physiol. 534:87-97. http://dx.doi.org/10.1111/j.1469-7793.2001.00087.x
22. Kargacin, M.E., and G.J. Kargacin. 1996. The sarcoplasmic reticulum calcium pump is functionally altered in dystrophic muscle. Biochim. Biophys. Acta. 1290:4-8. http://dx.doi.org/10.1016/0304-4165(95)00180-8
23. Mallouk, N., V. Jacquemond, and B. Allard. 2000. Elevated subsarcolemmal Ca2+ in mdx mouse skeletal muscle fibers detected with Ca2+-activated K+ channels. Proc. Natl. Acad. Sci. USA. 97:4950-4955. http://dx.doi.org/10.1073/pnas.97.9.4950
24. Plant, D.R., and G.S. Lynch. 2003. Depolarization-induced contraction and SR function in mechanically skinned muscle fibers from dystrophic mdx mice. Am. J. Physiol. Cell Physiol. 285:C522-C528.
25. 2+ release in the presence of maurocalcine in skeletal muscle. Biophys. J. 91:2206-2215. http://dx.doi.org/10.1529/biophysj.105.078089
26. Pouvreau, S., C. Collet, B. Allard, and V. Jacquemond. 2007. Wholecell voltage clamp on skeletal muscle fibers with the silicone-clamp technique. Methods Mol. Biol. 403:185-194. http://dx.doi.org/10.1007/978-1-59745-529-9_12
27. Ríos, E. 2010. The cell boundary theorem: a simple law of the control of cytosolic calcium concentration. J. Physiol. Sci. 60:81-84. http://dx.doi.org/10.1007/s12576-009-0069-z
28. Ruegg, U.T., V. Nicolas-Métral, C. Challet, K. Bernard-Hélary, O.M. Dorchies, S. Wagner, and T.M. Buetler. 2002. Pharmacological control of cellular calcium handling in dystrophic skeletal muscle. Neuromuscul. Disord. 12:S155-S161. http://dx.doi.org/10.1016/S0960-8966(02)00095-0
29. 2+) release in skeletal muscle. J. Gen. Physiol. 138:231-247. http://dx.doi.org/10.1085/jgp.201010592
30. Takagi, A., S. Kojima, M. Ida, and M. Araki. 1992. Increased leakage of calcium ion from the sarcoplasmic reticulum of the mdx mouse. J. Neurol. Sci. 110:160-164. http://dx.doi.org/10.1016/0022-510X(92)90023-E
31. Turner, P.R., T. Westwood, C.M. Regen, and R.A. Steinhardt. 1988. Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature. 335:735-738. http://dx.doi.org/10.1038/335735a0
32. Tutdibi, O., H. Brinkmeier, R. Rüdel, and K.J. Föhr. 1999. Increased calcium entry into dystrophin-deficient muscle fibres of MDX and ADR-MDX mice is reduced by ion channel blockers. J. Physiol. 515:859-868. http://dx.doi.org/10.1111/j.1469-7793.1999.859ab.x
33. Vandebrouck, C., D. Martin, M. Colson-Van Schoor, H. Debaix, and P. Gailly. 2002. Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J. Cell Biol. 158:1089-1096. http://dx.doi.org/10.1083/jcb.200203091
34. Wang, X., N. Weisleder, C. Collet, J. Zhou, Y. Chu, Y. Hirata, X. Zhao, Z. Pan, M. Brotto, H. Cheng, and J. Ma. 2005. Uncontrolled calcium sparks act as a dystrophic signal for mammalian skeletal muscle. Nat. Cell Biol. 7:525-530. http://dx.doi.org/10.1038/ncb1254
35. Woods, C.E., D. Novo, M. DiFranco, and J.L. Vergara. 2004. The action potential-evoked sarcoplasmic reticulum calcium release is impaired in mdx mouse muscle fibres. J. Physiol. 557:59-75. http://dx.doi.org/10.1113/jphysiol.2004.061291
36. 2(+) in the sarcoplasmic reticulum lumen of mammalian skeletal muscle. Biophys. J. 99:2705-2714. http://dx.doi.org/10.1016/j.bpj.2010.08.032