Impaired functional communication between the L-type calcium channel and mitochondria contributes to metabolic inhibition in the mdx heart

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 28, 2014, Pages

  Viola, Helena M ^a   Adams, Abbie M ^a   Davies, Stefan M K ^a   Fletcher, Susan ^a,b   Filipovska, Aleksandra ^a   Hool, Livia C ^a,c  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b MURDOCH UNIVERSITY   (Australia)

^c VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

Author keywords

Cytoskeleton; Ion channels; Structure

Indexed keywords

CALCIUM CHANNEL L TYPE; DYSTROPHIN; MORPHOLINO OLIGONUCLEOTIDE; VOLTAGE DEPENDENT ANION CHANNEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANION TRANSPORT; ARTICLE; CARDIOMYOPATHY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; EXON; EXON SKIPPING; HEART MUSCLE CELL; HEART VENTRICLE WALL; MALE; METABOLIC INHIBITION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

CYTOSKELETON; ION CHANNELS; STRUCTURE;

ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; DYSTROPHIN; EXONS; HEART VENTRICLES; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED MDX; MITOCHONDRIAL MEMBRANES; MORPHOLINOS; MUSCULAR DYSTROPHY, DUCHENNE; MYOCARDIUM; MYOCYTES, CARDIAC;

EID: 84904329149     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1402544111     Document Type: Article

References (43)

1. Finsterer J, Stöllberger C (2003) The heart in human dystrophinopathies. Cardiology 99(1):1-19. (Pubitemid 36206630)
2. Khairallah M, et al. (2007) Metabolic and signaling alterations in dystrophin-deficient hearts precede overt cardiomyopathy. J Mol Cell Cardiol 43(2):119-129. (Pubitemid 47069387)
3. Tokuyasu KT, Dutton AH, Singer SJ (1983) Immunoelectron microscopic studies of desmin (skeletin) localization and intermediate filament organization in chicken cardiac muscle. J Cell Biol 96(6):1736-1742. (Pubitemid 13034451)
4. Thornell LE, et al. (1985) Intermediate filament and associated proteins in heart Purkinje fibers: A membrane-myofibril anchored cytoskeletal system. Ann N Y Acad Sci 455:213-240.
5. Lader AS, Kwiatkowski DJ, Cantiello HF (1999) Role of gelsolin in the actin filament regulation of cardiac L-type calcium channels. Am J Physiol 277(6 Pt 1):C1277-C1283. (Pubitemid 30045985)
6. Hohaus A, et al. (2002) The carboxyl-terminal region of ahnak provides a link between cardiac L-type Ca2+ channels and the actin-based cytoskeleton. FASEB J 16(10):1205-1216. (Pubitemid 34815408)
7. 2+ currents via cofilin-activated depolymerization of F-actin in guinea-pig cardiomyocytes. J Physiol 537(Pt 2):363-370.
8. 2+) channel current in cultured vascular smooth muscle cells. Am J Physiol Cell Physiol 279(2):C480-C487.
9. 2+ channel in ventricular myocytes. J Mol Cell Cardiol 46(6):1016-1026.
10. Viola HM, Hool LC (2010) Cross-talk between L-type Ca2+ channels and mitochondria. Clin Exp Pharmacol Physiol 37(2):229- 235.
11. Woolf PJ, et al. (2006) Alterations in dihydropyridine receptors in dystrophin-deficient cardiac muscle. Am J Physiol Heart Circ Physiol 290(6):H2439-H2445. (Pubitemid 43846073)
12. Viola HM, Davies SM, Filipovska A, Hool LC (2013) L-type Ca(2+) channel contributes to alterations in mitochondrial calcium handling in the mdx ventricular myocyte. Am J Physiol Heart Circ Physiol 304(6):H767-H775.
13. Koenig X, et al. (2011) Voltage-gated ion channel dysfunction precedes cardiomyopathy development in the dystrophic heart. PLoS ONE 6(5):e20300.
14. 1- subunit. Nature 368(6466):67-70.
15. 2+ ions. J Biol Chem 280(13):12474-12485.
16. 1)-ATPase. Am J Physiol Cell Physiol 278(2):C423-C435.
17. Balaban RS (2002) Cardiac energy metabolism homeostasis: Role of cytosolic calcium. J Mol Cell Cardiol 34(10):1259-1271.
18. Gebski BL, Mann CJ, Fletcher S, Wilton SD (2003) Morpholino antisense oligonucleotide induced dystrophin exon 23 skipping in mdx mouse muscle. Hum Mol Genet 12(15):1801-1811. (Pubitemid 36944135)
19. Cirak S, et al. (2011) Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: An open-label, phase 2, dose-escalation study. Lancet 378(9791):595-605.
20. Kinali M, et al. (2009) Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: A single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol 8(10):918-928.
21. Crompton M, Virji S, Ward JM (1998) Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. Eur J Biochem 258(2):729-735. (Pubitemid 28557940)
22. Rostovtseva T, Colombini M (1996) ATP flux is controlled by a voltage-gated channel from the mitochondrial outer membrane. J Biol Chem 271(45):28006-28008. (Pubitemid 26374603)
23. Galli A, DeFelice LJ (1994) Inactivation of L-type Ca channels in embryonic chick ventricle cells: Dependence on the cytoskeletal agents colchicine and taxol. Biophys J 67(6):2296-2304. (Pubitemid 24369653)
24. Hao LY, Xu JJ, Minobe E, Kameyama A, Kameyama M (2008) Calmodulin kinase II activation is required for the maintenance of basal activity of L-type Ca2+ channels in guinea-pig ventricular myocytes. J Pharmacol Sci 108(3):290-300.
25. Nichols CB, et al. (2010) Sympathetic stimulation of adult cardiomyocytes requires association of AKAP5 with a subpopulation of L-type calcium channels. Circ Res 107(6):747-756.
26. Spurney CF, et al. (2008) Dystrophin-deficient cardiomyopathy in mouse: Expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart. Neuromuscul Disord 18(5):371-381.
27. Bloch RJ, et al. (2002) Costameres: Repeating structures at the sarcolemma of skeletal muscle. Clin Orthop Relat Res (403, Suppl):S203-S210. (Pubitemid 35346007)
28. Quinlan JG, et al. (2004) Evolution of the mdx mouse cardiomyopathy: Physiological and morphological findings. Neuromuscul Disord 14(8-9):491-496. (Pubitemid 39141704)
29. 2+ channel by the actin-binding proteins α-actinin and dystrophin. Am J Physiol Cell Physiol 282(6):C1502-C1511.
30. Capetanaki Y (2002) Desmin cytoskeleton: A potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc Med 12(8):339-348.
31. Braun U, et al. (2001) Lack of dystrophin is associated with altered integration of the mitochondria and ATPases in slow-twitch muscle cells of MDX mice. Biochim Biophys Acta 1505(2-3):258- 270.
32. 2+ signalling and reactive oxygen species-generating pathways. Cardiovasc Res 77(4):766-773.
33. Allen DG, Gervasio OL, Yeung EW, Whitehead NP (2010) Calcium and the damage pathways in muscular dystrophy. Can J Physiol Pharmacol 88(2):83-91.
34. Rostovtseva TK, et al. (2008) Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc Natl Acad Sci USA 105(48):18746-18751.
35. Kay L, et al. (1997) Study of regulation of mitochondrial respiration in vivo. An analysis of influence of ADP diffusion and possible role of cytoskeleton. Biochim Biophys Acta 1322(1):41-59. (Pubitemid 27497127)
36. Shoshan-Barmatz V, Ben-Hail D (2012) VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion 12(1):24-34.
37. Hool LC (2000) Hypoxia increases the sensitivity of the L-type Ca(2+) current to beta-adrenergic receptor stimulation via a C2 region-containing protein kinase C isoform. Circ Res 87(12):1164-1171.
38. Viola HM, Arthur PG, Hool LC (2007) Transient exposure to hydrogen peroxide causes an increase in mitochondria-derived superoxide as a result of sustained alteration in L-type Ca2+ channel function in the absence of apoptosis in ventricular myocytes. Circ Res 100(7):1036-1044. (Pubitemid 46598928)
39. Yaniv Y, et al. (2011) Ca2+-regulated-cAMP/PKA signaling in cardiac pacemaker cells links ATP supply to demand. J Mol Cell Cardiol 51(5):740-748.
40. Mann CJ, et al. (2001) Antisense-induced exon skipping and synthesis of dystrophin in the mdx mouse. Proc Natl Acad Sci USA 98(1):42-47. (Pubitemid 32095860)
41. Mann CJ, Honeyman K, McClorey G, Fletcher S, Wilton SD (2002) Improved antisense oligonucleotide induced exon skipping in the mdx mouse model of muscular dystrophy. J Gene Med 4(6):644-654. (Pubitemid 40277188)
42. Tang H, Viola HM, Filipovska A, Hool LC (2011) Ca(v)1.2 calcium channel is glutathionylated during oxidative stress in guinea pig and ischemic human heart. Free Radic Biol Med 51(8):1501-1511.
43. Davies SM, Poljak A, Duncan MW, Smythe GA, Murphy MP (2001) Measurements of protein carbonyls, ortho- and meta-tyrosine and oxidative phosphorylation complex activity in mitochondria from young and old rats. Free Radic Biol Med 31(2):181-190. (Pubitemid 32607585)