Long-term blocking of calcium channels in mdx mice results in differential effects on heart and skeletal muscle

American Journal of Pathology

Volumn 178, Issue 1, 2011, Pages 273-283

  Jørgensen, Louise H ^a,c   Blain, Alison ^a   Greally, Elizabeth ^a   Laval, Steve H ^a   Blamire, Andrew M ^b   Davison, Benjamin J ^a   Brinkmeier, Heinrich ^d   MacGowan, Guy A ^a,e   Schrøder, Henrik D ^c   Bushby, Kate ^a   Straub, Volker ^a   Lochmüller, Hanns ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^d UNIVERSITY OF GREIFSWALD   (Germany)

^e FREEMAN HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; STREPTOMYCIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3;

ANIMAL TISSUE; ARM MUSCLE; ARTICLE; CLINICAL ASSESSMENT; DIAPHRAGM; DISEASE MODEL; DRUG TREATMENT FAILURE; DUCHENNE MUSCULAR DYSTROPHY; FEMALE; FIBROSIS; HEART MUSCLE; HUMAN; LEG MUSCLE; MOUSE; MUSCLE ATROPHY; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOLEMMA; SKELETAL MUSCLE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

EID: 79251502961     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.11.027     Document Type: Article

References (65)

1. Pilgram GS, Potikanond S, Baines RA, Fradkin LG, Noordermeer JN: The roles of the dystrophin-associated glycoprotein complex at the synapse. Mol Neurobiol 2010, 41:1-21
2. Deconinck N and Dan B: Pathophysiology of Duchenne muscular dystrophy: current hypotheses. Pediatr Neurol 2007, 36:1-7
3. Bodensteiner JB and Engel AG: Intracellular calcium accumulation in Duchenne dystrophy and other myopathies: a study of 567,000 muscle fibers in 114 biopsies. Neurology 1978, 28:439-446
4. Bertorini TE, Palmieri GM, Griffin JW, Igarashi M, McGee J, Brown R, Nutting DF, Hinton AB, Karas JG: Effect of chronic treatment with the calcium antagonist diltiazem in Duchenne muscular dystrophy. Neurology 1988, 38:609-613
5. De Luca A, Nico B, Rolland JF, Cozzoli A, Burdi R, Mangieri D, Giannuzzi V, Liantonio A, Cippone V, De Bellis M, Nicchia GP, Camerino GM, Frigeri A, Svelto M, Camerino DC: Gentamicin treatment in exercised mdx mice: identification of dystrophin-sensitive pathways and evaluation of efficacy in work-loaded dystrophic muscle. Neurobiol Dis 2008, 32:243-253
6. Matsumura CY, Pertille A, Albuquerque TC, Santo Neto H, Marques MJ: Diltiazem and verapamil protect dystrophin-deficient muscle fibers of MDX mice from degeneration: a potential role in calcium buffering and sarcolemmal stability. Muscle Nerve 2009, 39:167-176
7. Pernice W, Beckmann R, Ketelsen UP, Frey M, Schmidt-Redemann B, Haap KP, Roehren R, Sauer M: A double-blind placebo controlled trial of diltiazem in Duchenne dystrophy. Klin Wochenschr 1988, 66:565-570
8. Yeung EW, Whitehead NP, Suchyna TM, Gottlieb PA, Sachs F, Allen DG: Effects of stretch-activated channel blockers on [Ca2+]i and muscle damage in the mdx mouse. J Physiol 2005, 562:367-380
9. Mongini T, Ghigo D, Doriguzzi C, Bussolino F, Pescarmona G, Pollo B, Schiffer D, Bosia A: Free cytoplasmic Ca++ at rest and after cholinergic stimulus is increased in cultured muscle cells from Duchenne muscular dystrophy patients. Neurology 1988, 38:476-480
10. Bakker AJ, Head SI, Williams DA, Stephenson DG: Ca2+ levels in myotubes grown from the skeletal muscle of dystrophic (mdx) and normal mice. J Physiol 1993, 460:1-13
11. Turner PR, Fong PY, Denetclaw WF, Steinhardt RA: Increased calcium influx in dystrophic muscle. J Cell Biol 1991, 115:1701-1712
12. McCarter GC and Steinhardt RA: Increased activity of calcium leak channels caused by proteolysis near sarcolemmal ruptures. J Membr Biol 2000, 176:169-174
13. Vandebrouck C, Martin D, Colson-Van Schoor M, Debaix H, Gailly P: Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J Cell Biol 2002, 158:1089-1096
14. Krüger J, Kunert-Keil C, Bisping F, Brinkmeier H: Transient receptor potential cation channels in normal and dystrophic mdx muscle. Neuromuscul Disord 2008, 18:501-513
15. Whitehead NP, Yeung EW, Allen DG: Muscle damage in mdx (dystrophic) mice: role of calcium and reactive oxygen species. Clin Exp Pharmacol Physiol 2006, 33:657-662
16. Vandebrouck A, Sabourin J, Rivet J, Balghi H, Sebille S, Kitzis A, Raymond G, Cognard C, Bourmeyster N, Constantin B: Regulation of capacitative calcium entries by alpha1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of alpha1- syntrophin. FASEB J 2007, 21:608-617
17. Lee EH, Cherednichenko G, Pessah IN, Allen PD: Functional coupling between TRPC3 and RyR1 regulates the expressions of key triadic proteins. J Biol Chem 2006, 281:10042-10048
18. Rosenberg P, Hawkins A, Stiber J, Shelton JM, Hutcheson K, Bassel-Duby R, Shin DM, Yan Z, Williams RS: TRPC3 channels confer cellular memory of recent neuromuscular activity. Proc Natl Acad Sci USA 2004, 101:9387-9392
19. Millay DP, Goonasekera SA, Sargent MA, Maillet M, Aronow BJ, Molkentin JD: Calcium influx is sufficient to induce muscular dystrophy through a TRPC-dependent mechanism. Proc Natl Acad Sci USA 2009, 106:19023-19028
20. Iwata Y, Katanosaka Y, Arai Y, Shigekawa M, Wakabayashi S: Dominant- negative inhibition of Ca2+ influx via TRPV2 ameliorates muscular dystrophy in animal models. Hum Mol Genet 2009, 18:824-834
21. Teichmann MD, Wegner FV, Fink RH, Chamberlain JS, Launikonis BS, Martinac B, Friedrich O: Inhibitory control over Ca(2+) sparks via mechanosensitive channels is disrupted in dystrophin deficient muscle but restored by mini-dystrophin expression. PLoS One 2008, 3:e3644
22. Bunnell TM, Jaeger MA, Fitzsimons DP, Prins KW, Ervasti JM: Destabilization of the dystrophin-glycoprotein complex without functional deficits in alpha-dystrobrevin null muscle. PLoS ONE 2008, 3:e2604
23. Squire S, Raymackers JM, Vandebrouck C, Potter A, Tinsley J, Fisher R, Gillis JM, Davies KE: Prevention of pathology in mdx mice by expression of utrophin: analysis using an inducible transgenic expression system. Hum Mol Genet 2002, 11:3333-3344
24. Spencer MJ, Croall DE, Tidball JG: Calpains are activated in necrotic fibers from mdx dystrophic mice. J Biol Chem 1995, 270:10909-10914
25. Alderton JM, Steinhardt RA: Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J Biol Chem 2000, 275:9452-9460
26. Courdier-Fruh I, Briguet A: Utrophin is a calpain substrate in muscle cells. Muscle Nerve 2006, 33:753-759
27. Kawamata H, Manfredi G: Mitochondrial dysfunction and intracellular calcium dysregulation in ALS. Mech Ageing Dev 2010, 131:517-526
28. Charge SB, Rudnicki MA: Cellular and molecular regulation of muscle regeneration. Physiol Rev 2004, 84:209-238
29. Bertorini TE, Cornelio F, Bhattacharya SK, Palmieri GM, Dones I, Dworzak F, Brambati B: Calcium and magnesium content in fetuses at risk and prenecrotic Duchenne muscular dystrophy. Neurology 1984, 34:1436-1440
30. Turkel SB, Howell R, Iseri AL, Chui L: Ultrastructure of muscle in fetal Duchenne's dystrophy. Arch Pathol Lab Med 1981, 105:414-418
31. Merrick D, Stadler LK, Larner D, Smith J: Muscular dystrophy begins early in embryonic development deriving from stem cell loss and disrupted skeletal muscle formation. Dis Model Mech 2009, 2:374-388
32. Ghahramani Seno MM, Graham IR, Athanasopoulos T, Trollet C, Pohlschmidt M, Crompton MR, Dickson G: RNAi-mediated knock-down of dystrophin expression in adult mice does not lead to overt muscular dystrophy pathology. Hum Mol Genet 2008, 17:2622-2632
33. Gannier F, White E, Lacampagne A, Garnier D, Le Guennec JY: Streptomycin reverses a large stretch induced increases in [Ca2+]i in isolated guinea pig ventricular myocytes. Cardiovasc Res 1994, 28:1193-1198
34. Willems ME, Stauber WT: Streptomycin and EDTA decrease the number of desmin-negative fibers following stretch injury. Muscle Nerve 2005, 32:310-315
35. Rubin A, Winston J, Rutledge ML: Effects of streptomycin upon the human fetus. AMA Am J Dis Child 1951, 82:14-16
36. Chiu YH, Hornsey MA, Klinge L, Jorgensen LH, Laval SH, Charlton R, Barresi R, Straub V, Lochmüller H, Bushby K: Attenuated muscle regeneration is a key factor in dysferlin-deficient muscular dystrophy. Hum Mol Genet 2009, 18:1976-1989
37. Jørgensen LH, Jensen CH, Wewer UM, Schrøder HD: Transgenic overexpression of ADAM12 suppresses muscle regeneration and aggravates dystrophy in aged mdx mice. Am J Pathol 2007, 171:1599-1607
38. Heiberg E, Engblom H, Engvall J, Hedström E, Ugander M, Arheden H: Semi-automatic quantification of myocardial infarction from delayed contrast enhanced magnetic resonance imaging. Scand Cardiovasc J 2005, 39:267-275
39. McGeachie JK, Grounds MD, Partridge TA, Morgan JE: Age-related changes in replication of myogenic cells in mdx mice: quantitative autoradiographic studies. J Neurol Sci 1993, 119:169-179
40. Tadros SF, Kim Y, Phan PA, Birnbaumer L, Housley GD: TRPC3 ion channel subunit immunolocalization in the cochlea. Histochem Cell Biol 2010, 133:137-147
41. Welch EM, Barton ER, Zhuo J, Tomizawa Y, Friesen WJ, Trifillis P, Paushkin S, Patel M, Trotta CR, Hwang S, Wilde RG, Karp G, Takasugi J, Chen G, Jones S, Ren H, Moon YC, Corson D, Turpoff AA, Campbell JA, Conn MM, Khan A, Almstead NG, Hedrick J, Mollin A, Risher N, Weetall M, Yeh S, Branstrom AA, Colacino JM, Babiak J, Ju WD, Hirawat S, Northcutt VJ, Miller LL, Spatrick P, He F, Kawana M, Feng H, Jacobson A, Peltz SW, Sweeney HL: PTC124 targets genetic disorders caused by nonsense mutations. Nature 2007, 447:87-91
42. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, Barnard PJ: The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 1989, 244:1578-1580
43. Dubois C, Figarella-Branger D, Pastoret C, Rampini C, Karpati G, Rougon G: Expression of NCAM and its polysialylated isoforms during mdx mouse muscle regeneration and in vitro myogenesis. Neuromuscul Disord 1994, 4:171-182
44. Turk R, Sterrenburg E, de Meijer EJ, van Ommen GJ, den Dunnen JT, 't Hoen PA: Muscle regeneration in dystrophin-deficient mdx mice studied by gene expression profiling. BMC Genomics 2005, 6:98
45. Jero J, Coling DE, Lalwani AK: The use of Preyer's reflex in evaluation of hearing in mice. Acta Otolaryngol 2001, 121:585-589 (Pubitemid 32831799)
46. Grounds MD, Radley HG, Lynch GS, Nagaraju K, De Luca A: Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol Dis 2008, 31:1-19
47. Bauer R, Straub V, Blain A, Bushby K, MacGowan GA: Contrasting effects of steroids and angiotensin-converting-enzyme inhibitors in a mouse model of dystrophin-deficient cardiomyopathy. Eur J Heart Fail 2009, 11:463-471
48. Quinlan JG, Hahn HS, Wong BL, Lorenz JN, Wenisch AS, Levin LS: Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscul Disord 2004, 14:491-496
49. Hoffman EP, Brown RH Jr, Kunkel LM: Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987, 51:919-928
50. Angelini C: The role of corticosteroids in muscular dystrophy: a critical appraisal. Muscle Nerve 2007, 36:424-435
51. Lanner JT, Bruton JD, Assefaw-Redda Y, Andronache Z, Zhang SJ, Severa D, Zhang ZB, Melzer W, Zhang SL, Katz A, Westerblad H: Knockdown of TRPC3 with siRNA coupled to carbon nanotubes results in decreased insulin-mediated glucose uptake in adult skeletal muscle cells. FASEB J 2009, 23:1728-1738
52. Goel M, Zuo CD, Sinkins WG, Schilling WP: TRPC3 channels colocalize with Na+/Ca2+ exchanger and Na+ pump in axial component of transverse-axial tubular system of rat ventricle. Am J Physiol Heart Circ Physiol 2007, 292:H874-H883
53. Franco-Obregón A Jr, Lansman JB: Mechanosensitive ion channels in skeletal muscle from normal and dystrophic mice. J Physiol 1994, 481:299-309
54. Zanou N, Shapovalov G, Louis M, Tajeddine N, Gallo C, Van Schoor M, Anguish I, Cao ML, Schakman O, Dietrich A, Lebacq J, Ruegg U, Roulet E, Birnbaumer L, Gailly P: Role of TRPC1 channel in skeletal muscle function. Am J Physiol Cell Physiol 2010, 298:C149-C162
55. Holliday R: Streptomycin, errors in mitochondria and ageing. Biogerontology 2005, 6:431-432
56. Grounds MD, Torrisi J: Anti-TNFalpha (Remicade) therapy protects dystrophic skeletal muscle from necrosis. FASEB J 2004, 18:676-682
57. Acharyya S, Butchbach ME, Sahenk Z, Wang H, Saji M, Carathers M, Ringel MD, Skipworth RJ, Fearon KC, Hollingsworth MA, Muscarella P, Burghes AH, Rafael-Fortney JA, Guttridge DC: Dystrophin glycoprotein complex dysfunction: a regulatory link between muscular dystrophy and cancer cachexia. Cancer Cell 2005, 8:421-432
58. Lullmann H and Vollmer B: An interaction of aminoglycoside antibiotics with Ca binding to lipid monolayers and to biomembranes. Biochem Pharmacol 1982, 31:3769-3773
59. Fayssoil A, Nardi O, Orlikowski D, Annane D: Cardiomyopathy in Duchenne muscular dystrophy: pathogenesis and therapeutics. Heart Fail Rev 2010, 15:103-107
60. Zhang W, ten Hove M, Schneider JE, Stuckey DJ, Sebag-Montefiore L, Bia BL, Radda GK, Davies KE, Neubauer S, Clarke K: Abnormal cardiac morphology, function and energy metabolism in the dystrophic mdx mouse: an MRI and MRS study. J Mol Cell Cardiol 2008, 45:754-760
61. Fanchaouy M, Polakova E, Jung C, Ogrodnik J, Shirokova N, Niggli E: Pathways of abnormal stress-induced Ca2+ influx into dystrophic mdx cardiomyocytes. Cell Calcium 2009, 46:114-121
62. Youm JB, Han J, Kim N, Zhang YH, Kim E, Joo H, Hun LC, Joon KS, Cha KA, Earm YE: Role of stretch-activated channels on the stretch-induced changes of rat atrial myocytes. Prog Biophys Mol Biol 2006, 90:186-206
63. Ward ML, Williams IA, Chu Y, Cooper PJ, Ju YK, Allen DG: Stretch-activated channels in the heart: contributions to length-dependence and to cardiomyopathy. Prog Biophys Mol Biol 2008, 97:232-249
64. Hu JF, Gilmer L, Hopkins R, Wolfinbarger L Jr: Effects of antibiotics on cellular viability in porcine heart valve tissue [Erratum appeared in Cardiovasc Res 1990;24:168]. Cardiovasc Res 1989, 23:960-964
65. Schirmer M, Kaiser A, Lessenich A, Lindemann S, Fedrowitz M, Gernert M, Löscher W: Auditory and vestibular defects and behavioral alterations after neonatal administration of streptomycin to Lewis rats: similarities and differences to the circling (ci2/ci2) Lewis rat mutant. Brain Res 2007, 1155:179-195