Alterations of excitation-contraction coupling and excitation coupled Ca 2+ entry in human myotubes carrying CAV3 mutations linked to rippling muscle

Human Mutation

Volumn 32, Issue 3, 2011, Pages 309-317

  Ullrich, Nina D ^a   Fischer, Dirk ^b,c   Kornblum, Cornelia ^d   Walter, Maggie C ^e   Niggli, Ernst ^a   Zorzato, Francesco ^c,f   Treves, Susan ^c,f  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d UNIVERSITY OF BONN   (Germany)

^e LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^f UNIVERSITY OF FERRARA   (Italy)

Author keywords

Ca 2+ homeostasis; CAV3; Caveolin 3; Excitation coupled Ca 2+ entry; Excitation contraction coupling; Rippling muscle disease; TIRF microscopy

Indexed keywords

CALCIUM ION; CAVEOLIN 3; RYANODINE RECEPTOR;

ARTICLE; AUTOSOMAL DOMINANT DISORDER; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; EXCITATION CONTRACTION COUPLING; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; INTRON; MYOTUBE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RIPPLING MUSCLE DISEASE; RNA SPLICING;

CALCIUM; CALCIUM CHANNELS; CALCIUM CHANNELS, L-TYPE; CAVEOLIN 3; CELLS, CULTURED; CRESOLS; EXCITATION CONTRACTION COUPLING; HUMANS; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MUSCULAR DISEASES; POTASSIUM CHLORIDE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 79951791043     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.21431     Document Type: Article

References (51)

1. Aboumousa A, Hoogendijk J, Charlton R, Barresi R, Herrmann R, Voit T, Hudson J, Roberts M, Hilton-Jones D, Eagle M, Bushby K, Straub V. 2008. Caveolinopathy-new mutations and additional symptoms. Neuromuscul Disord 18:572-578.
2. Armstrong CM, Bezanilla FM, Horowicz P. 1972. Twitches in the presence of ethylene glycol bis(-aminoethylether)-N, N'-tetraacetic acid. Biochim Biophys Acta 267:605-608.
3. 2+ entry. J Gen Physiol 133:79-91.
4. Barrett SD. 2002. Software for scanning microscopy. Proc R Microsc Soc 37:167-174.
5. Betz RC, Schoser BGH, Kasper D, Ricker K, Ramirez A, Stein V, Torbergsen T, Lee YA, Nöthen MM, Wienker TF, Malin JP, Propping P, Reis A, Mortier W, Jentsch TJ, Vorgerd M, Kubisch C. 2001. Mutations in CAV3 cause mechanical hyperirritability of skeletal muscle in rippling muscle disease. Nat Genet 28:218-219.
6. Calaghan S, White E. 2006. Caveolae modulate excitation-contraction coupling and β2-adrenergic signalling in adult rat ventricular myocytes. Cardiovasc Res 69:816-824.
7. Catteruccia M, Sanna T, Santorelli FM, Tessa A, Di Giacopo R, Sauchelli D, Verbo A, Lo Monaco M, Servidei S. 2009. Rippling muscle disease and cardiomyopathy associated with a mutation in the CAV3 gene. Neuromuscul Disord 19:779-783.
8. Cherednichenko G, Hurne AM, Fessenden JD, Lee EH, Allen PD, Beam KG, Pessah IN. 2004. Conformational activation of calcium entry by depolarisation of skeletal muscle myotubes. Proc Natl Acad Sci USA 101:15793-15798.
9. Cherednichenko G, Ward CW, Feng W, Cabrales E, Michaelson L, Samso M, López JR, Allen PD, Pessah IN. 2008. Enhanced Excitation-Coupled Calcium Entry (ECCE) in myotubes expressing malignant hyperthermia mutation R163C is attenuated by dantrolene. Mol Pharmacol 73:1203-1212.
10. Cohen AW, Hnasko R, Schubert W, Lisanti MP. 2004. Role of caveolae and caveolins in health and disease. Physiol Rev 84:1341-1379.
11. Couchoux H, Allard B, Legrand C, Jacquemond V, Berhier C. 2007. Loss of caveolin-3 induced by the dystrophys-associated P104L mutation impairs L-type calcium channel function in mouse skeletal muscle cells. J Physiol 580:745-754.
12. Dart C. 2010. Lipid microdomains and the regulation of ion channel function. J Physiol 588:3169-3178.
13. Delbono J, Xia JY, Treves S, Wang ZM, Jimenez-Moreno R, Payne AM, Messi L, Briguet A, Scharere F, Nishi M, Takeshima H, Zorzato F. 2007. Loss of skeletal muscle strength by ablation of the sarcoplasmic reticulum protein JP45. Proc Natl Acad Sci USA 104:20108-20113.
14. Ducreux S, Zorzato F, Müller C, Sewry C, Muntoni F, Quinlivan R, Restagno G, Girard T, Treves S. 2004. Effect of ryanodine receptor mutations on IL-6 release and intracellular calcium homeostasis in human myotubes from malignant hyperthermia susceptible individuals and patients affected by central core disease. J Biol Chem 279:43838-43846.
15. Edelman W, Lisanti MP. 2001. Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex and T-tubule abnormalities. J Biol Chem 276:21425-21433.
16. Fischer D, Schroers A, Blümcke I, Urbach H, Zerres K, Mortier W, Vorgerd M, Schröder R. 2003. Consequences of a novel caveolin-3 mutation in a large German family. Ann Neurol 53:233-241.
17. Fleischer S, Inui M. 1989. Biochemistry and biophysics of excitation-contraction coupling. Annu Rev Biophys Biophys Chem 18:333-364.
18. Franzini-Armstrong C, Jorgensen AO. 1994. Structure and development of E-C coupling units in skeletal muscle. Annu Rev Physiol 56:509-534.
19. Galbiati F, Engelman JA, Volonte D, Zhang XL, Minetti C, Li M, Hou H, Kneitz B, Galbiati F, Razani B, Lisanti MP. 2001. Caveolae and caveolin-3 in muscular dystrophy. Trends Mol Med 7:435-440.
20. Galbiati F, Volonte D, Minetti C, Chu JB, Lisanti MP. 1999. Phenotypic behavior of caveolin-3 mutations that cause autosomal dominant limb girdle muscular dystrophy (LGMD-1C). Retention of LGMD-1C caveolin-3 mutatnts within the golgi complex. J Biol Chem 274:25632-25641.
21. García-Cardeña G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, Lisanti MP, Sessa WC. 1997. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem 272:25437-25440.
22. Gazzerro E, Solgia F, Bruno C, Lisanti M, Minetti C. 2010. Caveolinopathies: from the biology of caveolin-3 to human diseases. Eur J Hum Genet 18:137-145.
23. Hansen CG, Nichols BJ. 2010. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 20:177-186.
24. Hayashi T, Arimura T, Ueda K, Shibata H, Hohda S, Takahashi M, Hori H, Koga Y, Oka N, Imaizumi T, Yasunami M, Kimura A. 2004. Identification and functional analysis of a caveolin-3 mutation associated with familial hypertrophic cardiomyopathy. Biochem Bophys Res Comm 313:178-184.
25. Hnasko R, Lisanti MP. 2003. The biology of caveolae: lessons from caveolin KO mice and implications for human disease. Mol Interv 3:445-464.
26. 2+ homeostasis of single smooth muscle cells from rat cerebral resistance arteries. Am J Physiol Heart Circ Physiol 293:H204-H214.
27. + pump location and translocation during muscle contraction in rat muscle. Eur J Physiol 456:979-989.
28. Lamb GD. 2005. Rippling muscle disease may be caused by "silent" action potentials in the tubular system of skeletal muscle fibers. Muscle Nerve 31:652-658.
29. 2+ release channel of sarcoplasmic reticulum. J Biol Chem 261:6300-6306.
30. Mizrahi V, Brooksbank RL, Nkabinde NC. 1994. Mutagenesis of the conserved aspartic acid 443, glutamic acid 478, asparagine 494, and aspartic acid 498 residues in the ribonuclease H domain of p66/p51 human immunodeficiency virus type I reverse transcriptase. Expression and biochemical analysis. J Biol Chem 269:19245-19249.
31. Müller JS, Piko H, Schoser BG, Schlotter-Weigel B, Reilich P, Gürster S, Born C, Karcagi V, Pongratz D, Lochmüller H, Walter MC. 2006. Novel splice site mutation in the caveolin-3 gene leading to autosomal recessive limb girdle muscular dystrophy. Neuromuscul Disord 16:432-436.
32. Murata T, Lin MI, Stan RV, Bauer PM, Yu J, Sessa WC. 2007. Genetic evidence supporting caveolae microdomain regulation of calcium entry in endothelial cells. J Biol Chem 282:16631-16643.
33. Murphy RM, Mollica JP, Lamb GD. 2009. Plasma membrane removal in rat skeletal muscle fibres reveals caveolin-3 hot-spots at the neck of the transverse tubules. Exp Cell Res 315:1015-1028.
34. Nixon SJ, Wegner J, Ferguson C, Méry PF, Hancock JF, Currie PD, Key B, Westerfield M, Parton RG. 2005. Zebrafish as a model for caveolin-associated muscle disease; caveolin-3 is required for myofibril organization and muscle cell patterning. Humn Mol Genet 14:1727-1743.
35. Rios E, Pizarro G. 1991. Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol Rev 71:849-908.
36. Scriven DR, Klimek A, Asghari P, Bellve K, Moore ED. 2005. Caveoli-3 is adjacent to a group of exradyadic ryanodine receptors. Biophys J 89:1893-1901.
37. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, Lisanti MP. 1996.Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 271:15160-15165.
38. Sotgia F, Bonuccelli G, Minetti C, Woodman SE, Capozza F, Kemp RG, Scherer PE, Lisanti MP. 2003. Phosphofructokinase muscle-specific isoform requires caveolin-3 expression for plasma membrane recruitment and caveolar targeting. Am J Pathol 163:2619-2634.
39. Sotgia F, Lee JK, Das K, Bedford M, Petrucci TC, Macioce P, Sargiacomo M, Bricarelli FD, Minetti C, Sudol M, Lisanti MP. 2000. Caveolin-3 directly interacts with the C-terminal tail of beta-dystroglycan. Identification of a central WW-like domain within caveolin family members. J Biol Chem 275:38048-38058.
40. Treves S, Anderson AA, Ducreux S, Divet A, Bleunven C, Grasso C, Paesante S, Zorzato F. 2005. Ryanodine receptor 1 mutations, dysregulation of calcium homeostasis and neuromuscular disorders. Neuromuscul Disord 15:577-587.
41. 2+ influx occurs at stable plasma membrane and endoplasmice reticulum junctions. J Cell Sci 123:4170-4181.
42. Treves S, Vukcevic M, Maj M, Thurnheer R, Mosca B, Zorzato F. 2009. Minor sarcoplasmic reticulum membrane components that modulate excitation-contraction coupling in striated muscles. J Physiol 587:3071-3079.
43. Vassilopoulos S, Oddoux S, Groh S, Cacheux M, Fauré J, Brocard J, Campbell KP, Marty I. 2010. Caveolin 3 is associated with the calcium release channel complex and is modified via in vivo triadin modification. Biochemistry 49:6130-6135.
44. Vatta M, Ackerman MJ, Ye B, Makielski JC, Ughanze EE, Taylor EW, Tester DJ, Balijepalli RC, Foell JD, Li Z, Kamp TJ, Towbin JA. 2006. Mutant Caveolin-3 induces persistent late sodium current and is associated with long-QT syndrome. Circulation 114:2104-2112.
45. Volonte D, Peoples AJ, Galbiati F. 2003. Modulation of myoblast fusion by caveolin-3 in dystrophic skeletal muscle cells: implications for Duchenne Muscular dystrophy and Limb-Girdle Muscular Dysrophy-1C. Mol Biol Cell 14:4075-4088.
46. 2+ channel function of the dihydropyridine receptor. Eur J Physiol 457:361-375.
47. Wilmshurst JM, Lillis S, Zhou H, Pillay K, Henderson H, Kress W, Müller CR, Ndondo A, Cloke V, Cullup T, Bertini E, Boennemann C, Straub V, Quinlivan R, Dowling JJ, Al-Sarraj S, Treves S, Manzur AY, Sewry CA, Muntoni FH. Jungbluth H. 2010. Mutations in RYR1 are a common cause of centronuclear myopathy. Ann Neurol (in press).
48. Woodman SE, Sotgia F, Galbiati F, Minetti C, Lisanti M. 2004. Caveolinopathies. Mutations in caveolin-3 cause four distinct autosomal dominant muscle diseases. Neurology 62:538-543.
49. Yang T, Allen PD, Pessah IN, Lopez JR. 2007. Enhanced excitation-coupled calcium entry in myotubes is associated with expression of RyR1 malignant hyperthermia mutations. J Biol Chem 282:37471-37478.
50. Zhou H, Jungbluth H, Sewry CA, Feng L, Bertini E, Bushby K, Straub V, Roper H, Rose MR, Brockington M, Kinali M, Manzur A, Robb S, Appleton R, Messina, S, D'Amico A, Müller CR, Brown S, Treves S, Muntoni F. 2007. Molecular mechanisms and phenotypic variation in RYR1-related congenital myopathies. Brain 130:2024-2036.
51. 2+ release. Mol Pharmacol 44:1192-1201.