Dysferlin interacts with calsequestrin-1, myomesin-2 and dynein in human skeletal muscle

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 8, 2013, Pages 1927-1938

  Flix, Bàrbara ^a,b   De La Torre, Carolina ^c   Castillo, Juan ^a,b   Casal, Carme ^d   Illa, Isabel ^a,b   Gallardo, Eduard ^a,b  

^a HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^d Servei de Microscopia   (Spain)

Author keywords

Blue native; Cytoplasmic dynein; Dysferlin; FLIM FRET analysis; Trim72 MG53

Indexed keywords

ANNEXIN; CALSEQUESTRIN; CALSEQUESTRIN 1; CAVEOLIN 3; CYTOPLASMIC DYNEIN; DYSFERLIN; MYOMESIN; MYOMESIN 2; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AMINO ACID SEQUENCE; ARTICLE; CASE REPORT; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; DYSFERLINOPATHY; FASCIO SCAPULO HUMERAL DYSTROPHY; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEL ELECTROPHORESIS; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; MALE; MUSCLE BIOPSY; MYOTUBE; PROTEIN PROTEIN INTERACTION; SKELETAL MUSCLE;

EID: 84880182169     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.06.007     Document Type: Article

References (66)

1. Agarkova I, Perriard JC. The M-band: an elastic web that crosslinks thick filamentsin the center of the sarcomere. Trends in Cell Biology 2005;15:477-85. (Pubitemid 41253467)
2. Agarkova I, Ehler E, Lange S, Schoenauer R, Perriard JC. M-band: a safe-guard for sarcomere stability? Journal of Muscle Research and Cell Motility 2003;24:191-203.
3. Agarkova I, Schoenauer R, Ehler E, Carlsson L, Carlsson E, Thornell LE, Perriard JC. Themolecular composition of the sarcomeric M-band correlates with muscle fibertype. European Journal of Cell Biology 2004;83:193-204. (Pubitemid 39117482)
4. Ahmad FJ, He Y, Myers KA, Hasaka TP, Francis F, Black MM, Baas PW. Effectsof dynactin disruption and dynein depletion on axonal microtubules. Traffic 2006;7:524-37. (Pubitemid 44026751)
5. Albrecht DE, Garg N, Rufibach LE, Williams BA, Monnier N, Hwang E, Mittal P. 4thAnnual Dysferlin Conference 11-14 September 2010, Washington, USA. Neuro-muscular Disorders: NMD 2010;21:304-10.
6. Ampong BN, Imamura M, Matsumiya T, Yoshida M, Takeda S. Intracellular local-ization of dysferlin and its association with the dihydropyridine receptor. Acta Myologica 2005;24:134-44. (Pubitemid 43287351)
7. Askanas V, Shafiq SA, Milhorat AT. Normal and dystrophic chicken muscle at suc-cessive stages in tissue culture. Archives of Neurology 1971;24:259-65.
8. Azakir BA, Di Fulvio S, Therrien C, Sinnreich M. Dysferlin interacts with tubulin andmicrotubules in mouse skeletal muscle. PLoS ONE 2010;5:e 10122.
9. Badiola N, de Oliveira RM, Herrera F, Guardia-Laguarta C, Goncalves SA, Pera M,Suarez-Calvet M, Clarimon J, Outeiro TF, Lleo A. Tau enhances alpha-synucleinaggregation and toxicity in cellular models of synucleinopathy. PLoS ONE 2011;6:e 26609.
10. Ban N, Escobar C, Garcia R, Hasel K, Day J, Greenwood A, McPherson A. Crystalstructure of an idiotype-anti-idiotype Fab complex. Proceedings of the National Academy of Sciences of the United States of America 1994;91:1604-8.
11. Bansal D, Campbell KP. Dysferlin and the plasma membrane repair in musculardystrophy. Trends in Cell Biology 2004;14:206-13. (Pubitemid 38447120)
12. Bashir R, Keers S, Strachan T, Passos-Bueno R, Zatz M, Weissenbach J, Le Paslier D,Meisler M, Bushby K. Genetic and physical mapping at the limb-girdle musculardystrophy locus (LGMD2B) on chromosome 2p. Genomics 1996;33:46-52. (Pubitemid 26119393)
13. Bashir R, Britton S, Strachan T, Keers S, Vafiadaki E, Lako M, Richard I, Marchand S,Bourg N, Argov Z, Sadeh M, Mahjneh I, Marconi G, Passos-Bueno MR, Moreira Ede S, Zatz M, Beckmann JS, Bushby K. A gene related to Caenorhabditis elegansspermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type2B. Nature Genetics 1998;20:37-42. (Pubitemid 28410340)
14. Bohm J, Leshinsky-Silver E, Vassilopoulos S, Le Gras S, Lerman-Sagie T, GinzbergM, Jost B, Lev D, Laporte J. Samaritan myopathy, an ultimately benign con-genital myopathy, is caused by a RYR1 mutation. Acta Neuropathologica 2012;124:575-81.
15. Borgonovo B, Cocucci E, Racchetti G, Podini P, Bachi A, Meldolesi J. Regulated exo-cytosis: a novel, widely expressed system. Nature Cell Biology 2002;4:955-62. (Pubitemid 35469425)
16. Brule C, Dargelos E, Diallo R, Listrat A, Bechet D, Cottin P, Poussard S. Proteomicstudy of calpain interacting proteins during skeletal muscle aging. Biochimie 2010;92:1923-33.
17. Cacciottolo M, Belcastro V, Laval S, Bushby K, di Bernardo D, Nigro V. Reverse engi-neering gene network identifies new dysferlin-interacting proteins. Journal ofBiological Chemistry 2010;286:5404-13.
18. Cagliani R, Magri F, Toscano A, Merlini L, Fortunato F, Lamperti C, Rodolico C, PrelleA, Sironi M, Aguennouz M, Ciscato P, Uncini A, Moggio M, Bresolin N, Comi GP. Mutation finding in patients with dysferlin deficiency and role of the dysfer-lin interacting proteins annexin A1 and A2 in muscular dystrophies. Human Mutation 2005;26:283.
19. Cai C, Masumiya H, Weisleder N, Matsuda N, Nishi M, Hwang M, Ko JK, Lin P,Thornton A, Zhao X, Pan Z, Komazaki S, Brotto M, Takeshima H, Ma J. MG53nucleates assembly of cell membrane repair machinery. Nature Cell Biology 2009a;11:56-64.
20. Cai C, Weisleder N, Ko JK, Komazaki S, Sunada Y, Nishi M, Takeshima H, Ma J. Membrane repair defects in muscular dystrophy are linked to altered interac-tion between MG53, caveolin-3, and dysferlin. Journal of Biological Chemistry 2009b;284:15894-902.
21. Campanaro S, Romualdi C, Fanin M, Celegato B, Pacchioni B, Trevisan S, LavederP, De Pitta C, Pegoraro E, Hayashi YK, Valle G, Angelini C, Lanfranchi G. Geneexpression profiling in dysferlinopathies using a dedicated muscle microarray. Human Molecular Genetics 2002;11:3283-98. (Pubitemid 36054657)
22. Collins JH, Tarcsafalvi A, Ikemoto N. Identification of a region of calsequestrin thatbinds to the junctional face membrane of sarcoplasmic reticulum. Biochemicaland Biophysical Research Communications 1990;167:189-93. (Pubitemid 20085368)
23. Davis DB, Doherty KR, Delmonte AJ, McNally EM. Calcium-sensitive phospholipidbinding properties of normal and mutant ferlin C2 domains. Journal of Biological Chemistry 2002;277:22883-8. (Pubitemid 34967270)
24. De Luna N, Gallardo E, Illa I. In vivo and in vitro dysferlin expression in humanmuscle satellite cells. Journal of Neuropathology and Experimental Neurology 2004;63:1104-13. (Pubitemid 39372594)
25. de Luna N, Gallardo E, Soriano M, Dominguez-Perles R, de la Torre C, Rojas-Garcia R,Garcia-Verdugo JM, Illa I. Absence of dysferlin alters myogenin expression anddelays human muscle differentiation in vitro. Journal of Biological Chemistry 2006;281:17092-8.
26. de Morree A, Hensbergen PJ, van Haagen HH, Dragan I, Deelder AM, t Hoen PA, Frants RR, van der Maarel SM. Proteomic analysis of the dysferlin protein complexunveils its importance for sarcolemmal maintenance and integrity. PLoS ONE 2010;5:e 13854.
27. Demonbreun AR, Fahrenbach JP, Deveaux K, Earley JU, Pytel P, McNally EM. Impairedmuscle growth and response to insulin-like growth factor 1 in dysferlin-mediated muscular dystrophy. Human Molecular Genetics 2010;20:779-89.
28. Di Fulvio S, Azakir BA, Therrien C, Sinnreich M. Dysferlin interacts withhistone deacetylase 6 and increases alpha-tubulin acetylation. PLoS ONE 2011;6:e 28563.
29. Dompierre JP, Godin JD, Charrin BC, Cordelieres FP, King SJ, Humbert S, SaudouF. Histone deacetylase 6 inhibition compensates for the transport deficit inHuntington's disease by increasing tubulin acetylation. Journal of Neuroscience 2007;27:3571-83. (Pubitemid 46515140)
30. Dujardin DL, Barnhart LE, Stehman SA, Gomes ER, Gundersen GG, Vallee RB. A role forcytoplasmic dynein and LIS1 in directed cell movement. Journal of Cell Biology 2003;163:1205-11. (Pubitemid 38032082)
31. Fliegel L, Ohnishi M, Carpenter MR, Khanna VK, Reithmeier RA, MacLennan DH. Amino acid sequence of rabbit fast-twitch skeletal muscle calsequestrin deducedfrom cDNA and peptide sequencing. Proceedings of the National Academy ofSciences of the United States of America 1987;84:1167-71. (Pubitemid 17027313)
32. Förster VT, Mielczarek EV, Greenbaum E, Knox RS. Intermolecular energy migra-tion and fluorescence (Translation of Förster, T., 1948). In: Biological Physics. American Institute of Physics; 1948. p. 183-221.
33. Glover L, Brown RH Jr. Dysferlin in membrane trafficking and patch repair. Traffic 2007;8:785-94. (Pubitemid 46971627)
34. Guardia-Laguarta C, Coma M, Pera M, Clarimon J, Sereno L, Agullo JM, Molina-Porcel L, Gallardo E, Deng A, Berezovska O, Hyman BT, Blesa R, Gomez-Isla T,Lleo A. Mild cholesterol depletion reduces amyloid-beta production by impair-ing APP trafficking to the cell surface. Journal of Neurochemistry 2009;110:220-30.
35. Haase H, Podzuweit T, Lutsch G, Hohaus A, Kostka S, Lindschau C, Kott M, Kraft R,Morano I. Signaling from beta-adrenoceptor to L-type calcium channel: iden-tification of a novel cardiac protein kinase A target possessing similarities toAHNAK. FASEB Journal 1999;13:2161-72.
36. Hernandez-Deviez DJ, Howes MT, Laval SH, Bushby K, Hancock JF, Parton RG. Cave-olin regulates endocytosis of the muscle repair protein, dysferlin. Journal ofBiological Chemistry 2008;283:6476-88.
37. Hohaus A, Person V, Behlke J, Schaper J, Morano I, Haase H. The carboxyl-terminalregion of ahnak provides a link between cardiac L-type Ca2+channels and theactin-based cytoskeleton. FASEB Journal 2002;16:1205-16. (Pubitemid 34815408)
38. Huang Y, Verheesen P, Roussis A, Frankhuizen W, Ginjaar I, Haldane F, Laval S, Ander-son LV, Verrips T, Frants RR, de Haard H, Bushby K, den Dunnen J, van der Maarel SM. Protein studies in dysferlinopathy patients using llama-derived antibodyfragments selected by phage display. European Journal of Human Genetics: EJHG 2005;13:721-30. (Pubitemid 40846844)
39. Huang Y, Laval SH, van Remoortere A, Baudier J, Benaud C, Anderson LV, Straub V,Deelder A, Frants RR, den Dunnen JT, Bushby K, van der Maarel SM. AHNAK,a novel component of the dysferlin protein complex, redistributes to thecytoplasm with dysferlin during skeletal muscle regeneration. FASEB Journal 2007;21:732-42. (Pubitemid 46348249)
40. Huang Y, de Morree A, van Remoortere A, Bushby K, Frants RR, Dunnen JT, van derMaarel SM. Calpain 3 is a modulator of the dysferlin protein complex in skeletalmuscle. Human Molecular Genetics 2008;17:1855-66. (Pubitemid 351791513)
41. Illa I, Serrano-Munuera C, Gallardo E, Lasa A, Rojas-Garcia R, Palmer J, Gallano P,Baiget M, Matsuda C, Brown RH. Distal anterior compartment myopathy: adysferlin mutation causing a new muscular dystrophy phenotype. Annals ofNeurology 2001;49:130-4. (Pubitemid 32163018)
42. Illa I, De Luna N, Dominguez-Perles R, Rojas-Garcia R, Paradas C, Palmer J, Mar-quez C, Gallano P, Gallardo E. Symptomatic dysferlin gene mutation carriers:characterization of two cases. Neurology 2007;68:1284-9. (Pubitemid 46625974)
43. Klinge L, Harris J, Sewry C, Charlton R, Anderson L, Laval S, Chiu YH, Hornsey M,Straub V, Barresi R, Lochmuller H, Bushby K. Dysferlin associates with the devel-oping T-tubule system in rodent and human skeletal muscle. Muscle and Nerve 2010;41:166-73.
44. Krahn M, Beroud C, Labelle V, Nguyen K, Bernard R, Bassez G, Figarella-Branger D,Fernandez C, Bouvenot J, Richard I, Ollagnon-Roman E, Bevilacqua JA, Salvo E,Attarian S, Chapon F, Pellissier JF, Pouget J, Hammouda el H, Laforet P, Urtizberea JA, Eymard B, Leturcq F, Levy N. Analysis of the DYSF mutational spectrum in alarge cohort of patients. Human Mutation 2009;30:E345-75.
45. Lennon NJ, Kho A, Bacskai BJ, Perlmutter SL, Hyman BT, Brown RH Jr. Dysferlininteracts with annexins A1 and A2 and mediates sarcolemmal wound-healing. Journal of Biological Chemistry 2003;278:50466-73. (Pubitemid 37548892)
46. Liu J, Aoki M, Illa I, Wu C, Fardeau M, Angelini C, Serrano C, Urtizberea JA, HentatiF, Hamida MB, Bohlega S, Culper EJ, Amato AA, Bossie K, Oeltjen J, Bejaoui K,McKenna-Yasek D, Hosler BA, Schurr E, Arahata K, de Jong PJ, Brown RH Jr. Dys-ferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limbgirdle muscular dystrophy. Nature Genetics 1998;20:31-6. (Pubitemid 28410339)
47. Madaro L, Marrocco V, Fiore P, Aulino P, Smeriglio P, Adamo S, Molinaro M, Bouche M.PKCtheta signaling is required for myoblast fusion by regulating the expressionof caveolin-3 and beta1D integrin upstream focal adhesion kinase. Molecular Biology of the Cell 2011;22:1409-19.
48. Matsuda C, Hayashi YK, Ogawa M, Aoki M, Murayama K, Nishino I, Nonaka I, ArahataK, Brown RH Jr. The sarcolemmal proteins dysferlin and caveolin-3 interact inskeletal muscle. Human Molecular Genetics 2001;10:1761-6. (Pubitemid 32899093)
49. Matsuda C, Kameyama K, Tagawa K, Ogawa M, Suzuki A, Yamaji S, OkamotoH, Nishino I, Hayashi YK. Dysferlin interacts with affixin (beta-parvin) atthe sarcolemma. Journal of Neuropathology and Experimental Neurology 2005;64:334-40. (Pubitemid 40489560)
50. Minetti C, Sotgia F, Bruno C, Scartezzini P, Broda P, Bado M, Masetti E, Mazzocco M,Egeo A, Donati MA, Volonte D, Galbiati F, Cordone G, Bricarelli FD, Lisanti MP,Zara F. Mutations in the caveolin-3 gene cause autosomal dominant limb-girdlemuscular dystrophy. Nature Genetics 1998;18:365-8. (Pubitemid 28158166)
51. Miyoshi K, Kawai H, Iwasa M, Kusaka K, Nishino H. Autosomal recessive distalmuscular dystrophy as a new type of progressive muscular dystrophy. Seven-teen cases in eight families including an autopsied case. Brain 1986;109(Pt 1):31-54. (Pubitemid 16125183)
52. Murphy RM, Larkins NT, Mollica JP, Beard NA, Lamb GD. Calsequestrin contentand SERCA determine normal and maximal Ca2+storage levels in sarcoplas-mic reticulum of fast- and slow-twitch fibres of rat. Journal of Physiology 2009;587:443-60.
53. Nguyen K, Bassez G, Krahn M, Bernard R, Laforet P, Labelle V, Urtizberea JA, Figarella-Branger D, Romero N, Attarian S, Leturcq F, Pouget J, LevyN, Eymard B. Phenotypic study in 40 patients with dysferlin gene muta-tions: high frequency of atypical phenotypes. Archives of Neurology 2007;64:1176-82. (Pubitemid 47258078)
54. Paradas C, Gonzalez-Quereda L, De Luna N, Gallardo E, Garcia-Consuegra I, Gomez H,Cabello A, Illa I, Gallano P. A new phenotype of dysferlinopathy with congenitalonset. Neuromuscular Disorders: NMD 2009;19:21-5.
55. Paradas C, Llauger J, Diaz-Manera J, Rojas-Garcia R, De Luna N, Iturriaga C, Mar-quez C, Uson M, Hankiewicz K, Gallardo E, Illa I. Redefining dysferlinopathyphenotypes based on clinical findings and muscle imaging studies. Neurology 2010;75:316-23.
56. Passos-Bueno MR, Bashir R, Moreira ES, Vainzof M, Marie SK, Vasquez L, Iughetti P,Bakker E, Keers S, Stephenson A, Strachan T, Mahneh I, Weissenbach J, BushbyK, Zatz M. Confirmation of the 2p locus for the mild autosomal recessive limb-girdle muscular dystrophy gene (LGMD2B) in three families allows refinementof the candidate region. Genomics 1995;27:192-5.
57. Piccolo F, Moore SA, Ford GC, Campbell KP. Intracellular accumulation and reducedsarcolemmal expression of dysferlin in limb - girdle muscular dystrophies. Annals of Neurology 2000;48:902-12.
58. Roche JA, Ru LW, O'Neill AM, Resneck WG, Lovering RM, Bloch RJ. Unmasking poten-tial intracellular roles for dysferlin through improved immunolabeling methods. Journal of Histochemistry and Cytochemistry 2011;59:964-75.
59. Royer L, Rios E. Deconstructing calsequestrin. Complex buffering in the calcium storeof skeletal muscle. Journal of Physiology 2009;587:3101-11.
60. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for massspectrometric characterization of proteins and proteomes. Nature Protocols 2006;1:2856-60.
61. Sun Y, Hays NM, Periasamy A, Davidson MW, Day RN. Monitoring protein interac-tions in living cells with fluorescence lifetime imaging microscopy. Methods inEnzymology 2011;504:371-91.
62. Therrien C, Di Fulvio S, Pickles S, Sinnreich M. Characterization of lipid bindingspecificities of dysferlin C2 domains reveals novel interactions with phospho-inositides. Biochemistry 2009;48:2377-84.
63. Vale RD. The molecular motor toolbox for intracellular transport. Cell 2003;112:467-80. (Pubitemid 36263080)
64. Waddell LB, Lemckert FA, Zheng XF, Tran J, Evesson FJ, Hawkes JM, Lek A, Street NE, Lin P, Clarke NF, Landstrom AP, Ackerman MJ, Weisleder N, Ma J, North KN, Cooper ST. Dysferlin, annexin A1, and mitsugumin 53 are upregulatedin muscular dystrophy and localize to longitudinal tubules of the T-systemwith stretch. Journal of Neuropathology and Experimental Neurology 2011;70:302-13.
65. Zacharias U, Purfurst B, Schowel V, Morano I, Spuler S, Haase H. Ahnak1 abnormallylocalizes in muscular dystrophies and contributes to muscle vesicle release. Journal of Muscle Research and Cell Motility 2011;32:271-80.
66. Zhu H, Lin P, De G, Choi KH, Takeshima H, Weisleder N, Ma J. Polymerase transcriptaserelease factor (PTRF) anchors MG53 protein to cell injury site for initiation ofmembrane repair. Journal of Biological Chemistry 2011;286:12820-4.