Dysferlin mediates membrane tubulation and links T-tubule biogenesis to muscular dystrophy

Journal of Cell Science

Volumn 130, Issue 5, 2017, Pages 841-852

  Hofhuis, Julia ^a   Bersch, Kristina ^a   Büssenschütt, Ronja ^a   Drzymalski, Marzena ^a,c   Liebetanz, David ^a   Nikolaev, Viacheslav O ^a,d   Wagner, Stefan ^b   Maier, Lars S ^b   Gärtner, Jutta ^a   Klinge, Lars ^a,e   Thoms, Sven ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^e Practice for Child and Adolescent Medicine and Paediatric Neurology   (Germany)

Author keywords

5 bisphosphate; C2 domain protein; Dysferlin; Dysferlinopathy; Limb girdle muscular dystrophy type 2B; Miyoshi myopathy; Muscular dystrophy; Phosphatidylinositol 4; T tubule system

Indexed keywords

DYSFERLIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; BIN1 PROTEIN, MOUSE; CALCIUM; CAVEOLIN 3; DYNAMIN; DYSF PROTEIN, HUMAN; DYSF PROTEIN, MOUSE; MEMBRANE PROTEIN; MUSCLE PROTEIN; NERVE PROTEIN; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BIOGENESIS; C2 DOMAIN; CELL MEMBRANE; CONTROLLED STUDY; COS-7 CELL LINE; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR MEMBRANE; MEMBRANE BINDING; MOUSE; MUSCLE ATROPHY; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSVERSE TUBULAR SYSTEM; ANIMAL; CHLOROCEBUS AETHIOPS; COS CELL LINE; DEFICIENCY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHENOTYPE; SARCOLEMMA; ULTRASTRUCTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CALCIUM; CAVEOLIN 3; CERCOPITHECUS AETHIOPS; COS CELLS; DYNAMINS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE, KNOCKOUT; MUSCLE PROTEINS; MUSCULAR DYSTROPHIES; NERVE TISSUE PROTEINS; PHENOTYPE; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHYSICAL CONDITIONING, ANIMAL; PROTEIN BINDING; SARCOLEMMA; TUMOR SUPPRESSOR PROTEINS;

EID: 85014348400     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.198861     Document Type: Article

References (55)

1. Al-Qusairi, L. and Laporte, J. (2011). T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases. Skelet Muscle 1, 26.
2. Ampong, B. N., Imamura, M., Matsumiya, T., Yoshida, M. and Takeda, S. (2005). Intracellular localization of dysferlin and its association with the dihydropyridine receptor. Acta Myol. 24, 134-144.
3. Anderson, L. V. B., Davison, K., Moss, J. A., Young, C., Cullen, M. J., Walsh, J., Johnson, M. A., Bashir, R., Britton, S., Keers, S. et al. (1999). Dysferlin is a plasma membrane protein and is expressed early in human development. Hum. Mol. Genet. 8, 855-861.
4. Azakir, B. A., Di Fulvio, S., Therrien, C. and Sinnreich, M. (2010). Dysferlin interacts with tubulin and microtubules in mouse skeletal muscle. PLoS ONE 5, e 10122.
5. Azakir, B. A., Di Fulvio, S., Salomon, S., Brockhoff, M., Therrien, C. and Sinnreich, M. (2012). Modular dispensability of Dysferlin C2 domains reveals rational design for mini-dysferlin molecules. J. Biol. Chem. 287, 27629-27636.
6. Balla, T. (2013). Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol. Rev. 93, 1019-1137.
7. Bansal, D., Miyake, K., Vogel, S. S., Groh, S., Chen, C.-C., Williamson, R., McNeil, P. L. and Campbell, K. P. (2003). Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423, 168-172.
8. Biondi, O., Villemeur, M., Marchand, A., Chretien, F., Bourg, N., Gherardi, R. K., Richard, I. and Authier, F.-J. (2013). Dual effects of exercise in dysferlinopathy. Am. J. Pathol. 182, 2298-2309.
9. Bohm, J., Biancalana, V., Malfatti, E., Dondaine, N., Koch, C., Vasli, N., Kress, W., Strittmatter, M., Taratuto, A. L., Gonorazky, H. et al. (2014). Adult-onset autosomal dominant centronuclear myopathy due to BIN1 mutations. Brain 137, 3160-3170.
10. Boittin, F.-X., Petermann, O., Hirn, C., Mittaud, P., Dorchies, O. M., Roulet, E. and Ruegg, U. T. (2006). Ca2+-independent phospholipase A2 enhances storeoperated Ca2+ entry in dystrophic skeletal muscle fibers. J. Cell Sci. 119, 3733-3742.
11. Capote, J., Bolanos, P., Schuhmeier, R. P., Melzer, W. and Caputo, C. (2005). Calcium transients in developing mouse skeletal muscle fibres. J. Physiol. 564, 451-464.
12. Chiu, Y.-H., Hornsey, M. A., Klinge, L., Jorgensen, L. H., Laval, S. H., Charlton, R., Barresi, R., Straub, V., Lochmuller, H. and Bushby, K. (2009). Attenuated muscle regeneration is a key factor in dysferlin-deficient muscular dystrophy. Hum. Mol. Genet. 18, 1976-1989.
13. Cooper, S. T. and Head, S. I. (2014). Membrane injury and repair in the muscular dystrophies. Neuroscientist 21, 653-668.
14. Davis, D. B., Doherty, K. R., Delmonte, A. J. and McNally, E. M. (2002). Calciumsensitive phospholipid binding properties of normal and mutant ferlin C2 domains. J. Biol. Chem. 277, 22883-22888.
15. Demonbreun, A. R., Rossi, A. E., Alvarez, M. G., Swanson, K. E., Kieran Deveaux, H., Earley, J. U., Hadhazy, M., Vohra, R., Walter, G. A., Pytel, P. et al. (2013). Dysferlin and myoferlin regulate transverse tubule formation and glycerol sensitivity. Am. J. Pathol. 184, 248-259.
16. Donaldson, M. R., Jensen, J. L., Tristani-Firouzi, M., Tawil, R., Bendahhou, S., Suarez, W. A., Cobo, A. M., Poza, J. J., Behr, E., Wagstaff, J. et al. (2003). PIP2 binding residues of Kir2.1 are common targets of mutations causing Andersen syndrome. Neurology 60, 1811-1816.
17. Engel, A. G. and Franzini-Armstrong, C. (2004). Myology. New York: McGraw-Hill.
18. Escobar, H., Schöwel, V., Spuler, S., Marg, A. and Izsvák, Z. (2016). Full-length dysferlin transfer by the hyperactive sleeping beauty transposase restores dysferlin-deficient muscle. Mol Ther Nucleic Acids 5, e 277.
19. Franzini-Armstrong, C. (1991). Simultaneous maturation of transverse tubules and sarcoplasmic reticulum during muscle differentiation in the mouse. Dev. Biol. 146, 353-363.
20. Fuson, K., Rice, A., Mahling, R., Snow, A., Nayak, K., Shanbhogue, P., Meyer, A. G., Redpath, G. M. I., Hinderliter, A., Cooper, S. T. et al. (2014). Alternate splicing of dysferlin C2A confers Ca(2)(+)-dependent and Ca(2)(+)-independent binding for membrane repair. Structure 22, 104-115.
21. Grose, W. E., Clark, K. R., Griffin, D., Malik, V., Shontz, K. M., Montgomery, C. L., Lewis, S., Brown, R. H., Jr., Janssen, P. M. L., Mendell, J. R. et al. (2012). Homologous recombination mediates functional recovery of dysferlin deficiency following AAV5 gene transfer. PLoS ONE 7, e 39233.
22. Hattori, H., Nagata, E., Oya, Y., Takahashi, T., Aoki, M., Ito, D. and Suzuki, N. (2007). A novel compound heterozygous dysferlin mutation in Miyoshi myopathy siblings responding to dantrolene. Eur. J. Neurol. 14, 1288-1291.
23. Hernandez-Deviez, D. J., Howes, M. T., Laval, S. H., Bushby, K., Hancock, J. F. and Parton, R. G. (2008). Caveolin regulates endocytosis of the muscle repair protein, dysferlin. J. Biol. Chem. 283, 6476-6488.
24. Hilgemann, D.W., Feng, S. and Nasuhoglu, C. (2001). The complex and intriguing lives of PIP2 with ion channels and transporters. Sci. STKE 2001, re 19.
25. Kerr, J. P., Ziman, A. P., Mueller, A. L., Muriel, J. M., Kleinhans-Welte, E., Gumerson, J. D., Vogel, S. S., Ward, C. W., Roche, J. A. and Bloch, R. J. (2013). Dysferlin stabilizes stress-induced Ca2+ signaling in the transverse tubule membrane. Proc. Natl. Acad. Sci. USA 110, 20831-20836.
26. Kerr, J. P., Ward, C. W. and Bloch, R. J. (2014). Dysferlin at transverse tubules regulates Ca homeostasis in skeletal muscle. Front. Physiol. 5, 89.
27. Klinge, L., Laval, S., Keers, S., Haldane, F., Straub, V., Barresi, R. and Bushby, K. (2007). From T-tubule to sarcolemma: damage-induced dysferlin translocation in early myogenesis. FASEB J. 21, 1768-1776.
28. Klinge, L., Dean, A. F., Kress, W., Dixon, P., Charlton, R., Müller, J. S., Anderson, L. V., Straub, V., Barresi, R., Lochmuller, H. et al. (2008). Late onset in dysferlinopathy widens the clinical spectrum. Neuromuscul. Disord. 18, 288-290.
29. Klinge, L., Aboumousa, A., Eagle, M., Hudson, J., Sarkozy, A., Vita, G., Charlton, R., Roberts, M., Straub, V., Barresi, R. et al. (2010). New aspects on patients affected by dysferlin deficient muscular dystrophy. J. Neurol. Neurosurg. Psychiatry 81, 946-953.
30. Klinge, L., Harris, J., Sewry, C., Charlton, R., Anderson, L., Laval, S., Chiu, Y.-H., Hornsey, M., Straub, V., Barresi, R. et al. (2010). Dysferlin associates with the developing T-tubule system in rodent and human skeletal muscle. Muscle Nerve 41, 166-173.
31. Klopfenstein, D. R. and Vale, R. D. (2004). The lipid binding pleckstrin homology domain in UNC-104 kinesin is necessary for synaptic vesicle transport in Caenorhabditis elegans. Mol. Biol. Cell 15, 3729-3739.
32. Krauss, M., Kinuta, M., Wenk, M. R., De Camilli, P., Takei, K. and Haucke, V. (2003). ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma. J. Cell Biol. 162, 113-124.
33. Krahn, M., Wein, N., Bartoli, M., Lostal, W., Courrier, S., Bourg-Alibert, N., Nguyen, K., Vial, C., Streichenberger N., Labelle V. et al. (2010) A naturally occurring human minidysferlin protein repairs sarcolemmal lesions in a mouse model of dysferlinopathy. Sci. Transl. Med. 2, 50ra 69.
34. Krolenko, S. A. and Lucy, J. A. (2002). Vacuolation in T-tubules as a model for tubular-vesicular transformations in biomembrane systems. Cell Biol. Int. 26, 893-904.
35. Lee, E., Marcucci, M., Daniell, L., Pypaert, M., Weisz, O. A., Ochoa, G.-C., Farsad, K., Wenk, M. R. and De Camilli, P. (2002). Amphiphysin 2 (Bin1) and Ttubule biogenesis in muscle. Science 297, 1193-1196.
36. Lemmon, M. A. (2008). Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111.
37. Lostal, W., Bartoli, M., Roudaut, C., Bourg, N., Krahn, M., Pryadkina, M., Borel, P., Suel, L., Roche, J. A., Stockholm, D. et al. (2012). Lack of correlation between outcomes of membrane repair assay and correction of dystrophic changes in experimental therapeutic strategy in dysferlinopathy. PLoS ONE 7, e 38036.
38. Marty, N. J., Holman, C. L., Abdullah, N. and Johnson, C. P. (2013). The C2 domains of otoferlin, dysferlin, and myoferlin alter the packing of lipid bilayers. Biochemistry 52, 5585-5592.
39. McMahon, H. T., Kozlov, M. M. and Martens, S. (2010). Membrane curvature in synaptic vesicle fusion and beyond. Cell 140, 601-605.
40. Middel, V., Zhou, L., Takamiya, M., Beil, T., Shahid, M., Roostalu, U., Grabher, C., Rastegar, S., Reischl, M., Nienhaus, G. U. et al. (2016). Dysferlin-mediated phosphatidylserine sorting engages macrophages in sarcolemma repair. Nat. Commun. 7, 12875.
41. Milting, H., Heilmeyer, L. M. G., Jr and Thieleczek, R. (1994). Phosphoinositides in membranes that build up the triads of rabbit skeletal muscle. FEBS Lett. 345, 211-218.
42. Min, S.-W., Chang, W.-P. and Sudhof, T. C. (2007). E-Syts, a family of membranous Ca2+-sensor proteins with multiple C2 domains. Proc. Natl. Acad. Sci. USA 104, 3823-3828.
43. Morrison, H. W. and Filosa, J. A. (2013). A quantitative spatiotemporal analysis of microglia morphology during ischemic stroke and reperfusion. J. Neuroinflammation 10, 4.
44. Nicot, A.-S., Toussaint, A., Tosch, V., Kretz, C., Wallgren-Pettersson, C., Iwarsson, E., Kingston, H., Garnier, J.-M., Biancalana, V., Oldfors, A. et al. (2007). Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat. Genet. 39, 1134-1139.
45. Oulhen, N., Onorato, T. M., Ramos, I. and Wessel, G. M. (2013). Dysferlin is essential for endocytosis in the sea star oocyte. Dev. Biol. 388, 94-102.
46. Posey, A. D., Jr, Swanson, K. E., Alvarez, M. G., Krishnan, S., Earley, J. U., Band, H., Pytel, P., McNally, E. M. and Demonbreun, A. R. (2014). EHD1 mediates vesicle trafficking required for normal muscle growth and transverse tubule development. Dev. Biol. 2, 179-190.
47. Pryadkina, M., Lostal, W., Bourg, N., Charton, K., Roudaut, C., Hirsch, M. L. and Richard, I. (2015). A comparison of AAV strategies distinguishes overlapping vectors for efficient systemic delivery of the 6.2 kb Dysferlin coding sequence. Mol. Ther. Methods Clin. Dev. 2, 15009.
48. Redpath, G. M. I., Sophocleous, R. A., Turnbull, L., Whitchurch, C. B. and Cooper, S. T. (2016). Ferlins show tissue-specific expression and segregate as plasma membrane/late endosomal or trans-golgi/recycling ferlins. Traffic 17, 245-266.
49. Rodríguez-Menchaca, A. A., Adney, S. K., Zhou, L. and Logothetis, D. E. (2012). Dual regulation of voltage-sensitive ion channels by PIP(2). Front. Pharmacol. 3, 170.
50. Roostalu, U. and Strähle, U. (2012). In vivo imaging of molecular interactions at damaged sarcolemma. Dev. Cell 22, 515-529.
51. Shin, O.-H., Han, W., Wang, Y. and Sudhof, T. C. (2005). Evolutionarily conserved multiple C2 domain proteins with two transmembrane regions (MCTPs) and unusual Ca2+ binding properties. J. Biol. Chem. 280, 1641-1651.
52. Sondergaard, P. C., Griffin, D. A., Pozsgai, E. R., Johnson, R. W., Grose, W. E., Heller, K. N., Shontz, K. M., Montgomery, C. L., Liu, J., Clark, K. R. et al. (2015). AAV.Dysferlin overlap vectors restore function in dysferlinopathy animal models. Ann. Clin. Transl. Neurol. 2, 256-270.
53. Therrien, C., Di Fulvio, S., Pickles, S. and Sinnreich, M. (2009). Characterization of lipid binding specificities of dysferlin C2 domains reveals novel interactions with phosphoinositides. Biochemistry 48, 2377-2384.
54. Tjondrokoesoemo, A., Park, K. H., Ferrante, C., Komazaki, S., Lesniak, S., Brotto, M., Ko, J.-K., Zhou, J., Weisleder, N. and Ma, J. (2011). Disrupted membrane structure and intracellular Ca(2)(+) signaling in adult skeletal muscle with acute knockdown of Bin1. PLoS ONE 6, e 25740.
55. Wu, T. and Baumgart, T. (2014). BIN1 membrane curvature sensing and generation showautoinhibition regulated by downstream ligands and PI(4, 5)P2. Biochemistry 53, 7297-7309.