Dysferlin stabilizes stress-induced Ca2+ signaling in the transverse tubule membrane

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

Volumn 110, Issue 51, 2013, Pages 20831-20836

  Kerr, Jaclyn P ^a   Ziman, Andrew P ^a   Mueller, Amber L ^a   Muriel, Joaquin M ^a   Kleinhans Welte, Emily ^a   Gumerson, Jessica D ^a   Vogel, Steven S ^b   Ward, Christopher W ^c   Roche, Joseph A ^a   Bloch, Robert J ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF NURSING   (United States)

Author keywords

Dihydropyridine receptor; Excitation contraction coupling; Muscle injury; Triad junction

Indexed keywords

CALCIUM CHANNEL L TYPE; CALCIUM ION; DILTIAZEM; DYSFERLIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DAMAGE; CELL DEATH; CELL MEMBRANE; CELL STRESS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ECCENTRIC MUSCLE CONTRACTION; FLEXOR DIGITORUM BREVIS; IN VITRO STUDY; INFLAMMATION; LIMB GIRDLE MUSCULAR DYSTROPHY; MIYOSHI MYOPATHY; MOUSE; MUSCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; SKELETAL MUSCLE; TRANSVERSE TUBULE MEMBRANE;

EID: 84890831113     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1307960110     Document Type: Article

References (51)

1. Barohn RJ, Miller RG, Griggs RC (1991) Autosomal recessive distal dystrophy. Neurology 41(9):1365-1370.
2. Bansal D, Campbell KP (2004) Dysferlin and the plasma membrane repair in muscular dystrophy. Trends Cell Biol 14(4):206-213.
3. Bansal D, et al. (2003) Defective membrane repair in dysferlin-Deficient muscular dystrophy. Nature 423(6936):168-172.
4. Lennon NJ, et al. (2003) Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-Healing. J Biol Chem 278(50):50466-50473.
5. Azakir BA, Di Fulvio S, Therrien C, Sinnreich M (2010) Dysferlin interacts with tubulin and microtubules in mouse skeletal muscle. PLoS ONE 5(4):e10122.
6. Di Fulvio S, Azakir BA, Therrien C, Sinnreich M (2011) Dysferlin interacts with histone deacetylase 6 and increases alpha-Tubulin acetylation. PLoS ONE 6(12):e28563.
7. de Morrée A, et al. (2013) Dysferlin regulates cell adhesion in human monocytes. J Biol Chem 288(20):14147-14157.
8. Sharma A, et al. (2010) A new role for the muscle repair protein dysferlin in endothelial cell adhesion and angiogenesis. Arterioscler Thromb Vasc Biol 30(11): 2196-2204.
9. Covian-Nares JF, Koushik SV, Puhl HL, III, Vogel SS (2010) Membrane wounding triggers ATP release and dysferlin-Mediated intercellular calcium signaling. J Cell Sci 123(Pt 11):1884-1893.
10. Roche JA, et al. (2011) Unmasking potential intracellular roles for dysferlin through improved immunolabeling methods. J Histochem Cytochem 59(11):964-975.
11. Ampong BN, Imamura M, Matsumiya T, Yoshida M, Takeda S (2005) Intracellular localization of dysferlin and its association with the dihydropyridine receptor. Acta Myol 24(2):134-144.
12. Matsuda C, et al. (2001) The sarcolemmal proteins dysferlin and caveolin-3 interact in skeletal muscle. Hum Mol Genet 10(17):1761-1766.
13. de Morrée A, et al. (2010) Proteomic analysis of the dysferlin protein complex unveils its importance for sarcolemmal maintenance and integrity. PLoS ONE 5(11):e13854.
14. Waddell LB, et al. (2011) Dysferlin, annexin A1, and mitsugumin 53 are upregulated in muscular dystrophy and localize to longitudinal tubules of the T-System with stretch. J Neuropathol Exp Neurol 70(4):302-313.
15. Klinge L, et al. (2010) Dysferlin associates with the developing T-Tubule system in rodent and human skeletal muscle. Muscle Nerve 41(2):166-173.
16. Terrill JR, et al. (2013) Oxidative stress and pathology in muscular dystrophies: Focus on protein thiol oxidation and dysferlinopathies. FEBS J 280(17):4149-4164.
17. Kobayashi K, Izawa T, Kuwamura M, Yamate J (2011) Comparative gene expression analysis in the skeletal muscles of dysferlin-Deficient SJL/J and A/J mice. J Toxicol Pathol 24(1):49-62.
18. Roche JA, Ru LW, Bloch RJ (2012) Distinct effects of contraction-Induced injury in vivo on four different murine models of dysferlinopathy. J Biomed Biotechnol 2012: 134031.
19. Roche JA, et al. (2010) Extensive mononuclear infiltration and myogenesis characterize recovery of dysferlin-Null skeletal muscle from contraction-Induced injuries. Am J Physiol Cell Physiol 298(2):C298-C312.
20. Roche JA, Lovering RM, Bloch RJ (2008) Impaired recovery of dysferlin-Null skeletal muscle after contraction-Induced injury in vivo. Neuroreport 19(16):1579-1584.
21. Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-Sensitive green fluorescent proteins. Nature 394(6689):192-195.
22. Menke A, Jockusch H (1991) Decreased osmotic stability of dystrophin-Less muscle cells from the mdx mouse. Nature 349(6304):69-71.
23. Martins AS, Shkryl VM, Nowycky MC, Shirokova N (2008) Reactive oxygen species contribute to Ca2+ signals produced by osmotic stress in mouse skeletal muscle fibres. J Physiol 586(1):197-210.
24. Shkryl VM, et al. (2009) Reciprocal amplification of ROS and Ca(2+) signals in stressed mdx dystrophic skeletal muscle fibers. Pflugers Arch 458(5):915-928.
25. Pickering JD, White E, Duke AM, Steele DS (2009) DHPR activation underlies SR Ca2+ release induced by osmotic stress in isolated rat skeletal muscle fibers. J Gen Physiol 133(5):511-524.
26. Friedrich O, BothM, Gillis JM, Chamberlain JS, Fink RH (2004) Mini-Dystrophin restores L-Type calcium currents in skeletal muscle of transgenic mdx mice. J Physiol 555(Pt 1): 251-265.
27. Hornsey MA, Laval SH, Barresi R, Lochmüller H, Bushby K (2013) Muscular dystrophy in dysferlin-Deficient mouse models. Neuromuscul Disord 23(5):377-387.
28. Gallardo E, et al. (2001) Inflammation in dysferlin myopathy: Immunohistochemical characterization of 13 patients. Neurology 57(11):2136-2138.
29. Rawat R, et al. (2010) Inflammasome up-Regulation and activation in dysferlindeficient skeletal muscle. Am J Pathol 176(6):2891-2900.
30. Anderson LV, et al. (1999) Dysferlin is a plasma membrane protein and is expressed early in human development. Hum Mol Genet 8(5):855-861.
31. Matsuda C, et al. (1999) Dysferlin is a surface membrane-Associated protein that is absent in Miyoshi myopathy. Neurology 53(5):1119-1122.
32. Han R, Rader EP, Levy JR, Bansal D, Campbell KP (2011) Dystrophin deficiency exacerbates skeletal muscle pathology in dysferlin-Null mice. Skelet Muscle 1(1):35.
33. Han R, et al. (2010) Genetic ablation of complement C3 attenuates muscle pathology in dysferlin-Deficient mice. J Clin Invest 120(12):4366-4374.
34. Azakir BA, et al. (2012) Modular dispensability of dysferlin C2 domains reveals rational design for mini-Dysferlin molecules. J Biol Chem 287(33):27629-27636.
35. Han WQ, et al. (2012) Lysosome fusion to the cell membrane is mediated by the dysferlin C2A domain in coronary arterial endothelial cells. J Cell Sci 125(Pt 5): 1225-1234.
36. Cenacchi G, Fanin M, De Giorgi LB, Angelini C (2005) Ultrastructural changes in dysferlinopathy support defective membrane repair mechanism. J Clin Pathol 58(2): 190-195.
37. Krahn M, et al. (2010) A naturally occurring human minidysferlin protein repairs sarcolemmal lesions in a mouse model of dysferlinopathy. Sci Transl Med 2(50): 50ra69.
38. Lostal W, et al. (2010) Efficient recovery of dysferlin deficiency by dual adeno-Associated vector-Mediated gene transfer. Hum Mol Genet 19(10):1897-1907.
39. Lostal W, 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(5):e38036.
40. Cai C, et al. (2009) Membrane repair defects in muscular dystrophy are linked to altered interaction between MG53, caveolin-3, and dysferlin. J Biol Chem 284(23): 15894-15902.
41. Cai C, et al. (2009) MG53 nucleates assembly of cell membrane repair machinery. Nat Cell Biol 11(1):56-64.
42. Dirksen RT (2009) Checking your SOCCs and feet: The molecular mechanisms of Ca2+ entry in skeletal muscle. J Physiol 587(Pt 13):3139-3147.
43. Lovering RM, Roche JA, Goodall MH, Clark BB, McMillan A (2011) An in vivo rodent model of contraction-Induced injury and non-Invasive monitoring of recovery. J Vis Exp (51), pii: 2782.
44. Ingalls CP, Warren GL, Zhang JZ, Hamilton SL, Armstrong RB (2004) Dihydropyridine and ryanodine receptor binding after eccentric contractions in mouse skeletal muscle. J Appl Physiol (1985) 96(5):1619-1625.
45. Brown LD, Rodney GG, Hernández-Ochoa E, Ward CW, Schneider MF (2007) Ca2+ sparks and T tubule reorganization in dedifferentiating adult mouse skeletal muscle fibers. Am J Physiol Cell Physiol 292(3):C1156-C1166.
46. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224(Pt 3):213-232.
47. DiFranco M, Quinonez M, Capote J, Vergara J (2009) DNA transfection of mammalian skeletal muscles using in vivo electroporation. J Vis Exp (32), pii: 1520.
48. Yeung EW, Balnave CD, Ballard HJ, Bourreau JP, Allen DG (2002) Development of T-Tubular vacuoles in eccentrically damaged mouse muscle fibres. J Physiol 540(Pt 2): 581-592.
49. Lovering RM, Michaelson L, Ward CW (2009) Malformed mdx myofibers have normal cytoskeletal architecture yet altered EC coupling and stress-Induced Ca2+ signaling. Am J Physiol Cell Physiol 297(3):C571-C580.
50. Goodall MH, Ward CW, Pratt SJ, Bloch RJ, Lovering RM (2012) Structural and functional evaluation of branched myofibers lacking intermediate filaments. Am J Physiol Cell Physiol 303(2):C224-C232.
51. Matsumura CY, Pertille A, Albuquerque TC, Santo Neto H, Marques MJ (2009) Diltiazem and verapamil protect dystrophin-Deficient muscle fibers of MDX mice from degeneration: A potential role in calcium buffering and sarcolemmal stability. Muscle Nerve 39(2):167-176.