Microtubule binding distinguishes dystrophin from utrophin

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

Volumn 111, Issue 15, 2014, Pages 5723-5728

  Belanto, Joseph J ^a   Mader, Tara L ^a   Eckhoff, Michael D ^a   Strandjord, Dana M ^a   Banks, Glen B ^a   Gardner, Melissa K ^b   Lowe, Dawn A ^a   Ervasti, James M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; UTROPHIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; DEPOLYMERIZATION; DYSTROPHINOPATHY; ECCENTRIC MUSCLE CONTRACTION; EXERCISE; IN VITRO STUDY; IN VIVO STUDY; MECHANICAL STRESS; MICROTUBULE; MICROTUBULE ASSEMBLY; MOUSE; NONHUMAN; PHENOTYPE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUADRICEPS FEMORIS MUSCLE;

ANIMALS; DYSTROPHIN; FLUORESCENCE; MICE; MICE, TRANSGENIC; MICROTUBULES; MUSCLE CONTRACTION; MUSCLE, SKELETAL; TORQUE; UTROPHIN;

EID: 84898789464     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1323842111     Document Type: Article

References (61)

1. Mendell JR, et al. (2012) Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann Neurol 71(3):304-313
2. Hoffman EP, Brown RH, Jr., Kunkel LM (1987) Dystrophin: The protein product of the Duchenne muscular dystrophy locus. Cell 51(6):919-928
3. Koenig M, Monaco AP, Kunkel LM (1988) The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53(2):219-228
4. Koenig M, Kunkel LM(1990) Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J Biol Chem265(8):4560-4566
5. Way M, Pope B, Cross RA, Kendrick-Jones J, Weeds AG (1992) Expression of the N-terminal domain of dystrophin in E. coli and demonstration of binding to F-Actin. FEBS Lett 301(3):243-245
6. Bork P, Sudol M (1994) The WW domain: A signalling site in dystrophin? Trends Biochem Sci 19(12):531-533
7. Ponting CP, Blake DJ, Davies KE, Kendrick-Jones J, Winder SJ (1996) ZZ and TAZ: New putative zinc fingers in dystrophin and other proteins. Trends Biochem Sci 21(1): 11-13
8. Rybakova IN, Ervasti JM (1997) Dystrophin-glycoprotein complex is monomeric and stabilizes actin filaments in vitro through a lateral association. J Biol Chem 272(45): 28771-28778
9. Lai Y, et al. (2009) Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J Clin Invest 119(3):624-635
10. Rybakova IN, Amann KJ, Ervasti JM (1996) A new model for the interaction of dystrophin with F-Actin. J Cell Biol 135(3):661-672
11. Rybakova IN, Patel JR, Ervasti JM (2000) The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J Cell Biol 150(5): 1209-1214
12. Ervasti JM (2003) Costameres: The Achilles' heel of Herculean muscle. J Biol Chem 278(16):13591-13594
13. Pardo JV, Siliciano JD, Craig SW (1983) A vinculin-containing cortical lattice in skeletal muscle: Transverse lattice elements ("costameres") mark sites of attachment between myofibrils and sarcolemma. Proc Natl Acad Sci USA 80(4):1008-1012
14. Street SF (1983) Lateral transmission of tension in frog myofibers: A myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114(3):346-364
15. Danowski BA, Imanaka-Yoshida K, Sanger JM, Sanger JW (1992) Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes. J Cell Biol 118(6): 1411-1420
16. Ayalon G, Davis JQ, Scotland PB, Bennett V (2008) An ankyrin-based mechanism for functional organization of dystrophin and dystroglycan. Cell 135(7):1189-1200
17. Ayalon G, et al. (2011) Ankyrin-B interactions with spectrin and dynactin-4 are required for dystrophin-based protection of skeletal muscle from exercise injury. J Biol Chem 286(9):7370-7378
18. Randazzo D, et al. (2013) Obscurin is required for ankyrinB-dependent dystrophin localization and sarcolemma integrity. J Cell Biol 200(4):523-536
19. Prins KW, et al. (2009) Dystrophin is a microtubule-Associated protein. J Cell Biol 186(3):363-369
20. Ralston E, Lu Z, Ploug T (1999) The organization of the Golgi complex and microtubules in skeletal muscle is fiber type-dependent. J Neurosci 19(24):10694-10705
21. Sicinski P, et al. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244(4912):1578-1580
22. Bulfield G, Siller WG, Wight PAL, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81(4):1189-1192
23. Carlson CG, Makiejus RV (1990) A noninvasive procedure to detect muscle weakness in the mdx mouse. Muscle Nerve 13(6):480-484
24. Moens P, Baatsen PH, Maréchal G (1993) Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. J Muscle Res Cell Motil 14(4):446-451
25. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90(8):3710-3714
26. Partridge TA (2013) The mdx mouse model as a surrogate for Duchenne muscular dystrophy. FEBS J 280(17):4177-4186
27. Blake DJ, Weir A, Newey SE, Davies KE (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82(2):291-329
28. Matsumura K, Ervasti JM, Ohlendieck K, Kahl SD, Campbell KP (1992) Association of dystrophin-related protein with dystrophin-Associated proteins in mdx mouse muscle. Nature 360(6404):588-591
29. Rybakova IN, Patel JR, Davies KE, Yurchenco PD, Ervasti JM (2002) Utrophin binds laterally along actin filaments and can couple costameric actin with sarcolemma when overexpressed in dystrophin-deficient muscle. Mol Biol Cell 13(5):1512-1521
30. Hirst RC, McCullagh KJA, Davies KE (2005) Utrophin upregulation in Duchenne muscular dystrophy. Acta Myol 24(3):209-216
31. Fairclough RJ, Wood MJ, Davies KE (2013) Therapy for Duchenne muscular dystrophy: Renewed optimism from genetic approaches. Nat Rev Genet 14(6):373-378
32. Kleopa KA, Drousiotou A, Mavrikiou E, Ormiston A, Kyriakides T (2006) Naturally occurring utrophin correlates with disease severity in Duchenne muscular dystrophy. Hum Mol Genet 15(10):1623-1628
33. Tinsley J, et al. (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4(12):1441-1444
34. Li D, et al. (2010) Sarcolemmal nNOS anchoring reveals a qualitative difference between dystrophin and utrophin. J Cell Sci 123(Pt 12):2008-2013
35. Percival JM, et al. (2007) rAAV6-microdystrophin rescues aberrant Golgi complex organization in mdx skeletal muscles. Traffic 8(10):1424-1439
36. Chang WJ, et al. (1996) Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci USA 93(17):9142-9147
37. Percival JM, Anderson KNE, Huang P, Adams ME, Froehner SC (2010) Golgi and sarcolemmal neuronal NOS differentially regulate contraction-induced fatigue and vasoconstriction in exercising mouse skeletal muscle. J Clin Invest 120(3):816-826
38. Percival JM, Anderson KNE, Gregorevic P, Chamberlain JS, Froehner SC (2008) Functional deficits in nNOSmu-deficient skeletal muscle: myopathy in nNOS knockout mice. PLoS ONE 3(10):e3387
39. Thomas GD, Shaul PW, Yuhanna IS, Froehner SC, Adams ME (2003) Vasomodulation by skeletal muscle-derived nitric oxide requires alpha-syntrophin-mediated sarcolemmal localization of neuronal nitric oxide synthase. Circ Res 92(5):554-560
40. Thomas GD, et al. (1998) Impaired metabolic modulation of alpha-Adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc Natl Acad Sci USA 95(25): 15090-15095
41. Crawford GE, et al. (2000) Assembly of the dystrophin-Associated protein complex does not require the dystrophin COOH-terminal domain. J Cell Biol 150(6):1399-1410
42. Li S, et al. (2006) A highly functional mini-dystrophin/GFP fusion gene for cell and gene therapy studies of Duchenne muscular dystrophy. Hum Mol Genet 15(10): 1610-1622
43. Khairallah RJ, et al. (2012) Microtubules underlie dysfunction in Duchenne muscular dystrophy. Sci Signal 5(236):ra56
44. Liu W, Ralston E (2014) A new directionality tool for assessing microtubule pattern alterations. Cytoskeleton (Hoboken), 10.1002/cm.21166
45. Oddoux S, et al. (2013) Microtubules that form the stationary lattice of muscle fibers are dynamic and nucleated at Golgi elements. J Cell Biol 203(2):205-213
46. Hendricks AG, et al. (2012) Dynein tethers and stabilizes dynamic microtubule plus ends. Curr Biol 22(7):632-637
47. Kobayashi YM, et al. (2008) Sarcolemma-localized nNOS is required to maintain activity after mild exercise. Nature 456(7221):511-515
48. Baltgalvis KA, Call JA, Nikas JB, Lowe DA (2009) Effects of prednisolone on skeletal muscle contractility in mdx mice. Muscle Nerve 40(3):443-454
49. Ingalls CP, Warren GL, Lowe DA, Boorstein DB, Armstrong RB (1996) Differential effects of anesthetics on in vivo skeletal muscle contractile function in the mouse. J Appl Physiol (1985) 80(1):332-340
50. Saitoh O, Arai T, Obinata T (1988) Distribution of microtubules and other cytoskeletal filaments during myotube elongation as revealed by fluorescence microscopy. Cell Tissue Res 252(2):263-273
51. Chang W, et al. (2002) Alteration of the C-terminal amino acid of tubulin specifically inhibits myogenic differentiation. J Biol Chem 277(34):30690-30698
52. Perez OD, Chang YT, Rosania G, Sutherlin D, Schultz PG (2002) Inhibition and reversal of myogenic differentiation by purine-based microtubule assembly inhibitors. Chem Biol 9(4):475-483
53. Zhang T, et al. (2009) Microtubule plus-end binding protein EB1 is necessary for muscle cell differentiation, elongation and fusion. J Cell Sci 122(Pt 9):1401-1409
54. Ralston E, Ploug T, Kalhovde J, Lomo T (2001) Golgi complex, endoplasmic reticulum exit sites, and microtubules in skeletal muscle fibers are organized by patterned activity. J Neurosci 21(3):875-883
55. Akhmanova A, et al. (2001) Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104(6): 923-935
56. Mimori-Kiyosue Y, et al. (2005) CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J Cell Biol 168(1):141-153
57. Lansbergen G, et al. (2006) CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5. Dev Cell 11(1):21-32
58. Prosser BL, Ward CW, Lederer WJ (2011) X-ROS signaling: Rapid mechano-chemo transduction in heart. Science 333(6048):1440-1445
59. Davis JQ, Bennett V (1984) Brain ankyrin. A membrane-Associated protein with binding sites for spectrin, tubulin, and the cytoplasmic domain of the erythrocyte anion channel. J Biol Chem 259(21):13550-13559
60. Sharma N, et al. (2012) Use of quantitative membrane proteomics identifies a novel role of mitochondria in healing injured muscles. J Biol Chem 287(36):30455-30467
61. Percival JM, Siegel MP, Knowels G, Marcinek DJ (2013) Defects in mitochondrial localization and ATP synthesis in the mdx mouse model of Duchenne muscular dystrophy are not alleviated by PDE5 inhibition. Hum Mol Genet 22(1):153-167. Diseases