Independent variability of microtubule perturbations associated with dystrophinopathy

Human Molecular Genetics

Volumn 25, Issue 22, 2016, Pages 4951-4961

  Belanto, Joseph J ^a   Olthoff, John T ^a   Mader, Tara L ^a   Chamberlain, Christopher M ^a   Nelson, D'anna M ^a   McCourt, Preston M ^a   Talsness, Dana M ^a   Gundersen, Gregg G ^b   Lowe, Dawn A ^a   Ervasti, James M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BETA SARCOGLYCAN; DYSTROPHIN; SPECTRIN; SPECTRIN LIKE REPEAT; UNCLASSIFIED DRUG; UTROPHIN; CYTOSKELETON PROTEIN; MEMBRANE PROTEIN; PROTEIN BINDING; SARCOGLYCAN; TUBULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DETYROSINATION; DYSTROPHINOPATHY; MALE; MICROTUBULE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN STRUCTURE; SARCOLEMMA; SKELETAL MUSCLE; TRANSGENE; ANIMAL; ANIMAL MUSCULAR DYSTROPHY; DUCHENNE MUSCULAR DYSTROPHY; GENETICS; HUMAN; METABOLISM; TRANSGENIC MOUSE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; CYTOSKELETAL PROTEINS; DYSTROPHIN; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED MDX; MICE, TRANSGENIC; MICROTUBULES; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; PROTEIN BINDING; PROTEIN DOMAINS; SARCOGLYCANS; SARCOLEMMA; TUBULIN; UTROPHIN;

EID: 85015804100     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw318     Document Type: Article

References (48)

1. Hoffman, E.P., Brown, R.H. and Kunkel, L.M. (1992) Dystrophin: the protein product of the Duchene muscular dystrophy locus. Biotechnology, 24, 457-466.
2. Worton, R.G. and Thompson, M.W. (1988) Genetics of Duchenne muscular dystrophy. Annu. Rev. Genet., 22, 601-629.
3. Mendell, J.R., Shilling, C., Leslie, N.D., Flanigan, K.M., Al-Dahhak, R., Gastier-Foster, J., Kneile, K., Dunn, D.M., Duval, B., Aoyagi, A., et al. (2012) Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann. Neurol., 71, 304-313.
4. Rall, S. and Grimm, T. (2012) Survival in Duchenne muscular dystrophy. Acta Myol., 31, 117-120.
5. Angelini, C. (2007) The role of corticosteroids in muscular dystrophy: a critical appraisal. Muscle Nerve, 36, 424-435.
6. Ricotti, V., Ridout, D.A., Scott, E., Quinlivan, R., Robb, S.A., Manzur, A.Y. and Muntoni, F. (2013) Long-term benefits and adverse effects of intermittent versus daily glucocorticoids in boys with Duchenne muscular dystrophy. J. Neurol. Neurosurg. Psychiatry, 84, 698-705.
7. Ervasti, J.M. (2003) Costameres: The Achilles' heel of Herculean muscle. J. Biol. Chem., 278, 13591-13594.
8. Prins, K.W., Humston, J.L., Mehta, A., Tate, V., Ralston, E. and Ervasti, J.M. (2009) Dystrophin is a microtubule-associated protein. J. Cell Biol., 186, 363-369.
9. Belanto, J.J., Mader, T.L., Eckhoff, M.D., Strandjord, D.M., Banks, G.B., Gardner, M.K., Lowe, D.A. and Ervasti, J.M. (2014) Microtubule binding distinguishes dystrophin from utrophin. Proc. Natl. Acad. Sci. U. S. A., 111, 5723-5728.
10. Percival, J.M., Gregorevic, P., Odom, G.L., Banks, G.B., Chamberlain, J.S. and Froehner, S.C. (2007) rAAV6-Microdystrophin rescues aberrant Golgi complex organization in mdx skeletal muscles. Traffic, 8, 1424-1439.
11. Ayalon, G., Davis, J.Q., Scotland, P.B. and Bennett, V. (2008) An Ankyrin-based mechanism for functional organization of dystrophin and dystroglycan. Cell, 135, 1189-1200.
12. Ayalon, G., Hostettler, J.D., Hoffman, J., Kizhatil, K., Davis, J.Q. and Bennett, V. (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, 7370-7378.
13. Randazzo, D., Giacomello, E., Lorenzini, S., Rossi, D., Pierantozzi, E., Blaauw, B., Reggiani, C., Lange, S., Peter, A.K., Chen, J., et al. (2013) Obscurin is required for ankyrinB-dependent dystrophin localization and sarcolemma integrity. J. Cell Biol., 200, 523-536.
14. Saitoh, O., Arai, T. and Obinata, T. (1988) Distribution of microtubules and other cytoskeletal filaments during myotube elongation as revealed by fluorescence microscopy. Cell Tissue Res., 252, 263-273.
15. Chang, W., Webster, D.R., Salam, A.A., Gruber, D., Prasad, A., Eiserich, J.P. and Bulinski, J.C. (2002) Alteration of the Cterminal amino acid of tubulin specifically inhibits myogenic differentiation. J. Biol. Chem., 277, 30690-30698.
16. Perez, O.D., Chang, Y.T., Rosania, G., Sutherlin, D. and Schultz, P.G. (2002) Inhibition and reversal of myogenic differentiation by purine-based microtubule assembly inhibitors. Chem. Biol., 9, 475-483.
17. Ralston, E., Lu, Z. and Ploug, T. (1999) The organization of the Golgi complex and microtubules in skeletal muscle is fiber type-dependent. J. Neurosci., 19, 10694-10705.
18. Ralston, E., Ploug, T., Kalhovde, J. and Lomo, T. (2001) Golgi complex, endoplasmic reticulum exit sites, and microtubules in skeletal muscle fibers are organized by patterned activity. J. Neurosci., 21, 875-883.
19. Prosser, B.L., Ward, C.W. and Lederer, W.J. (2011) X-ROS signaling: rapid mechano-chemo transduction in heart. Science, 333, 1440-1445.
20. Khairallah, R.J., Shi, G., Sbrana, F., Prosser, B.L., Borroto, C., Mazaitis, M.J., Hoffman, E.P., Mahurkar, A., Sachs, F., Sun, Y., et al. (2012) Microtubules underlie dysfunction in Duchenne muscular dystrophy. Sci. Signal, 5, ra56.
21. Kerr, J.P., Robison, P., Shi, G., Bogush, A.I., Kempema, A.M., Hexum, J.K., Becerra, N., Harki, D.A., Martin, S.S., Raiteri, R., et al. (2015) Detyrosinated microtubules modulate mechanotransduction in heart and skeletal muscle. Nat. Commun., 6, 8526.
22. Matsumura, K., Ervasti, J.M., Ohlendieck, K., Kahl, S.D. and Campbell, K.P. (1992) Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature, 360, 588-591.
23. Araishi, K., Sasaoka, T., Imamura, M., Noguchi, S., Hama, H., Wakabayashi, E., Yoshida, M., Hori, T. and Ozawa, E. (1999) Loss of the sarcoglycan complex and sarcospan leads to muscular dystrophy in b-sarcoglycan-deficient mice. Hum. Mol. Genet., 8, 1589-1598.
24. Durbeej, M., Cohn, R.D., Hrstka, R.F., Moore, S.A., Allamand, V., Davidson, B.L., Williamson, R.A. and Campbell, K.P. (2000) Disruption of the b-Sarcoglycan gene reveals pathogenetic complexity of limb-girdle muscular dystrophy type 2E. Mol. Cell, 5, 141-151.
25. Kobayashi, Y.M., Rader, E.P., Crawford, R.W., Iyengar, N.K., Thedens, D.R., Faulkner, J. A., Parikh, S.V., Weiss, R.M., Chamberlain, J.S., Moore, S. a., et al. (2008) Sarcolemmalocalized nNOS is required to maintain activity after mild exercise. Nature, 456, 511-515.
26. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A. M. and Sweeney, H.L. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl Acad. Sci. U. S. A., 90, 3710-3714.
27. Robison, P., Caporizzo, M.A., Ahmadzadeh, H., Bogush, A.I., Chen, C.Y., Margulies, K.B., Shenoy, V.B. and Prosser, B.L. (2016) Detyrosinated microtubules buckle and bear load in contracting cardiomyocytes. Science, 352, aaf0659.
28. Tinsley, J., Deconinck, N., Fisher, R., Kahn, D., Phelps, S., Gillis, J.M. and Davies, K. (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat. Med., 4, 1441-1444.
29. Crawford, G.E., Faulkner, J.A., Crosbie, R.H., Campbell, K.P., Froehner, S.C. and Chamberlain, J.S. (2000) Assembly of the dystrophin-associated protein complex does not require the dystrophin COOH-terminal domain. J. Cell Biol., 150, 1399-1409.
30. Ostlund, R.E., Leung, J.T. and Hajek, S.V. (1979) Biochemical determination of tubulin-microtubule equilibrium in cultured cells. Anal. Biochem., 96, 155-164.
31. Fassett, J.T., Xu, X., Kwak, D., Wang, H., Liu, X., Hu, X., Bache, R.J. and Chen, Y. (2013) Microtubule actin cross-linking factor 1 regulates cardiomyocyte microtubule distribution and adaptation to hemodynamic overload. PLoS One, 8, 1-12.
32. Li, D., Bareja, A., Judge, L., Yue, Y., Lai, Y., Fairclough, R., Davies, K.E., Chamberlain, J.S. and Duan, D. (2010) Sarcolemmal nNOS anchoring reveals a qualitative difference between dystrophin and utrophin. J. Cell Sci., 123, 2008-2013.
33. Lai, Y., Zhao, J., Yue, Y. and Duan, D. (2013) a2 and a3 helices of dystrophin R16 and R17 frame a microdomain in the a1 helix of dystrophin R17 for neuronal NOS binding. Proc. Natl Acad. Sci. U. S. A., 110, 525-530.
34. Way, M., Pope, B., Cross, R.A., Kendrick-Jones, J. and Weeds, A.G. (1992) Expression of the N-terminal domain of dystrophin in E. coli and demonstration of binding to F-actin. FEBS Lett., 301, 243-245.
35. Rybakova, I.N., Amann, K.J. and Ervasti, J.M. (1996) A new model for the interaction of dystrophin with F-actin. J. Cell Biol., 135, 661-672.
36. Warner, L.E., DelloRusso, C., Crawford, R.W., Rybakova, I.N., Patel, J.R., Ervasti, J.M. and Chamberlain, J.S. (2002) Expression of Dp260 in muscle tethers the actin cytoskeleton to the dystrophin-glycoprotein complex and partially prevents dystrophy. Hum. Mol. Genet., 11, 1095-1105.
37. Hanft, L.M., Rybakova, I.N., Patel, J.R., Rafael-Fortney, J.A. and Ervasti, J.M. (2006) Cytoplasmic gamma-actin contributes to a compensatory remodeling response in dystrophindeficient muscle. Proc. Natl Acad. Sci. U. S. A., 103, 5385-5390.
38. Singh, S.M., Bandi, S., Winder, S.J. and Mallela, K.M.G. (2014) The actin binding affinity of the utrophin tandem calponinhomology domain is primarily determined by its N-terminal domain. Biochemistry, 53, 1801-1809.
39. Wein, N., Vulin, A., Falzarano, M.S., Szigyarto, C.A.K., Maiti, B., Findlay, A., Heller, K.N., Uhlén, M., Bakthavachalu, B., Messina, S., et al. (2014) Translation from a DMD exon 5 IRES results in a functional dystrophin isoform that attenuates dystrophinopathy in humans and mice. Nat. Med., 20, 992-1000.
40. Sarkis, J., Vie, V., Winder, S.J., Renault, A., Le Rumeur, E. and Hubert, J.F. (2013) Resisting sarcolemmal rupture: dystrophin repeats increase membrane-actin stiffness. FASEB J, 27, 359-367.
41. Wang, B., Li, J., Qiao, C., Chen, C., Hu, P., Zhu, X., Zhou, L., Bogan, J., Kornegay, J. and Xiao, X. (2008) A canine minidystrophin is functional and therapeutic in mdx mice. Gene Ther., 15, 1099-1106.
42. Gundersen, G.G., Kalnoski, M.H. and Bulinski, J.C. (1984) Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell, 38, 779-789.
43. Poirier, M.G., Eroglu, S. and Marko, J.F. (2002) The bending rigidity of mitotic chromosomes. Mol. Biol. Cell, 13, 2170-2179.
44. Rybakova, I.N., Humston, J.L., Sonnemann, K.J. and Ervasti, J.M. (2006) Dystrophin and utrophin bind actin through distinct modes of contact. J. Biol. Chem., 281, 9996-10001.
45. Henderson, D.M., Lee, A. and Ervasti, J.M. (2010) Diseasecausing missense mutations in actin binding domain 1 of dystrophin induce thermodynamic instability and protein aggregation. Proc. Natl Acad. Sci. U. S. A., 107, 9632-9637.
46. Henderson, D.M., Belanto, J.J., Li, B., Heun-Johnson, H. and Ervasti, J.M. (2011) Internal deletion compromises the stability of dystrophin. Hum. Mol. Genet., 20, 2955-2963.
47. Imai, Y., Matsushima, Y., Sugimura, T. and Terada, M. (1991) A simple and rapid method for generating a deletion by PCR. Nucleic Acids Res., 19, 2785.
48. Liu, W. and Ralston, E. (2014) A new directionality tool for assessing microtubule pattern alterations. Cytoskeleton, 71, 230-240.