A new model for the interaction of dystrophin with F-actin

Journal of Cell Biology

Volumn 135, Issue 3, 1996, Pages 661-672

  Rybakova, Inna N ^a   Amann, Kurt J ^a   Ervasti, James M ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; ALPHA ACTININ; CALPAIN; DYSTROPHIN; F ACTIN; GLYCOPROTEIN;

ACTIN POLYMERIZATION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISSOCIATION CONSTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; RABBIT; SEDIMENTATION RATE; SEQUENCE HOMOLOGY; SKELETAL MUSCLE;

ACTININ; ACTINS; ANIMALS; BINDING SITES; CALCIUM CHLORIDE; CALMODULIN; CHELATING AGENTS; CROSS-LINKING REAGENTS; DYSTROPHIN; EGTAZIC ACID; HYDROGEN-ION CONCENTRATION; MEMBRANE GLYCOPROTEINS; MUSCLE, SKELETAL; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN BINDING; RABBITS; RECOMBINANT PROTEINS; SODIUM CHLORIDE;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0029804981     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.3.661     Document Type: Article

References (77)

1. Acsadi, G., G. Dickson, D.R. Love, A. Jani, F.S. Walsh, A. Gurusinghe, J.A. Wolff, and K.E. Davies. 1991. Human dystrophin expression in mdx mice after intramuscular injection of DNA constructs. Nature (Lond.). 352:815-818.
2. Ahn, A.H., and L.M. Kunkel. 1993. The structural and functional diversity of dystrophin. Nature Genet. 3:283-291.
3. Bard, F., and C. Franzini-Armstrong. 1991. Extra actin filaments at the periphery of skeletal muscle myofibrils. Tissue Cell. 23:191-197.
4. Beggs, A.H., E.P. Hoffman, J.R. Snyder, K. Arahata, L. Specht, F. Shapiro, C. Angelini, H. Sugita, and L.M. Kunkel. 1991. Exploring the molecular basis for variability among patients with Becker muscular dystrophy: dystrophin gene and protein studies. Am. J. Hum. Genet. 49:54-67.
5. Bonet-Kerrache, A., E. Fabbrizio, and D. Mornet. 1994. N-terminal domain of dystrophin. FEBS Lett. 355:49-53.
6. Brenman, J.E., D.S. Chao, S.H. Gee, A.W. McGee, S.E. Craven, D.R. Santillano, Z.Q. Wu, F. Huang, H.H. Xia, M.F. Peters, S.C. Froehner, and D.S. Bredt. 1996. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and (α-syntrophin mediated by PDZ domains. Cell. 84: 757-767.
7. Brooks, S.P.J. 1992. A simple computer program with statistical tests for the analysis of enzyme kinetics. Biotechniques. 13:906-911.
8. Broschat, K.O. 1990. Tropomyosin prevents depolymerization of actin filaments from the pointed end. J. Biol. Chem. 265:21323-21329.
9. Campbell, K.P. 1995. Three muscular dystrophies: Loss of cytoskeleton-extracellular matrix linkage. Cell. 80:675-679.
10. Cano, M.L., L. Cassimeris, M. Fechheimer, and S.H. Zigmond. 1992. Mechanisms responsible for F-actin stabilization after lysis of polymorphonuclear leukocytes. J. Cell Biol. 116:1123-1134.
11. Comi, G.P., A. Prelle, N. Bresolin, M. Moggio, A. Bardoni, A. Gallanti, G. Vita, A. Toscano, M.T. Ferro, A. Bordoni, et al. 1994. Clinical variability in Becker muscular dystrophy. Genetic, biochemical and immunohistochemical correlates. Brain. 117:1-14.
12. Cooper, J.A., S.B. Walker, and T.D. Pollard. 1983. Pyrene actin: documentation of the validity of a sensitive assay for actin polymerization. J. Muscle Res. Cell Motil. 4:253-262.
13. Corrado, K., P.L. Mills, and J.S. Chamberlain. 1994. Deletion analysis of the dystrophin-actin binding domain. FEBS Lett. 344:255-260.
14. Corrado, K., J.A. Rafael, P.L. Mills, N.M. Cole, J.A. Faulkner, K. Wang, and J.S. Chamberlain. 1996. Transgenic mdx mice expressing dystrophin with a deletion in the actin-binding domain display a "mild Becker" phenotype. J. Cell Biol. 134:873-884.
15. Cox, G.A., Y. Sunada, K.P. Campbell, and J.S. Chamberlain. 1994. Dp71 can restore the dystrophin-associated glycoprotein complex in muscle but fails to prevent dystrophy. Nature Genet. 8:333-339.
16. Cullen, M.J., J. Walsh, L.V.B. Nicholson, and J.B. Harris. 1990. Utrastructural localization of dystrophin in human muscle by using gold immunolabeling. Proc. R. Soc. Lond. 240:197-210.
17. D'Souza, V.N., N.T. Man, G.E. Morris, W. Karges, D.M. Pillers, and P.N. Ray. 1995. A novel dystrophin isoform is required for normal retinal electrophysiology. Hum. Mol. Genet. 4:837-842.
18. England, S.B., L.V.B. Nicholson, M.A. Johnson, S.M. Forrest, D.R. Love, E.E. Zubrzycka-Gaarn, D.E. Bulman, J.B. Harris, and K.E. Davies. 1990. Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature (Lond). 343:180-182.
19. Ervasti, J.M., K. Ohlendieck, S.D. Kahl, M.G. Gaver, and K.P. Campbell. 1990. Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature (Lond.). 345:315-319.
20. Ervasti, J.M., S.D. Kahl, and K.P. Campbell. 1991. Purification of dystrophin from skeletal muscle. J. Biol. Chem. 266:9161-9165.
21. Ervasti, J.M. and K.P. Campbell. 1991. Membrane organization of the dystrophin-glycoprotein complex. Cell. 66:1121-1131.
22. Ervasti, J.M., and K.P. Campbell. 1993a. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122:809-823.
23. Ervasti, J.M., and K.P. Campbell. 1993b. Dystrophin and the membrane skeleton. Curr. Opin. Cell Biol. 5:82-87.
24. Fabbrizio, E., A. Bonet-Kerrache, J.J. Leger, and D. Mornet. 1993. Actin-dystrophin interface. Biochemistry. 32:10457-10463.
25. Fukami, K., K. Furuhashi, M. Inagaki, T. Endo, S. Hatano, and T. Takenawa. 1992. Requirement of phosphatidylinositol 4,5-bisphosphate for α-actinin function. Nature (Lond.). 359:150-152.
26. Fukami, K., N. Sawada, T. Endo, and T. Takenawa. 1996. Identification of a phosphatidylinositol 4,5-bisphosphate-binding site in chicken skeletal muscle α-actinin. J. Biol. Chem. 271:2646-2650.
27. Goldberg, M.E., and L. Djavadi-Ohaniance. 1993. Methods for measurement of antibody/antigen affinity based on ELISA and RIA. Curr. Opin. Immunol. 5:278-281.
28. Greenberg, D.S., Y. Sunada, K.P. Campbell, D. Yaffe, and U. Nudel. 1994. Exogenous Dp71 restores the levels of dystrophin associated proteins but does not alleviate muscle damage in mdx mice. Nature Genet. 8:340-344.
29. Helliwell, T.R., J.M. Ellis, R.C. Mountford, R.E. Appleton, and G.E. Morris. 1992. A truncated dystrophin lacking the C-terminal domain is localized at the muscle membrane. Am. J. Hum. Genet. 58:508-514.
30. Hemmings, L., P.A. Kuhlman, and D.R. Critchley. 1992. Analysis of the actin-binding domain of α-actinin by mutagenesis and demonstration that dystrophin contains a functionally homologous domain. J. Cell Biol. 116:1369-1380.
31. Hoffman, E.P., C.A. Garcia, J.S. Chamberlain, C. Angelini, J.R. Lupski, and R. Fenwick. 1991. Is the carboxyl-terminus of dystrophin required for membrane association? A novel, severe case of Duchenne muscular dystrophy. Ann. Neurol. 30:605-610.
32. Hori, S., S. Ohtani, N. Man, and G.E. Morris. 1995. The N-terminal half of dystrophin is protected from proteolysis in situ. Biochem. Biophys. Res. Commun. 209:1062-1067.
33. Ibraghimov-Beskrovnaya, O., J.M. Ervasti, C.J. Leveille, C.A. Slaughter, S.W. Sernett, and K.P. Campbell. 1992. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature (Lond). 355:696-702.
34. Jarrett, H.W. and J.L. Foster. 1995. Alternate binding of actin and calmodulin to multiple sites on dystrophin. J. Biol. Chem. 270:5578-5586.
35. Kahana, E., P.J. Marsh, A.J. Henry, M. Way, and W.B. Gratzer. 1994. Conformation and phasing of dystrophin structural repeats. J. Mol. Biol. 235:1271-1277.
36. Koenig, M., A.P. Monaco, and L.M. Kunkel. 1988. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell. 53:219-228.
37. Koenig, M., and L.M. Kunkel. 1990. Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J. Biol. Chem. 265:4560-4566.
38. r 58,000 dystrophin-associated protein (syntrophin). J. Biol. Chem. 269:2870-2876.
39. Lebart, M.C., D. Casanova, and Y. Benyamin. 1995. Actin interaction with purified dystrophin from electric organ of Torpedo marmorata: possible resemblance with filamin actin interface. J. Muscle Res. Cell Motil. 16:543-552.
40. Li, X., and V. Bennett. 1996. Identification of the spectrin subunit and domains required for formation of spectrin/adducin/actin complexes. J. Biol. Chem. 271:15695-15702.
41. Lo, S.H., P.A. Janmey, J.H. Hartwig, and L.B. Chen. 1994. Interactions of tensin with actin and identification of its three distinct actin-binding domains. J. Cell Biol. 125:1067-1075.
42. MacLean-Fletcher, S., and T.D. Pollard. 1980a. Identification of a factor in conventional muscle actin preparations which inhibits actin filament self-association. Biochem. Biophys. Res. Commun. 96:18-27.
43. MacLean-Fletcher, S.D., and T.D. Pollard. 1980b. Viscometric analysis of the gelation of acanthamoeba extracts and purification of two gelation factors. J. Cell Biol. 85:414-428.
44. Matsudaira, P. 1991. Modular organization of actin crosslinking proteins. Trends Biochem. Sci. 16:87-92.
45. Matsumura, K., F.M.S. Tome, V. Ionasescu, J.M. Ervasti, R.D. Anderson, N.B. Romero, D. Simon, D. Recan, J.-C. Kaplan, M. Fardeau, and K.P. Campbell. 1993. Deficiency of dystrophin-associated proteins in Duchenne muscular dystrophy patients lacking COOH-terminal domains of dystrophin. J. Clin. Invest. 92:866-871.
46. Mejean, C., M.-C. Lebart, C. Roustan, and Y. Benyamin. 1995. Inhibition of actin-dystrophin interaction by inositide phosphate. Biochem. Biophys. Res. Commun. 210:152-158.
47. Menke, A., and H. Jockusch. 1991. Decreased osmotic stability of dystrophin-less muscle cells from the mdx mouse. Nature (Lond.). 349:69-71.
48. Meyer, R.K., and U. Aebi. 1990. Bundling of actin filaments by α-actinin depends on its molecular length. J. Cell Biol. 110:2013-2024.
49. Muntoni, F., P. Gobbi, C. Sewry, T. Sherratt, J. Taylor, S.K. Sandhu, S. Abbs, R. Roberts, S.V. Hodgson, M. Bobrow, and V. Dubowitz. 1994. Deletions in the 5′ region of dystrophin and resulting phenotypes. J. Med. Genet. 31:843-847.
50. Nicholson, L.V.B., K. Davison, G. Falkous, C. Harwood, E. O'Donnell, C.R. Slater, and J.B. Harris. 1989. Dystrophin in skeletal muscle I. Western blot analysis using a monoclonal antibody. J. Neurol. Sci. 94:125-136.
51. Pall, E.A., K.M. Bolton, and J.M. Ervasti. 1996. Differential heparin inhibition of skeletal muscle α-dystroglycan binding to laminins. J. Biol. Chem. 271: 3817-3821.
52. Pardee, J.D., and J.A. Spudich. 1982. Purification of muscle actin. Meth. Enzymol. 85:164-181.
53. Pasternak, C., S. Wong, and E.L. Elson. 1995. Mechanical function of dystrophin in muscle cells. J. Cell Biol. 128:355-361.
54. Petrof, B.J., J.B. Shrager, H.H. Stedman, A.M. Kelly, and H.L. Sweeney. 1993. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. USA. 90:3710-3714.
55. Pollard, T.D., and J.A. Cooper. 1982. Methods to characterize actin filament networks. Methods Enzymol. 85:211-233.
56. Pons, F., N. Augier, R. Heilig, J. Leger, D. Mornet, and J.J. Leger. 1990. Isolated dystrophin molecules as seen by electron microscopy. Proc. Natl. Acad. Sci. USA. 87:7851-7855.
57. Porter, G.A., G.M. Dmytrenko, J.C. Winkelmann, and R.J. Bloch. 1992. Dystrophin colocalizes with β-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J. Cell Biol. 117:997-1005.
58. Prior, T.W., A.C. Papp, P.J. Snyder, A.H.M. Burghes, C. Bartolo, M.S. Sedra, L.M. Western, and J.R. Mendell. 1993. A missense mutation in the dystrophin gene in a Duchenne muscular dystrophy patient. Nature Genet. 4:357-360.
59. Ridge, J.C., J.G. Tidball, K. Ahl, D.J. Law, and W.L. Rickoll. 1994. Modifications in myotendinous junction surface morphology in dystrophin-deficient mouse muscle. Exp. Mol. Pathol. 61:58-68.
60. Schafer, D.A. and J.A. Cooper. 1995. Control of actin assembly at filament ends. Annu. Rev. Cell Biol. 11:497-518.
61. Sealock, R., and S.C. Froehner. 1994. Dystrophin-associated proteins and synapse formation: Is α-dystroglycan the agrin receptor. Cell. 77:617-619.
62. Senter, L., M. Luise, C. Presotto, R. Betto, A. Teresi, S. Ceoldo, and G. Salviati. 1993. Interaction of dystrophin with cytoskeletal proteins: Binding to talin and actin. Biochem. Biophys. Res. Commun. 192:899-904.
63. Stedman, H.H., H.L. Sweeney, J.B. Shrager, H.C. Maguire, R.A. Panettieri, B. Petrof, M. Narusawa, J.M. Leferovich, J.T. Sladky, and A.M. Kelly. 1991. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature (Lond.). 352:536-539.
64. Sunada, Y., S.M. Bernier, C.A. Kozak, Y. Yamada, and K.P. Campbell. 1994. Deficiency of merosin in dystrophic dy mice and genetic linkage of laminin M chain gene to dy locus. J. Biol. Chem. 269:13729-13732.
65. Suzuki, A., M. Yoshida, H. Yamamoto, and E. Ozawa. 1992. Glycoprotein-binding site of dystrophin is confined to the cysteine-rich domain and the first half of the carboxy-terminal domain. FEBS Lett. 308:154-160.
66. Suzuki, A., M. Yoshida, K. Hayashi, Y. Mizuno, Y. Hagiwara, and E. Ozawa. 1994. Molecular organization at the glycoprotein-complex-binding site of dystrophin: Three dystrophin-associated proteins bind directly to the carboxy-terminal portion of dystrophin. Eur. J. Biochem. 220:283-292.
67. Tidball, J.G., and D.J. Law. 1991. Dystrophin is required for normal thin filament-membrane associations at myotendinous junctions. Am. J. Pathol. 138: 17-21.
68. Tinsley, J.M., D.J. Blake, A. Roche, B.C. Byth, A.E. Knight, J. Kendrick-Jones, G.K. Suthers, D.R. Love, Y.H. Edwards, and K.E. Davies. 1992. Primary structure of dystrophin-related protein. Nature (Lond.). 360:591-593.
69. Van Etten, R.A., P.K. Jackson, D. Baltimore, M.C. Sanders, P.T. Matsudaira, and P.A. Janmey. 1994. The COOH terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains with bundling activity. J. Cell Biol. 124:325-340.
70. Way, M., B. Pope, R.A. Cross, J. Kendrick-Jones, and A.G. Weeds. 1992. Expression of the N-terminal domain of dystrophin in E. coli and demonstration of binding to F-actin. FEBS Lett. 301:243-245.
71. Winder, S.J., T.J. Gibson, and J. Kendrick-Jones. 1995. Dystrophin and utrophin: The missing links. FEBS Lett. 369:27-33.
72. 2-terminal F-actin binding domain of utrophin. FEBS Lett. 357:125-128.
73. Winnard, A.V., C.J. Klein, D.D. Coovert, T. Prior, A. Papp, P. Snyder, D.E. Bulman, P.N. Ray, P. McAndrew, W. King, et al. 1993. Characterization of translational frame exception patients in Duchenne/Becker muscular dystrophy. Hum. Mol. Genet. 2:737-744.
74. Worton, R. 1995. Muscular dystrophies: diseases of the dystrophin-glycoprotein complex. Science (Wash. DC). 270:755-756.
75. Yang, B., D. Jung, D. Motto, J. Meyer, G. Koretzky, and K.P. Campbell. 1995. SH3 domain-mediated interaction of dystroglycan and Grb2. J. Biol. Chem. 270:11711-11714.
76. Yoshida, M., A. Suzuki, H. Yamamoto, S. Noguchi, Y. Mizuno, and E. Ozawa. 1994. Dissociation of the complex of dystrophin and its associated proteins into several unique groups by n-octyl β-D-glucoside. Eur.J.Biochem. 222: 1055-1061.
77. Yoshida, M., and E. Ozawa. 1990. Glycoprotein complex anchoring dystrophin to sarcolemma. J. Biochem. 108:748-752.