Skip to main content
SpringerLink
Log in

REVIEW: The membrane--cytoskeleton interface: the role of dystrophin and utrophin

  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Abstract

Recent studies with transgenic animals have consid erably advanced our knowledge of the roles of dystrophin and utrophin in both muscle and non-muscle tissues. Rigorous analyses of the roles of the various mdxmutations in mice, as well as the use of artificial transgenes in an mdxbackground, are beginning to define the functional importance of various regions of the dystrophin protein in normal muscle. Furthermore, recent biochemical analyses have revealed new insights into the role and organization of dystrophin at the membrane--cytoskeleton interface. Transgenic approaches have also revealed surprising and encouraging results with respect to utrophin. Against expectations, the long-awaited utrophin knockout mice have a remarkably mild phenotype with only subtle changes in neuromuscular junction architecture. On the other hand, mdxmice transgenic for a mini-utrophin construct showed rescue of the muscular dystrophy phenotype, clearly an encouraging finding with obvious therapeutic possibilities. These and other recent findings are discussed in the context of the structure and function of dystrophin and utrophin at the membrane--cytoskeleton interface

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • AHN, A. H. & KUNKEL, L. M. (1995) Syntrophin binds to an alternatively spliced exon of dystrophin. J. Cell Biol. 128, 363-71.

    Article  PubMed  CAS  Google Scholar 

  • AMALFITANO, A., RAFAEL, J. A. & CHAMBERLAIN, J. S. (1997) Structure and mutation of the dystrophin gene. In Dystrophin: Gene, Protein and Cell Biology (edited by LUCY, J. A. & BROWN, S. C.), pp. 1-26. Cambridge: Cambridge University Press.

    Google Scholar 

  • ANDRE, B. & SPRINGAEL, J. Y. (1994) WWP, a new amino acid motif present in single or multiple copies in various proteins including dystrophin and the SH3-binding Yes-associated protein YAP65. Biochem. Biophys. Res. Commun. 205, 1201-5.

    Article  PubMed  CAS  Google Scholar 

  • ASCADI, G., DICKSON, G., LOVE, D. R., JANI, A., WALSH, F. S., GURUSINGHE, A., WOLFF, J. A. & DAVIES, K. E. (1991) Human dystrophin expression in mdx mice after intramuscular injection of DNA constructs. Nature 352, 815-8.

    Article  Google Scholar 

  • BAR, S., BARNEA, E., LAVY, Z., NEUMAN, S., YAFFE, D. & NUDEL, U. (1990) A novel protein product of the Duchenne muscular dystrophy gene which greatly differs from known isoforms in its structure and tissue distribution. Biochem. J. 272, 557-60.

    PubMed  CAS  Google Scholar 

  • BEGGS, A. H., HOFFMAN, E. P., SNYDER, J. R., ARAHATA, K., SPECHT, L., SHAPIRO, F., ANGELINI, C., SUGITA, H. & KUNKEL, L. M. (1991) Exploring the molecular basis for variability among patients with Becker muscular dystrophy-dystrophin gene and protein studies. Am. J. Human Gen. 49, 54-67.

    CAS  Google Scholar 

  • BLAKE, D. J., TINSLEY, J. M., DAVIES, K. E., KNIGHT, A. E., WINDER, S. J. & KENDRICK-JONES, J. (1995a) Coiled-coil regions in the carboxy terminal domains of dystrophin and related proteins: potentials for protein-protein interactions. TIBS 20, 133-5.

    PubMed  CAS  Google Scholar 

  • BLAKE, D. J., SCHOLFIELD, J. N., ZUELLIG, R. A., GORECKI, D. G., PHELPS, S. R., BARNARD, E. A., EDWARDS, Y. H. & DAVIES, K. E. (1995b) G-utrophin, the autosomal homologue of dystrophin DP116, is expressed in sensory ganglia and brain. Proc. Nalt Acad. Sci. USA 92, 3697-701.

    Article  CAS  Google Scholar 

  • BLAKE, D. J., TINSLEY, J. M. & DAVIES, K. E. (1996a) Utrophin: a structural and functional comparison to dystrophin. Brain Path. 6, 37-47.

    CAS  Google Scholar 

  • BLAKE, D. J., NAWROTZKI, R., PETERS, M. F., FROEHNER, S. C. & DAVIES, K. E. (1996b) Isoform diversity of dystrobrevin, the murine 87-kDa postsynaptic protein. J. Biol. Chem. 271, 7802-10.

    Article  PubMed  CAS  Google Scholar 

  • BONNEMANN, C. G., et al. (1995) β-sarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex. Nature Genet. 11, 266-73.

    Article  PubMed  CAS  Google Scholar 

  • BORK, P. & SUDOL, M. (1994) The WW domain: a signalling site in dystrophin? Trends Biochem. Sci. 19, 531-3.

    Article  PubMed  CAS  Google Scholar 

  • BYERS, T. J., LIDOV, H. G. W. & KUNKEL, L. M. (1993) An alternative dystrophin transcript specific to peripheral nerve. Nature Genet. 4, 77-81.

    Article  PubMed  CAS  Google Scholar 

  • CAMPBELL, K. P. (1995) Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80, 675-9.

    Article  PubMed  CAS  Google Scholar 

  • CAMPBELL, K. P. & KAHL, S. D. (1989) Association of dystrophin and an integral membrane glycoprotein. Nature 338, 259-62.

    Article  PubMed  CAS  Google Scholar 

  • CHEN, H. I. & SUDOL, M. (1995) The WW domain of the Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc. Natl Acad. Sci. USA 92, 7819-23.

    Article  PubMed  CAS  Google Scholar 

  • COLLINS, A. F., PEARSON, H. A., GIARDINA, P., MCDONAGH, K. T., BRUSILOW, S. W. & DOVER, G. J. (1995) Oral sodium phenylbutyrate therapy in homozygous β-thalassemia: a clinical trial. Blood 85, 43-9.

    PubMed  CAS  Google Scholar 

  • CORRADO, K., RAFAEL, J. A., MILLS, P. L., COLE, N. M., FAULKNER, J. A., WANG, K. & CHAMBERLAIN, J. S. (1996) Transgenic mdx mice expressing dystrophin with a deletion in the actin-binding domain display a ”mild Becker” phenotype. J. Cell Biol. 134, 873-84.

    Article  PubMed  CAS  Google Scholar 

  • COX, G. A., PHELPS, S. F., CHAPMAN, V. M. & CHAMBERLAIN, J. S. (1993) New mdx mutation disrupts expression of muscle and nonmuscle isoforms of dystrophin. Nature Genet. 4, 87-93.

    Article  PubMed  CAS  Google Scholar 

  • COX, G. A., SUNADA, Y., CAMPBELL, K. P. & CHAMBERLAIN, J. S. (1994) Dp71 can restore the dystrophinassociated glycoprotein complex in muscle but fails to prevent dystrophy. Nature Genet. 8, 333-9.

    Article  PubMed  CAS  Google Scholar 

  • DAVISON, M. D. & CRITCHLEY, D. R. (1988) Alpha-actinins and the DMD protein contain spectrin-like repeats. Cell 52, 159-60.

    Article  PubMed  CAS  Google Scholar 

  • DAWSON, R.M.C., ELLIOTT, D.C., ELLIOTT, W.H. & JONES, K.M., (1986) Data for Biochemical Research. Oxford: Clarendon Press.

    Google Scholar 

  • DECONINCK, A. E., POTTER, A. C., TINSLEY, J. M., WOOD, S. J., VATER, R., YOUNG, C., METZINGER, L., VINCENT, A., SLATER, C. R. & DAVIES, K. E. (1997a) Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice. J. Cell Biol. 136, 883-940.

    Article  PubMed  CAS  Google Scholar 

  • DECONINCK, A. E., RAFAEL, J. A., SKINNER, J. A., BROWN, S. C., POTTER, A. C., METZINGER, L., WATT, D. J., DICKSON, J. G., TINSLEY, J. M. & DAVIES, K. E. (1997b) Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 90, 717-27.

    Article  PubMed  CAS  Google Scholar 

  • DOVER, G. J., BRUSILOW, S. & CHARACHE, S. (1994) Induction of fetal hemoglobin production in subjects with sickle-cell-anemia by oral sodium phenylbutyrate. Blood 84, 339-43.

    PubMed  CAS  Google Scholar 

  • D'SOUZA, V. N., NGUYEN THI MAN, MORRIS, G. E., KARGES, W., PILLERS, D. A. & RAY, P. N. (1995) A novel dystrophin isoform is required for normal retinal electrophysiology. Hum. Mol. Genet. 4, 837-42.

    PubMed  Google Scholar 

  • EMERY, A.E.H., (1993) Duchenne Muscular Dystrophy. Oxford: Oxford University Press.

    Google Scholar 

  • ENGLAND, S. B., NICHOLSON, L. V. B., JOHNSON, M. A., FORREST, S. M., LOVE, D. R., ZUBRZYCKA-GAARN, E. E., BULMAN, D. E., HARRIS, J. B. & DAVIES, K. E. (1990) Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature 343, 180-82.

    Article  PubMed  CAS  Google Scholar 

  • ERVASTI, J. M. & CAMPBELL, K. P. (1993) A role for the dystrophin glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122, 809-23.

    Article  PubMed  CAS  Google Scholar 

  • ERVASTI, J. M., OHLENDIECK, K., KAHL, S. D., GAVER, M. G. & CAMPBELL, K. P. (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345, 315-9.

    Article  PubMed  CAS  Google Scholar 

  • ERVASTI, J. M., KAHL, S. D. & CAMPBELL, K. P. (1991) Purification of dystrophin from skeletal muscle. J. Biol. Chem. 266, 9161-5.

    PubMed  CAS  Google Scholar 

  • FABBRIZIO, E., BONET-KERRACHE, A., LEGER, J. J. & MORNET, D. (1993) Actin-dystrophin interface. Biochem. 32, 10457-63.

    Article  CAS  Google Scholar 

  • FABBRIZIO, E., PONS, F., ROBERT, A., HUGNON, G., BONET-KERRACHE, A. & MORNET, D. (1994) The dystrophin superfamily: variability and complexity. J. Muscle Res. Cell Motil. 15, 595-606.

    Article  PubMed  CAS  Google Scholar 

  • GORECKI, D. C. & BARNARD, E. A. (1997) Expression of the dystrophin complex in brain. In Dystrophin: Gene, Protein and Cell Biology (edited by LUCY, J. A. & BROWN, S. C.), pp. 105-38. Cambridge: Cambridge University Press.

    Google Scholar 

  • GORECKI, D. C., MONACO, A. P., DERRY, J. M. J., WALKER, A. P., BARNARD, E. A. & BARNARD, P. J. (1992) Expression of four alternative transcripts in human brain regions regulated by different promoters. Hum. Mol. Genet. 1, 505-10.

    PubMed  CAS  Google Scholar 

  • GRADY, R. M., MERLIE, J. P. & SANES, J. R. (1997a) Subtle neuromuscular defects in utrophin-deficient mice. J. Cell Biol. 136, 871-82.

    Article  PubMed  CAS  Google Scholar 

  • GRADY, R. M., TENG, H., NICHOLL, M. C., CUNNINGHAM, J. C., WILKINSON, R. S. & SANES, J. R. (1997b) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90, 729-38.

    Article  PubMed  CAS  Google Scholar 

  • GRAMOLINI, A. O., DENNIS, C. L., TINSLEY, J. M., ROBERTSON, G. S., CARTAUD, J., DAVIES, K. E. & JASMIN, B. J. (1997) Local transcriptional control of utrophin expression at the neuromuscular synapase. J. Biol. Chem. Nature Genet. 272, 8117-20.

    CAS  Google Scholar 

  • GREENBERG, D. S., SUNADA, Y., CAMPBELL, K. P., YAFFE, D. & NUDEL, U. (1994) Exogenous Dp71 restores the levels of dystrophin-associated proteins but does not alleviate muscle damage in Mdx mice. Nature Genet. 8, 340-44.

    Article  PubMed  CAS  Google Scholar 

  • HAMMONDS, R. G. (1987) Protein sequence of DMD gene is related to actin binding domain of alpha-actinin. Cell 51, 1.

    Article  PubMed  CAS  Google Scholar 

  • HEMMINGS, L., KUHLMAN, P. A. & CRITCHLEY, D. R. (1992) Analysis of the actin-binding domain of α-actinin by mutatgenesis and demonstration that dystrophin contains a functionally homologous domain. J. Cell Biol. 116, 1369-80.

    Article  PubMed  CAS  Google Scholar 

  • HOFFMAN, E. P., BROWN, R. H. & KUNKEL, L. M. (1987) Dystrophin-the protein product of the Duchenne muscular-dystrophy locus. Cell 51, 919-28.

    Article  PubMed  CAS  Google Scholar 

  • HORI, S., OHTANI, S., NGUYEN THI MAN & MORRIS, G. E. (1995) The N-terminal half of dystrophin is protected from proteolysis in situ. Biochem. Biophys. Res. Commun. 209, 1062-7.

    Article  PubMed  CAS  Google Scholar 

  • IBRAGHIMOV-BESKROVNAYA, O., ERVASTI, J. M, LEVEILLE, C. J., SLAUGHTER, C. A., SERNETT, S. W. & CAMPBELL, K. P. (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355, 696-702.

    Article  PubMed  CAS  Google Scholar 

  • JUNG, D., YANG, B., MEYER, J., CHAMBERLAIN, J. S. & CAMPBELL, K. P. (1995) Identification and characterization on the dystrophin anchoring site on betadystroglycan. J. Biol. Chem. 270, 27305-10.

    Article  PubMed  CAS  Google Scholar 

  • JUNG, D., DUCLOS, F., APOSTOL, B., STRAUB, V., LEE, J. C., ALLAMAND, V., VENZKE, D. P., SUNADA, Y., MOOMAW, C. R., LEVEILLE, C. J., SLAUGHTER, C. A., CRAWFORD, T. O., McPHERSON, J. D. & CAMPBELL, K. P. (1996) Characterization of δ-sarcoglycan, a novel component of the oligomeric sarcoglycan complex involved in limb-girdle muscular dystrophy. J. Biol. Chem. 271, 32321-9.

    Article  PubMed  CAS  Google Scholar 

  • KAHANA, E., FLOOD, G. & GRATZER, W. B. (1997) Physical properties of dystrophin rod domain. Cell Motil. Cytoskel. 36, 246-52.

    Article  CAS  Google Scholar 

  • KHURANA, T. S., HOFFMAN, E. P. & KUNKEL, L. M. (1990) Identification of a chromosome-6-encoded dystrophinrelated protein. J. Biol. Chem. 265, 16717-20.

    PubMed  CAS  Google Scholar 

  • KLAMUT, H. J., GANGOPADHYAY, S. B., WORTON, R. G. & RAY, P. N. (1990) Molecular and functional analysis of the muscle-specific promoter region of the Duchenne muscular dystrophy gene. Mol. Cell. Biol. 10, 193-205.

    PubMed  CAS  Google Scholar 

  • KOENIG, M., HOFFMAN, E. P., BERTELSON, C. J., MONACO, A. P., FEENER, C. & KUNKEL, L. M. (1987) Complete cloning of the Duchenne muscular-dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50, 509-17.

    Article  PubMed  CAS  Google Scholar 

  • KOENIG, M., MONACO, A. P. & KUNKEL, L. M. (1988) The complete sequence of dystrophin predicts a rodshaped cytoskeletal protein. Cell 53, 219-28.

    Article  PubMed  CAS  Google Scholar 

  • KOENIG, M. et al. (1989) The molecular basis Duchenne versus Becker muscular-dystrophy-correlation of severity with type of deletion. Am. J. Hum. Genet. 45, 498-506.

    PubMed  CAS  Google Scholar 

  • KRAMARCY, N. R., VIDAL, A., FROEHNER, S. C. & SEALOCK, R. (1994) Association of utrophin and multiple dystrophin short forms with the mammalian Mr 58,000 dystrophin-associated protein (syntrophin). J. Biol. Chem. 269, 2870-6.

    PubMed  CAS  Google Scholar 

  • LEBART, M.-C., CASANOVA, D. & BENYAMIN, Y. (1995) Actin interaction with purified dystrophin from electric organ of Torpedo marmorata: possible resemblence with filamin-actin interface. J. Muscle Res. Cell Motil. 16, 543-52.

    Article  PubMed  CAS  Google Scholar 

  • LENK, U., OXELE, K., VOIT, T., ANCKER, U., HELLNER, K.-A., SPEER, A. & HUBNER, C. (1996) A cysteine 3340 substitution in the dystroglycan-binding of dystrophin associated with Duchenne muscular dystrophy, mental retardation and absence of the ERG b-wave. Hum. Mol. Genet. 5, 973-5.

    Article  PubMed  CAS  Google Scholar 

  • LIDOV, H. G. W., SELIG, S. & KUNKEL, L. M. (1995) Dp140: a novel 140 kDa cns transcript from the dystrophin locus. Hum. Mol. Genet. 4, 329-35.

    PubMed  CAS  Google Scholar 

  • LIM, L. E., DUCLOS, F., BROUX, O., BOURG, N., SUNADA, Y., ALLAMAND, V., MEYER, J., RICHARD, I., MOOMAW, C., SLAUGHTER, C., TOME, F. M. S., FARDEAU, M., JACKSON, C. E., BECKMANN, J. S. & CAMPBELL, K. P. (1995) β-sarcoglycan: characterization and role in limb-girdle muscular dystrophy linked to 4q12. Nature Genet. 11, 257-65.

    Article  PubMed  CAS  Google Scholar 

  • LOVE, D. R., HILL, D. F., DICKSON, G., SPURR, N. K., BYTH, B. C., MARSDEN, R. F., WALSH, F. S., EDWARDS, Y. H. & DAVIES, K. E. (1989) An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 339, 55-8.

    Article  PubMed  CAS  Google Scholar 

  • LOVE, D.R., MORRIS, G.E., ELLIS, J.M., FAIRBROTHER, O., MARSDEN, R.F., BLOOMFIELD, J.F., EDWARDS, Y.H., SLATER, C.P., PARRY, D.J. & DAVIES, K.E. (1991) Tissue distribution of the dystrophin-related gene product and expression in the mdx and dy mouse. Proc. Natl Acad. Sci. USA 88, 3243-7.

    Article  PubMed  CAS  Google Scholar 

  • MACIAS, M. J., HYVONEN, M., BARALDI, E., SCHULTZ, J., SUDOL, M., SARASTE, M. & OSCHKINAT, H. (1996) Structure of the WW domain of a kinase-associated protein complexed with a proline-rich peptide. Nature 382, 646-9.

    Article  PubMed  CAS  Google Scholar 

  • MICHALAK, M., FU, S. Y., MILNER, R. E., BUSAAN, J. L. & HANCE, J. E. (1996) Phosphorylation of the carboxyterminal region of dystrophin. Biochem. Cell Biol. 74, 431-7.

    Article  PubMed  CAS  Google Scholar 

  • MILNER, R. E., BUSSAN, J. L. & MICHALAK, M. (1992) Isolation and characterisation of different C-terminal fragments of dystrophin expressed in Escherichia coli. Biochem. J. 288, 1037-44.

    PubMed  CAS  Google Scholar 

  • MIZUNO, Y., YOSHIDA, M., YAMAMOTO, H., HIRAI, S. & OZAWA, E. (1993) Distribution of dystrophin isoforms and dystrophin-associated proteins 43DAG (A3a) and 50DAG (A2) in various monkey tissues. J. Biochem. 114, 936-41.

    PubMed  CAS  Google Scholar 

  • MONACO, A. P., BERTELSON, C. J., LIECHTI-GALLATI, S., MOSER, H. & KUNKEL, L. (1988) An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics 2, 90-95.

    Article  PubMed  CAS  Google Scholar 

  • NGUYEN THI MAN, ELLIS, J. M., LOVE, D. R., DAVIES, K. E., GATTER, K. C., DICKSON, G. & MORRIS, G. E. (1991) Localization of the DMDL gene-encoded dystrophinrelated protein using a panel of nineteen monoclocal antibodies: presence at neuromuscular junctions, in the sarcolemma of dystrophic skeletal muscle in vascular and other smooth muscles, and in proliferating brain cell lines. J. Cell Biol. 115, 1695-1700.

    Article  PubMed  CAS  Google Scholar 

  • NGUYEN THI MAN, HELLIWELL, T. R., SIMMONS, C., WINDER, S. J., KENDRICK-JONES, J., DAVIES, K. E. & MORRIS, G. (1995) Full-length and short forms of utrophin, the dystrophin-related protein. FEBS Lett. 258, 262-6.

    Article  Google Scholar 

  • NUDEL, U., ZUK, D., EINAT, P., ZEELON, E., LEVY, Z., NEUMAN, S. & YAFFE, D. (1989) Duchenne muscular dystrophy gene product is not identical in muscle and brain. Nature 337, 76-8.

    Article  PubMed  CAS  Google Scholar 

  • OHLENDIECK, K., ERVASTI, J. M., MATSUMURA, K., KAHL, S. D., LEVEILLE, C. J. & CAMPBELL, K. P. (1991) Dystrophin-related protein is localized to neuromuscular-junctions of adult skeletal-muscle. Neuron 7, 499-508.

    Article  PubMed  CAS  Google Scholar 

  • PASTERNACK, C., WONG, S. & ELSON, E. L. (1995) Mechanical function of dystrophin in muscle cells. J. Cell Biol. 128, 355-61.

    Article  Google Scholar 

  • PHELPS, S. F., HAUSER, M. A., COLE, N. M., RAFAEL, J. A., HINKLE, R. T. & FAULKNER, J. A. (1995) Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum. Mol. Genet. 4, 1251-8.

    PubMed  CAS  Google Scholar 

  • PONTING, C. P., BLAKE, D. J., DAVIES, K. E., KENDRICK-JONES, J. & WINDER, S. J. (1996) ZZ and TAZ: new putative zinc fingers in dystrophin, CBP, p300 and other proteins. Trends Biochem. Sci. 21, 11-13.

    Article  PubMed  CAS  Google Scholar 

  • PRIOR, T. W., PAPP, A. C., SNYDER, P. J., BURGHES, A. H. M., BARTOLO, C., SEDRA, M. S., WESTERN, L. M. & MENDELL, J. R. (1993) A missense mutation in the dystrophin gene in a Duchenne muscular dystrophy patient. Nature Genet. 4, 357-60.

    Article  PubMed  CAS  Google Scholar 

  • RAFAEL, J. A., COX, G. A., CORRADO, K., JUNG, D., CAMPBELL, K. P. & CHAMBERLAIN, J. S. (1996) Forced expression of dystrophin deletion constructs reveals structure-function correlations. J. Cell Biol. 134, 93-102.

    Article  PubMed  CAS  Google Scholar 

  • ROBERTS, R. G., GARDNER, R. J. & BOBROW, M. (1994) Searching for the 1 in 2,400,000: a review of dystrophin gene point mutations. Hum. Mutat. 4, 1-11.

    Article  PubMed  CAS  Google Scholar 

  • ROBERTS, R. G., FREEMAN, T. C., KENDALL, E., VETRIE, D. L. P., DIXON, A. K., SHAW-SMITH, C., BONE, Q. & BOBROW, M. (1996) Characterization of DRP2, a novel human dystrophin homologue. Nature Genet. 13, 223-6.

    Article  PubMed  CAS  Google Scholar 

  • ROSA, G., CECCARINI, M., CAVALDESI, M., ZINI, M. & PETRUCCI, T. C. (1996) Localisation of the dystrophin binding site at the carboxyl terminus of β-dystroglycan. Biochem. Biophys. Res. Commun. 223, 272-7.

    Article  PubMed  CAS  Google Scholar 

  • RYBAKOVA, I. N., AMMAN, K. J. & ERVASTI, J. M. (1996) A new model for the interaction of dystrophin with F-actin. J. Cell Biol. 135, 661-72.

    Article  PubMed  CAS  Google Scholar 

  • SADOULET-PUCCIO, H. M. & KUNKEL, L. M. (1996) Dystrophin and its isoforms. Brain Path. 6, 25-35.

    CAS  Google Scholar 

  • SARASTE, M. & MUSACCHIO, A. (1994) Backwards and forwards binding. Nature Struct. Biol. 1, 835-7.

    Article  PubMed  CAS  Google Scholar 

  • SENTER, L., LUISE, M., PRESOTTO, C., BETTO, R., TERESI, A., CEOLDO, S. & SALVIATI, G. (1993) Interaction of dystrophin with cytoskeletal proteins: binding to talin and actin. Biochem. Biophys. Res. Commun. 192, 899-904.

    Article  PubMed  CAS  Google Scholar 

  • SONG, K. S., SCHERER, P. E., TANG, Z., OKAMOTO, T., LI, S., CHAFEL, M., CHU, C., KOHTZ, D. S. & LISSANTI, M. P. (1996) Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J. Biol. Chem. 271, 15160-65.

    Article  PubMed  CAS  Google Scholar 

  • SUZUKI, A., YOSHIDA, M., YAMAMOTO, H. & OZAWA, E. (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, 154-60.

    Article  PubMed  CAS  Google Scholar 

  • SUZUKI, A., YOSHIDA, M., HAYASHI, K., MIZUNO, Y., HAGIWARA, Y. & OZAWA, E. (1994) Molecular organisation 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, 283-92.

    Article  PubMed  CAS  Google Scholar 

  • SUZUKI, A., YOSHIDA, M. & OZAWA, E. (1995) Mammalian α1-and β1-syntrophin bind to the alternative splice prone region of the dystrophin COOH-terminus. J. Cell Biol. 128, 373-81.

    Article  PubMed  CAS  Google Scholar 

  • THOMPSON, J. D., HIGGINS, D. G. & GIBSON, T. J. (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-80.

    PubMed  CAS  Google Scholar 

  • TINSLEY, J. M., BLAKE, D. J., ROCHE, A., FAIRBROTHER, U., RISS, J., BYTH, B. C., KNIGHT, A. E., KENDRICK-JONES, J., SUTHERS, G. K., LOVE, D. R., EDWARDS, Y. H. & DAVIES, K. E. (1992) Primary structure of dystrophinrelated protein. Nature 360, 591-3.

    Article  PubMed  CAS  Google Scholar 

  • TINSLEY, J. M., BLAKE, D. J. & DAVIES, K. E. (1993) Apodystrophin 3: a 2.2 kb transcript from the DMD locus encoding the dystrophin glycoprotein binding site. Hum. Mol. Genet. 2, 521-4.

    PubMed  CAS  Google Scholar 

  • TINSLEY, J. M., BLAKE, D. J., ZUELLIG, R. A. & DAVIES, K. E. (1994) Increasing complexity of the dystrophinassociated protein complex. Proc. Natl Acad. Sci. USA 91, 8307-13.

    Article  PubMed  CAS  Google Scholar 

  • TINSLEY, J. M., POTTER, A. C., PHELPS, S. R., FISHER, R., TRICKETT, J. I. & DAVIES, K. E. (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 384, 349-53.

    Article  PubMed  CAS  Google Scholar 

  • TINSLEY, J. M., BLAKE, D. J. & DAVIES, K. E. (1997) Dystrophin, utrophin and their associated proteins. In Dystrophin: Gene, Protein and Cell Biology (edited by LUCY, J. A. & BROWN, S. C.), pp. 56-78. Cambridge: Cambridge University Press.

    Google Scholar 

  • TUFTY, R. M. & KRETSINGER, R. H. (1975) Troponin and parvalbumin calcium binding regions predicted in myosin light chain and T4 iysozyme. Science 187, 167-9.

    PubMed  CAS  Google Scholar 

  • WAGNER, K. R., COHEN, J. B. & HUGANIR, R. L. (1993) The 87K postsynaptic membrane protein from Torpedo is a protein-tyrosine kinase substrate homologous to dystrophin. Neuron 10, 511-22.

    Article  PubMed  CAS  Google Scholar 

  • WAGNER, K. R., COHEN, J. B. & HUGANIR, R. L. (1993) The 87K postsynaptic membrane protein from Torpedo is a protein-tyrosine kinase substrate homologous to dystrophin. Neuron 10, 511-22.

    Article  PubMed  CAS  Google Scholar 

  • WAGNER, K. R. & HUGANIR, R. L. (1994) Tyrosine and serine phosphorylation of dystrophin and the 58 kDa protein in the postsynaptic membrane of Torpedo electric organ. J. Neurochem. 62, 1947-52.

    Article  PubMed  CAS  Google Scholar 

  • WATKINS, S. C., SWARTZ, D. R. & BYERS, T. J.. (1997) Localisation of dystrophin in skeletal, cardiac and smooth muscle. In Dystrophin: Gene, Protein and Cell Biology (edited by LUCY, J. A. & BROWN, S. C.), pp. 79-104. Cambridge: Cambridge University Press.

    Google Scholar 

  • WAY, M., POPE, B., CROSS, R. A., KENDRICK-JONES, J. & 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, 243-5.

    Article  PubMed  CAS  Google Scholar 

  • WELLS, D. J., WELLS, K. E., ASANTE, E. A., TURNER, G., SUNADA, Y., CAMPBELL, K. P., WALSH, F. S. & DICKSON, G. (1995) Expression of human full-length and minidystrophin in transgenic mdx mice: implications for gene therapy of Duchenne muscular dystrophy. Hum. Mol. Genet. 4, 1245-50.

    PubMed  CAS  Google Scholar 

  • WINDER, S. J. (1996) Structure-function relationships in dystrophin and utrophin. Biochem. Soc. Trans. 24, 497-501.

    PubMed  CAS  Google Scholar 

  • WINDER, S. J. & KENDRICK-JONES, J. (1995) Calcium/calmodulin-dependent regulation of the NH2-terminal F-actin binding domain of utrophin. FEBS Lett. 357, 125-8.

    Article  PubMed  CAS  Google Scholar 

  • WINDER, S. J., HEMMINGS, L., MACIVER, S. K., BOLTON, S. J., TINSLEY, J. M., DAVIES, K. E., CRITCHLEY, D. R. & KENDRICK-JONES, J. (1995a) Utrophin actin binding domain: analysis of actin binding and cellular targeting. J. Cell Sci. 108, 63-71.

    PubMed  CAS  Google Scholar 

  • WINDER, S. J., GIBSON, T. J. & KENDRICK-JONES, J. (1995b) Dystrophin and utrophin: the missing links! FEBS Lett. 369, 27-33.

    Article  PubMed  CAS  Google Scholar 

  • WINDER, S. J., GIBSON, T. J. & KENDRICK-JONES, J. (1996) Low probability of dystrophin and utrophin coiled coil regions forming dimers. Biochem. Soc. Trans. 24, 280S.

    PubMed  CAS  Google Scholar 

  • WINDER, S. J., KNIGHT, A. E. & KENDRICK-JONES, J. (1997) Protein Structure. In Dystrophin: Gene, Protein and Cell Biology (edited by LUCY, J. A. & BROWN, S. C.), pp. 27-55. Cambridge: Cambridge University Press.

    Google Scholar 

  • WORTON, R. (1995) Muscular dystrophies: diseases of the dystrophin-glycoprotein complex. Science 270, 755-6.

    PubMed  CAS  Google Scholar 

  • YAMAMOTO, H., MIZUNO, Y., HAYASHI, K., NONAKA, I., YOSHIDA, M. & OZAWA, E. (1994) Expression of dystrophin-associated protein 35DAG (A4) and 50DAG (A2) is confined to striated muscles. J. Biochem. 115, 162-7.

    PubMed  CAS  Google Scholar 

  • YOSHIDA, M., SUZUKI, A., SHIMIZU, T. & OZAWA, E. (1992) Proteinase sensitive sites on isolated rabbit dystrophin. J. Biochem. 112, 433-9.

    PubMed  CAS  Google Scholar 

  • YOSHIDA, M., SUZUKI, A., YAMAMOTO, H., NOGUCHI, S., MIZUNO, Y. & OZAWA, E. (1994) Dissociation of the complex of dystrophin and its associated proteins into several groups by n-octyl β-D-glucoside. Eur. J. Biochem. 222, 1055-61.

    Article  PubMed  CAS  Google Scholar 

  • YOSHIDA, M., YAMAMOTO, H., NOGUCHI, S., MIZUNO, Y., HAGIWARA, Y. & OZAWA, E. (1995) Dystrophinassociated protein A0 is a homologue of the Torpedo 87K protein. FEBS Lett. 367, 311-4.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Cell and Molecular Biology, University of Edinburgh, Mayfield Road, Edinburgh, UK

    Steven J. Winder

Authors
  1. Steven J. Winder
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Winder, S.J. REVIEW: The membrane--cytoskeleton interface: the role of dystrophin and utrophin. J Muscle Res Cell Motil 18, 617–629 (1997). https://doi.org/10.1023/A:1018627705273

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1018627705273

Keywords

Search

Navigation