Assembly of the Dystrophin-Associated Protein Complex Does Not Require the Dystrophin Cooh-Terminal Domain

doi:10.1083/jcb.150.6.1399

Published online 18 September 2000. doi:10.1083/jcb.150.6.1399

This Article

	Full Text
	Full Text (PDF, 661K)
	PPT slides of all figures
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Crawford, G. E.
	Articles by Chamberlain, J. S.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Crawford, G. E.
	Articles by Chamberlain, J. S.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/2000//1399 $5.00
The Journal of Cell Biology, Volume 150, Number 6, , 2000 1399-1410

Original Article

Assembly of the Dystrophin-Associated Protein Complex Does Not Require the Dystrophin Cooh-Terminal Domain

Gregory E. Crawford^a, John A. Faulkner^d, Rachelle H. Crosbie^e, Kevin P. Campbell^e, Stanley C. Froehner^f, and Jeffrey S. Chamberlain^a^,b^,c

^a Program in Cellular and Molecular Biology, University of Michigan, Ann Arbor, Michigan 48109-0618
^b Department of Human Genetics, University of Michigan, Ann Arbor, Michigan 48109-0618
^c Center for Gene Therapy, University of Michigan, Ann Arbor, Michigan 48109-0618
^d Department of Physiology, University of Michigan, Ann Arbor, Michigan 48109-0618
^e Howard Hughes Medical Institute, Department of Physiology and Biophysics, Department of Neurology, University of Iowa College of Medicine, Iowa City, Iowa 52242
^f Department of Cell and Molecular Physiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7545
Department of Human Genetics, University of Michigan, Ann Arbor, MI 48109-0618.(734) 764-6898(734) 764-4297

Dystrophin is a multidomain protein that links the actin cytoskeletonto laminin in the extracellular matrix through the dystrophinassociated protein (DAP) complex. The COOH-terminal domain ofdystrophin binds to two components of the DAP complex, syntrophinand dystrobrevin. To understand the role of syntrophin and dystrobrevin,we previously generated a series of transgenic mouse lines expressingdystrophins with deletions throughout the COOH-terminal domain.Each of these mice had normal muscle function and displayednormal localization of syntrophin and dystrobrevin. Since syntrophinand dystrobrevin bind to each other as well as to dystrophin,we have now generated a transgenic mouse deleted for the entiredystrophin COOH-terminal domain. Unexpectedly, this truncateddystrophin supported normal muscle function and assembly ofthe DAP complex. These results demonstrate that syntrophin anddystrobrevin functionally associate with the DAP complex inthe absence of a direct link to dystrophin. We also observedthat the DAP complexes in these different transgenic mouse strainswere not identical. Instead, the DAP complexes contained varyingratios of syntrophin and dystrobrevin isoforms. These resultssuggest that alternative splicing of the dystrophin gene, whichnaturally generates COOH-terminal deletions in dystrophin, mayfunction to regulate the isoform composition of the DAP complex.

Key Words: dystrophin • muscular dystrophy • syntrophin • dystrobrevin • mdx mice

Rachelle Crosbie's current address is Department of PhysiologicalScience, UCLA, College of Life Sciences, Los Angeles, CA 90095.

Abbreviations used in this paper: DAP, dystrophin-associatedprotein; EDL, extensor digitorum longus; HSA, human ${alpha}$ -skeletalactin; NMJ, neuromuscular junction; nNOS, neuronal nitric oxidesynthase.

CiteULike

Complore

Connotea

Del.icio.us Add to Digg

Digg

Facebook

Technorati

Twitter What's this?

This article has been cited by other articles:

Li, D., Long, C., Yue, Y., Duan, D. (2009). Sub-physiological sarcoglycan expression contributes to compensatory muscle protection in mdx mice. Hum Mol Genet 18: 1209-1220 [Abstract] [Full Text]
Iwata, Y., Katanosaka, Y., Arai, Y., Shigekawa, M., Wakabayashi, S. (2009). Dominant-negative inhibition of Ca2+ influx via TRPV2 ameliorates muscular dystrophy in animal models. Hum Mol Genet 18: 824-834 [Abstract] [Full Text]
Inoue, A., Setoguchi, K., Matsubara, Y., Okada, K., Sato, N., Iwakura, Y., Higuchi, O., Yamanashi, Y. (2009). Dok-7 Activates the Muscle Receptor Kinase MuSK and Shapes Synapse Formation. Sci Signal 2: ra7-ra7 [Abstract] [Full Text]
Quinn, L. S., Anderson, B. G., Strait-Bodey, L., Stroud, A. M., Argiles, J. M. (2009). Oversecretion of interleukin-15 from skeletal muscle reduces adiposity. Am. J. Physiol. Endocrinol. Metab. 296: E191-E202 [Abstract] [Full Text]
Steen, M. S., Adams, M. E., Tesch, Y., Froehner, S. C. (2009). Amelioration of Muscular Dystrophy by Transgenic Expression of Niemann-Pick C1. Mol. Biol. Cell 20: 146-152 [Abstract] [Full Text]
Banks, G. B., Combs, A. C., Chamberlain, J. R., Chamberlain, J. S. (2008). Molecular and cellular adaptations to chronic myotendinous strain injury in mdx mice expressing a truncated dystrophin. Hum Mol Genet 17: 3975-3986 [Abstract] [Full Text]
Peter, A. K., Marshall, J. L., Crosbie, R. H. (2008). Sarcospan reduces dystrophic pathology: stabilization of the utrophin-glycoprotein complex. JCB 183: 419-427 [Abstract] [Full Text]
Davis, J., Westfall, M. V., Townsend, D., Blankinship, M., Herron, T. J., Guerrero-Serna, G., Wang, W., Devaney, E., Metzger, J. M. (2008). Designing Heart Performance by Gene Transfer. Physiol. Rev. 88: 1567-1651 [Abstract] [Full Text]
Gavrilina, T. O., McGovern, V. L., Workman, E., Crawford, T. O., Gogliotti, R. G., DiDonato, C. J., Monani, U. R., Morris, G. E., Burghes, A. H.M. (2008). Neuronal SMN expression corrects spinal muscular atrophy in severe SMA mice while muscle-specific SMN expression has no phenotypic effect. Hum Mol Genet 17: 1063-1075 [Abstract] [Full Text]
Reynolds, J. G., McCalmon, S. A., Donaghey, J. A., Naya, F. J. (2008). Deregulated Protein Kinase A Signaling and Myospryn Expression in Muscular Dystrophy. J. Biol. Chem. 283: 8070-8074 [Abstract] [Full Text]
Quinn, L. S., Anderson, B. G., Plymate, S. R. (2007). Muscle-specific overexpression of the type 1 IGF receptor results in myoblast-independent muscle hypertrophy via PI3K, and not calcineurin, signaling. Am. J. Physiol. Endocrinol. Metab. 293: E1538-E1551 [Abstract] [Full Text]
Banks, G. B., Gregorevic, P., Allen, J. M., Finn, E. E., Chamberlain, J. S. (2007). Functional capacity of dystrophins carrying deletions in the N-terminal actin-binding domain. Hum Mol Genet 16: 2105-2113 [Abstract] [Full Text]
Rodino-Klapac, L. R., Chicoine, L. G., Kaspar, B. K., Mendell, J. R. (2007). Gene Therapy for Duchenne Muscular Dystrophy: Expectations and Challenges. Arch Neurol 64: 1236-1241 [Abstract] [Full Text]
Ryder, J. W., Lau, K. S., Kamm, K. E., Stull, J. T. (2007). Enhanced Skeletal Muscle Contraction with Myosin Light Chain Phosphorylation by a Calmodulin-sensing Kinase. J. Biol. Chem. 282: 20447-20454 [Abstract] [Full Text]
Peter, A. K., Miller, G., Crosbie, R. H. (2007). Disrupted mechanical stability of the dystrophin-glycoprotein complex causes severe muscular dystrophy in sarcospan transgenic mice. J. Cell Sci. 120: 996-1008 [Abstract] [Full Text]
Vandebrouck, A., Sabourin, J., Rivet, J., Balghi, H., Sebille, S., Kitzis, A., Raymond, G., Cognard, C., Bourmeyster, N., Constantin, B. (2007). Regulation of capacitative calcium entries by {alpha}1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of {alpha}1-syntrophin. FASEB J. 21: 608-617 [Abstract] [Full Text]
Duan, D. (2006). Challenges and opportunities in dystrophin-deficient cardiomyopathy gene therapy. Hum Mol Genet 15: R253-R261 [Abstract] [Full Text]
Garvey, S. M., Miller, S. E., Claflin, D. R., Faulkner, J. A., Hauser, M. A. (2006). Transgenic mice expressing the myotilin T57I mutation unite the pathology associated with LGMD1A and MFM. Hum Mol Genet 15: 2348-2362 [Abstract] [Full Text]
Mercado, M. L., Amenta, A. R., Hagiwara, H., Rafii, M. S., Lechner, B. E., Owens, R. T., McQuillan, D. J., Froehner, S. C., Fallon, J. R. (2006). Biglycan regulates the expression and sarcolemmal localization of dystrobrevin, syntrophin, and nNOS. FASEB J. 20: 1724-1726 [Abstract] [Full Text]
Anderson, J. E. (2006). The satellite cell as a companion in skeletal muscle plasticity: currency, conveyance, clue, connector and colander. J. Exp. Biol. 209: 2276-2292 [Abstract] [Full Text]
Li, S., Kimura, E., Ng, R., Fall, B. M., Meuse, L., Reyes, M., Faulkner, J. A., Chamberlain, J. S. (2006). A highly functional mini-dystrophin/GFP fusion gene for cell and gene therapy studies of Duchenne muscular dystrophy. Hum Mol Genet 15: 1610-1622 [Abstract] [Full Text]
Judge, L. M., Haraguchiln, M., Chamberlain, J. S. (2006). Dissecting the signaling and mechanical functions of the dystrophin-glycoprotein complex. J. Cell Sci. 119: 1537-1546 [Abstract] [Full Text]
Hanft, L. M., Rybakova, I. N., Patel, J. R., Rafael-Fortney, J. A., Ervasti, J. M. (2006). Cytoplasmic {gamma}-actin contributes to a compensatory remodeling response in dystrophin-deficient muscle. Proc. Natl. Acad. Sci. USA 103: 5385-5390 [Abstract] [Full Text]
Maguy, A., Hebert, T. E., Nattel, S. (2006). Involvement of lipid rafts and caveolae in cardiac ion channel function. Cardiovasc Res 69: 798-807 [Abstract] [Full Text]
Lovering, R. M, Porter, N. C, Bloch, R. J (2005). The Muscular Dystrophies: From Genes to Therapies. ptjournal 85: 1372-1388 [Abstract] [Full Text]
Nerbonne, J. M., Kass, R. S. (2005). Molecular Physiology of Cardiac Repolarization. Physiol. Rev. 85: 1205-1253 [Abstract] [Full Text]
Albert, Y., Whitehead, J., Eldredge, L., Carter, J., Gao, X., Tourtellotte, W. G. (2005). Transcriptional regulation of myotube fate specification and intrafusal muscle fiber morphogenesis. JCB 169: 257-268 [Abstract] [Full Text]
Srivastava, S., Moraes, C. T. (2005). Double-strand breaks of mouse muscle mtDNA promote large deletions similar to multiple mtDNA deletions in humans. Hum Mol Genet 14: 893-902 [Abstract] [Full Text]
Lapidos, K. A., Kakkar, R., McNally, E. M. (2004). The Dystrophin Glycoprotein Complex: Signaling Strength and Integrity for the Sarcolemma. Circ. Res. 94: 1023-1031 [Abstract] [Full Text]
Ishikawa-Sakurai, M., Yoshida, M., Imamura, M., Davies, K. E., Ozawa, E. (2004). ZZ domain is essentially required for the physiological binding of dystrophin and utrophin to {beta}-dystroglycan. Hum Mol Genet 13: 693-702 [Abstract] [Full Text]
Kent, M. P., Spencer, M. J., Koohmaraie, M. (2004). Postmortem proteolysis is reduced in transgenic mice overexpressing calpastatin. J ANIM SCI 82: 794-801 [Abstract] [Full Text]
Abmayr, S., Crawford, R.W., Chamberlain, J.S. (2004). Characterization of ARC, apoptosis repressor interacting with CARD, in normal and dystrophin-deficient skeletal muscle. Hum Mol Genet 13: 213-221 [Abstract] [Full Text]
Grady, R. M., Akaaboune, M., Cohen, A. L., Maimone, M. M., Lichtman, J. W., Sanes, J. R. (2003). Tyrosine-phosphorylated and nonphosphorylated isoforms of {alpha}-dystrobrevin: roles in skeletal muscle and its neuromuscular and myotendinous junctions. JCB 160: 741-752 [Abstract] [Full Text]
Tidball, J. G, Spencer, M. J (2002). Expression of a calpastatin transgene slows muscle wasting and obviates changes in myosin isoform expression during murine muscle disuse. J. Physiol. 545: 819-828 [Abstract] [Full Text]
Chamberlain, J. S. (2002). Gene therapy of muscular dystrophy. Hum Mol Genet 11: 2355-2362 [Abstract] [Full Text]
DelloRusso, C., Scott, J. M., Hartigan-O'Connor, D., Salvatori, G., Barjot, C., Robinson, A. S., Crawford, R. W., Brooks, S. V., Chamberlain, J. S. (2002). Functional correction of adult mdx mouse muscle using gutted adenoviral vectors expressing full-length dystrophin. Proc. Natl. Acad. Sci. USA 99: 12979-12984 [Abstract] [Full Text]
Harper, S. Q., Crawford, R. W., DelloRusso, C., Chamberlain, J. S. (2002). Spectrin-like repeats from dystrophin and {alpha}-actinin-2 are not functionally interchangeable. Hum Mol Genet 11: 1807-1815 [Abstract] [Full Text]
Ehmsen, J., Poon, E., Davies, K. (2002). The dystrophin-associated protein complex. J. Cell Sci. 115: 2801-2803 [Full Text]
Spencer, M. J., Guyon, J. R., Sorimachi, H., Potts, A., Richard, I., Herasse, M., Chamberlain, J., Dalkilic, I., Kunkel, L. M., Beckmann, J. S. (2002). Stable expression of calpain 3 from a muscle transgene in vivo: Immature muscle in transgenic mice suggests a role for calpain 3 in muscle maturation. Proc. Natl. Acad. Sci. USA 99: 8874-8879 [Abstract] [Full Text]
Warner, L. E., DelloRusso, C., Crawford, R. W., Rybakova, I. N., Patel, J. R., Ervasti, J. M., 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 [Abstract] [Full Text]
Blake, D. J., Weir, A., Newey, S. E., Davies, K. E. (2002). Function and Genetics of Dystrophin and Dystrophin-Related Proteins in Muscle. Physiol. Rev. 82: 291-329 [Abstract] [Full Text]
Crawford, G. E., Lu, Q. L., Partridge, T. A., Chamberlain, J. S. (2001). Suppression of revertant fibers in mdx mice by expression of a functional dystrophin. Hum Mol Genet 10: 2745-2750 [Abstract] [Full Text]
Chamberlain, J. S. (2000). Muscular Dystrophy Meets the Gene Chip: New Insights into Disease Pathogenesis. JCB 151: F43-F46 [Full Text]
Benson, M. A., Newey, S. E., Martin-Rendon, E., Hawkes, R., Blake, D. J. (2001). Dysbindin, a Novel Coiled-coil-containing Protein That Interacts with the Dystrobrevins in Muscle and Brain. J. Biol. Chem. 276: 24232-24241 [Abstract] [Full Text]
Sweeney, H. L., Barton, E. R. (2000). The dystrophin-associated glycoprotein complex: What parts can you do without?. Proc. Natl. Acad. Sci. USA 97: 13464-13466 [Full Text]