Biopolym. Cell. 2011; 27(6):423-431.
Reviews
Phenotypes of the Drosophila melanogaster caused by dysfunction of dystrophin and dystroglycan
- Ivan Franko National University of L'viv
4, Hrushevskoho Str., Lviv, Ukraine, 79005
Abstract
Dystrophin and dystroglycan, the main components of the dystrophin-glycoprotein complex, are essential for normal vital activity of the D. melanogaster during ontogenesis. Mutations in the genes, which encode these proteins, cause different phenotypes, among manifes- tations of which we noticed characters similar to those observed at human muscular dystrophy. Furthermore, several other phenotypes have beendescribed; their study will shed light on our understanding the development of different pathologies. In addition, it gives an opportunity to reveal new components of the dystrophin-glycoprotein complex as well as new regulatory proteins, which influence the functions of this complex. Thus, based on the D. melanogaster, an appropriate model has been developed to study human myopathies.
Keywords: Drosophila melanogaster, Dystrophin-Glycoprotein complex, muscular dystrophies, dystrophin (dystroglycan) expression
Full text: (PDF, in Ukrainian)
References
[1]
Davies K. E., Nowak K. J. Molecular mechanisms of muscular dystrophies: old and new players Nat. Rev. Mol. Cell Biol 2006 7, N 10 P. 762–773.
[2]
Matsumura K., Campbell K. P. Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies Muscle Nerve 1994 17, N 1 P. 2–15.
[3]
Rando T. A. The dystrophin-glycoprotein complex, cellular signaling, and the regulation of cell survival in the muscular dystrophies Muscle Nerve 2001 24, N 12 P. 1575–1594.
[4]
Durbeej M., Campbell K. P. Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models Curr. Opin. Genet. Dev 2002 12, N 3 P. 349–361.
[5]
Lapidos K. A., Kakkar R., McNally E. M. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma Circ. Res 2004 94, N 8 P. 1023–1031.
[6]
Hoffman E. P., Brown R. H. Jr., Kunkel L. M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus Cell 1987 51, N 6 P. 919–928.
[7]
Blake D. J., Weir A., Newey S. E., Davies K. E. Function and genetics of dystrophin and dystrophin-related proteins in muscle Physiol. Rev 2002 82, N 2 P. 291–329.
[8]
Bennett R. R., den Dunnen J., O'Brien K. F., Darras B. T., Kunkel L. M. Detection of mutations in the dystrophin gene via automated DHPLC screening and direct sequencing BMC Genet 2001 2, N 1 P. 17.
[9]
Byers T. J., Lidov H. G., Kunkel L. M. An alternative dystrophin transcript specific to peripheral nerve Nat. Genet 1993 4, N 1 P. 77–81.
[10]
Allamand V., Campbell K. P. Animal models for muscular dystrophy: valuable tools for the development of therapies Hum. Mol. Genet 2000 9, N 16 P. 2459–2467.
[11]
Godfrey C., Clement E., Mein R., Brockington M., Smith J., Talim B., Straub V., Robb S., Quinlivan R., Feng L., JimenezMallebrera C., Mercuri E., Manzur A.Y., Kinali M., Torelli S., Brown S.C., Sewry C.A., Bushby K., Topaloglu H., North K., Abbs S., Muntoni F. Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan Brain 2007 130, N 10 P. 2725–2735.
[12]
Barresi R., Campbell K. P. Dystroglycan: from biosynthesis to pathogenesis of human disease J. Cell Sci 2006 119, N 2 P. 199–207.
[13]
Willmann R., Possekel S., Dubach-Powell J., Meier T., Ruegg M. A. Mammalian animal models for Duchenne muscular dystrophy Neuromuscul. Disord 2009 19, N 4 P. 241–249.
[14]
Collins C. A., Morgan J. E. Duchenne's muscular dystrophy: animal models used to investigate pathogenesis and develop therapeutic strategies Int. J. Exp. Pathol 2003 84, N 4 P. 165–172.
[15]
Nowak K. J., Davies K. E. Duchenne muscular dystrophy and dystrophin: pathogenesis and opportunities for treatment EMBO Rep 2004 5, N 9 P. 872–876.
[16]
Nakamura A., Takeda S. Mammalian models of Duchenne Muscular Dystrophy: pathological characteristics and therapeutic applications J. Biomed. Biotechnol 2011 2011 Article ID 184393, 8 pages.
[17]
Bessou C., Giugia J. B., Franks C. J., Holden-Dye L., Segalat L. Mutations in the Caenorhabditis elegans dystrophin-like gene dys-1 lead to hyperactivity and suggest a link with cholinergic transmission Neurogenetics 1998 2, N 1 P. 61–72.
[18]
Pilgram G. S., Potikanond S., Baines R. A., Fradkin L. G., Noordermeer J. N. The roles of the dystrophin-associated glycoprotein complex at the synapse Mol. Neurobiol 2010 41, N 1 P. 1–21.
[19]
Bassett D., Currie P. D. Identification of a zebrafish model of muscular dystrophy Clin. Exp. Pharmacol. Physiol 2004 31, N 8 P. 537–540.
[20]
Greener M. J., Roberts R. G. Conservation of components of the dystrophin complex in Drosophila FEBS Lett 2000 482, N 1–2 P. 13–18.
[21]
Neuman S., Kovalio M., Yaffe D., Nudel U. The Drosophila homologue of the dystrophin gene – introns containing promoters are the major contributors to the large size of the gene FEBS Lett 2005 579, N 24 P. 5365–5371.
[22]
Deng W. M., Schneider M., Frock R., Castillejo-Lopez C., Gaman E. A., Baumgartner S., Ruohola-Baker H. Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila Development 2003 130, N 1 P. 173–184.
[23]
Huang X., Poy F., Zhang R., Joachimiak A., Sudol M., Eck M. J. Structure of a WW domain containing fragment of dystrophin in complex with beta-dystroglycan Nat. Struct. Biol 2000 7, N 8 P. 634–638.
[24]
Shcherbata H. R., Yatsenko A. S., Patterson L., Sood V. D., Nudel U., Yaffe D., Baker D., Ruohola-Baker H. Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy EMBO J 2007 26, N 2 P. 481–493.
[25]
Yatsenko A. S., Gray E. E., Shcherbata H. R., Patterson L. B., Sood V. D., Kucherenko M. M., Baker D., Ruohola-Baker H. A putative Src homology 3 domain binding motif but not the C-terminal dystrophin WW domain binding motif is required for dystroglycan function in cellular polarity in Drosophila J. Biol. Chem 2007 282, N 20 P. 15159–15169.
[26]
Dekkers L. C., van der Plas M. C., van Loenen P. B., den Dunnen J. T., van Ommen G. J., Fradkin L. G., Noordermeer J. N. Embryonic expression patterns of the Drosophila dystrophin-associated glycoprotein complex orthologs Gene Expr. Patterns 2004 4, N 2 P. 153–159.
[27]
van der Plas M. C., Pilgram G. S., Plomp J. J., de Jong A., Fradkin L. G., Noordermeer J. N. Dystrophin is required for appropriate retrograde control of neurotransmitter release at the Drosophila neuromuscular junction J. Neurosci 2006 26, N 1 P. 333–344.
[28]
van der Plas M. C., Pilgram G. S., de Jong A. W., Bansraj M. R., Fradkin L. G., Noordermeer J. N. Drosophila Dystrophin is required for integrity of the musculature Mech. Dev 2007 124, N 7–8 P. 617–630.
[29]
Neuman S., Kaban A., Volk T., Yaffe D., Nudel U. The dystrophin/utrophin homologues in Drosophila and in sea urchin Gene 2001 263, N 1–2 P. 17–29.
[30]
Schneider M., Khalil A. A., Poulton J., Castillejo-Lopez C., Egger-Adam D., Wodarz A., Deng W. M., Baumgartner S. Perlecan and Dystroglycan act at the basal side of the Drosophila follicular epithelium to maintain epithelial organization Development 2006 133, N 19 P. 3805–3815.
[31]
Yatsenko A. S., Kucherenko M. M., Pantoja M., Fischer K. A., Madeoy J., Deng W. M., Schneider M., Baumgartner S., Akey J., Shcherbata H. R., Ruohola-Baker H. The conserved WW-domain binding sites in Dystroglycan C-terminus are essential but partially redundant for Dystroglycan function BMC Dev. Biol 2009 9 P. 18.
[32]
Bogdanik L., Framery B., Frolich A., Franco B., Mornet D., Bockaert J., Sigrist S. J., Grau Y., Parmentier M. L. Muscle dystroglycan organizes the postsynapse and regulates presynaptic neurotransmitter release at the Drosophila neuromuscular junction PLoS One 2008 3, N 4 e2084.
[33]
Fradkin L. G., Baines R. A., van der Plas M. C., Noordermeer J. N. The dystrophin Dp186 isoform regulates neurotransmitter release at a central synapse in Drosophila J. Neurosci 2008 28, N 19 P. 5105–5114.
[34]
Taghli-Lamallem O., Akasaka T., Hogg G., Nudel U., Yaffe D., Chamberlain J. S., Ocorr K., Bodmer R. Dystrophin deficiency in Drosophila reduces lifespan and causes a dilated cardiomyopathy phenotype Aging Cell 2008 7, N 2 P. 237–249.
[35]
Kucherenko M. M., Marrone A. K., Rishko V. M., Magliarelli H. de F., Shcherbata H. R. Stress and muscular dystrophy: a genetic screen for dystroglycan and dystrophin interactors in Drosophila identifies cellular stress response components Dev. Biol 2011 352, N 2 P. 228–242.
[36]
Mirouse V., Christoforou C. P., Fritsch C., St Johnston D., Ray R. P. Dystroglycan and perlecan provide a basal cue required for epithelial polarity during energetic stress Dev. Cell 2009 16, N 1 P. 83–92.
[37]
Grady R. M., Merlie J. P., Sanes J. R. Subtle neuromuscular defects in utrophin-deficient mice J. Cell. Biol 1997 136, N 4 P. 871–882.
[38]
Grady R. M., Zhou H., Cunningham J. M., Henry M. D., Campbell K. P., Sanes J. R. Maturation and maintenance of the neuromuscular synapse: genetic evidence for roles of the dystrophin– glycoprotein complex Neuron 2000 25, N 2 P. 279–293.
[39]
Wairkar Y. P., Fradkin L. G., Noordermeer J. N., DiAntonio A. Synaptic defects in a Drosophila model of congenital muscular dystrophy J. Neurosci 2008 28, N 14 P. 3781–3789.
[40]
Haines N., Seabrooke S., Stewart B. A. Dystroglycan and protein O-mannosyltransferases 1 and 2 are required to maintain integrity of Drosophila larval muscles Mol. Biol Cell 2007 18, N 12 P. 4721–4730.
[41]
Takeuchi K., Nakano Y., Kato U., Kaneda M., Aizu M., Awano W., Yonemura S., Kiyonaka S., Mori Y., Yamamoto D., Umeda M. Changes in temperature preferences and energy homeostasis in dystroglycan mutants Science 2009 323, N 5922 P. 1740– 1743.
[42]
Rishko V., Poberezhnyk O., Kucherenko M., Holub N., Maksymiv D., Chernyk Ya. The influence of Dad and tkv genes on dystrophin-deficient phenotype in Drosophila melanogaster Visnyk of Lviv Univ. Biology series 2009 51 P. 55–62.
[43]
Christoforou C. P., Greer C. E., Challoner B. R., Charizanos D., Ray R. P. The detached locus encodes Drosophila Dystrophin, which acts with other components of the Dystrophin Associated Protein Complex to influence intercellular signalling in developing wing veins Dev. Biol 2008 313, N 2 P. 519–532.
[44]
Kucherenko M. M., Pantoja M., Yatsenko A. S., Shcherbata H. R., Fischer K. A., Maksymiv D. V., Chernyk Y. I., RuoholaBaker H. Genetic modifier screens reveal new components that interact with the Drosophila dystroglycan-dystrophin complex PLoS One 2008 3, N 6 e2418.
[45]
Kucherenko M., Yatsenko A., Ruohola-Baker H., Maksymiv D., Chernyk Ya. Drosophila melanogaster as a model system for searching of the Dystrophin-Dystroglycan Complex modiefiers Visnyk of Lviv Univ. Biology series 2008 46 P. 71–77.
[46]
Bridges C. B., Brehme K. F. The mutants of Drosophila melanogaster Washington: Carnegie Inst. Publ., 1944 Vol. 552 257 p.
[47]
Sturtevant M. A., Bier E. Analysis of the genetic hierarchy guiding wing vein development in Drosophila Development 1995 121, N 3 P. 785–801.
[48]
Zhan Y., Melian N. Y., Pantoja M., Haines N., Ruohola-Baker H., Bourque C. W., Rao Y., Carbonetto S. Dystroglycan and mitochondrial ribosomal protein l34 regulate differentiation in the Drosophila eye PLoS One 2010 5, N 5 e10488.