Duchenne muscular dystrophy drug discovery – the application of utrophin promoter activation screening

Bibliography

• Engel AG, Franzini-Armstrong C. Myology: basic and clinical. 3rd edition. Columbus, OH, Oxford; 1960
   Google Scholar
• Mendell JR, Shilling C, Leslie ND, Evidence-based path to newborn screening for duchenne muscular dystrophy. Ann Neurol 2012;71:304-13
   PubMed Web of Science ®Google Scholar
• Emery AE, Muntoni F. Duchenne muscular dystrophy. Oxford University Press, Oxford; 2003
   Google Scholar
• Hoffman EP, Brown RH Jr, Kunkel LM. Dystrophin: the protein product of the duchenne muscular dystrophy locus. Cell 1987;51:919-28
   PubMed Web of Science ®Google Scholar
• Kunkel LM; co-authors. Analysis of deletions in DNA from patients with Becker and Duchenne muscular dystrophy. Nature 1986;322:73-7
   PubMed Web of Science ®Google Scholar
• Monaco AP, Neve RL, Colletti-Feener C, Isolation of candidate cDNAs for portions of the duchenne muscular dystrophy gene. Nature 1986;323:646-50
   PubMed Web of Science ®Google Scholar
• Burghes AH, Logan C, Hu X, A cDNA clone from the Duchenne/Becker muscular dystrophy gene. Nature 1987;328:434-7
   PubMed Web of Science ®Google Scholar
• Cross GS, Speer A, Rosenthal A, Deletions of fetal and adult muscle cDNA in Duchenne and Becker muscular dystrophy patients. EMBO J 1987;6:3277-83
   PubMed Web of Science ®Google Scholar
• Durbeej M, Campbell KP. Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev 2002;12:349-61
   PubMed Web of Science ®Google Scholar
• Brown RH Jr, Hoffman EP. Molecular biology of duchenne muscular dystrophy. Trends Neurosci 1988;11:480-4
   PubMed Web of Science ®Google Scholar
• Kohler M, Clarenbach CF, Bahler C, Disability and survival in duchenne muscular dystrophy. J Neurol Neurosurg Psychiatry 2009;80:320-5
   PubMed Web of Science ®Google Scholar
• Bowles DE, McPhee S.W.J, Li C, Phase 1 gene therapy for duchenne muscular dystrophy using a translational optimized AAV vector. Mol Ther 2012;20:443-55
   PubMed Web of Science ®Google Scholar
• Cirak S, Feng L, Anthony K, Restoration of the dystrophin-associated glycoprotein complex after exon skipping therapy in duchenne muscular dystrophy. Mol Ther 2012;20:462-7
   PubMed Web of Science ®Google Scholar
• Hirawat S, Welch EM, Elfring GL, Safety, tolerability, and pharmacokinetics of PTC124, a nonaminoglycoside nonsense mutation suppressor, following single- and multiple-dose administration to healthy male and female adult volunteers. J Clin Pharmacol 2007;47:430-44
   PubMed Web of Science ®Google Scholar
• Clinicaltrials.gov. NIH. 2012. Available from: http://clinicaltrials.gov/ct2/results?term=duchenne+muscular+dystrophy&Search=Search [Last accessed 2012]
   Google Scholar
• Khurana TS, Davies KE. Pharmacological strategies for muscular dystrophy. Nat Rev Drug Discov 2003;2:379-90
   PubMed Web of Science ®Google Scholar
• Perkins KJ, Davies KE. Recent advances in duchenne muscular dystrophy. Degenerat Neurol Neuromus Dis 2012;2:141-64
   Google Scholar
• Pichavant C, Aartsma-Rus A, Clemens PR, Current status of pharmaceutical and genetic therapeutic approaches to treat DMD. Mol Ther 2011;19:830-40
   PubMed Web of Science ®Google Scholar
• Partridge TA. Impending therapies for duchenne muscular dystrophy. Curr Opin Neurol 2011;24:415-22
   PubMed Web of Science ®Google Scholar
• Hoffman EP, Bronson A, Levin AA, Restoring dystrophin expression in duchenne muscular dystrophy muscle progress in exon skipping and stop codon read through. Am J Pathol 2011;179:12-22
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A. Overview on DMD exon skipping. Methods Mol Biol 2012;867:97-116
   PubMedGoogle Scholar
• Meregalli M, Farini A, Parolini D, Stem cell therapies to treat muscular dystrophy: progress to date. BioDrugs 2010;24:237-47
   PubMed Web of Science ®Google Scholar
• Love DR, Hill DF, Dickson G, An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 1989;339:55-8
   PubMed Web of Science ®Google Scholar
• Khurana TS, Hoffman EP, Kunkel LM. Identification of a chromosome 6-encoded dystrophin-related protein. J Biol Chem 1990;265:16717-20
   PubMed Web of Science ®Google Scholar
• Tinsley JM, Blake DJ, Roche A, Primary structure of dystrophin-related protein. Nature 1992;360:591-3
   PubMed Web of Science ®Google Scholar
• Koenig M, Monaco AP, Kunkel LM. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 1988;53:219-28
   PubMed Web of Science ®Google Scholar
• Winder SJ, Hemmings L, Maciver SK, Utrophin actin binding domain: analysis of actin binding and cellular targeting. J Cell Sci 1995;108:63-71
   PubMed Web of Science ®Google Scholar
• Rybakova IN, Patel JR, Davies KE, Utrophin binds laterally along actin filaments and can couple costameric actin with sarcolemma when overexpressed in dystrophin-deficient muscle. Mol Biol Cell 2002;13:1512-21
   PubMed Web of Science ®Google Scholar
• Matsumura K, Ervasti JM, Ohlendieck K, Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature 1992;360:588-91
   PubMed Web of Science ®Google Scholar
• Prochniewicz E, Henderson D, Ervasti JM, Dystrophin and utrophin have distinct effects on the structural dynamics of actin. Proc Nat Acad Sci 2009;106:7822-7
   PubMed Web of Science ®Google Scholar
• Lin AY, Prochniewicz E, Henderson DM, Impacts of dystrophin and utrophin domains on actin structural dynamics: implications for therapeutic design. J Mol Biol 2012;420:87-98
   PubMed Web of Science ®Google Scholar
• Ishikawa-Sakurai M, Yoshida M, Imamura M, ZZ domain is essentially required for the physiological binding of dystrophin and utrophin to beta-dystroglycan. Hum Mol Genet 2004;13:693-702
   PubMed Web of Science ®Google Scholar
• Puttini S, Lekka M, Dorchies OM, Gene-mediated restoration of normal myofiber elasticity in dystrophic muscles. Mol Ther 2008;17:19-25
   PubMed Web of Science ®Google Scholar
• Khurana TS, Watkins SC, Chafey P, Immunolocalization and developmental expression of dystrophin related protein in skeletal muscle. Neuromuscul Disord 1991;1:185-94
   PubMedGoogle Scholar
• Nguyen TM, Ellis JM, Love DR, Localization of the DMDL gene-encoded dystrophin-related protein using a panel of nineteen monoclonal 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 1991;115:1695-700
   PubMed Web of Science ®Google Scholar
• Takemitsu M, Ishiura S, Koga R, Dystrophin-related protein in the fetal and denervated skeletal muscles of normal and mdx mice. Biochem Biophys Res Commun 1991;180:1179-86
   PubMed Web of Science ®Google Scholar
• Tanaka H, Ishiguro T, Eguchi C, Expression of a dystrophin-related protein associated with the skeletal muscle cell membrane. Histochemistry 1991;96:1-5
   PubMedGoogle Scholar
• Deconinck N, Tinsley J, De Backer F, Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat Med 1997;3:1216-21
   PubMed Web of Science ®Google Scholar
• Gilbert R, Nalbanoglu J, Tinsley JM, Efficient utrophin expression following adenovirus gene transfer in dystrophic muscle. Biochem Biophys Res Commun 1998;242:244-7
   PubMed Web of Science ®Google Scholar
• Rafael JA, Tinsley JM, Potter AC, Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nat Genet 1998;19:79-82
   PubMed Web of Science ®Google Scholar
• Tinsley J, Deconinck N, Fisher R, Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 1998;4:1441-4
   PubMed Web of Science ®Google Scholar
• Goudemant JF, Deconinck N, Tinsley JM, Expression of truncated utrophin improves pH recovery in exercising muscles of dystrophic mdx mice: a 31P NMR study. Neuromuscul Disord 1998;8:371-9
   PubMed Web of Science ®Google Scholar
• Gilbert R, Nalbantoglu J, Petrof BJ, Adenovirus-mediated utrophin gene transfer mitigates the dystrophic phenotype of mdx mouse muscles. Hum Gene Ther 1999;10:1299-310
   PubMed Web of Science ®Google Scholar
• Wakefield PM, Tinsley JM, Wood MJ, Prevention of the dystrophic phenotype in dystrophin/utrophin-deficient muscle following adenovirus-mediated transfer of a utrophin minigene. Gene Ther 2000;7:201-4
   PubMed Web of Science ®Google Scholar
• Cerletti M, Negri T, Cozzi F, Dystrophic phenotype of canine X-linked muscular dystrophy is mitigated by adenovirus-mediated utrophin gene transfer. Gene Ther 2003;10:750-7
   PubMed Web of Science ®Google Scholar
• Odom GL, Gregorevic P, Allen JM, Microutrophin delivery through rAAV6 increases lifespan and improves muscle function in dystrophic dystrophin/utrophin-deficient mice. Mol Ther 2008;16:1539-45
   PubMed Web of Science ®Google Scholar
• Call JA, Ervasti JM, Lowe DA. TAT-mu Utrophin mitigates the pathophysiology of dystrophin and utrophin double-knockout mice. J Appl Physiol 2011;111:200-5
   PubMed Web of Science ®Google Scholar
• Sonnemann KJ, Heun-Johnson H, Turner AJ, Functional substitution by TAT-utrophin in dystrophin-deficient mice. PLoS Med 2009;6:e1000083
   PubMed Web of Science ®Google Scholar
• Fisher R, Tinsley JM, Phelps SR, Non-toxic ubiquitous over-expression of utrophin in the mdx mouse. Neuromuscul Disord 2001;11:713-21
   PubMed Web of Science ®Google Scholar
• Ohlendieck K, Ervasti JM, Matsumura K, Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron 1991;7:499-508
   PubMed Web of Science ®Google Scholar
• Pearce M, Blake DJ, Tinsley JM, The utrophin and dystrophin genes share similarities in genomic structure. Hum Mol Genet 1993;2:1765-72
   PubMed Web of Science ®Google Scholar
• Burton EA, Tinsley JM, Holzfeind PJ, A second promoter provides an alternative target for therapeutic up-regulation of utrophin in duchenne muscular dystrophy. Proc Natl Acad Sci USA 1999;96:14025-30
   PubMed Web of Science ®Google Scholar
• Galvagni F, Oliviero S. Utrophin transcription is activated by an intronic enhancer. J Biol Chem 2000;275:3168-72
   PubMed Web of Science ®Google Scholar
• Weir AP, Burton EA, Harrod G, A- and B-utrophin have different expression patterns and are differentially up-regulated in mdx muscle. J Biol Chem 2002;277:45285-90
   PubMed Web of Science ®Google Scholar
• Dennis CL, Tinsley JM, Deconinck AE, Molecular and functional analysis of the utrophin promoter. Nucleic Acids Res 1996;24:1646-52
   PubMed Web of Science ®Google Scholar
• Takahashi J, Itoh Y, Fujimori K, The utrophin promoter A drives high expression of the transgenic LacZ gene in liver, testis, colon, submandibular gland, and small intestine. J Gene Med 2005;7:237-48
   PubMed Web of Science ®Google Scholar
• Stocksley MA, Chakkalakal JV, Bradford A, A 1.3 kb promoter fragment confers spatial and temporal expression of utrophin A mRNA in mouse skeletal muscle fibers. Neuromuscul Disord 2005;15:437-49
   PubMed Web of Science ®Google Scholar
• Perkins KJ, Burton EA, Davies KE. The role of basal and myogenic factors in the transcriptional activation of utrophin promoter A: implications for therapeutic up-regulation in Duchenne muscular dystrophy. Nucleic Acids Res 2001;29:4843-50
   PubMed Web of Science ®Google Scholar
• Gramolini AO, Dennis CL, Tinsley JM, Local transcriptional control of utrophin expression at the neuromuscular synapse. J Biol Chem 1997;272:8117-20
   PubMed Web of Science ®Google Scholar
• Gramolini AO, Burton EA, Tinsley JM, Muscle and neural isoforms of agrin increase utrophin expression in cultured myotubes via a transcriptional regulatory mechanism. J Biol Chem 1998;273:736-43
   PubMed Web of Science ®Google Scholar
• Gramolini AO, Angus LM, Schaeffer L, Induction of utrophin gene expression by heregulin in skeletal muscle cells: role of the N-box motif and GA binding protein. Proc Natl Acad Sci USA 1999;96:3223-7
   PubMed Web of Science ®Google Scholar
• Khurana TS, Rosmarin AG, Shang J, Activation of utrophin promoter by heregulin via the ets-related transcription factor complex GA-binding protein alpha/beta. Mol Biol Cell 1999;10:2075-86
   PubMed Web of Science ®Google Scholar
• Basu U, Gyrd-Hansen M, Baby SM, Heregulin-induced epigenetic regulation of the utrophin-A promoter. FEBS Lett 2007;581:4153-8
   PubMed Web of Science ®Google Scholar
• Perkins KJ, Basu U, Budak MT, Ets-2 repressor factor silences extrasynaptic utrophin by N-box mediated repression in skeletal muscle. Mol Biol Cell 2007;18:2864-72
   PubMed Web of Science ®Google Scholar
• Galvagni F, Capo S, Oliviero S. Sp1 and Sp3 physically interact and co-operate with GABP for the activation of the utrophin promoter. J Mol Biol 2001;306:985-96
   PubMed Web of Science ®Google Scholar
• Gyrd-Hansen M, Krag TO, Rosmarin AG, Sp1 and the ets-related transcription factor complex GABP alpha/beta functionally cooperate to activate the utrophin promoter. J Neurol Sci 2002;197:27-35
   PubMed Web of Science ®Google Scholar
• Rodova M, Brownback K, Werle MJ. Okadaic acid augments utrophin in myogenic cells. Neurosci Lett 2004;363:163-7
   PubMed Web of Science ®Google Scholar
• Gramolini AO, Belanger G, Jasmin BJ. Distinct regions in the 3' untranslated region are responsible for targeting and stabilizing utrophin transcripts in skeletal muscle cells. J Cell Biol 2001;154:1173-83
   PubMed Web of Science ®Google Scholar
• Gramolini AO, Belanger G, Thompson JM, Increased expression of utrophin in a slow vs. a fast muscle involves posttranscriptional events. Am J Physiol Cell Physiol 2001;281:C1300-9
   PubMed Web of Science ®Google Scholar
• Chakkalakal JV, Stocksley MA, Harrison MA, Expression of utrophin A mRNA correlates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signaling. Proc Natl Acad Sci USA 2003;100:7791-6
   PubMed Web of Science ®Google Scholar
• Miura P, Chakkalakal JV, Boudreault L, Pharmacological activation of PPARbeta/delta stimulates utrophin A expression in skeletal muscle fibers and restores sarcolemmal integrity in mature mdx mice. Hum Mol Genet 2009;18:4640-9
   PubMed Web of Science ®Google Scholar
• Chakkalakal JV, Harrison M.-A, Carbonetto S, Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice. Hum Mol Genet 2004;13:379-88
   PubMed Web of Science ®Google Scholar
• Angus LM, Chakkalakal JV, Mejat A, Calcineurin-NFAT signaling, together with GABP and peroxisome PGC-1{alpha}, drives utrophin gene expression at the neuromuscular junction. Am J Physiol Cell Physiol 2005;289:C908-17
   PubMed Web of Science ®Google Scholar
• Handschin C, Kobayashi YM, Chin S, PGC-1alpha regulates the neuromuscular junction program and ameliorates duchenne muscular dystrophy. Genes Dev 2007;21:770-83
   PubMed Web of Science ®Google Scholar
• Selsby JT, Morine KJ, Pendrak K, Rescue of dystrophic skeletal muscle by PGC-1alpha involves a fast to slow fiber type shift in the mdx mouse. PLoS One 2012;7:e30063
   PubMed Web of Science ®Google Scholar
• Bushby K, Finkel R, Birnkrant DJ, Diagnosis and management of duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol 2010;9:77-93
   PubMed Web of Science ®Google Scholar
• Moxley RT, Pandya S, Ciafaloni E, Change in natural history of duchenne muscular dystrophy with long-term corticosteroid treatment: implications for management. J Child Neurol 2010;25:1116-29
   PubMed Web of Science ®Google Scholar
• Courdier-Fruh I, Barman L, Briguet A, Glucocorticoid-mediated regulation of utrophin levels in human muscle fibers. Neuromuscul Disord 2002;12(Suppl 1):S95-104
   PubMed Web of Science ®Google Scholar
• St-Pierre SJ, Chakkalakal JV, Kolodziejczyk SM, Glucocorticoid treatment alleviates dystrophic myofiber pathology by activation of the calcineurin/NF-AT pathway. FASEB J 2004;18:1937-9
   PubMed Web of Science ®Google Scholar
• Bonet-Kerrache A, Fortier M, Comunale F, The GTPase RhoA increases utrophin expression and stability, as well as its localization at the plasma membrane. Biochem J 2005;391:261-8
   PubMed Web of Science ®Google Scholar
• Gauthier-Rouviere C, Bonet-Kerrache A. RhoA leads to up-regulation and relocalization of utrophin in muscle fibers. Biochem Biophys Res Commun 2009;384:322-8
   PubMed Web of Science ®Google Scholar
• Wang Q, Cao DH, Jin CL, A method of utrophin up-regulation through RNAi-mediated knockdown of the transcription factor EN1. J Int Med Res 2011;39:161-71
   PubMed Web of Science ®Google Scholar
• Perkins KJ, Davies KE. Ets, Ap-1 and GATA factor families regulate the utrophin B promoter: potential regulatory mechanisms for endothelial-specific expression. FEBS Lett 2003;538:168-72
   PubMed Web of Science ®Google Scholar
• Briguet A, Bleckmann D, Bettan M, Transcriptional activation of the utrophin promoter B by a constitutively active Ets-transcription factor. Neuromuscul Disord 2003;13:143-50
   PubMed Web of Science ®Google Scholar
• Galvagni F, Cantini M, Oliviero S. The utrophin gene is transcriptionally up-regulated in regenerating muscle. J Biol Chem 2002;277:19106-13
   PubMed Web of Science ®Google Scholar
• Tanihata J, Suzuki N, Miyagoe-Suzuki Y, Downstream utrophin enhancer is required for expression of utrophin in skeletal muscle. J Gene Med 2008;10:702-13
   PubMed Web of Science ®Google Scholar
• Gramolini AO, Karpati G, Jasmin BJ. Discordant expression of utrophin and its transcript in human and mouse skeletal muscles. J Neuropathol Exp Neurol 1999;58:235-44
   PubMed Web of Science ®Google Scholar
• Baby SM, Bogdanovich S, Willmann G, Differential expression of utrophin-A and -B promoters in the central nervous system (CNS) of normal and dystrophic mdx mice. Brain Pathol 2010;20:323-42
   PubMed Web of Science ®Google Scholar
• Miura P, Andrews M, Holcik M, IRES-mediated translation of utrophin A is enhanced by glucocorticoid treatment in skeletal muscle cells. PLoS One 2008;3:e2309
   PubMed Web of Science ®Google Scholar
• Miura P, Thompson J, Chakkalakal JV, The utrophin A 5'-untranslated region confers internal ribosome entry site-mediated translational control during regeneration of skeletal muscle fibers. J Biol Chem 2005;280:32997-3005
   PubMed Web of Science ®Google Scholar
• Basu U, Lozynska O, Moorwood C, Translational regulation of utrophin by miRNAs. PLoS One 2011;6:e29376
   PubMed Web of Science ®Google Scholar
• Rosenberg MI, Georges SA, Asawachaicharn A, MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J Cell Biol 2006;175:77-85
   PubMed Web of Science ®Google Scholar
• Kornegay JN, Bogan JR, Bogan DJ, Canine models of duchenne muscular dystrophy and their use in therapeutic strategies. Mamm Genome 2012;23:85-108
   PubMed Web of Science ®Google Scholar
• Nakamura A, Takeda S. Mammalian models of duchenne muscular Dystrophy: pathological characteristics and therapeutic applications. J Biomed Biotechnol 2011;2011:184393
   PubMedGoogle Scholar
• Willmann R, Possekel S, Dubach-Powell J, Mammalian animal models for duchenne muscular dystrophy. Neuromuscul Disord 2009;19:241-9
   PubMed Web of Science ®Google Scholar
• Bulfield G, Siller WG, Wight PA, X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 1984;81:1189-92
   PubMed Web of Science ®Google Scholar
• Sicinski P, Geng Y, Ryder-Cook AS, The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 1989;244:1578-80
   PubMed Web of Science ®Google Scholar
• Chapman VM, Miller DR, Armstrong D, Recovery of induced mutations for X chromosome-linked muscular dystrophy in mice. Proc Nat Acad Sci 1989;86:1292-6
   PubMed Web of Science ®Google Scholar
• Cox GA, Phelps SF, Chapman VM, New mdx mutation disrupts expression of muscle and nonmuscle isoforms of dystrophin. Nat Genet 1993;4:87-93
   PubMed Web of Science ®Google Scholar
• Im WB, Phelps SF, Copen EH, Differential expression of dystrophin isoforms in strains of mdx mice with different mutations. Hum Mol Genet 1996;5:1149-53
   PubMed Web of Science ®Google Scholar
• Deconinck AE, Rafael JA, Skinner JA, Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 1997;90:717-27
   PubMed Web of Science ®Google Scholar
• Grady RM, Teng H, Nichol MC, Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for duchenne muscular dystrophy. Cell 1997;90:729-38
   PubMed Web of Science ®Google Scholar
• Cooper BJ, Winand NJ, Stedman H, The homologue of the duchenne locus is defective in X-linked muscular dystrophy of dogs. Nature 1988;334:154-6
   PubMed Web of Science ®Google Scholar
• Sharp NJ, Kornegay JN, Van Camp SD, An error in dystrophin mRNA processing in golden retriever muscular dystrophy, an animal homologue of Duchenne muscular dystrophy. Genomics 1992;13:115-21
   PubMed Web of Science ®Google Scholar
• Squire S, Raymackers JM, Vandebrouck C, Prevention of pathology in mdx mice by expression of utrophin: analysis using an inducible transgenic expression system. Hum Mol Genet 2002;11:3333-44
   PubMed Web of Science ®Google Scholar
• Krag TO, Bogdanovich S, Jensen CJ, Heregulin ameliorates the dystrophic phenotype in mdx mice. Proc Natl Acad Sci USA 2004;101:13856-60
   PubMed Web of Science ®Google Scholar
• Ljubicic V, Miura P, Burt M, Chronic AMPK activation evokes the slow, oxidative myogenic program and triggers beneficial adaptations in mdx mouse skeletal muscle. Hum Mol Genet 2011;20:3478-93
   PubMed Web of Science ®Google Scholar
• Pauly M, Daussin F, Burelle Y, AMPK activation stimulates autophagy and ameliorates muscular dystrophy in the mdx mouse diaphragm. Am J Pathol 2012;181:583-92
   PubMed Web of Science ®Google Scholar
• Corbi N, Libri V, Fanciulli M, The artificial zinc finger coding gene 'Jazz' binds the utrophin promoter and activates transcription. Gene Ther 2000;7:1076-83
   PubMed Web of Science ®Google Scholar
• Desantis A, Onori A, Di Certo MG, Novel activation domain derived from Che-1 cofactor coupled with the artificial protein Jazz drives utrophin upregulation. Neuromuscul Disord 2009;19:158-62
   PubMed Web of Science ®Google Scholar
• Mattei E, Corbi N, Di Certo MG, Utrophin up-regulation by an artificial transcription factor in transgenic mice. PLoS One 2007;2:e774
   PubMedGoogle Scholar
• Onori A, Desantis A, Buontempo S, The artificial 4-zinc-finger protein Bagly binds human utrophin promoter A at the endogenous chromosomal site and activates transcription. Biochem Cell Biol 2007;85:358-65
   PubMed Web of Science ®Google Scholar
• Lu Y, Tian C, Danialou G, Targeting artificial transcription factors to the utrophin A promoter: effects on dystrophic pathology and muscle function. J Biol Chem 2008;283:34720-7
   PubMed Web of Science ®Google Scholar
• Chaubourt E, Fossier P, Baux G, Nitric oxide and l-arginine cause an accumulation of utrophin at the sarcolemma: a possible compensation for dystrophin loss in Duchenne muscular dystrophy. Neurobiol Dis 1999;6:499-507
   PubMed Web of Science ®Google Scholar
• Chaubourt E, Voisin V, Fossier P, The NO way to increase muscular utrophin expression? C R Acad Sci III 2000;323:735-40
   PubMed Web of Science ®Google Scholar
• Barton ER, Morris L, Kawana M, Systemic administration of L-arginine benefits mdx skeletal muscle function. Muscle Nerve 2005;32:751-60
   PubMed Web of Science ®Google Scholar
• Voisin V, Sebrie C, Matecki S, L-arginine improves dystrophic phenotype in mdx mice. Neurobiol Dis 2005;20:123-30
   PubMed Web of Science ®Google Scholar
• Chancellor DR, Davies KE, De Moor O, Discovery of 2-arylbenzoxazoles as upregulators of utrophin production for the treatment of Duchenne muscular dystrophy. J Med Chem 2011;54:3241-50
   PubMed Web of Science ®Google Scholar
• De Moor O, Dorgan CR, Johnson PD, Discovery and SAR of 2-arylbenzotriazoles and 2-arylindazoles as potential treatments for duchenne muscular dystrophy. Bioorg Med Chem Lett 2011;21:4828-31
   PubMed Web of Science ®Google Scholar
• Moorwood C, Lozynska O, Suri N, Drug discovery for duchenne muscular dystrophy via utrophin promoter activation screening. PLoS One 2011;6:e26169
   PubMed Web of Science ®Google Scholar
• Tinsley JM, Fairclough RJ, Storer R, Daily treatment with SMTC1100, a novel small molecule utrophin upregulator, dramatically reduces the dystrophic symptoms in the mdx mouse. PLoS One 2011;6:e19189
   PubMed Web of Science ®Google Scholar
• BioMarin announces results for phase 1 clinical study of BMN 195 for duchenne muscular dystrophy. BioMarin. 2010. Available from: http://phx.corporate-ir.net/phoenix.zhtml?c=106657&p=irol-newsArticle&ID=1455247&highlight [Last accessed 2012]
   Google Scholar
• Tinsley J, Fairclough RJ, Storer R, SMT C1100: A potential breakthrough treatment for Duchenne Muscular Dystrophy (DMD). 17th International Congress of the World Muscle Society. Perth, Western Australia; 2012
   Google Scholar
• Gordon BS, Delgado Diaz DC, Kostek MC. Resveratrol decreases inflammation and increases utrophin gene expression in the mdx mouse model of duchenne muscular dystrophy. Clin Nutr 2012
   PubMed Web of Science ®Google Scholar
• Chakkalakal JV, Miura P, Belanger G, Modulation of utrophin A mRNA stability in fast versus slow muscles via an AU-rich element and calcineurin signaling. Nucleic Acids Res 2008;36:826-38
   Google Scholar
• Miura P, Coriati A, Belanger G, The utrophin A 5'-UTR drives cap-independent translation exclusively in skeletal muscles of transgenic mice and interacts with eEF1A2. Hum Mol Genet 2010;19:1211-20
   PubMed Web of Science ®Google Scholar
• Kawahara G, Karpf JA, Myers JA, Drug screening in a zebrafish model of Duchenne muscular dystrophy. Proc Natl Acad Sci USA 2011;108:5331-6
   PubMed Web of Science ®Google Scholar
• Dunckley MG, Manoharan M, Villiet P, Eperon IC, Dickson G. Modification of splicing in the dystrophin gene in cultured mdx muscle cells by antisense oligoribonucleotides. Hum Mol Genet 1998;7(7):1083-90
   PubMed Web of Science ®Google Scholar
• Wilton SD, Lloyd F, Carville K, Fletcher S, Honeyman K, Agrawal S, Kole R. Specific removal of the nonsense mutation from the mdx dystrophin mRNA using antisense oligonucleotides. Neuromuscul Disord 1999;9(5):330-8
   PubMed Web of Science ®Google Scholar
• van Deutekom JC, Janson AA, Ginjaar IB, Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 2007;357:2677-86
   PubMed Web of Science ®Google Scholar
• Goemans NM, Tulinius M, van den Akker JT, Systemic administration of PRO051 in Duchenne's muscular dystrophy. N Engl J Med 2011;364:1513-22
   PubMed Web of Science ®Google Scholar
• Hoffman EP. Skipping toward personalized molecular medicine. N Engl J Med 2007;357:2719-22
   PubMed Web of Science ®Google Scholar
• Thomas GD, Sander M, Lau KS, Impaired metabolic modulation of α-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc Nat Acad Sci 1998;95:15090-5
   PubMed Web of Science ®Google Scholar
• Sander M, Chavoshan B, Harris SA, Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc Nat Acad Sci 2000;97:13818-23
   PubMed Web of Science ®Google Scholar
• Verma M, Asakura Y, Hirai H, Flt-1 haploinsufficiency ameliorates muscular dystrophy phenotype by developmentally increased vasculature in mdx mice. Hum Mol Genet 2010;19:4145-59
   PubMed Web of Science ®Google Scholar
• Ito K, Kimura S, Ozasa S, Smooth muscle-specific dystrophin expression improves aberrant vasoregulation in mdx mice. Hum Mol Genet 2006;15:2266-75
   PubMed Web of Science ®Google Scholar
• Moorwood C, Soni N, Patel G, A cell-based high-throughput screening assay for post-transcriptional utrophin upregulation. J Biomol Screen 2012; published online October 30 2012
   PubMedGoogle Scholar