Muscular dystrophy: Experimental animal models and therapeutic approaches (Review)
- Authors:
- Gisela Gaina
- Alexandra Popa (Gruianu)
-
Affiliations: Laboratory of Cell Biology, Neuroscience and Experimental Myology, ‘Victor Babes’ National Institute of Pathology, 050096 Bucharest, Romania - Published online on: April 14, 2021 https://doi.org/10.3892/etm.2021.10042
- Article Number: 610
-
Copyright: © Gaina et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Dalkilic I and Kunkel LM: Muscular dystrophies: Genes to pathogenesis. Curr Opin Genet Dev. 13:231–238. 2003.PubMed/NCBI View Article : Google Scholar | |
Hoffman EP, Brown RH Jr and Kunkel LM: Dystrophin: The protein product of the Duchenne muscular dystrophy locus. Cell. 51:919–928. 1987.PubMed/NCBI View Article : Google Scholar | |
Ervasti JM and Campbell KP: A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol. 122:809–823. 1993.PubMed/NCBI View Article : Google Scholar | |
Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW and Campbell KP: Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature. 355:696–702. 1992.PubMed/NCBI View Article : Google Scholar | |
Lapidos KA, Kakkar R and McNally EM: The Dystrophin glycoprotein complex: Signaling strength and integrity for the sarcolemma. Circ Res. 94:1023–1031. 2004.PubMed/NCBI View Article : Google Scholar | |
Constantin B: Dystrophin complex functions as a scaffold for signalling protein. Biochim Biophys Acta. 1838:635–642. 2014.PubMed/NCBI View Article : Google Scholar | |
Gaina G: Clinical and molecular diagnosis in muscular dystrophies. Ed Intech, 2019. | |
Bushby K, Norwood F and Straub V: The limb-girdle muscular dystrophies-Diagnostic strategies. Biochim Biophys Acta. 1772:238–242. 2007.PubMed/NCBI View Article : Google Scholar | |
McNally EM and Pytel P: Muscle diseases: The muscular dystrophies. Annu Rev Pathol. 2:87–109. 2007.PubMed/NCBI View Article : Google Scholar | |
Matthews RA: Medical progress depends on animal models-doesn't it? J R Soc Med. 101:95–98. 2008.PubMed/NCBI View Article : Google Scholar | |
Barré-Sinoussi F and Montagutelli S: Animal models are essential to biological research: Issues and perspectives. Future Sci OA. 1(FSO63)2015.PubMed/NCBI View Article : Google Scholar | |
Wells D: Tracking progress: An update on animal models for Duchenne muscular dystrophy. Dis Model Mech. 11(dmm035774)2018.PubMed/NCBI View Article : Google Scholar | |
Van Putten M, Lloyd EM, de Greef JC, Raz V, Willmann R and Grounds MD: Mouse models for muscular dystrophies: An overview. Dis Model Mech. 13(dmm043562)2020.PubMed/NCBI View Article : Google Scholar | |
Spurney C, Gordish-Dressman H, Guerron AD, Sali A, Pandey GS, Rawat R, Van Der Meulen JH, Cha HJ, Pistilli EE, Partridge TA, et al: Preclinical drug trials in the mdx mouse: Assessment of reliable and sensitive outcome measures. Muscle Nerve. 39:591–602. 2009.PubMed/NCBI View Article : Google Scholar | |
Gussoni E, Soneoka Y, Strickland CD, Buzney EA, Khan MK, Flint AF, Kunkel LM and Mulligan RC: Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature. 401:390–394. 1999.PubMed/NCBI View Article : Google Scholar | |
Hakim CH, Wasala NB, Pan X, Kodippili K, Yue Y, Zhang K, Yao G, Haffner B, Duan SX, Ramos J, et al: A five-repeat micro-dystrophin gene ameliorated dystrophic phenotype in the severe DBA/2J-mdx model of Duchenne muscular dystrophy. Mol Ther Methods Clin Dev. 6:216–230. 2017.PubMed/NCBI View Article : Google Scholar | |
Kornegay JN: The golden retriever model of Duchenne muscular dystrophy. Skelet Muscle. 7(9)2017.PubMed/NCBI View Article : Google Scholar | |
Kornegay JN, Bogan JR, Bogan DJ, Childers MK, Li J, Nghiem P, Detwiler DA, Larsen CA, Grange RW, Bhavaraju-Sanka RK, et al: Canine models of Duchenne muscular dystrophy and their use in therapeutic strategies. Mamm Genome. 23:85–108. 2012.PubMed/NCBI View Article : Google Scholar | |
Howell JM, Fletcher S, Kakulas BA, O'Hara M, Lochmuller H and Karpati G: Use of the dog model for Duchenne muscular dystrophy in gene therapy trials. Neuromuscul Disord. 7:325–328. 1997.PubMed/NCBI View Article : Google Scholar | |
Wernersson R, Schierup MH, Jørgensen FG, Gorodkin J, Panitz F, Stærfeldt HH, Christensen OF, Mailund T, Hornshøj H, Klein A, et al: Pigs in sequence space: A 0.66X coverage pig genome survey based on shotgun sequencing. BMC Genomics. 6(70)2005.PubMed/NCBI View Article : Google Scholar | |
Guiraud S, Squire SE, Edwards B, Chen H, Burns DT, Shah N, Babbs A, Davies SG, Wynne GM, Russell AJ, et al: Second generation compound for the modulation of utrophin in the therapy of DMD. Hum Mol Genet. 24:4212–4224. 2015.PubMed/NCBI View Article : Google Scholar | |
Witting N, Kruuse C, Nyhuus B, Prahm KP, Citirak G, Lundgaard SJ, von Huth S, Vejlstrup N, Lindberg U, Krag TO and Vissing J: Effect of sildenafil on skeletal and cardiac muscle in Becker muscular dystrophy. Ann Neurol. 76:550–557. 2014.PubMed/NCBI View Article : Google Scholar | |
Mata López S, Hammond JJ, Rigsby MB, Balog-Alvarez CJ, Kornegay JN and Nghiem PP: A novel canine model for Duchenne muscular dystrophy (DMD): Single nucleotide deletion in DMD gene exon 20. Skelet Muscle. 8(16)2018.PubMed/NCBI View Article : Google Scholar | |
Whitworth KM, Lee K, Benne JA, Beaton BP, Spate LD, Murphy SL, Samuel MS, Mao J, O'Gorman C, Walters EM, et al: Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos. Biol Reprod. 91(78)2014.PubMed/NCBI View Article : Google Scholar | |
Moretti A, Fonteyne L, Giesert F, Hoppmann P, Meier AB, Bozoglu T, Baehr A, Schneider CM, Sinnecker D, Klett K, et al: Somatic gene editing ameliorates skeletal and cardiac muscle failure in pig and human models of Duchenne muscular dystrophy. Nat Med. 26:207–214. 2020.PubMed/NCBI View Article : Google Scholar | |
Du M, Keeling KM, Fan L, Liu X, Kovaçs T, Sorscher E and Bedwell DM: Clinical doses of amikacin provide more effective suppression of the human CFTR-G542X stop mutation than gentamicin in a transgenic CF mouse model. J Mol Med (Berl). 84:573–582. 2006.PubMed/NCBI View Article : Google Scholar | |
Kayali R, Ku JM, Khitrov G, Jung ME, Prikhodko O and Bertoni C: Read-through compound 13 restores dystrophin expression and improves muscle function in the mdx mouse model for Duchenne muscular dystrophy. Hum Mol Genet. 21:4007–4020. 2012.PubMed/NCBI View Article : Google Scholar | |
Valentine BA, Cooper BJ, de Lahunta A, O'Quinn R and Blue JT: Canine X-linked muscular dystrophy. An animal model of Duchenne muscular dystrophy: Clinical studies. J Neurol Sci. 88:69–81. 1988.PubMed/NCBI View Article : Google Scholar | |
Beastrom N, Lu H, Macke A, Canan BD, Johnson EK, Penton CM, Kaspar BK, Rodino-Klapac LR, Zhou L, Janssen PM and Montanaro F: mdx(5cv) mice manifest more severe muscle dysfunction and diaphragm force deficits than do mdx Mice. Am J Pathol. 179:2464–2474. 2011.PubMed/NCBI View Article : Google Scholar | |
Wolfe JH: Gene therapy in large animal models of human genetic diseases. Introduction. ILAR J. 50:107–111. 2009.PubMed/NCBI View Article : Google Scholar | |
Allamand V and Campbell K: Animal models for muscular dystrophy: Valuable tools for the development of therapies. Hum Mol Genet. 9:2459–2467. 2000.PubMed/NCBI View Article : Google Scholar | |
Acosta CA, Izal I, Ripalda P, Douglas-Price AL and Forriol F: Gene expression and proliferation analysis in young, aged, and osteoarthritic sheep chondrocytes effect of growth factor treatment. J Orthop Res. 24:2087–2094. 2006.PubMed/NCBI View Article : Google Scholar | |
Mouse Genome Sequencing Consortium. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, et al: Initial sequencing and comparative analysis of the mouse genome. Nature. 420:520–562. 2002.PubMed/NCBI View Article : Google Scholar | |
Emery AEH and Muntoni F (eds.): Duchenne Muscular Dystrophy. Oxford University Press, New York, NY, 2003. | |
Koenig M, Beggs AH, Moyer M, Scherpf S, Heindrich K, Bettecken T, Meng G, Müller CR, Lindlöf M, Kaariainen H, et al: The molecular basis for Duchenne versus Becker muscular dystrophy: Correlation of severity with type of deletion. Am J Hum Genet. 45:498–506. 1989.PubMed/NCBI | |
Di Blasi L, Morandi L, Barresi R, Blasevich F, Cornelio F and Mora M: Dystrophin-associated protein abnormalities in dystrophin-deficient muscle fibers from symptomatic and asymptomatic Duchenne/Becker muscular dystrophy carriers. Acta Neuropathol (Berl). 92:369–377. 1996.PubMed/NCBI View Article : Google Scholar | |
Rodgers BD, Bishaw Y, Kagel D, Ramos JN and Maricelli JW: Micro-dystrophin gene therapy partially enhances exercise capacity in older adult mdx mice. Mol Ther Methods Clin Dev. 17:122–132. 2019.PubMed/NCBI View Article : Google Scholar | |
McGreevy JW, Hakim CH, McIntosh MA and Duan D: Animal models of Duchenne muscular dystrophy: From basic mechanisms to gene therapy. Dis Model Mech. 8:195–213. 2015.PubMed/NCBI View Article : Google Scholar | |
Koenig M, Monaco AP and Kunkel LM: The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell. 53:219–226. 1988.PubMed/NCBI View Article : Google Scholar | |
Bulfield G, Siller WG, Wight PA and Moore KJ: X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA. 81:1189–1192. 1984.PubMed/NCBI View Article : Google Scholar | |
Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG and Barnard PJ: The molecular basis of muscular dystrophy in the mdx mouse: A point mutation. Science. 244:1578–1580. 1989.PubMed/NCBI View Article : Google Scholar | |
Morgan SJ, Elangbam CS, Berens S, Janovitz E, Vitsky A, Zabka T and Conour L: Use of animal models of human disease for nonclinical safety assessment of novel pharmaceuticals. Toxicol Pathol. 41:508–518. 2013.PubMed/NCBI View Article : Google Scholar | |
Fukada S, Morikawa D, Yamamoto Y, Yoshida T, Sumie N, Yamaguchi M, Ito T, Miyagoe-Suzuki Y, Takeda S, Tsujikawa K and Yamamoto H: Genetic background affects properties of satellite cells and mdx phenotypes. Am J Pathol. 176:2414–2424. 2010.PubMed/NCBI View Article : Google Scholar | |
Carnwath JW and Shotton DM: Muscular dystrophy in the mdx mouse: Histopathology of the soleus and extensor digitorum longus muscles. J Neurol Sci Aug. 80:39–54. 1987.PubMed/NCBI View Article : Google Scholar | |
Manning J and O'Malley D: What has the mdx mouse model of Duchenne muscular dystrophy contributed to our understanding of this disease? J Muscle Res Cell Motil. 36:155–167. 2015.PubMed/NCBI View Article : Google Scholar | |
De Luca A, Nico B, Liantonio A, Didonna MP, Fraysse B, Pierno S, Burdi R, Mangieri D, Rolland JF, Camerino C, et al: A multidisciplinary evaluation of the effectiveness of cyclosporine A in dystrophic mdx mice. Am J Pathol. 166:477–489. 2005.PubMed/NCBI View Article : Google Scholar | |
Partridge TA, Morgan JE, Coulton GR, Hoffman EP and Kunkel LM: Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature. 337:176–179. 1989.PubMed/NCBI View Article : Google Scholar | |
Roy P, Rau F, Ochala J, Messéant J, Fraysse B, Lainé J, Agbulut O, Butler-Browne G, Furling D and Ferry A: Dystrophin restoration therapy improves both the reduced excitability and the force drop induced by lengthening contractions in dystrophic mdx skeletal muscle. Skelet Muscle. 6(23)2016.PubMed/NCBI View Article : Google Scholar | |
Im WB, Phelps FS, Copen RH, Adams EG, Slightom JL and Chamberlain JS: Differential expression of Dystrophin isoforms in strains of mdx mice with different mutations. Hum Mol Genet. 5:1149–1153. 1996.PubMed/NCBI View Article : Google Scholar | |
Bürger R, Willensdorfer M and Nowak MA: Why are phenotypic mutation rates much higher than genotypic mutation rates? Genetics. 172:197–206. 2006.PubMed/NCBI View Article : Google Scholar | |
Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS and Sanes JR: Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: A model for Duchenne muscular dystrophy. Cell. 90:729–738. 1997.PubMed/NCBI View Article : Google Scholar | |
Davies KE and Chamberlain JS: Surrogate gene therapy for muscular dystrophy. Nat Med. 25:1473–1474. 2019.PubMed/NCBI View Article : Google Scholar | |
Yucel N, Chang AC, Day JW, Rosenthal N and Blau HM: Humanizing the mdx mouse model of DMD: The long and the short of it. NPJ Regen Med. 3(4)2018.PubMed/NCBI View Article : Google Scholar | |
Chang AC, Ong SG, LaGory EL, Kraft PE, Giaccia AJ, Wu JC and Blau HM: Telomere shortening, and metabolic compromise underlie dystrophic cardiomyopathy. Proc Natl Acad Sci USA. 113:13120–13125. 2016.PubMed/NCBI View Article : Google Scholar | |
Mourkioti F, Kustan J, Kraft P, Day JW, Zhao MM, Kost-Alimova M, Protopopov A, DePinho RA, Bernstein D, Meeker AK and Blau HM: Role of telomere dysfunction in cardiac failure in Duchenne muscular dystrophy. Nat Cell Biol. 15:895–904. 2013.PubMed/NCBI View Article : Google Scholar | |
Wentink GH, van der Linde-Sipman JS, Meijer AEFH, Kamphuisen HAC, van Vorstenbosch CJAHV, Hartman W and Hendriks HJ: Myopathy with a possible recessive X-linked inheritance in a litter of Irish Terriers. Vet Pathol. 9:328–349. 1972.PubMed/NCBI View Article : Google Scholar | |
Cooper BJ, Gallagher EA, Smith CA, Valentine BA and Winand NJ: Mosaic expression of dystrophin in carriers of canine X-linked muscular dystrophy. Lab Invest. 62:171–178. 1990.PubMed/NCBI | |
Walmsley GL, Arechavala-Gomeza V, Fernandez-Fuente M, Burke MM, Nagel N, Holder A, Stanley R, Chandler K, Marks SL, Muntoni F, et al: A duchenne muscular dystrophy gene hot spot mutation in dystrophin-deficient cavalier king charles spaniels is amenable to exon 51 skipping. PLoS One. 5(e8647)2010.PubMed/NCBI View Article : Google Scholar | |
Meier H: Myopathies in the dog. Cornell Vet. 48:313–330. 1958.PubMed/NCBI | |
Cooper BJ, Winand NJ, Stedman H, Valentine BA, Hoffman EP, Kunkel LM, Scott MO, Fischbeck KH, Kornegay JN, Avery RJ, et al: The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs. Nature. 334:154–156. 1988.PubMed/NCBI View Article : Google Scholar | |
Sharp NJ, Kornegay JN, Van Camp SD, Herbstreith MH, Secore SL, Kettle S, Hung WY, Constantinou CD, Dykstra MJ, Roses AD, et al: An error in dystrophin mRNA processing in golden retriever muscular dystrophy, an animal homologue of Duchenne muscular dystrophy. Genomics. 13:115–121. 1992.PubMed/NCBI View Article : Google Scholar | |
Schatzberg SJ, Olby NJ, Breen M, Anderson LV, Langford CF, Dickens HF, Wilton SD, Zeiss CJ, Binns MM, Kornegay JN, et al: Molecular analysis of a spontaneous dystrophin ‘knockout’ dog. Neuromuscul Disord. 9:289–295. 1999.PubMed/NCBI View Article : Google Scholar | |
Vulin A, Barthélémy I, Goyenvalle A, Thibaud JL, Beley C, Griffith G, Benchaouir R, le Hir M, Unterfinger Y, Lorain S, et al: Muscle function recovery in golden retriever muscular dystrophy after AAV1-U7 exon skipping. Mol Ther. 20:2120–2133. 2012.PubMed/NCBI View Article : Google Scholar | |
Wasala N, Chen SJ and Duan D: Duchenne muscular dystrophy animal models for high-throughput drug discovery and precision medicine. Expert Opin Drug Discov. 15:443–456. 2020.PubMed/NCBI View Article : Google Scholar | |
Nghiem PP and Kornegay JN: Gene therapies in canine models for Duchenne muscular dystrophy. Hum Genet. 138:483–489. 2019.PubMed/NCBI View Article : Google Scholar | |
Lunney JK: Advances in swine biomedical model genomics. Int J Biol Sci. 3:179–184. 2007.PubMed/NCBI View Article : Google Scholar | |
Klymiuk N, Blutke A, Graf A, Krause S, Burkhardt K, Wuensch A, Krebs S, Kessler B, Zakhartchenko V, Kurome M, et al: Dystrophin-deficient pigs provide new insights into the hierarchy of physiological derangements of dystrophic muscle. Hum Mol Genet. 22:4368–4382. 2013.PubMed/NCBI View Article : Google Scholar | |
Muntoni F, Torelli S and Ferlini A: Dystrophin and mutations: One gene, several proteins, multiple phenotypes. Lancet Neurol. 2:731–740. 2003.PubMed/NCBI View Article : Google Scholar | |
Yu HH, Zhao H, Qing YB, Pan WR, Jia BY, Zhao HY, Huang XX and Wei HJ: Porcine zygote injection with Cas9/sgRNA results in DMD-modified pig with muscle dystrophy. Int J Mol Sci. 17(1668)2016.PubMed/NCBI View Article : Google Scholar | |
Nonneman DN, Brown-Brandl T, Jones SA, Wiedmann RT and Rohrer GA: A defect in dystrophin causes a novel porcine stress syndrome. BMC Genomics. 13(233)2012.PubMed/NCBI View Article : Google Scholar | |
Hollinger K, Yang CX, Montz RE, Nonneman D, Ross JW and Selsby JT: Dystrophin insufficiency causes selective muscle histopathology and loss of dystrophin-glycoprotein complex assembly in pig skeletal muscle. FASEB J. 28:1600–1609. 2014.PubMed/NCBI View Article : Google Scholar | |
Horiuchi N, Aihara N, Mizutani H, Kousaka S, Nagafuchi T, Ochiai M, Kobayashi Y, Furuoka H, Asai T and Oishi K: Becker muscular dystrophy-like myopathy regarded as so-called ‘fatty muscular dystrophy’ in a Pig: A case report and its diagnostic method. J Vet Med Sci. 76:243–248. 2014.PubMed/NCBI View Article : Google Scholar | |
Guiraud S, Aartsma-Rus A, Vieira NM, Davies KE, van Ommen GJB and Kunkel LM: The pathogenesis and therapy of muscular Dystrophies. Annu Rev Genomics Hum Genet. 16:281–308. 2015.PubMed/NCBI View Article : Google Scholar | |
Shimizu-Motohashi Y, Komaki H, Motohashi N, Takeda S, Yokota T and Aoki Y: Restoring Dystrophin expression in duchenne muscular dystrophy: Current status of therapeutic approaches. J Pers Med. 9(1)2019.PubMed/NCBI View Article : Google Scholar | |
Dabrowski M, Bukowy-Bieryllo Z and Zietkiewicz E: Advances in therapeutic use of a drug-stimulated translational readthrough of premature termination codons. Mol Med. 24(25)2018.PubMed/NCBI View Article : Google Scholar | |
Bladen CL, Salgado D, Monges S, Foncuberta ME, Kekou K, Kosma K, Dawkins H, Lamont L, Roy AJ, Chamova T, et al: The TREAT-NMD DMD global database: Analysis of more than 7,000 Duchenne muscular dystrophy mutations. Hum Mutat. 36:395–402. 2015.PubMed/NCBI View Article : Google Scholar | |
Barton-Davis ER, Cordier L, Shoturma DI, Leland SE and Sweeney HL: Aminoglycoside antibiotics restore dystrophin function to skeletal muscles of mdx mice. J Clin Invest. 104:375–381. 1999.PubMed/NCBI View Article : Google Scholar | |
Malik V, Rodino-Klapac LR, Viollet L, Wall C, King W, Al-Dahhak R, Lewis S, Shilling CJ, Kota J, Serrano-Munuera C, et al: Gentamicin-induced readthrough of stop codons in Duchenne muscular dystrophy. Ann Neurol. 67:771–780. 2010.PubMed/NCBI View Article : Google Scholar | |
Namgoong JH and Bertoni C: Clinical potential of ataluren in the treatment of Duchenne muscular dystrophy. Degener Neurol Neuromuscul Dis. 6:37–48. 2016.PubMed/NCBI View Article : Google Scholar | |
Welch EM, Barton ER, Zhuo J, Tomizawa Y, Friesen WJ, Trifillis P, Paushkin S, Patel M, Trotta CR, Hwang S, et al: PTC124 targets genetic disorders caused by nonsense mutations. Nature. 447:87–91. 2007.PubMed/NCBI View Article : Google Scholar | |
Dranchak PK, Di Pietro E, Snowden A, Oesch N, Braverman NE, Steinberg SJ and Hacia JG: Nonsense suppressor therapies rescue peroxisome lipid metabolism and assembly in cells from patients with specific PEX gene mutations. J Cell Biochem. 112:1250–1258. 2011.PubMed/NCBI View Article : Google Scholar | |
Aartsma-Rus A, Janson AA, Kaman WE, Bremmer-Bout M, den Dunnen JT, Baas F, van Ommen GJ and van Deutekom JC: Therapeutic antisense-induced exon skipping in cultured muscle cells from six different DMD patients. Hum Mol Genet. 12:907–914. 2003.PubMed/NCBI View Article : Google Scholar | |
Aoki Y, Nakamura A, Yokota T, Saito T, Okazawa H, Nagata T and Takeda S: In-frame dystrophin following exon 51-skipping improves muscle pathology and function in the exon 52-deficient mdx mouse. Mol Ther. 18:1995–2005. 2010.PubMed/NCBI View Article : Google Scholar | |
McClorey G, Moulton HM, Iversen PL, Fletcher S and Wilton SD: Antisense oligonucleotide-induced exon skipping restores dystrophin expression in vitro in a canine model of DMD. Gene Ther. 13:1373–1381. 2006.PubMed/NCBI View Article : Google Scholar | |
van Deutekom JC, Janson AA, Ginjaar IB, Frankhuizen WS, Aartsma-Rus A, Bremmer-Bout M, den Dunnen JT, Koop K, van der Kooi AJ, Goemans NM, et al: Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med. 357:2677–2686. 2007.PubMed/NCBI View Article : Google Scholar | |
Nguyen Q and Yokota T: Immortalized muscle cell model to test the exon skipping efficacy for duchenne muscular dystrophy. J Pers Med. 7(13)2017.PubMed/NCBI View Article : Google Scholar | |
Blain AM, Greally E, McClorey G, Manzano R, Betts CA, Godfrey C, O'Donovan L, Coursindel T, Gait MJ, Wood MJ, et al: Peptide-conjugated phosphodiamidate oligomer-mediated exon skipping has benefits for cardiac function in mdx and Cmah−/−mdx mouse models of Duchenne muscular dystrophy. PLoS One. 13(e0198897)2018.PubMed/NCBI View Article : Google Scholar | |
Ishino Y, Shinagawa H, Makino K, Amemura M and Nakata A: Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol. 169:5429–5433. 1987.PubMed/NCBI View Article : Google Scholar | |
Wright A, Nuñez JK and Doudna JA: Biology and Applications of CRISPR Systems: Harnessing Nature's Toolbox for Genome Engineering. Cell. 164:29–44. 2016.PubMed/NCBI View Article : Google Scholar | |
Duchêne BL, Cherif K, Iyombe-Engembe JP, Guyon A, Rousseau A, Ouellet DL, Barbeau X, Lague P and Tremblay JP: CRISPR-induced deletion with SaCas9 restores dystrophin expression in dystrophic models in vitro and in vivo. Mol Ther. 26:2604–2616. 2018.PubMed/NCBI View Article : Google Scholar | |
Bengtsson NE, Hall JK, Odom GL, Phelps MP, Andrus CR, Hawkins RD, Hauschka SD, Chamberlain JR and Chamberlain JS: Muscle-specific CRISPR/Cas9 dystrophin gene editing ameliorates pathophysiology in a mouse model for Duchenne muscular dystrophy. Nat Commun. 8(14454)2017.PubMed/NCBI View Article : Google Scholar | |
Gilbert R, Nalbantoglu J, Petrof BJ, Ebihara S, Guibinga GH, Tinsley JM, Kamen A, Massie B, Davies KE and Karpati G: Adenovirus-mediated utrophin gene transfer mitigates the dystrophic phenotype of mdx mouse muscles. Hum Gene Ther. 10:1299–1310. 1999.PubMed/NCBI View Article : Google Scholar | |
McPherron AC, Lawler AM and Lee SJ: Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 387:83–90. 1997.PubMed/NCBI View Article : Google Scholar | |
Acharyya S, Villalta SA, Bakkar N, Bupha-Intr T, Janssen PM, Carathers M, Li ZW, Beg AA, Ghosh S, Sahenk Z, et al: Interplay of IKK/NF-kappaB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J Clin Invest. 117:889–901. 2007.PubMed/NCBI View Article : Google Scholar | |
Larsen FJ, Schiffer TA, Borniquel S, Sahlin K, Ekblom B, Lundberg JO and Weitzberg E: Dietary inorganic nitrate improves mitochondrial efficiency in humans. Cell Metab. 13:149–159. 2011.PubMed/NCBI View Article : Google Scholar | |
Barton ER, Morris L, Kawana M, Bish LT and Toursel T: Systemic administration of L-arginine benefits mdx skeletal muscle function. Muscle Nerve. 32:751–760. 2005.PubMed/NCBI View Article : Google Scholar | |
Tinsley JM, Potter AC, Phelps SR, Fisher R, Trickett JI and Davies KE: Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature. 384:349–353. 1996.PubMed/NCBI View Article : Google Scholar | |
Khurana TS, Hoffman EP and Kunkel LM: Identification of a chromosome 6-encoded dystrophin-related protein. J Biol Chem. 265:16717–16720. 1990.PubMed/NCBI | |
Voisin V and la Porte S: Therapeutic strategies for Duchenne and Becker dystrophies. Int Rev Cytol. 240:1–30. 2004.PubMed/NCBI View Article : Google Scholar | |
Deconinck N, Tinsley J, De Backer F, Fisher R, Kahn D, Phelps S, Davies K and Gillis JM: Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat Med. 3:1216–1221. 1997.PubMed/NCBI View Article : Google Scholar | |
Deconinck AE, Rafael JA, Skinner JA, Brown SC, Potter AC, Metzinger L, Watt DJ, Dickson JG, Tinsley JM and Davies KE: Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell. 90:717–727. 1997.PubMed/NCBI View Article : Google Scholar | |
Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS and Sanes JR: Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: A model for Duchenne muscular dystrophy. Cell. 90:729–738. 1997.PubMed/NCBI View Article : Google Scholar | |
Fisher R, Tinsley JM, Phelps SR, Squire SE, Townsend ER, Martin JE and Davies KE: Non-toxic ubiquitous over-expression of utrophin in the mdx mouse. Neuromuscul Disord. 11:713–721. 2001.PubMed/NCBI View Article : Google Scholar | |
Walton JN and Nattrass FJ: On the classification, natural history and treatment of the myopathies. Brain. 77:169–231. 1954.PubMed/NCBI View Article : Google Scholar | |
Preisler N, Lukacs Z, Vinge L, Madsen KL, Husu E, Hansen RS, Duno M, Andersen H, Laub M and Vissing J: Late-onset Pompe disease is prevalent in unclassified limb-girdle muscular dystrophies. Mol Genet Metab. 110:287–289. 2013.PubMed/NCBI View Article : Google Scholar | |
Bushby KM: Diagnostic criteria for the limb-girdle muscular dystrophies: Report of the ENMC Consortium on Limb-Girdle Dystrophies. Neuromuscul Disord. 5:71–74. 1995.PubMed/NCBI View Article : Google Scholar | |
Norwood FL, Harling C, Chinnery PF, Eagle M, Bushby K and Straub V: Prevalence of genetic muscle disease in Northern England: In-depth analysis of a muscle clinic population. Brain. 132:3175–3186. 2009.PubMed/NCBI View Article : Google Scholar | |
Richard I, Roudaut C, Marchand S, Baghdiguian S, Herasse M, Stockholm D, Ono Y, Suel L, Bourg N, Sorimachi H, et al: Loss of Calpain 3 Proteolytic activity leads to muscular dystrophy and to apoptosis-associated IkappaBalpha/nuclear Factor kappa Pathway Perturbation in Mice. J Cell Biol. 151:1583–1590. 2000.PubMed/NCBI View Article : Google Scholar | |
Bartoli M, Roudaut C, Martin S, Fougerousse F, Suel L, Poupiot J, Gicquel E, Noulet F, Danos O and Richard I: Safety and efficacy of AAV-mediated Calpain 3 gene transfer in a mouse model of limb-girdle muscular dystrophy type 2A. Mol Ther. 13:250–259. 2006.PubMed/NCBI View Article : Google Scholar | |
Ng R, Banks GB, Hall JK, Muir LA, Ramos JN, Wicki J, Odom GL, Konieczny P, Seto J, Chamberlain JR and Chamberlain JS: Animal models of muscular dystrophy. Prog Mol Biol Transl Sci. 105:83–111. 2012.PubMed/NCBI View Article : Google Scholar | |
Kramerova I, Kudryashova E, Tidball JG and Spencer MJ: Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Hum Mol Genet. 13:1373–88. 2004.PubMed/NCBI View Article : Google Scholar | |
Lostal W, Roudaut C, Faivre M, Charton K, Suel L, Bourg N, Best H, Smith JE, Gohlke J, Corre G, et al: Titin splicing regulates cardiotoxicity associated with calpain 3 gene therapy for limb-girdle muscular dystrophy type 2A. Sci Transl Med. 11(eaat6072)2019.PubMed/NCBI View Article : Google Scholar | |
Blain AM and Straub VW: δ-Sarcoglycan-deficient muscular dystrophy: From discovery to therapeutic approaches. Skelet Muscle. 1(13)2011.PubMed/NCBI View Article : Google Scholar | |
Demonbreun A, Wyatt E, Fallon K, Oosterbaan C, Page P, Hadhazy M, Quattrocelli M, Barefield D and McNally E: A gene-edited mouse model of limb-girdle muscular dystrophy 2C for testing exon skipping. Dis Models Mech. 13(dmm040832)2019.PubMed/NCBI View Article : Google Scholar | |
Aartsma-Rus A and van Putten M: The use of genetically humanized animal models for personalized medicine approaches. Dis Model Mech. 13(dmm041673)2019.PubMed/NCBI View Article : Google Scholar | |
Sevastre B, Blidaru A, Sárpataki O, Marcus I and Coman C: Retrospective assessment of animals experimentation projects in Romania-a critical analysis of non-technical summaries. Bull UASVM Vet Med. 75:190–194. 2018. | |
Collins CA and Morgan JE: Duchenne's muscular dystrophy: Animal models used to investigate pathogenesis and develop therapeutic strategies. Int J Exp Pathol. 84:165–172. 2003.PubMed/NCBI View Article : Google Scholar |