Animal models of duchenne muscular dystrophy, with special reference to the mdx mouse

• Autorzy: Blain A. , Greally E. , Laval S. , Blamire A. , MacGowan G. , Straub V.
• Języki publikacji: EN

Abstrakty

EN

Duchenne muscular dystrophy (DMD) is a progressive muscle wasting disease that affects approximately l in 3500 male births. We describe animal models of DMD with special reference to the mdx mouse. We also describe some of the standard operating procedures (SOPs) developed by the TREAT-NMD neuromuscular network (http://www.treat-nmd. eu/) for assessment of the mdx mouse, with a focus on techniques for assessing cardiac function that are used in our lab, including the cardiac conductance catheter. We have also recently developed cardiac MRI as a novel cardiac assessment technique for mouse models of muscular dystrophy. We describe how this technique can be used both in the assessment of ventricular function and in the investigation of the role of abnormal calcium influx in muscular dystrophy-associated cardiomyopathy.

Słowa kluczowe

EN

duchenne muscular dystrophy; mdx mouse; cardiomyopathy; animal models; MRI; cardiac catheter; standard operating procedures

PL

kardiomiopatia; cewnik sercowy; model zwierzęcy

• Wydawca: Nałęcz Institute of Biocybernetics and Biomedical Engineering of the Polish Academy of Sciences ; Elsevier
• Czasopismo: Biocybernetics and Biomedical Engineering
• Rocznik: 2012
• Tom: Vol. 32, no. 4
• Strony: 3--15
• Opis fizyczny: Bibliogr. 83 poz., tab.

Twórcy

autor

Blain A.

autor

Greally E.

autor

Laval S.

autor

Blamire A.

autor

MacGowan G.

autor

Straub V.

• Institute of Genetic Medicine, Newcastle University, International Centre for Life, Newcastle upon Tyne, NE1 3 BZ United Kingdom,

Bibliografia

• [1] Emery A.E.: Population frequencies of inherited neuromuscular diseases-a world survey. Neuromuscul Disord. 1991, 1(1), 19–29.
• [2] Parsons E.P., Clarke A.J., Bradley D.M.: Developmental progress in Duchenne muscular dystrophy: lessons for earlier detection. Eur. J. Paediatr. Neurol. 2004, 8(3), 145–153.
• [3] Ciafaloni E. et al.: Delayed diagnosis in duchenne muscular dystrophy: data from the Muscular Dystrophy Surveillance. Tracking and Research Network (MD STARnet). J. Pediatr. 2009, 155(3), 380–385.
• [4] Essex C., Roper H.: Lesson of the week: late diagnosis of Duchenne’s muscular dystrophy presenting as global developmental delay. Bmj, 2001, 323(7303), 37–38.
• [5] Sejerson T., Bushby K.: Standards of care for Duchenne muscular dystrophy: brief TREAT-NMD recommendations. Adv. Exp. Med. Biol. 2009, 652, 13–21.
• [6] Birnkrant D.J. et al.: The respiratory management of patients with duchenne muscular dystrophy: a DMD care considerations working group specialty article. Pediatr. Pulmonol. 2010, 45(8), 739–748.
• [7] Roberto R. et al.: The Natural History of Cardiac and Pulmonary Function Decline in Patients with Duchenne Muscular Dystrophy. Spine (Phila Pa 1976), 2011.
• [8] Bach J.R., Martinez D.: Duchenne Muscular Dystrophy End-Stage Respiratory Muscle Failure: Prolongation of Survival by Noninvasive Interventions. Respir Care, 2011.
• [9] Sultan A., Fayaz M.: Prevalence of cardiomyopathy in Duchenne and Becker’s muscular dystrophy. J. Ayub. Med. Coll. Abbottabad, 2008, 20(2), 7–13.
• [10] Tomkins J.K.: The molecular defect in Duchenne muscular dystrophy. Muscle Nerve 1980, 3(6), 529–530.
• [11] Muntoni F., Torelli S., Ferlini A.: Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol. 2003, 2(12), 731–740.
• [12] Ohlendieck K. et al.: Duchenne muscular dystrophy: deficiency of dystrophin-associated proteins in the sarcolemma. Neurology 1993, 43(4), 795–800.
• [13] Wakayama Y. et al.: Localization of sarcoglycan, neuronal nitric oxide synthase, beta-dystroglycan, and dystrophin molecules in normal skeletal myofiber: triple immunogold labeling electron microscopy. Microsc. Res. Tech. 2001, 55(3), 154–163.
• [14] Adams M.E. et al.: Differential targeting of nNOS and AQP4 to dystrophin-deficient sarcolemma by membrane-directed alpha-dystrobrevin. J. Cell Sci. 2008, 121(Pt 1), 48–54.
• [15] Wells K.E. et al.: Relocalization of neuronal nitric oxide synthase (nNOS) as a marker for complete restoration of the dystrophin associated protein complex in skeletal muscle. Neuromuscul. Disord. 2003, 13(1), 21–31.
• [16] Jung D. et al.: Dystrophin in central nervous system: a developmental, regional distribution and subcellular localization study. Neurosci. Lett. 1991, 124(1), 87–91.
• [17] Bresolin N. et al.: Cognitive impairment in Duchenne muscular dystrophy. Neuromuscul. Disord. 1994, 4(4), 359–369.
• [18] Wu J.Y. et al.: Association of Duchenne muscular dystrophy with autism spectrum disorder. J. Child. Neurol. 2005, 20(10), 790–795.
• [19] Poysky J.: Learning and Behavior in Duchenne Muscular Dystrophy for parents and educators. Parent Project Muscular Dystrophy Education Matters Guides 2011.
• [20] Banks G.B., Chamberlain J.S.: The value of mammalian models for duchenne muscular dystrophy in developing therapeutic strategies. Curr. Top. Dev. Biol. 2008, 84, 431–453.
• [21] Grounds M.D. et al.: Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol. Dis. 2008, 31(1), 1–19.
• [22] Spurney C.F. et al.: Preclinical drug trials in the mdx mouse: assessment of reliable and sensitive outcome measures. Muscle Nerve 2009, 39(5), 591–602.
• [23] Bulfield G. et al.: X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci USA 1984, 81(4), 1189–1192.
• [24] Sicinski P. et al.: The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 1989, 244(4912), 1578–1580.
• [25] Bauer R. et al.: Contrasting effects of steroids and angiotensin-converting-enzyme inhibitors in a mouse model of dystrophin-deficient cardiomyopathy. Eur. J. Heart Fail. 2009, 11(5), 463–471.
• [26] Rezvani M., Cafarelli E., Hood D.A.: Performance and excitability of mdx mouse muscle at 2, 5, and 13 wk of age. J. Appl. Physiol. 1995, 78(3), 961–967.
• [27] Anderson J.E., Bressler B.H., Ovalle W.K.: Functional regeneration in the hindlimb skeletal muscle of the mdx mouse. J. Muscle Res. Cell Motil. 1988, 9(6), 499–515.
• [28] Weir A.P., Morgan J.E., Davies K.E.: A-utrophin up-regulation in mdx skeletal muscle is independent of regeneration. Neuromuscul. Disord. 2004, 14(1), 19–23.
• [29] Fisher R. et al.: Non-toxic ubiquitous over-expression of utrophin in the mdx mouse. Neuromuscul. Disord. 2001, 11(8), 713–721.
• [30] Di Certo M.G. et al.: The artificial gene Jazz, a transcriptional regulator of utrophin, corrects the dystrophic pathology in mdx mice. Hum. Mol. Genet. 2010, 19(5), 752–760.
• [31] Squire S. et al.: Prevention of pathology in mdx mice by expression of utrophin: analysis using an inducible transgenic expression system. Hum. Mol. Genet. 2002, 11(26), 3333–3344.
• [32] Janssen P.M. et al.: Utrophin deficiency worsens cardiac contractile dysfunction present in dystrophin-deficient mdx mice. Am. J. Physiol. Heart Circ. Physiol. 2005, 289(6), H2373–2378.
• [33] Mizuno Y. et al.: Reciprocal expression of dystrophin and utrophin in muscles of Duchenne muscular dystrophy patients, female DMD-carriers and control subjects. J. Neurol. Sci. 1993, 119(1), 43–52.
• [34] Decary S., Mouly V., Butler-Browne G.S.: Telomere length as a tool to monitor satellite cell amplification for cell-mediated gene therapy. Hum. Gene Ther. 1996, 7(11), 1347–1350.
• [35] Sacco A. et al.: Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 2011, 143(7), 1059–1071.
• [36] Mestas J., Hughes C.C.: Of mice and not men: differences between mouse and human immunology. J. Immunol. 2004, 172(5), 2731–2738.
• [37] Porter J.D. et al.: A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum. Mol. Genet. 2002, 11(3), 263–272.
• [38] Mingozzi F. et al.: CD8(+) T-cell responses to adeno-associated virus capsid in humans. Nat. Med. 2007, 13(4), 419–422.
• [39] Wood M.J.: Toward an oligonucleotide therapy for Duchenne muscular dystrophy: a complex development challenge. Sci. Transl. Med. 2010, 2(25), 25ps15.
• [40] Yin H. et al.: Optimization of peptide nucleic acid antisense oligonucleotides for local and systemic dystrophin splice correction in the mdx mouse. Mol. Ther. 2010, 18(4), 819–827.
• [41] Valentine B.A. et al.: Progressive muscular dystrophy in a golden retriever dog: light microscope and ultrastructural features at 4 and 8 months. Acta Neuropathol. 1986, 71(3-4), 301–310.
• [42] Kornegay J.N. et al.: Muscular dystrophy in a litter of golden retriever dogs. Muscle Nerve 1988, 11(10), 1056–1064.
• [43] Sharp N.J. et al.: An error in dystrophin mRNA processing in golden retriever muscular dystrophy, an animal homologue of Duchenne muscular dystrophy. Genomics 1992, 13(1), 115–121.
• [44] Ambrosio C.E. et al.: Identification of three distinguishable phenotypes in golden retriever muscular dystrophy. Genet. Mol. Res. 2009, 8(2), 389–396.
• [45] Shimatsu Y. et al.: Canine X-linked muscular dystrophy in Japan (CXMDJ). Exp. Anim. 2003, 52(2), 93–97.
• [46] Walmsley G.L. 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 2010, 5(1), e8647.
• [47] Chambers S.P. et al.: Dystrophin in adult zebrafish muscle. Biochem. Biophys. Res. Commun. 2001, 286(3), 478–483.
• [48] Neuman S., et al.: The dystrophin / utrophin homologues in Drosophila and in sea urchin. Gene 2001, 263(1-2), 17–29.
• [49] Bohm S. et al.: Dystrobrevin and dystrophin family gene expression in zebrafish. Gene Expr. Patterns 2008, 8(2), 71–78.
• [50] Bolanos-Jimenez F. et al.: Dystrophin and Dp71, two products of the DMD gene, show a different pattern of expression during embryonic development in zebrafish. Mech. Dev. 2001, 102(1-2), 239–241.
• [51] Dekkers L.C. et al.: Embryonic expression patterns of the Drosophila dystrophin-associated glycoprotein complex orthologs. Gene Expr. Patterns 2004, 4(2), 153–159.
• [52] Lecroisey C. et al.: DYC-1, a protein functionally linked to dystrophin in Caenorhabditis elegans is associated with the dense body, where it interacts with the muscle LIM domain protein ZYX-1. Mol. Biol. Cell 2008, 19(3), 785–796.
• [53] Grisoni K., Gieseler K., Segalat L.: Dystrobrevin requires a dystrophin-binding domain to function in Caenorhabditis elegans. Eur. J. Biochem., 2002, 269(6), 1607–1612.
• [54] Berger J. et al.: Dystrophin-deficient zebrafish feature aspects of the Duchenne muscular dystrophy pathology. Neuromuscul. Disord. 2011, 20(12), 826–832.
• [55] Kawahara G. et al.: Drug screening in a zebrafish model of Duchenne muscular dystrophy. Proc. Natl. Acad. Sci USA 2011, 108(13), 5331–5336.
• [56] Hamer P.W. et al.: Evans Blue Dye as an in vivo marker of myofibre damage: optimising parameters for detecting initial myofibre membrane permeability. J. Anat. 2002, 200(Pt 1), 69–79.
• [57] Bauer R. et al.: Steroid treatment causes deterioration of myocardial function in the {delta}-sarcoglycan-deficient mouse model for dilated cardiomyopathy. Cardiovasc. Res. 2008, 79(4), 652–661.
• [58] Bauer R. et al.: Intolerance to ss-blockade in a mouse model of delta-sarcoglycan-deficient muscular dystrophy cardiomyopathy. Eur. J. Heart Fail 2010, 12(11), 1163–1170.
• [59] Jorgensen L.H. et al.: Long-term blocking of calcium channels in mdx mice results in differential effects on heart and skeletal muscle. Am. J. Pathol.. 178(1), 273–283.
• [60] Dunn J.F., Zaim-Wadghiri Y.: Quantitative magnetic resonance imaging of the mdx mouse model of Duchenne muscular dystrophy. Muscle Nerve 1999, 22(10), 1367–1371.
• [61] Whitehead N.P., Yeung E.W., Allen D.G.: Muscle damage in mdx (dystrophic) mice: role of calcium and reactive oxygen species. Clin. Exp. Pharmacol. Physiol. 2006, 33(7), 657–662.
• [62] Hu T.C. et al.: Manganese-enhanced MRI of mouse heart during changes in inotropy. Magn. Reson. Med. 2001, 46(5), 884–890.
• [63] Silva A.C. et al.: Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed. 2004, 17(8), 532–543.
• [64] Tanabe Y., Esaki K., Nomura T.: Skeletal muscle pathology in X chromosome-linked muscular dystrophy (mdx) mouse. Acta Neuropathol. 1986, 69(1–2), 91–95.
• [65] Coulton G.R. et al.: The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation. Neuropathol. Appl. Neurobiol. 1988, 14(1), 53–70.
• [66] Head S.I., Williams D.A., D.G. Stephenson: Abnormalities in structure and function of limb skeletal muscle fibres of dystrophic mdx mice. Proc. Biol. Sci. 1992, 248(1322), 163–169.
• [67] Huang P. et al.: Impaired respiratory function in mdx and mdx/utrn(+/–) mice. Muscle Nerve 2011, 43(2), 263–267.
• [68] Deconinck A.E. et al.: Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 1997, 90(4), 717–727.
• [69] Barthelemy I. et al.: Gait analysis using accelerometry in dystrophin-deficient dogs. Neuromuscul. Disord. 2009, 19(11), 788–796.
• [70] Childers M.K. et al.: Eccentric contraction injury in dystrophic canine muscle. Arch. Phys. Med. Rehabil. 2002, 83(11), 1572–1578.
• [71] Shimatsu Y. et al.: Major clinical and histopathological characteristics of canine X-linked muscular dystrophy in Japan, CXMDJ. Acta Myol. 2005, 24(2), 145–154.
• [72] Yugeta N. et al.: Cardiac involvement in Beagle-based canine X-linked muscular dystrophy in Japan (CXMDJ): electrocardiographic, echocardiographic, and morphologic studies. BMC Cardiovasc. Disord. 2006, 6, 47.
• [73] Carpenter J.L. et al.: Feline muscular dystrophy with dystrophin deficiency. Am. J. Pathol. 1989, 135(5), 909–919.
• [74] Kohn B. et al.: [Muscular dystrophy in a cat]. Tierarztl. Prax. 1993, 21(5), 451–457.
• [75] Klymiuk N. et al.: 238 tailored pig model of duchenne muscular dystrophy. Reproduction, fertility and development. 2011, 24(1), 231.
• [76] Bassett D., Currie P.D.: Identification of a zebrafish model of muscular dystrophy. Clin. Exp. Pharmacol. Physiol. 2004, 31(8), 537–540.
• [77] Granato M. et al.: Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 1996, 123, 399–413.
• [78] Bassett D.I. et al.: Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo. Development 2003, 130(23), 5851–5860.
• [79] Guyon J.R. et al.: Genetic isolation and characterization of a splicing mutant of zebrafish dystrophin. Hum. Mol. Genet. 2009, 18(1), 202–211.
• [80] Bessou C. et al.: Mutations in the Caenorhabditis elegans dystrophin-like gene dys-1 lead to hyperactivity and suggest a link with cholinergic transmission. Neurogenetics 1998, 2(1), 61–72.
• [81] Giugia J. et al.: Mutations in the dystrophin-like dys-1 gene of Caenorhabditis elegans result in reduced acetylcholinesterase activity. FEBS Lett. 1999, 463(3), 270–272.
• [82] van der Plas M.C. et al.: Dystrophin is required for appropriate retrograde control of neurotransmitter release at the Drosophila neuromuscular junction. J. Neurosci. 2006, 26(1), 333–344.
• [83] van der Plas M.C. et al.: Drosophila Dystrophin is required for integrity of the musculature. Mech. Dev. 2007, 124(7–8), 617–630.