Implications for cardiac function following rescue of the dystrophic diaphragm in a mouse model of duchenne muscular dystrophy

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Betts, Corinne A ^a   Saleh, Amer F ^b,c   Carr, Carolyn A ^a   Muses, Sofia ^d   Wells, Kim E ^d   Hammond, Suzan M ^a   Godfrey, Caroline ^a   Mcclorey, Graham ^a   Woffindale, Caroline ^a   Clarke, Kieran ^a   Wells, Dominic J ^d   Gait, Michael J ^b   Wood, Matthew J A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c ASTRAZENECA   (United Kingdom)

^d ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; MORPHOLINO OLIGONUCLEOTIDE; NATRIURETIC PEPTIDE TYPE C; NOX4 PROTEIN, MOUSE; NPPA PROTEIN, MOUSE; PEPTIDE; PROTEIN PRECURSOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

AMINO ACID SEQUENCE; ANIMAL; ANIMAL EXPERIMENT; C57BL MOUSE; CHEMISTRY; DIAGNOSTIC IMAGING; DIAPHRAGM; DISEASE MODEL; DRUG EFFECTS; DUCHENNE MUSCULAR DYSTROPHY; GENE EXPRESSION; GENETICS; HEART; HUMAN; MALE; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; RADIOGRAPHY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; WESTERN BLOTTING; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; DIAPHRAGM; DISEASE MODELS, ANIMAL; DYSTROPHIN; GENE EXPRESSION; HEART; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MICE, INBRED C57BL; MICE, INBRED MDX; MORPHOLINOS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; NADPH OXIDASE; NATRIURETIC PEPTIDE, C-TYPE; PEPTIDES; PHYSICAL CONDITIONING, ANIMAL; PROTEIN PRECURSORS; RADIOGRAPHY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84933564872     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11632     Document Type: Article

References (39)

1. Connuck, D. M, et al. Characteristics and outcomes of cardiomyopathy in children with Duchenne or Becker muscular dystrophy: a comparative study from the Pediatric Cardiomyopathy Registry. Am Heart J 155, 998-1005, doi: 10.1016/j.ahj.2008.01.018 (2008
2. Benditt, J. O. & Boitano, L. Respiratory support of individuals with Duchenne muscular dystrophy: toward a standard of care. Physical medicine and rehabilitation clinics of North America 16, 1125-1139, xii, doi: 10.1016/j.pmr.2005.08.017 (2005
3. Dunckley, M. G., Manoharan, M., Villiet, P., Eperon, I. C. & Dickson, G. Modification of splicing in the dystrophin gene in cultured Mdx muscle cells by antisense oligoribonucleotides. Hum Mol Genet 7, 1083-1090 (1998
4. Wilton, S. D, et al. Specific removal of the nonsense mutation from the mdx dystrophin mRNA using antisense oligonucleotides. Neuromuscul Disord 9, 330-338, doi: S0960896699000103 (1999
5. Dickson, G., Hill, V. & Graham, I. R. Screening for antisense modulation of dystrophin pre-mRNA splicing. Neuromuscul Disord 12 (Suppl 1), , S67-70 (2002
6. Ohlendieck, K., Ervasti, J. M., Snook, J. B. & Campbell, K. P. Dystrophin-glycoprotein complex is highly enriched in isolated skeletal muscle sarcolemma. J Cell Biol 112, 135-148 (1991
7. Morrison, J., Lu, Q. L., Pastoret, C., Partridge, T. & Bou-Gharios, G. T-cell-dependent fibrosis in the mdx dystrophic mouse. Laboratory investigation; a journal of technical methods and pathology 80, 881-891 (2000
8. Carnwath, J. W. & Shotton, D. M. Muscular dystrophy in the mdx mouse: histopathology of the soleus and extensor digitorum longus muscles. J Neurol Sci 80, 39-54 (1987
9. Ishizaki, M, et al. Mdx respiratory impairment following fibrosis of the diaphragm. Neuromuscul Disord 18, 342-348, doi: 10.1016/j.nmd.2008.02.002 (2008
10. Melacini, P, et al. Cardiac and respiratory involvement in advanced stage Duchenne muscular dystrophy. Neuromuscul Disord 6, 367-376 (1996
11. Kirchmann, C., Kececioglu, D., Korinthenberg, R. & Dittrich, S. Echocardiographic and electrocardiographic findings of cardiomyopathy in Duchenne and Becker-Kiener muscular dystrophies. Pediatric cardiology 26, 66-72, doi: 10.1007/s00246-004-0689-2 (2005
12. Nigro, G., Comi, L. I., Politano, L. & Bain, R. J. The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int J Cardiol 26, 271-277 (1990
13. Malerba, A., Thorogood, F. C., Dickson, G. & Graham, I. R. Dosing regimen has a significant impact on the efficiency of morpholino oligomer-induced exon skipping in mdx mice. Hum Gene Ther 20, 955-965, doi: 10.1089/hum.2008.157 (2009
14. Malerba, A, et al. Chronic systemic therapy with low-dose morpholino oligomers ameliorates the pathology and normalizes locomotor behavior in mdx mice. Mol Ther 19, 345-354, doi: 10.1038/mt.2010.261 (2011
15. Alter, J, et al. Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat Med 12, 175-177, doi: nm1345 (2006
16. Lu, Q. L, et al. Systemic delivery of antisense oligoribonucleotide restores dystrophin expression in body-wide skeletal muscles. Proc Natl Acad Sci U S A 102, 198-203, doi: 10.1073/pnas.0406700102 (2005
17. Ishizaki, M, et al. Rescue from respiratory dysfunction by transduction of full-length dystrophin to diaphragm via the peritoneal cavity in utrophin/dystrophin double knockout mice. Mol Ther 19, 1230-1235, doi: 10.1038/mt.2011.58 (2011
18. Crisp, A, et al. Diaphragm rescue alone prevents heart dysfunction in dystrophic mice. Hum Mol Genet 20, 413-421, doi: 10.1093/hmg/ddq477 (2011
19. Costas, J. M., Nye, D. J., Henley, J. B. & Plochocki, J. H. Voluntary exercise induces structural remodeling in the hearts of dystrophin-deficient mice. Muscle Nerve 42, 881-885, doi: 10.1002/mus.21783 (2010
20. Jearawiriyapaisarn, N, et al. Sustained dystrophin expression induced by peptide-conjugated morpholino oligomers in the muscles of mdx mice. Mol Ther 16, 1624-1629, doi: 10.1038/mt.2008.120 (2008
21. Yin, H, et al. Cell-penetrating peptide-conjugated antisense oligonucleotides restore systemic muscle and cardiac dystrophin expression and function. Hum Mol Genet 17, 3909-3918, doi: 10.1093/hmg/ddn293 (2008
22. Fletcher, S, et al. Morpholino oligomer-mediated exon skipping averts the onset of dystrophic pathology in the mdx mouse. Mol Ther 15, 1587-1592, doi: 10.1038/sj.mt.6300245 (2007
23. Petrof, B. J., Shrager, J. B., Stedman, H. H., Kelly, A. M. & Sweeney, H. L. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci U S A 90, 3710-3714 (1993
24. Quinlan, J. G, et al. Poloxamer 188 failed to prevent exercise-induced membrane breakdown in mdx skeletal muscle fibers. Neuromuscul Disord 16, 855-864, doi: 10.1016/j.nmd.2006.09.016 (2006
25. Potter, L. R., Yoder, A. R., Flora, D. R., Antos, L. K. & Dickey, D. M. Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handbook of experimental pharmacology. 341-366, doi: 10.1007/978-3-540-68964-5 15 (2009
26. Kuroda, J, et al. NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci U S A 107, 15565-15570, doi: 10.1073/pnas.1002178107 (2010
27. Spurney, C. F, et al. Dystrophin-deficient cardiomyopathy in mouse: expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart. Neuromuscul Disord 18, 371-381, doi: 10.1016/j.nmd.2008.03.008 (2008
28. Loufrani, L, et al. Absence of dystrophin in mice reduces NO-dependent vascular function and vascular density: total recovery after a treatment with the aminoglycoside gentamicin. Arterioscler Thromb Vasc Biol 24, 671-676, doi: 10.1161/01. ATV.0000118683.99628.42 (2004
29. De Troyer, A. & Estenne, M. Functional anatomy of the respiratory muscles. Clinics in chest medicine 9, 175-193 (1988
30. Loufrani, L, et al. Flow (shear stress)-induced endothelium-dependent dilation is altered in mice lacking the gene encoding for dystrophin. Circulation 103, 864-870 (2001
31. Loufrani, L., Levy, B. I. & Henrion, D. Defect in microvascular adaptation to chronic changes in blood flow in mice lacking the gene encoding for dystrophin. Circ Res 91, 1183-1189 (2002
32. Palladino, M, et al. Angiogenic impairment of the vascular endothelium: a novel mechanism and potential therapeutic target in muscular dystrophy. Arteriosclerosis, thrombosis, and vascular biology 33, 2867-2876, doi: 10.1161/ATVBAHA.112.301172 (2013).
33. Ito, K, et al. Smooth muscle-specific dystrophin expression improves aberrant vasoregulation in mdx mice. Hum Mol Genet 15, 2266-2275, doi: 10.1093/hmg/ddl151 (2006
34. Malerba, A., Boldrin, L. & Dickson, G. Long-Term systemic administration of unconjugated morpholino oligomers for therapeutic expression of dystrophin by exon skipping in skeletal muscle: implications for cardiac muscle integrity. Nucleic Acid Ther 21, 293-298, doi: 10.1089/nat.2011.0306 (2011
35. Asai, A, et al. Primary role of functional ischemia, quantitative evidence for the two-hit mechanism, and phosphodiesterase-5 inhibitor therapy in mouse muscular dystrophy. PLoS One 2, e806, doi: 10.1371/journal.pone.0000806 (2007
36. Mosqueira, M., Baby, S. M., Lahiri, S. & Khurana, T. S. Ventilatory chemosensory drive is blunted in the mdx mouse model of Duchenne Muscular Dystrophy (DMD). PLoS One 8, e69567, doi: 10.1371/journal.pone.0069567 (2013
37. Betts, C, et al. Pip6-PMO, A New Generation of Peptide-oligonucleotide Conjugates With Improved Cardiac Exon Skipping Activity for DMD Treatment. Molecular therapy. Nucleic acids 1, e38, doi: 10.1038/mtna.2012.30 (2012
38. Yin, H, et al. Pip5 transduction peptides direct high efficiency oligonucleotide-mediated dystrophin exon skipping in heart and phenotypic correction in mdx mice. Mol Ther 19, 1295-1303, doi: 10.1038/mt.2011.79 (2011
39. Stuckey, D. J, et al. In vivo MRI Characterization of Progressive Cardiac Dysfunction in the mdx Mouse Model of Muscular Dystrophy. PLoS One 7, e28569, doi: 10.1371/journal.pone.0028569 PONE-D-11-08745 (2012