Prevention of exercised induced cardiomyopathy following Pip-PMO treatment in dystrophic mdx mice

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Betts, Corinne A ^a   Saleh, Amer F ^b,d   Carr, Carolyn A ^a   Hammond, Suzan M ^a   Coenen Stass, Anna M L ^a   Godfrey, Caroline ^a   McClorey, Graham ^a   Varela, Miguel A ^a   Roberts, Thomas C ^a,c   Clarke, Kieran ^a   Gait, Michael J ^b   Wood, Matthew J A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d ASTRAZENECA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; DYSTROPHIN; MORPHOLINO OLIGONUCLEOTIDE;

ADVERSE EFFECTS; ANIMAL; ANIMAL EXPERIMENT; CARDIAC MUSCLE; CARDIOMYOPATHIES; CARDIOMYOPATHY, DILATED; CINE MAGNETIC RESONANCE IMAGING; COMPLICATION; DISEASE MODEL; DUCHENNE MUSCULAR DYSTROPHY; FIBROSIS; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MOUSE; PATHOLOGY; PHENOTYPE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; BIOMARKERS; CARDIOMYOPATHIES; CARDIOMYOPATHY, DILATED; DISEASE MODELS, ANIMAL; DYSTROPHIN; FIBROSIS; GENE EXPRESSION; HUMANS; MAGNETIC RESONANCE IMAGING, CINE; MICE; MICE, INBRED MDX; MORPHOLINOS; MUSCULAR DYSTROPHY, DUCHENNE; MYOCARDIUM; PHENOTYPE; PHYSICAL CONDITIONING, ANIMAL;

EID: 84924777861     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08986     Document Type: Article

References (56)

1. Emery, A. E. Population frequencies of inherited neuromuscular diseases - aworld survey. Neuromuscul Disord 1, 19-29 (1991).
2. 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 (2005).
3. 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).
4. th June 2002, Naarden, the Netherlands. Neuromuscul Disord 13, 166-172 (2003).
5. Sultan, A. & Fayaz, M. Prevalence of cardiomyopathy in Duchenne and Becker's muscular dystrophy. Journal of Ayub Medical College, Abbottabad: JAMC 20, 7-13 (2008).
6. 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 (2005).
7. 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 (2008).
8. Goemans, N. & Buyse, G. Current treatment and management of dystrophinopathies. Current treatment options in neurology 16, 287 (2014).
9. Barton-Davis, E. R., Cordier, L., Shoturma, D. I., Leland, S. E. & Sweeney, H. L. Aminoglycoside antibiotics restore dystrophin function to skeletal muscles of mdx mice. J Clin Invest 104, 375-381 (1999).
10. Rodino-Klapac, L. R. et al. Persistent expression of FLAG-tagged micro dystrophin in nonhuman primates following intramuscular and vascular delivery. Mol Ther 18, 109-117 (2010).
11. Goyenvalle, A. et al. Rescue of severely affected dystrophin/utrophin-deficient mice through scAAV-U7snRNA-mediated exon skipping. Hum Mol Genet 21, 2559-2571 (2012).
12. Mattei, E. et al. Utrophin up-regulation by an artificial transcription factor in transgenic mice. PLoS One 2, e774 (2007).
13. Tinsley, J. M. et al. Daily treatment with SMTC1100, a novel small molecule utrophin upregulator, dramatically reduces the dystrophic symptoms in the mdx mouse. PLoS One 6, e19189 (2011).
14. Dickson, G., Hill, V. & Graham, I. R. Screening for antisense modulation of dystrophin pre-mRNA splicing. Neuromuscul Disord 12 Suppl 1, S67-70 (2002).
15. Alter, J. et al. Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat Med 12, 175-177 (2006).
16. 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).
17. Goemans, N. M. et al. Systemic administration of PRO051 in Duchenne's muscular dystrophy. N Engl J Med 364, 1513-1522 (2011).
18. van Deutekom, J. C. et al. Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 357, 2677-2686 (2007).
19. Cirak, S. et al. Restoration of the dystrophin-associated glycoprotein complex after exon skipping therapy in Duchenne muscular dystrophy. Mol Ther 20, 462-467 (2012).
20. Kinali, M. et al. Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol 8, 918-928 (2009).
21. Voit, T. et al. Safety and efficacy of drisapersen for the treatment of Duchenne muscular dystrophy (DEMAND II): an exploratory, randomised, placebo-controlled phase 2 study. Lancet Neurol 13 (2014).
22. 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, 345-35 (2011).
23. 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 (2005).
24. Jearawiriyapaisarn, N. et al. Sustained dystrophin expression induced by peptide-conjugated morpholino oligomers in the muscles of mdx mice. Mol Ther 16, 1624-1629 (2008).
25. Yin, H. et al. A fusion peptide directs enhanced systemic dystrophin exon skipping and functional restoration in dystrophin-deficient mdx mice. Hum Mol Genet 18, 4405-4414 (2009).
26. Yin, H. et al. Functional rescue of dystrophin-deficient mdx mice by a chimeric peptide-PMO. Mol Ther 18, 1822-1829 (2010).
27. Wu, B. et al. Effective rescue of dystrophin improves cardiac function in dystrophin-deficient mice by amodified morpholino oligomer. Proc Natl Acad Sci U S A 105, 14814-14819 (2008).
28. Crisp, A. et al. Diaphragm rescue alone prevents heart dysfunction in dystrophic mice. Hum Mol Genet 20, 413-421 (2011).
29. Abes, S. et al. Efficient splicing correction by PNA conjugation to an R6-Penetratin delivery peptide. Nucleic Acids Res 35, 4495-4502 (2007).
30. Betts, C. et al. Pip6-PMO, A New Generation of Peptide-oligonucleotide Conjugates With Improved Cardiac Exon Skipping Activity for DMDTreatment. Molecular therapy. Nucleic acids 1, e38 (2012).
31. 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 (2011).
32. Ivanova, G. D. et al. Improved cell-penetrating peptide-PNA conjugates for splicing redirection in HeLa cells and exon skipping in mdx mouse muscle. Nucleic Acids Res 36, 6418-6428 (2008).
33. Costas, J. M., Nye, D. J., Henley, J. B. & Plochocki, J. H. Voluntary exercise induces structural remodeling in the hearts of dystrophin-deficientmice. Muscle Nerve 42, 881-885 (2010).
34. Nakamura, A., Yoshida, K., Takeda, S., Dohi, N. & Ikeda, S. Progression of dystrophic features and activation of mitogen-activated protein kinases and calcineurin by physical exercise, in hearts of mdx mice. FEBS letters 520, 18-24 (2002).
35. 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 (2012).
36. 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 191, 341-366 (2009).
37. McGrath, M. F., de Bold, M. L. & de Bold, A. J. The endocrine function of the heart. Trends in endocrinology and metabolism: TEM 16, 469-477 (2005).
38. Zhang, M., Perino, A., Ghigo, A., Hirsch, E. & Shah, A. M. NADPH oxidases in heart failure: poachers or gamekeepers? Antioxidants & redox signaling 18, 1024-1041 (2013).
39. Spurney, C. F. et al. Dystrophin-deficient cardiomyopathy inmouse: expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart. Neuromuscul Disord 18, 371-381 (2008).
40. Condorelli, G., Latronico, M. V. & Cavarretta, E. microRNAs in Cardiovascular Diseases: Current Knowledge and the Road Ahead. J Am Coll Cardiol 63, 2177-2187 (2014).
41. Cirak, S. et al. Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study. Lancet 378, 595-605 (2011).
42. Heemskerk, H. A. et al. In vivo comparison of 2'-O-methyl phosphorothioate and morpholino antisense oligonucleotides for Duchenne muscular dystrophy exon skipping. J Gene Med 11, 257-266 (2009).
43. Call, J. A. et al. Endurance capacity in maturing mdx mice is markedly enhanced by combined voluntary wheel running and green tea extract. J Appl Physiol 105, 923-932 (2008).
44. Buyse, G. M. et al. Long-term blinded placebo-controlled study of SNT-MC17/idebenone in the dystrophin deficient mdx mouse: cardiac protection and improved exercise performance. European heart journal 30, 116-124 (2009).
45. Stuckey, D. J., Carr, C. A., Tyler, D. J. & Clarke, K. Cine-MRI versus twodimensional echocardiography to measure in vivo left ventricular function in rat heart. NMR Biomed 21 (2008).
46. Jefferies, J. L. et al. Genetic predictors and remodeling of dilated cardiomyopathy in muscular dystrophy. Circulation 112, 2799-2804 (2005).
47. Townsend, D., Yasuda, S., Li, S., Chamberlain, J. S. & Metzger, J. M. Emergent dilated cardiomyopathy caused by targeted repair of dystrophic skeletal muscle. Mol Ther 16, 832-835 (2008).
48. Sanyal, S. K., Johnson, W. W., Thapar, M. K. & Pitner, S. E. An ultrastructural basis for electrocardiographic alterations associated with Duchenne's progressive muscular dystrophy. Circulation 57, 1122-1129 (1978).
49. Perloff, J. K., Roberts, W. C., de Leon, A. C., Jr. & O'Doherty, D. The distinctive electrocardiogram of Duchenne's progressive muscular dystrophy. An electrocardiographic-pathologic correlative study. Am JMed 42, 179-188 (1967).
50. Khairallah, M. et al. Metabolic and signaling alterations in dystrophin-deficient hearts precede overt cardiomyopathy. J Mol Cell Cardiol 43, 119-129 (2007).
51. Burelle, Y. et al. Alterations in mitochondrial function as a harbinger of cardiomyopathy: lessons from the dystrophic heart. J Mol Cell Cardiol 48, 310-321 (2010).
52. McCauley, M. D. & Wehrens, X. H. Animal models of arrhythmogenic cardiomyopathy. Disease models & mechanisms 2, 563-570 (2009).
53. Gedicke-Hornung, C. et al. Rescue of cardiomyopathy through U7snRNA-mediated exon skipping in Mybpc3-targeted knock-in mice. EMBO molecular medicine 5, 1128-1145 (2013).
54. Arechavala-Gomeza, V. et al. Immunohistological intensity measurements as a tool to assess sarcolemma-associated protein expression. Neuropathol Appl Neurobiol 36, 265-274 (2010).
55. Roberts, T. C. et al. Extracellular microRNAs are dynamic non-vesicular biomarkers of muscle turnover. Nucleic Acids Res 41, 9500-9513 (2013).
56. Roberts, T. C. et al. Expression Analysis in Multiple Muscle Groups and Serum Reveals Complexity in the MicroRNA Transcriptome of the mdx Mouse with Implications for Therapy. Molecular therapy. Nucleic acids 1, e39 (2012).