Uniform low-level dystrophin expression in the heart partially preserved cardiac function in an aged mouse model of Duchenne cardiomyopathy

Journal of Molecular and Cellular Cardiology

Volumn 102, Issue , 2017, Pages 45-52

  Wasala, Nalinda B ^a   Yue, Yongping ^a   Vance, Jenna ^a   Duan, Dongsheng ^a,b,c  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

AAV; Adeno associated virus; Dilated cardiomyopathy; DMD; Duchenne cardiomyopathy; Duchenne muscular dystrophy; Dystrophin; ECG; Gene therapy; Heart; Hemodynamics; Low level expression

Indexed keywords

CALSEQUESTERIN; DYSTROPHIN; DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; PEPTIDES AND PROTEINS; PHOSPHOLAMBAN; PROTEIN SERCA2A; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG; UTROPHIN; BIOLOGICAL MARKER; CALCIUM BINDING PROTEIN; CALSEQUESTRIN;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOMYOPATHY; CONTROLLED STUDY; DIASTOLE; DUCHENNE MUSCULAR DYSTROPHY; ELECTROCARDIOGRAPHY; FEMALE; HEART FUNCTION; HEART HEMODYNAMICS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QRS INTERVAL; WESTERN BLOTTING; AGE; ANIMAL; CARDIAC MUSCLE; CARDIOMYOPATHIES; COMPLICATION; DISEASE MODEL; GENE EXPRESSION; GENETICS; HEART VENTRICLE FUNCTION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

AGE FACTORS; ANIMALS; BIOMARKERS; CALCIUM-BINDING PROTEINS; CALSEQUESTRIN; CARDIOMYOPATHIES; DIASTOLE; DISEASE MODELS, ANIMAL; DYSTROPHIN; ELECTROCARDIOGRAPHY; GENE EXPRESSION; MICE; MUSCULAR DYSTROPHY, DUCHENNE; MYOCARDIUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; VENTRICULAR FUNCTION;

EID: 85006391368     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2016.11.011     Document Type: Article

References (51)

1. [1] Kunkel, L.M., 2004 William Allan award address. Cloning of the DMD gene. Am. J. Hum. Genet. 76 (2005), 205–214.
2. [2] Hoffman, E.P., Brown, R.H. Jr., Kunkel, L.M., Dystrophin: the protein product of the duchenne muscular dystrophy locus. Cell 51 (1987), 919–928.
3. [3] Emery, A.E.H., Muntoni, F., Duchenne Muscular Dystrophy. 3rd ed. Oxford, 2003, Oxford University Press, New York.
4. [4] Muntoni, F., Cardiomyopathy in muscular dystrophies. Curr. Opin. Neurol. 16 (2003), 577–583.
5. [5] Finsterer, J., Stollberger, C., The heart in human dystrophinopathies. Cardiology 99 (2003), 1–19.
6. [6] Cox, G.F., Kunkel, L.M., Dystrophies and heart disease. Curr. Opin. Cardiol. 12 (1997), 329–343.
7. [7] Duan, D., Dystrophin gene replacement and gene repair therapy for Duchenne muscular dystrophy in 2016. Hum. Gene Ther. Clin. Dev. 27 (2016), 9–18.
8. [8] Bengtsson, N.E., Seto, J.T., Hall, J.K., Chamberlain, J.S., Odom, G.L., Progress and prospects of gene therapy clinical trials for the muscular dystrophies. Hum. Mol. Genet. 25:R1 (2016), R9–17.
9. [9] Phelps, S.F., Hauser, M.A., Cole, N.M., Rafael, J.A., Hinkle, R.T., Faulkner, J.A., et al. Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum. Mol. Genet. 4 (1995), 1251–1258.
10. [10] Wells, D.J., Wells, K.E., Asante, E.A., Turner, G., Sunada, Y., Campbell, K.P., et al. Expression of human full-length and minidystrophin in transgenic mdx mice: implications for gene therapy of Duchenne muscular dystrophy. Hum. Mol. Genet. 4 (1995), 1245–1250.
11. [11] Godfrey, C., Muses, S., McClorey, G., Wells, K.E., Coursindel, T., Terry, R.L., et al. How much dystrophin is enough: the physiological consequences of different levels of dystrophin in the mdx mouse. Hum. Mol. Genet. 24 (2015), 4225–4237.
12. [12] Sharp, P.S., Bye-a-Jee, H., Wells, D.J., Physiological characterization of muscle strength with variable levels of dystrophin restoration in mdx mice following local antisense therapy. Mol. Ther. 19 (2011), 165–171.
13. [13] Neri, M., Torelli, S., Brown, S., Ugo, I., Sabatelli, P., Merlini, L., et al. Dystrophin levels as low as 30% are sufficient to avoid muscular dystrophy in the human. Neuromuscul. Disord. 17 (2007), 913–918.
14. [14] Li, D., Yue, Y., Duan, D., Preservation of muscle force in mdx3cv mice correlates with low-level expression of a near full-length dystrophin protein. Am. J. Pathol. 172 (2008), 1332–1341.
15. [15] Li, D., Yue, Y., Duan, D., Marginal level dystrophin expression improves clinical outcome in a strain of dystrophin/utrophin double knockout mice. PLoS One, 5, 2010, e15286.
16. [16] van Putten, M., Hulsker, M., Nadarajah, V.D., van Heiningen, S.H., van Huizen, E., van Iterson, M., et al. The effects of low levels of dystrophin on mouse muscle function and pathology. PLoS One, 7, 2012, e31937.
17. [17] van Putten, M., Hulsker, M., Young, C., Nadarajah, V.D., Heemskerk, H., van der Weerd, L., et al. Low dystrophin levels increase survival and improve muscle pathology and function in dystrophin/utrophin double-knockout mice. FASEB J. 27 (2013), 2484–2495.
18. [18] Chamberlain, J.S., Dystrophin levels required for correction of Duchenne muscular dystrophy. Basic Appl. Myol. 7 (1997), 251–255.
19. [19] Hoffman, E.P., Arahata, K., Minetti, C., Bonilla, E., Rowland, L.P., Dystrophinopathy in isolated cases of myopathy in females. Neurology 42 (1992), 967–975.
20. [20] Arpke, R.W., Darabi, R., Mader, T.L., Zhang, Y., Toyama, A., Lonetree, C.L., et al. A new immuno-, dystrophin-deficient model, the NSG-mdx4cv mouse, provides evidence for functional improvement following allogeneic satellite cell transplantation. Stem Cells 31 (2013), 1611–1620.
21. [21] van Putten, M., van der Pijl, E.M., Hulsker, M., Verhaart, I.E., Nadarajah, V.D., van der Weerd, L., et al. Low dystrophin levels in heart can delay heart failure in mdx mice. J. Mol. Cell. Cardiol. 69 (2014), 17–23.
22. [22] Wu, B., Xiao, B., Cloer, C., Shaban, M., Sali, A., Lu, P., et al. One-year treatment of morpholino antisense oligomer improves skeletal and cardiac muscle functions in dystrophic mdx mice. Mol. Ther. 19 (2011), 576–583.
23. [23] Yue, Y., Skimming, J.W., Liu, M., Strawn, T., Duan, D., Full-length dystrophin expression in half of the heart cells ameliorates beta-isoproterenol-induced cardiomyopathy in mdx mice. Hum. Mol. Genet. 13 (2004), 1669–1675.
24. [24] Bostick, B., Yue, Y., Long, C., Duan, D., Prevention of dystrophin-deficient cardiomyopathy in twenty-one-month-old carrier mice by mosaic dystrophin expression or complementary dystrophin/utrophin expression. Circ. Res. 102 (2008), 121–130.
25. [25] Cox, G.A., Phelps, S.F., Chapman, V.M., Chamberlain, J.S., New mdx mutation disrupts expression of muscle and nonmuscle isoforms of dystrophin. Nat. Genet. 4 (1993), 87–93.
26. [26] Rafael, J.A., Nitta, Y., Peters, J., Davies, K.E., Testing of SHIRPA, a mouse phenotypic assessment protocol, on Dmd(mdx) and Dmd(mdx3cv) dystrophin-deficient mice. Mamm. Genome 11 (2000), 725–728.
27. [27] Chapman, V.M., Miller, D.R., Armstrong, D., Caskey, C.T., Recovery of induced mutations for X chromosome-linked muscular dystrophy in mice. Proc. Natl. Acad. Sci. 86 (1989), 1292–1296.
28. [28] Bostick, B., Yue, Y., Duan, D., Gender influences cardiac function in the mdx model of Duchenne cardiomyopathy. Muscle Nerve 42 (2010), 600–603.
29. [29] Lai, Y., Zhao, J., Yue, Y., Wasala, N.B., Duan, D., Partial restoration of cardiac function with ∆ PDZ nNOS in aged mdx model of Duchenne cardiomyopathy. Hum. Mol. Genet. 23 (2014), 3189–3199.
30. [30] Bostick, B., Yue, Y., Duan, D., Phenotyping cardiac gene therapy in mice. Methods Mol. Biol. 709 (2011), 91–104 (Clifton, NJ).
31. [31] Wasala, N.B., Bostick, B., Yue, Y., Duan, D., Exclusive skeletal muscle correction does not modulate dystrophic heart disease in the aged mdx model of Duchenne cardiomyopathy. Hum. Mol. Genet. 22 (2013), 2634–2641.
32. [32] Bostick, B., Shin, J.H., Yue, Y., Wasala, N.B., Lai, Y., Duan, D., AAV micro-dystrophin gene therapy alleviates stress-induced cardiac death but not myocardial fibrosis in > 21-m-old mdx mice, an end-stage model of Duchenne muscular dystrophy cardiomyopathy. J. Mol. Cell. Cardiol. 53 (2012), 217–222.
33. [33] Bostick, B., Shin, J.H., Yue, Y., Duan, D., AAV-microdystrophin therapy improves cardiac performance in aged female mdx mice. Mol. Ther. 19 (2011), 1826–1832.
34. [34] Aartsma-Rus, A., Ferlini, A., Goemans, N., Pasmooij, A.M., Wells, D.J., Bushby, K., et al. Translational and regulatory challenges for exon skipping therapies. Hum. Gene Ther. 25 (2014), 885–892.
35. [35] Koo, T., Wood, M.J., Clinical trials using antisense oligonucleotides in Duchenne muscular dystrophy. Hum. Gene Ther. 24 (2013), 479–488.
36. [36] Nelson, C.E., Hakim, C.H., Ousterout, D.G., Thakore, P.I., Moreb, E.A., Rivera, R.M., et al. In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351 (2016), 403–407.
37. [37] Townsend, D., Daly, M., Chamberlain, J.S., Metzger, J.M., Age-dependent dystrophin loss and genetic reconstitution establish a molecular link between dystrophin and heart performance during aging. Mol. Ther. 19 (2011), 1821–1825.
38. [38] Wasala, N.B., Lai, Y., Shin, J.H., Zhao, J., Yue, Y., Duan, D., Genomic removal of a therapeutic mini-dystrophin gene from adult mice elicits a Duchenne muscular dystrophy-like phenotype. Hum. Mol. Genet. 25 (2016), 2633–2644.
39. [39] Guiraud, S., Aartsma-Rus, A., Vieira, N.M., Davies, K.E., van Ommen, G.J., Kunkel, L.M., The pathogenesis and therapy of muscular dystrophies. Annu. Rev. Genomics Hum. Genet. 16 (2015), 281–308.
40. [40] Shirokova, N., Niggli, E., Cardiac phenotype of duchenne muscular dystrophy: insights from cellular studies. J. Mol. Cell. Cardiol. 58 (2013), 217–224.
41. [41] Kamdar, F., Garry, D.J., Dystrophin-deficient cardiomyopathy. J. Am. Coll. Cardiol. 67 (2016), 2533–2546.
42. [42] van Westering, T.L., Betts, C.A., Wood, M.J., Current understanding of molecular pathology and treatment of cardiomyopathy in duchenne muscular dystrophy. Molecules 20 (2015), 8823–8855.
43. [43] Bostick, B., Yue, Y., Lai, Y., Long, C., Li, D., Duan, D., Adeno-associated virus serotype-9 microdystrophin gene therapy ameliorates electrocardiographic abnormalities in mdx mice. Hum. Gene Ther. 19 (2008), 851–856.
44. [44] Gavillet, B., Rougier, J.S., Domenighetti, A.A., Behar, R., Boixel, C., Ruchat, P., et al. Cardiac sodium channel Nav1.5 is regulated by a multiprotein complex composed of syntrophins and dystrophin. Circ. Res. 99 (2006), 407–414.
45. [45] Willis, B.C., Ponce-Balbuena, D., Jalife, J., Protein assemblies of sodium and inward rectifier potassium channels control cardiac excitability and arrhythmogenesis. Am. J. Physiol. Heart Circ. Physiol. 308 (2015), H1463–H1473.
46. [46] Barouch, L.A., Harrison, R.W., Skaf, M.W., Rosas, G.O., Cappola, T.P., Kobeissi, Z.A., et al. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature 416 (2002), 337–339.
47. [47] Ahern, G.P., Hsu, S.F., Klyachko, V.A., Jackson, M.B., Induction of persistent sodium current by exogenous and endogenous nitric oxide. J. Biol. Chem. 275 (2000), 28810–28815.
48. [48] Li, D., Yue, Y., Lai, Y., Hakim, C.H., Duan, D., Nitrosative stress elicited by nNOSμ delocalization inhibits muscle force in dystrophin-null mice. J. Pathol. 223 (2011), 88–98.
49. [49] Mitchell, G.F., Jeron, A., Koren, G., Measurement of heart rate and Q-T interval in the conscious mouse. Am. J. Phys. 274 (1998), H747–H751.
50. [50] Nigro, G., Comi, L.I., Politano, L., Nigro, G., Cardiomyopathies associated with muscular dystrophies. Engel, A., Franzini-Armstrong, C., (eds.) Myology: Basic and Clinical, third ed., 2004, McGraw-Hill, Medical Pub. Division, New York, 1239–1256.
51. [51] Duan, D., Rafael-Fortney, J.A., Blain, A., Kass, D.A., McNally, E.M., Metzger, J.M., et al. Standard operating procedures (SOPs) for evaluating the heart in preclinical studies of Duchenne muscular dystrophy. J. Cardiovasc. Transl. Res. 9 (2016), 85–86.