Genomic removal of a therapeutic mini-dystrophin gene from adult mice elicits a Duchenne muscular dystrophy-like phenotype

Human Molecular Genetics

Volumn 25, Issue 13, 2016, Pages 2633-2644

  Wasala, Nalinda B ^a   Lai, Yi ^a   Shin, Jin Hong ^a,c   Zhao, Junling ^a   Yue, Yongping ^a   Duan, Dongsheng ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c Yangsan Hospital   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; DYSTROPHIN; GLYCOPROTEIN;

ADENO ASSOCIATED VIRUS 9; ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENSITOMETRY; DUCHENNE MUSCULAR DYSTROPHY; ELECTROCARDIOGRAPHY; FEMALE; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENE LOSS; HEART EJECTION FRACTION; HEART MUSCLE FIBROSIS; HEMODYNAMICS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LOXP SITE; MALE; MINI DYSTROPHIN GENE; MOUSE; MUSCLE ATROPHY; MUSCLE FUNCTION; MUSCLE LENGTH; NONHUMAN; PHENOTYPE; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; TRANSGENIC MOUSE; UPREGULATION; VIRUS GENOME; WESTERN BLOTTING; ANIMAL; ANIMAL MUSCULAR DYSTROPHY; CARDIAC MUSCLE; CBA MOUSE; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; GENOMICS; METABOLISM; PHYSIOLOGY; PROCEDURES; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; DYSTROPHIN; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; GENOMICS; MICE; MICE, INBRED CBA; MICE, INBRED MDX; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; MYOCARDIUM;

EID: 85015983319     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw123     Document Type: Article

References (52)

1. Kunkel, L.M. (2005) 2004 William Allan Award address. Cloning of the DMD gene. Am. J. Hum. Genet., 76, 205-214.
2. Mendell, J.R. and Lloyd-Puryear, M. (2013) Report of MDA muscle disease symposium on newborn screening for Duchenne muscular dystrophy. Muscle Nerve, 48, 21-26.
3. Bengtsson, N.E., Seto, J.T., Hall, J.K., Chamberlain, J.S. and Odom, G.L. (2016) Progress and prospects of gene therapy clinical trials for themuscular dystrophies. Hum. Mol. Genet., 25, R9-R17.
4. Duan, D. (2015) Duchenne muscular dystrophy gene therapy in the canine model. Hum. Gene Ther. Clin. Dev., 26, 57-69.
5. Al-Zaidy, S., Rodino-Klapac, L. and Mendell, J.R. (2014) Gene therapy for muscular dystrophy: moving the field forward. Pediatr. Neurol., 51, 607-618.
6. Kawecka, K., Theodoulides, M., Hasoglu, Y., Jarmin, S., Kymalainen, H., Le-Heron, A., Popplewell, L., Malerba, A., Dickson, G. and Athanasopoulos, T. (2015) Adeno-associated virus (AAV) mediated dystrophin gene transfer studies and exon skipping strategies for Duchenne muscular dystrophy (DMD). Curr. Gene Ther., 15, 395-415.
7. Ghahramani Seno, M.M., Graham, I.R., Athanasopoulos, T., Trollet, C., Pohlschmidt, M., Crompton, M.R. and Dickson, G. (2008) RNAi-mediated knockdown of dystrophin expression in adult mice does not lead to overt muscular dystrophy pathology. Hum. Mol. Genet., 17, 2622-2632.
8. Duan, D. (2008) Dystrophin knockdown mice suggest that early, transient dystrophin expression might be enough to prevent later pathology. Neuromuscul. Disord., 18, 904-905.
9. Ahmad, A., Brinson, M., Hodges, B.L., Chamberlain, J.S. and Amalfitano, A. (2000) Mdx mice inducibly expressing dystrophin provide insights into the potential of gene therapy for duchennemuscular dystrophy. Hum. Mol. Genet., 9, 2507-2515.
10. Wasala, N.B., Zhang, K., Wasala, L.P., Hakim, C.H. and Duan, D. (2015) The FVB background does not dramatically alter the dystrophic phenotype of mdx mice. PLoS Curr., 7, pii:ecurrents. md.28266819ca28266810ec28266815fefcac28266767 ea28266819a28263461c.
11. Lai, Y., Thomas, G.D., Yue, Y., Yang, H.T., Li, D., Long, C., Judge, L., Bostick, B., Chamberlain, J.S., Terjung, R.L. et al. (2009) Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J. Clin. Invest., 119, 624-635.
12. Zhang, Y., Yue, Y., Li, L., Hakim, C.H., Zhang, K., Thomas, G.D. and Duan, D. (2013) Dual AAV therapy ameliorates exercise-induced muscle injury and functional ischemia in murine models of Duchenne muscular dystrophy. Hum. Mol. Genet., 22, 3720-3729.
13. Zhang, Y. and Duan, D. (2012) Novel mini-dystrophin gene dual adeno-associated virus vectors restore neuronal nitric oxide synthase expression at the sarcolemma. Hum. Gene Ther., 23, 98-103.
14. Hoffman, E.P., Brown, R.H., Jr and Kunkel, L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell, 51, 919-928.
15. Bonilla, E., Samitt, C.E., Miranda, A.F., Hays, A.P., Salviati, G., DiMauro, S., Kunkel, L.M., Hoffman, E.P. and Rowland, L.P. (1988) Duchenne muscular dystrophy: deficiency of dystrophin at the muscle cell surface. Cell, 54, 447-452.
16. Merrick, D., Stadler, L.K., Larner, D. and Smith, J. (2009) Muscular dystrophy begins early in embryonic development deriving from stem cell loss and disrupted skeletal muscle formation. Dis. Model. Mech., 2, 374-388.
17. Castro-Gago, M. (2014) Milder course in Duchenne patients with nonsense mutations and no muscle dystrophin. Neuromuscul. Disord., 25, 443.
18. Zatz, M., Pavanello, R.C., Lazar, M., Yamamoto, G.L., Lourenco, N.C., Cerqueira, A., Nogueira, L. and Vainzof, M. (2014) Milder course in Duchenne patients with nonsense mutations and no muscle dystrophin. Neuromuscul. Disord., 24, 986-989.
19. Grange, R.W., Gainer, T.G., Marschner, K.M., Talmadge, R.J. and Stull, J.T. (2002) Fast-twitch skeletal muscles of dystrophic mouse pups are resistant to injury from acute mechanical stress. Am. J. Physiol. Cell Physiol., 283, C1090-C1101.
20. Reed, P. and Bloch, R.J. (2005) Postnatal changes in sarcolemmal organization in the mdx mouse. Neuromuscul. Disord., 15, 552-561.
21. Grady, R.M., Teng, H., Nichol, M.C., Cunningham, J.C., Wilkinson, R.S. and Sanes, J.R. (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell, 90, 729-738.
22. Deconinck, A.E., Rafael, J.A., Skinner, J.A., Brown, S.C., Potter, A.C., Metzinger, L., Watt, D.J., Dickson, J.G., Tinsley, J.M. and Davies, K.E. (1997) Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell, 90, 717-727.
23. Shin, J.H., Pan, X., Hakim, C.H., Yang, H.T., Yue, Y., Zhang, K., Terjung, R.L. and Duan, D. (2013) Microdystrophin ameliorates muscular dystrophy in the canine model of Duchenne muscular dystrophy. Mol. Ther., 21, 750-757.
24. Yue, Y., Pan, X., Hakim, C.H., Kodippili, K., Zhang, K., Shin, J.H., Yang, H.T., McDonald, T. and Duan, D. (2015) Safe and bodywide muscle transduction in young adult Duchenne muscular dystrophy dogs with adeno-associated virus. Hum. Mol. Genet., 24, 5880-5890.
25. Liu, M., Yue, Y., Harper, S.Q., Grange, R.W., Chamberlain, J.S. and Duan, D. (2005) Adeno-associated virus-mediated microdystrophin expression protects young mdx muscle fromcontraction-induced injury. Mol. Ther., 11, 245-256.
26. Bostick, B., Ghosh, A., Yue, Y., Long, C. and Duan, D. (2007) Systemic AAV-9 transduction in mice is influenced by animal age but not by the route of administration. Gene Ther., 14, 1605-1609.
27. Davis, J., Maillet, M., Miano, J.M. and Molkentin, J.D. (2012) Lost in transgenesis: a user's guide for genetically manipulating the mouse in cardiac research. Circ. Res., 111, 761-777.
28. Iwatate, M., Gu, Y., Dieterle, T., Iwanaga, Y., Peterson, K.L., Hoshijima, M., Chien, K.R. and Ross, J. (2003) In vivo highefficiency transcoronary gene delivery and Cre-LoxP gene switching in the adult mouse heart. Gene Ther., 10, 1814-1820.
29. Werfel, S., Jungmann, A., Lehmann, L., Ksienzyk, J., Bekeredjian, R., Kaya, Z., Leuchs, B., Nordheim, A., Backs, J., Engelhardt, S. et al. (2014) Rapid and highly efficient inducible cardiac gene knockout in adult mice using AAVmediated expression of Cre recombinase. Cardiovasc. Res., 104, 15-23.
30. Bostick, B., Shin, J.H., Yue, Y., Wasala, N.B., Lai, Y. and Duan, D. (2012) 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, 217-222.
31. Bostick, B., Shin, J.H., Yue, Y. and Duan, D. (2011) AAV-microdystrophin therapy improves cardiac performance in aged female mdx mice. Mol. Ther., 19, 1826-1832.
32. Ghosh, A., Yue, Y., Shin, J.H. and Duan, D. (2009) Systemic trans-splicing AAV delivery efficiently transduces the heart of adult mdx mouse, a model for Duchenne muscular dystrophy. Hum. Gene. Ther., 20, 1319-1328.
33. van Putten, M., Hulsker, M., Nadarajah, V.D., van Heiningen, S.H., van Huizen, E., van Iterson, M., Admiraal, P., Messemaker, T., den Dunnen, J.T., t Hoen, P.A. et al. (2012) The effects of low levels of dystrophin on mouse muscle function and pathology. PLoS One, 7, e31937.
34. van Putten, M., Hulsker, M., Young, C., Nadarajah, V.D., Heemskerk, H., van der Weerd, L., t'Hoen, P.A., van Ommen, G.J. and Aartsma-Rus, A.M. (2013) Low dystrophin levels increase survival and improve muscle pathology and function in dystrophin/utrophin double-knockout mice. FASEB J., 27, 2484-2495.
35. Li, D., Yue, Y. and Duan, D. (2010) Marginal level dystrophin expression improves clinical outcome in a strain of dystrophin/utrophin double knockout mice. PLoS One, 5, e15286.
36. Li, D., Yue, Y. and Duan, D. (2008) Preservation of muscle force in mdx3cv mice correlates with low-level expression of a near full-length dystrophin protein. Am. J. Pathol., 172, 1332-1341.
37. Godfrey, C., Muses, S., McClorey, G., Wells, K.E., Coursindel, T., Terry, R.L., Betts, C., Hammond, S., O'Donovan, L., Hildyard, J. et al. (2015) How much dystrophin is enough: the physiological consequences of different levels of dystrophin in the mdx mouse. Hum. Mol. Genet., 24, 4225-4237.
38. Yue, Y., Skimming, J.W., Liu, M., Strawn, T. and Duan, D. (2004) Full-length dystrophin expression in half of the heart cells ameliorates beta-isoproterenol-induced cardiomyopathy in mdx mice. Hum. Mol. Genet., 13, 1669-1675.
39. Bostick, B., Yue, Y., Long, C. and Duan, D. (2008) Prevention of dystrophin-deficient cardiomyopathy in twenty-onemonth-old carrier mice by mosaic dystrophin expression or complementary dystrophin/utrophin expression. Circ. Res., 102, 121-130.
40. Bostick, B., Yue, Y. and Duan, D. (2010) Gender influences cardiac function in the mdx model of Duchenne cardiomyopathy. Muscle Nerve, 42, 600-603.
41. Hakim, C.H. and Duan, D. (2012) Gender differences in contractile and passive properties of mdx extensor digitorum longus muscle. Muscle Nerve, 45, 250-256.
42. Wang, J., Xie, J., Lu, H., Chen, L., Hauck, B., Samulski, R.J. and Xiao, W. (2007) Existence of transient functional doublestranded DNA intermediates during recombinant AAV transduction. Proc. Natl. Acad. Sci. U. S. A., 104, 13104-13109.
43. Gao, G., Vandenberghe, L.H., Alvira, M.R., Lu, Y., Calcedo, R., Zhou, X. and Wilson, J.M. (2004) Clades of Adeno-associated viruses are widely disseminated in human tissues. J. Virol., 78, 6381-6388.
44. Shin, J.H., Yue, Y. and Duan, D. (2012) Recombinant adenoassociated viral vector production and purification. Methods Mol. Biol., 798, 267-284.
45. Kodippili, K., Vince, L., Shin, J.H., Yue, Y., Morris, G.E., McIntosh, M.A. and Duan, D. (2014) Characterization of 65 epitope-specific dystrophin monoclonal antibodies in canine and murine models of duchenne muscular dystrophy by immunostaining and western blot. PLoS One, 9, e88280.
46. Wasala, N.B., Bostick, B., Yue, Y. and Duan, D. (2013) Exclusive skeletal muscle correction does not modulate dystrophic heart disease in the aged mdx model of Duchenne cardiomyopathy. Hum. Mol. Genet., 22, 2634-2641.
47. Li, D., Long, C., Yue, Y. and Duan, D. (2009) Sub-physiological sarcoglycan expression contributes to compensatory muscle protection in mdx mice. Hum. Mol. Genet., 18, 1209-1220.
48. Hakim, C.H., Li, D. and Duan, D. (2011) Monitoring murine skeletal muscle function for muscle gene therapy. Methods Mol. Biol., 709, 75-89.
49. Hakim, C.H., Wasala, N.B. and Duan, D. (2013) Evaluation of muscle function of the extensor digitorum longus muscle ex vivo and tibialis anterior muscle in situ in mice. J. Vis. Exp., 72, e50183.
50. Bostick, B., Yue, Y. and Duan, D. (2011) Phenotyping cardiac gene therapy in mice. Methods Mol. Biol., 709, 91-104.
51. Mitchell, G.F., Jeron, A. and Koren, G. (1998) Measurement of heart rate and Q-T interval in the conscious mouse. Am. J. Physiol., 274, H747-H751.
52. Nigro, G., Comi, L.I., Politano, L. and Nigro, G. (2004) Cardiomyopathies associated with muscular dystrophies. In Engel, A. and Franzini-Armstrong, C. (eds), Myology: Basic and Clinical. McGraw-Hill, Medical Pub. Division, New York, Vol. 2, pp. 1239-1256.