Low dystrophin levels increase survival and improve muscle pathology and function in dystrophin/utrophin double-knockout mice

FASEB Journal

Volumn 27, Issue 6, 2013, Pages 2484-2495

  Van Putten, Maaike ^a   Hulsker, Margriet ^a   Young, Courtney ^a   Nadarajah, Vishna D ^a,b   Heemskerk, Hans ^a   Van Der Weerd, Louise ^a   'T Hoen, Peter A C ^a   Van Ommen, Gert Jan B ^a   Aartsma Rus, Annemieke M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b INTERNATIONAL MEDICAL UNIVERSITY   (Malaysia)

Author keywords

Becker muscular dystrophy; Biomarkers; Cardiomyopathy; Duchenne muscular dystrophy; Mouse models

Indexed keywords

DYSTROPHIN; UTROPHIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEATH; DUCHENNE MUSCULAR DYSTROPHY; FEMALE; HEART FAILURE; HISTOPATHOLOGY; KYPHOSIS; MOTOR PERFORMANCE; MOUSE; MUSCLE FUNCTION; MUSCLE WEAKNESS; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY FAILURE; SURVIVAL;

BECKER MUSCULAR DYSTROPHY; BIOMARKERS; CARDIOMYOPATHY; DUCHENNE MUSCULAR DYSTROPHY; MOUSE MODELS;

ANIMALS; BIOLOGICAL MARKERS; DYSTROPHIN; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICE, KNOCKOUT; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; PHENOTYPE; UTROPHIN;

ANIMALIA; MUS;

EID: 84878756586     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-224170     Document Type: Article

References (34)

1. Hoffman, E. P., Brown, R. H., Jr., and Kunkel, L. M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-9288
2. Muntoni, F., Torelli, S., and Ferlini, A. (2003) Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol. 2, 731-7400
3. Kohler, M., Clarenbach, C. F., Bahler, C., Brack, T., Russi, E. W., and Bloch, K. E. (2009) Disability and survival in Duchenne muscular dystrophy. J. Neurol. Neurosurg. Psychiatry 80, 320-3255
4. Sicinski, P., Geng, Y., Ryder-Cook, A. S., Barnard, E. A., Darlison, M. G., and Barnard, P. J. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244, 1578-15800
5. Stedman, H. H., Sweeney, H. L., Shrager, J. B., Maguire, H. C., Panettieri, R. A., Petrof, B., Narusawa, M., Leferovich, J. M., Sladky, J. T., and Kelly, A. M. (1991) The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352, 536-5399
6. 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, 717-7277
7. 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, 729-7388
8. Goemans, N. M., Tulinius, M., van den Akker, J. T., Burm, B. E., Ekhart, P. F., Heuvelmans, N., Holling, T., Janson, A. A., Platenburg, G. J., Sipkens, J. A., Sitsen, J. M., Aartsma-Rus, A., van Ommen, G. J., Buyse, G., Darin, N., Verschuuren, J. J., Campion, G. V., de Kimpe, S. J., and van Deutekom, J. C. (2011) Systemic administration of PRO051 in Duchenne's muscular dystrophy. N. Engl. J. Med. 364, 1513-15222
9. Cirak, S., Arechavala-Gomeza, V., Guglieri, M., Feng, L., Torelli, S., Anthony, K., Abbs, S., Garralda, M. E., Bourke, J., Wells, D. J., Dickson, G., Wood, M. J., Wilton, S. D., Straub, V., Kole, R., Shrewsbury, S. B., Sewry, C., Morgan, J. E., Bushby, K., and Muntoni, F. (2011) 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, 595-6055
10. Bowles, D. E., McPhee, S. W., Li, C., Gray, S. J., Samulski, J. J., Camp, A. S., Li, J., Wang, B., Monahan, P. E., Rabinowitz, J. E., Grieger, J. C., Govindasamy, L., Agbandje-McKenna, M., Xiao, X., and Samulski, R. J. (2012) Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol. Ther. 20, 443-455
11. Malik, V., Rodino-Klapac, L. R., Viollet, L., Wall, C., King, W., Al-Dahhak, R., Lewis, S., Shilling, C. J., Kota, J., Serrano- Munuera, C., Hayes, J., Mahan, J. D., Campbell, K. J., Banwell, B., Dasouki, M., Watts, V., Sivakumar, K., Bien-Willner, R., Flanigan, K. M., Sahenk, Z., Barohn, R. J., Walker, C. M., and Mendell, J. R. (2010) Gentamicin-induced readthrough of stop codons in Duchenne muscular dystrophy. Ann. Neurol. 67, 771-7800
12. Skuk, D., Goulet, M., Roy, B., Chapdelaine, P., Bouchard, J. P., Roy, R., Dugre, F. J., Sylvain, M., Lachance, J. G., Deschenes, L., Senay, H., and Tremblay, J. P. (2006) Dystrophin expression in muscles of Duchenne muscular dystrophy patients after highdensity injections of normal myogenic cells. J. Neuropathol. Exp. Neurol. 65, 371-3866
13. Rafael, J. A., Trickett, J. I., Potter, A. C., and Davies, K. E. (1999) Dystrophin and utrophin do not play crucial roles in nonmuscle tissues in mice. Muscle Nerve 22, 517-5199
14. 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, e152866
15. Newall, A. E., Duthie, S., Formstone, E., Nesterova, T., Alexiou, M., Johnston, C., Caparros, M. L., and Brockdorff, N. (2001) Primary non-random X inactivation associated with disruption of Xist promoter regulation. Hum. Mol. Genet. 10, 581-589
16. 'T Hoen, P. A., de Meijer, E. J., Boer, J. M., Vossen, R. H., Turk, R., Maatman, R. G., Davies, K. E., van Ommen, G. J., van Deutekom, J. C., and den Dunnen, J. T. (2008) Generation and characterization of transgenic mice with the full-length human DMD gene. J. Biol. Chem. 283, 5899-59077
17. Nadarajah, V. D., van Putten, M., Chaouch, A., Garrood, P., Straub, V., Lochmuller, H., Ginjaar, H. B., Aartsma-Rus, A. M., van Ommen, G. J., den Dunnen, J. T., and 't Hoen, P. A. (2011) Serum matrix metalloproteinase-9 (MMP-9) as a biomarker for monitoring disease progression in Duchenne muscular dystrophy (DMD). Neuromuscul. Disord. 21, 569-5788
18. Saito, T., Yamamoto, Y., Matsumura, T., Fujimura, H., and Shinno, S. (2009) Serum levels of vascular endothelial growth factor elevated in patients with muscular dystrophy. Brain Dev. 31, 612-6177
19. Verhaart, I. E., van Duijn, R. J., den Adel, B., Roest, A. A., Verschuuren, J. J., Aartsma-Rus, A., and van der Weerd, L. (2011) Assessment of cardiac function in three mouse dystrophinopathies by magnetic resonance imaging. Neuromuscul. Disord. 5, 418-4266
20. Van der Geest, R. J., and Reiber, J. H. (1999) Quantification in cardiac MRI. J. Magn. Reson. Imaging 10, 602-6088
21. Van Putten, M., de Winter, C. L., van Roon-Mom, W., van Ommen, G. J., 't Hoen, P. A., and Aartsma-Rus, A. (2010) A 3 months mild functional test regime does not affect disease parameters in young mdx mice. Neuromuscul. Disord. 20, 273-2800
22. Ramakers, C., Ruijter, J. M., Deprez, R. H., and Moorman, A. F. (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62-666
23. 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., and Aartsma-Rus, A. (2012) The effects of low levels of dystrophin on mouse muscle function and pathology. PLoS One 7, e319377
24. Van Putten, M., Kumar, D., Hulsker, M., Hoogaars, W. M., Plomp, J. J., van Opstal, A., van Iterson, M., Admiraal, P., van Ommen, G. J., 't Hoen, P. A., and Aartsma-Rus, A. (2012) Comparison of skeletal muscle pathology and motor function of dystrophin and utrophin deficient mouse strains. Neuromuscul. Disord. 5, 406-4177
25. Danko, I., Chapman, V., and Wolff, J. A. (1992) The frequency of revertants in mdx mouse genetic models for Duchenne muscular dystrophy. Pediatr. Res. 32, 128-1311
26. Karpati, G., Zubrzycka-Gaarn, E. E., Carpenter, S., Bulman, D. E., Ray, P. N., and Worton, R. G. (1990) Age-related conversion of dystrophin-negative to -positive fiber segments of skeletal but not cardiac muscle fibers in heterozygote mdx mice. J. Neuropathol. Exp. Neurol. 49, 96-1055
27. Crisp, A., Yin, H., Goyenvalle, A., Betts, C., Moulton, H. M., Seow, Y., Babbs, A., Merritt, T., Saleh, A. F., Gait, M. J., Stuckey, D. J., Clarke, K., Davies, K. E., and Wood, M. J. (2011) Diaphragm rescue alone prevents heart dysfunction in dystrophic mice. Hum. Mol. Genet. 20, 413-4211
28. Neri, M., Torelli, S., Brown, S., Ugo, I., Sabatelli, P., Merlini, L., Spitali, P., Rimessi, P., Gualandi, F., Sewry, C., Ferlini, A., and Muntoni, F. (2007) Dystrophin levels as low as 30% are sufficient to avoid muscular dystrophy in the human. Neuromuscul. Disord. 17, 913-9188
29. Hauser, M. A., Amalfitano, A., Kumar-Singh, R., Hauschka, S. D., and Chamberlain, J. S. (1997) Improved adenoviral vectors for gene therapy of Duchenne muscular dystrophy. Neuromuscul. Disord. 7, 277-2833
30. Phelps, S. F., Hauser, M. A., Cole, N. M., Rafael, J. A., Hinkle, R. T., Faulkner, J. A., and Chamberlain, J. S. (1995) Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum. Mol. Genet. 4, 1251-12588
31. Wells, D. J., Wells, K. E., Asante, E. A., Turner, G., Sunada, Y., Campbell, K. P., Walsh, F. S., and Dickson, G. (1995) Expression of human full-length and minidystrophin in transgenic mdx mice: implications for gene therapy of Duchenne muscular dystrophy. Hum. Mol. Genet. 4, 1245-12500
32. Goyenvalle, A., Babbs, A., Powell, D., Kole, R., Fletcher, S., Wilton, S. D., and Davies, K. E. (2010) Prevention of dystrophic pathology in severely affected dystrophin/utrophin-deficient mice by morpholino-oligomer-mediated exon-skipping. Mol. Ther. 18, 198-2055
33. Goyenvalle, A., Babbs, A., Wright, J., Wilkins, V., Powell, D., Garcia, L., and Davies, K. E. (2012) Rescue of severely affected dystrophin/utrophin- deficient mice through scAAV-U7snRNAmediated exon skipping. Hum. Mol. Genet. 21, 2559-2571
34. Kawano, R., Ishizaki, M., Maeda, Y., Uchida, Y., Kimura, E., and Uchino, M. (2008) Transduction of full-length dystrophin to multiple skeletal muscles improves motor performance and life span in utrophin/dystrophin double knockout mice. Mol. Ther. 16, 825-8311