The artificial gene Jazz, a transcriptional regulator of utrophin, corrects the dystrophic pathology in mdx mice

Human Molecular Genetics

Volumn 19, Issue 5, 2010, Pages 752-760

  di Certo, Maria Grazia ^a   Corbi, Nicoletta ^a   Strimpakos, Georgios ^a,e   Onori, Annalisa ^a   Luvisetto, Siro ^a   Severini, Cinzia ^a   Guglielmotti, Angelo ^b   Batassa, Enrico Maria ^a   Pisani, Cinzia ^a,e   Floridi, Aristide ^e   Benassi, Barbara ^c   Fanciulli, Maurizio ^c   Magrelli, Armando ^d   Mattei, Elisabetta ^a,c   Passananti, Claudio ^a,c  

^a CNR   (Italy)

^b Università Politecnica delle Marche ACRAF Gruppo Angelini   (Italy)

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^d ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^e UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UTROPHIN; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN JAZZ;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CROSS LINKING; DRUG EFFICACY; DRUG TARGETING; DUCHENNE MUSCULAR DYSTROPHY; FEMALE; GENE EXPRESSION PROFILING; GENE TARGETING; GENETIC ENGINEERING; HISTOPATHOLOGY; IN VIVO STUDY; MALE; MOUSE; MUSCLE FUNCTION; NONHUMAN; NONVIRAL GENE THERAPY; PRIORITY JOURNAL; SARCOLEMMA; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; DYSTROPHIN; FEMALE; MALE; MICE; MICE, INBRED MDX; MICE, TRANSGENIC; MUSCULAR DYSTROPHY, ANIMAL; TRANSCRIPTION FACTORS; UTROPHIN; ZINC FINGERS;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 77950540612     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp539     Document Type: Article

References (45)

1. Hirst, R.C., McCullagh, K.J. and Davies, K.E. (2005) Utrophin upregulation in Duchenne muscular dystrophy. Acta Myol., 24, 219-216
2. Miura, P. and Jasmin, B.J. (2006) Utrophin upregulation for treating Duchenne or Becker muscular dystrophy: how close are we? Trends Mol. Med., 3, 122-129.
3. Nowak, K.J. and Davies, K.E. (2004) Duchenne muscular dystrophy and dystrophin: pathogenesis and opportunities for treatment. EMBO Rep., 5, 872-876.
4. McNally, E.M. and Pytel, P. (2007) Muscle disease: the muscular dystrophies. Annu. Rev. Pathol. Mech. Dis., 2, 87-109.
5. Cossu, G. and Sampaolesi, M. (2007) New therapies for Duchenne muscular dystrophy: challenges, prospects and clinical trials. Trends Mol. Med., 13, 520-526.
6. Matsumura, K., Ervasti, J.M., Ohlendieck, K., Kahl, S.D. and Campbell, K.P. (1992) Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature, 360, 588-591.
7. Blake, D.J., Weir, A., Newey, S.E. and Davies, K.E. (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev., 82, 291-329.
8. Clerk, A., Morris, G.E., Dubowitz, V., Davies, K.E. and Sewry, C.A. (1993) Dystrophin-related protein, utrophin, in normal and dystrophic human fetal skeletal muscle. Histochem. J., 25, 554-561.
9. Ohlendieck, K., Ervasti, J.M., Matsumura, K., Kahl, S.D., Leveille, C.J. and Campbell, K.P. (1991) Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron, 7, 499-508
10. Gramolini, A.O. and Jasmin, B.J. (1997) Duchenne muscular dystrophy and the neuromuscular junction: the utrophin link. Bioassays, 19, 747-750.
11. Love, D.R., Morris, G.E., Ellis, J.M., Fairbrother, U., Marsden, R.F., Bloomfield, J.F., Edwards, Y.H., Slater, C.P., Parry, D.J. and Davies, K.E. (1991) Tissue distribution of the dystrophin-related gene product and expression in the mdx and dy mouse. Proc. Natl. Acad. Sci. USA, 88, 3243-3247.
12. Taylor, J., Muntoni, F., Dubowitz, V. and Sewry, C.A. (1997) The abnormal expression of utrophin in Duchenne and Becker muscular dystrophy is age related. Neuropathol. Appl. Neurobiol., 23, 399-405
13. Tinsley, J.M., Potter, A.C., Phelps, S.R., Fisher, R., Tricket, J.I. and Davies, K.E. (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature, 384, 349-353.
14. Deconinck, N., Tinsley, J., De Backer, F., Fisher, R., Kahn, D., Phelps, S., Davies, K.E. and Gillis, J.M. (1997) Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat. Med., 3, 1216-1221.
15. Tinsley, J., Deconinck, N., Fisher, R., Kahn, D., Phelps, S., Gillis, J.M. and Davies, K. (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat. Med., 4, 1441-1444.
16. Squire, S., Raymackers, J.M., Vandebrouck, C., Potter, A., Tinsley, J., Fisher, R., Gillis, J.M. and Davies, K.E. (2002) Prevention of pathology in mdx mice by expression of utrophin: analysis using an inducible transgenic expression system. Hum. Mol. Gene., 11, 3333-3344.
17. Khurana, T.S. and Davies, K.E. (2003) Pharmacological strategies for muscular dystrophy. Nat. Rev. Drug. Discov., 2, 379-390.
18. Corbi, N., Libri, V., Fanciulli, M., Tinsley, J.M., Davies, K.E. and Passananti, C. (2000) The artificial zinc finger coding gene 'Jazz' binds the utrophin promoter and activates transcription. Gene Ther., 7, 1076-1083.
19. Onori, A., Desantis, A., Buontempo, S., Di Certo, M.G., Fanciulli, M., Salvatori, L., Passananti, C. and Corbi, N. (2007) The artificial 4-zinc-finger Bagly binds human utrophin promoter A at the endogenous chromosomal site and activates transcription. Biochem. Cell. Biol., 85, 358-365.
20. Desantis, A., Onori, A., Di Certo, M.G., Mattei, E., Fanciulli, M., Passananti, C. and Corbi, N. (2009) Novel activation domain derived from Che-1 cofactor coupled with the artificial protein Jazz drives utrophin upregulation. Neuromus. Disord., 19, 158-162.
21. Cho, Y. and Klug, A. (1997) Physical basis of a protein-DNA recognition code. Curr. Opin. Struct. Biol., 7, 117-125.
22. Pabo, C.O., Peisach, E. and Grant, R. (2001) Design and selection of novel Cys2His2 zinc finger proteins. Annu. Rev. Biochem., 70, 313-340
23. Blancafort, P., Segal, D.J. and Barbas, C.F.I.I.I. (2004) Designing transcription factor architectures for drug discovery. Mol. Pharmacol., 66, 1361-1371.
24. Gommans, W.M., Haisma, H.J. and Rots, M.G. (2005) Engineering Zinc Finger Protein Transcription Factors: The Therapeutic Relevance of Switching Endogenous Gene Expression On or Off at Command. J. Mol. Biol., 354, 507-519.
25. Sera, T. (2009) Zinc-finger-based artificial transcription factors and their applications. Adv. Drug Deliv. Rev., 61, 513-526.
26. Mattei, E., Corbi, N., Di Certo, M.G., Strimpakos, G., Severini, C., Onori, A., Desantis, A., Libri, V., Buontempo, S., Floridi, A. et al. (2007) Utrophin up-regulation by an artificial transcription factor in transgenic mice. PLoS ONE, 2, e774.
27. Matsuda, R., Spector, D.H. and Strohman, R.C. (1983) Regenerating adult chicken skeletal muscle and satellite cell cultures express embryonic patterns of myosin and tropomyosin lsoforms. Dev. Biol., 100, 478-488
28. Dimario, J.X., Uzman, A. and Strohman, R.C. (1991) Fiber regeneration is not persistent in dystrophic (MDX) mouse skeletal muscle. Dev. Biol., 148, 314-321.
29. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A.M. and Sweeney, H.L. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. USA, 90, 3710-3714
30. Moens, P., Baatsen, P.H. and Marechal, G. (1993) Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. J. Muscle Res. Cell. Motil., 14, 446-451.
31. Webster, C., Silberstein, L., Hays, A.P. and Blau, H.M. (1988) Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell, 52, 502-513.
32. Lerman, I., Harrison, B.C., Freeman, K., Hewett, T.E., Allen, D.L., Robbins, J. and Leinwand, L.A. (2002) Genetic variability in forced and voluntary endurance exercise performance in seven inbred mouse strains. J. Appl. Physiol., 92, 2245-2255.
33. Baban, D. and Davies, K.E. (2008) Microarray analysis of mdx mice expressing high levels of utrophin: therapeutic implications for dystrophin deficiency. Neuromus. Disord., 18, 239-247.
34. Campbell, K.P. and Crosbie, R.H. (1996) Muscular dystrophy. Utrophin to the rescue. Nature, 384, 308-309.
35. Fisher, R., Tinsley, J.M., Phelps, S.R., Squire, S.E., Townsend, E.R., Martin, J.E. and Davies, K.E. (2001) Non-toxic ubiquitous over-expression of utrophin in the mdx mouse. Neuromus. Disord., 11, 713-721.
36. Krag, T., Bogdanovich, S., Jensen, C.J., Fischer, M.D., Hansen-Schwartz, J., Javazon, E.H., Flake, A.W., Edvinsson, L. and Khurana, T.S. (2004) Heregulin ameliorates the dystrophic phenotype in mdx mice. Proc. Natl. Acad. Sci. USA, 101, 13856-13860.
37. Voisin, V., Sebrie, C., Matecki, S., Yu, H. and Gillet, B. (2005) L-arginine improves dystrophic phenotype in mdx mice. Neurobiol. Dis., 20, 123-130.
38. Sonnemann, K.J., Heun-Johnson, H., Turner, A.J., Baltgalvis, K.A., Lowe, D.A. and Ervasti, J.M. (2009) Functional substitution by TAT-utrophin in dystrophin-deficient mice. PLoS Med., 6, e1000083.
39. Gregorevic, P., Blankinship, M.J., Allen, J.M., Crawford, R.W., Meuse, L., Miller, D.G., Russell, D.W. and Chamberlain, J.S. (2004) Systemicdelivery of genes to striated muscles using adeno-associated viral vectors. Nat. Med., 10, 828-834.
40. Rebar, E.J., Huang, Y., Hickey, R., Nath, A.K., Meoli, D., Nath, S., Nath, S., Chen, B., Xu, L., Liang, Y. et al. (2002) Induction of angiogenesis in a mouse model using engineered transcription factors. Nat. Med., 8, 1427-1432.
41. Minetti, G.C., Colussi, C., Adami, R., Serra, C., Mozzetta, C., Parente, V., Fortuni, S., Straino, S., Sampaolesi, M., Di Padova, M. et al. (2006) Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors. Nat. Med., 1210, 1147-1150.
42. Lu, Y., Tian, C., Danialou, G., Gilbert, R., Petrof, B.J., Karpati, G. and Nalbantoglu, J. (2008) Targeting artificial transcription factors to the utrophin a promoter effects on dystrophic pathology and muscle function. J. Biol. Chem., 283, 34720-34727.
43. Sharp, P.S., Dick, J.R. and Greensmith, L. (2005) The effect of peripheral nerve injury on disease progression in the SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Neuroscience, 130, 897-910.
44. Li, C. and Wong, W.H. (2001a) Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc. Natl. Acad. Sci. USA, 98, 31-36.
45. Li, C. and Wong, W.H. (2001b) Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol., 2, 0032.1-0032.11.