Vascular delivery of rAAVrh74.MCK.GALGT2 to the gastrocnemius muscle of the rhesus macaque stimulates the expression of dystrophin and laminin α2 surrogates

Molecular Therapy

Volumn 22, Issue 4, 2014, Pages 713-724

  Chicoine, Louis G ^a,b,c   Rodino Klapac, Louise R ^a,b   Shao, Guohong ^b   Xu, Rui ^b   Bremer, William G ^c   Camboni, Marybeth ^b   Golden, Bethannie ^b   Montgomery, Chrystal L ^b   Shontz, Kimberly ^b   Heller, Kristin N ^b   Griffin, Danielle A ^b   Lewis, Sarah ^b   Coley, Brian D ^a,d   Walker, Christopher M ^a,c   Clark, K Reed ^a,b   Sahenk, Zarife ^a,b   Mendell, Jerry R ^a,b   Martin, Paul T ^a,b,c  

^a OHIO STATE UNIVERSITY   (United States)

^b THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^c NATIONWIDE CHILDREN S HOSPITAL   (United States)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; ALPHA DYSTROGLYCAN; BETA1 4 N ACETYL DEXTRO GALACTOSAMINE GLYCOSYLTRANSFERASE; CREATINE KINASE MM; DYSTROPHIN; GENE THERAPY AGENT; LAMININ; LAMININ ALPHA2; LAMININ ALPHA5; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; NEUTRALIZING ANTIBODY; PARVOVIRUS VECTOR; PLECTIN; PLECTIN1; PREDNISOLONE; TACROLIMUS; UNCLASSIFIED DRUG; UTROPHIN; DYSTROGLYCAN; GLYCOSYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; FEMORAL ARTERY; GASTROCNEMIUS MUSCLE; IMMUNOSUPPRESSIVE TREATMENT; MALE; MUSCULAR DYSTROPHY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; RHESUS MONKEY; T LYMPHOCYTE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ANIMAL; BIOSYNTHESIS; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE EXPRESSION REGULATION; GENE THERAPY; GENE TRANSFER; GENETICS; METABOLISM; MUSCULAR DYSTROPHIES; PATHOLOGY; SKELETAL MUSCLE;

ADENO-ASSOCIATED VIRUS; ANIMALIA; MACACA; MACACA MULATTA;

ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DYSTROGLYCANS; DYSTROPHIN; GENE EXPRESSION REGULATION; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GLYCOSYLTRANSFERASES; LAMININ; MACACA MULATTA; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES;

EID: 84897573789     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.246     Document Type: Article

References (50)

1. Xia, B, Hoyte, K, Kammesheidt, A, Deerinck, T, Ellisman, M and Martin, PT (2002). Overexpression of the CT GalNAc transferase in skeletal muscle alters myofiber growth, neuromuscular structure, and laminin expression. Dev Biol 242: 58-73
2. Nguyen, HH, Jayasinha, V, Xia, B, Hoyte, K and Martin, PT (2002). Overexpression of the cytotoxic T cell GalNAc transferase in skeletal muscle inhibits muscular dystrophy in mdx mice. Proc Natl Acad Sci USA 99: 5616-5621
3. Martin, PT (2003). Glycobiology of the neuromuscular junction. J Neurocytol 32: 915-929
4. Martin, PT, Scott, LJ, Porter, BE and Sanes, JR (1999). Distinct structures and functions of related pre-And postsynaptic carbohydrates at the mammalian neuromuscular junction. Mol Cell Neurosci 13: 105-118
5. Xu, R, Camboni, M and Martin, PT (2007). Postnatal overexpression of the CT GalNAc transferase inhibits muscular dystrophy in mdx mice without altering muscle growth or neuromuscular development: Evidence for a utrophin-independent mechanism. Neuromuscul Disord 17: 209-220
6. Yoon, JH, Chandrasekharan, K, Xu, R, Glass, M, Singhal, N and Martin, PT (2009). The synaptic CT carbohydrate modulates binding and expression of extracellular matrix proteins in skeletal muscle: Partial dependence on utrophin. Mol Cell Neurosci 41: 448-463
7. Martin, PT, Xu, R, Rodino-Klapac, LR, Oglesbay, E, Camboni, M, Montgomery, CL et al. (2009). Overexpression of Galgt2 in skeletal muscle prevents injury resulting from eccentric contractions in both mdx and wild-Type mice. Am J Physiol, Cell Physiol 296: C476-C488
8. Xu, R, Chandrasekharan, K, Yoon, JH, Camboni, M and Martin, PT (2007). Overexpression of the cytotoxic T cell (CT) carbohydrate inhibits muscular dystrophy in the dyW mouse model of congenital muscular dystrophy 1A. Am J Pathol 171: 181-199
9. Xu, R, DeVries, S, Camboni, M and Martin, PT (2009). Overexpression of Galgt2 reduces dystrophic pathology in the skeletal muscles of alpha sarcoglycan-deficient mice. Am J Pathol 175: 235-247
10. Tinsley, J, Deconinck, N, Fisher, R, Kahn, D, Phelps, S, Gillis, JM et al. (1998). Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4: 1441-1444
11. Burkin, DJ, Wallace, GQ, Nicol, KJ, Kaufman, DJ and Kaufman, SJ (2001). Enhanced expression of the alpha 7 beta 1 integrin reduces muscular dystrophy and restores viability in dystrophic mice. J Cell Biol 152: 1207-1218
12. Peter, AK, Marshall, JL and Crosbie, RH (2008). Sarcospan reduces dystrophic pathology: Stabilization of the utrophin-glycoprotein complex. J Cell Biol 183: 419-427
13. Gawlik, K, Miyagoe-Suzuki, Y, Ekblom, P, Takeda, S and Durbeej, M (2004). Laminin alpha1 chain reduces muscular dystrophy in laminin alpha2 chain deficient mice. Hum Mol Genet 13: 1775-1784
14. Bentzinger, CF, Barzaghi, P, Lin, S and Ruegg, MA (2005). Overexpression of miniagrin in skeletal muscle increases muscle integrity and regenerative capacity in laminin-Alpha2-deficient mice. FASEB J 19: 934-942
15. Rodino-Klapac, LR, Janssen, PM, Montgomery, CL, Coley, BD, Chicoine, LG, Clark, KR et al. (2007). A translational approach for limb vascular delivery of the microdystrophin gene without high volume or high pressure for treatment of Duchenne muscular dystrophy. J Transl Med 5: 45
16. Wang, Z, Zhu, T, Qiao, C, Zhou, L, Wang, B, Zhang, J et al. (2005). Adeno-Associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat Biotechnol 23: 321-328
17. Gao, GP, Alvira, MR, Wang, L, Calcedo, R, Johnston, J and Wilson, JM (2002). Novel adeno-Associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA 99: 11854-11859
18. Rapti, K, Louis-Jeune, V, Kohlbrenner, E, Ishikawa, K, Ladage, D, Zolotukhin, S et al. (2012). Neutralizing antibodies against AAV serotypes 1, 2, 6, and 9 in sera of commonly used animal models. Mol Ther 20: 73-83
19. Hoyte, K, Kang, C and Martin, PT (2002). Definition of pre-And postsynaptic forms of the CT carbohydrate antigen at the neuromuscular junction: Ubiquitous expression of the CT antigens and the CT GalNAc transferase in mouse tissues. Brain Res Mol Brain Res 109: 146-160
20. Chicoine, LG, Montgomery, CL, Bremer, WG, Shontz, KM, Griffin, DA, Heller, KN et al. (2013). Plasmapheresis eliminates the negative Impact of AAV antibodies on microdystrophin gene expression following vascular delivery. Mol Ther advance online publication 3 December 2013; doi:10.1038/mt.2013.244
21. Mendell, JR, Moxley, RT, Griggs, RC, Brooke, MH, Fenichel, GM, Miller, JP et al. (1989). Randomized, double-blind six-month trial of prednisone in Duchenne's muscular dystrophy. N Engl J Med 320: 1592-1597
22. Mingozzi, F and High, KA (2011). Therapeutic in vivo gene transfer for genetic disease using AAV: Progress and challenges. Nat Rev Genet 12: 341-355
23. Montiel, MD, Krzewinski-Recchi, MA, Delannoy, P and Harduin-Lepers, A (2003). Molecular cloning, gene organization and expression of the human UDPGalNAc: Neu5Acalpha2-3Galbeta-R beta1,4-N-Acetylgalactosaminyltransferase responsible for the biosynthesis of the blood group Sda/Cad antigen: Evidence for an unusual extended cytoplasmic domain. Biochem J 373(Pt 2): 369-379
24. Meier, T, Marangi, PA, Moll, J, Hauser, DM, Brenner, HR and Ruegg, MA (1998). A minigene of neural agrin encoding the laminin-binding and acetylcholine receptoraggregating domains is sufficient to induce postsynaptic differentiation in muscle fibres. Eur J Neurosci 10: 3141-3152
25. Martin, LT, Glass, M, Dosunmu, E and Martin, PT (2007). Altered expression of natively glycosylated alpha dystroglycan in pediatric solid tumors. Hum Pathol 38: 1657-1668
26. Yoon, JH, Johnson, E, Xu, R, Martin, LT, Martin, PT and Montanaro, F (2012). Comparative proteomic profiling of dystroglycan-Associated proteins in wild type, mdx, and Galgt2 transgenic mouse skeletal muscle. J Proteome Res 11: 4413-4424
27. Rezniczek, GA, Konieczny, P, Nikolic, B, Reipert, S, Schneller, D, Abrahamsberg, C et al. (2007). Plectin 1f scaffolding at the sarcolemma of dystrophic (mdx) muscle fibers through multiple interactions with beta-dystroglycan. J Cell Biol 176: 965-977
28. Rafael, JA, Tinsley, JM, Potter, AC, Deconinck, AE and Davies, KE (1998). Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nat Genet 19: 79-82
29. Ehrig, K, Leivo, I, Argraves, WS, Ruoslahti, E and Engvall, E (1990). Merosin, a tissuespecific basement membrane protein, is a laminin-like protein. Proc Natl Acad Sci USA 87: 3264-3268
30. Manno, CS, Pierce, GF, Arruda, VR, Glader, B, Ragni, M, Rasko, JJ et al. (2006). Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med 12: 342-347
31. Mingozzi, F and High, KA (2013). Immune responses to AAV vectors: Overcoming barriers to successful gene therapy. Blood 122: 23-36
32. Kornegay, JN, Bogan, JR, Bogan, DJ, Childers, MK, Li, J, Nghiem, P et al. (2012). Canine models of Duchenne muscular dystrophy and their use in therapeutic strategies. Mamm Genome 23: 85-108
33. Murphy, SL, Li, H, Zhou, S, Schlachterman, A, High, KA and High, K (2008). Prolonged susceptibility to antibody-mediated neutralization for adeno-Associated vectors targeted to the liver. Mol Ther 16: 138-145
34. Jiang, H, Couto, LB, Patarroyo-White, S, Liu, T, Nagy, D, Vargas, JA et al. (2006). Effects of transient immunosuppression on adenoassociated, virus-mediated, liverdirected gene transfer in rhesus macaques and implications for human gene therapy. Blood 108: 3321-3328
35. Monteilhet, V, Saheb, S, Boutin, S, Leborgne, C, Veron, P, Montus, MF et al. (2011). A 10 patient case report on the impact of plasmapheresis upon neutralizing factors against adeno-Associated virus (AAV) types 1, 2, 6, and 8. Mol Ther 19: 2084-2091
36. Sack, BK, Merchant, S, Markusic, DM, Nathwani, AC, Davidoff, AM, Byrne, BJ et al. (2012). Transient B cell depletion or improved transgene expression by codon optimization promote tolerance to factor VIII in gene therapy. PLoS ONE 7: E37671
37. Mingozzi, F, Chen, Y, Edmonson, SC, Zhou, S, Thurlings, RM, Tak, PP et al. (2013). Prevalence and pharmacological modulation of humoral immunity to AAV vectors in gene transfer to synovial tissue. Gene Ther 20: 417-424
38. Mendell, JR, Campbell, K, Rodino-Klapac, L, Sahenk, Z, Shilling, C, Lewis, S et al. (2010). Dystrophin immunity in Duchenne's muscular dystrophy. N Engl J Med 363: 1429-1437
39. Dohi, T, Yuyama, Y, Natori, Y, Smith, PL, Lowe, JB and Oshima, M (1996). Detection of N-Acetylgalactosaminyltransferase mRNA which determines expression of Sda blood group carbohydrate structure in human gastrointestinal mucosa and cancer. Int J Cancer 67: 626-631
40. Dohi, T and Kawamura, YI (2008). Incomplete synthesis of the Sda/Cad blood group carbohydrate in gastrointestinal cancer. Biochim Biophys Acta 1780: 467-471
41. Morton, JA, Pickles, MM and Terry, AM (1970). The Sda blood group antigen in tissues and body fluids. Vox Sang 19: 472-482
42. Tinsley, JM, Fairclough, RJ, Storer, R, Wilkes, FJ, Potter, AC, Squire, SE et al. (2011). Daily treatment with SMTC1100, a novel small molecule utrophin upregulator, dramatically reduces the dystrophic symptoms in the mdx mouse. PLoS ONE 6: E19189
43. Gao, G, Lebherz, C, Weiner, DJ, Grant, R, Calcedo, R, McCullough, B et al. (2004). Erythropoietin gene therapy leads to autoimmune anemia in macaques. Blood 103: 3300-3302
44. Chenuaud, P, Larcher, T, Rabinowitz, JE, Provost, N, Cherel, Y, Casadevall, N et al. (2004). Autoimmune anemia in macaques following erythropoietin gene therapy. Blood 103: 3303-3304
45. Marshall, JL, Holmberg, J, Chou, E, Ocampo, AC, Oh, J, Lee, J et al. (2012). Sarcospandependent Akt activation is required for utrophin expression and muscle regeneration. J Cell Biol 197: 1009-1027
46. Rabinowitz, JE, Rolling, F, Li, C, Conrath, H, Xiao, W, Xiao, X et al. (2002). Crosspackaging of a single adeno-Associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J Virol 76: 791-801
47. Clark, KR, Liu, X, McGrath, JP and Johnson, PR (1999). Highly purified recombinant adeno-Associated virus vectors are biologically active and free of detectable helper and wild-Type viruses. Hum Gene Ther 10: 1031-1039
48. Rodino-Klapac, LR, Montgomery, CL, Bremer, WG, Shontz, KM, Malik, V, Davis, N et al. (2010). Persistent expression of FLAG-Tagged micro dystrophin in nonhuman primates following intramuscular and vascular delivery. Mol Ther 18: 109-117
49. Hämäläinen, N and Pette, D (1993). The histochemical profiles of fast fiber types IIB, IID, and IIA in skeletal muscles of mouse, rat, and rabbit. J Histochem Cytochem 41: 733-743
50. Hoyte, K, Jayasinha, V, Xia, B and Martin, PT (2004). Transgenic overexpression of dystroglycan does not inhibit muscular dystrophy in mdx mice. Am J Pathol 164: 711-718.