Sustained AAV-mediated dystrophin expression in a canine model of duchenne muscular dystrophy with a brief course of immunosuppression

Molecular Therapy

Volumn 15, Issue 6, 2007, Pages 1160-1166

  Wang, Zejing ^a,b   Kuhr, Christian S ^a,c   Allen, James M ^b   Blankinship, Michael ^b   Gregorevic, Paul ^b   Chamberlain, Jeffrey S ^b,c   Tapscott, Stephen J ^a,b   Storb, Rainer ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOSPORIN; DYSTROPHIN; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PARVOVIRUS VECTOR; THYMOCYTE ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOG; DRUG BLOOD LEVEL; DUCHENNE MUSCULAR DYSTROPHY; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; MUSCLE FIBER MEMBRANE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN LOCALIZATION; SKELETAL MUSCLE; TIME; TRANSGENE; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; ANTILYMPHOCYTE SERUM; CYCLOSPORINE; DEPENDOVIRUS; DOGS; DRUG THERAPY, COMBINATION; DYSTROPHIN; FLOW CYTOMETRY; GENE EXPRESSION; GENE THERAPY; GENETIC VECTORS; IMMUNOSUPPRESSION; IMMUNOSUPPRESSIVE AGENTS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; MYCOPHENOLIC ACID;

ADENO-ASSOCIATED VIRUS; ANIMALIA; CANIS FAMILIARIS; MIRIDAE;

EID: 34249276065     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/sj.mt.6300161     Document Type: Article

References (50)

1. Muntoni, F, Torelli, S and Ferlini, A (2003). Dystrophin and mutations: one gene, several proteins, multiple phenotypes (Review). Lancet Neurol 2: 731-740.
2. Koenig, M, Hoffman, EP, Bertelson, CJ, Monaco, AP, Feener, C and Kunkel LM (1987). Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50: 509-517.
3. Athanasopoulos, T, Fabb, S and Dickson G (2000). Gene therapy vectors based on adeno-associated virus: Characteristics and applications to acquired and inherited diseases (Review). Int J Mol Med 6: 363-375.
4. Blankinship, MJ, Gregorevic, P, Allen, JM, Harper, SQ, Harper, H, Halbert, CL et al. (2004). Efficient transduction of skeletal muscle using vectors based on adeno-associated virus serotype 6. Mol Ther 10: 671-678.
5. Inagaki, K, Fuess, S, Storm, TA, Gibson, GA, Mctiernan, CF, Kay, MA et al. (2006). Robust systemic transduction with AAV9 vectors in mice: Efficient global cardiac gene transfer superior to that of AAV8. Mol Ther 14: 45-53.
6. 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.
7. Athanasopoulos, T, Graham, IR, Foster, H and Dickson G (2004). Recombinant adeno-associated viral (rAAV) vectors as therapeutic tools for Duchenne muscular dystrophy (DMD) (Review). Gene Ther 11 Suppl. 1): S109-S121.
8. Blankinship, MJ, Gregorevic, P and Chamberlain, JS (2006). Gene therapy strategies for Duchenne muscular dystrophy utilizing recombinant adeno-associated virus vectors. Mol Ther 13: 241-249.
9. England, SB, Nicholson, LV, Johnson, MA, Forrest, SM, Love, DR, Zubrzycka-Gaarn, EE et al. (1990). Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature 343 180-182.
10. Phelps, SF, Hauser, MA, Cole, NM, Rafael, JA, Hinkle, RT, Faulkner, JA et al. (1995). Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum Mol Genet 4: 1251-1258.
11. Harper, SQ, Hauser, MA, DelloRusso, C, Duan, D, Crawford, RW, Phelps, SF et al. (2002). Modular flexibility of dystrophin: Implications for gene therapy of Duchenne muscular dystrophy. Nat Med 8: 253-261.
12. Crawford, GE, Faulkner JA, Crosbie, RH, Campbell, KP, Froehner, SC and Chamberlain, JS (2000). Assembly of the dystrophin-associated protein complex does not require the dystrophin COOH-terminal domain. J Cell Biol 150: 1399-1410.
13. Scott, JM, Li, S, Harper, SQ, Welikson, R, Bourque, D, DelloRusso, C et al. (2002). Viral vectors for gene transfer of micro-, mini-, or full-length dystrophin (Review). Neuromuscul Disord 112 Suppl. 1): S23-S29.
14. Gregorevic, P, Allen, JM, Minami, E, Blankinship, MJ, Haraguchi, M, Meuse, L et al. (2006). rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat Med 12: 787-789.
15. Gregorevic, P, Blankinship, MJ, Allen, JM, Crawford, RW, Meuse, L, Miller, DG et al. (2004). Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat Med 10: 828-834.
16. Liu, M, Yue, Y, Harper, SQ, Grange, RW, Chamberlain, JS and Duan, D (2005). Adeno-associated virus-mediated microdystrophin expression protects young mdx muscle from contraction-induced injury. Mol Ther 11: 245-256.
17. Yue, Y, Li, Z, Harper, SQ, Davisson, RL, Chamberlain, JS and Duan, D (2003). Microdystrophin gene therapy of cardiomyopathy restores dystrophin-glycoprotein complex and improves sarcolemma integrity in the mdx mouse heart. Circulation 108: 1626-1632.
18. Yue, Y, Liu, M and Duan D (2006). C-terminal-truncated microdystrophin recruits dystrobrevin and syntrophin to the dystrophin-associated glycoprotein complex and reduces muscular dystrophy in symptomatic utrophin/dystrophin double-knockout mice. Mol Ther 14: 79-87.
19. Wang, Z, Allen, JM, Riddell, SR, Gregorevic, P, Storb, R, Tapscott, SJ et al. (2007). Immunity to adeno-associated virus-mediated gene transfer in a random-bred canine model of Duchenne muscular dystrophy. Hum Gene Ther 18: 18-26.
20. Deeg, HJ, Storb, R, Gerhard-Miller, L, Shulman, HM, Weiden, PL and Thomas, ED (1980). Cyclosporin A, a powerful immunosuppressant in vivo and in vitro in the dog, fails to induce tolerance. Transplantation 29: 230-235.
21. Allison, AC and Eugui, EM (2000). Mycophenolate mofetil and its mechanisms of action(Review). Immunopharmocology 47: 85-118.
22. Taylor, AL, Watson, CJ and Bradley JA (2005). Immunosuppressive agents in solid organ transplantation: Mechanisms of action and therapeutic efficacy (Review). Crit Rev OncolHematol 56: 23-46.
23. Storb, R, Yu, C, Wagner, JL, Deeg, HJ, Nash, RA, Kiem, H-P et al. (1997). Stable mixed hematopoietic chimerism in DLA-identical littermate dogs given sublethal total body irradiation before and pharmacological immunosuppression after marrow transplantation. Blood 89: 3048-3054.
24. Yu, C, Seidel, K, Nash, RA, Deeg, HJ, Sandmaier, BM, Barsoukov, A et al. (1998). Synergism between mycophenolate mofetil and cyclosporine in preventing graft-versus-host disease among lethally irradiated dogs given DLA-nonidentical unrelated marrow grafts. Blood 91: 2581-2587.
25. Kirk, AD (2003). Crossing the bridge: Large animal models in translational transplantation research (Review). Immunol Rev 196: 176-196.
26. Sharp, NJ, Kornegay, JN, Van Camp, SD, Herbstreith, MH, Secore, SL, Kettle, S et al. (1992). An error in dystrophin mRNA processing in golden retriever muscular dystrophy, an animal homologue of Duchenne muscular dystrophy. Genomics 13: 115-121.
27. Herzog, RW, Mount JD, Arruda, VR, High, KA and Lothrop, CD, Jr. (2001). Muscle-directed gene transfer and transient immune suppression result in sustained partial correction of canine hemophilia B caused by a null mutation. Mol Ther 4: 192-200.
28. High, K (2002). AAV-mediated gene transfer for hemophilia (Review). GenetMed 4: 56S-61S.
29. Arruda, VR, Schuettrumpf, J, Herzog, RW, Nichols, TC, Robinson, N, Lotfi, Y et al. (2004). Safety and efficacy of factor IX gene transfer to skeletal muscle in murine and canine hemophilia B models by adeno-associated viral vector serotype 1. Blood 103: 85-92.
30. Porter, JD, Merriam, AP, Leahy, P, Gong, B and Khanna S (2003). Dissection of temporal gene expression signatures of affected and spared muscle groups in dystrophin-deficient (mdx) mice. Hum Mol Genet 12: 1813-1821.
31. Porter, JD, Guo, W, Merriam, AP, Khanna, S, Cheng, G, Zhou, X et al. (2003). Persistent over-expression of specific CC class chemokines correlates with macrophage and T-cell recruitment in mdx skeletal muscle. Neuromuscul Disord 13: 223-235.
32. Tidball, JG and Wehling-Henricks, M (2005). Damage and inflammation in muscular dystrophy: Potential implications and relationships with autoimmune myositis (Review). Curr Opin Rheumatol 17: 707-713.
33. Wiendl H, Hohlfeld R and Kieseler BC (2005). Muscle-derived positive and negative regulators of the immune response (Review). Curr Opin Rheumatol 17: 714-719.
34. Hartigan-O'Connor, D, Kirk, CJ, Crawford, R, Mule, JJ and Chamberlain, JS (2001). Immune evasion by muscle-specific gene expression in dystrophic muscle. Mol Ther 4: 525-533.
35. Yuasa, K, Sakamoto, M, Miyagoe-Suzuki, Y, Tanouchi, A, Yamamoto, H, Li, J et al. (2002). Adeno-associated virus vector-mediated gene transfer into dystrophin-deficient skeletal muscles evokes enhanced immune response against the transgene product. Gene Ther 9: 1576-1588.
36. Storb, R, Kolb, HJ, Graham, TC, Kolb, H, Welden, PL and Thomas, ED (1973). Treatment of established graft-versus-host disease in dogs by antithymocyte serum or prednisone. Blood 42: 601-609.
37. Storb, R, Floersheim, GL, Weiden, PL, Graham, TC, Kolb, H-J, Lerner KG et al. (1974). Effect of prior blood transfusions on marrow grafts: Abrogation of sensitization by procarbazine and antithymocyte serum. J Immunol 112: 1508-1516.
38. Storb, R, Gluckman, E, Thomas, ED, Buckner, CD, Clift, RA, Fefer, A et al. (1974). Treatment of established human graft-versus-host disease by antithymocyte globulin. Blood 44: 57-75.
39. Storb, R, Etzioni, R, Anasetti, C, Appelbaum, FR, Buckner, CD, Bensinger, W et al. (1994). Cyclophosphamide combined with antithymocyte globulin in preparation for allogeneic marrow transplants in patients with aplastic anemia. Blood 84: 941-949.
40. Kahl, C, Leisenring, W, Deeg, HJ, Chauncey, TR, Flowers, MED, Martin, PJ et al. (2005). Cyclophosphamide and antithymocyte globulin as a conditioning regimen for allogeneic marrow transplantation in patients with aplastic anaemia: A long-term follow-up. Br J Haematol 130 747-751.
41. Diaconescu, R, Little, M-T, Leisenring, W, Yunusov, M, Hogan, WJ, Sorror, ML et al. (2005). What role is there for antithymocyte globulin in allogeneic nonmyeloablative canine hematopoietic cell transplantation? Biol Blood Marrow Transplant 11: 335-344.
42. Tyler, KL (2003). Origins and early descriptions of "Duchenne muscular dystrophy". Muscle Nerve 28: 402-422.
43. Manno, CS, Pierce, GF, Arruda, MR, Glader, B, Ragni, M, Rasko, JJE et al. (2006). Successful transduction of liver in hemophilia by AAV-factor IX and limitations imposed by the host immunce response. Nat Med 12: 342-347.
44. + T cell epitopes. Mol Ther 12: 1023-1033.
45. Chen, J, Wu, Q, Yang, P, Hsu, HC and Mountz, JD (2006). Determination of specific CD4 and CD8 T cell epitopes after AAV2- and AAV8-hF.IX gene therapy. Mol Ther 13: 260-269.
46. Gao, G, Lu, Y, Calcedo, R, Grant RL, Bell, P, Wang, L et al. (2006). Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates. Mol Ther 13: 77-87.
47. Dell'Agnola, C, Wang, Z, Storb, R, Tapscott, SJ, Kuhr, CS, Hauschka, SD et al. (2004). Hematopoietic stem cell transplantation does not restore dystrophin expression in Duchenne muscular dystrophy dogs. Blood 104: 4311-4318.
48. Chamberlain, J (2004). PCR-mediated mutagenesis. In: Encyclopedia of Life Sciences. John Wiley & Sons: Hoboken, NJ. Online publication doi: 10.1038/npg.els.0003766.
49. Grimm, D and Kleinschmidt, JA (1999). Progress in adeno-associated virus type 2 vector production: Promises and prospects for clinical use (Review). Hum Gene Ther 10: 2445-2450.
50. Rafael, JA, Cox, GA, Corrado, K, Jung, D, Campbell, KP and Chamberlain, JS (1996). Forced expression of dystrophin deletion constructs reveals structure-function correlations. J Cell Biol 134: 93-102.