Systemic delivery of AAV8 in utero results in gene expression in diaphragm and limb muscle: Treatment implications for muscle disorders

Gene Therapy

Volumn 16, Issue 9, 2009, Pages 1130-1137

  Koppanati, B M ^a   Li, J ^b   Xiao, X ^b   Clemens, P R ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b University of North Carolina   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; PARVOVIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIAPHRAGM; FETUS; GENE EXPRESSION; GENETIC TRANSDUCTION; HEART; INTERCOSTAL MUSCLE; MOUSE; MUSCLE DISEASE; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; SEROTYPE; SYSTEMIC THERAPY; TISSUE DISTRIBUTION; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; BETA-GALACTOSIDASE; DEPENDOVIRUS; DIAPHRAGM; FEMALE; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENES, REPORTER; GENETIC VECTORS; INJECTIONS, INTRAPERITONEAL; LAC OPERON; MICE; MUSCLE FIBERS, FAST-TWITCH; MUSCLE, SKELETAL; MUSCULAR DISEASES; PREGNANCY; TISSUE DISTRIBUTION; TRANSDUCTION, GENETIC;

MUS;

EID: 70249117075     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2009.71     Document Type: Article

References (45)

1. Xiao X, Li J, Samulski RJ. Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J Virol 1996; 70: 8098-8108.
2. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 2008; 16: 1073-1080.
3. Ziegler RJ, Bercury SD, Fidler J, Zhao MA, Foley J, Taksir TV et al Ability of adeno-associated virus serotype 8-mediated hepatic expression of acid alpha-glucosidase to correct the biochemical and motor function deficits of presymptomatic and symptomatic Pompe mice. Hum Gene Ther 2008; 19: 60-21.
4. Qiao C, Li J, Jiang J, Zhu X, Wang B, Li J et al. Myostatin propeptide gene delivery by adeno-associated virus serotype 8 vectors enhances muscle growth and ameliorates dystrophic phenotypes in mdx mice. Hum Gene Ther 2008; 19: 241-254.
5. Rodino-Klapac LR, Janssen PM, Montgomery CL, Coley BD, Chicoine LG, Clark KR et al. A translational approach for limb vascular delivery of the micro-dystrophin gene without high volume or high pressure for treatment of Duchenne muscular dystrophy. J Transl Med 2007; 5: 45.
6. Inagaki K, Fuess S, Storm TA, Gibson GA, McTiernan CF, Kay MA et al Robust systemic transduction with AAV9 vectors in mice: Efficient global cardiac gene transfer superior to that of AAV8. Mol Ther 2006; 14: 45-53.
7. Wang Z, Zhu T, Qiao C, Zhou L, Wang B, Zhang J et al. Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat Biotechnol 2005; 23: 321-328.
8. Louboutin JP, Wang L, Wilson JM. Gene transfer into skeletal muscle using novel AAV serotypes. J Gene Med 2005; 7: 442-451.
9. Sun B, Zhang H, Franco LM, Young SP, Schneider A, Bird A et al. Efficacy of an adeno-associated virus 8-pseudotyped vector in glycogen storage disease type II. Mol Ther 2005; 11: 57-65.
10. Vandenberghe LH, Wang L, Somanathan S, Zhi Y, Figueredo J, Calcedo R et al. Heparin binding directs activation of T cells against adeno-associated virus serotype 2 capsid. Nat Med 2006; 12: 967-971.
11. Thomas CE, Storm TA, Huang Z, Kay MA. Rapid uncoating of vector genomes is the key to efficient liver transduction with pseudotyped adeno-associated virus vectors. J Virol 2004; 78: 3110-3122.
12. Davidoff AM, Gray JT, Ng CY, Zhang Y, Zhou J, Spence Y et al. Comparison of the ability of adeno-associated viral vectors pseudotyped with serotype 2, 5 and 8 capsid proteins to mediate efficient transduction of the liver in murine and nonhuman primate models. Mol Ther 2005; 11: 875-888.
13. Nathwani AC, Gray JT, Ng CY, Zhou J, Spence Y, Waddington SN et al Self-complementary adeno-associated virus vectors containing a novel liver-specific human factor IX expression cassette enable highly efficient transduction of murine and nonhuman primate liver. Blood 2006; 107: 2653-2661.
14. Nathwani AC, Gray JT, McIntosh J, Ng CY, Zhou J, Spence Y et al. Safe and efficient transduction of the liver after peripheral vein infusion of self-complementary AAV vector results in stable therapeutic expression of human FIX in nonhuman primates. Blood 2007; 109 1414-1421.
15. Cheng H,Wolfe SH, Valencia V, Qian K, Shen L, Phillips MI et al. Efficient and persistent transduction of exocrine and endocrine pancreas by adeno-associated virus type 8. J Biomed Sci 2007; 14: 585-594.
16. Foust KD, Poirier A, Pacak CA, Mandel RJ, Flotte TR. Neonatal intraperitoneal or intravenous injections of recombinant adeno-associated virus type 8 transduce dorsal root ganglia and lower motor neurons. Hum Gene Ther 2008; 19: 61-70.
17. Nakai H, Fuess S, Storm TA, Muramatsu S, Nara Y, Kay MA. Unrestricted hepatocyte transduction with adeno-associated virus serotype 8 vectors in mice. J Virol 2005; 79: 214-224.
18. Graham T, McIntosh J, Work LM, Nathwani A, Baker AH. Performance of AAV8 vectors expressing human factor IX from a hepatic-selective promoter following intravenous injection into rats. Genet Vaccines Ther 2008; 6: 9.
19. Bilbao R, Reay DP, Li J, Xiao X, Clemens PR. Patterns of gene expression from in utero delivery of adenoviral-associated vector serotype 1. Hum Gene Ther 2005; 16: 678-684.
20. Mitchell M, Jerebtsova M, Batshaw ML, Newman K, Ye X. Long-term gene transfer to mouse fetuses with recombinant adenovirus and adeno-associated virus (AAV) vectors. Gene Therapy 2000; 7: 1986-1992.
21. Reiser PJ, Greaser ML, Moss RL. Myosin heavy chain composition of single cells from avian slow skeletal muscle is strongly correlated with velocity of shortening during development. Dev Biol 1988; 129 400-407.
22. Barany M. ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 1967; 50(Suppl): 197-218.
23. Lai Y, Yue Y, Liu M, Ghosh A, Engelhardt JF, Chamberlain JS et al. Efficient in vivo gene expression by trans-splicing adeno-associated viral vectors. Nat Biotechnol 2005; 23: 1435-1439.
24. Blankinship MJ, Gregorevic P, Allen JM, Harper SQ, Harper H, Halbert CL et al. Efficient transduction of skeletal muscle using vectors based on adeno-associated virus serotype 6. Mol Ther 2004; 10 671-678.
25. Pruchnic R, Cao B, Peterson ZQ, Xiao X, Li J, Samulski RJ et al. The use of adeno-associated virus to circumvent the maturation-dependent viral transduction of muscle fibers. Hum Gene Ther 2000; 11: 521-536.
26. Bostick B, Ghosh A, Yue Y, Long C, Duan D. Systemic AAV-9 transduction in mice is influenced by animal age but not by the route of administration. Gene Therapy 2007; 14: 1605-1609.
27. Yue Y, Ghosh A, Long C, Bostick B, Smith BF, Kornegay JN et al. A single intravenous injection of adeno-associated virus serotype-9 leads to whole body skeletal muscle transduction in dogs. Mol Ther 2008; 16: 1944-1952.
28. Bilbao R, Reay DP, Wu E, Zheng H, Biermann V, Kochanek S et al. Comparison of high-capacity and first-generation adenoviral vector gene delivery to murine muscle in utero. Gene Therapy 2005; 12: 39-47.
29. Boyle MP, Enke RA, Adams RJ, Guggino WB, Zeitlin PL. In utero AAV-mediated gene transfer to rabbit pulmonary epithelium. Mol Ther 2001; 4: 115-121.
30. Sabatino DE, Mackenzie TC, Peranteau W, Edmonson S, Campagnoli C, Liu YL et al. Persistent expression of hF.IX after tolerance induction by in utero or neonatal administration of AAV-1-F.IX in hemophilia B mice. Mol Ther 200; 15: 1677-1685.
31. Bouchard S, MacKenzie TC, Radu AP, Hayashi S, Peranteau WH, Chirmule N et al. Long-term transgene expression in cardiac and skeletal muscle following fetal administration of adenoviral or adeno-associated viral vectors in mice. J Gene Med 2003; 5: 941-950.
32. Reay DP, Bilbao R, Koppanati BM, Cai L, O'Day TL, Jiang Z et al. Full-length dystrophin gene transfer to the mdx mouse in utero. Gene Therapy 2008; 15: 531-536.
33. MacKenzie TC, Kobinger GP, Louboutin JP, Radu A, Javazon EH, Sena-Esteves M et al. Transduction of satellite cells after prenatal intramuscular administration of lentiviral vectors. J Gene Med 2005; 7: 50-58.
34. Akache B, Grimm D, Pandey K, Yant SR, Xu H, Kay MA. The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3 and 9. J Virol 2006; 80: 9831-9836.
35. Taylor PA, McElmurry RT, Lees CJ, Harrison DE, Blazar BR. Allogenic fetal liver cells have a distinct competitive engraftment advantage over adult bone marrow cells when infused into fetal as compared with adult severe combined immunodeficient recipients. Blood 2002; 99: 1870-1872.
36. O'Donoghue K, Fisk NM. Fetal stem cells. Best Pract Res Clin Obstet Gynaecol 2004; 18: 853-875.
37. Lansdorp PM, Dragowska W, Mayani H. Ontogeny-related changes in proliferative potential of human hematopoietic cells. J Exp Med 1993; 178: 787-791.
38. Marshall E. Gene therapy death prompts review of adenovirus vector. Science 1999; 286: 2244-2245.
39. Lipshutz GS, Gruber CA, Cao Y, Hardy J, Contag CH, Gaensler KM. In utero delivery of adeno-associated viral vectors: Intraperitoneal gene transfer produces long-term expression. Mol Ther 2001; 3: 284-292.
40. Winkel LP, Hagemans ML, van Doorn PA, Loonen MC, Hop WJ, Reuser AJ et al. The natural course of non-classic Pompe's disease; a review of 225 published cases. J Neurol 2005; 252: 875-884.
41. Xiao X, Li J, Samulski RJ. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J Virol 1998; 72: 2224-2232.
42. Li J, Samulski RJ, Xiao X. Role for highly regulated rep gene expression in adeno-associated virus vector production. J Virol 1997; 71 5236-5243.
43. Bilbao R, Reay DP, Hughes T, Biermann V, Volpers C, Goldberg L et al Fetal muscle gene transfer is not enhanced by an RGD capsid modification to high-capacity adenoviral vectors. Gene Therapy 2003; 10: 1821-1829.
44. Senoo M, Matsubara Y, Fujii K, Nagasaki Y, Hiratsuka M, Kure S et al Adenovirus-mediated in utero gene transfer in mice and guinea pigs: tissue distribution of recombinant adenovirus determined by quantitative TaqMan-polymerase chain reaction assay. Mol Genet Metab 2000; 69: 269-276.
45. Pan D, Gunther R, Duan W, Wendell S, Kaemmerer W, Kafri T et al. Biodistribution and toxicity studies of VSVG-pseudotyped lentiviral vector after intravenous administration in mice with the observation of in vivo transduction of bone marrow. Mol Ther 2002; 6: 19-29.