Efficient central nervous system AAVrh10-mediated intrathecal gene transfer in adult and neonate rats

Gene Therapy

Volumn 22, Issue 4, 2015, Pages 316-324

  Hordeaux, J ^a,b,c   Dubreil, L ^a,b   Deniaud, J ^a,b   Iacobelli, F ^a,b   Moreau, S ^a,b   Ledevin, M ^a,b   Le Guiner, C ^d   Blouin, V ^d   Le Duff, J ^d   Mendes Madeira, A ^d   Rolling, F ^d   Cherel, Y ^a,b   Moullier, P ^d,e   Colle, M A ^a,b  

^a INRA UMR 703   (France)

^b LUNAM UNIVERSITÉ   (France)

^c UNIVERSITÉ DE NANTES   (France)

^d UNIVERSITÉ DE NANTES   (France)

^e UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; GREEN FLUORESCENT PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN STEM; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CEREBROSPINAL FLUID; CONTROLLED STUDY; GENE DOSAGE; GENE EXPRESSION; GENETIC TRANSDUCTION; GIGANTOCELLULAR RETICULAR NUCLEUS; GROUPS BY AGE; HEMISPHERE; HUMORAL IMMUNITY; MOTOR CORTEX; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PURKINJE CELL; RAT; SAFETY; SENSORY NERVE CELL; SPINAL CORD; SPINAL CORD MOTONEURON; SPINAL CORD NERVE CELL; SPINAL GANGLION; TRANSGENE; TRIGEMINAL NERVE; TRIGEMINAL NUCLEUS; VIRAL GENE DELIVERY SYSTEM; VIRAL TROPISM; ANIMAL; GENE TRANSFER; GENE VECTOR; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; SPRAGUE DAWLEY RAT;

RATTUS;

ADMINISTRATION, INTRAVENOUS; ANIMALS; ANIMALS, NEWBORN; GANGLIA, SPINAL; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; PURKINJE CELLS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SPINAL CORD;

EID: 84926421140     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2014.121     Document Type: Article

References (43)

1. Haskins ME. Gene therapy for lysosomal storage diseases (LSDs) in large animal models. ILAR J 2009; 50: 112-121.
2. McCown TJ, Xiao X, Li J, Breese GR, Samulski RJ. Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res 1996; 713: 99-107.
3. Vite CH, Passini Ma, Haskins ME, Wolfe JH. Adeno-associated virus vectormediated transduction in the cat brain. Gene Therapy 2003; 10: 1874-1881.
4. Ciron C, Desmaris N, Colle M-A, Raoul S, Joussemet B, Vérot L et al. Gene therapy of the brain in the dog model of Hurler's syndrome. Ann Neurol 2006; 60: 204-213.
5. Ciron C, Cressant A, Raoul S, Cherel Y, Hantraye P, De N. Human alpha-iduronidase gene transfer mediated of nonhuman primates: vector diffusion and biodistribution. Hum Gene Ther 2009; 20: 350-360.
6. Colle M-A, Piguet F, Bertrand L, Raoul S, Bieche I, Dubreil L et al. Efficient intracerebral delivery of AAV5 vector encoding human ARSA in non-human primate. Hum Mol Genet 2010; 19: 147-158.
7. Ellinwood NM, Ausseil J, Desmaris N, Bigou S, Liu S, Jens JK et al. Safe, efficient, and reproducible gene therapy of the brain in the dog models of Sanfilippo and Hurler syndromes. Mol Ther 2011; 19: 251-259.
8. Cearley CN, Wolfe JH. Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol Ther 2006; 13: 528-537.
9. Klein RL, Dayton RD, Tatom JB, Henderson KM, Henning PP. AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Mol Ther 2008; 16: 89-96.
10. Piguet F, Sondhi D, Piraud M, Fouquet F, Hackett NR, Ahouansou O et al. Correction of brain oligodendrocytes by AAVrh.10 intracerebral gene therapy in metachromatic leukodystrophy mice. Hum Gene Ther 2012; 23: 903-914.
11. Swain GP, Prociuk M, Bagel JH, Donnell PO, Berger K, Drobatz K et al. Adeno-associated virus serotypes 9 and rh10 mediate strong neuronal transduction of the dog brain. Gene Therapy 2014; 21: 28-36.
12. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, Kaspar BK. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 2009; 27: 59-65.
13. Duque S, Joussemet B, Riviere C, Marais T, Dubreil L, Douar A-M et al. Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol Ther 2009; 17: 1187-1196.
14. Bevan AK, Duque S, Foust KD, Morales PR, Braun L, Schmelzer L et al. Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Mol Ther 2011; 19: 1971-1980.
15. Wang DB, Dayton RD, Henning PP, Cain CD, Zhao LR, Schrott LM et al. Expansive gene transfer in the rat CNS rapidly produces amyotrophic lateral sclerosis relevant sequelae when TDP-43 is overexpressed. Mol Ther 2010; 18: 2064-2074.
16. Snyder BR, Gray SJ, Quach ET, Huang JW, Leung CH, Samulski RJ et al. Comparison of adeno-associated viral vector serotypes for spinal cord and motor neuron gene delivery. Hum Gene Ther 2011; 1135: 1129-1135.
17. Federici T, Taub JS, Baum GR, Gray SJ, Grieger JC, Matthews Ka et al. Robust spinal motor neuron transduction following intrathecal delivery of AAV9 in pigs. Gene Therapy 2012; 19: 852-859.
18. Samaranch L, Salegio EA, Sebastian WS, Kells AP, Foust KD, Bringas JR et al. AAV9 transduction inthe CNS of non-human primate. Hum Gene Ther 2012; 23: 382-389.
19. Samaranch L, Salegio Ea, San Sebastian W, Kells AP, Bringas JR, Forsayeth J et al. Strong cortical and spinal cord transduction after AAV7 and AAV9 delivery into the cerebrospinal fluid of nonhuman primates. Hum Gene Ther 2013; 24: 526-532.
20. Haurigot V, Marcó S, Ribera A, Garcia M, Ruzo A, Villacampa P et al. Whole body correction of mucopolysaccharidosis IIIA by intracerebrospinal fluid gene therapy. J Clin Invest 2013; 123: 3254-3271.
21. Gray SJ, Nagabhushan Kalburgi S, McCown TJ, Jude Samulski R. Global CNS gene delivery and evasion of anti-AAV-neutralizing antibodies by intrathecal AAV administration in non-human primates. Gene Therapy 2013; 20: 450-459.
22. Bucher T, Colle M-A, Wakeling E, Dubreil L, Fyfe J, Briot-Nivard D et al. scAAV9 intracisternal delivery results in efficient gene transfer to the central nervous system of a feline model of motor neuron disease. Hum Gene Ther 2013; 24: 670-682.
23. Miyake N, Miyake K, Yamamoto M, Hirai Y, Shimada T. Global gene transfer into the CNS across the BBB after neonatal systemic delivery of single-stranded AAV vectors. Brain Res 2011; 1389: 19-26.
24. Hu C, Busuttil RW, Lipshutz GS. RH10 provides superior transgene expression in mice when compared with natural AAV serotypes for neonatal gene therapy. J Gene Med 2010; 12: 766-778.
25. Zhang H, Yang B, Mu X, Ahmed SS, Su Q, He R et al. Several rAAV vectors efficiently cross the blood-brain barrier and transduce neurons and astrocytes in the neonatal mouse central nervous system. Mol Ther 2011; 19: 1440-1448.
26. McCarty DM. Self-complementary AAV vectors; advances and applications. Mol Ther 2008; 16: 1648-1656.
27. Dong B, Nakai H, Xiao W. Characterization of genome integrity for oversized recombinant AAV vector. Mol Ther 2010; 18: 87-92.
28. Wang Y, Ling C, Song L, Wang L, Aslanidi GV, Tan M et al. Limitations of encapsidation of recombinant self-complementary adeno-associated viral genomes in different serotype capsids and their quantitation. Hum Gene Ther Methods 2012; 23: 225-233.
29. Hirsch ML, Li C, Bellon I, Yin C, Chavala S, Pryadkina M et al. Oversized AAV transductifon is mediated via a DNA-PKcs-independent, Rad51C-dependent repair pathway. Mol Ther 2013; 21: 2205-2216.
30. Xu Y, Gu Y, Wu P, Li G-W, Huang L-YM. Efficiencies of transgene expression in nociceptive neurons through different routes of delivery of adeno-associated viral vectors. Hum Gene Ther 2003; 14: 897-906.
31. Storek B, Harder NM, Banck MS, Wang C, McCarty DM, Janssen WG et al. Intrathecal long-term gene expression by self-complementary adeno-associated virus type 1 suitable for chronic pain studies in rats. Mol Pain 2006; 2: 4.
32. Towne C, Pertin M, Beggah AT, Aebischer P, Decosterd I. Recombinant adenoassociated virus serotype 6 (rAAV2/6)-mediated gene transfer to nociceptive neurons through different routes of delivery. Mol Pain 2009; 5: 52.
33. Vulchanova L, Schuster DJ, Belur LR, Riedl MS, Podetz-Pedersen KM, Kitto KF et al. Differential adeno-associated virus mediated gene transfer to sensory neurons following intrathecal delivery by direct lumbar puncture. Mol Pain 2010; 6: 31.
34. Fu H, Muenzer J, Samulski RJ, Breese G, Sifford J, Zeng X et al. Self-complementary adeno-associated virus serotype 2 vector: global distribution and broad dispersion of AAV-mediated transgene expression in mouse brain. Mol Ther 2003; 8: 911-917.
35. Dirren E, Towne CL, Setola V, Redmond DE, Schneider BL, Aebischer P. Intracerebroventricular injection of adeno-associated virus 6 and 9 vectors for cell type-specific transgene expression in the spinal cord. Hum Gene Ther 2014; 25: 109-120.
36. Gao G, Vandenberghe LH, Alvira MR, Lu Y, Calcedo R, Zhou X et al. Clades of adeno-associated viruses are widely disseminated in human tissues clades of adeno-associated viruses are widely disseminated in human tissues. J Virol 2004; 78: 6381-6388.
37. Boutin S, Monteilhet V, Veron P, Leborgne C, Benveniste O, Montus MF et al. Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) Types 1,2,5,6,8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum Gene Ther 2010; 21: 704-712.
38. Wang H, Yang B, Qiu L, Yang C, Kramer J, Su Q et al. Widespread spinal cord transduction by intrathecal injection of rAAV delivers efficacious RNAi therapy for amyotrophic lateral sclerosis. Hum Mol Genet 2014; 23: 668-681.
39. Gray SJ, Foti SB, Schwartz JW, Bachabiona L, Taylor-Blake B, Coleman J et al. Optimizing promoters for rAAV-mediated gene expression in the peripheral and central nervous system using self-complementary vectors. Hum Gene Ther 2011; 22: 1143-1153.
40. Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M et al. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest 2013; 123: 1299-1309.
41. Zhou X, Zeng X, Fan Z, Li C, McCown T, Samulski RJ et al. Adeno-associated virus of a single-polarity DNA genome is capable of transduction in vivo. Mol Ther 2008; 16: 494-499.
42. Milward Ea, Fitzsimmons C, Szklarczyk A, Conant K. The matrix metalloproteinases and CNS plasticity: an overview. J Neuroimmunol 2007; 187: 9-19.
43. Rabinowitz JE, Rolling F, Li C, Xiao W, Xiao X, Samulski RJ. Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J Virol 2002; 76: 791-801.