Systemic delivery of scAAV9 in fetal macaques facilitates neuronal transduction of the central and peripheral nervous systems

Gene Therapy

Volumn 20, Issue 1, 2013, Pages 69-83

  Mattar, C N ^a   Waddington, S N ^b   Biswas, A ^a   Johana, N ^a   Ng, X W ^c   Fisk, A S ^d   Fisk, N M ^a,d   Tan, L G ^a   Rahim, A A ^b   Buckley, S M K ^b   Tan, M H ^e   Lu, J ^e   Choolani, M ^a   Chan, J K Y ^a,c,f  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c KK WOMEN'S AND CHILDREN'S HOSPITAL   (Singapore)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e DSO NATIONAL LABORATORIES   (Singapore)

^f DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

AAV9; central nervous system; intrauterine gene transfer; neuron; non human primate

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; NESTIN;

ADENO ASSOCIATED VIRUS; ARTICLE; ASTROCYTE; CENTRAL NERVOUS SYSTEM; COPY NUMBER VARIATION; CYTOMEGALOVIRUS; FEMALE; FETUS; GENE TARGETING; GENE THERAPY; MACACA; MALE; MOTONEURON; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; PERIPHERAL NERVOUS SYSTEM; PHOTORECEPTOR; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UMBILICAL VEIN;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CEREBRAL CORTEX; CYTOMEGALOVIRUS; DEPENDOVIRUS; FEMALE; FETUS; GENETIC THERAPY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; MACACA; OLIGODENDROGLIA; PERIPHERAL NERVOUS SYSTEM; PREGNANCY; RETINA; TRANSDUCTION, GENETIC;

MACACA; PRIMATES;

EID: 84871994994     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2011.216     Document Type: Article

References (77)

1. Costantini L, Bakowska J, Breakefield X, Isacson O. Gene therapy in the CNS. Gene Therapy 2000; 7: 93-109 (Pubitemid 30088955)
2. Rahim AA, Wong AM, Buckley SM, Chan JK, David AL, Cooper JD et al. In utero gene transfer to the mouse nervous system. Biochem Soc Trans 2010; 38: 1489-1493
3. Matzner U, Matthes F, Weigelt C, Andersson C, Eistrup C, Fogh J et al. Non-inhibitory antibodies impede lysosomal storage reduction during enzyme replacement therapy of a lysosomal storage disease. J Mol Med 2008; 86: 433-442
4. Brightman M, Ishihara S, Chang L. Penetration of solutes, viruses, and cells across the blood-brain barrier. Curr Top Microbiol Immunol 1995; 202: 63-78
5. Pardridge WM. Drug and gene targeting to the brain with molecular Trojan horses. Nat Rev Drug Discov 2002; 1: 131-139 (Pubitemid 41646520)
6. Ek C, Dziegielewska K, Stolp H, Saunders N. Functional effectiveness of the bloodbrain barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica). J Comp Neurol 2006; 496: 13-26
7. Pastores G, Sibille A, Grabowski G. Enzyme therapy in Gaucher disease type 1: dosage efficacy and adverse effects in 33 patients treated for 6 to 24 months. Blood 1993; 82: 408-416 (Pubitemid 23206103)
8. Wynn R, Wraith J, Mercer J, O'Meara A, Tylee K, Thornley M et al. Improved metabolic correction in patients with lysosomal storage disease treated with hematopoietic stem cell transplant compared with enzyme replacement therapy. J Pediatr 2009; 154: 609-611
9. Krivit W, Shapiro EG, Peters C, Wagner JE, Cornu G, Kurtzberg J et al. Hematopoietic stem-cell transplantation in globoid-cell leukodystrophy. N Engl J Med 1998; 338: 1119-1126 (Pubitemid 28227482)
10. Krall WJ, Challita PM, Perlmutter LS, Skelton DC, Kohn DB. Cells expressing human glucocerebrosidase from a retroviral vector repopulate macrophages and central nervous system microglia after murine bone marrow transplantation. Blood 1994; 83: 2737-2748 (Pubitemid 24135869)
11. Peters C, Steward CG. Hematopoietic cell transplantation for inherited metabolic diseases: an overview of outcomes and practice guidelines. Bone Marrow Transplant 2003; 31: 229-239 (Pubitemid 36336225)
12. Ringden O, Groth CG, Erikson A, Granqvist S, Mansson JE, Sparrelid E. Ten years' experience of bone marrow transplantation for Gaucher disease. Transplantation 1995; 59: 864-870
13. Kirik D, Georgievska B, Burger C, Winkler C, Muzyczka N, Mandel RJ et al. Reversal of motor impairments in parkinsonian rats by continuous intrastriatal delivery of L-dopa using rAAV-mediated gene transfer. Proc Natl Acad Sci USA 2002; 99: 4708-4713 (Pubitemid 34286049)
14. Powers JM, Moser HW. Peroxisomal disorders: genotype, phenotype, major neuropathologic lesions, and pathogenesis. Brain Pathol 1998; 8: 101-120 (Pubitemid 28055768)
15. McIntyre C, Byers S, Anson DS. Correction of mucopolysaccharidosis type IIIA somatic and central nervous system pathology by lentiviral-mediated gene transfer. J Gene Med 2010; 12: 717-728
16. Griffey MA, Wozniak D, Wong M, Bible E, Johnson K, Rothman SM et al. CNSdirected AAV2-mediated gene therapy ameliorates functional deficits in a murine model of infantile neuronal ceroid lipofuscinosis. Mol Ther 2006; 13: 538-547 (Pubitemid 43257621)
17. Wu Z, Asokan A, Samulski RJ. Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol Ther 2006; 14: 316-327 (Pubitemid 44184972)
18. Penaud-Budloo M, Le Guiner C, Nowrouzi A, Toromanoff A, Cherel Y, Chenuaud P et al. Adeno-associated virus vector genomes persist as episomal chromatin in primate muscle. J Virol 2008; 82: 7875-7885
19. Berges BK, Yellayi S, Karolewski BA, Miselis RR, Wolfe JH, Fraser NW. Widespread correction of lysosomal storage in the mucopolysaccharidosis type VII mouse brain with a herpes simplex virus type 1 vector expressing beta-glucuronidase. Mol Ther 2006; 13: 859-869
20. Mandel R, Manfredsson F, Foust K, Rising A, Reimsnider S, Nash K et al. Recombinant adeno-associated viral vectors as therapeutic agents to treat neurological disorders. Mol Ther 2006; 13: 463-483 (Pubitemid 43257615)
21. Inagaki K, Fuess S, Storm TA, Gibson GA, McTiernan CF, Kay MA. Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol Ther 2006; 14: 45-53 (Pubitemid 43899488)
22. Gao G, Vandenberghe LH, Alvira MR, Lu Y, Calcedo R, Zhou X. Clades of adenoassociated viruses are widely disseminated in human tissues. J Virol 2004; 78: 6381-6388 (Pubitemid 38715936)
23. 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
24. Rahim AA, Wong AM, Hoefer K, Buckley SM, Mattar CN, Cheng SH et al. Intravenous administration of AAV2/9 to the fetal and neonatal mouse leads to differential targeting of CNS cell types and extensive transduction of the nervous system. FASEB J 2011; 25: 3505-3518
25. Foust K, Wang X, McGovern V, Braun L, Bevan A, Haidet A et al. Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat Biotechnol 2010; 28: 271-274
26. Duque S, Joussemet B, Riviere C, Marais T, Dubreil L, Douar AM et al. Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol Ther 2009; 17: 1187-1196
27. Thrasher AJ, Hacein-Bey-Abina S, Gaspar HB, Blanche S, Davies EG, Parsley K et al. Failure of SCID-X1 gene therapy in older patients. Blood 2005; 105: 4255-4257 (Pubitemid 40720770)
28. Stewart P, Farrell C, Holash J, Elliot D, Neiman J, Resch L et al. Effect of bile duct ligation-induced liver damage on the blood-brain barrier. Can J Neurol Sci 1989; 16: 451-452 (Pubitemid 19278347)
29. Wolburg H, Lippoldt A. Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 2002; 38: 323-337 (Pubitemid 36398254)
30. Coutelle C, Themis M, Waddington SN, Buckley SM, Gregory LG, Nivsarkar MS et al. Gene therapy progress and prospects: fetal gene therapy-first proofs of concept-some adverse effects. Gene Ther 2005; 12: 1601-1607 (Pubitemid 41670350)
31. Waddington SN, Kramer MG, Hernandez-Alcoceba R, Buckley SM, Themis M, Coutelle C et al. In utero gene therapy: current challenges and perspectives. Mol Ther 2005; 11: 661-676 (Pubitemid 40575612)
32. Karolewski BA, Wolfe JH. Genetic correction of the fetal brain increases the lifespan of mice with the severe multisystemic disease mucopolysaccharidosis type VII. Mol Ther 2006; 14: 14-24 (Pubitemid 43899484)
33. Mestas J, Hughes C. Of mice and not men: differences between mouse and human immunology. J Immunol 2004; 172: 2731-2738 (Pubitemid 38263654)
34. Holladay S, Smialowicz R. Development of the murine and human immune system: differential effects of immunotoxicants depend on time of exposure. Environ Health Perspect 2000; 108 (Suppl 3): 463-473 (Pubitemid 30466174)
35. Fu H, Dirosario J, Killedar S, Zaraspe K, McCarty DM. Correction of neurological disease of mucopolysaccharidosis IIIB in adult mice by rAAV9 trans-blood-brain barrier gene delivery. Mol Ther 2011; 19: 1025-1033
36. 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; 22: 1129-1135
37. 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
38. Geisler A, Jungmann A, Kurreck J, Poller W, Katus HA, Vetter R et al. MicroRNA122-regulated transgene expression increases specificity of cardiac gene transfer upon intravenous delivery of AAV9 vectors. Gene Therapy 2011; 18: 199-209
39. Pulicherla N, Shen S, Yadav S, Debbink K, Govindasamy L, Agbandje-McKenna M et al. Engineering liver-detargeted AAV9 vectors for cardiac and musculoskeletal gene transfer. Mol Ther 2011; 19: 1070-1078
40. Bell CL, Vandenberghe LH, Bell P, Limberis MP, Gao GP, Van Vliet K et al. The AAV9 receptor and its modification to improve in vivo lung gene transfer in mice. J Clin Invest 2011; 121: 2427-2435
41. Gray SJ, Matagne V, Bachaboina L, Yadav S, Ojeda SR, Samulski RJ. Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol Ther 2011; 19: 1058-1069
42. 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
43. Stites D, Carr M, Fundenberg H. Ontogeny of cellular immunity in the human fetus. Development of responses to phytohaemmagglutinin and to allogeneic cells. Cell Immunol 1974; 11: 257-271
44. Hendrickx A, Makori N, Peterson P. The nonhuman primate as a model of developmental immunotoxicity. Hum Exp Toxicol 2002; 21: 537-542 (Pubitemid 35385992)
45. Rashmi N, Phillipa K, Peter WS. A classification of pregnancy losses after invasive prenatal diagnostic procedures: an approach to allow comparison of units with a different case mix. Prenat Diagn 2003; 23: 488-492
46. Chan J, Kumar S, Fisk NM. First trimester embryo-fetoscopic and ultrasoundguided fetal blood sampling for ex vivo viral transduction of cultured human fetal mesenchymal stem cells. Hum Reprod 2008; 23: 2427-2437
47. Rodeck CH. Fetoscopy guided by real-time ultrasound for pure fetal blood samples, fetal skin samples, and examination of the fetus in utero. Br J Obstet Gynaecol 1980; 87: 449-456 (Pubitemid 10082790)
48. Holladay SD, Smialowicz RJ. Development of the murine and human immune system: differential effects of immunotoxicants depend on time of exposure. Environ Health Perspect 2000; 108 (Suppl 3): 463-473 (Pubitemid 30466174)
49. Goodnow CC, Sprent J, Fazekas de St Groth B, Vinuesa CG. Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 2005; 435: 590-597 (Pubitemid 40825498)
50. Mattar CN, Nathwani AC, Waddington SN, Dighe N, Kaeppel C, Nowrouzi A et al. Stable human FIX expression after 0. 9 G intrauterine gene transfer of selfcomplementary adeno-associated viral vector 5 and 8 in macaques. Mol Ther 2011; 19: 1950-1960
51. Danzer KM, Krebs SK, Wolff M, Birk G, Hengerer B. Seeding induced by alphasynuclein oligomers provides evidence for spreading of alpha-synuclein pathology. J Neurochem 2009; 111: 192-203
52. Lee HJ, Suk JE, Bae EJ, Lee JH, Paik SR, Lee SJ. Assembly-dependent endocytosis and clearance of extracellular alpha-synuclein. Int J Biochem Cell Biol 2008; 40: 1835-1849
53. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, Crews L et al. Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci USA 2009; 106: 13010-13015
54. Gousset K, Schiff E, Langevin C, Marijanovic Z, Caputo A, Browman DT et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat Cell Biol 2009; 11: 328-336
55. Brundin P, Melki R, Kopito R. Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat Rev Mol Cell Biol 2010; 11: 301-307
56. Miao CH, Nakai H, Thompson AR, Storm TA, Chiu W, Snyder RO et al. Nonrandom transduction of recombinant adeno-associated virus vectors in mouse hepatocytes in vivo: cell cycling does not influence hepatocyte transduction. J Virol 2000; 74: 3793-3803 (Pubitemid 30180322)
57. Cunningham SC, Spinoulas A, Carpenter KH, Wilcken B, Kuchel PW, Alexander IE. AAV2/8-mediated correction of OTC deficiency is robust in adult but not neonatal Spfash mice. Mol Ther 2009; 17: 1340-1346
58. Wang L, Bell P, Lin J, Calcedo R, Tarantal AF, Wilson JM. AAV8-mediated hepatic gene transfer in infant rhesus monkeys (Macaca mulatta). Mol Ther 2011; 19: 2012-2020
59. Gray SJ, Foti SB, Schwartz JW, Bachaboina L, Taylor-Blake B, Coleman J et al. Optimizing promoters for recombinant adeno-associated virus-mediated gene expression in the peripheral and central nervous system using self-complementary vectors. Hum Gene Ther 2011; 22: 1143-1153
60. Salva MZ, Himeda CL, Tai PW, Nishiuchi E, Gregorevic P, Allen JM et al. Design of tissue-specific regulatory cassettes for high-level rAAV-mediated expression in skeletal and cardiac muscle. Mol Ther 2007; 15: 320-329 (Pubitemid 46111882)
61. 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 (Pubitemid 39650967)
62. Nakai H, Thomas CE, Storm TA, Fuess S, Powell S, Wright JF. A limited number of transducible hepatocytes restricts a wide-range linear vector dose response in recombinant adeno-associated virus-mediated liver transduction. J Virol 2002; 76: 11343-11349 (Pubitemid 35231289)
63. Hahnewald R, Wegner W, Reiss J. AAV-mediated gene therapy for metabolic diseases: dosage and reapplication studies in the molybdenum cofactor deficiency model. Genet Vaccines Ther 2009; 7: 9
64. Themis M, Schneider H, Kiserud T, Cook T, Adebakin S, Jezzard S et al. Successful expression of beta-galactosidase and factor IX transgenes in fetal and neonatal sheep after ultrasound-guided percutaneous adenovirus vector administration into the umbilical vein. Gene Therapy 1999; 6: 1239-1248 (Pubitemid 29359017)
65. Tran ND, Porada CD, Almeida-Porada Ga, Glimp HA, Anderson WF, Zanjani ED. Induction of stable prenatal tolerance to b-galactosidase by in utero gene transfer into preimmune sheep fetuses. Blood 2001; 97: 3417-3423
66. Waddington SN, Buckley SMK, Nivsarkar M, Jezzard S, Schneider H, Dahse T et al. In utero gene transfer of human factor IX to fetal mice can induce postnatal tolerance of the exogenous clotting factor. Blood 2003; 101: 1359-1366 (Pubitemid 36182507)
67. 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 2007; 15: 1677-1685 (Pubitemid 47289012)
68. Wang Z, Kuhr CS, Allen JM, Blankinship M, Gregorevic P, Chamberlain JS et al. Sustained AAV-mediated dystrophin expression in a canine model of Duchenne muscular dystrophy with a brief course of immunosuppression. Mol Ther 2007; 15: 1160-1166 (Pubitemid 46813619)
69. Xie J, Xie Q, Zhang H, Ameres SL, Hung JH, Su Q et al. MicroRNA-regulated, systemically delivered rAAV9: a step closer to CNS-restricted transgene expression. Mol Ther 2011; 19: 526-535
70. Michalski A, Leonard JV, Taylor DS. The eye and inherited metabolic disease: a review. J R Soc Med 1988; 81: 286-290
71. Blackshaw S, Fraioli RE, Furukawa T, Cepko CL. Comprehensive analysis of photoreceptor gene expression and the identification of candidate retinal disease genes. Cell 2001; 107: 579-589 (Pubitemid 34014860)
72. Simonelli F, Maguire AM, Testa F, Pierce EA, Mingozzi F, Bennicelli JL et al. Gene therapy for Leber's congenital amaurosis is safe and effective through 1. 5 years after vector administration. Mol Ther 2010; 18: 643-650
73. Kousta E, Hadjiathanasiou CG, Tolis G, Papathanasiou A. Pleiotropic genetic syndromes with developmental abnormalities associated with obesity. J Pediatr Endocrinol Metab 2009; 22: 581-592
74. Zamel R, Khan R, Pollex RL, Hegele RA. Abetalipoproteinemia: two case reports and literature review. Orphanet J Rare Dis 2008; 3: 19
75. Nicolini U, Nicolaidis P, Fisk NM, Tannirandorn Y, Rodeck CH. Fetal blood sampling from the intrahepatic vein: analysis of safety and clinical experience with 214 procedures. Obstet Gynecol 1990; 76: 47-53 (Pubitemid 20205217)
76. Asokan A, Conway JC, Phillips JL, Li C, Hegge J, Sinnott R et al. Reengineering a receptor footprint of adeno-associated virus enables selective and systemic gene transfer to muscle. Nat Biotechnol 2010; 28: 79-82
77. Weatherall DJ. The Use of Non-Human Primates in Research. Academy of Medical Sciences: London, 2006