Widespread spinal cord transduction by intrathecal injection of rAAV delivers efficacious RNAi therapy for amyotrophic lateral sclerosis

Human Molecular Genetics

Volumn 23, Issue 3, 2014, Pages 668-681

  Wang, Hongyan ^a   Yang, Bin ^a,d   Qiu, Linghua ^a   Yang, Chunxing ^a   Kramer, Joshua ^b   Su, Qin ^a   Guo, Yansu ^a,c   Brown, Robert H ^a   Gao, Guangping ^a   Xu, Zuoshang ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HEBEI MEDICAL UNIVERSITY   (China)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; MICRORNA; RECOMBINANT ADENOASSOCIATED VIRUS; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN THIRD VENTRICLE; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CONTROLLED STUDY; DISEASE COURSE; FEMALE; FOREBRAIN; GENE EXPRESSION; MOTONEURON; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SEROTYPE; SPINAL CORD; SYSTEMATIC REVIEW; VIRAL GENE THERAPY;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CALLITHRIX; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; DEPENDOVIRUS; FEMALE; GENETIC THERAPY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; INJECTIONS, SPINAL; MICE; MICE, TRANSGENIC; RNA INTERFERENCE; SPINAL CORD; SUPEROXIDE DISMUTASE; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 84892474913     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt454     Document Type: Article

References (53)

1. Andersen, P.M. and Al-Chalabi, A. (2011) Clinical genetics of amyotrophic lateral sclerosis: what do we really know?. Nat. Rev. Neurol., 7, 603-615.
2. Ludolph, A.C., Brettschneider, J. and Weishaupt, J.H. (2012) Amyotrophic lateral sclerosis. Curr. Opin. Neurol., 25, 530-535.
3. Xu, Z. (2000) Mechanism and treatment of motoneuron degeneration in ALS: what have SOD1 mutants told us?. ALS Other Mot. Neu. Disord., 1, 225-234.
4. Ding, H., Schwarz, D.S., Keene, A., Affarel, B., Fenton, L., Xia, X., Shi, Y., Zamore, P.D. and Xu, Z. (2003) Selective silencing by RNAi of a dominant allele that causes amyotrophic lateral sclerosis. Aging Cell, 2, 209-217.
5. Ralph, G.S., Radcliffe, P.A., Day, D.M., Carthy, J.M., Leroux, M.A., Lee, D.C.P., Wong, L.-F., Bilsland, L.G., Greensmith, L., Kingsman, S.M. et al. (2005) Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat. Med., 11, 429-433.
6. Raoul, C., Abbas-Terki, T., Bensadoun, J.-C., Guillot, S., Haase, G., Szulc, J., Henderson, C.E. and Aebischer, P. (2005) Lentiviral-mediated silencing of SOD1 throughRNA interference retards disease onset and progression in a mouse model of ALS. Nat. Med., 11, 423-428.
7. Smith, R.A., Miller, T.M., Yamanaka, K., Monia, B.P., Condon, T.P., Hung, G., Lobsiger, C.S., Ward, C.M.,McAlonis-Downes, M., Wei, H. et al. (2006) Antisense oligonucleotide therapy for neurodegenerative disease. J. Clin. Investig., 116, 2290-2296.
8. Xia, X., Zhou, H., Huang, Y. and Xu, Z. (2006) Allele-specific RNAi selectively silences mutant SOD1 and achieves significant therapeutic benefit in vivo. Neurobiol. Dis., 23, 578-586.
9. Wu, R., Wang, H., Xia, X., Zhou, H., Liu, C., Castro, M. and Xu, Z. (2009) Nerve injection of viral vectors efficiently transfers transgenes into motor neurons and delivers RNAi therapy against ALS. Antioxid. Redox Signal., 11, 1523-1534.
10. Wang, H., Ghosh, A., Baigude, H., Yang, C.S., Qiu, L., Xia, X., Zhou, H., Rana, T.M. and Xu, Z. (2008) Therapeutic gene silencing delivered by a chemically modified small interfering RNA against mutant SOD1 slows amyotrophic lateral sclerosis progression. J. Biol. Chem., 283, 15845- 15852.
11. Boudreau, R.L., Rodriguez-Lebron, E. and Davidson, B.L. (2011) RNAi medicine for the brain: progresses and challenges. Hum. Mol. Genet., 20, R21-R27.
12. Grieger, J.C. and Samulski, R.J. (2012) Adeno-associated virus vectorology, manufacturing, and clinical applications. Methods Enzymol., 507, 229-254.
13. Manfredsson, F.P. and Mandel, R.J. (2010) Development of gene therapy for neurological disorders. Discov. Med., 9, 204-211.
14. Vandenberghe, L.H., Wilson, J.M. and Gao, G. (2009) Tailoring the AAV vector capsid for gene therapy. Gene Ther., 16, 311-319.
15. Mittermeyer, G., Christine, C.W., Rosenbluth, K.H., Baker, S.L., Starr, P., Larson, P., Kaplan, P.L., Forsayeth, J., Aminoff, M.J. and Bankiewicz, K.S. (2012) Long-term evaluation of a phase 1 study of AADC gene therapy for Parkinson's disease. Hum. Gene Ther., 23, 377-381.
16. Bennett, J., Ashtari, M., Wellman, J., Marshall, K.A., Cyckowski, L.L., Chung, D.C., McCague, S., Pierce, E.A., Chen, Y., Bennicelli, J.L. et al. (2012) AAV2 gene therapy readministration in three adults with congenital blindness. Sci. Transl. Med., 4, 120ra115.
17. Kim, S.R., Kareva, T., Yarygina, O., Kholodilov, N. and Burke, R.E. (2012) AAV transduction of dopamine neurons with constitutively active Rheb protects from neurodegeneration and mediates axon regrowth. Mol. Ther., 20, 275-286.
18. McBride, J.L., Boudreau, R.L., Harper, S.Q., Staber, P.D., Monteys, A.M., Martins, I., Gilmore, B.L., Burstein, H., Peluso, R.W., Polisky, B. et al. (2008) Artificial miRNAs mitigate shRNA-mediated toxicity in the brain: Implications for the therapeutic development ofRNAi.Proc. Natl. Acad. Sci. USA, 105, 5868-5873.
19. Xia, H., Mao, Q., Eliason, S.L., Harper, S.Q., Martins, I.H., Orr, H.T., Paulson, H.L., Yang, L., Kotin, R.M. and Davidson, B.L. (2004) RNAi suppresses polyglutamine-induced neurodegeneration in a model of spinocerebellar ataxia. Nat. Med., 10, 816-820.
20. Snyder, B.R., Gray, S.J., Quach, E.T., Huang, J.W., Leung, C.H., Samulski, R.J., Boulis, N.M. and Federici, T. (2011) Comparison of adeno-associated viral vector serotypes for spinal cord and motor neuron gene delivery. Hum. Gene. Ther., 22, 1129-1135.
21. Kaspar, B.K., Llado, J., Sherkat, N., Rothstein, J.D. and Gage, F.H. (2003) Retrograde Viral Delivery of IGF-1 Prolongs Survival in a Mouse ALS Model. Science, 301, 839-842.
22. Azzouz, M., Ralph, G.S., Storkebaum, E., Walmsley, L.E., Mitrophanous, K.A., Kingsman, S.M., Carmeliet, P. and Mazarakis, N.D. (2004) VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature, 429, 413-417.
23. Towne, C., Setola, V., Schneider, B.L. and Aebischer, P. (2010) Neuroprotection by gene therapy targeting mutant SOD1in individual pools of motor neurons does not translate into therapeutic benefit in fALS mice. Mol. Ther., 19, 274-283.
24. Boulis, N.M., Turner, D.E., Dice, J.A., Bhatia, V. and Feldman, E.L. (1999) Characterization of adenoviral gene expression in spinal cord after remote vector delivery. Neurosurgery, 45, 131-138.
25. Foust, K.D., Nurre, E., Montgomery, C.L., Hernandez, A., Chan, C.M. and Kaspar, B.K. (2009) Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat. Biotechnol., 27, 59-65.
26. Duque, S., Joussemet, B., Riviere, C., Marais, T., Dubreil, L., Douar, A.M., Fyfe, J., Moullier, P., Colle, M.A. and Barkats, M. (2009) Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol. Ther., 17, 1187-1196.
27. Bevan, A.K., Duque, S., Foust, K.D., Morales, P.R., Braun, L., Schmelzer, L., Chan, C.M., McCrate, M., Chicoine, L.G., Coley, B.D. et al. (2011) Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Mol. Ther., 19, 1971-1980.
28. Zhang, H., Yang, B.,Mu, X., Ahmed,S.S., Su, Q., He, R., Wang, H., Mueller, C., Sena-Esteves, M., Brown, R. et al. (2011) Several rAAV vectors efficiently cross the blood-brain barrier and transduce neurons and astrocytes in the neonatal mouse central nervous system. Mol. Ther., 19, 1440-1448.
29. Gray, S.J., Matagne, V., Bachaboina, L., Yadav, S., Ojeda, S.R. and Samulski, R.J. (2011) Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol. Ther., 19, 1058-1069.
30. Federici, T., Taub, J.S., Baum, G.R., Gray, S.J., Grieger, J.C., Matthews, K.A., Handy, C.R., Passini, M.A., Samulski, R.J. and Boulis, N.M. (2012) Robust spinal motor neuron transduction following intrathecal delivery of AAV9 in pigs. Gene Ther., 19, 852-859.
31. Samaranch, L., Salegio, E.A., San Sebastian, W., Kells, A.P., Foust, K.D., Bringas, J.R., Lamarre, C., Forsayeth, J., Kaspar, B.K. and Bankiewicz, K.S. (2012) Adeno-associated virus serotype 9 transduction in the central nervous system of nonhuman primates. Hum. Gene Ther., 23, 382-389.
32. Gray, S.J., Nagabhushan Kalburgi, S., McCown, T.J. and Jude Samulski, R. (2013) Global CNS gene delivery and evasion of anti-AAV-neutralizing antibodies by intrathecalAAVadministration in non-human primates. Gene Ther., 20, 465.
33. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., Polchow, C.Y., Alexander, D.D., Caliendo, J., Hentati, A., Kwon, Y.W., Deng, H.-X. et al. (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase. Science, 264, 1772-1775.
34. Baker, H.F. and Ridley, R.M. (1987) Use of common marmoset (Callithrix jacchus) in psychopharmacological research. In Waddington, S. and Joseph, M.H. (eds), Working Methods in Multidisciplinary Psychopharmacology. Manchester University Press, Manchester, pp. 41-73.
35. Annett, L.E., Torres, E.M., Clarke, D.J., Ishida, Y., Barker, R.A., Ridley, R.M., Baker, H.F. and Dunnett, S.B. (1997) Survival of nigral grafts within the striatum of marmosets with 6-OHDA lesions depends critically on donor embryo age. Cell Transplant., 6, 557-569.
36. Kendall, A.L., Rayment, F.D., Torres, E.M., Baker, H.F., Ridley, R.M. and Dunnett, S.B. (1998) Functional integration of striatal allografts in a primate model of Huntington's disease. Nat. Med., 4, 727-729.
37. Besret, L., Kendall, A.L. and Dunnett, S.B. (2000) Aspects of PET imaging relevant to the assessment of striatal transplantation in Huntington's disease. J. Anat., 196, 597-607.
38. Costa, S., Iravani, M.M., Pearce, R.K.B. and Jenner, P. (2001) Glial cell line-derived neurotrophic factor concentration dependently improves disability and motor activity in MPTP-treated common marmosets. Eur. J. Pharmacol., 412, 45-50.
39. Eslamboli, A., Georgievska, B., Ridley, R.M., Baker, H.F., Muzyczka, N., Burger, C., Mandel, R.J., Annett, L. and Kirik, D. (2005) Continuous low-level glial cell line-derived neurotrophic factor delivery using recombinant adeno-associated viral vectors provides neuroprotection and induces behavioral recovery in a primate model of Parkinson's disease. J. Neurosci., 25, 769-777.
40. Maratos, E.C., Jackson, M.J., Pearce, R.K., Cannizzaro, C. and Jenner, P. (2003) Both short- and long-acting D-1/D-2 dopamine agonists induce less dyskinesia than L-DOPA in the MPTP-lesioned common marmoset (Callithrix jacchus). Exp. Neurol., 179, 90-102.
41. Okano, H., Hikishima, K., Iriki, A. and Sasaki, E. (2012) The common marmoset as a novel animal model system for biomedical and neuroscience research applications. Semin. Fetal Neonatal. Med., 17, 336-340.
42. Ilieva, H., Polymenidou, M. and Cleveland, D.W. (2009) Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J. Cell Biol., 187, 761-772.
43. Papadeas, S.T., Kraig, S.E., O'Banion, C., Lepore, A.C. and Maragakis, N.J. (2011) Astrocytes carrying the superoxide dismutase 1 (SOD1G93A) mutation induce wild-type motor neuron degeneration in vivo. Proc. Natl. Acad. Sci. USA, 108, 17803-17808.
44. Nagai, M., Re, D.B., Nagata, T., Chalazonitis, A., Jessell, T.M., Wichterle, H. and Przedborski, S. (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci., 10, 615-622.
45. Di Giorgio, F.P., Carrasco, M.A., Siao, M.C., Maniatis, T. and Eggan, K. (2007) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat. Neurosci., 10, 608-614.
46. Lee, Y., Morrison, B.M., Li, Y., Lengacher, S., Farah, M.H., Hoffman, P.N., Liu, Y., Tsingalia, A., Jin, L., Zhang, P.W. et al. (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature, 487, 443-448.
47. Gray, S.J., Foti, S.B., Schwartz, J.W., Bachaboina, L., Taylor-Blake, B., Coleman, J., Ehlers, M.D., Zylka, M.J., McCown, T.J. and Samulski, R.J. (2011) Optimizing promoters for recombinant adeno-associated virus-mediated gene expression in the peripheral and central nervous system using self-complementary vectors. Hum. Gene Ther., 22, 1143-1153.
48. Gao, G., Vandenberghe, L.H. and Wilson, J.M. (2005) New recombinant serotypes of AAV vectors. Curr. Gene Ther., 5, 285-297.
49. Shen, S., Bryant, K.D., Brown, S.M., Randell, S.H. and Asokan, A. (2011) Terminal N-linked galactose is the primary receptor for adeno-associated virus 9. J. Biol. Chem., 286, 13532-13540.
50. Akache, B., Grimm, D., Pandey, K., Yant, S.R., Xu, H. and Kay, M.A. (2006) The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J. Virol., 80, 9831-9836.
51. Iliff, J.J., Wang, M., Liao, Y., Plogg, B.A., Peng, W., Gundersen, G.A., Benveniste, H., Vates, G.E., Deane, R., Goldman, S.A. et al. (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci. Transl. Med., 4, 147ra111.
52. Yang, C., Qiu, L. and Xu, Z. (2011) Specific gene silencing using RNAi in cell culture. Methods Mol. Biol., 793, 457-477.
53. Gao, G., Lu, Y., Calcedo, R., Grant, R.L., Bell, P., Wang, L., Figueredo, J., Lock, M. and Wilson, J.M. (2006) Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates. Mol. Ther., 13, 77-87.