Development of Intrathecal AAV9 Gene Therapy for Giant Axonal Neuropathy

Molecular Therapy Methods and Clinical Development

Volumn 9, Issue , 2018, Pages 160-171

  Bailey, Rachel M ^a   Armao, Diane ^a   Nagabhushan Kalburgi, Sahana ^a,b   Gray, Steven J ^a,c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

AAV9; adeno associated virus; biodistribution; dorsal root ganglia; fibroblast; gene therapy; giant axonal neuropathy; gigaxonin; intrathecal; sciatic nerve

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; GIGAXONIN; PROTEIN; UNCLASSIFIED DRUG;

ADENO ASSOCIATED VIRUS 9; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; ENHANCER REGION; EXPRESSION VECTOR; GENE REPLACEMENT THERAPY; GENE SEQUENCE; GENETIC TRANSFECTION; GIANT AXONAL NEUROPATHY; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; INTERMEDIATE FILAMENT; LOSS OF FUNCTION MUTATION; MISSENSE MUTATION; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; SCHWANN CELL; SCIATIC NERVE; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; WESTERN BLOTTING;

EID: 85044870981     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1016/j.omtm.2018.02.005     Document Type: Article

References (46)

1. Asbury, A.K., Gale, M.K., Cox, S.C., Baringer, J.R., Berg, B.O., Giant axonal neuropathy—a unique case with segmental neurofilamentous masses. Acta Neuropathol. 20 (1972), 237–247.
2. Berg, B.O., Rosenberg, S.H., Asbury, A.K., Giant axonal neuropathy. Pediatrics 49 (1972), 894–899.
3. Yang, Y., Allen, E., Ding, J., Wang, W., Giant axonal neuropathy. Cell. Mol. Life Sci. 64 (2007), 601–609.
4. Peiffer, J., Schlote, W., Bischoff, A., Boltshauser, E., Müller, G., Generalized giant axonal neuropathy: a filament-forming disease of neuronal, endothelial, glial, and schwann cells in a patient without kinky hair. Acta Neuropathol. 40 (1977), 213–218.
5. Houlden, H., Groves, M., Miedzybrodzka, Z., Roper, H., Willis, T., Winer, J., Cole, G., Reilly, M.M., New mutations, genotype phenotype studies and manifesting carriers in giant axonal neuropathy. J. Neurol. Neurosurg. Psychiatry 78 (2007), 1267–1270.
6. Yiu, E.M., Ryan, M.M., Genetic axonal neuropathies and neuronopathies of pre-natal and infantile onset. J. Peripher. Nerv. Syst. 17 (2012), 285–300.
7. Johnson-Kerner, B.L., Roth, L., Greene, J.P., Wichterle, H., Sproule, D.M., Giant axonal neuropathy: An updated perspective on its pathology and pathogenesis. Muscle Nerve 50 (2014), 467–476.
8. Mahammad, S., Murthy, S.N., Didonna, A., Grin, B., Israeli, E., Perrot, R., Bomont, P., Julien, J.P., Kuczmarski, E., Opal, P., Goldman, R.D., Giant axonal neuropathy-associated gigaxonin mutations impair intermediate filament protein degradation. J. Clin. Invest. 123 (2013), 1964–1975.
9. Igisu, H., Ohta, M., Tabira, T., Hosokawa, S., Goto, I., Giant axonal neuropathy. A clinical entity affecting the central as well as the peripheral nervous system. Neurology 25 (1975), 717–721.
10. Ouvrier, R.A., Giant axonal neuropathy. A review. Brain Dev. 11 (1989), 207–214.
11. Mohri, I., Taniike, M., Yoshikawa, H., Higashiyama, M., Itami, S., Okada, S., A case of giant axonal neuropathy showing focal aggregation and hypophosphorylation of intermediate filaments. Brain Dev. 20 (1998), 594–597.
12. Cleveland, D.W., Yamanaka, K., Bomont, P., Gigaxonin controls vimentin organization through a tubulin chaperone-independent pathway. Hum. Mol. Genet. 18 (2009), 1384–1394.
13. Pena, S.D., Opas, M., Turksen, K., Kalnins, V.I., Carpenter, S., Immunocytochemical studies of intermediate filament aggregates and their relationship to microtubules in cultured skin fibroblasts from patients with giant axonal neuropathy. Eur. J. Cell Biol. 31 (1983), 227–234.
14. Kantor, B., Bailey, R.M., Wimberly, K., Kalburgi, S.N., Gray, S.J., Methods for gene transfer to the central nervous system. Adv. Genet. 87 (2014), 125–197.
15. Hocquemiller, M., Giersch, L., Audrain, M., Parker, S., Cartier, N., Adeno-associated virus-based gene therapy for CNS diseases. Hum. Gene Ther. 27 (2016), 478–496.
16. Murlidharan, G., Samulski, R.J., Asokan, A., Biology of adeno-associated viral vectors in the central nervous system. Front. Mol. Neurosci., 7, 2014, 76.
17. 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., Boulis, N.M., Robust spinal motor neuron transduction following intrathecal delivery of AAV9 in pigs. Gene Ther. 19 (2012), 852–859.
18. Samaranch, L., Salegio, E.A., San Sebastian, W., Kells, A.P., Foust, K.D., Bringas, J.R., Lamarre, C., Forsayeth, J., Kaspar, B.K., Bankiewicz, K.S., Adeno-associated virus serotype 9 transduction in the central nervous system of nonhuman primates. Hum. Gene Ther. 23 (2012), 382–389.
19. Gray, S.J., Nagabhushan Kalburgi, S., McCown, T.J., Jude Samulski, R., Global CNS gene delivery and evasion of anti-AAV-neutralizing antibodies by intrathecal AAV administration in non-human primates. Gene Ther. 20 (2013), 450–459.
20. Passini, M.A., Bu, J., Richards, A.M., Treleaven, C.M., Sullivan, J.A., O'Riordan, C.R., Scaria, A., Kells, A.P., Samaranch, L., San Sebastian, W., et al. Translational fidelity of intrathecal delivery of self-complementary AAV9-survival motor neuron 1 for spinal muscular atrophy. Hum. Gene Ther. 25 (2014), 619–630.
21. Meyer, K., Ferraiuolo, L., Schmelzer, L., Braun, L., McGovern, V., Likhite, S., Michels, O., Govoni, A., Fitzgerald, J., Morales, P., et al. Improving single injection CSF delivery of AAV9-mediated gene therapy for SMA: a dose-response study in mice and nonhuman primates. Mol. Ther. 23 (2015), 477–487.
22. Mussche, S., Devreese, B., Nagabhushan Kalburgi, S., Bachaboina, L., Fox, J.C., Shih, H.J., Van Coster, R., Samulski, R.J., Gray, S.J., Restoration of cytoskeleton homeostasis after gigaxonin gene transfer for giant axonal neuropathy. Hum. Gene Ther. 24 (2013), 209–219.
23. Johnson-Kerner, B.L., Ahmad, F.S., Diaz, A.G., Greene, J.P., Gray, S.J., Samulski, R.J., Chung, W.K., Van Coster, R., Maertens, P., Noggle, S.A., et al. Intermediate filament protein accumulation in motor neurons derived from giant axonal neuropathy iPSCs rescued by restoration of gigaxonin. Hum. Mol. Genet. 24 (2015), 1420–1431.
24. Israeli, E., Dryanovski, D.I., Schumacker, P.T., Chandel, N.S., Singer, J.D., Julien, J.P., Goldman, R.D., Opal, P., Intermediate filament aggregates cause mitochondrial dysmotility and increase energy demands in giant axonal neuropathy. Hum. Mol. Genet. 25 (2016), 2143–2157.
25. Tornøe, J., Kusk, P., Johansen, T.E., Jensen, P.R., Generation of a synthetic mammalian promoter library by modification of sequences spacing transcription factor binding sites. Gene 297 (2002), 21–32.
26. Levitt, N., Briggs, D., Gil, A., Proudfoot, N.J., Definition of an efficient synthetic poly(A) site. Genes Dev. 3 (1989), 1019–1025.
27. McCarty, D.M., Monahan, P.E., Samulski, R.J., Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther. 8 (2001), 1248–1254.
28. McCarty, D.M., Fu, H., Monahan, P.E., Toulson, C.E., Naik, P., Samulski, R.J., Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Ther. 10 (2003), 2112–2118.
29. McCarty, D.M., Self-complementary AAV vectors; advances and applications. Mol. Ther. 16 (2008), 1648–1656.
30. Gray, S.J., Matagne, V., Bachaboina, L., Yadav, S., Ojeda, S.R., Samulski, R.J., Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol. Ther. 19 (2011), 1058–1069.
31. Pena, S.D., Giant axonal neuropathy: intermediate filament aggregates in cultured skin fibroblasts. Neurology 31 (1981), 1470–1473.
32. Bomont, P., Degradation of the intermediate filament family by gigaxonin. Methods Enzymol. 569 (2016), 215–231.
33. Ding, J., Allen, E., Wang, W., Valle, A., Wu, C., Nardine, T., Cui, B., Yi, J., Taylor, A., Jeon, N.L., et al. Gene targeting of GAN in mouse causes a toxic accumulation of microtubule-associated protein 8 and impaired retrograde axonal transport. Hum. Mol. Genet. 15 (2006), 1451–1463.
34. Dequen, F., Bomont, P., Gowing, G., Cleveland, D.W., Julien, J.P., Modest loss of peripheral axons, muscle atrophy and formation of brain inclusions in mice with targeted deletion of gigaxonin exon 1. J. Neurochem. 107 (2008), 253–264.
35. Ganay, T., Boizot, A., Burrer, R., Chauvin, J.P., Bomont, P., Sensory-motor deficits and neurofilament disorganization in gigaxonin-null mice. Mol. Neurodegener., 6, 2011, 25.
36. Hadaczek, P., Eberling, J.L., Pivirotto, P., Bringas, J., Forsayeth, J., Bankiewicz, K.S., Eight years of clinical improvement in MPTP-lesioned primates after gene therapy with AAV2-hAADC. Mol. Ther. 18 (2010), 1458–1461.
37. Samaranch, L., Salegio, E.A., San Sebastian, W., Kells, A.P., Bringas, J.R., Forsayeth, J., Bankiewicz, K.S., Strong cortical and spinal cord transduction after AAV7 and AAV9 delivery into the cerebrospinal fluid of nonhuman primates. Hum. Gene Ther. 24 (2013), 526–532.
38. Sorrentino, N.C., Maffia, V., Strollo, S., Cacace, V., Romagnoli, N., Manfredi, A., Ventrella, D., Dondi, F., Barone, F., Giunti, M., et al. A comprehensive map of CNS transduction by eight recombinant adeno-associated virus serotypes upon cerebrospinal fluid administration in pigs. Mol. Ther. 24 (2016), 276–286.
39. King, R.H.M., The pathology of peripheral nerve diseases. Adv. Clin. Neurosci. Rehabil. 6 (2006), 16–18.
40. Tandan, R., Little, B.W., Emery, E.S., Good, P.S., Pendlebury, W.W., Bradley, W.G., Childhood giant axonal neuropathy. Case report and review of the literature. J. Neurol. Sci. 82 (1987), 205–228.
41. Midroni, G., Bilbao, J.M., Biopsy Diagnosis of Peripheral Neuropathy. 1995, Butterworth-Heinmann, 45–74.
42. Clément, N., Grieger, J.C., Manufacturing of recombinant adeno-associated viral vectors for clinical trials. Mol. Ther. Methods Clin. Dev., 3, 2016, 16002.
43. Gray, S.J., Choi, V.W., Asokan, A., Haberman, R.A., McCown, T.J., Samulski, R.J., Production of recombinant adeno-associated viral vectors and use in in vitro and in vivo administration. Curr. Protoc. Neurosci., 4, 2011 4.17.
44. Karumuthil-Melethil, S., Nagabhushan Kalburgi, S., Thompson, P., Tropak, M., Kaytor, M.D., Keimel, J.G., Mark, B.L., Mahuran, D., Walia, J.S., Gray, S.J., Novel vector design and hexosaminidase variant enabling self-complementary adeno-associated virus for the treatment of Tay-Sachs disease. Hum. Gene Ther. 27 (2016), 509–521.
45. Lawson, S.N., The postnatal development of large light and small dark neurons in mouse dorsal root ganglia: a statistical analysis of cell numbers and size. J. Neurocytol. 8 (1979), 275–294.
46. Karumuthil-Melethil, S., Marshall, M.S., Heindel, C., Jakubauskas, B., Bongarzone, E.R., Gray, S.J., Intrathecal administration of AAV/GALC vectors in 10-11-day-old twitcher mice improves survival and is enhanced by bone marrow transplant. J. Neurosci. Res. 94 (2016), 1138–1151.