Rescue of Hearing by Gene Delivery to Inner-Ear Hair Cells Using Exosome-Associated AAV

Molecular Therapy

Volumn 25, Issue 2, 2017, Pages 379-391

  György, Bence ^a   Sage, Cyrille ^a   Indzhykulian, Artur A ^a   Scheffer, Deborah I ^a   Brisson, Alain R ^b   Tan, Sisareuth ^b   Wu, Xudong ^a   Volak, Adrienn ^a   Mu, Dakai ^a   Tamvakologos, Panos I ^a   Li, Yaqiao ^a   Fitzpatrick, Zachary ^a   Ericsson, Maria ^a   Breakefield, Xandra O ^a   Corey, David P ^a   Maguire, Casey A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

adeno associated virus vector; balance; cochlea; exosomes; gene therapy; hair cell; hearing; inner ear; LHFPL5; TMHS

Indexed keywords

EXOSOME ASSOCIATED ADENO ASSOCIATED VIRUS VECTOR; GREEN FLUORESCENT PROTEIN; LIPOMA HMGIC FUSION PARTNER LIKE 5; TETRASPANIN; UNCLASSIFIED DRUG; VIRUS VECTOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COCHLEA EXPLANT; CONGENITAL DEAFNESS; CONTROLLED STUDY; DRUG SAFETY; EVOKED BRAIN STEM AUDITORY RESPONSE; EXPLANT; FEMALE; GENETIC TRANSDUCTION; HEARING TEST; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INNER HAIR CELL; MALE; MECHANOTRANSDUCTION; MOUSE; MOUSE MODEL; NONHUMAN; OPEN FIELD TEST; OUTER HAIR CELL; STARTLE REFLEX; TRANSGENE; VESTIBULAR FUNCTION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ADMINISTRATION AND DOSAGE; ANIMAL; CELL CULTURE; CLASSIFICATION; DEPENDOPARVOVIRUS; EXOSOME; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; HEARING; KNOCKOUT MOUSE; METABOLISM; PHENOTYPE; REPORTER GENE;

ANIMALS; CELLS, CULTURED; DEPENDOVIRUS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; EXOSOMES; FEMALE; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENES, REPORTER; GENETIC THERAPY; GENETIC VECTORS; HAIR CELLS, AUDITORY, INNER; HEARING; MALE; MICE; MICE, KNOCKOUT; PHENOTYPE; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 85016287110     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1016/j.ymthe.2016.12.010     Document Type: Article

References (28)

1. 1 Lin, F.R., Niparko, J.K., Ferrucci, L., Hearing loss prevalence in the United States. Arch. Intern. Med. 171 (2011), 1851–1852.
2. 2 Alzheimer's Association. 2016 Alzheimer's disease facts and figures. Alzheimers Dement. 12 (2016), 459–509.
3. 3 Mason, J.A., Herrmann, K.R., Universal infant hearing screening by automated auditory brainstem response measurement. Pediatrics 101 (1998), 221–228.
4. 4 Géléoc, G.S., Holt, J.R., Sound strategies for hearing restoration. Science, 344, 2014, 1241062.
5. 5 Wise, A.K., Tu, T., Atkinson, P.J., Flynn, B.O., Sgro, B.E., Hume, C., O'Leary, S.J., Shepherd, R.K., Richardson, R.T., The effect of deafness duration on neurotrophin gene therapy for spiral ganglion neuron protection. Hear. Res. 278 (2011), 69–76.
6. 6 Kawamoto, K., Sha, S.H., Minoda, R., Izumikawa, M., Kuriyama, H., Schacht, J., Raphael, Y., Antioxidant gene therapy can protect hearing and hair cells from ototoxicity. Mol. Ther. 9 (2004), 173–181.
7. 7 Kawamoto, K., Yagi, M., Stöver, T., Kanzaki, S., Raphael, Y., Hearing and hair cells are protected by adenoviral gene therapy with TGF-beta1 and GDNF. Mol. Ther. 7 (2003), 484–492.
8. 8 Li, W., Wu, J., Yang, J., Sun, S., Chai, R., Chen, Z.Y., Li, H., Notch inhibition induces mitotically generated hair cells in mammalian cochleae via activating the Wnt pathway. Proc. Natl. Acad. Sci. USA 112 (2015), 166–171.
9. 9 Liberman, M.C., Gao, J., He, D.Z., Wu, X., Jia, S., Zuo, J., Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419 (2002), 300–304.
10. 10 Kohrman, D.C., Raphael, Y., Gene therapy for deafness. Gene Ther. 20 (2013), 1119–1123.
11. 11 Sacheli, R., Delacroix, L., Vandenackerveken, P., Nguyen, L., Malgrange, B., Gene transfer in inner ear cells: a challenging race. Gene Ther. 20 (2013), 237–247.
12. 12 Akil, O., Seal, R.P., Burke, K., Wang, C., Alemi, A., During, M., Edwards, R.H., Lustig, L.R., Restoration of hearing in the VGLUT3 knockout mouse using virally mediated gene therapy. Neuron 75 (2012), 283–293.
13. 13 Askew, C., Rochat, C., Pan, B., Asai, Y., Ahmed, H., Child, E., Schneider, B.L., Aebischer, P., Holt, J.R., Tmc gene therapy restores auditory function in deaf mice. Sci. Transl. Med., 7, 2015, 295ra108.
14. 14 Fitzpatrick, Z., György, B., Skog, J., Maguire, C.A., Extracellular vesicles as enhancers of virus vector-mediated gene delivery. Hum. Gene Ther. 25 (2014), 785–786.
15. 15 György, B., Hung, M.E., Breakefield, X.O., Leonard, J.N., Therapeutic applications of extracellular vesicles: clinical promise and open questions. Annu. Rev. Pharmacol. Toxicol. 55 (2015), 439–464.
16. 16 György, B., Fitzpatrick, Z., Crommentuijn, M.H., Mu, D., Maguire, C.A., Naturally enveloped AAV vectors for shielding neutralizing antibodies and robust gene delivery in vivo. Biomaterials 35 (2014), 7598–7609.
17. 17 Maguire, C.A., Balaj, L., Sivaraman, S., Crommentuijn, M.H., Ericsson, M., Mincheva-Nilsson, L., Baranov, V., Gianni, D., Tannous, B.A., Sena-Esteves, M., et al. Microvesicle-associated AAV vector as a novel gene delivery system. Mol. Ther. 20 (2012), 960–971.
18. 18 Xiong, W., Grillet, N., Elledge, H.M., Wagner, T.F., Zhao, B., Johnson, K.R., Kazmierczak, P., Müller, U., TMHS is an integral component of the mechanotransduction machinery of cochlear hair cells. Cell 151 (2012), 1283–1295.
19. 19 Hudry, E., Martin, C., Gandhi, S., György, B., Scheffer, D.I., Mu, D., Merkel, S.F., Mingozzi, F., Fitzpatrick, Z., Dimant, H., et al. Exosome-associated AAV vector as a robust and convenient neuroscience tool. Gene Ther. 23 (2016), 380–392.
20. 20 Gibson, F., Walsh, J., Mburu, P., Varela, A., Brown, K.A., Antonio, M., Beisel, K.W., Steel, K.P., Brown, S.D., A type VII myosin encoded by the mouse deafness gene shaker-1. Nature 374 (1995), 62–64.
21. 21 Anderson, D.W., Probst, F.J., Belyantseva, I.A., Fridell, R.A., Beyer, L., Martin, D.M., Wu, D., Kachar, B., Friedman, T.B., Raphael, Y., et al. The motor and tail regions of myosin XV are critical for normal structure and function of auditory and vestibular hair cells. Hum. Mol. Genet. 9 (2000), 1729–1738.
22. 22 Di Palma, F., Holme, R.H., Bryda, E.C., Belyantseva, I.A., Pellegrino, R., Kachar, B., Steel, K.P., Noben-Trauth, K., Mutations in Cdh23, encoding a new type of cadherin, cause stereocilia disorganization in waltzer, the mouse model for Usher syndrome type 1D. Nat. Genet. 27 (2001), 103–107.
23. 23 Yu, Q., Wang, Y., Chang, Q., Wang, J., Gong, S., Li, H., Lin, X., Virally expressed connexin26 restores gap junction function in the cochlea of conditional Gjb2 knockout mice. Gene Ther. 21 (2014), 71–80.
24. 24 Longo-Guess, C.M., Gagnon, L.H., Cook, S.A., Wu, J., Zheng, Q.Y., Johnson, K.R., A missense mutation in the previously undescribed gene Tmhs underlies deafness in hurry-scurry (hscy) mice. Proc. Natl. Acad. Sci. USA 102 (2005), 7894–7899.
25. 25 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.
26. 26 Wang, Z., Ma, H.I., Li, J., Sun, L., Zhang, J., Xiao, X., Rapid and highly efficient transduction by double-stranded adeno-associated virus vectors in vitro and in vivo. Gene Ther. 10 (2003), 2105–2111.
27. 27 Xiao, X., Li, J., Samulski, R.J., Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol. 72 (1998), 2224–2232.
28. 28 Rabinowitz, J.E., Rolling, F., Li, C., Conrath, H., Xiao, W., Xiao, X., Samulski, R.J., Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J. Virol. 76 (2002), 791–801.