Rod Outer Segment Development Influences AAV-Mediated Photoreceptor Transduction After Subretinal Injection
Open accessAbstract
Vectors based on the adeno-associated virus (AAV) are currently the preferred tools for delivering genes to photoreceptors (PR) in small and large animals. AAVs have been applied successfully in various models of PR dystrophies. However, unknown barriers still limit AAV's efficient application in several forms of severe PR degenerations due to insufficient transgene expression and/or treated cells at the time of injection. Optimizations of PR gene therapy strategies will likely benefit from the identification of the cellular factors that influence PR transduction. Interestingly, recent studies have shown that the AAV transduction profile of PRs differs significantly between neonatal and adult mouse retinas after subretinal injection. This phenomenon may provide clues to identify host factors that influence the efficiency of AAV-mediated PR transduction. This study demonstrates that rod outer segments are critical modulators of efficient AAV-mediated rod transduction. During retinal development, rod transduction correlated temporally and spatially with the differentiation order of PRs when vectors were introduced subretinally but not when introduced intravitreally. All subretinally injected vectors had an initial preference to transduce cones in the absence of formed rod outer segments and then displayed a preference for rods as the cells matured, independently of the expression cassette or AAV serotype. Consistent with this observation, altered development of rod outer segments was associated with a strong reduction of rod transduction and an increase in the percentage of transduced cones by 2- to 2.8-fold. A similar increase of cone transduction was observed in the adult retinal degeneration 1 ( rd1 ) retina compared to wild-type mice. These results suggest that the loss of rod outer segments in diseased retinas could markedly affect gene transfer efficiency of AAV vectors by limiting the ability of AAVs to infect dying rods efficiently. This information could be exploited for the development of more efficient AAV-based PR gene delivery procedures.
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Access to and quality of donor human fetal material limits the application for many researchers.
“However, the access to and quality of the donor human fetal material limits the application for many researchers [62,299,300].”
From Recombinant Adeno-Associated Viral Vectors (rAAV)-Vector Elements in Ocular Gene Therapy Clinical Trials and Transgene Expression and Bioactivity Assays (2020) · cites this paper as [299]
The Materials and Methods passages describe mouse retinal explants and other experimental materials, while the Discussion addresses factors affecting photoreceptor transduction. Neither addresses access to or quality of donor human fetal material (searched: human fetal material, donor access and quality, fetal human retina). (LLM, conf=0.74)
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Sun, X., Pawlyk, B. S., Xu, X., Liu, X., Bulgakov, O. V., Adamian, M., Sandberg, M. A., Khani, S. C., Tan, M.-H., Smith, A. J., et al. (2009) · Gene Therapy · doi:10.1038/gt.2009.104 · Cited by 123 · see citing works
RetractedSafety and Efficacy of Gene Transfer for Leber's Congenital Amaurosis
Maguire, A. M., Simonelli, F., Pierce, E. A., Pugh, E. N., Mingozzi, F., Bennicelli, J., Banfi, S., Marshall, K. A., Testa, F., Surace, E. M., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0802315 · Cited by 2,145 · see citing works
Effect of gene therapy on visual function in Leber’s congenital amaurosis
Bainbridge, J. W. B., Smith, A. J., Barker, S. S., Robbie, S., Henderson, R., Balaggan, K., Viswanathan, A., Holder, G. E., Stockman, A., Tyler, N., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0802268 · Cited by 1,924 · see citing works
A common progenitor for neurons and glia persists in rat retina late in development
Turner, D. L., & Cepko, C. L. (1987) · Nature · doi:10.1038/328131a0 · Cited by 1,430 · see citing works
Hauswirth, W. W., Aleman, T. S., Kaushal, S., Cideciyan, A. V., Schwartz, S. B., Wang, L., Conlon, T. J., Boye, S. L., Flotte, T. R., Byrne, B. J., et al. (2008) · Human Gene Therapy · doi:10.1089/hum.2008.107 · Cited by 954 · see citing works
MacLaren, R. E., Groppe, M., Barnard, A. R., Cottriall, C. L., Tolmachova, T., Seymour, L., Clark, K. R., During, M. J., Cremers, F. P. M., Black, G. C. M., et al. (2014) · The Lancet · doi:10.1016/s0140-6736(13)62117-0 · Cited by 796 · see citing works
Long-Term Effect of Gene Therapy on Leber’s Congenital Amaurosis
Bainbridge, J. W. B., Mehat, M. S., Sundaram, V., Robbie, S. J., Barker, S. E., Ripamonti, C., Georgiadis, A., Mowat, F. M., Beattie, S. G., Gardner, P. J., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1414221 · Cited by 743 · see citing works
Production and characterization of adeno-associated viral vectors
Grieger, J. C., Choi, V. W., & Samulski, R. J. (2006) · Nature Protocols · doi:10.1038/nprot.2006.207 · Cited by 567 · see citing works
Transcriptional regulation of photoreceptor development and homeostasis in the mammalian retina
Swaroop, A., Kim, D., & Forrest, D. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2880 · Cited by 560 · see citing works
Retinopathy induced in mice by targeted disruption of the rhodopsin gene
Humphries, M. M., Rancourt, D., Farrar, G. J., Kenna, P., Hazel, M., Bush, R. A., Sieving, P. A., Sheils, D. M., Creighton, P., Erven, A., et al. (1997) · Nature Genetics · doi:10.1038/ng0297-216 · Cited by 529 · see citing works
Stimulation of the insulin/mTOR pathway delays cone death in a mouse model of retinitis pigmentosa
Punzo, C., Kornacker, K., & Cepko, C. L. (2008) · Nature Neuroscience · doi:10.1038/nn.2234 · Cited by 515 · see citing works
Self-citationGargini, C., Tozzini, E. T., Mazzoni, F., & Strettoi, E. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21144 · Cited by 496 · see citing works
Bennett, J., Wellman, J., Marshall, K. A., McCague, S., Ashtari, M., DiStefano-Pappas, J., Elci, O. U., Chung, D. C., Sun, J., Wright, J. F., et al. (2016) · The Lancet · doi:10.1016/s0140-6736(16)30371-3 · Cited by 461 · see citing works
Cideciyan, A. V., Jacobson, S. G., Beltran, W. A., Sumaroka, A., Świder, M., Iwabe, S., Román, A. J., Olivares, M. B., Schwartz, S., Komáromy, A. M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218933110 · Cited by 441 · see citing works
AAV2 Gene Therapy Readministration in Three Adults with Congenital Blindness
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) · Science Translational Medicine · doi:10.1126/scitranslmed.3002865 · Cited by 395 · see citing works
Morphological, physiological, and biochemical changes in rhodopsin knockout mice
Lem, J., Krasnoperova, N. V., Calvert, P. D., Kosaras, B., Cameron, D. A., Nicolò, M., Makino, C. L., & Sidman, R. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.2.736 · Cited by 395 · see citing works
Auricchio, A. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.26.3075 · Cited by 394 · see citing works
Intrinsically different retinal progenitor cells produce specific types of progeny
Cepko, C. L. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3767 · Cited by 388 · see citing works
Improvement and Decline in Vision with Gene Therapy in Childhood Blindness
Jacobson, S. G., Cideciyan, A. V., Román, A. J., Sumaroka, A., Schwartz, S., Héon, E., & Hauswirth, W. W. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1412965 · Cited by 370 · see citing works
Ali, R. R., Sarra, G., Stephens, C., de Alwis, M., Bainbridge, J. W., Munro, P., Fauser, S., Reichel, M. B., Kinnon, C., Hunt, D. M., et al. (2000) · Nature Genetics · doi:10.1038/77068 · Cited by 302 · see citing works
NRF2 promotes neuronal survival in neurodegeneration and acute nerve damage
Xiong, W., Garfinkel, A. M., Li, Y., Benowitz, L. I., & Cepko, C. L. (2015) · Journal of Clinical Investigation · doi:10.1172/jci79735 · Cited by 284 · see citing works
Ayuso, E., Mingozzi, F., Montané, J., León, X., Anguela, X. M., Haurigot, V., Edmonson, S. A., Africa, L. M., Zhou, S., High, K. A., et al. (2009) · Gene Therapy · doi:10.1038/gt.2009.157 · Cited by 279 · see citing works
Novel adeno-associated virus serotypes efficiently transduce murine photoreceptors
Allocca, M., Mussolino, C., Garcia-Hoyos, M., Sanges, D., Iodice, C., Petrillo, M., Vandenberghe, L. H., Wilson, J. M., Marigo, V., Surace, E. M., et al. (2007) · Journal of Virology · doi:10.1128/jvi.01327-07 · Cited by 246 · see citing works
Ghazi, N. G., Abboud, E. B., Nowilaty, S. R., Alkuraya, H., Alhommadi, A., Cai, H., Hou, R., Deng, W.-T., Boye, S. L., Almaghamsi, A., et al. (2016) · Human Genetics · doi:10.1007/s00439-016-1637-y · Cited by 243 · see citing works
Bennett, J., Maguire, A. M., Cideciyan, A. V., Schnell, M. A., Glover, E., Anand, V., Alemán, T. S., Chirmule, N. B., Gupta, A. R., Huang, Y., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9920 · Cited by 242 · see citing works
Self-citationDosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey
Vandenberghe, L. H., Bell, P., Maguire, A. M., Cearley, C. N., Xiao, R., Calcedo, R., Wang, L., Castle, M. J., Maguire, A. C., Grant, R., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3002103 · Cited by 242 · see citing works
Weleber, R. G., Pennesi, M. E., Wilson, D. J., Kaushal, S., Erker, L. R., Jensen, L., McBride, M. T., Flotte, T. R., Humphries, M., Calcedo, R., et al. (2016) · Ophthalmology · doi:10.1016/j.ophtha.2016.03.003 · Cited by 218 · see citing works
Visual Acuity after Retinal Gene Therapy for Choroideremia
Edwards, T. L., Jolly, J. K., Groppe, M., Barnard, A. R., Cottriall, C. L., Tolmachova, T., Black, G. C., Webster, A. R., Lotery, A. J., Holder, G. E., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmc1509501 · Cited by 195 · see citing works
Ramamurthy, V., Niemi, G. A., Reh, T. A., & Hurley, J. B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404197101 · Cited by 180 · see citing works
C57BL/6J Mice With inherited Retinal Degeneration
LaVail, M. M., & Sidman, R. L. (1974) · Archives of Ophthalmology · doi:10.1001/archopht.1974.03900060406015 · Cited by 172 · see citing works
Liang, F.-Q., Dejneka, N. S., Cohen, D. R., Krasnoperova, N. V., Lem, J., Maguire, A. M., Dudus, L., Fisher, K. J., & Bennett, J. (2001) · Molecular Therapy · doi:10.1006/mthe.2000.0252 · Cited by 167 · see citing works
West, E. L., Pearson, R. A., Tschernutter, M., Sowden, J. C., MacLaren, R. E., & Ali, R. R. (2008) · Experimental Eye Research · doi:10.1016/j.exer.2008.01.004 · Cited by 163 · see citing works
Epigenomic landscapes of retinal rods and cones
Mo, A., Luo, C., Davis, F. P., Mukamel, E. A., Henry, G. L., Nery, J. R., Urich, M. A., Picard, S., Lister, R., Eddy, S. R., et al. (2016) · eLife · doi:10.7554/elife.11613 · Cited by 158 · see citing works
Hafler, B. P., Surzenko, N., Beier, K. T., Punzo, C., Trimarchi, J. M., Kong, J. H., & Cepko, C. L. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1203138109 · Cited by 154 · see citing works
Self-citationTwo Phases of Rod Photoreceptor Differentiation during Rat Retinal Development
Morrow, E. M., Belliveau, M. J., & Cepko, C. L. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-10-03738.1998 · Cited by 151 · see citing works
Pang, J., Dai, X., Boye, S. L., Barone, I., Boye, S. L., Mao, S., Everhart, D., Dinculescu, A., Liu, L., Umino, Y., et al. (2010) · Molecular Therapy · doi:10.1038/mt.2010.273 · Cited by 148 · see citing works
Versatility of AAV vectors for retinal gene transfer
Surace, E. M., & Auricchio, A. (2007) · Vision Research · doi:10.1016/j.visres.2007.07.027 · Cited by 145 · see citing works
Zonulae adherentes pore size in the external limiting membrane of the rabbit retina.
Milam, A. H., Saari, J. C., Klock, I. B., & Garwin, G. G. (1985) · PubMed · Cited by 142 · see citing works
Natkunarajah, M., Trittibach, P., McIntosh, J., Duran, Y., Barker, S. E., Smith, A. J., Nathwani, A. C., & Ali, R. R. (2008) · Gene Therapy · doi:10.1038/sj.gt.3303074 · Cited by 138 · see citing works
Pang, J., Boye, S. L., Kumar, A., Dinculescu, A., Deng, W., Li, J., Li, Q., Rani, A., Foster, T. C., Chang, B., et al. (2008) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.07-1622 · Cited by 137 · see citing works
Photoreceptor degeneration and synaptogenesis in retinal‐degenerative (rd) mice
Blanks, J. C., Adinolfi, A. M., & Lolley, R. N. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901560108 · Cited by 136 · see citing works
Novel adeno-associated viral vectors for retinal gene therapy.
Vandenberghe, L. H., & Auricchio, A. (2012) · Gene Therapy · doi:10.1038/gt.2011.151 · Cited by 131 · see citing works
Sarra, G. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.21.2353 · Cited by 127 · see citing works
Pawlyk, B. S., Smith, A. J., Buch, P. K., Adamian, M., Hong, D.-H., Sandberg, M. A., Ali, R. R., & Li, T. (2005) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.05-0371 · Cited by 126 · see citing works
Evaluation of the rhodopsin knockout mouse as a model of pure cone function.
Jaissle, G. B., May, C. A., Reinhard, J., Köhler, K., Fauser, S., Lütjen-Drecoll, E., Zrenner, E., & Seeliger, M. W. (2001) · PubMed · Cited by 120 · see citing works
Boye, S. E., Alexander, J. J., Boye, S. L., Witherspoon, C. D., Sandefer, K. J., Conlon, T. J., Erger, K., Sun, J., Ryals, R., Chiodo, V. A., et al. (2012) · Human Gene Therapy · doi:10.1089/hum.2012.125 · Cited by 117 · see citing works
Johnson, J. S., Li, C., DiPrimio, N., Weinberg, M. S., McCown, T. J., & Samulski, R. J. (2010) · Journal of Virology · doi:10.1128/jvi.00687-10 · Cited by 105 · see citing works
AAV-mediated photoreceptor transduction of the pig cone-enriched retina
Mussolino, C., della Corte, M., Rossi, S., Viola, F., Di Vicino, U., Marrocco, E., Neglia, S., Doria, M., Testa, F., Giovannoni, R., et al. (2011) · Gene Therapy · doi:10.1038/gt.2011.3 · Cited by 102 · see citing works
Targeted expression of Cre recombinase to cone photoreceptors in transgenic mice.
Le, Y.-Z., Ash, J. D., Al‐Ubaidi, M. R., Chen, Y., Ma, J.-X., & Anderson, R. E. (2004) · PubMed · Cited by 101 · see citing works
Pang, J.-J., Lauramore, A., Deng, W.-T., Li, Q., Doyle, T. J., Chiodo, V., Li, J., & Hauswirth, W. W. (2008) · Vision Research · doi:10.1016/j.visres.2007.08.009 · Cited by 97 · see citing works
AAV9 targets cone photoreceptors in the nonhuman primate retina
Vandenberghe, L. H., Bell, P., Maguire, A. M., Xiao, R., Hopkins, T. B., Grant, R., Bennett, J., & Wilson, J. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053463 · Cited by 97 · see citing works
Beltran, W. A., Boye, S. L., Boye, S. E., Chiodo, V. A., Lewin, A. S., Hauswirth, W. W., & Aguirre, G. D. (2010) · Gene Therapy · doi:10.1038/gt.2010.56 · Cited by 96 · see citing works
Koch, S., Sothilingam, V., Garrido, M. G., Tanimoto, N., Bećirović, E., Koch, F., Seide, C., Beck, S. C., Seeliger, M. W., Biel, M., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds290 · Cited by 96 · see citing works
Beltran, W. A., Cideciyan, A. V., Iwabe, S., Świder, M., Kosyk, M. S., McDaid, K. S., Martynyuk, I., Ying, G., Shaffer, J., Deng, W., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1509914112 · Cited by 90 · see citing works
Halting progressive neurodegeneration in advanced retinitis pigmentosa
Koch, S., Tsai, Y.-T., Duong, J., Wu, W.-H., Hsu, C., Wu, W., Bonet‐Ponce, L., Lin, C., & Tsang, S. H. (2015) · Journal of Clinical Investigation · doi:10.1172/jci82462 · Cited by 85 · see citing works
Cone-Specific Promoters for Gene Therapy of Achromatopsia and Other Retinal Diseases
Ye, G., Budzynski, E., Sonnentag, P. J., Nork, T. M., Sheibani, N., Gürel, Z., Boye, S. L., Peterson, J. J., Boye, S. L., Hauswirth, W. W., et al. (2015) · Human Gene Therapy · doi:10.1089/hum.2015.130 · Cited by 85 · see citing works
Degenerations of the Dog Retina : II. Generalized Progressive Atrophy of Hereditary Origin
Parry, H. B. (1953) · British Journal of Ophthalmology · doi:10.1136/bjo.37.8.487 · Cited by 84 · see citing works
Advances in gene therapy for diseases of the eye
Petit, L., Khanna, H., & Punzo, C. (2016) · Human Gene Therapy · doi:10.1089/hum.2016.040 · Cited by 82 · see citing works
Self-citationRod-Cone Dysplasia (Progressive Retinal Atrophy) in Irish Setters
Aguirre, G. K., & Rubin, L. F. (1975) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.1975.166.02.157 · Cited by 79 · see citing works
Stieger, K., Colle, M.-A., Dubreil, L., Mendes-Madeira, A., Weber, M., Meur, G. L., Deschamps, J. Y., Provost, N., Nivard, D., Chérel, Y., et al. (2008) · Molecular Therapy · doi:10.1038/mt.2008.41 · Cited by 75 · see citing works
Successful Gene Therapy in the RPGRIP1-deficient Dog: a Large Model of Cone–Rod Dystrophy
Lhériteau, E., Petit, L., Weber, M., Meur, G. L., Deschamps, J., Libeau, L., Mendes-Madeira, A., Guihal, C., François, A., Guyon, R., et al. (2013) · Molecular Therapy · doi:10.1038/mt.2013.232 · Cited by 71 · see citing works
Self-citationNew mouse models for recessive retinitis pigmentosa caused by mutations in the Pde6a gene
Sakamoto, K., McCluskey, M. P., Wensel, T. G., Naggert, J. Κ., & Nishina, P. M. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn327 · Cited by 70 · see citing works
RPGRIP1 is essential for normal rod photoreceptor outer segment elaboration and morphogenesis
Won, J., Gifford, E. J., Smith, R. S., Yi, H., Ferreira, P. A., Hicks, W. L., Li, T., Naggert, J. Κ., & Nishina, P. M. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp385 · Cited by 66 · see citing works
Hereditary Degeneration of the Mouse Retina
Tansley, K. (1951) · British Journal of Ophthalmology · doi:10.1136/bjo.35.10.573 · Cited by 66 · see citing works
Restoration of Vision in the pde6β-deficient Dog, a Large Animal Model of Rod-cone Dystrophy
Petit, L., Lhériteau, E., Weber, M., Meur, G. L., Deschamps, J., Provost, N., Mendes-Madeira, A., Libeau, L., Guihal, C., Colle, M.-A., et al. (2012) · Molecular Therapy · doi:10.1038/mt.2012.134 · Cited by 65 · see citing works
Self-citationTargeting gene expression to cones with human cone opsin promoters in recombinant AAV
Komáromy, A. M., Alexander, J. J., Cooper, A. E., Chiodo, V. A., Acland, G. M., Hauswirth, W. W., & Aguirre, G. K. (2008) · Gene Therapy · doi:10.1038/gt.2008.32 · Cited by 64 · see citing works
Tuntivanich, N., Pittler, S. J., Fischer, A. J., Omar, G., Kiupel, M., Weber, A. J., Yao, S., Steibel, J. P., Khan, N. W., & Petersen‐Jones, S. M. (2009) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.08-2562 · Cited by 60 · see citing works
Fei, Y. (2003) · PubMed · Cited by 60 · see citing works
Watanabe, S., Sanuki, R., Ueno, S., Koyasu, T., Hasegawa, T., & Furukawa, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054146 · Cited by 59 · see citing works
Palfi, A., Millington‐Ward, S., Chadderton, N., O’Reilly, M., Goldmann, T., Humphries, M. M., Li, T., Uwe Wolfrum, B., Humphries, P., Kenna, P. F., et al. (2009) · Human Gene Therapy · doi:10.1089/hum.2009.119 · Cited by 56 · see citing works
Gene therapy provides long-term visual function in a pre-clinical model of retinitis pigmentosa
Wert, K. J., Davis, R. J., Sancho-Pellúz, J., Nishina, P. M., & Tsang, S. H. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds466 · Cited by 56 · see citing works
Surace, E. M., Auricchio, A., Reich, S. J., Rex, T., Glover, E., Pineles, S., Tang, W., O'Connor, E., Lyubarsky, A., Savchenko, A., et al. (2003) · Journal of Virology · doi:10.1128/jvi.77.14.7957-7963.2003 · Cited by 46 · see citing works
Ku, C. A., Chiodo, V. A., Boye, S. L., Goldberg, A. F. X., Li, T., Hauswirth, W. W., & Ramamurthy, V. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr391 · Cited by 46 · see citing works
Combined Rod and Cone Transduction by Adeno-Associated Virus 2/8
Manfredi, A., Marrocco, E., Puppo, A., Cesi, G., Sommella, A., Corte, M. D., Rossi, S., Giunti, M., Craft, C. M., Bacci, M. L., et al. (2013) · Human Gene Therapy · doi:10.1089/hum.2013.154 · Cited by 43 · see citing works
New Rods Move before Differentiating in Adult Teleost Retina
Mack, A. F., & Fernald, R. D. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1202 · Cited by 43 · see citing works
Boye, S. L., Peterson, J. J., Choudhury, S., Min, S. H., Ruan, Q., McCullough, K. T., 张忠红, Olshevskaya, E. V., Peshenko, I. V., Hauswirth, W. W., et al. (2015) · Human Gene Therapy · doi:10.1089/hum.2015.053 · Cited by 41 · see citing works
Wert, K. J., Sancho-Pellúz, J., & Tsang, S. H. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt452 · Cited by 37 · see citing works
Retinal Gene Delivery by rAAV and DNA Electroporation
Venkatesh, A., Ma, S., Langellotto, F., Gao, G., & Punzo, C. (2013) · Current Protocols in Microbiology · doi:10.1002/9780471729259.mc14d04s28 · Cited by 35 · see citing works
Self-citationBeltran, W. A., Acland, G. M., & Aguirre, G. K. (2009) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.08-3364 · Cited by 35 · see citing works
Retinal Degeneration Progression Changes Lentiviral Vector Cell Targeting in the Retina
Calame, M., Cachafeiro, M. C. B., Philippe, S., Schouwey, K., Tekaya, M., Wanner, D., Sarkis, C., Kostic, C., & Arsenijévic, Y. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023782 · Cited by 29 · see citing works
Bruewer, A. R., Mowat, F. M., Bartoe, J. T., Boye, S. L., Hauswirth, W. W., & Petersen‐Jones, S. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060218 · Cited by 29 · see citing works
Comparison of photoreceptor-specific matrix domains in the cat and monkey retinas
Fariss, R. N., Anderson, D. H., & Fisher, S. K. (1990) · Experimental Eye Research · doi:10.1016/0014-4835(90)90160-v · Cited by 28 · see citing works
Ultrasound‐guided in utero injections allow studies of the development and function of the eye
Punzo, C., & Cepko, C. L. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21500 · Cited by 27 · see citing works
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Yao, J., Jia, L., Khan, N. W., Zheng, Q.-D., Moncrief, A., Hauswirth, W. W., Thompson, D. A., & Zacks, D. N. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037197 · Cited by 21 · see citing works
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Minella, A., Mowat, F. M., Willett, K. L., Sledge, D. G., Bartoe, J. T., Bennett, J., & Petersen‐Jones, S. M. (2014) · Gene Therapy · doi:10.1038/gt.2014.65 · Cited by 9 · see citing works
Xiong, W., & Cepko, C. (2016) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-319-17121-0_67 · Cited by 9 · see citing works
Henderson, R. G., & Fernald, R. D. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2004.04.001 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
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Ludwig, P. E., Freeman, S. C., & Janot, A. C. (2019) · International Journal of Retina and Vitreous · doi:10.1186/s40942-019-0158-y · Cited by 41 · see citing works
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Self-citationTao, Y., Yang, Z. L., Wei, F., Ma, Z., Huang, Y. F., & Li, Z. (2017) · Therapeutics and Clinical Risk Management · doi:10.2147/tcrm.s144822 · Cited by 6 · see citing works
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AAV-mediated transduction of songbird retina
Seth, P. K., Heyers, D., Satish, B., Mendoza, E., Haase, K., Borowsky, L., Musielak, I., Koch, K., Feederle, R., Scharff, C., et al. (2025) · Frontiers in Physiology · doi:10.3389/fphys.2025.1549585 · Cited by 1 · see citing works
Rajala, R. V. S. (2019) · PubMed · Cited by 1 · see citing works
Punzo, C. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816222-4.00019-8 · Cited by 1 · see citing works
Self-citationTran, S., Trinquier, J., Meter, T. V., Zin, E. A., Nanteau, C., Riancho, L., Potey, A., Slembrouck-Brec, A., Delmas, M., Ferrari, U., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.05.730342
- Authors
- Petit, L., Ma, S., Cheng, S.-Y., Gao, G., & Punzo, C.
- Affiliations
- University of Massachusetts Chan Medical School (US)
- Corresponding author
- Punzo, Claudio
- Venue
- Human Gene Therapy
- Publisher
- SAGE Publications
- Published
- 2017-06
- Volume
- 28
- Issue
- 6
- Pages
- 464-481
- ISSN
- 1043-0342 (ISSN-L)
- 1557-7422
- PMC
- PMC5488363
- OpenAlex
- W2616731639
- Cited by
- 24
- References
- 90
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 3 · 2022: 1 · 2021: 4 · 2020: 3 · 2019: 4 · 2018: 2 · 2017: 3
- FWCI
- 1.34
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Human Gene Therapy (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship@UMassChan (submittedVersion, cc-by)
- Funders
- University of Massachusetts
- Fondation de France
- National Institutes of Health
- University of Massachusetts Medical School
- National Heart, Lung, and Blood Institute (P01HL131471)
- National Eye Institute (R21EY030166, R01EY023570)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Keywords
- adeno-associated virus vectors, phototransduction, rod outer segments, subretinal injection, retinal development, rod photoreceptors, cone photoreceptors, rd1 mouse, AAV serotypes, intravitreal injection, photoreceptor degeneration
- MeSH terms
- Dependovirus, Animals, Cell Differentiation, Cricetulus, Cytomegalovirus, Disease Models, Animal, Genetic Engineering, Genetic Vectors, Mice, Transgenic, Organ Specificity, Promoter Regions, Genetic, Retinal Degeneration, Rod Cell Outer Segment, Transduction, Genetic, CHO Cells, Genes, Reporter, Retinal Cone Photoreceptor Cells, Green Fluorescent Proteins, Mice, Injections, Intraocular, Intravitreal Injections
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