Optogenetic approaches to restoring visual function in retinitis pigmentosa

Current Opinion in Neurobiology

Volumn 21, Issue 6, 2011, Pages 942-946

  Busskamp, Volker ^a   Roska, Botond ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHANNELRHODOPSIN 2; PARVOVIRUS VECTOR; RHODOPSIN; UNCLASSIFIED DRUG;

BIOSENSOR; BLINDNESS; CELL ACTIVITY; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL MEMBRANE DEPOLARIZATION; CELL TYPE; CLINICAL EFFECTIVENESS; COLOR VISION; DISEASE COURSE; GENE EXPRESSION; GENE MUTATION; GENE THERAPY; GENETIC DISORDER; HUMAN; NONHUMAN; PATIENT SAFETY; PHOTORECEPTOR; PHOTOSENSITIVITY; PRIORITY JOURNAL; PROMOTER REGION; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA CELL; RETINA CONE; RETINA DEGENERATION; RETINA GANGLION CELL; RETINA ROD; RETINITIS PIGMENTOSA; REVIEW; TARGET CELL; VISUAL CORTEX; VISUAL DISORDER; VISUAL IMPAIRMENT; VISUAL SYSTEM FUNCTION;

ANIMALS; GENE THERAPY; HUMANS; RETINITIS PIGMENTOSA;

EID: 83455187486     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2011.06.001     Document Type: Review

References (44)

1. Hartong D.T., Berson E.L., Dryja T.P. Retinitis pigmentosa. Lancet 2006, 368:1795-1809.
2. Jacobson S.G., Roman A.J., Aleman T.S., Sumaroka A., Herrera W., Windsor E.A., Atkinson L.A., Schwartz S.B., Steinberg J.D., Cideciyan A.V. Normal central retinal function and structure preserved in retinitis pigmentosa. Invest Ophthalmol Vis Sci 2010, 51:1079-1085.
3. Sancho-Pelluz J., Arango-Gonzalez B., Kustermann S., Romero F.J., van Veen T., Zrenner E., Ekstrom P., Paquet-Durand F. Photoreceptor cell death mechanisms in inherited retinal degeneration. Mol Neurobiol 2008, 38:253-269.
4. Li Z.Y., Kljavin I.J., Milam A.H. Rod photoreceptor neurite sprouting in retinitis pigmentosa. J Neurosci 1995, 15:5429-5438.
5. Lin B., Masland R.H., Strettoi E. Remodeling of cone photoreceptor cells after rod degeneration in rd mice. Exp Eye Res 2009, 88:589-599.
6. Allocca M., Doria M., Petrillo M., Colella P., Garcia-Hoyos M., Gibbs D., Kim S.R., Maguire A., Rex T.S., Di Vicino U., et al. Serotype-dependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J Clin Invest 2008, 118:1955-1964.
7. Stieger K., Lorenz B. Gene therapy for vision loss-recent developments. Discov Med 2010, 10:425-433.
8. Baehr W., Frederick J.M. Naturally occurring animal models with outer retina phenotypes. Vis Res 2009, 49:2636-2652.
9. Tomita H., Sugano E., Fukazawa Y., Isago H., Sugiyama Y., Hiroi T., Ishizuka T., Mushiake H., Kato M., Hirabayashi M., et al. Visual properties of transgenic rats harboring the channelrhodopsin-2 gene regulated by the thy-1.2 promoter. PLoS ONE 2009, 4:e7679.
10. Gollisch T., Meister M. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 2010, 65:150-164.
11. Kuffler S.W. Discharge patterns and functional organization of mammalian retina. J Neurophysiol 1953, 16:37-68.
12. Boyden E.S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 2005, 8:1263-1268.
13. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N., Berthold P., Ollig D., Hegemann P., Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A 2003, 100:13940-13945.
14. Deisseroth K. Optogenetics. Nat Methods 2011, 8:26-29.
15. Kleinlogel S., Feldbauer K., Dempski R.E., Fotis H., Wood P.G., Bamann C., Bamberg E. Ultra light-sensitive and fast neuronal activation with the Ca(2+)-permeable channelrhodopsin CatCh. Nat Neurosci 2011, 14:513-518.
16. Chow B.Y., Han X., Dobry A.S., Qian X., Chuong A.S., Li M., Henninger M.A., Belfort G.M., Lin Y., Monahan P.E., et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 2010, 463:98-102.
17. Schobert B., Lanyi J.K. Halorhodopsin is a light-driven chloride pump. J Biol Chem 1982, 257:10306-10313.
18. Zhang F., Wang L.P., Brauner M., Liewald J.F., Kay K., Watzke N., Wood P.G., Bamberg E., Nagel G., Gottschalk A., et al. Multimodal fast optical interrogation of neural circuitry. Nature 2007, 446:633-639.
19. Surace E.M., Auricchio A. Versatility of AAV vectors for retinal gene transfer. Vision Res 2008, 48:353-359.
20. Kwon I., Schaffer D.V. Designer gene delivery vectors: molecular engineering and evolution of adeno-associated viral vectors for enhanced gene transfer. Pharm Res 2008, 25:489-499.
21. Bi A., Cui J., Ma Y.P., Olshevskaya E., Pu M., Dizhoor A.M., Pan Z.H. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 2006, 50:23-33.
22. Lin B., Koizumi A., Tanaka N., Panda S., Masland R.H. Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc Natl Acad Sci U S A 2008, 105:16009-16014.
23. Thyagarajan S., van Wyk M., Lehmann K., Lowel S., Feng G., Wassle H. Visual function in mice with photoreceptor degeneration and transgenic expression of channelrhodopsin 2 in ganglion cells. J Neurosci 2010, 30:8745-8758.
24. Farah N., Reutsky I., Shoham S. Patterned optical activation of retinal ganglion cells. Conf Proc IEEE Eng Med Biol Soc 2007, 2007:6368-6370.
25. Tomita H., Sugano E., Isago H., Hiroi T., Wang Z., Ohta E., Tamai M. Channelrhodopsin-2 gene transduced into retinal ganglion cells restores functional vision in genetically blind rats. Exp Eye Res 2010, 90:429-436.
26. Tomita H., Sugano E., Yawo H., Ishizuka T., Isago H., Narikawa S., Kugler S., Tamai M. Restoration of visual response in aged dystrophic RCS rats using AAV-mediated channelopsin-2 gene transfer. Invest Ophthalmol Vis Sci 2007, 48:3821-3826.
27. Zhang Y., Ivanova E., Bi A., Pan Z.H. Ectopic expression of multiple microbial rhodopsins restores ON and OFF light responses in retinas with photoreceptor degeneration. J Neurosci 2009, 29:9186-9196.
28. Greenberg K.P., Pham A., Werblin F.S. Differential targeting of optical neuromodulators to ganglion cell soma and dendrites allows dynamic control of center-surround antagonism. Neuron 2011, 69:713-720.
29. Yoshida K., Watanabe D., Ishikane H., Tachibana M., Pastan I., Nakanishi S. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 2001, 30:771-780.
30. Molnar A., Hsueh H.A., Roska B., Werblin F.S. Crossover inhibition in the retina: circuitry that compensates for nonlinear rectifying synaptic transmission. J Comput Neurosci 2009, 27:569-590.
31. Lagali P.S., Balya D., Awatramani G.B., Munch T.A., Kim D.S., Busskamp V., Cepko C.L., Roska B. Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat Neurosci 2008, 11:667-675.
32. Matsuda T., Cepko C.L. Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc Natl Acad Sci U S A 2004, 101:16-22.
33. Doroudchi M.M., Greenberg K.P., Liu J., Silka K.A., Boyden E.S., Lockridge J.A., Arman A.C., Janani R., Boye S.E., Boye S.L., et al. Virally delivered channelrhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness. Mol Ther 2011, Apr 19 (Epub ahead of print).
34. Busskamp V., Duebel J., Balya D., Fradot M., Viney T.J., Siegert S., Groner A.C., Cabuy E., Forster V., Seeliger M., et al. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 2010, 329:413-417.
35. Wang Y., Macke J.P., Merbs S.L., Zack D.J., Klaunberg B., Bennett J., Gearhart J., Nathans J. A locus control region adjacent to the human red and green visual pigment genes. Neuron 1992, 9:429-440.
36. Leveillard T., Sahel J.A. Rod-derived cone viability factor for treating blinding diseases: from clinic to redox signaling. Sci Transl Med 2010, 2:26ps16.
37. Punzo C., Kornacker K., Cepko C.L. Stimulation of the insulin/mTOR pathway delays cone death in a mouse model of retinitis pigmentosa. Nat Neurosci 2009, 12:44-52.
38. 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. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 2008, 358:2240-2248.
39. Ivanova E., Hwang G.S., Pan Z.H., Troilo D. Evaluation of AAV-mediated expression of Chop2-GFP in the marmoset retina. Invest Ophthalmol Vis Sci 2010, 51:5288-5296.
40. Ivanova E., Pan Z.H. Evaluation of the adeno-associated virus mediated long-term expression of channelrhodopsin-2 in the mouse retina. Mol Vis 2009, 15:1680-1689.
41. Sugano E., Isago H., Wang Z., Murayama N., Tamai M., Tomita H. Immune responses to adeno-associated virus type 2 encoding channelrhodopsin-2 in a genetically blind rat model for gene therapy. Gene Ther 2011, 18:266-274.
42. Degenaar P., Grossman N., Memon M.A., Burrone J., Dawson M., Drakakis E., Neil M., Nikolic K. Optobionic vision-a new genetically enhanced light on retinal prosthesis. J Neural Eng 2009, 6:035007.
43. Grossman N., Poher V., Grubb M.S., Kennedy G.T., Nikolic K., McGovern B., Berlinguer Palmini R., Gong Z., Drakakis E.M., Neil M.A., et al. Multi-site optical excitation using ChR2 and micro-LED array. J Neural Eng 2010, 7:16004.
44. Guler A.D., Ecker J.L., Lall G.S., Haq S., Altimus C.M., Liao H.W., Barnard A.R., Cahill H., Badea T.C., Zhao H., et al. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 2008, 453:102-105.