Retinal prosthetics, optogenetics, and chemical photoswitches

ACS Chemical Neuroscience

Volumn 5, Issue 10, 2014, Pages 895-901

  Marc, Robert ^a   Pfeiffer, Rebecca ^a   Jones, Bryan ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

blindness; chemical photoswitches; optogenetics; prosthetics; remodeling; reprogramming; Retinal degeneration

Indexed keywords

AZOBENZENE DERIVATIVE; OPSIN; QUATERNARY AMMONIUM DERIVATIVE; RETINAL;

CHEMICAL PHOTOSWITCH; HUMAN; MOUSE; NERVE CELL; NONHUMAN; OPTOGENETICS; PHOTOTRANSDUCTION; RETINA DEGENERATION; RETINA NERVE CELL; RETINAL IMPLANT; REVIEW; SENSOR; VISUAL PROSTHESIS; ANIMAL; PATHOPHYSIOLOGY; PROCEDURES; RETINA; RETINAL DEGENERATION;

ANIMALS; HUMANS; OPTOGENETICS; RETINA; RETINAL DEGENERATION; VISUAL PROSTHESIS;

EID: 84908014576     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn5001233     Document Type: Review

References (63)

1. Nirenberg, S., and Pandarinath, C. (2012) Retinal prosthetic strategy with the capacity to restore normal vision. Proc. Natl. Acad. Sci. U.S.A. 109, 15012-15017.
2. Margalit, E., Maia, M., Weiland, J. D., Greenberg, R. J., Fujii, G. Y., Torres, G., Piyathaisere, D. V., O'Hearn, T. M., Liu, W., Lazzi, G., Dagnelie, G., Scribner, D. A., de Juan, E. J., and Humayun, M. S. (2002) Retinal prosthesis for the blind. Surv. Ophthalmol. 47, 335-356.
3. Zrenner, E. (2002) Will Retinal Implants Restore Vision? Science 295, 1022-1025.
4. Eberdt, M., Brown, P. K., and Lazzi, G. (2003) Two-dimensional SPICE-linked multiresolution impedance method for low-frequency electromagnetic interactions. IEEE Trans. Biomed. Eng. 50, 881-889.
5. Xie, J., G.J, W., Yow, L., Humayun, M. S., Weiland, J. D., Cela, C. J., Jadvar, H., Lazzi, G., Dhrami-Gavazi, E., and Tsang, S. H. (2012) Preservation of retinotopic map in retinal degeneration. Exp. Eye Res. 98, 88-96.
6. Stingl, K., Bartz-Schmidt, K. U., Besch, D., Braun, A., Bruckmann, A., Gekeler, F., Greppmaier, U., Hipp, S., Hörtdörfer, G., Kernstock, C., Koitschev, A., Kusnyerik, A., Sachs, H., Schatz, A., Stingl, K. T., Peters, T., Wilhelm, B., and Zrenner, E. (2013) Artificial vision with wirelessly powered subretinal electronic implant alpha-IMS. Proc. Biol. Sci. 280, 20130077.
7. Zrenner, E. (2013) Fighting blindness with microelectronics. Sci. Transl. Med. 5, 210-216.
8. Jiang, L., Li, T. Z., Boye, S. E., Hauswirth, W. W., Frederick, J. M., and Baehr, W. (2013) RNAi-mediated gene suppression in a GCAP1(L151F) cone-rod dystrophy mouse model. PLoS One 8, e57676.
9. Jiang, L., Zhang, H., Dizhoor, A. M., Boye, S. E., Hauswirth, W. W., Frederick, J. M., and Baehr, W. (2011) Long-term RNA interference Gene Therapy in a dominant retinitis pigmentosa mouse model. Proc. Natl. Acad. Sci. U.S.A. 108, 18476-18481.
10. Stieger, K., Cronin, T., Bennett, J., and Rolling, F. (2011) Adeno-associated virus mediated Gene Therapy for retinal degenerative diseases. Methods Mol. Biol. 807, 179-218.
11. Gonzalez-Cordero, A., West, E. L., Pearson, R. A., Duran, Y., Carvalho, L. S., Chu, C. J., Naeem, A., Blackford, S. J., Georgiadis, A., Lakowski, J., Hubank, M., Smith, A. J., Bainbridge, J. W., Sowden, J. C., and Ali, R. R. (2013) Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat. Biotechnol. 31, 741-747.
12. Lagali, P. S., Balya, D., Awatramani, G. B., Münch, T. A., Kim, D. S., Busskamp, V., Cepko, C. L., and Roska, B. (2008) Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat. Neurosci. 11, 667-675.
13. Busskamp, V., Picaud, S., Sahel, J. A., and Roska, B. (2012) Optogenetic therapy for retinitis pigmentosa. Gene Ther. 19, 169-175.
14. Busskamp, V., Duebel, J., Baly, D., Fradot, M., Viney, T. J., Siegert, S., Groner, A. C., Cabuy, E., Forster, V., Seeliger, M., Biel, M., Humphries, P., Paques, M., Mohand-Said, S., Trono, D., Deisseroth, K., Sahel, J. A., Picaud, S., and Roska, B. (2010) Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329, 413-417.
15. 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., Gordon, G. M., Matteo, B. C., Sampath, A. P., Hauswirth, W. W., and Horsager, A. (2011) Virally delivered channelrhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness. Mol. Ther 19, 1220-1229.
16. Mutter, M., Swietek, N., and Münch, T. A. (2014) Salvaging ruins: reverting blind retinas into functional visual sensors. Methods Mol. Biol. 1148, 149-160.
17. Tochitsky, I., Polosukhina, A., Degtyar, V. E., Gallerani, N., Smith, C. M., Friedman, A., Van Gelder, R. N., Trauner, D., Kaufer, D., and Kramer, R. H. (2014) Restoring visual function to blind mice with a photoswitch that exploits electrophysiological remodeling of retinal ganglion cells. Neuron 81, 800-813.
18. Polosukhina, A., Litt, J., Tochitsky, I., Nemargut, J., Sychev, Y., De Kouchkovsky, I., Huang, T., Borges, K., Trauner, D., Van Gelder, R. N., and Kramer, R. H. (2012) Photochemical restoration of visual responses in blind mice. Neuron 75, 271-282.
19. Jones, B. W., Kondo, M., Terasaki, H., Lin, Y., McCall, M., and Marc, R. E. (2012) Retinal remodeling. Jpn. J. Ophthalmol. 56, 289-306.
20. Marc, R. E. (2010) Synaptic Organization of the Retina. In Adler's Physiology of the Eye (Levin, L. A., Nilsson, S. F. E., Ver Hoeve, J., Wu, S. M., Kaufman, P. L., and Alm, A., Eds.), pp 443-458, Elsevier, Amsterdam.
21. Daiger, S. P., Sullivan, L. S., and Bowne, S. (2014) http://www.sph.uth.tmc.edu/Retnet/ (accessed 23 July 2014).
22. Schuster, A., Weisschuh, N., Jägle, H., Besch, D., Janecke, A. R., Zierler, H., Tippmann, S., Zrenner, E., and Wissinger, B. (2005) Novel rhodopsin mutations and genotype-phenotype correlation in patients with autosomal dominant retinitis pigmentosa. Br. J. Ophthalmol. 89, 1258-1264.
23. Redmond, T. M., Yu, S., Lee, E., Bok, D., Hamasaki, D., Chen, N., Goletz, P., Ma, J. X., Crouch, R. K., and Pfeifer, K. (1998) Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat. Genet. 20, 344-351.
24. Acland, G. M., Aguirre, G. D., Ray, J., Zhang, Q., Aleman, T. S., Cideciyan, A. V., Pearce-Kelling, S. E., Anand, V., Zeng, Y., Maguire, A. M., Jacobson, S. G., Hauswirth, W. W., and Bennett, J. (2001) Gene Therapy restores vision in a canine model of childhood blindness. Nat. Genet. 28, 92-95.
25. den Hollander, A. I., Black, A., Bennett, J., and Cremers, F. P. (2010) Lighting a candle in the dark: advances in genetics and gene therapy of recessive retinal dystrophies. J. Clin. Invest. 120, 3042-3053.
26. Perederiy, J. V., and Westbrook, G. L. (2013) Structural plasticity in the dentate gyrus- revisiting a classic injury model. Front. Neural Circuits 7, 17.
27. Jones, B. W., Watt, C. B., Frederick, J. M., Baehr, W., Chen, C. K., Levine, E. M., Milam, A. H., LaVail, M. M., and Marc, R. E. (2003) Retinal remodeling triggered by photoreceptor degenerations. J. Comp. Neurol. 464, 1-16.
28. Marc, R. E., Jones, B. W., Watt, C. B., and Strettoi, E. (2003) Neural Remodeling in Retinal Degeneration. Prog. Retinal Eye Res. 22, 607-655.
29. Marc, R. (2010) Injury and Repair: Retinal Remodeling. In Encyclopedia of the Eye (Dana, R., Ed.), pp 414-420, Elsevier, Amsterdam.
30. Marc, R. E., Jones, B. W., Anderson, J. R., Kinard, K., Marshak, D. W., Wilson, J. H., Wensel, T., and Lucas, R. J. (2007) Neural reprogramming in retinal degeneration. Invest. Ophthalmol. Visual Sci. 48, 3364-3371.
31. Jones, B. W., Kondo, M., Terasaki, H., Watt, C. B., Rapp, K., Anderson, J. R., Lin, Y., Shaw, M. V., Yang, J. H., and Marc, R. E. (2011) Retinal remodeling in the Tg P347L rabbit, a large-eye model of retinal degeneration. J. Comp. Neurol. 519, 2713-2733.
32. Lin, Y., Jones, B. W., Liu, A., Tucker, J. F., Rapp, K., Luo, L., Baehr, W., Bernstein, P. S., Watt, C. B., Yang, J. H., Shaw, M. V., and Marc, R. E. (2012) Retinoid receptors trigger neuritogenesis in retinal degenerations. FASEB J. 26, 81-92.
33. Lin, Y., Jones, B. W., Liu, A., Vazquez-Chona, F. R., Lauritzen, J. S., Ferrell, W., and Marc, R. E. (2012) Rapid glutamate receptor 2 trafficking during retinal degeneration. Mol. Neurodegener. 7, 7.
34. Marc, R. E. (2004) Retinal Neurotransmitters. In The Visual Neurosciences (Chalupa, L. M., and Werner, J., Eds.), pp 315-330, MIT Press, Cambridge, MA.
35. Marc, R., Jones, B., Watt, C., Vazquez-Chona, F., Vaughan, D., and Organisciak, D. (2008) Extreme retinal remodeling triggered by light damage: Implications for AMD. Mol. Vision 14, 782-806.
36. Pfeiffer, R. L., Jones, B. W., and Marc, R. E. (2014) Metabolic changes associated with Muller cells in a transgenic rabbit model of retinal degeneration. Invest. Ophthalmol. Visual Sci. 55, 829.
37. Ahuja, A. K., and Behrend, M. R. (2013) The Argus II retinal prosthesis: factors affecting patient selection for implantation. Prog. Retinal Eye Res. 36, 1-23.
38. Dorn, J. D., Ahuja, A. K., Caspi, A., da Cruz, L., Dagnelie, G., Sahel, J. A., Greenberg, R. J., McMahon, M. J., and Group, A. I. S. (2013) The Detection of Motion by Blind Subjects With the Epiretinal 60-Electrode (Argus II) Retinal Prosthesis. JAMA Ophthalmol. 131, 183-189.
39. Rizzo, S., Beltin, C., Cinelli, L., Allegrini, L., Genovesi-Ebert, F., Barca, F., and di Bartolo, E. (2014) The Argus II Retinal Prosthesis: Twelve-Month Outcomes from a Single-Study Center. Am. J. Ophthalmol. 157, 1282-1290.
40. Perry, V. H., and Cowey, A. (1985) The ganglion cell and cone distributions in the monkey's retina: Implications for central magnification factors. Vision Res. 25, 1795-1810.
41. Wässle, H., Grünert, U., Röhrenbeck, J., and Boycott, B. B. (1989) Cortical magnification factor and the ganglion cell density of the primate retina. Nature 341, 643-646.
42. Jepson, L. H., Hottowy, P., Mathieson, K., Gunning, D. E., Da¸browski, W., Litke, A. M., and Chichilnisky, E. J. (2014) Spatially patterned electrical stimulation to enhance resolution of retinal prostheses. J. Neurosci. 34, 4871-4881.
43. Weitz, A. C., Behrend, M. R., Ahuja, A. K., Christopher, P., Wei, J., Wuyyuru, V., Patel, U., Greenberg, R. J., Humayun, M. S., Chow, R. H., and Weiland, J. D. (2014) Interphase gap as a means to reduce electrical stimulation thresholds for epiretinal prostheses. J. Neural Eng. 11, 016007.
44. Stingl, K., Bartz-Schmidt, K. U., Gekeler, F., Kusnyerik, A., Sachs, H., and Zrenner, E. (2013) Functional outcome in subretinal electronic implants depends on foveal eccentricity. Invest. Ophthalmol. Visual Sci. 54, 7658-7665.
45. Nishida, K., Kamei, M., Kondo, M., Sakaguchi, H., Suzuki, M., Fujikado, T., and Tano, Y. (2010) Efficacy of suprachoroidal-transretinal stimulation in a rabbit model of retinal degeneration. Invest. Ophthalmol. Visual Sci. 51, 2263-2268.
46. Nayagam, D. A., Williams, R. A., Allen, P. J., Shivdasani, M. N., Luu, C. D., Salinas-LaRosa, C. M., Finch, S., Ayton, L. N., Saunders, A. L., McPhedran, M., McGowan, C., Villalobos, J., Fallon, J. B., Wise, A. K., Yeoh, J., Xu, J., Feng, H., Millard, R., McWade, M., Thien, P. C., Williams, C. E., and Shepherd, R. K. (2014) Chronic electrical stimulation with a suprachoroidal retinal prosthesis: a preclinical safety and efficacy study. PLoS One 9, e97182.
47. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., Ollig, D., Hegemann, P., and Bamberg, E. (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. U.S.A. 100, 13940-13945.
48. Kolbe, M., Besir, H., Essen, L. O., and Oesterhelt, D. (2000) Structure of the light-driven chloride pump halorhodopsin at 1.8 A˚ resolution. Science 288, 1390-1396.
49. Zhang, F., Wang, L. P., Brauner, M., Liewald, J. F., Kay, K., Watzke, N., Wood, P. G., Bamberg, E., Nagel, G., Gottschalk, A., and Deisseroth, K. (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446, 633-639.
50. Dalkara, D., Byrne, L. C., Lee, T., Hoffmann, N. V., Schaffer, D. V., and Flannery, J. G. (2012) Enhanced gene delivery to the neonatal retina through systemic administration of tyrosine-mutated AAV9. Gene Ther. 19, 176-181.
51. Lin, B., Koizumi, A., Tanaka, N., Panda, S., and Masland, R. H. (2008) Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc. Natl. Acad. Sci. U.S.A. 105, 16009-16014.
52. Strettoi, E., Pignatelli, V., Rossi, C., Porciatti, V., and Falsini, B. (2003) Remodeling of second-order neurons in the retina of rd/rd mutant mice. Vision Res. 43, 867-877.
53. Strettoi, E., Porciatti, V., Falsini, B., Pignatelli, V., and Rossi, C. (2002) Morphological and functional abnormalities in the inner retina of the rd/rd mouse. J. Neurosci. 22, 5492-5504.
54. G, N., Tan, A., Farhatnia, Y., Rajadas, J., Hamblin, M. R., Khaw, P. T., and Seifalian, A. M. (2013) Channelrhodopsins: visual regeneration and neural activation by a light switch. Nat. Biotechnol. 30, 461-474.
55. Mourot, A., Kienzler, M. A., Banghart, M. R., Fehrentz, T., Huber, F. M., Stein, M., Kramer, R. H., and Trauner, D. (2011) Tuning photochromic ion channel blockers. ACS Chem. Neurosci. 2, 536-543.
56. Fortin, D. L., Banghart, M. R., Dunn, T. W., Borges, K., Wagenaar, D. A., Gaudry, Q., Karakossian, M. H., Otis, T. S., Kristan, W. B., Trauner, D., and Kramer, R. H. (2008) Photochemical control of endogenous ion channels and cellular excitability. Nat. Methods 5, 331-338.
57. Marc, R. E., and Jones, B. W. (2002) Molecular phenotyping of retinal ganglion cells. J. Neurosci. 22, 412-427.
58. Marc, R. E., and Liu, W. (2000) Fundamental GABAergic amacrine cell circuitries in the retina: nested feedback, concatenated inhibition, and axosomatic synapses. J. Comp. Neurol. 425, 560-582.
59. Margolis, D. J., Gartland, A. J., Singer, J. H., and Detwiler, P. B. (2014) Network oscillations drive correlated spiking of ON and OFF ganglion cells in the rd1 mouse model of retinal degeneration. PLoS One 9, e86253.
60. Margolis, D. J., Newkirk, G., Euler, T., and Detwiler, P. B. (2008) Functional stability of retinal ganglion cells after degeneration-induced changes in synaptic input. J. Neurosci. 28, 6526-6536.
61. Stasheff, S. F. (2008) Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse. J. Neurophysiol. 99, 1408-1421.
62. Yee, C. W., Toychiev, A. H., and Sagdullaev, B. T. (2012) Network deficiency exacerbates impairment in a mouse model of retinal degeneration. Front Syst. Neurosci. 6, 8.
63. He, C., Chen, F., Li, B., and Hu, Z. (2014) Neurophysiology of HCN channels: from cellular functions to multiple regulations. Prog. Neurobiol. 112, 1-23.