Restoration of the majority of the visual spectrum by using modified volvox channelrhodopsin-1

Molecular Therapy

Volumn 22, Issue 8, 2014, Pages 1434-1440

  Tomita, Hiroshi ^a,b   Sugano, Eriko ^a   Murayama, Namie ^a   Ozaki, Taku ^c   Nishiyama, Fumiaki ^a   Tabata, Kitako ^a   Takahashi, Maki ^a   Saito, Takehiko ^a   Tamai, Makoto ^d  

^a IWATE UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY HOSPITAL   (Japan)

^c HIROSAKI UNIVERSITY   (Japan)

^d TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHANNELRHODOPSIN 1; PARVOVIRUS VECTOR; RHODOPSIN; UNCLASSIFIED DRUG; HYBRID PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLINDNESS; CELL MEMBRANE; CELL STIMULATION; CONTROLLED STUDY; EVOKED VISUAL RESPONSE; EXPLORATORY BEHAVIOR TEST; GENE; GENE EXPRESSION PROFILING; GENE TARGETING; GENE THERAPY; HUMAN; HUMAN CELL; MALE; MEMBRANE CURRENT; MVCHR1 GNEE; NONHUMAN; PROTEIN EXPRESSION; RAT; SPECTRAL SENSITIVITY; VIRAL GENE DELIVERY SYSTEM; VISION; VOLVOX; WHOLE CELL PATCH CLAMP; ANIMAL MODEL; CELLULAR DISTRIBUTION; CHLAMYDOMONAS; CYTOPLASM; GENE EXPRESSION; HEK293 CELL LINE; HUMAN TISSUE; PATCH CLAMP TECHNIQUE; RETINA GANGLION CELL; SPATIAL FREQUENCY DISCRIMINATION; VIRAL GENE THERAPY; ADMINISTRATION AND DOSAGE; ANIMAL; DEPENDOPARVOVIRUS; GENE VECTOR; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PROCEDURES; RETINA; THERAPEUTIC USE;

ADENO-ASSOCIATED VIRUS; CHLAMYDOMONAS; RATTUS; VOLVOX;

ANIMALS; BLINDNESS; CHLAMYDOMONAS; DEPENDOVIRUS; GENETIC THERAPY; GENETIC VECTORS; HEK293 CELLS; HUMANS; RATS; RECOMBINANT FUSION PROTEINS; RETINA; RHODOPSIN; VOLVOX;

EID: 84905491806     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.81     Document Type: Article

References (44)

1. Sineshchekov, OA, Jung, KH and Spudich, JL (2002). Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 99: 8689-8694.
2. Suzuki, T, Yamasaki, K, Fujita, S, Oda, K, Iseki, M, Yoshida, K et al. (2003). Archaealtype rhodopsins in Chlamydomonas: model structure and intracellular localization. Biochem Biophys Res Commun 301: 711-717.
3. Nagel, G, Szellas, T, Huhn, W, Kateriya, S, Adeishvili, N, Berthold, P et al. (2003). Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci USA 100: 13940-13945.
4. Oesterhelt, D and Stoeckenius, W (1973). Functions of a new photoreceptor membrane. Proc Natl Acad Sci USA 70: 2853-2857.
5. Ishizuka, T, Kakuda, M, Araki, R and Yawo, H (2006). Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels. Neurosci Res 54: 85-94.
6. Boyden, ES, Zhang, F, Bamberg, E, Nagel, G and Deisseroth, K (2005). Millisecondtimescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268.
7. Andrasfalvy, BK, Zemelman, BV, Tang, J and Vaziri, A (2010). Two-photon single-cell optogenetic control of neuronal activity by sculpted light. Proc Natl Acad Sci USA107: 11981-11986.
8. Stark, E, Koos, T and Buzsáki, G (2012). Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. J Neurophysiol 108: 349-363.
9. Bi, A, Cui, J, Ma, YP, Olshevskaya, E, Pu, M, Dizhoor, AM et al. (2006). Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50: 23-33.
10. Tomita, H, Sugano, E, Yawo, H, Ishizuka, T, Isago, H, Narikawa, S et al. (2007). Restoration of visual response in aged dystrophic RCS rats using AAV-mediated channelopsin-2 gene transfer. Invest Ophthalmol Vis Sci 48: 3821-3826.
11. Lagali, PS, Balya, D, Awatramani, GB, Münch, TA, Kim, DS, Busskamp, V et al. (2008). Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat Neurosci 11: 667-675.
12. Bowes, C, Li, T, Danciger, M, Baxter, LC, Applebury, ML and Farber, DB (1990). Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature 347: 677-680.
13. Pittler, SJ and Baehr, W (1991). Identification of a nonsense mutation in the rod photoreceptor cGMPphosphodiesterase beta-subunit gene of the rd mouse. Proc Natl Acad Sci USA 88: 8322-8326.
14. D'Cruz, PM, Yasumura, D, Weir, J, Matthes, MT, Abderrahim, H, LaVail, MM et al. (2000). Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum Mol Genet 9: 645-651.
15. Gal, A, Li, Y, Thompson, DA, Weir, J, Orth, U, Jacobson, SG et al. (2000). Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet 26: 270-271.
16. Zobor, D and Zrenner, E (2012). Retinitis pigmentosa - a review. Pathogenesis, guidelines for diagnostics and perspectives. Ophthalmologe 109: 501-514.
17. Tomita, H, Sugano, E, Isago, H and Tamai, M (2009). Channelrhodopsins provide a breakthrough insight into strategies for curing blindness. J Genet 88: 409-415.
18. Tomita, H, Sugano, E, Isago, H, Hiroi, T, Wang, Z, Ohta, E et al. (2010). Channelrhodopsin-2 gene transduced into retinal ganglion cells restores functional vision in genetically blind rats. Exp Eye Res 90: 429-436.
19. Zhang, F, Prigge, M, Beyrière, F, Tsunoda, SP, Mattis, J, Yizhar, O et al. (2008). Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvoxcarteri. Nat Neurosci 11: 631-633.
20. Yizhar, O, Fenno, LE, Prigge, M, Schneider, F, Davidson, TJ, O'Shea, DJ et al. (2011). Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477: 171-178.
21. Berndt, A, Yizhar, O, Gunaydin, LA, Hegemann, P and Deisseroth, K (2009). Bi-stable neural state switches. Nat Neurosci 12: 229-234.
22. Gomi, M, Sonoyama, M and Mitaku, S (2004). High performance system for signal peptide prediction: SOSUI signal. Chem-Bio Info J 4: 142-147.
23. Prusky, GT, Alam, NM, Beekman, S and Douglas, RM (2004). Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45: 4611-4616.
24. Gradinaru, V, Thompson, KR and Deisseroth, K (2008). eNpHR: a Natronomonashalorhodopsin enhanced for optogenetic applications. Brain Cell Biol 36: 129-139.
25. Zhang, F, Wang, LP, Brauner, M, Liewald, JF, Kay, K, Watzke, N et al. (2007). Multimodal fast optical interrogation of neural circuitry. Nature 446: 633-639.
26. Busskamp, V, Duebel, J, Balya, D, Fradot, M, Viney, TJ, Siegert, S et al. (2010). Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329: 413-417.
27. Wang, H, Sugiyama, Y, Hikima, T, Sugano, E, Tomita, H, Takahashi, T et al. (2009). Molecular determinants differentiating photocurrent properties of two channelrhodopsins from chlamydomonas. J BiolChem 284: 5685-5696.
28. von Heijne, G (1986). A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14: 4683-4690.
29. Nakai, K and Kanehisa, M (1992). A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14: 897-911.
30. Jung, M, Sommer, I, Schachner, M and Nave, KA (1996). Monoclonal antibody O10 defines a conformationally sensitive cell-surface epitope of proteolipid protein (PLP): evidence that PLP misfolding underlies dysmyelination in mutant mice. J Neurosci 16: 7920-7929.
31. Hetz, C and Soto, C (2003). Protein misfolding and disease: the case of prion disorders. Cell Mol Life Sci 60: 133-143.
32. Welihinda, AA, Tirasophon, W and Kaufman, RJ (1999). The cellular response to protein misfolding in the endoplasmic reticulum. Gene Expr 7: 293-300.
33. Denning, GM, Anderson, MP, Amara, JF, Marshall, J, Smith, AE and Welsh, MJ (1992). Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358: 761-764.
34. Sato, S, Ward, CL, Krouse, ME, Wine, JJ and Kopito, RR (1996). Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. J BiolChem271: 635-638.
35. Kaushal, S and Khorana, HG (1994). Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry 33: 6121-6128.
36. Sung, CH, Schneider, BG, Agarwal, N, Papermaster, DS and Nathans, J (1991). Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci USA 88: 8840-8844.
37. Sugano, E, Isago, H, Wang, Z, Murayama, N, Tamai, M and Tomita, H (2011). Immune responses to adeno-associated virus type 2 encoding channelrhodopsin-2 in a genetically blind rat model for gene therapy. Gene Ther 18: 266-274.
38. Doroudchi, MM, Greenberg, KP, Liu, J, Silka, KA, Boyden, ES, Lockridge, JA et al. (2011). Virally delivered channelrhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness. MolTher 19: 1220-1229.
39. Simpson, E (2006). A historical perspective on immunological privilege. Immunol Rev 213: 12-22.
40. Wu, C, Ivanova, E, Zhang, Y and Pan, ZH (2013). rAAV-mediated subcellular targeting of optogenetic tools in retinal ganglion cells in vivo. PLoS One 8: e66332.
41. Kato, HE, Zhang, F, Yizhar, O, Ramakrishnan, C, Nishizawa, T, Hirata, K et al. (2012). Crystal structure of the channelrhodopsin light-gated cation channel. Nature 482: 369-374.
42. Tomita, H, Sugano, E, Fukazawa, Y, Isago, H, Sugiyama, Y, Hiroi, T et al. (2009). Visual properties of transgenic rats harboring the channelrhodopsin-2 gene regulated by the thy-1. 2 promoter. PLoS One 4: e7679.
43. LaVail, MM and Battelle, BA (1975). Influence of eye pigmentation and light deprivation on inherited retinal dystrophy in the rat. Exp Eye Res 21: 167-192.
44. Sugano, E, Tomita, H, Ishiguro, S, Abe, T and Tamai, M (2005). Establishment of effective methods for transducing genes into iris pigment epithelial cells by using adeno-associated virus type 2. Invest Ophthalmol Vis Sci 46: 3341-3348.