Ectopic Expression of a Microbial-Type Rhodopsin Restores Visual Responses in Mice with Photoreceptor Degeneration

Neuron

Volumn 50, Issue 1, 2006, Pages 23-33

  Bi, Anding ^a   Cui, Jinjuan ^a   Ma, Yu Ping ^a   Olshevskaya, Elena ^b   Pu, Mingliang ^c   Dizhoor, Alexander M ^a,b   Pan, Zhuo Hua ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PENNSYLVANIA COLLEGE OF OPTOMETRY   (United States)

^c PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

HUMDISEASE; MOLNEURO; PROTEINS

Indexed keywords

ADENOVIRUS VECTOR; CHANNELRHODOPSIN 2; RHODOPSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEGENERATION; CONTROLLED STUDY; FEASIBILITY STUDY; IN VIVO STUDY; LIGHT; MOUSE; NEWBORN; NONHUMAN; PHOTOREACTIVITY; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA; RETINA CONE; RETINA DEGENERATION; RETINA NERVE CELL; RETINA ROD; VISION; VISUAL CORTEX;

ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; EVOKED POTENTIALS, VISUAL; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NEURONS; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; PHOTORECEPTORS, VERTEBRATE; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; RETINA; RETINAL DEGENERATION; RHODOPSIN; VISUAL PATHWAYS;

EID: 33645974269     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.02.026     Document Type: Article

References (57)

1. 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., et al. Gene therapy restores vision in a canine model of childhood blindness. Nat. Genet. 28 (2001) 92-95
2. Ali R.R., Sarra G.M., Stephens C., Alwis M.D., Bainbridge J.W., Munro P.M., Fauser S., Reichel M.B., Kinnon C., Hunt D.M., et al. Restoration of photoreceptor ultrastructure and function in retinal degeneration slow mice by gene therapy. Nat. Genet. 25 (2000) 306-310
3. Auricchio A., Kobinger G., Anand V., Hildinger M., O' Connor E., Maguire A.M., Wilson J.M., and Bennett J. Exchange of surface proteins impacts on viral vector cellular specificity and transduction characteristics: the retina as a model. Hum. Mol. Genet. 10 (2001) 3075-3081
4. Banghart M., Borges K., Isacoff E., Trauner D., and Kramer R.H. Light-activated ion channels for remote control of neuronal firing. Nat. Neurosci. 7 (2004) 1381-1386
5. Barlow H.B., Levick W.R., and Yoon M. Responses to single quanta of light in retinal ganglion cells of the cat. Vision Res. 3 (1971) 87-101
6. Baylor D. How photons start vision. Proc. Natl. Acad. Sci. USA 93 (1996) 560-565
7. Bennett J., Maguire A.M., Cideciyan A.V., Schnell M., Glover E., Anand V., Aleman T.S., Chirmule N., Gupta A.R., Huang Y., et al. Stable transgene expression in rod photoreceptors after recombinant adeno-associated virus-mediated gene transfer to monkey retina. Proc. Natl. Acad. Sci. USA 96 (1999) 9920-9925
8. Bok D. Retinal transplantation and gene therapy. Present realities and future possibilities. Invest. Ophthalmol. Vis. Sci. 34 (1993) 473-476
9. Bowes C., Li T., Danciger M., Baxter L.C., Applebury M.L., and Farber D.B. Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature 347 (1990) 677-680
10. Boyden E.S., Zhang F., Bamberg E., Nagel G., and Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8 (2005) 1263-1268
11. Chang B., Hawes N.L., Hurd R.E., Davisson M.T., Nusinowitz S., and Heckenlively J.R. Retinal degeneration mutants in the mouse. Vision Res. 42 (2002) 517-525
12. Cui J., Ma Y.P., Lipton S.A., and Pan Z.-H. Glycine receptors and glycinergic synaptic input at the axon terminals of mammalian retinal rod bipolar cells. J. Physiol. 553 (2003) 895-909
13. Dacey D.M., Liao H.W., Peterson B.B., Robinson F.R., Smith V.C., Pokorny J., Yau K.W., and Gamlin P.D. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433 (2005) 749-754
14. Fitzsimons H.L., Bland R.J., and During M.J. Promoters and regulatory elements that improve adeno-associated virus transgene expression in the brain. Methods 28 (2002) 227-236
15. Flannery J.G., Zolotukhin S., Vaquero M.I., LaVail M.M., Muzyczka N., and Hauswirth W.W. Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus. Proc. Natl. Acad. Sci. USA 94 (1997) 6916-6921
16. Flotte T.R. Gene therapy progress and prospects: recombinant adeno-associated virus (rAAV) vectors. Gene Ther. 11 (2004) 805-810
17. Harvey A.R., Kamphuis W., Eggers R., Symons N.A., Blits B., Niclou S., Boer G.J., and Verhaagen J. Intravitreal injection of adeno-associated viral vectors results in the transduction of different types of retinal neurons in neonatal and adult rats: a comparison with lentiviral vectors. Mol. Cell. Neurosci. 21 (2002) 141-157
18. Humphries P., Kenna P., and Farrar G.J. On the molecular genetics of retinitis pigmentosa. Science 256 (1992) 804-808
19. Ishizuka T., Kakuda M., Araki R., and Yawo H. Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels. Neurosci. Res. 54 (2006) 85-94
20. Jimenez A.J., Garcia-Fernandez J.M., Gonzalez B., and Foster R.G. The spatio-temporal pattern of photoreceptor degeneration in the aged rd/rd mouse retina. Cell Tissue Res. 284 (1996) 193-202
21. Jones B.W., and Marc R.E. Retinal remodeling during retinal degeneration. Exp. Eye Res. 81 (2005) 123-137
22. 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. Retinal remodeling triggered by photoreceptor degenerations. J. Comp. Neurol. 464 (2003) 1-16
23. Kaneko A. Physiological and morphological identification of horizontal, bipolar, and amacrine cells in the goldfish retina. J. Physiol. 207 (1970) 623-633
24. Kateriya S., Nagel G., Bamberg E., and Hegemann P. "Vision" in single-celled algae. News Physiol. Sci. 19 (2004) 133-137
25. Kim C.I., Leo M.A., and Lieber C.S. Retinol forms retinoic acid via retinal. Arch. Biochem. Biophys. 294 (1992) 388-393
26. Li X., Gutierrez D.V., Hanson M.G., Han J., Mark M.D., Chiel H., Hegemann P., Landmesser L.T., and Herlitze S. Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc. Natl. Acad. Sci. USA 102 (2005) 17816-17821
27. Lund R.D., Kwan A.S., Keegan D.J., Sauve Y., Coffey P.J., and Lawrence J.M. Cell transplantation as a treatment for retinal disease. Prog. Retin. Eye Res. 20 (2001) 415-449
28. Martin K.R., Quigley H.A., Zack D.J., Levkovitch-Verbin H., Kielczewski J., Valenta D., Baumrind L., Pease M.E., Klein R.L., and Hauswirth W.W. Gene therapy with brain-derived neurotrophic factor as a protection: retinal ganglion cells in a rat glaucoma model. Invest. Ophthalmol. Vis. Sci. 44 (2003) 4357-4365
29. McLaughlin M.E., Sandberg M.A., Berson E.L., and Dryja T.P. Recessive mutations in the gene encoding the beta-subunit of rod phosphodiesterase in patients with retinitis pigmentosa. Nat. Genet. 4 (1993) 130-134
30. Melyan Z., Tarttelin E.E., Bellingham J., Lucas R.J., and Hankins M.W. Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433 (2005) 741-745
31. Milam A.H., Li Z.Y., and Fariss R.N. Histopathology of the human retina in retinitis pigmentosa. Prog. Retin. Eye Res. 17 (1998) 175-205
32. Nagel G., Ollig D., Fuhrmann M., Kateriya S., Musti A.M., Bamberg E., and Hegemann P. Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296 (2002) 2395-2398
33. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N., Berthold P., Ollig D., Hegemann P., and Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100 (2003) 13940-13945
34. Oesterhelt D. The structure and mechanism of the family of retinal proteins from halophilic archaea. Curr. Opin. Struct. Biol. 8 (1998) 489-500
35. Oesterhelt D., and Stoeckenius W. Functions of a new photoreceptor membrane. Proc. Natl. Acad. Sci. USA 70 (1973) 2853-2857
36. 2+ and causes photoreceptor degeneration in transgenic mice. J. Neurosci. 24 (2004) 6078-6085
37. Pan Z.-H. Differential expression of high- and two types of low-voltage-activated calcium currents in rod and cone bipolar cells of the rat retina. J. Neurophysiol. 83 (2000) 513-527
38. Panda S., Nayak S.K., Campo B., Walker J.R., Hogenesch J.B., and Jegla T. Illumination of the melanopsin signaling pathway. Science 307 (2005) 600-604
39. 1 based) visual pigments. Vision Res. 31 (1991) 619-630
40. Qiu X., Kumbalasiri T., Carlson S.M., Wong K.Y., Krishna V., Provencio I., and Berson D.M. Induction of photosensitivity by heterologous expression of melanopsin. Nature 433 (2005) 745-749
41. Santos A., Humayun M.S., de Juan Jr. E., Greenburg R.J., Marsh M.J., Klock I.B., and Milam A.H. Preservation of the inner retina in retinitis pigmentosa. A morphometric analysis. Arch. Ophthalmol. 115 (1997) 511-515
42. Schiller P.H., Sandell J.H., and Maunsell J.H. Functions of the ON and OFF channels of the visual system. Nature 322 (1986) 824-825
43. Sineshchekov O.A., Jung K.H., and Spudich J.L. Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 99 (2002) 8689-8694
44. Steinberg R.H., Fisher S.K., and Anderson D.H. Disc morphogenesis in vertebrate photoreceptors. J. Comp. Neurol. 190 (1980) 501-518
45. Strettoi E., and Pignatelli V. Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proc. Natl. Acad. Sci. USA 97 (2000) 11020-11025
46. Stryer L. Visual excitation and recovery. J. Biol. Chem. 266 (1991) 10711-10724
47. Sung C.H., Davenport C.M., Hennessey J.C., Maumenee I.H., Jacobson S.G., Heckenlively J.R., Nowakowski R., Fishman G., Gouras P., and Nathans J. Rhodopsin mutations in autosomal dominant retinitis pigmentosa. Proc. Natl. Acad. Sci. USA 88 (1991) 6481-6485
48. Suzuki T., Yamasaki K., Fujita S., Oda K., Iseki M., Yoshida K., Watanabe M., Daiyasu H., Toh H., Asamizu E., et al. Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization. Biochem. Biophys. Res. Commun. 301 (2003) 711-717
49. Tian N., and Copenhagen D.R. Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39 (2003) 85-96
50. Thompson D.A., and Gal A. Vitamin A metabolism in the retinal pigment epithelium: genes, mutations, and diseases. Prog. Retin. Eye Res. 22 (2003) 683-703
51. Tu D.C., Zhang D., Demas J., Slutsky E.B., Provencio I., Holy T.E., and Van Gelder R.N. Physiologic diversity and development of intrinsically photosensitive retinal ganglion cells. Neuron 48 (2005) 987-999
52. Wald G. The molecular basis of visual excitation. Nature 219 (1968) 800-807
53. Wässle H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5 (2004) 747-757
54. Weleber R.G. Retinitis pigmentosa and allied disorders. In: Ryan S.J. (Ed). Retina (1994), Mosby, St. Louis, MO 335-466
55. Werblin F.S., and Dowling J.E. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J. Neurophysiol. 32 (1969) 339-355
56. Zemelman B.V., Lee G.A., Ng M., and Miesenbock G. Selective photostimulation of genetically chARGed neurons. Neuron 33 (2002) 15-22
57. Zrenner E. Will retinal implants restore vision?. Science 295 (2002) 1022-1025