Melanopsin is highly resistant to light and chemical bleaching in vivo

Journal of Biological Chemistry

Volumn 287, Issue 25, 2012, Pages 20888-20897

  Sexton, Timothy J ^a   Golczak, Marcin ^c   Palczewski, Krzysztof ^c   Van Gelder, Russell N ^a,b  

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

^b UNIVERSITY OF WASHINGTON   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDERSONS; BISTABLE MECHANISMS; CIRCADIAN RHYTHMS; CONE PHOTORECEPTORS; COVALENTLY BOUND; DATA SUPPORT; EX-VIVO; FUNCTIONAL PIGMENTS; IN-VIVO; LIGHT RESPONSE; MELANOPSIN; PHOTOCYCLES; RETINAL GANGLION CELLS;

BLEACHING; CHROMOPHORES; CLEANING; MAMMALS; OPHTHALMOLOGY;

ALDEHYDES;

9 CIS RETINAL; 9 CIS RETINOL ACETATE; HYDROXYLAMINE; MELANOPSIN; RETINAL; RETINOID; SERINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLEACHING; CELL ACTIVITY; CHROMATOPHORE; CONTROLLED STUDY; EX VIVO STUDY; IN VIVO STUDY; INTRINSICALLY PHOTOSENSITIVE RETINAL GANGLION CELL; LIGHT EXPOSURE; MOUSE; NONHUMAN; PHOTOACTIVATION; PHOTOREACTIVITY; PHOTORECEPTOR; PHOTOSENSITIVITY; PHYSICAL RESISTANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; RETINA GANGLION CELL; RETINA ROD; ULTRAVIOLET RADIATION;

ANIMALS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PHOTOBLEACHING; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; RETINALDEHYDE; ROD OPSINS; ULTRAVIOLET RAYS;

EID: 84862274052     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.325969     Document Type: Article

References (54)

1. Tu, D. C., Owens, L. A., Anderson, L., Golczak, M., Doyle, S. E., McCall, M., Menaker, M., Palczewski, K., and Van Gelder, R. N. (2006) Inner retinal photoreception independent of the visual retinoid cycle. Proc. Natl. Acad. Sci. U.S.A. 103, 10426-10431 (Pubitemid 44051183)
2. Güler, A. D., Altimus, C. M., Ecker, J. L., and Hattar, S. (2007) Multiple photoreceptors contribute to nonimage-forming visual functions predominantly through melanopsin-containing retinal ganglion cells. Cold Spring Harbor Symp. Quant. Biol. 72, 509-515
3. Peirson, S., and Foster, R. G. (2006) Melanopsin. Another way of signaling light. Neuron 49, 331-339 (Pubitemid 43152235)
4. Do, M. T., and Yau, K. W. (2010) Intrinsically photosensitive retinal ganglion cells. Physiol. Rev. 90, 1547-1581
5. Chen, S. K., Badea, T. C., and Hattar, S. (2011) Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature 476, 92-95
6. Hattar, S., Lucas, R. J., Mrosovsky, N., Thompson, S., Douglas, R. H., Hankins, M. W., Lem, J., Biel, M., Hofmann, F., Foster, R. G., and Yau, K. W. (2003) Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424, 76-81 (Pubitemid 36834844)
7. Tu, D. C., Zhang, D., Demas, J., Slutsky, E. B., Provencio, I., Holy, T. E., and Van Gelder, R. N. (2005) Physiologic diversity and development of intrinsically photosensitive retinal ganglion cells. Neuron 48, 987-999 (Pubitemid 41814702)
8. Panda, S., Provencio, I., Tu, D. C., Pires, S. S., Rollag, M. D., Castrucci, A. M., Pletcher, M. T., Sato, T. K., Wiltshire, T., Andahazy, M., Kay, S. A., Van Gelder, R. N., and Hogenesch, J. B. (2003) Melanopsin is required for non-image-forming photic responses in blind mice. Science 301, 525-527 (Pubitemid 36900311)
9. Kuksa, V., Imanishi, Y., Batten, M., Palczewski, K., and Moise, A. R. (2003) Retinoid cycle in the vertebrate retina. Experimental approaches and mechanisms of isomerization. Vision Res. 43, 2959-2981 (Pubitemid 37383728)
10. Nickle, B., and Robinson, P. R. (2007) The opsins of the vertebrate retina. Insights from structural, biochemical, and evolutionary studies. Cell Mol. Life Sci. 64, 2917-2932 (Pubitemid 351152247)
11. Fu, Y., Zhong, H., Wang, M. H., Luo, D. G., Liao, H. W., Maeda, H., Hattar, S., Frishman, L. J., and Yau, K. W. (2005) Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. Proc. Natl. Acad. Sci. U.S.A. 102, 10339-10344 (Pubitemid 41023372)
12. Walker, M. T., Brown, R. L., Cronin, T. W., and Robinson, P. R. (2008) Photochemistry of retinal chromophore in mouse melanopsin. Proc. Natl. Acad. Sci. U.S.A. 105, 8861-8865
13. Panda, S., Sato, T. K., Castrucci, A. M., Rollag, M. D., DeGrip, W. J., Hogenesch, J. B., Provencio, I., and Kay, S. A. (2002) Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298, 2213-2216 (Pubitemid 35471251)
14. Wong, W. T., Myhr, K. L., Miller, E. D., and Wong, R. O. (2000) Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity. J. Neurosci. 20, 351-360 (Pubitemid 30220522)
15. Holy, T. E., Dulac, C., and Meister, M. (2000) Responses of vomeronasal neurons to natural stimuli. Science 289, 569-572
16. Garwin, G. G., and Saari, J. C. (2000) High-performance liquid chromatography analysis of visual cycle retinoids. Methods Enzymol. 316, 313-324 (Pubitemid 30235676)
17. Saari, J. C., Nawrot, M., Kennedy, B. N., Garwin, G. G., Hurley, J. B., Huang, J., Possin, D. E., and Crabb, J. W. (2001) Visual cycle impairment in cellular retinaldehyde binding protein (CRALBP) knockout mice results in delayed dark adaptation. Neuron 29, 739-748 (Pubitemid 32323946)
18. Saari, J. C., Nawrot, M., Garwin, G. G., Kennedy, M. J., Hurley, J. B., Ghyselinck, N. B., and Chambon, P. (2002) Analysis of the visual cycle in cellular retinol-binding protein type I (CRBPI) knockout mice. Invest. Ophthalmol. Vis. Sci. 43, 1730-1735 (Pubitemid 34587014)
19. Tu, D. C., Batten, M. L., Palczewski, K., and Van Gelder, R. N. (2004) Nonvisual photoreception in the chick iris. Science 306, 129-131 (Pubitemid 39451955)
20. Maeda, A., Maeda, T., Golczak, M., Chou, S., Desai, A., Hoppel, C. L., Matsuyama, S., and Palczewski, K. (2009) Involvement of all-trans-retinal in acute light-induced retinopathy of mice. J. Biol. Chem. 284, 15173-15183
21. Do, M. T., Kang, S. H., Xue, T., Zhong, H., Liao, H. W., Bergles, D. E., and Yau, K. W. (2009) Photon capture and signalling by melanopsin retinal ganglion cells. Nature 457, 281-287
22. Wang, J. S., and Kefalov, V. J. (2011) The cone-specific visual cycle. Prog. Retin. Eye Res. 30, 115-128
23. Wald, G., Brown, P. K., and Smith, P. H. (1955) Iodopsin. J. Gen. Physiol. 38, 623-681
24. Abrahamson, E. W., Fager, R. S., and Mason, W. T. (1974) Comparative properties of vertebrate and invertebrate photoreceptors. Exp. Eye Res. 18, 51-67
25. Dartnall, H. J. (1968) The photosensitivities of visual pigments in the presence of hydroxylamine. Vision Res. 8, 339-358
26. Leibrock, C. S., and Lamb, T. D. (1997) Effect of hydroxylamine on photon-like events during dark adaptation in toad rod photoreceptors. J. Physiol. 501, 97-109 (Pubitemid 27230405)
27. Brin, K. P., and Ripps, H. (1977) Rhodopsin photoproducts and rod sensitivity in the skate retina. J. Gen. Physiol. 69, 97-120 (Pubitemid 8019373)
28. Wald, G., and Brown, P. K. (1950) The synthesis of rhodopsin from Retinene(1). Proc. Natl. Acad. Sci. U.S.A. 36, 84-92
29. Hubbard, R., and St. George, R. C. (1958) The rhodopsin system of the squid. J. Gen. Physiol. 41, 501-528
30. Bowmaker, J. K., and Loew, E. R. (1976) The action of hydroxylamine on visual pigments in the intact retina of the frog (Rana temporaria). Vision Res. 16, 811-818
31. Nemargut, J. P., and Wang, G. Y. (2009) Inhibition of nitric oxide synthase desensitizes retinal ganglion cells to light by diminishing their excitatory synaptic currents under light adaptation. Vision Res. 49, 2936-2947
32. Provencio, I., Jiang, G., De Grip, W. J., Hayes, W. P., and Rollag, M. D. (1998) Melanopsin. An opsin in melanophores, brain, and eye. Proc. Natl. Acad. Sci. U.S.A. 95, 340-345 (Pubitemid 28103955)
33. Bellingham, J., Whitmore, D., Philp, A. R., Wells, D. J., and Foster, R. G. (2002) Zebrafish melanopsin. Isolation, tissue localisation and phylogenetic position. Brain Res. Mol. Brain Res. 107, 128-136 (Pubitemid 35335530)
34. Palczewski, K. (2006) G protein-coupled receptor rhodopsin. Annu. Rev. Biochem. 75, 743-767
35. Kiser, P. D., Golczak, M., Maeda, A., and Palczewski, K. (2011) Key enzymes of the retinoid (visual) cycle in the vertebrate retina. Biochim. Biophys. Acta 1821, 137-151
36. Hardie, R. C., and Postma, M. (2007) in The Senses: A Comprehensive Review (Bushnell, M., Smith, D., Beauchamp, G., Firestein, S., Dallos, P., Oertel, D., Masland, R., Albright, T., Kaas, J., Gardner, E., and Basbaum, A., eds) Vol. 1, pp. 77-130, Academic Press, Waltham, MA
37. Hillman, P., Hochstein, S., and Minke, B. (1983) Transduction in invertebrate photoreceptors. Role of pigment bistability. Physiol. Rev. 63, 668-772 (Pubitemid 13134311)
38. Panda, S., Nayak, S. K., Campo, B., Walker, J. R., Hogenesch, J. B., and Jegla, T. (2005) Illumination of the melanopsin signaling pathway. Science 307, 600-604 (Pubitemid 40165686)
39. Melyan, Z., Tarttelin, E. E., Bellingham, J., Lucas, R. J., and Hankins, M. W. (2005) Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433, 741-745 (Pubitemid 40292982)
40. Davies, W. I., Zheng, L., Hughes, S., Tamai, T. K., Turton, M., Halford, S., Foster, R. G., Whitmore, D., and Hankins, M. W. (2011) Functional diversity of melanopsins and their global expression in the teleost retina. Cell Mol. Life Sci. 68, 4115-4132
41. Matos-Cruz, V., Blasic, J., Nickle, B., Robinson, P. R., Hattar, S., and Halpern, M. E. (2011) Unexpected diversity and photoperiod dependence of the zebrafish melanopsin system. PLoS ONE 6, e25111
42. Wong, K. Y., Dunn, F. A., and Berson, D. M. (2005) Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron 48, 1001-1010 (Pubitemid 41814703)
43. Stecher, H., and Palczewski, K. (2000) Multienzyme analysis of visual cycle. Methods Enzymol. 316, 330-344 (Pubitemid 30235678)
44. Pepperberg, D. (1992) Hydroxylamine-dependent inhibition of rhodopsin phosphorylation in the isolated retina. Exp. Eye Res. 54, 369-376
45. Pepperberg, D. R., Morrison, D. F., and O'Brien, P. J. (1995) Depalmitoylation of rhodopsin with hydroxylamine. Methods Enzymol. 250, 348-361
46. Thompson, C. L., Selby, C. P., Van Gelder, R. N., Blaner, W. S., Lee, J., Quadro, L., Lai, K., Gottesman, M. E., and Sancar, A. (2004) Effect of vitamin A depletion on nonvisual phototransduction pathways in cryptochromeless mice. J. Biol. Rhythms 19, 504-517 (Pubitemid 39507176)
47. Mure, L. S., Rieux, C., Hattar, S., and Cooper, H. M. (2007) Melanopsin-dependent nonvisual responses. Evidence for photopigment bistability in vivo. J. Biol. Rhythms 22, 411-424 (Pubitemid 47507059)
48. Mawad, K., and Van Gelder, R. N. (2008) Absence of long-wavelength photic potentiation of murine intrinsically photosensitive retinal ganglion cell firing in vitro. J. Biol. Rhythms 23, 387-391
49. Koyanagi, M., Kubokawa, K., Tsukamoto, H., Shichida, Y., and Terakita, A. (2005) Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr. Biol. 15, 1065-1069 (Pubitemid 40772156)
50. Terakita, A., Tsukamoto, H., Koyanagi, M., Sugahara, M., Yamashita, T., and Shichida, Y. (2008) Expression and comparative characterization of Gq-coupled invertebrate visual pigments and melanopsin. J. Neurochem. 105, 883-890 (Pubitemid 351562728)
51. Vought, B. W., Salcedo, E., Chadwell, L. V., Britt, S. G., Birge, R. R., and Knox, B. E. (2000) Characterization of the primary photointermediates of Drosophila rhodopsin. Biochemistry 39, 14128-14137
52. Koutalos, Y., Ebrey, T. G., Tsuda, M., Odashima, K., Lien, T., Park, M. H., Shimizu, N., Derguini, F., Nakanishi, K., and Gilson, H. R. (1989) Regeneration of bovine and octopus opsins in situ with natural and artificial retinals. Biochemistry 28, 2732-2739 (Pubitemid 19094396)
53. Chow, B. Y., Han, X., Bernstein, J. G., Monahan, P. E., and Boyden, E. S. (2011) in Neuromethods (Walz, W., ed) Vol. 55, pp. 99-132, Humana Press, New York
54. Ozaki, K., Hara, R., Hara, T., and Kakitani, T. (1983) Squid retinochrome. Configurational changes of the retinal chromophore. Biophys. J. 44, 127-137