Photon capture and signalling by melanopsin retinal ganglion cells

H., Michael Tri; Kang, Shin-Hyoung; Xue, Tian; Zhong, Haining; Liao, Hsi Wen; Bergles, Dwight E.; Yau, King Wai

doi:10.1038/nature07682

Cited by 253 publications

(341 citation statements)

References 47 publications

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“…Nevertheless, the present result reveals that complete removal of conventional photoreceptors substantially reduced but did not completely abolish PLR. Thus our result is in agreement with previous reports [25][26][27] and suggests that the residual PLR could be contributed by surviving ipRGCs.…”

Section: Discussionsupporting

confidence: 94%

“…It is expected because light signal is sensed by two different types of photoreceptors, the conventional photoreceptors and intrinsically photosensitive retinal ganglion cells or melanopsin expressing retinal ganglion cells (ipRGCs), and the latter is much less sensitive than conventional photoreceptors [25]. Although there is substantial evidence that both conventional photoreceptors and ipRGCs contribute to PLR, depleting ipRGCs could substantially diminish PLR [25][26][27]. Since there is no melanopsin antibody available that specifically targets ipRGCs in the cat, we cannot evaluate the impact of IAA on ipRGCs in the cats.…”

Section: Discussionmentioning

confidence: 99%

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Functional evaluation of iodoacetic acid induced photoreceptor degeneration in the cat

Zhang

Ren

et al. 2013

Sci. China Life Sci.

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Iodoacetic acid (IAA) has been applied to different species to acutely induce photoreceptor degeneration. The purpose of the present study was to use this toxin to thoroughly eliminate photoreceptors and induce complete blindness in the cat. IAA was delivered by single ear vein injection (20 mg kg 1 ). Six months after the IAA treatment, functional evaluations including pupillary light reflex (PLR), electroretinogram (ERG), visual behavior tests were performed. Morphological examinations were carried out after the functional evaluation. The present result shows that, six months after the IAA application, animals lost visual functions and became completely blind. High dose IAA application via ear vein delivery created an acute and reliable complete photoreceptor degeneration model in the cat. This model can be applied to genetic and cellular therapies for visual function restoration.

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Section: Discussionsupporting

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Functional evaluation of iodoacetic acid induced photoreceptor degeneration in the cat

Zhang

Ren

et al. 2013

Sci. China Life Sci.

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“…A high sensitivity of melanopsins would also be consistent with their presence in extraretina locations such as in pineal complex, deep brain, and derma of nonmammalian vertebrates (e.g., amphibian) (16)(17)(18). The amount of light that can penetrate into such regions is limited and enriched in the red component due to light scattering by the surrounding tissues (14).…”

mentioning

confidence: 67%

“…The different studies carried out so far on melanopsin light sensitivity do not lead to consistent results. Although Do et al (14) argue that ipRGCs work at extremely low irradiation intensities showing a single-photon response larger than rods, Ferrer et al (15) conclude that the melanopsin has a reduced sensitivity relative to visual pigments. On the other hand, these photoreceptors would be expected to display high light sensitivity (14).…”

mentioning

confidence: 99%

Comparison of the isomerization mechanisms of human melanopsin and invertebrate and vertebrate rhodopsins

Rinaldi

Melaccio

Gozem

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Comparative modeling and ab initio multiconfigurational quantum chemistry are combined to investigate the reactivity of the human nonvisual photoreceptor melanopsin. It is found that both the thermal and photochemical isomerization of the melanopsin 11-cis retinal chromophore occur via a space-saving mechanism involving the unidirectional, counterclockwise twisting of the =C11H-C12H= moiety with respect to its Lys340-linked frame as proposed by Warshel for visual pigments [Warshel A (1976) Nature 260 (5553):679-683]. A comparison with the mechanisms documented for vertebrate (bovine) and invertebrate (squid) visual photoreceptors shows that such a mechanism is not affected by the diversity of the three chromophore cavities. Despite such invariance, trajectory computations indicate that although all receptors display less than 100 fs excited state dynamics, human melanopsin decays from the excited state ∼40 fs earlier than bovine rhodopsin. Some diversity is also found in the energy barriers controlling thermal isomerization. Human melanopsin features the highest computed barrier which appears to be ∼2.5 kcal mol −1 higher than that of bovine rhodopsin. When assuming the validity of both the reaction speed/quantum yield correlation discussed by Warshel, Mathies and coworkers [Weiss RM, Warshel A (1979) J Am Chem Soc 101:6131-6133; Schoenlein RW, Peteanu LA, Mathies RA, Shank CV (1991) Science 254(5030):412-415] and of a relationship between thermal isomerization rate and thermal activation of the photocycle, melanopsin turns out to be a highly sensitive pigment consistent with the low number of melanopsincontaining cells found in the retina and with the extraretina location of melanopsin in nonmammalian vertebrates.F or a long time it was assumed that the human retina contains only two types of photoreceptor cells: the rods and cones responsible for dim-light and daylight vision, respectively. However, recent studies have revealed the existence of a small number of intrinsically photosensitive retinal ganglion cells (ipRGCs) that regulate nonvisual photoresponses (1). ipRGCs express an atypical opsin-like protein named melanopsin (2, 3) which plays a role in the regulation of unconscious visual reflexes and in the synchronization of endogenous physiological responses to the dawn/dusk cycle (circadian rhythms) (4, 5).Melanopsins are unique among vertebrate photoreceptors because their amino acid sequence shares greater similarity to invertebrate than vertebrate rhodopsin (i.e., the photoreceptor of rods) (6, 7). Like rhodopsins, melanopsins feature an up-down bundle architecture of seven transmembrane α-helices incorporating the 11-cis isomer of retinal as a covalently bound protonated Schiff base (PSB11 in Fig. 1A). Light-induced (i.e., photochemical) isomerization of PSB11 to its all-trans isomer (PSBAT) triggers an opsin conformational change that, ultimately, activates the receptor and signaling cascade (8, 9). However, similar to invertebrate and in contrast to vertebrate rhodopsins, melanopsins are bistable ...

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“…In invertebrate visual cells and mammalian intrinsic photosensitive retinal ganglion cells, a photon captured by bistable pigments, Gq-coupled visual pigment and melanopsin, respectively, is also efficiently transduced to cellular light response. 37 Downstream of G-protein signaling rather than the pigment/G-protein step might contribute the high light-signaling efficiency in such bistable pigment-photoreceptor cells. 38 The difference in the amplitude of the lightinduced conformational change may also be related to the difference in photoreversibility between the two opsin-based pigments.…”

Section: Mutation Of Glu181 To His181mentioning

confidence: 99%

Evolution and diversity of opsins

Terakita

Kawano‐Yamashita

Koyanagi

2011

WIREs Membr Transp Signal

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Many animals capture light information via opsin-based pigments. Several thousands of opsins have been identified thus far and the opsin family is divided into eight groups. Members belonging to four out of the eight groups have been elucidated to couple to transducin, Go, Gs, and Gq, respectively, in photoreceptor cells. Accumulated evidence suggests a novel classification of the animal phototransductions, cyclic nucleotide signaling mediated by transducin, Go or Gs in ciliary photoreceptor cells and phosphoinositol signaling mediated by Gq in rhabdomeric photoreceptor cells. Varied opsin-based pigments are spectroscopically classified into two types, bleaching and bistable pigments; that is, the photoproduct of vertebrate visual pigments dissociates its chromophore retinal over time and bleaches, whereas most other opsin-based pigments convert to a stable photoproduct, which can revert to original dark state by subsequent light absorption. Mutational analyses of the both types of pigments implied that during molecular evolution of the vertebrae visual pigments, displacement of the counterion, important amino acid residue for visible light absorption of opsin-based pigment, resulted in not only unique bleaching property but also acquisition of red-sensitive visual pigment and higher G-protein activation ability generated by larger light-induced conformational change of the pigment. Interestingly, a bleaching pigment rhodopsin and parapinopsin, which closely relates to the vertebrate visual pigment but has a bistable nature, couple to visual arrestin and β arrestin, respectively, in the lamprey pineal organ, suggesting the bleaching property also might facilitate the evolution of visual arrestin which is specialized for vertebrate visual function. 

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Photon capture and signalling by melanopsin retinal ganglion cells

Cited by 253 publications

References 47 publications

Functional evaluation of iodoacetic acid induced photoreceptor degeneration in the cat

Functional evaluation of iodoacetic acid induced photoreceptor degeneration in the cat

Comparison of the isomerization mechanisms of human melanopsin and invertebrate and vertebrate rhodopsins

Evolution and diversity of opsins

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