TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells

Morgans, Catherine W.; Zhang, Jianmei; Jeffrey, Brett G.; Nelson, Steve; Burke, Neal S.; Duvoisin, Robert M.; Brown, R. Lane

doi:10.1073/pnas.0908711106

Cited by 269 publications

(331 citation statements)

References 29 publications

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“…As expected, application of LY341495 did not produce a detectable response in RBCs ( Fig. 2A, Left), as mGluR6 transduction is absent in this mouse model (2)(3)(4). Moreover, we were unable to detect responses to capsaicin in RBCs from trpm1 tm1Lex mice ( Fig.…”

Section: Resultsmentioning

confidence: 48%

“…Insight into the molecular identity of the transduction channel was gained from the observation that low levels of mRNA encoding the transient receptor potential ion channel TRPM1 was associated with a form of congenital stationary night blindness (CSNB) in a population of Appaloosa horses (1). Soon after, it was shown that ON bipolar cell function was absent or severely impaired in a mouse model that lacked TRPM1 expression (2-4), although there is evidence that one or more classes of cone-driven ON bipolar cells may use an additional channel (3). Mutations in TRPM1 have now been positively linked to CSNB in humans as well (5)(6)(7).…”

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confidence: 99%

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G-protein–mediated inhibition of the Trp channel TRPM1 requires the Gβγ dimer

Shen

Rampino

Carroll

et al. 2012

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

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ON bipolar cells are critical for the function of the ON pathway in the visual system. They express a metabotropic glutamate receptor (mGluR6) that, when activated, couples to the G o class of G protein. The channel that is primarily responsible for the synaptic response has been recently identified as the transient receptor potential cation channel subfamily M member 1 (TRPM1); TRPM1 is negatively coupled to the mGluR6/Go cascade such that activation of the cascade results in closure of the channel. Light indirectly opens TRPM1 by reducing transmitter release from presynaptic photoreceptors, resulting in a decrease in mGluR6 activation. Conversely, in the dark, binding of synaptic glutamate to mGluR6 inhibits TRPM1 current. Closure of TRPM1 by G-protein activation in the dark is a critical step in the process of ON bipolar cell signal transduction, but the precise pathway linking these two events is not understood. To address this question, we measured TRPM1 activity in retinal bipolar cells, in human ependymal melanocytes (HEMs) that endogenously express TRPM1, and in HEK293 cells transfected with TRPM1. Dialysis of the Gβγ subunit dimer, but not Gα o , closed TRPM1 channels in every cell type that we tested. In addition, activation of an endogenous G-protein-coupled receptor pathway in HEK293 cells that releases Gβγ without activating Go protein also closed TRPM1 channels. These results suggest a model in which the Gβγ dimer that is released as a result of the dissociation from Gα o upon activation of mGluR6 closes the TRPM1 channel, perhaps via a direct interaction. patch clamp | calcium imaging R etinal ON bipolar cells are connected to photoreceptors through a sign-inverting synapse. At this synapse, glutamate binds to the metabotropic glutamate receptor mGluR6, which couples to the closure of a cation-selective transduction channel. Insight into the molecular identity of the transduction channel was gained from the observation that low levels of mRNA encoding the transient receptor potential ion channel TRPM1 was associated with a form of congenital stationary night blindness (CSNB) in a population of Appaloosa horses (1). Soon after, it was shown that ON bipolar cell function was absent or severely impaired in a mouse model that lacked TRPM1 expression (2-4), although there is evidence that one or more classes of cone-driven ON bipolar cells may use an additional channel (3). Mutations in TRPM1 have now been positively linked to CSNB in humans as well (5-7). Taken together, studies of mouse, horse, and human provide convincing evidence that the ON bipolar cell transduction channel is composed of TRPM1, either alone or in conjunction with other channels. However, all these studies do not provide insight into the mechanism by which activation of mGluR6 leads to closure of TRPM1.The metabotropic receptor mGluR6 preferentially couples to the G o class of G protein, both in bipolar cells (8, 9) and expression systems (10, 11). Activation of mGluR6 and, correspondingly, Go, results in closure of TRPM1. However...

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Section: Resultsmentioning

confidence: 48%

mentioning

confidence: 99%

G-protein–mediated inhibition of the Trp channel TRPM1 requires the Gβγ dimer

Shen

Rampino

Carroll

et al. 2012

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

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“…These cells express the metabotropic glutamate receptor, mGluR6 [47 -51]. Activation of mGluR6 by glutamate leads, via an intracellular cascade, to the closure of TrpM1 channels on the dendrites of ON-BCs [52][53][54]. Glutamate induces a hyperpolarization of these neurons.…”

Section: General Neuronal Processing In the Outer Plexiform Layermentioning

confidence: 99%

Teleost polarization vision: how it might work and what it might be good for

Kamermans

Hawryshyn

2011

Phil. Trans. R. Soc. B

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In this review, we will discuss the recent literature on fish polarization vision and we will present a model on how the retina processes polarization signals. The model is based on a general retinalprocessing scheme and will be compared with the available electrophysiological data on polarization processing in the retina. The results of this model will help illustrate the functional significance of polarization vision for both feeding behaviour and navigation. First, we examine the linkage between structure and function in polarization vision in general.

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“…In addition, RPRG and TRPM1 exhibited upregulation in domestic chickens. Both genes play important roles in vision [50,51], for instance, RPGR encodes a retinitis pigmentosa GTPase regulator and overexpression of a RPGR transcript leads to severe photoreceptor degeneration in mice [52].…”

Section: Differential Expression Of Psgs In the Retina Between Domestmentioning

confidence: 99%

Positive selection rather than relaxation of functional constraint drives the evolution of vision during chicken domestication

Wang

Zhang

et al. 2016

Cell Res

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As noted by Darwin, chickens have the greatest phenotypic diversity of all birds, but an interesting evolutionary difference between domestic chickens and their wild ancestor, the Red Junglefowl, is their comparatively weaker vision. Existing theories suggest that diminished visual prowess among domestic chickens reflect changes driven by the relaxation of functional constraints on vision, but the evidence identifying the underlying genetic mechanisms responsible for this change has not been definitively characterized. Here, a genome-wide analysis of the domestic chicken and Red Junglefowl genomes showed significant enrichment for positively selected genes involved in the development of vision. There were significant differences between domestic chickens and their wild ancestors regarding the level of mRNA expression for these genes in the retina. Numerous additional genes involved in the development of vision also showed significant differences in mRNA expression between domestic chickens and their wild ancestors, particularly for genes associated with phototransduction and photoreceptor development, such as RHO (rhodopsin), GUCA1A, PDE6B and NR2E3. Finally, we characterized the potential role of the VIT gene in vision, which experienced positive selection and downregulated expression in the retina of the village chicken. Overall, our results suggest that positive selection, rather than relaxation of purifying selection, contributed to the evolution of vision in domestic chickens. The progenitors of domestic chickens harboring weaker vision may have showed a reduced fear response and vigilance, making them easier to be unconsciously selected and/or domesticated.

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TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells

Cited by 269 publications

References 29 publications

G-protein–mediated inhibition of the Trp channel TRPM1 requires the Gβγ dimer

G-protein–mediated inhibition of the Trp channel TRPM1 requires the Gβγ dimer

Teleost polarization vision: how it might work and what it might be good for

Positive selection rather than relaxation of functional constraint drives the evolution of vision during chicken domestication

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