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Melanopsin-expressing amphioxus photoreceptors transduce light via a phospholipase C signaling cascade
Authors
A Fein
A Hartwick
+56 more
A Terakita
AC Newton
AK Thompson
Camila Pulido
D Arendt
D Berson
DC Plachetzki
DM Graham
E Nasi
EC Johnson
EE Fesenko
EJ Warren
Enrico Nasi
Gerardo Malagón
HG Khorana
I Provencio
J Bacigalupo
J Fahrenkrug
JE Brown
JG Bilmen
JK Acharya
Juan Manuel Angueyra
K Nagy
LA Newman
LV Salvini-Plawen
M Estacion
M Koyanagi
M Koyanagi
Maria del Pilar Gomez
MP Gomez
MP Gomez
MTH Do
NH Putnam
P Raghu
PR Robinson
RB Gregory
RJ Smith
RM Eakin
S Chyb
S Hattar
S Ruiz
S Sekaran
S Sekaran
SK Panda
SN Peirson
Steven Barnes
T Maruyama
T Nakamura
T Nakao
T Watanabe
T Xue
TD Hill
WJ Gehring
WJ Gehring
X Qiu
Z Melyan
Publication date
3 January 2012
Publisher
'Public Library of Science (PLoS)'
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Abstract
© The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 7 (2012): e29813, doi:10.1371/journal.pone.0029813.Melanopsin, the receptor molecule that underlies light sensitivity in mammalian ‘circadian’ receptors, is homologous to invertebrate rhodopsins and has been proposed to operate via a similar signaling pathway. Its downstream effectors, however, remain elusive. Melanopsin also expresses in two distinct light-sensitive cell types in the neural tube of amphioxus. This organism is the most basal extant chordate and can help outline the evolutionary history of different photoreceptor lineages and their transduction mechanisms; moreover, isolated amphioxus photoreceptors offer unique advantages, because they are unambiguously identifiable and amenable to single-cell physiological assays. In the present study whole-cell patch clamp recording, pharmacological manipulations, and immunodetection were utilized to investigate light transduction in amphioxus photoreceptors. A Gq was identified and selectively localized to the photosensitive microvillar membrane, while the pivotal role of phospholipase C was established pharmacologically. The photocurrent was profoundly depressed by IP3 receptor antagonists, highlighting the importance of IP3 receptors in light signaling. By contrast, surrogates of diacylglycerol (DAG), as well as poly-unsaturated fatty acids failed to activate a membrane conductance or to alter the light response. The results strengthen the notion that calcium released from the ER via IP3-sensitive channels may fulfill a key role in conveying - directly or indirectly - the melanopsin-initiated light signal to the photoconductance; moreover, they challenge the dogma that microvillar photoreceptors and phoshoinositide-based light transduction are a prerogative of invertebrate eyes.This work was supported by the National Science Foundation of the USA (grant 0918930)
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