LRIT3 Differentially Affects Connectivity and Synaptic Transmission of Cones to ON- and OFF-Bipolar Cells

Mutations in LRIT3 lead to complete congenital stationary night blindness (cCSNB). Using a cCSNB mouse model lacking Lrit3 (nob6), we recently have shown that LRIT3 has a role in the correct localization of TRPM1 (transient receptor potential melastatin 1) to the dendritic tips of ON-bipolar cells (...

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Veröffentlicht in:Investigative ophthalmology & visual science 2017-03, Vol.58 (3), p.1768-1778
Hauptverfasser: Neuillé, Marion, Cao, Yan, Caplette, Romain, Guerrero-Given, Debbie, Thomas, Connon, Kamasawa, Naomi, Sahel, José-Alain, Hamel, Christian P, Audo, Isabelle, Picaud, Serge, Martemyanov, Kirill A, Zeitz, Christina
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container_issue 3
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container_title Investigative ophthalmology & visual science
container_volume 58
creator Neuillé, Marion
Cao, Yan
Caplette, Romain
Guerrero-Given, Debbie
Thomas, Connon
Kamasawa, Naomi
Sahel, José-Alain
Hamel, Christian P
Audo, Isabelle
Picaud, Serge
Martemyanov, Kirill A
Zeitz, Christina
description Mutations in LRIT3 lead to complete congenital stationary night blindness (cCSNB). Using a cCSNB mouse model lacking Lrit3 (nob6), we recently have shown that LRIT3 has a role in the correct localization of TRPM1 (transient receptor potential melastatin 1) to the dendritic tips of ON-bipolar cells (BCs), contacting both rod and cone photoreceptors. Furthermore, postsynaptic clustering of other mGluR6 cascade components is selectively eliminated at the dendritic tips of cone ON-BCs. The purpose of this study was to further define the role of LRIT3 in structural and functional organization of cone synapses. Exhaustive electroretinogram analysis was performed in a patient with LRIT3 mutations. Multielectrode array recordings were performed at the level of retinal ganglion cells in nob6 mice. Targeting of GluR1 and GluR5 at the dendritic tips of OFF-BCs in nob6 retinas was assessed by immunostaining and confocal microscopy. The ultrastructure of photoreceptor synapses was evaluated by electron microscopy in nob6 mice. The patient with LRIT3 mutations had a selective ON-BC dysfunction with relatively preserved OFF-BC responses. In nob6 mice, complete lack of ON-pathway function with robust, yet altered signaling processing in OFF-pathways was detected. Consistent with these observations, molecules essential for the OFF-BC signaling were normally targeted to the synapse. Finally, synaptic contacts made by ON-BC but not OFF-BC neurons with the cone pedicles were disorganized without ultrastructural alterations in cone terminals, horizontal cell processes, or synaptic ribbons. These results suggest that LRIT3 is likely involved in coordination of the transsynaptic communication between cones and ON-BCs during synapse formation and function.
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Using a cCSNB mouse model lacking Lrit3 (nob6), we recently have shown that LRIT3 has a role in the correct localization of TRPM1 (transient receptor potential melastatin 1) to the dendritic tips of ON-bipolar cells (BCs), contacting both rod and cone photoreceptors. Furthermore, postsynaptic clustering of other mGluR6 cascade components is selectively eliminated at the dendritic tips of cone ON-BCs. The purpose of this study was to further define the role of LRIT3 in structural and functional organization of cone synapses. Exhaustive electroretinogram analysis was performed in a patient with LRIT3 mutations. Multielectrode array recordings were performed at the level of retinal ganglion cells in nob6 mice. Targeting of GluR1 and GluR5 at the dendritic tips of OFF-BCs in nob6 retinas was assessed by immunostaining and confocal microscopy. The ultrastructure of photoreceptor synapses was evaluated by electron microscopy in nob6 mice. The patient with LRIT3 mutations had a selective ON-BC dysfunction with relatively preserved OFF-BC responses. In nob6 mice, complete lack of ON-pathway function with robust, yet altered signaling processing in OFF-pathways was detected. Consistent with these observations, molecules essential for the OFF-BC signaling were normally targeted to the synapse. Finally, synaptic contacts made by ON-BC but not OFF-BC neurons with the cone pedicles were disorganized without ultrastructural alterations in cone terminals, horizontal cell processes, or synaptic ribbons. 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Using a cCSNB mouse model lacking Lrit3 (nob6), we recently have shown that LRIT3 has a role in the correct localization of TRPM1 (transient receptor potential melastatin 1) to the dendritic tips of ON-bipolar cells (BCs), contacting both rod and cone photoreceptors. Furthermore, postsynaptic clustering of other mGluR6 cascade components is selectively eliminated at the dendritic tips of cone ON-BCs. The purpose of this study was to further define the role of LRIT3 in structural and functional organization of cone synapses. Exhaustive electroretinogram analysis was performed in a patient with LRIT3 mutations. Multielectrode array recordings were performed at the level of retinal ganglion cells in nob6 mice. Targeting of GluR1 and GluR5 at the dendritic tips of OFF-BCs in nob6 retinas was assessed by immunostaining and confocal microscopy. The ultrastructure of photoreceptor synapses was evaluated by electron microscopy in nob6 mice. The patient with LRIT3 mutations had a selective ON-BC dysfunction with relatively preserved OFF-BC responses. In nob6 mice, complete lack of ON-pathway function with robust, yet altered signaling processing in OFF-pathways was detected. Consistent with these observations, molecules essential for the OFF-BC signaling were normally targeted to the synapse. Finally, synaptic contacts made by ON-BC but not OFF-BC neurons with the cone pedicles were disorganized without ultrastructural alterations in cone terminals, horizontal cell processes, or synaptic ribbons. 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Cao, Yan ; Caplette, Romain ; Guerrero-Given, Debbie ; Thomas, Connon ; Kamasawa, Naomi ; Sahel, José-Alain ; Hamel, Christian P ; Audo, Isabelle ; Picaud, Serge ; Martemyanov, Kirill A ; Zeitz, Christina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c487t-db2530a76df20fd9aa58dba8623830c9266456b4c5075fc18adf384a8946f1273</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Dendrites - metabolism</topic><topic>Dendrites - ultrastructure</topic><topic>DNA - genetics</topic><topic>DNA Mutational Analysis</topic><topic>Electroretinography</topic><topic>Eye Diseases, Hereditary - genetics</topic><topic>Eye Diseases, Hereditary - metabolism</topic><topic>Eye Diseases, Hereditary - pathology</topic><topic>Female</topic><topic>Genetic Diseases, X-Linked - genetics</topic><topic>Genetic Diseases, X-Linked - metabolism</topic><topic>Genetic Diseases, X-Linked - pathology</topic><topic>Human health and pathology</topic><topic>Humans</topic><topic>Immunohistochemistry</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - metabolism</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Microscopy, Electron</topic><topic>Mutation</topic><topic>Myopia - genetics</topic><topic>Myopia - metabolism</topic><topic>Myopia - pathology</topic><topic>Night Blindness - genetics</topic><topic>Night Blindness - metabolism</topic><topic>Night Blindness - pathology</topic><topic>Retinal Bipolar Cells - metabolism</topic><topic>Retinal Bipolar Cells - ultrastructure</topic><topic>Retinal Cone Photoreceptor Cells - metabolism</topic><topic>Retinal Cone Photoreceptor Cells - ultrastructure</topic><topic>Retrospective Studies</topic><topic>Sensory Organs</topic><topic>Synapses - metabolism</topic><topic>Synapses - ultrastructure</topic><topic>Synaptic Transmission - genetics</topic><topic>Visual Neuroscience</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Neuillé, Marion</creatorcontrib><creatorcontrib>Cao, Yan</creatorcontrib><creatorcontrib>Caplette, Romain</creatorcontrib><creatorcontrib>Guerrero-Given, Debbie</creatorcontrib><creatorcontrib>Thomas, Connon</creatorcontrib><creatorcontrib>Kamasawa, Naomi</creatorcontrib><creatorcontrib>Sahel, José-Alain</creatorcontrib><creatorcontrib>Hamel, Christian P</creatorcontrib><creatorcontrib>Audo, Isabelle</creatorcontrib><creatorcontrib>Picaud, Serge</creatorcontrib><creatorcontrib>Martemyanov, Kirill A</creatorcontrib><creatorcontrib>Zeitz, Christina</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Investigative ophthalmology &amp; 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The patient with LRIT3 mutations had a selective ON-BC dysfunction with relatively preserved OFF-BC responses. In nob6 mice, complete lack of ON-pathway function with robust, yet altered signaling processing in OFF-pathways was detected. Consistent with these observations, molecules essential for the OFF-BC signaling were normally targeted to the synapse. Finally, synaptic contacts made by ON-BC but not OFF-BC neurons with the cone pedicles were disorganized without ultrastructural alterations in cone terminals, horizontal cell processes, or synaptic ribbons. 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subjects Animals
Dendrites - metabolism
Dendrites - ultrastructure
DNA - genetics
DNA Mutational Analysis
Electroretinography
Eye Diseases, Hereditary - genetics
Eye Diseases, Hereditary - metabolism
Eye Diseases, Hereditary - pathology
Female
Genetic Diseases, X-Linked - genetics
Genetic Diseases, X-Linked - metabolism
Genetic Diseases, X-Linked - pathology
Human health and pathology
Humans
Immunohistochemistry
Life Sciences
Male
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mice
Mice, Knockout
Microscopy, Electron
Mutation
Myopia - genetics
Myopia - metabolism
Myopia - pathology
Night Blindness - genetics
Night Blindness - metabolism
Night Blindness - pathology
Retinal Bipolar Cells - metabolism
Retinal Bipolar Cells - ultrastructure
Retinal Cone Photoreceptor Cells - metabolism
Retinal Cone Photoreceptor Cells - ultrastructure
Retrospective Studies
Sensory Organs
Synapses - metabolism
Synapses - ultrastructure
Synaptic Transmission - genetics
Visual Neuroscience
Young Adult
title LRIT3 Differentially Affects Connectivity and Synaptic Transmission of Cones to ON- and OFF-Bipolar Cells
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