Classification of missense variants in the N-methyl-d-aspartate receptor GRIN gene family as gain- or loss-of-function

Abstract Advances in sequencing technology have generated a large amount of genetic data from patients with neurological conditions. These data have provided diagnosis of many rare diseases, including a number of pathogenic de novo missense variants in GRIN genes encoding N-methyl-d-aspartate recept...

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Veröffentlicht in:Human molecular genetics 2023-09, Vol.32 (19), p.2857-2871
Hauptverfasser: Myers, Scott J, Yuan, Hongjie, Perszyk, Riley E, Zhang, Jing, Kim, Sukhan, Nocilla, Kelsey A, Allen, James P, Bain, Jennifer M, Lemke, Johannes R, Lal, Dennis, Benke, Timothy A, Traynelis, Stephen F
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container_end_page 2871
container_issue 19
container_start_page 2857
container_title Human molecular genetics
container_volume 32
creator Myers, Scott J
Yuan, Hongjie
Perszyk, Riley E
Zhang, Jing
Kim, Sukhan
Nocilla, Kelsey A
Allen, James P
Bain, Jennifer M
Lemke, Johannes R
Lal, Dennis
Benke, Timothy A
Traynelis, Stephen F
description Abstract Advances in sequencing technology have generated a large amount of genetic data from patients with neurological conditions. These data have provided diagnosis of many rare diseases, including a number of pathogenic de novo missense variants in GRIN genes encoding N-methyl-d-aspartate receptors (NMDARs). To understand the ramifications for neurons and brain circuits affected by rare patient variants, functional analysis of the variant receptor is necessary in model systems. For NMDARs, this functional analysis needs to assess multiple properties in order to understand how variants could impact receptor function in neurons. One can then use these data to determine whether the overall actions will increase or decrease NMDAR-mediated charge transfer. Here, we describe an analytical and comprehensive framework by which to categorize GRIN variants as either gain-of-function (GoF) or loss-of-function (LoF) and apply this approach to GRIN2B variants identified in patients and the general population. This framework draws on results from six different assays that assess the impact of the variant on NMDAR sensitivity to agonists and endogenous modulators, trafficking to the plasma membrane, response time course and channel open probability. We propose to integrate data from multiple in vitro assays to arrive at a variant classification, and suggest threshold levels that guide confidence. The data supporting GoF and LoF determination are essential to assessing pathogenicity and patient stratification for clinical trials as personalized pharmacological and genetic agents that can enhance or reduce receptor function are advanced. This approach to functional variant classification can generalize to other disorders associated with missense variants.
doi_str_mv 10.1093/hmg/ddad104
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These data have provided diagnosis of many rare diseases, including a number of pathogenic de novo missense variants in GRIN genes encoding N-methyl-d-aspartate receptors (NMDARs). To understand the ramifications for neurons and brain circuits affected by rare patient variants, functional analysis of the variant receptor is necessary in model systems. For NMDARs, this functional analysis needs to assess multiple properties in order to understand how variants could impact receptor function in neurons. One can then use these data to determine whether the overall actions will increase or decrease NMDAR-mediated charge transfer. Here, we describe an analytical and comprehensive framework by which to categorize GRIN variants as either gain-of-function (GoF) or loss-of-function (LoF) and apply this approach to GRIN2B variants identified in patients and the general population. This framework draws on results from six different assays that assess the impact of the variant on NMDAR sensitivity to agonists and endogenous modulators, trafficking to the plasma membrane, response time course and channel open probability. We propose to integrate data from multiple in vitro assays to arrive at a variant classification, and suggest threshold levels that guide confidence. The data supporting GoF and LoF determination are essential to assessing pathogenicity and patient stratification for clinical trials as personalized pharmacological and genetic agents that can enhance or reduce receptor function are advanced. 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This framework draws on results from six different assays that assess the impact of the variant on NMDAR sensitivity to agonists and endogenous modulators, trafficking to the plasma membrane, response time course and channel open probability. We propose to integrate data from multiple in vitro assays to arrive at a variant classification, and suggest threshold levels that guide confidence. The data supporting GoF and LoF determination are essential to assessing pathogenicity and patient stratification for clinical trials as personalized pharmacological and genetic agents that can enhance or reduce receptor function are advanced. This approach to functional variant classification can generalize to other disorders associated with missense variants.</description><subject>Humans</subject><subject>Models, Biological</subject><subject>Mutation, Missense - genetics</subject><subject>Nervous System Diseases - metabolism</subject><subject>Neurons - metabolism</subject><subject>Original</subject><subject>Receptors, N-Methyl-D-Aspartate - genetics</subject><subject>Receptors, N-Methyl-D-Aspartate - metabolism</subject><issn>0964-6906</issn><issn>1460-2083</issn><issn>1460-2083</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kdFrFDEQxoMo9qw--S55EkHSTja57O6TlENroVQo9TnMZpO7yG6yJtmD--_dcmfRlz4NzPz4vpn5CHnP4YJDKy534_ay77HnIF-QFZcKWAWNeElW0CrJVAvqjLzJ-RcAV1LUr8mZqMXSrviK7DcD5uydN1h8DDQ6OvqcbciW7jF5DCVTH2jZWXrHRlt2h4H1DPOEqWCxNFljpxITvb6_uaNbGyx1OPrhQDHTLfrA6DIcYs4sOubmYB593pJXDods353qOfn57evD5ju7_XF9s7m6ZUZyUVjlBK_auhOdgt7Itq97B7VrsF1XqhFubdoWhHPQg5HK1Uo2qKTrEBWC6VCcky9H3WnuRtsbG0rCQU_Jj5gOOqLX_0-C3-lt3GsOa2hAtIvCp5NCir9nm4te_mPsMGCwcc66agSoupINX9DPR9Sk5dxk3ZMPB_0YlV6i0qeoFvrDv6s9sX-zWYCPRyDO07NKfwAOqZ--</recordid><startdate>20230916</startdate><enddate>20230916</enddate><creator>Myers, Scott J</creator><creator>Yuan, Hongjie</creator><creator>Perszyk, Riley E</creator><creator>Zhang, Jing</creator><creator>Kim, Sukhan</creator><creator>Nocilla, Kelsey A</creator><creator>Allen, James P</creator><creator>Bain, Jennifer M</creator><creator>Lemke, Johannes R</creator><creator>Lal, Dennis</creator><creator>Benke, Timothy A</creator><creator>Traynelis, Stephen F</creator><general>Oxford University Press</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8127-7145</orcidid><orcidid>https://orcid.org/0000-0002-6642-8902</orcidid><orcidid>https://orcid.org/0000-0002-3750-9615</orcidid></search><sort><creationdate>20230916</creationdate><title>Classification of missense variants in the N-methyl-d-aspartate receptor GRIN gene family as gain- or loss-of-function</title><author>Myers, Scott J ; 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subjects Humans
Models, Biological
Mutation, Missense - genetics
Nervous System Diseases - metabolism
Neurons - metabolism
Original
Receptors, N-Methyl-D-Aspartate - genetics
Receptors, N-Methyl-D-Aspartate - metabolism
title Classification of missense variants in the N-methyl-d-aspartate receptor GRIN gene family as gain- or loss-of-function
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