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 |
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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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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.</description><identifier>ISSN: 0964-6906</identifier><identifier>ISSN: 1460-2083</identifier><identifier>EISSN: 1460-2083</identifier><identifier>DOI: 10.1093/hmg/ddad104</identifier><identifier>PMID: 37369021</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>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</subject><ispartof>Human molecular genetics, 2023-09, Vol.32 (19), p.2857-2871</ispartof><rights>The Author(s) 2023. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c413t-2f31297b3b60dc49d7df07f8a952683f5c9903ff0d0c46f7648a64fbaa6a0cba3</citedby><cites>FETCH-LOGICAL-c413t-2f31297b3b60dc49d7df07f8a952683f5c9903ff0d0c46f7648a64fbaa6a0cba3</cites><orcidid>0000-0002-8127-7145 ; 0000-0002-6642-8902 ; 0000-0002-3750-9615</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,1578,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37369021$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Myers, Scott J</creatorcontrib><creatorcontrib>Yuan, Hongjie</creatorcontrib><creatorcontrib>Perszyk, Riley E</creatorcontrib><creatorcontrib>Zhang, Jing</creatorcontrib><creatorcontrib>Kim, Sukhan</creatorcontrib><creatorcontrib>Nocilla, Kelsey A</creatorcontrib><creatorcontrib>Allen, James P</creatorcontrib><creatorcontrib>Bain, Jennifer M</creatorcontrib><creatorcontrib>Lemke, Johannes R</creatorcontrib><creatorcontrib>Lal, Dennis</creatorcontrib><creatorcontrib>Benke, Timothy A</creatorcontrib><creatorcontrib>Traynelis, Stephen F</creatorcontrib><title>Classification of missense variants in the N-methyl-d-aspartate receptor GRIN gene family as gain- or loss-of-function</title><title>Human molecular genetics</title><addtitle>Hum Mol Genet</addtitle><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.</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 ; 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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c413t-2f31297b3b60dc49d7df07f8a952683f5c9903ff0d0c46f7648a64fbaa6a0cba3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Humans</topic><topic>Models, Biological</topic><topic>Mutation, Missense - genetics</topic><topic>Nervous System Diseases - metabolism</topic><topic>Neurons - metabolism</topic><topic>Original</topic><topic>Receptors, N-Methyl-D-Aspartate - genetics</topic><topic>Receptors, N-Methyl-D-Aspartate - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Myers, Scott J</creatorcontrib><creatorcontrib>Yuan, Hongjie</creatorcontrib><creatorcontrib>Perszyk, Riley E</creatorcontrib><creatorcontrib>Zhang, Jing</creatorcontrib><creatorcontrib>Kim, Sukhan</creatorcontrib><creatorcontrib>Nocilla, Kelsey A</creatorcontrib><creatorcontrib>Allen, James P</creatorcontrib><creatorcontrib>Bain, Jennifer M</creatorcontrib><creatorcontrib>Lemke, Johannes R</creatorcontrib><creatorcontrib>Lal, Dennis</creatorcontrib><creatorcontrib>Benke, Timothy A</creatorcontrib><creatorcontrib>Traynelis, Stephen F</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><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>PubMed Central (Full Participant titles)</collection><jtitle>Human molecular genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Myers, Scott J</au><au>Yuan, Hongjie</au><au>Perszyk, Riley E</au><au>Zhang, Jing</au><au>Kim, Sukhan</au><au>Nocilla, Kelsey A</au><au>Allen, James P</au><au>Bain, Jennifer M</au><au>Lemke, Johannes R</au><au>Lal, Dennis</au><au>Benke, Timothy A</au><au>Traynelis, Stephen F</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Classification of missense variants in the N-methyl-d-aspartate receptor GRIN gene family as gain- or loss-of-function</atitle><jtitle>Human molecular genetics</jtitle><addtitle>Hum Mol Genet</addtitle><date>2023-09-16</date><risdate>2023</risdate><volume>32</volume><issue>19</issue><spage>2857</spage><epage>2871</epage><pages>2857-2871</pages><issn>0964-6906</issn><issn>1460-2083</issn><eissn>1460-2083</eissn><abstract>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.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>37369021</pmid><doi>10.1093/hmg/ddad104</doi><tpages>15</tpages><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><oa>free_for_read</oa></addata></record> |
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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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