Morphological profiling of human T and NK lymphocytes by high-content cell imaging
The immunological synapse is a complex structure that decodes stimulatory signals into adapted lymphocyte responses. It is a unique window to monitor lymphocyte activity because of development of systematic quantitative approaches. Here we demonstrate the applicability of high-content imaging to hum...
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| Veröffentlicht in: | Cell reports (Cambridge) 2021-07, Vol.36 (1), p.109318-109318, Article 109318 |
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| creator | German, Yolla Vulliard, Loan Kamnev, Anton Pfajfer, Laurène Huemer, Jakob Mautner, Anna-Katharina Rubio, Aude Kalinichenko, Artem Boztug, Kaan Ferrand, Audrey Menche, Jörg Dupré, Loïc |
| description | The immunological synapse is a complex structure that decodes stimulatory signals into adapted lymphocyte responses. It is a unique window to monitor lymphocyte activity because of development of systematic quantitative approaches. Here we demonstrate the applicability of high-content imaging to human T and natural killer (NK) cells and develop a pipeline for unbiased analysis of high-definition morphological profiles. Our approach reveals how distinct facets of actin cytoskeleton remodeling shape immunological synapse architecture and affect lytic granule positioning. Morphological profiling of CD8+ T cells from immunodeficient individuals allows discrimination of the roles of the ARP2/3 subunit ARPC1B and the ARP2/3 activator Wiskott-Aldrich syndrome protein (WASP) in immunological synapse assembly. Single-cell analysis further identifies uncoupling of lytic granules and F-actin radial distribution in ARPC1B-deficient lymphocytes. Our study provides a foundation for development of morphological profiling as a scalable approach to monitor primary lymphocyte responsiveness and to identify complex aspects of lymphocyte micro-architecture.
[Display omitted]
•Cytotoxic lymphocytes can be profiled in depth using high-content imaging•Morphological changes are identified with dedicated analytical tools•Distinct immunological synapse alterations in ARPC1B- and WASP-deficient T cells•3D distribution of lytic granules is impaired in ARPC1B-deficient CD8+ T cells
German et al. provide a workflow to study activation of cytotoxic T and NK lymphocytes by high-content confocal microscopy. Images are analyzed to characterize morphological variation in immunological synapses induced by actin compounds in primary cells as well as in CD8+ T cells derived from ARPC1B- and WASP-deficient individuals. |
| doi_str_mv | 10.1016/j.celrep.2021.109318 |
| format | Article |
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[Display omitted]
•Cytotoxic lymphocytes can be profiled in depth using high-content imaging•Morphological changes are identified with dedicated analytical tools•Distinct immunological synapse alterations in ARPC1B- and WASP-deficient T cells•3D distribution of lytic granules is impaired in ARPC1B-deficient CD8+ T cells
German et al. provide a workflow to study activation of cytotoxic T and NK lymphocytes by high-content confocal microscopy. Images are analyzed to characterize morphological variation in immunological synapses induced by actin compounds in primary cells as well as in CD8+ T cells derived from ARPC1B- and WASP-deficient individuals.</description><identifier>ISSN: 2211-1247</identifier><identifier>EISSN: 2211-1247</identifier><identifier>DOI: 10.1016/j.celrep.2021.109318</identifier><identifier>PMID: 34233185</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>actin cytoskeleton ; Actin-Related Protein 2-3 Complex - deficiency ; Actin-Related Protein 2-3 Complex - metabolism ; Adolescent ; ARPC1B deficiency ; Biotechnology ; CD8-Positive T-Lymphocytes - cytology ; CD8-Positive T-Lymphocytes - drug effects ; Cell Line ; Cell Shape - drug effects ; Cellular Biology ; Cytoskeleton - drug effects ; Cytoskeleton - metabolism ; cytotoxic T lymphocytes ; Exocytosis - drug effects ; high-content imaging ; Human health and pathology ; Humans ; Imaging, Three-Dimensional ; immunological synapse ; Immunological Synapses - drug effects ; Immunological Synapses - metabolism ; Killer Cells, Natural - cytology ; Killer Cells, Natural - drug effects ; Killer Cells, Natural - metabolism ; Life Sciences ; lytic granules ; Male ; morphological profiling ; NK cells ; Organoselenium Compounds - pharmacology ; Organosilicon Compounds - pharmacology ; Single-Cell Analysis ; T-Lymphocytes - cytology ; T-Lymphocytes - drug effects ; T-Lymphocytes - metabolism ; Thiones - pharmacology ; Uracil - analogs & derivatives ; Uracil - pharmacology ; WASP deficiency ; Wiskott-Aldrich Syndrome Protein - deficiency ; Wiskott-Aldrich Syndrome Protein - metabolism</subject><ispartof>Cell reports (Cambridge), 2021-07, Vol.36 (1), p.109318-109318, Article 109318</ispartof><rights>2021 The Author(s)</rights><rights>Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><rights>Attribution - NonCommercial - NoDerivatives</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-64ec0e4aec8e862da8c06909bf8140d40dd9c408c821980c42d81c81f0cef7663</citedby><cites>FETCH-LOGICAL-c442t-64ec0e4aec8e862da8c06909bf8140d40dd9c408c821980c42d81c81f0cef7663</cites><orcidid>0000-0002-2260-4935 ; 0000-0002-7020-7256 ; 0000-0003-0471-4601 ; 0000-0002-6279-3486 ; 0000-0002-7278-6503 ; 0000-0001-8387-9185</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,864,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34233185$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-03335500$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>German, Yolla</creatorcontrib><creatorcontrib>Vulliard, Loan</creatorcontrib><creatorcontrib>Kamnev, Anton</creatorcontrib><creatorcontrib>Pfajfer, Laurène</creatorcontrib><creatorcontrib>Huemer, Jakob</creatorcontrib><creatorcontrib>Mautner, Anna-Katharina</creatorcontrib><creatorcontrib>Rubio, Aude</creatorcontrib><creatorcontrib>Kalinichenko, Artem</creatorcontrib><creatorcontrib>Boztug, Kaan</creatorcontrib><creatorcontrib>Ferrand, Audrey</creatorcontrib><creatorcontrib>Menche, Jörg</creatorcontrib><creatorcontrib>Dupré, Loïc</creatorcontrib><title>Morphological profiling of human T and NK lymphocytes by high-content cell imaging</title><title>Cell reports (Cambridge)</title><addtitle>Cell Rep</addtitle><description>The immunological synapse is a complex structure that decodes stimulatory signals into adapted lymphocyte responses. It is a unique window to monitor lymphocyte activity because of development of systematic quantitative approaches. Here we demonstrate the applicability of high-content imaging to human T and natural killer (NK) cells and develop a pipeline for unbiased analysis of high-definition morphological profiles. Our approach reveals how distinct facets of actin cytoskeleton remodeling shape immunological synapse architecture and affect lytic granule positioning. Morphological profiling of CD8+ T cells from immunodeficient individuals allows discrimination of the roles of the ARP2/3 subunit ARPC1B and the ARP2/3 activator Wiskott-Aldrich syndrome protein (WASP) in immunological synapse assembly. Single-cell analysis further identifies uncoupling of lytic granules and F-actin radial distribution in ARPC1B-deficient lymphocytes. Our study provides a foundation for development of morphological profiling as a scalable approach to monitor primary lymphocyte responsiveness and to identify complex aspects of lymphocyte micro-architecture.
[Display omitted]
•Cytotoxic lymphocytes can be profiled in depth using high-content imaging•Morphological changes are identified with dedicated analytical tools•Distinct immunological synapse alterations in ARPC1B- and WASP-deficient T cells•3D distribution of lytic granules is impaired in ARPC1B-deficient CD8+ T cells
German et al. provide a workflow to study activation of cytotoxic T and NK lymphocytes by high-content confocal microscopy. Images are analyzed to characterize morphological variation in immunological synapses induced by actin compounds in primary cells as well as in CD8+ T cells derived from ARPC1B- and WASP-deficient individuals.</description><subject>actin cytoskeleton</subject><subject>Actin-Related Protein 2-3 Complex - deficiency</subject><subject>Actin-Related Protein 2-3 Complex - metabolism</subject><subject>Adolescent</subject><subject>ARPC1B deficiency</subject><subject>Biotechnology</subject><subject>CD8-Positive T-Lymphocytes - cytology</subject><subject>CD8-Positive T-Lymphocytes - drug effects</subject><subject>Cell Line</subject><subject>Cell Shape - drug effects</subject><subject>Cellular Biology</subject><subject>Cytoskeleton - drug effects</subject><subject>Cytoskeleton - metabolism</subject><subject>cytotoxic T lymphocytes</subject><subject>Exocytosis - drug effects</subject><subject>high-content imaging</subject><subject>Human health and pathology</subject><subject>Humans</subject><subject>Imaging, Three-Dimensional</subject><subject>immunological synapse</subject><subject>Immunological Synapses - drug effects</subject><subject>Immunological Synapses - metabolism</subject><subject>Killer Cells, Natural - cytology</subject><subject>Killer Cells, Natural - drug effects</subject><subject>Killer Cells, Natural - metabolism</subject><subject>Life Sciences</subject><subject>lytic granules</subject><subject>Male</subject><subject>morphological profiling</subject><subject>NK cells</subject><subject>Organoselenium Compounds - pharmacology</subject><subject>Organosilicon Compounds - pharmacology</subject><subject>Single-Cell Analysis</subject><subject>T-Lymphocytes - cytology</subject><subject>T-Lymphocytes - drug effects</subject><subject>T-Lymphocytes - metabolism</subject><subject>Thiones - pharmacology</subject><subject>Uracil - analogs & derivatives</subject><subject>Uracil - pharmacology</subject><subject>WASP deficiency</subject><subject>Wiskott-Aldrich Syndrome Protein - deficiency</subject><subject>Wiskott-Aldrich Syndrome Protein - metabolism</subject><issn>2211-1247</issn><issn>2211-1247</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kNFLHDEQxoNUVNT_QCSP7cNeM9lczL4URNoqngqizyE3O3ubY3dzTfaE---bY1X61BDIMPy--SYfYxcgZiBAf1_PkLpIm5kUEnKrKsEcsBMpAQqQ6urLP_UxO09pLfLRAqBSR-y4VLLMivkJe34IcdOGLqw8uo5vYmh854cVDw1vt70b-At3Q80f73m36zOJu5ESX-5461dtgWEYaRh53qbjvnerLD1jh43rEp2_v6fs9dfPl5vbYvH0--7melGgUnIstCIUpByhIaNl7QwKXYlq2RhQos63rlAJg0ZCZQQqWRtAA41Aaq60Lk_Zt2lu6zq7idk97mxw3t5eL-y-J8qynM-FeIPMfp3Y_ME_W0qj7X3aL-0GCttk5VxVugJdyoyqCcUYUorUfM4GYffh27Wdwrf78O0UfpZdvjtslz3Vn6KPqDPwYwIoZ_LmKdqEngak2kfC0dbB_9_hL1K2lWA</recordid><startdate>20210706</startdate><enddate>20210706</enddate><creator>German, Yolla</creator><creator>Vulliard, Loan</creator><creator>Kamnev, Anton</creator><creator>Pfajfer, Laurène</creator><creator>Huemer, Jakob</creator><creator>Mautner, Anna-Katharina</creator><creator>Rubio, Aude</creator><creator>Kalinichenko, Artem</creator><creator>Boztug, Kaan</creator><creator>Ferrand, Audrey</creator><creator>Menche, Jörg</creator><creator>Dupré, Loïc</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</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>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-2260-4935</orcidid><orcidid>https://orcid.org/0000-0002-7020-7256</orcidid><orcidid>https://orcid.org/0000-0003-0471-4601</orcidid><orcidid>https://orcid.org/0000-0002-6279-3486</orcidid><orcidid>https://orcid.org/0000-0002-7278-6503</orcidid><orcidid>https://orcid.org/0000-0001-8387-9185</orcidid></search><sort><creationdate>20210706</creationdate><title>Morphological profiling of human T and NK lymphocytes by high-content cell imaging</title><author>German, Yolla ; Vulliard, Loan ; Kamnev, Anton ; Pfajfer, Laurène ; Huemer, Jakob ; Mautner, Anna-Katharina ; Rubio, Aude ; Kalinichenko, Artem ; Boztug, Kaan ; Ferrand, Audrey ; Menche, Jörg ; Dupré, Loïc</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-64ec0e4aec8e862da8c06909bf8140d40dd9c408c821980c42d81c81f0cef7663</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>actin cytoskeleton</topic><topic>Actin-Related Protein 2-3 Complex - deficiency</topic><topic>Actin-Related Protein 2-3 Complex - metabolism</topic><topic>Adolescent</topic><topic>ARPC1B deficiency</topic><topic>Biotechnology</topic><topic>CD8-Positive T-Lymphocytes - cytology</topic><topic>CD8-Positive T-Lymphocytes - drug effects</topic><topic>Cell Line</topic><topic>Cell Shape - drug effects</topic><topic>Cellular Biology</topic><topic>Cytoskeleton - drug effects</topic><topic>Cytoskeleton - metabolism</topic><topic>cytotoxic T lymphocytes</topic><topic>Exocytosis - drug effects</topic><topic>high-content imaging</topic><topic>Human health and pathology</topic><topic>Humans</topic><topic>Imaging, Three-Dimensional</topic><topic>immunological synapse</topic><topic>Immunological Synapses - drug effects</topic><topic>Immunological Synapses - metabolism</topic><topic>Killer Cells, Natural - cytology</topic><topic>Killer Cells, Natural - drug effects</topic><topic>Killer Cells, Natural - metabolism</topic><topic>Life Sciences</topic><topic>lytic granules</topic><topic>Male</topic><topic>morphological profiling</topic><topic>NK cells</topic><topic>Organoselenium Compounds - pharmacology</topic><topic>Organosilicon Compounds - pharmacology</topic><topic>Single-Cell Analysis</topic><topic>T-Lymphocytes - cytology</topic><topic>T-Lymphocytes - drug effects</topic><topic>T-Lymphocytes - metabolism</topic><topic>Thiones - pharmacology</topic><topic>Uracil - analogs & derivatives</topic><topic>Uracil - pharmacology</topic><topic>WASP deficiency</topic><topic>Wiskott-Aldrich Syndrome Protein - deficiency</topic><topic>Wiskott-Aldrich Syndrome Protein - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>German, Yolla</creatorcontrib><creatorcontrib>Vulliard, Loan</creatorcontrib><creatorcontrib>Kamnev, Anton</creatorcontrib><creatorcontrib>Pfajfer, Laurène</creatorcontrib><creatorcontrib>Huemer, Jakob</creatorcontrib><creatorcontrib>Mautner, Anna-Katharina</creatorcontrib><creatorcontrib>Rubio, Aude</creatorcontrib><creatorcontrib>Kalinichenko, Artem</creatorcontrib><creatorcontrib>Boztug, Kaan</creatorcontrib><creatorcontrib>Ferrand, Audrey</creatorcontrib><creatorcontrib>Menche, Jörg</creatorcontrib><creatorcontrib>Dupré, Loïc</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Cell reports (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>German, Yolla</au><au>Vulliard, Loan</au><au>Kamnev, Anton</au><au>Pfajfer, Laurène</au><au>Huemer, Jakob</au><au>Mautner, Anna-Katharina</au><au>Rubio, Aude</au><au>Kalinichenko, Artem</au><au>Boztug, Kaan</au><au>Ferrand, Audrey</au><au>Menche, Jörg</au><au>Dupré, Loïc</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Morphological profiling of human T and NK lymphocytes by high-content cell imaging</atitle><jtitle>Cell reports (Cambridge)</jtitle><addtitle>Cell Rep</addtitle><date>2021-07-06</date><risdate>2021</risdate><volume>36</volume><issue>1</issue><spage>109318</spage><epage>109318</epage><pages>109318-109318</pages><artnum>109318</artnum><issn>2211-1247</issn><eissn>2211-1247</eissn><abstract>The immunological synapse is a complex structure that decodes stimulatory signals into adapted lymphocyte responses. It is a unique window to monitor lymphocyte activity because of development of systematic quantitative approaches. Here we demonstrate the applicability of high-content imaging to human T and natural killer (NK) cells and develop a pipeline for unbiased analysis of high-definition morphological profiles. Our approach reveals how distinct facets of actin cytoskeleton remodeling shape immunological synapse architecture and affect lytic granule positioning. Morphological profiling of CD8+ T cells from immunodeficient individuals allows discrimination of the roles of the ARP2/3 subunit ARPC1B and the ARP2/3 activator Wiskott-Aldrich syndrome protein (WASP) in immunological synapse assembly. Single-cell analysis further identifies uncoupling of lytic granules and F-actin radial distribution in ARPC1B-deficient lymphocytes. Our study provides a foundation for development of morphological profiling as a scalable approach to monitor primary lymphocyte responsiveness and to identify complex aspects of lymphocyte micro-architecture.
[Display omitted]
•Cytotoxic lymphocytes can be profiled in depth using high-content imaging•Morphological changes are identified with dedicated analytical tools•Distinct immunological synapse alterations in ARPC1B- and WASP-deficient T cells•3D distribution of lytic granules is impaired in ARPC1B-deficient CD8+ T cells
German et al. provide a workflow to study activation of cytotoxic T and NK lymphocytes by high-content confocal microscopy. Images are analyzed to characterize morphological variation in immunological synapses induced by actin compounds in primary cells as well as in CD8+ T cells derived from ARPC1B- and WASP-deficient individuals.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>34233185</pmid><doi>10.1016/j.celrep.2021.109318</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-2260-4935</orcidid><orcidid>https://orcid.org/0000-0002-7020-7256</orcidid><orcidid>https://orcid.org/0000-0003-0471-4601</orcidid><orcidid>https://orcid.org/0000-0002-6279-3486</orcidid><orcidid>https://orcid.org/0000-0002-7278-6503</orcidid><orcidid>https://orcid.org/0000-0001-8387-9185</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | actin cytoskeleton Actin-Related Protein 2-3 Complex - deficiency Actin-Related Protein 2-3 Complex - metabolism Adolescent ARPC1B deficiency Biotechnology CD8-Positive T-Lymphocytes - cytology CD8-Positive T-Lymphocytes - drug effects Cell Line Cell Shape - drug effects Cellular Biology Cytoskeleton - drug effects Cytoskeleton - metabolism cytotoxic T lymphocytes Exocytosis - drug effects high-content imaging Human health and pathology Humans Imaging, Three-Dimensional immunological synapse Immunological Synapses - drug effects Immunological Synapses - metabolism Killer Cells, Natural - cytology Killer Cells, Natural - drug effects Killer Cells, Natural - metabolism Life Sciences lytic granules Male morphological profiling NK cells Organoselenium Compounds - pharmacology Organosilicon Compounds - pharmacology Single-Cell Analysis T-Lymphocytes - cytology T-Lymphocytes - drug effects T-Lymphocytes - metabolism Thiones - pharmacology Uracil - analogs & derivatives Uracil - pharmacology WASP deficiency Wiskott-Aldrich Syndrome Protein - deficiency Wiskott-Aldrich Syndrome Protein - metabolism |
| title | Morphological profiling of human T and NK lymphocytes by high-content cell imaging |
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