NDR1-Dependent Regulation of Kindlin-3 Controls High-Affinity LFA-1 Binding and Immune Synapse Organization
Antigen-specific adhesion between T cells and antigen-presenting cells (APC) during the formation of the immunological synapse (IS) is mediated by LFA-1 and ICAM-1. Here, LFA-1-ICAM-1 interactions were measured at the single-molecule level on supported lipid bilayers. High-affinity binding was detec...
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| Veröffentlicht in: | Molecular and cellular biology 2017-04, Vol.37 (8) |
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| creator | Kondo, Naoyuki Ueda, Yoshihiro Kita, Toshiyuki Ozawa, Madoka Tomiyama, Takashi Yasuda, Kaneki Lim, Dae-Sik Kinashi, Tatsuo |
| description | Antigen-specific adhesion between T cells and antigen-presenting cells (APC) during the formation of the immunological synapse (IS) is mediated by LFA-1 and ICAM-1. Here, LFA-1-ICAM-1 interactions were measured at the single-molecule level on supported lipid bilayers. High-affinity binding was detected at low frequencies in the inner peripheral supramolecular activation cluster (SMAC) zone that contained high levels of activated Rap1 and kindlin-3. Rap1 was essential for T cell attachment, whereas deficiencies of ste20-like kinases, Mst1/Mst2, diminished high-affinity binding and abrogated central SMAC (cSMAC) formation with mislocalized kindlin-3 and vesicle transport regulators involved in T cell receptor recycling/releasing machineries, resulting in impaired T cell-APC interactions. We found that NDR1 kinase, activated by the Rap1 signaling cascade through RAPL and Mst1/Mst2, associated with and recruited kindlin-3 to the IS, which was required for high-affinity LFA-1/ICAM-1 binding and cSMAC formation. Our findings reveal crucial roles for Rap1 signaling via NDR1 for recruitment of kindlin-3 and IS organization. |
| doi_str_mv | 10.1128/MCB.00424-16 |
| format | Article |
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Here, LFA-1-ICAM-1 interactions were measured at the single-molecule level on supported lipid bilayers. High-affinity binding was detected at low frequencies in the inner peripheral supramolecular activation cluster (SMAC) zone that contained high levels of activated Rap1 and kindlin-3. Rap1 was essential for T cell attachment, whereas deficiencies of ste20-like kinases, Mst1/Mst2, diminished high-affinity binding and abrogated central SMAC (cSMAC) formation with mislocalized kindlin-3 and vesicle transport regulators involved in T cell receptor recycling/releasing machineries, resulting in impaired T cell-APC interactions. We found that NDR1 kinase, activated by the Rap1 signaling cascade through RAPL and Mst1/Mst2, associated with and recruited kindlin-3 to the IS, which was required for high-affinity LFA-1/ICAM-1 binding and cSMAC formation. Our findings reveal crucial roles for Rap1 signaling via NDR1 for recruitment of kindlin-3 and IS organization.</description><identifier>ISSN: 1098-5549</identifier><identifier>ISSN: 0270-7306</identifier><identifier>EISSN: 1098-5549</identifier><identifier>DOI: 10.1128/MCB.00424-16</identifier><identifier>PMID: 28137909</identifier><language>eng</language><publisher>United States: Taylor & Francis</publisher><subject>Animals ; Cell Cycle Proteins - metabolism ; Cytoskeletal Proteins - metabolism ; HEK293 Cells ; Hepatocyte Growth Factor - metabolism ; Humans ; ICAM-1 ; immunological synapse ; Immunological Synapses - metabolism ; Intercellular Adhesion Molecule-1 - metabolism ; Intracellular Signaling Peptides and Proteins - metabolism ; LFA-1 ; Lymphocyte Function-Associated Antigen-1 - metabolism ; Mice, Inbred C57BL ; NDR1 ; Protein Binding ; Protein-Serine-Threonine Kinases - metabolism ; Proto-Oncogene Proteins - metabolism ; Rap1 ; rap1 GTP-Binding Proteins - metabolism ; Signal Transduction ; Single Molecule Imaging ; single-molecule measurement ; Spotlight ; Transport Vesicles - metabolism ; vesicular transport</subject><ispartof>Molecular and cellular biology, 2017-04, Vol.37 (8)</ispartof><rights>Copyright © 2017 Kondo et al. 2017</rights><rights>Copyright © 2017 Kondo et al.</rights><rights>Copyright © 2017 Kondo et al. 2017 Kondo et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c508t-dbd73ffe01e04e23e2bb3a38dd6ffec0c0855b41c065b95a92eca04bbd7df6673</citedby><cites>FETCH-LOGICAL-c508t-dbd73ffe01e04e23e2bb3a38dd6ffec0c0855b41c065b95a92eca04bbd7df6673</cites><orcidid>0000-0002-6624-5989</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5376635/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5376635/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28137909$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kondo, Naoyuki</creatorcontrib><creatorcontrib>Ueda, Yoshihiro</creatorcontrib><creatorcontrib>Kita, Toshiyuki</creatorcontrib><creatorcontrib>Ozawa, Madoka</creatorcontrib><creatorcontrib>Tomiyama, Takashi</creatorcontrib><creatorcontrib>Yasuda, Kaneki</creatorcontrib><creatorcontrib>Lim, Dae-Sik</creatorcontrib><creatorcontrib>Kinashi, Tatsuo</creatorcontrib><title>NDR1-Dependent Regulation of Kindlin-3 Controls High-Affinity LFA-1 Binding and Immune Synapse Organization</title><title>Molecular and cellular biology</title><addtitle>Mol Cell Biol</addtitle><description>Antigen-specific adhesion between T cells and antigen-presenting cells (APC) during the formation of the immunological synapse (IS) is mediated by LFA-1 and ICAM-1. Here, LFA-1-ICAM-1 interactions were measured at the single-molecule level on supported lipid bilayers. High-affinity binding was detected at low frequencies in the inner peripheral supramolecular activation cluster (SMAC) zone that contained high levels of activated Rap1 and kindlin-3. Rap1 was essential for T cell attachment, whereas deficiencies of ste20-like kinases, Mst1/Mst2, diminished high-affinity binding and abrogated central SMAC (cSMAC) formation with mislocalized kindlin-3 and vesicle transport regulators involved in T cell receptor recycling/releasing machineries, resulting in impaired T cell-APC interactions. We found that NDR1 kinase, activated by the Rap1 signaling cascade through RAPL and Mst1/Mst2, associated with and recruited kindlin-3 to the IS, which was required for high-affinity LFA-1/ICAM-1 binding and cSMAC formation. Our findings reveal crucial roles for Rap1 signaling via NDR1 for recruitment of kindlin-3 and IS organization.</description><subject>Animals</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Cytoskeletal Proteins - metabolism</subject><subject>HEK293 Cells</subject><subject>Hepatocyte Growth Factor - metabolism</subject><subject>Humans</subject><subject>ICAM-1</subject><subject>immunological synapse</subject><subject>Immunological Synapses - metabolism</subject><subject>Intercellular Adhesion Molecule-1 - metabolism</subject><subject>Intracellular Signaling Peptides and Proteins - metabolism</subject><subject>LFA-1</subject><subject>Lymphocyte Function-Associated Antigen-1 - metabolism</subject><subject>Mice, Inbred C57BL</subject><subject>NDR1</subject><subject>Protein Binding</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Proto-Oncogene Proteins - metabolism</subject><subject>Rap1</subject><subject>rap1 GTP-Binding Proteins - metabolism</subject><subject>Signal Transduction</subject><subject>Single Molecule Imaging</subject><subject>single-molecule measurement</subject><subject>Spotlight</subject><subject>Transport Vesicles - metabolism</subject><subject>vesicular transport</subject><issn>1098-5549</issn><issn>0270-7306</issn><issn>1098-5549</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>0YH</sourceid><sourceid>EIF</sourceid><recordid>eNqNkc9PFDEYhhsjEQRvnk2PHiy202mnczFZFhHCIgnouen0x1CdaZd2RrP-9VYWCCYePH3N16dP-uYF4DXBh4RU4v3F8ugQ47qqEeHPwB7BrUCM1e3zJ-dd8DLnbxhj3mL6AuxWgtCmxe0e-P75-IqgY7u2wdgwwSvbz4OafAwwOnjugxl8QBQuY5hSHDI89f0NWjjng582cHWyQAQeFcyHHqpg4Nk4zsHC601Q62zhZepV8L_ujAdgx6kh21f3cx98Pfn4ZXmKVpefzpaLFdIMiwmZzjTUOYuJxbWtqK26jioqjOFlq7HGgrGuJhpz1rVMtZXVCtddeWYc5w3dBx-23vXcjdbokiupQa6TH1XayKi8_Psm-BvZxx-S0YZzyorg7b0gxdvZ5kmOPms7DCrYOGdJREtEQzkh_4FyWhHB2qqg77aoTjHnZN3jjwiWf6qUpUp5V6UkvOBvnqZ4hB-6K0CzBXxwMY3qZ0yDkZPaDDG5pIL2WdJ_qn8D5tqs3A</recordid><startdate>20170401</startdate><enddate>20170401</enddate><creator>Kondo, Naoyuki</creator><creator>Ueda, Yoshihiro</creator><creator>Kita, Toshiyuki</creator><creator>Ozawa, Madoka</creator><creator>Tomiyama, Takashi</creator><creator>Yasuda, Kaneki</creator><creator>Lim, Dae-Sik</creator><creator>Kinashi, Tatsuo</creator><general>Taylor & Francis</general><general>American Society for Microbiology</general><scope>0YH</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>7T5</scope><scope>H94</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6624-5989</orcidid></search><sort><creationdate>20170401</creationdate><title>NDR1-Dependent Regulation of Kindlin-3 Controls High-Affinity LFA-1 Binding and Immune Synapse Organization</title><author>Kondo, Naoyuki ; Ueda, Yoshihiro ; Kita, Toshiyuki ; Ozawa, Madoka ; Tomiyama, Takashi ; Yasuda, Kaneki ; Lim, Dae-Sik ; Kinashi, Tatsuo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c508t-dbd73ffe01e04e23e2bb3a38dd6ffec0c0855b41c065b95a92eca04bbd7df6673</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>Cytoskeletal Proteins - metabolism</topic><topic>HEK293 Cells</topic><topic>Hepatocyte Growth Factor - metabolism</topic><topic>Humans</topic><topic>ICAM-1</topic><topic>immunological synapse</topic><topic>Immunological Synapses - metabolism</topic><topic>Intercellular Adhesion Molecule-1 - metabolism</topic><topic>Intracellular Signaling Peptides and Proteins - metabolism</topic><topic>LFA-1</topic><topic>Lymphocyte Function-Associated Antigen-1 - metabolism</topic><topic>Mice, Inbred C57BL</topic><topic>NDR1</topic><topic>Protein Binding</topic><topic>Protein-Serine-Threonine Kinases - metabolism</topic><topic>Proto-Oncogene Proteins - metabolism</topic><topic>Rap1</topic><topic>rap1 GTP-Binding Proteins - metabolism</topic><topic>Signal Transduction</topic><topic>Single Molecule Imaging</topic><topic>single-molecule measurement</topic><topic>Spotlight</topic><topic>Transport Vesicles - metabolism</topic><topic>vesicular transport</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kondo, Naoyuki</creatorcontrib><creatorcontrib>Ueda, Yoshihiro</creatorcontrib><creatorcontrib>Kita, Toshiyuki</creatorcontrib><creatorcontrib>Ozawa, Madoka</creatorcontrib><creatorcontrib>Tomiyama, Takashi</creatorcontrib><creatorcontrib>Yasuda, Kaneki</creatorcontrib><creatorcontrib>Lim, Dae-Sik</creatorcontrib><creatorcontrib>Kinashi, Tatsuo</creatorcontrib><collection>Taylor & Francis 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>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular and cellular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kondo, Naoyuki</au><au>Ueda, Yoshihiro</au><au>Kita, Toshiyuki</au><au>Ozawa, Madoka</au><au>Tomiyama, Takashi</au><au>Yasuda, Kaneki</au><au>Lim, Dae-Sik</au><au>Kinashi, Tatsuo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>NDR1-Dependent Regulation of Kindlin-3 Controls High-Affinity LFA-1 Binding and Immune Synapse Organization</atitle><jtitle>Molecular and cellular biology</jtitle><addtitle>Mol Cell Biol</addtitle><date>2017-04-01</date><risdate>2017</risdate><volume>37</volume><issue>8</issue><issn>1098-5549</issn><issn>0270-7306</issn><eissn>1098-5549</eissn><abstract>Antigen-specific adhesion between T cells and antigen-presenting cells (APC) during the formation of the immunological synapse (IS) is mediated by LFA-1 and ICAM-1. Here, LFA-1-ICAM-1 interactions were measured at the single-molecule level on supported lipid bilayers. High-affinity binding was detected at low frequencies in the inner peripheral supramolecular activation cluster (SMAC) zone that contained high levels of activated Rap1 and kindlin-3. Rap1 was essential for T cell attachment, whereas deficiencies of ste20-like kinases, Mst1/Mst2, diminished high-affinity binding and abrogated central SMAC (cSMAC) formation with mislocalized kindlin-3 and vesicle transport regulators involved in T cell receptor recycling/releasing machineries, resulting in impaired T cell-APC interactions. We found that NDR1 kinase, activated by the Rap1 signaling cascade through RAPL and Mst1/Mst2, associated with and recruited kindlin-3 to the IS, which was required for high-affinity LFA-1/ICAM-1 binding and cSMAC formation. Our findings reveal crucial roles for Rap1 signaling via NDR1 for recruitment of kindlin-3 and IS organization.</abstract><cop>United States</cop><pub>Taylor & Francis</pub><pmid>28137909</pmid><doi>10.1128/MCB.00424-16</doi><orcidid>https://orcid.org/0000-0002-6624-5989</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Cell Cycle Proteins - metabolism Cytoskeletal Proteins - metabolism HEK293 Cells Hepatocyte Growth Factor - metabolism Humans ICAM-1 immunological synapse Immunological Synapses - metabolism Intercellular Adhesion Molecule-1 - metabolism Intracellular Signaling Peptides and Proteins - metabolism LFA-1 Lymphocyte Function-Associated Antigen-1 - metabolism Mice, Inbred C57BL NDR1 Protein Binding Protein-Serine-Threonine Kinases - metabolism Proto-Oncogene Proteins - metabolism Rap1 rap1 GTP-Binding Proteins - metabolism Signal Transduction Single Molecule Imaging single-molecule measurement Spotlight Transport Vesicles - metabolism vesicular transport |
| title | NDR1-Dependent Regulation of Kindlin-3 Controls High-Affinity LFA-1 Binding and Immune Synapse Organization |
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