Analysis of classical neutrophils and polymorphonuclear myeloid-derived suppressor cells in cancer patients and tumor-bearing mice
In this study, using single-cell RNA-seq, cell mass spectrometry, flow cytometry, and functional analysis, we characterized the heterogeneity of polymorphonuclear neutrophils (PMNs) in cancer. We describe three populations of PMNs in tumor-bearing mice: classical PMNs, polymorphonuclear myeloid-deri...
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| Veröffentlicht in: | The Journal of experimental medicine 2021-04, Vol.218 (4) |
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| creator | Veglia, Filippo Hashimoto, Ayumi Dweep, Harsh Sanseviero, Emilio De Leo, Alessandra Tcyganov, Evgenii Kossenkov, Andrew Mulligan, Charles Nam, Brian Masters, Gregory Patel, Jaymala Bhargava, Vipul Wilkinson, Patrick Smirnov, Denis Sepulveda, Manuel A Singhal, Sunil Eruslanov, Evgeniy B Cristescu, Razvan Loboda, Andrey Nefedova, Yulia Gabrilovich, Dmitry I |
| description | In this study, using single-cell RNA-seq, cell mass spectrometry, flow cytometry, and functional analysis, we characterized the heterogeneity of polymorphonuclear neutrophils (PMNs) in cancer. We describe three populations of PMNs in tumor-bearing mice: classical PMNs, polymorphonuclear myeloid-derived suppressor cells (PMN-MDSCs), and activated PMN-MDSCs with potent immune suppressive activity. In spleens of mice, PMN-MDSCs gradually replaced PMNs during tumor progression. Activated PMN-MDSCs were found only in tumors, where they were present at the very early stages of the disease. These populations of PMNs in mice could be separated based on the expression of CD14. In peripheral blood of cancer patients, we identified two distinct populations of PMNs with characteristics of classical PMNs and PMN-MDSCs. The gene signature of tumor PMN-MDSCs was similar to that in mouse activated PMN-MDSCs and was closely associated with negative clinical outcome in cancer patients. Thus, we provide evidence that PMN-MDSCs are a distinct population of PMNs with unique features and potential for selective targeting opportunities. |
| doi_str_mv | 10.1084/JEM.20201803 |
| format | Article |
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We describe three populations of PMNs in tumor-bearing mice: classical PMNs, polymorphonuclear myeloid-derived suppressor cells (PMN-MDSCs), and activated PMN-MDSCs with potent immune suppressive activity. In spleens of mice, PMN-MDSCs gradually replaced PMNs during tumor progression. Activated PMN-MDSCs were found only in tumors, where they were present at the very early stages of the disease. These populations of PMNs in mice could be separated based on the expression of CD14. In peripheral blood of cancer patients, we identified two distinct populations of PMNs with characteristics of classical PMNs and PMN-MDSCs. The gene signature of tumor PMN-MDSCs was similar to that in mouse activated PMN-MDSCs and was closely associated with negative clinical outcome in cancer patients. Thus, we provide evidence that PMN-MDSCs are a distinct population of PMNs with unique features and potential for selective targeting opportunities.</description><identifier>ISSN: 0022-1007</identifier><identifier>EISSN: 1540-9538</identifier><identifier>DOI: 10.1084/JEM.20201803</identifier><identifier>PMID: 33566112</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Animals ; Carcinoma, Lewis Lung - immunology ; Carcinoma, Lewis Lung - pathology ; Carcinoma, Non-Small-Cell Lung - blood ; Carcinoma, Non-Small-Cell Lung - immunology ; Case-Control Studies ; Cell Line, Tumor ; Disease Models, Animal ; Female ; Humans ; Innate Immunity and Inflammation ; Lung Neoplasms - blood ; Lung Neoplasms - immunology ; Lymphoma - immunology ; Lymphoma - pathology ; Mice ; Mice, Inbred C57BL ; Neutrophils - classification ; Neutrophils - immunology ; RNA-Seq ; Single-Cell Analysis ; Technical Advances and Resources ; Transcriptome ; Tumor Immunology</subject><ispartof>The Journal of experimental medicine, 2021-04, Vol.218 (4)</ispartof><rights>2021 Veglia et al.</rights><rights>2021 Veglia et al. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c384t-cb5e27ca6b143c58346c9f2e4ab97bd7e29871da0fb676f26603bf2a92462d9e3</citedby><cites>FETCH-LOGICAL-c384t-cb5e27ca6b143c58346c9f2e4ab97bd7e29871da0fb676f26603bf2a92462d9e3</cites><orcidid>0000-0001-6864-5516 ; 0000-0002-1956-9315 ; 0000-0001-6710-1584 ; 0000-0001-8021-2967 ; 0000-0003-4452-7042 ; 0000-0002-9978-0339 ; 0000-0002-8538-3826 ; 0000-0003-4239-184X ; 0000-0002-2413-7082 ; 0000-0001-7196-7823 ; 0000-0002-0232-2260 ; 0000-0002-0958-1564 ; 0000-0002-5121-9294 ; 0000-0001-8605-7291 ; 0000-0003-0743-5026 ; 0000-0002-2643-0573 ; 0000-0001-9913-6407 ; 0000-0003-3630-5765 ; 0000-0002-2274-4110 ; 0000-0002-1536-0418 ; 0000-0002-6655-4896</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33566112$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Veglia, Filippo</creatorcontrib><creatorcontrib>Hashimoto, Ayumi</creatorcontrib><creatorcontrib>Dweep, Harsh</creatorcontrib><creatorcontrib>Sanseviero, Emilio</creatorcontrib><creatorcontrib>De Leo, Alessandra</creatorcontrib><creatorcontrib>Tcyganov, Evgenii</creatorcontrib><creatorcontrib>Kossenkov, Andrew</creatorcontrib><creatorcontrib>Mulligan, Charles</creatorcontrib><creatorcontrib>Nam, Brian</creatorcontrib><creatorcontrib>Masters, Gregory</creatorcontrib><creatorcontrib>Patel, Jaymala</creatorcontrib><creatorcontrib>Bhargava, Vipul</creatorcontrib><creatorcontrib>Wilkinson, Patrick</creatorcontrib><creatorcontrib>Smirnov, Denis</creatorcontrib><creatorcontrib>Sepulveda, Manuel A</creatorcontrib><creatorcontrib>Singhal, Sunil</creatorcontrib><creatorcontrib>Eruslanov, Evgeniy B</creatorcontrib><creatorcontrib>Cristescu, Razvan</creatorcontrib><creatorcontrib>Loboda, Andrey</creatorcontrib><creatorcontrib>Nefedova, Yulia</creatorcontrib><creatorcontrib>Gabrilovich, Dmitry I</creatorcontrib><title>Analysis of classical neutrophils and polymorphonuclear myeloid-derived suppressor cells in cancer patients and tumor-bearing mice</title><title>The Journal of experimental medicine</title><addtitle>J Exp Med</addtitle><description>In this study, using single-cell RNA-seq, cell mass spectrometry, flow cytometry, and functional analysis, we characterized the heterogeneity of polymorphonuclear neutrophils (PMNs) in cancer. We describe three populations of PMNs in tumor-bearing mice: classical PMNs, polymorphonuclear myeloid-derived suppressor cells (PMN-MDSCs), and activated PMN-MDSCs with potent immune suppressive activity. In spleens of mice, PMN-MDSCs gradually replaced PMNs during tumor progression. Activated PMN-MDSCs were found only in tumors, where they were present at the very early stages of the disease. These populations of PMNs in mice could be separated based on the expression of CD14. In peripheral blood of cancer patients, we identified two distinct populations of PMNs with characteristics of classical PMNs and PMN-MDSCs. The gene signature of tumor PMN-MDSCs was similar to that in mouse activated PMN-MDSCs and was closely associated with negative clinical outcome in cancer patients. Thus, we provide evidence that PMN-MDSCs are a distinct population of PMNs with unique features and potential for selective targeting opportunities.</description><subject>Animals</subject><subject>Carcinoma, Lewis Lung - immunology</subject><subject>Carcinoma, Lewis Lung - pathology</subject><subject>Carcinoma, Non-Small-Cell Lung - blood</subject><subject>Carcinoma, Non-Small-Cell Lung - immunology</subject><subject>Case-Control Studies</subject><subject>Cell Line, Tumor</subject><subject>Disease Models, Animal</subject><subject>Female</subject><subject>Humans</subject><subject>Innate Immunity and Inflammation</subject><subject>Lung Neoplasms - blood</subject><subject>Lung Neoplasms - immunology</subject><subject>Lymphoma - immunology</subject><subject>Lymphoma - pathology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Neutrophils - classification</subject><subject>Neutrophils - immunology</subject><subject>RNA-Seq</subject><subject>Single-Cell Analysis</subject><subject>Technical Advances and Resources</subject><subject>Transcriptome</subject><subject>Tumor Immunology</subject><issn>0022-1007</issn><issn>1540-9538</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkU1P3DAQhq0KVBbaW8-Vjxwa8Fds51IJrSgtAnFpz5bjTFgjx07tBGmv_HKCdhe1pznMM8_M6EXoCyUXlGhxeXt9f8EII1QT_gGtaC1I1dRcH6EVIYxVlBB1gk5LeSKEClHLj-iE81pKStkKvVxFG7bFF5x67IItxTsbcIR5ymnc-FCwjR0eU9gOKY-bFGcXwGY8bCEk31UdZP8MHS7zOGYoJWXsICxjPmJno4OMRzt5iNPONM2Lp2oXhY-PePAOPqHj3oYCn_f1DP35cf17_bO6e7j5tb66qxzXYqpcWwNTzsqWCu5qzYV0Tc9A2LZRbaeANVrRzpK-lUr2TErC257ZhgnJugb4Gfq-845zO0DnlpOyDWbMfrB5a5L15v9O9BvzmJ6N0qqpNVsE53tBTn9nKJMZfHl71kZIczFMaL0kIZha0G871OVUSob-fQ0l5i028wSDOcS24F__Pe0dPuTEXwGQAZfa</recordid><startdate>20210405</startdate><enddate>20210405</enddate><creator>Veglia, Filippo</creator><creator>Hashimoto, Ayumi</creator><creator>Dweep, Harsh</creator><creator>Sanseviero, Emilio</creator><creator>De Leo, Alessandra</creator><creator>Tcyganov, Evgenii</creator><creator>Kossenkov, Andrew</creator><creator>Mulligan, Charles</creator><creator>Nam, Brian</creator><creator>Masters, Gregory</creator><creator>Patel, Jaymala</creator><creator>Bhargava, Vipul</creator><creator>Wilkinson, Patrick</creator><creator>Smirnov, Denis</creator><creator>Sepulveda, Manuel A</creator><creator>Singhal, Sunil</creator><creator>Eruslanov, Evgeniy B</creator><creator>Cristescu, Razvan</creator><creator>Loboda, Andrey</creator><creator>Nefedova, Yulia</creator><creator>Gabrilovich, Dmitry I</creator><general>Rockefeller University Press</general><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/0000-0001-6864-5516</orcidid><orcidid>https://orcid.org/0000-0002-1956-9315</orcidid><orcidid>https://orcid.org/0000-0001-6710-1584</orcidid><orcidid>https://orcid.org/0000-0001-8021-2967</orcidid><orcidid>https://orcid.org/0000-0003-4452-7042</orcidid><orcidid>https://orcid.org/0000-0002-9978-0339</orcidid><orcidid>https://orcid.org/0000-0002-8538-3826</orcidid><orcidid>https://orcid.org/0000-0003-4239-184X</orcidid><orcidid>https://orcid.org/0000-0002-2413-7082</orcidid><orcidid>https://orcid.org/0000-0001-7196-7823</orcidid><orcidid>https://orcid.org/0000-0002-0232-2260</orcidid><orcidid>https://orcid.org/0000-0002-0958-1564</orcidid><orcidid>https://orcid.org/0000-0002-5121-9294</orcidid><orcidid>https://orcid.org/0000-0001-8605-7291</orcidid><orcidid>https://orcid.org/0000-0003-0743-5026</orcidid><orcidid>https://orcid.org/0000-0002-2643-0573</orcidid><orcidid>https://orcid.org/0000-0001-9913-6407</orcidid><orcidid>https://orcid.org/0000-0003-3630-5765</orcidid><orcidid>https://orcid.org/0000-0002-2274-4110</orcidid><orcidid>https://orcid.org/0000-0002-1536-0418</orcidid><orcidid>https://orcid.org/0000-0002-6655-4896</orcidid></search><sort><creationdate>20210405</creationdate><title>Analysis of classical neutrophils and polymorphonuclear myeloid-derived suppressor cells in cancer patients and tumor-bearing mice</title><author>Veglia, Filippo ; Hashimoto, Ayumi ; Dweep, Harsh ; Sanseviero, Emilio ; De Leo, Alessandra ; Tcyganov, Evgenii ; Kossenkov, Andrew ; Mulligan, Charles ; Nam, Brian ; Masters, Gregory ; Patel, Jaymala ; Bhargava, Vipul ; Wilkinson, Patrick ; Smirnov, Denis ; Sepulveda, Manuel A ; Singhal, Sunil ; Eruslanov, Evgeniy B ; Cristescu, Razvan ; Loboda, Andrey ; Nefedova, Yulia ; Gabrilovich, Dmitry I</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c384t-cb5e27ca6b143c58346c9f2e4ab97bd7e29871da0fb676f26603bf2a92462d9e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Carcinoma, Lewis Lung - immunology</topic><topic>Carcinoma, Lewis Lung - pathology</topic><topic>Carcinoma, Non-Small-Cell Lung - blood</topic><topic>Carcinoma, Non-Small-Cell Lung - immunology</topic><topic>Case-Control Studies</topic><topic>Cell Line, Tumor</topic><topic>Disease Models, Animal</topic><topic>Female</topic><topic>Humans</topic><topic>Innate Immunity and Inflammation</topic><topic>Lung Neoplasms - blood</topic><topic>Lung Neoplasms - immunology</topic><topic>Lymphoma - immunology</topic><topic>Lymphoma - pathology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Neutrophils - classification</topic><topic>Neutrophils - immunology</topic><topic>RNA-Seq</topic><topic>Single-Cell Analysis</topic><topic>Technical Advances and Resources</topic><topic>Transcriptome</topic><topic>Tumor Immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Veglia, Filippo</creatorcontrib><creatorcontrib>Hashimoto, Ayumi</creatorcontrib><creatorcontrib>Dweep, Harsh</creatorcontrib><creatorcontrib>Sanseviero, Emilio</creatorcontrib><creatorcontrib>De Leo, Alessandra</creatorcontrib><creatorcontrib>Tcyganov, Evgenii</creatorcontrib><creatorcontrib>Kossenkov, Andrew</creatorcontrib><creatorcontrib>Mulligan, Charles</creatorcontrib><creatorcontrib>Nam, Brian</creatorcontrib><creatorcontrib>Masters, Gregory</creatorcontrib><creatorcontrib>Patel, Jaymala</creatorcontrib><creatorcontrib>Bhargava, Vipul</creatorcontrib><creatorcontrib>Wilkinson, Patrick</creatorcontrib><creatorcontrib>Smirnov, Denis</creatorcontrib><creatorcontrib>Sepulveda, Manuel A</creatorcontrib><creatorcontrib>Singhal, Sunil</creatorcontrib><creatorcontrib>Eruslanov, Evgeniy B</creatorcontrib><creatorcontrib>Cristescu, Razvan</creatorcontrib><creatorcontrib>Loboda, Andrey</creatorcontrib><creatorcontrib>Nefedova, Yulia</creatorcontrib><creatorcontrib>Gabrilovich, Dmitry I</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>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of experimental medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Veglia, Filippo</au><au>Hashimoto, Ayumi</au><au>Dweep, Harsh</au><au>Sanseviero, Emilio</au><au>De Leo, Alessandra</au><au>Tcyganov, Evgenii</au><au>Kossenkov, Andrew</au><au>Mulligan, Charles</au><au>Nam, Brian</au><au>Masters, Gregory</au><au>Patel, Jaymala</au><au>Bhargava, Vipul</au><au>Wilkinson, Patrick</au><au>Smirnov, Denis</au><au>Sepulveda, Manuel A</au><au>Singhal, Sunil</au><au>Eruslanov, Evgeniy B</au><au>Cristescu, Razvan</au><au>Loboda, Andrey</au><au>Nefedova, Yulia</au><au>Gabrilovich, Dmitry I</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Analysis of classical neutrophils and polymorphonuclear myeloid-derived suppressor cells in cancer patients and tumor-bearing mice</atitle><jtitle>The Journal of experimental medicine</jtitle><addtitle>J Exp Med</addtitle><date>2021-04-05</date><risdate>2021</risdate><volume>218</volume><issue>4</issue><issn>0022-1007</issn><eissn>1540-9538</eissn><abstract>In this study, using single-cell RNA-seq, cell mass spectrometry, flow cytometry, and functional analysis, we characterized the heterogeneity of polymorphonuclear neutrophils (PMNs) in cancer. We describe three populations of PMNs in tumor-bearing mice: classical PMNs, polymorphonuclear myeloid-derived suppressor cells (PMN-MDSCs), and activated PMN-MDSCs with potent immune suppressive activity. In spleens of mice, PMN-MDSCs gradually replaced PMNs during tumor progression. Activated PMN-MDSCs were found only in tumors, where they were present at the very early stages of the disease. These populations of PMNs in mice could be separated based on the expression of CD14. In peripheral blood of cancer patients, we identified two distinct populations of PMNs with characteristics of classical PMNs and PMN-MDSCs. The gene signature of tumor PMN-MDSCs was similar to that in mouse activated PMN-MDSCs and was closely associated with negative clinical outcome in cancer patients. 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| subjects | Animals Carcinoma, Lewis Lung - immunology Carcinoma, Lewis Lung - pathology Carcinoma, Non-Small-Cell Lung - blood Carcinoma, Non-Small-Cell Lung - immunology Case-Control Studies Cell Line, Tumor Disease Models, Animal Female Humans Innate Immunity and Inflammation Lung Neoplasms - blood Lung Neoplasms - immunology Lymphoma - immunology Lymphoma - pathology Mice Mice, Inbred C57BL Neutrophils - classification Neutrophils - immunology RNA-Seq Single-Cell Analysis Technical Advances and Resources Transcriptome Tumor Immunology |
| title | Analysis of classical neutrophils and polymorphonuclear myeloid-derived suppressor cells in cancer patients and tumor-bearing mice |
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