Comprehensive single-cell analysis demonstrates radiotherapy-induced infiltration of macrophages expressing immunosuppressive genes into tumor in esophageal squamous cell carcinoma
Radiotherapy (RT) combined with immunotherapy is promising; however, the immune response signature in the clinical setting after RT remains unclear. Here, by integrative spatial and single-cell analyses using multiplex immunostaining (CODEX), spatial transcriptome (VISIUM), and single-cell RNA seque...
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| Veröffentlicht in: | Science advances 2023-12, Vol.9 (50), p.eadh9069-eadh9069 |
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| creator | Oyoshi, Hidekazu Du, Junyan Sakai, Shunsuke A Yamashita, Riu Okumura, Masayuki Motegi, Atsushi Hojo, Hidehiro Nakamura, Masaki Hirata, Hidenari Sunakawa, Hironori Kotani, Daisuke Yano, Tomonori Kojima, Takashi Nakamura, Yuka Kojima, Motohiro Suzuki, Ayako Zenkoh, Junko Tsuchihara, Katsuya Akimoto, Tetsuo Shibata, Atsushi Suzuki, Yutaka Kageyama, Shun-Ichiro |
| description | Radiotherapy (RT) combined with immunotherapy is promising; however, the immune response signature in the clinical setting after RT remains unclear. Here, by integrative spatial and single-cell analyses using multiplex immunostaining (CODEX), spatial transcriptome (VISIUM), and single-cell RNA sequencing, we substantiated the infiltration of immune cells into tumors with dynamic changes in immunostimulatory and immunosuppressive gene expression after RT. In addition, our comprehensive analysis uncovered time- and cell type-dependent alterations in the gene expression profile after RT. Furthermore, myeloid cells showed prominent up-regulation of immune response-associated genes after RT. Notably, a subset of infiltrating tumor-associated myeloid cells showing PD-L1 positivity exhibited significant up-regulation of immunostimulatory (HMGB1 and ISG15), immunosuppressive (SIRPA and IDO1), and protumor genes (CXCL8, CCL3, IL-6, and IL-1AB), which can be targets of immunotherapy in combination with PD-L1. These datasets will provide information on the RT-induced gene signature to seek an appropriate target for personalized immunotherapy combined with RT and guide the timing of combination therapy. |
| doi_str_mv | 10.1126/sciadv.adh9069 |
| format | Article |
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Here, by integrative spatial and single-cell analyses using multiplex immunostaining (CODEX), spatial transcriptome (VISIUM), and single-cell RNA sequencing, we substantiated the infiltration of immune cells into tumors with dynamic changes in immunostimulatory and immunosuppressive gene expression after RT. In addition, our comprehensive analysis uncovered time- and cell type-dependent alterations in the gene expression profile after RT. Furthermore, myeloid cells showed prominent up-regulation of immune response-associated genes after RT. Notably, a subset of infiltrating tumor-associated myeloid cells showing PD-L1 positivity exhibited significant up-regulation of immunostimulatory (HMGB1 and ISG15), immunosuppressive (SIRPA and IDO1), and protumor genes (CXCL8, CCL3, IL-6, and IL-1AB), which can be targets of immunotherapy in combination with PD-L1. These datasets will provide information on the RT-induced gene signature to seek an appropriate target for personalized immunotherapy combined with RT and guide the timing of combination therapy.</description><identifier>ISSN: 2375-2548</identifier><identifier>EISSN: 2375-2548</identifier><identifier>DOI: 10.1126/sciadv.adh9069</identifier><identifier>PMID: 38091397</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>B7-H1 Antigen - metabolism ; Biomedicine and Life Sciences ; Cancer ; Carcinoma, Squamous Cell - pathology ; Esophageal Neoplasms - genetics ; Esophageal Neoplasms - pathology ; Esophageal Squamous Cell Carcinoma ; Humans ; Immunology ; Immunosuppressive Agents ; Macrophages - metabolism ; SciAdv r-articles</subject><ispartof>Science advances, 2023-12, Vol.9 (50), p.eadh9069-eadh9069</ispartof><rights>Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). 2023 The Authors</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c346t-74a8deef518d71e1033b3ef7bdaf545914c986da38c42068d9437ae976d5d7433</cites><orcidid>0000-0003-3130-6857 ; 0000-0001-7507-2349 ; 0000-0002-9842-165X ; 0000-0002-4431-8892 ; 0000-0001-9917-2280 ; 0000-0002-6072-0144 ; 0000-0002-5600-0312 ; 0000-0001-8912-6977 ; 0000-0002-7559-5139 ; 0000-0003-0881-1345</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/PMC10848745/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10848745/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38091397$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Oyoshi, Hidekazu</creatorcontrib><creatorcontrib>Du, Junyan</creatorcontrib><creatorcontrib>Sakai, Shunsuke A</creatorcontrib><creatorcontrib>Yamashita, Riu</creatorcontrib><creatorcontrib>Okumura, Masayuki</creatorcontrib><creatorcontrib>Motegi, Atsushi</creatorcontrib><creatorcontrib>Hojo, Hidehiro</creatorcontrib><creatorcontrib>Nakamura, Masaki</creatorcontrib><creatorcontrib>Hirata, Hidenari</creatorcontrib><creatorcontrib>Sunakawa, Hironori</creatorcontrib><creatorcontrib>Kotani, Daisuke</creatorcontrib><creatorcontrib>Yano, Tomonori</creatorcontrib><creatorcontrib>Kojima, Takashi</creatorcontrib><creatorcontrib>Nakamura, Yuka</creatorcontrib><creatorcontrib>Kojima, Motohiro</creatorcontrib><creatorcontrib>Suzuki, Ayako</creatorcontrib><creatorcontrib>Zenkoh, Junko</creatorcontrib><creatorcontrib>Tsuchihara, Katsuya</creatorcontrib><creatorcontrib>Akimoto, Tetsuo</creatorcontrib><creatorcontrib>Shibata, Atsushi</creatorcontrib><creatorcontrib>Suzuki, Yutaka</creatorcontrib><creatorcontrib>Kageyama, Shun-Ichiro</creatorcontrib><title>Comprehensive single-cell analysis demonstrates radiotherapy-induced infiltration of macrophages expressing immunosuppressive genes into tumor in esophageal squamous cell carcinoma</title><title>Science advances</title><addtitle>Sci Adv</addtitle><description>Radiotherapy (RT) combined with immunotherapy is promising; however, the immune response signature in the clinical setting after RT remains unclear. Here, by integrative spatial and single-cell analyses using multiplex immunostaining (CODEX), spatial transcriptome (VISIUM), and single-cell RNA sequencing, we substantiated the infiltration of immune cells into tumors with dynamic changes in immunostimulatory and immunosuppressive gene expression after RT. In addition, our comprehensive analysis uncovered time- and cell type-dependent alterations in the gene expression profile after RT. Furthermore, myeloid cells showed prominent up-regulation of immune response-associated genes after RT. Notably, a subset of infiltrating tumor-associated myeloid cells showing PD-L1 positivity exhibited significant up-regulation of immunostimulatory (HMGB1 and ISG15), immunosuppressive (SIRPA and IDO1), and protumor genes (CXCL8, CCL3, IL-6, and IL-1AB), which can be targets of immunotherapy in combination with PD-L1. These datasets will provide information on the RT-induced gene signature to seek an appropriate target for personalized immunotherapy combined with RT and guide the timing of combination therapy.</description><subject>B7-H1 Antigen - metabolism</subject><subject>Biomedicine and Life Sciences</subject><subject>Cancer</subject><subject>Carcinoma, Squamous Cell - pathology</subject><subject>Esophageal Neoplasms - genetics</subject><subject>Esophageal Neoplasms - pathology</subject><subject>Esophageal Squamous Cell Carcinoma</subject><subject>Humans</subject><subject>Immunology</subject><subject>Immunosuppressive Agents</subject><subject>Macrophages - metabolism</subject><subject>SciAdv r-articles</subject><issn>2375-2548</issn><issn>2375-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUctu3CAUtaJGSZRmm2XFshtPwOAHq6oa9SVF6qZdoztwPaYy4IA96vxXPzBMPY3SFVdwHvdwiuKe0Q1jVfOQtAVz2IAZJG3kRXFT8bYuq1p0b17N18VdSr8opUw0Tc3kVXHNOyoZl-1N8Wcb3BRxQJ_sAUmyfj9iqXEcCXgYj8kmYtAFn-YIMyYSwdgwDxhhOpbWm0WjIdb3djwBbPAk9MSBjmEaYJ8J-Dvrp5Mwsc4tPqRlWm-y3x59hlg_BzIvLsQ8EkwrFUaSnhZwYUnk70IaorY-OHhbXPYwJrw7n7fFz8-ffmy_lo_fv3zbfnwsNRfNXLYCOoPY16wzLUNGOd9x7Nudgb4WtWRCy64xwDstKtp0RgreAsq2MbVpBee3xYdVd1p2Do1GnzOOaorWQTyqAFb9_-LtoPbhoBjtRNeKOiu8PyvE8LRgmpWz6RQGPOZcqpK0kkJmywzdrND8dSlF7F98GFWnutVatzrXnQnvXm_3Av9XLn8GcOOwyg</recordid><startdate>20231215</startdate><enddate>20231215</enddate><creator>Oyoshi, Hidekazu</creator><creator>Du, Junyan</creator><creator>Sakai, Shunsuke A</creator><creator>Yamashita, Riu</creator><creator>Okumura, Masayuki</creator><creator>Motegi, Atsushi</creator><creator>Hojo, Hidehiro</creator><creator>Nakamura, Masaki</creator><creator>Hirata, Hidenari</creator><creator>Sunakawa, Hironori</creator><creator>Kotani, Daisuke</creator><creator>Yano, Tomonori</creator><creator>Kojima, Takashi</creator><creator>Nakamura, Yuka</creator><creator>Kojima, Motohiro</creator><creator>Suzuki, Ayako</creator><creator>Zenkoh, Junko</creator><creator>Tsuchihara, Katsuya</creator><creator>Akimoto, Tetsuo</creator><creator>Shibata, Atsushi</creator><creator>Suzuki, Yutaka</creator><creator>Kageyama, Shun-Ichiro</creator><general>American Association for the Advancement of Science</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/0000-0003-3130-6857</orcidid><orcidid>https://orcid.org/0000-0001-7507-2349</orcidid><orcidid>https://orcid.org/0000-0002-9842-165X</orcidid><orcidid>https://orcid.org/0000-0002-4431-8892</orcidid><orcidid>https://orcid.org/0000-0001-9917-2280</orcidid><orcidid>https://orcid.org/0000-0002-6072-0144</orcidid><orcidid>https://orcid.org/0000-0002-5600-0312</orcidid><orcidid>https://orcid.org/0000-0001-8912-6977</orcidid><orcidid>https://orcid.org/0000-0002-7559-5139</orcidid><orcidid>https://orcid.org/0000-0003-0881-1345</orcidid></search><sort><creationdate>20231215</creationdate><title>Comprehensive single-cell analysis demonstrates radiotherapy-induced infiltration of macrophages expressing immunosuppressive genes into tumor in esophageal squamous cell carcinoma</title><author>Oyoshi, Hidekazu ; Du, Junyan ; Sakai, Shunsuke A ; Yamashita, Riu ; Okumura, Masayuki ; Motegi, Atsushi ; Hojo, Hidehiro ; Nakamura, Masaki ; Hirata, Hidenari ; Sunakawa, Hironori ; Kotani, Daisuke ; Yano, Tomonori ; Kojima, Takashi ; Nakamura, Yuka ; Kojima, Motohiro ; Suzuki, Ayako ; Zenkoh, Junko ; Tsuchihara, Katsuya ; Akimoto, Tetsuo ; Shibata, Atsushi ; Suzuki, Yutaka ; Kageyama, Shun-Ichiro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c346t-74a8deef518d71e1033b3ef7bdaf545914c986da38c42068d9437ae976d5d7433</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>B7-H1 Antigen - metabolism</topic><topic>Biomedicine and Life Sciences</topic><topic>Cancer</topic><topic>Carcinoma, Squamous Cell - pathology</topic><topic>Esophageal Neoplasms - genetics</topic><topic>Esophageal Neoplasms - pathology</topic><topic>Esophageal Squamous Cell Carcinoma</topic><topic>Humans</topic><topic>Immunology</topic><topic>Immunosuppressive Agents</topic><topic>Macrophages - metabolism</topic><topic>SciAdv r-articles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Oyoshi, Hidekazu</creatorcontrib><creatorcontrib>Du, Junyan</creatorcontrib><creatorcontrib>Sakai, Shunsuke A</creatorcontrib><creatorcontrib>Yamashita, Riu</creatorcontrib><creatorcontrib>Okumura, Masayuki</creatorcontrib><creatorcontrib>Motegi, Atsushi</creatorcontrib><creatorcontrib>Hojo, Hidehiro</creatorcontrib><creatorcontrib>Nakamura, Masaki</creatorcontrib><creatorcontrib>Hirata, Hidenari</creatorcontrib><creatorcontrib>Sunakawa, Hironori</creatorcontrib><creatorcontrib>Kotani, Daisuke</creatorcontrib><creatorcontrib>Yano, Tomonori</creatorcontrib><creatorcontrib>Kojima, Takashi</creatorcontrib><creatorcontrib>Nakamura, Yuka</creatorcontrib><creatorcontrib>Kojima, Motohiro</creatorcontrib><creatorcontrib>Suzuki, Ayako</creatorcontrib><creatorcontrib>Zenkoh, Junko</creatorcontrib><creatorcontrib>Tsuchihara, Katsuya</creatorcontrib><creatorcontrib>Akimoto, Tetsuo</creatorcontrib><creatorcontrib>Shibata, Atsushi</creatorcontrib><creatorcontrib>Suzuki, Yutaka</creatorcontrib><creatorcontrib>Kageyama, Shun-Ichiro</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>Science advances</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Oyoshi, Hidekazu</au><au>Du, Junyan</au><au>Sakai, Shunsuke A</au><au>Yamashita, Riu</au><au>Okumura, Masayuki</au><au>Motegi, Atsushi</au><au>Hojo, Hidehiro</au><au>Nakamura, Masaki</au><au>Hirata, Hidenari</au><au>Sunakawa, Hironori</au><au>Kotani, Daisuke</au><au>Yano, Tomonori</au><au>Kojima, Takashi</au><au>Nakamura, Yuka</au><au>Kojima, Motohiro</au><au>Suzuki, Ayako</au><au>Zenkoh, Junko</au><au>Tsuchihara, Katsuya</au><au>Akimoto, Tetsuo</au><au>Shibata, Atsushi</au><au>Suzuki, Yutaka</au><au>Kageyama, Shun-Ichiro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comprehensive single-cell analysis demonstrates radiotherapy-induced infiltration of macrophages expressing immunosuppressive genes into tumor in esophageal squamous cell carcinoma</atitle><jtitle>Science advances</jtitle><addtitle>Sci Adv</addtitle><date>2023-12-15</date><risdate>2023</risdate><volume>9</volume><issue>50</issue><spage>eadh9069</spage><epage>eadh9069</epage><pages>eadh9069-eadh9069</pages><issn>2375-2548</issn><eissn>2375-2548</eissn><abstract>Radiotherapy (RT) combined with immunotherapy is promising; however, the immune response signature in the clinical setting after RT remains unclear. Here, by integrative spatial and single-cell analyses using multiplex immunostaining (CODEX), spatial transcriptome (VISIUM), and single-cell RNA sequencing, we substantiated the infiltration of immune cells into tumors with dynamic changes in immunostimulatory and immunosuppressive gene expression after RT. In addition, our comprehensive analysis uncovered time- and cell type-dependent alterations in the gene expression profile after RT. Furthermore, myeloid cells showed prominent up-regulation of immune response-associated genes after RT. Notably, a subset of infiltrating tumor-associated myeloid cells showing PD-L1 positivity exhibited significant up-regulation of immunostimulatory (HMGB1 and ISG15), immunosuppressive (SIRPA and IDO1), and protumor genes (CXCL8, CCL3, IL-6, and IL-1AB), which can be targets of immunotherapy in combination with PD-L1. 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| subjects | B7-H1 Antigen - metabolism Biomedicine and Life Sciences Cancer Carcinoma, Squamous Cell - pathology Esophageal Neoplasms - genetics Esophageal Neoplasms - pathology Esophageal Squamous Cell Carcinoma Humans Immunology Immunosuppressive Agents Macrophages - metabolism SciAdv r-articles |
| title | Comprehensive single-cell analysis demonstrates radiotherapy-induced infiltration of macrophages expressing immunosuppressive genes into tumor in esophageal squamous cell carcinoma |
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