Single-cell RNA profiling reveals classification and characteristics of mononuclear phagocytes in colorectal cancer
Colorectal cancer (CRC) is a major cause of cancer mortality and a serious health problem worldwide. Mononuclear phagocytes are the main immune cells in the tumor microenvironment of CRC with remarkable plasticity, and current studies show that macrophages are closely related to tumor progression, i...
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| creator | Ji, Tiantian Fu, Haoyu Wang, Liping Chen, Jinyun Tian, Shaobo Wang, Guobin Wang, Lin Wang, Zheng |
| description | Colorectal cancer (CRC) is a major cause of cancer mortality and a serious health problem worldwide. Mononuclear phagocytes are the main immune cells in the tumor microenvironment of CRC with remarkable plasticity, and current studies show that macrophages are closely related to tumor progression, invasion and dissemination. To understand the immunological function of mononuclear phagocytes comprehensively and deeply, we use single-cell RNA sequencing and classify mononuclear phagocytes in CRC into 6 different subsets, and characterize the heterogeneity of each subset. We find that tissue inhibitor of metalloproteinases (TIMPs) involved in the differentiation of proinflammatory and anti-inflammatory mononuclear phagocytes. Trajectory of circulating monocytes differentiation into tumor-associated macrophages (TAMs) and the dynamic changes at levels of transcription factor (TF) regulons during differentiation were revealed. We also find that C5 subset, characterized by activation of lipid metabolism, is in the terminal state of differentiation, and that the abundance of C5 subset is negatively correlated with CRC patients' prognosis. Our findings advance the understanding of circulating monocytes' differentiation into macrophages, identify a new subset associated with CRC prognosis, and reveal a set of TF regulons regulating mononuclear phagocytes differentiation, which are expected to be potential therapeutic targets for reversing immunosuppressive tumor microenvironment. |
| doi_str_mv | 10.1371/journal.pgen.1011176 |
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Mononuclear phagocytes are the main immune cells in the tumor microenvironment of CRC with remarkable plasticity, and current studies show that macrophages are closely related to tumor progression, invasion and dissemination. To understand the immunological function of mononuclear phagocytes comprehensively and deeply, we use single-cell RNA sequencing and classify mononuclear phagocytes in CRC into 6 different subsets, and characterize the heterogeneity of each subset. We find that tissue inhibitor of metalloproteinases (TIMPs) involved in the differentiation of proinflammatory and anti-inflammatory mononuclear phagocytes. Trajectory of circulating monocytes differentiation into tumor-associated macrophages (TAMs) and the dynamic changes at levels of transcription factor (TF) regulons during differentiation were revealed. We also find that C5 subset, characterized by activation of lipid metabolism, is in the terminal state of differentiation, and that the abundance of C5 subset is negatively correlated with CRC patients' prognosis. Our findings advance the understanding of circulating monocytes' differentiation into macrophages, identify a new subset associated with CRC prognosis, and reveal a set of TF regulons regulating mononuclear phagocytes differentiation, which are expected to be potential therapeutic targets for reversing immunosuppressive tumor microenvironment.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1011176</identifier><identifier>PMID: 38408082</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Biology and Life Sciences ; Cancer ; Cell cycle ; Cell Differentiation - genetics ; Classification ; Colorectal cancer ; Colorectal carcinoma ; Colorectal Neoplasms - pathology ; Gene expression ; Genetic aspects ; Health aspects ; Humans ; Inflammation ; Leukocytes (mononuclear) ; Lipid metabolism ; Macrophages ; Macrophages - metabolism ; Medical prognosis ; Medicine and Health Sciences ; Monocytes ; Patients ; Phagocytes ; Phagocytes - metabolism ; Physiological aspects ; Prognosis ; RNA ; RNA - metabolism ; Therapeutic targets ; Tissue inhibitor of metalloproteinases ; Tumor microenvironment ; Tumor Microenvironment - genetics ; Tumors</subject><ispartof>PLoS genetics, 2024-02, Vol.20 (2), p.e1011176-e1011176</ispartof><rights>Copyright: © 2024 Ji et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Ji et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 Ji et al 2024 Ji et al</rights><rights>2024 Ji et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c642t-5d944eb9b82ef68fe349288a951b30f05f03d581bb451014fea741dc7aa8426e3</cites><orcidid>0009-0001-1226-4607 ; 0000-0002-9330-0728</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/PMC10919852/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10919852/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23870,27928,27929,53795,53797</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38408082$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Kwiatkowski, David J.</contributor><creatorcontrib>Ji, Tiantian</creatorcontrib><creatorcontrib>Fu, Haoyu</creatorcontrib><creatorcontrib>Wang, Liping</creatorcontrib><creatorcontrib>Chen, Jinyun</creatorcontrib><creatorcontrib>Tian, Shaobo</creatorcontrib><creatorcontrib>Wang, Guobin</creatorcontrib><creatorcontrib>Wang, Lin</creatorcontrib><creatorcontrib>Wang, Zheng</creatorcontrib><title>Single-cell RNA profiling reveals classification and characteristics of mononuclear phagocytes in colorectal cancer</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Colorectal cancer (CRC) is a major cause of cancer mortality and a serious health problem worldwide. Mononuclear phagocytes are the main immune cells in the tumor microenvironment of CRC with remarkable plasticity, and current studies show that macrophages are closely related to tumor progression, invasion and dissemination. To understand the immunological function of mononuclear phagocytes comprehensively and deeply, we use single-cell RNA sequencing and classify mononuclear phagocytes in CRC into 6 different subsets, and characterize the heterogeneity of each subset. We find that tissue inhibitor of metalloproteinases (TIMPs) involved in the differentiation of proinflammatory and anti-inflammatory mononuclear phagocytes. Trajectory of circulating monocytes differentiation into tumor-associated macrophages (TAMs) and the dynamic changes at levels of transcription factor (TF) regulons during differentiation were revealed. We also find that C5 subset, characterized by activation of lipid metabolism, is in the terminal state of differentiation, and that the abundance of C5 subset is negatively correlated with CRC patients' prognosis. Our findings advance the understanding of circulating monocytes' differentiation into macrophages, identify a new subset associated with CRC prognosis, and reveal a set of TF regulons regulating mononuclear phagocytes differentiation, which are expected to be potential therapeutic targets for reversing immunosuppressive tumor microenvironment.</description><subject>Biology and Life Sciences</subject><subject>Cancer</subject><subject>Cell cycle</subject><subject>Cell Differentiation - genetics</subject><subject>Classification</subject><subject>Colorectal cancer</subject><subject>Colorectal carcinoma</subject><subject>Colorectal Neoplasms - pathology</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Inflammation</subject><subject>Leukocytes (mononuclear)</subject><subject>Lipid metabolism</subject><subject>Macrophages</subject><subject>Macrophages - metabolism</subject><subject>Medical prognosis</subject><subject>Medicine and Health Sciences</subject><subject>Monocytes</subject><subject>Patients</subject><subject>Phagocytes</subject><subject>Phagocytes - metabolism</subject><subject>Physiological aspects</subject><subject>Prognosis</subject><subject>RNA</subject><subject>RNA - metabolism</subject><subject>Therapeutic targets</subject><subject>Tissue inhibitor of metalloproteinases</subject><subject>Tumor microenvironment</subject><subject>Tumor Microenvironment - genetics</subject><subject>Tumors</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk12L1DAUhoso7rr6D0QDgujFjEmTtOmVDIsfA4sLu-ptSNPTToZMMibt4v57U6e7TGUvJISU5Dlvet6ck2UvCV4SWpIPWz8Ep-xy34FbEkwIKYtH2SnhnC5Khtnjo--T7FmMW4wpF1X5NDuhgmGBRX6axWvjOgsLDdaiq28rtA--NTZtogA3oGxE2qoYTWu06o13SLkG6Y0KSvcQTOyNjsi3aOedd4O2oALab1Tn9W0PERmHtLc-gO6VRVo5DeF59qRNwvBiWs-yH58_fT__uri4_LI-X10sdMHyfsGbijGoq1rk0BaiBcqqXAhVcVJT3GLeYtpwQeqa8ZQ_a0GVjDS6VEqwvAB6lr0-6O6tj3LyK0qKi4qUVfIwEesD0Xi1lftgdircSq-M_LvhQydVSBlakAzrotI0TVawBuoa2qbQXGCtCOWlSFofp9uGegeNBtcHZWei8xNnNrLzN5LgilSC50nh3aQQ_K8BYi93Jo4Poxz4Icq8ojmjnBGc0Df_oA-nN1GdShkY1_p0sR5F5aoUFU9-8vHHlw9QaTSwM9o7SPUA84D3s4DE9PC779QQo1xfX_0_e_lzzr49Yjep-PpN9HYYyy7OQXYAdfAxBmjvXSZYjs1x54Ycm0NOzZHCXh2_0H3QXTfQP4ISC0M</recordid><startdate>20240226</startdate><enddate>20240226</enddate><creator>Ji, Tiantian</creator><creator>Fu, Haoyu</creator><creator>Wang, Liping</creator><creator>Chen, Jinyun</creator><creator>Tian, Shaobo</creator><creator>Wang, Guobin</creator><creator>Wang, Lin</creator><creator>Wang, Zheng</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0009-0001-1226-4607</orcidid><orcidid>https://orcid.org/0000-0002-9330-0728</orcidid></search><sort><creationdate>20240226</creationdate><title>Single-cell RNA profiling reveals classification and characteristics of mononuclear phagocytes in colorectal cancer</title><author>Ji, Tiantian ; Fu, Haoyu ; Wang, Liping ; Chen, Jinyun ; Tian, Shaobo ; Wang, Guobin ; Wang, Lin ; Wang, Zheng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c642t-5d944eb9b82ef68fe349288a951b30f05f03d581bb451014fea741dc7aa8426e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Biology and Life Sciences</topic><topic>Cancer</topic><topic>Cell cycle</topic><topic>Cell Differentiation - genetics</topic><topic>Classification</topic><topic>Colorectal cancer</topic><topic>Colorectal carcinoma</topic><topic>Colorectal Neoplasms - pathology</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Inflammation</topic><topic>Leukocytes (mononuclear)</topic><topic>Lipid metabolism</topic><topic>Macrophages</topic><topic>Macrophages - metabolism</topic><topic>Medical prognosis</topic><topic>Medicine and Health Sciences</topic><topic>Monocytes</topic><topic>Patients</topic><topic>Phagocytes</topic><topic>Phagocytes - metabolism</topic><topic>Physiological aspects</topic><topic>Prognosis</topic><topic>RNA</topic><topic>RNA - metabolism</topic><topic>Therapeutic targets</topic><topic>Tissue inhibitor of metalloproteinases</topic><topic>Tumor microenvironment</topic><topic>Tumor Microenvironment - genetics</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ji, Tiantian</creatorcontrib><creatorcontrib>Fu, Haoyu</creatorcontrib><creatorcontrib>Wang, Liping</creatorcontrib><creatorcontrib>Chen, Jinyun</creatorcontrib><creatorcontrib>Tian, Shaobo</creatorcontrib><creatorcontrib>Wang, Guobin</creatorcontrib><creatorcontrib>Wang, Lin</creatorcontrib><creatorcontrib>Wang, Zheng</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ji, Tiantian</au><au>Fu, Haoyu</au><au>Wang, Liping</au><au>Chen, Jinyun</au><au>Tian, Shaobo</au><au>Wang, Guobin</au><au>Wang, Lin</au><au>Wang, Zheng</au><au>Kwiatkowski, David J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Single-cell RNA profiling reveals classification and characteristics of mononuclear phagocytes in colorectal cancer</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2024-02-26</date><risdate>2024</risdate><volume>20</volume><issue>2</issue><spage>e1011176</spage><epage>e1011176</epage><pages>e1011176-e1011176</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Colorectal cancer (CRC) is a major cause of cancer mortality and a serious health problem worldwide. Mononuclear phagocytes are the main immune cells in the tumor microenvironment of CRC with remarkable plasticity, and current studies show that macrophages are closely related to tumor progression, invasion and dissemination. To understand the immunological function of mononuclear phagocytes comprehensively and deeply, we use single-cell RNA sequencing and classify mononuclear phagocytes in CRC into 6 different subsets, and characterize the heterogeneity of each subset. We find that tissue inhibitor of metalloproteinases (TIMPs) involved in the differentiation of proinflammatory and anti-inflammatory mononuclear phagocytes. Trajectory of circulating monocytes differentiation into tumor-associated macrophages (TAMs) and the dynamic changes at levels of transcription factor (TF) regulons during differentiation were revealed. We also find that C5 subset, characterized by activation of lipid metabolism, is in the terminal state of differentiation, and that the abundance of C5 subset is negatively correlated with CRC patients' prognosis. Our findings advance the understanding of circulating monocytes' differentiation into macrophages, identify a new subset associated with CRC prognosis, and reveal a set of TF regulons regulating mononuclear phagocytes differentiation, which are expected to be potential therapeutic targets for reversing immunosuppressive tumor microenvironment.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>38408082</pmid><doi>10.1371/journal.pgen.1011176</doi><tpages>e1011176</tpages><orcidid>https://orcid.org/0009-0001-1226-4607</orcidid><orcidid>https://orcid.org/0000-0002-9330-0728</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Biology and Life Sciences Cancer Cell cycle Cell Differentiation - genetics Classification Colorectal cancer Colorectal carcinoma Colorectal Neoplasms - pathology Gene expression Genetic aspects Health aspects Humans Inflammation Leukocytes (mononuclear) Lipid metabolism Macrophages Macrophages - metabolism Medical prognosis Medicine and Health Sciences Monocytes Patients Phagocytes Phagocytes - metabolism Physiological aspects Prognosis RNA RNA - metabolism Therapeutic targets Tissue inhibitor of metalloproteinases Tumor microenvironment Tumor Microenvironment - genetics Tumors |
| title | Single-cell RNA profiling reveals classification and characteristics of mononuclear phagocytes in colorectal cancer |
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