SPP1+ TAM subpopulations in tumor microenvironment promote intravasation and metastasis of head and neck squamous cell carcinoma
Macrophages are heterogeneous cells that play multifaceted roles in cancer progression and metastasis. However, the phenotypic diversity of tumor-associated macrophages (TAMs) in head and neck squamous carcinomas (HNSCC) remains poorly characterized. Here, we comprehensively analyzed the HNSCC singl...
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| Veröffentlicht in: | Cancer gene therapy 2024-02, Vol.31 (2), p.311-321 |
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| creator | Wu, Jiashun Shen, Yi Zeng, Guozhong Liang, Yujie Liao, Guiqing |
| description | Macrophages are heterogeneous cells that play multifaceted roles in cancer progression and metastasis. However, the phenotypic diversity of tumor-associated macrophages (TAMs) in head and neck squamous carcinomas (HNSCC) remains poorly characterized. Here, we comprehensively analyzed the HNSCC single-cell transcriptomic dataset (GSE172577) and identified 5 subsets of myeloid-driven cells as TAMs using Seurat. Deciphering the lineage trajectory of TAMs, we revealed that
FCN1
+
TAMs could give rise to pro-angiogenesis
SPP1
+
CCL18
+
and
SPP1
+
FOLR2
+
populations through
SPP1
−
CCL18
+
and
CXCL9
+
CXCL10
+
TAMs.
SPP1
+
CCL18
+
and
SPP1
+
FOLR2
+
TAMs harbored pro-angiogenic and metastatic transcriptional programs and were correlated with poor survival of HNSCC patients. Our immunostaining examination revealed that infiltration of SPP1
+
TAMs is associated with lymph node metastasis and poor prognosis in patients with HNSCC. Cell-cell communication analysis implied that
SPP1
+
TAM populations may employ SPP1 signaling to activate metastasis-related ECs. In vitro and in vivo studies, we demonstrated that SPP1
hi
TAMs enhanced tumor intravasation and metastasis in HNSCC in a manner dependent on the secretion of SPP1, CCL18, and CXCL8. Taken together, our study characterized the cellular heterogeneity of TAM populations and identified two SPP1
+
TAM populations that play key roles in HNSCC intravasation and metastasis and serve as predictive markers for patients with HNSCC. |
| doi_str_mv | 10.1038/s41417-023-00704-0 |
| format | Article |
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FCN1
+
TAMs could give rise to pro-angiogenesis
SPP1
+
CCL18
+
and
SPP1
+
FOLR2
+
populations through
SPP1
−
CCL18
+
and
CXCL9
+
CXCL10
+
TAMs.
SPP1
+
CCL18
+
and
SPP1
+
FOLR2
+
TAMs harbored pro-angiogenic and metastatic transcriptional programs and were correlated with poor survival of HNSCC patients. Our immunostaining examination revealed that infiltration of SPP1
+
TAMs is associated with lymph node metastasis and poor prognosis in patients with HNSCC. Cell-cell communication analysis implied that
SPP1
+
TAM populations may employ SPP1 signaling to activate metastasis-related ECs. In vitro and in vivo studies, we demonstrated that SPP1
hi
TAMs enhanced tumor intravasation and metastasis in HNSCC in a manner dependent on the secretion of SPP1, CCL18, and CXCL8. Taken together, our study characterized the cellular heterogeneity of TAM populations and identified two SPP1
+
TAM populations that play key roles in HNSCC intravasation and metastasis and serve as predictive markers for patients with HNSCC.</description><identifier>ISSN: 0929-1903</identifier><identifier>EISSN: 1476-5500</identifier><identifier>DOI: 10.1038/s41417-023-00704-0</identifier><identifier>PMID: 38052857</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>13/21 ; 13/95 ; 14/19 ; 38/1 ; 45/91 ; 631/250/2504 ; 631/67/69 ; 692/699/67 ; 82/51 ; Angiogenesis ; Biomedical and Life Sciences ; Biomedicine ; Cell Communication ; Cell interactions ; CXCL10 protein ; Folate Receptor 2 ; Gene Expression ; Gene Therapy ; Head & neck cancer ; Head and neck carcinoma ; Head and Neck Neoplasms - genetics ; Humans ; Lymph nodes ; Macrophages ; Medical prognosis ; Metastases ; Metastasis ; Osteopontin ; Signal Transduction ; Squamous cell carcinoma ; Squamous Cell Carcinoma of Head and Neck - genetics ; Transcriptomics ; Tumor Microenvironment ; Tumors</subject><ispartof>Cancer gene therapy, 2024-02, Vol.31 (2), p.311-321</ispartof><rights>The Author(s), under exclusive licence to Springer Nature America, Inc. 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2023. The Author(s), under exclusive licence to Springer Nature America, Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-6999febecaa4ec6984c9c16c61d9b9cdad56e1091747686b9216fdbf37780a5c3</citedby><cites>FETCH-LOGICAL-c375t-6999febecaa4ec6984c9c16c61d9b9cdad56e1091747686b9216fdbf37780a5c3</cites><orcidid>0009-0001-9411-1443 ; 0000-0002-8658-4304</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41417-023-00704-0$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41417-023-00704-0$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38052857$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wu, Jiashun</creatorcontrib><creatorcontrib>Shen, Yi</creatorcontrib><creatorcontrib>Zeng, Guozhong</creatorcontrib><creatorcontrib>Liang, Yujie</creatorcontrib><creatorcontrib>Liao, Guiqing</creatorcontrib><title>SPP1+ TAM subpopulations in tumor microenvironment promote intravasation and metastasis of head and neck squamous cell carcinoma</title><title>Cancer gene therapy</title><addtitle>Cancer Gene Ther</addtitle><addtitle>Cancer Gene Ther</addtitle><description>Macrophages are heterogeneous cells that play multifaceted roles in cancer progression and metastasis. However, the phenotypic diversity of tumor-associated macrophages (TAMs) in head and neck squamous carcinomas (HNSCC) remains poorly characterized. Here, we comprehensively analyzed the HNSCC single-cell transcriptomic dataset (GSE172577) and identified 5 subsets of myeloid-driven cells as TAMs using Seurat. Deciphering the lineage trajectory of TAMs, we revealed that
FCN1
+
TAMs could give rise to pro-angiogenesis
SPP1
+
CCL18
+
and
SPP1
+
FOLR2
+
populations through
SPP1
−
CCL18
+
and
CXCL9
+
CXCL10
+
TAMs.
SPP1
+
CCL18
+
and
SPP1
+
FOLR2
+
TAMs harbored pro-angiogenic and metastatic transcriptional programs and were correlated with poor survival of HNSCC patients. Our immunostaining examination revealed that infiltration of SPP1
+
TAMs is associated with lymph node metastasis and poor prognosis in patients with HNSCC. Cell-cell communication analysis implied that
SPP1
+
TAM populations may employ SPP1 signaling to activate metastasis-related ECs. In vitro and in vivo studies, we demonstrated that SPP1
hi
TAMs enhanced tumor intravasation and metastasis in HNSCC in a manner dependent on the secretion of SPP1, CCL18, and CXCL8. Taken together, our study characterized the cellular heterogeneity of TAM populations and identified two SPP1
+
TAM populations that play key roles in HNSCC intravasation and metastasis and serve as predictive markers for patients with HNSCC.</description><subject>13/21</subject><subject>13/95</subject><subject>14/19</subject><subject>38/1</subject><subject>45/91</subject><subject>631/250/2504</subject><subject>631/67/69</subject><subject>692/699/67</subject><subject>82/51</subject><subject>Angiogenesis</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cell Communication</subject><subject>Cell interactions</subject><subject>CXCL10 protein</subject><subject>Folate Receptor 2</subject><subject>Gene Expression</subject><subject>Gene Therapy</subject><subject>Head & neck cancer</subject><subject>Head and neck carcinoma</subject><subject>Head and Neck Neoplasms - genetics</subject><subject>Humans</subject><subject>Lymph nodes</subject><subject>Macrophages</subject><subject>Medical prognosis</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Osteopontin</subject><subject>Signal Transduction</subject><subject>Squamous cell carcinoma</subject><subject>Squamous Cell Carcinoma of Head and Neck - genetics</subject><subject>Transcriptomics</subject><subject>Tumor Microenvironment</subject><subject>Tumors</subject><issn>0929-1903</issn><issn>1476-5500</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU9LHTEUxUNR6tP2C3RRAm4EGb2ZzOTPUkRtQVGoXYdM5o6OviTPZEborh_d-J5toQshEMj9nZOTHEK-MDhiwNVxbljDZAU1rwAkNBV8IAvWSFG1LcAWWYCudcU08B2ym_MDQBlK_pHscAVtrVq5IL9_3NywQ3p7ckXz3K3ial7aaYwh0zHQafYxUT-6FDE8jykGj2GiqxR9nLAQU7LPNq8F1IaeepxsLmvMNA70Hm2_Pg7oHml-mq2Pc6YOl0vqbHJjiN5-ItuDXWb8_LbvkZ_nZ7en36rL64vvpyeXleOynSqhtR6wQ2dtg05o1TjtmHCC9brTrrd9K5CBZrK8X4lO10wMfTdwKRXY1vE9crDxLemfZsyT8WN-jWIDllSmVlrpVgJvCrr_H_oQ5xRKOlPrWoEQQopC1Ruq_E7OCQezSqO36ZdhYF77MZt-TOnHrPsxUERf36znzmP_V_KnkALwDZDLKNxh-nf3O7Yv0UidBw</recordid><startdate>20240201</startdate><enddate>20240201</enddate><creator>Wu, Jiashun</creator><creator>Shen, Yi</creator><creator>Zeng, Guozhong</creator><creator>Liang, Yujie</creator><creator>Liao, Guiqing</creator><general>Nature Publishing Group US</general><general>Nature Publishing Group</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>7QP</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0009-0001-9411-1443</orcidid><orcidid>https://orcid.org/0000-0002-8658-4304</orcidid></search><sort><creationdate>20240201</creationdate><title>SPP1+ TAM subpopulations in tumor microenvironment promote intravasation and metastasis of head and neck squamous cell carcinoma</title><author>Wu, Jiashun ; Shen, Yi ; Zeng, Guozhong ; Liang, Yujie ; Liao, Guiqing</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c375t-6999febecaa4ec6984c9c16c61d9b9cdad56e1091747686b9216fdbf37780a5c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>13/21</topic><topic>13/95</topic><topic>14/19</topic><topic>38/1</topic><topic>45/91</topic><topic>631/250/2504</topic><topic>631/67/69</topic><topic>692/699/67</topic><topic>82/51</topic><topic>Angiogenesis</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Cell Communication</topic><topic>Cell interactions</topic><topic>CXCL10 protein</topic><topic>Folate Receptor 2</topic><topic>Gene Expression</topic><topic>Gene Therapy</topic><topic>Head & neck cancer</topic><topic>Head and neck carcinoma</topic><topic>Head and Neck Neoplasms - genetics</topic><topic>Humans</topic><topic>Lymph nodes</topic><topic>Macrophages</topic><topic>Medical prognosis</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>Osteopontin</topic><topic>Signal Transduction</topic><topic>Squamous cell carcinoma</topic><topic>Squamous Cell Carcinoma of Head and Neck - genetics</topic><topic>Transcriptomics</topic><topic>Tumor Microenvironment</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Jiashun</creatorcontrib><creatorcontrib>Shen, Yi</creatorcontrib><creatorcontrib>Zeng, Guozhong</creatorcontrib><creatorcontrib>Liang, Yujie</creatorcontrib><creatorcontrib>Liao, Guiqing</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Cancer gene therapy</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Jiashun</au><au>Shen, Yi</au><au>Zeng, Guozhong</au><au>Liang, Yujie</au><au>Liao, Guiqing</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>SPP1+ TAM subpopulations in tumor microenvironment promote intravasation and metastasis of head and neck squamous cell carcinoma</atitle><jtitle>Cancer gene therapy</jtitle><stitle>Cancer Gene Ther</stitle><addtitle>Cancer Gene Ther</addtitle><date>2024-02-01</date><risdate>2024</risdate><volume>31</volume><issue>2</issue><spage>311</spage><epage>321</epage><pages>311-321</pages><issn>0929-1903</issn><eissn>1476-5500</eissn><abstract>Macrophages are heterogeneous cells that play multifaceted roles in cancer progression and metastasis. However, the phenotypic diversity of tumor-associated macrophages (TAMs) in head and neck squamous carcinomas (HNSCC) remains poorly characterized. Here, we comprehensively analyzed the HNSCC single-cell transcriptomic dataset (GSE172577) and identified 5 subsets of myeloid-driven cells as TAMs using Seurat. Deciphering the lineage trajectory of TAMs, we revealed that
FCN1
+
TAMs could give rise to pro-angiogenesis
SPP1
+
CCL18
+
and
SPP1
+
FOLR2
+
populations through
SPP1
−
CCL18
+
and
CXCL9
+
CXCL10
+
TAMs.
SPP1
+
CCL18
+
and
SPP1
+
FOLR2
+
TAMs harbored pro-angiogenic and metastatic transcriptional programs and were correlated with poor survival of HNSCC patients. Our immunostaining examination revealed that infiltration of SPP1
+
TAMs is associated with lymph node metastasis and poor prognosis in patients with HNSCC. Cell-cell communication analysis implied that
SPP1
+
TAM populations may employ SPP1 signaling to activate metastasis-related ECs. In vitro and in vivo studies, we demonstrated that SPP1
hi
TAMs enhanced tumor intravasation and metastasis in HNSCC in a manner dependent on the secretion of SPP1, CCL18, and CXCL8. Taken together, our study characterized the cellular heterogeneity of TAM populations and identified two SPP1
+
TAM populations that play key roles in HNSCC intravasation and metastasis and serve as predictive markers for patients with HNSCC.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>38052857</pmid><doi>10.1038/s41417-023-00704-0</doi><tpages>11</tpages><orcidid>https://orcid.org/0009-0001-9411-1443</orcidid><orcidid>https://orcid.org/0000-0002-8658-4304</orcidid></addata></record> |
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| subjects | 13/21 13/95 14/19 38/1 45/91 631/250/2504 631/67/69 692/699/67 82/51 Angiogenesis Biomedical and Life Sciences Biomedicine Cell Communication Cell interactions CXCL10 protein Folate Receptor 2 Gene Expression Gene Therapy Head & neck cancer Head and neck carcinoma Head and Neck Neoplasms - genetics Humans Lymph nodes Macrophages Medical prognosis Metastases Metastasis Osteopontin Signal Transduction Squamous cell carcinoma Squamous Cell Carcinoma of Head and Neck - genetics Transcriptomics Tumor Microenvironment Tumors |
| title | SPP1+ TAM subpopulations in tumor microenvironment promote intravasation and metastasis of head and neck squamous cell carcinoma |
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