Cytotoxic T-Cell Trafficking Chemokine Profiles Correlate With Defined Mucosal Microbial Communities in Colorectal Cancer
The involvement of gut microbiota in T-cell trafficking into tumor tissue of colorectal cancer (CRC) remains to be further elucidated. The current study aimed to evaluate the expression of major cytotoxic T-cell trafficking chemokines (CTTCs) and chemokine-associated microbiota profiles in both tumo...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2021-09-01
|
| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.715559/full |
| _version_ | 1818609624541036544 |
|---|---|
| author | Jiali Zhang Jiali Zhang Ji Tao Ruo-Nan Gao Zhi-Yuan Wei Yu-Shan He Chun-Yan Ren Qi-Chun Li Yan-Shan Liu Ke-Wei Wang Ke-Wei Wang Gong Yang Gong Yang Chengjia Qian Jian-Huan Chen |
| author_facet | Jiali Zhang Jiali Zhang Ji Tao Ruo-Nan Gao Zhi-Yuan Wei Yu-Shan He Chun-Yan Ren Qi-Chun Li Yan-Shan Liu Ke-Wei Wang Ke-Wei Wang Gong Yang Gong Yang Chengjia Qian Jian-Huan Chen |
| author_sort | Jiali Zhang |
| collection | DOAJ |
| description | The involvement of gut microbiota in T-cell trafficking into tumor tissue of colorectal cancer (CRC) remains to be further elucidated. The current study aimed to evaluate the expression of major cytotoxic T-cell trafficking chemokines (CTTCs) and chemokine-associated microbiota profiles in both tumor and adjacent normal tissues during CRC progression. We analyzed the expression of chemokine C-X-C motif ligands 9, 10, and 11 (CXCL9, CXCL10, and CXCL11), and C-C motif ligand 5 (CCL5), characterized gut mucosa-associated microbiota (MAM), and investigated their correlations in CRC patients. Our results showed that the expression of CXCL9, CXCL10, and CXCL11 was significantly higher in tumor than in adjacent normal tissues in 136 CRC patients. Notably, the high expression of CXCL9 in tumor tissues was associated with enhanced CD8+ T-cell infiltration and improved survival. Moreover, the MAM in tumor tissues showed reduction of microbial diversity and increase of oral bacteria. Microbial network analysis identified differences in microbial composition and structure between tumor and adjacent normal tissues. In addition, stronger associations between oral bacteria and other gut microbes were observed. Furthermore, the correlation analysis between the defined MAM and individual CTTCs showed that the CTTCs’ correlated operational taxonomic units (OTUs) in tumor and adjacent normal tissues rarely overlap with each other. Notably, all the enriched OTUs were positively correlated with the CTTCs in either tumor or adjacent normal tissues. Our findings demonstrated stronger interactions between oral bacteria and gut microbes, and a shifted correlation pattern between MAM and major CTTCs in tumor tissues, underlining possible mechanisms of gut microbiota–host interaction in CRC. |
| first_indexed | 2024-12-16T15:01:30Z |
| format | Article |
| id | doaj.art-c06b04db376347a496aff85b9bd1af21 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-16T15:01:30Z |
| publishDate | 2021-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-c06b04db376347a496aff85b9bd1af212022-12-21T22:27:16ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-09-011210.3389/fimmu.2021.715559715559Cytotoxic T-Cell Trafficking Chemokine Profiles Correlate With Defined Mucosal Microbial Communities in Colorectal CancerJiali Zhang0Jiali Zhang1Ji Tao2Ruo-Nan Gao3Zhi-Yuan Wei4Yu-Shan He5Chun-Yan Ren6Qi-Chun Li7Yan-Shan Liu8Ke-Wei Wang9Ke-Wei Wang10Gong Yang11Gong Yang12Chengjia Qian13Jian-Huan Chen14Laboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaCentral Laboratory, The Fifth People’s Hospital of Shanghai Fudan University, Shanghai, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaDepartment of Hospital Infection, Affiliated Hospital of Jiangnan University, Wuxi, ChinaCentral Laboratory, The Fifth People’s Hospital of Shanghai Fudan University, Shanghai, ChinaCancer Institute, Fudan University Shanghai Cancer Center, Shanghai, ChinaDepartment of General Surgery, Affiliated Hospital of Jiangnan University, Wuxi, ChinaLaboratory of Genomic and Precision Medicine, Wuxi School of Medicine, Jiangnan University, Wuxi, ChinaThe involvement of gut microbiota in T-cell trafficking into tumor tissue of colorectal cancer (CRC) remains to be further elucidated. The current study aimed to evaluate the expression of major cytotoxic T-cell trafficking chemokines (CTTCs) and chemokine-associated microbiota profiles in both tumor and adjacent normal tissues during CRC progression. We analyzed the expression of chemokine C-X-C motif ligands 9, 10, and 11 (CXCL9, CXCL10, and CXCL11), and C-C motif ligand 5 (CCL5), characterized gut mucosa-associated microbiota (MAM), and investigated their correlations in CRC patients. Our results showed that the expression of CXCL9, CXCL10, and CXCL11 was significantly higher in tumor than in adjacent normal tissues in 136 CRC patients. Notably, the high expression of CXCL9 in tumor tissues was associated with enhanced CD8+ T-cell infiltration and improved survival. Moreover, the MAM in tumor tissues showed reduction of microbial diversity and increase of oral bacteria. Microbial network analysis identified differences in microbial composition and structure between tumor and adjacent normal tissues. In addition, stronger associations between oral bacteria and other gut microbes were observed. Furthermore, the correlation analysis between the defined MAM and individual CTTCs showed that the CTTCs’ correlated operational taxonomic units (OTUs) in tumor and adjacent normal tissues rarely overlap with each other. Notably, all the enriched OTUs were positively correlated with the CTTCs in either tumor or adjacent normal tissues. Our findings demonstrated stronger interactions between oral bacteria and gut microbes, and a shifted correlation pattern between MAM and major CTTCs in tumor tissues, underlining possible mechanisms of gut microbiota–host interaction in CRC.https://www.frontiersin.org/articles/10.3389/fimmu.2021.715559/fullT cell traffickingmucosa-associated bacteriatumoradjacent normal tissuescolorectal cancerchemokines |
| spellingShingle | Jiali Zhang Jiali Zhang Ji Tao Ruo-Nan Gao Zhi-Yuan Wei Yu-Shan He Chun-Yan Ren Qi-Chun Li Yan-Shan Liu Ke-Wei Wang Ke-Wei Wang Gong Yang Gong Yang Chengjia Qian Jian-Huan Chen Cytotoxic T-Cell Trafficking Chemokine Profiles Correlate With Defined Mucosal Microbial Communities in Colorectal Cancer Frontiers in Immunology T cell trafficking mucosa-associated bacteria tumor adjacent normal tissues colorectal cancer chemokines |
| title | Cytotoxic T-Cell Trafficking Chemokine Profiles Correlate With Defined Mucosal Microbial Communities in Colorectal Cancer |
| title_full | Cytotoxic T-Cell Trafficking Chemokine Profiles Correlate With Defined Mucosal Microbial Communities in Colorectal Cancer |
| title_fullStr | Cytotoxic T-Cell Trafficking Chemokine Profiles Correlate With Defined Mucosal Microbial Communities in Colorectal Cancer |
| title_full_unstemmed | Cytotoxic T-Cell Trafficking Chemokine Profiles Correlate With Defined Mucosal Microbial Communities in Colorectal Cancer |
| title_short | Cytotoxic T-Cell Trafficking Chemokine Profiles Correlate With Defined Mucosal Microbial Communities in Colorectal Cancer |
| title_sort | cytotoxic t cell trafficking chemokine profiles correlate with defined mucosal microbial communities in colorectal cancer |
| topic | T cell trafficking mucosa-associated bacteria tumor adjacent normal tissues colorectal cancer chemokines |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2021.715559/full |
| work_keys_str_mv | AT jializhang cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT jializhang cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT jitao cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT ruonangao cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT zhiyuanwei cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT yushanhe cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT chunyanren cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT qichunli cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT yanshanliu cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT keweiwang cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT keweiwang cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT gongyang cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT gongyang cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT chengjiaqian cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer AT jianhuanchen cytotoxictcelltraffickingchemokineprofilescorrelatewithdefinedmucosalmicrobialcommunitiesincolorectalcancer |