A Positive Feedback Loop Between Cancer Stem‐Like Cells and Tumor‐Associated Neutrophils Controls Hepatocellular Carcinoma Progression
Tumor‐associated neutrophils (TANs) play a crucial role in tumor development and progression in the cancer microenvironment. Despite increased understanding of TAN contributions to hepatocellular carcinoma (HCC) progression and prognosis, the direct interaction between TANs and HCC cells is not full...
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| Published in | Hepatology (Baltimore, Md.) Vol. 70; no. 4; pp. 1214 - 1230 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
01.10.2019
|
| Online Access | Get full text |
| ISSN | 0270-9139 1527-3350 1527-3350 |
| DOI | 10.1002/hep.30630 |
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| Abstract | Tumor‐associated neutrophils (TANs) play a crucial role in tumor development and progression in the cancer microenvironment. Despite increased understanding of TAN contributions to hepatocellular carcinoma (HCC) progression and prognosis, the direct interaction between TANs and HCC cells is not fully understood. In this study, we tested the effect of TANs on HCC cells in vitro and in vivo and investigated the mechanism of interaction between them. Our results showed that TANs secreted bone morphogenetic protein 2 and transforming growth factor beta 2 and triggered microRNA 301b‐3p (miR‐301‐3p) expression in HCC cells, subsequently suppressed gene expression of limbic system–associated membrane protein (LSAMP) and CYLD lysine 63 deubiquitinase (CYLD), and increased stem cell characteristics in HCC cells. These TAN‐induced HCC stem‐like cells were hyperactive in nuclear factor kappa B signaling, secreted higher levels of chemokine (C‐X‐C motif) ligand 5 (CXCL5), and recruited more TAN infiltration, suggesting a positive feedback loop. In clinical HCC samples, increased TANs correlated with elevated miR‐301b‐3p, decreased LSAMP and CYLD expression, and increased nuclear p65 accumulation and CXCL5 expression, all of which predicted patient outcome. Conclusion: Our work identified a positive feedback loop governing cancer stem‐like cells and TANs in HCC that controls tumor progression and patient outcome. |
|---|---|
| AbstractList | Tumor-associated neutrophils (TANs) play a crucial role in tumor development and progression in the cancer microenvironment. Despite increased understanding of TAN contributions to hepatocellular carcinoma (HCC) progression and prognosis, the direct interaction between TANs and HCC cells is not fully understood. In this study, we tested the effect of TANs on HCC cells in vitro and in vivo and investigated the mechanism of interaction between them. Our results showed that TANs secreted bone morphogenetic protein 2 and transforming growth factor beta 2 and triggered microRNA 301b-3p (miR-301-3p) expression in HCC cells, subsequently suppressed gene expression of limbic system-associated membrane protein (LSAMP) and CYLD lysine 63 deubiquitinase (CYLD), and increased stem cell characteristics in HCC cells. These TAN-induced HCC stem-like cells were hyperactive in nuclear factor kappa B signaling, secreted higher levels of chemokine (C-X-C motif) ligand 5 (CXCL5), and recruited more TAN infiltration, suggesting a positive feedback loop. In clinical HCC samples, increased TANs correlated with elevated miR-301b-3p, decreased LSAMP and CYLD expression, and increased nuclear p65 accumulation and CXCL5 expression, all of which predicted patient outcome. Conclusion: Our work identified a positive feedback loop governing cancer stem-like cells and TANs in HCC that controls tumor progression and patient outcome. Tumor‐associated neutrophils (TANs) play a crucial role in tumor development and progression in the cancer microenvironment. Despite increased understanding of TAN contributions to hepatocellular carcinoma (HCC) progression and prognosis, the direct interaction between TANs and HCC cells is not fully understood. In this study, we tested the effect of TANs on HCC cells in vitro and in vivo and investigated the mechanism of interaction between them. Our results showed that TANs secreted bone morphogenetic protein 2 and transforming growth factor beta 2 and triggered microRNA 301b‐3p (miR‐301‐3p) expression in HCC cells, subsequently suppressed gene expression of limbic system–associated membrane protein (LSAMP) and CYLD lysine 63 deubiquitinase (CYLD), and increased stem cell characteristics in HCC cells. These TAN‐induced HCC stem‐like cells were hyperactive in nuclear factor kappa B signaling, secreted higher levels of chemokine (C‐X‐C motif) ligand 5 (CXCL5), and recruited more TAN infiltration, suggesting a positive feedback loop. In clinical HCC samples, increased TANs correlated with elevated miR‐301b‐3p, decreased LSAMP and CYLD expression, and increased nuclear p65 accumulation and CXCL5 expression, all of which predicted patient outcome. Conclusion : Our work identified a positive feedback loop governing cancer stem‐like cells and TANs in HCC that controls tumor progression and patient outcome. Tumor-associated neutrophils (TANs) play a crucial role in tumor development and progression in the cancer microenvironment. Despite increased understanding of TAN contributions to hepatocellular carcinoma (HCC) progression and prognosis, the direct interaction between TANs and HCC cells is not fully understood. In this study, we tested the effect of TANs on HCC cells in vitro and in vivo and investigated the mechanism of interaction between them. Our results showed that TANs secreted bone morphogenetic protein 2 and transforming growth factor beta 2 and triggered microRNA 301b-3p (miR-301-3p) expression in HCC cells, subsequently suppressed gene expression of limbic system-associated membrane protein (LSAMP) and CYLD lysine 63 deubiquitinase (CYLD), and increased stem cell characteristics in HCC cells. These TAN-induced HCC stem-like cells were hyperactive in nuclear factor kappa B signaling, secreted higher levels of chemokine (C-X-C motif) ligand 5 (CXCL5), and recruited more TAN infiltration, suggesting a positive feedback loop. In clinical HCC samples, increased TANs correlated with elevated miR-301b-3p, decreased LSAMP and CYLD expression, and increased nuclear p65 accumulation and CXCL5 expression, all of which predicted patient outcome. Conclusion: Our work identified a positive feedback loop governing cancer stem-like cells and TANs in HCC that controls tumor progression and patient outcome.Tumor-associated neutrophils (TANs) play a crucial role in tumor development and progression in the cancer microenvironment. Despite increased understanding of TAN contributions to hepatocellular carcinoma (HCC) progression and prognosis, the direct interaction between TANs and HCC cells is not fully understood. In this study, we tested the effect of TANs on HCC cells in vitro and in vivo and investigated the mechanism of interaction between them. Our results showed that TANs secreted bone morphogenetic protein 2 and transforming growth factor beta 2 and triggered microRNA 301b-3p (miR-301-3p) expression in HCC cells, subsequently suppressed gene expression of limbic system-associated membrane protein (LSAMP) and CYLD lysine 63 deubiquitinase (CYLD), and increased stem cell characteristics in HCC cells. These TAN-induced HCC stem-like cells were hyperactive in nuclear factor kappa B signaling, secreted higher levels of chemokine (C-X-C motif) ligand 5 (CXCL5), and recruited more TAN infiltration, suggesting a positive feedback loop. In clinical HCC samples, increased TANs correlated with elevated miR-301b-3p, decreased LSAMP and CYLD expression, and increased nuclear p65 accumulation and CXCL5 expression, all of which predicted patient outcome. Conclusion: Our work identified a positive feedback loop governing cancer stem-like cells and TANs in HCC that controls tumor progression and patient outcome. |
| Author | Zhou, Jian Zhou, Shao‐Lai Xin, Hao‐Yang Fan, Jia Wang, Zheng Hu, Zhi‐Qiang Luo, Chu‐Bin Huang, Xiao‐Wu Yang, Xin‐Rong Cao, Ya Zhou, Zheng‐Jun Yin, Dan Shi, Ying‐Hong |
| Author_xml | – sequence: 1 givenname: Shao‐Lai surname: Zhou fullname: Zhou, Shao‐Lai organization: Fudan University – sequence: 2 givenname: Dan surname: Yin fullname: Yin, Dan organization: Fudan University – sequence: 3 givenname: Zhi‐Qiang surname: Hu fullname: Hu, Zhi‐Qiang organization: Fudan University – sequence: 4 givenname: Chu‐Bin surname: Luo fullname: Luo, Chu‐Bin organization: Fudan University – sequence: 5 givenname: Zheng‐Jun surname: Zhou fullname: Zhou, Zheng‐Jun organization: Fudan University – sequence: 6 givenname: Hao‐Yang surname: Xin fullname: Xin, Hao‐Yang organization: Fudan University – sequence: 7 givenname: Xin‐Rong surname: Yang fullname: Yang, Xin‐Rong organization: Fudan University – sequence: 8 givenname: Ying‐Hong surname: Shi fullname: Shi, Ying‐Hong organization: Fudan University – sequence: 9 givenname: Zheng surname: Wang fullname: Wang, Zheng organization: Fudan University – sequence: 10 givenname: Xiao‐Wu surname: Huang fullname: Huang, Xiao‐Wu organization: Zhongshan Hospital, Fudan University – sequence: 11 givenname: Ya surname: Cao fullname: Cao, Ya organization: Ministry of Education – sequence: 12 givenname: Jia surname: Fan fullname: Fan, Jia organization: Fudan University – sequence: 13 givenname: Jian surname: Zhou fullname: Zhou, Jian email: zhou.jian@zs-hospital.sh.cn organization: Fudan University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30933361$$D View this record in MEDLINE/PubMed |
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| Title | A Positive Feedback Loop Between Cancer Stem‐Like Cells and Tumor‐Associated Neutrophils Controls Hepatocellular Carcinoma Progression |
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