Increased neutrophil extracellular traps promote metastasis potential of hepatocellular carcinoma via provoking tumorous inflammatory response
Identifieur interne : 000129 ( an2020/Analysis ); précédent : 000128; suivant : 000130Increased neutrophil extracellular traps promote metastasis potential of hepatocellular carcinoma via provoking tumorous inflammatory response
Auteurs : Lu-Yu Yang [République populaire de Chine] ; Qin Luo [République populaire de Chine] ; Lu Lu [République populaire de Chine] ; Wen-Wei Zhu [République populaire de Chine] ; Hao-Ting Sun [République populaire de Chine] ; Ran Wei [République populaire de Chine] ; Zhi-Fei Lin [République populaire de Chine] ; Xiang-Yu Wang [République populaire de Chine] ; Chao-Qun Wang [République populaire de Chine] ; Ming Lu [République populaire de Chine] ; Hu-Liang Jia [République populaire de Chine] ; Jin-Hong Chen [République populaire de Chine] ; Ju-Bo Zhang [République populaire de Chine] ; Lun-Xiu Qin [République populaire de Chine]Source :
- Journal of Hematology & Oncology [ 1756-8722 ] ; 2020.
Abstract
The propensity of the activated neutrophils to form extracellular traps (NETs) is demonstrated in multiple inflammatory conditions. In this study, we investigated the roles of NETs in metastasis of hepatocellular carcinoma (HCC) and further explored the underlying mechanism of how NETs affect metastasis as well as the therapeutic value.
The neutrophils were isolated from the blood of human HCC patients and used to evaluate the formation of NETs. The expression of NET markers was detected in tumor specimens. A LPS-induced NET model was used to investigate the role of NETs on HCC metastasis. RNA-seq was performed to identify the key molecular event triggered by NETs, and their underlying mechanism and therapeutic significance were explored using both in vitro and in vivo assays.
NET formation was enhanced in neutrophils derived from HCC patients, especially those with metastatic HCCs. NETs trapped HCC cells and subsequently induced cell-death resistance and enhanced invasiveness to trigger their metastatic potential, which was mediated by internalization of NETs into trapped HCC cells and activation of Toll-like receptors TLR4/9-COX2 signaling. Inhibition of TLR4/9-COX2 signaling abrogated the NET-aroused metastatic potential. A combination of DNase 1 directly wrecking NETs with anti-inflammation drugs aspirin/hydroxychloroquine effectively reduced HCC metastasis in mice model.
NETs trigger tumorous inflammatory response and fuel HCC metastasis. Targeting NETs rather than neutrophils themselves can be a practice strategy against HCC metastasis.
Url:
DOI: 10.1186/s13045-019-0836-0
PubMed: 31907001
PubMed Central: 6945602
Affiliations:
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sort="Lu, Lu" uniqKey="Lu L" first="Lu" last="Lu">Lu Lu</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Zhu, Wen Wei" sort="Zhu, Wen Wei" uniqKey="Zhu W" first="Wen-Wei" last="Zhu">Wen-Wei Zhu</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Sun, Hao Ting" sort="Sun, Hao Ting" uniqKey="Sun H" first="Hao-Ting" last="Sun">Hao-Ting Sun</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Wei, Ran" sort="Wei, Ran" uniqKey="Wei R" first="Ran" last="Wei">Ran Wei</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Lin, Zhi Fei" sort="Lin, Zhi Fei" uniqKey="Lin Z" first="Zhi-Fei" last="Lin">Zhi-Fei Lin</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Wang, Xiang Yu" sort="Wang, Xiang Yu" uniqKey="Wang X" first="Xiang-Yu" last="Wang">Xiang-Yu Wang</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Wang, Chao Qun" sort="Wang, Chao Qun" uniqKey="Wang C" first="Chao-Qun" last="Wang">Chao-Qun Wang</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Lu, Ming" sort="Lu, Ming" uniqKey="Lu M" first="Ming" last="Lu">Ming Lu</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Jia, Hu Liang" sort="Jia, Hu Liang" uniqKey="Jia H" first="Hu-Liang" last="Jia">Hu-Liang Jia</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Chen, Jin Hong" sort="Chen, Jin Hong" uniqKey="Chen J" first="Jin-Hong" last="Chen">Jin-Hong Chen</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author><author><name sortKey="Zhang, Ju Bo" sort="Zhang, Ju Bo" uniqKey="Zhang J" first="Ju-Bo" last="Zhang">Ju-Bo Zhang</name><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of Infection Disease, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Qin, Lun Xiu" sort="Qin, Lun Xiu" uniqKey="Qin L" first="Lun-Xiu" last="Qin">Lun-Xiu Qin</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Department of General Surgery, Huashan Hospital,</institution><institution>Fudan University,</institution></institution-wrap>12 Urumqi Road (M), Shanghai, 200040 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>12 Urumqi Road (M), Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0125 2443</institution-id><institution-id institution-id-type="GRID">grid.8547.e</institution-id><institution>Cancer Metastasis Institute,</institution><institution>Fudan University,</institution></institution-wrap>Shanghai, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai</wicri:regionArea></affiliation></author></analytic><series><title level="j">Journal of Hematology & Oncology</title><idno type="eISSN">1756-8722</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p id="Par1">The propensity of the activated neutrophils to form extracellular traps (NETs) is demonstrated in multiple inflammatory conditions. In this study, we investigated the roles of NETs in metastasis of hepatocellular carcinoma (HCC) and further explored the underlying mechanism of how NETs affect metastasis as well as the therapeutic value.</p></sec><sec><title>Methods</title><p id="Par2">The neutrophils were isolated from the blood of human HCC patients and used to evaluate the formation of NETs. The expression of NET markers was detected in tumor specimens. A LPS-induced NET model was used to investigate the role of NETs on HCC metastasis. RNA-seq was performed to identify the key molecular event triggered by NETs, and their underlying mechanism and therapeutic significance were explored using both in vitro and in vivo assays.</p></sec><sec><title>Results</title><p id="Par3">NET formation was enhanced in neutrophils derived from HCC patients, especially those with metastatic HCCs. NETs trapped HCC cells and subsequently induced cell-death resistance and enhanced invasiveness to trigger their metastatic potential, which was mediated by internalization of NETs into trapped HCC cells and activation of Toll-like receptors TLR4/9-COX2 signaling. Inhibition of TLR4/9-COX2 signaling abrogated the NET-aroused metastatic potential. A combination of DNase 1 directly wrecking NETs with anti-inflammation drugs aspirin/hydroxychloroquine effectively reduced HCC metastasis in mice model.</p></sec><sec><title>Conclusions</title><p id="Par4">NETs trigger tumorous inflammatory response and fuel HCC metastasis. Targeting NETs rather than neutrophils themselves can be a practice strategy against HCC metastasis.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Lambert, Aw" uniqKey="Lambert A">AW Lambert</name></author><author><name sortKey="Pattabiraman, Dr" uniqKey="Pattabiraman D">DR Pattabiraman</name></author><author><name sortKey="Weinberg, Ra" uniqKey="Weinberg R">RA Weinberg</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Quail, Df" uniqKey="Quail D">DF Quail</name></author><author><name sortKey="Joyce, Ja" uniqKey="Joyce J">JA Joyce</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dannenberg, Aj" uniqKey="Dannenberg A">AJ Dannenberg</name></author><author><name sortKey="Subbaramaiah, K" uniqKey="Subbaramaiah K">K Subbaramaiah</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tuting, T" uniqKey="Tuting T">T 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sortKey="Lin, Zhi Fei" sort="Lin, Zhi Fei" uniqKey="Lin Z" first="Zhi-Fei" last="Lin">Zhi-Fei Lin</name><name sortKey="Lu, Lu" sort="Lu, Lu" uniqKey="Lu L" first="Lu" last="Lu">Lu Lu</name><name sortKey="Lu, Lu" sort="Lu, Lu" uniqKey="Lu L" first="Lu" last="Lu">Lu Lu</name><name sortKey="Lu, Ming" sort="Lu, Ming" uniqKey="Lu M" first="Ming" last="Lu">Ming Lu</name><name sortKey="Lu, Ming" sort="Lu, Ming" uniqKey="Lu M" first="Ming" last="Lu">Ming Lu</name><name sortKey="Luo, Qin" sort="Luo, Qin" uniqKey="Luo Q" first="Qin" last="Luo">Qin Luo</name><name sortKey="Qin, Lun Xiu" sort="Qin, Lun Xiu" uniqKey="Qin L" first="Lun-Xiu" last="Qin">Lun-Xiu Qin</name><name sortKey="Qin, Lun Xiu" sort="Qin, Lun Xiu" uniqKey="Qin L" first="Lun-Xiu" last="Qin">Lun-Xiu Qin</name><name sortKey="Sun, Hao Ting" sort="Sun, Hao Ting" uniqKey="Sun H" first="Hao-Ting" last="Sun">Hao-Ting Sun</name><name sortKey="Sun, Hao Ting" sort="Sun, Hao Ting" uniqKey="Sun H" first="Hao-Ting" last="Sun">Hao-Ting Sun</name><name sortKey="Wang, Chao Qun" sort="Wang, Chao Qun" uniqKey="Wang C" first="Chao-Qun" last="Wang">Chao-Qun Wang</name><name sortKey="Wang, Chao Qun" sort="Wang, Chao Qun" uniqKey="Wang C" first="Chao-Qun" last="Wang">Chao-Qun Wang</name><name sortKey="Wang, Xiang Yu" sort="Wang, Xiang Yu" uniqKey="Wang X" first="Xiang-Yu" last="Wang">Xiang-Yu Wang</name><name sortKey="Wang, Xiang Yu" sort="Wang, Xiang Yu" uniqKey="Wang X" first="Xiang-Yu" last="Wang">Xiang-Yu Wang</name><name sortKey="Wei, Ran" sort="Wei, Ran" uniqKey="Wei R" first="Ran" last="Wei">Ran Wei</name><name sortKey="Wei, Ran" sort="Wei, Ran" uniqKey="Wei R" first="Ran" last="Wei">Ran Wei</name><name sortKey="Yang, Lu Yu" sort="Yang, Lu Yu" uniqKey="Yang L" first="Lu-Yu" last="Yang">Lu-Yu Yang</name><name sortKey="Zhang, Ju Bo" sort="Zhang, Ju Bo" uniqKey="Zhang J" first="Ju-Bo" last="Zhang">Ju-Bo Zhang</name><name sortKey="Zhang, Ju Bo" sort="Zhang, Ju Bo" uniqKey="Zhang J" first="Ju-Bo" last="Zhang">Ju-Bo Zhang</name><name sortKey="Zhu, Wen Wei" sort="Zhu, Wen Wei" uniqKey="Zhu W" first="Wen-Wei" last="Zhu">Wen-Wei Zhu</name><name sortKey="Zhu, Wen Wei" sort="Zhu, Wen Wei" uniqKey="Zhu W" first="Wen-Wei" last="Zhu">Wen-Wei Zhu</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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