Fusobacterium nucleatum Promotes Metastasis in Colorectal Cancer by Activating Autophagy Signaling via the Upregulation of CARD3 Expression
Identifieur interne : 000D97 ( Ncbi/Merge ); précédent : 000D96; suivant : 000D98Fusobacterium nucleatum Promotes Metastasis in Colorectal Cancer by Activating Autophagy Signaling via the Upregulation of CARD3 Expression
Auteurs : Yongyu Chen [République populaire de Chine] ; Yan Chen [République populaire de Chine] ; Jixiang Zhang [République populaire de Chine] ; Pan Cao [République populaire de Chine] ; Wenhao Su [République populaire de Chine] ; Yunchao Deng [République populaire de Chine] ; Na Zhan [République populaire de Chine] ; Xiangsheng Fu [République populaire de Chine] ; Yun Huang [États-Unis] ; Weiguo Dong [République populaire de Chine]Source :
- Theranostics [ 1838-7640 ] ; 2020.
Abstract
Url:
DOI: 10.7150/thno.38870
PubMed: 31903123
PubMed Central: 6929621
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en"><italic>Fusobacterium nucleatum</italic> Promotes Metastasis in Colorectal Cancer by Activating Autophagy Signaling via the Upregulation of CARD3 Expression</title><author><name sortKey="Chen, Yongyu" sort="Chen, Yongyu" uniqKey="Chen Y" first="Yongyu" last="Chen">Yongyu Chen</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Yan" sort="Chen, Yan" uniqKey="Chen Y" first="Yan" last="Chen">Yan Chen</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Jixiang" sort="Zhang, Jixiang" uniqKey="Zhang J" first="Jixiang" last="Zhang">Jixiang Zhang</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Cao, Pan" sort="Cao, Pan" uniqKey="Cao P" first="Pan" last="Cao">Pan Cao</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Su, Wenhao" sort="Su, Wenhao" uniqKey="Su W" first="Wenhao" last="Su">Wenhao Su</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Deng, Yunchao" sort="Deng, Yunchao" uniqKey="Deng Y" first="Yunchao" last="Deng">Yunchao Deng</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Zhan, Na" sort="Zhan, Na" uniqKey="Zhan N" first="Na" last="Zhan">Na Zhan</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Fu, Xiangsheng" sort="Fu, Xiangsheng" uniqKey="Fu X" first="Xiangsheng" last="Fu">Xiangsheng Fu</name><affiliation wicri:level="1"><nlm:aff id="A4">Department of Gastroenterology, The Affiliated Hospitalof North Sichuan Medical College, Road Wenhua 63#, Region Shunqing, Nanchong City 637000, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, The Affiliated Hospitalof North Sichuan Medical College, Road Wenhua 63#, Region Shunqing, Nanchong City 637000</wicri:regionArea><wicri:noRegion>Nanchong City 637000</wicri:noRegion></affiliation></author><author><name sortKey="Huang, Yun" sort="Huang, Yun" uniqKey="Huang Y" first="Yun" last="Huang">Yun Huang</name><affiliation wicri:level="1"><nlm:aff id="A5">Center for Epigenetics & Disease Prevention, Institute of Biosciences and Technology, Texas A&M University, Houston, TX77030, USA.</nlm:aff><country xml:lang="fr" wicri:curation="lc">États-Unis</country><wicri:regionArea>Center for Epigenetics & Disease Prevention, Institute of Biosciences and Technology, Texas A&M University, Houston, TX77030</wicri:regionArea><wicri:noRegion>TX77030</wicri:noRegion></affiliation></author><author><name sortKey="Dong, Weiguo" sort="Dong, Weiguo" uniqKey="Dong W" first="Weiguo" last="Dong">Weiguo Dong</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31903123</idno><idno type="pmc">6929621</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6929621</idno><idno type="RBID">PMC:6929621</idno><idno type="doi">10.7150/thno.38870</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">000824</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000824</idno><idno type="wicri:Area/Pmc/Curation">000824</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000824</idno><idno type="wicri:Area/Pmc/Checkpoint">000220</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000220</idno><idno type="wicri:Area/Ncbi/Merge">000D97</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main"><italic>Fusobacterium nucleatum</italic> Promotes Metastasis in Colorectal Cancer by Activating Autophagy Signaling via the Upregulation of CARD3 Expression</title><author><name sortKey="Chen, Yongyu" sort="Chen, Yongyu" uniqKey="Chen Y" first="Yongyu" last="Chen">Yongyu Chen</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Yan" sort="Chen, Yan" uniqKey="Chen Y" first="Yan" last="Chen">Yan Chen</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Jixiang" sort="Zhang, Jixiang" uniqKey="Zhang J" first="Jixiang" last="Zhang">Jixiang Zhang</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Cao, Pan" sort="Cao, Pan" uniqKey="Cao P" first="Pan" last="Cao">Pan Cao</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Su, Wenhao" sort="Su, Wenhao" uniqKey="Su W" first="Wenhao" last="Su">Wenhao Su</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Deng, Yunchao" sort="Deng, Yunchao" uniqKey="Deng Y" first="Yunchao" last="Deng">Yunchao Deng</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Zhan, Na" sort="Zhan, Na" uniqKey="Zhan N" first="Na" last="Zhan">Na Zhan</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A3">Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author><author><name sortKey="Fu, Xiangsheng" sort="Fu, Xiangsheng" uniqKey="Fu X" first="Xiangsheng" last="Fu">Xiangsheng Fu</name><affiliation wicri:level="1"><nlm:aff id="A4">Department of Gastroenterology, The Affiliated Hospitalof North Sichuan Medical College, Road Wenhua 63#, Region Shunqing, Nanchong City 637000, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, The Affiliated Hospitalof North Sichuan Medical College, Road Wenhua 63#, Region Shunqing, Nanchong City 637000</wicri:regionArea><wicri:noRegion>Nanchong City 637000</wicri:noRegion></affiliation></author><author><name sortKey="Huang, Yun" sort="Huang, Yun" uniqKey="Huang Y" first="Yun" last="Huang">Yun Huang</name><affiliation wicri:level="1"><nlm:aff id="A5">Center for Epigenetics & Disease Prevention, Institute of Biosciences and Technology, Texas A&M University, Houston, TX77030, USA.</nlm:aff><country xml:lang="fr" wicri:curation="lc">États-Unis</country><wicri:regionArea>Center for Epigenetics & Disease Prevention, Institute of Biosciences and Technology, Texas A&M University, Houston, TX77030</wicri:regionArea><wicri:noRegion>TX77030</wicri:noRegion></affiliation></author><author><name sortKey="Dong, Weiguo" sort="Dong, Weiguo" uniqKey="Dong W" first="Weiguo" last="Dong">Weiguo Dong</name><affiliation wicri:level="1"><nlm:aff id="A1">Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="A2">Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province</wicri:regionArea><wicri:noRegion>Hubei Province</wicri:noRegion></affiliation></author></analytic><series><title level="j">Theranostics</title><idno type="eISSN">1838-7640</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><bold>Aims</bold>: We aimed to measure the abundance of <italic>Fusobacterium nucleatum</italic> (<italic>F. nucleatum</italic>) in colorectal cancer (CRC) tissues from patients and to uncover the function of this bacterium in colorectal tumor metastasis.</p><p><bold>Methods</bold>: We collected metastatic and non-metastatic CRC tissues to analyze <italic>F. nucleatum</italic> abundance. Cells were incubated with <italic>F. nucleatum</italic> or chloroquine (CQ) or were transfected with CARD3-targeting siRNA; the expression of mRNAs and proteins was then measured. CRC cells stably transfected with shRNA-luc were mixed with <italic>F. nucleatum</italic> and intravenously injected into BALB/cJ mice. APC<sup>Min/+</sup>, CARD3<sup>-/-</sup>and CARD3<sup>wt</sup> C57BL mice were given <italic>F. nucleatum</italic>; some mice were given azoxymethane (AOM) and dextran sodium sulfate (DSS).</p><p><bold>Results</bold>: <italic>F. nucleatum</italic> was abundant in CRC tissues from patients with metastasis. <italic>F. nucleatum</italic> infection increased CRC cell motility and upregulated the expression of CARD3, LC3-II, Beclin1 and Vimentin, and downregulated the expression of E-cadherin and P62 in CRC cells. These effects were attenuated by treatment with CQ, siCARD3 or both. APC<sup>Min/+</sup> mice gavaged with <italic>F. nucleatum</italic> developed more aggressive tumors than control mice. After AOM/DSS administration, the colorectums of CARD3<sup>-/-</sup> mice had fewer tumors than those of control mice. Tumors from CARD3<sup>-/-</sup> mice had lower levels of LC3-II and Beclin1 and higher levels of P62 than those from control mice. BALB/cJ mice injected with both CT26-luc cells and <italic>F. nucleatum</italic> formed more metastases than control mice. CQ treatment, CARD3 knockdown or both reduced the ability of CT26-luc cells to form metastases <italic>in vivo</italic>.</p><p><bold>Conclusions</bold>: <italic>F. nucleatum</italic> is enriched in CRC tissues from patients with metastasis. <italic>F. nucleatum</italic> orchestrates CARD3 and autophagy to control CRC metastasis. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Theranostics</journal-id><journal-id journal-id-type="iso-abbrev">Theranostics</journal-id><journal-id journal-id-type="publisher-id">thno</journal-id><journal-title-group><journal-title>Theranostics</journal-title></journal-title-group><issn pub-type="epub">1838-7640</issn><publisher><publisher-name>Ivyspring International Publisher</publisher-name><publisher-loc>Sydney</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31903123</article-id><article-id pub-id-type="pmc">6929621</article-id><article-id pub-id-type="doi">10.7150/thno.38870</article-id><article-id pub-id-type="publisher-id">thnov10p0323</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Paper</subject></subj-group></article-categories><title-group><article-title><italic>Fusobacterium nucleatum</italic> Promotes Metastasis in Colorectal Cancer by Activating Autophagy Signaling via the Upregulation of CARD3 Expression</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Yongyu</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref><xref ref-type="author-notes" rid="FNA_number">#</xref></contrib><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Yan</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref><xref ref-type="author-notes" rid="FNA_number">#</xref></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Jixiang</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref><xref ref-type="aff" rid="A3">3</xref></contrib><contrib contrib-type="author"><name><surname>Cao</surname><given-names>Pan</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref></contrib><contrib contrib-type="author"><name><surname>Su</surname><given-names>Wenhao</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref><xref ref-type="aff" rid="A3">3</xref></contrib><contrib contrib-type="author"><name><surname>Deng</surname><given-names>Yunchao</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref></contrib><contrib contrib-type="author"><name><surname>Zhan</surname><given-names>Na</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref><xref ref-type="aff" rid="A3">3</xref></contrib><contrib contrib-type="author"><name><surname>Fu</surname><given-names>Xiangsheng</given-names></name><xref ref-type="aff" rid="A4">4</xref></contrib><contrib contrib-type="author"><name><surname>Huang</surname><given-names>Yun</given-names></name><xref ref-type="aff" rid="A5">5</xref></contrib><contrib contrib-type="author"><name><surname>Dong</surname><given-names>Weiguo</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref><xref ref-type="corresp" rid="FNA_envelop">✉</xref></contrib></contrib-group><aff id="A1"><label>1</label>Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</aff><aff id="A2"><label>2</label>Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, Hubei Province, China.</aff><aff id="A3"><label>3</label>Central Laboratory, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China.</aff><aff id="A4"><label>4</label>Department of Gastroenterology, The Affiliated Hospitalof North Sichuan Medical College, Road Wenhua 63#, Region Shunqing, Nanchong City 637000, China.</aff><aff id="A5"><label>5</label>Center for Epigenetics & Disease Prevention, Institute of Biosciences and Technology, Texas A&M University, Houston, TX77030, USA.</aff><author-notes><corresp id="FNA_envelop">✉ Corresponding author: Weiguo Dong, MD and PhD, Department of Gastroenterology, Key Laboratory of Hubei Province for Digestive System Disease, Renmin Hospital of Wuhan University, Jiefang Road 238, Wuhan 430060, China. E-mail, <email>dongweiguo@whu.edu.cn</email>, Tel., +86 13986167388.</corresp><fn fn-type="equal" id="FNA_number"><p># These authors contributed equally to this work.</p></fn><fn fn-type="COI-statement"><p>Competing Interests: The authors have declared that no competing interest exists.</p></fn></author-notes><pub-date pub-type="collection"><year>2020</year></pub-date><pub-date pub-type="epub"><day>1</day><month>1</month><year>2020</year></pub-date><volume>10</volume><issue>1</issue><fpage>323</fpage><lpage>339</lpage><history><date date-type="received"><day>30</day><month>7</month><year>2019</year></date><date date-type="accepted"><day>25</day><month>9</month><year>2019</year></date></history><permissions><copyright-statement>© The author(s)</copyright-statement><copyright-year>2020</copyright-year><license license-type="open-access"><license-p>This is an open access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">https://creativecommons.org/licenses/by/4.0/</ext-link>). See <ext-link ext-link-type="uri" xlink:href="http://ivyspring.com/terms">http://ivyspring.com/terms</ext-link> for full terms and conditions.</license-p></license></permissions><abstract><p><bold>Aims</bold>: We aimed to measure the abundance of <italic>Fusobacterium nucleatum</italic> (<italic>F. nucleatum</italic>) in colorectal cancer (CRC) tissues from patients and to uncover the function of this bacterium in colorectal tumor metastasis.</p><p><bold>Methods</bold>: We collected metastatic and non-metastatic CRC tissues to analyze <italic>F. nucleatum</italic> abundance. Cells were incubated with <italic>F. nucleatum</italic> or chloroquine (CQ) or were transfected with CARD3-targeting siRNA; the expression of mRNAs and proteins was then measured. CRC cells stably transfected with shRNA-luc were mixed with <italic>F. nucleatum</italic> and intravenously injected into BALB/cJ mice. APC<sup>Min/+</sup>, CARD3<sup>-/-</sup>and CARD3<sup>wt</sup> C57BL mice were given <italic>F. nucleatum</italic>; some mice were given azoxymethane (AOM) and dextran sodium sulfate (DSS).</p><p><bold>Results</bold>: <italic>F. nucleatum</italic> was abundant in CRC tissues from patients with metastasis. <italic>F. nucleatum</italic> infection increased CRC cell motility and upregulated the expression of CARD3, LC3-II, Beclin1 and Vimentin, and downregulated the expression of E-cadherin and P62 in CRC cells. These effects were attenuated by treatment with CQ, siCARD3 or both. APC<sup>Min/+</sup> mice gavaged with <italic>F. nucleatum</italic> developed more aggressive tumors than control mice. After AOM/DSS administration, the colorectums of CARD3<sup>-/-</sup> mice had fewer tumors than those of control mice. Tumors from CARD3<sup>-/-</sup> mice had lower levels of LC3-II and Beclin1 and higher levels of P62 than those from control mice. BALB/cJ mice injected with both CT26-luc cells and <italic>F. nucleatum</italic> formed more metastases than control mice. CQ treatment, CARD3 knockdown or both reduced the ability of CT26-luc cells to form metastases <italic>in vivo</italic>.</p><p><bold>Conclusions</bold>: <italic>F. nucleatum</italic> is enriched in CRC tissues from patients with metastasis. <italic>F. nucleatum</italic> orchestrates CARD3 and autophagy to control CRC metastasis. Measuring and targeting <italic>F. nucleatum</italic> and its associated pathways will yield approaches for the prevention and treatment of CRC metastasis.</p></abstract><kwd-group><kwd>microbe</kwd><kwd>gene regulation</kwd><kwd>gene targeting</kwd><kwd>colorectal cancer</kwd></kwd-group></article-meta></front><floats-group><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold><italic>F. nucleatum</italic> is Associated with Colorectal Cancer Metastasis.</bold> (A) A cladogram representation of by 16S rDNA sequencing data from CRC patients with (n = 9) and without (n = 7) metastasis. Taxa enriched in patients with metastasis (red) and without metastasis (green). The brightness of each dot is proportional to its effect size. (B) Linear discriminant analysis (LDA) coupled with effect size measurements identified the significantly differential abundances in the data referenced in A. Only taxa with values greater than the LDA threshold of 3.6 are shown. (C) Statistical analysis of the abundance of <italic>F. nucleatum</italic> in CRC patients with or without metastasis (**<italic>P</italic> < 0.01, and ***<italic>P</italic> < 0.001; nonparametric Mann-Whitney test). (D) Representative images of FISH to assess the amount of <italic>F. nucleatum</italic> in metastatic CRC tissues (n = 62), non-metastatic CRC tissues (n = 32) and matched lymph nodes. EUB338 (red) is a Cy3-conjugated “universal bacterial” oligonucleotide probe; FUS664 (green) is a FITC-conjugated <italic>F. nucleatum</italic> oligonucleotide probe. 200× magnification. (E-H) Statistical analysis of the mRNA expression of E-cadherin and Vimentin in CRC patients with or without metastasis (E-F; *<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, and ***<italic>P</italic> < 0.001; nonparametric Mann-Whitney test; the error bars indicate the SDs). Correlation analysis of the abundance of <italic>F. nucleatum</italic> and the expression levels of E-cadherin and Vimentin in cancer tissues (G-H; two-tailed, nonparametric Spearman correlation). (I-J) Western blot analysis was performed with CRC cells cocultured with <italic>F. nucleatum</italic> (F01), <italic>F. nucleatum</italic> (ATCC10951), <italic>E. coli</italic> or PBS (control).</p></caption><graphic xlink:href="thnov10p0323g001"></graphic></fig><fig id="F2" position="float"><label>Figure 2</label><caption><p><bold><italic>F. nucleatum</italic> Promotes Cancer Autophagy Activation <italic>in vitro.</italic></bold>(A) ssGSEA was conducted to reveal the relationship between the abundance of <italic>F. nucleatum</italic> and the autophagy-related pathway activity in CRC cells. (B-F) Real-time PCR was performed in HCT116 cells cocultured with <italic>F. nucleatum</italic> (F01) or PBS (control) (*<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, and ***<italic>P</italic> < 0.001; unpaired Student's<italic> t</italic>-test; the bars indicate the SD of three experiments). (G-H) Western blot analysis was performed to detect autophagy element expression in HCT116 (G) and SW480 (H) cells cocultured with <italic>F. nucleatum</italic>, <italic>E. coli</italic> or PBS (control). (I-J) Immunofluorescence images of LC3-Ⅱ in HCT116 cells infected with or without <italic>F. nucleatum</italic> (F01; I). The positive cells were counted in five randomly chosen fields, and the data are presented as the means ± SDs (J; **<italic>P</italic> < 0.01; unpaired Student's <italic>t</italic>-test). (K-L) Representative electron micrographs of autophagosomes (red arrows) in HCT116 cells infected with or without <italic>F. nucleatum</italic> (F01) (K; scale bar, 0.5 µm). Quantification of cells containing autophagosomes (from K) in five randomly chosen fields, and the data are presented as the means ± SDs (L; *<italic>P</italic> < 0.05, and **<italic>P</italic> < 0.01; unpaired Student's <italic>t</italic>-test).</p></caption><graphic xlink:href="thnov10p0323g002"></graphic></fig><fig id="F3" position="float"><label>Figure 3</label><caption><p><bold><italic>F. nucleatum</italic> Induces Cancer Metastasis via the Autophagy Pathway.</bold> (A) Western blot analysis was performed in HCT116 cells cocultured with <italic>F. nucleatum</italic> (F01), the autophagy inhibitor CQ (20 µM) or PBS (control). (B-D) Transwell assays (B) were conducted with HCT116 cells cocultured with <italic>F. nucleatum</italic> (F01), CQ or PBS (control). The indicated migrated (C) and invaded (D) cells were quantified in five randomly selected fields, and the data are presented as the means ± SDs (**<italic>P</italic> < 0.01, and ***<italic>P</italic> < 0.001; unpaired Student's <italic>t</italic>-test). (E-F) The mRNA expression of E-cadherin (E) and Vimentin (F) was analyzed in HCT116 cells cocultured with <italic>F. nucleatum</italic> (F01), CQ or PBS (control) (*<italic>P</italic> < 0.05 and **<italic>P</italic> < 0.01; unpaired Student's <italic>t</italic>-test; the bars indicate the SD of three experiments) (G) Schematic of the experimental setup. (H-K) Representative colorectal tumors (red arrows) and H&E staining and FISH images of tumors in APC<sup>Min/+</sup> mice treated with <italic>F. nucleatum</italic> (F01), CQ or PBS control (I). Statistical analysis of mouse weights (H; two-way ANOVA combined with Bonferroni's post hoc test), tumor numbers (J; nonparametric Mann-Whitney test) and tumor sizes (K) in the different groups (n = 5-6 mice/group; *<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, and ***<italic>P</italic> < 0.001; the error bars indicate the SDs). (L) E-cadherin expression in tumors from APC<sup>Min/+</sup> mice treated with PBS (control), CQ, <italic>F. nucleatum</italic> (F01) or <italic>F. nucleatum</italic>(F01) + CQ was measured by immunohistochemical analysis. (M) Western blot analysis was performed with tissues from APC<sup>Min/+</sup> mice in the different groups.</p></caption><graphic xlink:href="thnov10p0323g003"></graphic></fig><fig id="F4" position="float"><label>Figure 4</label><caption><p><bold> CARD3 Expression is Associated with <italic>F. nucleatum.</italic></bold>(A) GSEA for CARD3 expression with metastatic gene sets using the GSE21510 dataset (NES = -1.860, <italic>P</italic> = 0.0058, FDR = 0.055). (B-C) Statistical analysis of CARD3 mRNA expression in CRC tissues from patients with or without metastasis (B; ***<italic>P</italic> < 0.001; nonparametric Mann-Whitney test; the error bars indicate the SDs). Correlation analysis of the abundance of <italic>F.nucleatum</italic> and the expression of CARD3 in CRC tissues (C; r = 0.6839, <italic>P</italic> < 0.001; two-tailed, nonparametric Spearman correlation). (D-E) Representative images showing that the abundance of invasive <italic>F. nucleatum</italic> in CRC tissues is associated with CARD3 expression. 100× or 200× magnification (D). CARD3 protein levels in 21 <italic>F. nucleatum-</italic>low and 22 <italic>F. nucleatum-</italic>high CRC tissues from patients were measured by immunohistochemical analysis (E; *<italic>P</italic> < 0.05; unpaired Student's <italic>t</italic>-test; the error bars indicate the SDs). (F) Representative images of Western blots comparing the expression of CARD3 in <italic>F. nucleatum-</italic>low and <italic>F. nucleatum-</italic>high CRC tissues from patients. (G-I) Statistical analysis of CARD3 mRNA expression in HCT116 cells cocultured with <italic>F. nucleatum</italic> (F01, G). Western blot analysis was performed to measure CARD3 expression in HCT116 cells cocultured with <italic>F. nucleatum</italic> (F01) or <italic>E. coli</italic> in a time-dependent (H) or MOI-dependent (I) manner.</p></caption><graphic xlink:href="thnov10p0323g004"></graphic></fig><fig id="F5" position="float"><label>Figure 5</label><caption><p><bold> CARD3 is Involved in <italic>F. nucleatum</italic>-Mediated Autophagy.</bold> (A) Domain architecture of CARD3 and alignment of the LIR motifs (pink) between humans and rodents. (B) Western blot analysis was performed with HCT116 cells transfected with CARD3-targeting siRNA and cocultured with either PBS or<italic> F. nucleatum</italic> (F01). (C-D) Representative electron micrographs of autophagosomes (red arrows) in HCT116 cells infected with <italic>F. nucleatum</italic> (F01, blue arrows) or transfected with CARD3-targeting siRNA (C; scale bar, 0.5 µm). Quantification of cells containing autophagosomes (from C) was conducted with five random fields, and the data are presented as the means ± SDs (D; *<italic>P</italic> < 0.05, and **<italic>P</italic> < 0.01; unpaired Student's <italic>t</italic>-test). (E-F) Representative immunofluorescence images of LC3-Ⅱ in HCT116 cells (E; scale bar, 10 µm). The positive cells were counted in five random fields, and the data are presented as the means ± SDs (F; *<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, and ***<italic>P</italic> < 0.001; unpaired Student's <italic>t</italic>-test). (G) Schematic of the experimental setup. (H-J) Representative colorectal tumors (red arrows) and H&E staining of tumors from CARD3<sup>wt</sup> and CARD3<sup>-/-</sup> mice (I; 200× magnification). Statistical analysis of the tumor numbers (H) and sizes (J) in the different groups of mice (n = 5 mice/group; *<italic>P</italic> < 0.05; unpaired Student's <italic>t</italic>-test; the error bars indicate the SDs). (K) Western blot analysis was performed with CARD3<sup>wt</sup> and CARD3<sup>-/-</sup> mouse tissues.</p></caption><graphic xlink:href="thnov10p0323g005"></graphic></fig><fig id="F6" position="float"><label>Figure 6</label><caption><p><bold> CARD3 is Involved in <italic>F. nucleatum</italic>-Mediated Autophagy <italic>in vitro.</italic></bold>(A-F) Transwell assays were conducted with HCT116 cells (A) and SW480 cells (B) treated with <italic>F. nucleatum</italic> (F01), CQ or siCARD3. The indicated migrated and invaded cells were quantified in five random fields, and the data are presented as the means ± SDs (C-F; *<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, and ***<italic>P</italic> < 0.001; unpaired Student's <italic>t</italic>-test). (G) Western blot analysis was performed with HCT116 cells treated with <italic>F. nucleatum</italic> (F01), CQ or siCARD3.</p></caption><graphic xlink:href="thnov10p0323g006"></graphic></fig><fig id="F7" position="float"><label>Figure 7</label><caption><p><bold> CARD3 is Involved in <italic>F. nucleatum</italic>-Mediated Autophagy <italic>in vivo.</italic></bold>(A-D) Bioluminescence imaging (BLI) was used to monitor metastases (A) in the lungs (B), livers (C), and intestines (D) of wild-type BALB/cJ mice (n = 5-6 mice/group). Representative gross lungs and H&E-stained lung and liver sections from mice (A). The data are presented as the means ± SDs (*<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, and ***<italic>P</italic> < 0.001; Mann-Whitney test). (E-F) The metastatic foci in lungs (E) and livers (F) were counted. The data are presented as the means ± SDs. (*<italic>P</italic> < 0.05, **<italic>P</italic> < 0.01, and ***<italic>P</italic> < 0.001; Mann-Whitney test).</p></caption><graphic xlink:href="thnov10p0323g007"></graphic></fig><table-wrap id="T1" position="float"><label>Table 1</label><caption><p>Clinicopathologic characteristics in <italic>F. nucleatum</italic>-low vs. <italic>F. nucleatum</italic>-high colorectal cancers</p></caption><table frame="hsides" rules="groups"><thead valign="top"><tr><th rowspan="2" colspan="1">Characteristics</th><th colspan="2" rowspan="1"><italic>F. nucleatum</italic>.</th><th rowspan="2" colspan="1"><italic>p-</italic>value<sup>a</sup></th></tr><tr><th rowspan="1" colspan="1">Low (n=33)</th><th rowspan="1" colspan="1">High (n=61)</th></tr></thead><tbody valign="top"><tr><td rowspan="1" colspan="1"><bold>Gender</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1">0.551</td></tr><tr><td rowspan="1" colspan="1">Female</td><td rowspan="1" colspan="1">16</td><td rowspan="1" colspan="1">29</td><td rowspan="2" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">Male</td><td rowspan="1" colspan="1">17</td><td rowspan="1" colspan="1">32</td></tr><tr><td rowspan="1" colspan="1"><bold>Age</bold></td><td rowspan="1" colspan="1">59.94</td><td rowspan="1" colspan="1">61.20</td><td rowspan="1" colspan="1">0.460</td></tr><tr><td rowspan="1" colspan="1">(Range )</td><td rowspan="1" colspan="1">25-81</td><td rowspan="1" colspan="1">23-86</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1"><bold>Location</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1">0.031*</td></tr><tr><td rowspan="1" colspan="1">Proximal</td><td rowspan="1" colspan="1">9</td><td rowspan="1" colspan="1">31</td><td rowspan="2" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">Distal</td><td rowspan="1" colspan="1">24</td><td rowspan="1" colspan="1">30</td></tr><tr><td rowspan="1" colspan="1"><bold>Tumor size</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1">0.423</td></tr><tr><td rowspan="1" colspan="1">d<4cm</td><td rowspan="1" colspan="1">8</td><td rowspan="1" colspan="1">19</td><td rowspan="3" colspan="1">0.002*</td></tr><tr><td rowspan="1" colspan="1">4≤d<8cm</td><td rowspan="1" colspan="1">22</td><td rowspan="1" colspan="1">40</td></tr><tr><td rowspan="1" colspan="1">d≥8cm</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">2</td></tr><tr><td rowspan="1" colspan="1"><bold>AJCC stage</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">Ⅰ-Ⅱ</td><td rowspan="1" colspan="1">18</td><td rowspan="1" colspan="1">14</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">Ⅲ-Ⅳ</td><td rowspan="1" colspan="1">15</td><td rowspan="1" colspan="1">47</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1"><bold>Histologic grade</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1">0.065</td></tr><tr><td rowspan="1" colspan="1">Well differentiated</td><td rowspan="1" colspan="1">6</td><td rowspan="1" colspan="1">3</td><td rowspan="3" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">Moderately differentiated</td><td rowspan="1" colspan="1">24</td><td rowspan="1" colspan="1">46</td></tr><tr><td rowspan="1" colspan="1">Poorly differentiated</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">12</td></tr><tr><td rowspan="1" colspan="1"><bold>Pathological type</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1">0.709</td></tr><tr><td rowspan="1" colspan="1">eminence type</td><td rowspan="1" colspan="1">18</td><td rowspan="1" colspan="1">29</td><td rowspan="2" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">ulcer type</td><td rowspan="1" colspan="1">11</td><td rowspan="1" colspan="1">21</td></tr><tr><td rowspan="1" colspan="1">Infiltrating type</td><td rowspan="1" colspan="1">4</td><td rowspan="1" colspan="1">11</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1"><bold>Depth of invasion</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1">0.023*</td></tr><tr><td rowspan="1" colspan="1">T1</td><td rowspan="1" colspan="1">2</td><td rowspan="1" colspan="1">2</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">T2</td><td rowspan="1" colspan="1">10</td><td rowspan="1" colspan="1">5</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">T3</td><td rowspan="1" colspan="1">20</td><td rowspan="1" colspan="1">47</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">T4</td><td rowspan="1" colspan="1">1</td><td rowspan="1" colspan="1">7</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1"><bold>Lymph node metastasis</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1">0.005*</td></tr><tr><td rowspan="1" colspan="1">N0</td><td rowspan="1" colspan="1">19</td><td rowspan="1" colspan="1">16</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">N1</td><td rowspan="1" colspan="1">9</td><td rowspan="1" colspan="1">19</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">N2</td><td rowspan="1" colspan="1">5</td><td rowspan="1" colspan="1">26</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1"><bold>Distant metastasis</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1">0.037*</td></tr><tr><td rowspan="1" colspan="1">M0</td><td rowspan="1" colspan="1">32</td><td rowspan="1" colspan="1">50</td><td rowspan="1" colspan="1"></td></tr><tr><td rowspan="1" colspan="1">M1</td><td rowspan="1" colspan="1">1</td><td rowspan="1" colspan="1">11</td><td rowspan="1" colspan="1"></td></tr></tbody></table><table-wrap-foot><fn><p><sup>a</sup> Chi-square test or Fisher's exact test, *<italic>P</italic> < 0.05; AJCC, American Joint Committee On Cancer.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list><country><li>République populaire de Chine</li><li>États-Unis</li></country></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Chen, Yongyu" sort="Chen, Yongyu" uniqKey="Chen Y" first="Yongyu" last="Chen">Yongyu Chen</name></noRegion><name sortKey="Cao, Pan" sort="Cao, Pan" uniqKey="Cao P" first="Pan" last="Cao">Pan Cao</name><name sortKey="Cao, Pan" sort="Cao, Pan" uniqKey="Cao P" first="Pan" last="Cao">Pan Cao</name><name sortKey="Chen, Yan" sort="Chen, Yan" uniqKey="Chen Y" first="Yan" last="Chen">Yan Chen</name><name sortKey="Chen, Yan" sort="Chen, Yan" uniqKey="Chen Y" first="Yan" last="Chen">Yan Chen</name><name sortKey="Chen, Yongyu" sort="Chen, Yongyu" uniqKey="Chen Y" first="Yongyu" last="Chen">Yongyu Chen</name><name sortKey="Deng, Yunchao" sort="Deng, Yunchao" uniqKey="Deng Y" first="Yunchao" last="Deng">Yunchao Deng</name><name sortKey="Deng, Yunchao" sort="Deng, Yunchao" uniqKey="Deng Y" first="Yunchao" last="Deng">Yunchao Deng</name><name sortKey="Dong, Weiguo" sort="Dong, Weiguo" uniqKey="Dong W" first="Weiguo" last="Dong">Weiguo Dong</name><name sortKey="Dong, Weiguo" sort="Dong, Weiguo" uniqKey="Dong W" first="Weiguo" last="Dong">Weiguo Dong</name><name sortKey="Fu, Xiangsheng" sort="Fu, Xiangsheng" uniqKey="Fu X" first="Xiangsheng" last="Fu">Xiangsheng Fu</name><name sortKey="Su, Wenhao" sort="Su, Wenhao" uniqKey="Su W" first="Wenhao" last="Su">Wenhao Su</name><name sortKey="Su, Wenhao" sort="Su, Wenhao" uniqKey="Su W" first="Wenhao" last="Su">Wenhao Su</name><name sortKey="Su, Wenhao" sort="Su, Wenhao" uniqKey="Su W" first="Wenhao" last="Su">Wenhao Su</name><name sortKey="Zhan, Na" sort="Zhan, Na" uniqKey="Zhan N" first="Na" last="Zhan">Na Zhan</name><name sortKey="Zhan, Na" sort="Zhan, Na" uniqKey="Zhan N" first="Na" last="Zhan">Na Zhan</name><name sortKey="Zhan, Na" sort="Zhan, Na" uniqKey="Zhan N" first="Na" last="Zhan">Na Zhan</name><name sortKey="Zhang, Jixiang" sort="Zhang, Jixiang" uniqKey="Zhang J" first="Jixiang" last="Zhang">Jixiang Zhang</name><name sortKey="Zhang, Jixiang" sort="Zhang, Jixiang" uniqKey="Zhang J" first="Jixiang" last="Zhang">Jixiang Zhang</name><name sortKey="Zhang, Jixiang" sort="Zhang, Jixiang" uniqKey="Zhang J" first="Jixiang" last="Zhang">Jixiang Zhang</name></country><country name="États-Unis"><noRegion><name sortKey="Huang, Yun" sort="Huang, Yun" uniqKey="Huang Y" first="Yun" last="Huang">Yun Huang</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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