FKBP9 promotes the malignant behavior of glioblastoma cells and confers resistance to endoplasmic reticulum stress inducers
Identifieur interne : 000154 ( Main/Exploration ); précédent : 000153; suivant : 000155FKBP9 promotes the malignant behavior of glioblastoma cells and confers resistance to endoplasmic reticulum stress inducers
Auteurs : Huizhe Xu ; Peng Liu [République populaire de Chine] ; Yumei Yan ; Kun Fang ; Dapeng Liang ; Xiukun Hou ; Xiaohong Zhang ; Songyan Wu ; Jianmei Ma ; Ruoyu Wang ; Tao Li ; Haozhe Piao ; Songshu MengSource :
- Journal of Experimental & Clinical Cancer Research : CR [ 0392-9078 ] ; 2020.
Abstract
FK506-binding protein 9 (FKBP9) is amplified in high-grade gliomas (HGGs). However, the roles and mechanism(s) of FKBP9 in glioma are unknown.
The expression of FKBP9 in clinical glioma tissues was detected by immunohistochemistry (IHC). The correlation between FKBP9 expression levels and the clinical prognosis of glioma patients was examined by bioinformatic analysis. Glioblastoma (GBM) cell lines stably depleted of FKBP9 were established using lentiviruses expressing shRNAs against FKBP9. The effects of FKBP9 on GBM cells were determined by cell-based analyses, including anchorage-independent growth, spheroid formation, transwell invasion assay, confocal microscopy, immunoblot (IB) and coimmunoprecipitation assays. In vivo tumor growth was determined in both chick chorioallantoic membrane (CAM) and mouse xenograft models.
High FKBP9 expression correlated with poor prognosis in glioma patients. Knockdown of FKBP9 markedly suppressed the malignant phenotype of GBM cells in vitro and inhibited tumor growth in vivo. Mechanistically, FKBP9 expression induced the activation of p38MAPK signaling via ASK1. Furthermore, ASK1-p38 signaling contributed to the FKBP9-mediated effects on GBM cell clonogenic growth. In addition, depletion of FKBP9 activated the IRE1α-XBP1 pathway, which played a role in the FKBP9-mediated oncogenic effects. Importantly, FKBP9 expression conferred GBM cell resistance to endoplasmic reticulum (ER) stress inducers that caused FKBP9 ubiquitination and degradation.
Our findings suggest an oncogenic role for FKBP9 in GBM and reveal FKBP9 as a novel mediator in the IRE1α-XBP1 pathway.
Url:
DOI: 10.1186/s13046-020-1541-0
PubMed: 32111229
PubMed Central: 7048151
Affiliations:
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last="Xu">Huizhe Xu</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.411971.b</institution-id><institution-id institution-id-type="ISNI">0000 0000 9558 1426</institution-id><institution>Institute of Cancer Stem Cell, Dalian Medical University Cancer Center,</institution></institution-wrap>9 Lvshun Road South, Dalian, 116044 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116044 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Liu, Peng" sort="Liu, Peng" uniqKey="Liu P" first="Peng" last="Liu">Peng Liu</name><affiliation wicri:level="3"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.263488.3</institution-id><institution-id institution-id-type="ISNI">0000 0001 0472 9649</institution-id><institution>Department of General Surgery,</institution><institution>Shenzhen University General Hospital,</institution></institution-wrap>No. 1098, Xueyuan avenue, Shenzhen, 518055 China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>No. 1098, Xueyuan avenue, Shenzhen</wicri:regionArea><placeName><settlement type="city">Shenzhen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Yan, Yumei" sort="Yan, Yumei" uniqKey="Yan Y" first="Yumei" last="Yan">Yumei Yan</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="GRID">grid.411971.b</institution-id><institution-id institution-id-type="ISNI">0000 0000 9558 1426</institution-id><institution>The First Department of Ultrasound, The First Affiliated Hospital,</institution><institution>Dalian Medical University,</institution></institution-wrap>No. 222 Zhongshan Road, Dalian, 116021 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116021 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Fang, Kun" sort="Fang, Kun" uniqKey="Fang K" first="Kun" last="Fang">Kun Fang</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.411971.b</institution-id><institution-id institution-id-type="ISNI">0000 0000 9558 1426</institution-id><institution>Institute of Cancer Stem Cell, Dalian Medical University Cancer Center,</institution></institution-wrap>9 Lvshun Road South, Dalian, 116044 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116044 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Liang, Dapeng" sort="Liang, Dapeng" uniqKey="Liang D" first="Dapeng" last="Liang">Dapeng Liang</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.411971.b</institution-id><institution-id institution-id-type="ISNI">0000 0000 9558 1426</institution-id><institution>Institute of Cancer Stem Cell, Dalian Medical University Cancer Center,</institution></institution-wrap>9 Lvshun Road South, Dalian, 116044 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116044 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Hou, Xiukun" sort="Hou, Xiukun" uniqKey="Hou X" first="Xiukun" last="Hou">Xiukun Hou</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="GRID">grid.411971.b</institution-id><institution-id institution-id-type="ISNI">0000 0000 9558 1426</institution-id><institution>The First Department of Ultrasound, The First Affiliated Hospital,</institution><institution>Dalian Medical University,</institution></institution-wrap>No. 222 Zhongshan Road, Dalian, 116021 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116021 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Zhang, Xiaohong" sort="Zhang, Xiaohong" uniqKey="Zhang X" first="Xiaohong" last="Zhang">Xiaohong Zhang</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.411971.b</institution-id><institution-id institution-id-type="ISNI">0000 0000 9558 1426</institution-id><institution>Institute of Cancer Stem Cell, Dalian Medical University Cancer Center,</institution></institution-wrap>9 Lvshun Road South, Dalian, 116044 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116044 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Wu, Songyan" sort="Wu, Songyan" uniqKey="Wu S" first="Songyan" last="Wu">Songyan Wu</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.411971.b</institution-id><institution-id institution-id-type="ISNI">0000 0000 9558 1426</institution-id><institution>Institute of Cancer Stem Cell, Dalian Medical University Cancer Center,</institution></institution-wrap>9 Lvshun Road South, Dalian, 116044 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116044 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Ma, Jianmei" sort="Ma, Jianmei" uniqKey="Ma J" first="Jianmei" last="Ma">Jianmei Ma</name><affiliation><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.411971.b</institution-id><institution-id institution-id-type="ISNI">0000 0000 9558 1426</institution-id><institution>Department of Anatomy,</institution><institution>Dalian Medical University,</institution></institution-wrap>9 Lvshun Road South, Dalian, 116044 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116044 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Wang, Ruoyu" sort="Wang, Ruoyu" uniqKey="Wang R" first="Ruoyu" last="Wang">Ruoyu Wang</name><affiliation><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="GRID">grid.459353.d</institution-id><institution-id institution-id-type="ISNI">0000 0004 1800 3285</institution-id><institution>Department of Oncology,</institution><institution>Affiliated Zhongshan Hospital of Dalian University,</institution></institution-wrap>No.6 Jiefang Street, Dalian, 116001 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116001 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Li, Tao" sort="Li, Tao" uniqKey="Li T" first="Tao" last="Li">Tao Li</name><affiliation><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="GRID">grid.452435.1</institution-id><institution>Department of Neurosurgery,</institution><institution>The First Affiliated Hospital of Dalian Medical University,</institution></institution-wrap>No. 222 Zhongshan Road, Dalian, 116011 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116011 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Piao, Haozhe" sort="Piao, Haozhe" uniqKey="Piao H" first="Haozhe" last="Piao">Haozhe Piao</name><affiliation><nlm:aff id="Aff7"><institution-wrap><institution-id institution-id-type="GRID">grid.459742.9</institution-id><institution-id institution-id-type="ISNI">0000 0004 1798 5889</institution-id><institution>Department of Neurosurgery, Cancer Hospital of China Medical University,</institution><institution>Liaoning Cancer Hospital & Institute,</institution></institution-wrap>No. 44 Xiaoheyan Road, Dadong District, Shenyang, 110042 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">110042 Liaoning Province China</wicri:noCountry></affiliation></author><author><name sortKey="Meng, Songshu" sort="Meng, Songshu" uniqKey="Meng S" first="Songshu" last="Meng">Songshu Meng</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.411971.b</institution-id><institution-id institution-id-type="ISNI">0000 0000 9558 1426</institution-id><institution>Institute of Cancer Stem Cell, Dalian Medical University Cancer Center,</institution></institution-wrap>9 Lvshun Road South, Dalian, 116044 Liaoning Province China</nlm:aff><wicri:noCountry code="subfield">116044 Liaoning Province China</wicri:noCountry></affiliation></author></analytic><series><title level="j">Journal of Experimental & Clinical Cancer Research : CR</title><idno type="ISSN">0392-9078</idno><idno type="eISSN">1756-9966</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">FK506-binding protein 9 (FKBP9) is amplified in high-grade gliomas (HGGs). However, the roles and mechanism(s) of FKBP9 in glioma are unknown.</p></sec><sec><title>Methods</title><p id="Par2">The expression of FKBP9 in clinical glioma tissues was detected by immunohistochemistry (IHC). The correlation between FKBP9 expression levels and the clinical prognosis of glioma patients was examined by bioinformatic analysis. Glioblastoma (GBM) cell lines stably depleted of FKBP9 were established using lentiviruses expressing shRNAs against FKBP9. The effects of FKBP9 on GBM cells were determined by cell-based analyses, including anchorage-independent growth, spheroid formation, transwell invasion assay, confocal microscopy, immunoblot (IB) and coimmunoprecipitation assays. In vivo tumor growth was determined in both chick chorioallantoic membrane (CAM) and mouse xenograft models.</p></sec><sec><title>Results</title><p id="Par3">High FKBP9 expression correlated with poor prognosis in glioma patients. Knockdown of FKBP9 markedly suppressed the malignant phenotype of GBM cells in vitro and inhibited tumor growth in vivo. Mechanistically, FKBP9 expression induced the activation of p38MAPK signaling via ASK1. Furthermore, ASK1-p38 signaling contributed to the FKBP9-mediated effects on GBM cell clonogenic growth. In addition, depletion of FKBP9 activated the IRE1α-XBP1 pathway, which played a role in the FKBP9-mediated oncogenic effects. Importantly, FKBP9 expression conferred GBM cell resistance to endoplasmic reticulum (ER) stress inducers that caused FKBP9 ubiquitination and degradation.</p></sec><sec><title>Conclusions</title><p id="Par4">Our findings suggest an oncogenic role for FKBP9 in GBM and reveal FKBP9 as a novel mediator in the IRE1α-XBP1 pathway.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Ghartey Kwansah, G" uniqKey="Ghartey Kwansah G">G Ghartey-Kwansah</name></author><author><name sortKey="Li, Z" uniqKey="Li Z">Z Li</name></author><author><name sortKey="Feng, R" uniqKey="Feng R">R Feng</name></author><author><name sortKey="Wang, L" uniqKey="Wang L">L Wang</name></author><author><name sortKey="Zhou, X" uniqKey="Zhou X">X Zhou</name></author><author><name sortKey="Chen, Fz" uniqKey="Chen F">FZ Chen</name></author><author><name sortKey="Xu, Mm" uniqKey="Xu M">MM Xu</name></author><author><name sortKey="Jones, O" uniqKey="Jones O">O 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sort="Fang, Kun" uniqKey="Fang K" first="Kun" last="Fang">Kun Fang</name><name sortKey="Hou, Xiukun" sort="Hou, Xiukun" uniqKey="Hou X" first="Xiukun" last="Hou">Xiukun Hou</name><name sortKey="Li, Tao" sort="Li, Tao" uniqKey="Li T" first="Tao" last="Li">Tao Li</name><name sortKey="Liang, Dapeng" sort="Liang, Dapeng" uniqKey="Liang D" first="Dapeng" last="Liang">Dapeng Liang</name><name sortKey="Ma, Jianmei" sort="Ma, Jianmei" uniqKey="Ma J" first="Jianmei" last="Ma">Jianmei Ma</name><name sortKey="Meng, Songshu" sort="Meng, Songshu" uniqKey="Meng S" first="Songshu" last="Meng">Songshu Meng</name><name sortKey="Piao, Haozhe" sort="Piao, Haozhe" uniqKey="Piao H" first="Haozhe" last="Piao">Haozhe Piao</name><name sortKey="Wang, Ruoyu" sort="Wang, Ruoyu" uniqKey="Wang R" first="Ruoyu" last="Wang">Ruoyu Wang</name><name sortKey="Wu, Songyan" sort="Wu, Songyan" uniqKey="Wu S" first="Songyan" last="Wu">Songyan Wu</name><name sortKey="Xu, Huizhe" sort="Xu, Huizhe" uniqKey="Xu H" first="Huizhe" last="Xu">Huizhe Xu</name><name sortKey="Yan, Yumei" sort="Yan, Yumei" uniqKey="Yan Y" first="Yumei" last="Yan">Yumei Yan</name><name sortKey="Zhang, Xiaohong" sort="Zhang, Xiaohong" uniqKey="Zhang X" first="Xiaohong" last="Zhang">Xiaohong Zhang</name></noCountry><country name="République populaire de Chine"><region name="Guangdong"><name sortKey="Liu, Peng" sort="Liu, Peng" uniqKey="Liu P" first="Peng" last="Liu">Peng Liu</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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