NOX4-Derived ROS Mediates TGF- β 1-Induced Metabolic Reprogramming during Epithelial-Mesenchymal Transition through the PI3K/AKT/HIF-1 α Pathway in Glioblastoma
Current studies on tumor progression focus on the roles of cytokines in the tumor microenvironment (TME), and recent research shows that transforming growth factor- 1 (TGF- 1) released from TME plays a pivotal role in tumor development and malignant transformation. The alteration in cellular metabol...
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Published in | Oxidative medicine and cellular longevity Vol. 2021; no. 1; p. 5549047 |
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Abstract | Current studies on tumor progression focus on the roles of cytokines in the tumor microenvironment (TME), and recent research shows that transforming growth factor-
1 (TGF-
1) released from TME plays a pivotal role in tumor development and malignant transformation. The alteration in cellular metabolism is a hallmark of cancer, which not only provides cancer cells with ATP for fuel cellular reactions, but also generates metabolic intermediates for the synthesis of essential cellular ingredients, to support cell proliferation, migration, and invasion. Interestingly, we found a distinct metabolic change during TGF-
1-induced epithelial-mesenchymal transition (EMT) in glioblastoma cells. Indeed, TGF-
1 participates in metabolic reprogramming, and the molecular basis is still not well understood. NADPH oxidases 4 (NOX4), a member of the Nox family, also plays a key role in the biological effects of glioblastoma. However, the relationship between NOX4, TGF-
1, and cellular metabolic changes during EMT in glioblastoma remains obscure. Here, our findings demonstrated that TGF-
1 upregulated NOX4 expression accompanied by reactive oxygen species (ROS) through Smad-dependent signaling and then induced hypoxia-inducible factor 1
(HIF-1
) overexpression and nuclear accumulation resulting in metabolic reprogramming and promoting EMT. Besides, inhibition of glycolysis reversed EMT suggesting a causal relationship between TGF-
1-induced metabolic changes and tumorigenesis. Moreover, TGF-
1-induced metabolic reprogramming and EMT which modulated by NOX4/ROS were blocked when the phosphoinositide3-kinase (PI3K)/AKT/HIF-1
signaling pathways were inhibited. In conclusion, these suggest that NOX4/ROS induction by TGF-
1 can be one of the main mechanisms mediating the metabolic reprogramming during EMT of glioblastoma cells and provide promising strategies for cancer therapy. |
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AbstractList | Current studies on tumor progression focus on the roles of cytokines in the tumor microenvironment (TME), and recent research shows that transforming growth factor‐ β 1 (TGF‐ β 1) released from TME plays a pivotal role in tumor development and malignant transformation. The alteration in cellular metabolism is a hallmark of cancer, which not only provides cancer cells with ATP for fuel cellular reactions, but also generates metabolic intermediates for the synthesis of essential cellular ingredients, to support cell proliferation, migration, and invasion. Interestingly, we found a distinct metabolic change during TGF‐ β 1‐induced epithelial‐mesenchymal transition (EMT) in glioblastoma cells. Indeed, TGF‐ β 1 participates in metabolic reprogramming, and the molecular basis is still not well understood. NADPH oxidases 4 (NOX4), a member of the Nox family, also plays a key role in the biological effects of glioblastoma. However, the relationship between NOX4, TGF‐ β 1, and cellular metabolic changes during EMT in glioblastoma remains obscure. Here, our findings demonstrated that TGF‐ β 1 upregulated NOX4 expression accompanied by reactive oxygen species (ROS) through Smad‐dependent signaling and then induced hypoxia‐inducible factor 1 α (HIF‐1 α ) overexpression and nuclear accumulation resulting in metabolic reprogramming and promoting EMT. Besides, inhibition of glycolysis reversed EMT suggesting a causal relationship between TGF‐ β 1‐induced metabolic changes and tumorigenesis. Moreover, TGF‐ β 1‐induced metabolic reprogramming and EMT which modulated by NOX4/ROS were blocked when the phosphoinositide3‐kinase (PI3K)/AKT/HIF‐1 α signaling pathways were inhibited. In conclusion, these suggest that NOX4/ROS induction by TGF‐ β 1 can be one of the main mechanisms mediating the metabolic reprogramming during EMT of glioblastoma cells and provide promising strategies for cancer therapy. Current studies on tumor progression focus on the roles of cytokines in the tumor microenvironment (TME), and recent research shows that transforming growth factor- 1 (TGF- 1) released from TME plays a pivotal role in tumor development and malignant transformation. The alteration in cellular metabolism is a hallmark of cancer, which not only provides cancer cells with ATP for fuel cellular reactions, but also generates metabolic intermediates for the synthesis of essential cellular ingredients, to support cell proliferation, migration, and invasion. Interestingly, we found a distinct metabolic change during TGF- 1-induced epithelial-mesenchymal transition (EMT) in glioblastoma cells. Indeed, TGF- 1 participates in metabolic reprogramming, and the molecular basis is still not well understood. NADPH oxidases 4 (NOX4), a member of the Nox family, also plays a key role in the biological effects of glioblastoma. However, the relationship between NOX4, TGF- 1, and cellular metabolic changes during EMT in glioblastoma remains obscure. Here, our findings demonstrated that TGF- 1 upregulated NOX4 expression accompanied by reactive oxygen species (ROS) through Smad-dependent signaling and then induced hypoxia-inducible factor 1 (HIF-1 ) overexpression and nuclear accumulation resulting in metabolic reprogramming and promoting EMT. Besides, inhibition of glycolysis reversed EMT suggesting a causal relationship between TGF- 1-induced metabolic changes and tumorigenesis. Moreover, TGF- 1-induced metabolic reprogramming and EMT which modulated by NOX4/ROS were blocked when the phosphoinositide3-kinase (PI3K)/AKT/HIF-1 signaling pathways were inhibited. In conclusion, these suggest that NOX4/ROS induction by TGF- 1 can be one of the main mechanisms mediating the metabolic reprogramming during EMT of glioblastoma cells and provide promising strategies for cancer therapy. |
Author | Yang, Yihang Guo, Changfa Qiao, Qiujiang Su, Xiangsheng Wang, Yanjun Fu, Yibing Pang, Qi Zhang, Rui Sun, Shicheng |
Author_xml | – sequence: 1 givenname: Xiangsheng surname: Su fullname: Su, Xiangsheng organization: Department of Neurosurgery, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, China – sequence: 2 givenname: Yihang surname: Yang fullname: Yang, Yihang organization: Department of Neurosurgery, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, China – sequence: 3 givenname: Changfa surname: Guo fullname: Guo, Changfa organization: Department of Neurosurgery, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, China – sequence: 4 givenname: Rui surname: Zhang fullname: Zhang, Rui organization: Department of Neurosurgery, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, China – sequence: 5 givenname: Shicheng surname: Sun fullname: Sun, Shicheng organization: Department of Neurosurgery, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, China – sequence: 6 givenname: Yanjun surname: Wang fullname: Wang, Yanjun organization: Department of Neurosurgery, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, China – sequence: 7 givenname: Qiujiang surname: Qiao fullname: Qiao, Qiujiang organization: Department of Neurosurgery, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, China – sequence: 8 givenname: Yibing orcidid: 0000-0001-8731-0586 surname: Fu fullname: Fu, Yibing organization: Department of Obstetrics and Gynecology, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, China – sequence: 9 givenname: Qi orcidid: 0000-0001-8333-5647 surname: Pang fullname: Pang, Qi organization: Department of Neurosurgery, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250012, China |
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Cites_doi | 10.1007/s00441-011-1201-y 10.4049/jimmunol.1800782 10.3390/ijms20112767 10.1016/j.cell.2011.02.013 10.1186/s13046-018-0730-6 10.1038/s41467-017-01106-1 10.1016/j.canlet.2012.12.024 10.1111/febs.14090 10.1111/febs.14201 10.3892/ijmm.2018.3923 10.1002/ijc.23569 10.1126/science.123.3191.309 10.1074/jbc.M005912200 10.1172/JCI39104 10.1111/jcmm.13126 10.1371/journal.pone.0023945 10.1093/carcin/bgn032 10.1002/jcp.27955 10.4049/jimmunol.1701325 10.1016/j.freeradbiomed.2017.01.004 10.1016/j.brainresbull.2007.06.021 10.1016/j.apsb.2015.05.007 10.1038/cr.2009.5 10.1016/j.semcdb.2017.05.023 10.1016/j.tcb.2018.12.001 10.1074/jbc.M304854200 10.1089/ars.2014.5973 10.1155/2014/581732 10.7554/eLife.25217 10.1016/j.trecan.2016.11.008 10.1038/nn.4185 10.1016/j.stem.2010.11.028 10.1016/j.freeradbiomed.2012.06.016 10.1016/j.freeradbiomed.2016.10.500 10.1016/j.intimp.2018.10.035 10.1002/hep.31076 10.1016/j.immuni.2019.03.024 10.1038/s41586-020-2850-3 10.1158/1055-9965.EPI-14-0275 10.1016/j.freeradbiomed.2012.06.009 10.3892/ijmm.2018.3733 10.1002/1878-0261.12623 10.1007/s00018-019-03398-6 10.3389/fonc.2017.00295 10.1186/s13046-017-0628-8 10.1016/j.devcel.2019.04.026 10.1038/nri1312 |
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References | e_1_2_9_30_2 e_1_2_9_10_2 e_1_2_9_33_2 e_1_2_9_34_2 e_1_2_9_12_2 e_1_2_9_31_2 e_1_2_9_32_2 e_1_2_9_14_2 e_1_2_9_37_2 e_1_2_9_13_2 e_1_2_9_38_2 e_1_2_9_16_2 e_1_2_9_35_2 e_1_2_9_15_2 e_1_2_9_36_2 e_1_2_9_18_2 e_1_2_9_17_2 e_1_2_9_39_2 e_1_2_9_19_2 e_1_2_9_40_2 e_1_2_9_41_2 e_1_2_9_21_2 e_1_2_9_44_2 e_1_2_9_20_2 e_1_2_9_45_2 e_1_2_9_23_2 e_1_2_9_42_2 e_1_2_9_22_2 e_1_2_9_43_2 e_1_2_9_7_2 e_1_2_9_6_2 e_1_2_9_5_2 e_1_2_9_4_2 e_1_2_9_3_2 e_1_2_9_2_2 e_1_2_9_1_2 Hiraga R. (e_1_2_9_11_2) 2013; 33 e_1_2_9_9_2 e_1_2_9_8_2 e_1_2_9_25_2 e_1_2_9_48_2 e_1_2_9_24_2 e_1_2_9_27_2 e_1_2_9_46_2 e_1_2_9_26_2 e_1_2_9_47_2 e_1_2_9_29_2 e_1_2_9_28_2 |
References_xml | – ident: e_1_2_9_42_2 doi: 10.1007/s00441-011-1201-y – ident: e_1_2_9_25_2 doi: 10.4049/jimmunol.1800782 – ident: e_1_2_9_8_2 doi: 10.3390/ijms20112767 – ident: e_1_2_9_3_2 doi: 10.1016/j.cell.2011.02.013 – ident: e_1_2_9_32_2 doi: 10.1186/s13046-018-0730-6 – volume: 33 start-page: 4431 year: 2013 ident: e_1_2_9_11_2 article-title: Nox 4-derived ROS signaling contributes to TGF-β-induced epithelial-mesenchymal transition in pancreatic cancer cells publication-title: Anticancer Research contributor: fullname: Hiraga R. – ident: e_1_2_9_22_2 doi: 10.1038/s41467-017-01106-1 – ident: e_1_2_9_2_2 doi: 10.1016/j.canlet.2012.12.024 – ident: e_1_2_9_20_2 doi: 10.1111/febs.14090 – ident: e_1_2_9_29_2 doi: 10.1111/febs.14201 – ident: e_1_2_9_4_2 doi: 10.3892/ijmm.2018.3923 – ident: e_1_2_9_13_2 doi: 10.1002/ijc.23569 – ident: e_1_2_9_19_2 doi: 10.1126/science.123.3191.309 – ident: e_1_2_9_30_2 doi: 10.1074/jbc.M005912200 – ident: e_1_2_9_17_2 doi: 10.1172/JCI39104 – ident: e_1_2_9_44_2 doi: 10.1111/jcmm.13126 – ident: e_1_2_9_24_2 doi: 10.1371/journal.pone.0023945 – ident: e_1_2_9_48_2 doi: 10.1093/carcin/bgn032 – ident: e_1_2_9_5_2 doi: 10.1002/jcp.27955 – ident: e_1_2_9_38_2 doi: 10.4049/jimmunol.1701325 – ident: e_1_2_9_43_2 doi: 10.1016/j.freeradbiomed.2017.01.004 – ident: e_1_2_9_34_2 doi: 10.1016/j.brainresbull.2007.06.021 – ident: e_1_2_9_31_2 doi: 10.1016/j.apsb.2015.05.007 – ident: e_1_2_9_6_2 doi: 10.1038/cr.2009.5 – ident: e_1_2_9_21_2 doi: 10.1016/j.semcdb.2017.05.023 – ident: e_1_2_9_26_2 doi: 10.1016/j.tcb.2018.12.001 – ident: e_1_2_9_28_2 doi: 10.1074/jbc.M304854200 – ident: e_1_2_9_41_2 doi: 10.1089/ars.2014.5973 – ident: e_1_2_9_14_2 doi: 10.1155/2014/581732 – ident: e_1_2_9_46_2 doi: 10.7554/eLife.25217 – ident: e_1_2_9_40_2 doi: 10.1016/j.trecan.2016.11.008 – ident: e_1_2_9_35_2 doi: 10.1038/nn.4185 – ident: e_1_2_9_45_2 doi: 10.1016/j.stem.2010.11.028 – ident: e_1_2_9_12_2 doi: 10.1016/j.freeradbiomed.2012.06.016 – ident: e_1_2_9_23_2 doi: 10.1016/j.freeradbiomed.2016.10.500 – ident: e_1_2_9_47_2 doi: 10.1016/j.intimp.2018.10.035 – ident: e_1_2_9_33_2 doi: 10.1002/hep.31076 – ident: e_1_2_9_7_2 doi: 10.1016/j.immuni.2019.03.024 – ident: e_1_2_9_39_2 doi: 10.1038/s41586-020-2850-3 – ident: e_1_2_9_1_2 doi: 10.1158/1055-9965.EPI-14-0275 – ident: e_1_2_9_15_2 doi: 10.1016/j.freeradbiomed.2012.06.009 – ident: e_1_2_9_27_2 doi: 10.3892/ijmm.2018.3733 – ident: e_1_2_9_36_2 doi: 10.1002/1878-0261.12623 – ident: e_1_2_9_18_2 doi: 10.1007/s00018-019-03398-6 – ident: e_1_2_9_37_2 doi: 10.3389/fonc.2017.00295 – ident: e_1_2_9_9_2 doi: 10.1186/s13046-017-0628-8 – ident: e_1_2_9_16_2 doi: 10.1016/j.devcel.2019.04.026 – ident: e_1_2_9_10_2 doi: 10.1038/nri1312 |
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SubjectTerms | Animals Epithelial-Mesenchymal Transition Glioblastoma - genetics Glioblastoma - pathology Humans Male Mice Mice, Nude NADPH Oxidase 4 - metabolism Phosphatidylinositol 3-Kinases - metabolism Proto-Oncogene Proteins c-akt - metabolism Reactive Oxygen Species - metabolism Signal Transduction Transfection Transforming Growth Factor beta1 - metabolism |
Title | NOX4-Derived ROS Mediates TGF- β 1-Induced Metabolic Reprogramming during Epithelial-Mesenchymal Transition through the PI3K/AKT/HIF-1 α Pathway in Glioblastoma |
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