Skip to main content
Top
Published in: Journal of Experimental & Clinical Cancer Research 1/2018

Open Access 01-12-2018 | Review

Role of metabolism in cancer cell radioresistance and radiosensitization methods

Authors: Le Tang, Fang Wei, Yingfen Wu, Yi He, Lei Shi, Fang Xiong, Zhaojian Gong, Can Guo, Xiayu Li, Hao Deng, Ke Cao, Ming Zhou, Bo Xiang, Xiaoling Li, Yong Li, Guiyuan Li, Wei Xiong, Zhaoyang Zeng

Published in: Journal of Experimental & Clinical Cancer Research | Issue 1/2018

Login to get access

Abstract

Background

Radioresistance is a major factor leading to the failure of radiotherapy and poor prognosis in tumor patients. Following the application of radiotherapy, the activity of various metabolic pathways considerably changes, which may result in the development of resistance to radiation.

Main body

Here, we discussed the relationships between radioresistance and mitochondrial and glucose metabolic pathways, aiming to elucidate the interplay between the tumor cell metabolism and radiotherapy resistance. In this review, we additionally summarized the potential therapeutic targets in the metabolic pathways.

Short conclusion

The aim of this review was to provide a theoretical basis and relevant references, which may lead to the improvement of the sensitivity of radiotherapy and prolong the survival of cancer patients.
Literature
1.
go back to reference Wei F, Wu Y, Tang L, Xiong F, Guo C, Li X, et al. Trend analysis of cancer incidence and mortality in China. Sci China Life Sci. 2017;60:1271–5.PubMedCrossRef Wei F, Wu Y, Tang L, Xiong F, Guo C, Li X, et al. Trend analysis of cancer incidence and mortality in China. Sci China Life Sci. 2017;60:1271–5.PubMedCrossRef
2.
go back to reference He Y, Jing Y, Wei F, Tang Y, Yang L, Luo J, et al. Long non-coding RNA PVT1 predicts poor prognosis and induces radioresistance by regulating DNA repair and cell apoptosis in nasopharyngeal carcinoma. Cell Death Dis. 2018;9:235. He Y, Jing Y, Wei F, Tang Y, Yang L, Luo J, et al. Long non-coding RNA PVT1 predicts poor prognosis and induces radioresistance by regulating DNA repair and cell apoptosis in nasopharyngeal carcinoma. Cell Death Dis. 2018;9:235.
3.
go back to reference Jagsi R. Progress and controversies: radiation therapy for invasive breast cancer. CA Cancer J Clin. 2014;64:135–52.PubMedCrossRef Jagsi R. Progress and controversies: radiation therapy for invasive breast cancer. CA Cancer J Clin. 2014;64:135–52.PubMedCrossRef
4.
go back to reference Rekers NH, Troost EG, Zegers CM, Germeraad WT, Dubois LJ, Lambin P. Stereotactic ablative body radiotherapy combined with immunotherapy: present status and future perspectives. Cancer Radiother. 2014;18:391–5.PubMedCrossRef Rekers NH, Troost EG, Zegers CM, Germeraad WT, Dubois LJ, Lambin P. Stereotactic ablative body radiotherapy combined with immunotherapy: present status and future perspectives. Cancer Radiother. 2014;18:391–5.PubMedCrossRef
5.
go back to reference Zhong Y, Du Y, Yang X, Mo Y, Fan C, Xiong F, et al. Circular RNAs function as ceRNAs to regulate and control human cancer progression. Mol Cancer. 2018;17:79. Zhong Y, Du Y, Yang X, Mo Y, Fan C, Xiong F, et al. Circular RNAs function as ceRNAs to regulate and control human cancer progression. Mol Cancer. 2018;17:79.
6.
go back to reference Tang Y, He Y, Zhang P, Wang J, Fan C, Yang L, et al. LncRNAs regulate the cytoskeleton and related Rho/ROCK signaling in cancer metastasis. Mol Cancer. 2018;17:77. Tang Y, He Y, Zhang P, Wang J, Fan C, Yang L,  et al. LncRNAs regulate the cytoskeleton and related Rho/ROCK signaling in cancer metastasis. Mol Cancer. 2018;17:77.
7.
8.
go back to reference Liu Z, Xiao Y, Zhou Z, Mao X, Cai J, Xiong L, et al. Extensive metabolic disorders are present in APC(min) tumorigenesis mice. Mol Cell Endocrinol. 2016;427:57–64.PubMedCrossRef Liu Z, Xiao Y, Zhou Z, Mao X, Cai J, Xiong L, et al. Extensive metabolic disorders are present in APC(min) tumorigenesis mice. Mol Cell Endocrinol. 2016;427:57–64.PubMedCrossRef
9.
go back to reference Rani V, Deep G, Singh RK, Palle K, Yadav UC. Oxidative stress and metabolic disorders: pathogenesis and therapeutic strategies. Life Sci. 2016;148:183–93.PubMedCrossRef Rani V, Deep G, Singh RK, Palle K, Yadav UC. Oxidative stress and metabolic disorders: pathogenesis and therapeutic strategies. Life Sci. 2016;148:183–93.PubMedCrossRef
10.
go back to reference Tang Y, Wang J, Lian Y, Fan C, Zhang P, Wu Y, et al. Linking long non-coding RNAs and SWI/SNF complexes to chromatin remodeling in cancer. Mol Cancer. 2017;16:42. Tang Y, Wang J, Lian Y, Fan C, Zhang P, Wu Y, et al. Linking long non-coding RNAs and SWI/SNF complexes to chromatin remodeling in cancer. Mol Cancer. 2017;16:42.
11.
13.
go back to reference Priolo C, Pyne S, Rose J, Regan ER, Zadra G, Photopoulos C, et al. AKT1 and MYC induce distinctive metabolic fingerprints in human prostate cancer. Cancer Res. 2014;74:7198–204.PubMedPubMedCentralCrossRef Priolo C, Pyne S, Rose J, Regan ER, Zadra G, Photopoulos C, et al. AKT1 and MYC induce distinctive metabolic fingerprints in human prostate cancer. Cancer Res. 2014;74:7198–204.PubMedPubMedCentralCrossRef
14.
go back to reference Yang L, Hou Y, Yuan J, Tang S, Zhang H, Zhu Q, et al. Twist promotes reprogramming of glucose metabolism in breast cancer cells through PI3K/AKT and p53 signaling pathways. Oncotarget. 2015;6:25755–69.PubMedPubMedCentral Yang L, Hou Y, Yuan J, Tang S, Zhang H, Zhu Q, et al. Twist promotes reprogramming of glucose metabolism in breast cancer cells through PI3K/AKT and p53 signaling pathways. Oncotarget. 2015;6:25755–69.PubMedPubMedCentral
15.
go back to reference Faubert B, Vincent EE, Griss T, Samborska B, Izreig S, Svensson RU, et al. Loss of the tumor suppressor LKB1 promotes metabolic reprogramming of cancer cells via HIF-1alpha. Proc Natl Acad Sci U S A. 2014;111:2554–9.PubMedPubMedCentralCrossRef Faubert B, Vincent EE, Griss T, Samborska B, Izreig S, Svensson RU, et al. Loss of the tumor suppressor LKB1 promotes metabolic reprogramming of cancer cells via HIF-1alpha. Proc Natl Acad Sci U S A. 2014;111:2554–9.PubMedPubMedCentralCrossRef
16.
go back to reference Gruber S, Straub BK, Ackermann PJ, Wunderlich CM, Mauer J, Seeger JM, et al. Obesity promotes liver carcinogenesis via Mcl-1 stabilization independent of IL-6Ralpha signaling. Cell Rep. 2013;4:669–80.PubMedCrossRef Gruber S, Straub BK, Ackermann PJ, Wunderlich CM, Mauer J, Seeger JM, et al. Obesity promotes liver carcinogenesis via Mcl-1 stabilization independent of IL-6Ralpha signaling. Cell Rep. 2013;4:669–80.PubMedCrossRef
18.
go back to reference Zagar TM, Cardinale DM, Marks LB. Breast cancer therapy-associated cardiovascular disease. Nat Rev Clin Oncol. 2016;13:172–84.PubMedCrossRef Zagar TM, Cardinale DM, Marks LB. Breast cancer therapy-associated cardiovascular disease. Nat Rev Clin Oncol. 2016;13:172–84.PubMedCrossRef
19.
go back to reference Szablewski L. Diabetes mellitus: influences on cancer risk. Diabetes Metab Res Rev. 2014;30:543–53.PubMedCrossRef Szablewski L. Diabetes mellitus: influences on cancer risk. Diabetes Metab Res Rev. 2014;30:543–53.PubMedCrossRef
20.
go back to reference Chong RW, Vasudevan V, Zuber J, Solomon SS. Metformin has a positive therapeutic effect on prostate Cancer in patients with type 2 diabetes mellitus. Am J Med Sci. 2016;351:416–9.PubMedPubMedCentralCrossRef Chong RW, Vasudevan V, Zuber J, Solomon SS. Metformin has a positive therapeutic effect on prostate Cancer in patients with type 2 diabetes mellitus. Am J Med Sci. 2016;351:416–9.PubMedPubMedCentralCrossRef
21.
go back to reference Xu H, Chen K, Jia X, Tian Y, Dai Y, Li D, et al. Metformin use is associated with better survival of breast Cancer patients with diabetes: a meta-analysis. Oncologist. 2015;20:1236–44.PubMedPubMedCentralCrossRef Xu H, Chen K, Jia X, Tian Y, Dai Y, Li D, et al. Metformin use is associated with better survival of breast Cancer patients with diabetes: a meta-analysis. Oncologist. 2015;20:1236–44.PubMedPubMedCentralCrossRef
22.
go back to reference Tseng CH. Metformin reduces ovarian cancer risk in Taiwanese women with type 2 diabetes mellitus. Diabetes Metab Res Rev. 2015;31:619–26.PubMedCrossRef Tseng CH. Metformin reduces ovarian cancer risk in Taiwanese women with type 2 diabetes mellitus. Diabetes Metab Res Rev. 2015;31:619–26.PubMedCrossRef
23.
go back to reference Jones NP, Schulze A. Targeting cancer metabolism--aiming at a tumour's sweet-spot. Drug Discov Today. 2012;17:232–41.PubMedCrossRef Jones NP, Schulze A. Targeting cancer metabolism--aiming at a tumour's sweet-spot. Drug Discov Today. 2012;17:232–41.PubMedCrossRef
24.
go back to reference Pitroda SP, Wakim BT, Sood RF, Beveridge MG, Beckett MA, MacDermed DM, et al. STAT1-dependent expression of energy metabolic pathways links tumour growth and radioresistance to the Warburg effect. BMC Med. 2009;7:68.PubMedPubMedCentralCrossRef Pitroda SP, Wakim BT, Sood RF, Beveridge MG, Beckett MA, MacDermed DM, et al. STAT1-dependent expression of energy metabolic pathways links tumour growth and radioresistance to the Warburg effect. BMC Med. 2009;7:68.PubMedPubMedCentralCrossRef
25.
go back to reference Shimura T, Noma N, Sano Y, Ochiai Y, Oikawa T, Fukumoto M, et al. AKT-mediated enhanced aerobic glycolysis causes acquired radioresistance by human tumor cells. Radiother Oncol. 2014;112:302–7.PubMedCrossRef Shimura T, Noma N, Sano Y, Ochiai Y, Oikawa T, Fukumoto M, et al. AKT-mediated enhanced aerobic glycolysis causes acquired radioresistance by human tumor cells. Radiother Oncol. 2014;112:302–7.PubMedCrossRef
26.
go back to reference Sattler UG, Meyer SS, Quennet V, Hoerner C, Knoerzer H, Fabian C, et al. Glycolytic metabolism and tumour response to fractionated irradiation. Radiother Oncol. 2010;94:102–9.PubMedCrossRef Sattler UG, Meyer SS, Quennet V, Hoerner C, Knoerzer H, Fabian C, et al. Glycolytic metabolism and tumour response to fractionated irradiation. Radiother Oncol. 2010;94:102–9.PubMedCrossRef
27.
go back to reference Viale A, Pettazzoni P, Lyssiotis CA, Ying H, Sanchez N, Marchesini M, et al. Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function. Nature. 2014;514:628–32.PubMedPubMedCentralCrossRef Viale A, Pettazzoni P, Lyssiotis CA, Ying H, Sanchez N, Marchesini M, et al. Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function. Nature. 2014;514:628–32.PubMedPubMedCentralCrossRef
28.
go back to reference Liu R, Fan M, Candas D, Qin L, Zhang X, Eldridge A, et al. CDK1-mediated SIRT3 activation enhances mitochondrial function and tumor Radioresistance. Mol Cancer Ther. 2015;14:2090–102.PubMedPubMedCentralCrossRef Liu R, Fan M, Candas D, Qin L, Zhang X, Eldridge A, et al. CDK1-mediated SIRT3 activation enhances mitochondrial function and tumor Radioresistance. Mol Cancer Ther. 2015;14:2090–102.PubMedPubMedCentralCrossRef
29.
30.
go back to reference Delaney G, Jacob S, Featherstone C, Barton M. The role of radiotherapy in cancer treatment: estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer. 2005;104:1129–37.PubMedCrossRef Delaney G, Jacob S, Featherstone C, Barton M. The role of radiotherapy in cancer treatment: estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer. 2005;104:1129–37.PubMedCrossRef
31.
go back to reference Dahm-Daphi J, Sass C, Alberti W. Comparison of biological effects of DNA damage induced by ionizing radiation and hydrogen peroxide in CHO cells. Int J Radiat Biol. 2000;76:67–75.PubMedCrossRef Dahm-Daphi J, Sass C, Alberti W. Comparison of biological effects of DNA damage induced by ionizing radiation and hydrogen peroxide in CHO cells. Int J Radiat Biol. 2000;76:67–75.PubMedCrossRef
32.
go back to reference Chevalier F, Hamdi DH, Saintigny Y, Lefaix JL. Proteomic overview and perspectives of the radiation-induced bystander effects. Mutat Res Rev Mutat Res. 2015;763:280–93.PubMedCrossRef Chevalier F, Hamdi DH, Saintigny Y, Lefaix JL. Proteomic overview and perspectives of the radiation-induced bystander effects. Mutat Res Rev Mutat Res. 2015;763:280–93.PubMedCrossRef
33.
go back to reference Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–60.PubMedCrossRef Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–60.PubMedCrossRef
34.
go back to reference Luo M, Ding L, Li Q, Yao H. miR-668 enhances the radioresistance of human breast cancer cell by targeting IkappaBalpha. Breast cancer. 2017;24:673–82.PubMedCrossRef Luo M, Ding L, Li Q, Yao H. miR-668 enhances the radioresistance of human breast cancer cell by targeting IkappaBalpha. Breast cancer. 2017;24:673–82.PubMedCrossRef
35.
go back to reference Huang T, Yin L, Wu J, Gu JJ, Wu JZ, Chen D, et al. MicroRNA-19b-3p regulates nasopharyngeal carcinoma radiosensitivity by targeting TNFAIP3/NF-kappaB axis. J Exp Clin Cancer Res. 2016;35:188.PubMedPubMedCentralCrossRef Huang T, Yin L, Wu J, Gu JJ, Wu JZ, Chen D, et al. MicroRNA-19b-3p regulates nasopharyngeal carcinoma radiosensitivity by targeting TNFAIP3/NF-kappaB axis. J Exp Clin Cancer Res. 2016;35:188.PubMedPubMedCentralCrossRef
36.
go back to reference Toulany M, Schickfluss TA, Eicheler W, Kehlbach R, Schittek B, Rodemann HP. Impact of oncogenic K-RAS on YB-1 phosphorylation induced by ionizing radiation. Breast Cancer Res. 2011;13:R28.PubMedPubMedCentralCrossRef Toulany M, Schickfluss TA, Eicheler W, Kehlbach R, Schittek B, Rodemann HP. Impact of oncogenic K-RAS on YB-1 phosphorylation induced by ionizing radiation. Breast Cancer Res. 2011;13:R28.PubMedPubMedCentralCrossRef
37.
go back to reference Bur H, Haapasaari KM, Turpeenniemi-Hujanen T, Kuittinen O, Auvinen P, Marin K, et al. Low Rap1-interacting factor 1 and sirtuin 6 expression predict poor outcome in radiotherapy-treated Hodgkin lymphoma patients. Leuk Lymphoma. 2018;59:679–89. Bur H, Haapasaari KM, Turpeenniemi-Hujanen T, Kuittinen O, Auvinen P, Marin K, et al. Low Rap1-interacting factor 1 and sirtuin 6 expression predict poor outcome in radiotherapy-treated Hodgkin lymphoma patients. Leuk Lymphoma. 2018;59:679–89.
38.
go back to reference Jang NY, Kim DH, Cho BJ, Choi EJ, Lee JS, Wu HG, et al. Radiosensitization with combined use of olaparib and PI-103 in triple-negative breast cancer. BMC Cancer. 2015;15:89.PubMedPubMedCentralCrossRef Jang NY, Kim DH, Cho BJ, Choi EJ, Lee JS, Wu HG, et al. Radiosensitization with combined use of olaparib and PI-103 in triple-negative breast cancer. BMC Cancer. 2015;15:89.PubMedPubMedCentralCrossRef
39.
go back to reference de Sousa MML, Bjoras KO, Hanssen-Bauer A, Solvang-Garten K, Otterlei M. p38 MAPK signaling and phosphorylations in the BRCT1 domain regulate XRCC1 recruitment to sites of DNA damage. Sci Rep. 2017;7:6322.PubMedPubMedCentralCrossRef de Sousa MML, Bjoras KO, Hanssen-Bauer A, Solvang-Garten K, Otterlei M. p38 MAPK signaling and phosphorylations in the BRCT1 domain regulate XRCC1 recruitment to sites of DNA damage. Sci Rep. 2017;7:6322.PubMedPubMedCentralCrossRef
40.
go back to reference Jang J, Huh YJ, Cho HJ, Lee B, Park J, Hwang DY, et al. SIRT1 enhances the survival of human embryonic stem cells by promoting DNA repair. Stem Cell Reports. 2017;9:629–41.PubMedPubMedCentralCrossRef Jang J, Huh YJ, Cho HJ, Lee B, Park J, Hwang DY, et al. SIRT1 enhances the survival of human embryonic stem cells by promoting DNA repair. Stem Cell Reports. 2017;9:629–41.PubMedPubMedCentralCrossRef
41.
go back to reference Chen Y, Li Z, Dong Z, Beebe J, Yang K, Fu L, et al. 14-3-3sigma contributes to Radioresistance by regulating DNA repair and cell cycle via PARP1 and CHK2. Mol Cancer Res. 2017;15:418–28.PubMedPubMedCentralCrossRef Chen Y, Li Z, Dong Z, Beebe J, Yang K, Fu L, et al. 14-3-3sigma contributes to Radioresistance by regulating DNA repair and cell cycle via PARP1 and CHK2. Mol Cancer Res. 2017;15:418–28.PubMedPubMedCentralCrossRef
42.
go back to reference Gogineni VR, Nalla AK, Gupta R, Dinh DH, Klopfenstein JD, Rao JS. Chk2-mediated G2/M cell cycle arrest maintains radiation resistance in malignant meningioma cells. Cancer Lett. 2011;313:64–75.PubMedPubMedCentralCrossRef Gogineni VR, Nalla AK, Gupta R, Dinh DH, Klopfenstein JD, Rao JS. Chk2-mediated G2/M cell cycle arrest maintains radiation resistance in malignant meningioma cells. Cancer Lett. 2011;313:64–75.PubMedPubMedCentralCrossRef
43.
go back to reference Wei F, Tang L, He Y, Wu Y, Shi L, Xiong F, et al. BPIFB1 (LPLUNC1) inhibits radioresistance in nasopharyngeal carcinoma by inhibiting VTN expression. Cell Death Dis. 2018;9:432.PubMedCrossRefPubMedCentral Wei F, Tang L, He Y, Wu Y, Shi L, Xiong F, et al. BPIFB1 (LPLUNC1) inhibits radioresistance in nasopharyngeal carcinoma by inhibiting VTN expression. Cell Death Dis. 2018;9:432.PubMedCrossRefPubMedCentral
44.
go back to reference Wei F, Wu Y, Tang L, He Y, Shi L, Xiong F, et al. BPIFB1 (LPLUNC1) inhibits migration and invasion of nasopharyngeal carcinoma by interacting with VTN and VIM. Br J Cancer. 2018;118:233–47.PubMedCrossRef Wei F, Wu Y, Tang L, He Y, Shi L, Xiong F, et al. BPIFB1 (LPLUNC1) inhibits migration and invasion of nasopharyngeal carcinoma by interacting with VTN and VIM. Br J Cancer. 2018;118:233–47.PubMedCrossRef
45.
go back to reference Zhou R, Wu Y, Wang W, Su W, Liu Y, Wang Y, et al. Circular RNAs (circRNAs) in cancer. Cancer Lett. 2018;425:134–42. Zhou R, Wu Y, Wang W, Su W, Liu Y, Wang Y, et al. Circular RNAs (circRNAs) in cancer. Cancer Lett. 2018;425:134–42.
46.
go back to reference Zhang X, Li Y, Wang D, Wei X. miR-22 suppresses tumorigenesis and improves radiosensitivity of breast cancer cells by targeting Sirt1. Biol Res. 2017;50:27.PubMedPubMedCentralCrossRef Zhang X, Li Y, Wang D, Wei X. miR-22 suppresses tumorigenesis and improves radiosensitivity of breast cancer cells by targeting Sirt1. Biol Res. 2017;50:27.PubMedPubMedCentralCrossRef
47.
go back to reference Tang Y, He Y, Shi L, Yang L, Wang J, Lian Y, et al. Co-expression of AFAP1-AS1 and PD-1 predicts poor prognosis in nasopharyngeal carcinoma. Oncotarget. 2017;8:39001–11.PubMedPubMedCentral Tang Y, He Y, Shi L, Yang L, Wang J, Lian Y, et al. Co-expression of AFAP1-AS1 and PD-1 predicts poor prognosis in nasopharyngeal carcinoma. Oncotarget. 2017;8:39001–11.PubMedPubMedCentral
48.
go back to reference Goffart N, Lombard A, Lallemand F, Kroonen J, Nassen J, Di Valentin E, et al. CXCL12 mediates glioblastoma resistance to radiotherapy in the subventricular zone. Neuro-Oncology. 2017;19:66–77.PubMedCrossRef Goffart N, Lombard A, Lallemand F, Kroonen J, Nassen J, Di Valentin E, et al. CXCL12 mediates glioblastoma resistance to radiotherapy in the subventricular zone. Neuro-Oncology. 2017;19:66–77.PubMedCrossRef
49.
go back to reference Zhang Y, Xia M, Jin K, Wang S, Wei H, Fan C, et al. Function of the c-Met receptor tyrosine kinase in carcinogenesis and associated therapeutic opportunities. Mol Cancer. 2018;17:45. Zhang Y, Xia M, Jin K, Wang S, Wei H, Fan C, et al. Function of the c-Met receptor tyrosine kinase in carcinogenesis and associated therapeutic opportunities. Mol Cancer. 2018;17:45.
50.
go back to reference Zhang H, Luo H, Jiang Z, Yue J, Hou Q, Xie R, et al. Fractionated irradiation-induced EMT-like phenotype conferred radioresistance in esophageal squamous cell carcinoma. J Radiat Res. 2016;57:370–80.PubMedPubMedCentralCrossRef Zhang H, Luo H, Jiang Z, Yue J, Hou Q, Xie R, et al. Fractionated irradiation-induced EMT-like phenotype conferred radioresistance in esophageal squamous cell carcinoma. J Radiat Res. 2016;57:370–80.PubMedPubMedCentralCrossRef
51.
go back to reference Xie G, Liu Y, Yao Q, Zheng R, Zhang L, Lin J, et al. Hypoxia-induced angiotensin II by the lactate-chymase-dependent mechanism mediates radioresistance of hypoxic tumor cells. Sci Rep. 2017;7:42396.PubMedPubMedCentralCrossRef Xie G, Liu Y, Yao Q, Zheng R, Zhang L, Lin J, et al. Hypoxia-induced angiotensin II by the lactate-chymase-dependent mechanism mediates radioresistance of hypoxic tumor cells. Sci Rep. 2017;7:42396.PubMedPubMedCentralCrossRef
52.
go back to reference Yoshida GJ, Saya H. Therapeutic strategies targeting cancer stem cells. Cancer Sci. 2016;107:5–11.PubMedCrossRef Yoshida GJ, Saya H. Therapeutic strategies targeting cancer stem cells. Cancer Sci. 2016;107:5–11.PubMedCrossRef
53.
54.
go back to reference Yang L, Tang Y, Xiong F, He Y, Wei F, Zhang S, et al. LncRNAs regulate cancer metastasis via binding to functional proteins. Oncotarget. 2017;9(1):1426–43. Yang L, Tang Y, Xiong F, He Y, Wei F, Zhang S, et al. LncRNAs regulate cancer metastasis via binding to functional proteins. Oncotarget. 2017;9(1):1426–43.
55.
56.
go back to reference Gao AM, Ke ZP, Shi F, Sun GC, Chen H. Chrysin enhances sensitivity of BEL-7402/ADM cells to doxorubicin by suppressing PI3K/Akt/Nrf2 and ERK/Nrf2 pathway. Chem Biol Interact. 2013;206:100–8.PubMedCrossRef Gao AM, Ke ZP, Shi F, Sun GC, Chen H. Chrysin enhances sensitivity of BEL-7402/ADM cells to doxorubicin by suppressing PI3K/Akt/Nrf2 and ERK/Nrf2 pathway. Chem Biol Interact. 2013;206:100–8.PubMedCrossRef
57.
go back to reference Chang L, Graham PH, Hao J, Ni J, Bucci J, Cozzi PJ, et al. PI3K/Akt/mTOR pathway inhibitors enhance radiosensitivity in radioresistant prostate cancer cells through inducing apoptosis, reducing autophagy, suppressing NHEJ and HR repair pathways. Cell Death Dis. 2014;5:e1437.PubMedPubMedCentralCrossRef Chang L, Graham PH, Hao J, Ni J, Bucci J, Cozzi PJ, et al. PI3K/Akt/mTOR pathway inhibitors enhance radiosensitivity in radioresistant prostate cancer cells through inducing apoptosis, reducing autophagy, suppressing NHEJ and HR repair pathways. Cell Death Dis. 2014;5:e1437.PubMedPubMedCentralCrossRef
58.
go back to reference Chen X, Wang P, Guo F, Wang X, Wang J, Xu J, et al. Autophagy enhanced the radioresistance of non-small cell lung cancer by regulating ROS level under hypoxia condition. Int J Radiat Biol. 2017;93:764–70.PubMedCrossRef Chen X, Wang P, Guo F, Wang X, Wang J, Xu J, et al. Autophagy enhanced the radioresistance of non-small cell lung cancer by regulating ROS level under hypoxia condition. Int J Radiat Biol. 2017;93:764–70.PubMedCrossRef
59.
go back to reference Lei Y, Zhang D, Yu J, Dong H, Zhang J, Yang S. Targeting autophagy in cancer stem cells as an anticancer therapy. Cancer Lett. 2017;393:33–9.PubMedCrossRef Lei Y, Zhang D, Yu J, Dong H, Zhang J, Yang S. Targeting autophagy in cancer stem cells as an anticancer therapy. Cancer Lett. 2017;393:33–9.PubMedCrossRef
60.
go back to reference Chan R, Sethi P, Jyoti A, McGarry R, Upreti M. Investigating the Radioresistant properties of lung Cancer stem cells in the context of the tumor microenvironment. Radiat Res. 2016;185:169–81.PubMedPubMedCentralCrossRef Chan R, Sethi P, Jyoti A, McGarry R, Upreti M. Investigating the Radioresistant properties of lung Cancer stem cells in the context of the tumor microenvironment. Radiat Res. 2016;185:169–81.PubMedPubMedCentralCrossRef
61.
go back to reference Li F, Zhou K, Gao L, Zhang B, Li W, Yan W, et al. Radiation induces the generation of cancer stem cells: a novel mechanism for cancer radioresistance. Oncol Lett. 2016;12:3059–65.PubMedPubMedCentralCrossRef Li F, Zhou K, Gao L, Zhang B, Li W, Yan W, et al. Radiation induces the generation of cancer stem cells: a novel mechanism for cancer radioresistance. Oncol Lett. 2016;12:3059–65.PubMedPubMedCentralCrossRef
62.
go back to reference Chi HC, Tsai CY, Tsai MM, Yeh CT, Lin KH. Roles of long noncoding RNAs in recurrence and metastasis of radiotherapy-resistant Cancer stem cells. Int J Mol Sci. 2017;18:E1903.PubMedCrossRef Chi HC, Tsai CY, Tsai MM, Yeh CT, Lin KH. Roles of long noncoding RNAs in recurrence and metastasis of radiotherapy-resistant Cancer stem cells. Int J Mol Sci. 2017;18:E1903.PubMedCrossRef
63.
go back to reference Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11:69–82.PubMedCrossRef Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11:69–82.PubMedCrossRef
64.
go back to reference Osuka S, Sampetrean O, Shimizu T, Saga I, Onishi N, Sugihara E, et al. IGF1 receptor signaling regulates adaptive radioprotection in glioma stem cells. Stem cells. 2013;31:627–40.PubMedCrossRef Osuka S, Sampetrean O, Shimizu T, Saga I, Onishi N, Sugihara E, et al. IGF1 receptor signaling regulates adaptive radioprotection in glioma stem cells. Stem cells. 2013;31:627–40.PubMedCrossRef
65.
go back to reference Shimizu T, Sugihara E, Yamaguchi-Iwai S, Tamaki S, Koyama Y, Kamel W, et al. IGF2 preserves osteosarcoma cell survival by creating an autophagic state of dormancy that protects cells against chemotherapeutic stress. Cancer Res. 2014;74:6531–41.PubMedCrossRef Shimizu T, Sugihara E, Yamaguchi-Iwai S, Tamaki S, Koyama Y, Kamel W, et al. IGF2 preserves osteosarcoma cell survival by creating an autophagic state of dormancy that protects cells against chemotherapeutic stress. Cancer Res. 2014;74:6531–41.PubMedCrossRef
66.
go back to reference Ning X, Shu J, Du Y, Ben Q, Li Z. Therapeutic strategies targeting cancer stem cells. Cancer Biol Therapy. 2013;14:295–303.CrossRef Ning X, Shu J, Du Y, Ben Q, Li Z. Therapeutic strategies targeting cancer stem cells. Cancer Biol Therapy. 2013;14:295–303.CrossRef
67.
go back to reference Yu L, Sun Y, Li J, Wang Y, Zhu Y, Shi Y, et al. Silencing the Girdin gene enhances radio-sensitivity of hepatocellular carcinoma via suppression of glycolytic metabolism. J Exp Clin Cancer Res. 2017;36:110.PubMedPubMedCentralCrossRef Yu L, Sun Y, Li J, Wang Y, Zhu Y, Shi Y, et al. Silencing the Girdin gene enhances radio-sensitivity of hepatocellular carcinoma via suppression of glycolytic metabolism. J Exp Clin Cancer Res. 2017;36:110.PubMedPubMedCentralCrossRef
68.
go back to reference Bol V, Bol A, Bouzin C, Labar D, Lee JA, Janssens G, et al. Reprogramming of tumor metabolism by targeting mitochondria improves tumor response to irradiation. Acta Oncol. 2015;54:266–74.PubMedCrossRef Bol V, Bol A, Bouzin C, Labar D, Lee JA, Janssens G, et al. Reprogramming of tumor metabolism by targeting mitochondria improves tumor response to irradiation. Acta Oncol. 2015;54:266–74.PubMedCrossRef
70.
go back to reference Nicolau-Galmes F, Asumendi A, Alonso-Tejerina E, Perez-Yarza G, Jangi SM, Gardeazabal J, et al. Terfenadine induces apoptosis and autophagy in melanoma cells through ROS-dependent and -independent mechanisms. Apoptosis. 2011;16:1253–67.PubMedPubMedCentralCrossRef Nicolau-Galmes F, Asumendi A, Alonso-Tejerina E, Perez-Yarza G, Jangi SM, Gardeazabal J, et al. Terfenadine induces apoptosis and autophagy in melanoma cells through ROS-dependent and -independent mechanisms. Apoptosis. 2011;16:1253–67.PubMedPubMedCentralCrossRef
71.
go back to reference Jeong HJ, Oh HA, Nam SY, Han NR, Kim YS, Kim JH, et al. The critical role of mast cell-derived hypoxia-inducible factor-1alpha in human and mice melanoma growth. Int J Cancer. 2013;132:2492–501.PubMedCrossRef Jeong HJ, Oh HA, Nam SY, Han NR, Kim YS, Kim JH, et al. The critical role of mast cell-derived hypoxia-inducible factor-1alpha in human and mice melanoma growth. Int J Cancer. 2013;132:2492–501.PubMedCrossRef
72.
go back to reference Li Z, Zhang H. Reprogramming of glucose, fatty acid and amino acid metabolism for cancer progression. Cell Mol Life Sci. 2016;73:377–92.PubMedCrossRef Li Z, Zhang H. Reprogramming of glucose, fatty acid and amino acid metabolism for cancer progression. Cell Mol Life Sci. 2016;73:377–92.PubMedCrossRef
73.
go back to reference Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029–33.PubMedPubMedCentralCrossRef Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029–33.PubMedPubMedCentralCrossRef
74.
75.
go back to reference Li L, Li W. Epithelial-mesenchymal transition in human cancer: comprehensive reprogramming of metabolism, epigenetics, and differentiation. Pharmacol Ther. 2015;150:33–46.PubMedCrossRef Li L, Li W. Epithelial-mesenchymal transition in human cancer: comprehensive reprogramming of metabolism, epigenetics, and differentiation. Pharmacol Ther. 2015;150:33–46.PubMedCrossRef
76.
go back to reference Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer. 2004;4:891–9.PubMedCrossRef Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer. 2004;4:891–9.PubMedCrossRef
77.
go back to reference Bhatt AN, Chauhan A, Khanna S, Rai Y, Singh S, Soni R, et al. Transient elevation of glycolysis confers radio-resistance by facilitating DNA repair in cells. BMC Cancer. 2015;15:335.PubMedPubMedCentralCrossRef Bhatt AN, Chauhan A, Khanna S, Rai Y, Singh S, Soni R, et al. Transient elevation of glycolysis confers radio-resistance by facilitating DNA repair in cells. BMC Cancer. 2015;15:335.PubMedPubMedCentralCrossRef
78.
go back to reference Fang J, Zhou SH, Fan J, Yan SX. Roles of glucose transporter-1 and the phosphatidylinositol 3kinase/protein kinase B pathway in cancer radioresistance (review). Mol Med Rep. 2015;11:1573–81.PubMedCrossRef Fang J, Zhou SH, Fan J, Yan SX. Roles of glucose transporter-1 and the phosphatidylinositol 3kinase/protein kinase B pathway in cancer radioresistance (review). Mol Med Rep. 2015;11:1573–81.PubMedCrossRef
79.
go back to reference Liu J, Zhang J, Wang X, Li Y, Chen Y, Li K, et al. HIF-1 and NDRG2 contribute to hypoxia-induced radioresistance of cervical cancer Hela cells. Exp Cell Res. 2010;316:1985–93.PubMedCrossRef Liu J, Zhang J, Wang X, Li Y, Chen Y, Li K, et al. HIF-1 and NDRG2 contribute to hypoxia-induced radioresistance of cervical cancer Hela cells. Exp Cell Res. 2010;316:1985–93.PubMedCrossRef
80.
go back to reference Quennet V, Yaromina A, Zips D, Rosner A, Walenta S, Baumann M, et al. Tumor lactate content predicts for response to fractionated irradiation of human squamous cell carcinomas in nude mice. Radiother Oncol. 2006;81:130–5.PubMedCrossRef Quennet V, Yaromina A, Zips D, Rosner A, Walenta S, Baumann M, et al. Tumor lactate content predicts for response to fractionated irradiation of human squamous cell carcinomas in nude mice. Radiother Oncol. 2006;81:130–5.PubMedCrossRef
81.
go back to reference Sun L, Zeng X, Yan C, Sun X, Gong X, Rao Y, et al. Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature. 2012;490:361–6.PubMedCrossRef Sun L, Zeng X, Yan C, Sun X, Gong X, Rao Y, et al. Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature. 2012;490:361–6.PubMedCrossRef
82.
go back to reference Chung FY, Huang MY, Yeh CS, Chang HJ, Cheng TL, Yen LC, et al. GLUT1 gene is a potential hypoxic marker in colorectal cancer patients. BMC Cancer. 2009;9:241.PubMedPubMedCentralCrossRef Chung FY, Huang MY, Yeh CS, Chang HJ, Cheng TL, Yen LC, et al. GLUT1 gene is a potential hypoxic marker in colorectal cancer patients. BMC Cancer. 2009;9:241.PubMedPubMedCentralCrossRef
83.
go back to reference Kunkel M, Moergel M, Stockinger M, Jeong JH, Fritz G, Lehr HA, et al. Overexpression of GLUT-1 is associated with resistance to radiotherapy and adverse prognosis in squamous cell carcinoma of the oral cavity. Oral Oncol. 2007;43:796–803.PubMedCrossRef Kunkel M, Moergel M, Stockinger M, Jeong JH, Fritz G, Lehr HA, et al. Overexpression of GLUT-1 is associated with resistance to radiotherapy and adverse prognosis in squamous cell carcinoma of the oral cavity. Oral Oncol. 2007;43:796–803.PubMedCrossRef
84.
go back to reference De Schutter H, Landuyt W, Verbeken E, Goethals L, Hermans R, Nuyts S. The prognostic value of the hypoxia markers CA IX and GLUT 1 and the cytokines VEGF and IL 6 in head and neck squamous cell carcinoma treated by radiotherapy +/− chemotherapy. BMC Cancer. 2005;5:42.PubMedPubMedCentralCrossRef De Schutter H, Landuyt W, Verbeken E, Goethals L, Hermans R, Nuyts S. The prognostic value of the hypoxia markers CA IX and GLUT 1 and the cytokines VEGF and IL 6 in head and neck squamous cell carcinoma treated by radiotherapy +/− chemotherapy. BMC Cancer. 2005;5:42.PubMedPubMedCentralCrossRef
85.
go back to reference Luo XM, Zhou SH, Fan J. Glucose transporter-1 as a new therapeutic target in laryngeal carcinoma. J Int Med Res. 2010;38:1885–92.PubMedCrossRef Luo XM, Zhou SH, Fan J. Glucose transporter-1 as a new therapeutic target in laryngeal carcinoma. J Int Med Res. 2010;38:1885–92.PubMedCrossRef
86.
go back to reference Melstrom LG, Salabat MR, Ding XZ, Strouch MJ, Grippo PJ, Mirzoeva S, et al. Apigenin down-regulates the hypoxia response genes: HIF-1alpha, GLUT-1, and VEGF in human pancreatic cancer cells. J Surg Res. 2011;167:173–81.PubMedCrossRef Melstrom LG, Salabat MR, Ding XZ, Strouch MJ, Grippo PJ, Mirzoeva S, et al. Apigenin down-regulates the hypoxia response genes: HIF-1alpha, GLUT-1, and VEGF in human pancreatic cancer cells. J Surg Res. 2011;167:173–81.PubMedCrossRef
87.
go back to reference Bao YY, Zhou SH, Lu ZJ, Fan J, Huang YP. Inhibiting GLUT-1 expression and PI3K/Akt signaling using apigenin improves the radiosensitivity of laryngeal carcinoma in vivo. Oncol Rep. 2015;34:1805–14.PubMedCrossRef Bao YY, Zhou SH, Lu ZJ, Fan J, Huang YP. Inhibiting GLUT-1 expression and PI3K/Akt signaling using apigenin improves the radiosensitivity of laryngeal carcinoma in vivo. Oncol Rep. 2015;34:1805–14.PubMedCrossRef
88.
go back to reference Fang J, Bao YY, Zhou SH, Fan J. Apigenin inhibits the proliferation of adenoid cystic carcinoma via suppression of glucose transporter-1. Mol Med Rep. 2015;12:6461–6.PubMedPubMedCentralCrossRef Fang J, Bao YY, Zhou SH, Fan J. Apigenin inhibits the proliferation of adenoid cystic carcinoma via suppression of glucose transporter-1. Mol Med Rep. 2015;12:6461–6.PubMedPubMedCentralCrossRef
89.
go back to reference Erdogan S, Doganlar O, Doganlar ZB, Serttas R, Turkekul K, Dibirdik I, et al. The flavonoid apigenin reduces prostate cancer CD44(+) stem cell survival and migration through PI3K/Akt/NF-kappaB signaling. Life Sci. 2016;162:77–86.PubMedCrossRef Erdogan S, Doganlar O, Doganlar ZB, Serttas R, Turkekul K, Dibirdik I, et al. The flavonoid apigenin reduces prostate cancer CD44(+) stem cell survival and migration through PI3K/Akt/NF-kappaB signaling. Life Sci. 2016;162:77–86.PubMedCrossRef
90.
go back to reference Liu W, Fang Y, Wang X-T, Liu J, Dan X, Sun L-L. Overcoming 5-Fu resistance of Colon cells through inhibition of Glut1 by the specific inhibitor WZB117. Asian Pac J Cancer Prev. 2014;15:7037–41.PubMedCrossRef Liu W, Fang Y, Wang X-T, Liu J, Dan X, Sun L-L. Overcoming 5-Fu resistance of Colon cells through inhibition of Glut1 by the specific inhibitor WZB117. Asian Pac J Cancer Prev. 2014;15:7037–41.PubMedCrossRef
91.
go back to reference Zhao F, Ming J, Zhou Y, Fan L. Inhibition of Glut1 by WZB117 sensitizes radioresistant breast cancer cells to irradiation. Cancer Chemother Pharmacol. 2016;77:963–72.PubMedCrossRef Zhao F, Ming J, Zhou Y, Fan L. Inhibition of Glut1 by WZB117 sensitizes radioresistant breast cancer cells to irradiation. Cancer Chemother Pharmacol. 2016;77:963–72.PubMedCrossRef
92.
go back to reference Yan SX, Luo XM, Zhou SH, Bao YY, Fan J, Lu ZJ, et al. Effect of antisense oligodeoxynucleotides glucose transporter-1 on enhancement of radiosensitivity of laryngeal carcinoma. Int J Med Sci. 2013;10:1375–86.PubMedPubMedCentralCrossRef Yan SX, Luo XM, Zhou SH, Bao YY, Fan J, Lu ZJ, et al. Effect of antisense oligodeoxynucleotides glucose transporter-1 on enhancement of radiosensitivity of laryngeal carcinoma. Int J Med Sci. 2013;10:1375–86.PubMedPubMedCentralCrossRef
93.
go back to reference Zhou SH, Fan J, Chen XM, Cheng KJ, Wang SQ. Inhibition of cell proliferation and glucose uptake in human laryngeal carcinoma cells by antisense oligonucleotides against glucose transporter-1. Head neck. 2009;31:1624–33.PubMedCrossRef Zhou SH, Fan J, Chen XM, Cheng KJ, Wang SQ. Inhibition of cell proliferation and glucose uptake in human laryngeal carcinoma cells by antisense oligonucleotides against glucose transporter-1. Head neck. 2009;31:1624–33.PubMedCrossRef
94.
go back to reference Luo XM, Xu B, Zhou ML, Bao YY, Zhou SH, Fan J, et al. Co-inhibition of GLUT-1 expression and the PI3K/Akt signaling pathway to enhance the Radiosensitivity of laryngeal carcinoma xenografts in vivo. PLoS One. 2015;10:e0143306.PubMedPubMedCentralCrossRef Luo XM, Xu B, Zhou ML, Bao YY, Zhou SH, Fan J, et al. Co-inhibition of GLUT-1 expression and the PI3K/Akt signaling pathway to enhance the Radiosensitivity of laryngeal carcinoma xenografts in vivo. PLoS One. 2015;10:e0143306.PubMedPubMedCentralCrossRef
95.
go back to reference Blatt S, Voelxen N, Sagheb K, Pabst AM, Walenta S, Schroeder T, et al. Lactate as a predictive marker for tumor recurrence in patients with head and neck squamous cell carcinoma (HNSCC) post radiation: a prospective study over 15 years. Clin Oral Investig. 2016;20:2097–104.PubMedCrossRef Blatt S, Voelxen N, Sagheb K, Pabst AM, Walenta S, Schroeder T, et al. Lactate as a predictive marker for tumor recurrence in patients with head and neck squamous cell carcinoma (HNSCC) post radiation: a prospective study over 15 years. Clin Oral Investig. 2016;20:2097–104.PubMedCrossRef
96.
go back to reference Voelxen NF, Blatt S, Knopf P, Henkel M, Appelhans C, Righesso LAR, et al. Comparative metabolic analysis in head and neck cancer and the normal gingiva. Clin Oral Investig. 2018;22:1033–43. Voelxen NF, Blatt S, Knopf P, Henkel M, Appelhans C, Righesso LAR, et al. Comparative metabolic analysis in head and neck cancer and the normal gingiva. Clin Oral Investig. 2018;22:1033–43.
97.
go back to reference Fujiwara S, Wada N, Kawano Y, Okuno Y, Kikukawa Y, Endo S, et al. Lactate, a putative survival factor for myeloma cells, is incorporated by myeloma cells through monocarboxylate transporters 1. Exp Hematol Oncol. 2015;4:12.PubMedPubMedCentralCrossRef Fujiwara S, Wada N, Kawano Y, Okuno Y, Kikukawa Y, Endo S, et al. Lactate, a putative survival factor for myeloma cells, is incorporated by myeloma cells through monocarboxylate transporters 1. Exp Hematol Oncol. 2015;4:12.PubMedPubMedCentralCrossRef
98.
go back to reference Sandulache VC, Chen Y, Skinner HD, Lu T, Feng L, Court LE, et al. Acute tumor lactate perturbations as a biomarker of genotoxic stress: development of a biochemical model. Mol Cancer Ther. 2015;14:2901–8.PubMedPubMedCentralCrossRef Sandulache VC, Chen Y, Skinner HD, Lu T, Feng L, Court LE, et al. Acute tumor lactate perturbations as a biomarker of genotoxic stress: development of a biochemical model. Mol Cancer Ther. 2015;14:2901–8.PubMedPubMedCentralCrossRef
99.
go back to reference Koukourakis MI, Giatromanolaki A, Harris AL, Sivridis E. Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: a metabolic survival role for tumor-associated stroma. Cancer Res. 2006;66:632–7.PubMedCrossRef Koukourakis MI, Giatromanolaki A, Harris AL, Sivridis E. Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: a metabolic survival role for tumor-associated stroma. Cancer Res. 2006;66:632–7.PubMedCrossRef
100.
go back to reference Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, Edinger M, et al. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood. 2007;109:3812–9.PubMedCrossRef Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, Edinger M, et al. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood. 2007;109:3812–9.PubMedCrossRef
101.
go back to reference Feng J, Yang H, Zhang Y, Wei H, Zhu Z, Zhu B, et al. Tumor cell-derived lactate induces TAZ-dependent upregulation of PD-L1 through GPR81 in human lung cancer cells. Oncogene. 2017;36(42):5829–39.PubMedCrossRef Feng J, Yang H, Zhang Y, Wei H, Zhu Z, Zhu B, et al. Tumor cell-derived lactate induces TAZ-dependent upregulation of PD-L1 through GPR81 in human lung cancer cells. Oncogene. 2017;36(42):5829–39.PubMedCrossRef
102.
go back to reference Hirschhaeuser F, Sattler UG, Mueller-Klieser W. Lactate: a metabolic key player in cancer. Cancer Res. 2011;71:6921–5.PubMedCrossRef Hirschhaeuser F, Sattler UG, Mueller-Klieser W. Lactate: a metabolic key player in cancer. Cancer Res. 2011;71:6921–5.PubMedCrossRef
103.
go back to reference Halestrap AP. The monocarboxylate transporter family--structure and functional characterization. IUBMB Life. 2012;64:1–9.PubMedCrossRef Halestrap AP. The monocarboxylate transporter family--structure and functional characterization. IUBMB Life. 2012;64:1–9.PubMedCrossRef
104.
go back to reference Yan C, Yang F, Zhou C, Chen X, Han X, Liu X, et al. MCT1 promotes the cisplatin-resistance by antagonizing Fas in epithelial ovarian cancer. Int J Clin Exp Pathol. 2015;8:2710–8.PubMedPubMedCentral Yan C, Yang F, Zhou C, Chen X, Han X, Liu X, et al. MCT1 promotes the cisplatin-resistance by antagonizing Fas in epithelial ovarian cancer. Int J Clin Exp Pathol. 2015;8:2710–8.PubMedPubMedCentral
105.
go back to reference Hao J, Graham P, Chang L, Ni J, Wasinger V, Beretov J, et al. Proteomic identification of the lactate dehydrogenase a in a radioresistant prostate cancer xenograft mouse model for improving radiotherapy. Oncotarget. 2016;7:74269–85.PubMedPubMedCentral Hao J, Graham P, Chang L, Ni J, Wasinger V, Beretov J, et al. Proteomic identification of the lactate dehydrogenase a in a radioresistant prostate cancer xenograft mouse model for improving radiotherapy. Oncotarget. 2016;7:74269–85.PubMedPubMedCentral
106.
go back to reference Koukourakis MI, Giatromanolaki A, Winter S, Leek R, Sivridis E, Harris AL. Lactate dehydrogenase 5 expression in squamous cell head and neck cancer relates to prognosis following radical or postoperative radiotherapy. Oncology. 2009;77:285–92.PubMedCrossRef Koukourakis MI, Giatromanolaki A, Winter S, Leek R, Sivridis E, Harris AL. Lactate dehydrogenase 5 expression in squamous cell head and neck cancer relates to prognosis following radical or postoperative radiotherapy. Oncology. 2009;77:285–92.PubMedCrossRef
107.
go back to reference Koukourakis MI, Giatromanolaki A, Panteliadou M, Pouliliou SE, Chondrou PS, Mavropoulou S, et al. Lactate dehydrogenase 5 isoenzyme overexpression defines resistance of prostate cancer to radiotherapy. Br J Cancer. 2014;110:2217–23.PubMedPubMedCentralCrossRef Koukourakis MI, Giatromanolaki A, Panteliadou M, Pouliliou SE, Chondrou PS, Mavropoulou S, et al. Lactate dehydrogenase 5 isoenzyme overexpression defines resistance of prostate cancer to radiotherapy. Br J Cancer. 2014;110:2217–23.PubMedPubMedCentralCrossRef
108.
go back to reference Koukourakis MI, Kakouratos C, Kalamida D, Bampali Z, Mavropoulou S, Sivridis E, et al. Hypoxia-inducible proteins HIF1alpha and lactate dehydrogenase LDH5, key markers of anaerobic metabolism, relate with stem cell markers and poor post-radiotherapy outcome in bladder cancer. Int J Radiat Biol. 2016;92:353–63.PubMedCrossRef Koukourakis MI, Kakouratos C, Kalamida D, Bampali Z, Mavropoulou S, Sivridis E, et al. Hypoxia-inducible proteins HIF1alpha and lactate dehydrogenase LDH5, key markers of anaerobic metabolism, relate with stem cell markers and poor post-radiotherapy outcome in bladder cancer. Int J Radiat Biol. 2016;92:353–63.PubMedCrossRef
109.
go back to reference Appukuttan A, Flacke JP, Flacke H, Posadowsky A, Reusch HP, Ladilov Y. Inhibition of soluble adenylyl cyclase increases the radiosensitivity of prostate cancer cells. Biochim Biophys Acta. 1842;2014:2656–63. Appukuttan A, Flacke JP, Flacke H, Posadowsky A, Reusch HP, Ladilov Y. Inhibition of soluble adenylyl cyclase increases the radiosensitivity of prostate cancer cells. Biochim Biophys Acta. 1842;2014:2656–63.
110.
go back to reference He R, Liu P, Xie X, Zhou Y, Liao Q, Xiong W, et al. circGFRA1 and GFRA1 act as ceRNAs in triple negative breast cancer by regulating miR-34a. J Exp Clin Cancer Res. 2017;36:145.PubMedPubMedCentralCrossRef He R, Liu P, Xie X, Zhou Y, Liao Q, Xiong W, et al. circGFRA1 and GFRA1 act as ceRNAs in triple negative breast cancer by regulating miR-34a. J Exp Clin Cancer Res. 2017;36:145.PubMedPubMedCentralCrossRef
111.
go back to reference Li X, Lu P, Li B, Yang R, Chu Y, Zhang Z, et al. Sensitization of hepatocellular carcinoma cells to irradiation by miR34a through targeting lactate dehydrogenaseA. Mol Med Rep. 2016;13:3661–7.PubMedCrossRef Li X, Lu P, Li B, Yang R, Chu Y, Zhang Z, et al. Sensitization of hepatocellular carcinoma cells to irradiation by miR34a through targeting lactate dehydrogenaseA. Mol Med Rep. 2016;13:3661–7.PubMedCrossRef
112.
go back to reference Harada H. Hypoxia-inducible factor 1-mediated characteristic features of cancer cells for tumor radioresistance. J Radiat Res. 2016;57(Suppl 1):i99–i105.PubMedPubMedCentralCrossRef Harada H. Hypoxia-inducible factor 1-mediated characteristic features of cancer cells for tumor radioresistance. J Radiat Res. 2016;57(Suppl 1):i99–i105.PubMedPubMedCentralCrossRef
113.
go back to reference Parks SK, Chiche J, Pouyssegur J. Disrupting proton dynamics and energy metabolism for cancer therapy. Nat Rev Cancer. 2013;13:611–23.PubMedCrossRef Parks SK, Chiche J, Pouyssegur J. Disrupting proton dynamics and energy metabolism for cancer therapy. Nat Rev Cancer. 2013;13:611–23.PubMedCrossRef
114.
go back to reference Peitzsch C, Perrin R, Hill RP, Dubrovska A, Kurth I. Hypoxia as a biomarker for radioresistant cancer stem cells. Int J Radiat Biol. 2014;90:636–52.PubMedCrossRef Peitzsch C, Perrin R, Hill RP, Dubrovska A, Kurth I. Hypoxia as a biomarker for radioresistant cancer stem cells. Int J Radiat Biol. 2014;90:636–52.PubMedCrossRef
115.
go back to reference Feng H, Wang J, Chen W, Shan B, Guo Y, Xu J, et al. Hypoxia-induced autophagy as an additional mechanism in human osteosarcoma radioresistance. J bone Oncol. 2016;5:67–73.PubMedPubMedCentralCrossRef Feng H, Wang J, Chen W, Shan B, Guo Y, Xu J, et al. Hypoxia-induced autophagy as an additional mechanism in human osteosarcoma radioresistance. J bone Oncol. 2016;5:67–73.PubMedPubMedCentralCrossRef
116.
go back to reference Lee SL, Ryu H, Son AR, Seo B, Kim J, Jung SY, et al. TGF-beta and Hypoxia/Reoxygenation promote Radioresistance of A549 lung Cancer cells through activation of Nrf2 and EGFR. Oxidative Med Cell Longev. 2016;2016:6823471. Lee SL, Ryu H, Son AR, Seo B, Kim J, Jung SY, et al. TGF-beta and Hypoxia/Reoxygenation promote Radioresistance of A549 lung Cancer cells through activation of Nrf2 and EGFR. Oxidative Med Cell Longev. 2016;2016:6823471.
117.
go back to reference Nakashima R, Goto Y, Koyasu S, Kobayashi M, Morinibu A, Yoshimura M, et al. UCHL1-HIF-1 axis-mediated antioxidant property of cancer cells as a therapeutic target for radiosensitization. Sci Rep. 2017;7:6879.PubMedPubMedCentralCrossRef Nakashima R, Goto Y, Koyasu S, Kobayashi M, Morinibu A, Yoshimura M, et al. UCHL1-HIF-1 axis-mediated antioxidant property of cancer cells as a therapeutic target for radiosensitization. Sci Rep. 2017;7:6879.PubMedPubMedCentralCrossRef
118.
go back to reference Mandl M, Depping R. Hypoxia-inducible aryl hydrocarbon receptor nuclear translocator (ARNT) (HIF-1beta): is it a rare exception? Mol Med. 2014;20:215–20.PubMedPubMedCentralCrossRef Mandl M, Depping R. Hypoxia-inducible aryl hydrocarbon receptor nuclear translocator (ARNT) (HIF-1beta): is it a rare exception? Mol Med. 2014;20:215–20.PubMedPubMedCentralCrossRef
119.
go back to reference Mandl M, Lieberum M, Dunst J, Depping R. The expression level of the transcription factor aryl hydrocarbon receptor nuclear translocator (ARNT) determines cellular survival after radiation treatment. Radiat Oncol. 2015;10:229.PubMedPubMedCentralCrossRef Mandl M, Lieberum M, Dunst J, Depping R. The expression level of the transcription factor aryl hydrocarbon receptor nuclear translocator (ARNT) determines cellular survival after radiation treatment. Radiat Oncol. 2015;10:229.PubMedPubMedCentralCrossRef
120.
121.
go back to reference Slominski A, Kim TK, Brozyna AA, Janjetovic Z, Brooks DL, Schwab LP, et al. The role of melanogenesis in regulation of melanoma behavior: melanogenesis leads to stimulation of HIF-1alpha expression and HIF-dependent attendant pathways. Arch Biochem Biophys. 2014;563:79–93.PubMedPubMedCentralCrossRef Slominski A, Kim TK, Brozyna AA, Janjetovic Z, Brooks DL, Schwab LP, et al. The role of melanogenesis in regulation of melanoma behavior: melanogenesis leads to stimulation of HIF-1alpha expression and HIF-dependent attendant pathways. Arch Biochem Biophys. 2014;563:79–93.PubMedPubMedCentralCrossRef
122.
go back to reference Harada H, Kizaka-Kondoh S, Li G, Itasaka S, Shibuya K, Inoue M, et al. Significance of HIF-1-active cells in angiogenesis and radioresistance. Oncogene. 2007;26:7508–16.PubMedCrossRef Harada H, Kizaka-Kondoh S, Li G, Itasaka S, Shibuya K, Inoue M, et al. Significance of HIF-1-active cells in angiogenesis and radioresistance. Oncogene. 2007;26:7508–16.PubMedCrossRef
123.
go back to reference Fu Z, Chen D, Cheng H, Wang F. Hypoxia-inducible factor-1alpha protects cervical carcinoma cells from apoptosis induced by radiation via modulation of vascular endothelial growth factor and p53 under hypoxia. Med Sci Monit. 2015;21:318–25.PubMedPubMedCentralCrossRef Fu Z, Chen D, Cheng H, Wang F. Hypoxia-inducible factor-1alpha protects cervical carcinoma cells from apoptosis induced by radiation via modulation of vascular endothelial growth factor and p53 under hypoxia. Med Sci Monit. 2015;21:318–25.PubMedPubMedCentralCrossRef
124.
go back to reference Moeller BJ, Dreher MR, Rabbani ZN, Schroeder T, Cao Y, Li CY, et al. Pleiotropic effects of HIF-1 blockade on tumor radiosensitivity. Cancer Cell. 2005;8:99–110.PubMedCrossRef Moeller BJ, Dreher MR, Rabbani ZN, Schroeder T, Cao Y, Li CY, et al. Pleiotropic effects of HIF-1 blockade on tumor radiosensitivity. Cancer Cell. 2005;8:99–110.PubMedCrossRef
125.
go back to reference Li XP, Yang XY, Biskup E, Zhou J, Li HL, Wu YF, et al. Co-expression of CXCL8 and HIF-1alpha is associated with metastasis and poor prognosis in hepatocellular carcinoma. Oncotarget. 2015;6:22880–9.PubMedPubMedCentral Li XP, Yang XY, Biskup E, Zhou J, Li HL, Wu YF, et al. Co-expression of CXCL8 and HIF-1alpha is associated with metastasis and poor prognosis in hepatocellular carcinoma. Oncotarget. 2015;6:22880–9.PubMedPubMedCentral
126.
go back to reference Marampon F, Gravina GL, Zani BM, Popov VM, Fratticci A, Cerasani M, et al. Hypoxia sustains glioblastoma radioresistance through ERKs/DNA-PKcs/HIF-1alpha functional interplay. Int J Oncol. 2014;44:2121–31.PubMedCrossRef Marampon F, Gravina GL, Zani BM, Popov VM, Fratticci A, Cerasani M, et al. Hypoxia sustains glioblastoma radioresistance through ERKs/DNA-PKcs/HIF-1alpha functional interplay. Int J Oncol. 2014;44:2121–31.PubMedCrossRef
127.
go back to reference Zhong R, Xu H, Chen G, Zhao G, Gao Y, Liu X, et al. The role of hypoxia-inducible factor-1alpha in radiation-induced autophagic cell death in breast cancer cells. Tumour Biol. 2015;36:7077–83.PubMedCrossRef Zhong R, Xu H, Chen G, Zhao G, Gao Y, Liu X, et al. The role of hypoxia-inducible factor-1alpha in radiation-induced autophagic cell death in breast cancer cells. Tumour Biol. 2015;36:7077–83.PubMedCrossRef
128.
go back to reference Sun Y, Xing X, Liu Q, Wang Z, Xin Y, Zhang P, et al. Hypoxia-induced autophagy reduces radiosensitivity by the HIF-1alpha/miR-210/Bcl-2 pathway in colon cancer cells. Int J Oncol. 2015;46:750–6.PubMedCrossRef Sun Y, Xing X, Liu Q, Wang Z, Xin Y, Zhang P, et al. Hypoxia-induced autophagy reduces radiosensitivity by the HIF-1alpha/miR-210/Bcl-2 pathway in colon cancer cells. Int J Oncol. 2015;46:750–6.PubMedCrossRef
129.
go back to reference Zou YM, Hu GY, Zhao XQ, Lu T, Zhu F, Yu SY, et al. Hypoxia-induced autophagy contributes to radioresistance via c-Jun-mediated Beclin1 expression in lung cancer cells. J Huazhong Univ Sci Technolog Med Sci. 2014;34:761–7.PubMedCrossRef Zou YM, Hu GY, Zhao XQ, Lu T, Zhu F, Yu SY, et al. Hypoxia-induced autophagy contributes to radioresistance via c-Jun-mediated Beclin1 expression in lung cancer cells. J Huazhong Univ Sci Technolog Med Sci. 2014;34:761–7.PubMedCrossRef
130.
go back to reference Liang D, Ma Y, Liu J, Trope CG, Holm R, Nesland JM, et al. The hypoxic microenvironment upgrades stem-like properties of ovarian cancer cells. BMC Cancer. 2012;12:201.PubMedPubMedCentralCrossRef Liang D, Ma Y, Liu J, Trope CG, Holm R, Nesland JM, et al. The hypoxic microenvironment upgrades stem-like properties of ovarian cancer cells. BMC Cancer. 2012;12:201.PubMedPubMedCentralCrossRef
132.
133.
go back to reference Tsubouchi K, Minami K, Hayashi N, Yokoyama Y, Mori S, Yamamoto H, et al. The CD44 standard isoform contributes to radioresistance of pancreatic cancer cells. J Radiat Res. 2017;58:816–26.PubMedPubMedCentralCrossRef Tsubouchi K, Minami K, Hayashi N, Yokoyama Y, Mori S, Yamamoto H, et al. The CD44 standard isoform contributes to radioresistance of pancreatic cancer cells. J Radiat Res. 2017;58:816–26.PubMedPubMedCentralCrossRef
134.
go back to reference Yae T, Tsuchihashi K, Ishimoto T, Motohara T, Yoshikawa M, Yoshida GJ, et al. Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell. Nat Commun. 2012;3:883.PubMedCrossRef Yae T, Tsuchihashi K, Ishimoto T, Motohara T, Yoshikawa M, Yoshida GJ, et al. Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell. Nat Commun. 2012;3:883.PubMedCrossRef
135.
go back to reference Yoshida GJ, Fuchimoto Y, Osumi T, Shimada H, Hosaka S, Morioka H, et al. Li-Fraumeni syndrome with simultaneous osteosarcoma and liver cancer: increased expression of a CD44 variant isoform after chemotherapy. BMC Cancer. 2012;12:444.PubMedPubMedCentralCrossRef Yoshida GJ, Fuchimoto Y, Osumi T, Shimada H, Hosaka S, Morioka H, et al. Li-Fraumeni syndrome with simultaneous osteosarcoma and liver cancer: increased expression of a CD44 variant isoform after chemotherapy. BMC Cancer. 2012;12:444.PubMedPubMedCentralCrossRef
137.
go back to reference Yoshida GJ, Saya H. Inversed relationship between CD44 variant and c-Myc due to oxidative stress-induced canonical Wnt activation. Biochem Biophys Res Commun. 2014;443:622–7.PubMedCrossRef Yoshida GJ, Saya H. Inversed relationship between CD44 variant and c-Myc due to oxidative stress-induced canonical Wnt activation. Biochem Biophys Res Commun. 2014;443:622–7.PubMedCrossRef
138.
go back to reference Welcker M, Clurman BE. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer. 2008;8:83–93.PubMedCrossRef Welcker M, Clurman BE. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer. 2008;8:83–93.PubMedCrossRef
139.
go back to reference de Jong MC, Pramana J, van der Wal JE, Lacko M, Peutz-Kootstra CJ, de Jong JM, et al. CD44 expression predicts local recurrence after radiotherapy in larynx cancer. Clin Cancer Res. 2010;16:5329–38.PubMedCrossRef de Jong MC, Pramana J, van der Wal JE, Lacko M, Peutz-Kootstra CJ, de Jong JM, et al. CD44 expression predicts local recurrence after radiotherapy in larynx cancer. Clin Cancer Res. 2010;16:5329–38.PubMedCrossRef
140.
go back to reference Wang L, Li P, Hu W, Xia Y, Hu C, Liu L, et al. CD44(+)CD24(+) subset of PANC-1 cells exhibits radiation resistance via decreased levels of reactive oxygen species. Oncol Lett. 2017;14:1341–6.PubMedPubMedCentralCrossRef Wang L, Li P, Hu W, Xia Y, Hu C, Liu L, et al. CD44(+)CD24(+) subset of PANC-1 cells exhibits radiation resistance via decreased levels of reactive oxygen species. Oncol Lett. 2017;14:1341–6.PubMedPubMedCentralCrossRef
141.
go back to reference Pietras A, Katz AM, Ekstrom EJ, Wee B, Halliday JJ, Pitter KL, et al. Osteopontin-CD44 signaling in the glioma perivascular niche enhances cancer stem cell phenotypes and promotes aggressive tumor growth. Cell Stem Cell. 2014;14:357–69.PubMedPubMedCentralCrossRef Pietras A, Katz AM, Ekstrom EJ, Wee B, Halliday JJ, Pitter KL, et al. Osteopontin-CD44 signaling in the glioma perivascular niche enhances cancer stem cell phenotypes and promotes aggressive tumor growth. Cell Stem Cell. 2014;14:357–69.PubMedPubMedCentralCrossRef
142.
go back to reference Meijer TW, Kaanders JH, Span PN, Bussink J. Targeting hypoxia, HIF-1, and tumor glucose metabolism to improve radiotherapy efficacy. Clin Cancer Res. 2012;18:5585–94.PubMedCrossRef Meijer TW, Kaanders JH, Span PN, Bussink J. Targeting hypoxia, HIF-1, and tumor glucose metabolism to improve radiotherapy efficacy. Clin Cancer Res. 2012;18:5585–94.PubMedCrossRef
143.
go back to reference Kessler J, Hahnel A, Wichmann H, Rot S, Kappler M, Bache M, et al. HIF-1alpha inhibition by siRNA or chetomin in human malignant glioma cells: effects on hypoxic radioresistance and monitoring via CA9 expression. BMC Cancer. 2010;10:605.PubMedPubMedCentralCrossRef Kessler J, Hahnel A, Wichmann H, Rot S, Kappler M, Bache M, et al. HIF-1alpha inhibition by siRNA or chetomin in human malignant glioma cells: effects on hypoxic radioresistance and monitoring via CA9 expression. BMC Cancer. 2010;10:605.PubMedPubMedCentralCrossRef
144.
go back to reference Doi N, Ogawa R, Cui ZG, Morii A, Watanabe A, Kanayama S, et al. The acquired radioresistance in HeLa cells under conditions mimicking hypoxia was attenuated by a decreased expression of HIF subunit genes induced by RNA interference. Exp Cell Res. 2015;333:249–60.PubMedCrossRef Doi N, Ogawa R, Cui ZG, Morii A, Watanabe A, Kanayama S, et al. The acquired radioresistance in HeLa cells under conditions mimicking hypoxia was attenuated by a decreased expression of HIF subunit genes induced by RNA interference. Exp Cell Res. 2015;333:249–60.PubMedCrossRef
145.
go back to reference Oommen D, Prise KM. KNK437, abrogates hypoxia-induced radioresistance by dual targeting of the AKT and HIF-1alpha survival pathways. Biochem Biophys Res Commun. 2012;421:538–43.PubMedCrossRef Oommen D, Prise KM. KNK437, abrogates hypoxia-induced radioresistance by dual targeting of the AKT and HIF-1alpha survival pathways. Biochem Biophys Res Commun. 2012;421:538–43.PubMedCrossRef
146.
go back to reference Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM, Johnson MS, et al. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell. 2003;3:363–75.PubMedCrossRef Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM, Johnson MS, et al. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell. 2003;3:363–75.PubMedCrossRef
147.
go back to reference Zhao H, Jiang H, Li Z, Zhuang Y, Liu Y, Zhou S, et al. 2-Methoxyestradiol enhances radiosensitivity in radioresistant melanoma MDA-MB-435R cells by regulating glycolysis via HIF-1alpha/PDK1 axis. Int J Oncol. 2017;50:1531–40.PubMedPubMedCentralCrossRef Zhao H, Jiang H, Li Z, Zhuang Y, Liu Y, Zhou S, et al. 2-Methoxyestradiol enhances radiosensitivity in radioresistant melanoma MDA-MB-435R cells by regulating glycolysis via HIF-1alpha/PDK1 axis. Int J Oncol. 2017;50:1531–40.PubMedPubMedCentralCrossRef
148.
go back to reference Wu SL, Li YJ, Liao K, Shi L, Zhang N, Liu S, et al. 2-Methoxyestradiol inhibits the proliferation and migration and reduces the radioresistance of nasopharyngeal carcinoma CNE-2 stem cells via NF-kappaB/HIF-1 signaling pathway inactivation and EMT reversal. Oncol Rep. 2017;37:793–802.PubMedCrossRef Wu SL, Li YJ, Liao K, Shi L, Zhang N, Liu S, et al. 2-Methoxyestradiol inhibits the proliferation and migration and reduces the radioresistance of nasopharyngeal carcinoma CNE-2 stem cells via NF-kappaB/HIF-1 signaling pathway inactivation and EMT reversal. Oncol Rep. 2017;37:793–802.PubMedCrossRef
149.
go back to reference Wang J, Kang M, Wen Q, Qin YT, Wei ZX, Xiao JJ, et al. Berberine sensitizes nasopharyngeal carcinoma cells to radiation through inhibition of Sp1 and EMT. Oncol Rep. 2017;37:2425–32.PubMedCrossRef Wang J, Kang M, Wen Q, Qin YT, Wei ZX, Xiao JJ, et al. Berberine sensitizes nasopharyngeal carcinoma cells to radiation through inhibition of Sp1 and EMT. Oncol Rep. 2017;37:2425–32.PubMedCrossRef
150.
go back to reference Zhang C, Yang X, Zhang Q, Yang B, Xu L, Qin Q, et al. Berberine radiosensitizes human nasopharyngeal carcinoma by suppressing hypoxia-inducible factor-1alpha expression. Acta Otolaryngol. 2014;134:185–92.PubMedCrossRef Zhang C, Yang X, Zhang Q, Yang B, Xu L, Qin Q, et al. Berberine radiosensitizes human nasopharyngeal carcinoma by suppressing hypoxia-inducible factor-1alpha expression. Acta Otolaryngol. 2014;134:185–92.PubMedCrossRef
151.
go back to reference Miyasaka A, Oda K, Ikeda Y, Sone K, Fukuda T, Inaba K, et al. PI3K/mTOR pathway inhibition overcomes radioresistance via suppression of the HIF1-alpha/VEGF pathway in endometrial cancer. Gynecol Oncol. 2015;138:174–80.PubMedCrossRef Miyasaka A, Oda K, Ikeda Y, Sone K, Fukuda T, Inaba K, et al. PI3K/mTOR pathway inhibition overcomes radioresistance via suppression of the HIF1-alpha/VEGF pathway in endometrial cancer. Gynecol Oncol. 2015;138:174–80.PubMedCrossRef
152.
go back to reference Zhang C, Yang X, Zhang Q, Guo Q, He J, Qin Q, et al. STAT3 inhibitor NSC74859 radiosensitizes esophageal cancer via the downregulation of HIF-1alpha. Tumour Biol. 2014;35:9793–9.PubMedCrossRef Zhang C, Yang X, Zhang Q, Guo Q, He J, Qin Q, et al. STAT3 inhibitor NSC74859 radiosensitizes esophageal cancer via the downregulation of HIF-1alpha. Tumour Biol. 2014;35:9793–9.PubMedCrossRef
153.
go back to reference Zhang Q, Zhang C, He J, Guo Q, Hu D, Yang X, et al. STAT3 inhibitor stattic enhances radiosensitivity in esophageal squamous cell carcinoma. Tumour Biol. 2015;36:2135–42.PubMedCrossRef Zhang Q, Zhang C, He J, Guo Q, Hu D, Yang X, et al. STAT3 inhibitor stattic enhances radiosensitivity in esophageal squamous cell carcinoma. Tumour Biol. 2015;36:2135–42.PubMedCrossRef
154.
go back to reference Alsamarai S, Charpidou AG, Matthay RA, Confeld D, Syrigos KN, Saif MW. Pneumonitis related to docetaxel: case report and review of the literature. In Vivo. 2009;23:635–7.PubMed Alsamarai S, Charpidou AG, Matthay RA, Confeld D, Syrigos KN, Saif MW. Pneumonitis related to docetaxel: case report and review of the literature. In Vivo. 2009;23:635–7.PubMed
155.
go back to reference Oh ET, Kim CW, Kim SJ, Lee JS, Hong SS, Park HJ. Docetaxel induced-JNK2/PHD1 signaling pathway increases degradation of HIF-1alpha and causes cancer cell death under hypoxia. Sci Rep. 2016;6:27382.PubMedPubMedCentralCrossRef Oh ET, Kim CW, Kim SJ, Lee JS, Hong SS, Park HJ. Docetaxel induced-JNK2/PHD1 signaling pathway increases degradation of HIF-1alpha and causes cancer cell death under hypoxia. Sci Rep. 2016;6:27382.PubMedPubMedCentralCrossRef
156.
go back to reference Lai KG, Lin YH, Ho CT, Chen CY, Peng CY, Liu TZ, et al. Paclitaxel pretreatment overcomes hypoxia inducible factor-1alpha-induced radioresistance acquisition of human hepatoma and lung adenocarcinoma cells. Life Sci. 2015;136:7–12.PubMedCrossRef Lai KG, Lin YH, Ho CT, Chen CY, Peng CY, Liu TZ, et al. Paclitaxel pretreatment overcomes hypoxia inducible factor-1alpha-induced radioresistance acquisition of human hepatoma and lung adenocarcinoma cells. Life Sci. 2015;136:7–12.PubMedCrossRef
157.
go back to reference Yang W, Sun T, Cao J, Liu F, Tian Y, Zhu W. Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro. Exp Cell Res. 2012;318:944–54.PubMedCrossRef Yang W, Sun T, Cao J, Liu F, Tian Y, Zhu W. Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro. Exp Cell Res. 2012;318:944–54.PubMedCrossRef
158.
go back to reference Grosso S, Doyen J, Parks SK, Bertero T, Paye A, Cardinaud B, et al. MiR-210 promotes a hypoxic phenotype and increases radioresistance in human lung cancer cell lines. Cell Death Dis. 2013;4:e544.PubMedPubMedCentralCrossRef Grosso S, Doyen J, Parks SK, Bertero T, Paye A, Cardinaud B, et al. MiR-210 promotes a hypoxic phenotype and increases radioresistance in human lung cancer cell lines. Cell Death Dis. 2013;4:e544.PubMedPubMedCentralCrossRef
159.
go back to reference Yang W, Wei J, Guo T, Shen Y, Liu F. Knockdown of miR-210 decreases hypoxic glioma stem cells stemness and radioresistance. Exp Cell Res. 2014;326:22–35.PubMedCrossRef Yang W, Wei J, Guo T, Shen Y, Liu F. Knockdown of miR-210 decreases hypoxic glioma stem cells stemness and radioresistance. Exp Cell Res. 2014;326:22–35.PubMedCrossRef
160.
go back to reference Song L, Liu S, Zhang L, Yao H, Gao F, Xu D, et al. MiR-21 modulates radiosensitivity of cervical cancer through inhibiting autophagy via the PTEN/Akt/HIF-1alpha feedback loop and the Akt-mTOR signaling pathway. Tumour Biol. 2016;37:12161–8.PubMedCrossRef Song L, Liu S, Zhang L, Yao H, Gao F, Xu D, et al. MiR-21 modulates radiosensitivity of cervical cancer through inhibiting autophagy via the PTEN/Akt/HIF-1alpha feedback loop and the Akt-mTOR signaling pathway. Tumour Biol. 2016;37:12161–8.PubMedCrossRef
161.
go back to reference Gu H, Liu M, Ding C, Wang X, Wang R, Wu X, et al. Hypoxia-responsive miR-124 and miR-144 reduce hypoxia-induced autophagy and enhance radiosensitivity of prostate cancer cells via suppressing PIM1. Cancer med. 2016;5:1174–82.PubMedPubMedCentralCrossRef Gu H, Liu M, Ding C, Wang X, Wang R, Wu X, et al. Hypoxia-responsive miR-124 and miR-144 reduce hypoxia-induced autophagy and enhance radiosensitivity of prostate cancer cells via suppressing PIM1. Cancer med. 2016;5:1174–82.PubMedPubMedCentralCrossRef
162.
go back to reference Zhang X, Shi H, Lin S, Ba M, Cui S. MicroRNA-216a enhances the radiosensitivity of pancreatic cancer cells by inhibiting beclin-1-mediated autophagy. Oncol Rep. 2015;34:1557–64.PubMedCrossRef Zhang X, Shi H, Lin S, Ba M, Cui S. MicroRNA-216a enhances the radiosensitivity of pancreatic cancer cells by inhibiting beclin-1-mediated autophagy. Oncol Rep. 2015;34:1557–64.PubMedCrossRef
163.
go back to reference Qu JQ, Yi HM, Ye X, Li LN, Zhu JF, Xiao T, et al. MiR-23a sensitizes nasopharyngeal carcinoma to irradiation by targeting IL-8/Stat3 pathway. Oncotarget. 2015;6:28341–56.PubMedCrossRef Qu JQ, Yi HM, Ye X, Li LN, Zhu JF, Xiao T, et al. MiR-23a sensitizes nasopharyngeal carcinoma to irradiation by targeting IL-8/Stat3 pathway. Oncotarget. 2015;6:28341–56.PubMedCrossRef
164.
go back to reference Shen H, Hau E, Joshi S, Dilda PJ, McDonald KL. Sensitization of glioblastoma cells to irradiation by modulating the glucose metabolism. Mol Cancer Ther. 2015;14:1794–804.PubMedCrossRef Shen H, Hau E, Joshi S, Dilda PJ, McDonald KL. Sensitization of glioblastoma cells to irradiation by modulating the glucose metabolism. Mol Cancer Ther. 2015;14:1794–804.PubMedCrossRef
165.
go back to reference Meng MB, Wang HH, Guo WH, Wu ZQ, Zeng XL, Zaorsky NG, et al. Targeting pyruvate kinase M2 contributes to radiosensitivity of non-small cell lung cancer cells in vitro and in vivo. Cancer Lett. 2015;356:985–93.PubMedCrossRef Meng MB, Wang HH, Guo WH, Wu ZQ, Zeng XL, Zaorsky NG, et al. Targeting pyruvate kinase M2 contributes to radiosensitivity of non-small cell lung cancer cells in vitro and in vivo. Cancer Lett. 2015;356:985–93.PubMedCrossRef
166.
go back to reference Yuan S, Qiao T, Zhuang X, Chen W, Xing N, Zhang Q. Knockdown of the M2 isoform of pyruvate kinase (PKM2) with shRNA enhances the effect of docetaxel in human NSCLC cell lines in vitro. Yonsei Med J. 2016;57:1312–23.PubMedPubMedCentralCrossRef Yuan S, Qiao T, Zhuang X, Chen W, Xing N, Zhang Q. Knockdown of the M2 isoform of pyruvate kinase (PKM2) with shRNA enhances the effect of docetaxel in human NSCLC cell lines in vitro. Yonsei Med J. 2016;57:1312–23.PubMedPubMedCentralCrossRef
167.
go back to reference Liu G, Li YI, Gao X. Overexpression of microRNA-133b sensitizes non-small cell lung cancer cells to irradiation through the inhibition of glycolysis. Oncol Lett. 2016;11:2903–8.PubMedPubMedCentralCrossRef Liu G, Li YI, Gao X. Overexpression of microRNA-133b sensitizes non-small cell lung cancer cells to irradiation through the inhibition of glycolysis. Oncol Lett. 2016;11:2903–8.PubMedPubMedCentralCrossRef
168.
go back to reference Saleem W, Suzuki Y, Mobaraki A, Yoshida Y, Noda S, Saitoh JI, et al. Reduction of nitric oxide level enhances the radiosensitivity of hypoxic non-small cell lung cancer. Cancer Sci. 2011;102:2150–6.PubMedCrossRef Saleem W, Suzuki Y, Mobaraki A, Yoshida Y, Noda S, Saitoh JI, et al. Reduction of nitric oxide level enhances the radiosensitivity of hypoxic non-small cell lung cancer. Cancer Sci. 2011;102:2150–6.PubMedCrossRef
169.
go back to reference Dong G, Chen Q, Jiang F, Yu D, Mao Q, Xia W, et al. Diisopropylamine dichloroacetate enhances radiosensitization in esophageal squamous cell carcinoma by increasing mitochondria-derived reactive oxygen species levels. Oncotarget. 2016;7:68170–8.PubMedPubMedCentral Dong G, Chen Q, Jiang F, Yu D, Mao Q, Xia W, et al. Diisopropylamine dichloroacetate enhances radiosensitization in esophageal squamous cell carcinoma by increasing mitochondria-derived reactive oxygen species levels. Oncotarget. 2016;7:68170–8.PubMedPubMedCentral
170.
go back to reference Zhong JT, Zhou SH. Warburg effect, hexokinase-II, and radioresistance of laryngeal carcinoma. Oncotarget. 2017;8:14133–46.PubMed Zhong JT, Zhou SH. Warburg effect, hexokinase-II, and radioresistance of laryngeal carcinoma. Oncotarget. 2017;8:14133–46.PubMed
171.
go back to reference Bala M, Goel HC. Modification of low dose radiation induced Radioresistance by 2-deoxy-D-glucose in Saccharomyces cerevisiae: mechanistic aspects. J Radiat Res. 2007;48:335–46.PubMedCrossRef Bala M, Goel HC. Modification of low dose radiation induced Radioresistance by 2-deoxy-D-glucose in Saccharomyces cerevisiae: mechanistic aspects. J Radiat Res. 2007;48:335–46.PubMedCrossRef
172.
go back to reference Dwarkanath BS, Zolzer F, Chandana S, Bauch T, Adhikari JS, Muller WU, et al. Heterogeneity in 2-deoxy-D-glucose-induced modifications in energetics and radiation responses of human tumor cell lines. Int J Radiat Oncol Biol Phys. 2001;50:1051–61.PubMedCrossRef Dwarkanath BS, Zolzer F, Chandana S, Bauch T, Adhikari JS, Muller WU, et al. Heterogeneity in 2-deoxy-D-glucose-induced modifications in energetics and radiation responses of human tumor cell lines. Int J Radiat Oncol Biol Phys. 2001;50:1051–61.PubMedCrossRef
173.
go back to reference Egler V, Korur S, Failly M, Boulay JL, Imber R, Lino MM, et al. Histone deacetylase inhibition and blockade of the glycolytic pathway synergistically induce glioblastoma cell death. Clin Cancer Res. 2008;14:3132–40.PubMedCrossRef Egler V, Korur S, Failly M, Boulay JL, Imber R, Lino MM, et al. Histone deacetylase inhibition and blockade of the glycolytic pathway synergistically induce glioblastoma cell death. Clin Cancer Res. 2008;14:3132–40.PubMedCrossRef
174.
go back to reference Cerella C, Dicato M, Diederich M. Modulatory roles of glycolytic enzymes in cell death. Biochem Pharmacol. 2014;92:22–30.PubMedCrossRef Cerella C, Dicato M, Diederich M. Modulatory roles of glycolytic enzymes in cell death. Biochem Pharmacol. 2014;92:22–30.PubMedCrossRef
175.
go back to reference Lee J. Mitochondrial drug targets in neurodegenerative diseases. Bioorg Med Chem Lett. 2016;26:714–20.PubMedCrossRef Lee J. Mitochondrial drug targets in neurodegenerative diseases. Bioorg Med Chem Lett. 2016;26:714–20.PubMedCrossRef
176.
go back to reference Lynam-Lennon N, Maher SG, Maguire A, Phelan J, Muldoon C, Reynolds JV, et al. Altered mitochondrial function and energy metabolism is associated with a radioresistant phenotype in oesophageal adenocarcinoma. PLoS One. 2014;9:e100738.PubMedPubMedCentralCrossRef Lynam-Lennon N, Maher SG, Maguire A, Phelan J, Muldoon C, Reynolds JV, et al. Altered mitochondrial function and energy metabolism is associated with a radioresistant phenotype in oesophageal adenocarcinoma. PLoS One. 2014;9:e100738.PubMedPubMedCentralCrossRef
177.
go back to reference Fisher CJ, Goswami PC. Mitochondria-targeted antioxidant enzyme activity regulates radioresistance in human pancreatic cancer cells. Cancer Biol Ther. 2008;7:1271–9.PubMedCrossRef Fisher CJ, Goswami PC. Mitochondria-targeted antioxidant enzyme activity regulates radioresistance in human pancreatic cancer cells. Cancer Biol Ther. 2008;7:1271–9.PubMedCrossRef
178.
go back to reference Maus F, Sakry D, Biname F, Karram K, Rajalingam K, Watts C, et al. The NG2 proteoglycan protects oligodendrocyte precursor cells against oxidative stress via interaction with OMI/HtrA2. PLoS One. 2015;10:e0137311.PubMedPubMedCentralCrossRef Maus F, Sakry D, Biname F, Karram K, Rajalingam K, Watts C, et al. The NG2 proteoglycan protects oligodendrocyte precursor cells against oxidative stress via interaction with OMI/HtrA2. PLoS One. 2015;10:e0137311.PubMedPubMedCentralCrossRef
179.
go back to reference Tamari Y, Kashino G, Mori H. Acquisition of radioresistance by IL-6 treatment is caused by suppression of oxidative stress derived from mitochondria after gamma-irradiation. J Radiat Res. 2017;58:412–20.PubMedPubMedCentralCrossRef Tamari Y, Kashino G, Mori H. Acquisition of radioresistance by IL-6 treatment is caused by suppression of oxidative stress derived from mitochondria after gamma-irradiation. J Radiat Res. 2017;58:412–20.PubMedPubMedCentralCrossRef
180.
go back to reference Chiou J-F, Tai C-J, Wang Y-H, Liu T-Z, Jen Y-M, Shiau C-Y. Sorafenib induces preferential apoptotic killing of a drug- and radio-resistant hep G2 cells through a mitochondria-dependent oxidative stress mechanism. Cancer Biol Ther. 2014;8:1904–13.CrossRef Chiou J-F, Tai C-J, Wang Y-H, Liu T-Z, Jen Y-M, Shiau C-Y. Sorafenib induces preferential apoptotic killing of a drug- and radio-resistant hep G2 cells through a mitochondria-dependent oxidative stress mechanism. Cancer Biol Ther. 2014;8:1904–13.CrossRef
181.
go back to reference Alphonse G, Bionda C, Aloy MT, Ardail D, Rousson R, Rodriguez-Lafrasse C. Overcoming resistance to gamma-rays in squamous carcinoma cells by poly-drug elevation of ceramide levels. Oncogene. 2004;23:2703–15.PubMedCrossRef Alphonse G, Bionda C, Aloy MT, Ardail D, Rousson R, Rodriguez-Lafrasse C. Overcoming resistance to gamma-rays in squamous carcinoma cells by poly-drug elevation of ceramide levels. Oncogene. 2004;23:2703–15.PubMedCrossRef
182.
go back to reference Tu C, Zeng Z, Qi P, Li X, Yu Z, Guo C, et al. Genome-Wide Analysis of 18 Epstein-Barr Viruses Isolated from Primary Nasopharyngeal Carcinoma Biopsy Specimens. J Virol. 2017;91. Tu C, Zeng Z, Qi P, Li X, Yu Z, Guo C, et al. Genome-Wide Analysis of 18 Epstein-Barr Viruses Isolated from Primary Nasopharyngeal Carcinoma Biopsy Specimens. J Virol. 2017;91.
183.
go back to reference You WC, Chiou SH, Huang CY, Chiang SF, Yang CL, Sudhakar JN, et al. Mitochondrial protein ATPase family, AAA domain containing 3A correlates with radioresistance in glioblastoma. Neuro-Oncology. 2013;15:1342–52.PubMedPubMedCentralCrossRef You WC, Chiou SH, Huang CY, Chiang SF, Yang CL, Sudhakar JN, et al. Mitochondrial protein ATPase family, AAA domain containing 3A correlates with radioresistance in glioblastoma. Neuro-Oncology. 2013;15:1342–52.PubMedPubMedCentralCrossRef
184.
go back to reference Candas D, Lu CL, Fan M, Chuang FY, Sweeney C, Borowsky AD, et al. Mitochondrial MKP1 is a target for therapy-resistant HER2-positive breast cancer cells. Cancer Res. 2014;74:7498–509.PubMedPubMedCentralCrossRef Candas D, Lu CL, Fan M, Chuang FY, Sweeney C, Borowsky AD, et al. Mitochondrial MKP1 is a target for therapy-resistant HER2-positive breast cancer cells. Cancer Res. 2014;74:7498–509.PubMedPubMedCentralCrossRef
185.
go back to reference Li YL, Chang JT, Lee LY, Fan KH, Lu YC, Li YC, et al. GDF15 contributes to radioresistance and cancer stemness of head and neck cancer by regulating cellular reactive oxygen species via a SMAD-associated signaling pathway. Oncotarget. 2017;8:1508–28.PubMed Li YL, Chang JT, Lee LY, Fan KH, Lu YC, Li YC, et al. GDF15 contributes to radioresistance and cancer stemness of head and neck cancer by regulating cellular reactive oxygen species via a SMAD-associated signaling pathway. Oncotarget. 2017;8:1508–28.PubMed
186.
go back to reference Shonai T, Adachi M, Sakata K, Takekawa M, Endo T, Imai K, et al. MEK/ERK pathway protects ionizing radiation-induced loss of mitochondrial membrane potential and cell death in lymphocytic leukemia cells. Cell Death Differ. 2002;9:963–71.PubMedCrossRef Shonai T, Adachi M, Sakata K, Takekawa M, Endo T, Imai K, et al. MEK/ERK pathway protects ionizing radiation-induced loss of mitochondrial membrane potential and cell death in lymphocytic leukemia cells. Cell Death Differ. 2002;9:963–71.PubMedCrossRef
187.
go back to reference Dong Q, Sharma S, Liu H, Chen L, Gu B, Sun X, et al. HDAC inhibitors reverse acquired radio resistance of KYSE-150R esophageal carcinoma cells by modulating Bmi-1 expression. Toxicol lett. 2014;224:121–9. Dong Q, Sharma S, Liu H, Chen L, Gu B, Sun X, et al. HDAC inhibitors reverse acquired radio resistance of KYSE-150R esophageal carcinoma cells by modulating Bmi-1 expression. Toxicol lett. 2014;224:121–9.
188.
go back to reference Kuwahara Y, Roudkenar MH, Suzuki M, Urushihara Y, Fukumoto M, Saito Y, et al. The involvement of mitochondrial membrane potential in cross-resistance between radiation and docetaxel. Int J Radiat Oncol Biol Phys. 2016;96:556–65.PubMedCrossRef Kuwahara Y, Roudkenar MH, Suzuki M, Urushihara Y, Fukumoto M, Saito Y, et al. The involvement of mitochondrial membrane potential in cross-resistance between radiation and docetaxel. Int J Radiat Oncol Biol Phys. 2016;96:556–65.PubMedCrossRef
190.
go back to reference Huang L, Li B, Tang S, Guo H, Li W, Huang X, et al. Mitochondrial KATP channels control glioma Radioresistance by regulating ROS-induced ERK activation. Mol Neurobiol. 2015;52:626–37.PubMedCrossRef Huang L, Li B, Tang S, Guo H, Li W, Huang X, et al. Mitochondrial KATP channels control glioma Radioresistance by regulating ROS-induced ERK activation. Mol Neurobiol. 2015;52:626–37.PubMedCrossRef
Metadata
Title
Role of metabolism in cancer cell radioresistance and radiosensitization methods
Authors
Le Tang
Fang Wei
Yingfen Wu
Yi He
Lei Shi
Fang Xiong
Zhaojian Gong
Can Guo
Xiayu Li
Hao Deng
Ke Cao
Ming Zhou
Bo Xiang
Xiaoling Li
Yong Li
Guiyuan Li
Wei Xiong
Zhaoyang Zeng
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Experimental & Clinical Cancer Research / Issue 1/2018
Electronic ISSN: 1756-9966
DOI
https://doi.org/10.1186/s13046-018-0758-7

Other articles of this Issue 1/2018

Journal of Experimental & Clinical Cancer Research 1/2018 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine