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Review Article

The Role of Reactive Oxygen Species in Tumor Treatment and its Impact on Bone Marrow Hematopoiesis

Author(s): Yongfeng Chen*, Xingjing Luo, Zhenyou Zou and Yong Liang

Volume 21, Issue 5, 2020

Page: [477 - 498] Pages: 22

DOI: 10.2174/1389450120666191021110208

Price: $65

Abstract

Reactive oxygen species (ROS), an important molecule inducing oxidative stress in organisms, play a key role in tumorigenesis, tumor progression and recurrence. Recent findings on ROS have shown that ROS can be used to treat cancer as they accelerate the death of tumor cells. At present, pro-oxidant drugs that are intended to increase ROS levels of the tumor cells have been widely used in the clinic. However, ROS are a double-edged sword in the treatment of tumors. High levels of ROS induce not only the death of tumor cells but also oxidative damage to normal cells, especially bone marrow hemopoietic cells, which leads to bone marrow suppression and (or) other side effects, weak efficacy of tumor treatment and even threatening patients’ life. How to enhance the killing effect of ROS on tumor cells while avoiding oxidative damage to the normal cells has become an urgent issue. This study is a review of the latest progress in the role of ROS-mediated programmed death in tumor treatment and prevention and treatment of oxidative damage in bone marrow induced by ROS.

Keywords: ROS, programmed cell death, bone marrow protection, chemotherapy, tumor, hematopoiesis.

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[1]
Yarosz EL, Chang CH. The role of reactive oxygen species in regulating t cell-mediated immunity and disease. Immune Netw 2018; 18(1)e14
[http://dx.doi.org/10.4110/in.2018.18.e14] [PMID: 29503744]
[2]
Zou Z, Cai J, Zhong A, et al. Using the synthesized peptide HAYED (5) to protect the brain against iron catalyzed radical attack in a naturally senescence Kunming mouse model. Free Radic Biol Med 2019; 130: 458-70.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.11.014] [PMID: 30448512]
[3]
Little AC, Sulovari A, Danyal K, Heppner DE, Seward DJ, van der Vliet A. Paradoxical roles of dual oxidases in cancer biology. Free Radic Biol Med 2017; 110: 117-32.
[http://dx.doi.org/10.1016/j.freeradbiomed.2017.05.024] [PMID: 28578013]
[4]
Zou Z, Shen Q, Pang Y, et al. The synthesized transporter K16APoE enabled the therapeutic HAYED peptide to cross the blood-brain barrier and remove excess iron and radicals in the brain, thus easing Alzheimer’s disease. Drug Deliv Transl Res 2019; 9(1): 394-403.
[http://dx.doi.org/10.1007/s13346-018-0579-4] [PMID: 30136122]
[5]
Dharmaraja AT. Role of reactive oxygen species (ROS) in therapeutics and drug resistance in cancer and bacteria. J Med Chem 2017; 60(8): 3221-40.
[http://dx.doi.org/10.1021/acs.jmedchem.6b01243] [PMID: 28135088]
[6]
Chen Y, Zou Z, Wu Z, et al. TNF-α-induced programmed cell death in the pathogenesis of acquired aplastic anemia. Expert Rev Hematol 2015; 8(4): 515-26.
[http://dx.doi.org/10.1586/17474086.2015.1049593] [PMID: 26149913]
[7]
Kim J, Kim J, Bae JS. ROS homeostasis and metabolism: a critical liaison for cancer therapy. Exp Mol Med 2016; 48(11)e269
[http://dx.doi.org/10.1038/emm.2016.119] [PMID: 27811934]
[8]
Xiao H, Xiong L, Song X, et al. Angelica sinensis polysaccharides ameliorate stress-induced premature senescence of hematopoietic cell via protecting bone marrow stromal cells from oxidative injuries caused by 5-fluorouracil. Int J Mol Sci 2017; 18(11)E2265
[http://dx.doi.org/10.3390/ijms18112265] [PMID: 29143796]
[9]
Qu C, Lu Y, Liu W. Severe bone marrow suppression accompanying pulmonary infection and hemorrhage of the digestive tract associated with leflunomide and low-dose methotrexate combination therapy. J Pharmacol Pharmacother 2017; 8(1): 35-7.
[http://dx.doi.org/10.4103/jpp.JPP_93_16] [PMID: 28405135]
[10]
Cao H, Wang Y, Wang Q, et al. Taxol prevents myocardial ischemia-reperfusion injury by inducing JNK-mediated HO-1 expression. Pharm Biol 2016; 54(3): 555-60.
[PMID: 26270131]
[11]
Fruehauf JP, Meyskens FL Jr. Reactive oxygen species: a breath of life or death? Clin Cancer Res 2007; 13(3): 789-94.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-2082] [PMID: 17289868]
[12]
Bauer G, Motz M. The antitumor effect of single-domain antibodies directed towards membrane-associated catalase and superoxide dismutase. Anticancer Res 2016; 36(11): 5945-56.
[http://dx.doi.org/10.21873/anticanres.11182] [PMID: 27793920]
[13]
Chen YF, Liu H, Luo XJ, et al. The roles of reactive oxygen species (ROS) and autophagy in the survival and death of leukemia cells. Crit Rev Oncol Hematol 2017; 112: 21-30.
[http://dx.doi.org/10.1016/j.critrevonc.2017.02.004] [PMID: 28325262]
[14]
Diehn M, Cho RW, Lobo NA, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009; 458(7239): 780-3.
[http://dx.doi.org/10.1038/nature07733] [PMID: 19194462]
[15]
Kobayashi CI, Suda T. Regulation of reactive oxygen species in stem cells and cancer stem cells. J Cell Physiol 2012; 227(2): 421-30.
[http://dx.doi.org/10.1002/jcp.22764] [PMID: 21448925]
[16]
Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 2009; 8(7): 579-91.
[http://dx.doi.org/10.1038/nrd2803] [PMID: 19478820]
[17]
DeNicola GM, Karreth FA, Humpton TJ, et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011; 475(7354): 106-9.
[http://dx.doi.org/10.1038/nature10189] [PMID: 21734707]
[18]
Medici S, Peana M, Nurchi VM, Lachowicz JI, Maria GC, Zoroddu A. Noble metals in medicine: Latest advances. Coord Chem Rev 2015; 284: 329-50.
[http://dx.doi.org/10.1016/j.ccr.2014.08.002]
[19]
Circu ML, Aw TY. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 2010; 48(6): 749-62.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.12.022] [PMID: 20045723]
[20]
Suzuki Y, Ono Y, Hirabayashi Y. Rapid and specific reactive oxygen species generation via NADPH oxidase activation during Fas-mediated apoptosis. FEBS Lett 1998; 425(2): 209-12.
[http://dx.doi.org/10.1016/S0014-5793(98)00228-2] [PMID: 9559649]
[21]
Stewart JH IV, Tran TL, Levi N, Tsai WS, Schrump DS, Nguyen DM. The essential role of the mitochondria and reactive oxygen species in Cisplatin-mediated enhancement of fas ligand-induced apoptosis in malignant pleural mesothelioma. J Surg Res 2007; 141(1): 120-31.
[http://dx.doi.org/10.1016/j.jss.2007.03.048] [PMID: 17574045]
[22]
Lee MW, Park SC, Kim JH, et al. The involvement of oxidative stress in tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in HeLa cells. Cancer Lett 2002; 182(1): 75-82.
[http://dx.doi.org/10.1016/S0304-3835(02)00074-5] [PMID: 12175526]
[23]
González-Flores D, Rodríguez AB, Pariente JA. TNFα-induced apoptosis in human myeloid cell lines HL-60 and K562 is dependent of intracellular ROS generation. Mol Cell Biochem 2014; 390(1-2): 281-7.
[http://dx.doi.org/10.1007/s11010-014-1979-5] [PMID: 24488173]
[24]
Zhang W, Kudo H, Kawai K, et al. Tumor necrosis factor-alpha accelerates apoptosis of steatotic hepatocytes from a murine model of non-alcoholic fatty liver disease. Biochem Biophys Res Commun 2010; 391(4): 1731-6.
[http://dx.doi.org/10.1016/j.bbrc.2009.12.144] [PMID: 20043871]
[25]
Chao H, Liu Y, Fu X, et al. Lowered iPLA2γ activity causes increased mitochondrial lipid peroxidation and mitochondrial dysfunction in a rotenone-induced model of Parkinson’s disease. Exp Neurol 2018; 300: 74-86.
[http://dx.doi.org/10.1016/j.expneurol.2017.10.031] [PMID: 29104115]
[26]
Cao XH, Zhao SS, Liu DY, et al. ROS-Ca(2+) is associated with mitochondria permeability transition pore involved in surfactin-induced MCF-7 cells apoptosis. Chem Biol Interact 2011; 190(1): 16-27.
[http://dx.doi.org/10.1016/j.cbi.2011.01.010] [PMID: 21241685]
[27]
Chami M, Prandini A, Campanella M, et al. Bcl-2 and Bax exert opposing effects on Ca2+ signaling, which do not depend on their putative pore-forming region. J Biol Chem 2004; 279(52): 54581-9.
[http://dx.doi.org/10.1074/jbc.M409663200] [PMID: 15485871]
[28]
Budanov AV. The role of tumor suppressor p53 in the antioxidant defense and metabolism. Subcell Biochem 2014; 85: 337-58.
[http://dx.doi.org/10.1007/978-94-017-9211-0_18] [PMID: 25201203]
[29]
Kim JJ, Lee SB, Park JK, Yoo YD. TNF-alpha-induced ROS production triggering apoptosis is directly linked to Romo1 and Bcl-X(L). Cell Death Differ 2010; 17(9): 1420-34.
[http://dx.doi.org/10.1038/cdd.2010.19] [PMID: 20203691]
[30]
Zhang M, Lee SJ, An C, et al. Caveolin-1 mediates Fas-BID signaling in hyperoxia-induced apoptosis. Free Radic Biol Med 2011; 50(10): 1252-62.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.02.031] [PMID: 21382479]
[31]
Zong WX, Thompson CB. Necrotic death as a cell fate. Genes Dev 2006; 20(1): 1-15.
[http://dx.doi.org/10.1101/gad.1376506] [PMID: 16391229]
[32]
Fu Z, Deng B, Liao Y, et al. The anti-tumor effect of shikonin on osteosarcoma by inducing RIP1 and RIP3 dependent necroptosis. BMC Cancer 2013; 13: 580.
[http://dx.doi.org/10.1186/1471-2407-13-580] [PMID: 24314238]
[33]
Cho YS, Challa S, Moquin D, et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009; 137(6): 1112-23.
[http://dx.doi.org/10.1016/j.cell.2009.05.037] [PMID: 19524513]
[34]
Rathore R, McCallum JE, Varghese E, Florea AM, Büsselberg D. Overcoming chemotherapy drug resistance by targeting inhibitors of apoptosis proteins (IAPs). Apoptosis 2017; 22(7): 898-919.
[http://dx.doi.org/10.1007/s10495-017-1375-1] [PMID: 28424988]
[35]
Bonapace L, Bornhauser BC, Schmitz M, et al. Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J Clin Invest 2010; 120(4): 1310-23.
[http://dx.doi.org/10.1172/JCI39987] [PMID: 20200450]
[36]
Han W, Li L, Qiu S, et al. Shikonin circumvents cancer drug resistance by induction of a necroptotic death. Mol Cancer Ther 2007; 6(5): 1641-9.
[http://dx.doi.org/10.1158/1535-7163.MCT-06-0511] [PMID: 17513612]
[37]
Safferthal C, Rohde K, Fulda S. Therapeutic targeting of necroptosis by Smac mimetic bypasses apoptosis resistance in acute myeloid leukemia cells. Oncogene 2017; 36(11): 1487-502.
[http://dx.doi.org/10.1038/onc.2016.310] [PMID: 27869161]
[38]
Shahsavari Z, Karami-Tehrani F, Salami S, Ghasemzadeh M. RIP1K and RIP3K provoked by shikonin induce cell cycle arrest in the triple negative breast cancer cell line, MDA-MB-468: necroptosis as a desperate programmed suicide pathway. Tumour Biol 2016; 37(4): 4479-91.
[http://dx.doi.org/10.1007/s13277-015-4258-5] [PMID: 26496737]
[39]
Steinhart L, Belz K, Fulda S. Smac mimetic and demethylating agents synergistically trigger cell death in acute myeloid leukemia cells and overcome apoptosis resistance by inducing necroptosis. Cell Death Dis 2013; 4e802
[http://dx.doi.org/10.1038/cddis.2013.320] [PMID: 24030154]
[40]
Dikic I, Elazar Z. Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol 2018; 19(6): 349-64.
[http://dx.doi.org/10.1038/s41580-018-0003-4] [PMID: 29618831]
[41]
Hamurcu Z, Delibaşı N, Geçene S, et al. Targeting LC3 and Beclin-1 autophagy genes suppresses proliferation, survival, migration and invasion by inhibition of Cyclin-D1 and uPAR/Integrin β1/Src signaling in triple negative breast cancer cells. J Cancer Res Clin Oncol 2018; 144(3): 415-30.
[http://dx.doi.org/10.1007/s00432-017-2557-5] [PMID: 29288363]
[42]
Kimmelman AC, White E. Autophagy and tumor metabolism. Cell Metab 2017; 25(5): 1037-43.
[http://dx.doi.org/10.1016/j.cmet.2017.04.004] [PMID: 28467923]
[43]
Kumar A, Singh UK, Chaudhary A. Targeting autophagy to overcome drug resistance in cancer therapy. Future Med Chem 2015; 7(12): 1535-42.
[http://dx.doi.org/10.4155/fmc.15.88] [PMID: 26334206]
[44]
Nguyen HG, Yang JC, Kung HJ, et al. Targeting autophagy overcomes Enzalutamide resistance in castration-resistant prostate cancer cells and improves therapeutic response in a xenograft model. Oncogene 2014; 33(36): 4521-30.
[http://dx.doi.org/10.1038/onc.2014.25] [PMID: 24662833]
[45]
Yu Y, Chen YF, Wu ZM, Bai S. Experimental study of the RIP3 expression and cell death resistance in acute lymphoblastic leukemia Jurkat cells under TNF-α administration. Int J Clin Exp Med 2018; 11: 1845-54.
[46]
Zou Z, Ni M, Zhang J, et al. miR-30a can inhibit DNA replication by targeting RPA1 thus slowing cancer cell proliferation. Biochem J 2016; 473(14): 2131-9.
[http://dx.doi.org/10.1042/BCJ20160177] [PMID: 27208176]
[47]
Chaabane W, Appell ML. Interconnections between apoptotic and autophagic pathways during thiopurine-induced toxicity in cancer cells: the role of reactive oxygen species. Oncotarget 2016; 7(46): 75616-34.
[http://dx.doi.org/10.18632/oncotarget.12313] [PMID: 27689330]
[48]
Chen Q, Ye L, Fan J, et al. Autophagy suppression potentiates the anti-glioblastoma effect of asparaginase in vitro and in vivo. Oncotarget 2017; 8(53): 91052-66.
[http://dx.doi.org/10.18632/oncotarget.19409] [PMID: 29207624]
[49]
Donadelli M, Dando I, Zaniboni T, et al. Gemcitabine/cannabinoid combination triggers autophagy in pancreatic cancer cells through a ROS-mediated mechanism. Cell Death Dis 2011; 2e152
[http://dx.doi.org/10.1038/cddis.2011.36] [PMID: 21525939]
[50]
Liu S, Li X. Autophagy inhibition enhances sensitivity of endometrial carcinoma cells to paclitaxel. Int J Oncol 2015; 46(6): 2399-408.
[http://dx.doi.org/10.3892/ijo.2015.2937] [PMID: 25825088]
[51]
Liu Z, Liu J, Li L, et al. Inhibition of autophagy potentiated the antitumor effect of nedaplatin in cisplatin-resistant nasopharyngeal carcinoma cells. PLoS One 2015; 10(8)e0135236
[http://dx.doi.org/10.1371/journal.pone.0135236] [PMID: 26288183]
[52]
Shen Y, Yang J, Zhao J, Xiao C, Xu C, Xiang Y. The switch from ER stress-induced apoptosis to autophagy via ROS-mediated JNK/p62 signals: A survival mechanism in methotrexate-resistant choriocarcinoma cells. Exp Cell Res 2015; 334(2): 207-18.
[http://dx.doi.org/10.1016/j.yexcr.2015.04.010] [PMID: 25912909]
[53]
Lin CJ, Lee CC, Shih YL, et al. Resveratrol enhances the therapeutic effect of temozolomide against malignant glioma in vitro and in vivo by inhibiting autophagy. Free Radic Biol Med 2012; 52(2): 377-91.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.10.487] [PMID: 22094224]
[54]
Cheng P, Ni Z, Dai X, et al. The novel BH-3 mimetic apogossypolone induces Beclin-1- and ROS-mediated autophagy in human hepatocellular carcinoma [corrected] cells. Cell Death Dis 2013; 4e489
[http://dx.doi.org/10.1038/cddis.2013.17] [PMID: 23392177]
[55]
Niu Q, Zhao W, Wang J, et al. LicA induces autophagy through ULK1/Atg13 and ROS pathway in human hepatocellular carcinoma cells. Int J Mol Med 2018; 41(5): 2601-8.
[http://dx.doi.org/10.3892/ijmm.2018.3499] [PMID: 29484365]
[56]
Fan TF, Wu TF, Bu LL, et al. Dihydromyricetin promotes autophagy and apoptosis through ROS-STAT3 signaling in head and neck squamous cell carcinoma. Oncotarget 2016; 7(37): 59691-703.
[http://dx.doi.org/10.18632/oncotarget.10836] [PMID: 27474168]
[57]
Lu C, Wang W, Jia Y, Liu X, Tong Z, Li B. Inhibition of AMPK/autophagy potentiates parthenolide-induced apoptosis in human breast cancer cells. J Cell Biochem 2014; 115(8): 1458-66.
[http://dx.doi.org/10.1002/jcb.24808] [PMID: 24619908]
[58]
Qu X, Sheng J, Shen L, et al. Autophagy inhibitor chloroquine increases sensitivity to cisplatin in QBC939 cholangiocarcinoma cells by mitochondrial ROS. PLoS One 2017; 12(3)e0173712
[http://dx.doi.org/10.1371/journal.pone.0173712] [PMID: 28301876]
[59]
Harhaji-Trajkovic L, Vilimanovich U, Kravic-Stevovic T, Bumbasirevic V, Trajkovic V. AMPK-mediated autophagy inhibits apoptosis in cisplatin-treated tumour cells. J Cell Mol Med 2009; 13(9B): 3644-54.
[http://dx.doi.org/10.1111/j.1582-4934.2009.00663.x] [PMID: 20196784]
[60]
Yang C, Yang QO, Kong QJ, Yuan W, Ou Yang YP. Parthenolide induces reactive oxygen species-mediated autophagic cell death in human osteosarcoma cells. Cell Physiol Biochem 2016; 40(1-2): 146-54.
[http://dx.doi.org/10.1159/000452532] [PMID: 27855364]
[61]
Shinohara H, Taniguchi K, Kumazaki M, et al. Anti-cancer fatty-acid derivative induces autophagic cell death through modulation of PKM isoform expression profile mediated by bcr-abl in chronic myeloid leukemia. Cancer Lett 2015; 360(1): 28-38.
[http://dx.doi.org/10.1016/j.canlet.2015.01.039] [PMID: 25644089]
[62]
Itoh T, Ito Y, Ohguchi K, et al. Eupalinin A isolated from Eupatorium chinense L. induces autophagocytosis in human leukemia HL60 cells. Bioorg Med Chem 2008; 16(2): 721-31.
[http://dx.doi.org/10.1016/j.bmc.2007.10.033] [PMID: 17980607]
[63]
Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB. Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J Cell Sci 2007; 120(Pt 23): 4155-66.
[http://dx.doi.org/10.1242/jcs.011163] [PMID: 18032788]
[64]
Pan X, Liu D, Wang J, et al. Peneciraistin C induces caspase-independent autophagic cell death through mitochondrial-derived reactive oxygen species production in lung cancer cells. Cancer Sci 2013; 104(11): 1476-82.
[http://dx.doi.org/10.1111/cas.12253] [PMID: 23952056]
[65]
Yu L, Wan F, Dutta S, et al. Autophagic programmed cell death by selective catalase degradation. Proc Natl Acad Sci USA 2006; 103(13): 4952-7.
[http://dx.doi.org/10.1073/pnas.0511288103] [PMID: 16547133]
[66]
Jiang J, Maeda A, Ji J, et al. Are mitochondrial reactive oxygen species required for autophagy? Biochem Biophys Res Commun 2011; 412(1): 55-60.
[http://dx.doi.org/10.1016/j.bbrc.2011.07.036] [PMID: 21806968]
[67]
Chen YF, Wu ZM, Luo XJ, Bai S, Zhao LD. Effect of the conditional knockout of bone marrow specific RIPK3 gene on bone marrow hematopoiesis in mice. Int J Clin Exp Pathol 2018; 11: 568-76.
[68]
Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425(6960): 836-41.
[http://dx.doi.org/10.1038/nature02041] [PMID: 14574412]
[69]
Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007; 110(8): 3056-63.
[http://dx.doi.org/10.1182/blood-2007-05-087759] [PMID: 17595331]
[70]
Ludin A, Gur-Cohen S, Golan K, et al. Reactive oxygen species regulate hematopoietic stem cell self-renewal, migration and development, as well as their bone marrow microenvironment. Antioxid Redox Signal 2014; 21(11): 1605-19.
[http://dx.doi.org/10.1089/ars.2014.5941] [PMID: 24762207]
[71]
Ito K, Hirao A, Arai F, et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 2004; 431(7011): 997-1002.
[http://dx.doi.org/10.1038/nature02989] [PMID: 15496926]
[72]
Zhang X, Rielland M, Yalcin S, Ghaffari S. Regulation and function of FoxO transcription factors in normal and cancer stem cells: what have we learned? Curr Drug Targets 2011; 12(9): 1267-83.
[http://dx.doi.org/10.2174/138945011796150325] [PMID: 21443463]
[73]
Tothova Z, Kollipara R, Huntly BJ, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007; 128(2): 325-39.
[http://dx.doi.org/10.1016/j.cell.2007.01.003] [PMID: 17254970]
[74]
Chen C, Liu Y, Liu R, et al. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med 2008; 205(10): 2397-408.
[http://dx.doi.org/10.1084/jem.20081297] [PMID: 18809716]
[75]
Juntilla MM, Patil VD, Calamito M, Joshi RP, Birnbaum MJ, Koretzky GA. AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 2010; 115(20): 4030-8.
[http://dx.doi.org/10.1182/blood-2009-09-241000] [PMID: 20354168]
[76]
Liu J, Cao L, Chen J, et al. Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 2009; 459(7245): 387-92.
[http://dx.doi.org/10.1038/nature08040] [PMID: 19404261]
[77]
Schuringa JJ, Vellenga E. Role of the polycomb group gene BMI1 in normal and leukemic hematopoietic stem and progenitor cells. Curr Opin Hematol 2010; 17(4): 294-9.
[http://dx.doi.org/10.1097/MOH.0b013e328338c439] [PMID: 20308890]
[78]
Abbas HA, Maccio DR, Coskun S, et al. Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell Stem Cell 2010; 7(5): 606-17.
[http://dx.doi.org/10.1016/j.stem.2010.09.013] [PMID: 21040902]
[79]
Taniguchi IE, Gonzalez-Nieto D, Ghiaur G, et al. Connexin-43 prevents hematopoietic stem cell senescence through transfer of reactive oxygen species to bone marrow stromal cells. Proc Natl Acad Sci USA 2012; 109(23): 9071-6.
[http://dx.doi.org/10.1073/pnas.1120358109] [PMID: 22611193]
[80]
Hu M, Zeng H, Chen S, et al. SRC-3 is involved in maintaining hematopoietic stem cell quiescence by regulation of mitochondrial metabolism in mice. Blood 2018; 132(9): 911-23.
[http://dx.doi.org/10.1182/blood-2018-02-831669] [PMID: 29959189]
[81]
Kim TG, Kim S, Jung S, et al. CCCTC-binding factor is essential to the maintenance and quiescence of hematopoietic stem cells in mice. Exp Mol Med 2017; 49(8)e371
[http://dx.doi.org/10.1038/emm.2017.124] [PMID: 28857086]
[82]
Zhang Y, Dépond M, He L, et al. CXCR4/CXCL12 axis counteracts hematopoietic stem cell exhaustion through selective protection against oxidative stress. Sci Rep 2016; 6: 37827.
[http://dx.doi.org/10.1038/srep37827] [PMID: 27886253]
[83]
Fan C, Zheng W, Fu X, Li X, Wong YS, Chen T. Strategy to enhance the therapeutic effect of doxorubicin in human hepatocellular carcinoma by selenocystine, a synergistic agent that regulates the ROS-mediated signaling. Oncotarget 2014; 5(9): 2853-63.
[http://dx.doi.org/10.18632/oncotarget.1854] [PMID: 24797310]
[84]
Kim EH, Jang H, Roh JL. A novel polyphenol conjugate sensitizes cisplatin-resistant head and neck cancer cells to cisplatin via nrf2 inhibition. Mol Cancer Ther 2016; 15(11): 2620-9.
[http://dx.doi.org/10.1158/1535-7163.MCT-16-0332] [PMID: 27550943]
[85]
Martin-Cordero C, Leon-Gonzalez AJ, Calderon-Montano JM, Burgos-Moron E, Lopez-Lazaro M. Pro-oxidant natural products as anticancer agents. Curr Drug Targets 2012; 13(8): 1006-28.
[http://dx.doi.org/10.2174/138945012802009044] [PMID: 22594470]
[86]
El-Sayed el-SM, Abdel-Aziz AA, Helal GK, Saleh S, and Saad AS. Protective effect of N-acetylcysteine against carmustine-induced myelotoxicity in rats. Food Chem Toxicol 2010; 48: 1576-80.
[http://dx.doi.org/10.1016/j.fct.2010.03.027]
[87]
Numazawa S, Sugihara K, Miyake S, et al. Possible involvement of oxidative stress in 5-fluorouracil-mediated myelosuppression in mice. Basic Clin Pharmacol Toxicol 2011; 108(1): 40-5.
[http://dx.doi.org/10.1111/j.1742-7843.2010.00621.x] [PMID: 20722640]
[88]
Deng J, Zhong YF, Wu YP, et al. Carnosine attenuates cyclophosphamide-induced bone marrow suppression by reducing oxidative DNA damage. Redox Biol 2018; 14: 1-6.
[http://dx.doi.org/10.1016/j.redox.2017.08.003] [PMID: 28826042]
[89]
Diaz-Montero CM, Wang Y, Shao L, et al. The glutathione disulfide mimetic NOV-002 inhibits cyclophosphamide-induced hematopoietic and immune suppression by reducing oxidative stress. Free Radic Biol Med 2012; 52(9): 1560-8.
[http://dx.doi.org/10.1016/j.freeradbiomed.2012.02.007] [PMID: 22343421]
[90]
Itoh T, Terazawa R, Kojima K, et al. Cisplatin induces production of reactive oxygen species via NADPH oxidase activation in human prostate cancer cells. Free Radic Res 2011; 45(9): 1033-9.
[http://dx.doi.org/10.3109/10715762.2011.591391] [PMID: 21682664]
[91]
Naka K, Muraguchi T, Hoshii T, Hirao A. Regulation of reactive oxygen species and genomic stability in hematopoietic stem cells. Antioxid Redox Signal 2008; 10(11): 1883-94.
[http://dx.doi.org/10.1089/ars.2008.2114] [PMID: 18627347]
[92]
Richardson C, Yan S, Vestal CG. Oxidative stress, bone marrow failure, and genome instability in hematopoietic stem cells. Int J Mol Sci 2015; 16(2): 2366-85.
[http://dx.doi.org/10.3390/ijms16022366] [PMID: 25622253]
[93]
Newman NB, Sidhu MK, Baby R, et al. Long-term bone marrow suppression during postoperative chemotherapy in rectal cancer patients after preoperative chemoradiation therapy. Int J Radiat Oncol Biol Phys 2016; 94(5): 1052-60.
[http://dx.doi.org/10.1016/j.ijrobp.2015.12.374] [PMID: 27026312]
[94]
Boohaker RJ, Xu B. The versatile functions of ATM kinase. Biomed J 2014; 37(1): 3-9.
[http://dx.doi.org/10.4103/2319-4170.125655] [PMID: 24667671]
[95]
Ruzankina Y, Pinzon-Guzman C, Asare A, et al. Deletion of the developmentally essential gene ATR in adult mice leads to age-related phenotypes and stem cell loss. Cell Stem Cell 2007; 1(1): 113-26.
[http://dx.doi.org/10.1016/j.stem.2007.03.002] [PMID: 18371340]
[96]
Wang M, Guo L, Wu Q, et al. ATR/Chk1/Smurf1 pathway determines cell fate after DNA damage by controlling RhoB abundance. Nat Commun 2014; 5: 4901.
[http://dx.doi.org/10.1038/ncomms5901] [PMID: 25249323]
[97]
Sancar A, Lindsey-Boltz LA, Unsal-Kaçmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73: 39-85.
[http://dx.doi.org/10.1146/annurev.biochem.73.011303.073723] [PMID: 15189136]
[98]
Shao L, Li H, Pazhanisamy SK, Meng A, Wang Y, Zhou D. Reactive oxygen species and hematopoietic stem cell senescence. Int J Hematol 2011; 94(1): 24-32.
[http://dx.doi.org/10.1007/s12185-011-0872-1] [PMID: 21567162]
[99]
von Zglinicki T, Saretzki G, Ladhoff J, d’Adda di Fagagna F, Jackson SP. Human cell senescence as a DNA damage response. Mech Ageing Dev 2005; 126(1): 111-7.
[http://dx.doi.org/10.1016/j.mad.2004.09.034] [PMID: 15610769]
[100]
Ito K, Hirao A, Arai F, et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 2006; 12(4): 446-51.
[http://dx.doi.org/10.1038/nm1388] [PMID: 16565722]
[101]
Bartkova J, Lukas J, Guldberg P, et al. The p16-cyclin D/Cdk4-pRb pathway as a functional unit frequently altered in melanoma pathogenesis. Cancer Res 1996; 56(23): 5475-83.
[PMID: 8968104]
[102]
Semczuk A, Jakowicki JA. Alterations of pRb1-cyclin D1-cdk4/6-p16(INK4A) pathway in endometrial carcinogenesis. Cancer Lett 2004; 203(1): 1-12.
[http://dx.doi.org/10.1016/j.canlet.2003.09.012] [PMID: 14670612]
[103]
Ingold KU, Pratt DA. Advances in radical-trapping antioxidant chemistry in the 21st century: a kinetics and mechanisms perspective. Chem Rev 2014; 114(18): 9022-46.
[http://dx.doi.org/10.1021/cr500226n] [PMID: 25180889]
[104]
Saso L, Firuzi O. Pharmacological applications of antioxidants: lights and shadows. Curr Drug Targets 2014; 15(13): 1177-99.
[http://dx.doi.org/10.2174/1389450115666141024113925] [PMID: 25341421]
[105]
Li H, Wang Y, Pazhanisamy SK, et al. Mn(III) meso-tetrakis-(N-ethylpyridinium-2-yl) porphyrin mitigates total body irradiation-induced long-term bone marrow suppression. Free Radic Biol Med 2011; 51(1): 30-7.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.04.016] [PMID: 21565268]
[106]
Mehrotra S, Pecaut MJ, Freeman TL, et al. Analysis of a metalloporphyrin antioxidant mimetic (MnTE-2-PyP) as a radiomitigator: prostate tumor and immune status. Technol Cancer Res Treat 2012; 11(5): 447-57.
[http://dx.doi.org/10.7785/tcrt.2012.500260] [PMID: 22475066]
[107]
Gumireddy K, Li A, Cao L, et al. NOV-002, A Glutathione Disulfide Mimetic, Suppresses Tumor Cell Invasion and Metastasis. J Carcinog Mutagen 2013; S7-S002.
[108]
Jenderny S, Lin H, Garrett T, Tew KD, Townsend DM. Protective effects of a glutathione disulfide mimetic (NOV-002) against cisplatin induced kidney toxicity. Biomed Pharmacother 2010; 64(1): 73-6.
[http://dx.doi.org/10.1016/j.biopha.2009.09.009] [PMID: 19896793]
[109]
Basu A, Bhattacharjee A, Baral R, Biswas J, Samanta A, Bhattacharya S. Vanadium(III)-l-cysteine enhances the sensitivity of murine breast adenocarcinoma cells to cyclophosphamide by promoting apoptosis and blocking angiogenesis. Tumour Biol 2017; 39(5)1010428317705759
[http://dx.doi.org/10.1177/1010428317705759] [PMID: 28466788]
[110]
Basu A, Ghosh P, Bhattacharjee A, Patra AR, Bhattacharya S. Prevention of myelosuppression and genotoxicity induced by cisplatin in murine bone marrow cells: effect of an organovanadium compound vanadium(III)-l-cysteine. Mutagenesis 2015; 30(4): 509-17.
[http://dx.doi.org/10.1093/mutage/gev011] [PMID: 25778689]
[111]
Capizzi RL. Amifostine reduces the incidence of cumulative nephrotoxicity from cisplatin: laboratory and clinical aspects. Semin Oncol 1999; 26(2)(Suppl. 7): 72-81.
[PMID: 10348264]
[112]
Sinha S, Jothiramajayam M, Ghosh M, Jana A, Chatterji U, Mukherjee A. Vetiver oil (Java) attenuates cisplatin-induced oxidative stress, nephrotoxicity and myelosuppression in Swiss albino mice. Food Chem Toxicol 2015; 81: 120-8.
[http://dx.doi.org/10.1016/j.fct.2015.04.018] [PMID: 25910835]
[113]
Alberts DS. Protection by amifostine of cyclophosphamide-induced myelosuppression. Semin Oncol 1999; 26(2)(Suppl. 7): 37-40.
[PMID: 10348259]
[114]
Chen T, Shen HM, Deng ZY, et al. A herbal formula, SYKT, reverses doxorubicin-induced myelosuppression and cardiotoxicity by inhibiting ROS-mediated apoptosis. Mol Med Rep 2017; 15(4): 2057-66.
[http://dx.doi.org/10.3892/mmr.2017.6272] [PMID: 28260045]
[115]
Guimarães R, Barreira JC, Barros L, Carvalho AM, Ferreira IC. Effects of oral dosage form and storage period on the antioxidant properties of four species used in traditional herbal medicine. Phytother Res 2011; 25(4): 484-92.
[http://dx.doi.org/10.1002/ptr.3284] [PMID: 20740475]
[116]
Khan HY, Zubair H, Ullah MF, Ahmad A, Hadi SM. A prooxidant mechanism for the anticancer and chemopreventive properties of plant polyphenols. Curr Drug Targets 2012; 13(14): 1738-49.
[http://dx.doi.org/10.2174/138945012804545560] [PMID: 23140285]
[117]
Rezk YA, Balulad SS, Keller RS, Bennett JA. Use of resveratrol to improve the effectiveness of cisplatin and doxorubicin: study in human gynecologic cancer cell lines and in rodent heart. Am J Obstet Gynecol 2006; 194(5): e23-6.
[http://dx.doi.org/10.1016/j.ajog.2005.11.030] [PMID: 16647892]
[118]
Zhou QM, Zhang H, Lu YY, Wang XF, Su SB. Curcumin reduced the side effects of mitomycin C by inhibiting GRP58-mediated DNA cross-linking in MCF-7 breast cancer xenografts. Cancer Sci 2009; 100(11): 2040-5.
[http://dx.doi.org/10.1111/j.1349-7006.2009.01297.x] [PMID: 19703194]
[119]
Alaikov T, Konstantinov SM, Tzanova T, Dinev K, Topashka-Ancheva M, Berger MR. Antineoplastic and anticlastogenic properties of curcumin. Ann N Y Acad Sci 2007; 1095: 355-70.
[http://dx.doi.org/10.1196/annals.1397.039] [PMID: 17404048]
[120]
Chen J, Wanming D, Zhang D, Liu Q, Kang J. Water-soluble antioxidants improve the antioxidant and anticancer activity of low concentrations of curcumin in human leukemia cells. Pharmazie 2005; 60(1): 57-61.
[PMID: 15700780]
[121]
Yamamoto T, Hsu S, Lewis J, et al. Green tea polyphenol causes differential oxidative environments in tumor versus normal epithelial cells. J Pharmacol Exp Ther 2003; 307(1): 230-6.
[http://dx.doi.org/10.1124/jpet.103.054676] [PMID: 12954803]
[122]
Jain P, Kumar N, Josyula VR, et al. A study on the role of (+)-catechin in suppression of HepG2 proliferation via caspase dependent pathway and enhancement of its in vitro and in vivo cytotoxic potential through liposomal formulation. Eur J Pharm Sci 2013; 50(3-4): 353-65.
[http://dx.doi.org/10.1016/j.ejps.2013.08.005] [PMID: 23954456]
[123]
Papiez MA, Baran J, Bukowska-Straková K, Wiczkowski W. Antileukemic action of (-)-epicatechin in the spleen of rats with acute myeloid leukemia. Food Chem Toxicol 2010; 48(12): 3391-7.
[http://dx.doi.org/10.1016/j.fct.2010.09.010] [PMID: 20837083]
[124]
Feng R, Ni HM, Wang SY, et al. Cyanidin-3-rutinoside, a natural polyphenol antioxidant, selectively kills leukemic cells by induction of oxidative stress. J Biol Chem 2007; 282(18): 13468-76.
[http://dx.doi.org/10.1074/jbc.M610616200] [PMID: 17360708]
[125]
Chen F, Li D, Shen H, et al. Polysaccharides from Trichosanthes Fructus via Ultrasound-Assisted Enzymatic Extraction Using Response Surface Methodology. BioMed Res Int 2017.20176160785
[http://dx.doi.org/10.1155/2017/6160785] [PMID: 29147656]
[126]
Hu J, Jia X, Fang X, Li P, He C, Chen M. Ultrasonic extraction, antioxidant and anticancer activities of novel polysaccharides from Chuanxiong rhizome. Int J Biol Macromol 2016; 85: 277-84.
[http://dx.doi.org/10.1016/j.ijbiomac.2015.12.046] [PMID: 26712703]
[127]
Jiang YY, Wang L, Zhang L, et al. Characterization, antioxidant and antitumor activities of polysaccharides from Salvia miltiorrhiza Bunge. Int J Biol Macromol 2014; 70: 92-9.
[http://dx.doi.org/10.1016/j.ijbiomac.2014.06.036] [PMID: 24984021]
[128]
Liu LQ, Li HS, Nie SP, Shen MY, Hu JL, Xie MY. tea polysaccharide prevents colitis-associated carcinogenesis in mice by inhibiting the proliferation and invasion of tumor cells. Int J Mol Sci 2018; 19(2)E506
[http://dx.doi.org/10.3390/ijms19020506] [PMID: 29419740]
[129]
Wei C, He P, He L, et al. Structure characterization and biological activities of a pectic polysaccharide from cupule of Castanea henryi. Int J Biol Macromol 2018; 109: 65-75.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.12.081] [PMID: 29248551]
[130]
Xin YF, Wan LL, Peng JL, Guo C. Alleviation of the acute doxorubicin-induced cardiotoxicity by Lycium barbarum polysaccharides through the suppression of oxidative stress. Food Chem Toxicol 2011; 49(1): 259-64.
[http://dx.doi.org/10.1016/j.fct.2010.10.028] [PMID: 21056614]
[131]
Zhao QS, Xie BX, Yan J, et al. In vitro antioxidant and antitumor activities of polysaccharides extracted from Asparagus officinalis. Carbohydr Polym 2012; 87: 392-6.
[http://dx.doi.org/10.1016/j.carbpol.2011.07.068]
[132]
Cai Z, Li W, Wang H, et al. Antitumor effects of a purified polysaccharide from Rhodiola rosea and its action mechanism. Carbohydr Polym 2012; 90(1): 296-300.
[http://dx.doi.org/10.1016/j.carbpol.2012.05.039] [PMID: 24751044]
[133]
Wang H, Yu P, Gou H, et al. Cardioprotective effects of 20(s)-ginsenoside rh2 against doxorubicin-induced cardiotoxicity in vitro and in vivo. Evid Based Complement Alternat Med 2012.2012506214
[http://dx.doi.org/10.1155/2012/506214] [PMID: 23125868]
[134]
Zhao J, Xu F, Huang H, et al. Evaluation on Anti-Inflammatory, Analgesic, Antitumor, and Antioxidant Potential of Total Saponins from Nigella glandulifera Seeds. Evid Based Complement Alternat Med 2013.2013827230
[http://dx.doi.org/10.1155/2013/827230] [PMID: 23533525]
[135]
Iman V, Mohan S, Abdelwahab SI, et al. Anticancer and anti-inflammatory activities of girinimbine isolated from Murraya koenigii. Drug Des Devel Ther 2016; 11: 103-21.
[http://dx.doi.org/10.2147/DDDT.S115135] [PMID: 28096658]
[136]
Sanchez-Gonzalez PD, Lopez-Hernandez FJ, Perez-Barriocanal F, Morales AI, Lopez-Novoa JM. Quercetin reduces cisplatin nephrotoxicity in rats without compromising its anti-tumour activity. Nephrol Dial Transplant 2011; 26(11): 3484-95.
[http://dx.doi.org/10.1093/ndt/gfr195] [PMID: 21602180]
[137]
Attia SM, Ahmad SF, Harisa GI, Mansour AM, El Sayed SM, Bakheet SA. Wogonin attenuates etoposide-induced oxidative DNA damage and apoptosis via suppression of oxidative DNA stress and modulation of OGG1 expression. Food Chem Toxicol 2013; 59: 724-30.
[http://dx.doi.org/10.1016/j.fct.2013.07.022] [PMID: 23872129]
[138]
Bokemeyer C, Fels LM, Dunn T, et al. Silibinin protects against cisplatin-induced nephrotoxicity without compromising cisplatin or ifosfamide anti-tumour activity. Br J Cancer 1996; 74(12): 2036-41.
[http://dx.doi.org/10.1038/bjc.1996.673] [PMID: 8980410]
[139]
Juan ME, Wenzel U, Daniel H, Planas JM. Resveratrol induces apoptosis through ROS-dependent mitochondria pathway in HT-29 human colorectal carcinoma cells. J Agric Food Chem 2008; 56(12): 4813-8.
[http://dx.doi.org/10.1021/jf800175a] [PMID: 18522405]
[140]
Bianchi G, Ravera S, Traverso C, et al. Curcumin induces a fatal energetic impairment in tumor cells in vitro and in vivo by inhibiting ATP-synthase activity. Carcinogenesis 2018; 39(9): 1141-50.
[http://dx.doi.org/10.1093/carcin/bgy076] [PMID: 29860383]
[141]
Liu SM, Ou SY, Huang HH. Green tea polyphenols induce cell death in breast cancer MCF-7 cells through induction of cell cycle arrest and mitochondrial-mediated apoptosis. J Zhejiang Univ Sci B 2017; 18(2): 89-98.
[http://dx.doi.org/10.1631/jzus.B1600022] [PMID: 28124838]
[142]
Yan CM, Chai EQ, Cai HY, Miao GY, Ma W. Oleuropein induces apoptosis via activation of caspases and suppression of phosphatidylinositol 3-kinase/protein kinase B pathway in HepG2 human hepatoma cell line. Mol Med Rep 2015; 11(6): 4617-24.
[http://dx.doi.org/10.3892/mmr.2015.3266] [PMID: 25634350]
[143]
Attoub S, Ramadan G, Arafat K, Bajbouj K, Karuvantevida N, AbuQamar S, Eid A, and Iratni R. Carnosol induces ROS-mediated beclin1-independent autophagy and apoptosis in triple negative breast cancer. PLoS One 2014; 9e109630
[http://dx.doi.org/10.1371/journal.pone.0109630]
[144]
Zhang L, Chen QS, Xu PP, et al. Catechins induced acute promyelocytic leukemia cell apoptosis and triggered PML-RARα oncoprotein degradation. J Hematol Oncol 2014; 7: 75.
[http://dx.doi.org/10.1186/s13045-014-0075-3] [PMID: 25270015]
[145]
Yang LH, Ho YJ, Lin JF, Yeh CW, Kao SH, Hsu LS. Butein inhibits the proliferation of breast cancer cells through generation of reactive oxygen species and modulation of ERK and p38 activities. Mol Med Rep 2012; 6(5): 1126-32.
[http://dx.doi.org/10.3892/mmr.2012.1023] [PMID: 22895548]
[146]
Zhen D, Su L, Miao Y, et al. Purification, partial characterization and inducing tumor cell apoptosis activity of a polysaccharide from Ganoderma applanatum. Int J Biol Macromol 2018; 115: 10-7.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.03.062] [PMID: 29653168]
[147]
Zhang S, Nie S, Huang D, Feng Y, Xie M. A novel polysaccharide from Ganoderma atrum exerts antitumor activity by activating mitochondria-mediated apoptotic pathway and boosting the immune system. J Agric Food Chem 2014; 62(7): 1581-9.
[http://dx.doi.org/10.1021/jf4053012] [PMID: 24506418]
[148]
Wang J, Li W, Huang X, et al. A polysaccharide from Lentinus edodes inhibits human colon cancer cell proliferation and suppresses tumor growth in athymic nude mice. Oncotarget 2017; 8(1): 610-23.
[http://dx.doi.org/10.18632/oncotarget.13481] [PMID: 27888812]
[149]
Liu WB, Xie F, Sun HQ, Meng M, Zhu ZY. Anti-tumor effect of polysaccharide from Hirsutella sinensis on human non-small cell lung cancer and nude mice through intrinsic mitochondrial pathway. Int J Biol Macromol 2017; 99: 258-64.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.02.071] [PMID: 28235606]
[150]
Liu G, Kuang S, Wu S, Jin W, Sun C. A novel polysaccharide from Sargassum integerrimum induces apoptosis in A549 cells and prevents angiogensis in vitro and in vivo. Sci Rep 2016; 6: 26722.
[http://dx.doi.org/10.1038/srep26722] [PMID: 27216943]
[151]
Ren D, Wang N, Guo J, Yuan L, Yang X. Chemical characterization of Pleurotus eryngii polysaccharide and its tumor-inhibitory effects against human hepatoblastoma HepG-2 cells. Carbohydr Polym 2016; 138: 123-33.
[http://dx.doi.org/10.1016/j.carbpol.2015.11.051] [PMID: 26794745]
[152]
Chen J, Yao D, Yuan H, et al. Dipsacus asperoides polysaccharide induces apoptosis in osteosarcoma cells by modulating the PI3K/Akt pathway. Carbohydr Polym 2013; 95(2): 780-4.
[http://dx.doi.org/10.1016/j.carbpol.2013.03.009] [PMID: 23648042]
[153]
Ma B, Zhu J, Zhao A, et al. Raddeanin A, a natural triterpenoid saponin compound, exerts anticancer effect on human osteosarcoma via the ROS/JNK and NF-κB signal pathway. Toxicol Appl Pharmacol 2018; 353: 87-101.
[http://dx.doi.org/10.1016/j.taap.2018.05.025] [PMID: 29847772]
[154]
Mbaveng AT, Ndontsa BL, Kuete V, et al. A naturally occuring triterpene saponin ardisiacrispin B displayed cytotoxic effects in multi-factorial drug resistant cancer cells via ferroptotic and apoptotic cell death. Phytomedicine 2018; 43: 78-85.
[http://dx.doi.org/10.1016/j.phymed.2018.03.035] [PMID: 29747757]
[155]
Lin CL, Lee CH, Chen CM, et al. Protodioscin Induces Apoptosis Through ROS-Mediated Endoplasmic Reticulum Stress via the JNK/p38 Activation Pathways in Human Cervical Cancer Cells. Cell Physiol Biochem 2018; 46(1): 322-34.
[http://dx.doi.org/10.1159/000488433] [PMID: 29590661]
[156]
Li S, Cheng B, Hou L, et al. Dioscin inhibits colon cancer cells’ growth by reactive oxygen species-mediated mitochondrial dysfunction and p38 and JNK pathways. Anticancer Drugs 2018; 29(3): 234-42.
[PMID: 29389802]
[157]
Zhang S, He Y, Tong Q, Chen Q, Wu X, Huang W. Deltonin induces apoptosis in MDA-MB-231 human breast cancer cells via reactive oxygen species-mediated mitochondrial dysfunction and ERK/AKT signaling pathways. Mol Med Rep 2013; 7(3): 1038-44.
[http://dx.doi.org/10.3892/mmr.2013.1273] [PMID: 23314115]
[158]
Kim DS, Jeon BK, Lee YE, Woo WH, Mun YJ. Diosgenin induces apoptosis in hepg2 cells through generation of reactive oxygen species and mitochondrial pathway. Evid Based Complement Alternat Med 2012.2012981675
[http://dx.doi.org/10.1155/2012/981675] [PMID: 22719792]
[159]
Wu Q, Deng J, Fan D, et al. Ginsenoside Rh4 induces apoptosis and autophagic cell death through activation of the ROS/JNK/p53 pathway in colorectal cancer cells. Biochem Pharmacol 2018; 148: 64-74.
[http://dx.doi.org/10.1016/j.bcp.2017.12.004] [PMID: 29225132]
[160]
Farooqui A, Khan F, Khan I, Ansari IA. Glycyrrhizin induces reactive oxygen species-dependent apoptosis and cell cycle arrest at G0/G1 in HPV18+ human cervical cancer HeLa cell line. Biomed Pharmacother 2018; 97: 752-64.
[http://dx.doi.org/10.1016/j.biopha.2017.10.147] [PMID: 29107932]
[161]
Wu JP, Kang NX, Zhang MY, et al. Oleiferoside W from the roots of Camellia oleifera C. Abel, inducing cell cycle arrest and apoptosis in A549 cells. J Asian Nat Prod Res 2017; 6: 1-14.
[PMID: 28679317]
[162]
Zhu WB, Tian FJ, Liu LQ. Chikusetsu (CHI) triggers mitochondria-regulated apoptosis in human prostate cancer via reactive oxygen species (ROS) production. Biomed Pharmacother 2017; 90: 446-54.
[http://dx.doi.org/10.1016/j.biopha.2017.03.050] [PMID: 28391166]
[163]
Yang JB, Khan M, He YY, et al. Tubeimoside-1 induces oxidative stress-mediated apoptosis and G0/G1 phase arrest in human prostate carcinoma cells in vitro. Acta Pharmacol Sin 2016; 37(7): 950-62.
[http://dx.doi.org/10.1038/aps.2016.34] [PMID: 27292614]
[164]
Liu J, Wei X, Wu Y, et al. Giganteaside D induces ROS-mediated apoptosis in human hepatocellular carcinoma cells through the MAPK pathway. Cell Oncol (Dordr) 2016; 39(4): 333-42.
[http://dx.doi.org/10.1007/s13402-016-0273-9] [PMID: 27016209]
[165]
Li J, Wu DD, Zhang JX, et al. Mitochondrial pathway mediated by reactive oxygen species involvement in α-hederin-induced apoptosis in hepatocellular carcinoma cells. World J Gastroenterol 2018; 24(17): 1901-10.
[http://dx.doi.org/10.3748/wjg.v24.i17.1901] [PMID: 29740205]
[166]
Shan Y, Guan F, Zhao X, et al. Macranthoside B induces apoptosis and autophagy via reactive oxygen species accumulation in human ovarian cancer A2780 cells. Nutr Cancer 2016; 68(2): 280-9.
[http://dx.doi.org/10.1080/01635581.2016.1142587] [PMID: 26943028]
[167]
Wang J, Yuan L, Xiao H, Xiao C, Wang Y, Liu X. Momordin Ic induces HepG2 cell apoptosis through MAPK and PI3K/Akt-mediated mitochondrial pathways. Apoptosis 2013; 18(6): 751-65.
[http://dx.doi.org/10.1007/s10495-013-0820-z] [PMID: 23417763]
[168]
Ji Y, Ji C, Yue L, Xu H. Saponins isolated from Asparagus induce apoptosis in human hepatoma cell line HepG2 through a mitochondrial-mediated pathway. Curr Oncol 2012; 19(Suppl. 2): eS1-9.
[http://dx.doi.org/10.3747/co.19.1139] [PMID: 22876162]
[169]
Mo S, Xiong H, Shu G, et al. Phaseoloideside E, a novel natural triterpenoid saponin identified from Entada phaseoloides, induces apoptosis in Ec-109 esophageal cancer cells through reactive oxygen species generation. J Pharmacol Sci 2013; 122(3): 163-75.
[http://dx.doi.org/10.1254/jphs.12193FP] [PMID: 23782641]
[170]
Zhu X, Wang K, Zhang K, Zhu L, Zhou F. Ziyuglycoside II induces cell cycle arrest and apoptosis through activation of ROS/JNK pathway in human breast cancer cells. Toxicol Lett 2014; 227(1): 65-73.
[http://dx.doi.org/10.1016/j.toxlet.2014.03.015] [PMID: 24680927]
[171]
Zhang C, Jia X, Bao J, et al. Polyphyllin VII induces apoptosis in HepG2 cells through ROS-mediated mitochondrial dysfunction and MAPK pathways. BMC Complement Altern Med 2016; 16: 58.
[http://dx.doi.org/10.1186/s12906-016-1036-x] [PMID: 26861252]
[172]
Wu S, Yang Y, Li F, et al. Chelerythrine induced cell death through ROS-dependent ER stress in human prostate cancer cells. OncoTargets Ther 2018; 11: 2593-601.
[http://dx.doi.org/10.2147/OTT.S157707] [PMID: 29780252]
[173]
Jiang JH, Pi J, Jin H, Yang F, Cai JY. Chinese herb medicine matrine induce apoptosis in human esophageal squamous cancer KYSE-150 cells through increasing reactive oxygen species and inhibiting mitochondrial function. Pathol Res Pract 2018; 214(5): 691-9.
[http://dx.doi.org/10.1016/j.prp.2018.03.015] [PMID: 29567333]
[174]
Santos LS, Silva VR, Menezes LRA, Soares MBP, Costa EV, Bezerra DP. Xylopine induces oxidative stress and causes g2/m phase arrest, triggering caspase-mediated apoptosis by p53-independent pathway in hct116 cells. Oxid Med Cell Longev 2017.20177126872
[http://dx.doi.org/10.1155/2017/7126872] [PMID: 29362667]
[175]
Rattanawong A, Payon V, Limpanasittikul W, Boonkrai C, Mutirangura A, Wonganan P. Cepharanthine exhibits a potent anticancer activity in p53-mutated colorectal cancer cells through upregulation of p21Waf1/Cip1. Oncol Rep 2018; 39(1): 227-38.
[PMID: 29138869]
[176]
Eid W, Abdel-Rehim W. Neferine enhances the antitumor effect of mitomycin-c in hela cells through the activation of p38-mapk pathway. J Cell Biochem 2017; 118(10): 3472-9.
[http://dx.doi.org/10.1002/jcb.26006] [PMID: 28328092]
[177]
Stefanowicz-Hajduk J, Sparzak-Stefanowska B, Krauze-Baranowska M, Ochocka JR. Securinine from Phyllanthus glaucus Induces Cell Cycle Arrest and Apoptosis in Human Cervical Cancer HeLa Cells. PLoS One 2016; 11(10)e0165372
[http://dx.doi.org/10.1371/journal.pone.0165372] [PMID: 27792748]
[178]
Lin YJ, Peng SF, Lin ML, et al. Tetrandrine induces apoptosis of human nasopharyngeal carcinoma npc-tw 076 cells through reactive oxygen species accompanied by an endoplasmic reticulum stress signaling pathway. Molecules 2016; 21(10)E1353
[http://dx.doi.org/10.3390/molecules21101353] [PMID: 27754332]
[179]
Wang XD, Li CY, Jiang MM, et al. Induction of apoptosis in human leukemia cells through an intrinsic pathway by cathachunine, a unique alkaloid isolated from Catharanthus roseus. Phytomedicine 2016; 23(6): 641-53.
[http://dx.doi.org/10.1016/j.phymed.2016.03.003] [PMID: 27161405]
[180]
Gu S, Yang XC, Xiang XY, et al. Sanguinarine-induced apoptosis in lung adenocarcinoma cells is dependent on reactive oxygen species production and endoplasmic reticulum stress. Oncol Rep 2015; 34(2): 913-9.
[http://dx.doi.org/10.3892/or.2015.4054] [PMID: 26081590]
[181]
Li J, Sharkey CC, King MR. Piperlongumine and immune cytokine TRAIL synergize to promote tumor death. Sci Rep 2015; 5: 9987.
[http://dx.doi.org/10.1038/srep09987] [PMID: 25984950]
[182]
Park SH, Sung JH, Kim EJ, Chung N. Berberine induces apoptosis via ROS generation in PANC-1 and MIA-PaCa2 pancreatic cell lines. Braz J Med Biol Res 2015; 48(2): 111-9.
[http://dx.doi.org/10.1590/1414-431x20144293] [PMID: 25517919]
[183]
Jayasooriya RG, Choi YH, Hyun JW, Kim GY. Camptothecin sensitizes human hepatoma Hep3B cells to TRAIL-mediated apoptosis via ROS-dependent death receptor 5 upregulation with the involvement of MAPKs. Environ Toxicol Pharmacol 2014; 38(3): 959-67.
[http://dx.doi.org/10.1016/j.etap.2014.10.012] [PMID: 25461556]
[184]
Das R, Bhattacharya K, Sarkar S, Samanta SK, Pal BC, Mandal C. Mahanine synergistically enhances cytotoxicity of 5-fluorouracil through ROS-mediated activation of PTEN and p53/p73 in colon carcinoma. Apoptosis 2014; 19(1): 149-64.
[http://dx.doi.org/10.1007/s10495-013-0907-6] [PMID: 24052409]
[185]
Bi YL, Min M, Shen W, Liu Y. Genistein induced anticancer effects on pancreatic cancer cell lines involves mitochondrial apoptosis, G0/G1cell cycle arrest and regulation of STAT3 signalling pathway. Phytomedicine 2018; 39: 10-6.
[http://dx.doi.org/10.1016/j.phymed.2017.12.001] [PMID: 29433670]
[186]
Zhang J, Song J, Wu D, Wang J, Dong W. Hesperetin induces the apoptosis of hepatocellular carcinoma cells via mitochondrial pathway mediated by the increased intracellular reactive oxygen species, ATP and calcium. Med Oncol 2015; 32(4): 101.
[http://dx.doi.org/10.1007/s12032-015-0516-z] [PMID: 25737432]
[187]
Sun Q, Lu NN, Feng L. Apigetrin inhibits gastric cancer progression through inducing apoptosis and regulating ROS-modulated STAT3/JAK2 pathway. Biochem Biophys Res Commun 2018; 498(1): 164-70.
[http://dx.doi.org/10.1016/j.bbrc.2018.02.009] [PMID: 29408335]
[188]
Zhou M, Shen S, Zhao X, Gong X. Luteoloside induces G0/G1 arrest and pro-death autophagy through the ROS-mediated AKT/mTOR/p70S6K signalling pathway in human non-small cell lung cancer cell lines. Biochem Biophys Res Commun 2017; 494(1-2): 263-9.
[http://dx.doi.org/10.1016/j.bbrc.2017.10.042] [PMID: 29024631]
[189]
Zhang L, Wang X, Wang R, et al. Baicalin potentiates TRAIL-induced apoptosis through p38 MAPK activation and intracellular reactive oxygen species production. Mol Med Rep 2017; 16(6): 8549-55.
[http://dx.doi.org/10.3892/mmr.2017.7633] [PMID: 28983599]
[190]
Wang Q, Wang H, Jia Y, Pan H, Ding H. Luteolin induces apoptosis by ROS/ER stress and mitochondrial dysfunction in gliomablastoma. Cancer Chemother Pharmacol 2017; 79(5): 1031-41.
[http://dx.doi.org/10.1007/s00280-017-3299-4] [PMID: 28393257]
[191]
Hyun HB, Lee WS, Go SI, et al. The flavonoid morin from Moraceae induces apoptosis by modulation of Bcl-2 family members and Fas receptor in HCT 116 cells. Int J Oncol 2015; 46(6): 2670-8.
[http://dx.doi.org/10.3892/ijo.2015.2967] [PMID: 25892545]
[192]
Qian C, Wang Y, Zhong Y, et al. Wogonin-enhanced reactive oxygen species-induced apoptosis and potentiated cytotoxic effects of chemotherapeutic agents by suppression Nrf2-mediated signaling in HepG2 cells. Free Radic Res 2014; 48(5): 607-21.
[http://dx.doi.org/10.3109/10715762.2014.897342] [PMID: 24666416]
[193]
Yang X, Li X, An L, Bai B, Chen J. Silibinin induced the apoptosis of Hep-2 cells via oxidative stress and down-regulating survivin expression. Eur Arch Otorhinolaryngol 2013; 270(8): 2289-97.
[http://dx.doi.org/10.1007/s00405-013-2444-x] [PMID: 23580032]
[194]
Liang W, Cui J, Zhang K, et al. Shikonin induces ROS-based mitochondria-mediated apoptosis in colon cancer. Oncotarget 2017; 8(65): 109094-106.
[http://dx.doi.org/10.18632/oncotarget.22618] [PMID: 29312593]
[195]
Wang Y, Luo Q, He X, et al. Emodin induces apoptosis of colon cancer cells via induction of autophagy in a ros-dependent manner. Oncol Res 2018; 26(6): 889-99.
[http://dx.doi.org/10.3727/096504017X15009419625178] [PMID: 28762328]

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