Induction of reactive oxygen species: an emerging approach for cancer therapy

Apoptosis

Volumn 22, Issue 11, 2017, Pages 1321-1335

  Zou, Zhengzhi ^a,b   Chang, Haocai ^a   Li, Haolong ^a   Wang, Songmao ^a  

^a SOUTH CHINA NORMAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

Author keywords

Cancer; Cell death; ROS; Therapy

Indexed keywords

ABEXINOSTAT; AFATINIB; ALKOXYL RADICAL; AXITINIB; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BEVACIZUMAB; BORTEZOMIB; CETUXIMAB; CHLOROQUINE; CISPLATIN; ERLOTINIB; GEFITINIB; HYDROGEN PEROXIDE; HYDROXYL RADICAL; PANOBINOSTAT; PAZOPANIB; PERTUZUMAB; PROTEIN TYROSINE KINASE; RADICAL; REACTIVE OXYGEN METABOLITE; RESVERATROL; ROMIDEPSIN; SINGLET OXYGEN; SORAFENIB; SUNITINIB; SUPEROXIDE; TRASTUZUMAB; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT; ANTINEOPLASTIC AGENT; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MULTIENZYME COMPLEX; PHOTOSENSITIZING AGENT; PROTEIN KINASE B;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AUTOPHAGY; BIOLOGICAL FUNCTIONS; CANCER CELL; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER THERAPY; CELL DEATH; CELL KILLING; CELL METABOLISM; FERROPTOSIS; IONIZING RADIATION; MAMMAL CELL; MITOCHONDRION; MOLECULARLY TARGETED THERAPY; OXIDATIVE STRESS; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVIEW; SIGNAL TRANSDUCTION; AGONISTS; CHEMICALLY INDUCED; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NECROSIS; NEOPLASM; PATHOLOGY; PHOTOCHEMOTHERAPY; PROCEDURES; RADIATION RESPONSE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MITOCHONDRIA; MOLECULAR TARGETED THERAPY; NECROSIS; NEOPLASMS; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; PROTO-ONCOGENE PROTEINS C-AKT; RADIATION, IONIZING; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 85029671217     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-017-1424-9     Document Type: Review

References (136)

1. Trachootham D, Alexandre J, Huang P (2009) Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8:579–591
2. Idelchik M, Begley U, Begley TJ, Melendez JA (2017) Mitochondrial ROS control of cancer. Semin Cancer Biol. doi:10.1016/S1044-579X(17)30098-6
3. Hendrick E, Peixoto P, Blomme A, Polese C, Matheus N, Cimino J et al (2017) Metabolic inhibitors accentuate the anti-tumoral effect of HDAC5 inhibition. Oncogene 36:4859–4874
4. Chen P, Luo X, Nie P, Wu B, Xu W, Shi X et al (2017) CQ synergistically sensitizes human colorectal cancer cells to SN-38/CPT-11 through lysosomal and mitochondrial apoptotic pathway via p53-ROS cross-talk. Free Radic Biol Med 104:280–297
5. Scialo F, Mallikarjun V, Stefanatos R, Sanz A (2013) Regulation of lifespan by the mitochondrial electron transport chain: reactive oxygen species-dependent and reactive oxygen species-independent mechanisms. Antioxid Redox Signal 19:1953–1969
6. Raj L, Ide T, Gurkar AU, Foley M, Schenone M, Li X et al (2011) Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475:231–234
7. Trachootham D, Zhang H, Zhang W, Feng L, Du M, Zhou Y et al (2008) Effective elimination of fludarabine-resistant CLL cells by PEITC through a redox-mediated mechanism. Blood 112:1912–1922
8. Chio I, Tuveson DA (2017) ROS in cancer: the burning question. Trends Mol Med 23:411–429
9. Nakamura S, Nakanishi A, Takazawa M, Okihiro S, Urano S, Fukui K (2016) Ionomycin-induced calcium influx induces neurite degeneration in mouse neuroblastoma cells: analysis of a time-lapse live cell imaging system. Free Radic Res 50:1214–1225
10. Zou ZZ, Nie PP, Li YW, Hou BX, Rui-Li, Shi XP et al (2017) Synergistic induction of apoptosis by salinomycin and gefitinib through lysosomal and mitochondrial dependent pathway overcomes gefitinib resistance in colorectal cancer. Oncotarget 8:22414–22432
11. Dickinson BC, Chang CJ (2011) Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 7:504–511
12. Sumimoto H (2008) Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J 275:3249–3277
13. Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24:R453-R462
14. Jeon SM, Chandel NS, Hay N (2012) AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress. Nature 485:661–665
15. Luo X, Yao J, Nie P, Yang Z, Feng H, Chen P et al (2016) FOXM1 promotes invasion and migration of colorectal cancer cells partially dependent on HSPA5 transactivation. Oncotarget 7:26480–26495
16. Zhang S, Zhao BS, Zhou A, Lin K, Zheng S, Lu Z et al (2017) m6A demethylase ALKBH5 maintains tumorigenicity of glioblastoma stem-like cells by sustaining FOXM1 expression and cell proliferation program. Cancer Cell 31:591–606
17. Park HJ, Carr JR, Wang Z, Nogueira V, Hay N, Tyner AL et al (2009) FoxM1, a critical regulator of oxidative stress during oncogenesis. EMBO J 28:2908–2918
18. Liou GY, Doppler H, DelGiorno KE, Zhang L, Leitges M, Crawford HC et al (2016) Mutant KRas-induced mitochondrial oxidative stress in acinar cells upregulates EGFR signaling to drive formation of pancreatic precancerous lesions. Cell Rep 14:2325–2336
19. Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24:981–990
20. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K et al (2001) ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2:222–228
21. Dhanasekaran DN, Reddy EP (2008) JNK signaling in apoptosis. Oncogene 27:6245–6251
22. Zhang J, Wang X, Vikash V, Ye Q, Wu D, Liu Y et al (2016) ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev 2016:4350965
23. Alexander A, Cai SL, Kim J, Nanez A, Sahin M, MacLean KH et al (2010) ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci USA 107:4153–4158
24. Potter CJ, Pedraza LG, Xu T (2002) Akt regulates growth by directly phosphorylating Tsc2. Nat Cell Biol 4:658–665
25. Ishaq M, Kumar S, Varinli H, Han ZJ, Rider AE, Evans MD et al (2014) Atmospheric gas plasma-induced ROS production activates TNF-ASK1 pathway for the induction of melanoma cancer cell apoptosis. Mol Biol Cell 25:1523–1531
26. Nadeau PJ, Charette SJ, Landry J (2009) REDOX reaction at ASK1-Cys250 is essential for activation of JNK and induction of apoptosis. Mol Biol Cell 20:3628–3637
27. Kim S, Lee TJ, Leem J, Choi KS, Park JW, Kwon TK (2008) Sanguinarine-induced apoptosis: generation of ROS, down-regulation of Bcl-2, c-FLIP, and synergy with TRAIL. J Cell Biochem 104:895–907
28. Wang L, Azad N, Kongkaneramit L, Chen F, Lu Y, Jiang BH et al (2008) The Fas death signaling pathway connecting reactive oxygen species generation and FLICE inhibitory protein down-regulation. J Immunol 180:3072–3080
29. Devadas S, Zaritskaya L, Rhee SG, Oberley L, Williams MS (2002) Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J Exp Med 195:59–70
30. Gulow K, Kaminski M, Darvas K, Suss D, Li-Weber M, Krammer PH (2005) HIV-1 trans-activator of transcription substitutes for oxidative signaling in activation-induced T cell death. J Immunol 174:5249–5260
31. Jin X, Song L, Liu X, Chen M, Li Z, Cheng L et al (2014) Protective efficacy of vitamins C and E on p,p’-DDT-induced cytotoxicity via the ROS-mediated mitochondrial pathway and NF-kappaB/FasL pathway. PLoS ONE 9:e113257
32. Faris M, Latinis KM, Kempiak SJ, Koretzky GA, Nel A (1998) Stress-induced Fas ligand expression in T cells is mediated through a MEK kinase 1-regulated response element in the Fas ligand promoter. Mol Cell Biol 18:5414–5424
33. Liu Y, Borchert GL, Surazynski A, Hu CA, Phang JM (2006) Proline oxidase activates both intrinsic and extrinsic pathways for apoptosis: the role of ROS/superoxides, NFAT and MEK/ERK signaling. Oncogene 25:5640–5647
34. Dewangan J, Tandon D, Srivastava S, Verma AK, Yapuri A, Rath SK (2017) Novel combination of salinomycin and resveratrol synergistically enhances the anti-proliferative and pro-apoptotic effects on human breast cancer cells. Apoptosis. doi:10.1007/s10495-017-1394-y
35. Madesh M, Hajnoczky G (2001) VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J Cell Biol 155:1003–1015
36. Queiroga CS, Almeida AS, Martel C, Brenner C, Alves PM, Vieira HL (2010) Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilization and apoptosis. J Biol Chem 285:17077–17088
37. Zuo Y, Xiang B, Yang J, Sun X, Wang Y, Cang H et al (2009) Oxidative modification of caspase-9 facilitates its activation via disulfide-mediated interaction with Apaf-1. Cell Res 19:449–457
38. Katoh I, Tomimori Y, Ikawa Y, Kurata S (2004) Dimerization and processing of procaspase-9 by redox stress in mitochondria. J Biol Chem 279:15515–15523
39. Luanpitpong S, Chanvorachote P, Stehlik C, Tse W, Callery PS, Wang L et al (2013) Regulation of apoptosis by Bcl-2 cysteine oxidation in human lung epithelial cells. Mol Biol Cell 24:858–869
40. Li D, Ueta E, Kimura T, Yamamoto T, Osaki T (2004) Reactive oxygen species (ROS) control the expression of Bcl-2 family proteins by regulating their phosphorylation and ubiquitination. Cancer Sci 95:644–650
41. Luanpitpong S, Chanvorachote P, Nimmannit U, Leonard SS, Stehlik C, Wang L et al (2012) Mitochondrial superoxide mediates doxorubicin-induced keratinocyte apoptosis through oxidative modification of ERK and Bcl-2 ubiquitination. Biochem Pharmacol 83:1643–1654
42. Zou Z, Yuan Z, Zhang Q, Long Z, Chen J, Tang Z et al (2012) Aurora kinase A inhibition-induced autophagy triggers drug resistance in breast cancer cells. Autophagy 8:1798–1810
43. Zhao Y, Qu T, Wang P, Li X, Qiang J, Xia Z et al (2016) Unravelling the relationship between macroautophagy and mitochondrial ROS in cancer therapy. Apoptosis 21:517–531
44. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB (2008) Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 15:171–182
45. Tripathi DN, Zhang J, Jing J, Dere R, Walker CL (2016) A new role for ATM in selective autophagy of peroxisomes (pexophagy). Autophagy 12:711–712
46. Byun YJ, Kim SK, Kim YM, Chae GT, Jeong SW, Lee SB (2009) Hydrogen peroxide induces autophagic cell death in C6 glioma cells via BNIP3-mediated suppression of the mTOR pathway. Neurosci Lett 461:131–135
47. Pallichankandy S, Rahman A, Thayyullathil F, Galadari S (2015) ROS-dependent activation of autophagy is a critical mechanism for the induction of anti-glioma effect of sanguinarine. Free Radic Biol Med 89:708–720
48. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26:1749–1760
49. Song C, Mitter SK, Qi X, Beli E, Rao HV, Ding J et al (2017) Oxidative stress-mediated NFkappaB phosphorylation upregulates p62/SQSTM1 and promotes retinal pigmented epithelial cell survival through increased autophagy. PLoS ONE 12:e171940
50. Zhang Y, Su SS, Zhao S, Yang Z, Zhong CQ, Chen X et al (2017) RIP1 autophosphorylation is promoted by mitochondrial ROS and is essential for RIP3 recruitment into necrosome. Nat Commun 8:14329
51. Sun W, Wu X, Gao H, Yu J, Zhao W, Lu JJ et al (2017) Cytosolic calcium mediates RIP1/RIP3 complex-dependent necroptosis through JNK activation and mitochondrial ROS production in human colon cancer cells. Free Radic Biol Med 108:433–444
52. Zhou Z, Lu B, Wang C, Wang Z, Luo T, Piao M et al (2017) RIP1 and RIP3 contribute to shikonin-induced DNA double-strand breaks in glioma cells via increase of intracellular reactive oxygen species. Cancer Lett 390:77–90
53. Chauhan AK, Min KJ, Kwon TK (2017) RIP1-dependent reactive oxygen species production executes artesunate-induced cell death in renal carcinoma Caki cells. Mol Cell Biochem. doi:10.1007/s11010-017-3052-7
54. Dixon SJ, Stockwell BR (2014) The role of iron and reactive oxygen species in cell death. Nat Chem Biol 10:9–17
55. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC et al (2009) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325:332–336
56. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE et al (2012) Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149:1060–1072
57. Viswanathan VS, Ryan MJ, Dhruv HD, Gill S, Eichhoff OM, Seashore-Ludlow B et al (2017) Dependency of a therapy-resistant state of cancer cells on a lipid peroxidase pathway. Nature 547:453–457
58. Yang WS, SriRamaratnam R, Welsch ME, Shimada K, Skouta R, Viswanathan VS et al (2014) Regulation of ferroptotic cancer cell death by GPX4. Cell 156:317–331
59. Gao M, Monian P, Quadri N, Ramasamy R, Jiang X (2015) Glutaminolysis and transferrin regulate ferroptosis. Mol Cell 59:298–308
60. Liu L, Wei Y, Zhai S, Chen Q, Xing D (2015) Dihydroartemisinin and transferrin dual-dressed nano-graphene oxide for a pH-triggered chemotherapy. Biomaterials 62:35–46
61. Roh JL, Kim EH, Jang H, Shin D (2017) Nrf2 inhibition reverses the resistance of cisplatin-resistant head and neck cancer cells to artesunate-induced ferroptosis. Redox Biol 11:254–262
62. Mi YJ, Geng GJ, Zou ZZ, Gao J, Luo XY, Liu Y et al (2015) Dihydroartemisinin inhibits glucose uptake and cooperates with glycolysis inhibitor to induce apoptosis in non-small cell lung carcinoma cells. PLoS ONE 10:e120426
63. Hamai A, Caneque T, Muller S, Mai TT, Hienzsch A, Ginestier C et al (2017) An iron hand over cancer stem cells. Autophagy 13:1465–1466
64. Guo J, Xu B, Han Q, Zhou H, Xia Y, Gong C et al (2017) Ferroptosis: a novel anti-tumor action for cisplatin. Cancer Res Treat. doi:10.4143/crt.2016.572
65. Yang Y, Guo R, Tian X, Zhang Z, Zhang P, Li C et al (2017) Synergistic anti-tumor activity of Nimotuzumab in combination with Trastuzumab in HER2-positive breast cancer. Biochem Biophys Res Commun 489:523–527
66. Santoro V, Jia R, Thompson H, Nijhuis A, Jeffery R, Kiakos K et al (2016) Role of reactive oxygen species in the abrogation of oxaliplatin activity by cetuximab in colorectal cancer. J Natl Cancer Inst 108:v394
67. Cao S, Xia M, Mao Y, Zhang Q, Donkor PO, Qiu F et al (2016) Combined oridonin with cetuximab treatment shows synergistic anticancer effects on laryngeal squamous cell carcinoma: involvement of inhibition of EGFR and activation of reactive oxygen species-mediated JNK pathway. Int J Oncol 49:2075–2087
68. Fack F, Espedal H, Keunen O, Golebiewska A, Obad N, Harter PN et al (2015) Bevacizumab treatment induces metabolic adaptation toward anaerobic metabolism in glioblastomas. Acta Neuropathol 129:115–131
69. Guo XL, Li D, Sun K, Wang J, Liu Y, Song JR et al (2013) Inhibition of autophagy enhances anticancer effects of bevacizumab in hepatocarcinoma. J Mol Med (Berl) 91:473–483
70. Gautam J, Ku JM, Regmi SC, Jeong H, Wang Y, Banskota S et al (2017) Dual inhibition of NOX2 and receptor tyrosine kinase by BJ-1301 enhances anticancer therapy efficacy via suppression of autocrine stimulatory factors in lung cancer. Mol Cancer Ther. doi:10.1158/1535-7163
71. Abdel-Aziz AK, Shouman S, El-Demerdash E, Elgendy M, Abdel-Naim AB (2014) Chloroquine synergizes sunitinib cytotoxicity via modulating autophagic, apoptotic and angiogenic machineries. Chem Biol Interact 217:28–40
72. Leone A, Roca MS, Ciardiello C, Terranova-Barberio M, Vitagliano C, Ciliberto G et al (2015) Vorinostat synergizes with EGFR inhibitors in NSCLC cells by increasing ROS via up-regulation of the major mitochondrial porin VDAC1 and modulation of the c-Myc-NRF2-KEAP1 pathway. Free Radic Biol Med 89:287–299
73. Okon IS, Coughlan KA, Zhang M, Wang Q, Zou MH (2015) Gefitinib-mediated reactive oxygen specie (ROS) instigates mitochondrial dysfunction and drug resistance in lung cancer cells. J Biol Chem 290:9101–9110
74. Shan F, Shao Z, Jiang S, Cheng Z (2016) Erlotinib induces the human non-small-cell lung cancer cells apoptosis via activating ROS-dependent JNK pathways. Cancer Med 5:3166–3175
75. Orcutt KP, Parsons AD, Sibenaller ZA, Scarbrough PM, Zhu Y, Sobhakumari A et al (2011) Erlotinib-mediated inhibition of EGFR signaling induces metabolic oxidative stress through NOX4. Cancer Res 71:3932–3940
76. Nie P, Hu W, Zhang T, Yang Y, Hou B, Zou Z (2015) Synergistic induction of Erlotinib-mediated apoptosis by resveratrol in human non-small-cell lung cancer cells by down-regulating survivin and up-regulating PUMA. Cell Physiol Biochem 35:2255–2271
77. Wardman P (2007) Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic Biol Med 43:995–1022
78. Bonini MG, Siraki AG, Atanassov BS, Mason RP (2007) Immunolocalization of hypochlorite-induced, catalase-bound free radical formation in mouse hepatocytes. Free Radic Biol Med 42:530–540
79. Hui KF, Lam BH, Ho DN, Tsao SW, Chiang AK (2013) Bortezomib and SAHA synergistically induce ROS-driven caspase-dependent apoptosis of nasopharyngeal carcinoma and block replication of Epstein-Barr virus. Mol Cancer Ther 12:747–758
80. Yin L, Kufe T, Avigan D, Kufe D (2014) Targeting MUC1-C is synergistic with bortezomib in downregulating TIGAR and inducing ROS-mediated myeloma cell death. Blood 123:2997–3006
81. Xian M, Cao H, Cao J, Shao X, Zhu D, Zhang N et al (2017) Bortezomib sensitizes human osteosarcoma cells to adriamycin-induced apoptosis through ROS-dependent activation of p-eIF2alpha/ATF4/CHOP axis. Int J Cancer 141:1029–1041
82. Fan WH, Hou Y, Meng FK, Wang XF, Luo YN, Ge PF (2011) Proteasome inhibitor MG-132 induces C6 glioma cell apoptosis via oxidative stress. Acta Pharmacol Sin 32:619–625
83. Park S, Park JA, Yoo H, Park HB, Lee Y (2017) Proteasome inhibitor-induced cleavage of HSP90 is mediated by ROS generation and caspase 10-activation in human leukemic cells. Redox Biol 13:470–476
84. Bhalla S, Balasubramanian S, David K, Sirisawad M, Buggy J, Mauro L et al (2009) PCI-24781 induces caspase and reactive oxygen species-dependent apoptosis through NF-kappaB mechanisms and is synergistic with bortezomib in lymphoma cells. Clin Cancer Res 15:3354–3365
85. Sholler GS, Currier EA, Dutta A, Slavik MA, Illenye SA, Mendonca MC et al (2013) PCI-24781 (abexinostat), a novel histone deacetylase inhibitor, induces reactive oxygen species-dependent apoptosis and is synergistic with bortezomib in neuroblastoma. J Cancer Ther Res 2:21
86. Cornago M, Garcia-Alberich C, Blasco-Angulo N, Vall-Llaura N, Nager M, Herreros J et al (2014) Histone deacetylase inhibitors promote glioma cell death by G2 checkpoint abrogation leading to mitotic catastrophe. Cell Death Dis 5:e1435
87. Karthik S, Sankar R, Varunkumar K, Anusha C, Ravikumar V (2015) Blocking NF-kappaB sensitizes non-small cell lung cancer cells to histone deacetylase inhibitor induced extrinsic apoptosis through generation of reactive oxygen species. Biomed Pharmacother 69:337–344
88. Hedrick E, Crose L, Linardic CM, Safe S (2015) Histone deacetylase inhibitors inhibit rhabdomyosarcoma by reactive oxygen species-dependent targeting of specificity protein transcription factors. Mol Cancer Ther 14:2143–2153
89. Miao Z, Yu F, Ren Y, Yang J (2017) d, l-Sulforaphane induces ROS-dependent apoptosis in human gliomablastoma cells by inactivating STAT3 signaling pathway. Int J Mol Sci 18
90. Hu Y, Zhao C, Zheng H, Lu K, Shi D, Liu Z et al (2017) A novel STAT3 inhibitor HO-3867 induces cell apoptosis by reactive oxygen species-dependent endoplasmic reticulum stress in human pancreatic cancer cells. Anticancer Drugs 28:392–400
91. Shackelford DB, Shaw RJ (2009) The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer 9:563–575
92. Wu S, Xing D (2012) Mechanism of mitochondrial membrane permeabilization during apoptosis under photofrin-mediated photodynamic therapy. J Xray Sci Technol 20:363–372
93. van Straten D, Mashayekhi V, de Bruijn HS, Oliveira S, Robinson DJ (2017) Oncologic photodynamic therapy: basic principles, current clinical status and future directions. Cancers (Basel) 9(2):E19
94. Gdovin MJ, Kadri N, Rios L, Holliday S, Jordan Z (2017) Focal photodynamic intracellular acidification as a cancer therapeutic. Semin Cancer Biol 43:147–156
95. Garg AD, Dudek AM, Ferreira GB, Verfaillie T, Vandenabeele P, Krysko DV et al (2013) ROS-induced autophagy in cancer cells assists in evasion from determinants of immunogenic cell death. Autophagy 9:1292–1307
96. Wei Y, Song J, Chen Q, Xing D (2012) Enhancement of photodynamic antitumor effect with pro-oxidant ascorbate. Lasers Surg Med 44:69–75
97. McHale AP, Callan JF, Nomikou N, Fowley C, Callan B (2016) Sonodynamic therapy: concept, mechanism and application to cancer treatment. Adv Exp Med Biol 880:429–450
98. Trendowski M (2014) The promise of sonodynamic therapy. Cancer Metastasis Rev 33:143–160
99. Misik V, Riesz P (2000) Free radical intermediates in sonodynamic therapy. Ann N Y Acad Sci 899:335–348
100. Trendowski M (2015) Using the promise of sonodynamic therapy in the clinical setting against disseminated cancers. Chemother Res Pract 2015:316015
101. Chen H, Gao W, Yang Y, Guo S, Wang H, Wang W et al (2014) Inhibition of VDAC1 prevents Ca(2)(+)-mediated oxidative stress and apoptosis induced by 5-aminolevulinic acid mediated sonodynamic therapy in THP-1 macrophages. Apoptosis 19:1712–1726
102. Wang H, Yang Y, Chen H, Dan J, Cheng J, Guo S et al (2014) The predominant pathway of apoptosis in THP-1 macrophage-derived foam cells induced by 5-aminolevulinic acid-mediated sonodynamic therapy is the mitochondria-caspase pathway despite the participation of endoplasmic reticulum stress. Cell Physiol Biochem 33:1789–1801
103. Wang S, Hu Z, Wang X, Gu C, Gao Z, Cao W et al (2014) 5-Aminolevulinic acid-mediated sonodynamic therapy reverses macrophage and dendritic cell passivity in murine melanoma xenografts. Ultrasound Med Biol 40:2125–2133
104. Sena LA, Li S, Jairaman A, Prakriya M, Ezponda T, Hildeman DA et al (2013) Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38:225–236
105. + T cell function. J Immunol 177:852–862
106. + T cells during primary but not secondary viral infection. J Virol 78:11246–11257
107. Chaudhri G, Clark IA, Hunt NH, Cowden WB, Ceredig R (1986) Effect of antioxidants on primary alloantigen-induced T cell activation and proliferation. J Immunol 137:2646–2652
108. Schwindling C, Quintana A, Krause E, Hoth M (2010) Mitochondria positioning controls local calcium influx in T cells. J Immunol 184:184–190
109. Hehner SP, Breitkreutz R, Shubinsky G, Unsoeld H, Schulze-Osthoff K, Schmitz ML et al (2000) Enhancement of T cell receptor signaling by a mild oxidative shift in the intracellular thiol pool. J Immunol 165:4319–4328
110. + T cells. Antioxid Redox Signal 20:1533–1547
111. Tkachev V, Goodell S, Opipari AW, Hao LY, Franchi L, Glick GD et al (2015) Programmed death-1 controls T cell survival by regulating oxidative metabolism. J Immunol 194:5789–5800
112. Lysechko TL, Cheung SM, Ostergaard HL (2010) Regulation of the tyrosine kinase Pyk2 by calcium is through production of reactive oxygen species in cytotoxic T lymphocytes. J Biol Chem 285:31174–31184
113. Aguilo JI, Anel A, Catalan E, Sebastian A, Acin-Perez R, Naval J et al (2010) Granzyme B of cytotoxic T cells induces extramitochondrial reactive oxygen species production via caspase-dependent NADPH oxidase activation. Immunol Cell Biol 88:545–554
114. Murphy MP, Siegel RM (2013) Mitochondrial ROS fire up T cell activation. Immunity 38:201–202
115. Gelderman KA, Hultqvist M, Holmberg J, Olofsson P, Holmdahl R (2006) T cell surface redox levels determine T cell reactivity and arthritis susceptibility. Proc Natl Acad Sci U S A 103:12831–12836
116. Cemerski S, Cantagrel A, Van Meerwijk JP, Romagnoli P (2002) Reactive oxygen species differentially affect T cell receptor-signaling pathways. J Biol Chem 277:19585–19593
117. + effector T cells. PLoS One 6:e16013
118. Kraaij MD, Koekkoek KM, van der Kooij SW, Gelderman KA, van Kooten C (2013) Subsets of human type 2 macrophages show differential capacity to produce reactive oxygen species. Cell Immunol 284:1–8
119. Wei J, Zhang M, Zhou J (2015) Myeloid-derived suppressor cells in major depression patients suppress T cell responses through the production of reactive oxygen species. Psychiatry Res 228:695–701
120. + T cell tolerance in cancer. Nat Med 13:828–835
121. Wang Q, Hu B, Hu X, Kim H, Squatrito M, Scarpace L et al (2017) Tumor evolution of glioma-intrinsic gene expression subtypes associates with immunological changes in the microenvironment. Cancer Cell 32:42–56
122. Shan M, Qin J, Jin F, Han X, Guan H, Li X et al (2017) Autophagy suppresses isoprenaline-induced M2 macrophage polarization via the ROS/ERK and mTOR signaling pathway. Free Radic Biol Med 110:432–443
123. Magda D, Miller RA (2006) Motexafin gadolinium: a novel redox active drug for cancer therapy. Semin Cancer Biol 16:466–476
124. Ray T, Chakrabarti MK, Pal A (2016) Hemagglutinin protease secreted by V. cholerae induced apoptosis in breast cancer cells by ROS mediated intrinsic pathway and regresses tumor growth in mice model. Apoptosis 21:143–154
125. Pluchino LA, Choudhary S, Wang HC (2016) Reactive oxygen species-mediated synergistic and preferential induction of cell death and reduction of clonogenic resistance in breast cancer cells by combined cisplatin and FK228. Cancer Lett 381:124–132
126. Ao X, Nie P, Wu B, Xu W, Zhang T, Wang S et al (2016) Decreased expression of microRNA-17 and microRNA-20b promotes breast cancer resistance to taxol therapy by upregulation of NCOA3. Cell Death Dis 7:e2463
127. Zhu J, Zou Z, Nie P, Kou X, Wu B, Wang S et al (2016) Downregulation of microRNA-27b-3p enhances tamoxifen resistance in breast cancer by increasing NR5A2 and CREB1 expression. Cell Death Dis 7:e2454
128. Zhang LH, Yang AJ, Wang M, Liu W, Wang CY, Xie XF et al (2016) Enhanced autophagy reveals vulnerability of P-gp mediated epirubicin resistance in triple negative breast cancer cells. Apoptosis 21:473–488
129. Ledoux S, Yang R, Friedlander G, Laouari D (2003) Glucose depletion enhances P-glycoprotein expression in hepatoma cells: role of endoplasmic reticulum stress response. Cancer Res 63:7284–7290
130. Terada Y, Ogura J, Tsujimoto T, Kuwayama K, Koizumi T, Sasaki S et al (2014) Intestinal P-glycoprotein expression is multimodally regulated by intestinal ischemia-reperfusion. J Pharm Pharm Sci 17:266–276
131. Li L, Xu J, Min T, Huang W (2006) Up-regulation of P-glycoprotein expression by catalase via JNK activation in HepG2 cells. Redox Rep 11:173–178
132. Pandey V, Chaube B, Bhat MK (2011) Hyperglycemia regulates MDR-1, drug accumulation and ROS levels causing increased toxicity of carboplatin and 5-fluorouracil in MCF-7 cells. J Cell Biochem 112:2942–2952
133. Dayal R, Singh A, Pandey A, Mishra KP (2014) Reactive oxygen species as mediator of tumor radiosensitivity. J Cancer Res Ther 10:811–818
134. Yu S, Wang L, Cao Z, Gong D, Liang Q, Chen H et al (2017) Anticancer effect of Polyphyllin Iota in colorectal cancer cells through ROS-dependent autophagy and G2/M arrest mechanisms. Nat Prod Res 16:1–4
135. Sun M, Pan D, Chen Y, Li Y, Gao K, Hu B (2017) Coroglaucigenin enhances the radiosensitivity of human lung cancer cells through Nrf2/ROS pathway. Oncotarget 8:32807–32820
136. Zhang G, Wang W, Yao C, Ren J, Zhang S, Han M (2017) Salinomycin overcomes radioresistance in nasopharyngeal carcinoma cells by inhibiting Nrf2 level and promoting ROS generation. Biomed Pharmacother 91:147–154