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Published in: Tumor Biology 4/2016

01-04-2016 | Review

The role of oxidative stress on breast cancer development and therapy

Authors: Fabio Hecht, Carolina F. Pessoa, Luciana B. Gentile, Doris Rosenthal, Denise P. Carvalho, Rodrigo S. Fortunato

Published in: Tumor Biology | Issue 4/2016

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Abstract

Reactive oxygen species (ROS) are produced by both enzymatic and non-enzymatic systems within eukaryotic cells and play important roles in cellular physiology and pathophysiology. Although physiological concentrations are crucial for ensuring cell survival, ROS overproduction is detrimental to cells, and considered key-factors for the development of several diseases, such as neurodegenerative diseases, cardiovascular disorders, and cancer. Cancer cells are usually submitted to higher ROS levels that further stimulate malignant phenotype through stimulus to sustained proliferation, death evasion, angiogenesis, invasiveness, and metastasis. The role of ROS on breast cancer etiology and progression is being progressively elucidated. However, less attention has been given to the development of redox system-targeted strategies for breast cancer therapy. In this review, we address the basic mechanisms of ROS production and scavenging in breast tumor cells, and the emerging possibilities of breast cancer therapies targeting ROS homeostasis.
Literature
1.
go back to reference Jones DP. Radical-free biology of oxidative stress. Am J Physiol Cell Physiol. 2008;4:C849–68.CrossRef Jones DP. Radical-free biology of oxidative stress. Am J Physiol Cell Physiol. 2008;4:C849–68.CrossRef
2.
go back to reference Halliwell B, Gutteridge J. Free radicals in biology and medicine. 4th ed. Oxford University Press; 2007. Halliwell B, Gutteridge J. Free radicals in biology and medicine. 4th ed. Oxford University Press; 2007.
3.
go back to reference Liochev SI. Reactive oxygen species and the free radical theory of aging. Free Radic Biol Med. 2013;60:1–4.CrossRefPubMed Liochev SI. Reactive oxygen species and the free radical theory of aging. Free Radic Biol Med. 2013;60:1–4.CrossRefPubMed
4.
go back to reference Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39:44–84.CrossRefPubMed Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39:44–84.CrossRefPubMed
5.
go back to reference Sosa V, Moliné T, Somoza R, Paciucci R, Kondoh H, LLeonart ME. Oxidative stress and cancer: an overview. Ageing Res Rev. 2013;12:376–90.CrossRefPubMed Sosa V, Moliné T, Somoza R, Paciucci R, Kondoh H, LLeonart ME. Oxidative stress and cancer: an overview. Ageing Res Rev. 2013;12:376–90.CrossRefPubMed
6.
go back to reference Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov. 2013;12:931–47.CrossRefPubMed Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov. 2013;12:931–47.CrossRefPubMed
7.
go back to reference Federico A, Morgillo F, Tuccillo C, Ciardiello F, Loguercio C. Chronic inflammation and oxidative stress in human carcinogenesis. Int J Cancer J Int Du Cancer. 2007;121:2381–6.CrossRef Federico A, Morgillo F, Tuccillo C, Ciardiello F, Loguercio C. Chronic inflammation and oxidative stress in human carcinogenesis. Int J Cancer J Int Du Cancer. 2007;121:2381–6.CrossRef
11.
go back to reference Nohl H, Gille L, Kozlov A, Staniek K. Are mitochondria a spontaneous and permanent source of reactive oxygen species? Redox Rep : Commun Free Radic Res. 2003;8:135–41.CrossRef Nohl H, Gille L, Kozlov A, Staniek K. Are mitochondria a spontaneous and permanent source of reactive oxygen species? Redox Rep : Commun Free Radic Res. 2003;8:135–41.CrossRef
12.
go back to reference Meng T, Lou Y, Chen Y, Hsu S, Huang Y. Cys-oxidation of protein tyrosine phosphatases: its role in regulation of signal transduction and its involvement in human cancers. J Cancer Mol. 2006;2:9–16. Meng T, Lou Y, Chen Y, Hsu S, Huang Y. Cys-oxidation of protein tyrosine phosphatases: its role in regulation of signal transduction and its involvement in human cancers. J Cancer Mol. 2006;2:9–16.
13.
go back to reference Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact. 2006;160:1–40.CrossRefPubMed Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact. 2006;160:1–40.CrossRefPubMed
14.
go back to reference Wood ZA, Schröder E, Harris JR, Poole LB. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci. 2003;28:32–40.CrossRefPubMed Wood ZA, Schröder E, Harris JR, Poole LB. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci. 2003;28:32–40.CrossRefPubMed
15.
go back to reference Lambeth JD, Neish AS. Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited. Annu Rev Pathol. 2014;9:119–45.CrossRefPubMed Lambeth JD, Neish AS. Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited. Annu Rev Pathol. 2014;9:119–45.CrossRefPubMed
16.
17.
go back to reference Weitzman SA, Gordon LI. Inflammation and cancer: role of phagocyte-generated oxidants in carcinogenesis. Blood. 1990;76:655–63.PubMed Weitzman SA, Gordon LI. Inflammation and cancer: role of phagocyte-generated oxidants in carcinogenesis. Blood. 1990;76:655–63.PubMed
18.
19.
go back to reference Cooke MS, Evans MD, Dizdaroglu M, Lunec J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 2003;17:1195–214.CrossRefPubMed Cooke MS, Evans MD, Dizdaroglu M, Lunec J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 2003;17:1195–214.CrossRefPubMed
21.
go back to reference Ameziane-El-Hassani R, Boufraqech M, Lagente-Chevallier O, Weyemi U, Talbot M, Métivier D, et al. Role of H2O2 in RET/PTC1 chromosomal rearrangement produced by ionizing radiation in human thyroid cells. Cancer Res. 2010;70:4123–32.CrossRefPubMed Ameziane-El-Hassani R, Boufraqech M, Lagente-Chevallier O, Weyemi U, Talbot M, Métivier D, et al. Role of H2O2 in RET/PTC1 chromosomal rearrangement produced by ionizing radiation in human thyroid cells. Cancer Res. 2010;70:4123–32.CrossRefPubMed
22.
go back to reference Stone JR, Yang S. Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal. 2006;8:243–70.CrossRefPubMed Stone JR, Yang S. Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal. 2006;8:243–70.CrossRefPubMed
23.
go back to reference Gao N, Jiang BH, Leonard SS, Corum L, Zhang Z, Roberts JR, et al. p38 signaling-mediated hypoxia-inducible factor 1alpha and vascular endothelial growth factor induction by Cr(VI) in DU145 human prostate carcinoma cells. J Biol Chem. 2002;277:45041–8.CrossRefPubMed Gao N, Jiang BH, Leonard SS, Corum L, Zhang Z, Roberts JR, et al. p38 signaling-mediated hypoxia-inducible factor 1alpha and vascular endothelial growth factor induction by Cr(VI) in DU145 human prostate carcinoma cells. J Biol Chem. 2002;277:45041–8.CrossRefPubMed
24.
go back to reference Bae GU, Seo DW, Kwon HK, Lee HY, Hong S, Lee ZW, et al. Hydrogen peroxide activates p70S6k signaling pathway. J Biol Chem. 1999;274:32596–602.CrossRefPubMed Bae GU, Seo DW, Kwon HK, Lee HY, Hong S, Lee ZW, et al. Hydrogen peroxide activates p70S6k signaling pathway. J Biol Chem. 1999;274:32596–602.CrossRefPubMed
25.
go back to reference Natarajan V, Taher MM, Roehm B, Parinandi NL, Schmid HH, Kiss Z, et al. Activation of endothelial cell phospholipase D by hydrogen peroxide and fatty acid hydroperoxide. J Biol Chem. 1993;268:930–7.PubMed Natarajan V, Taher MM, Roehm B, Parinandi NL, Schmid HH, Kiss Z, et al. Activation of endothelial cell phospholipase D by hydrogen peroxide and fatty acid hydroperoxide. J Biol Chem. 1993;268:930–7.PubMed
26.
go back to reference Simon AR, Rai U, Fanburg BL, Cochran BH. Activation of the JAK-STAT pathway by reactive oxygen species. Am J Physiol. 1998;275:C1640–52.PubMed Simon AR, Rai U, Fanburg BL, Cochran BH. Activation of the JAK-STAT pathway by reactive oxygen species. Am J Physiol. 1998;275:C1640–52.PubMed
27.
28.
29.
go back to reference Gebremedhin D, Terashvili M, Wickramasekera N, Zhang DX, Rau N, Miura H, et al. Redox signaling via oxidative inactivation of PTEN modulates pressure-dependent myogenic tone in rat middle cerebral arteries. PLoS One. 2013;8:e68498.CrossRefPubMedPubMedCentral Gebremedhin D, Terashvili M, Wickramasekera N, Zhang DX, Rau N, Miura H, et al. Redox signaling via oxidative inactivation of PTEN modulates pressure-dependent myogenic tone in rat middle cerebral arteries. PLoS One. 2013;8:e68498.CrossRefPubMedPubMedCentral
30.
go back to reference Kwon J, Lee SR, Yang KS, Ahn Y, Kim YJ, Stadtman ER, et al. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci U S A. 2004;101:16419–24.CrossRefPubMedPubMedCentral Kwon J, Lee SR, Yang KS, Ahn Y, Kim YJ, Stadtman ER, et al. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci U S A. 2004;101:16419–24.CrossRefPubMedPubMedCentral
31.
go back to reference Niecknig H, Tug S, Reyes BD, Kirsch M, Fandrey J, Berchner-Pfannschmidt U. Role of reactive oxygen species in the regulation of HIF-1 by prolyl hydroxylase 2 under mild hypoxia. Free Radic Res. 2012;46:705–17.CrossRefPubMed Niecknig H, Tug S, Reyes BD, Kirsch M, Fandrey J, Berchner-Pfannschmidt U. Role of reactive oxygen species in the regulation of HIF-1 by prolyl hydroxylase 2 under mild hypoxia. Free Radic Res. 2012;46:705–17.CrossRefPubMed
32.
go back to reference Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez M, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000;275:25130–8.CrossRefPubMed Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez M, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000;275:25130–8.CrossRefPubMed
33.
go back to reference Comito G, Calvani M, Giannoni E, Bianchini F, Calorini L, Torre E, et al. HIF-1α stabilization by mitochondrial ROS promotes Met-dependent invasive growth and vasculogenic mimicry in melanoma cells. Free Radic Biol Med. 2011;51:893–904.CrossRefPubMed Comito G, Calvani M, Giannoni E, Bianchini F, Calorini L, Torre E, et al. HIF-1α stabilization by mitochondrial ROS promotes Met-dependent invasive growth and vasculogenic mimicry in melanoma cells. Free Radic Biol Med. 2011;51:893–904.CrossRefPubMed
34.
go back to reference Arbiser JL, Petros J, Klafter R, Govindajaran B, McLaughlin ER, Brown LF, et al. Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc Natl Acad Sci U S A. 2002;99:715–20.CrossRefPubMedPubMedCentral Arbiser JL, Petros J, Klafter R, Govindajaran B, McLaughlin ER, Brown LF, et al. Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc Natl Acad Sci U S A. 2002;99:715–20.CrossRefPubMedPubMedCentral
35.
go back to reference Coso S, Harrison I, Harrison CB, Vinh A, Sobey CG, Drummond GR, et al. NADPH oxidases as regulators of tumor angiogenesis: current and emerging concepts. Antioxid Redox Signal. 2012;16:1229–47.CrossRefPubMed Coso S, Harrison I, Harrison CB, Vinh A, Sobey CG, Drummond GR, et al. NADPH oxidases as regulators of tumor angiogenesis: current and emerging concepts. Antioxid Redox Signal. 2012;16:1229–47.CrossRefPubMed
36.
37.
go back to reference Musarrat J, Arezina-Wilson J, Wani AA. Prognostic and aetiological relevance of 8-hydroxyguanosine in human breast carcinogenesis. Eur J Cancer. 1996;32A:1209–14.CrossRefPubMed Musarrat J, Arezina-Wilson J, Wani AA. Prognostic and aetiological relevance of 8-hydroxyguanosine in human breast carcinogenesis. Eur J Cancer. 1996;32A:1209–14.CrossRefPubMed
38.
go back to reference Okoh V, Deoraj A, Roy D. Estrogen-induced reactive oxygen species-mediated signalings contribute to breast cancer. Biochim Biophys Acta. 1815;2011:115–33. Okoh V, Deoraj A, Roy D. Estrogen-induced reactive oxygen species-mediated signalings contribute to breast cancer. Biochim Biophys Acta. 1815;2011:115–33.
39.
go back to reference Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D. Estrogens as endogenous genotoxic agents--DNA adducts and mutations. J Natl Cancer Inst Monogr. 2000;27:75–93.CrossRef Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D. Estrogens as endogenous genotoxic agents--DNA adducts and mutations. J Natl Cancer Inst Monogr. 2000;27:75–93.CrossRef
41.
go back to reference Li Y, Meeran SM, Patel SN, Chen H, Hardy TM, Tollefsbol TO. Epigenetic reactivation of estrogen receptor-a (ERa) by genistein enhances hormonal therapy sensitivity in ERa-negative breast cancer. Mol Cancer. 2013;12:9.CrossRefPubMedPubMedCentral Li Y, Meeran SM, Patel SN, Chen H, Hardy TM, Tollefsbol TO. Epigenetic reactivation of estrogen receptor-a (ERa) by genistein enhances hormonal therapy sensitivity in ERa-negative breast cancer. Mol Cancer. 2013;12:9.CrossRefPubMedPubMedCentral
42.
go back to reference Mahalingaiah PK, Ponnusamy L, Singh KP. Chronic oxidative stress causes estrogen-independent aggressive phenotype, and epigenetic inactivation of estrogen receptor alpha in MCF-7 breast cancer cells. Breast Cancer Res Treat. 2015;153(1):41–56.CrossRefPubMed Mahalingaiah PK, Ponnusamy L, Singh KP. Chronic oxidative stress causes estrogen-independent aggressive phenotype, and epigenetic inactivation of estrogen receptor alpha in MCF-7 breast cancer cells. Breast Cancer Res Treat. 2015;153(1):41–56.CrossRefPubMed
43.
go back to reference Weydert CJ, Waugh TA, Ritchie JM, Iyer KS, Smith JL, Li L, et al. Overexpression of manganese or copper-zinc superoxide dismutase inhibits breast cancer growth. Free Radic Biol Med. 2006;41:226–37.CrossRefPubMed Weydert CJ, Waugh TA, Ritchie JM, Iyer KS, Smith JL, Li L, et al. Overexpression of manganese or copper-zinc superoxide dismutase inhibits breast cancer growth. Free Radic Biol Med. 2006;41:226–37.CrossRefPubMed
44.
go back to reference Hitchler MJ, Wikainapakul K, Yu L, Powers K, Attatippaholkun W, Domann FE. Epigenetic regulation of manganese superoxide dismutase expression in human breast cancer cells. Epigenetics: Off J DNA Methylation Soc. 2006;1:163–71.CrossRef Hitchler MJ, Wikainapakul K, Yu L, Powers K, Attatippaholkun W, Domann FE. Epigenetic regulation of manganese superoxide dismutase expression in human breast cancer cells. Epigenetics: Off J DNA Methylation Soc. 2006;1:163–71.CrossRef
45.
go back to reference Yuzefovych LV, Kahn AG, Schuler MA, Eide L, Arora R, Wilson GL, et al. Mitochondrial DNA repair through OGG1 activity attenuates breast cancer progression and metastasis. Cancer Res. 2016;76(1):30–4.CrossRefPubMed Yuzefovych LV, Kahn AG, Schuler MA, Eide L, Arora R, Wilson GL, et al. Mitochondrial DNA repair through OGG1 activity attenuates breast cancer progression and metastasis. Cancer Res. 2016;76(1):30–4.CrossRefPubMed
47.
go back to reference Lim JC, You Z, Kim G, Levine RL. Methionine sulfoxide reductase A is a stereospecific methionine oxidase. Proc Natl Acad Sci U S A. 2011;108:10472–7.CrossRefPubMedPubMedCentral Lim JC, You Z, Kim G, Levine RL. Methionine sulfoxide reductase A is a stereospecific methionine oxidase. Proc Natl Acad Sci U S A. 2011;108:10472–7.CrossRefPubMedPubMedCentral
48.
go back to reference Harris IS, Treloar AE, Inoue S, Sasaki M, Gorrini C, Lee KC, et al. Glutathione and thioredoxin antioxidant pathways synergize to drive cancer initiation and progression. Cancer Cell. 2015;27(2):211–22.CrossRefPubMed Harris IS, Treloar AE, Inoue S, Sasaki M, Gorrini C, Lee KC, et al. Glutathione and thioredoxin antioxidant pathways synergize to drive cancer initiation and progression. Cancer Cell. 2015;27(2):211–22.CrossRefPubMed
49.
go back to reference Moon EJ, Giaccia A. Dual roles of NRF2 in tumor prevention and progression: possible implications in cancer treatment. Free Radic Biol Med. 2015;79:292–9.CrossRefPubMed Moon EJ, Giaccia A. Dual roles of NRF2 in tumor prevention and progression: possible implications in cancer treatment. Free Radic Biol Med. 2015;79:292–9.CrossRefPubMed
50.
go back to reference Onodera Y, Motohashi H, Takagi K, Miki Y, Shibahara Y, Watanabe M, et al. NRF2 immunolocalization in human breast cancer patients as a prognostic factor. Endocr Relat Cancer. 2014;27:241–52.CrossRef Onodera Y, Motohashi H, Takagi K, Miki Y, Shibahara Y, Watanabe M, et al. NRF2 immunolocalization in human breast cancer patients as a prognostic factor. Endocr Relat Cancer. 2014;27:241–52.CrossRef
51.
go back to reference Zhong Y, Zhang F, Sun Z, Zhou W, Li ZY, You QD, et al. Drug resistance associates with activation of Nrf2 in MCF-7/DOX cells, and wogonin reverses it by down-regulating Nrf2-mediated cellular defense response. Mol Carcinog. 2013;52:824–34.CrossRefPubMed Zhong Y, Zhang F, Sun Z, Zhou W, Li ZY, You QD, et al. Drug resistance associates with activation of Nrf2 in MCF-7/DOX cells, and wogonin reverses it by down-regulating Nrf2-mediated cellular defense response. Mol Carcinog. 2013;52:824–34.CrossRefPubMed
52.
go back to reference Kim SK, Yang JW, Kim MR, Roh SH, Kim HG, Lee KY, et al. Increased expression of Nrf2/ARE-dependent anti-oxidant proteins in tamoxifen-resistant breast cancer cells. Free Radic Biol Med. 2008;45:537–46.CrossRefPubMed Kim SK, Yang JW, Kim MR, Roh SH, Kim HG, Lee KY, et al. Increased expression of Nrf2/ARE-dependent anti-oxidant proteins in tamoxifen-resistant breast cancer cells. Free Radic Biol Med. 2008;45:537–46.CrossRefPubMed
53.
go back to reference Khatri R, Shah P, Guha R, Rassool FV, Tomkinson AE, Brodie A, et al. Aromatase inhibitor-mediated downregulation of INrf2 (Keap1) leads to increased Nrf2 and resistance in breast cancer. Mol Cancer Ther. 2015;14(7):1728–37.CrossRefPubMedPubMedCentral Khatri R, Shah P, Guha R, Rassool FV, Tomkinson AE, Brodie A, et al. Aromatase inhibitor-mediated downregulation of INrf2 (Keap1) leads to increased Nrf2 and resistance in breast cancer. Mol Cancer Ther. 2015;14(7):1728–37.CrossRefPubMedPubMedCentral
54.
go back to reference Kang HJ, Yi YW, Hong YB, Kim HJ, Jang YJ, Seong YS, et al. HER2 confers drug resistance of human breast cancer cells through activation of NRF2 by direct interaction. Sci Rep. 2014;3:7201. Kang HJ, Yi YW, Hong YB, Kim HJ, Jang YJ, Seong YS, et al. HER2 confers drug resistance of human breast cancer cells through activation of NRF2 by direct interaction. Sci Rep. 2014;3:7201.
55.
go back to reference Futreal PA, Liu Q, Shattuck-Eidens D, Cochran C, Harshman K, Tavtigian S, et al. BRCA1 mutations in primary breast and ovarian carcinomas. Science. 1994;266:120–2.CrossRefPubMed Futreal PA, Liu Q, Shattuck-Eidens D, Cochran C, Harshman K, Tavtigian S, et al. BRCA1 mutations in primary breast and ovarian carcinomas. Science. 1994;266:120–2.CrossRefPubMed
56.
go back to reference Acharya A, Das I, Chandhok D, Saha T. Redox regulation in cancer: a double-edged sword with therapeutic potential. Oxidative Med Cell Longev. 2010;3:23–34.CrossRef Acharya A, Das I, Chandhok D, Saha T. Redox regulation in cancer: a double-edged sword with therapeutic potential. Oxidative Med Cell Longev. 2010;3:23–34.CrossRef
58.
go back to reference Gorrini C, Baniasadi PS, Harris IS, Silvester J, Inoue S, Snow B, et al. BRCA1 interacts with Nrf2 to regulate antioxidant signaling and cell survival. J Exp Med. 2013;210:1529–44.CrossRefPubMedPubMedCentral Gorrini C, Baniasadi PS, Harris IS, Silvester J, Inoue S, Snow B, et al. BRCA1 interacts with Nrf2 to regulate antioxidant signaling and cell survival. J Exp Med. 2013;210:1529–44.CrossRefPubMedPubMedCentral
59.
go back to reference Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;14:52–67.CrossRef Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;14:52–67.CrossRef
60.
go back to reference Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9:239–52.CrossRefPubMed Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9:239–52.CrossRefPubMed
61.
go back to reference Palermo C, Joyce JA. Cysteine cathepsin proteases as pharmacological targets in cancer. Trends Pharmacol Sci. 2008;29:22–8.CrossRefPubMed Palermo C, Joyce JA. Cysteine cathepsin proteases as pharmacological targets in cancer. Trends Pharmacol Sci. 2008;29:22–8.CrossRefPubMed
62.
go back to reference Mohamed MM, Sloane BF. Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer. 2006;6:764–75.CrossRefPubMed Mohamed MM, Sloane BF. Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer. 2006;6:764–75.CrossRefPubMed
63.
go back to reference Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall AL, et al. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 2010;24:241–55.CrossRefPubMedPubMedCentral Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall AL, et al. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 2010;24:241–55.CrossRefPubMedPubMedCentral
65.
go back to reference Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res. 2007;67:2649–56.CrossRefPubMed Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res. 2007;67:2649–56.CrossRefPubMed
66.
go back to reference Tobar N, Guerrero J, Smith PC, Martínez J. NOX4-dependent ROS production by stromal mammary cells modulates epithelial MCF-7 cell migration. Br J Cancer. 2010;103:1040–7.CrossRefPubMedPubMedCentral Tobar N, Guerrero J, Smith PC, Martínez J. NOX4-dependent ROS production by stromal mammary cells modulates epithelial MCF-7 cell migration. Br J Cancer. 2010;103:1040–7.CrossRefPubMedPubMedCentral
67.
go back to reference Martinez-Outschoorn UE, Balliet RM, Rivadeneira D, Chiavarina B, Pavlides S, Wang C, et al. Oxidative stress in cancer associated fibroblasts drives tumor-stroma co-evolution. Cell Cycle. 2010;9:3276–96.CrossRef Martinez-Outschoorn UE, Balliet RM, Rivadeneira D, Chiavarina B, Pavlides S, Wang C, et al. Oxidative stress in cancer associated fibroblasts drives tumor-stroma co-evolution. Cell Cycle. 2010;9:3276–96.CrossRef
68.
go back to reference Martinez-Outschoorn UE, Lin Z, Trimmer C, Flomenberg N, Wang C, Pavlides S, et al. Cancer cells metabolically “fertilize” the tumor microenvironment with hydrogen peroxide, driving the Warburg effect. Cell Cycle. 2011;10:2504–20.CrossRefPubMedPubMedCentral Martinez-Outschoorn UE, Lin Z, Trimmer C, Flomenberg N, Wang C, Pavlides S, et al. Cancer cells metabolically “fertilize” the tumor microenvironment with hydrogen peroxide, driving the Warburg effect. Cell Cycle. 2011;10:2504–20.CrossRefPubMedPubMedCentral
69.
go back to reference Boudreau HE, Casterline BW, Rada B, Korzeniowska A, Leto TL. Nox4 involvement in TGF-beta and SMAD3-driven induction of the epithelial-to-mesenchymal transition and migration of breast epithelial cells. Free Radic Biol Med. 2012;53:1–11.CrossRef Boudreau HE, Casterline BW, Rada B, Korzeniowska A, Leto TL. Nox4 involvement in TGF-beta and SMAD3-driven induction of the epithelial-to-mesenchymal transition and migration of breast epithelial cells. Free Radic Biol Med. 2012;53:1–11.CrossRef
71.
go back to reference Giannoni E, Parri M, Chiarugi P. EMT and oxidative stress: a bidirectional interplay affecting tumor malignancy. Antioxid Redox Signal. 2012;16:1248–63.CrossRefPubMed Giannoni E, Parri M, Chiarugi P. EMT and oxidative stress: a bidirectional interplay affecting tumor malignancy. Antioxid Redox Signal. 2012;16:1248–63.CrossRefPubMed
72.
go back to reference Boudreau HE, Casterline BW, Burke DJ, Leto TL. Wild-type and mutant p53 differentially regulate NADPH oxidase 4 in TGF-β-mediated migration of human lung and breast epithelial cells. Br J Cancer. 2014;110:2569–82.CrossRefPubMedPubMedCentral Boudreau HE, Casterline BW, Burke DJ, Leto TL. Wild-type and mutant p53 differentially regulate NADPH oxidase 4 in TGF-β-mediated migration of human lung and breast epithelial cells. Br J Cancer. 2014;110:2569–82.CrossRefPubMedPubMedCentral
73.
go back to reference Blot WJ, Li JY, Taylor PR, Guo W, Dawsey S, Wang GQ, et al. Nutrition intervention trials in Linxian, China: supplementation with specific vitamin/mineral combinations, cancer incidence, and disease-specific mortality in the general population. J Natl Cancer Inst. 1993;85:1483–92.CrossRefPubMed Blot WJ, Li JY, Taylor PR, Guo W, Dawsey S, Wang GQ, et al. Nutrition intervention trials in Linxian, China: supplementation with specific vitamin/mineral combinations, cancer incidence, and disease-specific mortality in the general population. J Natl Cancer Inst. 1993;85:1483–92.CrossRefPubMed
74.
go back to reference The Alpha-Tocopherol, Beta Carotene Cancer Prevention Study Group. The alpha-tocopherol, the effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. N Engl J Med. 1994;330:1029–35.CrossRef The Alpha-Tocopherol, Beta Carotene Cancer Prevention Study Group. The alpha-tocopherol, the effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. N Engl J Med. 1994;330:1029–35.CrossRef
75.
go back to reference Omenn GS, Goodman GE, Thornquist MD, Balmes J, Cullen MR, Glass A, et al. Risk factors for lung cancer and for intervention effects in CARET, the Beta-Carotene and Retinol Efficacy Trial. J Natl Cancer Inst. 1996;88:1550–9.CrossRefPubMed Omenn GS, Goodman GE, Thornquist MD, Balmes J, Cullen MR, Glass A, et al. Risk factors for lung cancer and for intervention effects in CARET, the Beta-Carotene and Retinol Efficacy Trial. J Natl Cancer Inst. 1996;88:1550–9.CrossRefPubMed
76.
go back to reference Sayin VI, Ibrahim MX, Larsson E, Nilsson JA, Lindahl P, Bergo MO. Antioxidants accelerate lung cancer progression in mice. Sci Transl Med. 2014;29:221ra15.CrossRef Sayin VI, Ibrahim MX, Larsson E, Nilsson JA, Lindahl P, Bergo MO. Antioxidants accelerate lung cancer progression in mice. Sci Transl Med. 2014;29:221ra15.CrossRef
77.
go back to reference Lippman SM, Klein EA, Goodman PJ, Lucia MS, Thompson IM, Ford LG, et al. Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA. 2009;301:39–51.CrossRefPubMed Lippman SM, Klein EA, Goodman PJ, Lucia MS, Thompson IM, Ford LG, et al. Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA. 2009;301:39–51.CrossRefPubMed
78.
go back to reference Lonn E, Bosch J, Yusuf S, Sheridan P, Pogue J, Arnold JMO, et al. Effects of long-term vitamin E supplementation on cardiovascular events and cancer: a randomized controlled trial. JAMA. 2005;293:1338–47.CrossRefPubMed Lonn E, Bosch J, Yusuf S, Sheridan P, Pogue J, Arnold JMO, et al. Effects of long-term vitamin E supplementation on cardiovascular events and cancer: a randomized controlled trial. JAMA. 2005;293:1338–47.CrossRefPubMed
79.
go back to reference Hercberg S, Galan P, Preziosi P, Bertrais S, Mennen L, Malvy D, et al. The SU.VI.MAX study: a randomized, placebo-controlled trial of the health effects of antioxidant vitamins and minerals. Arch Intern Med. 2004;164:2335–42.CrossRefPubMed Hercberg S, Galan P, Preziosi P, Bertrais S, Mennen L, Malvy D, et al. The SU.VI.MAX study: a randomized, placebo-controlled trial of the health effects of antioxidant vitamins and minerals. Arch Intern Med. 2004;164:2335–42.CrossRefPubMed
80.
go back to reference Greenlee H, Hershman DL, Jacobson JS. Use of antioxidant supplements during breast cancer treatment: a comprehensive review. Breast Cancer Res Treat. 2009;115:437–52.CrossRefPubMed Greenlee H, Hershman DL, Jacobson JS. Use of antioxidant supplements during breast cancer treatment: a comprehensive review. Breast Cancer Res Treat. 2009;115:437–52.CrossRefPubMed
81.
go back to reference Uetaki M, Tabata S, Nakasuka F, Soga T, Tomita M. Metabolomic alterations in human cancer cells by vitamin C-induced oxidative stress. Sci Rep. 2015;5:13896.CrossRefPubMedPubMedCentral Uetaki M, Tabata S, Nakasuka F, Soga T, Tomita M. Metabolomic alterations in human cancer cells by vitamin C-induced oxidative stress. Sci Rep. 2015;5:13896.CrossRefPubMedPubMedCentral
82.
go back to reference Raj L, Ide T, Gurkar AU, Foley M, Schenone M, Li X, et al. Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature. 2011;475(7355):231–4.CrossRefPubMedPubMedCentral Raj L, Ide T, Gurkar AU, Foley M, Schenone M, Li X, et al. Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature. 2011;475(7355):231–4.CrossRefPubMedPubMedCentral
83.
go back to reference Pons DG, Nadal-Serrano M, Torrens-Mas M, Valle A, Oliver J, Roca P. UCP2 inhibition sensitizes breast cancer cells to therapeutic agents by increasing oxidative stress. Free Radic Biol Med. 2015;86:67–77.CrossRefPubMed Pons DG, Nadal-Serrano M, Torrens-Mas M, Valle A, Oliver J, Roca P. UCP2 inhibition sensitizes breast cancer cells to therapeutic agents by increasing oxidative stress. Free Radic Biol Med. 2015;86:67–77.CrossRefPubMed
84.
go back to reference Theriault RL, Carlson RW, Allred C, Anderson BO, Burstein HJ, Edge SB, et al. Breast cancer, version 3.2013: featured updates to the NCCN guidelines. J Natl Compr Cancer Netw. 2013;11:753–60. Theriault RL, Carlson RW, Allred C, Anderson BO, Burstein HJ, Edge SB, et al. Breast cancer, version 3.2013: featured updates to the NCCN guidelines. J Natl Compr Cancer Netw. 2013;11:753–60.
85.
go back to reference Kaufmann SH, Earnshaw WC. Induction of apoptosis by cancer chemotherapy. Exp Cell Res. 2000;256:42–9.CrossRefPubMed Kaufmann SH, Earnshaw WC. Induction of apoptosis by cancer chemotherapy. Exp Cell Res. 2000;256:42–9.CrossRefPubMed
86.
go back to reference Florea AM, Büsselberg D. Cisplatin as an anti-tumor drug: cellular mechanisms of activity, drug resistance and induced side effects. Cancers (Basel). 2011;3:1351–71.CrossRef Florea AM, Büsselberg D. Cisplatin as an anti-tumor drug: cellular mechanisms of activity, drug resistance and induced side effects. Cancers (Basel). 2011;3:1351–71.CrossRef
87.
go back to reference Simůnek T, Stérba M, Popelová O, Adamcová M, Hrdina R, Gersl V. Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol Rep. 2009;61:154–71.CrossRefPubMed Simůnek T, Stérba M, Popelová O, Adamcová M, Hrdina R, Gersl V. Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol Rep. 2009;61:154–71.CrossRefPubMed
88.
go back to reference Narayanan P, Goodwin E, Lehnert B. α-particles initiate biological production of superoxide anions and hydrogen peroxide. Cancer Res. 1997;57:3963–71.PubMed Narayanan P, Goodwin E, Lehnert B. α-particles initiate biological production of superoxide anions and hydrogen peroxide. Cancer Res. 1997;57:3963–71.PubMed
89.
go back to reference Crow JP. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide. 1997;1:145–57.CrossRefPubMed Crow JP. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide. 1997;1:145–57.CrossRefPubMed
90.
go back to reference Leach JK, Van Tuyle G, Lin PS, Schmidt-Ullrich R, Mikkelsen RB. Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res. 2001;61:3894–901.PubMed Leach JK, Van Tuyle G, Lin PS, Schmidt-Ullrich R, Mikkelsen RB. Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res. 2001;61:3894–901.PubMed
91.
go back to reference Kim GJ, Fiskum GM, Morgan WF. A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer Res. 2006;66:10377–83.CrossRefPubMedPubMedCentral Kim GJ, Fiskum GM, Morgan WF. A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer Res. 2006;66:10377–83.CrossRefPubMedPubMedCentral
93.
go back to reference Watson GE, Lorimore SA, Macdonald DA, Wright EG. Chromosomal instability in unirradiated cells induced in vivo by a bystander effect of ionizing radiation. Cancer Res. 2000;60:5608–11.PubMed Watson GE, Lorimore SA, Macdonald DA, Wright EG. Chromosomal instability in unirradiated cells induced in vivo by a bystander effect of ionizing radiation. Cancer Res. 2000;60:5608–11.PubMed
94.
go back to reference Tulard A, Hoffschir F, de Boisferon FH, Luccioni C, Bravard A. Persistent oxidative stress after ionizing radiation is involved in inherited radiosensitivity. Free Radic Biol Med. 2003;35:68–77.CrossRefPubMed Tulard A, Hoffschir F, de Boisferon FH, Luccioni C, Bravard A. Persistent oxidative stress after ionizing radiation is involved in inherited radiosensitivity. Free Radic Biol Med. 2003;35:68–77.CrossRefPubMed
95.
go back to reference Meister A. Glutathione metabolism and its selective modification. J Biol Chem. 1988;263:17205–8.PubMed Meister A. Glutathione metabolism and its selective modification. J Biol Chem. 1988;263:17205–8.PubMed
96.
go back to reference Nishimura T, Newkirk K, Sessions RB, Andrews PA, Trock BJ, Rasmussen AA, et al. Immunohistochemical staining for glutathione S-transferase predicts response to platinum-based chemotherapy in head and neck cancer. Clin Cancer Res. 1996;2:1859–65.PubMed Nishimura T, Newkirk K, Sessions RB, Andrews PA, Trock BJ, Rasmussen AA, et al. Immunohistochemical staining for glutathione S-transferase predicts response to platinum-based chemotherapy in head and neck cancer. Clin Cancer Res. 1996;2:1859–65.PubMed
97.
go back to reference Lewis-Wambi JS, Kim HR, Wambi C, Patel R, Pyle JR, Klein-Szanto AJ, et al. Buthionine sulfoximine sensitizes antihormone-resistant human breast cancer cells to estrogen-induced apoptosis. Breast Cancer Res. 2008;10:R104.CrossRefPubMedPubMedCentral Lewis-Wambi JS, Kim HR, Wambi C, Patel R, Pyle JR, Klein-Szanto AJ, et al. Buthionine sulfoximine sensitizes antihormone-resistant human breast cancer cells to estrogen-induced apoptosis. Breast Cancer Res. 2008;10:R104.CrossRefPubMedPubMedCentral
98.
go back to reference Rudin CM, Yang Z, Schumaker LM, VanderWeele DJ, Newkirk K, Egorin MJ, et al. Inhibition of glutathione synthesis reverses Bcl-2-mediated cisplatin resistance. Cancer Res. 2003;63:312–8.PubMed Rudin CM, Yang Z, Schumaker LM, VanderWeele DJ, Newkirk K, Egorin MJ, et al. Inhibition of glutathione synthesis reverses Bcl-2-mediated cisplatin resistance. Cancer Res. 2003;63:312–8.PubMed
99.
go back to reference Montero AJ, Diaz-Montero CM, Deutsch YE, Hurley J, Koniaris LG, Rumboldt T, et al. Phase 2 study of neoadjuvant treatment with NOV-002 in combination with doxorubicin and cyclophosphamide followed by docetaxel in patients with HER-2 negative clinical stage II-IIIc breast cancer. Breast Cancer Res Treat. 2012;132:215–23.CrossRefPubMed Montero AJ, Diaz-Montero CM, Deutsch YE, Hurley J, Koniaris LG, Rumboldt T, et al. Phase 2 study of neoadjuvant treatment with NOV-002 in combination with doxorubicin and cyclophosphamide followed by docetaxel in patients with HER-2 negative clinical stage II-IIIc breast cancer. Breast Cancer Res Treat. 2012;132:215–23.CrossRefPubMed
100.
go back to reference Gumireddy K, Li A, Cao L, Yan J, Liu L. NOV-002, a glutathione disulfide mimetic, suppresses tumor cell invasion and metastasis. J Carcinog Mutagen. 2013;7:997–1003. Gumireddy K, Li A, Cao L, Yan J, Liu L. NOV-002, a glutathione disulfide mimetic, suppresses tumor cell invasion and metastasis. J Carcinog Mutagen. 2013;7:997–1003.
101.
go back to reference Bin Wang J, Erickson JW, Fuji R, Ramachandran S, Gao P, Dinavahi R, et al. Targeting mitochondrial glutaminase activity inhibits oncogenic transformation. Cancer Cell. 2010;18:207–19.CrossRef Bin Wang J, Erickson JW, Fuji R, Ramachandran S, Gao P, Dinavahi R, et al. Targeting mitochondrial glutaminase activity inhibits oncogenic transformation. Cancer Cell. 2010;18:207–19.CrossRef
Metadata
Title
The role of oxidative stress on breast cancer development and therapy
Authors
Fabio Hecht
Carolina F. Pessoa
Luciana B. Gentile
Doris Rosenthal
Denise P. Carvalho
Rodrigo S. Fortunato
Publication date
01-04-2016
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 4/2016
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-016-4873-9

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