Advertisement

Reactive Oxygen Species: Friends or Foes of Lung Cancer?

  • Deblina Guha
  • Shruti Banerjee
  • Shravanti Mukherjee
  • Apratim Dutta
  • Tanya DasEmail author
Chapter
First Online:

Abstract

Reactive oxygen species (ROS) are important biological radicals essential for determining different stages and phenotypes of cells from quiescence to proliferation, differentiation, self-renewal and even apoptosis. Low ROS favours quiescence and self-renewal in contrast to high ROS that dictates proliferation, differentiation or apoptosis. Such wide variety of cell fates depends upon specific signalling pathways that regulate the cellular ROS, thus contributing to tissue homeostasis. Imbalance of ROS causes several pathological conditions including cancer which is associated with higher level of ROS that supports tumour development and progression. However, to restrain from the excessive oxidative damage of ROS, cancer cells efficiently control the antioxidative pathways, thus favouring its own survival and maintenance at the same time. Furthermore, importance of ROS has been an active field of research in ‘cancer stem cells’ (CSCs), a subpopulation of cancer cells with stem cell-like properties and features. CSCs possess low ROS level that make them resistant to the existing chemotherapy or radiotherapy that ultimately leads to cancer recurrence. Though several evidences have proved the role of ROS in self-renewal and stemness of CSCs, there is a lot to explore about ROS-regulated signalling mechanisms in CSCs. An understanding of ROS regulation in CSCs can provide an idea about the application of oxidative stress as a therapeutic strategy in treatment of cancer. In this book chapter, we have raised the debate as to whether ROS acts as ‘friend or foe’ for cancer cells. Moreover, exploring the significance of ROS and redox regulation in lung cancer stem cells has been our major focus. Finally, it is suggested that in order to get an effective treatment and recurrence-free survival, sensitization of the cancer stem cells to high ROS environment is a must.

Keywords

Reactive oxygen species Cancer stem cells Lung CSCs Oxidative stress Redox regulation 
This is a preview of subscription content, log in to check access.

References

  1. 1.
    Giannoni E, Buricchi F, Raugei G et al (2005) Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol Cell Biol 25(15):6391–6403PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Yee C, Yang W, Hekimi S (2014) The intrinsic apoptosis pathway mediates the pro-longevity response to mitochondrial ROS in C. elegans. Cell 157(4):897–909PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Hoeijmakers JHJ (2009) DNA damage, aging, and cancer. N Engl J Med 361(15):1475–1485PubMedCrossRefGoogle Scholar
  4. 4.
    D’Autréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8(10):813–824PubMedCrossRefGoogle Scholar
  5. 5.
    Fruehauf JP, Meyskens FL (2007) Reactive oxygen species: a breath of life or death? Clin Cancer Res 13(3):789–794PubMedCrossRefGoogle Scholar
  6. 6.
    Mohanty S, Saha S, Hossain DMS et al (2014) ROS-PIASγ cross talk channelizes ATM signaling from resistance to apoptosis during chemosensitization of resistant tumors. Cell Death Dis 5(1):e1021PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Chakraborti S, Chakraborty S, Saha S et al (2017) PEG-functionalized zinc oxide nanoparticles induce apoptosis in breast cancer cells through reactive oxygen species-dependent impairment of DNA damage repair enzyme NEIL2. Free Radic Biol Med 103:35–47PubMedCrossRefGoogle Scholar
  8. 8.
    Ambrosone CB (2000) Oxidants and antioxidants in breast cancer. Antioxid Redox Signal 2(4):903–917PubMedCrossRefGoogle Scholar
  9. 9.
    Szatrowski TP, Nathan CF (1991) Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51(3):794–798PubMedGoogle Scholar
  10. 10.
    Halliwell B (2007) Oxidative stress and cancer: have we moved forward? Biochem J 401(1):1–11PubMedCrossRefGoogle Scholar
  11. 11.
    Ramsey MR, Sharpless NE (2006) ROS as a tumour suppressor? Nat Cell Biol 8(11):1213–1215PubMedCrossRefGoogle Scholar
  12. 12.
    Ozben T (2007) Oxidative stress and apoptosis: impact on cancer therapy. J Pharm Sci 96(9):2181–2196PubMedCrossRefGoogle Scholar
  13. 13.
    Toler SM, Noe D, Sharma A (2006) Selective enhancement of cellular oxidative stress by chloroquine: implications for the treatment of glioblastoma multiforme. Neurosurg Focus 21(6):E10PubMedCrossRefGoogle Scholar
  14. 14.
    Nguyen LV, Vanner R, Dirks P et al (2012) Cancer stem cells: an evolving concept. Nat Rev Cancer 12(2):133–143PubMedCrossRefGoogle Scholar
  15. 15.
    Kobayashi CI, Suda T (2012) Regulation of reactive oxygen species in stem cells and cancer stem cells. J Cell Physiol 227(2):421–430PubMedCrossRefGoogle Scholar
  16. 16.
    Al-Hajj M, Wicha MS, Benito-Hernandez A et al (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100(7):3983–3988PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Hermann PC, Huber SL, Herrler T et al (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1(3):313–323PubMedCrossRefGoogle Scholar
  18. 18.
    Dave B, Mittal V, Tan NM, Chang JC (2012) Epithelial-mesenchymal transition, cancer stem cells and treatment resistance. Breast Cancer Res BCR 14(1):202PubMedCrossRefGoogle Scholar
  19. 19.
    Eyler CE, Rich JN (2008) Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol 26(17):2839–2845PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Kurtova AV, Xiao J, Mo Q et al (2015) Blocking PGE2-induced tumour repopulation abrogates bladder cancer chemoresistance. Nature 517(7533):209–213PubMedCrossRefGoogle Scholar
  21. 21.
    Doherty MR, Smigiel JM, Junk DJ, Jackson MW (2016) Cancer stem cell plasticity drives therapeutic resistance. Cancers (Basel) 8(1):pii: E8CrossRefGoogle Scholar
  22. 22.
    Roesch A, Fukunaga-Kalabis M, Schmidt EC et al (2010) A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141(4):583–594PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Kim HM, Haraguchi N, Ishii H et al (2012) Increased CD13 expression reduces reactive oxygen species, promoting survival of liver cancer stem cells via an epithelial-mesenchymal transition-like phenomenon. Ann Surg Oncol 19(Suppl 3):S539–S548PubMedCrossRefGoogle Scholar
  24. 24.
    Hudson TJ, Anderson W, Artez A et al (2010) International network of cancer genome projects. Nature 464(7291):993–998PubMedCrossRefGoogle Scholar
  25. 25.
    Diehn M, Cho RW, Lobo NA et al (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458(7239):780–783PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Ambudkar SV, Dey S, Hrycyna CA et al (1999) Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol 39:361–398PubMedCrossRefGoogle Scholar
  27. 27.
    Townsend DM, Tew KD (2003) The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 22(47):7369–7375PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Eastman A, Schulte N (1988) Enhanced DNA repair as a mechanism of resistance to cis-diamminedichloroplatinum(II). Biochemistry 27(13):4730–4734PubMedCrossRefGoogle Scholar
  29. 29.
    Kavallaris M, Kuo DY, Burkhart CA et al (1997) Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific beta-tubulin isotypes. J Clin Invest 100(5):1282–1293PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Sethi T, Rintoul RC, Moore SM et al (1999) Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat Med 5(6):662–668PubMedCrossRefGoogle Scholar
  31. 31.
    Park HS, Kim SR, Lee YC (2009) Impact of oxidative stress on lung diseases. Respirol Carlton Vic 14(1):27–38CrossRefGoogle Scholar
  32. 32.
    Ciencewicki J, Trivedi S, Kleeberger SR (2008) Oxidants and the pathogenesis of lung diseases. J Allergy Clin Immunol 122(3):456–468; quiz 469–70PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Azad N, Rojanasakul Y, Vallyathan V (2008) Inflammation and lung cancer: roles of reactive oxygen/nitrogen species. J Toxicol Environ Health B Crit Rev 11(1):1–15CrossRefGoogle Scholar
  34. 34.
    Zhou D, Shao L, Spitz DR (2014) Reactive oxygen species in normal and tumor stem cells. Adv Cancer Res 122:1–67PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Storz P, Döppler H, Toker A (2004) Protein kinase Cdelta selectively regulates protein kinase D-dependent activation of NF-kappaB in oxidative stress signaling. Mol Cell Biol 24(7):2614–2626PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Petros JA, Baumann AK, Ruiz-Pesini E et al (2005) mtDNA mutations increase tumorigenicity in prostate cancer. Proc Natl Acad Sci U S A 102(3):719–724PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Masri F (2010) Role of nitric oxide and its metabolites as potential markers in lung cancer. Ann Thorac Med 5(3):123–127PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Ezashi T, Das P, Roberts RM (2005) Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci U S A 102(13):4783–4788PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Juntilla MM, Patil VD, Calamito M et al (2010) AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 115(20):4030–4038PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Kinder M, Wei C, Shelat SG et al (2010) Hematopoietic stem cell function requires 12/15-lipoxygenase-dependent fatty acid metabolism. Blood 115(24):5012–5022PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Lewandowski JP, Sheehan KB, Bennett PE, Boswell RE (2010) Mago Nashi, Tsunagi/Y14 and Ranshi form a complex that influences oocyte differentiation in Drosophila melanogaster. Dev Biol 339(2):307–319PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Owusu-Ansah E, Banerjee U (2009) Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461(7263):537–541PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Sauer H, Wartenberg M (2005) Reactive oxygen species as signaling molecules in cardiovascular differentiation of embryonic stem cells and tumor-induced angiogenesis. Antioxid Redox Signal 7(11–12):1423–1434PubMedCrossRefGoogle Scholar
  45. 45.
    Chen C, Liu Y, Liu R et al (2008) TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med 205(10):2397–2408PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Miyamoto K, Araki KY, Naka K et al (2007) Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1(1):101–112PubMedCrossRefGoogle Scholar
  47. 47.
    Tothova Z, Kollipara R, Huntly BJ et al (2007) FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128(2):325–339PubMedCrossRefGoogle Scholar
  48. 48.
    Shao L, Wu L, Zhou D (2012) Sensitization of tumor cells to cancer therapy by molecularly targeted inhibition of the inhibitor of nuclear factor κB kinase. Transl Cancer Res 1(2):100–108PubMedPubMedCentralGoogle Scholar
  49. 49.
    Shao L, Sun Y, Zhang Z et al (2010) Deletion of proapoptotic Puma selectively protects hematopoietic stem and progenitor cells against high-dose radiation. Blood 115(23):4707–4714PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Yu H, Shen H, Yuan Y et al (2010) Deletion of Puma protects hematopoietic stem cells and confers long-term survival in response to high-dose gamma-irradiation. Blood 115(17):3472–3480PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Ji A-R, Ku S-Y, Cho MS et al (2010) Reactive oxygen species enhance differentiation of human embryonic stem cells into mesendodermal lineage. Exp Mol Med 42(3):175–186PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Schmelter M, Ateghang B, Helmig S et al (2006) Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB J 20(8):1182–1184PubMedCrossRefGoogle Scholar
  53. 53.
    Bedard K, Krause K-H (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87(1):245–313CrossRefGoogle Scholar
  54. 54.
    van der Vliet A (2008) NADPH oxidases in lung biology and pathology: host defense enzymes, and more. Free Radic Biol Med 44(6):938–955CrossRefGoogle Scholar
  55. 55.
    Zhang C, Lan T, Hou J et al (2014) NOX4 promotes non-small cell lung cancer cell proliferation and metastasis through positive feedback regulation of PI3K/Akt signaling. Oncotarget 5(12):4392–4405PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Boudreau HE, Casterline BW, Burke DJ, Leto TL (2014) 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 110(10):2569–2582PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Fischer H (2009) Mechanisms and function of DUOX in epithelia of the lung. Antioxid Redox Signal 11(10):2453–2465PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Luxen S, Belinsky SA, Knaus UG (2008) Silencing of DUOX NADPH oxidases by promoter hypermethylation in lung cancer. Cancer Res 68(4):1037–1045PubMedCrossRefGoogle Scholar
  59. 59.
    Colavitti R, Pani G, Bedogni B et al (2002) Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/KDR. J Biol Chem 277(5):3101–3108PubMedCrossRefGoogle Scholar
  60. 60.
    Finkel T (2000) Redox-dependent signal transduction. FEBS Lett 476(1–2):52–54PubMedCrossRefGoogle Scholar
  61. 61.
    Chiarugi P, Fiaschi T (2007) Redox signalling in anchorage-dependent cell growth. Cell Signal 19(4):672–682PubMedCrossRefGoogle Scholar
  62. 62.
    Rhee SG, Bae YS, Lee SR, Kwon J (2000) Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE Signal Transduct Knowl Environ 2000(53):pe1Google Scholar
  63. 63.
    Irani K, Xia Y, Zweier JL et al (1997) Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275(5306):1649–1652PubMedCrossRefGoogle Scholar
  64. 64.
    Reddy KB, Glaros S (2007) Inhibition of the MAP kinase activity suppresses estrogen-induced breast tumor growth both in vitro and in vivo. Int J Oncol 30(4):971–975PubMedGoogle Scholar
  65. 65.
    Lander HM, Hajjar DP, Hempstead BL et al (1997) A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J Biol Chem 272(7):4323–4326PubMedCrossRefGoogle Scholar
  66. 66.
    Chan DW, Liu VWS, Tsao GSW et al (2008) Loss of MKP3 mediated by oxidative stress enhances tumorigenicity and chemoresistance of ovarian cancer cells. Carcinogenesis 29(9):1742–1750PubMedCrossRefGoogle Scholar
  67. 67.
    McCubrey JA, Steelman LS, Chappell WH et al (2007) Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 1773(8):1263–1284PubMedCrossRefGoogle Scholar
  68. 68.
    Steelman LS, Abrams SL, Whelan J et al (2008) Contributions of the Raf/MEK/ERK, PI3K/PTEN/Akt/mTOR and Jak/STAT pathways to leukemia. Leukemia 22(4):686–707PubMedCrossRefGoogle Scholar
  69. 69.
    Lee WC, Choi CH, Cha SH, Oh HL, Kim YK (2005) Role of ERK in hydrogen peroxide-induced cell death of human glioma cells. Neurochem Res 30(2):263–270PubMedCrossRefGoogle Scholar
  70. 70.
    Rygiel TP, Mertens AE, Strumane K et al (2008) The Rac activator Tiam1 prevents keratinocyte apoptosis by controlling ROS-mediated ERK phosphorylation. J Cell Sci 121(Pt 8):1183–1192PubMedCrossRefGoogle Scholar
  71. 71.
    Ostrakhovitch EA, Cherian MG (2005) Inhibition of extracellular signal regulated kinase (ERK) leads to apoptosis inducing factor (AIF) mediated apoptosis in epithelial breast cancer cells: the lack of effect of ERK in p53 mediated copper induced apoptosis. J Cell Biochem 95(6):1120–1134PubMedCrossRefGoogle Scholar
  72. 72.
    Zhou J, Chen Y, Lang J-Y (2008) Salvicine inactivates beta 1 integrin and inhibits adhesion of MDA-MB-435 cells to fibronectin via reactive oxygen species signaling. Mol Cancer Res MCR 6(2):194–204PubMedCrossRefGoogle Scholar
  73. 73.
    Lewis A, Du J, Liu J, Ritchie JM, Oberley LW, Cullen JJ (2005) Metastatic progression of pancreatic cancer: changes in antioxidant enzymes and cell growth. Clin Exp Metastasis 22(7):523–532PubMedCrossRefGoogle Scholar
  74. 74.
    Mazzio EA, Soliman KFA (2004) Glioma cell antioxidant capacity relative to reactive oxygen species produced by dopamine. J Appl Toxicol JAT 24(2):99–106PubMedCrossRefGoogle Scholar
  75. 75.
    Brunet A, Bonni A, Zigmond MJ et al (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96(6):857–868PubMedCrossRefGoogle Scholar
  76. 76.
    Pastorino JG, Tafani M, Farber JL (1999) Tumor necrosis factor induces phosphorylation and translocation of BAD through a phosphatidylinositide-3-OH kinase-dependent pathway. J Biol Chem 274(27):19411–19416PubMedCrossRefGoogle Scholar
  77. 77.
    Burdick AD, Davis JW, Liu KJ et al (2003) Benzo(a)pyrene quinones increase cell proliferation, generate reactive oxygen species, and transactivate the epidermal growth factor receptor in breast epithelial cells. Cancer Res 63(22):7825–7833PubMedGoogle Scholar
  78. 78.
    Park S-A, Na H-K, Kim E-H et al (2009) 4-hydroxyestradiol induces anchorage-independent growth of human mammary epithelial cells via activation of IkappaB kinase: potential role of reactive oxygen species. Cancer Res 69(6):2416–2424PubMedCrossRefGoogle Scholar
  79. 79.
    Liu L-Z, Hu X-W, Xia C et al (2006) Reactive oxygen species regulate epidermal growth factor-induced vascular endothelial growth factor and hypoxia-inducible factor-1alpha expression through activation of AKT and P70S6K1 in human ovarian cancer cells. Free Radic Biol Med 41(10):1521–1533PubMedCrossRefGoogle Scholar
  80. 80.
    Li N, Karin M (1999) Is NF-kappaB the sensor of oxidative stress? FASEB J 13(10):1137–1143PubMedCrossRefGoogle Scholar
  81. 81.
    Schreck R, Albermann K, Baeuerle PA (1992) Nuclear factor kappa B: an oxidative stress-responsive transcription factor of eukaryotic cells (a review). Free Radic Res Commun 17(4):221–237PubMedCrossRefGoogle Scholar
  82. 82.
    Wang Y, Huang X, Cang H et al (2007) The endogenous reactive oxygen species promote NF-kappaB activation by targeting on activation of NF-kappaB-inducing kinase in oral squamous carcinoma cells. Free Radic Res 41(9):963–971PubMedCrossRefGoogle Scholar
  83. 83.
    Storz P, Toker A (2003) Protein kinase D mediates a stress-induced NF-kappaB activation and survival pathway. EMBO J 22(1):109–120PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Cowell CF, Döppler H, Yan IK et al (2009) Mitochondrial diacylglycerol initiates protein-kinase D1-mediated ROS signaling. J Cell Sci 122(Pt 7):919–928PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Döppler H, Storz P (2007) A novel tyrosine phosphorylation site in protein kinase D contributes to oxidative stress-mediated activation. J Biol Chem 282(44):31873–31881PubMedCrossRefGoogle Scholar
  86. 86.
    Storz P, Döppler H, Toker A (2004) Activation loop phosphorylation controls protein kinase D-dependent activation of nuclear factor kappaB. Mol Pharmacol 66(4):870–879PubMedCrossRefGoogle Scholar
  87. 87.
    Antonicelli F, Parmentier M, Drost EM et al (2002) Nacystelyn inhibits oxidant-mediated interleukin-8 expression and NF-kappaB nuclear binding in alveolar epithelial cells. Free Radic Biol Med 32(6):492–502PubMedCrossRefGoogle Scholar
  88. 88.
    Goudar RK, Vlahovic G (2008) Hypoxia, angiogenesis, and lung cancer. Curr Oncol Rep 10(4):277–282PubMedCrossRefGoogle Scholar
  89. 89.
    Cho KH, Choi MJ, Jeong KJ et al (2014) A ROS/STAT3/HIF-1α signaling cascade mediates EGF-induced TWIST1 expression and prostate cancer cell invasion. The Prostate 74(5):528–536PubMedCrossRefGoogle Scholar
  90. 90.
    Zhao T, Zhu Y, Morinibu A et al (2014) HIF-1-mediated metabolic reprogramming reduces ROS levels and facilitates the metastatic colonization of cancers in lungs. Sci Rep 4:3793PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Sarsour EH, Venkataraman S, Kalen AL et al (2008) Manganese superoxide dismutase activity regulates transitions between quiescent and proliferative growth. Aging Cell 7(3):405–417PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Felty Q, Singh KP, Roy D (2005) Estrogen-induced G1/S transition of G0-arrested estrogen-dependent breast cancer cells is regulated by mitochondrial oxidant signaling. Oncogene 24(31):4883–4893PubMedCrossRefGoogle Scholar
  93. 93.
    Menon SG, Coleman MC, Walsh SA et al (2005) Differential susceptibility of nonmalignant human breast epithelial cells and breast cancer cells to thiol antioxidant-induced G(1)-delay. Antioxid Redox Signal 7(5–6):711–718PubMedCrossRefGoogle Scholar
  94. 94.
    Ruiz-Ramos R, Lopez-Carrillo L, Rios-Perez AD et al (2009) Sodium arsenite induces ROS generation, DNA oxidative damage, HO-1 and c-Myc proteins, NF-kappaB activation and cell proliferation in human breast cancer MCF-7 cells. Mutat Res 674(1–2):109–115PubMedCrossRefGoogle Scholar
  95. 95.
    Cullen JJ, Weydert C, Hinkhouse MM et al (2003) The role of manganese superoxide dismutase in the growth of pancreatic adenocarcinoma. Cancer Res 63(6):1297–1303PubMedGoogle Scholar
  96. 96.
    Browne SE, Roberts LJ, Dennery PA et al (2004) Treatment with a catalytic antioxidant corrects the neurobehavioral defect in ataxia-telangiectasia mice. Free Radic Biol Med 36(7):938–942PubMedCrossRefGoogle Scholar
  97. 97.
    Reichenbach J, Schubert R, Schindler D et al (2002) Elevated oxidative stress in patients with ataxia telangiectasia. Antioxid Redox Signal 4(3):465–469PubMedCrossRefGoogle Scholar
  98. 98.
    Pelicano H, Lu W, Zhou Y et al (2009) Mitochondrial dysfunction and reactive oxygen species imbalance promote breast cancer cell motility through a CXCL14-mediated mechanism. Cancer Res 69(6):2375–2383PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Chiarugi P (2008) From anchorage dependent proliferation to survival: lessons from redox signalling. IUBMB Life 60(5):301–307PubMedCrossRefGoogle Scholar
  100. 100.
    Taddei ML, Parri M, Mello T et al (2007) Integrin-mediated cell adhesion and spreading engage different sources of reactive oxygen species. Antioxid Redox Signal 9(4):469–481PubMedCrossRefGoogle Scholar
  101. 101.
    Broom OJ, Massoumi R, Sjölander A (2006) Alpha2beta1 integrin signalling enhances cyclooxygenase-2 expression in intestinal epithelial cells. J Cell Physiol 209(3):950–958PubMedCrossRefGoogle Scholar
  102. 102.
    Svineng G, Ravuri C, Rikardsen O et al (2008) The role of reactive oxygen species in integrin and matrix metalloproteinase expression and function. Connect Tissue Res 49(3):197–202PubMedCrossRefGoogle Scholar
  103. 103.
    Werner E, Werb Z (2002) Integrins engage mitochondrial function for signal transduction by a mechanism dependent on Rho GTPases. J Cell Biol 158(2):357–368PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Giannoni E, Fiaschi T, Ramponi G, Chiarugi P (2009) Redox regulation of anoikis resistance of metastatic prostate cancer cells: key role for Src and EGFR-mediated pro-survival signals. Oncogene 28(20):2074–2086PubMedCrossRefGoogle Scholar
  105. 105.
    Cadenas E (2004) Mitochondrial free radical production and cell signaling. Mol Aspects Med 25(1–2):17–26PubMedCrossRefGoogle Scholar
  106. 106.
    Simon HU, Haj-Yehia A, Levi-Schaffer F (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis Int J Program Cell Death 5(5):415–418CrossRefGoogle Scholar
  107. 107.
    Chung YM, Bae YS, Lee SY (2003) Molecular ordering of ROS production, mitochondrial changes, and caspase activation during sodium salicylate-induced apoptosis. Free Radic Biol Med 34(4):434–442PubMedCrossRefGoogle Scholar
  108. 108.
    Storz P (2007) Mitochondrial ROS--radical detoxification, mediated by protein kinase D. Trends Cell Biol 17(1):13–18PubMedCrossRefGoogle Scholar
  109. 109.
    Saitoh M, Nishitoh H, Fujii M et al (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17(9):2596–2606PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Takeda K, Matsuzawa A, Nishitoh H, Ichijo H (2003) Roles of MAPKKK ASK1 in stress-induced cell death. Cell Struct Funct 28(1):23–29PubMedCrossRefGoogle Scholar
  111. 111.
    You H, Yamamoto K, Mak TW (2006) Regulation of transactivation-independent proapoptotic activity of p53 by FOXO3a. Proc Natl Acad Sci U S A 103(24):9051–9056PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Schulze-Osthoff K, Beyaert R, Vandevoorde V et al (1993) Depletion of the mitochondrial electron transport abrogates the cytotoxic and gene-inductive effects of TNF. EMBO J 12(8):3095–3104PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Xu YC, Wu RF, Gu Y et al (2002) Involvement of TRAF4 in oxidative activation of c-Jun N-terminal kinase. J Biol Chem 277(31):28051–28057PubMedCrossRefGoogle Scholar
  114. 114.
    Leon G, MacDonagh L, Finn SP et al (2016) Cancer stem cells in drug resistant lung cancer: targeting cell surface markers and signaling pathways. Pharmacol Ther 158:71–90PubMedCrossRefGoogle Scholar
  115. 115.
    MacDonagh L, Gray SG, Breen E et al (2016) Lung cancer stem cells: the root of resistance. Cancer Lett 372(2):147–156PubMedCrossRefGoogle Scholar
  116. 116.
    Ho MM, Ng AV, Lam S, Hung JY (2007) Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 67(10):4827–4833PubMedCrossRefGoogle Scholar
  117. 117.
    Jiang F, Qiu Q, Khanna A et al (2009) Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res MCR 7(3):330–338PubMedCrossRefGoogle Scholar
  118. 118.
    Eramo A, Lotti F, Sette G et al (2008) Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15(3):504–514PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Yan X, Luo H, Zhou X et al (2013) Identification of CD90 as a marker for lung cancer stem cells in A549 and H446 cell lines. Oncol Rep 30(6):2733–2740PubMedCrossRefGoogle Scholar
  120. 120.
    Tian C, Huang D, Yu Y et al (2017) ABCG1 as a potential oncogene in lung cancer. Exp Ther Med 13(6):3189–3194PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Dai Y, Liu S, Zhang W-Q et al (2017) YAP1 regulates ABCG2 and cancer cell side population in human lung cancer cells. Oncotarget 8(3):4096–4109PubMedCrossRefGoogle Scholar
  122. 122.
    Nie S, Huang Y, Shi M et al (2018) Protective role of ABCG2 against oxidative stress in colorectal cancer and its potential underlying mechanism. Oncol Rep 40(4):2137–2146PubMedGoogle Scholar
  123. 123.
    Yu W-K, Wang Z, Fong C-C et al (2017) Chemoresistant lung cancer stem cells display high DNA repair capability to remove cisplatin-induced DNA damage. Br J Pharmacol 174(4):302–313PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Zeuner A, Francescangeli F, Contavalli P et al (2014) Elimination of quiescent/slow-proliferating cancer stem cells by Bcl-XL inhibition in non-small cell lung cancer. Cell Death Differ 21(12):1877–1888PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Singh S, Bora-Singhal N, Kroeger J et al (2013) βArrestin-1 and Mcl-1 modulate self-renewal growth of cancer stem-like side-population cells in non-small cell lung cancer. PLoS ONE 8(2):e55982PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Chong SJF, Low ICC, Pervaiz S (2014) Mitochondrial ROS and involvement of Bcl-2 as a mitochondrial ROS regulator. Mitochondrion 19(Pt A):39–48PubMedCrossRefGoogle Scholar
  127. 127.
    Wang K, Zhang T, Dong Q et al (2013) Redox homeostasis: the linchpin in stem cell self-renewal and differentiation. Cell Death Dis 4:e537PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Dong C, Yuan T, Wu Y et al (2013) Loss of FBP1 by Snail-mediated repression provides metabolic advantages in basal-like breast cancer. Cancer Cell 23(3):316–331PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Fang L, Zhu Q, Neuenschwander M et al (2016) A small-molecule antagonist of the β-catenin/TCF4 interaction blocks the self-renewal of cancer stem cells and suppresses tumorigenesis. Cancer Res 76(4):891–901PubMedCrossRefGoogle Scholar
  130. 130.
    Schieber MS, Chandel NS (2013) ROS links glucose metabolism to breast cancer stem cell and EMT phenotype. Cancer Cell 23(3):265–267PubMedCrossRefGoogle Scholar
  131. 131.
    Mut-Salud N, Álvarez PJ, Garrido JM, Carrasco E, Aránega A, Rodríguez-Serrano F (2016) Antioxidant intake and antitumor therapy: toward nutritional recommendations for optimal results. Oxid Med Cell Longev 2016:6719534PubMedCrossRefGoogle Scholar
  132. 132.
    Ogasawara MA, Zhang H (2009) Redox regulation and its emerging roles in stem cells and stem-like cancer cells. Antioxid Redox Signal 11(5):1107–1122PubMedCrossRefGoogle Scholar
  133. 133.
    Dey-Guha I, Wolfer A, Yeh AC, Albeck J, Darp R, Leon E et al (2011) Asymmetric cancer cell division regulated by AKT. Proc Natl Acad Sci U S A 108(31):12845–12850PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Lan D, Wang L (2018) He R, et al Exogenous glutathione contributes to cisplatin resistance in lung cancer A549 cells. Am J Transl Res 10(5):1295–1309PubMedPubMedCentralGoogle Scholar
  135. 135.
    Nagano O, Okazaki S, Saya H (2013) Redox regulation in stem-like cancer cells by CD44 variant isoforms. Oncogene 32(44):5191–5198PubMedCrossRefGoogle Scholar
  136. 136.
    Kwon T, Bak Y, Park Y-H et al (2016) Peroxiredoxin II is essential for maintaining stemness by redox regulation in liver cancer cells. Stem Cells Dayt Ohio 34(5):1188–1197CrossRefGoogle Scholar
  137. 137.
    Chandimali N, Jeong DK, Kwon T (2018) Peroxiredoxin II regulates cancer stem cells and stemness-associated properties of cancers. Cancers 10(9):305PubMedCentralCrossRefPubMedGoogle Scholar
  138. 138.
    Soini Y, Kinnula VL (2012) High association of peroxiredoxins with lung cancer. Lung Cancer Amst Neth 78(2):167CrossRefGoogle Scholar
  139. 139.
    Chandimali N, Huynh DL, Zhang JJ, Lee JC, Yu D-Y, Jeong DK et al (2018) MicroRNA-122 negatively associates with peroxiredoxin-II expression in human gefitinib-resistant lung cancer stem cells. Cancer Gene Ther 19Google Scholar
  140. 140.
    Lee KW, Lee DJ, Lee JY, Kang DH, Kwon J, Kang SW (2011) Peroxiredoxin II restrains DNA damage-induced death in cancer cells by positively regulating JNK-dependent DNA repair. J Biol Chem 286(10):8394–8404PubMedCrossRefGoogle Scholar
  141. 141.
    Soini Y, Kahlos K (2001) Näpänkangas U, et al Widespread expression of thioredoxin and thioredoxin reductase in non-small cell lung carcinoma. Clin Cancer Res 7(6):1750–1757PubMedGoogle Scholar
  142. 142.
    Cho H-Y, Reddy SP, Kleeberger SR (2006) Nrf2 defends the lung from oxidative stress. Antioxid Redox Signal 8(1–2):76–87PubMedCrossRefGoogle Scholar
  143. 143.
    Ohta T, Iijima K, Miyamoto M et al (2008) Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth. Cancer Res 68(5):1303–1309PubMedCrossRefGoogle Scholar
  144. 144.
    Ryoo I, Lee S, Kwak M-K (2016) Redox modulating NRF2: a potential mediator of cancer stem cell resistance. Oxid Med Cell Longev 2016:2428153PubMedCrossRefGoogle Scholar
  145. 145.
    Morgan MJ, Liu Z (2011) Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res 21(1):103–115PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Park HJ, Carr JR, Wang Z et al (2009) FoxM1, a critical regulator of oxidative stress during oncogenesis. EMBO J 28(19):2908–2918PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Yang DK, Son CH, Lee SK et al (2009) Forkhead box M1 expression in pulmonary squamous cell carcinoma: correlation with clinicopathologic features and its prognostic significance. Hum Pathol 40(4):464–470PubMedCrossRefGoogle Scholar
  148. 148.
    Kwok CTD, Leung MH, Qin J et al (2016) The Forkhead box transcription factor FOXM1 is required for the maintenance of cell proliferation and protection against oxidative stress in human embryonic stem cells. Stem Cell Res 16(3):651–661PubMedCrossRefGoogle Scholar
  149. 149.
    Fu Z, Cao X, Yang Y et al (2018) Upregulation of FoxM1 by MnSOD overexpression contributes to cancer stem-like cell characteristics in the lung cancer H460 cell line. Technol Cancer Res Treat 17:1533033818789635PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Jeannot V, Mazzaferro S, Lavaud J et al (2016) Targeting CD44 receptor-positive lung tumors using polysaccharide-based nanocarriers: Influence of nanoparticle size and administration route. Nanomedicine Nanotechnol Biol Med 12(4):921–932CrossRefGoogle Scholar
  151. 151.
    Benhar M, Shytaj IL, Stamler JS, Savarino A (2016) Dual targeting of the thioredoxin and glutathione systems in cancer and HIV. J Clin Invest 126(5):1630–1639PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Lagadinou ED, Sach A, Callahan K et al (2013) BCL-2 inhibition targets oxidative phosphorylation and selectively eradicates quiescent human leukemia stem cells. Cell Stem Cell 12(3):329–341PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Ren D, Villeneuve NF, Jiang T et al (2011) Brusatol enhances the efficacy of chemotherapy by inhibiting the Nrf2-mediated defense mechanism. Proc Natl Acad Sci U S A 108(4):1433–1438PubMedPubMedCentralCrossRefGoogle Scholar
  154. 154.
    Sun X, Wang Q, Wang Y, Du L, Xu C, Liu Q (2016) Brusatol enhances the radiosensitivity of A549 cells by promoting ROS production and enhancing DNA damage. Int J Mol Sci 17(7):997PubMedCentralCrossRefPubMedGoogle Scholar
  155. 155.
    Zhang H, Mi J-Q, Fang H et al (2013) Preferential eradication of acute myelogenous leukemia stem cells by fenretinide. Proc Natl Acad Sci U S A 110(14):5606–5611PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Deblina Guha
    • 1
  • Shruti Banerjee
    • 1
  • Shravanti Mukherjee
    • 1
  • Apratim Dutta
    • 1
  • Tanya Das
    • 1
    Email author
  1. 1.Division of Molecular MedicineBose InstituteKolkataIndia

Personalised recommendations

Cite chapter

Buy options