Involvement of ERK-Nrf-2 Signaling in Ionizing Radiation Induced Cell Death in Normal and Tumor Cells

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Patwardhan, Raghavendra S ^a   Checker, Rahul ^a   Sharma, Deepak ^a   Sandur, Santosh K ^a   Sainis, Krishna B ^a  

^a BHABHA ATOMIC RESEARCH CENTRE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL LEVEL; CELL NUCLEUS; CLONOGENESIS; CONTROLLED STUDY; GENE ACTIVATION; GENE FUNCTION; GENE LOCATION; GENE SILENCING; IONIZING RADIATION; LYMPHOMA CELL; MALE; MOUSE; NONHUMAN; OXIDATION REDUCTION POTENTIAL; RADIATION RESPONSE; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; SPLEEN LYMPHOCYTE; T CELL LYMPHOMA; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CELL DEATH; CELL LINE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLOW CYTOMETRY; MALE; MICE; MICE, INBRED C57BL; NF-E2-RELATED FACTOR 2; RADIATION, IONIZING; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

MURINAE;

EID: 84878948638     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065929     Document Type: Article

References (50)

1. Deorukhkar A, Krishnan S, (2010) Targeting inflammatory pathways for tumor radiosensitization. Biochem Pharmacol 80: 1904-1914.
2. D'Autreaux B, Toledano MB, (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8: 813-824.
3. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, et al. (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458: 780-783.
4. Shankar B, Kumar SS, Sainis KB, (2003) Generation of reactive oxygen species and radiation response in lymphocytes and tumor cells. Radiat Res 160: 478-487.
5. McDonald JT, Kim K, Norris AJ, Vlashi E, Phillips TM, et al. (2011) Ionizing radiation activates the Nrf2 antioxidant response. Cancer Res 70: 8886-8895.
6. Klaunig JE, Wang Z, Pu X, Zhou S, (2011) Oxidative stress and oxidative damage in chemical carcinogenesis. Toxicol Appl Pharmacol 254: 86-99.
7. Nguyen T, Nioi P, Pickett CB, (2009) The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284: 13291-13295.
8. Kaspar JW, Niture SK, Jaiswal AK, (2009) Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 47: 1304-1309.
9. Surh YJ, Kundu JK, Na HK, (2008) Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med 74: 1526-1539.
10. Ikeda H, Nishi S, Sakai M, (2004) Transcription factor Nrf2/MafK regulates rat placental glutathione S-transferase gene during hepatocarcinogenesis. Biochem J 380: 515-521.
11. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, et al. (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13: 76-86.
12. Sun Z, Huang Z, Zhang DD, (2009) Phosphorylation of Nrf2 at multiple sites by MAP kinases has a limited contribution in modulating the Nrf2-dependent antioxidant response. PLoS One 4: e6588.
13. Kim AN, Jeon WK, Lee JJ, Kim BC, (2011) Up-regulation of heme oxygenase-1 expression through CaMKII-ERK1/2-Nrf2 signaling mediates the anti-inflammatory effect of bisdemethoxycurcumin in LPS-stimulated macrophages. Free Radic Biol Med 49: 323-331.
14. Hayes JD, McMahon M, (2006) The double-edged sword of Nrf2: subversion of redox homeostasis during the evolution of cancer. Mol Cell 21: 732-734.
15. Ryter SW, Kim HP, Hoetzel A, Park JW, Nakahira K, et al. (2007) Mechanisms of cell death in oxidative stress. Antioxid Redox Signal 9: 49-89.
16. Rodemann HP, (2009) Molecular radiation biology: perspectives for radiation oncology. Radiother Oncol 92: 293-298.
17. Jackson AL, Loeb LA, (2001) The contribution of endogenous sources of DNA damage to the multiple mutations in cancer. Mutat Res 477: 7-21.
18. Cakir Y, Ballinger SW, (2005) Reactive species-mediated regulation of cell signaling and the cell cycle: the role of MAPK. Antioxid Redox Signal 7: 726-740.
19. den Hertog J, Groen A, van der Wijk T, (2005) Redox regulation of protein-tyrosine phosphatases. Arch Biochem Biophys 434: 11-15.
20. Meng TC, Fukada T, Tonks NK, (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 9: 387-399.
21. Aggarwal BB, Shishodia S, Sandur SK, Pandey MK, Sethi G, (2006) Inflammation and cancer: how hot is the link? Biochem Pharmacol 72: 1605-1621.
22. Aggarwal BB, Vijayalekshmi RV, Sung B, (2009) Targeting inflammatory pathways for prevention and therapy of cancer: short-term friend, long-term foe. Clin Cancer Res 15: 425-430.
23. Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB, (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 49: 1603-1616.
24. Li F, Sethi G, (2011) Targeting transcription factor NF-kappaB to overcome chemoresistance and radioresistance in cancer therapy. Biochim Biophys Acta 1805: 167-180.
25. Tanaka H, Matsumura I, Ezoe S, Satoh Y, Sakamaki T, et al. (2002) E2F1 and c-Myc potentiate apoptosis through inhibition of NF-kappaB activity that facilitates MnSOD-mediated ROS elimination. Mol Cell 9: 1017-1029.
26. Wang XJ, Sun Z, Villeneuve NF, Zhang S, Zhao F, et al. (2008) Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 29: 1235-1243.
27. DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, et al. (2011) Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475: 106-109.
28. Li W, Kong AN, (2009) Molecular mechanisms of Nrf2-mediated antioxidant response. Mol Carcinog 48: 91-104.
29. Fang J, Seki T, Maeda H, (2009) Therapeutic strategies by modulating oxygen stress in cancer and inflammation. Adv Drug Deliv Rev 61: 290-302.
30. Singh A, Boldin-Adamsky S, Thimmulappa RK, Rath SK, Ashush H, et al. (2008) RNAi-mediated silencing of nuclear factor erythroid-2-related factor 2 gene expression in non-small cell lung cancer inhibits tumor growth and increases efficacy of chemotherapy. Cancer Res 68: 7975-7984.
31. Kwak MK, Itoh K, Yamamoto M, Kensler TW, (2002) Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol Cell Biol 22: 2883-2892.
32. Surh YJ, Na HK, (2008) NF-kappaB and Nrf2 as prime molecular targets for chemoprevention and cytoprotection with anti-inflammatory and antioxidant phytochemicals. Genes Nutr 2: 313-317.
33. Surh YJ, (2008) NF-kappa B and Nrf2 as potential chemopreventive targets of some anti-inflammatory and antioxidative phytonutrients with anti-inflammatory and antioxidative activities. Asia Pac J Clin Nutr 17Suppl 1: 269-272.
34. Ohta T, Iijima K, Miyamoto M, Nakahara I, Tanaka H, et al. (2008) Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth. Cancer Res 68: 1303-1309.
35. Hayes JD, McMahon M, (2009) NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci 34: 176-188.
36. Khan NM, Sandur SK, Checker R, Sharma D, Poduval TB, et al. (2011) Pro-oxidants ameliorate radiation-induced apoptosis through activation of the calcium-ERK1/2-Nrf2 pathway. Free Radic Biol Med 51: 115-128.
37. Zipper LM, Mulcahy RT, (2003) Erk activation is required for Nrf2 nuclear localization during pyrrolidine dithiocarbamate induction of glutamate cysteine ligase modulatory gene expression in HepG2 cells. Toxicol Sci 73: 124-134.
38. Checker R, Chatterjee S, Sharma D, Gupta S, Variyar P, et al. (2008) Immunomodulatory and radioprotective effects of lignans derived from fresh nutmeg mace (Myristica fragrans) in mammalian splenocytes. Int Immunopharmacol 8: 661-669.
39. Muppidi J, Porter M, Siegel RM (2004) Measurement of apoptosis and other forms of cell death. Curr Protoc Immunol Chapter 3: Unit 3 17.
40. Checker R, Sharma D, Sandur SK, Khanam S, Poduval TB, (2009) Anti-inflammatory effects of plumbagin are mediated by inhibition of NF-kappaB activation in lymphocytes. Int Immunopharmacol 9: 949-958.
41. Rahman I, Kode A, Biswas SK, (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1: 3159-3165.
42. Patwardhan RS, Checker R, Sharma D, Kohli V, Priyadarsini KI, et al. (2011) Dimethoxycurcumin, a metabolically stable analogue of curcumin, exhibits anti-inflammatory activities in murine and human lymphocytes. Biochem Pharmacol 82: 642-657.
43. Kunwar A, Jayakumar S, Srivastava AK, Priyadarsini KI (2011) Dimethoxycurcumin-induced cell death in human breast carcinoma MCF7 cells: evidence for pro-oxidant activity, mitochondrial dysfunction, and apoptosis. Arch Toxicol.
44. Sandur SK, Ichikawa H, Pandey MK, Kunnumakkara AB, Sung B, et al. (2007) Role of pro-oxidants and antioxidants in the anti-inflammatory and apoptotic effects of curcumin (diferuloylmethane). Free Radic Biol Med 43: 568-580.
45. Sandur SK, Ichikawa H, Sethi G, Ahn KS, Aggarwal BB, (2006) Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone) suppresses NF-kappaB activation and NF-kappaB-regulated gene products through modulation of p65 and IkappaBalpha kinase activation, leading to potentiation of apoptosis induced by cytokine and chemotherapeutic agents. J Biol Chem 281: 17023-17033.
46. Ryter SW, Alam J, Choi AM, (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86: 583-650.
47. Willis D, Moore AR, Frederick R, Willoughby DA, (1996) Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat Med 2: 87-90.
48. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S, (2011) Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 80: 1895-1903.
49. Copple IM, Goldring CE, Kitteringham NR, Park BK, (2008) The Nrf2-Keap1 defence pathway: role in protection against drug-induced toxicity. Toxicology 246: 24-33.
50. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, et al. (2003) Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 35: 238-245.