Advertisement

Biochemistry (Moscow)

, Volume 78, Issue 2, pp 111–126 | Cite as

Keap1-Nrf2 signaling pathway: Mechanisms of regulation and role in protection of cells against toxicity caused by xenobiotics and electrophiles

  • K. T. TurpaevEmail author
Review

Abstract

The transcription factor Nrf2 governs the expression of a considerable group of genes involved in cell protection against oxidants, electrophiles, and genotoxic compounds. The activity of Nrf2 is sensitive to xenobiotics and endogenous electrophiles. Nrf2 is negatively regulated by specific suppressor protein Keap1, which is also a receptor of electrophiles and adapter for Cul3 ubiquitin ligase. Electrophiles react with critical thiol groups of Keap1 leading to the loss of its ability to inhibit Nrf2. The Keap1-Nrf2 signaling pathway also down-regulates NF-κB transcriptional activity and attenuates cytokine-mediated induction of proinflammatory genes. Pharmacological activation of the Keap1-Nrf2 pathway can be used for treatment and prevention of many diseases. Widely known natural Keap1-Nrf2 activators include curcumin, quercetin, resveratrol, and sulforaphane. The most effective Keap1-Nrf2 activators are synthetic oleanane triterpenoids.

Key words

protective genes xenobiotics thiols electrophiles Keap1 Nrf2 

Abbreviations

AKR

aldo-keto reductase

ARE

antioxidant response element

CBP

cAMP-responsive element-binding protein-binding protein (protein that binds the protein binding to the cAMP sensitive regulatory region)

COX2

cyclooxygenase 2

15d-PGJ2

15-deoxy-Δ12,14-prostaglandin J2

GSK-3

glycogen synthase kinase 3

GST

glutathione-S-transferase

HO-1

heme oxygenase 1

iNOS

inducible nitric oxide synthase

MRP

multidrug resistant protein

NQO1

NAD(P)H:quinone oxidoreductase 1

PPARγ

peroxisome proliferator-activated receptor γ

PRDX

peroxiredoxin

ROS

reactive oxygen species

SGK-1

serum- and glucocorticoid-induced protein kinase 1

tBHQ

tert-butylhydroquinone

XRE

xenobiotic response element (the regulatory region sensitive to xenobiotics)

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Hayes, J. D., McMahon, M., Chowdhry, S., and Dinkova-Kostova, A. T. (2010) Antioxid. Redox Signal., 13, 1713–1748.PubMedCrossRefGoogle Scholar
  2. 2.
    Baird, L., and Dinkova-Kostova, A. T. (2011) Arch. Toxicol., 85, 241–272.PubMedCrossRefGoogle Scholar
  3. 3.
    Gupta, S. C., Kim, J. H., Prasad, S., and Aggarwal, B. B. (2010) Cancer Metastasis Rev., 29, 405–434.PubMedCrossRefGoogle Scholar
  4. 4.
    Dinkova-Kostova, A. T., and Talalay, P. (2008) Mol. Nutr. Food Res., 52, 128–138.Google Scholar
  5. 5.
    Paine, A., Eiz-Vesper, B., Blasczyk, R., and Immenschuh, S. (2010) Biochem. Pharmacol., 80, 1895–1903.PubMedCrossRefGoogle Scholar
  6. 6.
    Dinkova-Kostova, A. T., and Talalay, P. (2010) Arch. Biochem. Biophys., 501, 116–123.PubMedCrossRefGoogle Scholar
  7. 7.
    Winterbourn, C. C., and Hampton, M. B. (2008) Free Radic. Biol. Med., 45, 549–561.PubMedCrossRefGoogle Scholar
  8. 8.
    Shuvaeva, T. M., Novoselov, V. I., Fesenko, E. E., and Lipkin, V. M. (2009) Bioorg. Khim., 35, 581–596.PubMedGoogle Scholar
  9. 9.
    Abbas, K., Breton, J., Planson, A. G., Bouton, C., Bignon, J., Seguin, C., Riquier, S., Toledano, M. B., and Drapier, J. C. (2011) Free Radic. Biol. Med., 51, 107–114.PubMedCrossRefGoogle Scholar
  10. 10.
    Lyakhovich, V. V., Vavilin, V. A., Zenkov, N. K., and Menshchikova, E. B. (2006) Biochemistry (Moscow), 71, 962–974.CrossRefGoogle Scholar
  11. 11.
    Rushmore, T. H., and Pickett, C. B. (1990) J. Biol. Chem., 265, 14648–14653.PubMedGoogle Scholar
  12. 12.
    Friling, R. S., Bensimon, A., Tichauer, Y., and Daniel, V. (1990) Proc. Natl. Acad. Sci. USA, 87, 6258–6262.PubMedCrossRefGoogle Scholar
  13. 13.
    Liby, K., Hock, T., Yore, M. M., Suh, N., Place, A. E., Risingsong, R., Williams, C. R., Royce, D. B., Honda, T., Honda, Y., Gribble, G. W., Hill-Kapturczak, N., Agarwal, A., and Sporn, M. B. (2005) Cancer Res., 65, 4789–4798.PubMedCrossRefGoogle Scholar
  14. 14.
    Chambers, K. F., Bacon, J. R., Kemsley, E. K., Mills, R. D., Ball, R. Y., Mithen, R. F., and Traka, M. H. (2009) Prostate, 69, 1411–1421.PubMedCrossRefGoogle Scholar
  15. 15.
    MacLeod, A. K., McMahon, M., Plummer, S. M., Higgins, L. G., Penning, T. M., Igarashi, K., and Hayes, J. D. (2009) Carcinogenesis, 30, 1571–1580.PubMedCrossRefGoogle Scholar
  16. 16.
    Blank, V. (2008) J. Mol. Biol., 376, 913–925.PubMedCrossRefGoogle Scholar
  17. 17.
    Levy, S., Jaiswal, A. K., and Forman, H. J. (2009) Free Radic. Biol. Med., 47, 1172–1179.PubMedCrossRefGoogle Scholar
  18. 18.
    Biswas, M., and Chan, J. Y. (2010) Toxicol. Appl. Pharmacol., 244, 16–20.PubMedCrossRefGoogle Scholar
  19. 19.
    Taguchi, K., Motohashi, H., and Yamamoto, M. (2011) Genes Cells, 16, 123–140.PubMedCrossRefGoogle Scholar
  20. 20.
    Villeneuve, N. F., Lau, A., and Zhang, D. D. (2010) Antioxid. Redox Signal., 13, 1699–1712.PubMedCrossRefGoogle Scholar
  21. 21.
    Kobayashi, A., Kang, M. I., Watai, Y., Tong, K. I., Shibata, T., Uchida, K., and Yamamoto, M. (2006) Mol. Cell Biol., 26, 221–229.PubMedCrossRefGoogle Scholar
  22. 22.
    Dinkova-Kostova, A. T., Holtzclaw, W. D., and Wakabayashi, N. (2005) Biochemistry, 44, 6889–6899.PubMedCrossRefGoogle Scholar
  23. 23.
    Tong, K. I., Katoh, Y., Kusunoki, H., Itoh, K., Tanaka, T., and Yamamoto, M. (2006) Mol. Cell. Biol., 26, 2887–2900.PubMedCrossRefGoogle Scholar
  24. 24.
    Willems, A. R., Schwab, M., and Tyers, M. (2004) Biochim. Biophys. Acta, 1695, 133–170.PubMedCrossRefGoogle Scholar
  25. 25.
    He, X., Chen, M. G., and Ma, Q. (2008) Chem. Res. Toxicol., 21, 1375–1383.PubMedCrossRefGoogle Scholar
  26. 26.
    Okuyama, T., Inoue, H., Ookuma, S., Satoh, T., Kano, K., Honjoh, S., Hisamoto, N., Matsumoto, K., and Nishida, E. (2010) J. Biol. Chem., 285, 30274–30281.PubMedCrossRefGoogle Scholar
  27. 27.
    Sykiotis, G. P., and Bohmann, D. (2010) Sci. Signal., 3, re3.PubMedCrossRefGoogle Scholar
  28. 28.
    Ivanov, A. V., Smirnova, O. A., Ivanova, O. N., Masalova, O. V., Kochetkov, S. N., and Isaguliants, M. G. (2011) PLoS One, 6, e24957.PubMedCrossRefGoogle Scholar
  29. 29.
    Niture, S. K., Jain, A. K., Shelton, P. M., and Jaiswal, A. K. (2011) J. Biol. Chem., 286, 28821–28832.PubMedCrossRefGoogle Scholar
  30. 30.
    Niture, S. K., Kaspar, J. W., Shen, J., and Jaiswal, A. K. (2010) Toxicol. Appl. Pharmacol., 244, 37–42.PubMedCrossRefGoogle Scholar
  31. 31.
    Sun, Z., Huang, Z., and Zhang, D. D. (2009) PLoS One, 24, e6588.CrossRefGoogle Scholar
  32. 32.
    Devling, T. W., Lindsay, C. D., McLellan, L. I., McMahon, M., and Hayes, J. D. (2005) Proc. Natl. Acad. Sci. USA, 102, 7280–7285.PubMedCrossRefGoogle Scholar
  33. 33.
    Turpaev, K., Ermolenko, M., Cresteil, T., and Drapier, J. C. (2011) Biochem. Pharmacol., 82, 535–547.PubMedCrossRefGoogle Scholar
  34. 34.
    Wakabayashi, N., Slocum, S. L., Skoko, J. J., Shin, S., and Kensler, T. W. (2010) Antioxid. Redox Signal., 13, 1649–1663.PubMedCrossRefGoogle Scholar
  35. 35.
    Vaz, M., Machireddy, N., Irving, A., Potteti, H. R., Chevalier, K., Kalvakolanu, D., and Reddy, S. P. (2012) Mol. Cell. Biol., 32, 1694–1709.PubMedCrossRefGoogle Scholar
  36. 36.
    Chen, W., Sun, Z., Wang, X. J., Jiang, T., Huang, Z., Fang, D., and Zhang, D. D. (2009) Mol. Cell., 34, 663–673.PubMedCrossRefGoogle Scholar
  37. 37.
    Liu, G. H., Qu, J., and Shen, X. (2008) Biochim. Biophys. Acta, 1783, 713–727.PubMedCrossRefGoogle Scholar
  38. 38.
    Dinkova-Kostova, A. T., Holtzclaw, W. D., and Kensler, T. W. (2005) Chem. Res. Toxicol., 18, 1779–1791.PubMedCrossRefGoogle Scholar
  39. 39.
    Tkachev, V. O., Menshchikova, E. B., and Zenkov, N. K. (2011) Biochemistry (Moscow), 76, 407–422.CrossRefGoogle Scholar
  40. 40.
    Yamamoto, T., Suzuki, T., Kobayashi, A., Wakabayashi, J., Maher, J., Motohashi, H., and Yamamoto, M. (2008) Mol. Cell. Biol., 28, 2758–2770.PubMedCrossRefGoogle Scholar
  41. 41.
    Zhang, D. D., and Hannink, M. (2003) Mol. Cell. Biol., 23, 8137–8151.PubMedCrossRefGoogle Scholar
  42. 42.
    Kobayashi, M., Li, L., Iwamoto, N., Nakajima-Takagi, Y., Kaneko, H., Nakayama, Y., Eguchi, M., Wada, Y., Kumagai, Y., and Yamamoto, M. (2009) Mol. Cell. Biol., 29, 493–502.PubMedCrossRefGoogle Scholar
  43. 43.
    Fourquet, S., Guerois, R., Biard, D., and Toledano, M. B. (2010) J. Biol. Chem., 285, 8463–8471.PubMedCrossRefGoogle Scholar
  44. 44.
    McMahon, M., Lamont, D. J., Beattie, K. A., and Hayes, J. D. (2010) Proc. Natl. Acad. Sci. USA, 107, 18838–18843.PubMedCrossRefGoogle Scholar
  45. 45.
    Eggler, A. L., Small, E., Hannink, M., and Mesecar, A. D. (2009) Biochem. J., 422, 171–180.PubMedCrossRefGoogle Scholar
  46. 46.
    Wakabayashi, N., Itoh, K., Wakabayashi, J., Motohashi, H., Noda, S., Takahashi, S., Imakado, S., Kotsuji, T., Otsuka, F., Roop, D. R., Harada, T., Engel, J. D., and Yamamoto, M. (2003) Nat. Genet., 35, 238–245.PubMedCrossRefGoogle Scholar
  47. 47.
    Hong, F., Freeman, M. L., and Liebler, D. C. (2005) Chem. Res. Toxicol., 18, 1917–1926.PubMedCrossRefGoogle Scholar
  48. 48.
    Luo, Y., Eggler, A. L., Liu, D., Liu, G., Mesecar, A. D., and van Breemen, R. B. (2007) J. Am. Soc. Mass. Spectrom., 18, 2226–2232.PubMedCrossRefGoogle Scholar
  49. 49.
    Hu, C., Eggler, A. L., Mesecar, A. D., and van Breemen, R. B. (2011) Chem. Res. Toxicol., 24, 515–521.PubMedCrossRefGoogle Scholar
  50. 50.
    Dinkova-Kostova, A. T., Holtzclaw, W. D., Cole, R. N., Itoh, K., Wakabayashi, N., Katoh, Y., Yamamoto, M., and Talalay, P. (2002) Proc. Natl. Acad. Sci. USA, 99, 11908–11913.PubMedCrossRefGoogle Scholar
  51. 51.
    Ahn, Y. H., Hwang, Y., Liu, H., Wang, X. J., Zhang, Y., Stephenson, K. K., Boronina, T. N., Cole, R. N., Dinkova-Kostova, A. T., Talalay, P., and Cole, P. A. (2010) Proc. Natl. Acad. Sci. USA, 107, 9590–9595.PubMedCrossRefGoogle Scholar
  52. 52.
    Holland, R., Hawkins, A. E., Eggle, A. L., Mesecar, A. D., Fabris, D., and Fishbein, J. C. (2008) Chem. Res. Toxicol., 21, 2051–2060.PubMedCrossRefGoogle Scholar
  53. 53.
    Rachakonda, G., Xiong, Y., Sekha, K. R., Stamer, S. L., Liebler, D. C., and Freeman, M. L. (2008) Chem. Res. Toxicol., 21, 705–710.PubMedCrossRefGoogle Scholar
  54. 54.
    Hong, F., Sekhar, K. R., Freeman, M. L., and Liebler, D. C. (2005) J. Biol. Chem., 280, 31768–31775.PubMedCrossRefGoogle Scholar
  55. 55.
    Sawa, T., Zaki, M. H., Okamoto, T., Akuta, T., Tokutomi, Y., Kim-Mitsuyama, S., Ihara, H., Kobayashi, A., Yamamoto, M., Fujii, S., Arimoto, H., and Akaike, T. (2007) Nat. Chem. Biol., 3, 727–735.PubMedCrossRefGoogle Scholar
  56. 56.
    Akaike, T., Fujii, S., Sawa, T., and Ihara, H. (2010) Nitric Oxide, 23, 166–174.PubMedCrossRefGoogle Scholar
  57. 57.
    Fujii, S., Sawa, T., Ihara, H., Tong, K. I., Ida, T., Okamoto, T., Ahtesham, A. K., Ishima, Y., Motohashi, H., Yamamoto, M., and Akaike, T. (2010) J. Biol. Chem., 285, 23970–23984.PubMedCrossRefGoogle Scholar
  58. 58.
    Boots, A. W., Balk, J. M., Bast, A., and Haenen, G. R. (2005) Biochem. Biophys. Res. Commun., 338, 923–929.PubMedCrossRefGoogle Scholar
  59. 59.
    Dinkova-Kostova, A. T., Talalay, P., Sharkey, J., Zhang, Y., Holtzclaw, W. D., Wang, X. J., David, E., Schiavoni, K. H., Finlayson, S., Mierke, D. F., and Honda, T. (2010) J. Biol. Chem., 285, 33747–33755.PubMedCrossRefGoogle Scholar
  60. 60.
    Kohle, C., and Bock, K. W. (2006) Biochem. Pharmacol., 72, 795–805.PubMedCrossRefGoogle Scholar
  61. 61.
    Hayes, J. D., Dinkova-Kostova, A. T., and McMahon, M. (2009) Toxicol. Sci., 111, 199–201.PubMedCrossRefGoogle Scholar
  62. 62.
    Pustylnyak, V. O., Gulyaeva, L. F., and Lyakhovich, V. V. (2007) Biochemistry (Moscow), 72, 608–617.CrossRefGoogle Scholar
  63. 63.
    Miao, W., Hu, L., Scrivens, P. J., and Batist, G. (2005) J. Biol. Chem., 280, 20340–20348.PubMedCrossRefGoogle Scholar
  64. 64.
    Yeager, R. L., Reisman, S. A., Aleksunes, L. M., and Klaassen, C. D. (2009) Toxicol. Sci., 111, 238–246.PubMedCrossRefGoogle Scholar
  65. 65.
    Giaginis, C., Giagini, A., and Theocharis, S. (2009) Pharmacol. Res., 60, 160–169.PubMedCrossRefGoogle Scholar
  66. 66.
    Zieleniak, A., Wojcik, M., and Wozniak, L. A. (2008) Arch. Immunol. Ther. Exp., 56, 331–345.CrossRefGoogle Scholar
  67. 67.
    Kim, E. H., and Surh, Y. J. (2006) Biochem. Pharmacol., 72, 1516–1528.PubMedCrossRefGoogle Scholar
  68. 68.
    Ramanan, S., Kooshki, M., Zhao, W., Hsu, F. C., and Robbins, M. E. (2008) Free Radic. Biol. Med., 45, 1695–1704.PubMedCrossRefGoogle Scholar
  69. 69.
    Liby, K. T., Yore, M. M., and Sporn, M. B. (2007) Nat. Rev. Cancer, 7, 357–369.PubMedCrossRefGoogle Scholar
  70. 70.
    Tsao, T., Kornblau, S., Safe, S., Watt, J. C., Ruvolo, V., Chen, W., Qiu, Y., Coombes, K. R., Ju, Z., Abdelrahim, M., Schober, W., Ling, X., Kardassis, D., Meyer, C., Schimmer, A., Kantarjian, H., Andreeff, M., and Konopleva, M. (2010) Cancer Res., 70, 4949–4960.PubMedCrossRefGoogle Scholar
  71. 71.
    Heilman, J. M., Burke, T. J., McClain, C. J., and Watson, W. H. (2011) Free Radic. Biol. Med., 51, 1533–1542.PubMedCrossRefGoogle Scholar
  72. 72.
    Collett, G. P., and Campbell, F. C. (2004) Carcinogenesis, 25, 2183–2189.PubMedCrossRefGoogle Scholar
  73. 73.
    Couch, R. D., Ganem, N. J., Zhou, M., Popov, V. M., Honda, T., Veenstra, T. D., Sporn, M. B., and Anderson, A. C. (2006) Mol. Pharmacol., 69, 1158–1165.PubMedCrossRefGoogle Scholar
  74. 74.
    Turpaev, K., and Drapier, J. C. (2009) Eur. J. Pharmacol., 606, 1–8.PubMedCrossRefGoogle Scholar
  75. 75.
    Deeb, D., Gao, X., Jiang, H., Janic, B., Arbab, A. S., Rojanasakul, Y., Dulchavsky, S. A., and Gautam, S. C. (2010) Biochem. Pharmacol., 79, 350–360.PubMedCrossRefGoogle Scholar
  76. 76.
    Samudio, I., Konopleva, M., Hail, N., Shi, Y. X., McQueen, T., Hsu, T., Evans, R., Honda, T., Gribble, G. W., Sporn, M., Gilbert, H. F., Safe, S., and Andreeff, M. (2005) J. Biol. Chem., 280, 36273–36282.PubMedCrossRefGoogle Scholar
  77. 77.
    Pautz, A., Art, J., Hahn, S., Nowag, S., Voss, C., and Kleinert, H. (2010) Nitric Oxide, 23, 75–93.PubMedCrossRefGoogle Scholar
  78. 78.
    Kang, Y. J., Mbonye, U. R., DeLong, C. J., Wada, M., and Smith, W. L. (2007) Prog. Lipid Res., 46, 108–125.PubMedCrossRefGoogle Scholar
  79. 79.
    Dinkova-Kostova, A. T., Liby, K. T., Stephenson, K. K., Holtzclaw, W. D., Gao, X., Suh, N., Williams, C., Risingsong, R., Honda, T., Gribble, G. W., Sporn, M. B., and Talalay, P. (2005) Proc. Natl. Acad. Sci. USA, 102, 4584–4589.PubMedCrossRefGoogle Scholar
  80. 80.
    Liu, H., Dinkova-Kostova, A. T., and Talalay, P. (2008) Proc. Natl. Acad. Sci. USA, 105, 15926–15931.PubMedCrossRefGoogle Scholar
  81. 81.
    Ahmad, R., Raina, D., Meyer, C., Kharbanda, S., and Kufe, D. (2006) J. Biol. Chem., 281, 35764–35769.PubMedCrossRefGoogle Scholar
  82. 82.
    Wu, R. P., Hayashi, T., Cottam, H. B., Jin, G., Yao, S., Wu, C. C., Rosenbach, M. D., Corr, M., Schwab, R. B., and Carson, D. A. (2010) Proc. Natl. Acad. Sci. USA, 107, 7479–7484.PubMedCrossRefGoogle Scholar
  83. 83.
    Dinkova-Kostova, A. T., Massiah, M. A., Bozak, R. E., Hicks, R. J., and Talalay, P. (2001) Proc. Natl. Acad. Sci. USA, 98, 3404–3409.PubMedCrossRefGoogle Scholar
  84. 84.
    Deeb, D., Gao, X., Dulchavsky, S. A., and Gautam, S. C. (2007) Anticancer Res., 27, 3035–3044.PubMedGoogle Scholar
  85. 85.
    Jackson, J. K., Higo, T., Hunter, W. L., and Burt, H. M. (2006) Inflamm. Res., 55, 168–175.PubMedCrossRefGoogle Scholar
  86. 86.
    Gao, X., Deeb, D., Jiang, H., Liu, Y., Dulchavsky, S. A., and Gautam, S. C. (2007) J. Neurooncol., 84, 147–157.PubMedCrossRefGoogle Scholar
  87. 87.
    Liby, K., Yore, M. M., Roebuck, B. D., Baumgartner, K. J., Honda, T., Sundararajan, C., Yoshizawa, H., Gribble, G. W., Williams, C. R., Risingsong, R., Royce, D. B., Dinkova-Kostova, A. T., Stephenson, K. K., Egner, P. A., Yates, M. S., Groopman, J. D., Kensler, T. W., and Sporn, M. B. (2008) Cancer Res., 68, 6727–6733.PubMedCrossRefGoogle Scholar
  88. 88.
    Kim, J. E., You, D. J., Lee, C., Ahn, C., Seong, J. Y., and Hwang, J. I. (2010) Cell. Signal., 22, 1645–1654.PubMedCrossRefGoogle Scholar
  89. 89.
    Lee, Y., Shin, D. H., Kim, J. H., Hong, S., Choi, D., Kim, Y. J., Kwak, M. K., and Jung, Y. (2010) Eur. J. Pharmacol., 643, 21–28.PubMedCrossRefGoogle Scholar
  90. 90.
    Sporn, M. B., Liby, K. T., Yore, M. M., Fu, L., Lopchuk, J. M., and Gribble, G. W. (2011) J. Nat. Prod., 74, 537–545.PubMedCrossRefGoogle Scholar
  91. 91.
    Couch, R. D., Browning, R. G., Honda, T., Gribble, G. W., Wright, D. L., Sporn, M. B., and Anderson, A. C. (2005) Bioorg. Med. Chem. Lett., 15, 2215–2219.PubMedCrossRefGoogle Scholar
  92. 92.
    Yore, M. M., Liby, K. T., Honda, T., Gribble, G. W., and Sporn, M. B. (2006) Mol. Cancer Ther., 5, 3232–3239.PubMedCrossRefGoogle Scholar
  93. 93.
    Albini, A., and Sporn, M. B. (2007) Nat. Rev. Cancer, 7, 139–147.PubMedCrossRefGoogle Scholar
  94. 94.
    Dinkova-Kostova, A. T., and Wang, X. J. (2011) Chem. Biol. Interact., 192, 101–106.PubMedCrossRefGoogle Scholar
  95. 95.
    Hur, W., and Gray, N. S. (2011) Curr. Opin. Chem. Biol., 15, 162–173.PubMedCrossRefGoogle Scholar
  96. 96.
    Ishii, T., Ishikawa, M., Miyoshi, N., Yasunaga, M., Akagawa, M., Uchida, K., and Nakamura, Y. (2009) Chem. Res. Toxicol., 22, 1689–1698.PubMedCrossRefGoogle Scholar
  97. 97.
    Chung, S., Yao, H., Caito, S., Hwang, J. W., Arunachalam, G., and Rahman, I. (2010) Arch. Biochem. Biophys., 501, 79–90.PubMedCrossRefGoogle Scholar
  98. 98.
    Lei, M., Wang, J. G., Xiao, D. M., Fan, M., Wang, D. P., Xiong, J. Y., Chen, Y., Ding, Y., and Liu, S. L. (2012) Eur. J. Pharmacol., 674, 73–79.PubMedCrossRefGoogle Scholar
  99. 99.
    Zhang, Y. (2000) Carcinogenesis, 21, 1175–1182.PubMedCrossRefGoogle Scholar
  100. 100.
    Shih, A. Y., Erb, H., and Murphy, T. H. (2007) J. Neurochem., 101, 109–119.PubMedCrossRefGoogle Scholar
  101. 101.
    Sumi, D., Numasawa, Y., Endo, A., Iwamoto, N., and Kumagai, Y. (2009) J. Toxicol. Sci., 34, 627–635.PubMedCrossRefGoogle Scholar
  102. 102.
    Frankfurt, O. S., Lipchina, L. P., Bunto, T. V., and Emanuel, N. M. (1967) Byul. Eksp. Biol. Med., 64, 86–88.CrossRefGoogle Scholar
  103. 103.
    Wattenberg, L. W. (1977) J. Natl. Cancer Inst., 58, 395–398.PubMedGoogle Scholar
  104. 104.
    Reuter, S., Gupta, S. C., Chaturvedi, M. M., and Aggarwal, B. B. (2010) Free Radic. Biol. Med., 49, 1603–1616.PubMedCrossRefGoogle Scholar
  105. 105.
    Hayes, J. D., and McMahon, M. (2009) Trends Biochem. Sci., 34, 176–188.PubMedCrossRefGoogle Scholar
  106. 106.
    Thu, K. L., Pikor, L. A., Chari, R., Wilson, I. M., Macaulay, C. E., English, J. C., Tsao, M. S., Gazdar, A. F., Lam, S., Lam, W. L., and Lockwood, W. W. (2011) J. Thorac. Oncol., 6, 1521–1529.PubMedCrossRefGoogle Scholar
  107. 107.
    Ren, D., Villeneuve, N. F., Jiang, T., Wu, T., Lau, A., Toppin, H. A., and Zhang, D. D. (2011) Proc. Natl. Acad. Sci. USA, 108, 1433–1438.PubMedCrossRefGoogle Scholar
  108. 108.
    Magesh, S., Chen, Y., and Hu, L. (2012) Med. Res. Rev., 32, 687–726.PubMedCrossRefGoogle Scholar
  109. 109.
    Saha, P. K., Reddy, V. T., Konopleva, M., Andreeff, M., and Chan, L. (2010) J. Biol. Chem., 285, 40581–40592.PubMedCrossRefGoogle Scholar
  110. 110.
    Tran, T. A., McCoy, M. K., Sporn, M. B., and Tansey, M. G. (2008) J. Neuroinflammation, 5, 1–14.CrossRefGoogle Scholar
  111. 111.
    Wei, Y., Gong, J., Yoshida, T., Eberhart, C. G., Xu, Z., Kombairaju, P., Sporn, M. B., Handa, J. T., and Duh, E. J. (2011) Free Radic. Biol. Med., 51, 216–224.PubMedCrossRefGoogle Scholar
  112. 112.
    Pergola, P. E., Raskin, P., Toto, R. D., Meyer, C. J., Huff, J. W., Grossman, E. B., Krauth, M., Ruiz, S., Audhya, P., Christ-Schmidt, H., Wittes, J., and Warnock, D. G. (2011) N. Engl. J. Med., 365, 327–336.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2013

Authors and Affiliations

  1. 1.Center for Theoretical Problems of Physicochemical PharmacologyRussian Academy of SciencesMoscowRussia

Personalised recommendations