Advertisement

A Perspective on Dietary Phytochemicals and Cancer Chemoprevention: Oxidative Stress, Nrf2, and Epigenomics

  • Zheng-Yuan Su
  • Limin Shu
  • Tin Oo Khor
  • Jong Hun Lee
  • Francisco Fuentes
  • Ah-Ng Tony Kong
Chapter
Part of the Topics in Current Chemistry book series (TOPCURRCHEM, volume 329)

Abstract

Oxidative stress is caused by an imbalance of reactive oxygen species (ROS)/reactive nitrogen species (RNS) and the antioxidative stress defense systems in cells. ROS/RNS or carcinogen metabolites can attack intracellular proteins, lipids, and nucleic acids, which can result in genetic mutations, carcinogenesis, and other diseases. Nrf2 plays a critical role in the regulation of many antioxidative stress/antioxidant and detoxification enzyme genes, such as glutathione S-transferases (GSTs), NAD(P)H:quinone oxidoreductase 1 (NQO1), UDP-glucuronyl transferases (UGTs), and heme oxygenase-1 (HO-1), directly via the antioxidant response element (ARE). Recently, many studies have shown that dietary phytochemicals possess cancer chemopreventive potential through the induction of Nrf2-mediated antioxidant/detoxification enzymes and anti-inflammatory signaling pathways to protect organisms against cellular damage caused by oxidative stress. In addition, carcinogenesis can be caused by epigenetic alterations such as DNA methylation and histone modifications in tumor–suppressor genes and oncogenes. Interestingly, recent studies have shown that several naturally occurring dietary phytochemicals can epigenetically modify the chromatin, including reactivating Nrf2 via demethylation of CpG islands and the inhibition of histone deacetylases (HDACs) and/or histone acetyltransferases (HATs). The advancement and development of dietary phytochemicals in cancer chemoprevention research requires the integration of the known, and as-yet-unknown, compounds with the Nrf2-mediated antioxidant, detoxification, and anti-inflammatory systems and their in vitro and in vivo epigenetic mechanisms; human clinical efficacy studies must also be performed.

Keywords

Antioxidant response Inflammation Keap1 Nrf2 

Notes

Acknowledgments

This work is supported in part by Institutional Funds and by RO1-CA073674, RO1-CA094828, R01-CA118947, and R01-CA152826 awarded to Dr. Ah-Ng Tony Kong from the National Institutes of Health (NIH).

References

  1. 1.
    Brüne B, Zhou J, von Knethen A (2003) Kidney Int Suppl:S22Google Scholar
  2. 2.
    Darley-Usmar V, Halliwell B (1996) Pharm Res 13:649CrossRefGoogle Scholar
  3. 3.
    Yu BP (1994) Physiol Rev 74:139Google Scholar
  4. 4.
    Beckman KB, Ames BN (1998) Physiol Rev 78:547Google Scholar
  5. 5.
    Halliwell B, Gutteridge J (1999) Free radicals in biology and medicine. Oxford University Press, OxfordGoogle Scholar
  6. 6.
    Emerit J, Edeas M, Bricaire F (2004) Biomed Pharmacother 58:39CrossRefGoogle Scholar
  7. 7.
    Cataldi A (2010) Curr Pharm Des 16:1387CrossRefGoogle Scholar
  8. 8.
    Azad N, Iyer A, Vallyathan V, Wang L, Castranova V, Stehlik C, Rojanasakul Y (2010) Ann N Y Acad Sci 1203:1CrossRefGoogle Scholar
  9. 9.
    Ryter SW, Kim HP, Hoetzel A, Park JW, Nakahira K, Wang X, Choi AM (2007) Antioxid Redox Signal 9:49CrossRefGoogle Scholar
  10. 10.
    Shen HM, Liu ZG (2006) Free Radic Biol Med 40:928CrossRefGoogle Scholar
  11. 11.
    Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Chem Biol Interact 160:1CrossRefGoogle Scholar
  12. 12.
    Tan AC, Konczak I, Sze DM, Ramzan I (2011) Nutr Cancer 63:495CrossRefGoogle Scholar
  13. 13.
    Zamocky M, Furtmuller PG, Obinger C (2008) Antioxid Redox Signal 10:1527CrossRefGoogle Scholar
  14. 14.
    Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Int J Biochem Cell Biol 39:44CrossRefGoogle Scholar
  15. 15.
    Bartsch H, Nair J (2006) Langenbecks Arch Surg 391:499CrossRefGoogle Scholar
  16. 16.
    Klaunig JE, Kamendulis LM (2004) Annu Rev Pharmacol Toxicol 44:239CrossRefGoogle Scholar
  17. 17.
    Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J (2004) Mol Cell Biochem 266:37CrossRefGoogle Scholar
  18. 18.
    Dizdaroglu M, Jaruga P, Birincioglu M, Rodriguez H (2002) Free Radic Biol Med 32:1102CrossRefGoogle Scholar
  19. 19.
    Brown GC, Borutaite V (2001) IUBMB Life 52:189CrossRefGoogle Scholar
  20. 20.
    Shigenaga MK, Gimeno CJ, Ames BN (1989) Proc Natl Acad Sci USA 86:9697CrossRefGoogle Scholar
  21. 21.
    Dreher D, Junod AF (1996) Eur J Cancer 32A:30CrossRefGoogle Scholar
  22. 22.
    Carmeliet P (2000) Nat Med 6:389CrossRefGoogle Scholar
  23. 23.
    He X, Ma Q (2009) Mol Pharmacol 76:1265CrossRefGoogle Scholar
  24. 24.
    Reddy SP (2008) Curr Mol Med 8:376CrossRefGoogle Scholar
  25. 25.
    Jomova K, Vondrakova D, Lawson M, Valko M (2010) Mol Cell Biochem 345:91CrossRefGoogle Scholar
  26. 26.
    Mamede AC, Tavares SD, Abrantes AM, Trindade J, Maia JM, Botelho MF (2011) Nutr Cancer 63:479CrossRefGoogle Scholar
  27. 27.
    Kojo S (2004) Curr Med Chem 11:1041CrossRefGoogle Scholar
  28. 28.
    Fukai T, Ushio-Fukai M (2011) Antioxid Redox Signal 15:1583CrossRefGoogle Scholar
  29. 29.
    Nishikawa M, Hashida M, Takakura Y (2009) Adv Drug Deliv Rev 61:319CrossRefGoogle Scholar
  30. 30.
    Limon-Pacheco JH, Gonsebatt ME (2010) Cent Nerv Syst Agents Med Chem 10:287CrossRefGoogle Scholar
  31. 31.
    Jung KA, Kwak MK (2010) Molecules 15:7266CrossRefGoogle Scholar
  32. 32.
    Rushmore TH, Morton MR, Pickett CB (1991) J Biol Chem 266:11632Google Scholar
  33. 33.
    Shen G, Kong AN (2009) Biopharm Drug Dispos 30:345CrossRefGoogle Scholar
  34. 34.
    Boutten A, Goven D, Artaud-Macari E, Boczkowski J, Bonay M (2011) Trends Mol Med 17:363CrossRefGoogle Scholar
  35. 35.
    Moi P, Chan K, Asunis I, Cao A, Kan YW (1994) Proc Natl Acad Sci USA 91:9926CrossRefGoogle Scholar
  36. 36.
    Chan JY, Han XL, Kan YW (1993) Proc Natl Acad Sci USA 90:11366CrossRefGoogle Scholar
  37. 37.
    Chan K, Kan YW (1999) Proc Natl Acad Sci USA 96:12731CrossRefGoogle Scholar
  38. 38.
    Slocum SL, Kensler TW (2011) Arch Toxicol 85:273CrossRefGoogle Scholar
  39. 39.
    Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M (1999) Genes Dev 13:76CrossRefGoogle Scholar
  40. 40.
    Shu L, Cheung KL, Khor TO, Chen C, Kong AN (2010) Cancer Metastasis Rev 29:483CrossRefGoogle Scholar
  41. 41.
    Chinenov Y, Kerppola TK (2001) Oncogene 20:2438CrossRefGoogle Scholar
  42. 42.
    Kobayashi M, Yamamoto M (2005) Antioxid Redox Signal 7:385CrossRefGoogle Scholar
  43. 43.
    Kong AN, Yu R, Hebbar V, Chen C, Owuor E, Hu R, Ee R, Mandlekar S (2001) Mutat Res 480–481:231Google Scholar
  44. 44.
    Hu R, Shen G, Yerramilli UR, Lin W, Xu C, Nair S, Kong AN (2006) Arch Pharm Res 29:911CrossRefGoogle Scholar
  45. 45.
    Keum YS, Yu S, Chang PP, Yuan X, Kim JH, Xu C, Han J, Agarwal A, Kong AN (2006) Cancer Res 66:8804CrossRefGoogle Scholar
  46. 46.
    Huang HC, Nguyen T, Pickett CB (2000) Proc Natl Acad Sci USA 97:12475CrossRefGoogle Scholar
  47. 47.
    Huang HC, Nguyen T, Pickett CB (2002) J Biol Chem 277:42769CrossRefGoogle Scholar
  48. 48.
    Numazawa S, Ishikawa M, Yoshida A, Tanaka S, Yoshida T (2003) Am J Physiol Cell Physiol 285:C334Google Scholar
  49. 49.
    Bloom DA, Jaiswal AK (2003) J Biol Chem 278:44675CrossRefGoogle Scholar
  50. 50.
    Kang KW, Lee SJ, Park JW, Kim SG (2002) Mol Pharmacol 62:1001CrossRefGoogle Scholar
  51. 51.
    Lee JM, Hanson JM, Chu WA, Johnson JA (2001) J Biol Chem 276:20011CrossRefGoogle Scholar
  52. 52.
    Kang KW, Choi SH, Kim SG (2002) Nitric Oxide 7:244CrossRefGoogle Scholar
  53. 53.
    Nakaso K, Yano H, Fukuhara Y, Takeshima T, Wada-Isoe K, Nakashima K (2003) FEBS Lett 546:181CrossRefGoogle Scholar
  54. 54.
    Sun Z, Huang Z, Zhang DD (2009) PLoS One 4:e6588CrossRefGoogle Scholar
  55. 55.
    Li W, Thakor N, Xu EY, Huang Y, Chen C, Yu R, Holcik M, Kong AN (2010) Nucleic Acids Res 38:778CrossRefGoogle Scholar
  56. 56.
    Saw CL, Cintron M, Wu TY, Guo Y, Huang Y, Jeong WS, Kong AN (2011) Biopharm Drug Dispos 32:289CrossRefGoogle Scholar
  57. 57.
    Shu L, Khor TO, Lee JH, Boyanapalli SS, Huang Y, Wu TY, Saw CL, Cheung KL, Kong AN (2011) AAPS J 13:606CrossRefGoogle Scholar
  58. 58.
    Chun KS, Keum YS, Han SS, Song YS, Kim SH, Surh YJ (2003) Carcinogenesis 24:1515CrossRefGoogle Scholar
  59. 59.
    Reuter S, Eifes S, Dicato M, Aggarwal BB, Diederich M (2008) Biochem Pharmacol 76:1340CrossRefGoogle Scholar
  60. 60.
    Aggarwal BB, Kumar A, Bharti AC (2003) Anticancer Res 23:363Google Scholar
  61. 61.
    Deeb D, Xu YX, Jiang H, Gao X, Janakiraman N, Chapman RA, Gautam SC (2003) Mol Cancer Ther 2:95Google Scholar
  62. 62.
    Pandey M, Gupta S (2009) Front Biosci (Elite Ed) 1:13Google Scholar
  63. 63.
    Jeong WS, Kim IW, Hu R, Kong AN (2004) Pharm Res 21:649CrossRefGoogle Scholar
  64. 64.
    Jagtap S, Meganathan K, Wagh V, Winkler J, Hescheler J, Sachinidis A (2009) Curr Med Chem 16:1451CrossRefGoogle Scholar
  65. 65.
    Trachootham D, Lu W, Ogasawara MA, Nilsa RD, Huang P (2008) Antioxid Redox Signal 10:1343CrossRefGoogle Scholar
  66. 66.
    Rahman I, Biswas SK, Jimenez LA, Torres M, Forman HJ (2005) Antioxid Redox Signal 7:42CrossRefGoogle Scholar
  67. 67.
    Dinkova-Kostova AT, Talalay P (2008) Mol Nutr Food Res 52(Suppl 1):S128Google Scholar
  68. 68.
    Conney AH (2003) Annu Rev Pharmacol Toxicol 43:1CrossRefGoogle Scholar
  69. 69.
    Jakoby WB, Ziegler DM (1990) J Biol Chem 265:20715Google Scholar
  70. 70.
    Jana S, Mandlekar S (2009) Curr Drug Metab 10:595CrossRefGoogle Scholar
  71. 71.
    Chen C, Kong AN (2004) Free Radic Biol Med 36:1505CrossRefGoogle Scholar
  72. 72.
    Kundu JK, Surh YJ (2010) Pharm Res 27:999CrossRefGoogle Scholar
  73. 73.
    Hayes JD, McMahon M, Chowdhry S, Dinkova-Kostova AT (2010) Antioxid Redox Signal 13:1713CrossRefGoogle Scholar
  74. 74.
    Wasserman WW, Fahl WE (1997) Proc Natl Acad Sci USA 94:5361CrossRefGoogle Scholar
  75. 75.
    Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima Y (1997) Biochem Biophys Res Commun 236:313CrossRefGoogle Scholar
  76. 76.
    Kwak MK, Egner PA, Dolan PM, Ramos-Gomez M, Groopman JD, Itoh K, Yamamoto M, Kensler TW (2001) Mutat Res 480–481:305Google Scholar
  77. 77.
    Venugopal R, Jaiswal AK (1996) Proc Natl Acad Sci USA 93:14960CrossRefGoogle Scholar
  78. 78.
    He CH, Gong P, Hu B, Stewart D, Choi ME, Choi AM, Alam J (2001) J Biol Chem 276:20858CrossRefGoogle Scholar
  79. 79.
    Katsuoka F, Motohashi H, Ishii T, Aburatani H, Engel JD, Yamamoto M (2005) Mol Cell Biol 25:8044CrossRefGoogle Scholar
  80. 80.
    Igarashi K, Kataoka K, Itoh K, Hayashi N, Nishizawa M, Yamamoto M (1994) Nature 367:568CrossRefGoogle Scholar
  81. 81.
    Motohashi H, O’Connor T, Katsuoka F, Engel JD, Yamamoto M (2002) Gene 294:1CrossRefGoogle Scholar
  82. 82.
    Hu R, Xu C, Shen G, Jain MR, Khor TO, Gopalkrishnan A, Lin W, Reddy B, Chan JY, Kong AN (2006) Cancer Lett 243:170CrossRefGoogle Scholar
  83. 83.
    Hu R, Xu C, Shen G, Jain MR, Khor TO, Gopalkrishnan A, Lin W, Reddy B, Chan JY, Kong AN (2006) Life Sci 79:1944CrossRefGoogle Scholar
  84. 84.
    Kwak MK, Kensler TW (2010) Toxicol Appl Pharmacol 244:66CrossRefGoogle Scholar
  85. 85.
    Nair S, Xu C, Shen G, Hebbar V, Gopalakrishnan A, Hu R, Jain MR, Lin W, Keum YS, Liew C, Chan JY, Kong AN (2006) Pharm Res 23:2621CrossRefGoogle Scholar
  86. 86.
    Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, Biswal S (2002) Cancer Res 62:5196Google Scholar
  87. 87.
    Yates MS, Tran QT, Dolan PM, Osburn WO, Shin S, McCulloch CC, Silkworth JB, Taguchi K, Yamamoto M, Williams CR, Liby KT, Sporn MB, Sutter TR, Kensler TW (2009) Carcinogenesis 30:1024CrossRefGoogle Scholar
  88. 88.
    Yates MS, Kwak MK, Egner PA, Groopman JD, Bodreddigari S, Sutter TR, Baumgartner KJ, Roebuck BD, Liby KT, Yore MM, Honda T, Gribble GW, Sporn MB, Kensler TW (2006) Cancer Res 66:2488CrossRefGoogle Scholar
  89. 89.
    Hayes JD, Flanagan JU, Jowsey IR (2005) Annu Rev Pharmacol Toxicol 45:51CrossRefGoogle Scholar
  90. 90.
    Reisman SA, Yeager RL, Yamamoto M, Klaassen CD (2009) Toxicol Sci 108:35CrossRefGoogle Scholar
  91. 91.
    Hayes JD, Chanas SA, Henderson CJ, McMahon M, Sun C, Moffat GJ, Wolf CR, Yamamoto M (2000) Biochem Soc Trans 28:33Google Scholar
  92. 92.
    Tan KP, Wood GA, Yang M, Ito S (2010) Br J Pharmacol 161:1111CrossRefGoogle Scholar
  93. 93.
    Tukey RH, Strassburg CP (2000) Annu Rev Pharmacol Toxicol 40:581CrossRefGoogle Scholar
  94. 94.
    Vienneau DS, DeBoni U, Wells PG (1995) Cancer Res 55:1045Google Scholar
  95. 95.
    Leung HY, Wang Y, Leung LK (2007) Toxicology 242:153CrossRefGoogle Scholar
  96. 96.
    Yueh MF, Tukey RH (2007) J Biol Chem 282:8749CrossRefGoogle Scholar
  97. 97.
    Yeager RL, Reisman SA, Aleksunes LM, Klaassen CD (2009) Toxicol Sci 111:238CrossRefGoogle Scholar
  98. 98.
    Buckley DB, Klaassen CD (2009) Drug Metab Dispos 37:847CrossRefGoogle Scholar
  99. 99.
    Paonessa JD, Ding Y, Randall KL, Munday R, Argoti D, Vouros P, Zhang Y (2011) Cancer Res 71:3904CrossRefGoogle Scholar
  100. 100.
    Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, Kensler TW (2001) Proc Natl Acad Sci USA 98:3410CrossRefGoogle Scholar
  101. 101.
    Nioi P, Hayes JD (2004) Mutat Res 555:149CrossRefGoogle Scholar
  102. 102.
    Ross D (2004) Drug Metab Rev 36:639CrossRefGoogle Scholar
  103. 103.
    Long DJ 2nd, Waikel RL, Wang XJ, Perlaky L, Roop DR, Jaiswal AK (2000) Cancer Res 60:5913Google Scholar
  104. 104.
    Tripathi DN, Jena GB (2010) Mutat Res 696:69CrossRefGoogle Scholar
  105. 105.
    Yang CM, Huang SM, Liu CL, Hu ML (2012) J Agric Food Chem 60:1576Google Scholar
  106. 106.
    Khor TO, Huang Y, Wu TY, Shu L, Lee J, Kong AN (2011) Biochem Pharmacol 82:1073CrossRefGoogle Scholar
  107. 107.
    Loboda A, Jazwa A, Grochot-Przeczek A, Rutkowski AJ, Cisowski J, Agarwal A, Jozkowicz A, Dulak J (2008) Antioxid Redox Signal 10:1767CrossRefGoogle Scholar
  108. 108.
    Prestera T, Talalay P, Alam J, Ahn YI, Lee PJ, Choi AM (1995) Mol Med 1:827Google Scholar
  109. 109.
    Wunder C, Potter RF (2003) Curr Drug Targets 3:199Google Scholar
  110. 110.
    Guo X, Shin VY, Cho CH (2001) Life Sci 69:3113CrossRefGoogle Scholar
  111. 111.
    Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL (1999) J Biol Chem 274:26071CrossRefGoogle Scholar
  112. 112.
    Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y, Bannai S, Yamamoto M (2000) J Biol Chem 275:16023CrossRefGoogle Scholar
  113. 113.
    Rojo AI, Medina-Campos ON, Rada P, Zuniga-Toala A, Lopez-Gazcon A, Espada S, Pedraza-Chaverri J, Cuadrado A (2012) Free Radic Biol Med 52:473CrossRefGoogle Scholar
  114. 114.
    Chen JH, Huang SM, Tan TW, Lin HY, Chen PY, Yeh WL, Chou SC, Tsai CF, Wei IH, Lu DY (2012) Int Immunopharmacol 12:94CrossRefGoogle Scholar
  115. 115.
    Chen XL, Dodd G, Thomas S, Zhang X, Wasserman MA, Rovin BH, Kunsch C (2006) Am J Physiol 290:H1862Google Scholar
  116. 116.
    Chen XL, Kunsch C (2004) Curr Pharm Des 10:879CrossRefGoogle Scholar
  117. 117.
    Khor TO, Huang MT, Kwon KH, Chan JY, Reddy BS, Kong AN (2006) Cancer Res 66:11580CrossRefGoogle Scholar
  118. 118.
    Li N, Nel AE (2006) Antioxid Redox Signal 8:88CrossRefGoogle Scholar
  119. 119.
    Rahman I, Biswas SK, Kirkham PA (2006) Biochem Pharmacol 72:1439CrossRefGoogle Scholar
  120. 120.
    Yates MS, Kensler TW (2007) Drug News Perspect 20:109CrossRefGoogle Scholar
  121. 121.
    Thimmulappa RK, Scollick C, Traore K, Yates M, Trush MA, Liby KT, Sporn MB, Yamamoto M, Kensler TW, Biswal S (2006) Biochem Biophys Res Commun 351:883CrossRefGoogle Scholar
  122. 122.
    Thimmulappa RK, Lee H, Rangasamy T, Reddy SP, Yamamoto M, Kensler TW, Biswal S (2006) J Clin Invest 116:984CrossRefGoogle Scholar
  123. 123.
    Yang H, Magilnick N, Ou X, Lu SC (2005) Biochem J 391:399CrossRefGoogle Scholar
  124. 124.
    Liu GH, Qu J, Shen X (2008) Biochim Biophys Acta 1783:713CrossRefGoogle Scholar
  125. 125.
    Cho HY, Reddy SP, Yamamoto M, Kleeberger SR (2004) FASEB J 18:1258Google Scholar
  126. 126.
    Ishii Y, Itoh K, Morishima Y, Kimura T, Kiwamoto T, Iizuka T, Hegab AE, Hosoya T, Nomura A, Sakamoto T, Yamamoto M, Sekizawa K (2005) J Immunol 175:6968Google Scholar
  127. 127.
    Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, Yamamoto M, Petrache I, Tuder RM, Biswal S (2004) J Clin Invest 114:1248Google Scholar
  128. 128.
    Rangasamy T, Guo J, Mitzner WA, Roman J, Singh A, Fryer AD, Yamamoto M, Kensler TW, Tuder RM, Georas SN, Biswal S (2005) J Exp Med 202:47CrossRefGoogle Scholar
  129. 129.
    Khor TO, Yu S, Kong AN (2008) Planta Med 74:1540CrossRefGoogle Scholar
  130. 130.
    Lin W, Wu RT, Wu T, Khor TO, Wang H, Kong AN (2008) Biochem Pharmacol 76:967CrossRefGoogle Scholar
  131. 131.
    Wattenberg LW (1985) Cancer Res 45:1CrossRefGoogle Scholar
  132. 132.
    Hu R, Saw CL, Yu R, Kong AN (2010) Antioxid Redox Signal 13:1679CrossRefGoogle Scholar
  133. 133.
    Yu S, Kong AN (2007) Curr Cancer Drug Targets 7:416CrossRefGoogle Scholar
  134. 134.
    Lau A, Villeneuve NF, Sun Z, Wong PK, Zhang DD (2008) Pharmacol Res 58:262CrossRefGoogle Scholar
  135. 135.
    Finley JW, Kong AN, Hintze KJ, Jeffery EH, Ji LL, Lei XG (2011) J Agric Food Chem 59:6837CrossRefGoogle Scholar
  136. 136.
    Kim HJ, di Luccio E, Kong AN, Kim JS (2011) Biotechnol J 6:525CrossRefGoogle Scholar
  137. 137.
    Kobayashi A, Kang MI, Watai Y, Tong KI, Shibata T, Uchida K, Yamamoto M (2006) Mol Cell Biol 26:221CrossRefGoogle Scholar
  138. 138.
    Surh YJ, Kundu JK, Na HK, Lee JS (2005) J Nutr 135:2993SGoogle Scholar
  139. 139.
    Saw CL, Wu Q, Kong AN (2010) Chinese Med 5:37CrossRefGoogle Scholar
  140. 140.
    Xu C, Huang MT, Shen G, Yuan X, Lin W, Khor TO, Conney AH, Kong AN (2006) Cancer Res 66:8293CrossRefGoogle Scholar
  141. 141.
    Shen G, Xu C, Hu R, Jain MR, Nair S, Lin W, Yang CS, Chan JY, Kong AN (2005) Pharm Res 22:1805CrossRefGoogle Scholar
  142. 142.
    Kang HJ, Hong YB, Kim HJ, Wang A, Bae I (2011) Toxicol Lett 209:154Google Scholar
  143. 143.
    Barve A, Khor TO, Nair S, Reuhl K, Suh N, Reddy B, Newmark H, Kong AN (2009) Int J Cancer 124:1693CrossRefGoogle Scholar
  144. 144.
    Haridas V, Hanausek M, Nishimura G, Soehnge H, Gaikwad A, Narog M, Spears E, Zoltaszek R, Walaszek Z, Gutterman JU (2004) J Clin Invest 113:65Google Scholar
  145. 145.
    Higgins LG, Cavin C, Itoh K, Yamamoto M, Hayes JD (2008) Toxicol Appl Pharmacol 226:328CrossRefGoogle Scholar
  146. 146.
    Chen CC, Chen HL, Hsieh CW, Yang YL, Wung BS (2011) Acta Pharmacol Sin 32:62CrossRefGoogle Scholar
  147. 147.
    Feng R, Lu Y, Bowman LL, Qian Y, Castranova V, Ding M (2005) J Biol Chem 280:27888CrossRefGoogle Scholar
  148. 148.
    Chen C, Pung D, Leong V, Hebbar V, Shen G, Nair S, Li W, Kong AN (2004) Free Radic Biol Med 37:1578CrossRefGoogle Scholar
  149. 149.
    Wu TY, Saw CL, Khor TO, Pung D, Boyanapalli SS, Kong AN (2011) Mol CarcinogGoogle Scholar
  150. 150.
    Lian F, Wang XD (2008) Int J Cancer 123:1262CrossRefGoogle Scholar
  151. 151.
    Wondrak GT, Cabello CM, Villeneuve NF, Zhang S, Ley S, Li Y, Sun Z, Zhang DD (2008) Free Radic Biol Med 45:385CrossRefGoogle Scholar
  152. 152.
    Shin JW, Ohnishi K, Murakami A, Lee JS, Kundu JK, Na HK, Ohigashi H, Surh YJ (2011) Cancer Prev Res 4:860CrossRefGoogle Scholar
  153. 153.
    Hou DX, Korenori Y, Tanigawa S, Yamada-Kato T, Nagai M, He X, He J (2011) J Agric Food Chem 59:11975CrossRefGoogle Scholar
  154. 154.
    Swanson HI, Njar VC, Yu Z, Castro DJ, Gonzalez FJ, Williams DE, Huang Y, Kong AN, Doloff JC, Ma J, Waxman DJ, Scott EE (2010) Drug Metab Dispos 38:539CrossRefGoogle Scholar
  155. 155.
    Wu TY, Khor TO, Saw CL, Loh SC, Chen AI, Lim SS, Park JH, Cai L, Kong AN (2011) AAPS J 13:1CrossRefGoogle Scholar
  156. 156.
    Yu R, Chen C, Mo YY, Hebbar V, Owuor ED, Tan TH, Kong AN (2000) J Biol Chem 275:39907CrossRefGoogle Scholar
  157. 157.
    Yu R, Lei W, Mandlekar S, Weber MJ, Der CJ, Wu J, Kong AN (1999) J Biol Chem 274:27545CrossRefGoogle Scholar
  158. 158.
    Yu R, Mandlekar S, Lei W, Fahl WE, Tan TH, Kong AN (2000) J Biol Chem 275:2322CrossRefGoogle Scholar
  159. 159.
    Esteller M (2008) N Engl J Med 358:1148CrossRefGoogle Scholar
  160. 160.
    Waddington CH (1942) Endeavour 1:18Google Scholar
  161. 161.
    Wolffe AP, Matzke MA (1999) Science 286:481CrossRefGoogle Scholar
  162. 162.
    Baylin SB, Herman JG (2000) Trends Genet 16:168CrossRefGoogle Scholar
  163. 163.
    Esteller M (2005) Annu Rev Pharmacol Toxicol 45:629CrossRefGoogle Scholar
  164. 164.
    Jones PA, Baylin SB (2002) Nat Rev Genet 3:415CrossRefGoogle Scholar
  165. 165.
    Fraga MF, Ballestar E, Villar-Garea A, Boix-Chornet M, Espada J, Schotta G, Bonaldi T, Haydon C, Ropero S, Petrie K, Iyer NG, Perez-Rosado A, Calvo E, Lopez JA, Cano A, Calasanz MJ, Colomer D, Piris MA, Ahn N, Imhof A, Caldas C, Jenuwein T, Esteller M (2005) Nat Genet 37:391CrossRefGoogle Scholar
  166. 166.
    Issa JP (2002) J Nutr 132:2388SGoogle Scholar
  167. 167.
    Esteller M (2002) Oncogene 21:5427CrossRefGoogle Scholar
  168. 168.
    Bird A (2002) Genes Dev 16:6CrossRefGoogle Scholar
  169. 169.
    Suzuki MM, Bird A (2008) Nat Rev Genet 9:465CrossRefGoogle Scholar
  170. 170.
    Esteller M (2007) Nat Rev Genet 8:286CrossRefGoogle Scholar
  171. 171.
    Prendergast GC, Ziff EB (1991) Science 251:186CrossRefGoogle Scholar
  172. 172.
    Hendrich B, Bird A (1998) Mol Cell Biol 18:6538Google Scholar
  173. 173.
    Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F, Bird A (1992) Cell 69:905CrossRefGoogle Scholar
  174. 174.
    Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998) Nature 393:386CrossRefGoogle Scholar
  175. 175.
    Feng Q, Zhang Y (2001) Genes Dev 15:827Google Scholar
  176. 176.
    Lee BH, Yegnasubramanian S, Lin X, Nelson WG (2005) J Biol Chem 280:40749CrossRefGoogle Scholar
  177. 177.
    Yu SW, Khor TO, Cheung KL, Li WG, Wu TY, Huang Y, Foster BA, Kan YW, Kong AN (2010) PLoS One 5:e8579Google Scholar
  178. 178.
    Li E, Bestor TH, Jaenisch R (1992) Cell 69:915CrossRefGoogle Scholar
  179. 179.
    Okano M, Bell DW, Haber DA, Li E (1999) Cell 99:247CrossRefGoogle Scholar
  180. 180.
    Herman JG, Baylin SB (2003) N Engl J Med 349:2042CrossRefGoogle Scholar
  181. 181.
    Ellis L, Atadja PW, Johnstone RW (2009) Mol Cancer Ther 8:1409CrossRefGoogle Scholar
  182. 182.
    Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Nature 389:251CrossRefGoogle Scholar
  183. 183.
    Tremethick DJ (2007) Cell 128:651CrossRefGoogle Scholar
  184. 184.
    Berlowitz L, Pallotta D (1972) Exp Cell Res 71:45CrossRefGoogle Scholar
  185. 185.
    Jenuwein T, Allis CD (2001) Science 293:1074CrossRefGoogle Scholar
  186. 186.
    Lund AH, van Lohuizen M (2004) Genes Dev 18:2315CrossRefGoogle Scholar
  187. 187.
    Berger SL (2007) Nature 447:407CrossRefGoogle Scholar
  188. 188.
    Kouzarides T (2007) Cell 128:693CrossRefGoogle Scholar
  189. 189.
    Rodenhiser D, Mann M (2006) CMAJ 174:341CrossRefGoogle Scholar
  190. 190.
    Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Nature 410:120CrossRefGoogle Scholar
  191. 191.
    Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI (2001) Science 292:110CrossRefGoogle Scholar
  192. 192.
    Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Nature 416:556CrossRefGoogle Scholar
  193. 193.
    Tamaru H, Selker EU (2001) Nature 414:277CrossRefGoogle Scholar
  194. 194.
    Kim SH, Kang HJ, Na H, Lee MO (2010) Breast Cancer Res 12:R22CrossRefGoogle Scholar
  195. 195.
    Sigalotti L, Fratta E, Coral S, Cortini E, Covre A, Nicolay HJ, Anzalone L, Pezzani L, Di Giacomo AM, Fonsatti E, Colizzi F, Altomonte M, Calabro L, Maio M (2007) J Cell Physiol 212:330CrossRefGoogle Scholar
  196. 196.
    Mai A, Altucci L (2009) Int J Biochem Cell Biol 41:199CrossRefGoogle Scholar
  197. 197.
    Abdulhaq H, Rossetti JM (2007) Expert Opin Investig Drugs 16:1967CrossRefGoogle Scholar
  198. 198.
    Fenaux P, Ades L (2009) Leuk Res 33(Suppl 2):S7CrossRefGoogle Scholar
  199. 199.
    Griffiths EA, Gore SD (2008) Semin Hematol 45:23CrossRefGoogle Scholar
  200. 200.
    Issa JP (2007) Clin Cancer Res 13:1634CrossRefGoogle Scholar
  201. 201.
    Rasheed WK, Johnstone RW, Prince HM (2007) Expert Opin Investig Drugs 16:659CrossRefGoogle Scholar
  202. 202.
    Prince HM, Bishton MJ, Harrison SJ (2009) Clin Cancer Res 15:3958CrossRefGoogle Scholar
  203. 203.
    Garcia-Manero G, Assouline S, Cortes J, Estrov Z, Kantarjian H, Yang H, Newsome WM, Miller WH Jr, Rousseau C, Kalita A, Bonfils C, Dubay M, Patterson TA, Li Z, Besterman JM, Reid G, Laille E, Martell RE, Minden M (2008) Blood 112:981CrossRefGoogle Scholar
  204. 204.
    Davis CD, Uthus EO (2004) Exp Biol Med (Maywood) 229:988Google Scholar
  205. 205.
    Fang M, Chen D, Yang CS (2007) J Nutr 137:223SGoogle Scholar
  206. 206.
    Yang CS, Fang M, Lambert JD, Yan P, Huang TH (2008) Nutr Rev 66(Suppl 1):S18CrossRefGoogle Scholar
  207. 207.
    Ravindran J, Prasad S, Aggarwal BB (2009) AAPS J 11:495CrossRefGoogle Scholar
  208. 208.
    Kanai Y (2008) Pathol Int 58:544CrossRefGoogle Scholar
  209. 209.
    Liu Z, Xie Z, Jones W, Pavlovicz RE, Liu S, Yu J, Li PK, Lin J, Fuchs JR, Marcucci G, Li C, Chan KK (2009) Bioorg Med Chem Lett 19:706CrossRefGoogle Scholar
  210. 210.
    Medina-Franco JL, Lopez-Vallejo F, Kuck D, Lyko F (2011) Mol Divers 15:293CrossRefGoogle Scholar
  211. 211.
    Jha AK, Nikbakht M, Parashar G, Shrivastava A, Capalash N, Kaur J (2010) Folia Biol (Praha) 56:195Google Scholar
  212. 212.
    Liu YL, Yang HP, Gong L, Tang CL, Wang HJ (2011) Mol Med Rep 4:675CrossRefGoogle Scholar
  213. 213.
    Timmermann S, Lehrmann H, Polesskaya A, Harel-Bellan A (2001) Cell Mol Life Sci 58:728CrossRefGoogle Scholar
  214. 214.
    Balasubramanyam K, Varier RA, Altaf M, Swaminathan V, Siddappa NB, Ranga U, Kundu TK (2004) J Biol Chem 279:51163CrossRefGoogle Scholar
  215. 215.
    Morimoto T, Sunagawa Y, Kawamura T, Takaya T, Wada H, Nagasawa A, Komeda M, Fujita M, Shimatsu A, Kita T, Hasegawa K (2008) J Clin Invest 118:868Google Scholar
  216. 216.
    Li HL, Liu C, de Couto G, Ouzounian M, Sun M, Wang AB, Huang Y, He CW, Shi Y, Chen X, Nghiem MP, Liu Y, Chen M, Dawood F, Fukuoka M, Maekawa Y, Zhang L, Leask A, Ghosh AK, Kirshenbaum LA, Liu PP (2008) J Clin Invest 118:879CrossRefGoogle Scholar
  217. 217.
    Kundu TK, Palhan VB, Wang Z, An W, Cole PA, Roeder RG (2000) Mol Cell 6:551CrossRefGoogle Scholar
  218. 218.
    Brooks CL, Gu W (2003) Curr Opin Cell Biol 15:164CrossRefGoogle Scholar
  219. 219.
    Kang SK, Cha SH, Jeon HG (2006) Stem Cells Dev 15:165CrossRefGoogle Scholar
  220. 220.
    Marcu MG, Jung YJ, Lee S, Chung EJ, Lee MJ, Trepel J, Neckers L (2006) Med Chem 2:169CrossRefGoogle Scholar
  221. 221.
    Chen Y, Shu W, Chen W, Wu Q, Liu H, Cui G (2007) Basic Clin Pharmacol Toxicol 101:427CrossRefGoogle Scholar
  222. 222.
    Liu HL, Chen Y, Cui GH, Zhou JF (2005) Acta Pharmacol Sin 26:603CrossRefGoogle Scholar
  223. 223.
    Bora-Tatar G, Dayangac-Erden D, Demir AS, Dalkara S, Yelekci K, Erdem-Yurter H (2009) Bioorg Med Chem 17:5219CrossRefGoogle Scholar
  224. 224.
    Lee SJ, Krauthauser C, Maduskuie V, Fawcett PT, Olson JM, Rajasekaran SA (2011) BMC Cancer 11:144CrossRefGoogle Scholar
  225. 225.
    Cheung KL, Kong AN (2010) AAPS J 12:87CrossRefGoogle Scholar
  226. 226.
    Meeran SM, Patel SN, Tollefsbol TO (2010) PLoS One 5:e11457CrossRefGoogle Scholar
  227. 227.
    Wang LG, Beklemisheva A, Liu XM, Ferrari AC, Feng J, Chiao JW (2007) Mol Carcinog 46:24CrossRefGoogle Scholar
  228. 228.
    Myzak MC, Karplus PA, Chung FL, Dashwood RH (2004) Cancer Res 64:5767CrossRefGoogle Scholar
  229. 229.
    Clarke JD, Hsu A, Yu Z, Dashwood RH, Ho E (2011) Mol Nutr Food Res 55:999CrossRefGoogle Scholar
  230. 230.
    Rajendran P, Delage B, Dashwood WM, Yu TW, Wuth B, Williams DE, Ho E, Dashwood RH (2011) Mol Cancer 10:68CrossRefGoogle Scholar
  231. 231.
    Myzak MC, Hardin K, Wang R, Dashwood RH, Ho E (2006) Carcinogenesis 27:811CrossRefGoogle Scholar
  232. 232.
    Myzak MC, Dashwood WM, Orner GA, Ho E, Dashwood RH (2006) FASEB J 20:506Google Scholar
  233. 233.
    Myzak MC, Tong P, Dashwood WM, Dashwood RH, Ho E (2007) Exp Biol Med (Maywood) 232:227Google Scholar
  234. 234.
    Wang LG, Liu XM, Fang Y, Dai W, Chiao FB, Puccio GM, Feng J, Liu D, Chiao JW (2008) Int J Oncol 33:375Google Scholar
  235. 235.
    Graham HN (1992) Prev Med 21:334CrossRefGoogle Scholar
  236. 236.
    Yang CS, Wang H (2011) Mol Nutr Food Res 55:819CrossRefGoogle Scholar
  237. 237.
    Li Y, Tollefsbol TO (2010) Curr Med Chem 17:2141CrossRefGoogle Scholar
  238. 238.
    Fang MZ, Wang Y, Ai N, Hou Z, Sun Y, Lu H, Welsh W, Yang CS (2003) Cancer Res 63:7563Google Scholar
  239. 239.
    Kato K, Long NK, Makita H, Toida M, Yamashita T, Hatakeyama D, Hara A, Mori H, Shibata T (2008) Br J Cancer 99:647CrossRefGoogle Scholar
  240. 240.
    Pandey M, Shukla S, Gupta S (2010) Int J Cancer 126:2520Google Scholar
  241. 241.
    Nandakumar V, Vaid M, Katiyar SK (2011) Carcinogenesis 32:537CrossRefGoogle Scholar
  242. 242.
    Lee WJ, Zhu BT (2006) Carcinogenesis 27:269CrossRefGoogle Scholar
  243. 243.
    Morey Kinney SR, Zhang W, Pascual M, Greally JM, Gillard BM, Karasik E, Foster BA, Karpf AR (2009) Cancer Prev Res (Phila) 2:1065CrossRefGoogle Scholar
  244. 244.
    Mittal A, Piyathilake C, Hara Y, Katiyar SK (2003) Neoplasia 5:555Google Scholar
  245. 245.
    Choi KC, Jung MG, Lee YH, Yoon JC, Kwon SH, Kang HB, Kim MJ, Cha JH, Kim YJ, Jun WJ, Lee JM, Yoon HG (2009) Cancer Res 69:583CrossRefGoogle Scholar
  246. 246.
    Adlercreutz H (2002) Lancet Oncol 3:364CrossRefGoogle Scholar
  247. 247.
    Wu AH, Ziegler RG, Nomura AM, West DW, Kolonel LN, Horn-Ross PL, Hoover RN, Pike MC (1998) Am J Clin Nutr 68:1437SGoogle Scholar
  248. 248.
    Majid S, Dar AA, Ahmad AE, Hirata H, Kawakami K, Shahryari V, Saini S, Tanaka Y, Dahiya AV, Khatri G, Dahiya R (2009) Carcinogenesis 30:662CrossRefGoogle Scholar
  249. 249.
    King-Batoon A, Leszczynska JM, Klein CB (2008) Environ Mol Mutagen 49:36CrossRefGoogle Scholar
  250. 250.
    Majid S, Kikuno N, Nelles J, Noonan E, Tanaka Y, Kawamoto K, Hirata H, Li LC, Zhao H, Okino ST, Place RF, Pookot D, Dahiya R (2008) Cancer Res 68:2736CrossRefGoogle Scholar
  251. 251.
    Kikuno N, Shiina H, Urakami S, Kawamoto K, Hirata H, Tanaka Y, Majid S, Igawa M, Dahiya R (2008) Int J Cancer 123:552CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Zheng-Yuan Su
    • 1
  • Limin Shu
    • 1
  • Tin Oo Khor
    • 1
  • Jong Hun Lee
    • 1
  • Francisco Fuentes
    • 1
    • 2
  • Ah-Ng Tony Kong
    • 1
  1. 1.Department of Pharmaceutics, Center for Cancer Prevention Research, Ernest-Mario School of Pharmacy, Rutgersthe State University of New JerseyPiscatawayUSA
  2. 2.Departamento de Agricultura del Desierto y BiotecnologíaUniversidad Arturo PratIquiqueChile

Personalised recommendations