DOI QR코드

DOI QR Code

Effect of Natural Compounds on Catechol Estrogen-Induced Carcinogenesis

  • Sung, Nam-Ji (Department of Biomedical Laboratory Science, College of Medical Sciences, Soonchunhyang University) ;
  • Park, Sin-Aye (Department of Biomedical Laboratory Science, College of Medical Sciences, Soonchunhyang University)
  • Received : 2019.01.28
  • Accepted : 2019.03.25
  • Published : 2019.03.31

Abstract

The hydroxylation of estradiol results in the formation of catechol estrogens such as 2-hydroxyestradiol ($2-OHE_2$) and 4-hydroxyestradiol ($4-OHE_2$). These catechol estrogens are further oxidized to quinone metabolites by peroxidases or cytochrome P450 (CYP450) enzymes. Catechol estrogens contribute to hormone-induced carcinogenesis by generating DNA adducts or reactive oxygen species (ROS). Interestingly, many of the natural products found in living organisms have been reported to show protective effects against carcinogenesis induced by catechol estrogens. Although some compounds have been reported to increase the activity of catechol estrogens via oxidation to quinone metabolites, many natural products decreased the activity of catechol estrogens by inhibiting DNA adduct formation, ROS production, or oxidative cell damage. Here we focus specifically on the chemopreventive effects of these natural compounds against carcinogenesis induced by catechol estrogens.

Keywords

References

  1. Borras C, Gambini J, Gomez-Cabrera MC, Sastre J, Pallardo FV, Mann GE, Vina J. Genistein, a soy isoflavone, up-regulates expression of antioxidant genes: Involvement of estrogen receptors, erk1/2, and nfkappab. FASEB J. 2006. 20: 2136-2138. https://doi.org/10.1096/fj.05-5522fje
  2. Cavalieri E, Chakravarti D, Guttenplan J, Hart E, Ingle J, Jankowiak R, Muti P, Rogan E, Russo J, Santen R, Sutter T. Catechol estrogen quinones as initiators of breast and other human cancers: Implications for biomarkers of susceptibility and cancer prevention. Biochim Biophys Acta. 2006. 1766: 63-78.
  3. Cavalieri EL, Stack DE, Devanesan PD, Todorovic R, Dwivedy I, Higginbotham S, Johansson SL, Patil KD, Gross ML, Gooden JK, Ramanathan R, Cerny RL, Rogan EG. Molecular origin of cancer: Catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc Natl Acad Sci USA. 1997. 94: 10937-10942. https://doi.org/10.1073/pnas.94.20.10937
  4. Chen ZH, Hurh YJ, Na HK, Kim JH, Chun YJ, Kim DH, Kang KS, Cho MH, Surh YJ. Resveratrol inhibits tcdd-induced expression of cyp1a1 and cyp1b1 and catechol estrogen-mediated oxidative DNA damage in cultured human mammary epithelial cells. Carcinogenesis. 2004. 25: 2005-2013. https://doi.org/10.1093/carcin/bgh183
  5. Dias DA, Urban S, Roessner U. A historical overview of natural products in drug discovery. Metabolites. 2012. 2: 303-336. https://doi.org/10.3390/metabo2020303
  6. Fussell KC, Udasin RG, Smith PJ, Gallo MA, Laskin JD. Catechol metabolites of endogenous estrogens induce redox cycling and generate reactive oxygen species in breast epithelial cells. Carcinogenesis. 2011. 32: 1285-1293. https://doi.org/10.1093/carcin/bgr109
  7. Gaikwad NW, Rogan EG, Cavalieri EL. Evidence from esi-ms for nqo1-catalyzed reduction of estrogen ortho-quinones. Free Radic Biol Med. 2007. 43: 1289-1298. https://doi.org/10.1016/j.freeradbiomed.2007.07.021
  8. Ji Y, Olson J, Zhang J, Hildebrandt M, Wang L, Ingle J, Fredericksen Z, Sellers T, Miller W, Dixon JM, Brauch H, Eichelbaum M, Justenhoven C, Hamann U, Ko Y, Bruning T, Chang-Claude J, Wang-Gohrke S, Schaid D, Weinshilboum R. Breast cancer risk reduction and membrane-bound catechol o-methyltransferase genetic polymorphisms. Cancer Res. 2008. 68: 5997-6005. https://doi.org/10.1158/0008-5472.CAN-08-0043
  9. Jiang YL, Liu ZP. Natural products as anti-invasive and antimetastatic agents. Curr Med Chem. 2011. 18: 808-829. https://doi.org/10.2174/092986711794927711
  10. Lareef MH, Garber J, Russo PA, Russo IH, Heulings R, Russo J. The estrogen antagonist ici-182-780 does not inhibit the transformation phenotypes induced by 17-beta-estradiol and 4-oh estradiol in human breast epithelial cells. Int J Oncol. 2005. 26: 423-429.
  11. Lee EJ, Oh SY, Kim MK, Ahn SH, Son BH, Sung MK. Modulatory effects of alpha- and gamma-tocopherols on 4-hydroxyestradiol induced oxidative stresses in mcf-10a breast epithelial cells. Nutr Res Pract. 2009. 3: 185-191. https://doi.org/10.4162/nrp.2009.3.3.185
  12. Lehmann L, Jiang L, Wagner J. Soy isoflavones decrease the catechol-o-methyltransferase-mediated inactivation of 4-hydroxyestradiol in cultured mcf-7 cells. Carcinogenesis. 2008. 29: 363-370. https://doi.org/10.1093/carcin/bgm235
  13. Lu F, Zahid M, Wang C, Saeed M, Cavalieri EL, Rogan EG. Resveratrol prevents estrogen-DNA adduct formation and neoplastic transformation in mcf-10f cells. Cancer Prev Res (Phila). 2008. 1: 135-145. https://doi.org/10.1158/1940-6207.CAPR-08-0037
  14. MacLusky NJ, Naftolin F, Krey LC, Franks S. The catechol estrogens. J Steroid Biochem. 1981. 15: 111-124. https://doi.org/10.1016/0022-4731(81)90265-X
  15. Mense SM, Chhabra J, Bhat HK. Preferential induction of cytochrome p450 1a1 over cytochrome p450 1b1 in human breast epithelial cells following exposure to quercetin. J Steroid Biochem Mol Biol. 2008. 110: 157-162. https://doi.org/10.1016/j.jsbmb.2008.03.029
  16. Mense SM, Singh B, Remotti F, Liu X, Bhat HK. Vitamin C and alpha-naphthoflavone prevent estrogen-induced mammary tumors and decrease oxidative stress in female aci rats. Carcinogenesis. 2009. 30: 1202-1208. https://doi.org/10.1093/carcin/bgp093
  17. Moon YJ, Wang X, Morris ME. Dietary flavonoids: Effects on xenobiotic and carcinogen metabolism. Toxicol In Vitro. 2006. 20: 187-210. https://doi.org/10.1016/j.tiv.2005.06.048
  18. Park SA, Na HK, Kim EH, Cha YN, Surh YJ. 4-hydroxyestradiol induces anchorage-independent growth of human mammary epithelial cells via activation of ikappab kinase: Potential role of reactive oxygen species. Cancer Res. 2009. 69: 2416-2424. https://doi.org/10.1158/0008-5472.CAN-08-2177
  19. Park SA, Na HK, Surh YJ. Resveratrol suppresses 4-hydroxyestradiol -induced transformation of human breast epithelial cells by blocking ikappab kinasebeta-nf-kappab signalling. Free Radic Res. 2012. 46: 1051-1057. https://doi.org/10.3109/10715762.2012.671940
  20. Parl FF, Dawling S, Roodi N, Crooke PS. Estrogen metabolism and breast cancer: A risk model. Ann NY Acad Sci. 2009. 1155: 68-75. https://doi.org/10.1111/j.1749-6632.2008.03676.x
  21. Pastore A, Federici G, Bertini E, Piemonte F. Analysis of glutathione: Implication in redox and detoxification. Clin Chim Acta. 2003. 333: 19-39. https://doi.org/10.1016/S0009-8981(03)00200-6
  22. Takemura H, Itoh T, Yamamoto K, Sakakibara H, Shimoi K. Selective inhibition of methoxyflavonoids on human cyp1b1 activity. Bioorg Med Chem. 2010a. 18: 6310-6315. https://doi.org/10.1016/j.bmc.2010.07.020
  23. Takemura H, Uchiyama H, Ohura T, Sakakibara H, Kuruto R, Amagai T, Shimoi K. A methoxyflavonoid, chrysoeriol, selectively inhibits the formation of a carcinogenic estrogen metabolite in mcf-7 breast cancer cells. J Steroid Biochem Mol Biol. 2010b. 118: 70-76. https://doi.org/10.1016/j.jsbmb.2009.10.002
  24. Thompson PA, Ambrosone C. Molecular epidemiology of genetic polymorphisms in estrogen metabolizing enzymes in human breast cancer. J Natl Cancer Inst Monogr. 2000. 125-134.
  25. van Duursen MB, Sanderson JT, de Jong PC, Kraaij M, van den Berg M. Phytochemicals inhibit catechol-o-methyltransferase activity in cytosolic fractions from healthy human mammary tissues: Implications for catechol estrogen-induced DNA damage. Toxicol Sci. 2004. 81: 316-324. https://doi.org/10.1093/toxsci/kfh216
  26. Wagner J, Jiang L, Lehmann L. Phytoestrogens modulate the expression of 17alpha-estradiol metabolizing enzymes in cultured mcf-7 cells. Adv Exp Med Biol. 2008. 617: 625-632. https://doi.org/10.1007/978-0-387-69080-3_65
  27. Xu X, Duncan AM, Merz BE, Kurzer MS. Effects of soy isoflavones on estrogen and phytoestrogen metabolism in premenopausal women. Cancer Epidemiol Biomarkers Prev. 1998. 7: 1101-1108.
  28. Yang L, Zahid M, Liao Y, Rogan EG, Cavalieri EL, Davidson NE, Yager JD, Visvanathan K, Groopman JD, Kensler TW. Reduced formation of depurinating estrogen-DNA adducts by sulforaphane or keap1 disruption in human mammary epithelial mcf-10a cells. Carcinogenesis. 2013. 34: 2587-2592. https://doi.org/10.1093/carcin/bgt246
  29. Yuan G, Wahlqvist ML, He G, Yang M, Li D. Natural products and anti-inflammatory activity. Asia Pac J Clin Nutr. 2006. 15: 143-152.
  30. Zahid M, Gaikwad NW, Ali MF, Lu F, Saeed M, Yang L, Rogan EG, Cavalieri EL. Prevention of estrogen-DNA adduct formation in mcf-10f cells by resveratrol. Free Radic Biol Med. 2008. 45: 136-145. https://doi.org/10.1016/j.freeradbiomed.2008.03.017
  31. Zahid M, Gaikwad NW, Rogan EG, Cavalieri EL. Inhibition of depurinating estrogen-DNA adduct formation by natural compounds. Chem Res Toxicol. 2007. 20: 1947-1953. https://doi.org/10.1021/tx700269s
  32. Zahid M, Saeed M, Beseler C, Rogan EG, Cavalieri EL. Resveratrol and n-acetylcysteine block the cancer-initiating step in mcf-10f cells. Free Radic Biol Med. 2011. 50: 78-85. https://doi.org/10.1016/j.freeradbiomed.2010.10.662
  33. Zhou X, Zhao Y, Wang J, Wang X, Chen C, Yin D, Zhao F, Yin J, Guo M, Zhang L, Du L, Zhang B, Yin X. Resveratrol represses estrogen-induced mammary carcinogenesis through nrf2-ugt1a8-estrogen metabolic axis activation. Biochem Pharmacol. 2018. 155: 252-263. https://doi.org/10.1016/j.bcp.2018.07.006
  34. Zhu BT, Conney AH. Functional role of estrogen metabolism in target cells: Review and perspectives. Carcinogenesis. 1998. 19: 1-27. https://doi.org/10.1093/carcin/19.1.1
  35. Zitka O, Skalickova S, Gumulec J, Masarik M, Adam V, Hubalek J, Trnkova L, Kruseova J, Eckschlager T, Kizek R. Redox status expressed as gsh:Gssg ratio as a marker for oxidative stress in paediatric tumour patients. Oncol Lett. 2012. 4: 1247-1253. https://doi.org/10.3892/ol.2012.931