Reversal of multidrug resistance in cancer treatment by regulating multidrug resistance gene1: focus on nuclear receptors and epigenetics

doi:10.5246/jcps.2015.05.036

Abstract

Abstract:

Overexpression of P-glycoprotein (P-gp) encoded by the multidrug resistance gene-1 (MDR-1) is the main mechanism responsible for multidrug resistance (MDR) in a majority of cancer cells. However, the mechanism by which cancer cells acquire high levels of P-gp has not been well defined. Accumulating evidence suggests that nuclear receptors (NRs), especially human pregnane X receptor (PXR), play a crucial role in multidrug resistance. It has been shown that chemotherapeutic drug activates PXR and then enhances P-gp expression. Genetic knockdown or pharmacologic inhibition of PXR led to attenuation of drug-inducedMDR1 over expression, implying that NRs may be an effective target to reverse multidrug resistance. Recent investigations suggested that transcriptional activity of NRs is mediated by methylases, the important enzymes involved in epigenetic regulation. Other epigenetic modifications, such as promoter methylation, histone deacetylases and microRNAs, were also found to be involved in activation of MDR1 promoter, though the underlying mechanisms are not thoroughly known. In this review, we summarized recent researches in the regulation of P-gp expression, with particular focus on NRs and epigenetics, aiming to provide references and options to reverse and/or prevent MDR in cancer treatment.

Key words: Multidrug resistance, P-glycoprotein, Nuclear receptors, Epigenetics

CLC Number:

R962

Supporting:

Tingting Li, Zhijun Wang, Haiyan Liu, Huiru Xie, Xuehua Jiang, Ling Wang. Reversal of multidrug resistance in cancer treatment by regulating multidrug resistance gene1: focus on nuclear receptors and epigenetics[J]. Journal of Chinese Pharmaceutical Sciences, 2015, 24(5): 273-284.

References

[1] Gottesman, M.M.; Pastan, I. Annu. Rev. Biochem. , 62, 385-427.1993

[2] Amiri-Kordestani, L.; Basseville, A.; Kurdziel, K.; Fojo, A.T.; Bates, S.E. Drug Resist. Updat. 2012, 15, 50-61.

[3] Zhu, C.Y.; Lv, Y.P.; Yan, D.F.; Gao, F.L. Asian. Pac. J. Cancer. P. 2013, 14, 6757- 6760.

[4] Silva, R.; Vilas-Boas, V.; Carmo, H.; Dinis-Oliveira, R.J.; Carvalho, F.; de-Lourdes Bastos, M.; Remião, F. Pharmacol. Ther. 2014, [Epub ahead of print]. This article can be found online at http://www.sciencedirect.com/science/article/pii/S0163725814002137

[5] Varma, M.V.; Ashokraj, Y.; Dey, C.S.; Panchagnula, R. Pharmacol. Res. 2003, 48, 347-359.

[6] Akhtar, N.; Ahad, A.; Khar, R.K.; Jaggi, M.; Aqil, M.; Iqbal, Z.; Ahmad, F.J.; Talegaonkar, S. Expert. Opin. Ther. Pat. 2011, 21, 561-557.

[7] Fox, E.; Bates, S.E. Expert. Rev. Anticancer. 2007, 7, 447-459.

[8] Prakash, A.S. J. Excip. Food Chem. 2010, 1, 51-59.

[9] Varma, M.V.; Ashokraj, Y.; Dey, C.S.; Panchagnula, R. Pharmacol. Res. 2003, 48, 347-359.

[10] Palmeira, A.; Sousa, E.; Vasconcelos, M.H.; Pinto, M.M. Curr. Med. Chem. 2012, 19, 1946-2025.

[11] Kelly, R.J.; Draper, D.; Chen, C.C.; Robey, R.W.; Figg, W.D.; Piekarz, R.L.; Chen, X.; Gardner, E.R.; Balis, F.M.; Venkatesan, A.M.; Steinberg, S.M.; Fojo, T.; Bates, S.E. Clin. Cancer Res. 2011, 17, 569-580.

[12] De, G.J.; Demeler, J.; Skuce, P.; Mitreva, M.; Samson-Himmelstjerna, G.V.; Vercruysse, J.; Claerebout, E.; Geldhof, P. Parasitology. 2013, 140, 499-508.

[13] Huang, L.; Li, X.; Roberts, J.; Janosky, B.; Lin, M.J. Xenobiotica. 2014, 24, 1-9.

[14] Zhang, Z.J.; Saito, T.; Kimura, Y.; Sugimoto, C.; Ohtsubo, T.; Saito, H. Brain Res. 2000, 852, 116-126.

[15] Yakun, C.; Yong, T.; Chang, X.G.; Boral, D.; Nie, D. Biochem. Pharmacol. 2012, 83, 1112-1126.

[16] Chen, T. Adv. Drug Deliv. Rev. 2010, 62, 1257-1264.

[17] Piedade, R.; Traub, S.; Bitter, A.; Nüssler, A.K.; Gil, J.P.; Schwab, M. Burk, O. Antimicrob. Agents. Ch. , 59, 96-104.2015

[18] Pondugula, S.R.; Mani, S. Cancer Lett. 2013, 328, 1-9.

[19] Rathod, V.; Jain, S.; Nandekar, P.; Sangamwar, A.T. Drug Discov. Today. 2014, 19, 63-70.

[20] Xie, Y.; Ke, S.; Ouyang, N.; He, J.; Xie, W.; Bedford, M.T.; Tian, Y. J. Biol. Chem. 2009, 284, 9199-9205.

[21] Tian, Y. Drug Metab. Rev. 2013, 45, 166-172.

[22] Tomiyasu, H.; Goto-Koshino, Y.; Fujino, Y.; Ohno, K.; Tsujimoto, H. Vet. J. 2014, 199, 103-109.

[23] Toth, M.; Boros, I.M.; Balint, E. Cancer Sci. 2012, 103, 659- 669.

[24] Mohan, R.; Heyman, R.A. Curr. Top. Med. Chem. 2003, 3, 1637-1647.

[25] Taosheng, C. Adv. Drug Deliver. Rev. 2010, 62, 1257-1264.

[26] Baker, E.K.; Assam, E.O. Exp. Cell Res. , 290, 177-194.2003

[27] Yakun, C.; Yong, T.; Man-Tzu, W.; Zeng, S.; Dao, T.N. Cancer Res. 2007, 67, 10361-10367.

[28] Caroline, R.; Jean, M.P.; Géraldine, L.; Cyril, B.; Jovana, K.; Benjamin, L.; Sylvain, P.; Caroline, B.; Dominique, J.; Frédéric, H.; Serge, L.; Jean, P.B.; Alexandre, E. Mol. Cancer. 2010, 9, 46.

[29] Enqi, Q.; Minghua, J.; Jianzhong, W.; Rong, M.; Xiaohua, Z.; Yuejun, H.; Quanbin, Z.; Xue, S.; Liwei, Z.; Jin, H.T. Oncol. Lett. 2013, 5, 1093-1100.

[30] Koutsounas, I.; Patsouris, E.; Theocharis, S. Histol. Histopathol. 2013, 28, 405- 420.

[31] Ya, K.C.; Yong, T.; Shu, Q.C.; Dao, T.N. Cancer Boil. Ther. 2009, 8, 1265-1272.

[32] Divya, G.; Madhukumar, V.; Hongwei, W.; Sean, K.; Michael, S.; Gary, L.G.; Kathleen, W.; Clifford, L.; Sridhar, M. Clin. Cancer Res. 2008, 14, 5332-5340.

[33] Stefan, H.I.; Meijerman, C.L.; Febus, R.F.; Maas-Bakker, J.H.; Beijnen, J.H.M. Cancer Chemother. Pharm. 2010, 66, 765-771.

[34] Chen, Y.; Tang, Y.; Chen, S.; Nie, D. Cancer Biol. Ther. 2009, 8, 1265-1272.

[35] Katsuyoshi, K.; Togo, I.; Yasuhito, K.; Osamu, G.; Ken, T.; Kaname, K. Mol. Pharmacol. 2003, 63, 524-531.

[36] Synold, T.W.; Dussault, I.; Forman, B.M. Nat. Med. 2001, 7, 584-559.

[37] Yue, M.W.; Wen, W.L.; Sergio, C.C.; Jing, W.; Su, S.O.; Erin, G.S.; Tao, S.C. Toxicol. Appl. Pharm. 2013, 272, 96-107.

[38] Oliver, B.; Katja, A.A.; Andreas, K.N.; Elke, S.; Ekaterina, E.; Bonnie, A.A.; Mitchell, A.A.; Martin, F.F.; Michel, E. Mol. Pharmacol. 2005, 67, 1954-1965.

[39] Devinder, S.; Aik, J.L.; Matthew, A.; Sherman; Thomas, K.H.C. Biochem.Pharmacol. 2013, 85, 1700-1711.

[40] Harmsen, S.; Meijerman, I.; Maas-Bakker, R.F.; Beijnen, J.H.; Schellens, J.H.M. Eur. J. Pharm. Sci. 2013, 48, 644-649.

[41] Rigalli, J.P.; Perdomo, V.G.; Luquita, M.G.; Villanueva, S.S.; Arias, A.; Theile, D.; Weiss, J.; Mottino, A.D.; Ruiz, M.L.; Catania, V.A. PloS. Neglect. Trop. D. , 6, 1951. 2012

[42] Navaratnarajah, P.; Steele, B.L.; Redinbo, M.R.; Thompson, N.L. Biochemistry. 2011, 51, 19-31.

[43] Hao, L.; Matthew, R.R.; Madhukumar, V.; Sean, E.; Anik, C.; Nicolin, B.; Abdissa, N.; Paromita, M.; Ganjam, K.; Sridhar, M.J. Biol. Chem. 2013, 288, 13655-13668.

[44] Christopher, K.G.; David, W.R.; Michael, G.R. Curr. Opin. Cell. Biol. 1997, 9, 222-232.

[45] Giovanni, R.; Barbara, R.; Elisabetta, A.; Daniela, P.; Roberto, P.; Stefano, F. Mol. Pharmacol. , 68, 551-558.2005

[46] Liu, C.L.; Lim, Y.P.; Hu, M.L. Mar. Drugs. 2012, 10, 242-257.

[47] Huang, H.; Wang, H.; Sinz, M.; Zoeckler, M.; Staudinger, J.; Redinbo, M.R.; Teotico, D.G.; Locker, J.; Kalpana, G.V.; Mani, S. Oncogene. 2007, 26, 258-268.

[48] Mandlekar, S.; Hong, J.L.; Kong, A.N. Curr. Drug Metab. 2006, 7, 661-675.

[49] Linda, B.M.; Derek, J.P.; Stacey, A.J.; Randy, K.B.; Thomas, G.C.; Julie, B.S.; Bryan, G.; Christopher, L.; Steven, G.B.; Timothy, M.W.; Jon, L.C.; Steven, A.K.J. Biol. Chem. 2000, 275, 15122-15127.

[50] Oliver, B.; Katja, A.A.; Anke, G.; Heike, T.; Michel, E. Biol. Chem. 2005, 386, 503-513.

[51] Yue, L.; Qi, W.; Xiao, M.Y.; Yan, L. Eur. J. Pharmacol. 2010, 640, 46-54.

[52] Supratim, C.; Yue, C.; Curtis, D.K. Toxicol. Appl. Pharmacol. 2010, 245, 378-393.

[53] Melson, J.; Li, Y.; Cassinotti, E.; Melnikov, A.; Boni, L.; Ai, J.; Greenspan, M.; Mobarhan, S.; Levenson, V.; Deng, Y. Int. J. Cancer. 2014, 134, 2656-2662.

[54] Emma, K.B.; Assam, E.O. Cancer Biol. Ther. 2004, 3, 819-824.

[55] Kamel, J.; Giorgio, B. Gene. 2004, 333, 143-149.

[56] Shi, C.J.; Wang, F.; Ren, M.F.; Mi, Y.J.; Yan, Y.Y.; To, K.K.W.; Dai, C.L.; Wang, Y.S.; Chen, L.M.; Tong, X.Z. Leukemia. Res. 2011, 35, 73-79.

[57] Reed, K.; Hembruff, S.L.; Sprowl, J.A.; Parissenti, A.M. Pharmacogenomics. J. 2010, 10, 489-504.

[58] Gayatri, S.; Sameer, M.; Rajinder, P.; Anurag, S.; Siddartha, D.G.; Pranav, P.; Ranju, R. Clin. Biochem. 2010, 43, 373-379.

[59] Huang, C.; Cao, P.; Xie, Z. J. Central South Univ. (Med Sci). 2009, 34, 369-374.

[60] Emma, K.B.; Ricky, W.J.; John, R.Z.; Assam, E.O. Oncogene. 2005, 24, 8061- 8075.

[61] Kim, S.N.; Kim, N.H.; Lee, W.; Seo, D.W.; Kim, Y.K. Mol. Cancer. Res. 2009, 7, 735-744.

[62] Tabe, Y.; Konopleva, M.; Contractor, R.; Munsell, M.; Schober, W.D.; Jin, L.; Tsutsumi-Ishii, Y.; Nagaoka, I.; Igari, J.; Andreeff, M. Blood. 2006, 107, 1546-1554.

[63] El-Khoury, V.; Breuzard, G.; Fourré, N.; Dufer, J. Br. J. Cancer. 2007, 97, 562-573.

[64] Sonia, Y.; Victoria, E.K.; Chantal, T.; Aurelie, T.R.; Rym, B.; Franck, B.; Jean, D. Int. J. Oncol. , 30, 1003-10020079.

[65] Curtis, D.K.; Hong, L.; Julia, Y.C. Toxicol. Mech. Method. 2011, 21, 312-324.

[66] Zhi, P.J.; Ping, X.; Guan, P.W.; Xie, L.Z.; Fang, P.C. Med. Hypotheses. 2010, 74, 92-94.

[67] Henrique, R.; Oliveira, A.I.; Costa, V.L.; Baptista, T. Martins, A.T.; Morais, A. Oliveira, J.; Jerónimo, C. BMC. Genomics. 2013, 14, 898.

[68] Hairong, H.; Pellegrino, G.M.; E-Christy, P.; Brijesh, B.P.; Kathleen, W.S. Cancer Res. 2010, 70, 8726-8735.

[69] Tang, B.; Zhang, Y.; Liang, R.; Gao, Z.; Sun, D.; Wang, L. Oncol. Rep. 2013, 29, 1037-1042.

[70] Gisel, A.; Valvano, M.; Elldrissi, I.G.; Nardulli, P.; Azzariti, A.; Carrieri, A.; Contino, M.; Colabufo, N.A. Molecules. 2014, 19, 5611-5623.

[71] Lopes-Rodrigues, V.; Seca, H.; Sousa, D.; Sousa, E.; Lima, R.T.; Vasconcelos, M.H. Int. J. Cancer. 2014, 135, 253- 263.

[72] Dong, Z.; Ren, L.; Lin, L.; Li, J.; Huang, Y.; Li, J. Mol. Med. Rep. 2015, 11, 682- 690.

[73] Zhang, H.; Li, M.; Han, Y.; Hong, L.; Gong, T.; Sun, L.; Zheng, X. Dig. Dis. Sci. 2010, 55, 2545-2551.

[74] Olga, K.; Jody, F.; James, M.; Yaroslav, I.; Volodymyr, P.T.; Vasy, F.C.; Igor, P.P. Mol. Cancer Ther. 2008, 7, 2152-2159.

[75] Liu, Z.M.; Hu, S.; Wang, J. Gynecol. Oncol. 2010, 119, 125-130.

[76] Callegari, E.; Liu, S.; Alder, H.; Costinean, S.; Fernandez-Cy-mering, C.; Volinia, S.; Guler, G.; Morrison, C.D.; Chan, K.K.; Marcucci, G.; Calin, G.A.; Huebner, K.; Croce, C.M. Natl. Acad. Sci. USA. , 104, 15805-15810.2007

[77] Sierk, H.; Ingolf, C. Pharmacogenomics. 2012, 13, 1321-1324.

[78] Tian, Y. Drug Metab. Rev. 2013, 45, 166-172.

[79] Ying, X.; Sui, K.; Nengtai, O.; Jinhan, H.; Wen, X.; Mark, T.B.; Yanan, T. J. Biol. Chem. 2009, 284, 9199-9205.

[80] Misra, R.; Das, M.; Sahoo, B.S.; Sahoo, S.K. Int. J. Pharm. 2014, 475, 372-384.

[81] Munoz, J.L.; Rodriguez-Cruz, V.; Greco, S.J.; Nagula, V.; Scotto, K.W.; Rameshwar, P. Mol. Cancer Ther. , 13, 2399-2411.2014