Asian Pacific Journal of Cancer Prevention

  • 제16권16호
  • /
  • Pages.6831-6839
  • /
  • 2015
  • /
  • 1513-7368(pISSN)
  • /
  • 2476-762X(eISSN)
아시아태평양암예방학회 (Asian Pacific Journal of Cancer Prevention)
권호 표지
DOI QR코드

DOI QR Code

Enhancing Activity of Anticancer Drugs in Multidrug Resistant Tumors by Modulating P-Glycoprotein through Dietary Nutraceuticals

  • Khan, Muhammad (College of Basic Medical Sciences, Dalian Medical University) ;
  • Maryam, Amara (College of Basic Medical Sciences, Dalian Medical University) ;
  • Mehmood, Tahir (College of Basic Medical Sciences, Dalian Medical University) ;
  • Zhang, Yaofang (College of Basic Medical Sciences, Dalian Medical University) ;
  • Ma, Tonghui (College of Basic Medical Sciences, Dalian Medical University)
  • 발행 : 2015.11.04
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Multidrug resistance is a principal mechanism by which tumors become resistant to structurally and functionally unrelated anticancer drugs. Resistance to chemotherapy has been correlated with overexpression of p-glycoprotein (p-gp), a member of the ATP-binding cassette (ABC) superfamily of membrane transporters. P-gp mediates resistance to a broad-spectrum of anticancer drugs including doxorubicin, taxol, and vinca alkaloids by actively expelling the drugs from cells. Use of specific inhibitors/blocker of p-gp in combination with clinically important anticancer drugs has emerged as a new paradigm for overcoming multidrug resistance. The aim of this paper is to review p-gp regulation by dietary nutraceuticals and to correlate this dietary nutraceutical induced-modulation of p-gp with activity of anticancer drugs.

키워드

참고문헌

  1. Abdallah HM, Al-Abd AM, El-Dine RS, et al (2015). P-glycoprotein inhibitors of natural origin as potential tumor chemo-sensitizers: A review. J Adv Res, 6, 45-62. https://doi.org/10.1016/j.jare.2014.11.008
  2. Aggarwal BB, Ichikawa H, (2005). Molecular targets and anticancer potential of indole-3-carbinol and its derivatives. Cell Cycle, 4, 1201-15. https://doi.org/10.4161/cc.4.9.1993
  3. Aggarwal BB, Kunnumakkara AB, Harikumar KB, et al (2008). Potential of spicederived phytochemicals for cancer prevention. Planta Med, 74, 1560-9. https://doi.org/10.1055/s-2008-1074578
  4. Aggarwal BB, Van Kuiken ME, Iyer LH, et al (2009). Molecular targets of nutraceuticals derived from dietary spices: potential role in suppression ofinflammation and tumorigenesis. Exp Biol Med, 234, 825-49. https://doi.org/10.3181/0902-MR-78
  5. Anuchapreeda S, Leechanachai P, Smith MM, et al (2002). Modulation of P-glycoprotein expression and function by curcumin in multidrug-resistant human KB cells. Biochem Pharmacol, 64, 573-82. https://doi.org/10.1016/S0006-2952(02)01224-8
  6. Arora A, Shukla Y (2003). Modulation of vinca-alkaloid induced P-glycoprotei expression by indole-3- carbinol. Cancer Lett, 189, 167-73. https://doi.org/10.1016/S0304-3835(02)00550-5
  7. Arora A, Seth K, Shukla Y, (2004). Reversal of P-glycoprotein-mediated multidrug resistance by diallyl sulfide in K562 leukemic cells and in mouse liver. Carcinogenesis, 25, 941-9. https://doi.org/10.1093/carcin/bgh060
  8. Arora A, Seth K, Kalra N, et al (2005). Modulation of P-glycoprotein-mediated multidrug resistance in K562 leukemic cells by indole-3-carbinol. Toxicol Appl Pharmacol, 202, 237-43. https://doi.org/10.1016/j.taap.2004.06.017
  9. Baguley BC, (2010). Multiple drug resistance mechanisms in cancer. Mol Biotechnol, 46, 308-16. https://doi.org/10.1007/s12033-010-9321-2
  10. Barthomeuf C, Grassi J, Demeule M, et al (2005). Inhibition of P-glycoprotein transport function and reversion of MDR1 multidrug resistance by cnidiadin. Cancer Chemother Pharmacol, 56, 173-81. https://doi.org/10.1007/s00280-004-0914-y
  11. Bezerra DP, de Castro FO, Alves AP, et al (2008). In vitro and in vivo antitumor effect of 5-FU combined with piplartine and piperine. J Appl Toxicol, 28, 156-63. https://doi.org/10.1002/jat.1261
  12. Bhardwaj RK, Glaeser H, Becquemont L,et al (2002). Piperine, a major constituent of black pepper, inhibits human P-glycoprotein and CYP3A4. J Pharmacol Exp Ther, 302, 645-50. https://doi.org/10.1124/jpet.102.034728
  13. Borska S, Chmielewska M, Wysocka T, et al (2012). In vitro effect of quercetin on human gastric carcinoma: targeting cancer cells death and MDR. Food Chem Toxicol, 50, 3375-83. https://doi.org/10.1016/j.fct.2012.06.035
  14. Callaghan R, Luk F, Bebawy M, (2014). Inhibition of the multidrug resistance P-glycoprotein: time for a change of strategy? Drug Metab Dispos, 42, 623-31. https://doi.org/10.1124/dmd.113.056176
  15. Chang C, Bahadduri PM, Polli JE, et al (2006). Rapid identification of P-glycoprotein substrates and inhibitors. Drug Metab Dispos, 34, 1976-84. https://doi.org/10.1124/dmd.106.012351
  16. Chang XB, (2010). Molecular mechanism of ATPdependent solute transport by multidrug resistance associated protein 1. Methods Mol Biol, 596, 223-49 https://doi.org/10.1007/978-1-60761-416-6_11
  17. Chen L, Li Y, Yu H, et al (2012). Computational models for predicting substrates or inhibitors of P-glycoprotein. Drug Discov Today, 17, 343-51. https://doi.org/10.1016/j.drudis.2011.11.003
  18. Chen Q, Zhang R, Li WM, et al (2013). The protective effect of grape seed procyanidin extract against cadmium-induced renal oxidative damage in mice. Environ Toxicol Pharmacol, 36, 759-68. https://doi.org/10.1016/j.etap.2013.07.006
  19. Chieli E, Romiti N, Rodeiro I, et al (2010). In vitro modulation of ABCB1/P-glycoprotein expression by polyphenols from Mangiferaindica. Chem Biol Interact, 186, 287-94. https://doi.org/10.1016/j.cbi.2010.05.012
  20. Choi BH, Kim CG, Lim Y, et al (2008). Curcumin downregulates the multidrug-resistance mdr1b gene by inhibiting the PI3K/Akt/NF kappa B pathway. Cancer Lett, 259, 111-8. https://doi.org/10.1016/j.canlet.2007.10.003
  21. Christensen JG, LeBlanc GA, (1996). Reversal of multidrug resistance in vivo by dietary administration of the phytochemical indole-3-carbinol. Cancer Res, 56, 574-581.
  22. Do MT, Kim HG, Choi JH, et al (2013).Anti-tumor efficacy of piperine in the treatment of human HER2-overexpressing breast cancer cells. Food Chem, 141, 2591-9. https://doi.org/10.1016/j.foodchem.2013.04.125
  23. Eichhorn T, Efferth T (2012). P-glycoprotein and its inhibition in tumors by phytochemicals derived from Chinese herbs. J Ethnopharmacol, 141, 557-70. https://doi.org/10.1016/j.jep.2011.08.053
  24. Eid SY, El-Readi MZ, Wink M (2012). Carotenoids reverse multidrug resistance in cancer cells by interfering with ABC-transporters. Phytomedicine, 19, 977-87. https://doi.org/10.1016/j.phymed.2012.05.010
  25. Eid SY, El-Readi MZ, Eldin EE, et al (2013). Influence of combinations of digitonin with selected phenolics, terpenoids, and alkaloids on the expression and activity of P-glycoprotein in leukaemia and colon cancer cells. Phytomedicine, 21, 47-61. https://doi.org/10.1016/j.phymed.2013.07.019
  26. Ferlay J, Soerjomataram I, Dikshit R, et al (2015). Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer, 136, 359-86. https://doi.org/10.1002/ijc.29210
  27. Ferreira MJ, Duarte N, Gyemant N, et al (2006). Interaction between doxorubicin and the resistance modifier stilbene on multidrug resistant mouse lymphoma and human breast cancer cells. Anticancer Res, 26, 3541-6.
  28. Ganta S, Amiji M (2009). Coadministration of Paclitaxel and curcumin in nanoemulsion formulations to overcome multidrug resistance in tumor cells. Mol Pharm, 6, 928-39. https://doi.org/10.1021/mp800240j
  29. Gillet JP, Gottesman MM, (2010). Mechanisms of multidrug resistance in cancer. Methods Mol Biol, 596, 47-76. https://doi.org/10.1007/978-1-60761-416-6_4
  30. Gottesman MM, Fojo T, Bates SE (2002). Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer, 2, 48-58. https://doi.org/10.1038/nrc706
  31. Han Y, Chin Tan TM, Lim LY (2008). In vitro and in vivo evaluation of the effects of piperine on P-gp function and expression. Toxicol Appl Pharmacol, 230, 283-9. https://doi.org/10.1016/j.taap.2008.02.026
  32. Han YL, Yu HL, Li D, et al (2011). Inhibitory effects of limonin on six human cytochrome P450 enzymes and P-glycoprotein in vitro. Toxicol In vitro, 25, 1828-33. https://doi.org/10.1016/j.tiv.2011.09.023
  33. Hsu CP, Lin YH, Chou CC, et al (2009). Mechanisms of grape seed procyanidin-induced apoptosis in colorectal carcinoma cells. Anticancer Res, 29, 283-9.
  34. Huang F, Wu XN, Chen J, et al (2014). Resveratrol reverses multidrug resistance in human breast cancer doxorubicin-resistant cells. Exp Ther Med, 7, 1611-6.
  35. Jasinski M, Jasinska L, Ogrodowczyk M, (2013). Resveratrol in prostate diseases - a short review. Cent European J Urol, 66, 144-9.
  36. Jemal A, Siegel R, Ward E, et al (2008). Cancer statistics, 2008. CA Cancer J Clin, 58, 71-96. https://doi.org/10.3322/CA.2007.0010
  37. Jodoin J, Demeule M, Beliveau R (2002). Inhibition of the multidrug resistance P-glycoprotein activity by green tea polyphenols. Biochim Biophys Acta, 1542, 149-59. https://doi.org/10.1016/S0167-4889(01)00175-6
  38. Kibria G, Hatakeyama H, Harashima H, (2014). Cancer multidrug resistance: mechanisms involved and strategies for circumvention using a drug delivery system. Arch Pharm Res, 37, 4-15. https://doi.org/10.1007/s12272-013-0276-2
  39. Kim TH, Shin YJ, Won AJ, et al (2014). Resveratrol enhances chemosensitivity of doxorubicin in multidrug-resistant human breast cancer cells via increased cellular influx of doxorubicin. Biochim Biophys Acta, 1840, 615-25. https://doi.org/10.1016/j.bbagen.2013.10.023
  40. Kweon SH, Song JH, Kim TS (2010). Resveratrolmediated reversal of doxorubicin resistance in acute myeloid leukemia cells via downregulation of MRP1 expression. Biochem Biophys Res Commun, 395, 104-10. https://doi.org/10.1016/j.bbrc.2010.03.147
  41. Lai KC, Kuo CL, Ho HC, et al (2012). Diallyl sulfide, diallyl disulfide and diallyltrisulfide affect drug resistant gene expression in colo 205 human colon cancer cells in vitro and in vivo. Phytomedicine, 19, 625-30. https://doi.org/10.1016/j.phymed.2012.02.004
  42. Li S, Lei Y, Jia Y, et al (2011). Piperine, apiperidine alkaloid from Piper nigrum re-sensitizes P-gp, MRP1 and BCRP dependent multidrug resistant cancer cells. Phytomedicine, 19, 83-7. https://doi.org/10.1016/j.phymed.2011.06.031
  43. Li S, Lo CY, Pan MH, et al (2013). Black tea: chemical analysis and stability. Food Funct, 4, 10-8. https://doi.org/10.1039/C2FO30093A
  44. Liu Z, Duan ZJ, Chang JY, et al (2014). Sinomenine sensitizes multidrug-resistant colon cancer cells (Caco-2) to doxorubicin by downregulation of MDR-1 expression. PLoS One, 9, 98560. https://doi.org/10.1371/journal.pone.0098560
  45. Mahmoud MF, Gamal S, El-Fayoumi HM (2014). Limonin attenuates hepatocellular injury following liver ischemia and reperfusion in rats via toll-like receptor dependent pathway. Eur J Pharmacol, 740, 676-82. https://doi.org/10.1016/j.ejphar.2014.06.010
  46. Mahringer A, Karamustafa S, Klotz D, et al (2010). Inhibition of P-glycoprotein at the blood-brain barrier by phytochemicals derived from traditional Chinese medicine. Cancer Genomics Proteomics, 7, 191-205.
  47. Mei Y, Qian F, Wei D, et al (2004). Reversal of cancer multidrug resistance by green tea polyphenols. J Pharm Pharmacol, 56, 1307-14. https://doi.org/10.1211/0022357044364
  48. Molnar J, Engi H, Hohmann J, et al (2010). Reversal of multidrug resitance by natural substances from plants. Curr Top Med Chem, 10, 1757-68. https://doi.org/10.2174/156802610792928103
  49. Mukkavilli R, Gundala SR, Yang C, et al (2014). Modulation of cytochrome P450 metabolism and transport across intestinal epithelial barrier by ginger biophenolics. PLoS One, 9, 108386. https://doi.org/10.1371/journal.pone.0108386
  50. NabekuraT, Kamiyama S, Kitagawa S, (2005). Effects of dietary chemopreventive phytochemicals on P-glycoprotein function. Biochem Biophys Res Commun, 327, 866-70. https://doi.org/10.1016/j.bbrc.2004.12.081
  51. Nabekura T, Yamaki T, Kitagawa S (2008a). Effects of chemopreventive citrus phytochemicals on human P-glycoprotein and multidrug resistance protein 1. Eur J Pharmacol, 600, 45-9. https://doi.org/10.1016/j.ejphar.2008.10.025
  52. Nabekura T, Yamaki T, Ueno K, et al (2008b). Inhibition of P-glycoprotein and multidrug resistance protein 1 by dietary phytochemicals. Cancer Chemother Pharmacol, 62, 867-73 https://doi.org/10.1007/s00280-007-0676-4
  53. Nabekura T (2010a). Overcoming multidrug resistance in human cancer cells by natural compounds. Toxins (Basel), 2, 1207-24. Nabekura T, Yamaki T, Hiroi T, et al (2010b). Inhibition of anticancer drug efflux transporter P-glycoprotein by rosemary phytochemicals. Pharmacol Res, 61, 259-63. https://doi.org/10.1016/j.phrs.2009.11.010
  54. Nabekura T, Yamaki T, Hiroi T, et al (2010b). Inhibition of anticancer drug efflux transporter P-glycoprotein by rosemary phytochemicals. Pharmacol Res, 61, 259-63. https://doi.org/10.1016/j.phrs.2009.11.010
  55. Nile SH, Park SW, (2014). Edible berries: bioactive components and their effect on human health. Nutrition, 30, 134-44. https://doi.org/10.1016/j.nut.2013.04.007
  56. Perestelo NR, Sanchez-Canete MP, Gamarro F, et al (2011). Overcoming human P-glycoprotein-dependent multidrug resistance with novel dihydro-beta- agarofuransesquiterpenes. Eur J Med Chem, 46, 4915-23. https://doi.org/10.1016/j.ejmech.2011.07.048
  57. Pitchakarn P, Ohnuma S, Pintha K, et al (2012). Kuguacin J isolated from Momordica charantia leaves inhibits P-glycoprotein (ABCB1)-mediated multidrug resistance. J Nutr Biochem, 23, 76-84. https://doi.org/10.1016/j.jnutbio.2010.11.005
  58. Polli JW, Wring SA, Humphreys JE, et al (2001). Rational use of in vitro P-glycoprotein assays in drug discovery. J Pharmacol Exp Ther, 299, 620-8.
  59. Pratheeshkumar P, Sreekala C, Zhang Z, et al (2012). Cancer prevention with promising natural products: mechanisms of action and molecular targets. Anticancer Agents Med Chem, 12, 1159-84. https://doi.org/10.2174/187152012803833035
  60. Qian F, Wei D, Zhang Q, et al (2005). Modulation of P-glycoprotein function and reversal of multidrug resistance by (-)-epigallocatechingallate in human cancer cells. Biomed Pharmacother, 59, 64-9. https://doi.org/10.1016/j.biopha.2005.01.002
  61. Sagor AT, Chowdhury MR, Tabassum N, et al (2015). Supplementation of fresh ucche (Momordicacharantia L. var. muricataWilld) prevented oxidative stress, fibrosis and hepatic damage in CCl4 treated rats. BMC Complement Altern Med, 15, 115. https://doi.org/10.1186/s12906-015-0636-1
  62. Siegel R, Naishadham D, Jemal A (2012). Cancer statistics for Hispanics/Latinos, 2012. CA Cancer J Clin, 62, 283-98. https://doi.org/10.3322/caac.21153
  63. Singh AK, Misra K, (2013). Human papilloma virus 16 E6 protein as a target for curcuminoids, curcumin conjugates and congeners for chemoprevention of oral and cervical cancers. Int Discip Sci, 5, 112-8.
  64. Szakacs G, Paterson JK, Ludwig JA, et al (2006). Targeting multidrug resistance in cancer. Nat Rev Drug Discov, 5, 219-34. https://doi.org/10.1038/nrd1984
  65. Temple NJ, Gladwin KK, (2003). Fruit, vegetables, and the prevention of cancer: research challenges. Nutrition, 19, 467-70. https://doi.org/10.1016/S0899-9007(02)01037-7
  66. Ueda K, Cardarelli C, Gottesman MM, et al (1987). Expression of a full-length cDNA for the human "MDR1" gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc Natl Acad Sci USA, 84, 3004-8. https://doi.org/10.1073/pnas.84.9.3004
  67. Vrolijk MF, Opperhuizen A, Jansen EH, et al (2015). The shifting perception on antioxidants: the case of vitamin E and beta-carotene. Redox Biol, 4, 272-8. https://doi.org/10.1016/j.redox.2014.12.017
  68. Wach A, Pyrzyńska K, Biesaga M (2007). Quercetincontent in some food and herbal samples. Food Chem, 100, 699-704. https://doi.org/10.1016/j.foodchem.2005.10.028
  69. Xia Q, Wang ZY, Li HQ, et al (2012). Reversion of p-glycoprotein-mediated multidrug resistance in human leukemic cell line by diallyltrisulfide. Evid Based Complement Alternat Med, 2012, 719805.
  70. Xu Y, Zhi F, Xu G, et al (2012). Overcoming multidrugresistance in vitro and in vivo using the novel P-glycoprotein inhibitor 1416. Bio Sci Rep, 32, 559-66. https://doi.org/10.1042/BSR20120020
  71. Yang C, Wong IL, Jin WB, et al (2014). Modification of marine natural product ningalin B and SAR study lead to potent P-glycoprotein inhibitors. Mar Drugs, 12, 5209-21. https://doi.org/10.3390/md12105209
  72. Ye MX, Zhao YL, Li Y, et al (2012). Curcumin reverses cis-platin resistance and promotes human lung adenocarcinoma A549/DDP cell apoptosis through HIF-1alpha and caspase-3 mechanisms. Phytomedicine, 19, 779-87. https://doi.org/10.1016/j.phymed.2012.03.005
  73. Yoshida N, Takagi A, Kitazawa H, et al (2005). Inhibition of P-glycoprotein-mediated transport by extracts of and monoterpenoids contained in Zanthoxylifructus. Toxicol Appl Pharmacol, 209, 167-73. https://doi.org/10.1016/j.taap.2005.04.001
  74. Zeino M, Paulsen MS, Zehl M, et al (2015). Identification of new P-glycoprotein inhibitors derived from cardiotonic steroids. Biochem Pharmacol, 93, 11-24. https://doi.org/10.1016/j.bcp.2014.10.009
  75. Zhang S, Morris ME (2003). Effects of the flavonoids biochanin A, morin, phloretin, and silymarin on P-glycoprotein-mediated transport. J Pharmacol Exp Ther, 304, 1258-67.
  76. Zhang W, Han Y, Lim SL, et al (2009). Dietary regulation of P-gp function and expression. Expert Opin Drug Metab Toxicol, 5, 789-801. https://doi.org/10.1517/17425250902997967
  77. Zhao BX, Sun YB, Wang SQ, et al (2013). Grape seed procyanidin reversal of p-glycoprotein associated multi-drug resistance via down-regulation of NF-КB and MAPK/ERK mediated YB-1 activity in A2780/T cells. PLoS One, 8, 71071. https://doi.org/10.1371/journal.pone.0071071
  78. Zhou S, Lim LY, Chowbay B (2004). Herbal modulation of P-glycoprotein. Drug Metab Rev, 36, 57-104. https://doi.org/10.1081/DMR-120028427
  79. Zorofchian Moghadamtousi S, Karimian H, Khanabdali R, et al (2014). Anticancer and antitumor potential of fucoidan and fucoxanthin, two main metabolites isolated from brown algae. Sci J, 768323.

피인용 문헌

  1. Complementary medicine in oncology and prognosis vol.23, pp.3, 2017, https://doi.org/10.1007/s00761-016-0155-9
  2. Multifunctional micelle delivery system for overcoming multidrug resistance of doxorubicin pp.1029-2330, 2017, https://doi.org/10.1080/1061186X.2017.1379525