Curcumin as a modulator of P-glycoprotein in cancer: Challenges and perspectives

Pharmaceuticals

Volumn 9, Issue 4, 2016, Pages

  Lopes Rodrigues, Vanessa ^a,b   Sousa, Emília ^b,c   Vasconcelos, M Helena ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

Author keywords

Curcumin; Curcumin analogs; Multidrug resistance; P glycoprotein

Indexed keywords

CURCUMIN; DEMETHOXYCURCUMIN; DIDEMETHOXYCURCUMIN; MULTIDRUG RESISTANCE PROTEIN;

ANTINEOPLASTIC ACTIVITY; CANCER CELL LINE; CANCER INHIBITION; DOWN REGULATION; DRUG DELIVERY SYSTEM; DRUG STRUCTURE; GENE OVEREXPRESSION; HUMAN; MULTIDRUG RESISTANCE; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TUMOR XENOGRAFT;

EID: 84997077016     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph9040071     Document Type: Review

References (61)

1. Gottesman, M.M., Fojo, T., Bates, S.E. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat. Revi. Cancer 2002, 2, 48-58. [CrossRef] [PubMed]
2. Lopes-Rodrigues, V., Seca, H., Sousa, D., Sousa, E., Lima, R.T., Vasconcelos, M.H. The network of P-glycoprotein and microRNAs interactions. Int. J. Cancer 2014, 135, 253-263. [CrossRef] [PubMed]
3. Eckford, P.D., Sharom, F.J. ABC efflux pump-based resistance to chemotherapy drugs. Chem. Rev. 2009, 109, 2989-3011. [CrossRef] [PubMed]
4. Krishna, R., Mayer, L.D. Modulation of P-glycoprotein (PGP) mediated multidrug resistance (MDR) using chemosensitizers: Recent advances in the design of selective MDR modulators. Curr. Med. Chem. Anticancer Agents 2001, 1, 163-174. [CrossRef] [PubMed]
5. Srinivas, E., Murthy, J.N., Rao, A.R., Sastry, G.N. Recent advances in molecular modeling and medicinal chemistry aspects of phospho-glycoprotein. Curr. Drug Metab. 2006, 7, 205-217. [CrossRef] [PubMed]
6. Stenham, D.R., Campbell, J.D., Sansom, M.S., Higgins, C.F., Kerr, I.D., Linton, K.J. An atomic detail model for the human ATP binding cassette transporter P-glycoprotein derived from disulfide cross-linking and homology modeling. FASEB J. 2003, 17, 2287-2289. [PubMed]
7. Palmeira, A., Vasconcelos, M.H., Paiva, A., Fernandes, M.X., Pinto, M., Sousa, E. Dual inhibitors of P-glycoprotein and tumor cell growth: (Re)discovering thioxanthones. Biochem. Pharmacol. 2012, 83, 57-68. [CrossRef] [PubMed]
8. Palmeira, A., Sousa, E., Vasconcelos, M.H., Pinto, M., Fernandes, M.X. Structure and ligand-based design of P-glycoprotein inhibitors: A historical perspective. Curr. Pharm. Des. 2012, 18, 4197-4214. [CrossRef] [PubMed]
9. Krishna, R., Mayer, L.D. Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs. Eur. J. Pharm. Sci. 2000, 11, 265-283. [CrossRef]
10. Liscovitch, M., Lavie, Y. Cancer multidrug resistance: A review of recent drug discovery research. IDrugs 2002, 5, 349-355. [PubMed]
11. Colegate, S.M., Molyneux, R.J. Bioactive Natural Products: Detection, Isolation and Structural Determination, 2nd ed., CRC Press: Boca Raton, FL, USA, 2008.
12. Newman, D.J., Cragg, G.M. Natural products as sources of new drugs over the last 25 years. J. Nat. Prod. 2007, 70, 461-477. [CrossRef] [PubMed]
13. Conseil, G., Baubichon-Cortay, H., Dayan, G., Jault, J.M., Barron, D., di Pietro, A. Flavonoids: A class of modulators with bifunctional interactions at vicinal ATP-and steroid-binding sites on mouse P-glycoprotein. Proc. Natl. Acad. Sci. USA 1998, 95, 9831-9836. [CrossRef] [PubMed]
14. Zhang, S., Morris, M.E. Effects of the flavonoids biochanin A, morin, phloretin, and silymarin on P-glycoprotein-mediated transport. J. Pharmacol. Exp. Ther. 2003, 304, 1258-1267. [CrossRef] [PubMed]
15. Nabekura, T., Kamiyama, S., Kitagawa, S. Effects of dietary chemopreventive phytochemicals on P-glycoprotein function. Biochem. Biophys. Res. Commun. 2005, 327, 866-870. [CrossRef] [PubMed]
16. Sharma, R.A., Gescher, A.J., Steward, W.P. Curcumin: The story so far. Eur. J. Cancer 2005, 41, 1955-1968. [CrossRef] [PubMed]
17. Chen, S.Y., Chen, Y., Li, Y.P., Chen, S.H., Tan, J.H., Ou, T.M., Gu, L.Q., Huang, Z.S. Design, synthesis, and biological evaluation of curcumin analogues as multifunctional agents for the treatment of Alzheimer’s disease. Bioorg. Med. Chem. 2011, 19, 5596-5604. [CrossRef] [PubMed]
18. Shishodia, S., Sethi, G., Aggarwal, B.B. Curcumin: Getting back to the roots. Ann. N. Y. Acad. Sci. 2005, 1056, 206-217. [CrossRef] [PubMed]
19. Mazumder, A., Raghavan, K., Weinstein, J., Kohn, K.W., Pommier, Y. Inhibition of human immunodeficiency virus type-1 integrase by curcumin. Biochem. Pharmacol. 1995, 49, 1165-1170. [CrossRef]
20. Rai, D., Singh, J.K., Roy, N., Panda, D. Curcumin inhibits FtsZ assembly: An attractive mechanism for its antibacterial activity. Biochem. J. 2008, 410, 1471-1455. [CrossRef] [PubMed]
21. Anand, P., Thomas, S.G., Kunnumakkara, A.B., Sundaram, C., Harikumar, K.B., Sung, B., Tharakan, S.T., Misra, K., Priyadarsini, I.K., Rajasekharan, K.N., et al. Biological activities of curcumin and its analogues (Congeners) made by man and Mother Nature. Biochem. Pharmacol. 2008, 76, 1590-1611. [CrossRef] [PubMed]
22. Yu, L.L., Wu, J.G., Dai, N., Yu, H.G., Si, J.M. Curcumin reverses chemoresistance of human gastric cancer cells by downregulating the NF-kappaB transcription factor. Oncol. Rep. 2011, 26, 1197-1203. [PubMed]
23. Wichitnithad, W., Nimmannit, U., Wacharasindhu, S., Rojsitthisak, P. Synthesis, characterization and biological evaluation of succinate prodrugs of curcuminoids for colon cancer treatment. Molecules 2011, 16, 1888-1900. [CrossRef] [PubMed]
24. Yodkeeree, S., Ampasavate, C., Sung, B., Aggarwal, B.B., Limtrakul, P. Demethoxycurcumin suppresses migration and invasion of MDA-MB-231 human breast cancer cell line. Eur. J. Pharmacol. 2010, 627, 8-15. [CrossRef] [PubMed]
25. He, Z.Y., Shi, C.B., Wen, H., Li, F.L., Wang, B.L., Wang, J. Upregulation of p53 expression in patients with colorectal cancer by administration of curcumin. Cancer. Investig. 2011, 29, 208-213. [CrossRef] [PubMed]
26. Dhillon, N., Aggarwal, B.B., Newman, R.A., Wolff, R.A., Kunnumakkara, A.B., Abbruzzese, J.L., Ng, C.S., Badmaev, V., Kurzrock, R. Phase II trial of curcumin in patients with advanced pancreatic cancer. Clin. Cancer Res. 2008, 14, 4491-4499. [CrossRef] [PubMed]
27. Ide, H., Tokiwa, S., Sakamaki, K., Nishio, K., Isotani, S., Muto, S., Hama, T., Masuda, H., Horie, S. Combined inhibitory effects of soy isoflavones and curcumin on the production of prostate-specific antigen. Prostate 2010, 70, 1127-1133. [CrossRef] [PubMed]
28. Wang, H., Geng, Q.R., Wang, L., Lu, Y. Curcumin potentiates antitumor activity of L-asparaginase via inhibition of the AKT signaling pathway in acute lymphoblastic leukemia. Leuk Lymphoma 2012, 53, 1376-1382. [CrossRef] [PubMed]
29. Hussain, A.R., Al-Rasheed, M., Manogaran, P.S., Al-Hussein, K.A., Platanias, L.C., al Kuraya, K., Uddin, S. Curcumin induces apoptosis via inhibition of PI3’-kinase/AKT pathway in acute T cell leukemias. Apoptosis 2006, 11, 245-254. [CrossRef] [PubMed]
30. Anuchapreeda, S., Thanarattanakorn, P., Sittipreechacharn, S., Tima, S., Chanarat, P., Limtrakul, P. Inhibitory effect of curcumin on MDR1 gene expression in patient leukemic cells. Arch. Pharm. Res. 2006, 29, 866-873. [CrossRef] [PubMed]
31. Choi, B.H., Kim, C.G., Lim, Y., Shin, S.Y., Lee, Y.H. Curcumin down-regulates the multidrug-resistance mdr1b gene by inhibiting the PI3K/Akt/NF kappa B pathway. Cancer Lett. 2008, 259, 111-118. [CrossRef] [PubMed]
32. Neerati, P., Sudhakar, Y.A., Kanwar, J.R. Curcumin Regulates Colon Cancer by Inhibiting P-Glycoprotein in In-situ Cancerous Colon Perfusion Rat Model. J. Cancer Sci. Ther. 2013, 5, 313-319. [PubMed]
33. Oliveira, A.S., Sousa, E., Vasconcelos, M.H., Pinto, M. Curcumin: A Natural Lead for Potential New Drug Candidates. Curr. Med. Chem. 2015, 22, 4196-4232. [CrossRef] [PubMed]
34. Anuchapreeda, S., Leechanachai, P., Smith, M.M., Ambudkar, S.V., Limtrakul, P.N. Modulation of P-glycoprotein expression and function by curcumin in multidrug-resistant human KB cells. Biochem. Pharmacol. 2002, 64, 573-582. [CrossRef]
35. Chearwae, W., Anuchapreeda, S., Nandigama, K., Ambudkar, S.V., Limtrakul, P. Biochemical mechanism of modulation of human P-glycoprotein (ABCB1) by curcumin I, II, and III purified from Turmeric powder. Biochem. Pharmacol. 2004, 68, 2043-2052. [CrossRef] [PubMed]
36. Tang, X.Q., Bi, H., Feng, J.Q., Cao, J.G. Effect of curcumin on multidrug resistance in resistant human gastric carcinoma cell line SGC7901/VCR. Acta Pharmacol. Sin. 2005, 26, 1009-1016. [CrossRef] [PubMed]
37. Limtrakul, P., Chearwae, W., Shukla, S., Phisalphong, C., Ambudkar, S.V. Modulation of function of three ABC drug transporters, P-glycoprotein (ABCB1), mitoxantrone resistance protein (ABCG2) and multidrug resistance protein 1 (ABCC1) by tetrahydrocurcumin, a major metabolite of curcumin. Mol. Cell. Biochem. 2007, 296, 85-95. [CrossRef] [PubMed]
38. Xu, D., Tian, W., Shen, H. Curcumin prevents induced drug resistance: A novel function? Chin. J. Cancer Res. 2011, 23, 218-223. [CrossRef] [PubMed]
39. Limtrakul, P., Anuchapreeda, S., Buddhasukh, D. Modulation of human multidrug-resistance MDR-1 gene by natural curcuminoids. BMC Cancer 2004, 4, 13. [CrossRef] [PubMed]
40. Lu, W. D., Qin, Y., Yang, C., Li, L., Fu, Z.X. Effect of curcumin on human colon cancer multidrug resistance in vitro and in vivo. Clinics 2013, 68, 694-701. [CrossRef]
41. Xu, D., Tian, W., Shen, H. P-gp upregulation may be blocked by natural curcuminoids, a novel class of chemoresistance-preventing agent. Mol. Med. Rep. 2013, 7, 115-121. [PubMed]
42. Noratto, G.D., Jutooru, I., Safe, S., Angel-Morales, G., Mertens-Talcott, S.U. The drug resistance suppression induced by curcuminoids in colon cancer SW-480 cells is mediated by reactive oxygen species-induced disruption of the microRNA-27a-ZBTB10-Sp axis. Mol. Nutr. Food Res. 2013, 57, 1638-1648. [CrossRef] [PubMed]
43. Anand, P., Kunnumakkara, A.B., Newman, R.A., Aggarwal, B.B. Bioavailability of curcumin: Problems and promises. Mol. Pharm. 2007, 4, 807-818. [CrossRef] [PubMed]
44. Cheng, A.L., Hsu, C.H., Lin, J.K., Hsu, M.M., Ho, Y.F., Shen, T.S., Ko, J.Y., Lin, J.T., Lin, B.R., Ming-Shiang, W., et al. Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res. 2001, 21, 2895-2900. [PubMed]
45. Vareed, S.K., Kakarala, M., Ruffin, M.T., Crowell, J.A., Normolle, D.P., Djuric, Z., Brenner, D.E. Pharmacokinetics of curcumin conjugate metabolites in healthy human subjects. Cancer Epidemiol. Biomark. Prev. 2008, 17, 1411-1417. [CrossRef] [PubMed]
46. Ganta, S., Amiji, M. Coadministration of Paclitaxel and curcumin in nanoemulsion formulations to overcome multidrug resistance in tumor cells. Mol. Pharm. 2009, 6, 928-939. [CrossRef] [PubMed]
47. Zhao, X., Chen, Q., Li, Y., Tang, H., Liu, W., Yang, X. Doxorubicin and curcumin co-delivery by lipid nanoparticles for enhanced treatment of diethylnitrosamine-induced hepatocellular carcinoma in mice. Eur. J. Pharm. Biopharm. 2015, 93, 27-36. [CrossRef] [PubMed]
48. Wang, J., Wang, F., Li, F., Zhang, W., Shen, Y., Zhou, D., Guo, S. A multifunctional poly(curcumin) nanomedicine for dual-modal targeted delivery, intracellular responsive release, dual-drug treatment and imaging of multidrug resistant cancer cells. J. Mater. Chem. B Mater. Biol. Med. 2016, 4, 2954-2962. [CrossRef] [PubMed]
49. Duan, J., Mansour, H.M., Zhang, Y., Deng, X., Chen, Y., Wang, J., Pan, Y., Zhao, J. Reversion of multidrug resistance by co-encapsulation of doxorubicin and curcumin in chitosan/poly(butyl cyanoacrylate) nanoparticles. Int. J. Pharm. 2012, 426, 193-201. [CrossRef] [PubMed]
50. Punfa, W., Yodkeeree, S., Pitchakarn, P., Ampasavate, C., Limtrakul, P. Enhancement of cellular uptake and cytotoxicity of curcumin-loaded PLGA nanoparticles by conjugation with anti-P-glycoprotein in drug resistance cancer cells. Acta Pharmacol. Sin. 2012, 33, 823-831. [CrossRef] [PubMed]
51. Punfa, W., Suzuki, S., Pitchakarn, P., Yodkeeree, S., Naiki, T., Takahashi, S., Limtrakul, P. Curcumin-loaded PLGA nanoparticles conjugated with anti-P-glycoprotein antibody to overcome multidrug resistance. Asian Pac. J. Cancer Prev. 2014, 15, 9249-9258. [CrossRef] [PubMed]
52. Patil, S., Choudhary, B., Rathore, A., Roy, K., Mahadik, K. Enhanced oral bioavailability and anticancer activity of novel curcumin loaded mixed micelles in human lung cancer cells. Phytomedicine 2015, 22, 1103-1111. [CrossRef] [PubMed]
53. Saxena, V., Hussain, M.D. Polymeric mixed micelles for delivery of curcumin to multidrug resistant ovarian cancer. J. Biomed. Nanotechnol. 2013, 9, 1146-1154. [CrossRef] [PubMed]
54. Wang, J., Ma, W., Tu, P. Synergistically Improved Anti-tumor Efficacy by Co-delivery Doxorubicin and Curcumin Polymeric Micelles. Macromol. Biosci. 2015, 15, 1252-1261. [CrossRef] [PubMed]
55. Lv, L., Qiu, K., Yu, X., Chen, C., Qin, F., Shi, Y., Ou, J., Zhang, T., Zhu, H., Wu, J., et al. Amphiphilic Copolymeric Micelles for Doxorubicin and Curcumin Co-Delivery to Reverse Multidrug Resistance in Breast Cancer. J. Biomed. Nanotechnol. 2016, 12, 973-985. [CrossRef] [PubMed]
56. Um, Y., Cho, S., Woo, H.B., Kim, Y.K., Kim, H., Ham, J., Kim, S.N., Ahn, C.M., Lee, S. Synthesis of curcumin mimics with multidrug resistance reversal activities. Bioorg. Med. Chem. 2008, 16, 3608-3615. [CrossRef] [PubMed]
57. Revalde, J.L., Li, Y., Hawkins, B.C., Rosengren, R.J., Paxton, J.W. Heterocyclic cyclohexanone monocarbonyl analogs of curcumin can inhibit the activity of ATP-binding cassette transporters in cancer multidrug resistance. Biochem. Pharmacol. 2015, 93, 305-317. [CrossRef] [PubMed]
58. Ooko, E., Alsalim, T., Saeed, B., Saeed, M.E., Kadioglu, O., Abbo, H.S., Titinchi, S.J., Efferth, T. Modulation of P-glycoprotein activity by novel synthetic curcumin derivatives in sensitive and multidrug-resistant T-cell acute lymphoblastic leukemia cell lines. Toxicol. Appl. Pharmacol. 2016, 305, 216-233. [CrossRef] [PubMed]
59. Mapoung, S., Pitchakarn, P., Yodkeeree, S., Ovatlarnporn, C., Sakorn, N., Limtrakul, P. Chemosensitizing effects of synthetic curcumin analogs on human multi-drug resistance leukemic cells. Chem. Biol. Interact. 2016, 244, 140-148. [CrossRef] [PubMed]
60. Liang, G., Shao, L., Wang, Y., Zhao, C., Chu, Y., Xiao, J., Zhao, Y., Li, X., Yang, S. Exploration and synthesis of curcumin analogues with improved structural stability both in vitro and in vivo as cytotoxic agents. Bioorg. Med. Chem. 2009, 17, 2623-2631. [CrossRef] [PubMed]
61. Ambudkar, S.V., Dey, S., Hrycyna, C.A., Ramachandra, M., Pastan, I., Gottesman, M.M. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol. Toxicol. 1999, 39, 361-398. [CrossRef] [PubMed]