Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

Curcumin-loaded PLGA Nanoparticles Conjugated with Anti-P-glycoprotein Antibody to Overcome Multidrug Resistance

  • Punfa, Wanisa (Department of Biochemistry, Faculty of Medicine, Chiang Mai University) ;
  • Suzuki, Shugo (Department of Experimental Pathology and Tumor Biology Graduate School of Medical Science, Nagoya City University) ;
  • Pitchakarn, Pornsiri (Department of Biochemistry, Faculty of Medicine, Chiang Mai University) ;
  • Yodkeeree, Supachai (Department of Biochemistry, Faculty of Medicine, Chiang Mai University) ;
  • Naiki, Taku (Department of Experimental Pathology and Tumor Biology Graduate School of Medical Science, Nagoya City University) ;
  • Takahashi, Satoru (Department of Experimental Pathology and Tumor Biology Graduate School of Medical Science, Nagoya City University) ;
  • Limtrakul, Pornngarm (Department of Biochemistry, Faculty of Medicine, Chiang Mai University)
  • Published : 2014.11.28
Download PDF
⟨ Previous Next ⟩

Abstract

Background: The encapsulation of curcumin (Cur) in polylactic-co-glycolic acid (PLGA) nanoparticles (Cur-NPs) was designed to improve its solubility and stability. Conjugation of the Cur-NPs with anti-P-glycoprotein (P-gp) antibody (Cur-NPs-APgp) may increase their targeting to P-gp, which is highly expressed in multidrugresistance (MDR) cancer cells. This study determined whether Cur-NPs-APgp could overcome MDR in a human cervical cancer model (KB-V1 cells) in vitro and in vivo. Materials and Methods: First, we determined the MDR-reversing property of Cur in P-gp-overexpressing KB-V1 cells in vitro and in vivo. Cur-NPs and Cur-NPs-APgp, in the range 150-180 nm, were constructed and subjected to an in vivo pharmacokinetic study compared with Cur. The in vitro and in vivo MDR-reversing properties of Cur-NPs and Cur-NPs-APgp were then investigated. Moreover, the stability of the NPs was determined in various solutions. Results: The combined treatment of paclitaxel (PTX) with Cur dramatically decreased cell viability and tumor growth compared to PTX treatment alone. After intravenous injection, Cur-NPs-APgp and Cur-NPs could be detected in the serum up to 60 and 120 min later, respectively, whereas Cur was not detected after 30 min. Pretreatment with Cur-NPs-APgp, but not with NPs or Cur-NPs, could enhance PTX sensitivity both in vitro and in vivo. The constructed NPs remained a consistent size, proving their stability in various solutions. Conclusions: Our functional Cur-NPs-APgp may be a suitable candidate for application in a drug delivery system for overcoming drug resistance. The further development of Cur-NPs-APgp may be beneficial to cancer patients by leading to its use as either as a MDR modulator or as an anticancer drug.

Keywords

References

  1. Abdelwahed W, Degobert G, Stainmesse S, Fessi H (2006). Freeze-drying of nanoparticles: formulation, process and storage considerations. Adv Drug Deliv Rev, 58, 1688-713. https://doi.org/10.1016/j.addr.2006.09.017
  2. Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB (2007). Bioavailability of curcumin: problems and promises. Mol Pharm, 4, 807-18. https://doi.org/10.1021/mp700113r
  3. Anuchapreeda S, Leechanachai P, Smith MM, Ambudkar SV, Limtrakul PN (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
  4. Bain LJ, McLachlan JB, LeBlanc GA (1997). Structureactivity relationships for xenobiotic transport substrates and inhibitory ligands of P-glycoprotein. Environ Health Perspect, 105, 812-8. https://doi.org/10.1289/ehp.97105812
  5. Burgio DE, Gosland MP, McNamara a PJ (1998). Effects of P-glycoprotein modulators on etoposide elimination and central nervous system distribution. J Pharmacol Exp Ther, 287, 911-7.
  6. Chang G (2003). Multidrug resistance ABC transporters. FEBS Letters, 555, 102-5. https://doi.org/10.1016/S0014-5793(03)01085-8
  7. Chearwae W, Anuchapreeda S, Nandigama K, Ambudkar SV, Limtrakul P (2004). Biochemical mechanism of modulation of human P-glycoprotein (ABCB1) by curcumin I, II, and III purified from Turmeric powder. Biochem Pharmacol, 68, 2043-52. https://doi.org/10.1016/j.bcp.2004.07.009
  8. Cho K, Wang X, Nie S, Chen ZG, Shin DM (2008). Therapeutic nanoparticles for drug delivery in cancer. Clin Cancer Res, 14, 1310-6. https://doi.org/10.1158/1078-0432.CCR-07-1441
  9. CIOMS (1985). International guiding principles for biomedical research involving animals. Altern Lab Anim, 12, 2.
  10. Cirstoiu-Hapca A, Buchegger F, Lange N, et al (2010). Benefit of anti-HER2-coated paclitaxel-loaded immuno-nanoparticles in the treatment of disseminated ovarian cancer: Therapeutic efficacy and biodistribution in mice. J Control Release, 144, 324-31. https://doi.org/10.1016/j.jconrel.2010.02.026
  11. Cisternino S, Rousselle C, Debray M, Scherrmann JM (2004). In situ transport of vinblastine and selected P-glycoprotein substrates: implications for drug-drug interactions at the mouse blood-brain barrier. Pharm Res, 21, 1382-9. https://doi.org/10.1023/B:PHAM.0000036911.49191.da
  12. Dai X-Z, Yin H-T, Sun L-F, et al (2013). Potential therapeutic efficacy of curcumin in liver cancer. Asian Pac J Cancer Prev, 14, 3855-9. https://doi.org/10.7314/APJCP.2013.14.6.3855
  13. Gallo JM, Li S, Guo P, Reed K, Ma J (2003). The effect of P-glycoprotein on paclitaxel brain and brain tumor distribution in mice. Cancer Res, 63, 5114-7.
  14. Hu YP, Pourquier P, Doignon F, Crouzet M, Robert J (1996). Effects of modulators of multidrug resistance on the expression of the MDR1 gene on human KB cells in culture. Anticancer Drugs, 7, 738-44. https://doi.org/10.1097/00001813-199609000-00004
  15. Iangcharoen P, Punfa W, Yodkeeree S, et al (2011). Anti-Pglycoprotein conjugated nanoparticles for targeting drug delivery in cancer treatment. Arch Pharm Res, 34, 1679-89. https://doi.org/10.1007/s12272-011-1012-4
  16. Jang SH, Wientjes MG, Au JL (2001). Kinetics of P-glycoproteinmediated efflux of paclitaxel. J Pharmacol Exp Ther, 298, 1236-42.
  17. Kiziltepe T, Ashley JD, Stefanick JF, et al (2012). Rationally engineered nanoparticles target multiple myeloma cells, overcome cell-adhesion-mediated drug resistance, and show enhanced efficacy in vivo. Blood Cancer J, 2, 64. https://doi.org/10.1038/bcj.2012.10
  18. Lazzari S, Moscatelli D, Codari F, et al (2012). Colloidal stability of polymeric nanoparticles in biological fluids. J Nanopart Res, 14, 920. https://doi.org/10.1007/s11051-012-0920-7
  19. Limtrakul P, Khantamat O, Pintha K (2004). Inhibition of P-glycoprotein activity and reversal of cancer multidrug resistance by Momordica charantia extract. Cancer Chemother Pharmacol, 54, 525-30. https://doi.org/10.1007/s00280-004-0848-4
  20. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K (2000). Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release, 65, 271-84. https://doi.org/10.1016/S0168-3659(99)00248-5
  21. Makadia HK, Siegel SJ (2011). Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers (Basel), 3, 1377-97. https://doi.org/10.3390/polym3031377
  22. Manjunath K, Venkateswarlu V (2005). Pharmacokinetics, tissue distribution and bioavailability of clozapine solid lipid nanoparticles after intravenous and intraduodenal administration. J Control Release, 107, 215-28. https://doi.org/10.1016/j.jconrel.2005.06.006
  23. Mechetner EB, Roninson IB (1992). Efficient inhibition of P-glycoprotein-mediated multidrug resistance with a monoclonal antibody. Proc Natl Acad Sci U S A, 89, 5824-8. https://doi.org/10.1073/pnas.89.13.5824
  24. Meng H, Mai WX, Zhang H, et al (2013). Codelivery of an optimal drug/siRNA combination using mesoporous silica nanoparticles to overcome drug resistance in breast cancer in vitro and in vivo. ACS Nano, 7, 994-1005. https://doi.org/10.1021/nn3044066
  25. Ohara Y, Oda T, Yamada K, et al (2012). Effective delivery of chemotherapeutic nanoparticles by depleting host Kupffer cells. Int J Cancer, 131, 2402-10. https://doi.org/10.1002/ijc.27502
  26. Oyagbemi AA, Saba AB, Ibraheem AO (2009). Curcumin: from food spice to cancer prevention. Asian Pac J Cancer Prev, 10, 963-7.
  27. Punfa W, Yodkeeree S, Pitchakarn P, Ampasavate C, Limtrakul P (2012). 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, 33, 823-31. https://doi.org/10.1038/aps.2012.34
  28. Qiao WJ, Cheng HY, Li CQ, et al (2011). Identification of pathways involved in paclitaxel activity in cervical cancer. Asian Pac J Cancer Prev, 12, 99-102.
  29. Qureshi S, Shah AH, Ageel AM (1992). Toxicity studies on Alpinia galanga and Curcuma longa. Planta Med, 58, 124-7. https://doi.org/10.1055/s-2006-961412
  30. Sadauskas E, Wallin H, Stoltenberg M, et al (2007). Kupffer cells are central in the removal of nanoparticles from the organism. Part Fibre Toxicol, 4, 10. https://doi.org/10.1186/1743-8977-4-10
  31. Shehzad A, Wahid F, Lee YS (2010). Curcumin in cancer chemoprevention: molecular targets, pharmacokinetics, bioavailability, and clinical trials. Arch Pharm, 343, 489-99. https://doi.org/10.1002/ardp.200900319
  32. Shen F, Chu S, Bence AK, et al (2008). Quantitation of doxorubicin uptake, efflux, and modulation of multidrug resistance (MDR) in MDR human cancer cells. J Pharmacol Exp Ther, 324, 95-102.
  33. Song Z, Feng R, Sun M, et al (2011). Curcumin-loaded PLGA-PEG-PLGA triblock copolymeric micelles: Preparation, pharmacokinetics and distribution in vivo. J Colloid Interface Sci, 354, 116-23. https://doi.org/10.1016/j.jcis.2010.10.024
  34. Tabatabaei Mirakabad FS, Nejati-Koshki K, Akbarzadeh A, et al (2014). PLGA-Based Nanoparticles as Cancer Drug Delivery Systems. Asian Pac J Cancer Prev, 15, 517-35. https://doi.org/10.7314/APJCP.2014.15.2.517
  35. Torchilin VP (2005). Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov, 4, 145-60. https://doi.org/10.1038/nrd1632
  36. Tsai YM, Chien CF, Lin LC, Tsai TH (2011). Curcumin and its nano-formulation: the kinetics of tissue distribution and blood-brain barrier penetration. Int J Pharm, 416, 331-8. https://doi.org/10.1016/j.ijpharm.2011.06.030
  37. Wang W, Zhu R, Xie Q, et al (2012). Enhanced bioavailability and efficiency of curcumin for the treatment of asthma by its formulation in solid lipid nanoparticles. Int J Nanomedicine, 7, 3667-77.
  38. Yadav D, Anwar MF, Garg V, et al (2014). Development of polymeric nanopaclitaxel and comparison with free paclitaxel for effects on cell proliferation of MCF-7 and B16F0 carcinoma cells. Asian Pac J Cancer Prev, 15, 2335-40. https://doi.org/10.7314/APJCP.2014.15.5.2335
  39. Yamate J, Tatsumi M, Nakatsuji S, et al (1993). Immunohistochemical observations of macrophages and perisinusoidal cells in carbon tetrachloride-induced rat liver injury. J Vet Med Sci, 55, 973-7. https://doi.org/10.1292/jvms.55.973
  40. Yin H-T, Zhang D-G, Wu X-L, Huang X-E, Chen G (2013). In vivo evaluation of curcumin-loaded nanoparticles in a A549 xenograft mice model. Asian Pac J Cancer Prev, 14, 409-12. https://doi.org/10.7314/APJCP.2013.14.1.409
  41. Zhang C, Qu G, Sun Y, et al (2008). Pharmacokinetics, biodistribution, efficacy and safety of N-octyl-O-sulfate chitosan micelles loaded with paclitaxel. Biomaterials, 29, 1233-41. https://doi.org/10.1016/j.biomaterials.2007.11.029
  42. Zhang L, Gu FX, Chan JM, et al (2008). Nanoparticles in medicine: therapeutic applications and developments. Clin Pharmacol Ther, 83, 761-9. https://doi.org/10.1038/sj.clpt.6100400

Cited by

  1. Passively Targeted Curcumin-Loaded PEGylated PLGA Nanocapsules for Colon Cancer Therapy In Vivo vol.11, pp.36, 2015, https://doi.org/10.1002/smll.201403799
  2. Thyroid-stimulating hormone (TSH)-armed polymer–lipid nanoparticles for the targeted delivery of cisplatin in thyroid cancers: therapeutic efficacy evaluation vol.5, pp.129, 2015, https://doi.org/10.1039/C5RA12588J
  3. Progress in nanotechnology-based drug carrier in designing of curcumin nanomedicines for cancer therapy: current state-of-the-art vol.24, pp.4, 2016, https://doi.org/10.3109/1061186X.2015.1055570
  4. Curcumin as a Modulator of P-Glycoprotein in Cancer: Challenges and Perspectives vol.9, pp.4, 2016, https://doi.org/10.3390/ph9040071
  5. Preclinical studies for the combination of paclitaxel and curcumin in cancer therapy vol.37, pp.6, 2017, https://doi.org/10.3892/or.2017.5593
  6. Decoration of Anti-CD38 on Nanoparticles Carrying a STAT3 Inhibitor Can Improve the Therapeutic Efficacy Against Myeloma vol.11, pp.2, 2019, https://doi.org/10.3390/cancers11020248
  7. Cyclohexanone curcumin analogs inhibit the progression of castration‐resistant prostate cancer in vitro and in vivo vol.110, pp.2, 2019, https://doi.org/10.1111/cas.13897