Synergism of cisplatin-oleanolic acid co-loaded calcium carbonate nanoparticles on hepatocellular carcinoma cells for enhanced apoptosis and reduced hepatotoxicity

References

• Choo SP, Tan WL, Goh BK, Tai WM, Zhu AX. Comparison of hepatocellular carcinoma in Eastern versus Western populations. Cancer. 2016;122(22):3430–3446. doi:10.1002/cncr.3023727622302
   PubMed Web of Science ®Google Scholar
• Abdel-Hamid NM, Abass SA, Mohamed AA, Hamid DM. Herbal management of hepatocellular carcinoma through cutting the pathways of the common risk factors. Biomed Pharmacother. 2018;107:1246–1258. doi:10.1016/j.biopha.2018.08.10430257339
   PubMedGoogle Scholar
• Bertuccio P, Turati F, Carioli G, et al. Global trends and predictions in hepatocellular carcinoma mortality. J Hepatol. 2017;67(2):302–309. doi:10.1016/j.jhep.2017.03.01128336466
   PubMed Web of Science ®Google Scholar
• Menahem B, Lubrano J, Duvoux C, et al. Liver transplantation versus liver resection for hepatocellular carcinoma in intention to treat: an attempt to perform an ideal meta‐analysis. Liver Transplant. 2017;23(6):836–844. doi:10.1002/lt.24758
   PubMed Web of Science ®Google Scholar
• Bruix J, Takayama T, Mazzaferro V, et al. Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2015;16(13):1344–1354. doi:10.1016/S1470-2045(15)00198-926361969
   PubMed Web of Science ®Google Scholar
• Roos WP, Kaina B. DNA damage-induced cell death: from specific DNA lesions to the DNA damage response and apoptosis. Cancer Lett. 2013;332(2):237–248. doi:10.1016/j.canlet.2012.01.00722261329
   PubMed Web of Science ®Google Scholar
• Galluzzi L, Senovilla L, Vitale I, et al. Molecular mechanisms of cisplatin resistance. Oncogene. 2012;31(15):1869. doi:10.1038/onc.2011.62721892204
   PubMed Web of Science ®Google Scholar
• Al-Malki AL, Sayed AAR. Thymoquinone attenuates cisplatin-induced hepatotoxicity via nuclear factor kappa-β. BMC Complement Altern Med. 2014;14(1):282. doi:10.1186/1472-6882-14-28225088145
   PubMedGoogle Scholar
• Yu Z, Sun W, Peng W, Yu R, Li G, Jiang T. Pharmacokinetics in vitro and in vivo of two novel prodrugs of oleanolic acid in rats and its hepatoprotective effects against liver injury induced by CCl4. Mol Pharm. 2016;13(5):1699–1710. doi:10.1021/acs.molpharmaceut.6b0012927018970
   PubMedGoogle Scholar
• Liese J, Abhari BA, Fulda S. Smac mimetic and oleanolic acid synergize to induce cell death in human hepatocellular carcinoma cells. Cancer Lett. 2015;365(1):47–56. doi:10.1016/j.canlet.2015.04.01825917078
   PubMed Web of Science ®Google Scholar
• Liu J, Zheng L, Wu N, et al. Oleanolic acid induces metabolic adaptation in cancer cells by activating the AMP-activated protein kinase pathway. J Agric Food Chem. 2014;62(24):5528–5537. doi:10.1021/jf500622p24856665
   PubMedGoogle Scholar
• Wu J, Yang C, Guo C, et al. SZC015, a synthetic oleanolic acid derivative, induces both apoptosis and autophagy in MCF-7 breast cancer cells. Chem Biol Interact. 2016;244:94–104. doi:10.1016/j.cbi.2015.11.01326612655
   PubMed Web of Science ®Google Scholar
• Nie H, Wang Y, Qin Y, Gong XG. Oleanolic acid induces autophagic death in human gastric cancer cells in vitro and in vivo. Cell Biol Int. 2016;40(7):770–778. doi:10.1002/cbin.1061227079177
   PubMedGoogle Scholar
• Wang X, Bai H, Zhang X, et al. Inhibitory effect of oleanolic acid on hepatocellular carcinoma via ERK–p53-mediated cell cycle arrest and mitochondrial-dependent apoptosis. Carcinogenesis. 2013;34(6):1323–1330. doi:10.1093/carcin/bgt05823404993
   PubMedGoogle Scholar
• Shyu M-H, Kao T-C, Yen G-C. Oleanolic acid and ursolic acid induce apoptosis in HuH7 human hepatocellular carcinoma cells through a mitochondrial-dependent pathway and downregulation of XIAP. J Agric Food Chem. 2010;58(10):6110–6118. doi:10.1021/jf100574j20415421
   PubMed Web of Science ®Google Scholar
• Sarfraz M, Afzal A, Raza SM, et al. Liposomal co-delivered oleanolic acid attenuates doxorubicin-induced multi-organ toxicity in hepatocellular carcinoma. Oncotarget. 2017;8(29):47136. doi:10.18632/oncotarget.1755928525367
   PubMedGoogle Scholar
• Khan IU, Khan RU, Asif H, et al. Co-delivery strategies to overcome multidrug resistance in ovarian cancer. Int J Pharm. 2017. doi:10.1016/j.ijpharm.2017.09.060
   Google Scholar
• Liao J, Zheng H, Fei Z, et al. Tumor-targeting and pH-responsive nanoparticles from hyaluronic acid for the enhanced delivery of doxorubicin. Int J Biol Macromol. 2018;113:737–747. doi:10.1016/j.ijbiomac.2018.03.00429505869
   PubMed Web of Science ®Google Scholar
• Li R, Liu B, Gao J. The application of nanoparticles in diagnosis and theranostics of gastric cancer. Cancer Lett. 2017;386:123–130. doi:10.1016/j.canlet.2016.10.03227845158
   PubMed Web of Science ®Google Scholar
• Dhar S, Daniel WL, Giljohann DA, Mirkin CA, Lippard SJ. Polyvalent oligonucleotide gold nanoparticle conjugates as delivery vehicles for platinum (IV) warheads. J Am Chem Soc. 2009;131(41):14652–14653. doi:10.1021/ja907128219778015
   PubMed Web of Science ®Google Scholar
• Wang Z, Deng X, Ding J, Zhou W, Zheng X, Tang G. Mechanisms of drug release in pH-sensitive micelles for tumour targeted drug delivery system: a review. Int J Pharm. 2018;535(1–2):253–260. doi:10.1016/j.ijpharm.2017.11.00329113804
   PubMed Web of Science ®Google Scholar
• Kim SK, Park H, Lee JM, Na K, Lee ES. pH‐responsive starch microparticles for a tumor‐targeting implant. Polym Adv Technol. 2018;29(5):1372–1376. doi:10.1002/pat.v29.5
   Web of Science ®Google Scholar
• Guragain S, Torad NL, Alghamdi YG, et al. Synthesis of nanoporous calcium carbonate spheres using double hydrophilic block copolymer poly (acrylic acid-bN-isopropylacrylamide). Mater Lett. 2018;230:143–147. doi:10.1016/j.matlet.2018.07.060
   Web of Science ®Google Scholar
• Dong Z, Feng L, Zhu W, et al. CaCO3 nanoparticles as an ultra-sensitive tumor-pH-responsive nanoplatform enabling real-time drug release monitoring and cancer combination therapy. Biomaterials. 2016;110:60–70. doi:10.1016/j.biomaterials.2016.09.02527710833
   PubMed Web of Science ®Google Scholar
• Gong M-Q, Wu J-L, Chen B, Zhuo R-X, Cheng S-X. Self-assembled polymer/inorganic hybrid nanovesicles for multiple drug delivery to overcome drug resistance in cancer chemotherapy. Langmuir. 2015;31(18):5115–5122. doi:10.1021/acs.langmuir.5b0054225927163
   PubMed Web of Science ®Google Scholar
• Zhao P, Li M, Wang Y, et al. Enhancing anti-tumor efficiency in hepatocellular carcinoma through the autophagy inhibition by miR-375/sorafenib in lipid-coated calcium carbonate nanoparticles. Acta Biomater. 2018;72:248–255. doi:10.1016/j.actbio.2018.03.02229555460
   PubMed Web of Science ®Google Scholar
• Guo S, Wang Y, Miao L, et al. Lipid-coated cisplatin nanoparticles induce neighboring effect and exhibit enhanced anticancer efficacy. ACS Nano. 2013;7(11):9896–9904. doi:10.1021/nn403606m24083505
   PubMed Web of Science ®Google Scholar
• Maleki Dizaj S, Barzegar-Jalali M, Zarrintan MH, Adibkia K, Lotfipour F. Calcium carbonate nanoparticles as cancer drug delivery system. Expert Opin Drug Deliv. 2015;12(10):1649–1660. doi:10.1517/17425247.2015.104953026005036
   PubMed Web of Science ®Google Scholar
• Kim SK, Foote MB, Huang L. Targeted delivery of EV peptide to tumor cell cytoplasm using lipid coated calcium carbonate nanoparticles. Cancer Lett. 2013;334(2):311–318. doi:10.1016/j.canlet.2012.07.01122796364
   PubMed Web of Science ®Google Scholar
• Cai S, Shi C-H, Zhang X, et al. Self-microemulsifying drug-delivery system for improved oral bioavailability of 20 (S)-25-methoxyl-dammarane-3β, 12β, 20-triol: preparation and evaluation. Int J Nanomedicine. 2014;9:913.24611008
   PubMed Web of Science ®Google Scholar
• Amna T, Hassan MS, Yang J, et al. Virgin olive oil blended polyurethane micro/nanofibers ornamented with copper oxide nanocrystals for biomedical applications. Int J Nanomedicine. 2014;9:891. doi:10.2147/IJN.S5411324611006
   PubMed Web of Science ®Google Scholar
• Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 2010;70(2)440–446. CAN-0009-1947.
   Web of Science ®Google Scholar
• Petrović S, Tačić A, Savić S, Nikolić V, Nikolić L, Savić S. Sulfanilamide in solution and liposome vesicles; in vitro release and UV-stability studies. Saudi Pharm J. 2017;25(8):1194–1200. doi:10.1016/j.jsps.2017.09.00330166909
   PubMed Web of Science ®Google Scholar
• Wu H, Zhong Q, Zhong R, et al. Preparation and antitumor evaluation of self-assembling oleanolic acid-loaded Pluronic P105/D-α-tocopheryl polyethylene glycol succinate mixed micelles for non-small-cell lung cancer treatment. Int J Nanomedicine. 2016;11:6337. doi:10.2147/IJN.S11983927932881
   PubMed Web of Science ®Google Scholar
• Cheng Y, Zhao P, Wu S, et al. Cisplatin and curcumin co-loaded nano-liposomes for the treatment of hepatocellular carcinoma. Int J Pharm. 2018;545(1–2):261–273. doi:10.1016/j.ijpharm.2018.05.00729730175
   PubMed Web of Science ®Google Scholar
• Awasthi BP, Kathuria M, Pant G, Kumari N, Mitra K. Plumbagin, a plant-derived naphthoquinone metabolite induces mitochondria mediated apoptosis-like cell death in Leishmania donovani: an ultrastructural and physiological study. Apoptosis. 2016;21(8):941–953. doi:10.1007/s10495-016-1259-927315817
   PubMed Web of Science ®Google Scholar
• ud Din F, Mustapha O, Kim DW, et al. Novel dual-reverse thermosensitive solid lipid nanoparticle-loaded hydrogel for rectal administration of flurbiprofen with improved bioavailability and reduced initial burst effect. Eur J Pharm Biopharm. 2015;94:64–72.25979136
   PubMed Web of Science ®Google Scholar
• Chen S, Li F, Zhuo R-X, Cheng S-X. Efficient non-viral gene delivery mediated by nanostructured calcium carbonate in solution-based transfection and solid-phase transfection. Mol Biosyst. 2011;7(10):2841–2847. doi:10.1039/c1mb05147d21773634
   PubMedGoogle Scholar
• Bnyan R, Khan I, Ehtezazi T, et al. Surfactant effects on lipid-based vesicles properties. J Pharm Sci. 2018;107(5):1237–1246. doi:10.1016/j.xphs.2018.01.00529336980
   PubMed Web of Science ®Google Scholar
• Khiati S, Luvino D, Oumzil K, Chauffert B, Camplo M, Barthélémy P. Nucleoside–lipid-based nanoparticles for cisplatin delivery. ACS Nano. 2011;5(11):8649–8655. doi:10.1021/nn202291k21961944
   PubMedGoogle Scholar
• Zhang J, Chen Y, Li X, Liang X, Luo X. The influence of different long-circulating materials on the pharmacokinetics of liposomal vincristine sulfate. Int J Nanomedicine. 2016;11:4187. doi:10.2147/IJN.S10954727616886
   PubMed Web of Science ®Google Scholar
• Rosen H, Abribat T. The rise and rise of drug delivery. Nat Rev Drug Discov. 2005;4(5):381. doi:10.1038/nrd187615864267
   PubMedGoogle Scholar
• Yan W, Ma X, Zhao X. Baicalein induces apoptosis and autophagy of breast cancer cells via inhibiting Pi3K/aKT pathway in vivo and vitro. Drug Des Devel Ther. 2018;12:3961–3972. doi:10.2147/DDDT.S181939
   PubMed Web of Science ®Google Scholar
• Yang N, Jiang Y, Zhang H, et al. Active targeting docetaxel-PLA nanoparticles eradicate circulating lung cancer stem-like cells and inhibit liver metastasis. Mol Pharm. 2014;12(1):232–239. doi:10.1021/mp500568z25418453
   PubMedGoogle Scholar
• Omar HA, Mohamed WR, Arafa E-SA, et al. Hesperidin alleviates cisplatin-induced hepatotoxicity in rats without inhibiting its antitumor activity. Pharmacol Rep. 2016;68(2):349–356. doi:10.1016/j.pharep.2015.09.00726922538
   PubMedGoogle Scholar
• Bentli R, Parlakpinar H, Polat A, Samdanci E, Sarihan ME, Sagir M. Molsidomine prevents cisplatin-induced hepatotoxicity. Arch Med Res. 2013;44(7):521–528. doi:10.1016/j.arcmed.2013.09.01324120390
   PubMed Web of Science ®Google Scholar
• Lu Y, Cederbaum AI. Cisplatin-induced hepatotoxicity is enhanced by elevated expression of cytochrome P450 2E1. Toxicol Sci. 2005;89(2):515–523. doi:10.1093/toxsci/kfj03116251482
   PubMedGoogle Scholar
• Wang X, Ye X-L, Liu R, et al. Antioxidant activities of oleanolic acid in vitro: possible role of Nrf2 and MAP kinases. Chem Biol Interact. 2010;184(3):328–337. doi:10.1016/j.cbi.2010.01.03420100471
   PubMedGoogle Scholar
• Chai J, Du X, Chen S, et al. Oral administration of oleanolic acid, isolated from Swertia mussotii Franch, attenuates liver injury, inflammation, and cholestasis in bile duct-ligated rats. Int J Clin Exp Med. 2015;8(2):1691.25932098
   PubMed Web of Science ®Google Scholar
• Liu C, Huang X, Li Y, et al. The anti-portal hypertension effect of oleanolic acid in CCl4-induced cirrhosis rats. J Chin Med Mater. 2012;35(6):930–935.
   Google Scholar
• Kim K-A, Lee J-S, Park H-J, et al. Inhibition of cytochrome P450 activities by oleanolic acid and ursolic acid in human liver microsomes. Life Sci. 2004;74(22):2769–2779. doi:10.1016/j.lfs.2003.10.02015043991
   PubMed Web of Science ®Google Scholar
• Liu J, Wang X, Liu R, et al. Oleanolic acid co-administration alleviates ethanol-induced hepatic injury via Nrf-2 and ethanol-metabolizing modulating in rats. Chem Biol Interact. 2014;221:88–98. doi:10.1016/j.cbi.2014.07.01725111957
   PubMedGoogle Scholar
• Shackelford DB, Shaw RJ. The LKB1–AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer. 2009;9(8):563. doi:10.1038/nrc267619629071
   PubMed Web of Science ®Google Scholar
• Hahne JC. Platinum-resistance and AKT over-expression in ovarian cancer. Int J Gynecol Clin Pract. 2015; 2:14–21.
   Google Scholar
• Sikka A, Kaur M, Agarwal C, Deep G, Agarwal R. Metformin suppresses growth of human head and neck squamous cell carcinoma via global inhibition of protein translation. Cell Cycle. 2012;11(7):1374–1382. doi:10.4161/cc.1979822421144
   PubMed Web of Science ®Google Scholar
• Kim G-J, Jo H-J, Lee K-J, Choi JW, An JH. Oleanolic acid induces p53-dependent apoptosis via the ERK/JNK/AKT pathway in cancer cell lines in prostatic cancer xenografts in mice. Oncotarget. 2018;9(41):26370. doi:10.18632/oncotarget.2531629899865
   PubMedGoogle Scholar
• Herůdková J, Paruch K, Khirsariya P, et al. Chk1 inhibitor SCH900776 effectively potentiates the cytotoxic effects of platinum-based chemotherapeutic drugs in human colon cancer cells. Neoplasia. 2017;19(10):830–841. doi:10.1016/j.neo.2017.08.00228888100
   PubMedGoogle Scholar
• Safta TB, Ziani L, Favre L, et al. Granzyme B–activated p53 interacts with Bcl-2 to promote cytotoxic lymphocyte–mediated apoptosis. J Immunol. 2015;194(1):418–428. doi:10.4049/jimmunol.140197825404359
   PubMedGoogle Scholar
• Fox MM, Phoenix KN, Kopsiaftis SG, Claffey KP. AMP-activated protein kinase α 2 isoform suppression in primary breast cancer alters AMPK growth control and apoptotic signaling. Genes Cancer. 2013;4(1–2):3–14. doi:10.1177/194760191348634623946867
   PubMedGoogle Scholar
• Godwin P, Baird A-M, Heavey S, Barr M, O’Byrne K, Gately KA. Targeting nuclear factor-kappa B to overcome resistance to chemotherapy. Front Oncol. 2013;3:120. doi:10.3389/fonc.2013.0012023720710
   PubMedGoogle Scholar
• Yu L, Li L, Medeiros LJ, Young KH. NF-κB signaling pathway and its potential as a target for therapy in lymphoid neoplasms. Blood Rev. 2017;31(2):77–92. doi:10.1016/j.blre.2016.10.001
   PubMed Web of Science ®Google Scholar
• Song W, Tang Z, Shen N, et al. Combining disulfiram and poly (l-glutamic acid)-cisplatin conjugates for combating cisplatin resistance. J Control Release. 2016;231:94–102. doi:10.1016/j.jconrel.2016.02.03926928530
   PubMedGoogle Scholar