Chemotherapeutic effects of Apigenin in breast cancer: Preclinical evidence and molecular mechanisms; enhanced bioavailability by nanoparticles

Zheng, 2021, The breast Cancer stem cells traits and drug resistance, Front. Pharmacol., 2120 Mitra S., Dash R. Natural products for the management and prevention of breast cancer. Evidence-based complementary and alternative medicine. 2018;2018. Mitra S., Dash R. Natural products for the management and prevention of breast cancer. Evidence-based complementary and alternative medicine. 2018;2018:8324696. Group, 2005, Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials, The Lancet, 366, 2087, 10.1016/S0140-6736(05)67887-7 Zhou, 2016, Dietary natural products for prevention and treatment of liver cancer, Nutrients, 8, 156, 10.3390/nu8030156 Harbeck, 2019, Breast cancer, Nat. Rev. Dis. Primers, 5, 1, 10.1038/s41572-019-0111-2 Abad, 2020, DNA damage response and resistance of cancer stem cells, Cancer Lett., 474, 106, 10.1016/j.canlet.2020.01.008 Eiro, 2019, Breast cancer tumor stroma: cellular components, phenotypic heterogeneity, intercellular communication, prognostic implications and therapeutic opportunities, Cancers (Basel), 11, 664, 10.3390/cancers11050664 Zahmatkeshan, 2015, Analytical characterization of label-free immunosensor subsystems based on multi-walled carbon nanotube array-modified gold interface, Comb. Chem. High Throughput Screen., 18, 83, 10.2174/1386207318666141212165513 Zahmatkeshan, 2016, Improved drug delivery and therapeutic efficacy of PEgylated liposomal doxorubicin by targeting anti-HER2 peptide in murine breast tumor model, Eur. J. Pharmaceutical Sci., 86, 125, 10.1016/j.ejps.2016.03.009 Mirzaei-Parsa, 2020, Preparation, characterization, and evaluation of the anticancer activity of artemether-loaded nano-niosomes against breast cancer, Breast Cancer, 27, 243, 10.1007/s12282-019-01014-w Nabavi, 2018, Apigenin as neuroprotective agent: of mice and men, Pharmacol. Res., 128, 359, 10.1016/j.phrs.2017.10.008 Martinez-Perez, 2014, Novel flavonoids as anti-cancer agents: mechanisms of action and promise for their potential application in breast cancer, Biochem. Soc. Trans., 42, 1017, 10.1042/BST20140073 Romagnolo, 2012, Flavonoids and cancer prevention: a review of the evidence, J. Nutr. Gerontol. Geriatr., 31, 206, 10.1080/21551197.2012.702534 Pan, 2012, Genistein inhibits MDA-MB-231 triple-negative breast cancer cell growth by inhibiting NF-κB activity via the Notch-1 pathway, Int. J. Mol. Med., 30, 337, 10.3892/ijmm.2012.990 Knekt, 1997, Dietary flavonoids and the risk of lung cancer and other malignant neoplasms, Am. J. Epidemiol., 146, 223, 10.1093/oxfordjournals.aje.a009257 Hoensch, 2008, Prospective cohort comparison of flavonoid treatment in patients with resected colorectal cancer to prevent recurrence, World J. Gastroenterol., 14, 2187, 10.3748/wjg.14.2187 Rossi, 2008, Flavonoids and ovarian cancer risk: a case-control study in Italy, Int. J. Cancer, 123, 895, 10.1002/ijc.23549 Bosetti, 2005, Flavonoids and breast cancer risk in Italy, Cancer Epidemiol. Prevention Biomarkers, 14, 805, 10.1158/1055-9965.EPI-04-0838 Shukla, 2010, Apigenin: a promising molecule for cancer prevention, Pharm. Res., 27, 962, 10.1007/s11095-010-0089-7 Yan, 2017, Apigenin in cancer therapy: anti-cancer effects and mechanisms of action, Cell Biosci., 7, 1, 10.1186/s13578-017-0179-x Li, 2018, Apigenin suppresses the stem cell-like properties of triple-negative breast cancer cells by inhibiting YAP/TAZ activity, Cell Death Discov., 4, 105, 10.1038/s41420-018-0124-8 Bauer, 2017, Apigenin inhibits TNFα/IL-1α-induced CCL2 release through IKBK-epsilon signaling in MDA-MB-231 human breast cancer cells, PLoS ONE, 12, 10.1371/journal.pone.0175558 Sudhakaran, 2020, Apigenin by targeting hnRNPA2 sensitizes triple-negative breast cancer spheroids to doxorubicin-induced apoptosis and regulates expression of ABCC4 and ABCG2 drug efflux transporters, Biochem. Pharmacol., 182, 10.1016/j.bcp.2020.114259 Korga-Plewko, 2020, Apigenin and hesperidin downregulate DNA repair genes in MCF-7 breast cancer cells and augment doxorubicin toxicity, Molecules, 25, 4421, 10.3390/molecules25194421 Pham, 2021, Apigenin, a partial antagonist of the estrogen receptor (ER), inhibits ER-positive breast cancer cell proliferation through Akt/FOXM1 signaling, Int .J. Mol. Sci., 22, 470, 10.3390/ijms22010470 Shendge, 2021, A natural flavonoid, apigenin isolated from Clerodendrum viscosum leaves, induces G2/M phase cell cycle arrest and apoptosis in MCF-7 cells through the regulation of p53 and caspase-cascade pathway, Clin. Translational Oncol., 23, 718, 10.1007/s12094-020-02461-0 Scherbakov, 2015, Apigenin inhibits growth of breast cancer cells: the role of ERα and HER2/neu, Acta Naturae (англоязычная версия), 7, 133, 10.32607/20758251-2015-7-3-133-139 Ross, 2000, Effect of hormone replacement therapy on breast cancer risk: estrogen versus estrogen plus progestin, J. Natl. Cancer Inst., 92, 328, 10.1093/jnci/92.4.328 Chlebowski, 2010, Estrogen plus progestin and breast cancer incidence and mortality in postmenopausal women, JAMA, 304, 1684, 10.1001/jama.2010.1500 Brusselmans, 2005, Induction of cancer cell apoptosis by flavonoids is associated with their ability to inhibit fatty acid synthase activity, J. Biol. Chem., 280, 5636, 10.1074/jbc.M408177200 Menendez, 2008, Analyzing effects of extra-virgin olive oil polyphenols on breast cancer-associated fatty acid synthase protein expression using reverse-phase protein microarrays, Int. J. Mol. Med., 22, 433 Lephart, 2015, Modulation of aromatase by phytoestrogens, Enzyme Res., 10.1155/2015/594656 Chen, 2004, Association of hormone replacement therapy to estrogen and progesterone receptor status in invasive breast carcinoma, Cancer, 101, 1490, 10.1002/cncr.20499 Hyder, 1998, Progestin regulation of vascular endothelial growth factor in human breast cancer cells, Cancer Res., 58, 392 Hyder, 2001, Pharmacological and endogenous progestins induce vascular endothelial growth factor expression in human breast cancer cells, International J. Cancer, 92, 469, 10.1002/ijc.1236 Mafuvadze, 2010, Apigenin blocks induction of vascular endothelial growth factor mRNA and protein in progestin-treated human breast cancer cells, Menopause, 17, 1055, 10.1097/gme.0b013e3181dd052f Zanconato, 2016, YAP/TAZ at the roots of cancer, Cancer Cell, 29, 783, 10.1016/j.ccell.2016.05.005 Zhao, 2010, The Hippo–YAP pathway in organ size control and tumorigenesis: an updated version, Genes Dev., 24, 862, 10.1101/gad.1909210 Lei, 2008, TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway, Mol. Cell. Biol., 28, 2426, 10.1128/MCB.01874-07 Harvey, 2013, The Hippo pathway and human cancer, Nat. Rev. Cancer, 13, 246, 10.1038/nrc3458 Marti, 2015, YAP promotes proliferation, chemoresistance, and angiogenesis in human cholangiocarcinoma through TEAD transcription factors, Hepatology, 62, 1497, 10.1002/hep.27992 Coombs, 2016, Apigenin inhibits the inducible expression of programmed death ligand 1 by human and mouse mammary carcinoma cells, Cancer Lett., 380, 424, 10.1016/j.canlet.2016.06.023 Seo, 2015, Induction of caspase-dependent extrinsic apoptosis by apigenin through inhibition of signal transducer and activator of transcription 3 (STAT3) signalling in HER2-overexpressing BT-474 breast cancer cells, Biosci. Rep., 35, 10.1042/BSR20150165 Mafuvadze, 2012, Apigenin induces apoptosis and blocks growth of medroxyprogesterone acetate-dependent BT-474 xenograft tumors, Hormones and Cancer, 3, 160, 10.1007/s12672-012-0114-x Seo, 2015, Apigenin induces caspase-dependent apoptosis by inhibiting signal transducer and activator of transcription 3 signaling in HER2-overexpressing SKBR3 breast cancer cells, Mol. Med. Rep., 12, 2977, 10.3892/mmr.2015.3698 Bai, 2014, Apigenin induced MCF-7 cell apoptosis-associated reactive oxygen species, Scanning: J. Scanning Microscopies, 36, 622, 10.1002/sca.21170 Harrison, 2014, Exposure of breast cancer cells to a subcytotoxic dose of apigenin causes growth inhibition, oxidative stress, and hypophosphorylation of Akt, Exp. Mol. Pathol., 97, 211, 10.1016/j.yexmp.2014.07.006 Fang, 2007, Apigenin inhibits tumor angiogenesis through decreasing HIF-1α and VEGF expression, Carcinogenesis, 28, 858, 10.1093/carcin/bgl205 Lee, 2019, Antitumor and anti-invasive effect of apigenin on human breast carcinoma through suppression of IL-6 expression, Int. J. Mol. Sci., 20, 3143, 10.3390/ijms20133143 Wang, 2013, Apigenin suppresses migration and invasion of transformed cells through down-regulation of CXC chemokine receptor 4 expression, Toxicol. Appl. Pharmacol., 272, 108, 10.1016/j.taap.2013.05.028 Long, 2008, Apigenin inhibits antiestrogen-resistant breast cancer cell growth through estrogen receptor-α-dependent and estrogen receptor-α-independent mechanisms, Mol. Cancer Ther., 7, 2096, 10.1158/1535-7163.MCT-07-2350 Zhang, 2004, Flavonoids are inhibitors of breast cancer resistance protein (ABCG2)-mediated transport, Mol. Pharmacol., 65, 1208, 10.1124/mol.65.5.1208 Seo, 2017, Apigenin overcomes drug resistance by blocking the signal transducer and activator of transcription 3 signaling in breast cancer cells, Oncol. Rep., 38, 715, 10.3892/or.2017.5752 Li, 2018, Apigenin suppresses the stem cell-like properties of triple-negative breast cancer cells by inhibiting YAP/TAZ activity, Cell Death Discov., 4, 1, 10.1038/s41420-018-0124-8 Bagwe-Parab, 2019, Absorption, metabolism, and disposition of flavonoids and their role in the prevention of distinctive cancer types, Current Aspects of Flavonoids: Their Role in Cancer Treatment, 125, 10.1007/978-981-13-5874-6_6 Kanha, 2019, Copigmentation of cyanidin 3-O-glucoside with phenolics: thermodynamic data and thermal stability, Food Biosci., 30, 10.1016/j.fbio.2019.100419 Pilon, 2019, Mass spectral similarity networking and gas-phase fragmentation reactions in the structural analysis of flavonoid glycoconjugates, Anal. Chem., 91, 10413, 10.1021/acs.analchem.8b05479 Madala, 2016, Distribution patterns of flavonoids from three Momordica species by ultra-high performance liquid chromatography quadrupole time of flight mass spectrometry: a metabolomic profiling approach, Revista Brasileira de Farmacognosia, 26, 507, 10.1016/j.bjp.2016.03.009 Muñoz, 2011, Polyphenol composition in the ripe fruits of Fragaria species and transcriptional analyses of key genes in the pathway, J. Agric. Food Chem., 59, 12598, 10.1021/jf203965j Wong, 2009, Quinacrine and a novel apigenin dimer can synergistically increase the pentamidine susceptibility of the protozoan parasite Leishmania, J. Antimicrobial Chemotherapy, 63, 1179, 10.1093/jac/dkp130 Mandery, 2010, Influence of the flavonoids apigenin, kaempferol, and quercetin on the function of organic anion transporting polypeptides 1A2 and 2B1, Biochem. Pharmacol., 80, 1746, 10.1016/j.bcp.2010.08.008 Handayani, 2013, Induction of Apoptosis on MCF-7 cells by Selaginella Fractions, J. Appl. Pharmaceutical Sci., 3, 31 Seo, 2011, Apoptotic effects of genistein, biochanin-A and apigenin on LNCaP and PC-3 cells by p21 through transcriptional inhibition of polo-like kinase-1, J. Korean Med. Sci., 26, 1489, 10.3346/jkms.2011.26.11.1489 Luo, 2015, Engineered biosynthesis of natural products in heterologous hosts, Chem. Soc. Rev., 44, 5265, 10.1039/C5CS00025D Gurung, 2013, Enzymatic synthesis of apigenin glucosides by glucosyltransferase (YjiC) from Bacillus licheniformis DSM 13, Mol. Cells, 36, 355, 10.1007/s10059-013-0164-0 Seijas, 2005, Solvent-free synthesis of functionalized flavones under microwave irradiation, J. Org. Chem., 70, 2855, 10.1021/jo048685z Verma, 2012, Chemistry of biologically important flavones, Tetrahedron, 68, 8523, 10.1016/j.tet.2012.06.097 Chauthe, 2012, Quantitative NMR: an applicable method for quantitative analysis of medicinal plant extracts and herbal products, Phytochem. Anal., 23, 689, 10.1002/pca.2375 S-m, 2014, Enhanced bioavailability of apigenin via preparation of a carbon nanopowder solid dispersion, Int. J. Nanomed., 9, 2327 Hanske, 2009, The bioavailability of apigenin-7-glucoside is influenced by human intestinal microbiota in rats, J. Nutr., 139, 1095, 10.3945/jn.108.102814 Falé, 2013, Effect of luteolin and apigenin on rosmarinic acid bioavailability in Caco-2 cell monolayers, Food Funct., 4, 426, 10.1039/C2FO30318C Telange, 2017, Formulation and characterization of an apigenin-phospholipid phytosome (APLC) for improved solubility, in vivo bioavailability, and antioxidant potential, Eur. J. Pharmaceutical Sci., 108, 36, 10.1016/j.ejps.2016.12.009 Rabiee, 2019 Kim, 2016, Enhancing oral bioavailability using preparations of apigenin-loaded W/O/W emulsions: in vitro and in vivo evaluations, Food Chem., 206, 85, 10.1016/j.foodchem.2016.03.052 Huang, 2016, Preparation of inclusion complex of apigenin-hydroxypropyl-β-cyclodextrin by using supercritical antisolvent process for dissolution and bioavailability enhancement, Int. J. Pharm., 511, 921, 10.1016/j.ijpharm.2016.08.007 Jain, 2013, Co-encapsulation of tamoxifen and quercetin in polymeric nanoparticles: implications on oral bioavailability, antitumor efficacy, and drug-induced toxicity, Mol. Pharm., 10, 3459, 10.1021/mp400311j Zhang, 2017, Improved solubility and oral bioavailability of apigenin via Soluplus/Pluronic F127 binary mixed micelles system, Drug Dev. Ind. Pharm., 43, 1276, 10.1080/03639045.2017.1313857 Khan, 2019, Nanoparticles: properties, applications and toxicities, Arabian J. Chem., 12, 908, 10.1016/j.arabjc.2017.05.011 Tavakol, 2021, The role of nanotechnology in current COVID-19 outbreak, Heliyon, e06841, 10.1016/j.heliyon.2021.e06841 De Jong, 2008, Drug delivery and nanoparticles:applications and hazards, Int. J. Nanomed., 3, 133, 10.2147/IJN.S596 Aiello, 2019, Dietary flavonoids: nano delivery and nanoparticles for cancer therapy, Semin Cancer Biol., 24 Lambricht, 2017, 185 Singh, 2019, Targeted therapy in chronic diseases using nanomaterial-based drug delivery vehicles, Signal Transduction and Targeted Therapy, 4, 33, 10.1038/s41392-019-0068-3 Khan, 2019, Flavonoids nanoparticles in cancer: treatment, prevention and clinical prospects, Semin. Cancer Biol., 30, 30182 Huang, 2019, Enhanced solubility and bioavailability of apigenin via preparation of solid dispersions of mesoporous silica nanoparticles, Iran J. Pharm. Res., 18, 168 Banerjee, 2017, Enhanced chemotherapeutic efficacy of apigenin liposomes in colorectal cancer based on flavone-membrane interactions, J. Colloid Interface Sci., 491, 98, 10.1016/j.jcis.2016.12.025 Sen, 2021, Apigenin-loaded PLGA-DMSA nanoparticles: a novel strategy to treat melanoma lung metastasis, Mol. Pharm., 18, 1920, 10.1021/acs.molpharmaceut.0c00977 Guo, 2019, 6-Bromoindirubin-3′-Oxime (6BIO) suppresses the mTOR pathway, promotes autophagy, and exerts anti-aging effects in rodent liver, Front. Pharmacol., 10 Leuner, 2000, Improving drug solubility for oral delivery using solid dispersions, Eur. J. Pharmaceutics and Biopharmaceutics: Official J. Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik eV, 50, 47, 10.1016/S0939-6411(00)00076-X Xie, 2010, Nanoparticle-based theranostic agents, Adv. Drug Deliv. Rev., 62, 1064, 10.1016/j.addr.2010.07.009 Karim, 2017, Development and evaluation of injectable nanosized drug delivery systems for apigenin, Int. J. Pharm., 532, 757, 10.1016/j.ijpharm.2017.04.064 Fernandes, 2021, Critical review of lipid-based nanoparticles as carriers of neuroprotective drugs and extracts, Nanomaterials, 11, 563, 10.3390/nano11030563 Zhang, 2013, Preparation of apigenin nanocrystals using supercritical antisolvent process for dissolution and bioavailability enhancement, Eur. J. Pharm. Sci., 48, 740, 10.1016/j.ejps.2012.12.026 Altamimi, 2018, Utilizing spray drying technique to improve oral bioavailability of apigenin, Adv. Powder Technol., 29, 1676, 10.1016/j.apt.2018.04.002 Telange, 2016, Formulation and characterization of an apigenin-phospholipid phytosome (APLC) for improved solubility, in vivo bioavailability, and antioxidant potential, Eur. J. Pharmaceutical Sci., 108 Wu, 2017, Preparation, characterization and antitumor activity evaluation of apigenin nanoparticles by the liquid antisolvent precipitation technique, Drug Deliv., 24, 1713, 10.1080/10717544.2017.1399302 Ding, 2014, Enhanced bioavailability of apigenin via preparation of a carbon nanopowder solid dispersion, Int. J. Nanomed., 9, 2327, 10.2147/IJN.S60938 Dutta, 2018, Aptamer-conjugated apigenin nanoparticles to target colorectal carcinoma: a promising safe alternative of colorectal cancer chemotherapy, ACS Appl. Bio. Mater., 1, 1538, 10.1021/acsabm.8b00441 Kumar, 2013, Pharmaceutical solid dispersion technology: a strategy to improve dissolution of poorly water-soluble drugs, Recent Pat. Drug Deliv. Formul., 7, 111, 10.2174/18722113113079990009 Bharti, 2015, Mesoporous silica nanoparticles in target drug delivery system: a review, Int. J. Pharm. Investig., 5, 124, 10.4103/2230-973X.160844 Huang, 2019, Enhanced solubility and bioavailability of apigenin via preparation of solid dispersions of mesoporous silica nanoparticles, Iranian J. Pharmaceutical Res. IJPR, 18, 168 Diniz, 2015, Pluronic F-127 hydrogel as a promising scaffold for encapsulation of dental-derived mesenchymal stem cells, J. Mater. Sci. Mater. Med., 26, 153, 10.1007/s10856-015-5493-4 Taha, 2014, Role of Pluronic F127 micelles in enhancing ocular delivery of ciprofloxacin, J. Mol. Liq., 199, 251, 10.1016/j.molliq.2014.09.021 Chenthamara, 2019, Therapeutic efficacy of nanoparticles and routes of administration, Biomater. Res., 23, 20, 10.1186/s40824-019-0166-x Sharma, 2016, PLGA-based nanoparticles: a new paradigm in biomedical applications, TrAC Trends in Analytical Chem., 80, 30, 10.1016/j.trac.2015.06.014 Bhattacharya, 2018, Apigenin loaded nanoparticle delayed development of hepatocellular carcinoma in rats, Nanomedicine, 14, 1905, 10.1016/j.nano.2018.05.011 Pal, 2017, Synergistic effect of graphene oxide coated nanotised apigenin with paclitaxel (GO-NA/PTX): a ROS dependent mitochondrial mediated apoptosis in ovarian cancer, Anticancer Agents Med. Chem., 17, 1721 Das, 2013, Strategic formulation of apigenin-loaded PLGA nanoparticles for intracellular trafficking, DNA targeting and improved therapeutic effects in skin melanoma in vitro, Toxicol. Lett., 223, 124, 10.1016/j.toxlet.2013.09.012 He, 2021, Apigenin nanoparticle attenuates renal ischemia/reperfusion inflammatory injury by regulation of miR-140-5p/CXCL12/NF-κB signaling pathway, J. Biomed. Nanotechnol., 17, 64, 10.1166/jbn.2021.3010 Drescher, 2020, The phospholipid research center: current research in phospholipids and their use in drug delivery, Pharmaceutics, 12, 1235, 10.3390/pharmaceutics12121235 Zhang, 2012, Vitamin E TPGS as a molecular biomaterial for drug delivery, Biomaterials, 33, 4889, 10.1016/j.biomaterials.2012.03.046 Jin, 2017, Synergistic apoptotic effects of apigenin TPGS liposomes and tyroservatide: implications for effective treatment of lung cancer, Int. J. Nanomed., 12, 5109, 10.2147/IJN.S140096 Li, 2020, Apigenin-loaded solid lipid nanoparticle attenuates diabetic nephropathy induced by Streptozotocin Nicotinamide through Nrf2/HO-1/NF-kB signalling pathway, Int. J. Nanomed., 15, 9115, 10.2147/IJN.S256494 Thomas, 2012, Characterising lipid lipolysis and its implication in lipid-based formulation development, AAPS J., 14, 860, 10.1208/s12248-012-9398-6 Xia, 2017, Size-dependent translocation of nanoemulsions via oral delivery, ACS Appl. Mater. Interfaces, 9, 21660, 10.1021/acsami.7b04916 Hu, 2015, Environment-responsive aza-BODIPY dyes quenching in water as potential probes to visualize the in vivo fate of lipid-based nanocarriers, Nanomed. Nanotechnol. Biol. Med., 11, 1939, 10.1016/j.nano.2015.06.013 Wang, 2018, Triple negative breast cancer in Asia: an insider's view, Cancer Treat. Rev., 62, 29, 10.1016/j.ctrv.2017.10.014 Nabavi, 2015, Apigenin and breast cancers: from chemistry to medicine, Anticancer Agents Med. Chem., 15, 728, 10.2174/1871520615666150304120643 Imran, 2020, Apigenin as an anticancer agent, Phytotherapy Res., 34, 1812, 10.1002/ptr.6647 Atanasov, 2021, Natural products in drug discovery: advances and opportunities, Nat. Rev. Drug Discovery, 20, 200, 10.1038/s41573-020-00114-z