Phytochemical-loaded mesoporous silica nanoparticles for nose-to-brain olfactory drug delivery

International Journal of Pharmaceutics

Volumn 513, Issue 1-2, 2016, Pages 280-293

  Lungare, Shital ^a   Hallam, Keith ^b   Badhan, Raj K S ^a  

^a ASTON UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Flavonoid; Mesoporous silica nanoparticle; Nose to brain; Olfactory; Phytochemical

Indexed keywords

CHRYSIN; CURCUMIN; CYTOTOXIC AGENT; MESOPOROUS SILICA NANOPARTICLE; NANOCARRIER; FLAVONOID; NANOPARTICLE; SILICON DIOXIDE;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; CAPILLARY ENDOTHELIAL CELL; CELL PROLIFERATION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DIFFERENTIAL SCANNING CALORIMETRY; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG RELEASE; ESTHESIONEUROBLASTOMA; HYDRODYNAMICS; HYDROGEN BOND; IC50; INCUBATION TIME; INFRARED SPECTROSCOPY; NEUROBLASTOMA CELL LINE; NONHUMAN; NOSE TO BRAIN DRUG DELIVERY SYSTEM; OLFACTORY SYSTEM; PARTICLE SIZE; PH; PHYTOCHEMISTRY; POROSITY; PRIORITY JOURNAL; THERMOSTABILITY; ZETA POTENTIAL; ANIMAL; BRAIN; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; INTRANASAL DRUG ADMINISTRATION; METABOLISM; PIG; TUMOR CELL LINE;

ADMINISTRATION, INTRANASAL; ANIMALS; BRAIN; CELL LINE, TUMOR; CELL SURVIVAL; CURCUMIN; DRUG DELIVERY SYSTEMS; DRUG LIBERATION; FLAVONOIDS; NANOPARTICLES; POROSITY; SILICON DIOXIDE; SWINE;

EID: 84987922658     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2016.09.042     Document Type: Article

References (121)

1. Abbott, N.J., Romero, I.A., Transporting therapeutics across the blood-brain barrier. Mol. Med. Today 2:3 (1996), 106–113.
2. Allen, J.D., van Loevezijn, A., Lakhai, J.M., van der Valk, M., van Tellingen, O., Reid, G., Schellens, J.H.M., Koomen, G.J., Schinkel, A.H., Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C 1 this work was supported in part by grant NKI 97–1433 from the dutch cancer society (to AHS). synthesis investigations by A. v. L. and GJ. K. were supported by the netherlands research council for chemical sciences (NWO/CW) and the Netherlands technology foundation (STW). 1. Mol. Cancer Ther. 1:6 (2002), 417–425.
3. Allen, J.D., van Loevezijn, A., Lakhai, J.M., van der Valk, M., van Tellingen, O., Reid, G., Schellens, J.H., Koomen, G.J., Schinkel, A.H., Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol. Cancer Ther. 1:6 (2002), 417–425.
4. Anitha, A., Deepagan, V.G., Divya Rani, V.V., Menon, D., Nair, S.V., Jayakumar, R., Preparation, characterization, in vitro drug release and biological studies of curcumin loaded dextran sulphate-chitosan nanoparticles. Carbohydr. Polym. 84:3 (2011), 1158–1164.
5. Ashida, H., Fukuda, I., Yamashita, T., Kanazawa, K., Flavones and flavonols at dietary levels inhibit a transformation of aryl hydrocarbon receptor induced by dioxin. FEBS Lett. 476:3 (2000), 213–217.
6. Barrett, E.G., Johnston, C., Oberdörster, G., Finkelstein, J.N., Silica binds serum proteins resulting in a shift of the dose-response for silica-induced chemokine expression in an alveolar type II cell line. Toxicol. Appl. Pharmacol. 161:2 (1999), 111–122.
7. Bennett, S., Grant, M.M., Aldred, S., Oxidative stress in vascular dementia and Alzheimer's disease: a common pathology. J. Alzheimer's Dis. 17:2 (2009), 245–257.
8. Blumberg, J.B., Ding, E.L., Dixon, R., Pasinetti, G.M., Villarreal, F., The science of cocoa flavanols: bioavailability, emerging evidence, and proposed mechanisms. Adv. Nutr. 5:5 (2014), 547–549.
9. Bottini, M., D'Annibale, F., Magrini, A., Cerignoli, F., Arimura, Y., Dawson, M.I., Bergamaschi, E., Rosato, N., Bergamaschi, A., Mustelin, T., Quantum dot-doped silica nanoparticles as probes for targeting of T-lymphocytes. Int. J. Nanomed. 2:2 (2007), 227–233.
10. Boussif, O., Lezoualch, F., Zanta, M.A., Mergny, M.D., Scherman, D., Demeneix, B., Behr, J.P., A versatile vector for gene and oligonucleotide transfer into cells in culture and in-vivo − polyethylenimine. Proc. Natl. Acad. Sci. U. S. A. 92:16 (1995), 7297–7301.
11. Breedveld, P., Beijnen, J.H., Schellens, J.H.M., Use of P-glycoprotein and BCRP inhibitors to improve oral bioavailability and CNS penetration of anticancer drugs. Trends Pharmacol. Sci. 27:1 (2006), 17–24.
12. Breedveld, P., Beijnen, J.H., Schellens, J.H., Use of P-glycoprotein and BCRP inhibitors to improve oral bioavailability and CNS penetration of anticancer drugs. Trends Pharmacol. Sci. 27:1 (2006), 17–24.
13. Brunauer, S., Emmett, P.H., Teller, E., Adsorption of gases in multimolecular layers. J. Am. Chem. Soc. 60:2 (1938), 309–319.
14. Cedervall, T., Lynch, I., Foy, M., Berggård, T., Donnelly, S.C., Cagney, G., Linse, S., Dawson, K.A., Detailed identification of plasma proteins adsorbed on copolymer nanoparticles. Angew. Chem. 119:30 (2007), 5856–5858.
15. Chakraborty, S., Basu, S., Lahiri, A., Basak, S., Inclusion of chrysin in beta-cyclodextrin nanocavity and its effect on antioxidant potential of chrysin: a spectroscopic and molecular modeling approach. J. Mol. Struct. 977:1–3 (2010), 180–188.
16. Cherniack, E.P., A berry thought-provoking idea: the potential role of plant polyphenols in the treatment of age-related cognitive disorders. Br. J. Nutr. 108:5 (2012), 794–800.
17. Choudhury, D., Ganguli, A., Dastidar, D.G., Acharya, B.R., Das, A., Chakrabarti, G., Apigenin shows synergistic anticancer activity with curcumin by binding at different sites of tubulin. Biochimie 95:6 (2013), 1297–1309.
18. Chung, T.H., Wu, S.H., Yao, M., Lu, C.W., Lin, Y.S., Hung, Y., Mou, C.Y., Chen, Y.C., Huang, D.M., The effect of surface charge on the uptake and biological function of mesoporous silica nanoparticles in 3T3-L1 cells and human mesenchymal stem cells. Biomaterials 28:19 (2007), 2959–2966.
19. Cooper, G., The Cell A Molecular Approach. 2nd ed., 2000, Sinauer Associates, Sunderland (MA).
20. DeMuth, P., Hurley, M., Wu, C., Galanie, S., Zachariah, M.R., DeShong, P., Mesoscale porous silica as drug delivery vehicles: synthesis, characterization, and pH-sensitive release profiles. Micropor. Mesopor. Mater. 141:1–3 (2011), 128–134.
21. Diniz, T.C., Silva, J.C., de Lima-Saraiva, S.R., Ribeiro, F.P., Pacheco, A.G., de Freitas, R.M., Quintans-Junior, L.J., Quintans Jde, S., Mendes, R.L., Almeida, J.R., The role of flavonoids on oxidative stress in epilepsy. Oxid. Med. Cell Longev., 2015, 2015, 171756.
22. Fan, J., Fang, G., Wang, X., Zeng, F., Xiang, Y., Wu, S., Targeted anticancer prodrug with mesoporous silica nanoparticles as vehicles. Nanotechnology, 22(45), 2011, 455102.
23. Farghali, A., Swiderska-Sroda, A., Lojkowski, W., Razin, A.-F.M., Khedr, M., AbouAitah, K.E., pH-controlled release system for curcumin based on functionalized dendritic mesoporous silica nanoparticles. J. Nanomed. Nanotechnol., 2016, 2016.
24. Feng, R., Song, Z., Zhai, G., Preparation and in vivo pharmacokinetics of curcumin-loaded PCL-PEG-PCL triblock copolymeric nanoparticles. Int. J. Nanomed. 7 (2012), 4089–4098.
25. Ferrandiz, M.L., Alcaraz, M.J., Anti-inflammatory activity and inhibition of arachidonic acid metabolism by flavonoids. Agents Actions 32:3–4 (1991), 283–288.
26. Fleisher, B., Unum, J., Shao, J., An, G., Ingredients in fruit juices interact with dasatinib through inhibition of BCRP: a new mechanism of beverage–drug interaction. J. Pharm. Sci. 104:1 (2015), 266–275.
27. Frey, W.H., 1997. Method for administering neurologic agents to the brain. US 5624898 A.
28. Frey, W.H., 1997. Neurologic agents for nasal administration to the brain. WO1991007947 A1.
29. Frey, W.H., 2001. Method for administering insulin to the brain. US 6313093 B1.
30. Gao, Y., Chen, Y., Ji, X., He, X., Yin, Q., Zhang, Z., Shi, J., Li, Y., Controlled intracellular release of doxorubicin in multidrug-resistant cancer cells by tuning the shell-pore sizes of mesoporous silica nanoparticles. ACS Nano 5:12 (2011), 9788–9798.
31. Gerion, D., Herberg, J., Bok, R., Gjersing, E., Ramon, E., Maxwell, R., Kurhanewicz, J., Budinger, T.F., Gray, J.W., Shuman, M.A., Chen, F.F., Paramagnetic silica-coated nanocrystals as an advanced MRI contrast agent. J. Phys. Chem. C 111:34 (2007), 12542–12551.
32. Gizurarson, S., Anatomical and histological factors affecting intranasal drug and vaccine delivery. Curr. Drug Deliv. 9:6 (2012), 566–582.
33. Gupta, N.K., Dixit, V.K., Development and evaluation of vesicular system for curcumin delivery. Arch. Dermatol. Res. 303:2 (2011), 89–101.
34. Gupta, N.K., Dixit, V.K., Bioavailability enhancement of curcumin by complexation with phosphatidyl choline. J. Pharm. Sci. 100:5 (2011), 1987–1995.
35. Gupta, V., Aseh, A., Rios, C.N., Aggarwal, B.B., Mathur, A.B., Fabrication and characterization of silk fibroin-derived curcumin nanoparticles for cancer therapy. Int. J. Nanomed. 4 (2009), 115–122.
36. Hao, N., Jayawardana, K.W., Chen, X., Yan, M., One-step synthesis of amine-functionalized hollow mesoporous silica nanoparticles as efficient antibacterial and anticancer materials. ACS Appl. Mater. Interfaces 7:2 (2015), 1040–1045.
37. He, Q., Zhang, J., Shi, J., Zhu, Z., Zhang, L., Bu, W., Guo, L., Chen, Y., The effect of PEGylation of mesoporous silica nanoparticles on nonspecific binding of serum proteins and cellular responses. Biomaterials 31:6 (2010), 1085–1092.
38. Huang, D.M., Hung, Y., Ko, B.S., Hsu, S.C., Chen, W.H., Chien, C.L., Tsai, C.P., Kuo, C.T., Kang, J.C., Yang, C.S., Mou, C.Y., Chen, Y.C., Highly efficient cellular labeling of mesoporous nanoparticles in human mesenchymal stem cells: implication for stem cell tracking. FASEB J. 19:12 (2005), 2014–2016.
39. Huang, X., Teng, X., Chen, D., Tang, F., He, J., The effect of the shape of mesoporous silica nanoparticles on cellular uptake and cell function. Biomaterials 31:3 (2010), 438–448.
40. Huang, X.Y., Young, N.P., Townley, H.E., Characterization and comparison of mesoporous silica particles for optimized drug delivery. Nanomater. Nanotechnol., 2014, 4.
41. Illum, L., Transport of drugs from the nasal cavity to the central nervous system. Eur. J. Pharm. Sci. 11:1 (2000), 1–18.
42. Jambhrunkar, S., Karmakar, S., Popat, A., Yu, M.H., Yu, C.Z., Mesoporous silica nanoparticles enhance the cytotoxicity of curcumin. RSC Adv. 4:2 (2014), 709–712.
43. Jia, W.Z., Zhao, J.C., Sun, X.L., Yao, Z.G., Wu, H.L., Xi, Z.Q., Additive anticancer effects of chrysin and low dose cisplatin in human malignant glioma cell (U87) proliferation and evaluation of the mechanistic pathway. J. BUON. 20:5 (2015), 1327–1336.
44. Katayama, K., Masuyama, K., Yoshioka, S., Hasegawa, H., Mitsuhashi, J., Sugimoto, Y., Flavonoids inhibit breast cancer resistance protein-mediated drug resistance: transporter specificity and structure-activity relationship. Cancer Chemother. Pharmacol. 60:6 (2007), 789–797.
45. Katz, L.C., Iarovici, D.M., Green fluorescent latex microspheres: a new retrograde tracer. Neuroscience 34:2 (1990), 511–520.
46. Katz, L.C., Burkhalter, A., Dreyer, W.J., Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310:5977 (1984), 498–500.
47. Kaur, M., Phytochemical Mediated Modulation Of Breast Cancer Resistance Protein At The Blood Brain Barrier And Blood Cerebrospinal Fluid Barrier. 2016, Aston University.
48. Khan, M.A., Akhtar, N., Sharma, V., Pathak, K., Product development studies on sonocrystallized curcumin for the treatment of gastric cancer. Pharmaceutics 7:2 (2015), 43–63.
49. Kim, S., Philippot, S., Fontanay, S., Duval, R.E., Lamouroux, E., Canilho, N., Pasc, A., pH- and glutathione-responsive release of curcumin from mesoporous silica nanoparticles coated using tannic acid-Fe(III) complex. RSC Adv. 5:110 (2015), 90550–90558.
50. Kipen, H.M., Laskin, D.L., Smaller is not always better: nanotechnology yields nanotoxicology. Am. J. Physiol. Lung Cell. Mol. Physiol. 289:5 (2005), L696–L697.
51. Kola, I., Landis, J., Can the pharmaceutical industry reduce attrition rates?. Nat. Rev. Drug Discov. 3:8 (2004), 711–715.
52. Kong, Y., Ma, W., Liu, X., Zu, Y.G., Fu, Y.J., Wu, N., Liang, L., Yao, L.P., Efferth, T., Cytotoxic activity of curcumin towards CCRF-CEM leukemia cells and its effect on DNA damage. Molecules (Basel Switzerland) 14:12 (2009), 5328–5338.
53. Krausz, A.E., Adler, B.L., Cabral, V., Navati, M., Doerner, J., Charafeddine, R.A., Chandra, D., Liang, H., Gunther, L., Clendaniel, A., Harper, S., Friedman, J.M., Nosanchuk, J.D., Friedman, A.J., Curcumin-encapsulated nanoparticles as innovative antimicrobial and wound healing agent. Nanomed. Nanotechnol. Biol. Med. 11:1 (2015), 195–206.
54. Kresge, C.T., Leonowicz, M.E., Roth, W.J., Vartuli, J.C., Beck, J.S., Ordered mesoporous molecular-sieves synthesized by a liquid-crystal template mechanism. Nature 359:6397 (1992), 710–712.
55. Kunnumakkara, A.B., Anand, P., Aggarwal, B.B., Curcumin inhibits proliferation, invasion, angiogenesis and metastasis of different cancers through interaction with multiple cell signaling proteins. Cancer Lett. 269:2 (2008), 199–225.
56. Lee, C.-H., Lo, L.-W., Mou, C.-Y., Yang, C.-S., Synthesis and characterization of positive-charge functionalized mesoporous silica nanoparticles for oral drug delivery of an anti-inflammatory drug. Adv. Funct. Mater. 18:20 (2008), 3283–3292.
57. Lee, W.H., Loo, C.Y., Bebawy, M., Luk, F., Mason, R.S., Rohanizadeh, R., Curcumin and its derivatives: their application in neuropharmacology and neuroscience in the 21 st century. Current Neuropharmacol. 11:4 (2013), 338–378.
58. Li, J., Jiang, Y., Wen, J., Fan, G., Wu, Y., Zhang, C., A rapid and simple HPLC method for the determination of curcumin in rat plasma: assay development, validation and application to a pharmacokinetic study of curcumin liposome. Biomed. Chromatogr. 23:11 (2009), 1201–1207.
59. Liao, Y.-T., Liu, C.-H., Yu, J., Wu, K.C., Liver cancer cells: targeting and prolonged-release drug carriers consisting of mesoporous silica nanoparticles and alginate microspheres. Int. J. Nanomed., 9, 2014, 2767.
60. Lin, W., Huang Y.-w. Zhou, X.-D., Ma, Y., In vitro toxicity of silica nanoparticles in human lung cancer cells. Toxicol. Appl. Pharmacol. 217:3 (2006), 252–259.
61. Lipinski, C.A., Drug-like properties and the causes of poor solubility and poor permeability. J. Pharmacol. Toxicol. Methods 44:1 (2000), 235–249.
62. Lu, X., Qian, J., Zhou, H., Gan, Q., Tang, W., Lu, J., Yuan, Y., Liu, C., In vitro cytotoxicity and induction of apoptosis by silica nanoparticles in human HepG2 hepatoma cells. Int. J. Nanomed. 6 (2011), 1889–1901.
63. Ma, X., Teh, C., Zhang, Q., Borah, P., Choong, C., Korzh, V., Zhao, Y., Redox-responsive mesoporous silica nanoparticles: a physiologically sensitive codelivery vehicle for siRNA and doxorubicin. Antioxid. Redox Signal. 21:5 (2013), 707–722.
64. Macready, A.L., Kennedy, O.B., Ellis, J.A., Williams, C.M., Spencer, J.P., Butler, L.T., Flavonoids and cognitive function: a review of human randomized controlled trial studies and recommendations for future studies. Genes Nutr. 4:4 (2009), 227–242.
65. Marzaioli, V., Aguilar-Pimentel, J.A., Weichenmeier, I., Luxenhofer, G., Wiemann, M., Landsiedel, R., Wohlleben, W., Eiden, S., Mempel, M., Behrendt, H., Surface modifications of silica nanoparticles are crucial for their inert versus proinflammatory and immunomodulatory properties. Int. J. Nanomed. 9 (2014), 2815–2832.
66. Mayor, S., Pagano, R.E., Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 8:8 (2007), 603–612.
67. Mecocci, P., Tinarelli, C., Schulz, R.J., Polidori, M.C., Nutraceuticals in cognitive impairment and Alzheimer's disease. Front. Pharmacol., 5, 2014, 147.
68. Medina, J.H., Paladini, A.C., Wolfman, C., de Stein, M.L., Calvo, D., Diaz, L.E., Peña, C.Chrysin, (5,7-di-OH-flavone), a naturally-occurring ligand for benzodiazepine receptors, with anticonvulsant properties. Biochem. Pharmacol. 40:10 (1990), 2227–2231.
69. Meng, X., Munishkina, L.A., Fink, A.L., Uversky, V.N., Molecular mechanisms underlying the flavonoid-induced inhibition of alpha-synuclein fibrillation. Biochemistry 48:34 (2009), 8206–8224.
70. Meng, H., Xue, M., Xia, T., Zhao, Y.-L., Tamanoi, F., Stoddart, J.F., Zink, J.I., Nel, A.E., Autonomous in vitro anticancer drug release from mesoporous silica nanoparticles by pH-Sensitive nanovalves. J. Am. Chem. Soc. 132:36 (2010), 12690–12697.
71. Mercer, L.D., Kelly, B.L., Horne, M.K., Beart, P.M., Dietary polyphenols protect dopamine neurons from oxidative insults and apoptosis: investigations in primary rat mesencephalic cultures. Biochem. Pharmacol. 69:2 (2005), 339–345.
72. Mohammadian, F., Pilehvar-Soltanahmadi, Y., Mofarrah, M., Dastani-Habashi, M., Zarghami, N., Down regulation of miR-18a, miR-21 and miR-221 genes in gastric cancer cell line by chrysin-loaded PLGA-PEG nanoparticles. Artif. Cells Nanomed. Biotechnol., 2016, 1–7.
73. Monroy, A., Lithgow, G.J., Alavez, S., Curcumin and neurodegenerative diseases. Biofactors 39:1 (2013), 122–132.
74. Mukerjee, A., Vishwanatha, J.K., Formulation, characterization and evaluation of curcumin-loaded PLGA nanospheres for cancer therapy. Anticancer Res. 29:10 (2009), 3867–3875.
75. Mythri, R.B., Harish, G., Dubey, S.K., Misra, K., Bharath, M.M., Glutamoyl diester of the dietary polyphenol curcumin offers improved protection against peroxynitrite-mediated nitrosative stress and damage of brain mitochondria in vitro: implications for Parkinson's disease. Mol. Cell. Biochem. 347:1–2 (2011), 135–143.
76. Nabavi, S.F., Braidy, N., Habtemariam, S., Orhan, I.E., Daglia, M., Manayi, A., Gortzi, O., Nabavi, S.M., Neuroprotective effects of chrysin: from chemistry to medicine. Neurochem. Int. 90 (2015), 224–231.
77. Napierska, D., Thomassen, L.C., Rabolli, V., Lison, D., Gonzalez, L., Kirsch‐Volders, M., Hoet, J.A., Martens, P.H., Size‐dependent cytotoxicity of monodisperse silica nanoparticles in human endothelial cells. Small 5:7 (2009), 846–853.
78. Nehoff, H., Parayath, N.N., Domanovitch, L., Taurin, S., Greish, K., Nanomedicine for drug targeting: strategies beyond the enhanced permeability and retention effect. Int. J. Nanomed. 9 (2014), 2539–2555.
79. Nel, A., Xia, T., Mädler, L., Li, N., Toxic potential of materials at the nanolevel. Science (New York N.Y.) 311:5761 (2006), 622–627.
80. Oberdörster, G., Oberdörster, E., Oberdörster, J., Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect., 2005, 823–839.
81. Pandey, K.B., Rizvi, S.I., Plant polyphenols as dietary antioxidants in human health and disease. Oxid. Med. Cell. Longev. 2:5 (2009), 270–278.
82. Pardridge, W.M., CNS drug design based on principles of blood-brain barrier transport. J. Neurochem. 70:5 (1998), 1781–1792.
83. Pardridge, W.M., The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2:1 (2005), 3–14.
84. Persson, H.G., Gatzinsky, K.P., Distribution of retrogradely transported fluorescent latex microspheres in rat lumbosacral ventral root axons following peripheral crush injury: a light and electron microscopic study. Brain Res. 630:1–2 (1993), 115–124.
85. Pick, A., Müller, H., Mayer, R., Haenisch, B., Pajeva, I.K., Weigt, M., Bönisch, H., Müller, C.E., Wiese, M., Structure–activity relationships of flavonoids as inhibitors of breast cancer resistance protein (BCRP). Bioorg. Med. Chem. 19:6 (2011), 2090–2102.
86. Pires, A., Fortuna, A., Alves, G., Falcão, A., Intranasal drug delivery: how, why and what for?. J. Pharm. Pharm. Sci. 12:3 (2009), 288–311.
87. Purves, D., et al. Purves, Dale, Freeman, W.H., (eds.) Neuroscience, 4th ed., 2007, Basingstoke: Palgrave [distributor], New York.
88. Robey, R.W., Steadman, K., Polgar, O., Morisaki, K., Blayney, M., Mistry, P., Bates, S.E., Pheophorbide a is a specific probe for ABCG2 function and inhibition. Cancer Res. 64:4 (2004), 1242–1246.
89. Salonen, J., Laitinen, L., Kaukonen, A.M., Tuura, J., Bjorkqvist, M., Heikkila, T., Vaha-Heikkila, K., Hirvonen, J., Lehto, V.P., Mesoporous silicon microparticles for oral drug delivery: loading and release of five model drugs. J. Controlled Release 108:2–3 (2005), 362–374.
90. Santos, B.L., Oliveira, M.N., Coelho, P.L., Pitanga, B.P., da Silva, A.B., Adelita, T., Silva, V.D., Costa Mde, F., El-Bacha, R.S., Tardy, M., Chneiweiss, H., Junier, M.P., Moura-Neto, V., Costa, S.L., Flavonoids suppress human glioblastoma cell growth by inhibiting cell metabolism, migration, and by regulating extracellular matrix proteins and metalloproteinases expression. Chem. Biol. Interact. 242 (2015), 123–138.
91. Sathishkumar, G., Bharti, R., Jha, P.K., Selvakumar, M., Dey, G., Jha, R., Jeyaraj, M., Mandal, M., Sivaramakrishnan, S., Dietary flavone chrysin (5,7-dihydroxyflavone ChR) functionalized highly-stable metal nanoformulations for improved anticancer applications. RSC Adv. 5:109 (2015), 89869–89878.
92. Shukitt-Hale, B., Blueberries and neuronal aging. Gerontology 58:6 (2012), 518–523.
93. Slowing, I.I., Vivero-Escoto, J.L., Wu, C.-W., Lin, V.S.Y., Mesoporous silica nanoparticles as controlled release drug delivery and gene transfection carriers. Adv. Drug Deliv. Rev. 60:11 (2008), 1278–1288.
94. Slowing, I.I., Vivero-Escoto, J.L., Wu, C.W., Lin, V.S.Y., Mesoporous silica nanoparticles as controlled release drug delivery and gene transfection carriers. Adv. Drug Deliv. Rev. 60:11 (2008), 1278–1288.
95. Solanki, I., Parihar, P., Mansuri, M.L., Parihar, M.S., Flavonoid-based therapies in the early management of neurodegenerative diseases. Adv. Nutr. 6:1 (2015), 64–72.
96. Souza, L.C., Antunes, M.S., Filho, C.B., Del Fabbro, L., de Gomes, M.G., Goes, A.T., Donato, F., Prigol, M., Boeira, S.P., Jesse, C.R., Flavonoid chrysin prevents age-related cognitive decline via attenuation of oxidative stress and modulation of BDNF levels in aged mouse brain. Pharmacol. Biochem. Behav. 134 (2015), 22–30.
97. Taebnia, N., Morshedi, D., Doostkam, M., Yaghmaei, S., Aliakbari, F., Singh, G., Arpanaei, A., The effect of mesoporous silica nanoparticle surface chemistry and concentration on the alpha-synuclein fibrillation. RSC Adv. 5:75 (2015), 60966–60974.
98. Tonnesen, H.H., Karlsen, J., Studies on curcumin and curcuminoids. VI. Kinetics of curcumin degradation in aqueous solution. Z. Lebensm. Unters. Forsch. 180:5 (1985), 402–404.
99. Uebing-Czipura, A.U., Dawson, H.D., Scherba, G., Immortalization and characterization of lineage-restricted neuronal progenitor cells derived from the porcine olfactory bulb. J. Neurosci. Methods 170:2 (2008), 262–276.
100. van Zanden, J.J., van der Woude, H., Vaessen, J., Usta, M., Wortelboer, H.M., Cnubben, N.H.P., Rietjens, I.M.C.M., The effect of quercetin phase II metabolism on its MRP1 and MRP2 inhibiting potential. Biochem. Pharmacol. 74:2 (2007), 345–351.
101. WHO, Neurological Disorders: Public Health Challenges. 2006, World Health Organization.
102. Wang, Y.J., Pan, M.H., Cheng, A.L., Lin, L.I., Ho, Y.S., Hsieh, C.Y., Lin, J.K., Stability of curcumin in buffer solutions and characterization of its degradation products. J. Pharm. Biomed. Anal. 15:12 (1997), 1867–1876.
103. Wang, Z., Fan, H., Li, Y., Wang, Y., Anti-hepatocarcinoma effects of chrysin loaded solid lipid nanoparticle against H22 tumor bearing mice. 3rd International Conference on Material, Mechanical and Manufacturing Engineering (IC3ME 2015), 2015.
104. Wanyika, H., Gatebe, E., Kioni, P., Tang, Z.Y., Gao, Y., Synthesis and characterization of ordered mesoporous silica nanoparticles with tunable physical properties by varying molar composition of reagents. Afr. J. Pharm. Pharm. 5:21 (2011), 2402–2410.
105. Wasowski, C., Marder, M., Viola, H., Medina, J.H., Paladini, A.C., Isolation and identification of 6-methylapigenin, a competitive ligand for the brain GABA(A) receptors, from Valeriana wallichii. Planta Med. 68:10 (2002), 934–936.
106. Williams, R.J., Spencer, J.P., Flavonoids, cognition, and dementia: actions, mechanisms, and potential therapeutic utility for Alzheimer disease. Free Radic. Biol. Med. 52:1 (2012), 35–45.
107. Wolfman, C., Viola, H., Paladini, A., Dajas, F., Medina, J.H., Possible anxiolytic effects of chrysin, a central benzodiazepine receptor ligand isolated from Passiflora coerulea. Pharmacol. Biochem. Behav. 47:1 (1994), 1–4.
108. Wu, X., Han, Z., Schur, R.M., Lu, Z.-R., Targeted mesoporous silica nanoparticles delivering arsenic trioxide with environment sensitive drug release for effective treatment of triple negative breast cancer. ACS Biomater. Sci. Eng. 2:4 (2016), 501–507.
109. Xiao, J., Zhai, H., Yao, Y., Wang, C., Jiang, W., Zhang, C., Simard, A.R., Zhang, R., Hao, J., Chrysin attenuates experimental autoimmune neuritis by suppressing immuno-inflammatory responses. Neuroscience 262 (2014), 156–164.
110. Yallapu, M.M., Gupta, B.K., Jaggi, M., Chauhan, S.C., Fabrication of curcumin encapsulated PLGA nanoparticles for improved therapeutic effects in metastatic cancer cells. J. Colloid Interf. Sci. 351:1 (2010), 19–29.
111. Yao, Y., Chen, L., Xiao, J., Wang, C., Jiang, W., Zhang, R., Hao, J., Chrysin protects against focal cerebral ischemia/reperfusion injury in mice through attenuation of oxidative stress and inflammation. Int. J. Mol. Sci. 15:11 (2014), 20913–20926.
112. Ye, Y., Liu, J., Chen, M., Sun, L., Lan, M., In vitro toxicity of silica nanoparticles in myocardial cells. Environ. Toxicol. Pharmacol. 29:2 (2010), 131–137.
113. Yin, H., Zhang, H., Liu, B., Superior anticancer efficacy of curcumin-loaded nanoparticles against lung cancer. Acta Biochim. Biophys. Sin., 2013.
114. Yu, K.O., Grabinski, C.M., Schrand, A.M., Murdock, R.C., Wang, W., Gu, B.H., Schlager, J.J., Hussain, S.M., Toxicity of amorphous silica nanoparticles in mouse keratinocytes. J. Nanopart. Res. 11:1 (2009), 15–24.
115. Zaveri, M., Khandhar, A., Jain, S., Quantification of baicalein, chrysin, biochanin-A and ellagic acid in root bark of Oroxylum indicum by RP-HPLC with UV detection. Eurasian J. Anal. Chem. 3:2 (2008), 245–257.
116. Zbarsky, V., Datla, K.P., Parkar, S., Rai, D.K., Aruoma, O.I., Dexter, D.T., Neuroprotective properties of the natural phenolic antioxidants curcumin and naringenin but not quercetin and fisetin in a 6-OHDA model of Parkinson's disease. Free Rad. Res. 39:10 (2005), 1119–1125.
117. Zeng, Y.B., Yang, N., Liu, W.S., Tang, N., Synthesis, characterization and DNA-binding properties of La(III) complex of chrysin. J. Inorg. Biochem. 97:3 (2003), 258–264.
118. Zhang, S., Yang, X., Morris, M.E., Flavonoids are inhibitors of breast cancer resistance protein (ABCG2)-mediated transport. Mol. Pharmacol. 65:5 (2004), 1208–1216.
119. Zhang, S., Wang, X., Sagawa, K., Morris, M.E., Flavonoids chrysin and benzoflavone, potent breast cancer resistance protein inhibitors, have no significant effect on topotecan pharmacokinetics in rats or mdr1a/1b (-/-) mice. Drug Metab. Dispos. 33:3 (2005), 341–348.
120. Zhu, Z.Y., Luo, Y., Liu, Y., Wang, X.T., Liu, F., Guo, M.Z., Wang, Z., Liu, A.J., Zhang, Y.M., Inclusion of chrysin in beta-cyclodextrin and its biological activities. J. Drug Deliv. Sci. Tecnol. 31 (2016), 176–186.
121. Zou, P., Helson, L., Maitra, A., Stern, S.T., McNeil, S.E., Polymeric curcumin nanoparticle pharmacokinetics and metabolism in bile duct cannulated rats. Mol. Pharm. 10:5 (2013), 1977–1987.