Ferritin cage for encapsulation and delivery of bioactive nutrients: From structure, property to applications

References

• Aggarwal, B. B., Kumar, A. and Bharti, A. C. (2003). Anticancer potential of curcumin: Preclinical and clinical studies. Anticancer Res. 23:363–398.
   PubMed Web of Science ®Google Scholar
• Anand, P., Kunnumakkara, A. B., Newman, R. A. and Aggarwal, B. B. (2007). Bioavailability of curcumin: Problems and promises. Mol. Pharm. 4:807–818.
   PubMed Web of Science ®Google Scholar
• Banyard, S. H., Stammers, D. K. and Harrison, P. M. (1978). Electron-density map of apoferritin at 2.8 Å resolution. Nature 271:282–284.
   PubMed Web of Science ®Google Scholar
• Bhawana,  , Basniwal, R. K., Buttar, H. S., Jain, V. K. and Jain, N. (2011). Curcumin nanoparticles: Preparation, characterization, and antimicrobial study. J. Agric. Food Chem. 59:2056–2061.
   PubMed Web of Science ®Google Scholar
• Chasteen, N. D. and Harrison, P. M. (1999). Mineralization in ferritin: an efficient means of iron storage. J. Struct. Biol. 126:182–194.
   PubMed Web of Science ®Google Scholar
• Chen, L., Bai, G., Yang, R., Zang, J., Zhou, T. and Zhao G. (2014a). Encapsulation of β-carotene within ferritin nanocages greatly increases its water-solubility and thermal stability. Food Chem.149:307–312.
   PubMed Web of Science ®Google Scholar
• Chen, L., Bai, G., Yang, S., Yang, R., Zhao, G., Xu, C. and Leung, W. (2014b). Encapsulation of curcumin in recombinant human H-chain ferritin increases its water-solubility and stability. Food Res. Int. 62:1147–1153.
   Web of Science ®Google Scholar
• Chiancone, E. and Ceci, P. (2010). The multifaceted capacity of Dps proteins to combat bacterial stress conditions: Detoxification of iron and hydrogen peroxide and DNA binding. BBA-Gen. Subjects 1800:798–805.
   PubMed Web of Science ®Google Scholar
• Colditz, G. A., Branch, L. G., Lipnick, R. J., Willett, W. C., Rosner, B., Posner, B. M. and Hennekens, C. H. (1985). Increased green and yellow vegetable intake and lowered cancer deaths in an elderly population. Am. J. Clin. Nutr. 41:32–36.
   PubMed Web of Science ®Google Scholar
• Corsi, B., Cozzi, A., Arosio, P., Drysdale, J., Santambrogio, P., Campanella, A., Biasiotto, G., Albertini, A. and Levi, S. (2002). Human mitochondrial ferritin expressed in HeLa cells incorporates iron and affects cellular iron metabolism. J. Biol. Chem. 277:22430–22437.
   PubMed Web of Science ®Google Scholar
• Crichton, R. R. and Declercq, J. P. (2010). X-ray structures of ferritins and related proteins. BBA-Gen. Subjects. 1800:706–718.
   PubMed Web of Science ®Google Scholar
• Crichton, R. R., Herbas, A., Chavez-Alba, O. and Roland, F. (1996). Identification of catalytic residues involved in iron uptake by L-chain ferritins. J. Biol. Inorg. Chem. 1:567–574.
   Web of Science ®Google Scholar
• Cutler, R. G. (1984). Carotenoids and retinol: Their possible importance in determining longevity of primate species. Proc. Natl. Acad. Sci. USA. 87:7627–7631.
   Web of Science ®Google Scholar
• Dickey, L. F., Sreedharan, S., Theil, E. C., Didsbury, J. R., Wang, Y. H. and Kaufman, R. E. (1987). Differences in the regulation of messenger RNA for housekeeping and specialized-cell ferritin. A comparison of three distinct ferritin complementary DNAs, the corresponding subunits, and identification of the first processed in amphibian. J. Biol. Chem. 262:7901–7907.
   PubMed Web of Science ®Google Scholar
• Engle-Stone, R., Yeung, A., Welch, R. and Glahn, R. (2005). Meat and ascorbic acid can promote Fe availability from Fe-phytate but not from Fe-tannic acid complexes. J. Agric. Food. Chem. 53:10276–10284.
   PubMed Web of Science ®Google Scholar
• Falvo, E., Tremante, E., Fraioli, R., Leonetti, C., Zamparelli, C., Boffi, A., Morea, V., Ceci, P. and Giacomini, P. (2013). Antibody-drug conjugates: targeting melanoma with cisplatin encapsulated in protein-cage nanoparticles based on human ferritin. Nanoscale 5:12278–12285.
   PubMed Web of Science ®Google Scholar
• Francis, F. J. (1989). Food colorants: Anthocyanins. Cri. Rev. Food Sci. Nutr. 28:273–314.
   PubMed Web of Science ®Google Scholar
• Frenkiel-Krispin, D., Levin-Zaidman, S., Shimoni, E., Wolf, S. G., Wachtel, E. J., Arad, T., Finkel, S. E., Kolter, R. and Minsky, A. (2001). Regulated phase transitions of bacterial chromatin: a non-enzymatic pathway for generic DNA protection. EMBO J. 20:1184–1191
   PubMed Web of Science ®Google Scholar
• Fu, X., Deng, J., Yang, H., Masuda, T., Goto, F., Yoshihara, T. and Zhao, G. (2010). A novel EP-involved pathway for iron release from soya bean seed ferritin. Biochem. J. 427:313–321.
   PubMed Web of Science ®Google Scholar
• Gerl, M. and Jaenicke, R. (1987). Mechanism of the self-assembly of apoferritin from horse spleen. Cross-linking and spectroscopic analysis. Eur. Biophys. J. Biophy. 15:103–109.
   PubMed Web of Science ®Google Scholar
• Gerster, H. (1993). Anticarcinogenic effect of common carotenoids. Int. J. Vitam. Nutr. Res. 63:93–121.
   PubMed Web of Science ®Google Scholar
• Glahn, R. P., Wortley, G. M., South, P. K. and Miller, D. D. (2002). Inhibition of iron uptake by phytic acid, tannic acid, and ZnCl2: studies using an in vitro digestion/Caco-2 cell model. J. Agric. Food Chem. 50:390–395.
   PubMed Web of Science ®Google Scholar
• Grant, R. A., Filman, D. J., Finkel, S. E., Kolter, R. and Hogle, J. M. (1998). The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat. Struct. Biol. 5:294–303.
   PubMedGoogle Scholar
• Gschwind, A., Fischer, O. M. and Ullrich, A. (2004). Timeline: the discovery of receptor tyrosine kinases: targets for cancer therapy. Nat. Rev. Cancer 4:361–370.
   PubMed Web of Science ®Google Scholar
• Hallberg, L., Brune, M., Erlandsson, M., Sandberg, A. S. and Rossander-Hultén, L. (1991). Calcium: effect of different amounts on nonheme- and heme-iron absorption in humans. Am. J. Clin. Nutr. 53:112–119.
   PubMed Web of Science ®Google Scholar
• Harrison, P. M. and Arosio, P. (1996). The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275:161–203.
   PubMed Web of Science ®Google Scholar
• Hoppler, M., Schönbächler, A., Meile, L., Hurrell, R. F. and Walczyk, T. (2008). Ferritin-iron is released during boiling and in vitro gastric digestion. J. Nutr. 138:878–884.
   PubMed Web of Science ®Google Scholar
• Huang, P., Rong, P., Jin, A., Yan, X., Zhang, M. G., Lin, J., Hu, H., Wang, Z., Yue, X., Li, W., Niu, G., Zeng, W., Wang, W., Zhou, K. and Chen, X. (2014). Dye-loaded ferritin nanocages for multimodal imaging and photothermal therapy. Adv. Mater. 26:6401–6408.
   PubMed Web of Science ®Google Scholar
• Ilari, A., Stefanini, S., Chiancone, E. and Tsernoglou, D. (2000). The dodecameric ferritin from Listeria innocua contains a novel intersubunit iron-binding site. Nat. Struct. Biol. 7:38–43.
   PubMedGoogle Scholar
• Iwahori, K., Yoshizawa, K., Muraoka, M. and Yamashita, I. (2005). Fabrication of ZnSe nanoparticles in the apoferritin cavity by designing a slow chemical reaction system. Inorg. Chem. 44:6393–6400.
   PubMed Web of Science ®Google Scholar
• Jackman, R. L., Yada, R. Y., Tung, M.A. and Speers, R. A. (1987). Anthocyanins as food colorants−A review. J. Food Biochem. 11:201–247.
   Web of Science ®Google Scholar
• Kalgaonkar, S and Lönnerdal, B. (2009). Receptor-mediated uptake of ferritin-bound iron by human intestinal Caco-2 cells. J. Nutr. Biochem. 20:304–311.
   PubMed Web of Science ®Google Scholar
• Kalantzi, L., Goumas, K., Kalioras, V., Abrahamsson, B., Dressman, J. B. and Reppas, C. (2006). Characterization of the human upper gastrointestinal contents under conditions simulating bioavailability/bioequivalence studies. Pharm. Res. 23:165–176.
   PubMed Web of Science ®Google Scholar
• Kang, S., Oltrogge, L. M., Broomell, C. C., Liepold, L. O., Prevelige, P. E., Young, M. and Douglas, T. (2008). Controlled assembly of bifunctional chimeric protein cages and composition analysis using noncovalent mass spectrometry. J. Am. Chem. Soc. 130:16527–16529.
   PubMed Web of Science ®Google Scholar
• Kim, M., Rho, Y., Jin, K. S., Ahn, B., Jung, S., Kim, H. and Ree, M. (2011). pH-dependent structures of ferritin and apoferritin in solution: Disassembly and reassembly. Biomacromolecules 12: 1629–1640.
   PubMed Web of Science ®Google Scholar
• Kritchevsky, S. B. (1999). β-Carotene, carotenoids and the prevention of coronary heart disease. J. Nutr. 129:5–8.
   PubMed Web of Science ®Google Scholar
• Laufberger, V. (1937). Sur la cristallisation de la ferritine. Bull Soc. Chim. Boil. 19: 1575–1582.
   Google Scholar
• Laulhère, J. P. and Briat, J. F. (1993). Iron release and uptake by plant ferritin as affected by pH, reduction and chelation. Biochem. J. 290:693–699.
   PubMed Web of Science ®Google Scholar
• Le Brun, N. E., Crow, A., Murphy, M. E. P., Mauk, A. G. and Moore, G. R. (2010). Iron core mineralization in prokaryotic ferritins. BBA-Gen. Subjects 1800:732–744.
   PubMed Web of Science ®Google Scholar
• Levi, S., Corsi, B., Bosisio, M., Invernizzi, R., Volz, A., Sanford, D., Arosio, P. and Drysdale, J. (2001). A human mitochondrial ferritin encoded by an intronless gene. J. Biol. Chem. 276:24437–24440.
   PubMed Web of Science ®Google Scholar
• Li, C., Fu, X., Qi, X., Hu, X., Chasteen, N. D. and Zhao, G. (2009). Protein association and dissociation regulated by ferric ion: A novel pathway for oxidative deposition of iron in pea seed ferritin. J. Biol. Chem. 284:16743–16751.
   PubMed Web of Science ®Google Scholar
• Li, L., Fang, C. J., Ryan, J. C., Niemi, E. C., Lebr´on, J. A., Björkman, P. J., Arase, H., Torti, F. M., Torti, S. V., Nakamura, M. C. and Seaman, W. E. (2010). Binding and uptake of H-ferritin are mediated by human transferrin receptor-1. Proc. Natl. Acad. Sci. USA 107:3505–3510.
   PubMed Web of Science ®Google Scholar
• Li, M., Zhang, T., Yang, H., Zhao, G. and Xu, C. (2014). A novel calcium supplement prepared by phytoferritin nanocages protects against absorption inhibitors through a unique pathway. Bone 64:115–123.
   PubMed Web of Science ®Google Scholar
• Li, X., Qiu, L., Zhu, P., Tao, X., Imanaka, T., Zhao, J., Huang, Y., Tu, Y. and Cao, X. (2012). Epidermal growth factor-ferritin H-chain protein nanoparticles for tumor active targeting. Small 8:2505–2514.
   PubMed Web of Science ®Google Scholar
• Liang, M., Fan, K., Zhou, M., Duan, D., Zheng, J., Yang, D., Feng, J. and Yan, X. (2014). H-ferritin-nanocaged doxorubicin nanoparticles specifically target and kill tumors with a single-dose injection. Proc. Natl. Acad. Sci. USA. 111:14900–14905.
   PubMed Web of Science ®Google Scholar
• Liao, X., Yun, S. and Zhao, G. (2014). Structure, function, and nutrition of phytoferritin: a newly functional factor for iron supplement. Crit. Rev. Food Sci. 54:1342–1352.
   PubMed Web of Science ®Google Scholar
• Lila, M. A. (2004). Anthocyanins and human health: An in vitro investigative approach. J. Biomed. Biotech. 2004:306–313.
   PubMedGoogle Scholar
• Lobréaux, S. and Briat, J. F. (1991). Ferritin accumulation and degradation in different organs of pea (Pisum sativum) during development. Biochem. J. 274:601–606.
   PubMed Web of Science ®Google Scholar
• Lönnerdal, B. (1997). Effects of milk and milk components on calcium,magnesium, and trace element absorption during infancy. Physiol. Rev. 77:643–669.
   PubMed Web of Science ®Google Scholar
• Lynch, S. R. (2000). The effect of calcium on iron absorption. Nutr. Res. Rev. 13:141–158.
   PubMed Web of Science ®Google Scholar
• Lv, C., Zhang, S., Zang, J., Zhao, G. and Xu, C. (2014). Four-fold channels are involved in iron diffusion into the inner cavity of plant ferritin. Biochemistry 53: 2232–2241.
   PubMed Web of Science ®Google Scholar
• Masuda, T., Goto, F. and Yoshihara, T. (2001). A novel plant ferritin subunit from soybean that is related to a mechanism in iron release. J. Biol. Chem. 276: 19575–19579.
   PubMed Web of Science ®Google Scholar
• Martinez, A. and Kolter, R. (1997). Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 179:5188–5194.
   PubMed Web of Science ®Google Scholar
• Masuda, T., Goto, F. and Yoshihara, T. and Mikami, B. (2010). Crystal structure of plant ferritin reveals a novel metal binding site that functions as a transit site for metal transfer in ferritin. J. Biol. Chem. 285:4049–4059.
   PubMed Web of Science ®Google Scholar
• Mauludin, R., Müller, R. H. and Keck, C. M. (2009). Kinetic solubility and dissolution velocity of rutin nanocrystals. Eur. J. Pharm. Sci. 36:502–510.
   PubMed Web of Science ®Google Scholar
• Miranda, G. and Pelissier, J. P. (1983). Kinetic studies of in vivo digestion of bovine unheated skim-milk proteins in the rat stomach. J. Dairy Res. 50:27–36.
   PubMed Web of Science ®Google Scholar
• Perales, S., Barberá, R., Lagarda, M. J. and Farré, R. (2005). Bioavailability of calcium from milk-based formulas and fruit juices containing milk and cereals estimated by in vitro methods. J. Agric. Food Chem. 53:3721–3726.
   PubMed Web of Science ®Google Scholar
• Pizzo, P., Scapin, C., Vitadello, M., Florean, C. and Gorza, L. (2010). Grp 94 acts as a mediator of curcumin-induced antioxidant defence in myogenic cells. J. Cell. Mol. Med. 14:970–981.
   PubMed Web of Science ®Google Scholar
• Qian, C., Decker, E. C., Xiao, H. and McClements, D. J. (2012). Physical and chemical stability of b-carotene-enriched nanoemulsions: Influence of pH, ionic strength, temperature, and emulsifier type. Food Chem. 132:1221–1229.
   PubMed Web of Science ®Google Scholar
• San Martin, C. D., Garri, C., Pizarro, F., Walter, T., Theil, E. C. and Núnez, M. T. (2008). Caco-2 intestinal epithelial cells absorb soybean ferritin by μ2 (AP2)-dependent endocytosis. J. Nutr. 138:659–666.
   PubMed Web of Science ®Google Scholar
• Santambrogio, P., Levi, S., Arosio, P., Palagi, L., Vecchio, G., Lawson, D. M., Yewdall, S. J., Artymiuk, P. J., Harrison, P. M. and Jappelli, R. (1992). Evidence that a salt bridge in the light chain contributes to the physical stability difference between heavy and light human ferritins. J. Biol. Chem. 267:14077–14083.
   PubMed Web of Science ®Google Scholar
• Schreiber, G., Haran, G. and Zhou, H-X. (2009). Fundamental aspects of protein-protein association kinetics. Chem. Rev. 109:839–860.
   PubMed Web of Science ®Google Scholar
• Simonian, H. P., Vo, L., Doma, S., Fisher, R. S. and Parkman, H. P. (2005). Regional postprandial differences in pH within the stomach and gastroesophageal junction. Dig. Dis. Sci. 50:2276–2285.
   PubMed Web of Science ®Google Scholar
• Soares, J. H. and Craft, N. E. (1992). Relative solubility, stability, and absorptivity of lutein and β-carotene in organic solvents. J. Agric. Food Chem. 40:431–434.
   Web of Science ®Google Scholar
• Stefanini, S., Cavallo, S., Wang, C. Q., Tataseo, P., Vecchini, P., Giartosio, A. and Emilia, C. (1996). Thermal stability of horse spleen apoferritin and human recombinant H apoferritin. Arch. Biochem. Biophys. 325:58–64.
   PubMed Web of Science ®Google Scholar
• Stefanini, S., Vecchini, P. and Chiancone, E. (1987). On the mechanism of horse spleen apoferritin assembly: A sedimentation-velocity and circular-dichroism study. Biochemistry 26:1831–1837.
   PubMed Web of Science ®Google Scholar
• Strimpakos, A. S. and Sharma, R. A. (2008). Curcumin: Preventive and therapeutic properties in laboratory studies and clinical trials. Antioxid. Redox. Sign. 10:511–545.
   PubMed Web of Science ®Google Scholar
• Sun, S., Arosio, P., Levi, S. and Chasteen, N. D. (1993). Ferroxidase kinetics of human liver apoferritin, recombinant H-chain apoferritin, and site-directed mutants. Biochemistry. 32:9362–9369.
   PubMed Web of Science ®Google Scholar
• Tai, C. Y. and Chen, B. H. (2000). Analysis and stability of carotenoids in the flowers of daylily (Hemerocallis disticha) as affected by various treatments. J. Agric. Food Chem. 48:5962–5968.
   PubMed Web of Science ®Google Scholar
• Toussaint, L., Bertrand, L., Hue, L., Crichton, R. R. and Declercq, J. P. (2007). High-resolution X-ray structures of human apoferritin H-chain mutants correlated with their activity and metal-binding sites. J. Mol. Biol. 365:440–452.
   PubMed Web of Science ®Google Scholar
• Uchida, M., Kang, S., Reichhardt, C., Harlen, K. and Douglas, T. (2010). The ferritin superfamily: supramolecular templates for materials synthesis. BBA-Gen. Subjects 1800:834–845.
   PubMed Web of Science ®Google Scholar
• van Wuytswinkel, O., Savino, G. and Briat, J. F. (1995). Purification and characterization of recombinant pea seed ferritins expressed in Escherichia coli: influence of N-terminus deletions on protein solubility and core formation in vitro. Biochem. J. 305:253–261.
   PubMed Web of Science ®Google Scholar
• von Lintig, J. (2010). Colors with functions: Elucidating the biochemical and molecular basis of carotenoid metabolism. Ann. Rev. Nutr. 30:35–56.
   PubMed Web of Science ®Google Scholar
• Weaver, C. M. (2009). Closing the gap between calcium intake and requirements. J. Acad. Nutr. Diet. 109:812–813.
   Google Scholar
• Wang, D. and Lippard, S. J. (2005) Cellular processing of platinum anticancer drugs. Nat. Rev. Drug Discov. 4:307–320.
   PubMed Web of Science ®Google Scholar
• Xing, R. M., Wang, X. Y., Zhang, C. L., Zhang, Y. M., Wang, Q., Yang, Z. and Guo, Z. (2009). Characterization and cellular uptake of platinum anticancer drugs encapsulated in apoferritin. J. Inorg. Biochem. 103:1039–1041.
   PubMed Web of Science ®Google Scholar
• Yamashita, I., Iwahori, K. and Kumagai, S. (2010). Ferritin in the field of nanodevices. BBA-Gen. Subjects 1800:846–857.
   PubMed Web of Science ®Google Scholar
• Yan, F., Zhang, Y., Kim, K. S., Yuan, H. K. and Vo-Dinh, T. (2010). Cellular uptake and photodynamic activity of protein nanocages containing methylene blue photosensitizing drug. Photochem. Photobiol. 86:662–666.
   PubMed Web of Science ®Google Scholar
• Yang, H., Fu, X., Li, M., Chen, B. and Zhao, G. (2010). Protein association and dissociation regulated by extension peptide: A mode for iron control by phytoferritin in seeds. Plant Physiol. 154:1481–1491.
   PubMed Web of Science ®Google Scholar
• Yang, R., Chen, L., Zhang, T., Yang, S., Leng, X. and Zhao, G. (2014a). Self-assembly of ferritin nanocages into linear chains induced by poly(α, L-lysine). Chem. Commun. 50:481–483.
   PubMed Web of Science ®Google Scholar
• Yang, R., Chen, L., Yang, S., Lv, C., Leng, X. and Zhao, G. (2014b). 2D square arrays of protein nanocages through channel-directed electrostatic interaction with poly(α, L-Lysine). Chem. Commun. 50:2879–2882.
   PubMed Web of Science ®Google Scholar
• Yang, Z., Wang, X. Y., Diao, H. J., Zhang, J. F., Li, H. Y., Sun, H. Z. and Guo, Z. (2007). Encapsulation of platinum anticancer drugs by apoferritin. Chem Commun. 3453–3455.
   PubMed Web of Science ®Google Scholar
• Yang, R., Zhou, Z., Sun, G., Gao, Y., Xu, J., Strappe, P., Blanchard, C., Cheng, Y. and Ding, X. (2015). Synthesis of homogeneous protein-stabilized rutin nanodispersions by reversible assembly of soybean (Glycine max) seed ferritin. RSC Adv. 5:31533–31540.
   Web of Science ®Google Scholar
• Yun, S., Habicht, J. P., Miller, D. D. and Glahn, R. P. (2004). An in vitro digestion/Caco-2 cell culture system accurately predicts the effects of ascorbic acid and polyphenolic compounds on iron bioavailability in humans. J. Nutr. 134:2717–2721.
   PubMed Web of Science ®Google Scholar
• Zafra-Stone, S., Yasmin, T., Bagchi, M., Chatterjee, A., Vinson, J. A. and Bagchi, D. (2007). Berry anthocyanins as novel antioxidants in human health and disease prevention. Mol. Nutr. Food Res. 51:675–683.
   PubMed Web of Science ®Google Scholar
• Ziberna, L., Tramer, F., Moze, S., Vrhovsek, U., Mattivi, F. and Passamonti, S. (2012). Transport and bioactivity of cyanidin 3-glucoside into the vascular endothelium. Free Rad. Biol. Med. 52:1750–1759.
   PubMed Web of Science ®Google Scholar
• Zhang, T., Lv, C., Chen, L., Bai, G., Zhao, G. and Xu, C. (2014). Encapsulation of anthocyanin molecules within a ferritin nanocage increases their stability and cell uptake efficiency. Food Res. Int. 62:183–192.
   Web of Science ®Google Scholar
• Zhao, G. (2010). Phytoferritin and its implications for human health and nutrition. BBA-Gen. Subjects. 1800:815–823.
   PubMed Web of Science ®Google Scholar
• Zhen, Z. P., Tang, W., Chen, H. M., Lin, X., Todd, T., Wang, G., Cowger, T., Chen, X. and Xie, J. (2013). RGD-modified apoferritin nanoparticles for efficient drug delivery to tumors. ACS Nano 7:4830–4837.
   PubMed Web of Science ®Google Scholar