1932

Abstract

Ferritins represent a class of iron storage proteins with detoxification functions. The importance of these proteins is reflected by their wide distribution throughout the animal and plant kingdoms. Ferritin has two forms: holo and apo. Holo ferritin can act as an efficient and safe factor for iron supplementation, whereas apo ferritin is able to serve as a promising delivery nanovehicle for nutrients and bioactive compounds. So far, the dual functions of ferritins from animal and plant sources have been extensively studied in several fields, such as food, nutrition, medicine, and materials. This review outlines the structure of animal and plant ferritin, the iron supplementation function of holo ferritin, and the delivery function of apo ferritin. Recent advances in iron supplementation and nutrient encapsulation and delivery are highlighted. Finally, the current challenges and future developments for multifunctional applications of ferritins are discussed.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-food-060721-024902
2023-03-27
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/food/14/1/annurev-food-060721-024902.html?itemId=/content/journals/10.1146/annurev-food-060721-024902&mimeType=html&fmt=ahah

Literature Cited

  1. Ahn B, Lee SG, Yoon HR, Lee JM, Oh HJ et al. 2018. Four-fold channel-nicked human ferritin nanocages for active drug loading and pH-responsive drug release. Angew. Chem. Int. Ed. 57:112909–13
    [Google Scholar]
  2. Alleyne M, Horne MK, Miller JL. 2008. Individualized treatment for iron-deficiency anemia in adults. Am. J. Med. 121:11943–48
    [Google Scholar]
  3. Arosio P, Levi S 2002. Ferritin, iron homeostasis, and oxidative damage. Free Radic. Biol. Med. 33:4457–63
    [Google Scholar]
  4. Bayat P, Farshchi M, Yousefian M, Mahmoudi M, Yazdian-Robati R. 2021. Flavonoids, the compounds with anti-inflammatory and immunomodulatory properties, as promising tools in multiple sclerosis (MS) therapy: a systematic review of preclinical evidence. Int. Immunopharmacol. 95:107562
    [Google Scholar]
  5. Beard JL, Burton JW, Theil EC. 1996. Purified ferritin and soybean meal can be sources of iron for treating iron deficiency in rats. J. Nutr. 126:1154–60
    [Google Scholar]
  6. Blanco-Rojo R, Vaquero MP 2019. Iron bioavailability from food fortification to precision nutrition. A review. Innov. Food Sci. Emerg. Technol. 51:126–38
    [Google Scholar]
  7. Bou-Abdallah F, Zhao G, Mayne HR, Arosio P, Chasteen ND. 2005. Origin of the unusual kinetics of iron deposition in human H-chain ferritin. J. Am. Chem. Soc. 127:113885–93
    [Google Scholar]
  8. Bovell-Benjamin AC, Guinard JX. 2003. Novel approaches and application of contemporary sensory evaluation practices in iron fortification programs. Crit. Rev. Food Sci. Nutr. 43:4379–400
    [Google Scholar]
  9. Ceci P, Forte E, Di Cecca G, Fornara M, Chiancone E. 2011. The characterization of Thermotoga maritima ferritin reveals an unusual subunit dissociation behavior and efficient DNA protection from iron-mediated oxidative stress. Extremophiles 15:3431–39
    [Google Scholar]
  10. Chakraborti S, Korpi A, Kumar M, Stpień P, Kostiainen MA, Heddle JG. 2019. Three-dimensional protein cage array capable of active enzyme capture and artificial chaperone activity. Nano Lett 19:63918–24
    [Google Scholar]
  11. Chasteen ND, Harrison PM. 1999. Mineralization in ferritin: an efficient means of iron storage. J. Struct. Biol. 126:3182–94
    [Google Scholar]
  12. Chen H, Zhang S, Xu C, Zhao G. 2016. Engineering protein interfaces yields ferritin disassembly and reassembly under benign experimental conditions. Chem. Commun. 52:467402–5
    [Google Scholar]
  13. Chen L, Bai G, Yang R, Zang J, Zhou T, Zhao G. 2014a. Encapsulation of β-carotene within ferritin nanocages greatly increases its water-solubility and thermal stability. Food Chem 149:307–12
    [Google Scholar]
  14. Chen L, Bai G, Yang S, Yang R, Zhao G et al. 2014b. Encapsulation of curcumin in recombinant human H-chain ferritin increases its water-solubility and stability. Food Res. Int. 62:1147–53
    [Google Scholar]
  15. Ciambellotti S, Pratesi A, Severi M, Ferraro G, Alessio E et al. 2018. The NAMI A-human ferritin system: a biophysical characterization. Dalton Trans 47:3311429–37
    [Google Scholar]
  16. Crich SG, Bussolati B, Tei L, Grange C, Esposito G et al. 2006. Magnetic resonance visualization of tumor angiogenesis by targeting neural cell adhesion molecules with the highly sensitive gadolinium-loaded apoferritin probe. Cancer Res 66:189196–201
    [Google Scholar]
  17. Crich SG, Cadenazzi M, Lanzardo S, Conti L, Ruiu R et al. 2015. Targeting ferritin receptors for the selective delivery of imaging and therapeutic agents to breast cancer cells. Nanoscale 7:156527–33
    [Google Scholar]
  18. Crichton RR, Declercq JP. 2010. X-ray structures of ferritins and related proteins. Biochim. Biophys. Acta 1800:8706–18
    [Google Scholar]
  19. Crichton RR, Herbas A, Chavez-Alba O, Roland F 1996. Identification of catalytic residues involved in iron uptake by L-chain ferritins. J. Biol. Inorg. Chem. 1:6567–74
    [Google Scholar]
  20. Davila-Hicks P, Theil EC, Lönnerdal B. 2004. Iron in ferritin or in salts (ferrous sulfate) is equally bioavailable in nonanemic women. Am. J. Clin. Nutr. 80:4936–40
    [Google Scholar]
  21. De Carvalho APA, Conte-Junior CA. 2021. Health benefits of phytochemicals from Brazilian native foods and plants: antioxidant, antimicrobial, anti-cancer, and risk factors of metabolic/endocrine disorders control. Trends Food Sci. Technol. 111:534–48
    [Google Scholar]
  22. Deng J, Li M, Zhang T, Chen B, Leng X, Zhao G. 2011. Binding of proanthocyanidins to soybean (Glycine max) seed ferritin inhibiting protein degradation by protease in vitro. Food Res. Int. 44:133–38
    [Google Scholar]
  23. Drewnowski A, Gomez-Carneros C. 2000. Bitter taste, phytonutrients, and the consumer: a review. Am. J. Clin. Nutr. 72:61424–35
    [Google Scholar]
  24. Engle-Stone R, Yeung A, Welch R, 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. 53:2610276–84
    [Google Scholar]
  25. Fan K, Cao C, Pan Y, Lu D, Yang D et al. 2012. Magnetoferritin nanoparticles for targeting and visualizing tumour tissues. Nat. Nanotechnol. 7:7459–64
    [Google Scholar]
  26. Ferrer-Miralles N, Rodríguez-Carmona E, Corchero JL, García-Fruitós E, Vázquez E, Villaverde A. 2015. Engineering protein self-assembling in protein-based nanomedicines for drug delivery and gene therapy. Crit. Rev. Biotechnol. 35:2209–21
    [Google Scholar]
  27. Fu X, Deng J, Yang H, Masuda T, Goto F, Yoshihara T, Zhao G. 2010. A novel EP-involved pathway for iron release from soya bean seed ferritin. Biochem. J. 427:313–21
    [Google Scholar]
  28. Gerl M, Jaenicke R. 1987. Mechanism of the self-assembly of apoferritin from horse spleen-cross-linking and spectroscopic analysis. Eur. Biophys. J. 15:2103–9
    [Google Scholar]
  29. Grant RA, Filman DJ, Finkel SE, Kolter R, Hogle JM. 1998. The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat. Struct. Biol. 5:4294–303
    [Google Scholar]
  30. Han O. 2011. Molecular mechanism of intestinal iron absorption. Metallomics 3:2103–9
    [Google Scholar]
  31. Harrison PM, Arosio P. 1996. Ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275:3161–203
    [Google Scholar]
  32. Hoppler M, Schönbächler A, Meile L, Hurrell RF, Walczyk T. 2008. Ferritin-iron is released during boiling and in vitro gastric digestion. J. Nutr. 138:5878–84
    [Google Scholar]
  33. Hoppler M, Zeder C, Walczyk T. 2009. Quantification of ferritin-bound iron in plant samples by isotope tagging and species-specific isotope dilution mass spectrometry. Anal. Chem. 81:177368–72
    [Google Scholar]
  34. Huang P, Rong P, Jin A, Yan X, Zhang MG et al. 2014. Dye-loaded ferritin nanocages for multimodal imaging and photothermal therapy. Adv. Mater. 26:376401–8
    [Google Scholar]
  35. Huard DJE, Kane KM, Tezcan FA. 2013. Re-engineering protein interfaces yields copper-inducible ferritin cage assembly. Nat. Chem. Biol. 9:3169–76
    [Google Scholar]
  36. Ilari A, Stefanini S, Chiancone E, Tsernoglou D. 2000. The dodecameric ferritin from Listeria innocua contains a novel intersubunit iron-binding site. Nat. Struct. Biol. 7:138–43
    [Google Scholar]
  37. Johnson E, Cascio D, Sawaya MR, Gingery M, Schröder I. 2005. Crystal structures of a tetrahedral open pore ferritin from the hyperthermophilic archaeon Archaeoglobus fulgidus. Structure 13:4637–48
    [Google Scholar]
  38. Jutz G, Van Rijn P, Miranda BS, Böker A. 2015. Ferritin: a versatile building block for bionanotechnology. Chem. Rev. 115:41653–701
    [Google Scholar]
  39. Kalantzi L, Goumas K, Kalioras V, Abrahamsson B, Dressman JB, Reppas C. 2006. Characterization of the human upper gastrointestinal contents under conditions simulating bioavailability/bioequivalence studies. Pharm. Res. 23:1165–76
    [Google Scholar]
  40. Kalgaonkar S, Lönnerdal B. 2008. Effects of dietary factors on iron uptake from ferritin by caco-2 cells. J. Nutr. Biochem. 19:133–39
    [Google Scholar]
  41. Kálmán FK, Geninatti-Crich S, Aime S 2010. Reduction/dissolution of a β-MnOOH nanophase in the ferritin cavity to yield a highly sensitive, biologically compatible magnetic resonance imaging agent. Angew. Chem. Int. Ed. 49:3612–15
    [Google Scholar]
  42. Kilic MA, Ozlu E, Calis S. 2012. A novel protein-based anticancer drug encapsulating nanosphere: apoferritin-doxorubicin complex. J. Biomed. Nanotechnol. 8:3508–14
    [Google Scholar]
  43. Kim M, Rho Y, Jin KS, Ahn B, Jung S et al. 2011. pH-Dependent structures of ferritin and apoferritin in solution: disassembly and reassembly. Biomacromolecules 12:51629–40
    [Google Scholar]
  44. Klem MT, Mosolf J, Young M, Douglas T 2008. Photochemical mineralization of europium, titanium, and iron oxyhydroxide nanoparticles in the ferritin protein cage. Inorg. Chem. 47:72237–39
    [Google Scholar]
  45. Kumari A, Chauhan AK. 2022. Iron nanoparticles as a promising compound for food fortification in iron deficiency anemia: a review. J. Food Sci. Technol. 59:93319–35
    [Google Scholar]
  46. Laufberger V 1937. Sur la cristallisation de la ferritine. Bull. Soc. Chim. Biol. 19:1575–82
    [Google Scholar]
  47. Lawson DM, Artymiuk PJ, Yewdall SJ, Smith JMA, Livingstone JC et al. 1991. Solving the structure of human H ferritin by genetically engineering intermolecular crystal contacts. Nature 349:6309541–44
    [Google Scholar]
  48. Lescure AM, Proudhon D, Pesey H, Ragland M, Theil EC, Briat JF. 1991. Ferritin gene transcription is regulated by iron in soybean cell cultures. PNAS 88:188222–26
    [Google Scholar]
  49. Levi S, Corsi B, Bosisio M, Invernizzi R, Volz A et al. 2001. A human mitochondrial ferritin encoded by an intronless gene. J. Biol. Chem. 276:2724437–40
    [Google Scholar]
  50. Levi S, Santambrogio P, Corsi B, Cozzi A, Arosio P. 1996. Evidence that residues exposed on the three-fold channels have active roles in the mechanism of ferritin iron incorporation. Biochem. J. 317:467–73
    [Google Scholar]
  51. Li C, Fu X, Qi X, Hu X, Chasteen ND, 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. 284:2516743–51
    [Google Scholar]
  52. Li H, Tan X, Xia X, Zang J, El-Seedi H et al. 2021. Improvement of thermal stability of oyster (Crassostrea gigas) ferritin by point mutation. Food Chem 346:128879
    [Google Scholar]
  53. Li H, Zang J, Tan X, Xia X, Wang Z, Du M. 2020. Purification and characterizations of a nanocage ferritin GF1 from oyster (Crassostrea gigas). LWT 127:109416
    [Google Scholar]
  54. Li L, Fang CJ, Ryan JC, Niemi EC, Lebrón JA et al. 2010. Binding and uptake of H-ferritin are mediated by human transferrin receptor-1. PNAS 107:83505–10
    [Google Scholar]
  55. Li M, Zhang T, Yang H, Zhao G, Xu C. 2014. A novel calcium supplement prepared by phytoferritin nanocages protects against absorption inhibitors through a unique pathway. Bone 64:115–23
    [Google Scholar]
  56. Liang M, Fan K, Zhou M, Duan D, Zheng J et al. 2014. H-ferritin-nanocaged doxorubicin nanoparticles specifically target and kill tumors with a single-dose injection. PNAS 111:4114900–5
    [Google Scholar]
  57. Liao X, Lv C, Zhang X, Masuda T, Li M, Zhao G. 2012. A novel strategy of natural plant ferritin to protect DNA from oxidative damage during iron oxidation. Free Radic. Biol. Med. 53:2375–82
    [Google Scholar]
  58. Liao X, Yun S, Zhao G 2014. Structure, function, and nutrition of phytoferritin: a newly functional factor for iron supplement. Crit. Rev. Food Sci. Nutr. 54:101342–52
    [Google Scholar]
  59. Liu G, Wang J, Lea SA, Lin Y. 2006. Bioassay labels based on apoferritin nanovehicles. ChemBioChem 7:91315–19
    [Google Scholar]
  60. Liu X, Jin W, Theil EC 2003. Opening protein pores with chaotropes enhances Fe reduction and chelation of Fe from the ferritin biomineral. PNAS 100:73653–58
    [Google Scholar]
  61. Liu X, Theil EC. 2004. Ferritin reactions: direct identification of the site for the diferric peroxide reaction intermediate. PNAS 101:238557–62
    [Google Scholar]
  62. Liu Y, Yang R, Liu J, Meng D, Zhou Z et al. 2019. Fabrication, structure, and function evaluation of the ferritin based nano-carrier for food bioactive compounds. Food Chem 299:125097
    [Google Scholar]
  63. Lönnerdal B. 2009. Soybean ferritin: implications for iron status of vegetarians. Am. J. Clin. Nutr. 89:5S1680–85
    [Google Scholar]
  64. Lönnerdal B, Bryant A, Liu X, Theil EC. 2006. Iron absorption from soybean ferritin in nonanemic women. Am. J. Clin. Nutr. 83:1103–7
    [Google Scholar]
  65. Lv C, Huang S, Wang Y, Hu Z, Zhao G et al. 2021a. Chicoric acid encapsulated within ferritin inhibits tau phosphorylation by regulating AMPK and GluT1 signaling cascade. J. Funct. Foods 86:104681
    [Google Scholar]
  66. Lv C, Yin S, Zhang X, Hu J, Zhang T, Zhao G. 2020. 16-Mer ferritin-like protein templated gold nanoclusters for bioimaging detection of methylmercury in the brain of living mice. Anal. Chim. Acta 1127:149–55
    [Google Scholar]
  67. Lv C, Zhang X, Liu Y, Zhang T, Chen H et al. 2021b. Redesign of protein nanocages: the way from 0D, 1D, 2D to 3D assembly. Chem. Soc. Rev. 50:63957–89
    [Google Scholar]
  68. Lv C, Zhao G, Lönnerdal B. 2015. Bioavailability of iron from plant and animal ferritins. J. Nutr. Biochem. 26:5532–40
    [Google Scholar]
  69. Macone A, Masciarelli S, Palombarini F, Quaglio D, Boffi A et al. 2019. Ferritin nanovehicle for targeted delivery of cytochrome C to cancer cells. Sci. Rep. 9:11749
    [Google Scholar]
  70. MaHam A, Tang Z, Wu H, Wang J, Lin Y 2009. Protein-based nanomedicine platforms for drug delivery. Small 5:151706–21
    [Google Scholar]
  71. Masuda T. 2015. Soybean ferritin forms an iron-containing oligomer in tofu even after heat treatment. J. Agric. Food Chem. 63:408890–95
    [Google Scholar]
  72. Masuda T, Goto F, Yoshihara T. 2001. A novel plant ferritin subunit from soybean that is related to a mechanism in iron release. J. Biol. Chem. 276:2219575–79
    [Google Scholar]
  73. Masuda T, Goto F, Yoshihara T, Mikami B. 2010a. 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. 285:64049–59
    [Google Scholar]
  74. Masuda T, Goto F, Yoshihara T, Mikami B. 2010b. The universal mechanism for iron translocation to the ferroxidase site in ferritin, which is mediated by the well conserved transit site. Biochem. Biophys. Res. Commun. 400:194–99
    [Google Scholar]
  75. Masuda T, Zang J, Zhao G, Mikami B. 2018. The first crystal structure of crustacean ferritin that is a hybrid type of H and L ferritin. Protein Sci 27:111955–60
    [Google Scholar]
  76. Meng D, Wang B, Zhen T, Zhang M, Yang R 2018. Pulsed electric fields-modified ferritin realizes loading of rutin by a moderate pH transition. J. Agric. Food Chem. 66:4612404–11
    [Google Scholar]
  77. Meng D, Zuo P, Song H, Yang R 2019. Influence of manothermosonication on the physicochemical and functional properties of ferritin as a nanocarrier of iron or bioactive compounds. J. Agric. Food Chem. 67:236633–41
    [Google Scholar]
  78. Miranda G, Pelissier JP. 1983. Kinetic studies of in vivo digestion of bovine unheated skim-milk proteins in the rat stomach. J. Dairy Res. 50:127–36
    [Google Scholar]
  79. Montemiglio LC, Testi C, Ceci P, Falvo E, Pitea M et al. 2019. Cryo-EM structure of the human ferritin-transferrin receptor 1 complex. Nat. Commun. 10:1121
    [Google Scholar]
  80. Murray-Kolb LE, Welch R, Theil EC, Beard JL. 2003. Women with low iron stores absorb iron from soybeans. Am. J. Clin. Nutr. 77:1180–84
    [Google Scholar]
  81. Nie G, Sheftel AD, Kim SF, Ponka P. 2005. Overexpression of mitochondrial ferritin causes cytosolic iron depletion and changes cellular iron homeostasis. Blood 105:52161–67
    [Google Scholar]
  82. Pandolfi L, Bellini M, Vanna R, Morasso C, Zago A et al. 2017. H-Ferritin enriches the curcumin uptake and improves the therapeutic efficacy in triple negative breast cancer cells. Biomacromolecules 18:103318–30
    [Google Scholar]
  83. Pereira AS, Small W, Krebs C, Tavares P, Edmondson DE et al. 1998. Direct spectroscopic and kinetic evidence for the involvement of a peroxodiferric intermediate during the ferroxidase reaction in fast ferritin mineralization. Biochemistry 37:289871–76
    [Google Scholar]
  84. Pereira DIA, Bruggraber SFA, Faria N, Poots LK, Tagmount MA et al. 2014. Nanoparticulate iron(III) oxo-hydroxide delivers safe iron that is well absorbed and utilised in humans. Nanomed. Nanotechnol. Biol. Med. 10:81877–86
    [Google Scholar]
  85. Pozzi C, Ciambellotti S, Bernacchioni C, Di Pisa F, Mangani S, Turano P. 2017. Chemistry at the protein-mineral interface in L-ferritin assists the assembly of a functional (μ3-oxo)Tris[(μ2-peroxo)] triiron(III) cluster. PNAS 114:102580–85
    [Google Scholar]
  86. Quintaes KD, Barbera R, Cilla A 2017. Iron bioavailability in iron-fortified cereal foods: the contribution of in vitro studies. Crit. Rev. Food Sci. Nutr. 57:102028–41
    [Google Scholar]
  87. Romagnani S. 2006. Immunological tolerance and autoimmunity. Intern. Emerg. Med. 1:3187–96
    [Google Scholar]
  88. San Martin CD, Garri C, Pizarro F, Walter T, Theil EC, Núñez MT. 2008. Caco-2 intestinal epithelial cells absorb soybean ferritin by μ2 (AP2)-dependent endocytosis. J. Nutr. 138:4659–66
    [Google Scholar]
  89. Santambrogio P, Levi S, Arosio P, Palagi L, Vecchio G et al. 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. 267:2014077–83
    [Google Scholar]
  90. Sato D, Ohtomo H, Yamada Y, Hikima T, Kurobe A et al. 2016a. Ferritin assembly revisited: a time-resolved small-angle X-ray scattering study. Biochemistry 55:2287–93
    [Google Scholar]
  91. Sato D, Takebe S, Kurobe A, Ohtomo H, Fujiwara K, Ikeguchi M. 2016b. Electrostatic repulsion during ferritin assembly and its screening by ions. Biochemistry 55:3482–88
    [Google Scholar]
  92. Schümann K, Elsenhans B, Mäurer A. 1998. Iron supplementation. J. Trace Elem. Med. Biol. 12:3129–40
    [Google Scholar]
  93. Shander A, Berth U, Betta J, Javidroozi M 2012. Iron overload and toxicity: implications for anesthesiologists. J. Clin. Anesth. 24:5419–25
    [Google Scholar]
  94. Siti Aisyah S, Hirokazu H, Mikihito T, Kenji S. 2014. Aligning CdS quantum dots in apo-ferritin protein and PS-b-P2VP organic templates. Adv. Mater. Res. 832:675–80
    [Google Scholar]
  95. Stefanini S, Cavallo S, Wang CQ, Tataseo P, Vecchini P et al. 1996. Thermal stability of horse spleen apoferritin and human recombinant H apoferritin. Arch. Biochem. Biophys. 325:158–64
    [Google Scholar]
  96. Tang J, Yu Y, Chen H, Zhao G. 2019. Thermal treatment greatly improves storage stability and monodispersity of pea seed ferritin. J. Food Sci. 84:51188–93
    [Google Scholar]
  97. Tetter S, Hilvert D. 2017. Enzyme encapsulation by a ferritin cage. Angew. Chem. Int. Ed. 56:4714933–36
    [Google Scholar]
  98. Theil EC. 2004. Iron, ferritin, and nutrition. Annu. Rev. Nutr. 24:327–43
    [Google Scholar]
  99. Theil EC, Liu XS, Tosha T 2008. Gated pores in the ferritin protein nanocage. Inorg. Chim. Acta 361:4868–74
    [Google Scholar]
  100. Toussaint L, Bertrand L, Hue L, Crichton RR, Declercq JP. 2007. High-resolution X-ray structures of human apoferritin H-chain mutants correlated with their activity and metal-binding sites. J. Mol. Biol. 365:2440–52
    [Google Scholar]
  101. Toxqui L, Vaquero MP. 2015. Chronic iron deficiency as an emerging risk factor for osteoporosis: a hypothesis. Nutrients 7:42324–44
    [Google Scholar]
  102. Treffry A, Bauminger ER, Hechel D, Hodson NW, Nowik I et al. 1993. Defining the roles of the threefold channels in iron uptake, iron oxidation and iron-core formation in ferritin: a study aided by site-directed mutagenesis. Biochem. J. 296:721–28
    [Google Scholar]
  103. Treffry A, Harrison PM, Luzzago A, Cesareni G. 1989. Recombinant H-chain ferritins: effects of changes in the 3-fold channels. FEBS Lett 247:2268–72
    [Google Scholar]
  104. Treffry A, Zhao Z, Quail MA, Guest JR, Harrison PM. 1995. Iron(II) oxidation by H chain ferritin: evidence from site-directed mutagenesis that a transient blue species is formed at the dinuclear iron center. Biochemistry 34:4615204–13
    [Google Scholar]
  105. Waldo GS, Theil EC. 1993. Formation of iron(III)-tyrosinate is the fastest reaction observed in ferritin. Biochemistry 32:4813262–69
    [Google Scholar]
  106. Waldo GS, Wright E, Whang ZH, Briat JF, Theil EC, Sayers DE. 1995. Formation of the ferritin iron mineral occurs in plastids: an X-ray absorption spectroscopy study. Plant Physiol 109:3797–802
    [Google Scholar]
  107. Wang A, Zhou K, Qi X, Zhao G. 2014. Phytoferritin association induced by EGCG inhibits protein degradation by proteases. Plant. Food Hum. Nutr. 69:4386–91
    [Google Scholar]
  108. Wang Q, Zhang C, Liu L, Li Z, Guo F et al. 2017. High hydrostatic pressure encapsulation of doxorubicin in ferritin nanocages with enhanced efficiency. J. Biotechnol. 254:34–42
    [Google Scholar]
  109. Wang Q, Zhou K, Ning Y, Zhao G. 2016. Effect of the structure of gallic acid and its derivatives on their interaction with plant ferritin. Food Chem 213:260–67
    [Google Scholar]
  110. Wang W, Wang L, Li G, Zhao G, Zhao X, Wang H. 2019. AB loop engineered ferritin nanocages for drug loading under benign experimental conditions. Chem. Commun. 55:8212344–47
    [Google Scholar]
  111. Wu T, Huang J, Jiang Y, Hu Y, Ye X et al. 2018. Formation of hydrogels based on chitosan/alginate for the delivery of lysozyme and their antibacterial activity. Food Chem 240:361–69
    [Google Scholar]
  112. Wu T, Jiang Q, Wu D, Hu Y, Chen S et al. 2019. What is new in lysozyme research and its application in food industry? A review. Food Chem 274:698–709
    [Google Scholar]
  113. Xing Y, Ma J, Yao Q, Chen X, Zang J, Zhao G. 2022. The change in the structure and functionality of ferritin during the production of pea seed milk. Foods 11:4557
    [Google Scholar]
  114. Yamashita I, Hayashi J, Hara M. 2004. Bio-template synthesis of uniform CdSe nanoparticles using cage-shaped protein, apoferritin. Chem. Lett. 33:91158–59
    [Google Scholar]
  115. Yang R, Gao Y, Zhou Z, Strappe P, Blanchard C. 2016a. Fabrication and characterization of ferritin-chitosan-lutein shell-core nanocomposites and lutein stability and release evaluation in vitro. RSC Adv 6:4235267–79
    [Google Scholar]
  116. Yang R, Liu Y, Blanchard C, Zhou Z. 2018a. Channel directed rutin nano-encapsulation in phytoferritin induced by guanidine hydrochloride. Food Chem 240:935–39
    [Google Scholar]
  117. Yang R, Liu Y, Gao Y, Wang Y, Blanchard C, Zhou Z. 2017a. Ferritin glycosylated by chitosan as a novel EGCG nano-carrier: structure, stability, and absorption analysis. Int. J. Biol. Macromol. 105:252–61
    [Google Scholar]
  118. Yang R, Liu Y, Meng D, Blanchard CL, Zhou Z. 2018b. Alcalase enzymolysis of red bean (adzuki) ferritin achieves nanoencapsulation of food nutrients in a mild condition. J. Agric. Food Chem. 66:81999–2007
    [Google Scholar]
  119. Yang R, Liu Y, Meng D, Chen Z, Blanchard CL, Zhou Z. 2017b. Urea-driven epigallocatechin gallate (EGCG) permeation into the ferritin cage, an innovative method for fabrication of protein-polyphenol co-assemblies. J. Agric. Food Chem. 65:71410–19
    [Google Scholar]
  120. Yang R, Liu Y, Meng D, Wang D, Blanchard CL, Zhou Z. 2018c. Effect of atmospheric cold plasma on structure, activity, and reversible assembly of the phytoferritin. Food Chem 264:41–48
    [Google Scholar]
  121. Yang R, Sun G, Zhang M, Zhou Z, Li Q et al. 2016b. Epigallocatechin gallate (EGCG) decorating soybean seed ferritin as a rutin nanocarrier with prolonged release property in the gastrointestinal tract. Plant Food Hum. Nutr. 71:3277–85
    [Google Scholar]
  122. Yang R, Tian J, Liu Y, Yang Z, Wu D, Zhou Z. 2017c. Thermally induced encapsulation of food nutrients into phytoferritin through the flexible channels without additives. J. Agric. Food Chem. 65:469950–55
    [Google Scholar]
  123. Yang R, Tian J, Wang D, Blanchard C, Zhou Z. 2018d. Chitosan binding onto the epigallocatechin-loaded ferritin nanocage enhances its transport across caco-2 cells. Food Funct 9:42015–24
    [Google Scholar]
  124. Yang R, Zhou Z, Sun G, Gao Y, Xu J. 2015. Ferritin, a novel vehicle for iron supplementation and food nutritional factors encapsulation. Trends Food Sci. Technol. 44:2189–200
    [Google Scholar]
  125. Yang X, Chen-Barrett Y, Arosio P, Chasteen ND. 1998. Reaction paths of iron oxidation and hydrolysis in horse spleen and recombinant human ferritins. Biochemistry 37:279743–50
    [Google Scholar]
  126. Yang Z, Wang X, Diao H, Zhang J, Li H et al. 2007. Encapsulation of platinum anticancer drugs by apoferritin. Chem. Commun. 33:3453–55
    [Google Scholar]
  127. Yildiz G, Andrade J, Engeseth NE, Feng H. 2017. Functionalizing soy protein nano-aggregates with pH-shifting and mano-thermo-sonication. J. Colloid Interface Sci. 505:836–46
    [Google Scholar]
  128. Yun S, Zhang T, Li M, Chen B, Zhao G 2011. Proanthocyanidins inhibit iron absorption from soybean (Glycine max) seed ferritin in rats with iron deficiency anemia. Plant Food Hum. Nutr. 66:3212–17
    [Google Scholar]
  129. Zang J, Chen H, Zhang X, Zhang C, Guo J et al. 2019. Disulfide-mediated conversion of 8-mer bowl-like protein architecture into three different nanocages. Nat. Commun. 10:778
    [Google Scholar]
  130. Zang J, Chen H, Zhao G, Wang F, Ren F 2017. Ferritin cage for encapsulation and delivery of bioactive nutrients: from structure, property to applications. Crit. Rev. Food Sci. Nutr. 57:173673–83
    [Google Scholar]
  131. Zhang C, Tan X, Lv C, Zang J, Zhao G. 2021. Shrimp ferritin greatly improves the physical and chemical stability of astaxanthin. J. Food Sci. 86:125295–306
    [Google Scholar]
  132. Zhang C, Zhang X, Zhao G. 2020. Ferritin nanocage: a versatile nanocarrier utilized in the field of food, nutrition, and medicine. Nanomaterials 10:91894
    [Google Scholar]
  133. Zhang S, Zang J, Wang W, Chen H, Zhang X et al. 2016a. Conversion of the native 24-mer ferritin nanocage into its non-native 16-mer analogue by insertion of extra amino acid residues. Angew. Chem. Int. Ed. 55:5216064–70
    [Google Scholar]
  134. Zhang S, Zang J, Zhang X, Chen H, Mikami B, Zhao G. 2016b.. “ Silent” amino acid residues at key subunit interfaces regulate the geometry of protein nanocages. ACS Nano 10:1110382–88
    [Google Scholar]
  135. Zhang T, Lv C, Chen L, Bai G, Zhao G, Xu C. 2014. Encapsulation of anthocyanin molecules within a ferritin nanocage increases their stability and cell uptake efficiency. Food Res. Int. 62:183–92
    [Google Scholar]
  136. Zhang T, Lv C, Yun S, Liao X, Zhao G, Leng X. 2012. Effect of high hydrostatic pressure (HHP) on structure and activity of phytoferritin. Food Chem 130:2273–78
    [Google Scholar]
  137. Zhang X, Zang J, Chen H, Zhou K, Zhang T et al. 2019. Thermostability of protein nanocages: the effect of natural extra peptide on the exterior surface. RSC Adv 9:4324777–82
    [Google Scholar]
  138. Zhang Y, Dong Y, Li X, Wang F 2019. Proanthocyanidin encapsulated in ferritin enhances its cellular absorption and antioxidant activity. J. Agric. Food Chem. 67:4111498–507
    [Google Scholar]
  139. Zhao G. 2010. Phytoferritin and its implications for human health and nutrition. Biochim. Biophys. Acta 1800:8815–23
    [Google Scholar]
  140. Zhao G, Bou-Abdallah F, Arosio P, Levi S, Janus-Chandler C, Chasteen ND 2003. Multiple pathways for mineral core formation in mammalian apoferritin. The role of hydrogen peroxide. Biochemistry 42:103142–50
    [Google Scholar]
  141. Zhao G, Su M, Chasteen ND. 2005. μ-1,2-Peroxo diferric complex formation in horse spleen ferritin. A mixed H/L-subunit heteropolymer. J. Mol. Biol. 352:2467–77
    [Google Scholar]
  142. Zhou B, Wan J, Wang J, Cao X 2012. Effect of chaotropes in reverse micellar extraction of kallikrein. Process Biochem 47:2229–33
    [Google Scholar]
/content/journals/10.1146/annurev-food-060721-024902
Loading
/content/journals/10.1146/annurev-food-060721-024902
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error