Functional ferritin nanoparticles for biomedical applications
Functional ferritin nanoparticles for biomedical applications
Ferritin, a major iron storage protein with a hollow interior cavity, has been reported recently to play many important roles in biomedical and bioengineering applications. Owing to the unique architecture and surface properties, ferritin nanoparticles offer favorable characteristics and can be either genetically or chemically modified to impart functionalities to their surfaces, and therapeutics or probes can be encapsulated in their interiors by controlled and reversible assembly/disassembly. There has been an outburst of interest regarding the employment of functional ferritin nanoparticles in nanomedicine. This review will highlight the recent advances in ferritin nanoparticles for drug delivery, bioassay, and molecular imaging with a particular focus on their biomedical applications.
nanomedicine / ferritin / drug delivery / bioassay / molecular imaging
[1] |
Worwood M, Cook J D. Serum ferritin. Critical Reviews in Clinical Laboratory Sciences, 1979, 10(2): 171–204
CrossRef
ADS
Google scholar
|
[2] |
Meldrum F C, Heywood B R, Mann S. Magnetoferritin: In vitro synthesis of a novel magnetic protein. Science, 1992, 257(5069): 522–523
CrossRef
ADS
Google scholar
|
[3] |
Zeth K, Hoiczyk E, Okuda M. Ferroxidase-mediated iron oxide biomineralization: Novel pathways to multifunctional nanoparticles. Trends in Biochemical Sciences, 2016, 41(2): 190–203
CrossRef
ADS
Google scholar
|
[4] |
Chasteen N D, Harrison P M. Mineralization in ferritin: An efficient means of iron storage. Journal of Structural Biology, 1999, 126(3): 182–194
CrossRef
ADS
Google scholar
|
[5] |
Uchida M, Kang S, Reichhardt C, Harlen K, Douglas T. The ferritin superfamily: Supramolecular templates for materials synthesis. Biochimica et Biophysica Acta, 2010, 1800(8): 834–845
CrossRef
ADS
Google scholar
|
[6] |
Bulte J W, Douglas T, Mann S, Frankel R B, Moskowitz B M, Brooks R A, Baumgarner C D, Vymazal J, Strub M P, Frank J A. Magnetoferritin: Characterization of a novel superparamagnetic MR contrast agent. Journal of Magnetic Resonance Imaging, 1994, 4(3): 497–505
CrossRef
ADS
Google scholar
|
[7] |
Uchida M, Flenniken M L, Allen M, Willits D A, Crowley B E, Brumfield S, Willis A F, Jackiw L, Jutila M, Young M J, Douglas T. Targeting of cancer cells with ferrimagnetic ferritin cage nanoparticles. Journal of the American Chemical Society, 2006, 128(51): 16626–16633
CrossRef
ADS
Google scholar
|
[8] |
Okuda M, Iwahori K, Yamashita I, Yoshimura H. Fabrication of nickel and chromium nanoparticles using the protein cage of apoferritin. Biotechnology and Bioengineering, 2003, 84(2): 187–194
CrossRef
ADS
Google scholar
|
[9] |
Galvez N, Sanchez P, Dominguez-Vera J M. Preparation of Cu and CuFe prussian blue derivative nanoparticles using the apoferritin cavity as nanoreactor. Dalton Transactions (Cambridge, England), 2005, 15(15): 2492–2494
CrossRef
ADS
Google scholar
|
[10] |
Jeong G H, Yamazaki A, Suzuki S, Yoshimura H, Kobayashi Y, Homma Y. Cobalt-filled apoferritin for suspended single-walled carbon nanotube growth with narrow diameter distribution. Journal of the American Chemical Society, 2005, 127(23): 8238–8239
CrossRef
ADS
Google scholar
|
[11] |
Fan R, Chew S W, Cheong V V, Orner B P. Fabrication of gold nanoparticles inside unmodified horse spleen apoferritin. Small, 2010, 6(14): 1483–1487
CrossRef
ADS
Google scholar
|
[12] |
Zhen Z, Tang W, Chen H, Lin X, Todd T, Wang G, Cowger T, Chen X, Xie J. RGD-modified apoferritin nanoparticles for efficient drug delivery to tumors. ACS Nano, 2013, 7(6): 4830–4837
CrossRef
ADS
Google scholar
|
[13] |
Zhen Z, Tang W, Guo C, Chen H, Lin X, Liu G, Fei B, Chen X, Xu B, Xie J. Ferritin nanocages to encapsulate and deliver photosensitizers for efficient photodynamic therapy against cancer. ACS Nano, 2013, 7(8): 6988–6996
CrossRef
ADS
Google scholar
|
[14] |
Tian Y, Yan X, Saha M L, Niu Z, Stang P J. Hierarchical self-assembly of responsive organoplatinum(ii) metallacycle-TMV complexes with turn-on fluorescence. Journal of the American Chemical Society, 2016, 138(37): 12033–12036
CrossRef
ADS
Google scholar
|
[15] |
Harrison P M, Arosio P. The ferritins: Molecular properties, iron storage function and cellular regulation. Biochimica et Biophysica Acta, 1996, 1275(3): 161–203
CrossRef
ADS
Google scholar
|
[16] |
Lin X, Xie J, Niu G, Zhang F, Gao H, Yang M, Quan Q, Aronova M A, Zhang G, Lee S, et al. Chimeric ferritin nanocages for multiple function loading and multimodal imaging. Nano Letters, 2011, 11(2): 814–819
CrossRef
ADS
Google scholar
|
[17] |
Yamashita I, Iwahori K, Kumagai S. Ferritin in the field of nanodevices. Biochimica et Biophysica Acta, 2010, 1800(8): 846–857
CrossRef
ADS
Google scholar
|
[18] |
Jolley C C, Uchida M, Reichhardt C, Harrington R, Kang S, Klem M T, Parise J B, Douglas T. Size and crystallinity in protein-templated inorganic nanoparticles. Chemistry of Materials, 2010, 22(16): 4612–4618
CrossRef
ADS
Google scholar
|
[19] |
Zhang L, Swift J, Butts C A, Yerubandi V, Dmochowski I J. Structure and activity of apoferritin-stabilized gold nanoparticles. Journal of Inorganic Biochemistry, 2007, 101(11-12): 1719–1729
CrossRef
ADS
Google scholar
|
[20] |
Rother M, Nussbaumer M G, Renggli K, Bruns N. Protein cages and synthetic polymers: A fruitful symbiosis for drug delivery applications, bionanotechnology and materials science. Chemical Society Reviews, 2016, 45(22): 6213–6249
CrossRef
ADS
Google scholar
|
[21] |
Ghirlando R, Mutskova R, Schwartz C. Enrichment and characterization of ferritin for nanomaterial applications. Nanotechnology, 2016, 27(4): 045102
CrossRef
ADS
Google scholar
|
[22] |
Konijn A, Meyron-Holtz E, Levy R, Ben-Bassat H, Matzner Y. Specific binding of placental acidic isoferritin to cells of the T-cell line HD-MAR. FEBS Letters, 1990, 263(2): 229–232
CrossRef
ADS
Google scholar
|
[23] |
Bretscher M S, Thomson J N. Distribution of ferritin receptors and coated pits on giant Hela cells. EMBO Journal, 1983, 2(4): 599–603
|
[24] |
Lei Y, Hamada Y, Li J, Cong L, Wang N, Li Y, Zheng W, Jiang X. Targeted tumor delivery and controlled release of neuronal drugs with ferritin nanoparticles to regulate pancreatic cancer progression. Journal of Controlled Release, 2016, 232: 131–142
CrossRef
ADS
Google scholar
|
[25] |
Zhao Y, Liang M, Li X, Fan K, Xiao J, Li Y, Shi H, Wang F, Choi H S, Cheng D, et al. Bioengineered magnetoferritin nanoprobes for single-dose nuclear-magnetic resonance tumor imaging. ACS Nano, 2016, 10(4): 4184–4191
CrossRef
ADS
Google scholar
|
[26] |
Adams P C, Powell L W, Halliday J W. Isolation of a human hepatic ferritin receptor. Hepatology (Baltimore, MD.), 1988, 8(4): 719–721
CrossRef
ADS
Google scholar
|
[27] |
Chen X. Multimodality imaging of tumor integrin alphavbeta3 expression. Mini-Reviews in Medicinal Chemistry, 2006, 6(2): 227–233
CrossRef
ADS
Google scholar
|
[28] |
Liu Y, Wang Z, Zhang H, Lang L, Ma Y, He Q, Lu N, Huang P, Song J, Liu Z, et al. A photothermally responsive nanoprobe for bioimaging based on edman degradation. Nanoscale, 2016, 8(20): 10553–10557
CrossRef
ADS
Google scholar
|
[29] |
Kitagawa T, Kosuge H, Uchida M, Dua M M, Iida Y, Dalman R L, Douglas T, McConnell M V. Rgd-conjugated human ferritin nanoparticles for imaging vascular inflammation and angiogenesis in experimental carotid and aortic disease. Molecular Imaging & Biology, 2012, 14(3): 315–324
CrossRef
ADS
Google scholar
|
[30] |
Choi H S, Nasr K, Alyabyev S, Feith D, Lee J H, Kim S H, Ashitate Y, Hyun H, Patonay G, Strekowski L, et al. Synthesis and in vivo fate of zwitterionic near—infrared fluorophores. Angewandte Chemie International Edition, 2011, 50(28): 6258–6263
CrossRef
ADS
Google scholar
|
[31] |
Agostinis P, Berg K, Cengel K A, Foster T H, Girotti A W, Gollnick S O, Hahn S M, Hamblin M R, Juzeniene A, Kessel D, et al. Photodynamic therapy of cancer: An update. CA: a Cancer Journal for Clinicians, 2011, 61(4): 250–281
CrossRef
ADS
Google scholar
|
[32] |
Ochsner M. Photophysical and photobiological processes in the photodynamic therapy of tumours. Journal of Photochemistry and Photobiology. B, Biology, 1997, 39(1): 1–18
CrossRef
ADS
Google scholar
|
[33] |
Brown S B, Brown E A, Walker I. The present and future role of photodynamic therapy in cancer treatment. Lancet Oncology, 2004, 5(8): 497–508
CrossRef
ADS
Google scholar
|
[34] |
Cairnduff F, Stringer M R, Hudson E J, Ash D V, Brown S B. Superficial photodynamic therapy with topical 5-aminolaevulinic acid for superficial primary and secondary skin cancer. British Journal of Cancer, 1994, 69(3): 605–608
CrossRef
ADS
Google scholar
|
[35] |
Falvo E, Tremante E, Fraioli R, Leonetti C, Zamparelli C, Boffi A, Morea V, Ceci P, Giacomini P. Antibody-drug conjugates: Targeting melanoma with cisplatin encapsulated in protein-cage nanoparticles based on human ferritin. Nanoscale, 2013, 5(24): 12278–12285
CrossRef
ADS
Google scholar
|
[36] |
MacKie R. Melanoma prevention and early detection. British Medical Bulletin, 1995, 51(3): 570–583
|
[37] |
Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA: a Cancer Journal for Clinicians, 2012, 62(1): 10–29
CrossRef
ADS
Google scholar
|
[38] |
Greenlee R T, Murray T, Bolden S, Wingo P A. Cancer statistics, 2000. CA: a Cancer Journal for Clinicians, 2000, 50(1): 7–33
CrossRef
ADS
Google scholar
|
[39] |
Rigel D S, Carucci J A. Malignant melanoma: Prevention, early detection, and treatment in the 21st century. CA: a Cancer Journal for Clinicians, 2000, 50(4): 215–236
CrossRef
ADS
Google scholar
|
[40] |
Morgenstern D A, Asher R A, Fawcett J W. Chondroitin sulphate proteoglycans in the CNS injury response. Progress in Brain Research, 2002, 137: 313–332
CrossRef
ADS
Google scholar
|
[41] |
Eisenmann K M, McCarthy J B, Simpson M A, Keely P J, Guan J L, Tachibana K, Lim L, Manser E, Furcht L T, Iida J. Melanoma chondroitin sulphate proteoglycan regulates cell spreading through Cdc42, Ack-1 and p130cas. Nature Cell Biology, 1999, 1(8): 507–513
CrossRef
ADS
Google scholar
|
[42] |
Thon N, Haas C A, Rauch U, Merten T, Fässler R, Frotscher M, Deller T. The chondroitin sulphate proteoglycan brevican is upregulated by astrocytes after entorhinal cortex lesions in adult rats. European Journal of Neuroscience, 2000, 12(7): 2547–2558
CrossRef
ADS
Google scholar
|
[43] |
Levine J, Nishiyama A. The NG2 chondroitin sulfate proteoglycan: A multifunctional proteoglycan associated with immature cells. Perspectives on Developmental Neurobiology, 1996, 3(4): 245–259
|
[44] |
Oohira A, Matsui F, Watanabe E, Kushima Y, Maeda N. Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody LG2 in the rat cerebrum. Neuroscience, 1994, 60(1): 145–157
CrossRef
ADS
Google scholar
|
[45] |
Levine J M, Stallcup W B. Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. Journal of Neuroscience, 1987, 7(9): 2721–2731
|
[46] |
Maeda H, Wu J, Sawa T, Matsumura Y, Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: A review. Journal of Controlled Release, 2000, 65(1): 271–284
CrossRef
ADS
Google scholar
|
[47] |
Mamo T, Poland G A. Nanovaccinology: The next generation of vaccines meets 21st century materials science and engineering. Vaccine, 2012, 30(47): 6609–6611
CrossRef
ADS
Google scholar
|
[48] |
des Rieux A, Fievez V, Garinot M, Schneider Y J, Préat V. Nanoparticles as potential oral delivery systems of proteins and vaccines: A mechanistic approach. Journal of Controlled Release, 2006, 116(1): 1–27
CrossRef
ADS
Google scholar
|
[49] |
Singh M, Chakrapani A, O’Hagan D. Nanoparticles and microparticles as vaccine-delivery systems. Expert Review of Vaccines, 2007, 6(5): 797–808
CrossRef
ADS
Google scholar
|
[50] |
Oyewumi M O, Kumar A, Cui Z. Nano-microparticles as immune adjuvants: Correlating particle sizes and the resultant immune responses. Expert Review of Vaccines, 2010, 9(9): 1095–1107
CrossRef
ADS
Google scholar
|
[51] |
Zhao L, Seth A, Wibowo N, Zhao C X, Mitter N, Yu C, Middelberg A P. Nanoparticle vaccines. Vaccine, 2014, 32(3): 327–337
CrossRef
ADS
Google scholar
|
[52] |
Zhao K, Chen G, Shi X, Gao T, Li W, Zhao Y, Zhang F, Wu J, Cui X, Wang Y F. Preparation and efficacy of a live newcastle disease virus vaccine encapsulated in chitosan nanoparticles. PLoS One, 2012, 7(12): e53314
CrossRef
ADS
Google scholar
|
[53] |
Borges O, Cordeiro-da-Silva A, Tavares J, Santarém N, de Sousa A, Borchard G, Junginger H E. Immune response by nasal delivery of hepatitis B surface antigen and codelivery of a CpG ODN in alginate coated chitosan nanoparticles. European Journal of Pharmaceutics and Biopharmaceutics, 2008, 69(2): 405–416
CrossRef
ADS
Google scholar
|
[54] |
Nochi T, Yuki Y, Takahashi H, Sawada S, Mejima M, Kohda T, Harada N, Kong I G, Sato A, Kataoka N, et al. Nanogel antigenic protein-delivery system for adjuvant-free intranasal vaccines. Nature Materials, 2010, 9(7): 572–578
CrossRef
ADS
Google scholar
|
[55] |
Stone J W, Thornburg N J, Blum D L, Kuhn S J, Wright D W, Crowe J E Jr. Gold nanorod vaccine for respiratory syncytial virus. Nanotechnology, 2013, 24(29): 295102
CrossRef
ADS
Google scholar
|
[56] |
Wang T, Zou M, Jiang H, Ji Z, Gao P, Cheng G. Synthesis of a novel kind of carbon nanoparticle with large mesopores and macropores and its application as an oral vaccine adjuvant. European Journal of Pharmaceutical Sciences, 2011, 44(5): 653–659
CrossRef
ADS
Google scholar
|
[57] |
Glück R, Moser C, Metcalfe I C. Influenza virosomes as an efficient system for adjuvanted vaccine delivery. Expert Opinion on Biological Therapy, 2004, 4(7): 1139–1145
CrossRef
ADS
Google scholar
|
[58] |
Zhu F C, Zhang J, Zhang X F, Zhou C, Wang Z Z, Huang S J, Wang H, Yang C L, Jiang H M, Cai J P, et al. Efficacy and safety of a recombinant hepatitise vaccine in healthy adults: A large-scale, randomised, double-blind placebo-controlled, phase 3 trial. Lancet, 2010, 376(9744): 895–902
CrossRef
ADS
Google scholar
|
[59] |
Sliepen K, Ozorowski G, Burger J A, van Montfort T, Stunnenberg M, LaBranche C, Montefiori D C, Moore J P, Ward A B, Sanders R W. Presenting native-like HIV-1 envelope trimers on ferritin nanoparticles improves their immunogenicity. Retrovirology, 2015, 12(82): 15–21
|
[60] |
Champion C I, Kickhoefer V A, Liu G, Moniz R J, Freed A S, Bergmann L L, Vaccari D, Raval-Fernandes S, Chan A M, Rome L H, Kelly K A. A vault nanoparticle vaccine induces protective mucosal immunity. PLoS One, 2009, 4(4): e5409
CrossRef
ADS
Google scholar
|
[61] |
Kanekiyo M, Wei C J, Yassine H M, McTamney P M, Boyington J C, Whittle J R, Rao S S, Kong W P, Wang L, Nabel G J. Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature, 2013, 499(7456): 102–106
CrossRef
ADS
Google scholar
|
[62] |
Cho K J, Shin H J, Lee J H, Kim K J, Park S S, Lee Y, Lee C, Park S S, Kim K H. The crystal structure of ferritin from helicobacter pylori reveals unusual conformational changes for iron uptake. Journal of Molecular Biology, 2009, 390(1): 83–98
CrossRef
ADS
Google scholar
|
[63] |
Steinman R M. Decisions about dendritic cells: Past, present, and future. Annual Review of Immunology, 2012, 30(1): 1–22
CrossRef
ADS
Google scholar
|
[64] |
Gilboa E. DC-based cancer vaccines. Journal of Clinical Investigation, 2007, 117(5): 1195–1203
CrossRef
ADS
Google scholar
|
[65] |
Aarntzen E, Figdor C, Adema G, Punt C, De Vries I. Dendritic cell vaccination and immune monitoring. Cancer Immunology, Immunotherapy, 2008, 57(10): 1559–1568
CrossRef
ADS
Google scholar
|
[66] |
Han J A, Kang Y J, Shin C, Ra J S, Shin H H, Hong S Y, Do Y, Kang S. Ferritin protein cage nanoparticles as versatile antigen delivery nanoplatforms for dendritic cell (DC)-based vaccine development. Nanomedicine; Nanotechnology, Biology, and Medicine, 2013, 10(3): 561–569
CrossRef
ADS
Google scholar
|
[67] |
Shimonkevitz R, Colon S, Kappler J W, Marrack P, Grey H M. Antigen recognition by H-2-restricted T cells. II. A tryptic ovalbumin peptide that substitutes for processed antigen. Journal of Immunology (Baltimore, MD: 1950), 1984, 133(4): 2067–2074
|
[68] |
Liu D, Wang Z, Jin A, Huang X, Sun X, Wang F, Yan Q, Ge S, Xia N, Niu G, Liu G, Hight Walker A R, Chen X. Acetylcholinesterase—catalyzed hydrolysis allows ultrasensitive detection of pathogens with the naked eye. Angewandte Chemie International Edition in English, 2013, 52(52): 14065–14069
CrossRef
ADS
Google scholar
|
[69] |
Lee S H, Lee H, Park J S, Choi H, Han K Y, Seo H S, Ahn K Y, Han S S, Cho Y, Lee K H, et al. A novel approach to ultrasensitive diagnosis using supramolecular protein nanoparticles. FASEB Journal, 2007, 21(7): 1324–1334
CrossRef
ADS
Google scholar
|
[70] |
Abbaspour A, Noori A. Electrochemical detection of individual single nucleotide polymorphisms using monobase-modified apoferritin-encapsulated nanoparticles. Biosensors & Bioelectronics, 2012, 37(1): 11–18
CrossRef
ADS
Google scholar
|
[71] |
Tang Z, Wu H, Zhang Y, Li Z, Lin Y. Enzyme-mimic activity of ferric nano-core residing in ferritin and its biosensing applications. Analytical Chemistry, 2011, 83(22): 8611–8616
CrossRef
ADS
Google scholar
|
[72] |
Men D, Zhang T T, Hou L W, Zhou J, Zhang Z P, Shi Y Y, Zhang J L, Cui Z Q, Deng J Y, Wang D B, et al. Self-assembly of ferritin nanoparticles into an enzyme nanocomposite with tunable size for ultrasensitive immunoassay. ACS Nano, 2015, 9(11): 10852–10860
CrossRef
ADS
Google scholar
|
[73] |
Liu G, Wang J, Wu H, Lin Y. Versatile apoferritin nanoparticle labels for assay of protein. Analytical Chemistry, 2006, 78(21): 7417–7423
CrossRef
ADS
Google scholar
|
[74] |
Liu G, Wu H, Wang J, Lin Y. Apoferritin-templated synthesis of metal phosphate nanoparticle labels for electrochemical immunoassay. Small, 2006, 2(10): 1139–1143
CrossRef
ADS
Google scholar
|
[75] |
Beutler B, Cerami A. Cachectin and tumour necrosis factor as two sides of the same biological coin. Nature, 1986, 320(6063): 584–588
CrossRef
ADS
Google scholar
|
[76] |
Scuderi P, Lam K, Ryan K, Petersen E, Sterling K, Finley P, Ray C G, Slymen D, Salmon S. Raised serum levels of tumour necrosis factor in parasitic infections. Lancet, 1986, 328(8520): 1364–1365
CrossRef
ADS
Google scholar
|
[77] |
Yu F, Li G, Qu B, Cao W. Electrochemical detection of DNA hybridization based on signal DNA probe modified with Au and apoferritin nanoparticles. Biosensors & Bioelectronics, 2010, 26(3): 1114–1117
CrossRef
ADS
Google scholar
|
[78] |
Li L, Fang C J, Ryan J C, Niemi E C, Lebrón J A, Björkman P J, Arase H, Torti F M, Torti S V, Nakamura M C, et al. Binding and uptake of H-ferritin are mediated by human transferrin receptor-1. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(8): 3505–3510
CrossRef
ADS
Google scholar
|
[79] |
Fan K, Cao C, Pan Y, Lu D, Yang D, Feng J, Song L, Liang M, Yan X. Magnetoferritin nanoparticles for targeting and visualizing tumour tissues. Nature Nanotechnology, 2012, 7(7): 459–464
CrossRef
ADS
Google scholar
|
[80] |
Lee E J, Ahn K Y, Lee J H, Park J S, Song J A, Sim S J, Lee E B, Cha Y J, Lee J. A novel bioassay platform using ferritin-based nanoprobe hydrogel. Advanced Materials, 2012, 24(35): 4739–4744
CrossRef
ADS
Google scholar
|
[81] |
Zhao J, Liu M, Zhang Y, Li H, Lin Y, Yao S. Apoferritin protein nanoparticles dually-labeled with aptamer and HRP as a sensing probe for thrombin detection. Analytica Chimica Acta, 2012, 1(759): 53–60
|
[82] |
John A, Tuszynski G. The role of matrix metalloproteinases in tumor angiogenesis and tumor metastasis. Pathology Oncology Research, 2001, 7(1): 14–23
CrossRef
ADS
Google scholar
|
[83] |
Stetler-Stevenson W G, Aznavoorian S, Liotta L A. Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annual Review of Cell Biology, 1993, 9(1): 541–573
CrossRef
ADS
Google scholar
|
[84] |
Malemud C J. Matrix metalloproteinases (MMPs) in health and disease: An overview. Frontiers in Bioscience: A Journal and Virtual Library, 2006, 11: 1696
|
[85] |
Lin X, Xie J, Zhu L, Lee S, Niu G, Ma Y, Kim K, Chen X. Hybrid ferritin nanoparticles as activatable probes for tumor imaging. Angewandte Chemie International Edition in English, 2011, 50(7): 1569–1572
CrossRef
ADS
Google scholar
|
[86] |
Zhu L, Ma Y, Kiesewetter D O, Wang Y, Lang L, Lee S, Niu G, Chen X. Rational design of matrix metalloproteinase-13 activatable probes for enhanced specificity. ACS Chemical Biology, 2013, 9(2): 510–516
CrossRef
ADS
Google scholar
|
[87] |
Zhu L, Xie J, Swierczewska M, Zhang F, Quan Q, Ma Y, Fang X, Kim K, Lee S, Chen X. Real-time video imaging of protease expression in vivo. Theranostics, 2011, 1: 18–27
CrossRef
ADS
Google scholar
|
[88] |
Wang J, Zhang L, Chen M, Gao S, Zhu L. Activatable ferritin nanocomplex for real-time monitoring of caspase-3 activation during photodynamic therapy. ACS Applied Materials & Interfaces, 2015, 7(41): 23248–23256
CrossRef
ADS
Google scholar
|
[89] |
Choi S H, Na H B, Park Y I, An K, Kwon S G, Jang Y, Park M H, Moon J, Son J S, Song I C, et al. Simple and generalized synthesis of oxide-metal heterostructured nanoparticles and their applications in multimodal biomedical probes. Journal of the American Chemical Society, 2008, 130(46): 15573–15580
CrossRef
ADS
Google scholar
|
[90] |
Wang H, Cao F, De A, Cao Y, Contag C, Gambhir S S, Wu J C, Chen X. Trafficking mesenchymal stem cell engraftment and differentiation in tumor-bearing mice by bioluminescence imaging. Stem Cells (Dayton, OH), 2009, 27(7): 1548–1558
CrossRef
ADS
Google scholar
|
[91] |
Xu C, Yuan Z, Kohler N, Kim J, Chung M A, Sun S. Fept nanoparticles as an Fe reservoir for controlled Fe release and tumor inhibition. Journal of the American Chemical Society, 2009, 131(42): 15346–15351
CrossRef
ADS
Google scholar
|
[92] |
Bhirde A, Xie J, Swierczewska M, Chen X. Nanoparticles for cell labeling. Nanoscale, 2011, 3(1): 142–153
CrossRef
ADS
Google scholar
|
[93] |
Terashima M, Uchida M, Kosuge H, Tsao P S, Young M J, Conolly S M, Douglas T, McConnell M V. Human ferritin cages for imaging vascular macrophages. Biomaterials, 2011, 32(5): 1430–1437
CrossRef
ADS
Google scholar
|
[94] |
Mills P H, Ahrens E T. Theoretical MRI contrast model for exogenous T2 agents. Magnetic Resonance in Medicine, 2007, 57(2): 442–447
CrossRef
ADS
Google scholar
|
[95] |
Charlton J R, Pearl V M, Denotti A R, Lee J B, Swaminathan S, Scindia Y M, Charlton N P, Baldelomar E J, Beeman S C, Bennett K M. Biocompatibility of ferritin-based nanoparticles as targeted mri contrast agents. Nanomedicine; Nanotechnology, Biology, and Medicine, 2016, 12(6): 1735–1745
CrossRef
ADS
Google scholar
|
[96] |
Domínguez-Vera J M, Fernandez B, Galvez N. Native and synthetic ferritins for nanobiomedical applications: Recent advances and new perspectives. Future Medicinal Chemistry, 2010, 2(4): 609–618
CrossRef
ADS
Google scholar
|
[97] |
Maraloiu V A, Appaix F, Broisat A, Le Guellec D, Teodorescu V S, Ghezzi C, van der Sanden B, Blanchin M G. Multiscale investigation of uspio nanoparticles in atherosclerotic plaques and their catabolism and storage in vivo. Nanomedicine; Nanotechnology, Biology, and Medicine, 2016, 12(1): 191–200
CrossRef
ADS
Google scholar
|
[98] |
Xie H, Cheng Y C, Kokeny P, Liu S, Hsieh C Y, Haacke E M, Palihawadana Arachchige M, Lawes G. A quantitative study of susceptibility and additional frequency shift of three common materials in MRI. Magnetic Resonance in Medicine, 2016, 76(4): 1263–1269
CrossRef
ADS
Google scholar
|
[99] |
Choi S H, Cho H R, Kim H S, Kim Y H, Kang K W, Kim H, Moon W K. Imaging and quantification of metastatic melanoma cells in lymph nodes with a ferritin MR reporter in living mice. NMR in Biomedicine, 2012, 25(5): 737–745
CrossRef
ADS
Google scholar
|
[100] |
Fan K, Gao L, Yan X. Human ferritin for tumor detection and therapy. Wiley Interdisciplinary Reviews. Nanomedicine and Nanobiotechnology, 2013, 5(4): 287–298
CrossRef
ADS
Google scholar
|
[101] |
Schenck J F, Zimmerman E A. High-field magnetic resonance imaging of brain iron: Birth of a biomarker? NMR in Biomedicine, 2004, 17(7): 433–445
CrossRef
ADS
Google scholar
|
[102] |
Christoforidis A, Haritandi A, Tsitouridis I, Tsatra I, Tsantali H, Karyda S, Dimitriadis A S, Athanassiou-Metaxa M. Correlative study of iron accumulation in liver, myocardium, and pituitary assessed with MRI in young thalassemic patients. Journal of Pediatric Hematology/Oncology, 2006, 28(5): 311–315
CrossRef
ADS
Google scholar
|
[103] |
Bartzokis G, Cummings J L, Markham C H, Marmarelis P Z, Treciokas L J, Tishler T A, Marder S R, Mintz J. MRI evaluation of brain iron in earlier-and later-onset Parkinson’s disease and normal subjects. Magnetic Resonance Imaging, 1999, 17(2): 213–222
CrossRef
ADS
Google scholar
|
[104] |
Bartzokis G, Tishler T. MRI evaluation of basal ganglia ferritin iron and neurotoxicity in Alzheimer’s and Huntingon’s disease. Cellular and Molecular Biology, 2000, 46(4): 821–833
|
[105] |
Bennett K M, Zhou H, Sumner J P, Dodd S J, Bouraoud N, Doi K, Star R A, Koretsky A P. MRI of the basement membrane using charged nanoparticles as contrast agents. Magnetic Resonance in Medicine, 2008, 60(3): 564–574
CrossRef
ADS
Google scholar
|
[106] |
Kim J W, Choi S H, Lillehei P T, Chu S H, King G C, Watt G D. Cobalt oxide hollow nanoparticles derived by bio-templating. Chemical Communications, 2005, (32): 4101–4103
CrossRef
ADS
Google scholar
|
[107] |
Deng Q Y, Yang B, Wang J F, Whiteley C G, Wang X N. Biological synthesis of platinum nanoparticles with apoferritin. Biotechnology Letters, 2009, 31(10): 1505–1509
CrossRef
ADS
Google scholar
|
[108] |
Sun C, Yang H, Yuan Y, Tian X, Wang L, Guo Y, Xu L, Lei J, Gao N, Anderson G J, et al. Controlling assembly of paired gold clusters within apoferritin nanoreactor for in vivo kidney targeting and biomedical imaging. Journal of the American Chemical Society, 2011, 133(22): 8617–8624
CrossRef
ADS
Google scholar
|
[109] |
Uchida M, Terashima M, Cunningham C H, Suzuki Y, Willits D A, Willis A F, Yang P C, Tsao P S, McConnell M V, Young M J, et al. A human ferritin iron oxide nano-composite magnetic resonance contrast agent. Magnetic Resonance in Medicine, 2008, 60(5): 1073–1081
CrossRef
ADS
Google scholar
|
[110] |
Jezierska A, Motyl T. Matrix metalloproteinase-2 involvement in breast cancer progression: A mini-review. Medical Science Monitor, 2009, 15(2): RA32–40
|
[111] |
Ravanti L, Kähäri V. Matrix metalloproteinases in wound repair. International Journal of Molecular Medicine, 2000, 6(4): 391–798
|
[112] |
Matsumura S, Aoki I, Saga T, Shiba K. A tumor-environment-responsive nanocarrier that evolves its surface properties upon sensing matrix metalloproteinase-2 and initiates agglomeration to enhance t(2) relaxivity for magnetic resonance imaging. Molecular Pharmaceutics, 2011, 8(5): 1970–1974
CrossRef
ADS
Google scholar
|
[113] |
Makino A, Harada H, Okada T, Kimura H, Amano H, Saji H, Hiraoka M, Kimura S. Effective encapsulation of a new cationic gadolinium chelate into apoferritin and its evaluation as an MRI contrast agent. Nanomedicine; Nanotechnology, Biology, and Medicine, 2011, 7(5): 638–646
CrossRef
ADS
Google scholar
|
[114] |
Sanchez P, Valero E, Galvez N, Dominguez-Vera J M, Marinone M, Poletti G, Corti M, Lascialfari A. MRI relaxation properties of water-soluble apoferritin-encapsulated gadolinium oxide-hydroxide nanoparticles. Dalton Transactions (Cambridge, England), 2009, (5): 800–804
CrossRef
ADS
Google scholar
|
[115] |
Lee S, Chen X. Dual-modality probes for in vivo molecular imaging. Molecular Imaging, 2009, 8(2): 87–100
|
[116] |
Cai W, Chen X. Multimodality molecular imaging of tumor angiogenesis. Journal of Nuclear Medicine, 2008, 49(Suppl 2): 113S–128S
CrossRef
ADS
Google scholar
|
[117] |
Cai W, Niu G, Chen X. Multimodality imaging of the HER-kinase axis in cancer. European Journal of Nuclear Medicine and Molecular Imaging, 2008, 35(1): 186–208
CrossRef
ADS
Google scholar
|
[118] |
Wang Z, Huang P, Jacobson O, Wang Z, Liu Y, Lin L, Lin J, Lu N, Zhang H, Tian R, et al. Biomineralization-inspired synthesis of copper sulfide-ferritin nanocages as cancer theranostics. ACS Nano, 2016, 10(3): 3453–3460
CrossRef
ADS
Google scholar
|
[119] |
Xu G, Zhao L, He Z. Performance of whole-body pet/ct for the detection of distant malignancies in various cancers: A systematic review and meta-analysis. Journal of Nuclear Medicine, 2012, 53(12): 1847–1854
CrossRef
ADS
Google scholar
|
[120] |
Ford E C, Herman J, Yorke E, Wahl R L. 18F-FDG PET/CT for image-guided and intensity-modulated radiotherapy. Journal of Nuclear Medicine, 2009, 50(10): 1655–1665
CrossRef
ADS
Google scholar
|
[121] |
Vach W, Hoilund-Carlsen P F, Gerke O, Weber W A. Generating evidence for clinical benefit of PET/CT in diagnosing cancer patients. Journal of Nuclear Medicine, 2011, 52(Suppl 2): 77S–85S
CrossRef
ADS
Google scholar
|
[122] |
Cai W, Sam Gambhir S, Chen X. Multimodality tumor imaging targeting integrin alphavbeta3. BioTechniques, 2005, 39(6 Suppl): S14–S25
CrossRef
ADS
Google scholar
|
[123] |
Vikram D S, Zweier J L, Kuppusamy P. Methods for noninvasive imaging of tissue hypoxia. Antioxidants & Redox Signaling, 2007, 9(10): 1745–1756
|
[124] |
Huang P, Lin J, Li W, Rong P, Wang Z, Wang S, Wang X, Sun X, Aronova M, Niu G, et al. Biodegradable gold nanovesicles with an ultrastrong plasmonic coupling effect for photoacoustic imaging and photothermal therapy. Angewandte Chemie International Edition, 2013, 52(52): 13958–13964
CrossRef
ADS
Google scholar
|
[125] |
Yang M, Fan Q, Zhang R, Cheng K, Yan J, Pan D, Ma X, Lu A, Cheng Z. Dragon fruit-like biocage as an iron trapping nanoplatform for high efficiency targeted cancer multimodality imaging. Biomaterials, 2015, 69: 30–37
CrossRef
ADS
Google scholar
|
[126] |
Vannucci L, Falvo E, Failla C M, Carbo M, Fornara M, Canese R, Cecchetti S, Rajsiglova L, Stakheev D, Krizan J, et al. In vivo targeting of cutaneous melanoma using an melanoma stimulating hormone-engineered human protein cage with fluorophore and magnetic resonance imaging tracers. Journal of Biomedical Nanotechnology, 2015, 11(1): 81–92
CrossRef
ADS
Google scholar
|
[127] |
Liang M, Fan K, Zhou M, Duan D, Zheng J, Yang D, Feng J, Yan X. H-ferritin-nanocaged doxorubicin nanoparticles specifically target and kill tumors with a single-dose injection. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(41): 14900–14905
CrossRef
ADS
Google scholar
|
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