|
|
Bioengineering Application of Ferritin |
Ling WANG,Yang WU,Sheng ZHANG,Hao QI() |
Key Laboratory of Systems Bioengineering of Ministry of Education, SynBio Research Platform, Collaborative Innovation Center of Chemical Science and Engineering,School of Chemical Engineering and Technology,Tianjin University,Tianjin 300072,China |
|
|
Abstract Widely conserved iron-storage protein plays crucial role in ferric ion metabolism maintaining iron homeostasis, resisting oxidative stress and eliminating other toxic effects of excessive metal ions. With gaining the knowledge from structural and molecular studies, iron-storage protein complex in which iron cluster formed from absorbing free iron has been successfully applied in fields of biomedical engineering, nanomaterial, and biomolecule imaging. Herein, the recent progresses in studying the catalytic mechanism of iron cluster formation are briefly introduced. And the cutting-edge bioengineering applications in which iron-storage protein were engineered as a versatile molecular scaffold for presenting special chemicals, or natural magnetic particle for constructing remote control molecular machine are reviewed, although related researches has arisen academic argument.
|
Received: 29 January 2018
Published: 06 July 2018
|
|
Corresponding Authors:
Hao QI
E-mail: haoq@tju.edu.cn
|
|
|
[1] |
Laufberger V . Sur la cristallisation de la Ferritin. Soc Chim Biol, 1937,19:1575-1582.
|
|
|
[2] |
Crichton R R . Structure and function of Ferritin. Angewandte Chemie International Edition, 1973,12(1):57-65.
doi: 10.1002/anie.197300571
pmid: 4631281
|
|
|
[3] |
Meldrum F C, Heywood B R, Mann S . MagnetoFerritin: in vitro synthesis of a novel magnetic protein. Science, 1992,257(5069):522-524.
doi: 10.1126/science.1636086
pmid: 1636086
|
|
|
[4] |
Wong K K W, Douglas T, Gider S , et al. Biomimetic synthesis and characterization of magnetic proteins (magnetoFerritin). Chemistry of Materials, 1998,10(1):279-285.
doi: 10.1021/cm970421o
|
|
|
[5] |
Liu X, Lopez P A, Giessen T W , et al. Engineering genetically-encoded mineralization and magnetism via directed evolution. Scientific Reports, 2016,6:38019.
doi: 10.1038/srep38019
pmid: 27897245
|
|
|
[6] |
Theil E C . Ferritin: the protein nanocage and iron biomineral in health and in disease. Inorganic Chemistry, 2013,52(21):12223-12233.
doi: 10.1021/ic400484n
pmid: 3882016
|
|
|
[7] |
Bernacchioni C, Ghini V, Pozzi C , et al. Loop electrostatics modulates the intersubunit interactions in Ferritin. ACS Chemical Biology, 2014,9(11):2517-2525.
doi: 10.1021/cb500431r
pmid: 25148224
|
|
|
[8] |
Giorgi A, Mignogna G, Bellapadrona G , et al. The unusual co-assembly of H-and M-chains in the ferritin molecule from the Antarctic teleosts Trematomus bernacchii and Trematomus newnesi. Archives of Biochemistry and Biophysics, 2008,478(1):69-74.
doi: 10.1016/j.abb.2008.06.022
pmid: 18625196
|
|
|
[9] |
Morrissey J, Bowler C . Iron utilization in marine cyanobacteria and eukaryotic algae. Frontiers in Microbiology, 2012,3:43.
doi: 10.3389/fmicb.2012.00043
pmid: 3296057
|
|
|
[10] |
Rahmanpour R , Bugg T D H . Assembly in vitro of Rhodococcus jostii RHA1 encapsulin and peroxidase DypB to form a nanocompartment. The FEBS Journal, 2013,280(9):2097-2104.
doi: 10.1111/febs.12234
pmid: 23560779
|
|
|
[11] |
Rahmanpour R , Bugg T D H . Characterisation of Dyp-type peroxidases from Pseudomonas fluorescens Pf-5: oxidation of Mn (II) and polymeric lignin by Dyp1B. Archives of Biochemistry and Biophysics, 2015,574:93-98.
doi: 10.1016/j.abb.2014.12.022
pmid: 25558792
|
|
|
[12] |
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.
doi: 10.1016/j.tibs.2015.11.011
pmid: 26719091
|
|
|
[13] |
Bradley J M , Le Brun N E, Moore G R . Ferritins: furnishing proteins with iron. Journal of Biological Inorganic Chemistry, 2016,21(1):13-28.
doi: 10.1007/s00775-016-1336-0
pmid: 26825805
|
|
|
[14] |
Ghirlando R, Mutskova R, Schwartz C . Enrichment and characterization of Ferritin for nanomaterial applications. Nanotechnology, 2015,27(4):045102.
doi: 10.1088/0957-4484/27/4/045102
pmid: 26656976
|
|
|
[15] |
He D, Marles-Wright J . Ferritin family proteins and their use in bionanotechnology. New Biotechnology, 2015,32(6):651-657.
doi: 10.1016/j.nbt.2014.12.006
pmid: 4571993
|
|
|
[16] |
Arosio P, Elia L, Poli M . Ferritin, cellular iron storage and regulation. IUBMB Life, 2017,69(6):414-422.
doi: 10.1002/iub.1621
pmid: 28349628
|
|
|
[17] |
Jutz G, van Rijn P, Santos Miranda B , et al. Ferritin: a versatile building block for bionanotechnology. Chemical Reviews, 2015,115(4):1653-1701.
doi: 10.1021/cr400011b
pmid: 25683244
|
|
|
[18] |
Honarmand Ebrahimi K, Hagedoorn P L, Hagen W R . Unity in the biochemistry of the iron-storage proteins Ferritin and bacterioFerritin. Chemical Reviews, 2014,115(1):295-326.
doi: 10.1021/cr5004908
pmid: 25418839
|
|
|
[19] |
杨彩云, 曹长乾, 蔡垚 , 等. 铁蛋白表面修饰及其应用. 化学进展, 2015,28(1):91-102.
|
|
|
[19] |
Yang C Y, Cao C Q, Cai Y , et al. Surface modification and application of iron protein. Progress in Chemistry, 2015,28(1):91-102.
|
|
|
[20] |
McHugh C A, Fontana J, Nemecek D , et al. A virus capsid‐like nanocompartment that stores iron and protects bacteria from oxidative stress. The EMBO Journal, 2014,33(17):1896-1911.
doi: 10.15252/embj.201488566
pmid: 25024436
|
|
|
[21] |
Theil E C . Ferritin protein nanocages use ion channels, catalytic sites, and nucleation channels to manage iron/oxygen chemistry. Current Opinion in Chemical Biology, 2011,15(2):304-311.
doi: 10.1016/j.cbpa.2011.01.004
pmid: 21296609
|
|
|
[22] |
Zeth K . Dps biomineralizing proteins: Multifunctional architects of nature. Biochemical Journal, 2012,445(3):297-311.
doi: 10.1042/BJ20120514
pmid: 22788214
|
|
|
[23] |
Arosio P, Ingrassia R, Cavadini P . Ferritins: A family of molecules for iron storage, antioxidation and more. Biochimica et Biophysica Acta (BBA)-General Subjects, 2009,1790(7):589-599.
doi: 10.1016/j.bbagen.2008.09.004
pmid: 18929623
|
|
|
[24] |
Park S, You X, Imlay J A . Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx-mutants of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 2005,102(26):9317-9322.
doi: 10.1073/pnas.0502051102
pmid: 15967999
|
|
|
[25] |
Chiancone E, Ceci P . The multifaceted capacity of Dps proteins to combat bacterial stress conditions: detoxification of iron and hydrogen peroxide and DNA binding. Biochimica et Biophysica Acta (BBA)-General Subjects, 2010,1800(8):798-805.
doi: 10.1016/j.bbagen.2010.01.013
pmid: 20138126
|
|
|
[26] |
Burgess A W, Johansen P M . Assault: patterns of emergency visits. Journal of Psychiatric Nursing and Mental Health Services, 1976,14(11):32-36.
|
|
|
[27] |
Ullrich S, Schüler D . Cre-lox-based method for generation of large deletions within the genomic magnetosome island of Magnetospirillum gryphiswaldense. Applied and Environmental Microbiology, 2010,76(8):2439-2444.
doi: 10.1128/AEM.02805-09
pmid: 2849187
|
|
|
[28] |
Granick S, Michaelis L. Ferritin II . ApoFerritin of horse spleen. Journal of Biological Chemistry, 1943,147(1):91-97.
|
|
|
[29] |
Bradley J M , Le Brun N E, Moore G R . Ferritins: furnishing proteins with iron. Journal of Biological Inorganic Chemistry, 2016,21(1):13-28.
doi: 10.1007/s00775-016-1336-0
pmid: 26825805
|
|
|
[30] |
Tatur J, Hagen W R, Matias P M . Crystal structure of the Ferritin from the hyperthermophilic archaeal anaerobe Pyrococcus furiosus. Journal of Biological Inorganic Chemistry, 2007,12(5):615-630.
doi: 10.1007/s00775-007-0212-3
pmid: 1915633
|
|
|
[31] |
Treffry A, Zhao Z, Quail M A , et al. How the presence of three iron binding sites affects the iron storage function of the Ferritin (EcFtnA) of Escherichia coli. FEBS letters, 1998,432(3):213-218.
doi: 10.1016/S0014-5793(98)00867-9
pmid: 9720927
|
|
|
[32] |
Tatur J, Hagen W R . The dinuclear iron‐oxo ferroxidase center of Pyrococcus furiosus Ferritin is a stable prosthetic group with unexpectedly high reduction potentials. FEBS letters, 2005,579(21):4729-4732.
doi: 10.1016/j.febslet.2005.07.045
pmid: 16107254
|
|
|
[33] |
Ebrahimi K H, Hagedoorn P L, Jongejan J A , et al. Catalysis of iron core formation in Pyrococcus furiosus Ferritin. Journal of Biological Inorganic Chemistry, 2009,14(8):1265.
doi: 10.1007/s00775-009-0571-z
pmid: 2771142
|
|
|
[34] |
Stillman T J, Hempstead P D, Artymiuk P J , et al. The high-resolution X-ray crystallographic structure of the Ferritin (EcFtnA) of Escherichia coli; comparison with human H Ferritin (HuHF) and the structures of the Fe 3+ and Zn 2+ derivatives . Journal of Molecular Biology, 2001,307(2):587-603.
doi: 10.1006/jmbi.2001.4475
|
|
|
[35] |
Yao H, Jepkorir G, Lovell S , et al. Two distinct Ferritin-like molecules in Pseudomonas aeruginosa: the product of the bfrA gene is a bacterial Ferritin (FtnA) and not a bacterioFerritin (Bfr). Biochemistry, 2011,50(23):5236-5248.
doi: 10.1021/bi2004119
pmid: 3130351
|
|
|
[36] |
Ebrahimi K H, Bill E, Hagedoorn P L , et al. The catalytic center of Ferritin regulates iron storage via Fe (II)-Fe (III) displacement. Nature Chemical Biology, 2012,8(11):941-948.
doi: 10.1038/nchembio.1071
pmid: 23001032
|
|
|
[37] |
Maity B, Abe S, Ueno T . Observation of gold sub-nanocluster nucleation within a crystalline protein cage. Nature Communications, 2017,8:14820.
doi: 10.1038/ncomms14820
pmid: 5357307
|
|
|
[38] |
Zhang Y, Fu J, Chee S Y , et al. Rational disruption of the oligomerization of the mini‐Ferritin E. coli DPS through protein‐protein interface mutation. Protein Science, 2011,20(11):1907-1917.
doi: 10.1002/pro.731
pmid: 21898653
|
|
|
[39] |
Gryzik M, Srivastava A, Longhi G , et al. Expression and characterization of the Ferritin binding domain of Nuclear Receptor Coactivator-4 (NCOA4). Biochimica et Biophysica Acta (BBA)-General Subjects, 2017,1861(11):2710-2716.
doi: 10.1016/j.bbagen.2017.07.015
pmid: 28754384
|
|
|
[40] |
Zhang Y, Zhou J, Ardejani M S , et al. Designability of aromatic interaction networks at E. coli BacterioFerritin B-Type Channels. Molecules, 2017,22(12):2184.
doi: 10.3390/molecules22122184
pmid: 29292762
|
|
|
[41] |
Liu X, Lopez P A, Giessen T W , et al. Engineering genetically-encoded mineralization and magnetism via directed evolution. Scientific Reports, 2016,6:38019.
doi: 10.1038/srep38019
pmid: 27897245
|
|
|
[42] |
Matsumoto Y, Chen R, Anikeeva P , et al. Engineering intracellular biomineralization and biosensing by a magnetic protein. Nature Communications, 2015,6:8721.
doi: 10.1038/ncomms9721
pmid: 4667635
|
|
|
[43] |
Uchida M, Kang S, Reichhardt C , et al. The Ferritin superfamily: Supramolecular templates for materials synthesis. Biochimica et Biophysica Acta (BBA)-General Subjects, 2010,1800(8):834-845.
|
|
|
[44] |
Kishida Y, Olsen B R, Berg R A , et al. Two improved methods for preparing Ferritin-protein conjugates for electron microscopy. The Journal of Cell Biology, 1975,64(2):331-339.
doi: 10.1083/jcb.64.2.331
pmid: 803973
|
|
|
[45] |
Hainfeld J F . Uranium-loaded apoferritin with antibodies attached: molecular design for uranium neutron-capture therapy. Proceedings of the National Academy of Sciences, 1992,89(22):11064-11068.
doi: 10.1073/pnas.89.22.11064
pmid: 1438316
|
|
|
[46] |
Tang Z, Wu H, Zhang Y , et al. Enzyme-mimic activity of ferric nano-core residing in Ferritin and its biosensing applications. Analytical Chemistry, 2011,83(22):8611-8616.
doi: 10.1021/ac202049q
pmid: 21910434
|
|
|
[47] |
Vannucci L, Falvo E, Fornara M , et al. Selective targeting of melanoma by PEG-masked protein-based multifunctional nanoparticles. International Journal of Nanomedicine, 2012,7:1489.
doi: 10.2147/IJN.S28242
pmid: 3356193
|
|
|
[48] |
Matsumura S, Aoki I, Saga T , et al. A tumor-environment-responsive nanocarrier that evolves its surface properties upon sensing matrix metalloproteinase-2 and initiates agglomeration to enhance T2 relaxivity for magnetic resonance imaging. Molecular Pharmaceutics, 2011,8(5):1970-1974.
doi: 10.1021/mp2001999
|
|
|
[49] |
Kim S, Kim G S, Seo J , et al. Double-chambered Ferritin platform: dual-function payloads of cytotoxic peptides and fluorescent protein. Biomacromolecules, 2015,17(1):12-19.
doi: 10.1021/acs.biomac.5b01134
pmid: 26646195
|
|
|
[50] |
Zhen Z, Tang W, Chen H , et al. RGD-modified apoFerritin nanoparticles for efficient drug delivery to tumors. ACS Nano, 2013,7(6):4830-4837.
doi: 10.1021/nn305791q
pmid: 3705644
|
|
|
[51] |
Ducasse R, Wang W A , Navarro M G J , et al. Programmed self-assembly of a biochemical and magnetic scaffold to trigger and manipulate microtubule structures. Scientific Reports, 2017,7:11344.
doi: 10.1038/s41598-017-10297-y
pmid: 28900114
|
|
|
[52] |
Radoul M, Lewin L, Cohen B , et al. Genetic manipulation of iron biomineralization enhances MR relaxivity in a Ferritin-M6A chimeric complex. Scientific Reports, 2016,6:26550.
doi: 10.1038/srep26550
|
|
|
[53] |
Wang Q, Mercogliano C P, Löwe J . A Ferritin-based label for cellular electron cryotomography. Structure, 2011,19(2):147-154.
doi: 10.1016/j.str.2010.12.002
pmid: 21300284
|
|
|
[54] |
Meister M . Physical limits to magnetogenetics. Elife, 2016,5:e17210.
doi: 10.7554/eLife.17210
pmid: 27529126
|
|
|
[55] |
Stanley S A, Gagner J E, Damanpour S , et al. Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice. Science, 2012,336(6081):604-608.
doi: 10.4161/cib.21148
pmid: 2255625720
|
|
|
[56] |
Stanley S A, Sauer J, Kane R S , et al. Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nature Medicine, 2015,21(1):92-98.
doi: 10.1038/nm.3730
pmid: 25501906
|
|
|
[57] |
Qin S, Yin H, Yang C , et al. A magnetic protein biocompass. Nature Materials, 2016,15(2):217.
doi: 10.1038/nmat4484
pmid: 26569474
|
|
|
[58] |
Cyranoski D . Compass protein attracts heap of criticism. Nature, 2017,544(7648):16.
doi: 10.1038/544016a
pmid: 28383006
|
|
|
[59] |
Damiani V, Falvo E, Fracasso G , et al. Therapeutic efficacy of the novel stimuli-sensitive nano-ferritins containing doxorubicin in a head and neck cancer model. International Journal of Molecular Sciences, 2017,18(7):1555.
doi: 10.3390/ijms18071555
pmid: 28718812
|
|
|
[60] |
Mazzucchelli S, Truffi M, Baccarini F , et al. H-Ferritin-nanocaged olaparib: a promising choice for both BRCA-mutated and sporadic triple negative breast cancer. Scientific Reports, 2017,7(1):7505.
doi: 10.1038/s41598-017-07617-7
pmid: 5548799
|
|
|
[61] |
Suci P A, Kang S, Young M , et al. A streptavidin-protein cage janus particle for polarized targeting and modular functionalization. Journal of the American Chemical Society, 2009,131(26):9164-9165.
doi: 10.1021/ja9035187
pmid: 19522495
|
|
|
[62] |
Williams S M, Chandran A V, Prakash S , et al. A mutation directs the structural switch of DNA binding proteins under starvation to a Ferritin-like protein cage. Structure, 2017.
doi: 10.1016/j.str.2017.07.006
pmid: 28823472
|
|
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|