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Moving metal ions through ferritin-protein nanocages from three-fold pores to catalytic sites.

Tosha T, Ng HL, Bhattasali O, Alber T, Theil EC
J Am Chem Soc 132 14562-9 (2010)
Related entries: 3ka3, 3ka6, 3ka8

Cited: 57 times
EuropePMC logo PMID: 20866049

Abstract

Ferritin nanocages synthesize ferric oxide minerals, containing hundreds to thousands of Fe(III) diferric oxo/hydroxo complexes, by reactions of Fe(II) ions with O(2) at multiple di-iron catalytic centers. Ferric-oxy multimers, tetramers, and/or larger mineral nuclei form during postcatalytic transit through the protein cage, and mineral accretion occurs in the central cavity. We determined how Fe(II) substrates can access catalytic sites using frog M ferritins, active and inactivated by ligand substitution, crystallized with 2.0 M Mg(II) ± 0.1 M Co(II) for Co(II)-selective sites. Co(II) inhibited Fe(II) oxidation. High-resolution (<1.5 Å) crystal structures show (1) a line of metal ions, 15 Å long, which penetrates the cage and defines ion channels and internal pores to the nanocavity that link external pores to the cage interior, (2) metal ions near negatively charged residues at the channel exits and along the inner cavity surface that model Fe(II) transit to active sites, and (3) alternate side-chain conformations, absent in ferritins with catalysis eliminated by amino acid substitution, which support current models of protein dynamics and explain changes in Fe-Fe distances observed during catalysis. The new structural data identify a ∼27-Å path Fe(II) ions can follow through ferritin entry channels between external pores and the central cavity and along the cavity surface to the active sites where mineral synthesis begins. This "bucket brigade" for Fe(II) ion access to the ferritin catalytic sites not only increases understanding of biological nanomineral synthesis but also reveals unexpected design principles for protein cage-based catalysts and nanomaterials.

Reviews - 3ka4 mentioned but not cited (2)

  1. Ferritin: the protein nanocage and iron biomineral in health and in disease. Theil EC. Inorg Chem 52 12223-12233 (2013)
  2. Ferritin: A Promising Nanoreactor and Nanocarrier for Bionanotechnology. Mohanty A, Parida A, Raut RK, Behera RK. ACS Bio Med Chem Au 2 258-281 (2022)

Articles - 3ka4 mentioned but not cited (6)

  1. Ferritins for Chemistry and for Life. Theil EC, Behera RK, Tosha T. Coord Chem Rev 257 579-586 (2013)
  2. Moving metal ions through ferritin-protein nanocages from three-fold pores to catalytic sites. Tosha T, Ng HL, Bhattasali O, Alber T, Theil EC. J Am Chem Soc 132 14562-14569 (2010)
  3. Ferritin protein nanocages-the story. Theil EC. Nanotechnol Percept 8 7-16 (2012)
  4. Fe(2+) substrate transport through ferritin protein cage ion channels influences enzyme activity and biomineralization. Behera RK, Torres R, Tosha T, Bradley JM, Goulding CW, Theil EC. J Biol Inorg Chem 20 957-969 (2015)
  5. Spectroscopic studies of single and double variants of M ferritin: lack of conversion of a biferrous substrate site into a cofactor site for O2 activation. Kwak Y, Schwartz JK, Haldar S, Behera RK, Tosha T, Theil EC, Solomon EI. Biochemistry 53 473-482 (2014)
  6. ASAXS measurements on ferritin and apoferritin at the bioSAXS beamline P12 (PETRA III, DESY). Wieland DCF, Schroer MA, Gruzinov AY, Blanchet CE, Jeffries CM, Svergun DI. J Appl Crystallogr 54 830-838 (2021)


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  1. The significance of ferritin in cancer: anti-oxidation, inflammation and tumorigenesis. Alkhateeb AA, Connor JR. Biochim Biophys Acta 1836 245-254 (2013)
  2. Iron, Ferritin, Hereditary Ferritinopathy, and Neurodegeneration. Muhoberac BB, Vidal R. Front Neurosci 13 1195 (2019)
  3. Ferritins: furnishing proteins with iron. Bradley JM, Le Brun NE, Moore GR. J Biol Inorg Chem 21 13-28 (2016)
  4. Protein cage assembly across multiple length scales. Aumiller WM, Uchida M, Douglas T. Chem Soc Rev 47 3433-3469 (2018)
  5. Mechanisms of iron mineralization in ferritins: one size does not fit all. Bradley JM, Moore GR, Le Brun NE. J Biol Inorg Chem 19 775-785 (2014)
  6. Diversity of Fe2+ entry and oxidation in ferritins. Bradley JM, Moore GR, Le Brun NE. Curr Opin Chem Biol 37 122-128 (2017)
  7. Biochemistry of mammalian ferritins in the regulation of cellular iron homeostasis and oxidative responses. Zhang J, Chen X, Hong J, Tang A, Liu Y, Xie N, Nie G, Yan X, Liang M. Sci China Life Sci 64 352-362 (2021)
  8. Physiological origin of biogenic magnetic nanoparticles in health and disease: from bacteria to humans. Gorobets O, Gorobets S, Koralewski M. Int J Nanomedicine 12 4371-4395 (2017)
  9. Plasmonics for the study of metal ion-protein interactions. Grasso G, Spoto G. Anal Bioanal Chem 405 1833-1843 (2013)

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  1. Serum ferritin is an important inflammatory disease marker, as it is mainly a leakage product from damaged cells. Kell DB, Pretorius E. Metallomics 6 748-773 (2014)
  2. The catalytic center of ferritin regulates iron storage via Fe(II)-Fe(III) displacement. Honarmand Ebrahimi K, Bill E, Hagedoorn PL, Hagen WR. Nat Chem Biol 8 941-948 (2012)
  3. Structural insights into the ferroxidase site of ferritins from higher eukaryotes. Bertini I, Lalli D, Mangani S, Pozzi C, Rosa C, Theil EC, Turano P. J Am Chem Soc 134 6169-6176 (2012)
  4. Moving Fe2+ from ferritin ion channels to catalytic OH centers depends on conserved protein cage carboxylates. Behera RK, Theil EC. Proc Natl Acad Sci U S A 111 7925-7930 (2014)
  5. Observation of gold sub-nanocluster nucleation within a crystalline protein cage. Maity B, Abe S, Ueno T. Nat Commun 8 14820 (2017)
  6. Ferritin protein nanocage ion channels: gating by N-terminal extensions. Tosha T, Behera RK, Ng HL, Bhattasali O, Alber T, Theil EC. J Biol Chem 287 13016-13025 (2012)
  7. Ferritin structure from Mycobacterium tuberculosis: comparative study with homologues identifies extended C-terminus involved in ferroxidase activity. Khare G, Gupta V, Nangpal P, Gupta RK, Sauter NK, Tyagi AK. PLoS One 6 e18570 (2011)
  8. Moving Iron through ferritin protein nanocages depends on residues throughout each four α-helix bundle subunit. Haldar S, Bevers LE, Tosha T, Theil EC. J Biol Chem 286 25620-25627 (2011)
  9. A conserved tyrosine in ferritin is a molecular capacitor. Ebrahimi KH, Hagedoorn PL, Hagen WR. Chembiochem 14 1123-1133 (2013)
  10. A new approach to the ferritin iron core growth: influence of the H/L ratio on the core shape. López-Castro JD, Delgado JJ, Perez-Omil JA, Gálvez N, Cuesta R, Watt RK, Domínguez-Vera JM. Dalton Trans 41 1320-1324 (2012)
  11. Receptor-mediated cellular uptake of nanoparticles: a switchable delivery system. Zhang L, Fischer W, Pippel E, Hause G, Brandsch M, Knez M. Small 7 1538-1541 (2011)
  12. The role of nonconserved residues of Archaeoglobus fulgidus ferritin on its unique structure and biophysical properties. Sana B, Johnson E, Le Magueres P, Criswell A, Cascio D, Lim S. J Biol Chem 288 32663-32672 (2013)
  13. Metal binding sites of human H-chain ferritin and iron transport mechanism to the ferroxidase sites: a molecular dynamics simulation study. Laghaei R, Evans DG, Coalson RD. Proteins 81 1042-1050 (2013)
  14. Recycling of kinesin-1 motors by diffusion after transport. Blasius TL, Reed N, Slepchenko BM, Verhey KJ. PLoS One 8 e76081 (2013)
  15. Ferritin ion channel disorder inhibits Fe(II)/O2 reactivity at distant sites. Tosha T, Behera RK, Theil EC. Inorg Chem 51 11406-11411 (2012)
  16. Concerted motions networking pores and distant ferroxidase centers enable bacterioferritin function and iron traffic. Yao H, Rui H, Kumar R, Eshelman K, Lovell S, Battaile KP, Im W, Rivera M. Biochemistry 54 1611-1627 (2015)
  17. Metal Chelation Assisted In Situ Migration and Functionalization of Catalysts on Peapod-Like Hollow SnO2 toward a Superior Chemical Sensor. Jang JS, Yu S, Choi SJ, Kim SJ, Koo WT, Kim ID. Small 12 5989-5997 (2016)
  18. Iron binding at specific sites within the octameric HbpS protects streptomycetes from iron-mediated oxidative stress. Wedderhoff I, Kursula I, Groves MR, Ortiz de Orué Lucana D. PLoS One 8 e71579 (2013)
  19. Labile iron potentiates ascorbate-dependent reduction and mobilization of ferritin iron. Badu-Boateng C, Pardalaki S, Wolf C, Lajnef S, Peyrot F, Naftalin RJ. Free Radic Biol Med 108 94-109 (2017)
  20. Local packing modulates diversity of iron pathways and cooperative behavior in eukaryotic and prokaryotic ferritins. Ruvinsky AM, Vakser IA, Rivera M. J Chem Phys 140 115104 (2014)
  21. The extension peptide of plant ferritin from sea lettuce contributes to shell stability and surface hydrophobicity. Masuda T, Morimoto S, Mikami B, Toyohara H. Protein Sci 21 786-796 (2012)
  22. The first crystal structure of crustacean ferritin that is a hybrid type of H and L ferritin. Masuda T, Zang J, Zhao G, Mikami B. Protein Sci 27 1955-1960 (2018)
  23. Tuning, inhibiting and restoring the enzyme mimetic activities of Pt-apoferritin. Carmona U, Zhang L, Li L, Münchgesang W, Pippel E, Knez M. Chem Commun (Camb) 50 701-703 (2014)
  24. Experimental and theoretical evaluation of multisite cadmium(II) exchange in designed three-stranded coiled-coil peptides. Chakraborty S, Iranzo O, Zuiderweg ER, Pecoraro VL. J Am Chem Soc 134 6191-6203 (2012)
  25. Pore structure controls stability and molecular flux in engineered protein cages. Adamson LSR, Tasneem N, Andreas MP, Close W, Jenner EN, Szyszka TN, Young R, Cheah LC, Norman A, MacDermott-Opeskin HI, O'Mara ML, Sainsbury F, Giessen TW, Lau YH. Sci Adv 8 eabl7346 (2022)
  26. Structural comparison of two ferritins from the marine invertebrate Phascolosoma esculenta. Ming T, Huan H, Su C, Huo C, Wu Y, Jiang Q, Qiu X, Lu C, Zhou J, Li Y, Su X. FEBS Open Bio 11 793-803 (2021)
  27. Coordinating subdomains of ferritin protein cages with catalysis and biomineralization viewed from the C4 cage axes. Theil EC, Turano P, Ghini V, Allegrozzi M, Bernacchioni C. J Biol Inorg Chem 19 615-622 (2014)
  28. Coordination design of cadmium ions at the 4-fold axis channel of the apo-ferritin cage. Abe S, Ito N, Maity B, Lu C, Lu D, Ueno T. Dalton Trans 48 9759-9764 (2019)
  29. Ferroxidase Activity in Eukaryotic Ferritin is Controlled by Accessory-Iron-Binding Sites in the Catalytic Cavity. Bernacchioni C, Pozzi C, Di Pisa F, Mangani S, Turano P. Chemistry 22 16213-16219 (2016)
  30. article-commentary Metalloenzymes: Cage redesign explains assembly. Theil EC, Turano P. Nat Chem Biol 9 143-144 (2013)
  31. Ferritin iron mineralization proceeds by different mechanisms in MOPS and imidazole buffers. Snow CL, Martineau LN, Hilton RJ, Brown S, Farrer J, Boerio-Goates J, Woodfield BF, Watt RK. J Inorg Biochem 105 972-977 (2011)
  32. Flavin-mediated reductive iron mobilization from frog M and Mycobacterial ferritins: impact of their size, charge and reactivities with NADH/O2. Koochana PK, Mohanty A, Parida A, Behera N, Behera PM, Dixit A, Behera RK. J Biol Inorg Chem 26 265-281 (2021)
  33. Interaction of Th(IV), Pu(IV) and Fe(III) with ferritin protein: how similar? Zurita C, Tsushima S, Solari PL, Jeanson A, Creff G, Den Auwer C. J Synchrotron Radiat 29 45-52 (2022)
  34. Iron sulfur clusters in protein nanocages for photocatalytic hydrogen generation in acidic aqueous solutions. Chen W, Li S, Li X, Zhang C, Hu X, Zhu F, Shen G, Feng F. Chem Sci 10 2179-2185 (2019)
  35. Cryo-EM structures and functional characterization of homo- and heteropolymers of human ferritin variants. Irimia-Dominguez J, Sun C, Li K, Muhoberac BB, Hallinan GI, Garringer HJ, Ghetti B, Jiang W, Vidal R. Sci Rep 10 20666 (2020)
  36. Design of a gold clustering site in an engineered apo-ferritin cage. Lu C, Maity B, Peng X, Ito N, Abe S, Sheng X, Ueno T, Lu D. Commun Chem 5 39 (2022)
  37. Structural Insights Into the Effects of Interactions With Iron and Copper Ions on Ferritin From the Blood Clam Tegillarca granosa. Ming T, Jiang Q, Huo C, Huan H, Wu Y, Su C, Qiu X, Lu C, Zhou J, Li Y, Han J, Zhang Z, Su X. Front Mol Biosci 9 800008 (2022)
  38. Bacterioferritin nanocage structures uncover the biomineralization process in ferritins. Jobichen C, Ying Chong T, Rattinam R, Basak S, Srinivasan M, Choong YK, Pandey KP, Ngoc TB, Shi J, Angayarkanni J, Sivaraman J. PNAS Nexus 2 pgad235 (2023)
  39. Optical Monitoring of In Situ Iron Loading into Single, Native Ferritin Proteins. Yousefi A, Ying C, Parmenter CDJ, Assadipapari M, Sanderson G, Zheng Z, Xu L, Zargarbashi S, Hickman GJ, Cousins RB, Mellor CJ, Mayer M, Rahmani M. Nano Lett 23 3251-3258 (2023)
  40. Structural and Biochemical Characterization of Silver/Copper Binding by Dendrorhynchus zhejiangensis Ferritin. Huo C, Ming T, Wu Y, Huan H, Qiu X, Lu C, Li Y, Zhang Z, Han J, Su X. Polymers (Basel) 15 1297 (2023)


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