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High-resolution X-ray structures of human apoferritin H-chain mutants correlated with their activity and metal-binding sites.

Toussaint L, Bertrand L, Hue L, Crichton RR, Declercq JP
J Mol Biol 365 440-52 (2007)
Related entries: 2cei, 2cih, 2clu, 2cn6, 2cn7, 2iu2

Cited: 48 times
EuropePMC logo PMID: 17070541

Abstract

Ferritins are a family of proteins distributed widely in nature. In bacterial, plant, and animal cells, ferritin appears to serve as a soluble, bioavailable, and non-toxic form of iron provider. Ferritins from animal sources are heteropolymers composed of two types of subunit, H and L, which differ mainly by the presence (H) or absence (L) of active ferroxidase centres. We report the crystallographic structures of four human H apoferritin variants at a resolution of up to 1.5 Angstrom. Crystal derivatives using Zn(II) as redox-stable alternative for Fe(II), allows us to characterize the different metal-binding sites. The ferroxidase centre, which is composed of sites A and B, binds metal with a preference for the A site. In addition, distinct Zn(II)-binding sites were found in the 3-fold axes, 4-fold axes and on the cavity surface near the ferroxidase centre. To study the importance of the distance of the two metal atoms in the ferroxidase centre, single and double replacement of glutamate 27 (site A) and glutamate 107 (site B), the two axial ligands, by aspartate residues have been carried out. The consequences for metal binding and the correlation with Fe(II) oxidation rates are discussed.

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Reviews citing this publication (10)

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  10. Cryo-electron Microscopy of Protein Cages. Burton-Smith RN, Murata K. Methods Mol Biol 2671 173-210 (2023)

Articles citing this publication (35)

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  5. Facilitated diffusion of iron(II) and dioxygen substrates into human H-chain ferritin. A fluorescence and absorbance study employing the ferroxidase center substitution Y34W. Bou-Abdallah F, Zhao G, Biasiotto G, Poli M, Arosio P, Chasteen ND. J Am Chem Soc 130 17801-17811 (2008)
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  9. 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)
  10. The ferritin Fe2 site at the diiron catalytic center controls the reaction with O2 in the rapid mineralization pathway. Tosha T, Hasan MR, Theil EC. Proc Natl Acad Sci U S A 105 18182-18187 (2008)
  11. Encapsulation of β-carotene within ferritin nanocages greatly increases its water-solubility and thermal stability. Chen L, Bai G, Yang R, Zang J, Zhou T, Zhao G. Food Chem 149 307-312 (2014)
  12. 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)
  13. Two novel secreted ferritins involved in immune defense of Chinese mitten crab Eriocheir sinensis. Kong P, Wang L, Zhang H, Zhou Z, Qiu L, Gai Y, Song L. Fish Shellfish Immunol 28 604-612 (2010)
  14. Catalysis of iron core formation in Pyrococcus furiosus ferritin. Honarmand Ebrahimi K, Hagedoorn PL, Jongejan JA, Hagen WR. J Biol Inorg Chem 14 1265-1274 (2009)
  15. Structural analysis of haemin demetallation by L-chain apoferritins. de Val N, Declercq JP, Lim CK, Crichton RR. J Inorg Biochem 112 77-84 (2012)
  16. 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)
  17. Ferritin variants: inspirations for rationally designing protein nanocarriers. Jin Y, He J, Fan K, Yan X. Nanoscale 11 12449-12459 (2019)
  18. Maxi- and mini-ferritins: minerals and protein nanocages. Bevers LE, Theil EC. Prog Mol Subcell Biol 52 29-47 (2011)
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  20. Structural basis of the zinc- and terbium-mediated inhibition of ferroxidase activity in Dps ferritin-like proteins. Havukainen H, Haataja S, Kauko A, Pulliainen AT, Salminen A, Haikarainen T, Finne J, Papageorgiou AC. Protein Sci 17 1513-1521 (2008)
  21. First biochemical and crystallographic characterization of a fast-performing ferritin from a marine invertebrate. De Meulenaere E, Bailey JB, Tezcan FA, Deheyn DD. Biochem J 474 4193-4206 (2017)
  22. Genome-wide comparison of ferritin family from Archaea, Bacteria, Eukarya, and Viruses: its distribution, characteristic motif, and phylogenetic relationship. Bai L, Xie T, Hu Q, Deng C, Zheng R, Chen W. Naturwissenschaften 102 64 (2015)
  23. Detection of isolated protein-bound metal ions by single-particle cryo-STEM. Elad N, Bellapadrona G, Houben L, Sagi I, Elbaum M. Proc Natl Acad Sci U S A 114 11139-11144 (2017)
  24. Iron redox pathway revealed in ferritin via electron transfer analysis. Chen P, De Meulenaere E, Deheyn DD, Bandaru PR. Sci Rep 10 4033 (2020)
  25. Purification and characterization of new phytoferritin from black bean (Phaseolus vulgaris L.) seed. Deng J, Liao X, Hu J, Leng X, Cheng J, Zhao G. J Biochem 147 679-688 (2010)
  26. 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)
  27. 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)
  28. Below 3 Å structure of apoferritin using a multipurpose TEM with a side entry cryoholder. Kayama Y, Burton-Smith RN, Song C, Terahara N, Kato T, Murata K. Sci Rep 11 8395 (2021)
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  30. Unsaturated Long-Chain Fatty Acids Are Preferred Ferritin Ligands That Enhance Iron Biomineralization. Zanzoni S, Pagano K, D'Onofrio M, Assfalg M, Ciambellotti S, Bernacchioni C, Turano P, Aime S, Ragona L, Molinari H. Chemistry 23 9879-9887 (2017)
  31. Comparative Fe and Zn K-edge X-ray absorption spectroscopic study of the ferroxidase centres of human H-chain ferritin and bacterioferritin from Desulfovibrio desulfuricans. Toussaint L, Cuypers MG, Bertrand L, Hue L, Romão CV, Saraiva LM, Teixeira M, Meyer-Klaucke W, Feiters MC, Crichton RR. J Biol Inorg Chem 14 35-49 (2009)
  32. Revelation of endogenously bound Fe(2+) ions in the crystal structure of ferritin from Escherichia coli. Thiruselvam V, Sivaraman P, Kumarevel T, Ponnuswamy MN. Biochem Biophys Res Commun 453 636-641 (2014)
  33. 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)
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