Ferritin protein nanocages use ion channels, catalytic sites, and nucleation channels to manage iron/oxygen chemistry

Current Opinion in Chemical Biology

Volumn 15, Issue 2, 2011, Pages 304-311

  Theil, Elizabeth C ^a,b  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; DNA; FERRIC ION; FERRIC OXIDE; FERRITIN; ION CHANNEL; IRON; MESSENGER RNA; NANOCAGE; NANOMATERIAL; OXIDOREDUCTASE; OXYGEN; UBIQUITIN PROTEIN LIGASE;

AMINO ACID SEQUENCE; CATALYSIS; CRYSTAL STRUCTURE; DRUG DELIVERY SYSTEM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME RELEASE; EUKARYOTE; GENETIC REGULATION; HUMAN; IRON TRANSPORT; NANOCATALYST; NONHUMAN; OXYGEN TRANSPORT; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CATALYTIC DOMAIN; FERRITINS; HUMANS; ION CHANNELS; IRON; MODELS, MOLECULAR; OXYGEN;

ANIMALIA; EUKARYOTA;

EID: 79953309867     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2011.01.004     Document Type: Review

References (58)

1. Liu X., Theil E.C. Ferritin: dynamic management of biological iron and oxygen chemistry. Acc Chem Res 2005, 38:167-175.
2. Chiancone E., Ceci P. Role of Dps (DNA-binding proteins from starved cells) aggregation on DNA. Front Biosci 2010, 15:122-131.
3. Crow A., Lawson T.L., Lewin A., Moore G.R., Le Brun N.E. Structural basis for iron mineralization by bacterioferritin. J Am Chem Soc 2009, 131:6808-6813.
4. Ilari A., Latella M.C., Ceci P., Ribacchi F., Su M., Giangiacomo L., Stefanini S., Chasteen N.D., Chiancone E. The unusual intersubunit ferroxidase center of Listeria innocua dps is required for hydrogen peroxide detoxification but not for iron uptake. A study with site-specific mutants. Biochemistry 2005, 44:5579-5587.
5. 2 substrates in reactivity of the di-iron catalytic centers. Biochemistry 2010, 49:10516-10525.
6. Touati D., Jacques M., Tardat B., Bouchard L., Despied S. Lethal oxidative damage and mutagenesis are generated by iron in delta fur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol 1995, 177:2305-2314.
7. Ferreira F., Bucchini D., Martin M.E., Levi S., Arosio P., Grandchamp B., Beaumont C. Early embryonic lethality of H ferritin gene deletion in mice. J Biol Chem 2000, 275:3021-3024.
8. Imlay J.A. Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 2008, 77:755-776.
9. Liu X., Kim K., Leighton T., Theil E.C. Paired Bacillus anthracis Dps (mini-ferritin) have different reactivities with peroxide. J Biol Chem 2006, 281:27827-27835.
10. Wrighting D.M., Andrews N.C. Iron homeostasis and erythropoiesis. Curr Top Dev Biol 2008, 82:141-167.
11. Briat J.F., Duc C., Ravet K., Gaymard F. Ferritins and iron storage in plants. Biochim Biophys Acta 2010, 1800:806-814.
12. Theil E.C., Goss D.J. Living with iron (and oxygen): questions and answers about iron homeostasis. Chem Rev 2009, 109:4568-4579.
13. Hintze K.J., Theil E.C. DNA and mRNA elements with complementary responses to hemin, antioxidant inducers, and iron control ferritin-L expression. Proc Natl Acad Sci U S A 2005, 102:15048-15052.
14. Hintze K.J., Katoh Y., Igarashi K., Theil E.C. Bach1 repression of ferritin and thioredoxin reductase1 is heme-sensitive in cells and in vitro and coordinates expression with heme oxygenase1, beta-globin, and NADP(H) quinone (oxido) reductase1. J Biol Chem 2007, 282:34365-34371.
15. 2+ sensing by iron-responsive messenger RNA:repressor complexes weakens binding. J Biol Chem 2009, 284:30122-30128.
16. Vashisht A.A., Zumbrennen K.B., Huang X., Powers D.N., Durazo A., Sun D., Bhaskaran N., Persson A., Uhlen M., Sangfelt O., et al. Control of iron homeostasis by an iron-regulated ubiquitin ligase. Science 2009, 326:718-721.
17. Salahudeen A.A., Thompson J.W., Ruiz J.C., Ma H.W., Kinch L.N., Li Q., Grishin N.V., Bruick R.K. An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science 2009, 326:722-726.
18. Rohrer J.S., Islam Q.T., Watt G.D., Sayers D.E., Theil E.C. Iron environment in ferritin with large amounts of phosphate, from Azotobacter vinelandii and horse spleen, analyzed using extended X-ray absorption fine structure (EXAFS). Biochemistry 1990, 29:259-264.
19. Mann S., Williams J.M., Treffry A., Harrison P.M. Reconstituted and native iron-cores of bacterioferritin and ferritin. J Mol Biol 1987, 198:405-416.
20. Ha Y., Theil E.C., Allewell N.M. Preliminary analysis of amphibian red cell M ferritin in a novel tetragonal unit cell. Acta Crystallogr D Biol Crystallogr 1997, 53:513-523.
21. Frenkiel-Krispin D., Minsky A. Nucleoid organization and the maintenance of DNA integrity in E. coli, B. subtilis and D. radiodurans. J Struct Biol 2006, 156:311-319.
22. Andrews S.C. The ferritin-like superfamily: evolution of the biological iron storeman from a rubrerythrin-like ancestor. Biochim Biophys Acta 2010, 1800:691-705.
23. Zhang Y., Raudah S., Teo H., Teo G.W., Fan R., Sun X., Orner B.P. Alanine-shaving mutagenesis to determine key interfacial residues governing the assembly of a nano-cage maxi-ferritin. J Biol Chem 2010, 285:12078-12086.
24. Radford R.J., Lawrenz M., Nguyen P.C., McCammon J.A., Tezcan F.A. Porous protein frameworks with unsaturated metal centers in sterically encumbered coordination sites. Chem Commun (Camb) 2010, Aug 25 [Epub ahead of print].
25. Le Brun N.E., Crow A., Murphy M.E., Mauk A.G., Moore G.R. Iron core mineralisation in prokaryotic ferritins. Biochim Biophys Acta 2010, 1800:732-744.
26. 2 in the rapid mineralization pathway. Proc Natl Acad Sci U S A 2008, 105:18182-18187.
27. Deng J., Liao X., Yang H., Zhang X., Hua Z., Masuda T., Goto F., Yoshihara T., Zhao G. Role of H-1 and H-2 subunits of soybean seed ferritin in oxidative deposition of iron in protein. J Biol Chem 2010, 285:32075-32086.
28. Arosio P., Ingrassia R., Cavadini P. Ferritins: a family of molecules for iron storage, antioxidation and more. Biochim Biophys Acta 2009, 1790:589-599.
29. Turano P., Lalli D., Felli I.C., Theil E.C., Bertini I. NMR reveals pathway for ferric mineral precursors to the central cavity of ferritin. Proc Natl Acad Sci U S A 2010, 107:545-550.
30. Chiancone E., Ceci P. The multifaceted capacity of Dps proteins to combat bacterial stress conditions: detoxification of iron and hydrogen peroxide and DNA binding. Biochim Biophys Acta 2010, 1800:798-805.
31. 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. Magn Reson Med 2008, 60:1073-1081.
32. May C.A., Grady J.K., Laue T.M., Poli M., Arosio P., Chasteen N.D. The sedimentation properties of ferritins. New insights and analysis of methods of nanoparticle preparation. Biochim Biophys Acta 2010, 1800:858-870.
33. Mann S., Williams J.M., Treffrey A., Harrison P.M. Reconstituted and native iron-cores of bacterioferritin and ferritin. J Mol Biol 1987, 198:405-416.
34. Wade V.J., Treffry A., Laulhere J.-P., Bauminger E.R., Cleton M.I., Mann S., Briat J.-F., Harrison P.M. Structure and composition of ferritin cores from pea seed (Pisum sativum). Biochim Biophys Acta 1993, 1161:91-96.
35. Waldo G.S., Wright E., Whang Z.H., Briat J.F., Theil E.C., Sayers D.E. Formation of the ferritin iron mineral occurs in plastids. Plant Physiol 1995, 109:797-802.
36. St Pierre T., Tran K.C., Webb J., Macey D.J., Heywood B.R., Sparks N.H., Wade V.J., Mann S., Pootrakul P. Organ-specific crystalline structures of ferritin cores in beta-thalassemia/hemoglobin E. Biol Met 1991, 4:162-165.
37. Tosha T., Nh H.-L., Bhatassali O., Alber T., Theil E.C. Moving metal ions through ferritin protein nanocages from the three-fold pores to catalytic sites. J Am Chem Soc 2010, 132:14562-14569.
38. Bellapadrona G., Stefanini S., Zamparelli C., Theil E.C., Chiancone E. Iron translocation into and out of Listeria innocua Dps and size distribution of the protein-enclosed nanomineral are modulated by the electrostatic gradient at the 3-fold " ferritin-like" pores. J Biol Chem 2009, 284:19101-19109.
39. Su M., Cavallo S., Stefanini S., Chiancone E., Chasteen N.D. The so-called Listeria innocua ferritin is a Dps protein. Iron incorporation, detoxification, and DNA protection properties. Biochemistry 2005, 44:5572-5578.
40. Stubbe J., Nocera D.G., Yee C.S., Chang M.C. Radical initiation in the class I ribonucleotide reductase: long-range proton-coupled electron transfer?. Chem Rev 2003, 103:2167-2201.
41. Wang D., Farquhar E.R., Stubna A., Munck E., Que L. A diiron(IV) complex that cleaves strong C-H and O-H bonds. Nat Chem 2009, 1:145-150.
42. Friedle S., Reisner E., Lippard S.J. Current challenges of modeling diiron enzyme active sites for dioxygen activation by biomimetic synthetic complexes. Chem Soc Rev 2010, 39:2768-2779.
43. Hwang J., Krebs C., Huynh B.H., Edmondson D.E., Theil E.C., Penner-Hahn J.E. A short Fe-Fe distance in peroxodiferric ferritin: control of Fe substrate versus cofactor decay?. Science 2000, 287:122-125.
44. Treffry A., Zhao Z., Quail M.A., Guest J.R., Harrison P.M. 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 1995, 34:15204-15213.
45. Mertz J.R., Theil E.C. Subunit dimers in sheep spleen apoferritin: the effect on iron storage. J Biol Chem 1983, 258:11719-11726.
46. Schwartz J.K., Liu X., Tosha T., Theil E.C., Solomon E.I. Spectroscopic definition of the ferroxidase site in M ferritin: comparison of binuclear substrate vs. cofactor active sites. J Am Chem Soc 2008, 130:9441-9450.
47. 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. J Am Chem Soc 2005, 127:8238-8239.
48. 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., et al. Targeting of cancer cells with ferrimagnetic ferritin cage nanoparticles. J Am Chem Soc 2006, 128:16626-16633.
49. Deng Q.Y., Yang B., Wang J.F., Whiteley C.G., Wang X.N. Biological synthesis of platinum nanoparticles with apoferritin. Biotechnol Lett 2009, 31:1505-1509.
50. Abe S., Hirata K., Ueno T., Morino K., Shimizu N., Yamamoto M., Takata M., Yashima E., Watanabe Y. Polymerization of phenylacetylene by rhodium complexes within a discrete space of apo-ferritin. J Am Chem Soc 2009, 131:6958-6960.
51. Abe S., Niemeyer J., Abe M., Takezawa Y., Ueno T., Hikage T., Erker G., Watanabe Y. Control of the coordination structure of organometallic palladium complexes in an apo-ferritin cage. J Am Chem Soc 2008, 130:10512-10514.
52. Theil E.C., Liu X.S., Tosha T. Gated pores in the ferritin protein nanocage. Inorg Chim Acta 2008, 361:868-874.
53. Burton J.W., Harlow C., Theil E.C. Evidence for reutilization of nodule iron in soybean seed development. J Plant Nutr 1998, 21:913-927.
54. Murray-Kolb L.E., Welch R., Theil E.C., Beard J.L. Women with low iron stores absorb iron from soybeans. Am J Clin Nutr 2003, 77:180-184.
55. Yasmin S., Andrew SC, Moores GR, Lebrum NE. A new role for heme: facilitating release of iron from the bacterioferritin iron biomineral. J. Biol Chem. 2010 Nov 23. [Epub ahead of print] PMID 21106523.
56. 59Fe) in cells when the protein pores are unfolded by mutation. J Biol Chem 2008, 283:31394-31400.
57. Haldar S, Tosha T, Theil EC: Moving iron in ferritin: Leucine 154, a residue near Fe(III) during mineral buildup minimizes mineral dissolution. Indian J Chem A 2010: in press.
58. Luscieti S., Santambrogio P., Langlois d'Estaintot B., Granier T., Cozzi A., Poli M., Gallois B., Finazzi D., Cattaneo A., Levi S., et al. Mutant ferritin L-chains that cause neurodegeneration act in a dominant-negative manner to reduce ferritin iron incorporation. J Biol Chem 2010, 285:11948-11957.