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

Biochemistry

Volumn 53, Issue 3, 2014, Pages 473-482

  Kwak, Yeonju ^a   Schwartz, Jennifer K ^a   Haldar, Suranjana ^b   Behera, Rabindra K ^b   Tosha, Takehiko ^b   Theil, Elizabeth C ^b,c   Solomon, Edward I ^a  

^a STANFORD UNIVERSITY   (United States)

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

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COORDINATION ENVIRONMENT; HYDROPHOBIC NATURE; IRON MINERALS; LIGAND BINDING; NON-HEME IRON ENZYMES; RIBONUCLEOTIDE REDUCTASE; SPECTRAL CHANGE; SPECTROSCOPIC STUDIES;

CARBOXYLATION; ENZYMES; IRON; LIGANDS; PORPHYRINS; SPECTROSCOPIC ANALYSIS;

SUBSTRATES;

CARBOXYLIC ACID; FERRITIN; IRON; LIGAND; M FERRITIN; OXYGEN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; WATER;

ARTICLE; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ESCHERICHIA COLI; LIGAND BINDING; METAL BINDING; METHODOLOGY; MUTAGENESIS; NEAR INFRARED SPECTROSCOPY; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; CIRCULAR DICHROISM; FERRITINS; FERROUS COMPOUNDS; HISTIDINE; IRON; LIGANDS; MODELS, MOLECULAR; MUTATION; OXYGEN; RANA CATESBEIANA; RIBONUCLEOTIDE REDUCTASES;

EID: 84893466576     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4013726     Document Type: Article

References (40)

1. Nordlund, P. and Reichard, P. (2006) Ribonucleotide reductases Annu. Rev. Biochem. 75, 681-706
2. Tinberg, C. E. and Lippard, S. J. (2011) Dioxygen activation in soluble methane monooxygenase Acc. Chem. Res. 44, 280-288
3. Fox, B. G., Lyle, K. S., and Rogge, C. E. (2004) Reactions of the diiron enzyme stearoyl-acyl carrier protein desaturase Acc. Chem. Res. 37, 421-429
4. Logan, D. T., Su, X. D., Aberg, A., Regnström, K., Hajdu, J., Eklund, H., and Nordlund, P. (1996) Crystal structure of reduced protein R2 of ribonucleotide reductase: the structural basis for oxygen activation at a dinuclear iron site Structure 4, 1053-1064
5. Whittington, D. A. and Lippard, S. J. (2001) Crystal structures of the soluble methane monooxygenase hydroxylase from Methylococcus capsulatus (bath) demonstrating geometrical variability at the dinuclear iron active site J. Am. Chem. Soc. 123, 827-838
6. 9 stearoyl-acyl carrier protein desaturase from castor seed and its relationship to other di-iron proteins EMBO J. 15, 4081
7. 2 reactivity J. Am. Chem. Soc. 122, 8495-8510
8. 2 reactivity J. Am. Chem. Soc. 126, 3777-3788
9. Pulver, S., Froland, W. A., Fox, B. G., Lipscomb, J. D., and Solomon, E. I. (1993) Spectroscopic studies of the coupled binuclear non-heme iron active site in the fully reduced hydroxylase component of methane monooxygenase: comparison to deoxy and deoxy-azide hemerythrin J. Am. Chem. Soc. 115, 12409-12422
10. 9- desaturase: substrate binding and comparison to ribonucleotide reductase J. Am. Chem. Soc. 121, 2770-2783
11. peroxo, the putative peroxodiiron (III) complex from the methane monooxygenase catalytic cycle J. Am. Chem. Soc. 120, 1094-1095
12. Lee, S. K., Nesheim, J. C., and Lipscomb, J. D. (1993) Transient intermediates of the methane monooxygenase catalytic cycle J. Biol. Chem. 268, 21569-21577
13. 9 desaturase: oxidase reactivity during single turnover and implications for the mechanism of desaturation Biochemistry 37, 14664-14671
14. Sturgeon, B. E., Burdi, D., Chen, S., Huynh, B. H., Edmondson, D. E., Stubbe, J. A., and Hoffman, B. M. (1996) Reconsideration of X, the diiron intermediate formed during cofactor assembly in E. Coli ribonucleotide reductase J. Am. Chem. Soc. 118, 7551-7557
15. 2 diamond core structure for the key intermediate Q of methane monooxygenase Science 275, 515-518
16. Theil, E. C., Behera, R. K., and Tosha, T. (2013) Ferritins for chemistry and for life Coord. Chem. Rev. 257, 579-586
17. Pereira, A. S., Small, W., Krebs, C., Tavares, P., Edmondson, D. E., Theil, E. C., and Huynh, B. H. (1998) Direct spectroscopic and kinetic evidence for the involvement of a peroxodiferric intermediate during the ferroxidase reaction in fast ferritin mineralization Biochemistry 37, 9871-9876
18. 2-activating non-heme diiron proteins Biochemistry 38, 5290-5295
19. Takagi, H., Shi, D., Ha, Y., Allewell, N. M., and Theil, E. C. (1998) Localized unfolding at the junction of three ferritin subunits. A mechanism for iron release? J. Biol. Chem. 273, 18685-18688
20. Ha, Y., Shi, D., Small, G. W., Theil, E. C., and Allewell, N. M. (1999) Crystal structure of bullfrog M ferritin at 2.8 Å resolution: analysis of subunit interactions and the binuclear metal center J. Biol. Inorg. Chem. 4, 243-256
21. Hwang, J., Krebs, C., Huynh, B. H., Edmondson, D. E., Theil, E. C., and Penner-Hahn, J. E. (2000) A short Fe-Fe distance in peroxodiferric ferritin: control of Fe substrate versus cofactor decay? Science 287, 122-125
22. Liu, X. and Theil, E. C. (2004) Ferritin reactions: Direct identification of the site for the diferric peroxide reaction intermediate Proc. Natl. Acad. Sci. U.S.A. 101, 8557-8562
23. Theil, E. C. The ferritin protein nanocage and biomineral, from single Fe atoms to FeO nanoparticles: Starting with EXAFS. AIP Conf. Proc. 2007, 882, 15-18.
24. Schwartz, J. K., Liu, X. S., Tosha, T., Theil, E. C., and Solomon, E. I. (2008) Spectroscopic definition of the ferroxidase site in M ferritin: comparison of binuclear substrate vs cofactor active sites J. Am. Chem. Soc. 130, 9441-9450
25. 2 in the rapid mineralization pathway Proc. Natl. Acad. Sci. U.S.A. 105, 18182-18187
26. Turano, P., Lalli, D., Felli, I. C., Theil, E. C., and Bertini, I. (2010) NMR reveals pathway for ferric mineral precursors to the central cavity of ferritin Proc. Natl. Acad. Sci. U.S.A. 107, 545-550
27. Tosha, T., Ng, H.-L., Bhattasali, O., Alber, T., and Theil, E. C. (2010) Moving metal ions through ferritin-protein nanocages from three-fold pores to catalytic sites J. Am. Chem. Soc. 132, 14562-14569
28. Tosha, T., Behera, R. K., Ng, H.-L., Bhattasali, O., Alber, T., and Theil, E. C. (2012) Ferritin protein nanocage ion channels: gating by N-terminal extensions J. Biol. Chem. 287, 13016-13025
29. 2 reactivity at distant sites Inorg. Chem. 51, 11406-11411
30. Bertini, I., Lalli, D., Mangani, S., Pozzi, C., Rosa, C., Theil, E. C., and Turano, P. (2012) Structural insights into the ferroxidase site of ferritins from higher eukaryotes J. Am. Chem. Soc. 134, 6169-6176
31. Crow, A., Lawson, T. L., Lewin, A., Moore, G. R., and Le Brun, N. E. (2009) Structural basis for iron mineralization by bacterioferritin J. Am. Chem. Soc. 131, 6808-6813
32. Solomon, E. I., Brunold, T. C., Davis, M. I., Kemsley, J. N., Lee, S.-K., Lehnert, N., Neese, F., Skulan, A. J., Yang, Y.-S., and Zhou, J. (2000) Geometric and electronic structure/function correlations in non-heme iron enzymes Chem. Rev. 100, 235-350
33. Schwartz, J. K. (2008) Spectroscopic and Theoretical Elucidation of Structural Contribution to Reactivity in Binuclear Non-Heme Iron Enzymes: Substrate versus Cofactor Sites (Solomon, E. I., Ed.) Stanford University.
34. Reem, R. C. and Solomon, E. I. (1987) Spectroscopic studies of the binuclear ferrous active site of deoxyhemerythrin: coordination number and probable bridging ligands for the native and ligand-bound forms J. Am. Chem. Soc. 109, 1216-1226
35. Hagen, K. S. and Lachicotte, R. (1992) Diiron (II) μ-aqua bis (μ-carboxylato) models of reduced dinuclear non-heme iron sites in proteins J. Am. Chem. Soc. 114, 8741-8742
36. Brunold, T. C. and Solomon, E. I. (1999) Reversible dioxygen binding to hemerythrin. 1. Electronic structures of deoxy-and oxyhemerythrin J. Am. Chem. Soc. 121, 8277-8287
37. 2 reactivity J. Am. Chem. Soc. 127, 16098-16106
38. Frisch, M. J., Gaussian 09, revision D.01; Gaussian, Inc., Wallingford CT, 2009.
39. Voegtli, W. C., Sommerhalter, M., Saleh, L., Baldwin, J., Bollinger, J. M., and Rosenzweig, A. C. (2003) Variable coordination geometries at the diiron(II) active site of ribonucleotide reductase R2 J. Am. Chem. Soc. 125, 15822-15830
40. Theil, E. C. (2011) Ferritin protein nanocages use ion channels, catalytic sites, and nucleation channels to manage iron/oxygen chemistry Curr. Opin. Chem. Biol. 15, 304-311