A Mycobacterium tuberculosis ligand-binding Mn/Fe protein reveals a new cofactor in a remodeled R2-protein scaffold

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 14, 2009, Pages 5633-5638

  Andersson, Charlotta S ^a   Högbom, Martin ^a,b  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Bioinorganic chemistry; Diiron; Manganese; Monooxygenase; R2c

Indexed keywords

BACTERIAL MULTICOMPONENT MONOOXYGENASE; CARBOXYLIC ACID; IRON; MANGANESE; OXIDOREDUCTASE; PROTEIN RV0233; SCAFFOLD PROTEIN; SCAFFOLD PROTEIN R2; TYROSINE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE; VIRULENCE FACTOR;

ARTICLE; CONTROLLED STUDY; CRYSTALLOGRAPHY; ELECTRON; LIGAND BINDING; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATION; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; STRUCTURE ANALYSIS;

BACTERIAL PROTEINS; COENZYMES; IRON; MANGANESE; METALLOPROTEINS; MYCOBACTERIUM TUBERCULOSIS; OXIDOREDUCTASES; RIBONUCLEOTIDE REDUCTASES;

BACTERIA (MICROORGANISMS); CHLAMYDIA TRACHOMATIS; MYCOBACTERIUM TUBERCULOSIS; OVIS ARIES;

EID: 65249133078     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0812971106     Document Type: Article

References (38)

1. Shu L, et al. (1997) An Fe2IVO2 diamond core structure for the key intermediate Q of methane monooxygenase. Science 24:515-518.
2. Rosenzweig AC, Frederick CA, Lippard SJ, Nordlund P (1993) Crystal-structure of a bacterial nonheme iron hydroxylase that catalyzes the biological oxidation of methane. Nature 366:537-543.
3. Merkx M, et al. (2001) Dioxygen activation and methane hydroxylation by soluble methane monooxygenase: A tale of two irons and three proteins. Angew Chem Int Ed 40:2782-2807.
4. Sazinsky MH, Lippard SJ (2006) Correlating structure with function in bacterial multicomponent monooxygenases and related diiron proteins. Acc Chem Res 39:558-566.
5. Coleman NV, Bui NB, Holmes AJ (2006) Soluble di-iron monooxygenase gene diversity in soils, sediments and ethene enrichments. Environ Microbiol 8:1228-1239.
6. Leahy JG, Batchelor PJ, Morcomb SM (2003) Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27:449-479.
7. Bollinger JM, et al. (1991) Mechanism of assembly of the tyrosyl radical-dinuclear iron cluster cofactor of ribonucleotide reductase. Science 253:292-298.
8. Sjöberg BM (1997) Ribonucleotide reductases - A group of enzymes with different metallosites and a similar reaction mechanism. Struct Bond 88:139-173.
9. Stubbe J, Nocera DG, Yee CS, Chang MCY (2003) Radical initiation in the class I ribonucleotide reductase: Long-range proton-coupled electron transfer? Chem Rev 103:2167-2201.
10. Nordlund P, Reichard P (2006) Ribonucleotide reductases. Annu Rev Biochem 75:681-706.
11. Notomista E, Lahm A, Di Donato A, Tramontano A (2003) Evolution of bacterial and archaeal multicomponent monooxygenases. J Mol Evol 56:435-445.
12. Baldwin J, et al. (2001) Rational reprogramming of the R2 subunit of Escherichia coli ribonucleotide reductase into a self-hydroxylating monooxygenase. J Am Chem Soc 123:7017-7030.
13. Assarsson M, et al. (2001) Restoring proper radical generation by azide binding to the iron site of the E238A mutant R2 protein of ribonucleotide reductase from Escherichia coli. J Biol Chem 276:26852-26859.
14. Roshick C, lliffe-Lee ER, McClarty G (2000) Cloning and characterization of ribonucleotide reductase from Chiamydia trachomatis. J Biol Chem 275:38111-38119.
15. Hogbom M,et al. (2004) The radical site in chlamydial ribonucleotide reductase defines a new R2 subclass. Science 305:245-248.
16. Jiang W, et al. (2007) A manganese(IV)/iron(lll) cofactor in Chiamydia trachomatis ribonucleotide reductase. Science 316:1188-1191.
17. Voevodskaya N, Lendzian F, Ehrenberg A, Graslund A (2007) High catalytic activity achieved with a mixed manganese-iron site in protein R2 of Chiamydia ribonucleotide reductase. FEBS Lett 581:3351-3355.
18. Jiang W, Xie J, Norgaard H, Bollinger JM Jr, Krebs C (2008) Rapid and quantitative activation of Chiamydia trachomatis ribonucleotide reductase by hydrogen peroxide. Biochemistry 47:4477-4483.
19. Schmidt F, et al. (2004) Complementary analysis of the mycobacterium tuberculosis proteome by two-dimensional electrophoresis and isotope-coded affinity tag technology. Mol Cell Proteomics 3:24-42.
20. Cole ST, et al. (1998) Deciphering the biology of mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
21. World health organization (2008) WHO global report 2008.
22. Jiang W, et al. (2008) Branched activation-and catalysis-specific pathways for electron relay to the manganese/iron cofactor in ribonucleotide reductase from Chiamydia trachomatis. Biochemistry 47:8477-8484.
23. Yang F, et al. (1997) Characterization of two genes encoding the mycobacterium tuberculosis ribonucleotide reductase small subunit. J Bacteriol 179:6408-6415.
24. Nordlund P, Sjöberg B-M, Eklund H (1990) Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345:593-598.
25. Sazinsky MH, Dunten PW, McCormick MS, DiDonato A, Lippard SJ (2006) X-ray structure of a hydroxylase-regulatory protein complex from a hydrocarbon-oxidizing multicomponent monooxygenase, Pseudomonas sp. OX1 phenol hydroxylase. Biochemistry 45:15392-15404.
26. 2 activation and radical generation. J Biol Inorg Chem 6:315-323.
27. Andersson ME, et al. (1999) The crystal structure of an azide complex of the diferrous R2 subunit of ribonucleotide reductase displays a novel carboxylate shift with important mechanistic implications for diiron-catalyzed oxygen activation. J Am Chem Soc 121:2346-2352.
28. Logan DT, et al. (1998) Crystal structures of two self-hydroxylating ribonucleotide reductase protein R2 mutants: Structural basis for the oxygen-insertion step of hydroxylation reactions catalyzed by diiron proteins. Biochemistry 37:10798-10807.
29. 2 activation by protein R2 of Escherichia coli ribonucleotide reductase: Relevance to R1-R2 radical transfer in nucleotide reduction? Biochemistry 45:8823-8830.
30. Lindqvist Y, Huang WJ, Schneider G, Shanklin J (1996) Crystal structure of Delta(9) stearoyl-acyl carrier protein desaturase from castor seed and its relationship to other di-iron proteins. EMBO J 15:4081-4092.
31. Mitic N, Schwartz JK, Brazeau BJ, Lipscomb JD, Solomon El (2008) CD and MCD studies of the effects of component B variant binding on the biferrous active site of methane monooxygenase. Biochemistry 47:8386-8397.
32. Bailey LJ, McCoy JG, Phillips GN, Fox BG (2008) Structural consequences of effector protein complex formation in a diiron hydroxylase. Proc Natl Acad Sci USA 105:19194-19198.
33. Jiang W, Hoffart LM, Krebs C, Bollinger JM Jr. (2007) A manganese(IV)/iron(IV) intermediate in assembly of the manganese(IV)/iron(III) cofactor of Chiamydia trachomatis ribonucleotide reductase. Biochemistry 46:8709-8716.
34. Hogbom M, et al. (2005) A high throughput method for the detection of metalloproteins on a microgram scale. Mol Cell Proteomics 4:827-834.
35. Collaborative computational project n (1994) Acta Crystallogr C 50:760-763.
36. 2+ ions stabilizing its N-terminus and the unique S1 specificity pocket. Acta Crystallogr D 61:505-512.
37. Engh RA, Huber R (1991) Accurate bond and angle parameters for X-ray proteinstructure refinement. Acta Crystallogr A 47:392-400.
38. Kleywegt GJ, Jones TA (1996) Phi/psi-chology: Ramachandran revisited. Structure 4:1395-1400.