Identification and structural basis of the reaction catalyzed by CYP121, an essential cytochrome P450 in Mycobacterium tuberculosis

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

Volumn 106, Issue 18, 2009, Pages 7426-7431

  Belin, Pascal ^a   Du, Marie Hélène Le ^a   Fielding, Alistair ^a   Lequin, Olivier ^b   Jacquet, Mickaël ^a   Charbonnier, Jean Baptiste ^a   Lecoq, Alain ^a   Thai, Robert ^a   Courçon, Marie ^a   Masson, Cédric ^a   Dugave, Christophe ^a   Genet, Roger ^a,c   Pernodet, Jean Luc ^b   Gondry, Muriel ^a  

^a SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^b CNRS   (France)

^c CEMAGREF   (France)

Author keywords

C C coupling; Cyclopeptide

Indexed keywords

ARGININE; CARBON; CYCLO(LEVO TYROSYL LEVO TYROSYL); CYTOCHROME P450; CYTOCHROME P450 CYP121; FERREDOXIN; FERREDOXIN REDUCTASE; GLUTAMINE; HEME; IRON; SERINE; TYROSINE DERIVATIVE; TYROSYL CARBON; UNCLASSIFIED DRUG; WATER; CYCLOPEPTIDE; CYTOCHROME P 450 CYP121; CYTOCHROME P-450 CYP121; DIPEPTIDE; OXYGEN; TYROSYLTYROSINE;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBON CARBON BOND; CATALYSIS; CHEMICAL BOND; CROSS COUPLING REACTION; CROSS LINKING; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME SUBSTRATE; HYDROGEN BOND; LOW TEMPERATURE; MOLECULE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; REACTION ANALYSIS; SPINACH; X RAY CRYSTALLOGRAPHY; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION;

MYCOBACTERIUM TUBERCULOSIS; SPINACIA OLERACEA;

BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; CYTOCHROME P-450 ENZYME SYSTEM; DIPEPTIDES; HYDROGEN BONDING; MYCOBACTERIUM TUBERCULOSIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXYGEN; PEPTIDES, CYCLIC; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

EID: 66149152326     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0812191106     Document Type: Article

References (42)

1. Corbett EL, et al. (2003) The growing burden of tuberculosis: Global trends and interactions with the HIV epidemic. Arch Intern Med 163:1009-1021.
2. Cole ST, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
3. lsin EM, Guengerich FP (2007) Complex reactions catalyzed by cytochrome P450 enzymes. Biochim Biophys Acta 1770:314-329.
4. McLean KJ, et al. (2006) The preponderance of P450s in the Mycobacterium tuberculosis genome. Trends Microbiol 14:220-228.
5. Ahmad Z, Sharma S, Khuller GK (2006) Azole antifungals as novel chemotherapeutic agents against murine tuberculosis. FEMS Microbiol Lett 261:181-186.
6. Ahmad Z, Sharma S, Khuller GK (2006) The potential of azole antifungals against latent/persistent tuberculosis. FEMS Microbiol Lett 258:200-203.
7. Burguiere A, Hitchen PG, Dover LG, Dell A, Besra GS (2005) Altered expression profile of mycobacterial surface glycopeptidolipids following treatment with the antifungal azole inhibitors econazole and clotrimazole. Microbiology 151:2087-2095.
8. McLean KJ, et al. (2002) Azole antifungals are potent inhibitors of cytochrome P450 mono-oxygenases and bacterial growth in mycobacteria and streptomycetes. Microbiology 148:2937-2949.
9. McLean KJ, et al. (2008) Characterization of active site structure in CYP121: A cyto- chrome P450 essential for viability of Mycobacterium tuberculosis H37Rv. J Biol Chem 283:33406-33416.
10. Leys D, et al. (2003) Atomic structure of Mycobacterium tuberculosis CYP121 to 1.06 Å reveals novel features of cytochrome P450. J Biol Chem 278:5141-5147.
11. Roback P, et al. (2007) A predicted operon map for Mycobacterium tuberculosis. Nucleic Acids Res 35:5085-5095.
12. Gondry M, et al. (2009) Cyclodipeptide synthases are a family of tRNA-dependent peptide bond-forming enzymes. Nat Chem Biol, in press.
13. Schenkman JB, Jansson I (2006) Spectral analyses of cytochromes P450. Methods Mol Biol 320:11-18.
14. Seward HE, Roujeinikova A, McLean KJ, Munro AW, Leys D (2006) Crystal structure of the Mycobacterium tuberculosis P450 CYP121-fluconazole complex reveals new azole drug-P450 binding mode. J Biol Chem 281:39437-39443.
15. Hannemann F, Bichet A, Ewen KM, Bernhardt R (2007) Cytochrome P450 systems- biological variations of electron transport chains. Biochim Biophys Acta 1770:330-344.
16. MacDonald JC, WhitesidesJM (1994) Solid-state structures of hydrogen-bonded tapes based on cyclic secondary diamides. Chem Rev 94:2383-2420.
17. Kopple KD, Marr DH (1967) Conformations of cyclic peptides. The folding of cyclic dipeptides containing an aromatic side chain. J Am Chem Soc 89:6193-6200.
18. Zhao B, et al. (2005) Binding of two flaviolin substrate molecules, oxidative coupling, and crystal structure of Streptomyces coelicolorA3(2) cytochrome P450 158A2. J Biol Chem 280:11599-11607.
19. Healy FG, Krasnoff SB, Wach M, Gibson DM, Loria R(2002) Involvement of a cytochrome P450 monooxygenase in thaxtomin A biosynthesis by Streptomyces acidiscabies. J Bacteriol 184:2019-2029.
20. Schultz AW, et al. (2008) Biosynthesis and structures of cyclomarins and cyclomar- azines, prenylated cyclic peptides of marine actinobacterial origin. J Am Chem Soc 130:4507-4516.
21. Tang MR, Sternberg D, Behr RK, Sloma A, Berka RM (2006) Use of transciptional profiling and bioinformatics to solve production problems. Ind Biotechnol 2:66-74.
22. Denisov IG, Makris TM, Sligar SG, Schlichting I (2005) Structure and chemistry of cytochrome P450. Chem Rev105:2253-2277.
23. McLean KJ, et al. (2002) Expression, purification and spectroscopic characterization of the cytochrome P450 CYP121 from Mycobacterium tuberculosis. J Inorg Biochem 91:527-541.
24. Bischoff D, et al. (2001) The Biosynthesis of Vancomycin-Type Glycopeptide Antibiotics- The Order of the Cyclization Steps. Angew Chem Int Ed Engl 40:4688-4691.
25. Bischoff D, et al. (2001) The Biosynthesis of Vancomycin-Type Glycopeptide Antibiotics- New Insights into the Cyclization Steps. Angew Chem Int Ed Engl 40:1693-1696.
26. Funa N, Funabashi M, Ohnishi Y, Horinouchi S (2005) Biosynthesis of hexahy- droxyperylenequinone melanin via oxidative aryl coupling by cytochrome P-450 in Streptomyces griseus. J Bacteriol 187:8149-8155.
27. Howard-Jones AR, Walsh CT (2006) Staurosporine and rebeccamycin aglycones are assembled by the oxidative action of StaP,StaC, and Reb Con chromopyrrolic acid. J Am Chem Soc 128:12289-12298.
28. IkezawaN,IwasaK,SatoF (2008)MolecularCloning and Characterization of CYP80G2, a Cytochrome P450 That Catalyzes an Intramolecular C-C Phenol Coupling of (S)- Reticuline in Magnoflorine Biosynthesis, from Cultured Coptis japonica Cells. J Biol Chem 283:8810-8821.
29. Makino M, et al. (2007)Crystal structures and catalytic mechanism of cytochrome P450 StaP that produces the indolocarbazole skeleton. Proc Natl Acad Sci USA104:11591- 11596.
30. Ralston I, Dunford HB (1978) Horseradish peroxidase. XXXII. pH dependence of the oxidation of L-(-)-tyrosine bycompound. Can J Biochem 56:1115-1119.
31. Ralston IM, Dunford HB (1980) Horseradish peroxidase. XLII. Oxidations of L-tyrosine and 3,5-diiodo-L-tyrosine by compound II. Can J Biochem 58:1270-1276.
32. Eickhoff H, Jung G, Rieker A (2001) Oxidative phenol coupling-tyrosine dimers and libraries containing tyrosyl peptide dimers. Tetrahedron 57:353-364.
33. Betts JC, Lukey PT, Robb LC, McAdam RA, Duncan K (2002) Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43:717-731.
34. Gao Q, Kripke K, Arinc Z, Voskuil M, Small P (2004) Comparative expression studies of a complex phenotype: Cord formation in Mycobacterium tuberculosis. Tuberculosis 84:188-196.
35. Gao Q, et al. (2005) Gene expression diversity among Mycobacterium tuberculosis clinical isolates. Microbiology 151:5-14.
36. Prasad C (1995) Bioactive cyclic dipeptides. Peptides16:151-164.
37. Schuster I, Bernhardt R (2007) Inhibition of cytochromes P450: Existing and new promising therapeutic targets. Drug Met Rev 39:481-499.
38. Mowat CG, et al. (2002) Crystallization and preliminary crystallographic analysis of a novel cytochrome P450 from Mycobacterium tuberculosis. Acta Crystallogr D Biol Crystallogr 58:704-705.
39. CCP4 Collaborative Computational ProjectN (1994) Acta Crystallogr D Biol Crystallogr 50:760-763.
40. Vagin A, TeplyakovA(1997) MOLREP: An automated program for molecular replacement. J Appl Cryst 30:1022-1025.
41. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr53:240-255.
42. Roussel A, Cambillau C (1989) Silicon Graphics Geometry Partner Directory (Silicon Graphics, Mountain View, CA), pp 77-78.