Crystal structure of halogenase PltA from the pyoluteorin biosynthetic pathway

Journal of Structural Biology

Volumn 192, Issue 3, 2015, Pages 349-357

  Pang, Allan H ^a   Garneau Tsodikova, Sylvie ^a   Tsodikov, Oleg V ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Chlorination; FAD; Flavoprotein; Halogenation; Natural product

Indexed keywords

4,5 DICHLOROPYRROLYL PLTL; BACTERIAL ENZYME; CHLORIDE; FLAVINE ADENINE NUCLEOTIDE; PLTA ENZYME; PYRROLE; PYRROLYL PLTL; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CHLORINE; OXIDOREDUCTASE; PHENOL DERIVATIVE; PROTEIN BINDING; PYOLUTEORIN; PYRROLE DERIVATIVE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CHLORINATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME BINDING; HALOGENATION; HYDROPHOBICITY; PRIORITY JOURNAL; PSEUDOMONAS FLUORESCENS; STRUCTURE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; BINDING SITES; CHLORINE; CRYSTALLOGRAPHY, X-RAY; FLAVIN-ADENINE DINUCLEOTIDE; HALOGENATION; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHENOLS; PROTEIN BINDING; PSEUDOMONAS FLUORESCENS; PYRROLES;

EID: 84946893485     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2015.09.013     Document Type: Article

References (48)

1. Bister B., Bischoff D., Nicholson G.J., Stockert S., Wink J., Brunati C., Donadio S., Pelzer S., Wohlleben W., Süssmuth R.D. Bromobalhimycin and chlorobromobalhimycins-illuminating the potential of halogenases in glycopeptide antibiotic biosyntheses. ChemBioChem 2003, 4:658-662.
2. Biswas T., Tsodikov O.V. Hexameric ring structure of the N-terminal domain of Mycobacterium tuberculosis DnaB helicase. FEBS J. 2008, 275:3064-3071.
3. Bitto E., Huang Y., Bingman C.A., Singh S., Thorson J.S., Phillips G.N. The structure of flavin-dependent tryptophan 7-halogenase RebH. Proteins 2008, 70:289-293.
4. Blasiak L.C., Vaillancourt F.H., Walsh C.T., Drennan C.L. Crystal structure of the non-haem iron halogenase SyrB2 in syringomycin biosynthesis. Nature 2006, 440:368-371.
5. Buedenbender S., Rachid S., Muller R., Schulz G.E. Structure and action of the myxobacterial chondrochloren halogenase CndH: a new variant of FAD-dependent halogenases. J. Mol. Biol. 2009, 385:520-530.
6. Bush J.A., Long B.H., Catino J.J., Bradner W.T., Tomita K. Production and biological activity of rebeccamycin, a novel antitumor agent. J. Antibiot. 1987, 40:668-678.
7. Dong C., Huang F., Deng H., Schaffrath C., Spencer J.B., O'Hagan D., Naismith J.H. Crystal structure and mechanism of a bacterial fluorinating enzyme. Nature 2004, 427:561-565.
8. Dong C., Flecks S., Unversucht S., Haupt C., Van Pee K.-H., Naismith J.H. Tryptophan 7-halogenase (PrnA) structure suggests a mechanism for regioselective chlorination. Science 2005, 309:2216-2219.
9. 2-dependent halogenase PltA during pyoluteorin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:13843-13848.
10. Dym O., Eisenberg D. Sequence-structure analysis of FAD-containing proteins. Prot. Sci. 2001, 10:1712-1728.
11. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 2004, 60:2126-2132.
12. Eustaquio A.S., Gust B., Luft T., Li S.M., Chater K.F., Heide L. Clorobiocin biosynthesis in Streptomyces: identification of the halogenase and generation of structural analogs. Chem. Biol. 2003, 10:279-288.
13. Eustáquio A.S., Pojer F., Noel J.P., Moore B.S. Discovery and characterization of a marine bacterial SAM-dependent chlorinase. Nat. Chem. Biol. 2008, 4:69-74.
14. Fenna R., Zeng J., Davey C. Structure of the green heme in myeloperoxidase. Arch. Biochem. Biophys. 1995, 316:653-656.
15. Flecks S., Patallo E.P., Zhu X., Ernyei A.J., Seifert G., Schneider A., Dong C., Naismith J.H., van Pee K.H. New insights into the mechanism of enzymatic chlorination of tryptophan. Angew. Chem. 2008, 47:9533-9536.
16. Fournier J.B., Rebuffet E., Delage L., Grijol R., Meslet-Cladiere L., Rzonca J., Potin P., Michel G., Czjzek M., Leblanc C. The vanadium iodoperoxidase from the marine flavobacteriaceae species Zobellia galactanivorans reveals novel molecular and evolutionary features of halide specificity in the vanadium haloperoxidase enzyme family. Appl. Environ. Microbiol. 2014, 80:7561-7573.
17. Garneau S., Dorrestein P.C., Kelleher N.L., Walsh C.T. Characterization of the formation of the pyrrole moiety during clorobiocin and coumermycin A1 biosynthesis. Biochemistry 2005, 44:2770-2780.
18. Gribble G.W. The diversity of naturally produced organohalogens. Chemosphere 2003, 52:289-297.
19. Henriksen A., Schuller D.J., Meno K., Welinder K.G., Smith A.T., Gajhede M. Structural interactions between horseradish peroxidase C and the substrate benzohydroxamic acid determined by X-ray crystallography. Biochemistry 1998, 37:8054-8060.
20. Hu J., Xue Y.-C., Xie M.-Y., Zhang R., Otani T., Minami Y., Yamada Y., Marunaka T. A new macromolecular antitumor antibiotic, C-1027. I. Discovery, taxonomy of producing organism, fermentation and biological activity. J. Antibiot. 1988, 41:1575-1579.
21. Huijbers M.M., Montersino S., Westphal A.H., Tischler D., van Berkel W.J. Flavin dependent monooxygenases. Arch. Biochem. Biophys. 2014, 544:2-17.
22. Jansen R., Kunze B., Reichenbach H., Hofle G. Chondrochloren A and B, new b-amino styrenes from Chondromyces crocatus (myxobacteria). Eur. J. Org. Chem. 2003, 2003:2684-2689.
23. Khare D., Wang B., Gu L., Razelun J., Sherman D.H., Gerwick W.H., Hakansson K., Smith J.L. Conformational switch triggered by alpha-ketoglutarate in a halogenase of curacin A biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:14099-14104.
24. Kirner S., Hammer P.E., Hill D.S., Altmann A., Fischer I., Weislo L.J., Lanahan M., van Pée K.-H., Ligon J.M. Functions encoded by pyrrolnitrin biosynthetic genes from Pseudomonas fluorescens. J. Bacteriol. 1998, 180:1939-1943.
25. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 1993, 26:283-291.
26. Lin S., Van Lanen S.G., Shen B. Regiospecific chlorination of (S)-beta-tyrosyl-S-carrier protein catalyzed by SgcC3 in the biosynthesis of the enediyne antitumor antibiotic C-1027. J. Am. Chem. Soc. 2007, 129:12432-12438.
27. Luft J.R., Collins R.J., Fehrman N.A., Lauricella A.M., Veatch C.K., DeTitta G.T. A deliberate approach to screening for initial crystallization conditions of biological macromolecules. J. Struct. Biol. 2003, 142:170-179.
28. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., Read R.J. Phaser crystallographic software. J. Appl. Crystallogr. 2007, 40:658-674.
29. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 1997, 53:240-255.
30. Nowak-Thompson B., Chaney N., Wing J.S., Gould S.J., Loper J.E. Characterization of the pyoluteorin biosynthetic gene cluster of Pseudomonas fluorescens Pf-5. J. Bacteriol. 1999, 181:2166-2174.
31. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
32. Podzelinska K., Latimer R., Bhattacharya A., Vining L.C., Zechel D.L., Jia Z. Chloramphenicol biosynthesis: the structure of CmlS, a flavin-dependent halogenase showing a covalent flavin-aspartate bond. J. Mol. Biol. 2010, 397:316-331.
33. Renner M.K., Jensen P.R., Fenical W. Neomangicols: structures and absolute stereochemistries of unprecedented halogenated sesterterpenes from a marine fungus of the genus Fusarium. J. Org. Chem. 1998, 63:8346-8354.
34. Rodrigues Pereira E., Belin L., Sancelme M., Prudhomme M., Ollier M., Rapp M., Sevère D., Riou J.-F., Fabbro D., Meyer T. Structure-activity relationships in a series of substituted indolocarbazoles: topoisomerase I and protein kinase C inhibition and antitumoral and antimicrobial properties. J. Med. Chem. 1996, 39:4471-4477.
35. Schreuder H.A., Prick P.A., Wierenga R.K., Vriend G., Wilson K.S., Hol W.G., Drenth J. Crystal structure of the p-hydroxybenzoate hydroxylase-substrate complex refined at 1.9Å resolution: analysis of the enzyme-substrate and enzyme-product complexes. J. Mol. Biol. 1989, 208:679-696.
36. Sheikh I.A., Singh A.K., Singh N., Sinha M., Singh S.B., Bhushan A., Kaur P., Srinivasan A., Sharma S., Singh T.P. Structural evidence of substrate specificity in mammalian peroxidases: structure of the thiocyanate complex with lactoperoxidase and its interactions at 2.4Å resolution. J. Biol. Chem. 2009, 284:14849-14856.
37. Singh A.K., Singh N., Sharma S., Singh S.B., Kaur P., Bhushan A., Srinivasan A., Singh T.P. Crystal structure of lactoperoxidase at 2.4Å resolution. J. Mol. Biol. 2008, 376:1060-1075.
38. Singh A.K., Kumar R.P., Pandey N., Singh N., Sinha M., Bhushan A., Kaur P., Sharma S., Singh T.P. Mode of binding of the tuberculosis prodrug isoniazid to heme peroxidases: binding studies and crystal structure of bovine lactoperoxidase with isoniazid at 2.7 A resolution. J. Biol. Chem. 2010, 285:1569-1576.
39. Sundaramoorthy M., Terner J., Poulos T.L. The crystal structure of chloroperoxidase: a heme peroxidase - cytochrome P450 functional hybrid. Structure 1995, 3:1367-1378.
40. Thomas M.G., Burkart M.D., Walsh C.T. Conversion of l-proline to pyrrolyl-2-carboxyl-S-PCP during undecylprodigiosin and pyoluteorin biosynthesis. Chem. Biol. 2002, 9:171-184.
41. Tsodikov O.V., Record M.T., Sergeev Y.V. Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature. J. Comp. Chem. 2002, 23:600-609.
42. Weyand M., Hecht H.-J., Kiess M., Liaud M.-F., Vilter H., Schomburg D. X-ray structure determination of a vanadium-dependent haloperoxidase from Ascophyllum nodosum at 2.0Å resolution. J. Mol. Biol. 1999, 293:595-611.
43. Wierenga R.K., Drenth J., Schulz G.E. Comparison of the three-dimensional protein and nucleotide structure of the FAD-binding domain of p-hydroxybenzoate hydroxylase with the FAD- as well as NADPH-binding domains of glutathione reductase. J. Mol. Biol. 1983, 167:725-739.
44. Wong C., Fujimori D.G., Walsh C.T., Drennan C.L. Structural analysis of an open active site conformation of nonheme iron halogenase CytC3. J. Am. Chem. Soc. 2009, 131:4872-4879.
45. Xu Q., Eguchi T., Mathews I.I., Rife C.L., Chiu H.-J., Farr C.L., Feuerhelm J., Jaroszewski L., Klock H.E., Knuth M.W. Insights into substrate specificity of geranylgeranyl reductases revealed by the structure of digeranylgeranylglycerophospholipid reductase, an essential enzyme in the biosynthesis of archaeal membrane lipids. J. Mol. Biol. 2010, 404:403-417.
46. Yeh E., Cole L.J., Barr E.W., Bollinger J.M., Ballou D.P., Walsh C.T. Flavin redox chemistry precedes substrate chlorination during the reaction of the flavin-dependent halogenase RebH. Biochemistry 2006, 45:7904-7912.
47. Yeh E., Blasiak L.C., Koglin A., Drennan C.L., Walsh C.T. Chlorination by a long-lived intermediate in the mechanism of flavin-dependent halogenases. Biochemistry 2007, 46:1284-1292.
48. Zhu X., De Laurentis W., Leang K., Herrmann J., Ihlefeld K., van Pée K.-H., Naismith J.H. Structural insights into regioselectivity in the enzymatic chlorination of tryptophan. J. Mol. Biol. 2009, 391:74-85.