Comparison of the 1.85 Å structure of CYP154A1 from Streptomyces coelicolor A3(2) with the closely related CYP154C1 and CYPs from antibiotic biosynthetic pathways

Protein Science

Volumn 13, Issue 1, 2004, Pages 255-268

  Podust, Larissa M ^a,e   Bach, Horacio ^b   Kim, Youngchang ^c   Lamb, David C ^d   Arase, Miharu ^a   Sherman, David H ^b   Kelly, Steven L ^d   Waterman, Michael R ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d ABERYSTWYTH UNIVERSITY   (United Kingdom)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

Antibiotic biosynthesis; CYP154A1; Heme orientation; P450; Streptomyces; X ray structure

Indexed keywords

ANTIBIOTIC AGENT; CARBOMYCIN; COMPLESTATIN; CYTOCHROME P450; CYTOCHROME P450 154 A1; CYTOCHROME P450 154 C1; CYTOCHROME P450 1A1; CYTOCHROME P450 C1; ERYTHROMYCIN; GRISEORHODIN; HEME; LEINAMYCIN; MACROLIDE; METHYMYCIN; MITOMYCIN; MYCINAMICIN; NATURAL PRODUCT; OLEANDOMYCIN; OXIDOREDUCTASE; OXYGENASE; PIKROMYCIN; POLYKETIDE; POLYKETIDE SYNTHASE; PRADIMICIN; RAPAMYCIN; RUBROMYCIN; TEICOPLANIN; UNCLASSIFIED DRUG; VANCOMYCIN;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL STRAIN; BIOSYNTHESIS; CATALYSIS; ENZYME ENGINEERING; ENZYME STRUCTURE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; STREPTOMYCES COELICOLOR;

AMINO ACID SEQUENCE; AMINO ACIDS; BACTERIAL PROTEINS; BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; CYTOCHROME P-450 ENZYME SYSTEM; DATABASES, PROTEIN; ESCHERICHIA COLI; HEME; LIGANDS; MACROLIDES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MULTIENZYME COMPLEXES; OXIDATION-REDUCTION; PROTEIN STRUCTURE, SECONDARY; ROTATION; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOMYCES; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; VARIATION (GENETICS);

ACTINOBACTERIA (CLASS); BACTERIA (MICROORGANISMS); STREPTOMYCES; STREPTOMYCES COELICOLOR; UNCULTURED ACTINOMYCETE;

EID: 0346733324     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.03384804     Document Type: Article

References (53)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Andersen, J.F. and Hutchinson, C.R. 1992. Characterization of Saccharopolyspora erythraea cytochrome P-450 genes and enzymes, including 6-deoxy-erythronolide B hydroxylase. J. Bacteriol. 174: 725-735.
3. Aojula, H.S., Wilson, M.T., and Drake, A. 1986. Characterization of haem disorder by circular dichroism. Biochem. J. 237: 613-616.
4. Aparicio, J.F., Molnar, I., Schwecke, T., Konig, A., Haydock, S.F., Khaw, L.E., Staunton, J., and Leadlay, P.F. 1996. Organization of the biosynthetic gene cluster for rapamycin in Streptomyces hygroscopicus: Analysis of the enzymatic domains in the modular polyketide synthase. Gene 169: 9-16.
5. Arisawa, A., Tsunekawa, H., Okamura, K., and Okamoto, R. 1995. Nucleotide sequence analysis of the carbomycin biosynthetic genes including the 3-O-acyltransferase gene from Streptomyces thermotolerans. Biosci. Biotechnol. Biochem. 59: 582-588.
6. Banci, L., Bertini, I., Rosato, A., and Scacchieri, S. 2000. Solution structure of oxidized microsomal rabbit cytochrome b5. Factors determining the heterogeneous binding of the heme. Eur. J. Biochem. 267: 755-766.
7. Bate, N., Butler, A.R., Gandecha, A.R., and Cundliffe, E. 1999. Multiple regulatory genes in the tylosin biosynthetic cluster of Streptomyces fradiae. Chem. Biol. 6: 617-624.
8. Bentley, S.D., Chater, K.F., Cerdeno-Tarraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., Harris, D.E., Quail, M.A., Kieser, H., Harper, D., et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147.
9. Brunger, A.T., Adams, P.D., Clore, G.M., Delano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.-S., Kuszewski, J., Nilges, M., and Pannu, N.S. 1998. Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54: 905-921.
10. Cheng, Y.Q., Tang, G.L., and Shen, B. 2002. Identification and localization of the gene cluster encoding biosynthesis of the antitumor macrolactam leinamycin in Streptomyces atroolivaceus S-140. J. Bacteriol. 184: 7013-7024.
11. Chiu, H.T., Hubbard, B.K., Shah, A.N., Eide, J., Fredenburg, R.A., Walsh, C.T., and Khosla, C. 2001. Molecular cloning and sequence analysis of the complestatin biosynthetic gene cluster. Proc. Natl. Acad. Sci. 98: 8548-8553.
12. Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16: 10881-10890.
13. Cupp-Vickery, J.R. and Poulos, T.L. 1995. Structure of cytochrome P450eryF involved in erythromycin biosynthesis. Nat. Struct. Biol. 2: 144-153.
14. Dairi, T., Hamano, Y., Igarashi, Y., Furumai, T., and Oki, T. 1997. Cloning and nucleotide sequence of the putative polyketide synthase genes for pradimicin biosynthesis from Actinomadura hibisca. Biosci. Biotechnol. Biochem. 61: 1445-1453.
15. Djerassi, C. and Halpern, O. 1958. Macrolide antibiotics-VII: The structure of neomethymycin. Tetrahedron 3: 255-268.
16. Djerassi, C. and Zderic, J.A. 1956. The structure of the antibiotic methymycin. J. Am. Chem. Soc. 78: 6390-6395.
17. Evans, S.V. 1993. SETOR: Hardware-lighted three-dimensional solid model representations of macromolecules. J. Mol. Graph. 11: 134-138.
18. Fouces, R., Mellado, E., Diez, B., and Barredo, J.L. 1999. The tylosin biosynthetic cluster from Streptomyces fradiae: Genetic organization of the left region. Microbiology 145: 855-868.
19. Gotoh, O. 1992. Substrate recognition sites in cytochrome P450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences. J. Biol. Chem. 267: 83-90.
20. Gouet, P., Courcelle, E., Stuart, D.I., and Metoz, F. 1999. ESPript: Multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.
21. Guengerich, F.P. 2002. Cytochrome P450 enzymes in the generation of commercial products. Nat. Rev. Drug Discov. 1: 359-366.
22. Guengerich, F.P. and MacDonald, T.L. 1990. Mechanisms of cytochrome P-450 catalysis. FASEB J. 4: 2453-2459.
23. Guex, N. and Peitsch, M.C. 1997. SWISS-MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
24. Haydock, S.F., Dowson, J.A., Dhillon, N., Roberts, G.A., Cortes, J., and Leadlay, P.F. 1991. Cloning and sequence analysis of genes involved in erythromycin biosynthesis in Saccharopolyspora erythraea: Sequence similarities between EryG and a family of S-adenosylmethionine-dependent methyltransferases. Mol. Gen. Genet. 230: 120-128.
25. Hopwood, D.A. 1999. Forty years of genetics with Streptomyces: From in vivo through in vitro to in silico. Microbiology 145: 2183-2202.
26. Inouye, M., Takada, Y., Muto, N., Beppu, T., and Horinouchi, S. 1994. Characterization and expression of a P-450-like mycinamicin biosynthesis gene using a novel Micromonospora-Escherichia coli shuttle cosmid vector. Mol. Gen. Genet. 245: 456-464.
27. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
28. Keller, R.M. and Wuthrich, K. 1980. Structural study of the heme crevice in cytochrome b5 based on individual assignments of the 1H-NMR lines of the heme group and selected amino acid residues. Biochim. Biophys. Acta 621: 204-217.
29. La Mar, G.N., Davis, N.L., Parish, D.W., and Smith, K.M. 1983. Heme orientational disorder in reconstituted and native sperm whale myoglobin. Proton nuclear magnetic resonance characterizations by heme methyl deuterium labeling in the Met-cyano protein. J. Mol. Biol. 168: 887-896.
30. Lamb, D.C., Skaug, T., Song, H.-L., Jackson, C.J., Podust, L.M., Waterman, M.R., Kell, D.B., Kelly, D.E., and Kelly, S.L. 2002. The cytochrome P450 complement (CYPome) of Streptomyces coelicolor A3(2). J. Biol. Chem. 277: 24000-24005.
31. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
32. Leys, D., Mowat, C.G., McLean, K.J., Richmond, A., Chapman, S.K., Walkinshaw, M.D., and Munro, A.W. 2003. Atomic structure of Mycobacterium tuberculosis CYP121 to 1.06 A reveals novel features of cytochrome P450. J. Biol. Chem. 278: 5141-5147.
33. Li, H. and Poulos, T.L. 1997. The structure of the cytochrome p450BM-3 haem domain complexed with the fatty acid substrate, palmitoleic acid. Nat. Struct. Biol. 4: 140-146.
34. Mao, Y., Varoglu, M., and Sherman, D.H. 1999. Molecular characterization and analysis of the biosynthetic gene cluster for the antitumor antibiotic mitomycin C from Streptomyces lavendulae NRRL 2564. Chem. Biol. 6: 251-263.
35. McLachlan, S.J., La Mar, G.N., Burns, P.D., Smith, K.M., and Langry, K.C. 1986. 1H-NMR assignments and the dynamics of interconversion of the isomeric forms of cytochrome b5 in solution. Biochim. Biophys. Acta 874: 274-284.
36. Moczygemba, C., Guidry, J., and Wittung-Stafshede, P. 2000. Heme orientation affects holo-myoglobin folding and unfolding kinetics. FEBS Lett. 470: 203-206.
37. Molnar, I., Aparicio, J.F., Haydock, S.F., Khaw, L.E., Schwecke, T., Konig, A., Staunton, J., and Leadlay, P.F. 1996. Organisation of the biosynthetic gene cluster for rapamycin in Streptomyces hygroscopicus: Analysis of genes flanking the polyketide synthase. Gene 169: 1-7.
38. Molnar, I., Schupp, T., Ono, M., Zirkle, R., Milnamow, M., Nowak-Thompson, B., Engel, N., Toupet, C., Stratmann, A., Cyr, D.D., et al. 2000. The biosynthetic gene cluster for the microtubule-stabilizing agents epothilones A and B from Sorangium cellulosum So ce90. Chem. Biol. 7: 97-109.
39. Otwinowski, Z. and Minor, W. 1997. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
40. Park, S.Y., Yamane, K., Adachi, S., Shiro, Y., Weiss, K.E., Maves, S.A., and Sligar, S.G. 2002. Thermophilic cytochrome P450 (CYP119) from Sulfolobus solfataricus: High resolution structure and functional properties. J. Inorg. Biochem. 91: 491-501.
41. Podust, L.M., Kim, Y., Arase, M., Neely, B.A., Beck, B.J., Bach, H., Sherman, D.H., Lamb, D.C., Kelly, S.L., and Waterman, M.R. 2003. The 1.92-Å structure of Streptomyces coelicolor A3(2) CYP154C1. A new monooxygenase that functionalizes macrolide ring systems. J. Biol. Chem. 278: 12214-12221.
42. Pootoolal, J., Thomas, M.G., Marshall, C.G., Neu, J.M., Hubbard, B.K., Walsh, C.T., and Wright, G.D. 2002. Assembling the glycopeptide antibiotic scaffold: The biosynthesis of A47934 from Streptomyces toyocaensis NRRL15009. Proc. Natl. Acad. Sci. 99: 8962-8967.
43. Rix, U., Fischer, C., Remsing, L.L., and Rohr, J. 2002. Modification of post-PKS tailoring steps through combinatorial biosynthesis. Nat. Prod. Rep. 19: 542-580.
44. Rodriguez, A.M., Olano, C., Mendez, C., Hutchinson, C.R., and Salas, J.A. 1995. A cytochrome P450-like gene possibly involved in oleandomycin biosynthesis by Streptomyces antibioticus. FEMS Microbiol. Lett. 127: 117-120.
45. Schlichting, I., Berendzen, J., Chu, K., Stock, A.M., Maves, S.A., Benson, D.E., Sweet, R.M., Ringe, D., Petsko, G.A., and Sligar, S.G. 2000. The catalytic pathway of cytochrome P450cam at atomic resolution. Science 287: 1615-1622.
46. Smith, R.F., Wiese, B.A., Wojzynski, M.K., Davison, D.B., and Worley, K.C. 1996. BCM Search Launcher-An integrated interface to molecular biology data base search and analysis services available on the World Wide Web. Genome Res. 6: 454-462.
47. Solenberg, P.J., Matsushima, P., Stack, D.R., Wilkie, S.C., Thompson, R.C., and Baltz, R.H. 1997. Production of hybrid glycopeptide antibiotics in vitro and in Streptomyces toyocaensis. Chem. Biol. 4: 195-202.
48. Sullivan, J.T., Trzebiatowski, J.R., Cruickshank, R.W., Gouzy, J., Brown, S.D., Elliot, R.M., Fleetwood, D.J., McCallum, N.G., Rossbach, U., Stuart, G.S., et al. 2002. Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J. Bacteriol. 184: 3086-3095.
49. 5. J. Am. Chem. Soc. 110: 6234-6240.
50. Xue, Y., Wilson, D., Zhao, L., Liu, H., and Sherman, D.H. 1998a. Hydroxylation of macrolactones YC-17 and narbomycin is mediated by the pikC-encoded cytochrome P450 in Streptomyces venezuelae. Chem. Biol. 5: 661-667.
51. Xue, Y., Zhao, L., Liu, H.W., and Sherman, D.H. 1998b. A gene cluster for macrolide antibiotic biosynthesis in Streptomyces venezuelae: Architecture of metabolic diversity. Proc. Natl. Acad. Sci. 95: 12111-12116.
52. Yano, J.K., Koo, L.S., Schuller, D.J., Li, H., Ortiz de Montellano, P.R., and Poulos, T.L. 2000. Crystal structure of a thermophilic cytochrome P450 from the archaeon Sulfolobus solfataricus. J. Biol. Chem. 275: 31086-31092.
53. Zerbe, K., Pylypenko, O., Vitali, F., Zhang, W., Rouset, S., Heck, M., Vrijbloed, J.W., Bischoff, D., Bister, B., Sussmuth, R.D., et al. 2002. Crystal structure of OxyB, a cytochrome P450 implicated in an oxidative phenol coupling reaction during vancomycin biosynthesis. J. Biol. Chem. 277: 47476-47485.