Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Streptomyces Cytochrome P450 Enzymes and Their Roles in the Biosynthesis of Macrolide Therapeutic Agents

  • Cho, Myung-A (Department of Biological Sciences, Konkuk University) ;
  • Han, Songhee (Department of Biological Sciences, Konkuk University) ;
  • Lim, Young-Ran (Department of Biological Sciences, Konkuk University) ;
  • Kim, Vitchan (Department of Biological Sciences, Konkuk University) ;
  • Kim, Harim (Department of Biological Sciences, Konkuk University) ;
  • Kim, Donghak (Department of Biological Sciences, Konkuk University)
  • Received : 2018.09.20
  • Accepted : 2018.10.08
  • Published : 2019.03.01
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Abstract

The study of the genus Streptomyces is of particular interest because it produces a wide array of clinically important bioactive molecules. The genomic sequencing of many Streptomyces species has revealed unusually large numbers of cytochrome P450 genes, which are involved in the biosynthesis of secondary metabolites. Many macrolide biosynthetic pathways are catalyzed by a series of enzymes in gene clusters including polyketide and non-ribosomal peptide synthesis. In general, Streptomyces P450 enzymes accelerate the final, post-polyketide synthesis steps to enhance the structural architecture of macrolide chemistry. In this review, we discuss the major Streptomyces P450 enzymes research focused on the biosynthetic processing of macrolide therapeutic agents, with an emphasis on their biochemical mechanisms and structural insights.

Keywords

References

  1. Alayev, A. and Holz, M. K. (2013) mTOR signaling for biological control and cancer. J. Cell Physiol. 228, 1658-1664. https://doi.org/10.1002/jcp.24351
  2. Baranasic, D., Gacesa, R., Starcevic, A., Zucko, J., Blazic, M., Horvat, M., Gjuracic, K., Fujs, S., Hranueli, D., Kosec, G., Cullum, J. and Petkovic, H. (2013) Draft genome sequence of Streptomyces rapamycinicus Strain NRRL 5491, the producer of the immunosuppressant rapamycin. Genome Announc. 1, e00581-13.
  3. 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., Bateman, A., Brown, S., Chandra, G., Chen, C. W., Collins, M., Cronin, A., Fraser, A., Goble, A., Hidalgo, J., Hornsby, T., Howarth, S., Huang, C. H., Kieser, T., Larke, L., Murphy, L., Oliver, K., O'Neil, S., Rabbinowitsch, E., Rajandream, M. A., Rutherford, K., Rutter, S., Seeger, K., Saunders, D., Sharp, S., Squares, R., Squares, S., Taylor, K., Warren, T., Wietzorrek, A., Woodward, J., Barrell, B. G., Parkhill, J. and Hopwood, D. A. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141-147. https://doi.org/10.1038/417141a
  4. Berdy, J. (2005) Bioactive microbial metabolites. J. Antibiot. (Tokyo) 58, 1-26. https://doi.org/10.1038/ja.2005.1
  5. Bhattarai, S., Liou, K. and Oh, T. J. (2013) Hydroxylation of long chain fatty acids by CYP147F1, a new cytochrome P450 subfamily protein from Streptomyces peucetius. Arch. Biochem. Biophys. 539, 63-69. https://doi.org/10.1016/j.abb.2013.09.008
  6. Bradley, S. G. and Ritzi, D. (1968) Composition and ultrastructure of Streptomyces venezuelae. J. Bacteriol. 95, 2358-2364. https://doi.org/10.1128/JB.95.6.2358-2364.1968
  7. Chater, K. F. and Chandra, G. (2006) The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol. Rev. 30, 651-672. https://doi.org/10.1111/j.1574-6976.2006.00033.x
  8. Chun, Y. J., Shimada, T., Sanchez-Ponce, R., Martin, M. V., Lei, L., Zhao, B., Kelly, S. L., Waterman, M. R., Lamb, D. C. and Guengerich, F. P. (2007) Electron transport pathway for a Streptomyces cytochrome P450: cytochrome P450 105D5-catalyzed fatty acid hydroxylation in Streptomyces coelicolor A3(2). J. Biol. Chem. 282, 17486-17500. https://doi.org/10.1074/jbc.M700863200
  9. Chun, Y. J., Shimada, T., Waterman, M. R. and Guengerich, F. P. (2006) Understanding electron transport systems of Streptomyces cytochrome P450. Biochem. Soc. Trans. 34, 1183-1185. https://doi.org/10.1042/BST0341183
  10. Chung, L., Liu, L., Patel, S., Carney, J. R. and Reeves, C. D. (2001) Deletion of rapQONML from the rapamycin gene cluster of Streptomyces hygroscopicus gives production of the 16-O-desmethyl-27-desmethoxy analog. J. Antibiot. (Tokyo) 54, 250-256. https://doi.org/10.7164/antibiotics.54.250
  11. Cupp-Vickery, J. R., Garcia, C., Hofacre, A. and McGee-Estrada, K. (2001) Ketoconazole-induced conformational changes in the active site of cytochrome P450eryF. J. Mol. Biol. 311, 101-110. https://doi.org/10.1006/jmbi.2001.4803
  12. Dundas, J., Ouyang, Z., Tseng, J., Binkowski, A., Turpaz, Y. and Liang, J. (2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res. 34, W116-W118. https://doi.org/10.1093/nar/gkl282
  13. Dyson, P. (2011) Streptomyces: Molecular Biology and Biotechnology. Caister Academic Press, Norfolk, UK.
  14. Graziani, E. I. (2009) Recent advances in the chemistry, biosynthesis and pharmacology of rapamycin analogs. Nat. Prod. Rep. 26, 602-609. https://doi.org/10.1039/b804602f
  15. Guengerich, F. P. (2001) Analysis and characterization of enzymes and nucleic acids. In Principles and Methods of Toxicology (A. W. Hayes, Ed.), pp. 1625-1687. Taylor & Francis, Philadelphia.
  16. Gust, B., Challis, G. L., Fowler, K., Kieser, T. and Chater, K. F. (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. U.S.A. 100, 1541-1546. https://doi.org/10.1073/pnas.0337542100
  17. Han, S., Pham, T. V., Kim, J. H., Lim, Y. R., Park, H. G., Cha, G. S., Yun, C. H., Chun, Y. J., Kang, L. W. and Kim, D. (2015) Functional characterization of CYP107W1 from Streptomyces avermitilis and biosynthesis of macrolide oligomycin A. Arch. Biochem. Biophys. 575, 1-7. https://doi.org/10.1016/j.abb.2015.03.025
  18. Han, S., Pham, T. V., Kim, J. H., Lim, Y. R., Park, H. G., Cha, G. S., Yun, C. H., Chun, Y. J., Kang, L. W. and Kim, D. (2016) Structural analysis of the Streptomyces avermitilis CYP107W1-Oligomycin a complex and role of the Tryptophan 178 residue. Mol. Cells 39, 211-216. https://doi.org/10.14348/molcells.2016.2226
  19. Han, S., Pham, T. V., Kim, J. H., Lim, Y. R., Park, H. G., Jeong, D., Yun, C. H., Chun, Y. J., Kang, L. W. and Kim, D. (2017) Structural insights into the binding of lauric acid to CYP107L2 from Streptomyces avermitilis. Biochem. Biophys. Res. Commun. 482, 902-908. https://doi.org/10.1016/j.bbrc.2016.11.131
  20. He, W., Wu, L., Gao, Q., Du, Y. and Wang, Y. (2006) Identification of AHBA biosynthetic genes related to geldanamycin biosynthesis in Streptomyces hygroscopicus 17997. Curr. Microbiol. 52, 197-203. https://doi.org/10.1007/s00284-005-0203-y
  21. Ikeda, H. (2017) Natural products discovery from micro-organisms in the post-genome era. Biosci. Biotechnol. Biochem. 81, 13-22. https://doi.org/10.1080/09168451.2016.1248366
  22. Ikeda, H., Ishikawa, J., Hanamoto, A., Shinose, M., Kikuchi, H., Shiba, T., Sakaki, Y., Hattori, M. and Omura, S. (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol. 21, 526-531. https://doi.org/10.1038/nbt820
  23. Ikeda, H. and Omura, S. (1997) Avermectin biosynthesis. Chem. Rev. 97, 2591-2610. https://doi.org/10.1021/cr960023p
  24. Jakeman, D. L., Bandi, S., Graham, C. L., Reid, T. R., Wentzell, J. R. and Douglas, S. E. (2009) Antimicrobial activities of jadomycin B and structurally related analogues. Antimicrob. Agents Chemother. 53, 1245-1247. https://doi.org/10.1128/AAC.00801-08
  25. Kumar, Y. and Goodfellow, M. (2008) Five new members of the Streptomyces violaceusniger 16S rRNA gene clade: Streptomyces castelarensis sp. nov., comb. nov., Streptomyces himastatinicus sp. nov., Streptomyces mordarskii sp. nov., Streptomyces rapamycinicus sp. nov. and Streptomyces ruanii sp. nov. Int. J. Syst. Evol. Microbiol. 58, 1369-1378. https://doi.org/10.1099/ijs.0.65408-0
  26. Kumar, Y. and Goodfellow, M. (2010) Reclassification of Streptomyces hygroscopicus strains as Streptomyces aldersoniae sp. nov., Streptomyces angustmyceticus sp. nov., comb. nov., Streptomyces ascomycinicus sp. nov., Streptomyces decoyicus sp. nov., comb. nov., Streptomyces milbemycinicus sp. nov. and Streptomyces wellingtoniae sp. nov. Int. J. Syst. Evol. Microbiol. 60, 769-775. https://doi.org/10.1099/ijs.0.012161-0
  27. Lamb, D. C., Guengerich, F. P., Kelly, S. L. and Waterman, M. R. (2006) Exploiting Streptomyces coelicolor A3(2) P450s as a model for application in drug discovery. Expert Opin. Drug Metab. Toxicol. 2, 27-40. https://doi.org/10.1517/17425255.2.1.27
  28. Lamb, D. C., Ikeda, H., Nelson, D. R., Ishikawa, J., Skaug, T., Jackson, C., Omura, S., Waterman, M. R. and Kelly, S. L. (2003) Cytochrome p450 complement (CYPome) of the avermectin-producer Streptomyces avermitilis and comparison to that of Streptomyces coelicolor A3(2). Biochem. Biophys. Res. Commun. 307, 610-619. https://doi.org/10.1016/S0006-291X(03)01231-2
  29. Lamb, D. C., Lei, L., Zhao, B., Yuan, H., Jackson, C. J., Warrilow, A. G., Skaug, T., Dyson, P. J., Dawson, E. S., Kelly, S. L., Hachey, D. L. and Waterman, M. R. (2010) Streptomyces coelicolor A3(2) CYP102 protein, a novel fatty acid hydroxylase encoded as a heme domain without an N-terminal redox partner. Appl. Environ. Microbiol. 76, 1975-1980. https://doi.org/10.1128/AEM.03000-09
  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. https://doi.org/10.1074/jbc.M111109200
  31. Lamb, D. C., Zhao, B., Guengerich, F. P., Kelly, S. L. and Waterman, M. R. (2011) Genomics of Streptomyces cytochrome P450. In Streptomyces Molecular Biology and Biotechnology (P. Dyson, Ed.), pp. 233-253. Caister Academic Press, Norfolk, UK.
  32. Lee, C. W., Lee, J. H., Rimal, H., Park, H. and Oh, T. J. (2016) Crystal Structure of Cytochrome P450 (CYP105P2) from Streptomyces peucetius and its conformational changes in response to substrate binding. Int. J. Mol. Sci. 17, 813. https://doi.org/10.3390/ijms17060813
  33. Lee, D., Lee, K., Cai, X. F., Dat, N. T., Boovanahalli, S. K., Lee, M., Shin, J. C., Kim, W., Jeong, J. K., Lee, J. S., Lee, C. H., Lee, J. H., Hong, Y. S. and Lee, J. J. (2006) Biosynthesis of the heat-shock protein 90 inhibitor geldanamycin: new insight into the formation of the benzoquinone moiety. Chembiochem. 7, 246-248. https://doi.org/10.1002/cbic.200500441
  34. Lim, Y. R., Han, S., Kim, J. H., Park, H. G., Lee, G. Y., Le, T. K., Yun, C. H. and Kim, D. (2017) Characterization of a Biflaviolin Synthase CYP158A3 from Streptomyces avermitilis and its role in the biosynthesis of secondary metabolites. Biomol. Ther. (Seoul) 25, 171-176. https://doi.org/10.4062/biomolther.2016.182
  35. Lim, Y. R., Hong, M. K., Kim, J. K., Doan, T. T., Kim, D. H., Yun, C. H., Chun, Y. J., Kang, L. W. and Kim, D. (2012) Crystal structure of cytochrome P450 CYP105N1 from Streptomyces coelicolor, an oxidase in the coelibactin siderophore biosynthetic pathway. Arch. Biochem. Biophys. 528, 111-117. https://doi.org/10.1016/j.abb.2012.09.001
  36. Lomovskaya, N., Otten, S. L., Doi-Katayama, Y., Fonstein, L., Liu, X. C., Takatsu, T., Inventi-Solari, A., Filippini, S., Torti, F., Colombo, A. L. and Hutchinson, C. R. (1999) Doxorubicin overproduction in Streptomyces peucetius: cloning and characterization of the dnrU ketoreductase and dnrV genes and the doxA cytochrome P-450 hydroxylase gene. J. Bacteriol. 181, 305-318. https://doi.org/10.1128/JB.181.1.305-318.1999
  37. Madduri, K. and Hutchinson, C. R. (1995) Functional characterization and transcriptional analysis of a gene cluster governing early and late steps in daunorubicin biosynthesis in Streptomyces peucetius. J. Bacteriol. 177, 3879-3884. https://doi.org/10.1128/jb.177.13.3879-3884.1995
  38. McCarthy, A. J. and Williams, S. T. (1992) Actinomycetes as agents of biodegradation in the environment-a review. Gene 115, 189-192. https://doi.org/10.1016/0378-1119(92)90558-7
  39. 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. https://doi.org/10.1016/0378-1119(95)00799-7
  40. Moody, S. C., Zhao, B., Lei, L., Nelson, D. R., Mullins, J. G., Waterman, M. R., Kelly, S. L. and Lamb, D. C. (2012) Investigating conservation of the albaflavenone biosynthetic pathway and CYP170 bifunctionality in Streptomycetes. FEBS J. 279, 1640-1649. https://doi.org/10.1111/j.1742-4658.2011.08447.x
  41. Mukherjee, S. and Mukherjee, U. (2009) A comprehensive review of immunosuppression used for liver transplantation. J. Transplant. 2009, 701464.
  42. Nagano, S., Cupp-Vickery, J. R. and Poulos, T. L. (2005) Crystal structures of the ferrous dioxygen complex of wild-type cytochrome P450eryF and its mutants, A245S and A245T: investigation of the proton transfer system in P450eryF. J. Biol. Chem. 280, 22102-22107. https://doi.org/10.1074/jbc.M501732200
  43. Niraula, N. P., Bhattarai, S., Lee, N. R., Sohng, J. K. and Oh, T. J. (2012) Biotransformation of flavone by CYP105P2 from Streptomyces peucetius. J. Microbiol. Biotechnol. 22, 1059-1065. https://doi.org/10.4014/jmb.1201.01037
  44. Oliynyk, M., Samborskyy, M., Lester, J. B., Mironenko, T., Scott, N., Dickens, S., Haydock, S. F. and Leadlay, P. F. (2007) Complete genome sequence of the erythromycin-producing bacterium Saccharopolyspora erythraea NRRL23338. Nat. Biotechnol. 25, 447-453. https://doi.org/10.1038/nbt1297
  45. Ortiz de Montellano, P. R. (2005) In Cytochrome P450: Structure, Mechanism, and Biochemistry (P. R. Ortiz de Montellano, Ed.). Plenum Press, New York.
  46. Otten, S. L., Liu, X., Ferguson, J. and Hutchinson, C. R. (1995) Cloning and characterization of the Streptomyces peucetius dnrQS genes encoding a daunosamine biosynthesis enzyme and a glycosyl transferase involved in daunorubicin biosynthesis. J. Bacteriol. 177, 6688-6692. https://doi.org/10.1128/jb.177.22.6688-6692.1995
  47. Pandey, B. P., Roh, C., Choi, K. Y., Lee, N., Kim, E. J., Ko, S., Kim, T., Yun, H. and Kim, B. G. (2010) Regioselective hydroxylation of daidzein using P450 (CYP105D7) from Streptomyces avermitilis MA4680. Biotechnol. Bioeng. 105, 697-704. https://doi.org/10.1002/bit.22582
  48. Parajuli, N., Basnet, D. B., Chan Lee, H., Sohng, J. K. and Liou, K. (2004) Genome analyses of Streptomyces peucetius ATCC 27952 for the identification and comparison of cytochrome P450 complement with other Streptomyces. Arch. Biochem. Biophys. 425, 233-241. https://doi.org/10.1016/j.abb.2004.03.011
  49. Podust, L. M., Bach, H., Kim, Y., Lamb, D. C., Arase, M., Sherman, D. H., Kelly, S. L. and Waterman, M. R. (2004) Comparison of the 1.85 A structure of CYP154A1 from Streptomyces coelicolor A3(2) with the closely related CYP154C1 and CYPs from antibiotic biosynthetic pathways. Protein Sci. 13, 255-268. https://doi.org/10.1110/ps.03384804
  50. 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-A structure of Streptomyces coelicolor A3(2) CYP154C1. A new monooxygenase that functionalizes macrolide ring systems. J. Biol. Chem. 278, 12214-12221. https://doi.org/10.1074/jbc.M212210200
  51. Rimal, H., Yu, S. C., Lee, J. H., Tokutaro, Y. and Oh, T. J. (2018) Hydroxylation of Resveratrol with DoxA In Vitro: An Enzyme with the Potential for the Bioconversion of a Bioactive Stilbene. J. Microbiol. Biotechnol. 28, 561-565. https://doi.org/10.4014/jmb.1711.11047
  52. Rudolf, J. D., Chang, C. Y., Ma, M. and Shen, B. (2017) Cytochromes P450 for natural product biosynthesis in Streptomyces: sequence, structure, and function. Nat. Prod. Rep. 34, 1141-1172. https://doi.org/10.1039/C7NP00034K
  53. Savino, C., Montemiglio, L. C., Sciara, G., Miele, A. E., Kendrew, S. G., Jemth, P., Gianni, S. and Vallone, B. (2009) Investigating the structural plasticity of a cytochrome P450: three-dimensional structures of P450 EryK and binding to its physiological substrate. J. Biol. Chem. 284, 29170-29179. https://doi.org/10.1074/jbc.M109.003590
  54. Shafiee, A. and Hutchinson, C. R. (1987) Macrolide antibiotic biosynthesis: isolation and properties of two forms of 6-deoxyerythronolide B hydroxylase from Saccharopolyspora erythraea (Streptomyces erythreus). Biochemistry 26, 6204-6210. https://doi.org/10.1021/bi00393a037
  55. Sherman, D. H., Li, S., Yermalitskaya, L. V., Kim, Y., Smith, J. A., Waterman, M. R. and Podust, L. M. (2006) The structural basis for substrate anchoring, active site selectivity, and product formation by P450 PikC from Streptomyces venezuelae. J. Biol. Chem. 281, 26289-26297. https://doi.org/10.1074/jbc.M605478200
  56. Song, J. Y., Yoo, Y. J., Lim, S. K., Cha, S. H., Kim, J. E., Roe, J. H., Kim, J. F. and Yoon, Y. J. (2016) Complete genome sequence of Streptomyces venezuelae ATCC 15439, a promising cell factory for production of secondary metabolites. J. Biotechnol. 219, 57-58. https://doi.org/10.1016/j.jbiotec.2015.12.028
  57. Stach, J. E. and Bull, A. T. (2005) Estimating and comparing the diversity of marine actinobacteria. Antonie Van Leeuwenhoek 87, 3-9. https://doi.org/10.1007/s10482-004-6524-1
  58. Stassi, D., Donadio, S., Staver, M. J. and Katz, L. (1993) Identification of a Saccharopolyspora erythraea gene required for the final hydroxylation step in erythromycin biosynthesis. J. Bacteriol. 175, 182-189. https://doi.org/10.1128/jb.175.1.182-189.1993
  59. Tian, Z., Cheng, Q., Yoshimoto, F. K., Lei, L., Lamb, D. C. and Guengerich, F. P. (2013) Cytochrome P450 107U1 is required for sporulation and antibiotic production in Streptomyces coelicolor. Arch. Biochem. Biophys. 530, 101-107. https://doi.org/10.1016/j.abb.2013.01.001
  60. Ventura, M., Canchaya, C., Tauch, A., Chandra, G., Fitzgerald, G. F., Chater, K. F. and van Sinderen, D. (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol. Mol. Biol. Rev. 71, 495-548. https://doi.org/10.1128/MMBR.00005-07
  61. Vezina, C., Kudelski, A. and Sehgal, S. N. (1975) Rapamycin (AY- 22,989), a new antifungal antibiotic. I. Taxonomy of the producing streptomycete and isolation of the active principle. J. Antibiot. (Tokyo) 28, 721-726. https://doi.org/10.7164/antibiotics.28.721
  62. Wu, H., Qu, S., Lu, C., Zheng, H., Zhou, X., Bai, L. and Deng, Z. (2012) Genomic and transcriptomic insights into the thermo-regulated biosynthesis of validamycin in Streptomyces hygroscopicus 5008. BMC Genomics 13, 337. https://doi.org/10.1186/1471-2164-13-337
  63. Xu, L. H., Fushinobu, S., Ikeda, H., Wakagi, T. and Shoun, H. (2009) Crystal structures of cytochrome P450 105P1 from Streptomyces avermitilis: conformational flexibility and histidine ligation state. J. Bacteriol. 191, 1211-1219. https://doi.org/10.1128/JB.01276-08
  64. Xu, L. H., Fushinobu, S., Takamatsu, S., Wakagi, T., Ikeda, H. and Shoun, H. (2010) Regio- and stereospecificity of filipin hydroxylation sites revealed by crystal structures of cytochrome P450 105P1 and 105D6 from Streptomyces avermitilis. J. Biol. Chem. 285, 16844-16853. https://doi.org/10.1074/jbc.M109.092460
  65. Xu, L. H., Ikeda, H., Liu, L., Arakawa, T., Wakagi, T., Shoun, H. and Fushinobu, S. (2015) Structural basis for the 4'-hydroxylation of diclofenac by a microbial cytochrome P450 monooxygenase. Appl. Microbiol. Biotechnol. 99, 3081-3091. https://doi.org/10.1007/s00253-014-6148-y
  66. 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. https://doi.org/10.1016/S1074-5521(98)90293-9
  67. 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. U.S.A. 95, 12111-12116. https://doi.org/10.1073/pnas.95.21.12111
  68. Zhao, B., Guengerich, F. P., Voehler, M. and Waterman, M. R. (2005) Role of active site water molecules and substrate hydroxyl groups in oxygen activation by cytochrome P450 158A2: a new mechanism of proton transfer. J. Biol. Chem. 280, 42188-42197. https://doi.org/10.1074/jbc.M509220200
  69. Zhao, B., Lamb, D. C., Lei, L., Kelly, S. L., Yuan, H., Hachey, D. L. and Waterman, M. R. (2007) Different binding modes of two flaviolin substrate molecules in cytochrome P450 158A1 (CYP158A1) compared to CYP158A2. Biochemistry 46, 8725-8733. https://doi.org/10.1021/bi7006959
  70. Zhao, B., Lei, L., Vassylyev, D. G., Lin, X., Cane, D. E., Kelly, S. L., Yuan, H., Lamb, D. C. and Waterman, M. R. (2009) Crystal structure of albaflavenone monooxygenase containing a moonlighting terpene synthase active site. J. Biol. Chem. 284, 36711-36719. https://doi.org/10.1074/jbc.M109.064683
  71. Zhao, B., Moody, S. C., Hider, R. C., Lei, L., Kelly, S. L., Waterman, M. R. and Lamb, D. C. (2012) Structural analysis of cytochrome P450 105N1 involved in the biosynthesis of the zincophore, coelibactin. Int. J. Mol. Sci. 13, 8500-8513. https://doi.org/10.3390/ijms13078500

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