Identification of a cyclosporine-specific P450 hydroxylase gene through targeted cytochrome P450 complement (CYPome) disruption in Sebekia benihana

Applied and Environmental Microbiology

Volumn 79, Issue 7, 2013, Pages 2253-2262

  Lee, Mi Jin ^a   Kim, Hyun Bum ^a   Yoon, Yeo Joon ^b   Han, Kyuboem ^c   Kim, Eung Soo ^a  

^a Inha University   (South Korea)

^b Ewha Womans University   (South Korea)

^c Cha Bio and Diostech Bio Pharmaceutical Research Institute   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTECHNOLOGICAL APPLICATIONS; COMPLEMENTATION; CYTOCHROME P450; ELECTRON TRANSFER; FERREDOXIN REDUCTASE; GENOME SEQUENCING; RARE ACTINOMYCETES; STREPTOMYCES COELICOLOR;

AMINO ACIDS; BACTERIA; ESCHERICHIA COLI; FINITE DIFFERENCE METHOD; GENE EXPRESSION;

HYDROXYLATION;

BACTERIAL DNA; CYCLOSPORIN; CYTOCHROME P450; MIXED FUNCTION OXIDASE;

BACTERIUM; CYTOCHROME; DRUG; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ENGINEERING; MUTATION;

ACTINOMYCETALES; ARTICLE; BACTERIAL GENOME; BIOLOGY; CHEMISTRY; DNA SEQUENCE; ENZYMOLOGY; ESCHERICHIA COLI; GENE INACTIVATION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; STREPTOMYCES COELICOLOR;

ACTINOMYCETALES; COMPUTATIONAL BIOLOGY; CYCLOSPORINE; CYTOCHROME P-450 ENZYME SYSTEM; DNA, BACTERIAL; ESCHERICHIA COLI; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; GENOME, BACTERIAL; MIXED FUNCTION OXYGENASES; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; STREPTOMYCES COELICOLOR;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NONOMURAEA DIETZIAE; STREPTOMYCES COELICOLOR;

EID: 84875552115     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03722-12     Document Type: Article

References (55)

1. Hussain HA, Ward JM. 2003. Enhanced heterologous expression of two Streptomyces griseolus cytochrome P450s and Streptomyces coelicolor ferredoxin reductase as potentially efficient hydroxylation catalysts. Appl. Environ. Microbiol. 69:373-382. doi:10.1128/AEM.69.1.373-382.2003.
2. Vaufrey F, Delort AM, Jeminet G, Dauphin G. 1990. Bioconversion of monensin by a soil bacterium, Sebekia benihana. J. Antibiot. 43:1189-1191.
3. Lamb DC, Skaug T, Song H, Jackson CJ, Podust LM, Waterman MR, Kell DB, Kelly DE, Kelly SL. 2002. The cytochrome P450 complement (CYPome) of Streptomyces coelicolor A3(2). J. Biol. Chem. 277:24000-24005. doi:10.1074/jbc.M111109200.
4. Hopwood DA, Bibb MJ, Chater KF, Kieser T, Bruton CJ, Kieser HM, Lydiate DJ, Smith CP, Ward JM, Schrempf H (ed). 1985. Genetic manipulation of Streptomyces: a laboratory manual. John Innes Foundation, Norwich, United Kingdom.
5. Delort AM, Jeminet G, Sancelme M, Dauphin G. 1988. Microbial conversion of nigericin in three successive steps, by Sebekia benihana. J. Antibiot. 41: 916-924
6. Kuhnt M, Bitsch F, France J, Hofmann H, Sanglier JJ, Traber R. 1996. Microbial biotransformation products of cyclosporin A. J. Antibiot. 49: 781-787.
7. Park NS, Park HJ, Han K, Kim ES. 2004. Isolation and nucleotide sequence characterization of novel cytochrome P450 hydroxylase genes from rare actinomycetes, Sebekia benihana. Korean J. Biotechnol. Bioeng. 19:308-314.
8. Hussein AM, Stuart A, Peters WP. 1995. Protection against chemotherapy- induced alopecia by cyclosporin A in the newborn rat animal model. Dermatology 190:192-196.
9. Paus R, Handjiski B, Eichmüller S, Czarnetzki BM. 1994. Chemotherapy- induced alopecia in mice: induction by cyclophosphamide, inhibition by cyclosporine A, and modulation by dexamethasone. Am. J. Pathol. 144:719-734.
10. Shirai A, Tsunoda H, Tamaoki T, Kamiya T. 2001. Topical application of cyclosporin A induces rapid-remodeling of damaged anagen hair follicles produced in cyclophosphamide administered mice. J. Dermatol. Sci. 27:7-13.
11. Kim SN, Ahn HJ, Lee CW, Lee MH, Kim JH, Kim JI, Kim SJ, Cho HS, Lee HS, Kim HJ. 2004. The use of nonimmunosuppressive [δ-hydroxy- N-methyl-L-leucine4] cyclosporin derivatives for treating hair loss. Patent DE-1392224, WO02/092033 A1.
12. Shirai A, Tsunoda H, Tamaoki T, Kamiya T. 2001. Topical application of cyclosporin A induces rapid-remodeling of damaged anagen hair follicles produced in cyclophosphamide administered mice. J. Dermatol. Sci. 27:7-13.
13. Lee MJ, Han K, Kim ES. 2011. Targeted gene disruption and functional complementation of cytochrome P450 hydroxylase involved in cyclosporin A hydroxylation in Sebekia benihana. J. Microbiol. Biotechnol. 21:14-19.
14. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955-964.
15. Kang SH, Huang J, Lee HN, Hur YA, Cohen SN, Kim ES. 2007. Interspecies DNA microarray analysis identifies WblA as a pleiotropic down-regulator of antibiotic biosynthesis in Streptomyces. J. Bacteriol. 189:4315-4319.
16. Kim SH, Lee HN, Kim HJ, Kim ES. 2011. Transcriptome analysis of an antibiotic downregulator mutant and synergistic actinorhodin stimulation via disruption of a precursor flux regulator in Streptomyces coelicolor. Appl. Environ. Microbiol. 77:1872-1877.
17. Gust B, Challis GL, Fowler K, Kieser T, Chater KF. 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. doi:10.1073/pnas.0337542100.
18. Takano E, White J, Thompson CJ, Bibb MJ. 1995. Construction of thiostrepton-inducible, high-copy-number expression vectors for use in Streptomyces spp. Gene 166:133-137.
19. Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673-679.
20. Lagesen K, Hallin P, RØdland EA, Stærfeldt H, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35:3100-3108.
21. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH. 2007. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23:1282-1288.
22. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL. 2008. GenBank. Nucleic Acids Res. 36:D25-D30.
23. Tatusov RL, Koonin EV, Lipman DJ. 1997. A genomic perspective on protein families. Science 278:631-637.
24. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y. 2008. KEGGfor linking genomes to life and the environment. Nucleic Acids Res. 36:D480-D484.
25. Dawson JH, Holm RH, Trudell JR, Barth G, Linder RE, Bunnenberg E, Djerassi C, Tang SC. 1976. Oxidized cytochrome P-450. 1. Magnetic circular dichroism evidence for thiolate ligation in the substrate-bound form. Implications for the catalytic mechanism. J. Am. Chem. Soc. 98: 3707-3709.
26. Presnell SR, Cohen FE. 1989. Topological distribution of four-alphahelix bundles. Proc. Natl. Acad. Sci. U. S. A. 86:6592-6596.
27. Martinis SA, Atkins WM, Stayton PS, Sligar SG. 1989. A conserved residue of cytochrome P-450 is involved in heme-oxygen stability and activation. J. Am. Chem. Soc. 111:9252-9253.
28. Vidakovic M, Sligar SG, Li H, Poulos TL. 1998. Understanding the role of the essential Asp251 in cytochrome P450cam using site-directed mutagenesis, crystallography, and kinetic solvent isotope effect. Biochemistry 37:9211-9219.
29. Hasemann CA, Kurumbail RG, Boddupalli SS, Peterson JA, Deisenhofer J. 1995. Structure and function of cytochromes P450: a comparative analysis of three crystal structures. Structure 3:41-62.
30. Khatri Y, Hannemann F, Ewen KM, Pistorius D, Perlova O, Kagawa N, Brachmann AO, Müller R, Bernhardt R. 2010. The CYPome of Sorangium cellulosum So ce56 and identification of CYP109D1 as a new fatty acid hydroxylase. Chem. Biol. 17:1295-1305.
31. Agematu H, Matsumoto N, Fujii Y, Kabumoto H, Doi S, Machida K, Ishikawa J, Arisawa A. 2006. Hydroxylation of testosterone by bacterial cytochromes P450 using the Escherichia coli expression system. Biosci. Biotechnol. Biochem. 70:307-311.
32. Sawada N, Sakaki T, Yoneda S, Kusudo T, Shinkyo R, Ohta M, Inouye K. 2004. Conversion of vitamin D3 to 1α,25-dihydroxyvitamin D3 by Streptomyces griseolus cytochrome P450SU-1. Biochem. Biophys. Res. Commun. 320:156-164.
33. Matsuoka T, Miyakoshi S, Tanzawa K, Nakahara K, Hosobuchi M, Serizawa N. 1989. Purification and characterization of cytochrome P-450(sca) from Streptomyces carbophilus. ML-236B (compactin) induces a cytochrome P-450(sca) in Streptomyces carbophilus that hydroxylates ML-236B to pravastatin sodium (CS-514), a tissue-selective inhibitor of 3-hydroxy-3-methylglutaryl-coenzyme-A reductase. Eur. J. Biochem. 184:707-713.
34. Fujii Y, Kabumoto H, Nishimura K, Fujii T, Yanai S, Takeda K, Tamura N, Arisawa A, Tamura T. 2009. Purification, characterization, and directed evolution study of a vitamin D3 hydroxylase from Pseudonocardia autotrophica. Biochem. Biophys. Res. Commun. 385:170-175. doi:10 .1016/j.bbrc.2009.05.033.
35. Kumagai H, Umekita M, Sawa R, Takahashi Y, Arisawa A, Isshiki K, Nishimura Y, Akamatsu Y. 2008. Generation of new benanomicin analogues by biotransformation using Escherichia coli expressing actinomycete cytochrome P450. J. Antibiot. 61:394-399. doi:10.1038/ja.2008.55.
36. Yasutake Y, Fujii Y, Cheon WK, Arisawa A, Tamura T. 2009. Crystallization and preliminary X-ray diffraction studies of vitamin D3 hydroxylase, a novel cytochrome P450 isolated from Pseudonocardia autotrophica. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65:372-375. doi:10 .1107/S1744309109007829.
37. Omura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, Kikuchi H, Shiba T, Sakaki Y, Hattori M. 2001. Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc. Natl. Acad. Sci. U. S. A. 98:12215-12220.
38. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S. 2003. Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol. 21:526-531.
39. Lamb DC, Lei L, Zhao B, Yuan H, Jackson CJ, Warrilow AGS, Skaug T, Dyson PJ, Dawson ES, Kelly SL, Hachey DL, Waterman MR. 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.
40. Nelson DR. 1999. Cytochrome P450 and the individuality of species. Arch. Biochem. Biophys. 369:1-10.
41. Lamb DC, Ikeda H, Nelson DR, Ishikawa J, Skaug T, Jackson C, Omura S, Waterman MR, Kelly SL. 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. doi:10.1016/S0006-291X(03)01231-2.
42. Bernhardt R. 1996. Cytochrome P450: structure, function, and generation of reactive oxygen species. Rev. Physiol. Biochem. Pharmacol. 127: 137-221.
43. Hannemann F, Bichet A, Ewen KM, Bernhardt R. 2007. Cytochrome P450 systems- biological variations of electron transport chains. Biochim. Biophys. Acta 1770:330-344.
44. O'Keefe DP. 1991. Ferredoxins from two sulfonylurea herbicide monooxygenase systems in Streptomyces griseolus. Biochemistry 30:447-455.
45. Lei L, Waterman MR, Fulco AJ, Kelly SL, Lamb DC. 2004. Availability of specific reductases controls the temporal activity of the cytochrome P450 complement of Streptomyces coelicolor A3(2). Proc. Natl. Acad. Sci. U. S. A. 101:494-499.
46. Lee HN, Huang J, Im JH, Kim SH, Noh JH, Cohen SN, Kim ES. 2010. Putative TetR family transcriptional regulator SCO1712 encodes an antibiotic downregulator in Streptomyces coelicolor. Appl. Environ. Microbiol. 76:3039-3043.
47. Borodina I, Siebring J, Zhang J, Smith CP, Van Keulen G, Dijkhuizen L, Nielsen J. 2008. Antibiotic overproduction in Streptomyces coelicolor A3(2) mediated by phosphofructokinase deletion. J. Biol. Chem. 283: 25186-25199.
48. Aspeslet L, Freitag D, Trepanier D, Abel M, Naicker S, Kneteman N, Foster R, Yatscoff R. 2001. ISA TX247: a novel calcineurin inhibitor. Transplant. Proc. 33:1048-1051.
49. Cupp-Vickery JR, Poulos TL. 1995. Structure of cytochrome P450eryF involved in erythromycin biosynthesis. Nat. Struct. Biol. 2:144-153. doi: 10.1038/nsb0295-144.
50. Buchatskii AG, Kazachenko KY, Alexandrov AA. 2001. Cytochrome P450 pattern revision. J. Biomol. Struct. Dyn. 19:273-277.
51. Hanukoglu I, Gutfinger T. 1989. cDNA sequence of adrenodoxin reductase. Identification of NADP-binding sites in oxidoreductases. Eur. J. Biochem. 180:479-484.
52. McLean KJ, Dunford AJ, Neeli R, Driscoll MD, Munro AW. 2007. Structure, function and drug targeting in Mycobacterium tuberculosis cytochrome P450 systems. Arch. Biochem. Biophys. 464:228-240.
53. Sherman DH, Li S, Yermalitskaya LV, Kim Y, Smith JA, Waterman MR, Podust LM. 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.
54. Chun YJ, Shimada T, Sanchez-Ponce R, Martin MV, Lei L, Zhao B, Kelly SL, Waterman MR, Lamb DC, Guengerich FP. 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.
55. Shrestha P, Oh TJ, Niraula NP, Liou K, Yoo JC, Sohng JK. 2010. Characterization of CYP166B1 and its electron transfer system in Streptomyces peucetius var. caesius ATCC 27952. Enzyme Microb. Technol. 46: 372-377.