Fk506 maturation involves a cytochrome P450 protein-catalyzed four-electron C-9 oxidation in parallel with a C-31 O-methylation

Journal of Bacteriology

Volumn 195, Issue 9, 2013, Pages 1931-1939

  Chen, Dandan ^a,b   Zhang, Lihan ^c   Pang, Bo ^a   Chen, Jing ^a,c   Xu, Zhinan ^b   Abe, Ikuro ^c   Liu, Wen ^a  

^a SHANGHAI INSTITUTE OF ORGANIC CHEMISTRY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; FBKM PROTEIN; FKBD PROTEIN; METHYLTRANSFERASE; TACROLIMUS; UNCLASSIFIED DRUG;

ANTIFUNGAL ACTIVITY; ARTICLE; ASPERGILLUS TERREUS; CANDIDA ALBICANS; CATALYSIS; ELECTRON; ELECTROSPRAY MASS SPECTROMETRY; FUSARIUM SOLANI; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; METHYLATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OXIDATION; PH; PRIORITY JOURNAL; STREPTOMYCES TSUKUBAENSIS;

BACTERIAL PROTEINS; CYTOCHROME P-450 ENZYME SYSTEM; ELECTRONS; METHYLATION; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; SIROLIMUS; STREPTOMYCES; TACROLIMUS;

STREPTOMYCES TSUKUBAENSIS;

EID: 84876174397     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00033-13     Document Type: Article

References (35)

1. Kino T, Hatanaka H, Hashimoto M, Nishiyama M, Goto T, Okuhara M, Kohsaka M, Aoki H, Imanaka H. 1987. FK-506, a novel immunosuppressant isolated from a Streptomyces. 1. Fermentation, isolation, and physicochemical and biological characteristics. J. Antibiot. 40:1249 -1255.
2. Liu J, Farmer JD, Lane WS, Friedman J, Weissman I, Schreiber SL. 1991. Calcineurin is a common target of cyclophilin-cyclosporine-A and FKBP-FK506 complexes. Cell 66:807- 815.
3. Tocci MJ, Matkovich DA, Collier KA, Kwok P, Dumont F, Lin S, Degudicibus S, Siekierka JJ, Chin J, Hutchinson NI. 1989. The immunosuppressant FK506 selectively inhibits expression of early T-cell activation genes. J. Immunol. 143:718 -726.
4. Foor F, Parent SA, Morin N, Dahl AM, Ramadan N, Chrebet G, Bostian KA, Nielsen JB. 1992. Calcineurin mediates inhibition by FK506 and cyclosporine of recovery from alpha-factor arrest in yeast. Nature 360: 682-684.
5. Kunz J, Hall MN. 1993. Cyclosporine-A, FK506 and rapamycin-more than just immunosuppression. Trends Biochem. Sci. 18:334 -338.
6. Motamedi H, Shafiee A. 1998. The biosynthetic gene cluster for the macrolactone ring of the immunosuppressant FK506. Eur. J. Biochem. 256:528 -534.
7. Mo S, Kim DH, Lee JH, Park JW, Basnet DB, Ban YH, Yoo YJ, Chen SW, Park SR, Choi EA, Kim E, Jin YY, Lee SK, Park JY, Liu YA, Lee MO, Lee KS, Kim SJ, Kim D, Park BC, Lee SG, Kwon HJ, Suh JW, Moore BS, Lim SK, Yoon YJ. 2011. Biosynthesis of the allylmalonyl-CoA extender unit for the FK506 polyketide synthase proceeds through a dedicated polyketide synthase and facilitates the mutasynthesis of analogues. J. Am. Chem. Soc. 133:976 -985.
8. Wu K, Chung L, Revill WP, Katz L, Reeves CD. 2000. The FK520 gene cluster of Streptomyces hygroscopicus var. ascomyceticus (ATCC 14891) contains genes for biosynthesis of unusual polyketide extender units. Gene 251:81-90.
9. Schwecke T, Aparicio JF, Molnar I, Konig A, Khaw LE, Haydock SF, Oliynyk M, Caffrey P, Cortes J, Lester JB, Bohm GA, Staunton J, Leadlay PF. 1995. The biosynthetic gene-cluster for the polyketide immunosuppressant rapamycin. Proc. Natl. Acad. Sci. U. S. A. 92:7839 -7843.
10. Motamedi H, Cai SJ, Shafiee A, Elliston KO. 1997. Structural organization of a multifunctional polyketide synthase involved in the biosynthesis of the macrolide immunosuppressant FK506. Eur. J. Biochem. 244:74 - 80.
11. Andexer JN, Kendrew SG, Nur-e-Alam M, Lazos O, Foster TA, Zimmermann AS, Warneck TD, Suthar D, Coates NJ, Koehn FE, Skotnicki JS, Carter GT, Gregory MA, Martin CJ, Moss SJ, Leadlay PF, Wilkinson B. 2011. Biosynthesis of the immunosuppressants FK506, FK520, and rapamycin involves a previously undescribed family of enzymes acting on chorismate. Proc. Natl. Acad. Sci. U. S. A. 108:4776-4781.
12. Gatto GJ, Boyne MT, Kelleher NL, Walsh CT. 2006. Biosynthesis of pipecolic acid by RapL, a lysine cyclodeaminase encoded in the rapamycin gene cluster. J. Am. Chem. Soc. 128:3838 -3847.
13. Gatto GJ, McLoughlin SM, Kelleher NL, Walsh CT. 2005. Elucidating the substrate specificity and condensation domain activity of FkbP, the FK520 pipecolate-incorporating enzyme. Biochemistry 44:5993- 6002.
14. Carroll BJ, Moss SJ, Bai LQ, Kato Y, Toelzer S, Yu TW, Floss HG. 2002. Identification of a set of genes involved in the formation of the substrate for the incorporation of the unusual "glycolate" chain extension unit in ansamitocin biosynthesis. J. Am. Chem. Soc. 124:4176-4177.
15. Kato Y, Bai LQ, Xue Q, Revill WP, Yu TW, Floss HG. 2002. Functional expression of genes involved in the biosynthesis of the novel polyketide chain extension unit, methoxymalonyl-acyl carrier protein, and engineered biosynthesis of 2-desmethyl-2-methoxy-6-deoxyerythronolide B. J. Am. Chem. Soc. 124:5268 -5269.
16. Goranovic D, Kosec G, Mrak P, Fujs S, Horvat J, Kuscer E, Kopitar G, Petkovic H. 2010. Origin of the allyl group in FK506 biosynthesis. J. Biol. Chem. 285:14292-14300.
17. Chen DD, Zhang Q, Zhang QL, Cen PL, Xu ZN, Liu W. 2012. Improvement of FK506 production in Streptomyces tsukubaensis by genetic enhancement of the supply of unusual polyketide extender units via utilization of two distinct site-specific recombination systems. Appl. Environ. Microbiol. 78:5093-5103.
18. Shafiee A, Motamedi H, Chen T. 1994. Enzymology of FK-506 biosynthesis- purification and characterization of 31-O-desmethylFK-506 Omethyltransferase from Streptomyces sp MA6858. Eur. J. Biochem. 225: 755-764.
19. Shafiee A, Motamedi H, Dumont FJ, Arison BH, Miller RR. 1997. Chemical and biological characterization of two FK506 analogs produced by targeted gene disruption in Streptomyces sp. MA6548. J. Antibiot. 50: 418-423.
20. Motamedi H, Shafiee A, Cai SJ, Streicher SL, Arison BH, Miller RR. 1996. Characterization of methyltransferase and hydroxylase genes involved in the biosynthesis of the immunosuppressants FK506 and FK520. J. Bacteriol. 178:5243-5248.
21. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich, United Kingdom.
22. Liao RJ, Liu W. 2011. Thiostrepton maturation involving a deesterifica-tion-amidation way to process the C-terminally methylated peptide backbone. J. Am. Chem. Soc. 133:2852-2855.
23. Zhang Q, Chen DD, Lin J, Liao RJ, Tong W, Xu ZN, Liu W. 2011. Characterization of NocL involved in thiopeptide nocathiacin I biosynthesis: a [4Fe-4S] cluster and the catalysis of a radical S-adenosylmethionine enzyme. J. Biol. Chem. 286:21287-21294.
24. Lambalot RH, Cane DE, Aparicio JJ, Katz L. 1995. Overproduction and characterization of the erythromycin C-12 hydroxylase, EryK. Biochemistry 34:1858 -1866.
25. Ding W, Deng W, Tang MC, Zhang Q, Tang GL, Bi YR, Liu W. 2010. Biosynthesis of 3-methoxy-5-methyl naphthoic acid and its incorporation into the antitumor antibiotic azinomycin B. Mol. Biosyst. 6:1071-1081.
26. Walsh CT. 2004. Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303:1805-1810.
27. Fischbach MA, Walsh CT. 2006. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem. Rev. 106:3468 -3496.
28. Rix U, Fischer C, Remsing LL, Rohr J. 2002. Modification of post-PKS tailoring steps through combinatorial biosynthesis. Nat. Prod. Rep. 19: 542-580.
29. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J. 1991. Atomic-structure of FKBP-FK506, an immunophilin-immunosuppressant complex. Science 252:839-842.
30. Becker JW, Rotonda J, McKeever BM, Chan HK, Marcy AI, Wiederrecht G, Hermes JD, Springer JP. 1993. FK-506-binding protein-3- dimensional structure of the complex with the antagonist L-685,818. J. Biol. Chem. 268:11335-11339.
31. Gregory MA, Hong H, Lill RE, Gaisser S, Petkovic H, Low L, Sheehan LS, Carletti I, Ready SJ, Ward MJ, Kaja AL, Weston AJ, Challis IR, Leadlay PF, Martin CJ, Wilkinson B, Sheridan RM. 2006. Rapamycin biosynthesis: elucidation of gene product function. Org. Biomol. Chem. 4:3565-3568.
32. Quaderer R, Omura S, Ikeda H, Cane DE. 2006. Pentalenolactone biosynthesis. Molecular cloning and assignment of biochemical function to PtII, a cytochrome p450 of Streptomyces avermitilis. J. Am. Chem. Soc. 128:13036 -13037.
33. Takahashi S, Yeo YS, Zhao YX, O'Maille PE, Greenhagen BT, Noel JP, Coates RM, Chappell J. 2007. Functional characterization of premnaspirodiene oxygenase, a cytochrome P450 catalyzing regio- and stereospecific hydroxylations of diverse sesquiterpene substrates. J. Biol. Chem. 282:31744 -31754.
34. Zhao B, Lin X, Lei L, Lamb DC, Kelly SL, Waterman MR, Cane DE. 2008. Biosynthesis of the sesquiterpene antibiotic albaflavenone in Streptomyces coelicolor A3(2). J. Biol. Chem. 283:8183- 8189.
35. Wood AW, Swinney DC, Thomas PE, Ryan DE, Hall PF, Levin W, Garland WA. 1988. Mechanism of androstenedione formation from testosterone and epitestosterone catalyzed by purified cytochrome-P-450b. J. Biol. Chem. 263:17322-17332.