3eje › Citations

Structural insights from a P450 Carrier Protein complex reveal how specificity is achieved in the P450(BioI) ACP complex.

Cryle MJ, Schlichting I
Proc Natl Acad Sci U S A 105 15696-701 (2008)
Related entries: 3ejb, 3ejd

Cited: 87 times
EuropePMC logo PMID: 18838690

Abstract

Cytochrome P450(BioI) (CYP107H1) from the biotin operon of Bacillus subtilis forms a seven-carbon diacid through a multistep oxidative cleavage of a fatty acid linked to acyl carrier protein (ACP). Crystal structures of P450(BioI) in complex with three different length fatty acyl-ACP (Escherichia coli) ligands show that P450(BioI) binds the fatty acid such as to force the carbon chain into a U-shape above the active site heme. This positions the C7 and C8 carbons for oxidation, with a large additional cavity extending beyond the heme to accommodate the methyl termini of fatty acids beyond the site of cleavage. The structures explain the experimentally observed lack of stereo- and regiospecificity in the hydroxylation and cleavage of free fatty acids. The P450(BioI)-ACP complexes represent the only structurally characterized P450-carrier protein complexes to date, which has allowed the generation of a model of the interaction of the vancomycin biosynthetic P450 OxyB with its proposed carrier protein bound substrate.

Reviews - 3eje mentioned but not cited (1)

  1. Fatty acid biosynthesis revisited: structure elucidation and metabolic engineering. Beld J, Lee DJ, Burkart MD. Mol Biosyst 11 38-59 (2015)

Articles - 3eje mentioned but not cited (2)

  1. Structural insights from a P450 Carrier Protein complex reveal how specificity is achieved in the P450(BioI) ACP complex. Cryle MJ, Schlichting I. Proc. Natl. Acad. Sci. U.S.A. 105 15696-15701 (2008)
  2. Structure-Function Analysis of the Biotechnologically Important Cytochrome P450 107 (CYP107) Enzyme Family. Padayachee T, Lamb DC, Nelson DR, Syed K. Biomolecules 13 1733 (2023)


Reviews citing this publication (16)

  1. Diversity of P450 enzymes in the biosynthesis of natural products. Podust LM, Sherman DH. Nat Prod Rep 29 1251-1266 (2012)
  2. The structural role of the carrier protein--active controller or passive carrier. Crosby J, Crump MP. Nat Prod Rep 29 1111-1137 (2012)
  3. Closing in on complete pathways of biotin biosynthesis. Lin S, Cronan JE. Mol Biosyst 7 1811-1821 (2011)
  4. Conformational plasticity and structure/function relationships in cytochromes P450. Pochapsky TC, Kazanis S, Dang M. Antioxid. Redox Signal. 13 1273-1296 (2010)
  5. The chain-flipping mechanism of ACP (acyl carrier protein)-dependent enzymes appears universal. Cronan JE. Biochem. J. 460 157-163 (2014)
  6. Using modern tools to probe the structure-function relationship of fatty acid synthases. Finzel K, Lee DJ, Burkart MD. Chembiochem 16 528-547 (2015)
  7. Synthesis of the α,ω-dicarboxylic acid precursor of biotin by the canonical fatty acid biosynthetic pathway. Cronan JE, Lin S. Curr Opin Chem Biol 15 407-413 (2011)
  8. Understanding the crucial interactions between Cytochrome P450s and non-ribosomal peptide synthetases during glycopeptide antibiotic biosynthesis. Peschke M, Gonsior M, Süssmuth RD, Cryle MJ. Curr. Opin. Struct. Biol. 41 46-53 (2016)
  9. Carrier protein substrates in cytochrome P450-catalysed oxidation. Cryle MJ. Metallomics 3 323-326 (2011)
  10. Diversity of nature's assembly lines - recent discoveries in non-ribosomal peptide synthesis. Payne JA, Schoppet M, Hansen MH, Cryle MJ. Mol Biosyst 13 9-22 (2016)
  11. Expansion of chemical space for natural products by uncommon P450 reactions. Zhang X, Li S. Nat Prod Rep 34 1061-1089 (2017)
  12. Unrivalled diversity: the many roles and reactions of bacterial cytochromes P450 in secondary metabolism. Greule A, Stok JE, De Voss JJ, Cryle MJ. Nat Prod Rep 35 757-791 (2018)
  13. Formation and Cleavage of C-C Bonds by Enzymatic Oxidation-Reduction Reactions. Guengerich FP, Yoshimoto FK. Chem. Rev. 118 6573-6655 (2018)
  14. Cytochrome P450 Enzymes and Drug Metabolism in Humans. Zhao M, Ma J, Li M, Zhang Y, Jiang B, Zhao X, Huai C, Shen L, Zhang N, He L, Qin S. Int J Mol Sci 22 12808 (2021)
  15. The many faces and important roles of protein-protein interactions during non-ribosomal peptide synthesis. Izoré T, Cryle MJ. Nat Prod Rep 35 1120-1139 (2018)
  16. Cytochrome P450s in algae: Bioactive natural product biosynthesis and light-driven bioproduction. Zheng S, Guo J, Cheng F, Gao Z, Du L, Meng C, Li S, Zhang X. Acta Pharm Sin B 12 2832-2844 (2022)

Articles citing this publication (68)

  1. Trapping the dynamic acyl carrier protein in fatty acid biosynthesis. Nguyen C, Haushalter RW, Lee DJ, Markwick PR, Bruegger J, Caldara-Festin G, Finzel K, Jackson DR, Ishikawa F, O'Dowd B, McCammon JA, Opella SJ, Tsai SC, Burkart MD. Nature 505 427-431 (2014)
  2. Biotin synthesis begins by hijacking the fatty acid synthetic pathway. Lin S, Hanson RE, Cronan JE. Nat. Chem. Biol. 6 682-688 (2010)
  3. X-domain of peptide synthetases recruits oxygenases crucial for glycopeptide biosynthesis. Haslinger K, Peschke M, Brieke C, Maximowitsch E, Cryle MJ. Nature 521 105-109 (2015)
  4. Human cytochrome P450 2E1 structures with fatty acid analogs reveal a previously unobserved binding mode. Porubsky PR, Battaile KP, Scott EE. J. Biol. Chem. 285 22282-22290 (2010)
  5. Probiotic Bifidobacterium longum alters gut luminal metabolism through modification of the gut microbial community. Sugahara H, Odamaki T, Fukuda S, Kato T, Xiao JZ, Abe F, Kikuchi J, Ohno H. Sci Rep 5 13548 (2015)
  6. Structure of the enzyme-acyl carrier protein (ACP) substrate gatekeeper complex required for biotin synthesis. Agarwal V, Lin S, Lukk T, Nair SK, Cronan JE. Proc. Natl. Acad. Sci. U.S.A. 109 17406-17411 (2012)
  7. The structure of a transient complex of a nonribosomal peptide synthetase and a cytochrome P450 monooxygenase. Haslinger K, Brieke C, Uhlmann S, Sieverling L, Süssmuth RD, Cryle MJ. Angew. Chem. Int. Ed. Engl. 53 8518-8522 (2014)
  8. Chasing acyl carrier protein through a catalytic cycle of lipid A production. Masoudi A, Raetz CR, Zhou P, Pemble CW. Nature 505 422-426 (2014)
  9. Structural characterization of OxyD, a cytochrome P450 involved in beta-hydroxytyrosine formation in vancomycin biosynthesis. Cryle MJ, Meinhart A, Schlichting I. J. Biol. Chem. 285 24562-24574 (2010)
  10. Cytochrome P450 OxyBtei catalyzes the first phenolic coupling step in teicoplanin biosynthesis. Haslinger K, Maximowitsch E, Brieke C, Koch A, Cryle MJ. Chembiochem 15 2719-2728 (2014)
  11. Structural evidence for enhancement of sequential vitamin D3 hydroxylation activities by directed evolution of cytochrome P450 vitamin D3 hydroxylase. Yasutake Y, Fujii Y, Nishioka T, Cheon WK, Arisawa A, Tamura T. J. Biol. Chem. 285 31193-31201 (2010)
  12. Structure-based analysis of the molecular interactions between acyltransferase and acyl carrier protein in vicenistatin biosynthesis. Miyanaga A, Iwasawa S, Shinohara Y, Kudo F, Eguchi T. Proc. Natl. Acad. Sci. U.S.A. 113 1802-1807 (2016)
  13. Contributions of the peroxisome and β-oxidation cycle to biotin synthesis in fungi. Magliano P, Flipphi M, Arpat BA, Delessert S, Poirier Y. J. Biol. Chem. 286 42133-42140 (2011)
  14. Structures of the human mitochondrial ribosome in native states of assembly. Brown A, Rathore S, Kimanius D, Aibara S, Bai XC, Rorbach J, Amunts A, Ramakrishnan V. Nat. Struct. Mol. Biol. 24 866-869 (2017)
  15. Sequential In Vitro Cyclization by Cytochrome P450 Enzymes of Glycopeptide Antibiotic Precursors Bearing the X-Domain from Nonribosomal Peptide Biosynthesis. Brieke C, Peschke M, Haslinger K, Cryle MJ. Angew. Chem. Int. Ed. Engl. 54 15715-15719 (2015)
  16. Engineering biotin prototrophic Corynebacterium glutamicum strains for amino acid, diamine and carotenoid production. Peters-Wendisch P, Götker S, Heider SA, Komati Reddy G, Nguyen AQ, Stansen KC, Wendisch VF. J. Biotechnol. 192 Pt B 346-354 (2014)
  17. Plasmodium falciparum acyl carrier protein crystal structures in disulfide-linked and reduced states and their prevalence during blood stage growth. Gallagher JR, Prigge ST. Proteins 78 575-588 (2010)
  18. Structure of a dinuclear iron cluster-containing β-hydroxylase active in antibiotic biosynthesis. Makris TM, Knoot CJ, Wilmot CM, Lipscomb JD. Biochemistry 52 6662-6671 (2013)
  19. Development of biotin-prototrophic and -hyperauxotrophic Corynebacterium glutamicum strains. Ikeda M, Miyamoto A, Mutoh S, Kitano Y, Tajima M, Shirakura D, Takasaki M, Mitsuhashi S, Takeno S. Appl. Environ. Microbiol. 79 4586-4594 (2013)
  20. Structural analysis of HmtT and HmtN involved in the tailoring steps of himastatin biosynthesis. Zhang H, Chen J, Wang H, Xie Y, Ju J, Yan Y, Zhang H. FEBS Lett. 587 1675-1680 (2013)
  21. Structure-function analysis of the acyl carrier protein synthase (AcpS) from Mycobacterium tuberculosis. Dym O, Albeck S, Peleg Y, Schwarz A, Shakked Z, Burstein Y, Zimhony O. J. Mol. Biol. 393 937-950 (2009)
  22. The 1.5-A structure of XplA-heme, an unusual cytochrome P450 heme domain that catalyzes reductive biotransformation of royal demolition explosive. Sabbadin F, Jackson R, Haider K, Tampi G, Turkenburg JP, Hart S, Bruce NC, Grogan G. J. Biol. Chem. 284 28467-28475 (2009)
  23. Crystal structure of a phenol-coupling P450 monooxygenase involved in teicoplanin biosynthesis. Li Z, Rupasinghe SG, Schuler MA, Nair SK. Proteins 79 1728-1738 (2011)
  24. More than just recruitment: the X-domain influences catalysis of the first phenolic coupling reaction in A47934 biosynthesis by Cytochrome P450 StaH. Ulrich V, Peschke M, Brieke C, Cryle MJ. Mol Biosyst 12 2992-3004 (2016)
  25. Structural insights into the mechanism for recognizing substrate of the cytochrome P450 enzyme TxtE. Yu F, Li M, Xu C, Wang Z, Zhou H, Yang M, Chen Y, Tang L, He J. PLoS ONE 8 e81526 (2013)
  26. The crystal structure of the versatile cytochrome P450 enzyme CYP109B1 from Bacillus subtilis. Zhang A, Zhang T, Hall EA, Hutchinson S, Cryle MJ, Wong LL, Zhou W, Bell SG. Mol Biosyst 11 869-881 (2015)
  27. Pimelic acid, the first precursor of the Bacillus subtilis biotin synthesis pathway, exists as the free acid and is assembled by fatty acid synthesis. Manandhar M, Cronan JE. Mol. Microbiol. 104 595-607 (2017)
  28. Structure of OxyA tei: completing our picture of the glycopeptide antibiotic producing Cytochrome P450 cascade. Haslinger K, Cryle MJ. FEBS Lett. 590 571-581 (2016)
  29. The pimeloyl-CoA synthetase BioW defines a new fold for adenylate-forming enzymes. Estrada P, Manandhar M, Dong SH, Deveryshetty J, Agarwal V, Cronan JE, Nair SK. Nat. Chem. Biol. 13 668-674 (2017)
  30. Adaptation of aminoacyl-tRNA synthetase catalytic core to carrier protein aminoacylation. Mocibob M, Ivic N, Luic M, Weygand-Durasevic I. Structure 21 614-626 (2013)
  31. Structure of the quinoline N-hydroxylating cytochrome P450 RauA, an essential enzyme that confers antibiotic activity on aurachin alkaloids. Yasutake Y, Kitagawa W, Hata M, Nishioka T, Ozaki T, Nishiyama M, Kuzuyama T, Tamura T. FEBS Lett. 588 105-110 (2014)
  32. Using the pimeloyl-CoA synthetase adenylation fold to synthesize fatty acid thioesters. Wang M, Moynié L, Harrison PJ, Kelly V, Piper A, Naismith JH, Campopiano DJ. Nat. Chem. Biol. 13 660-667 (2017)
  33. Biochemical and structural characterisation of the second oxidative crosslinking step during the biosynthesis of the glycopeptide antibiotic A47934. Ulrich V, Brieke C, Cryle MJ. Beilstein J Org Chem 12 2849-2864 (2016)
  34. Biotin, a universal and essential cofactor: synthesis, ligation and regulation. Sirithanakorn C, Cronan JE. FEMS Microbiol Rev 45 fuab003 (2021)
  35. Crystallization and preliminary X-ray diffraction studies of vitamin D3 hydroxylase, a novel cytochrome P450 isolated from Pseudonocardia autotrophica. Yasutake Y, Fujii Y, Cheon WK, Arisawa A, Tamura T. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65 372-375 (2009)
  36. Comparative Analyses of Cytochrome P450s and Those Associated with Secondary Metabolism in Bacillus Species. Mthethwa BC, Chen W, Ngwenya ML, Kappo AP, Syed PR, Karpoormath R, Yu JH, Nelson DR, Syed K. Int J Mol Sci 19 (2018)
  37. Letter Direct protein-protein interactions and substrate channeling between cellular retinoic acid binding proteins and CYP26B1. Nelson CH, Peng CC, Lutz JD, Yeung CK, Zelter A, Isoherranen N. FEBS Lett. 590 2527-2535 (2016)
  38. Importance of the long-chain fatty acid beta-hydroxylating cytochrome P450 enzyme YbdT for lipopeptide biosynthesis in Bacillus subtilis strain OKB105. Youssef NH, Wofford N, McInerney MJ. Int J Mol Sci 12 1767-1786 (2011)
  39. Probing the Substrate Specificity and Protein-Protein Interactions of the E. coli Fatty Acid Dehydratase, FabA. Finzel K, Nguyen C, Jackson DR, Gupta A, Tsai SC, Burkart MD. Chem. Biol. 22 1453-1460 (2015)
  40. Solution structure of 4'-phosphopantetheine - GmACP3 from Geobacter metallireducens: a specialized acyl carrier protein with atypical structural features and a putative role in lipopolysaccharide biosynthesis. Ramelot TA, Smola MJ, Lee HW, Ciccosanti C, Hamilton K, Acton TB, Xiao R, Everett JK, Prestegard JH, Montelione GT, Kennedy MA. Biochemistry 50 1442-1453 (2011)
  41. A Canonical Biotin Synthesis Enzyme, 8-Amino-7-Oxononanoate Synthase (BioF), Utilizes Different Acyl Chain Donors in Bacillus subtilis and Escherichia coli. Manandhar M, Cronan JE. Appl. Environ. Microbiol. 84 (2018)
  42. A Promiscuous Cytochrome P450 Hydroxylates Aliphatic and Aromatic C-H Bonds of Aromatic 2,5-Diketopiperazines. Jiang G, Zhang Y, Powell MM, Hylton SM, Hiller NW, Loria R, Ding Y. Chembiochem 20 1068-1077 (2019)
  43. Carrier Protein-Free Enzymatic Biaryl Coupling in Arylomycin A2 Assembly and Structure of the Cytochrome P450 AryC. Aldemir H, Shu S, Schaefers F, Hong H, Richarz R, Harteis S, Einsiedler M, Milzarek TM, Schneider S, Gulder TAM. Chemistry 28 e202103389 (2022)
  44. Enzyme-substrate complementarity governs access to a cationic reaction manifold in the P450(BM3)-catalysed oxidation of cyclopropyl fatty acids. Cryle MJ, Hayes PY, De Voss JJ. Chemistry 18 15994-15999 (2012)
  45. In Vivo Roles of Fatty Acid Biosynthesis Enzymes in Biosynthesis of Biotin and α-Lipoic Acid in Corynebacterium glutamicum. Ikeda M, Nagashima T, Nakamura E, Kato R, Ohshita M, Hayashi M, Takeno S. Appl. Environ. Microbiol. 83 (2017)
  46. Isolation and structure elucidation of lipopeptide antibiotic taromycin B from the activated taromycin biosynthetic gene cluster. Reynolds KA, Luhavaya H, Li J, Dahesh S, Nizet V, Yamanaka K, Moore BS. J. Antibiot. 71 333-338 (2018)
  47. Ketonization of Proline Residues in the Peptide Chains of Actinomycins by a 4-Oxoproline Synthase. Semsary S, Crnovčić I, Driller R, Vater J, Loll B, Keller U. Chembiochem 19 706-715 (2018)
  48. Membrane fluidity adjusts the insertion of the transacylase PlsX to regulate phospholipid biosynthesis in Gram-positive bacteria. Sastre DE, Basso LGM, Trastoy B, Cifuente JO, Contreras X, Gueiros-Filho F, de Mendoza D, Navarro MVAS, Guerin ME. J Biol Chem 295 2136-2147 (2020)
  49. Preliminary kinetic analysis of acyl carrier protein-ketoacylsynthase interactions in the actinorhodin minimal polyketide synthase. Beltran-Alvarez P, Arthur CJ, Cox RJ, Crosby J, Crump MP, Simpson TJ. Mol Biosyst 5 511-518 (2009)
  50. 3,6-Dichlorosalicylate Catabolism Is Initiated by the DsmABC Cytochrome P450 Monooxygenase System in Rhizorhabdus dicambivorans Ndbn-20. Li N, Yao L, He Q, Qiu J, Cheng D, Ding D, Tao Q, He J, Jiang J. Appl. Environ. Microbiol. 84 (2018)
  51. An Unprecedented Number of Cytochrome P450s Are Involved in Secondary Metabolism in Salinispora Species. Malinga NA, Nzuza N, Padayachee T, Syed PR, Karpoormath R, Gront D, Nelson DR, Syed K. Microorganisms 10 871 (2022)
  52. Bacterial CYP154C8 catalyzes carbon-carbon bond cleavage in steroids. Dangi B, Oh TJ. FEBS Lett 593 67-79 (2019)
  53. BioWF: A Naturally-Fused, Di-Domain Biocatalyst from Biotin Biosynthesis Displays an Unexpectedly Broad Substrate Scope. Richardson SM, Harrison PJ, Herrera MA, Wang M, Verez R, Ortiz GP, Campopiano DJ. Chembiochem 23 e202200171 (2022)
  54. Biochemical and structural characterization of the BioZ enzyme engaged in bacterial biotin synthesis pathway. Zhang S, Xu Y, Guan H, Cui T, Liao Y, Wei W, Li J, Hassan BH, Zhang H, Jia X, Ouyang S, Feng Y. Nat Commun 12 2056 (2021)
  55. Three enigmatic BioH isoenzymes are programmed in the early stage of mycobacterial biotin synthesis, an attractive anti-TB drug target. Xu Y, Yang J, Li W, Song S, Shi Y, Wu L, Sun J, Hou M, Wang J, Jia X, Zhang H, Huang M, Lu T, Gan J, Feng Y. PLoS Pathog 18 e1010615 (2022)
  56. A Moraxella Virulence Factor Catalyzes an Essential Esterase Reaction of Biotin Biosynthesis. Zeng Q, Yang Q, Jia J, Bi H. Front Microbiol 11 148 (2020)
  57. Chimeric Fatty Acyl-Acyl Carrier Protein Thioesterases Provide Mechanistic Insight into Enzyme Specificity and Expression. Ziesack M, Rollins N, Shah A, Dusel B, Webster G, Silver PA, Way JC. Appl. Environ. Microbiol. 84 (2018)
  58. Cytochrome P450 168A1 from Pseudomonas aeruginosa is involved in the hydroxylation of biologically relevant fatty acids. Price CL, Warrilow AGS, Rolley NJ, Parker JE, Thoss V, Kelly DE, Corcionivoschi N, Kelly SL. PLoS One 17 e0265227 (2022)
  59. Discovery of the Azaserine Biosynthetic Pathway Uncovers a Biological Route for α-Diazoester Production. Van Cura D, Ng TL, Huang J, Hager H, Hartwig JF, Keasling JD, Balskus EP. Angew Chem Int Ed Engl 62 e202304646 (2023)
  60. Engineering C-C Bond Cleavage Activity into a P450 Monooxygenase Enzyme. Miller JC, Lee JHZ, Mclean MA, Chao RR, Stone ISJ, Pukala TL, Bruning JB, De Voss JJ, Schuler MA, Sligar SG, Bell SG. J Am Chem Soc 145 9207-9222 (2023)
  61. Impact of lifestyle on cytochrome P450 monooxygenase repertoire is clearly evident in the bacterial phylum Firmicutes. Padayachee T, Nzuza N, Chen W, Nelson DR, Syed K. Sci Rep 10 13982 (2020)
  62. Insights into Thiotemplated Pyrrole Biosynthesis Gained from the Crystal Structure of Flavin-Dependent Oxidase in Complex with Carrier Protein. Thapa HR, Robbins JM, Moore BS, Agarwal V. Biochemistry 58 918-929 (2019)
  63. P450-mediated dehydrotyrosine formation during WS9326 biosynthesis proceeds via dehydrogenation of a specific acylated dipeptide substrate. Zhang S, Zhang L, Greule A, Tailhades J, Marschall E, Prasongpholchai P, Leng DJ, Zhang J, Zhu J, Kaczmarski JA, Schittenhelm RB, Einsle O, Jackson CJ, Alberti F, Bechthold A, Zhang Y, Tosin M, Si T, Cryle MJ. Acta Pharm Sin B 13 3561-3574 (2023)
  64. Path to Actinorhodin: Regio- and Stereoselective Ketone Reduction by a Type II Polyketide Ketoreductase Revealed in Atomistic Detail. Serapian SA, Crosby J, Crump MP, van der Kamp MW. JACS Au 2 972-984 (2022)
  65. SNaPe: a versatile method to generate multiplexed protein fusions using synthetic linker peptides for in vitro applications. Ulrich V, Cryle MJ. J. Pept. Sci. 23 16-27 (2017)
  66. Specificity and mechanism of carbohydrate demethylation by cytochrome P450 monooxygenases. Robb CS, Reisky L, Bornscheuer UT, Hehemann JH. Biochem. J. 475 3875-3886 (2018)
  67. Structure of putative tumor suppressor ALDH1L1. Tsybovsky Y, Sereda V, Golczak M, Krupenko NI, Krupenko SA. Commun Biol 5 3 (2022)
  68. Structure-guided manipulation of the regioselectivity of the cyclosporine A hydroxylase CYP-sb21 from Sebekia benihana. Li F, Ma L, Zhang X, Chen J, Qi F, Huang Y, Qu Z, Yao L, Zhang W, Kim ES, Li S. Synth Syst Biotechnol 5 236-243 (2020)


Quick links