A natural heme-signature variant of CYP267A1 from Sorangium cellulosum so ce56 executes diverse ω-hydroxylation

FEBS Journal

Volumn 282, Issue 1, 2015, Pages 74-88

  Bernhardt, Rita ^a   Khatri, Yogan ^a   Hannemann, Frank ^a   Girhard, Marco ^b   Kappl, Reinhard ^c   Hutter, Michael ^a   Urlacher, Vlada B ^b  

^a SAARLAND UNIVERSITY   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

Author keywords

CYP267A1; EPR; L366F; Sorangium cellulosum So ce56; hydroxylation

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 CYP267A1; FATTY ACID; LEUCINE; PHENYLALANINE; PROTEIN VARIANT; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; HEME; RECOMBINANT PROTEIN; RETINOIC ACID 4-HYDROXYLASE;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ESCHERICHIA COLI; HYDROXYLATION; MASS FRAGMENTOGRAPHY; MOLECULAR DOCKING; MOLECULAR EVOLUTION; MOLECULAR MODEL; NONHUMAN; OMEGA HYDROXYLATION; OXIDATION REDUCTION STATE; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; SORANGIUM CELLULOSUM; STRUCTURAL HOMOLOGY; ULTRAVIOLET SPECTROSCOPY; AMINO ACID SEQUENCE; ANIMAL; BOVINAE; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYMOLOGY; GENETIC VARIABILITY; GENETICS; METABOLISM; MOLECULAR GENETICS; MYXOCOCCALES; NUCLEOTIDE SEQUENCE; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; SPECTROPHOTOMETRY; STATIC ELECTRICITY;

BACTERIA (MICROORGANISMS); BOVINAE; ESCHERICHIA COLI; POLYANGIUM CELLULOSUM;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CATTLE; CONSERVED SEQUENCE; CYTOCHROME P-450 ENZYME SYSTEM; ELECTRON SPIN RESONANCE SPECTROSCOPY; FATTY ACIDS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENETIC VARIATION; HEME; HYDROXYLATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MYXOCOCCALES; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROPHOTOMETRY; STATIC ELECTRICITY; SUBSTRATE SPECIFICITY;

EID: 84920836932     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13104     Document Type: Article

References (71)

1. Bernhardt R, (2006) Cytochromes P450 as versatile biocatalysts. J Biotechnol 124, 128-145.
2. Bernhardt R, &, Waterman MR, (2007) Cytochrome P450 and steroid hormone biosynthesis. In The Ubiquitous Roles of Cytochrome P450 Proteins. (, Sigel A, Sigel H, &, Sigel RKO, eds), pp. 361-396. John Wiley & Sons Ltd, Chichester, UK.
3. Bernhardt R, &, Urlacher VB, (2014) Cytochromes P450 as promising catalysts for biotechnological application: chances and limitations. Appl Microbiol Biotechnol 98, 6185-6203.
4. Urlacher VB, &, Girhard M, (2012) Cytochrome P450 monooxygenases: an update on perspectives for synthetic application. Trends Biotechnol 30, 26-36.
5. Nelson DR, (2011) Progress in tracing the evolutionary paths of cytochrome P450. Biochim Biophys Acta 1814, 14-18.
6. Nelson DR, (2013) A world of cytochrome P450s. Philos Trans R Soc Lond B Biol Sci 368, 20120430.
7. Presnell SR, &, Cohen FE, (1989) Topological distribution of four-alpha-helix bundles. Proc Natl Acad Sci USA 86, 6592-6596.
8. Johnson EF, &, Stout CD, (2013) Structural diversity of eukaryotic membrane cytochrome p450s. J Biol Chem 288, 17082-17090.
9. Mestres J, (2005) Representativity of target families in the Protein Data Bank: impact for family-directed structure-based drug discovery. Drug Discov Today 10, 1629-1637.
10. Otyepka M, Skopalík J, Anzenbacherová E, &, Anzenbacher P, (2007) What common structural features and variations of mammalian P450s are known to date? Biochim Biophys Acta 1770, 376-389.
11. Stayton PS, Poulos TL, &, Sligar SG, (1989) Putidaredoxin competitively inhibits cytochrome b5-cytochrome P-450cam association: a proposed molecular model for a cytochrome P-450cam electron-transfer complex. Biochemistry 28, 8201-8205.
12. Shimizu T, Hirano K, Takahashi M, Hatano M, &, Fujii-Kuriyama Y, (1988) Site-directed mutageneses of rat liver cytochrome P-450d: axial ligand and heme incorporation. Biochemistry 27, 4138-4141.
13. Porter TD, (1994) Mutagenesis at a highly conserved phenylalanine in cytochrome P450 2E1 affects heme incorporation and catalytic activity. Biochemistry 33, 5942-5946.
14. Ost TW, Miles CS, Munro AW, Murdoch J, Reid GA, &, Chapman SK, (2001) Phenylalanine 393 exerts thermodynamic control over the heme of flavocytochrome P450 BM3. Biochemistry 40, 13421-13429.
15. Chen Z, Ost TW, &, Schelvis JP, (2004) Phe393 mutants of cytochrome P450 BM3 with modified heme redox potentials have altered heme vinyl and propionate conformations. Biochemistry 43, 1798-1808.
16. McLean KJ, Carroll P, Lewis DG, Dunford AJ, Seward HE, Neeli R, Cheesman MR, Marsollier L, Douglas P, Smith WE, et al,. (2008) Characterization of active site structure in CYP121. A cytochrome P450 essential for viability of Mycobacterium tuberculosis H37Rv. J Biol Chem 283, 33406-33416.
17. Perera R, Sono M, Sigman JA, Pfister TD, Lu Y, &, Dawson JH, (2003) Neutral thiol as a proximal ligand to ferrous heme iron: implications for heme proteins that lose cysteine thiolate ligation on reduction. Proc Natl Acad Sci USA 100, 3641-3646.
18. Mosher CM, Hummel MA, Tracy TS, &, Rettie AE, (2008) Functional analysis of phenylalanine residues in the active site of cytochrome P450 2C9. Biochemistry 47, 11725-11734.
19. Ost TW, Munro AW, Mowat CG, Taylor PR, Pesseguiero A, Fulco AJ, Cho AK, Cheesman MA, Walkinshaw MD, &, Chapman SK, (2001) Structural and spectroscopic analysis of the F393H mutant of flavocytochrome P450. Biochemistry 40, 13430-13438.
20. 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.
21. Khatri Y, Hannemann F, Perlova O, Müller R, &, Bernhardt R, (2011) Investigation of cytochromes P450 in myxobacteria: excavation of cytochromes P450 from the genome of Sorangium cellulosum So ce56. FEBS Lett 585, 1506-1513.
22. Khatri Y, Girhard M, Romankiewicz A, Ringle M, Hannemann F, Urlacher VB, Hutter MC, &, Bernhardt R, (2010) Regioselective hydroxylation of norisoprenoids by CYP109D1 from Sorangium cellulosum So ce56. Appl Microbiol Biotechnol 88, 485-495.
23. Khatri Y, Hannemann F, Girhard M, Kappl R, Même A, Ringle M, Janocha S, Leize-Wagner E, Urlacher VB, &, Bernhardt R, (2013) Novel family members of CYP109 from Sorangium cellulosum So ce56 exhibit characteristic biochemical and biophysical properties. Biotechnol Appl Biochem 60, 18-29.
24. Ly TT, Khatri Y, Zapp J, Hutter MC, &, Bernhardt R, (2012) CYP264B1 from Sorangium cellulosum So ce56: a fascinating norisoprenoid and sesquiterpene hydroxylase. Appl Microbiol Biotechnol 95, 123-133.
25. Ringle M, Khatri Y, Zapp J, Hannemann F, &, Bernhardt R, (2013) Application of a new versatile electron transfer system for cytochrome P450-based Escherichia coli whole-cell bioconversions. Appl Microbiol Biotechnol 97, 7741-7754.
26. Hawkes DB, Adams GW, Burlingame AL, Ortiz de Montellano PR, &, De Voss JJ, (2002) Cytochrome P450(cin) (CYP176A), isolation, expression, and characterization. J Biol Chem 277, 27725-27732.
27. Meharenna YT, Li H, Hawkes DB, Pearson AG, De Voss J, &, Poulos TL, (2004) Crystal structure of P450cin in a complex with its substrate, 1,8-cineole, a close structural homologue to D-camphor, the substrate for P450cam. Biochemistry 43, 9487-9494.
28. Spiro TG, (1975) Resonance Raman spectroscopic studies of heme proteins. Biochim Biophys Acta 416, 169-189.
29. Wyer JA, &, Brøndsted NS, (2010) Absorption in the Q-band region by isolated ferric heme+ and heme+(histidine) in vacu. J Chem Phys 133, 084306.
30. Jung C, Ristau O, &, Rein H, (1991) The high-spin/low-spin equilibrium in cytochrome P-450 a new method for determination of the high-spin content. Biochem Biophys Acta 1076, 130-136.
31. Ewen KM, Hannemann F, Khatri Y, Perlova O, Kappl R, Krug D, Hüttermann J, Müller R, &, Bernhardt R, (2009) Genome mining in Sorangium cellulosum So ce56: identification and characterization of the homologous electron transfer proteins of a myxobacterial cytochrome P450. J Biol Chem 284, 28590-28598.
32. Miles JS, Munro AW, Rospendowski BN, Smith WE, McKnight J, &, Thomson AJ, (1992) Domains of the catalytically self-sufficient cytochrome P-450 BM-3. Genetic construction, overexpression, purification and spectroscopic characterization. Biochem J 288, 503-509.
33. Girvan HM, Seward HE, Toogood HS, Cheesman MR, Leys D, &, Munro AW, (2007) Structural and spectroscopic characterization of P450 BM3 mutants with unprecedented P450 heme iron ligand sets. New heme ligation states influence conformational equilibria in P450 BM3. J Biol Chem 282, 564-572.
34. Girvan HM, Toogood HS, Littleford RE, Seward HE, Smith WE, Ekanem IS, Leys D, Cheesman MR, &, Munro AW, (2009) Novel haem co-ordination variants of flavocytochrome P450BM3. Biochem J 417, 65-76.
35. Dawson JA, Andersson L, &, Sono M, (1982) Spectroscopic investigations of ferric cytochrome P-450-CAM ligand complexes. J Biol Chem 257, 3606-3609.
36. Lipscomb JD, (1980) Electron paramagnetic resonance detectable states of cytochrome P-450cam. Biochemistry 19, 3590-3599.
37. Sono M, Andersson LA, &, Dawson JH, (1982) Sulfur donor ligand binding to ferric cytochrome P-450-CAM and myoglobin. Ultraviolet-visible absorption, magnetic circular dichroism, and electron paramagnetic resonance spectroscopic investigation of the complexes. J Biol Chem 257, 8308-8320.
38. Green A, Rivers S, Cheesman M, Reid G, Quaroni L, Macdonald I, Chapman S, &, Munro A, (2001) Expression, purification and characterization of cytochrome P450 BioI: a novel P450 involved in biotin synthesis in Bacillus subtilis. J Biol Inorg Chem 6, 523-533.
39. Lawson RJ, Leys D, Sutcliffe MJ, Kemp CA, Cheesman MR, Smith SJ, Clarkson J, Smith WE, Haq I, Perkins JB, et al,. (2004) Thermodynamic and biophysical characterization of cytochrome P450 BioI from Bacillus subtilis. Biochemistry 43, 12410-12426.
40. Warman AJ, Robinson JW, Luciakova D, Lawrence AD, Marshall KR, Warren MJ, Cheesman MR, Rigby SE, Munro AW, &, McLean KJ, (2012) Characterization of Cupriavidus metallidurans CYP116B1 a thiocarbamate herbicide oxygenating P450-phthalate dioxygenase reductase fusion protein. FEBS J 279, 1675-1693.
41. McLean KJ, Warman AJ, Seward HE, Marshall KR, Girvan HM, Cheesman MR, Waterman MR, &, Munro AW, (2006) Biophysical characterization of the sterol demethylase P450 from Mycobacterium tuberculosis, its cognate ferredoxin, and their interactions. Biochemistry 45, 8427-8443.
42. McLean KJ, Cheesman MR, Rivers SL, Richmond A, Leys D, Chapman SK, Reid GA, Price NC, Kelly SM, Clarkson J, et al,. (2002) Expression, purification and spectroscopic characterization of the cytochrome P450 CYP121 from Mycobacterium tuberculosis. J Inorg Biochem 91, 527-541.
43. Belin P, Le DMH, Fielding A, Lequin O, Jacquet M, Charbonnier JB, Lecoq A, Thai R, Courçon M, Masson C, et al,. (2009) Identification and structural basis of the reaction catalyzed by CYP121, an essential cytochrome P450 in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 106, 7426-7431.
44. Leys D, Mowa CG, McLean KJ, Richmond A, Chapman SK, Walkinshaw MD, &, Munro AW, (2003) Atomic structure of Mycobacterium tuberculosis CYP121 to 1.06 A reveals novel features of cytochrome P450. J Biol Chem 278, 5141-5147.
45. McLean KJ, Lafite P, Levy C, Cheesman MR, Mast N, Pikuleva IA, Leys D, &, Munro AW, (2009) The Structure of Mycobacterium tuberculosis CYP125: molecular basis for cholesterol binding in a P450 needed for host infection. J Biol Chem 284, 35524-35533.
46. Driscoll MD, McLean KJ, Cheesman MR, Jowitt TA, Howard M, Carroll P, Parish T, &, Munro AW, (2011) Expression and characterization of Mycobacterium tuberculosis CYP144: common themes and lessons learned in the M. tuberculosis P450 enzyme family. Biochim Biophys Acta 1814, 76-87.
47. Driscoll MD, McLean KJ, Levy C, Mast N, Pikuleva IA, Lafite P, Rigby SE, Leys D, &, Munro AW, (2010) Structural and biochemical characterization of Mycobacterium tuberculosis CYP142: evidence for multiple cholesterol 27-hydroxylase activities in a human pathogen. J Biol Chem 285, 38270-38282.
48. Bui SH, McLean KJ, Cheesman MR, Bradley JM, Rigby SE, Levy CW, Leys D, &, Munro AW, (2012) Unusual spectroscopic and ligand binding properties of the cytochrome P450-flavodoxin fusion enzyme XplA. J Biol Chem 287, 19699-19714.
49. Belcher J, McLean KJ, Matthews S, Woodward LS, Fisher K, Rigby SE, Nelson DR, Potts D, Baynham MT, Parker DA, et al,. (2014) Structure and biochemical properties of the alkene producing cytochrome P450 OleTJE (CYP152L1) from the Jeotgalicoccus sp 8456 bacterium. J Biol Chem 289, 6535-6550.
50. Fujishiro T, Shoji O, Nagano S, Sugimoto H, Shiro Y, &, Watanabe Y, (2011) Crystal structure of H2O2-dependent cytochrome P450SPalpha with its bound fatty acid substrate: insight into the regioselective hydroxylation of fatty acids at the alpha position. J Biol Chem 286, 29941-29950.
51. Luthra A, Denisov IG, &, Sligar SG, (2011) Spectroscopic features of cytochrome P450 reaction intermediates. Arch Biochem Biophys 507, 26-35.
52. Hobler A, Kagawa N, Hutter MC, Hartmann MF, Wudy SA, Hannemann F, &, Bernhardt R, (2012) Human aldosterone synthase: recombinant expression in E. coli and purification enables a detailed biochemical analysis of the protein on the molecular level. J Steroid Biochem Mol Biol 132, 57-65.
53. Ring WM, Schwär G, &, Bode BH, (2009) Biosynthesis of 2-hydroxy and iso-even fatty acids is connected to sphingolipid formation in myxobacteria. ChemBioChem 10, 2003-2010.
54. Curtis DP, Geyer R, White CD, &, Shimkets JL, (2006) Novel lipids in Myxococcus xanthus and their role in chemotaxis. Environ Microbiol 8, 1935-1949.
55. Kaiser D, (2003) Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1, 45-54.
56. Bode HB, Ring MW, Kaiser D, David AC, Kroppenstedt RM, &, Schwär G, (2006) Straight-chain fatty acids are dispensable in the myxobacterium Myxococcus xanthus for vegetative growth and fruiting body formation. Identification of additional players in the alternative biosynthesis pathway to isovaleryl-CoA in the myxobacterium Myxococcus xanthus. J Bacteriol 188, 5632-5634.
57. English N, Palmer CN, Alworth WL, Kang L, Hughes V, &, Wolf CR, (1997) Fatty acid signals in Bacillus megaterium are attenuated by cytochrome P-450-mediated hydroxylation. Biochem J 327, 363-368.
58. Lu AY, Junk KW, &, Coon MJ, (1969) Resolution of the cytochrome P-450-containing omega-hydroxylation system of liver microsomes into three components. J Biol Chem 244, 3714-3721.
59. Dobritsa AA, Shrestha J, Morant M, Pinot F, Matsuno M, Swanson R, Møller BL, &, Preuss D, (2009) CYP704B1 is a long-chain fatty acid omega-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151, 574-589.
60. Perlova O, Gerth K, Kaiser O, Hans A, &, Müller R, (2006) Identification and analysis of the chivosazol biosynthetic gene cluster from the myxobacterial model strain Sorangium cellulosum So ce56. J Biotechnol 121, 174-191.
61. Uhlmann H, Kraft R, &, Bernhardt R, (1994) C-terminal region of adrenodoxin affects its structural integrity and determines differences in its electron transfer function to cytochrome P-450. J Biol Chem 269, 22557-22564.
62. Sagara Y, Wada A, Takata Y, Waterman MR, Sekimizu K, &, Horiuchi T, (1993) Direct expression of adrenodoxin reductase in Escherichia coli and the functional characterization. Biol Pharm Bull 16, 627-630.
63. Schewe H, Kaup BA, &, Schrader J, (2008) Improvement of P450(BM-3) whole-cell biocatalysis by integrating heterologous cofactor regeneration combining glucose facilitator and dehydrogenase in E. coli. Appl Microbiol Biotechnol 78, 55-65.
64. Omura T, &, Sato R, (1964) The carbon monoxide-binding pigment of liver microsomes. II. Solubilization, purification, and properties. J Biol Chem 239, 2379-2385.
65. Girhard M, Klaus T, Khatri Y, Bernhardt R, &, Urlacher VB, (2010) Characterization of the versatile monooxygenase CYP109B1 from Bacillus subtilis. Appl Microbiol Biotechnol 87, 595-607.
66. Arnold K, Bordoli L, Kopp J, &, Schwede T, (2006) The SWISS-MODEL Workspace: a web-based environment for protein structure homology modeling. Bioinformatics 22, 195-201.
67. Schwede T, Kopp J, Guex N, &, Peitsch MC, (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31, 3381-3385.
68. Guex N, &, Peitsch MC, (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modelling. Electrophoresis 18, 2714-2723.
69. Sanner MF, (1999) Python: a programming language for software integration and development. J Mol Graph Model 17, 57-61.
70. Huey R, Morris GM, Olson AJ, &, Goodsell DS, (2007) A semiempirical free energy force field with charge-based desolvation. J Comput Chem 28, 1145-1152.
71. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, &, Olson AJ, (1998) Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J Comput Chem 19, 1639-1662.