Identification of universal selectivity-determining positions in cytochrome P450 monooxygenases by systematic sequence-based literature mining

Proteins: Structure, Function and Bioinformatics

Volumn 83, Issue 9, 2015, Pages 1593-1603

  Gricman, Łukasz ^a   Vogel, Constantin ^a   Pleiss, Jürgen ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

Author keywords

CYP; Data mining; Database; Hotspot; Mutant

Indexed keywords

ALDOSTERONE SYNTHASE; CYTOCHROME P450; CYTOCHROME P450 2D6; CYTOCHROME P450 BM3; UNSPECIFIC MONOOXYGENASE; ISOENZYME;

ALGORITHM; AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; DATA MINING; ENZYME SPECIFICITY; HUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MUTATION; NUCLEIC ACID DATABASE; NUCLEOTIDE SEQUENCE; PROCEDURES; PROTEIN DATABASE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ALGORITHMS; BASE SEQUENCE; BINDING SITES; CYTOCHROME P-450 ENZYME SYSTEM; DATA MINING; DATABASES, NUCLEIC ACID; DATABASES, PROTEIN; ISOENZYMES; MODELS, MOLECULAR; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84939494127     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24840     Document Type: Article

References (72)

1. Ortiz de Montellano PR. Cytochrome P450: Structure, mechanism, and biochemistry, 3rd ed. New York: Kulwer Academic/Plenum Publishers; 2005.
2. Urlacher VB, Eiben S. Cytochrome P450 monooxygenases: perspectives for synthetic application. Trends Biotechnol 2006;24:324-330.
3. Nebert DW, Russell DW. Clinical importance of the cytochromes P450. Lancet 2002;360:1155-1162.
4. Danielson PB. The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. Current Drug Metabolism 2002;3:561-597.
5. Smith DA, Ackland MJ, Jones BC. Properties of cytochrome P450 isoenzymes and their substrates Part 1: active site characteristics. Drug Discov Today 1997;2:406-414.
6. Hasemann CA, Kurumbail RG, Boddupalli SS, Peterson JA, Deisenhofer J. Structure and function of cytochromes P450:a comparative analysis of three crystal structures. Structure 1995;3:41-62.
7. Poulos TL, Finzel BC, Howard AJ. High-resolution crystal structure of cytochrome P450cam. J Mol Biol 1987;195:687-700.
8. Gotoh O. Substrate recognition sites in cytochrome P450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences. J Biol Chem 1992;267:83-90.
9. Seifert A, Pleiss J. Identification of selectivity-determining residues in cytochrome P450 monooxygenases: a systematic analysis of the substrate recognition site 5. Proteins 2009;74:1028-1035.
10. Gricman Ł, Vogel C, Pleiss J. Conservation analysis of class-specific positions in cytochrome P450 monooxygenases: functional and structural relevance. Proteins 2014;82:491-504.
11. Seifert A, Vomund S, Grohmann K, Kriening S, Urlacher VB, Laschat S, Pleiss J. Rational design of a minimal and highly enriched CYP102A1 mutant library with improved regio-, stereo- and chemoselectivity. Chembiochem 2009;10:853-861.
12. Sirim D, Widmann M, Wagner F, Pleiss J. Prediction and analysis of the modular structure of cytochrome P450 monooxygenases. BMC Struct Biol 2010;10:34.
13. Hannemann F, Bichet A, Ewen KM, Bernhardt R. Cytochrome P450 systems-biological variations of electron transport chains. Biochim Biophys Acta 2007;1770:330-344.
14. Vogel C, Widmann M, Pohl M, Pleiss J. A standard numbering scheme for thiamine diphosphate-dependent decarboxylases. BMC Biochem 2012;13:24.
15. Rebholz-Schuhmann D, Marcel S, Albert S, Tolle R, Casari G, Kirsch H. Automatic extraction of mutations from Medline and cross-validation with OMIM. Nucleic Acids Res 2004;32:135-142.
16. Kuipers R, van den Bergh T, Joosten H-J, Lekanne dit Deprez RH, Mannens MM, Schaap PJ. Novel tools for extraction and validation of disease-related mutations applied to Fabry disease. Hum Mutat 2010;31:1026-1032.
17. Lee LC, Horn F, Cohen FE. Automatic extraction of protein point mutations using a graph bigram association. PLoS Comp Biol 2007;3:e16.
18. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res 2011;39(Database issue):D32-D37.
19. Nebert DW, Nelson DR, Adesnik M, Coon MJ, Estabrook RW, Gonzalez FJ, Guengerich FP, Gunsalus IC, Johnson EF, Kemper B. The P450 superfamily: updated listing of all genes and recommended nomenclature for the chromosomal loci. DNA 1989;8:1-13.
20. Vogel C, Pleiss J. The modular structure of ThDP-dependent enzymes. Proteins 2014;82:2523-2537.
21. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinform 2009;10:421.
22. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000;28:235-242.
23. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England) 2010;26:2460-2461.
24. Needleman SB, Wunsch CD. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 1970;48:443-453.
25. Vogel C, Reusch W, Pohl M, Rother D, Pleiss J. BioCatNet: a system for the analysis of sequence-structure-function relationships of protein families. Submitted.
26. Sayers E. A General Introduction to the E-utilities. 2010. Available at: http://www.ncbi.nlm.nih.gov/books/NBK25501/
27. Monk BC, Tomasiak TM, Keniya M V, Huschmann FU, Tyndall JDA, O'Connell JD, Cannon RD, McDonald JG, Rodriguez A, Finer-Moore JS, Stroud RM. Architecture of a single membrane spanning cytochrome P450 suggests constraints that orient the catalytic domain relative to a bilayer. Proc Natl Acad Sci USA 2014;111:3865-3870.
28. Whitehouse CJC, Bell SG, Wong L-L. P450(BM3) (CYP102A1): connecting the dots. Chem Soc Rev 2012;41:1218-1260.
29. Yu A, Idle JR, Gonzalez DFJ. Polymorphic cytochrome P450 2D6: humanized mouse model and endogenous substrates. Drug Metab Rev 2004;36:243-277.
30. Paine MJI, McLaughlin LA, Flanagan JU, Kemp CA, Sutcliffe MJ, Roberts GCK, Wolf CR. Residues glutamate 216 and aspartate 301 are key determinants of substrate specificity and product regioselectivity in cytochrome P450 2D6. J Biol Chem 2003;278:4021-4027.
31. Gaffney D, Howie AF, Bakkush AM El, Hoffmann TM, Mason JI, Wallace AM, Donaldson MDC. Functional characterisation of the H365Y mutation of the 21-hydroxylase gene in congenital adrenal hyperplasia. J Steroid Biochem Mol Biol 2011;123(3-5):109-114.
32. Szklarz GD, Ornstein RL, Halpert JR. Application of 3-dimensional homology modeling of cytochrome P450 2B1 for interpretation of site-directed mutagenesis results. J Biomol Struct Dynamics 1994;12:061-078.
33. Li QS, Ogawa J, Schmid RD, Shimizu S. Residue size at position 87 of cytochrome P450 BM-3 determines its stereoselectivity in propylbenzene and 3-chlorostyrene oxidation. FEBS Lett 2001;508:249-252.
34. Liu J, Ericksen SS, Sivaneri M, Besspiata D, Fisher CW, Szklarz GD. The effect of reciprocal active site mutations in human cytochromes P450 1A1 and 1A2 on alkoxyresorufin metabolism. Arch Biochem Biophys 2004;424:33-43.
35. Paulsen MD, Filipovic D, Sligar SG, Ornstein RL. Controlling the regiospecificity and coupling of cytochrome P450cam: T185F mutant increases coupling and abolishes 3-hydroxynorcamphor product. Protein Sci 1993;2:357-365.
36. Luo Z, He YA, Halpert JR. Role of residues 363 and 206 in conversion of cytochrome P450 2B1 from a steroid 16-hydroxylase to a 15 alpha-hydroxylase. Arch Biochem Biophys 1994;309:52-57.
37. Sugimoto H, Shinkyo R, Hayashi K, Yoneda S, Yamada M, Kamakura M, Ikushiro S, Shiro Y, Sakaki T. Crystal structure of CYP105A1 (P450SU-1) in complex with 1alpha, 25-dihydroxyvitamin D3. Biochemistry 2008;47:4017-4027.
38. Tardy V, Menassa R, Sulmont V, Lienhardt-Roussie A, Lecointre C, Brauner R, David M, Morel Y. Phenotype-genotype correlations of 13 rare CYP21A2 mutations detected in 46 patients affected with 21-hydroxylase deficiency and in one carrier. J Clin Endocrinol Metabol 2010;95:1288-1300.
39. Truan G, Peterson JA. Thr268 in substrate binding and catalysis in P450BM-3. Arch Biochem Biophys 1998;349:53-64.
40. Schlichting I, Berendzen J, Chu K, Stock AM, Maves SA, Benson DE, Sweet RM, Ringe D, Petsko GA, Sligar SG. The catalytic pathway of cytochrome p450cam at atomic resolution. Science (New York, N.Y.) 2000;287:1615-1622.
41. Nagano S, Poulos TL. Crystallographic study on the dioxygen complex of wild-type and mutant cytochrome P450cam. Implications for the dioxygen activation mechanism. J Biol Chem 2005;280:31659-31663.
42. Aikensf J, Sligar SG. Kinetic solvent isotope effects during oxygen activation. J Am Chem Soc 1994;12:1143-1144.
43. Bui SH, McLean KJ, Cheesman MR, Bradley JM, Rigby SEJ, Levy CW, Leys D, Munro AW. Unusual spectroscopic and ligand binding properties of the cytochrome P450-flavodoxin fusion enzyme XplA. J Biol Chem 2012;287:19699-19714.
44. Domanski TL, Liu J, Harlow GR, Halpert JR. Analysis of four residues within substrate recognition site 4 of human cytochrome P450 3A4: role in steroid hydroxylase activity and alpha-naphthoflavone stimulation. Arch Biochem Biophys 1998;350:223-232.
45. Sawada Y, Ayabe S. Multiple mutagenesis of P450 isoflavonoid synthase reveals a key active-site residue. Biochem Biophys Res Commun 2005;330:907-913.
46. Honda Malca S, Scheps D, Kühnel L, Venegas-Venegas E, Seifert A, Nestl BM, Hauer B. Bacterial CYP153A monooxygenases for the synthesis of omega-hydroxylated fatty acids. Chem Commun (Cambridge, England) 2012;48:5115-5117.
47. Zhao B, Lamb DC, Lei L, Kelly SL, Yuan H, Hachey DL, Waterman MR. Different binding modes of two flaviolin substrate molecules in cytochrome P450 158A1 (CYP158A1) compared to CYP158A2. Biochemistry 2007;46:8725-8733.
48. Kahn RA, Le Bouquin R, Pinot F, Benveniste I, Durst F. A conservative amino acid substitution alters the regiospecificity of CYP94A2, a fatty acid hydroxylase from the plant Vicia sativa. Arch Biochem Biophys 2001;391:180-187.
49. Xue L, Zgoda VG, Arison B, Almira Correia M. Structure-function relationships of rat liver CYP3A9 to its human liver orthologs: site-directed active site mutagenesis to a progesterone dihydroxylase. Arch Biochem Biophys 2003;409:113-126.
50. Melet A, Marques-Soares C, Schoch GA, Macherey A-C, Jaouen M, Dansette PM, Sari M-A, Johnson EF, Mansuy D. Analysis of human cytochrome P450 2C8 substrate specificity using a substrate pharmacophore and site-directed mutants. Biochemistry 2004;43:15379-15392.
51. Attia TZ, Yamashita T, Hammad MA, Hayasaki A, Sato T, Miyamoto M, Yasuhara Y, Nakamura T, Kagawa Y, Tsujino H, et al. Effect of cytochrome P450 2C19 and 2C9 amino acid residues 72 and 241 on metabolism of tricyclic antidepressant drugs. Chem Pharma Bull 2014;62:176-181.
52. Mast N, Zheng W, Stout CD, Pikuleva IA. Binding of a cyano- and fluoro-containing drug bicalutamide to cytochrome P450 46A1: unusual features and spectral response. J Biol Chem 2013;288:4613-4624.
53. Wang LH, Matijevic-Aleksic N, Hsu PY, Ruan KH, Wu KK, Kulmacz RJ. Identification of thromboxane A2 synthase active site residues by molecular modeling-guided site-directed mutagenesis. J Biol Chem 1996;271:19970-19975.
54. Toporkova YY, Ermilova VS, Gorina SS, Mukhtarova LS, Osipova E V, Gogolev Y V, Grechkin AN. Structure-function relationship in the CYP74 family: conversion of divinyl ether synthases into allene oxide synthases by site-directed mutagenesis. FEBS Lett 2013;587:2552-2558.
55. Stjernschantz E, van Vugt-Lussenburg BMA, Bonifacio A, de Beer SBA, van der Zwan G, Gooijer C, Commandeur JNM, Vermeulen NPE, Oostenbrink C. Structural rationalization of novel drug metabolizing mutants of cytochrome P450 BM3. Proteins 2008;71:336-352.
56. Lewis DFV, Hlavica P. Interactions between redox partners in various cytochrome P450 systems: functional and structural aspects. Biochimica et Biophysica Acta (BBA) 2000;1460(2-3):353-374.
57. Munro AW, Malarkey K, McKnight J, Thomson AJ, Kelly SM, Price NC, Lindsay JG, Coggins JR, Miles JS. The role of tryptophan 97 of cytochrome P450 BM3 from Bacillus megaterium in catalytic function. Evidence against the "covalent switching" hypothesis of P-450 electron transfer. Biochem J 1994;303(Part 2):423-428.
58. Ba L, Li P, Zhang H, Duan Y, Lin Z. Semi-rational engineering of cytochrome P450sca-2 in a hybrid system for enhanced catalytic activity: insights into the important role of electron transfer. Biotechnol Bioeng 2013;110:2815-2825.
59. Bridges A. Identification of the Binding Site on Cytochrome P450 2B4 for Cytochrome b5 and Cytochrome P450 Reductase. J Biol Chem 1998;273:17036-17049.
60. Lin H, Kenaan C, Zhang H, Hollenberg PF. Reaction of human cytochrome P450 3A4 with peroxynitrite: nitrotyrosine formation on the proximal side impairs its interaction with NADPH-cytochrome P450 reductase. Chem Res Toxicol 2012;25:2642-2653.
61. Zhao C, Gao Q, Roberts AG, Shaffer SA, Doneanu CE, Xue S, Goodlett DR, Nelson SD, Atkins WM. Cross-linking mass spectrometry and mutagenesis confirm the functional importance of surface interactions between CYP3A4 and holo/apo cytochrome b(5). Biochemistry 2012;51:9488-9500.
62. Koo LS, Immoos CE, Cohen MS, Farmer PJ, Ortiz de Montellano PR. Enhanced electron transfer and lauric acid hydroxylation by site-directed mutagenesis of CYP119. J Am Chem Soc 2002;124:5684-5691.
63. Fleuren WW, Alkema W. Application of text mining in the biomedical domain. Methods 2015;74:97-106.
64. Larsen PO, von Ins M. The rate of growth in scientific publication and the decline in coverage provided by Science Citation Index. Scientometrics 2010;84:575-603.
65. Björk B-C, Welling P, Laakso M, Majlender P, Hedlund T, Gudnason G. Open access to the scientific journal literature: situation 2009. PloS One 2010;5:e11273.
66. Jensen LJ, Saric J, Bork P. Literature mining for the biologist: from information retrieval to biological discovery. Nat Rev Gene 2006;7:119-129.
67. Delano W. The PyMOL Molecular Graphics System. 2002.
68. Sevrioukova IF, Li H, Zhang H, Peterson JA, Poulos TL. Structure of a cytochrome P450-redox partner electron-transfer complex. Proc Natl Acad Sci USA 1999;96:1863-1868.
69. Walsh AA, Szklarz GD, Scott EE. Human cytochrome P450 1A1 structure and utility in understanding drug and xenobiotic metabolism. J Biol Chem 2013;288:12932-12943.
70. Zhao B, Lei L, Kagawa N, Sundaramoorthy M, Banerjee S, Nagy LD, Guengerich FP, Waterman MR. Three-dimensional structure of steroid 21-hydroxylase (cytochrome P450 21A2) with two substrates reveals locations of disease-associated variants. J Biol Chem 2012;287:10613-10622.
71. Sabbadin F, Jackson R, Haider K, Tampi G, Turkenburg JP, Hart S, Bruce NC, Grogan G. The 1.5-A structure of XplA-heme, an unusual cytochrome P450 heme domain that catalyzes reductive biotransformation of royal demolition explosive. J Biol Chem 2009;284:28467-28475.
72. Williams PA, Cosme J, Vinkovic DM, Ward A, Angove HC, Day PJ, Vonrhein C, Tickle IJ, Jhoti H. Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone. Science (New York, N.Y.) 2004;305:683-686.