Identification, modeling and ligand affinity of early deuterostome CYP51s, and functional characterization of recombinant zebrafish sterol 14α-demethylase

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 6, 2014, Pages 1825-1836

  Morrison, Ann Michelle Stanley ^a,b,d   Goldstone, Jared V ^a   Lamb, David C ^a,c   Kubota, Akira ^a   Lemaire, Benjamin ^a   Stegeman, John J ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c SWANSEA UNIVERSITY   (United Kingdom)

^d EXPONENT INC   (United States)

Author keywords

Azole inhibition; CYP51; Deuterostome; Sterol 14 demethylase; Sterol biosynthesis; Zebrafish

Indexed keywords

COMPLEMENTARY DNA; KETOCONAZOLE; LANOSTEROL; PROPICONAZOLE; PYRROLE; RECOMBINANT ENZYME; STEROL 14ALPHA DEMETHYLASE; CARBON MONOXIDE; CHLORAMPHENICOL; CYTOCHROME P450;

ABUDEFDUF SAXATILIS; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CATALYSIS; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; CYP51 GENE; DEUTEROSTOMIA; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; GAS CHROMATOGRAPHY; GENE; HETEROLOGOUS EXPRESSION; HUMAN; INTESTINE; LIGAND BINDING; LIVER; MASS SPECTROMETRY; MATHEMATICAL ANALYSIS; MOLECULAR CLONING; MOLECULAR DOCKING; MOLECULAR MODEL; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; SEA URCHIN; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRONGYLOCENTROTUS PURPURATUS; TISSUE DISTRIBUTION; ZEBRA FISH; ADULT; CLADISTICS; CONCENTRATION RESPONSE; DNA SEQUENCE; DRUG METABOLISM; DRUG PROTEIN BINDING; ENZYME ANALYSIS; ENZYME BINDING; ENZYME SUBSTRATE; FEMALE; GENE EXPRESSION; MALE; MYCOSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; STEROL SYNTHESIS;

AZOLE INHIBITION; CYP51; DEUTEROSTOME; STEROL 14Α-DEMETHYLASE; STEROL BIOSYNTHESIS; ZEBRAFISH;

ANIMALS; FEMALE; HUMANS; LIGANDS; MALE; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; RECOMBINANT PROTEINS; STEROL 14-DEMETHYLASE; STEROLS; ZEBRAFISH;

EID: 84896949928     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.12.009     Document Type: Article

References (77)

1. G.I. Lepesheva, and M.R. Waterman Sterol 14alpha-demethylase cytochrome P450 (CYP51), a P450 in all biological kingdoms Biochim. Biophys. Acta 1770 2007 467 477
2. A.G. Byskov, C.Y. Andersen, L. Nordholm, H. Thogersen, X. Guoliang, O. Wassman, J.V.A.E. Guddal, and T. Roed Chemical structure of sterols that activate oocyte meiosis Nature 374 1995 559 562
3. A.G. Byskov, C.Y. Andersen, L. Leonardsen, and M. Baltsen Meiosis activating sterols (MAS) and fertility in mammals and man J. Exp. Zool. 285 1999 237 242
4. A.G. Byskov, C.Y. Andersen, and L. Leonardsen Role of meiosis activating sterols, MAS, in induced oocyte maturation Mol. Cell. Endocrinol. 187 2002 189 196
5. R. Keber, H. Motaln, K.D. Wagner, N. Debeljak, M. Rassoulzadegan, J. Acimovic, D. Rozman, and S. Horvat Mouse knockout of the cholesterogenic cytochrome P450 lanosterol 14{alpha}-demethylase (Cyp51) resembles Antley-Bixler syndrome J. Biol. Chem. 286 2011 29086 29097
6. H.C. Andersson Disorders of post-squalene cholesterol biosynthesis leading to human dysmorphogenesis Cell. Mol. Biol. (Noisy-le-grand) 48 2002 173 177
7. T. Akiyoshi, T. Saito, S. Murase, M. Miyazaki, N. Murayama, H. Yamazaki, F.P. Guengerich, K. Nakamura, K. Yamamoto, and H. Ohtani Comparison of the inhibitory profiles of itraconazole and cimetidine in cytochrome P450 3A4 genetic variants Drug Metab. Dispos. 39 2011 724 728
8. N. Mast, W. Zheng, C.D. Stout, and I.A. Pikuleva Antifungal azoles: structural insights into undesired tight binding to cholesterol-metabolizing CYP46A1 Mol. Pharmacol. 84 2013 86 94
9. H.M. Handley-Goldstone, M.W. Grow, and J.J. Stegeman Cardiovascular gene expression profiles of dioxin exposure in zebrafish embryos Toxicol. Sci. 85 2005 683 693
10. T. Gupta, and M.C. Mullins Dissection of organs from the adult zebrafish J. Vis. Exp. 37 2010 1717
11. A. Kubota, A.C. Bainy, B.R. Woodin, J.V. Goldstone, and J.J. Stegeman The cytochrome P450 2AA gene cluster in zebrafish (Danio rerio): expression of CYP2AA1 and CYP2AA2 and response to phenobarbital-type inducers Toxicol. Appl. Pharmacol. 272 2013 172 179
12. C. Ramakers, J.M. Ruijter, R.H. Deprez, and A.F. Moorman Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data Neurosci. Lett. 339 2003 62 66
13. J.M. Ruijter, C. Ramakers, W.M. Hoogaars, Y. Karlen, O. Bakker, M.J. van den Hoff, and A.F. Moorman Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data Nucleic Acids Res. 37 2009 e45
14. H.J. Barnes Maximizing expression of eukaryotic cytochrome P450s in Escherichia coli E.F. Johnson, M.R. Waterman, Methods in Enzymology. Cytochrome P450 (Part B) vol. 272 1996 Academic Press San Diego 3 14
15. M.R. Waterman, C.M. Jenkins, and I. Pikuleva Genetically engineered bacterial cells and applications Toxicol. Lett. 82-83 1995 807 813
16. M. Stromstedt, D. Rozman, and M.R. Waterman The ubiquitously expressed human CYP51 encodes lanosterol 14 alpha-demethylase, a cytochrome P450 whose expression is regulated by oxysterols Arch. Biochem. Biophys. 329 1996 73 81
17. K. Kusano, M.R. Waterman, M. Sakaguchi, T. Omura, and N. Kagawa Protein synthesis inhibitors and ethanol selectively enhance heterologous expression of P450s and related proteins in Escherichia coli Arch. Biochem. Biophys. 367 1999 129 136
18. T. Omura, and R. Sato The carbon monoxide binding pigment of liver microsomes. I. Evidence for its haemoprotein nature J. Biol. Chem. 239 1964 2370 2378
19. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, and D.G. Higgins Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
20. A. Stamatakis RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models Bioinformatics 22 2006 2688 2690
21. S. Whelan, and N. Goldman A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach Mol. Biol. Evol. 18 2001 691 699
22. F. Ronquist, M. Teslenko, P. van der Mark, D.L. Ayres, A. Darling, S. Hohna, B. Larget, L. Liu, M.A. Suchard, and J.P. Huelsenbeck MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space Syst. Biol. 61 2012 539 542
23. N. Eswar, B. Webb, M.A. Marti-Renom, M.S. Madhusudhan, D. Eramian, M.Y. Shen, U. Pieper, and A. Sali Comparative protein structure modeling using Modeller Curr. Protoc. Bioinform. Supplement 15 2006 5.6.1 5.6.30
24. N. Strushkevich, S.A. Usanov, and H.W. Park Structural basis of human CYP51 inhibition by antifungal azoles J. Mol. Biol. 397 2010 1067 1078
25. M.Y. Shen, and A. Sali Statistical potential for assessment and prediction of protein structures Protein Sci. 15 2006 2507 2524
26. D. Eramian, M.Y. Shen, D. Devos, F. Melo, A. Sali, and M.A. Marti-Renom A composite score for predicting errors in protein structure models Protein Sci. 15 2006 1653 1666
27. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Cryst. 26 1993 283 291
28. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R.D. Skeel, L. Kale, and K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802
29. S. Cosconati, S. Forli, A.L. Perryman, R. Harris, D.S. Goodsell, and A.J. Olson Virtual screening with AutoDock: theory and practice Expert Opin. Drug Discov. 5 2011 597 607
30. J.J. Stewart Optimization of parameters for semiempirical methods V: modification of NDDO approximations and application to 70 elements J. Mol. Model. 13 2007 1173 1213
31. J.J. Stewart MOPAC2009 MOPAC2009 2008 Stewart Computational Chemistry Colorado Springs, CO
32. O. Trott, and A.J. Olson AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 31 2010 455 461
33. Y. Yoshida, and Y. Aoyama Interaction of azole antifungal agents with cytochrome P-45014DM purified from Saccharomyces cerevisiae microsomes Biochem. Pharmacol. 36 1987 229 235
34. G.I. Lepesheva, and M.R. Waterman CYP51 - the omnipotent P450 Mol. Cell. Endocrinol. 215 2004 165 170
35. Y. Yoshida, Y. Aoyama, M. Noshiro, and O. Gotoh Sterol 14-demethylase P450 (CYP51) provides a breakthrough for the discussion on the evolution of cytochrome P450 gene superfamily Biochem. Biophys. Res. Commun. 273 2000 799 804
36. D.R. Nelson, J.V. Goldstone, and J.J. Stegeman The cytochrome P450 genesis locus: the origin and evolution of animal cytochrome P450s Philos. Trans. R. Soc. Lond. B Biol. Sci. 368 2013 20120474
37. A.G. Smith, and L.J. Goad Sterol biosynthesis by the sea urchin Echinus esculentus Biochem. J. 142 1974 421 427
38. J. Trzaskos, S. Kawata, and J.L. Gaylor Microsomal enzymes of cholesterol biosynthesis. Purification of lanosterol 14 alpha-methyl demethylase cytochrome P-450 from hepatic microsomes J. Biol. Chem. 261 1986 14651 14657
39. Y. Nitahara, Y. Aoyama, T. Horiuchi, M. Noshiro, and Y. Yoshida Purification and characterization of rat sterol 14-demethylase P450 (CYP51) expressed in Escherichia coli J. Biochem. (Tokyo) 126 1999 927 933
40. D.C. Lamb, D.E. Kelly, M.R. Waterman, M. Stromstedt, D. Rozman, and S.L. Kelly Characteristics of the heterologously expressed human lanosterol 14alpha-demethylase (other names: P45014DM, CYP51, P45051) and inhibition of the purified human and Candida albicans CYP51 with azole antifungal agents Yeast 15 1999 755 763
41. Y. Aoyama, M. Kudo, K. Asai, K. Okonogi, T. Horiuchi, O. Gotoh, and Y. Yoshida Emergence of fluconazole-resistant sterol 14-demethylase P450 (CYP51) in Candida albicans is a model demonstrating the diversification mechanism of P450 Arch. Biochem. Biophys. 379 2000 170 171
42. A.G. Warrilow, J.E. Parker, D.E. Kelly, and S.L. Kelly Azole affinity of sterol 14alpha-demethylase (CYP51) enzymes from Candida albicans and Homo sapiens Antimicrob. Agents Chemother. 57 2013 1352 1360
43. H.M. Guardiola-Diaz, L.A. Foster, D. Mushrush, and A.D. Vaz Azole-antifungal binding to a novel cytochrome P450 from Mycobacterium tuberculosis: implications for treatment of tuberculosis Biochem. Pharmacol. 61 2001 1463 1470
44. M. Blumberg, V. Thiel, T. Pape, and W. Michaelis The steroids of hexactinellid sponges Naturwissenschaften 89 2002 415 419
45. C. Djerassi, and C. Silva Sponge sterols: origin and biosynthesis Acc. Chem. Res. 24 1991 371 378
46. C.J. Silva, L. Wunsche, and C. Djerassi Biosynthetic studies of marine lipids. 35. The demonstration of de novo sterol biosynthesis in sponges using radiolabeled isoprenoid precursors Comp. Biochem. Physiol. B 99 1991 763 773
47. Z. Marijanovic, D. Laubner, G. Moller, C. Gege, B. Husen, J. Adamski, and R. Breitling Closing the gap: identification of human 3-ketosteroid reductase, the last unknown enzyme of mammalian cholesterol biosynthesis Mol. Endocrinol. 17 2003 1715 1725
48. P.A. Voogt, and J.W. van Rheenen On the sterols of some ascidians Arch. Int. Physiol. Biochim. 83 1975 563 572
49. M.S. Donia, W.F. Fricke, F. Partensky, J. Cox, S.I. Elshahawi, J.R. White, A.M. Phillippy, M.C. Schatz, J. Piel, M.G. Haygood, J. Ravel, and E.W. Schmidt Complex microbiome underlying secondary and primary metabolism in the tunicate-Prochloron symbiosis Proc. Natl. Acad. Sci. U. S. A. 108 2011 E1423 E1432
50. J.M. Trant, and P. Thomas Isolation of a novel maturation-inducing steroid produced in vitro by ovaries of Atlantic croaker Gen. Comp. Endocrinol. 75 1989 397 404
51. C. Tubbs, W. Tan, B. Shi, and P. Thomas Identification of 17,20beta,21-trihydroxy-4-pregnen-3-one (20beta-S) receptor binding and membrane progestin receptor alpha on southern flounder sperm (Paralichthys lethostigma) and their likely role in 20beta-S stimulation of sperm hypermotility Gen. Comp. Endocrinol. 170 2011 629 639
52. B. Dale, M. Marino, and M. Wilding The ins and outs of meiosis J. Exp. Zool. 285 1999 226 236
53. N. Sagata Introduction: meiotic maturation and arrest in animal oocytes Semin. Cell Dev. Biol. 9 1998 535 537
54. R. Keber, J. Acimovic, G. Majdic, H. Motaln, D. Rozman, and S. Horvat Male germ cell-specific knockout of cholesterogenic cytochrome P450 lanosterol 14alpha-demethylase (Cyp51) J. Lipid Res. 54 2013 1653 1661
55. G.L. Russo, M. Wilding, M. Marino, and B. Dale Ins and outs of meiosis in ascidians Semin. Cell Dev. Biol. 9 1998 559 567
56. T.J. Pursley, I.K. Blomquist, J. Abraham, H.F. Andersen, and J.A. Bartley Fluconazole-induced congenital anomalies in three infants Clin. Infect. Dis. 22 1996 336 340
57. S. Horvat, J. McWhir, and D. Rozman Defects in cholesterol synthesis genes in mouse and in humans: lessons for drug development and safer treatments Drug Metab. Rev. 43 2011 69 90
58. K. Hatai, and G. Hoshiai Mass mortality in cultured coho salmon (Oncorhynchus kisutch) due to Saprolegnia parasitica Coker J. Wildl. Dis. 28 1992 532 536
59. M.J. Ronis, M. Ingelman-Sundberg, and T.M. Badger Induction, suppression and inhibition of multiple hepatic cytochrome P450 isozymes in the male rat and bobwhite quail (Colinus virginianus) by ergosterol biosynthesis inhibiting fungicides (EBIFs) Biochem. Pharmacol. 48 1994 1953 1965
60. M.J. Ronis, and T.M. Badger Toxic interactions between fungicides that inhibit ergosterol biosynthesis and phosphorothioate insecticides in the male rat and bobwhite quail (Colinus virginianus) Toxicol. Appl. Pharmacol. 130 1995 221 228
61. M.J. Ronis, M. Celander, and T.M. Badger Cytochrome P450 enzymes in the kidney of the bobwhite quail (Colinus virginianus): induction and inhibition by ergosterol biosynthesis inhibiting fungicides Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 121 1998 221 229
62. A.D. Rodrigues, D.F. Lewis, C. Ioannides, and D.V. Parke Spectral and kinetic studies of the interaction of imidazole anti-fungal agents with microsomal cytochromes P-450 Xenobiotica 17 1987 1315 1327
63. T. Hegelund, K. Ottosson, M. Radinger, P. Tomberg, and M.C. Celander Effects of the antifungal imidazole ketoconazole on CYP1A and CYP3A in rainbow trout and killifish Environ. Toxicol. Chem. 23 2004 1326 1334
64. S.L. Levine, H. Czosnyka, and J.T. Oris Effect of the fungicide clotrimazole on the bioconcentration of benzo[a]pyrene in gizzard shad (Dorosoma cepedianum): In vivo and in vitro inhibition of cytochrome P4501A activity Environ. Toxicol. Chem. 16 1997 306 311
65. S.L. Levine, and J.T. Oris Enhancement of acute parathion toxicity to fathead minnows following pre-exposure to propiconazole Pestic. Biochem. Physiol. 65 1999 102 109
66. S.L. Levine, J.T. Oris, and M.S. Denison Modulation of CYP1A expression in rainbow trout by a technical grade formulation of propiconazole Environ. Toxicol. Chem. 18 1999 2565 2573
67. S.L. Levine, and J.T. Oris Noncompetitive mixed-type inhibition of rainbow trout CYP1A catalytic activity by clotrimazole Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 122 1999 205 210
68. A.H. Knoll, and S.B. Carroll Early animal evolution: emerging views from comparative biology and geology Science 284 1999 2129 2137
69. D.R.e. Maddison The Tree of Life Project D.R. Maddison, The Tree of Life Project 2004
70. L.J. Goad The sterols of marine invertebrates: composition, biosynthesis, and metabolites P.J. Scheuer, Marine Natural Products: Chemical and Biological Perspectives vol. 2 1978 Academic Press New York 76 172
71. A.O. Awharitoma, F.I. Opute, S.N. Ali, and B.A. Obiamiwe Lipid biosynthesis in Paramphistomum microbothrium (Trematoda) Angew. Parasitol. 31 1990 51 53
72. H. Meyer, L. Provasoli, and F. Meyer Lipid biosynthesis in the marine flatworm Convoluta roscoffensis and its algal symbiont Platymonas convoluta Biochim. Biophys. Acta 573 1979 464 480
73. D.R. Nelson The cytochrome p450 homepage Hum. Genomics 4 2009 59 65
74. T.Y. Hargrove, Z. Wawrzak, J. Liu, W.D. Nes, M.R. Waterman, and G.I. Lepesheva Substrate preferences and catalytic parameters determined by structural characteristics of sterol 14alpha-demethylase (CYP51) from Leishmania infantum J. Biol. Chem. 286 2011 26838 26848
75. Y. Aoyama, Y. Yoshida, and R. Sato Yeast cytochrome P-450 catalyzing lanosterol 14 alpha- demethylation. II. Lanosterol metabolism by purified P-450(14)DM and by intact microsomes J. Biol. Chem. 259 1984 1661 1666
76. D.C. Lamb, D.E. Kelly, and S.L. Kelly Molecular diversity of sterol 14alpha-demethylase substrates in plants, fungi and humans FEBS Lett. 425 1998 263 265
77. G.I. Lepesheva, N.G. Zaitseva, W.D. Nes, W. Zhou, M. Arase, J. Liu, G.C. Hill, and M.R. Waterman CYP51 from Trypanosoma cruzi: a phyla-specific residue in the B' helix defines substrate preferences of sterol 14alpha-demethylase J. Biol. Chem. 281 2006 3577 3585