Human steroid and oxysterol 7α-hydroxylase CYP7B1: Substrate specificity, azole binding and misfolding of clinically relevant mutants

FEBS Journal

Volumn 281, Issue 6, 2014, Pages 1700-1713

  Yantsevich, Aleksei V ^a   Dichenko, Yaroslav V ^a   Mackenzie, Farrell ^b   Mukha, Dmitry V ^a   Baranovsky, Alexander V ^a   Gilep, Andrei A ^a   Usanov, Sergey A ^a   Strushkevich, Natallia V ^a,b  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Belarus)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

azole drugs; cytochrome P450; neurodegenerative disease; neurosteroids; oxysterols

Indexed keywords

AZOLE DRUGS; CYTOCHROME P450; NEURODEGENERATIVE DISEASE; NEUROSTEROIDS; OXYSTEROLS;

17-ALPHA-HYDROXYPREGNENOLONE; AMINO ACID SUBSTITUTION; AZOLES; CATALYTIC DOMAIN; HUMANS; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PROTEIN FOLDING; RECOMBINANT PROTEINS; SPECTROPHOTOMETRY; STEROID HYDROXYLASES; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY;

EID: 84899455072     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12733     Document Type: Article

References (55)

1. Stiles AR, McDonald JG, Bauman DR, &, Russell DW, (2009) CYP7B1: one cytochrome P450, two human genetic diseases, and multiple physiological functions. J Biol Chem 284, 28485-28489.
2. Chiang JY, (1998) Regulation of bile acid synthesis. Front Biosci 3, d176-d193.
3. Steckelbroeck S, Watzka M, Lutjohann D, Makiola P, Nassen A, Hans VH, Clusmann H, Reissinger A, Ludwig M, Siekmann L, et al,. (2002) Characterization of the dehydroepiandrosterone (DHEA) metabolism via oxysterol 7alpha-hydroxylase and 17-ketosteroid reductase activity in the human brain. J Neurochem 83, 713-726. (Pubitemid 35231825)
4. Bauman DR, Bitmansour AD, McDonald JG, Thompson BM, Liang G, &, Russell DW, (2009) 25-Hydroxycholesterol secreted by macrophages in response to toll-like receptor activation suppresses immunoglobulin A production. Proc Natl Acad Sci USA 106, 16764-16769.
5. Omoto Y, Lathe R, Warner M, &, Gustafsson JA, (2005) Early onset of puberty and early ovarian failure in CYP7B1 knockout mice. Proc Natl Acad Sci USA 102, 2814-2819. (Pubitemid 40305279)
6. Weihua Z, Lathe R, Warner M, &, Gustafsson JA, (2002) An endocrine pathway in the prostate, ERbeta, AR, 5alpha-androstane-3beta,17beta-diol, and CYP7B1, regulates prostate growth. Proc Natl Acad Sci USA 99, 13589-13594. (Pubitemid 35221316)
7. Lundqvist J, &, Norlin M, (2012) Effects of CYP7B1-related steroids on androgen receptor activation in different cell lines. Biochim Biophys Acta 1821, 973-979.
8. Rose KA, Stapleton G, Dott K, Kieny MP, Best R, Schwarz M, Russell DW, Bjorkhem I, Seckl J, &, Lathe R, (1997) Cyp7b, a novel brain cytochrome P450, catalyzes the synthesis of neurosteroids 7alpha-hydroxy dehydroepiandrosterone and 7alpha-hydroxy pregnenolone. Proc Natl Acad Sci USA 94, 4925-4930. (Pubitemid 27214712)
9. Martin KO, Reiss AB, Lathe R, &, Javitt NB, (1997) 7Alpha-hydroxylation of 27-hydroxycholesterol: biologic role in the regulation of cholesterol synthesis. J Lipid Res 38, 1053-1058. (Pubitemid 27255213)
10. Diczfalusy U, Olofsson KE, Carlsson AM, Gong M, Golenbock DT, Rooyackers O, Flaring U, &, Bjorkbacka H, (2009) Marked upregulation of cholesterol 25-hydroxylase expression by lipopolysaccharide. J Lipid Res 50, 2258-2264.
11. Sundin M, Warner M, Haaparanta T, &, Gustafsson JA, (1987) Isolation and catalytic activity of cytochrome P-450 from ventral prostate of control rats. J Biol Chem 262, 12293-12297.
12. Tsutsui K, (2006) Biosynthesis, mode of action and functional significance of neurosteroids in the developing Purkinje cell. J Steroid Biochem Mol Biol 102, 187-194. (Pubitemid 44750641)
13. Morfin R, &, Starka L, (2001) Neurosteroid 7-hydroxylation products in the brain. Int Rev Neurobiol 46, 79-95. (Pubitemid 33798718)
14. Yau JL, Rasmuson S, Andrew R, Graham M, Noble J, Olsson T, Fuchs E, Lathe R, &, Seckl JR, (2003) Dehydroepiandrosterone 7-hydroxylase CYP7B: predominant expression in primate hippocampus and reduced expression in Alzheimer's disease. Neuroscience 121, 307-314. (Pubitemid 37176919)
15. Flood JF, Smith GE, &, Roberts E, (1988) Dehydroepiandrosterone and its sulfate enhance memory retention in mice. Brain Res 447, 269-278.
16. Doostzadeh J, Urban P, Pompon D, &, Morfin R, (1996) Pregnenolone-7 beta-hydroxylating activities of yeast-expressed mouse cytochrome P450-1A1 and mouse-tissue microsomes. Eur J Biochem 242, 641-647. (Pubitemid 27121147)
17. Doostzadeh J, Flinois JP, Beaune P, &, Morfin R, (1997) Pregnenolone-7beta-hydroxylating activity of human cytochrome P450-1A1. J Steroid Biochem Mol Biol 60, 147-152. (Pubitemid 27216435)
18. Muller C, Pompon D, Urban P, &, Morfin R, (2006) Inter-conversion of 7alpha- and 7beta-hydroxy-dehydroepiandrosterone by the human 11beta-hydroxysteroid dehydrogenase type 1. J Steroid Biochem Mol Biol 99, 215-222.
19. Schwarz M, Lund EG, &, Russell DW, (1998) Two 7 alpha-hydroxylase enzymes in bile acid biosynthesis. Curr Opin Lipidol 9, 113-118. (Pubitemid 28159708)
20. Russell DW, (2003) The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 72, 137-174. (Pubitemid 36930444)
21. Li-Hawkins J, Lund EG, Bronson AD, &, Russell DW, (2000) Expression cloning of an oxysterol 7alpha-hydroxylase selective for 24-hydroxycholesterol. J Biol Chem 275, 16543-16549. (Pubitemid 30398878)
22. Schule R, Brandt E, Karle KN, Tsaousidou M, Klebe S, Klimpe S, Auer-Grumbach M, Crosby AH, Hubner CA, Schols L, et al,. (2009) Analysis of CYP7B1 in non-consanguineous cases of hereditary spastic paraplegia. Neurogenetics 10, 97-104.
23. Guryev OL, Gilep AA, Usanov SA, &, Estabrook RW, (2001) Interaction of apo-cytochrome b5 with cytochromes P4503A4 and P45017A: relevance of heme transfer reactions. Biochemistry 40, 5018-5031. (Pubitemid 32332548)
24. Zarn JA, Bruschweiler BJ, &, Schlatter JR, (2003) Azole fungicides affect mammalian steroidogenesis by inhibiting sterol 14 alpha-demethylase and aromatase. Environ Health Perspect 111, 255-261. (Pubitemid 36395190)
25. Cui YL, Zhang JL, Zheng QC, Niu RJ, Xu Y, Zhang HX, &, Sun CC, (2013) Structural and dynamic basis of human cytochrome P450 7B1: a survey of substrate selectivity and major active site access channels. Chemistry 19, 549-557.
26. Siam A, Brancale A, &, Simons C, (2012) Comparative modeling of 25-hydroxycholesterol-7alpha-hydroxylase (CYP7B1): ligand binding and analysis of hereditary spastic paraplegia type 5 CYP7B1 mutations. J Mol Model 18, 441-453.
27. Schlichting I, Berendzen J, Chu K, Stock AM, Maves SA, Benson DE, Sweet RM, Ringe D, Petsko GA, &, Sligar SG, (2000) The catalytic pathway of cytochrome p450cam at atomic resolution. Science 287, 1615-1622. (Pubitemid 30127756)
28. Liu C, Yang XV, Wu J, Kuei C, Mani NS, Zhang L, Yu J, Sutton SW, Qin N, Banie H, et al,. (2011) Oxysterols direct B-cell migration through EBI2. Nature 475, 519-523.
29. Hannedouche S, Zhang J, Yi T, Shen W, Nguyen D, Pereira JP, Guerini D, Baumgarten BU, Roggo S, Wen B, et al,. (2011) Oxysterols direct immune cell migration via EBI2. Nature 475, 524-527.
30. Niwa T, Imamura H, &, Katagiri M, (2012) Inhibition of human steroidogenic cytochrome P450 c17 by 21-hydroxypregnenolone and related steroid hormones. Biol Pharm Bull 35, 1594-1597.
31. Shackleton CH, Homoki J, &, Taylor NF, (1987) A paradox: elevated 21-hydroxypregnenolone production in newborns with 21-hydroxylase deficiency. Steroids 49, 295-311.
32. Warner M, &, Gustafsson JA, (1995) Cytochrome P450 in the brain: neuroendocrine functions. Front Neuroendocrinol 16, 224-236.
33. Shibuya K, Takata N, Hojo Y, Furukawa A, Yasumatsu N, Kimoto T, Enami T, Suzuki K, Tanabe N, Ishii H, et al,. (2003) Hippocampal cytochrome P450s synthesize brain neurosteroids which are paracrine neuromodulators of synaptic signal transduction. Biochim Biophys Acta 1619, 301-316. (Pubitemid 36160608)
34. Vallee M, Mayo W, Koob GF, &, Le Moal M, (2001) Neurosteroids in learning and memory processes. Int Rev Neurobiol 46, 273-320. (Pubitemid 33798725)
35. Tsutsui K, Inoue K, Miyabara H, Suzuki S, Ogura Y, Tobari Y, &, Haraguchi S, (2009) Discovery of a novel avian neurosteroid, 7alpha-hydroxypregnenolone, and its role in the regulation of the diurnal rhythm of locomotor activity in Japanese quail. Gen Comp Endocrinol 163, 117-122.
36. Tsutsui K, Haraguchi S, Inoue K, Miyabara H, Suzuki S, Ogura Y, Koyama T, Matsunaga M, &, Vaudry H, (2009) Identification, biosynthesis, and function of 7alpha-hydroxypregnenolone, a new key neurosteroid controlling locomotor activity, in nonmammalian vertebrates. Ann N Y Acad Sci 1163, 308-315.
37. Yau JL, Noble J, Graham M, &, Seckl JR, (2006) Central administration of a cytochrome P450-7B product 7 alpha-hydroxypregnenolone improves spatial memory retention in cognitively impaired aged rats. J Neurosci 26, 11034-11040. (Pubitemid 44772193)
38. Tsutsui K, Inoue K, Miyabara H, Suzuki S, Ogura Y, &, Haraguchi S, (2008) 7Alpha-hydroxypregnenolone mediates melatonin action underlying diurnal locomotor rhythms. J Neurosci 28, 2158-2167. (Pubitemid 351317628)
39. Matsunaga M, Ukena K, Baulieu EE, &, Tsutsui K, (2004) 7Alpha-hydroxypregnenolone acts as a neuronal activator to stimulate locomotor activity of breeding newts by means of the dopaminergic system. Proc Natl Acad Sci USA 101, 17282-17287. (Pubitemid 39627811)
40. Tsutsui K, Haraguchi S, Matsunaga M, Koyama T, Do Rego JL, &, Vaudry H, (2012) 7Alpha-hydroxypregnenolone, a new key regulator of amphibian locomotion: discovery, progress and prospect. Gen Comp Endocrinol 176, 440-447.
41. Pringle AK, Schmidt W, Deans JK, Wulfert E, Reymann KG, &, Sundstrom LE, (2003) 7-Hydroxylated epiandrosterone (7-OH-EPIA) reduces ischaemia-induced neuronal damage both in vivo and in vitro. Eur J Neurosci 18, 117-124. (Pubitemid 36920852)
42. Hampl R, Lapcik O, Hill M, Klak J, Kasal A, Novacek A, Sterzl I, Sterzl J, &, Starka L, (2000) 7-Hydroxydehydroepiandrosterone-a natural antiglucocorticoid and a candidate for steroid replacement therapy? Physiol Res 49 (Suppl. 1), S107-S112. (Pubitemid 30399359)
43. Muller C, Hennebert O, &, Morfin R, (2006) The native anti-glucocorticoid paradigm. J Steroid Biochem Mol Biol 100, 95-105. (Pubitemid 44088612)
44. Setchell KD, Schwarz M, O'Connell NC, Lund EG, Davis DL, Lathe R, Thompson HR, Weslie Tyson R, Sokol RJ, &, Russell DW, (1998) Identification of a new inborn error in bile acid synthesis: mutation of the oxysterol 7alpha-hydroxylase gene causes severe neonatal liver disease. J Clin Invest 102, 1690-1703. (Pubitemid 28516254)
45. Johnson LB, &, Kauffman CA, (2003) Voriconazole: a new triazole antifungal agent. Clin Infect Dis 36, 630-637. (Pubitemid 36259570)
46. Aksoy F, Akdogan E, Aydin K, Yilmaz M, Altunayoglu V, Sozen EE, Omay SB, &, Koksal I, (2008) Voriconazole-induced neuropathy. Chemotherapy 54, 224-227. (Pubitemid 351929274)
47. Wagner U, &, Born J, (2008) Memory consolidation during sleep: interactive effects of sleep stages and HPA regulation. Stress 11, 28-41.
48. Omura T, &, Sato R, (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J Biol Chem 239, 2370-2378.
49. Paul KG, Theorell H, &, Akeson A, (1953) The molar light absorption of pyridine ferroprotoporphyrin (pyridine haemochromogen). Acta Chem Scand 7, 1284-1289.
50. Ishibashi M, Yamagishi E, &, Kobayashi J, (1997) Topsentinols A-J, new sterols with highly branched side chains from marine sponge Topsentia sp. Chern Pharm Bull 45, 1435-1438.
51. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, &, Sali A, (2000) Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29, 291-325. (Pubitemid 30599596)
52. Laskowski RA, MacArthur MW, Moss DS, &, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26, 283-291.
53. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, &, Ferrin TE, (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612.
54. Humphrey W, Dalke A, &, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14, 33-38. (Pubitemid 26152973)
55. Meng EC, Pettersen EF, Couch GS, Huang CC, &, Ferrin TE, (2006) Tools for integrated sequence-structure analysis with UCSF Chimera. BMC Bioinformatics 7, 339.