Functional expression and characterisation of human cytochrome P45017α in Pichia pastoris

Journal of Biotechnology

Volumn 129, Issue 4, 2007, Pages 635-644

  Kolar, Norbert W ^a   Swart, Amanda C ^a   Mason, J Ian ^b   Swart, Pieter ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

CYP17; Cytochrome P45017 (17 hydroxylase 17,20 lyase); Heterologous expression; Pichia pastoris

Indexed keywords

HETEROLOGOUS EXPRESSION; PICHIA PASTORIS; PROGESTERONE; STEROIDS;

CARBON MONOXIDE; CELL GROWTH; ENZYME KINETICS; HORMONES; PROTEINS; YEAST;

GENE EXPRESSION;

16 HYDROXYPROGESTERONE; ANDROGEN; CARBON MONOXIDE; CYTOCHROME P450 17; DETERGENT; GLUCOCORTICOID; HYDROXYPROGESTERONE; PROGESTERONE; STEROID 17,20 LYASE; STEROID 17ALPHA MONOOXYGENASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CATALYST; ENZYME ACTIVITY; HUMAN; HYDROPHOBICITY; HYDROXYLATION; NONHUMAN; PICHIA PASTORIS; PRIORITY JOURNAL; PROGESTERONE METABOLISM; PROTEIN EXPRESSION; REACTION ANALYSIS;

HUMANS; KINETICS; PICHIA; PROGESTERONE; RECOMBINANT PROTEINS; SOLUBILITY; STEROID 17-ALPHA-HYDROXYLASE; TRANSFECTION;

MAMMALIA; PAN; PICHIA PASTORIS;

EID: 34247140959     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2007.02.003     Document Type: Article

References (66)

1. Akhtar M.K., Kelly S.L., and Kaderbhai M.A. Cytochrome b (5) modulation of 17{alpha} hydroxylase and 17-20 lyase (CYP17) activities in steroidogenesis. J. Endocrinol. 187 (2005) 267-274
2. Amant F., Dorfling C.M., Brabanter J., Vandewalle J., Vergote I., Lindeque B.G., and van Rensburg E. A possible role of the cytochrome P450c17alpha gene (CYP17) polymorphism in the pathobiology of uterine leiomyomas from black South African women: a pilot study. Acta Obstet. Gynecol. Scand. 83 (2004) 234-239
3. Andersen M.D., Busk P.K., Svendsen I., and Møller B.L. Cytochromes P-450 from cassava (Manihot esculenta Crantz) catalyzing the first steps in the biosynthesis of the cyanogenic glucosides linamarin and lotaustralin. Cloning, functional expression in Pichia pastoris, and substrate specificity of the isolated recombinant enzymes. J. Biol. Chem. 275 (2000) 1966-1975
4. Arlt W., Martens J.W., Song M., Wang J.T., Auchus R.J., and Miller W.L. Molecular evolution of adrenarche: structural and functional analysis of p450c17 from four primate species. Endocrinology 143 (2002) 4665-4672
5. Auchus R.J., Geller D.H., Lee T.C., and Miller W.L. The regulation of human P450c17 activity: relationship to premature adrenarche, insulin resistance and the polycystic ovary syndrome. Trends Endocrinol. Metab. 9 (1998) 47-50
6. Auchus R.J., Lee T.C., and Miller W.L. Cytochrome b5 augments the 17,20-lyase activity of human P450c17 without direct electron transfer. J. Biol. Chem. 273 (1998) 3158-3165
7. Auchus R.J., Sampath Kumar A., Andrew Boswell C., Gupta M.K., Bruce K., Rath N.P., and Covey D.F. The enantiomer of progesterone (ent-progesterone) is a competitive inhibitor of human cytochromes P450c17 and P450c21. Arch. Biochem. Biophys. 409 (2003) 134-144
8. Barnes H.J., Arlotto M.P., and Waterman M.R. Expression and enzymatic activity of recombinant cytochrome P450 17 alpha-hydroxylase in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 5597-5601
9. Barnes H.J., Jenkins C.M., and Waterman M.R. Baculovirus expression of bovine cytochrome P450c17 in Sf9 cells and comparison with expression in yeast, mammalian cells, and E. coli. Arch. Biochem. Biophys. 315 (1994) 489-494
10. Boyle S.M., Popp M.P., Smith W.C., Greenberg R.M., and James M.O. Expression of CYP2L1 in the yeast Pichia pastoris, and determination of catalytic activity with progesterone and testosterone. Mar. Environ. Res. 46 (1998) 25-28
11. Bradshaw K.D., Waterman M.R., Couch R.T., Simpson E.R., and Zuber M.X. Characterization of complementary deoxyribonucleic acid for human adrenocortical 17 alpha-hydroxylase: a probe for analysis of 17 alpha-hydroxylase deficiency. Mol. Endocrinol. 1 (1987) 348-354
12. Cancel-Tassin G., and Cussenot O. Genetic susceptibility to prostate cancer. Br. J. Haematol. 96 (2005) 1380-1385
13. Cereghino G.P., Cereghino J.L., Ilgen C., and Cregg J.M. Production of recombinant proteins in fermenter cultures of the yeast Pichia pastoris. Curr. Opin. Biotechnol. 13 (2002) 329-332
14. Cereghino J.L., and Cregg J.M. Heterologous protein expression in the methylotrophic yeast Pichia pastoris. FEMS Microbiol. Rev. 24 (2000) 45-66
15. Chung B.C., Picardo-Leonard J., Haniu M., Bienkowski M., Hall P.F., Shively J.E., and Miller W.L. Cytochrome P450c17 (steroid 17 alpha-hydroxylase/17,20 lyase): cloning of human adrenal and testis cDNAs indicates the same gene is expressed in both tissues. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 407-411
16. Clark B.J., and Waterman M.R. The hydrophobic amino-terminal sequence of bovine 17 alpha-hydroxylase is required for the expression of a functional hemoprotein in COS 1 cells. J. Biol. Chem. 266 (1991) 5898-5904
17. Cloutier M., Fleury A., Courtemanche J., Ducharme L., Mason J.I., and LeHoux J.G. Cloning and expression of hamster adrenal cytochrome P450C17 cDNA. Ann. N.Y. Acad. Sci. 774 (1995) 294-296
18. Cregg J.M., Vedvick T.S., and Raschke W.C. Recent advances in the expression of foreign genes in Pichia pastoris. Bio/Technology 11 (1993) 905-910
19. Denzer A.J., Nabholz C.E., and Spiess M. Transmembrane orientation of signal-anchor proteins is affected by the folding state but not the size of the N-terminal domain. EMBO J. 14 (1995) 6311-6317
20. Dietrich M., Grundmann L., Kurr K., Valinotto L., Saussele T., Schmid R.D., and Lange S. Recombinant production of human microsomal cytochrome P450 2D6 in the methylotrophic yeast Pichia pastoris. ChemBioChem 6 (2005) 2014-2022
21. Fevold H.R., Lorence M.C., McCarthy J.L., Trant J.M., Kagimoto M., Waterman M.R., and Mason J.I. Rat P450(17 alpha) from testis: characterization of a full-length cDNA encoding a unique steroid hydroxylase capable of catalyzing both delta 4- and delta 5-steroid-17,20-lyase reactions. Mol. Endocrinol. 3 (1989) 968-975
22. Gelissen G. Heterologous protein production in methylotrophic yeasts. Appl. Microbiol. Biotechnol. 54 (2000) 741-750
23. Gilep A.A., Estabrook R.W., and Usanov S.A. Molecular cloning and heterologous expression in E. coli of cytochrome P45017alpha. Comparison of structural and functional properties of substrate-specific cytochromes P450 from different species. Biochemistry (Mosc.) 68 (2003) 86-98
24. Hadfield C. Construction of cloning and expression vectors. In: Johnston J.R. (Ed). Molecular Genetics of Yeast. A Practical Approach (1994), Oxford University Press Inc., New York 17-48
25. Higgins D.R., and Cregg J.M. Introduction to Pichia pastoris. In: Higgins D.R., and Cregg J.M. (Eds). Pichia Protocols vol. 103 (1998), Humana Press Inc., Totawa, NJ 1-16
26. Hollenberg C.P., and Gellisen G. Production of recombinant proteins by methylotrophic yeasts. Curr. Opin. Biotechnol. 8 (1997) 554-560
27. Imai T., Globerman H., Gertner J., Kagawa N., and Waterman M.R. Expression and purification of functional human 17 alpha-hydroxylase/17,20-lyase (P450c17) in Escherichia coli. Use of this system for study of a novel form of combined 17 alpha-hydroxylase/17,20-lyase deficiency. J. Biol. Chem. 268 (1993) 19681-19689
28. Kitamura M., Buczko E., and Dufau M.L. Dissociation of hydroxylase and lyase activities by site-directed mutagenesis of the rat P45017 alpha. Mol. Endocrinol. 5 (1991) 1373-1380
29. Kovaleva I.E., Novikova L.A., Nazarov P.A., Grivennikov S.I., and Luzikov V.N. Effects of various N-terminal addressing signals on sorting and folding of mammalian CYP11A1 in yeast mitochondria. Eur. J. Biochem. 270 (2003) 222-229
30. Kozak M. At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J. Mol. Biol. 196 (1987) 947-950
31. Kozak M. Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266 (1991) 19867-19870
32. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
33. Linder S., Schliwa M., and Kube-Granderath E. Direct PCR Screening of Pichia pastoris clones. BioTechniques 20 (1996) 980-982
34. Lorence M.C., Trant J.M., Clark B.J., Khyatt B., Mason J.I., Estabrook R.W., and Waterman M.R. Construction and expression of human/bovine P45017 alpha chimeric proteins: evidence for distinct tertiary structures in the same P450 from two different species. Biochemistry 29 (1990) 9819-9824
35. Matsuzaki F., and Wariishi H. Molecular characterization of cytochrome P450 catalyzing hydroxylation of benzoates from the white-rot fungus Phanerochaete chrysosporium. Biochem. Biophys. Res. Commun. 334 (2005) 1184-1190
36. Mast N., Andersson U., Nakayama K., Bjorkhem I., and Pikulevaa I.A. Expression of human cytochrome P450 46A1 in Escherichia coli: effects of N- and C-terminal modifications. Arch. Biochem. Biophys. 428 (2004) 99-108
37. Naffin-Olivos J.L., and Auchus R.J. Human cytochrome b5 requires residues E48 and E49 to stimulate the 17,20-lyase activity of cytochrome P450c17. Biochemistry 45 (2006) 755-762
38. Nakajin S., Shinoda M., Haniu M., Shively J.E., and Hall P.F. C21 steroid side chain cleavage enzyme from porcine adrenal microsomes. Purification and characterization of the 17 alpha-hydroxylase/C17,20-lyase cytochrome P-450. J. Biol. Chem. 259 (1984) 3971-3976
39. Nishihara H., Okamura T., Schmid R.D., Hauck A., and Reuß M. Biotechnological potential of P450 monooxygenases high-level production of bovine cytochrome P450c17 monooxygenase during medium cell density culture of a recombinant yeast, Saccharomyces cerevisiae GRF 18 (YEp-Toku1). J. Biotechnol. 56 (1997) 57-61
40. Omura T., and Sato R. The cabon-monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J. Biol. Chem. 239 (1964) 2370-2378
41. Owaki A., Takamasa A., Yamazaki T., and Kominami S. Membrane reconstitution of recombinant guinea pig cytochrome P45017alpha and the effects of site-directed mutagenesis on androgen formation. J. Steroid Biochem. Mol. Biol. 81 (2002) 255-262
42. Pan Z., Camara B., Gardner H.W., and Backhaus R.A. Aspirin inhibition and acetylation of the plant cytochrome P450, allene oxide synthase, resembles that of animal prostaglandin endoperoxide H synthase. J. Biol. Chem. 273 (1998) 18139-18145
43. Qin K., and Rosenfield R.L. Role of cytochrome P450c17 in polycystic ovary syndrome. Mol. Cell. Endocrinol. 145 (1998) 111-121
44. Rose A.B., and Broach J.R. Propagation and expression of cloned genes in yeast: 2-μm circle-based vectors. In: Goeddel D.V. (Ed). Methods in Enzymology. Gene Expression Technology vol. 185 (1990), Academic Press Inc., San Diego, CA 234-280
45. Sagara Y., Barnes H.J., and Waterman M.R. Expression in Escherichia coli of functional cytochrome P450c17 lacking its hydrophobic amino-terminal signal anchor. Arch. Biochem. Biophys. 304 (1993) 272-278
46. Sakai Y., Tanaka M., Adachi S., Miller W.L., and Nagahama Y. Rainbow trout cytochrome P-450c17 (17α-hydroxylase/17,20-lyase) cDNA cloning, enzymatic properties and temporal pattern of ovarian P-450c17 mRNA expression during oogenesis. FEBS. Lett. 301 (1992) 60-64
47. Sakaki T., Shibata M., Yabusaki Y., Murakami H., and Ohkawa H. Expression of bovine cytochrome P450c17 cDNA in Saccharomyces cerevisiae. DNA 8 (1989) 409-418
48. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
49. Sherbet D.P., Tiosano D., Kwist K.M., Hochberg Z., and Auchus R.J. CYP17 mutation E305G causes isolated 17,20-lyase deficiency by selectively altering substrate binding. J. Biol. Chem. 278 (2003) 48563-48569
50. Shibata M., Sakaki T., Yabusaki Y., Murakami H., and Ohkawa H. Genetically engineered P450 monooxygenases: construction of bovine P450c17/yeast reductase fused enzymes. DNA Cell Biol. 9 (1990) 27-36
51. Soucy P., Lacoste L., and Luu-The V. Assessment of porcine and human 16-ene-synthase, a third activity of P450c17, in the formation of an androstenol precursor. Role of recombinant cytochrome b5 and P450 reductase. Eur. J. Biochem. 270 (2003) 1349-1355
52. Swart A.C., Swart P., Roux S.P., van der Merwe K.J., Pretorius I.S., and Steyn A.J. Expression of human P450c17 as an export protein in Saccharomyces cerevisiae. Endocr. Res. 21 (1995) 289-295
53. Swart A.C., Kolar N.W., Lombard N., Mason J.I., and Swart P. Baboon cytochrome P450 17alpha-hydroxylase/17,20-lyase (CYP17). Eur. J. Biochem. 269 (2002) 5608-5616
54. Swart P., Swart A.C., Waterman M.R., Estabrook R.W., and Mason J.I. Progesterone 16 alpha-hydroxylase activity is catalyzed by human cytochrome P450 17 alpha-hydroxylase. J. Clin. Endocrinol. Metab. 77 (1993) 98-102
55. Swart P., Lombard N., Swart A.C., Merwe M.J., Murry B.A., Nicol M., and MasonF J.I. Ovine steroid 17α-hydroxylase (CYP17): hydroxylase and lyase activity in the adrenal cortex. Arch. Biochem. Biophys. 409 1 (2003) 145-152
56. Swart P., van der Merwe K.J., Swart A.C., Todres P.C., and Hofmeyr J.H. Inhibition of cytochrome P-450(11)beta by some naturally occurring acetophenones and plant extracts from the shrub Salsola tuberculatiformis. Planta Med. 59 (1993) 139-143
57. Szczesna-Skorupa E., Ahn K., Chen C.-D., Doray B., and Kemper B. The cytoplasmic and N-terminal transmembrane domains of cytochrome P450 contain independent signals for retention in the endoplasmic reticulum. J. Biol. Chem. 270 (1995) 24327-24333
58. Trant J.M. Isolation and characterization of the cDNA encoding the spiny dogfish shark (Squalus acanthias) form of cytochrome P450c17. J. Exp. Zool. 272 (1995) 25-33
59. Trant J.M. Heterologous expression of the spiny dogfish shark (Squalus acanthias) cytochrome P450c17 (17α-hydroxylase) in Escherichia coli. Gen. Comp. Endocrinol. 102 (1996) 173-182
60. Trant J.M. Functional expression of recombinant spiny dogfish shark (Squalus acanthias) cytochrome P450c17 (17 alpha-hydroxylase/C17,20-lyase) in yeast (Pichia pastoris). Arch. Biochem. Biophys. 326 (1996) 8-14
61. Tremblay Y., Fleury A., Beaudoin C., Vallee M., and Belanger A. Molecular cloning and expression of guinea pig cytochrome P450c17 cDNA (steroid 17 alpha-hydroxylase/17,20 lyase): tissue distribution, regulation, and substrate specificity of the expressed enzyme. DNA Cell Biol. 13 (1994) 1199-1212
62. van den Brink H.M., van Gorcom R.F., van den Hondel C.A., and Punt P.J. Cytochrome P450 enzyme systems in fungi. Fungal Genet. Biol. 23 (1998) 1-17
63. Yabusaki Y. Expression of mammalian cytochromes P450 in yeast. In: Phillips I.R., and Shephard E.A. (Eds). Cytochrome P450 Protocolls vol. 107 (1998), Humana Press Inc., Totawa, NJ 195-202
64. Yanase T., Kagimoto M., Suzuki S., Hashiba K., Simpson E.R., and Waterman M.R. Deletion of a phenylalanine in the N-terminal region of human cytochrome P-450(17 alpha) results in partial combined 17 alpha- hydroxylase/17,20-lyase deficiency. J. Biol. Chem. 264 (1989) 18076-18082
65. Yun C.H., Miller G.P., and Guengerich F.P. Rate-determining steps in phenacetin oxidations by human cytochrome P450 1A2 and selected mutants. Biochemistry 39 (2000) 11319-11329
66. Zuber M.X., Simpson E.R., and Waterman M.R. Expression of bovine 17 alpha-hydroxylase cytochrome P-450 cDNA in nonsteroidogenic (COS 1) cells. Science 234 (1986) 1258-1261