Metabolism of cholesterol, vitamin D3 and 20-hydroxyvitamin D3 incorporated into phospholipid vesicles by human CYP27A1

Journal of Steroid Biochemistry and Molecular Biology

Volumn 129, Issue 3-5, 2012, Pages 163-171

  Tieu, Elaine W ^a   Li, Wei ^b   Chen, Jianjun ^b   Baldisseri, Donna M ^c   Slominski, Andrzej T ^b   Tuckey, Robert C ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c BRUKER BIOSPIN CORPORATION   (United States)

Author keywords

Cholesterol; CYP27A1; Cytochrome P450; Phospholipid vesicles; Vitamin D

Indexed keywords

20 HYDROXYVITAMIN D3; 20,25 DIHYDROXYVITAMIN D3; 20,26 DIHYDROXYVITAMIN D3; CARBON; CHOLESTANETRIOL 26 MONOOXYGENASE; CHOLESTEROL; COLECALCIFEROL; HYDROXYL GROUP; PHOSPHOLIPID; UNCLASSIFIED DRUG; VITAMIN D DERIVATIVE;

ARTICLE; CATALYSIS; CHOLESTEROL METABOLISM; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HYDROXYLATION; MASS SPECTROMETRY; METABOLITE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHOLIPID VESICLE; VITAMIN METABOLISM;

CALCIFEDIOL; CHOLECALCIFEROL; CHOLESTEROL; CYTOCHROME P-450 CYP27A1; HUMANS; MITOCHONDRIAL MEMBRANES; PHOSPHOLIPIDS;

EID: 84858284104     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2011.11.012     Document Type: Article

References (52)

1. K.I. Okuda Liver mitochondrial P450 involved in cholesterol catabolism and vitamin D activation J. Lipid Res. 35 3 1994 361 372
2. I.A. Pikuleva, I. Bjorkhem, and M.R. Waterman Expression, purification, and enzymatic properties of recombinant human cytochrome P450c27 (CYP27) Arch. Biochem. Biophys. 343 1 1997 123 130 (Pubitemid 27274350)
3. I.A. Pikuleva, A. Babiker, M.R. Waterman, and I. Bjorkhem Activities of recombinant human cytochrome P450c27 (CYP27) which produce intermediates of alternative bile acid biosynthetic pathways J. Biol. Chem. 273 29 1998 18153 18160 (Pubitemid 28334733)
4. M. Norlin, and K. Wikvall Enzymes in the conversion of cholesterol into bile acids Curr. Mol. Med. 7 2 2007 199 218 (Pubitemid 46488191)
5. M. Ellfolk, M. Norlin, K. Gyllensten, and K. Wikvall Regulation of human vitamin D(3) 25-hydroxylases in dermal fibroblasts and prostate cancer LNCaP cells Mol. Pharmacol. 75 6 2009 1392 1399
6. M. Gascon-Barre, C. Demers, O. Ghrab, C. Theodoropoulos, R. Lapointe, G. Jones, L. Valiquette, and D. Menard Expression of CYP27A, a gene encoding a vitamin D-25 hydroxylase in human liver and kidney Clin. Endocrinol. 54 1 2001 107 115 (Pubitemid 32158712)
7. A.B. Reiss, K.O. Martin, D.E. Rojer, S. Iyer, E.A. Grossi, A.C. Galloway, and N.B. Javitt Sterol 27-hydroxylase: expression in human arterial endothelium J. Lipid Res. 38 6 1997 1254 1260 (Pubitemid 27281819)
8. M. Schuessler, N. Astecker, G. Herzig, G. Vorisek, and I. Schuster Skin is an autonomous organ in synthesis, two-step activation and degradation of vitamin D(3): CYP27 in epidermis completes the set of essential vitamin D(3)-hydroxylases Steroids 66 3-5 2001 399 408 (Pubitemid 32140917)
9. D.D. Bikle, M.K. Nemanic, E. Gee, and P. Elias 1,25-Dihydroxyvitamin D3 production by human keratinocytes. Kinetics and regulation J. Clin. Invest. 78 2 1986 557 566 (Pubitemid 16074095)
10. M.F. Holick Resurrection of vitamin D deficiency and rickets J. Clin. Invest. 116 8 2006 2062 2072 (Pubitemid 44162310)
11. A.S. Dusso, A.J. Brown, and E. Slatopolsky Vitamin D Am. J. Physiol. Renal Physiol. 289 1 2005 F8 F28
12. M.F. Holick Vitamin D: the underappreciated D-lightful hormone that is important for skeletal and cellular health Curr. Opin. Endocrinol. Diabetes Obes. 91 1 2002 87 98 (Pubitemid 34747893)
13. M.F. Holick Vitamin D deficiency N. Engl. J. Med. 357 3 2007 266 281
14. S. Masuda Promise of vitamin D analogues in the treatment of hyperproliferative conditions Mol. Cancer Ther. 5 4 2006 797 808 (Pubitemid 43724578)
15. R.C. Tuckey, W. Li, J.K. Zjawiony, M.A. Zmijewski, M.N. Nguyen, T. Sweatman, D. Miller, and A. Slominski Pathways and products for the metabolism of vitamin D3 by cytochrome P450scc FEBS J. 275 10 2008 2585 2596 (Pubitemid 351600097)
16. A. Slominski, I. Semak, J. Zjawiony, J. Wortsman, W. Li, A. Szczesniewski, and R.C. Tuckey The cytochrome P450scc system opens an alternate pathway of vitamin D3 metabolism FEBS J. 272 16 2005 4080 4090 (Pubitemid 41160916)
17. O. Guryev, R.A. Carvalho, S. Usanov, A. Gilep, and R.W. Estabrook A pathway for the metabolism of vitamin D3: unique hydroxylated metabolites formed during catalysis with cytochrome P450scc (CYP11A1) Proc. Natl. Acad. Sci. U. S. A. 100 25 2003 14754 14759 (Pubitemid 37517963)
18. A.T. Slominski, Z. Janjetovic, B.E. Fuller, M.A. Zmijewski, R.C. Tuckey, M.N. Nguyen, T. Sweatman, W. Li, J. Zjawiony, D. Miller, T.C. Chen, G. Lozanski, and M.F. Holick Products of vitamin D3 or 7-dehydrocholesterol metabolism by cytochrome P450scc show anti-leukemia effects, having low or absent calcemic activity PLoS One 5 3 2010 e9907
19. B. Zbytek, Z. Janjetovic, R.C. Tuckey, M.A. Zmijewski, T.W. Sweatman, E. Jones, M.N. Nguyen, and A.T. Slominski 20-hydroxyvitamin D3, a product of vitamin D3 hydroxylation by cytochrome P450scc, stimulates keratinocyte differentiation J. Invest. Dermatol. 128 9 2008 2271 2280
20. Z. Janjetovic, R.C. Tuckey, M.N. Nguyen, E.M. Thorpe Jr., and A.T. Slominski 20,23-dihydroxyvitamin D3, novel P450scc product, stimulates differentiation and inhibits proliferation and NF-kappaB activity in human keratinocytes J. Cell. Physiol. 223 1 2009 36 48
21. Z. Janjetovic, M.A. Zmijewski, R.C. Tuckey, D.A. DeLeon, M.N. Nguyen, L.M. Pfeffer, and A.T. Slominski 20-Hydroxycholecalciferol, product of vitamin D3 hydroxylation by P450scc, decreases NF-kappa B activity by increasing I kappa B alpha levels in human keratinocytes PLoS One 4 6 2009 e5988
22. A.T. Slominski, T.K. Kim, Z. Janjetovic, R.C. Tuckey, R. Bieniek, J. Yue, W. Li, J. Chen, M.N. Nguyen, E.K.Y. Tang, D. Miller, T.C. Chen, and M. Holick 20-Hydroxyvitamin D2 is a noncalcemic analog of vitamin D with potent antiproliferative and prodifferentiation activities in normal and malignant cells Am. J. Physiol. Cell Physiol. 300 3 2011 C526 C541
23. R.C. Tuckey Progesterone synthesis by the human placenta Placenta 26 4 2005 273 281 (Pubitemid 40485864)
24. I.A. Pikuleva, C. Cao, and M.R. Waterman An additional electrostatic interaction between adrenodoxin and P450c27 (CYP27A1) results in tighter binding than between adrenodoxin and P450scc (CYP11A1) J. Biol. Chem. 274 4 1999 2045 2052
25. D. Murtazina, A.V. Puchkaev, C.H. Schein, N. Oezguen, W. Braun, A. Nanavati, and I.A. Pikuleva Membrane-protein interactions contribute to efficient 27-hydroxylation of cholesterol by mitochondrial cytochrome P450 27A1 J. Biol. Chem. 277 40 2002 37582 37589
26. A.J. Annalora, D.B. Goodin, W.X. Hong, Q. Zhang, E.F. Johnson, and C.D. Stout Crystal structure of CYP24A1, a mitochondrial cytochrome P450 involved in vitamin D metabolism J. Mol. Biol. 396 2 2010 441 451
27. N. Mast, A.J. Annalora, D.T. Lodowski, K. Palczewski, C.D. Stout, and I.A. Pikuleva Structural basis for three-step sequential catalysis by the cholesterol side chain cleavage enzyme CYP11A1 J. Biol. Chem. 286 7 2011 5607 5613
28. N. Strushkevich, F. MacKenzie, T. Cherkesova, I. Grabovec, S. Usanov, and H.W. Park Structural basis for pregnenolone biosynthesis by the mitochondrial monooxygenase system Proc. Natl. Acad. Sci. U. S. A. 108 25 2011 10139 10143
29. D.A. Murtazina, U. Andersson, I.S. Hahn, I. Bjorkhem, G.A.S. Ansari, and I.A. Pikuleva Phospholipids modify substrate binding and enzyme activity of human cytochrome P450 27A1 J. Lipid Res. 45 12 2004 2345 2353 (Pubitemid 39602982)
30. E.K.Y. Tang, K.J.Q. Voo, M.N. Nguyen, and R.C. Tuckey Metabolism of substrates incorporated into phospholipid vesicles by mouse 25-hydroxyvitamin D3 1[alpha]-hydroxylase (CYP27B1) J. Steroid Biochem. Mol. Biol. 119 3-5 2010 171 179
31. R.C. Tuckey, M.N. Nguyen, and A. Slominski Kinetics of vitamin D3 metabolism by cytochrome P450scc (CYP11A1) in phospholipid vesicles and cyclodextrin Int. J. Biochem. Cell Biol. 40 11 2008 2619 2626
32. R.C. Tuckey, Z. Janjetovic, W. Li, M.N. Nguyen, M.A. Zmijewski, J. Zjawiony, and A. Slominski Metabolism of 1 alpha-hydroxyvitamin D3 by cytochrome P450scc to biologically active 1 alpha,20-dihydroxyvitamin D3 J. Steroid Biochem. Mol. Biol. 112 4-5 2008 213 219
33. R.C. Tuckey, and P.M. Stevenson Purification and analysis of phospholipids in the inner mitochondrial membrane fraction of bovine corpus luteum, and properties of cytochrome P-450scc incorporated into vesicles prepared from these phospholipids Eur. J. Biochem. 148 2 1985 379 384 (Pubitemid 15093621)
34. R.P. Gupta, K. Patrick, and N.H. Bell Mutational analysis of CYP27A1: assessment of 27-hydroxylation of cholesterol and 25-hydroxylation of vitamin D Metab. Clin. Exp. 56 9 2007 1248 1255 (Pubitemid 47223265)
35. R.C. Tuckey, W. Li, H.Z. Shehabi, Z. Janjetovic, M.N. Nguyen, T.K. Kim, J. Chen, D.E. Howell, H.A. Benson, T. Sweatman, D.M. Baldisseri, and A. Slominski Production of 22-hydroxy-metabolites of vitamin D3 by cytochrome P450scc (CYP11A1) and analysis of their biological activities on skin cells Drug Metab. Dispos. 39 9 2011 1577 1588
36. S.T. Woods, J. Sadleir, T. Downs, T. Triantopoulos, M.J. Headlam, and R.C. Tuckey Expression of catalytically active human cytochrome P450scc in Escherichia coli and mutagenesis of isoleucine-462 Arch. Biochem. Biophys. 353 1 1998 109 115 (Pubitemid 28373035)
37. J.J. Cali, and D.W. Russell Characterization of human sterol 27-hydroxylase. A mitochondrial cytochrome P-450 that catalyzes multiple oxidation reaction in bile acid biosynthesis J. Biol. Chem. 266 12 1991 7774 7778 (Pubitemid 21906433)
38. R.C. Tuckey, and H. Kamin Kinetics of the incorporation of adrenal cytochrome P-450scc into phosphatidylcholine vesicles J. Biol. Chem. 257 6 1982 2887 2893
39. J. Decaprio, J. Yun, and N.B. Javitt Bile acid and sterol solubilization in 2-hydroxypropyl-beta-cyclodextrin J. Lipid Res. 33 3 1992 441 443
40. T. Omura, and R. Sato The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature J. Biol. Chem. 239 1964 2370 2378
41. D1α (25-hydroxyvitamin D3-1α-hydroxylase) of bovine kidney mitochondria Biochem. Biophys. Res. Commun. 105 1 1982 320 327
42. K. Merz, and B. Sternberg Incorporation of vitamin D3-derivatives in liposomes of different lipid types J. Drug Target. 2 5 1994 411 417
43. N. Sawada, T. Sakaki, M. Ohta, and K. Inouye Metabolism of vitamin D3 by human CYP27A1 Biochem. Biophys. Res. Commun. 273 3 2000 977 984
44. E. Axen, H. Postlind, H. Sjoberg, and K. Wikvall Liver mitochondrial cytochrome-P450 CYP27 and recombinant-expressed human CYP27 catalyze 1-alpha-hydroxylation of 25-hydroxyvitamin D-3 Proc. Natl. Acad. Sci. U. S. A. 91 21 1994 10014 10018 (Pubitemid 24311939)
45. I. Pikuleva, and N.B. Javitt Novel sterols synthesized via the CYP27A1 metabolic pathway Arch. Biochem. Biophys. 420 1 2003 35 39 (Pubitemid 37393371)
46. R. Shinkyo, T. Sakaki, M. Kamakura, M. Ohta, and K. Inouye Metabolism of vitamin D by human microsomal CYP2R1 Biochem. Biophys. Res. Commun. 324 1 2004 451 457 (Pubitemid 39311516)
47. N. Strushkevich, S.A. Usanov, A.N. Plotnikov, G. Jones, and H.-W. Park Structural Analysis of CYP2R1 in Complex with Vitamin D3 J. Mol. Biol. 380 1 2008 95 106
48. I. Aiba, T. Yamasaki, T. Shinki, S. Izumi, K. Yamamoto, S. Yamada, H. Terato, H. Ide, and Y. Ohyama Characterization of rat and human CYP2J enzymes as vitamin D 25-hydroxylases Steroids 71 10 2006 849 856 (Pubitemid 44286955)
49. J.B. Cheng, M.A. Levine, N.H. Bell, D.J. Mangelsdorf, and D.W. Russell Genetic evidence that the human CYP2R1 enzyme is a key vitamin D 25-hydroxylase Proc. Natl. Acad. Sci. U. S. A. 101 20 2004 7711 7715 (Pubitemid 38658094)
50. M. Schlame, D. Rua, and M.L. Greenberg The biosynthesis and functional role of cardiolipin Prog. Lipid Res. 39 3 2000 257 288 (Pubitemid 30224706)
51. M.J. Headlam, M.C. Wilce, and R.C. Tuckey The F-G loop region of cytochrome P450scc (CYP11A1) interacts with the phospholipid membrane Biochim. Biophys. Acta 1617 1-2 2003 96 108 (Pubitemid 37456717)
52. E.D. Collins, J.E. Bishop, C.M. Bula, A. Acevedo, W.H. Okamura, and A.W. Norman Effect of 25-hydroxyl group orientation on biological activity and binding to the 1alpha, 25-dihydroxy vitamin D3 receptor J. Steroid Biochem. Mol. Biol. 94 4 2005 279 288 (Pubitemid 40602468)