Analysis of neurosterols and neurosteroids by mass spectrometry

Biochimie

Volumn 89, Issue 2, 2007, Pages 182-191

  Wang, Yuqin ^a   Karu, Kersti ^a   Griffiths, William J ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Derivatisation; LC MS; Mass spectrometry; MS MS; Oxysterols; Steroids

Indexed keywords

CHOLESTEROL; STEROID; STEROL;

ARTICLE; BLOOD BRAIN BARRIER; BODY WEIGHT; ELECTROENCEPHALOGRAM; HUMAN; MASS SPECTROMETRY; PROTEIN INTERACTION; SYNTHESIS;

ANIMALS; BRAIN CHEMISTRY; CHROMATOGRAPHY, LIQUID; HUMANS; MASS SPECTROMETRY; MOLECULAR STRUCTURE; STEROIDS; STEROLS;

EID: 33846483721     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2006.10.008     Document Type: Article

References (70)

1. Dietschy J.M., and Turley S.D. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J. Lipid Res. 45 (2004) 1375-1397
2. Dhar A.K., Teng J.I., and Smith L.L. Biosynthesis of cholest-5-ene-3beta, 24-diol (cerebrosterol) by bovine cerebral cortical microsomes. J. Neurochem. 21 (1973) 51-60
3. 2 techniques in vivo and in vitro. J. Biol. Chem. 272 (1997) 30178-30184
4. Björkhem I., Lütjohann D., Diczfalusy U., Stahle L., Ahlborg G., and Wahren J. Cholesterol homeostasis in human brain: turnover of 24S-hydroxycholesterol and evidence for a cerebral origin of most of this oxysterol in the circulation. J. Lipid Res. 39 (1998) 1594-1600
5. Lund E.G., Guileyardo J.M., and Russell D.W. cDNA cloning of cholesterol 24-hydroxylase, a mediator of cholesterol homeostasis in the brain. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 7238-7243
6. Nebert D.W., and Russell D.W. Clinical importance of the cytochromes P450. Lancet 360 (2002) 1155-1162
7. Kotti T.J., Ramirez D.M., Pfeiffer B.E., Huber K.M., and Russell D.W. Brain cholesterol turnover required for geranylgeraniol production and learning in mice. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 3869-3874
8. Horton J.D., Goldstein J.L., and Brown M.S. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109 (2002) 1125-1131
9. Baulieu E.E. Neurosteroids: a novel function of the brain. Psychoneuroendocrinology 23 (1998) 963-987
10. Vallée M., George O., Vitiello S., Le Moal M., and Mayo W. New insights into the role of neuroactive steroids in cognitive aging. Exp. Gerontol. 39 (2004) 1695-1704
11. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., and Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232 (1986) 1004-1007
12. Bowlby M.R. Pregnenolone sulfate potentiation of N-methyl-D-aspartate receptor channels in hippocampal neurons. Mol. Pharmacol. 43 (1993) 813-819
13. Irwin R.P., Lin S.Z., Rogawski M.A., Purdy R.H., and Paul S.M. Steroid potentiation and inhibition of N-methyl-D-aspartate receptor-mediated intracellular Ca++ responses: structure-activity studies. J. Pharmacol. Exp. Ther. 271 (1994) 677-682
14. Selye H. The anesthetic effect of steroid hormones. Proc. Soc. Exp. Biol. Med. 46 (1941) 116-121
15. Baulieu E.-E. Steroid hormones in the brain: several mechanisms?. In: Fuxe K., Gustafsson J.A., and Weterberg L. (Eds). Steroid Hormone Regulation of the Brain (1981), Pergamon Press, Oxford 3-14
16. Corpéchot C., Young J., Calvel M., Wehrey C., Veltz J.N., Touyer G., Mouren M., Prasad V.V., Banner C., Sjövall J., Ballieu E.-E., and Robel P. Neurosteroids: 3 alpha-hydroxy-5 alpha-pregnan-20-one and its precursors in the brain, plasma, and steroidogenic glands of male and female rats. Endocrinology 133 (1993) 1003-1009
17. Stoffel-Wagner B. Neurosteroid metabolism in the human brain. Eur. J. Endocrinol. 145 (2001) 669-679
18. Mellon S.H., and Griffin L.D. Neurosteroids: biochemistry and clinical significance. Trends Endocrinol. Metab. 13 (2002) 35-43
19. Heverin M., Bogdanovic N., Lütjohann D., Bayer T., Pikuleva I., Bretillon L., Diczfalusy U., Winblad B., and Björkhem I. Changes in the levels of cerebral and extracerebral sterols in the brain of patients with Alzheimer's disease. J. Lipid Res. 45 (2004) 186-193
20. Mast N., Norcross R., Andersson U., Shou M., Nakayama K., Björkhem I., and Pikuleva I.A. Broad substrate specificity of human cytochrome P450 46A1 which initiates cholesterol degradation in the brain. Biochemistry 42 (2003) 14284-14292
21. Zhang J., Akwa Y., el-Etr M., Baulieu E.E., and Sjövall J. Metabolism of 27-, 25- and 24-hydroxycholesterol in rat glial cells and neurons. Biochem J. 322 (1997) 175-184
22. Rose K., Allan A., Gauldie S., Stapleton G., Dobbie L., Dott K., Martin C., Wang L., Hedlund E., Seckl J.R., Gustafsson J.A., and Lathe R. Neurosteroid hydroxylase CYP7B: vivid reporter activity in dentate gyrus of gene-targeted mice and abolition of a widespread pathway of steroid and oxysterol hydroxylation. J. Biol. Chem. 276 (2001) 23937-23944
23. Lin Y.Y., Welch M., and Lieberman S. The detection of 20S-hydroxycholesterol in extracts of rat brains and human placenta by a gas chromatograph/mass spectrometry technique. J. Steroid Biochem. Mol. Biol. 85 (2003) 57-61
24. Yao Z.X., Brown R.C., Teper G., Greeson J., and Papadopoulos V. 22R-Hydroxycholesterol protects neuronal cells from beta-amyloid-induced cytotoxicity by binding to beta-amyloid peptide. J. Neurochem. 83 (2002) 1110-1119
25. Puglielli L., Friedlich A.L., Setchell K.D., Nagano S., Opazo C., Cherny R.A., Barnham K.J., Wade J.D., Melov S., Kovacs D.M., and Bush A.I. Alzheimer disease beta-amyloid activity mimics cholesterol oxidase. J. Clin. Invest. 115 (2005) 2556-2563
26. Zhang Q., Powers E.T., Nieva J., Huff M.E., Dendle M.A., Bieschke J., Glabe C.G., Eschenmoser A., Wentworth Jr. P., Lerner R.A., and Kelly J.W. Metabolite-initiated protein misfolding may trigger Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 4752-4757
27. Liu S., Sjövall J., and Griffiths W.J. Neurosteroids in rat brain: extraction, isolation, and analysis by nanoscale liquid chromatography-electrospray mass spectrometry. Anal. Chem. 75 (2003) 5835-5846
28. Corpéchot C., Robel P., Axelson M., Sjövall J., and Baulieu E.E. Characterization and measurement of dehydroepiandrosterone sulfate in rat brain. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 4704-4707
29. Corpéchot C., Synguelakis M., Talha S., Axelson M., Sjövall J., Vihko R., Baulieu E.E., and Robel P. Pregnenolone and its sulfate ester in the rat brain. Brain Res. 270 (1983) 119-125
30. Alomary A.A., Fitzgerald R.L., and Purdy R.H. Neurosteroid analysis. Int. Rev. Neurobiol. 46 (2001) 97-115
31. Vallée M., Mayo W., Darnaudery M., Corpéchot C., Young J., Koehl M., Le Moal M., Baulieu E.E., Robel P., and Simon H. Neurosteroids: deficient cognitive performance in aged rats depends on low pregnenolone sulfate levels in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14865-14870
32. Griffiths W.J., Shackleton C., and Sjövall J. Steroid analysis. In: Caprioli R. (Ed). Encyclopedia of Mass Spectrometry vol. 3 (2006), Elsevier, Oxford
33. Dzeletovic S., Breuer O., Lund E., and Diczfalusy U. Determination of cholesterol oxidation products in human plasma by isotope dilution-mass spectrometry. Anal. Biochem. 225 (1995) 73-80
34. Lütjohann D., Breuer O., Ahlborg G., Nennesmo I., Siden A., Diczfalusy U., and Björkhem I. Cholesterol homeostasis in human brain: evidence for an age-dependent flux of 24S-hydroxycholesterol from the brain into the circulation. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 9799-9804
35. Lütjohann D., Brzezinka A., Barth E., Abramowski D., Staufenbiel M., von Bergmann K., Beyreuther K., Multhaup G., and Bayer T.A. Profile of cholesterol-related sterols in aged amyloid precursor protein transgenic mouse brain. J. Lipid Res. 43 (2002) 1078-1085
36. Lütjohann D., Stroick M., Bertsch T., Kuhl S., Lindenthal B., Thelen K., Andersson U., Björkhem I., Bergmann K.v., and Fassbender K. High doses of simvastatin, pravastatin, and cholesterol reduce brain cholesterol synthesis in guinea pigs. Steroids 69 (2004) 431-438
37. Leoni V., Masterman T., Patel P., Meaney S., Diczfalusy U., and Björkhem I. Side chain oxidized oxysterols in cerebrospinal fluid and the integrity of blood-brain and blood-cerebrospinal fluid barriers. J. Lipid Res. 44 (2003) 793-799
38. Leoni V., Shafaati M., Salomon A., Kivipelto M., Björkhem I., and Wahlund L.O. Are the CSF levels of 24S-hydroxycholesterol a sensitive biomarker for mild cognitive impairment?. Neurosci. Lett. 397 (2006) 83-87
39. Kim Y.S., Zhang H., and Kim H.Y. Profiling neurosteroids in cerebrospinal fluids and plasma by gas chromatography/electron capture negative chemical ionization mass spectrometry. Anal. Biochem. 277 (2000) 187-195
40. Vallée M., Rivera J.D., Koob G.F., Purdy R.H., and Fitzgerald R.L. Quantification of neurosteroids in rat plasma and brain following swim stress and allopregnanolone administration using negative chemical ionization gas chromatography/mass spectrometry. Anal. Biochem. 287 (2000) 153-166
41. Liere P., Pianos A., Eychenne B., Cambourg A., Liu S., Griffiths W., Schumacher M., Sjövall J., and Baulieu E.E. Novel lipoidal derivatives of pregnenolone and dehydroepiandrosterone and absence of their sulfated counterparts in rodent brain. J. Lipid Res. 45 (2004) 2287-2302
42. Shimada K., and Mukai Y. Studies on neurosteroids. VII. Determination of pregnenolone and its 3-stearate in rat brains using high-performance liquid chromatography-atmospheric pressure chemical ionization mass spectrometry. J. Chromatogr. B Biomed. Sci. Appl. 714 (1998) 153-160
43. Mitamura K., Yatera M., and Shimada K. Quantitative determination of pregnenolone-3-sulfate in rat brains using liquid chromatography/electrospray ionization-mass spectrometry. Anal. Sci. 15 (1999) 951-955
44. Higashi T., Takido N., and Shimada K. Studies on neurosteroids XVII. Analysis of stress-induced changes in neurosteroid levels in rat brains using liquid chromatography-electron capture atmospheric pressure chemical ionization-mass spectrometry. Steroids 70 (2005) 1-11
45. Higashi T., Ninomiya Y., Iwaki N., Yamauchi A., Takayama N., and Shimada K. Studies on neurosteroids XVIII LC-MS analysis of changes in rat brain and serum testosterone levels induced by immobilization stress and ethanol administration. Steroids 71 (2006) 609-617
46. Griffiths W.J. Tandem mass spectrometry in the study of fatty acids, bile acids, and steroids. Mass. Spectrom. Rev. 22 (2003) 81-152
47. Higashi T., Daifu Y., Ikeshima T., Yagi T., and Shimada K. Studies on neurosteroids XV. Development of enzyme-linked immunosorbent assay for examining whether pregnenolone sulfate is a veritable neurosteroid. J. Pharm. Biomed. Anal. 30 (2003) 1907-1917
48. Liu S., Sjövall J., and Griffiths W.J. Analysis of oxosteroids by nano-electrospray mass spectrometry of their oximes. Rapid Commun. Mass Spectrom 14 (2000) 390-400
49. Uzunov D.P., Cooper T.B., Costa E., and Guidotti A. Fluoxetine-elicited changes in brain neurosteroid content measured by negative ion mass fragmentography. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 12599-12604
50. Higashi T., and Shimada K. Derivatization of neutral steroids to enhance their detection characteristics in liquid chromatography-mass spectrometry. Anal. Bioanal. Chem. 378 (2004) 875-882
51. Higashi T., Yamauchi A., and Shimada K. 2-hydrazino-1-methylpyridine: a highly sensitive derivatization reagent for oxosteroids in liquid chromatography-electrospray ionization-mass spectrometry. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 825 (2005) 214-222
52. Higashi T., Takido N., and Shimada K. Detection and characterization of 20-oxosteroids in rat brains using LC-electron capture APCI-MS after derivatization with 2-nitro-4-trifluoromethylphenylhydrazine. Analyst 128 (2003) 130-133
53. Lütjohann D., Papassotiropoulos A., Björkhem I., Locatelli S., Bagli M., Oehring R.D., Schlegel U., Jessen F., Rao M.L., von Bergmann K., and Heun R. Plasma 24S-hydroxycholesterol (cerebrosterol) is increased in Alzheimer and vascular demented patients. J. Lipid Res. 41 (2000) 195-198
54. Bretillon L., Siden A., Wahlund L.O., Lütjohann D., Minthon L., Crisby M., Hillert J., Groth C.G., Diczfalusy U., and Björkhem I. Plasma levels of 24S-hydroxycholesterol in patients with neurological diseases. Neurosci. Lett. 293 (2000) 87-90
55. Schönknecht P., Lütjohann D., Pantel J., Bardenheuer H., Hartmann T., von Bergmann K., Beyreuther K., and Schroder J. Cerebrospinal fluid 24S-hydroxycholesterol is increased in patients with Alzheimer's disease compared to healthy controls. Neurosci. Lett. 324 (2002) 83-85
56. Burkard I., Rentsch K.M., and von Eckardstein A. Determination of 24S- and 27-hydroxycholesterol in plasma by high-performance liquid chromatography-mass spectrometry. J. Lipid Res. 45 (2004) 776-781
57. Babiker A., and Diczfalusy U. Transport of side-chain oxidized oxysterols in the human circulation. Biochim. Biophys. Acta. 1392 (1998) 333-339
58. Griffiths W.J., Wang Y., Alvelius G., Liu S., Bodin K., and Sjövall J. Analysis of oxysterols by electrospray tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 17 (2006) 341-362
59. Wang Y., Hornshaw M., Alvelius G., Bodin K., Liu S., Sjövall J., and Griffiths W.J. Matrix-assisted laser desorption/ionization high-energy collision-induced dissociation of steroids: analysis of oxysterols in rat brain. Anal. Chem. 78 (2006) 164-173
60. Bosco D.A., Fowler D.M., Zhang Q., Nieva J., Powers E.T., Wentworth Jr. P., Lerner R.A., and Kelly J.W. Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization. Nat. Chem. Biol. 2 (2006) 249-253
61. Wentworth Jr. P., McDunn J.E., Wentworth A.D., Takeuchi C., Nieva J., Jones T., Bautista C., Ruedi J.M., Gutierrez A., Janda K.D., Babior B.M., Eschenmoser A., and Lerner R.A. Evidence for antibody-catalyzed ozone formation in bacterial killing and inflammation. Science 298 (2002) 2195-2199
62. Wentworth Jr. P., Nieva J., Takeuchi C., Galve R., Wentworth A.D., Dilley R.B., DeLaria G.A., Saven A., Babior B.M., Janda K.D., Eschenmoser A., and Lerner R.A. Evidence for ozone formation in human atherosclerotic arteries. Science 302 (2003) 1053-1056
63. Wang K., Bermudez E., and Pryor W.A. The ozonation of cholesterol: separation and identification of 2,4-dinitrophenylhydrazine derivatization products of 3beta-hydroxy-5-oxo-5,6-secocholestan-6-al. Steroids 58 (1993) 225-229
64. Pulfer M.K., and Murphy R.C. Formation of biologically active oxysterols during ozonolysis of cholesterol present in lung surfactant. J. Biol. Chem. 279 (2004) 26331-26338
65. Smith L.L. Oxygen, oxysterols, ouabain, and ozone: a cautionary tale. Free Radic. Biol. Med. 37 (2004) 318-324
66. Griffiths W.J., Liu S., Alvelius G., and Sjövall J. Derivatisation for the characterisation of neutral oxosteroids by electrospray and matrix-assisted laser desorption/ionisation tandem mass spectrometry: the Girard P derivative. Rapid Commun. Mass Spectrom 17 (2003) 924-935
67. Brooks C.J., Cole W.J., Lawrie T.D., MacLachlan J., Borthwick J.H., and Barrett G.M. Selective reactions in the analytical characterisation of steroids by gas chromatography-mass spectrometry. J. Steroid Biochem. 19 (1983) 189-201
68. MacLachlan J., Wotherspoon A.T., Ansell R.O., and Brooks C.J. Cholesterol oxidase: sources, physical properties and analytical applications. J. Steroid Biochem. Mol. Biol. 72 (2000) 169-195
69. Teng J.I., and Smith L.L. Sterol peroxidation by Pseudomonas fluorescens cholesterol oxidase. Steroids 61 (1996) 627-633
70. Mano N., Goto T., Uchida M., Nishimura K., Ando M., Kobayashi N., and Goto J. Presence of protein-bound unconjugated bile acids in the cytoplasmic fraction of rat brain. J. Lipid Res. 45 (2004) 295-300