Central administration of a cytochrome P450-7B product 7α- hydroxypregnenolone improves spatial memory retention in cognitively impaired aged rats

Journal of Neuroscience

Volumn 26, Issue 43, 2006, Pages 11034-11040

  Yau, Joyce L W ^a   Noble, June ^a   Graham, Mags ^a   Seckl, Jonathan R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Aging; DHEA; Hippocampus; Neurosteroids; Pregnenolone; Water maze

Indexed keywords

7ALPHA HYDROXYPREGNENOLONE; CYTOCHROME; CYTOCHROME P450 7B; NEUROSTEROID; PRASTERONE; PREGNENOLONE DERIVATIVE; STEROID; UNCLASSIFIED DRUG;

AGED; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; HIPPOCAMPUS; HYDROXYLATION; IMMUNE RESPONSE; MALE; MAZE TEST; MEMORY CONSOLIDATION; NONHUMAN; OSMOTIC PUMP; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; WORKING MEMORY;

17-ALPHA-HYDROXYPREGNENOLONE; AGING; ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; INJECTIONS, INTRAVENTRICULAR; MALE; MAZE LEARNING; MEMORY; RATS; RETENTION (PSYCHOLOGY); SPATIAL BEHAVIOR; STEROID HYDROXYLASES;

EID: 33751100895     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3189-06.2006     Document Type: Article

References (46)

1. Akwa Y, Morfin RF, Robel P, Baulieu EE (1992) Neurosteroid metabolism. 7Alpha-hydroxylation of dehydroepiandrosterone and pregnenolone by rat brain microsomes. Biochem J 288:959-964.
2. Alhaj HA, Massey AE, McAllister-Williams RH (2006) Effects of DHEA administration on episodic memory, cortisol and mood in healthy young men: a double-blind, placebo-controlled study. Psychopharmacology (Berl), in press.
3. Bean R, Seckl JR, Lathe R, Martin C (2001) Ontogeny of the neurosteroid enzyme Cyp7b in the mouse. Mol Cell Endocrinol 174:137-144.
4. Dellu F, Mayo W, Vallee M, Le Moal M, Simon H (1997) Facilitation of cognitive performance in aged rats by past experience depends on the type of information processing involved: a combined cross-sectional and longitudinal study. Neurobiol Learn Mem 67:121-128.
5. Diamond DM, Park CR, Heman KL, Rose GM (1999) Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9:542-552.
6. Doostzadeh J, Morfin R (1996) Studies of the enzyme complex responsible for pregnenolone and dehydroepiandrosterone 7a-hydroxylation in mouse tissues. Steroids 61:613-620.
7. Ebner MJ, Corol DI, Havlikova H, Honour JW, Fry JP (2006) Identification of neuroactive steroids and their precursors and metabolites in adult male rat brain. Endocrinology 147:179-190.
8. Flood JF, Roberts E (1988) Dehydroepiandrosterone sulfate improves memory in aging mice. Brain Res 448:178-181.
9. Flood JF, Smith GE, Roberts E (1988) Dehydroepiandrosterone and its sulfate enhance memory retention in mice. Brain Res 447:269-278.
10. Flood JF, Morley JE, Roberts E (1992) Memory-enhancing effects in male mice of pregnenolone and steroids metabolically derived from it. Proc Natl Acad Sci USA 89:1567-1571.
11. Flood JF, Morley JE, Roberts E (1995) Pregnenolone sulfate enhances post-training memory processes when injected in very low doses into limbic system structures: the amygdala is by far the most sensitive. Proc Natl Acad Sci USA 92:10806-10810.
12. Gallagher M, Burwell R, Burchinal M (1993) Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav Neurosci 107:618-626.
13. 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:S107-S112.
14. Huppert FA, Van Niekerk JK (2001) Dehydroepiandrosterone (DHEA) supplementation for cognitive function. Cochrane Database Syst Rev:CD000304.
15. Issa AM, Rowe W, Gauthier S, Meaney MJ (1990) Hypothalamic-pituitary- adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. J Neurosci 10:3247-3254.
16. Ladurelle N, Eychenne B, Denton D, Blair-West J, Schumacher M, Robel P, Baulieu E (2000) Prolonged intracerebroventricular infusion of neurosteroids affects cognitive performances in the mouse. Brain Res 858:371-379.
17. Lafaye P, Chmielewski V, Nato F, Mazie JC, Morfin R (1999) The 7alpha-hydroxysteroids produced in human tonsils enhance the immune response to tetanus toxoid and Bordetella pertussis antigens. Biochim Biophys Acta 1472:222-231.
18. Le Goascogne C, Sananes N, Gouezou M, Takemori S, Kominami S, Baulieu EE, Robel P (1991) Immunoreactive cytochrome P-450(17 alpha) in rat and guinea-pig gonads, adrenal glands and brain. J Reprod Fertil 93:609-622.
19. Loria RM, Padgett DA (1998) Control of the immune response by DHEA and its metabolites. Rinsho Byori 46:505-517.
20. May M, Holmes E, Rogers W, Poth M (1990) Protection from glucocorticoid induced thymic involution by dehydroepiandrosterone. Life Sci 46:1627-1631.
21. Mayo W, George O, Darbra S, Bouyer JJ, Vallee M, Darnaudery M, Pallares M, Lemaire-Mayo V, Le Moal M, Piazza PV, Abrous N (2003) Individual differences in cognitive aging: implication of pregnenolone sulfate. Prog Neurobiol 71:43-48.
22. Mellon SH, Deschepper CF (1993) Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Res 629:283-292.
23. Moisan M-P, Seckl JR, Edwards CRW (1990) 11β-hydroxysteroid dehydrogenase bioactivity and messenger RNA expression in rat forebrain: localization in hypothalamus, hippocampus and cortex. Endocrinology 127:1450-1455.
24. Morfin R, Courchay G (1994) Pregnenolone and dehydroepiandrosterone as precursors of native 7-hydroxylated metabolites which increase the immune response in mice. J Steroid Biochem Mol Biol 50:91-100.
25. Morfin R, Starka L (2001) Neurosteroid 7-hydroxylation products in the brain. Int Rev Neurobiol 46:79-95.
26. Muller C, Cluzeaud F, Pinon GM, Rafestin-Oblin ME, Morfin R (2004) Dehydroepiandrosterone and its 7-hydroxylated metabolites do not interfere with the transactivation and cellular trafficking of the glucocorticoid receptor. J Steroid Biochem Mol Biol 92:469-476.
27. Orentreich N, Brind JL, Vogelman JH, Andres R, Baldwin H (1992) Long-term longitudinal measurements of plasma dehydroepiandrosterone sulphate in normal men. J Clin Endocrinol Metab 75:1002-1004.
28. Paul SM, Purdy RH (1992) Neuroactive steroids. FASEB J 6:2311-2322.
29. 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.
30. Robel P, Baulieu EE (1995) Neurosteroids: biosynthesis and function. Crit Rev Neurobiol 9:383-394.
31. Robinzon B, Michael KK, Ripp SL, Winters SJ, Prough RA (2003) Glucocorticoids inhibit interconversion of 7-hydroxy and 7-oxo metabolites of dehydroepiandrosterone: a role for 11beta-hydroxysteroid dehydrogenases? Arch Biochem Biophys 412:251-258.
32. Rose K, Allan A, Gauldie S, Stapleton G, Dobbie L, Dott K, Martin C, Wang L, Hedlund E, Seckl JR, Gustafsson JA, Lathe R (2001) 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 276:23937-23944.
33. Rose KA, Stapleton G, Dott K, Kieny MP, Best R, Schwarz M, Russell DW, Björkhem I, Seckl J, Lathe R (1997) Cyp7b, a novel brain cytochrome P450, catalyzes the synthesis of neurosteroids 7a-hydroxy dehydroepiandrosterone and 7a-hydroxy pregnenolone. Proc Natl Acad Sci USA 94:4925-4930.
34. Seckl JR (1997) 11Beta-hydroxysteroid dehydrogenase in the brain: a novel regulator of glucocorticoid action? Front Neuroendocrinol 18:49-99.
35. Shi J, Schulze S, Lardy HA (2000) The effect of 7-oxo-DHEA acetate on memory in young and old C57BL/6 mice. Steroids 65:124-129.
36. Sliwinski A, Monnet FP, Schumacher M, Morin-Surun MP (2004) Pregnenolone sulfate enhances long-term potentiation in CA1 in rat hippocampus slices through the modulation of N-methyl-D-aspartate receptors. J Neurosci Res 78:691-701.
37. Stapleton G, Steel M, Richardson M, Mason JO, Rose KA, Morris RGM, Lathe R (1995) A novel cytochrome P450 expressed primarily in brain. J Biol Chem 270:29739-29745.
38. Vallee M, Mayo W, Darnaudery M, Corpechot C, Young J, Koehl M, Le Moal M, Baulieu EE, Robel P, Simon H (1997) Neurosteroids: deficient cognitive performance in aged rats depends on low pregnenolone sulfate levels in the hippocampus. Proc Natl Acad Sci USA 94:14865-14870.
39. Vallee M, Mayo W, Le Moal M (2001) Role of pregnenolone, dehydroepiandrosterone and their sulfate esters on learning and memory in cognitive aging. Brain Res Brain Res Rev 37:301-312.
40. Vallee M, George O, Vitiello S, Le Moal M, Mayo W (2004) New insights into the role of neuroactive steroids in cognitive aging. Exp Gerontol 39:1695-1704.
41. van Groen T, Kadish I, Wyss JM (2002) Old rats remember old tricks; memories of the water maze persist for 12 months. Behav Brain Res 136:247-255.
42. Weill-Engerer S, David JP, Sazdovitch V, Liere P, Schumacher M, Delacourte A, Baulieu EE, Akwa Y (2003) In vitro metabolism of dehydroepiandrosterone (DHEA) to 7alpha-hydroxy-DHEA and Delta5-androstene- 3beta,17beta-diol in specific regions of the aging brain from Alzheimer's and non-demented patients. Brain Res 969:117-125.
43. Wolf OT, Neumann O, Hellhammer DH, Geiben AC, Strasburger CJ, Dressendorfer RA, Pirke KM, Kirschbaum C (1997) Effects of a two-week physiological dehydroepiandrosterone substitution on cognitive performance and well-being in healthy elderly women and men. J Clin Endocrinol Metab 82:2363-2367.
44. Yau JL, Olsson T, Morris RGM, Meaney MJ, Seckl JR (1995) Glucocorticoids, hippocampal corticosteroid receptor gene expression and antidepressant treatment: relationship with spatial learning in young and aged rats. Neuroscience 66:571-581.
45. Yau JL, Noble J, Kenyon CJ, Hibberd C, Kotelevtsev Y, Mullins JJ, Seckl JR (2001) Lack of tissue glucocorticoid reactivation in 11beta -hydroxysteroid dehydrogenase type 1 knockout mice ameliorates age-related learning impairments. Proc Natl Acad Sci USA 98:4716-4721.
46. Yau JL, Rasmuson S, Andrew R, Graham M, Noble J, Olsson T, Fuchs E, Lathe R, Seckl JR (2003) Dehydroepiandrosterone 7-hydroxylase CYP7B: predominant ex pression in primate hippocampus and reduced expression in Alzheimer's disease. Neuroscience 121:307-314.