Allopregnanolone prevents memory impairment: Effect on mRNA expression and enzymatic activity of hippocampal 3-α hydroxysteroid oxide-reductase

Brain Research Bulletin

Volumn 87, Issue 2-3, 2012, Pages 280-285

  Escudero, Carla ^a   Casas, Sebastián ^a   Giuliani, Fernando ^a   Bazzocchini, Vanesa ^a   García, Sebastián ^a   Yunes, Roberto ^a   Cabrera, Ricardo ^a  

^a FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

Author keywords

3 HOR; 3 HSD; Allopregnanolone; Memory; Oestrogen; Progesterone

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 3ALPHA HYDROXYSTEROID DEHYDROGENASE; ESTRADIOL BENZOATE; MESSENGER RNA; PROGESTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; COGNITION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HORMONE SUBSTITUTION; LEARNING; LOCOMOTION; MEMORY; MEMORY DISORDER; MOBILIZATION; NERVE CELL NETWORK; NONHUMAN; OPEN FIELD TEST; OVARIECTOMY; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; TRAINING;

3-ALPHA-HYDROXYSTEROID DEHYDROGENASE (B-SPECIFIC); ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; ESTRADIOL; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HIPPOCAMPUS; INHIBITION (PSYCHOLOGY); MEMORY DISORDERS; MOTOR ACTIVITY; OVARIECTOMY; PREGNANOLONE; PROGESTERONE; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 84856596884     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2011.11.019     Document Type: Article

References (43)

1. Agís-Balboa R., Pinna G., Zhubi A., Maloku E., Veldic M., Costa E., Guidotti A. Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:14602-21407.
2. Alonso M., Viola H., Izquierdo I., Medina H. Aversive experiences are associated with a rapid and transient activation of ERKs in the rat hippocampus. Neurobiol. Learn. Mem. 2002, 77:119-124.
3. Bekinschtein P., Katche C., Slipczuk L., Gonzalez C., Dorman G., Cammarota M., Izquierdo I., Medina J.H. Persistence of long-term memory storage: new insights into its molecular signatures in the hippocampus and related structures. Neurotox. Res. 2010, 18:377-385.
4. Bimonte-Nelson H.A., Singleton R.S., Hunter C.L., Price K.L., Moore A.B., Granholm A.C. Ovarian hormones and cognition in the aged female rat. I. Long-term, but not short-term, ovariectomy enhances spatial performance. Behav. Neurosci. 2003, 117:1395-1406.
5. Bimonte-Nelson H.A., Singleton R.S., Williams B.J., Granholm A.C. Ovarian hormones and cognition in the aged female rat. II. Progesterone supplementation reverses the cognitive enhancing effects of ovariectomy. Behav. Neurosci. 2004, 118:707-714.
6. Caligaris L., Astrada J.J., Taleisnik S. Effect of oestrogen and progesterone on the release of luteinizing hormone in pseudopregnant rats. Acta Endocrinol. (Copenh.) 1972, 70:163-166.
7. Cammarota M., Bevilaqua L.R., Rossato J.I., Lima R.H., Medina J.H., Izquierdo I. Parallel memory processing by the CA1 region of the dorsal hippocampus and the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10279-10284.
8. Compagnone N.A., Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinol. 2000, 21:1-56.
9. Díaz-Véliz G., Urresta F., Dussaubat N., Mora S. Progesterone effects on the acquisition of conditioned avoidance responses an other motoric behaviors in intact and ovariectomized rats. Psychoneuroendocrinology 1994, 19:387-394.
10. Do Rego J.L., Seong J.Y., Burel D., Leprince J., Luu-The V., Tsutsui K., Tonon M.C., Pelletier G., Vaudry H. Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides. Front. Neuroendocrinol. 2009, 30:259-301.
11. Ebner D.L., Richardson R., Riccio D.C. Ovarian hormones and retention of learned fear in rats. Behav. Neural Biol. 1981, 33:45-58.
12. Frye C.A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol. Behav. 1995, 57:5-14.
13. Frye C.A., Bayon L.E. Mating stimuli influence endogenous variations in the neurosteroids 3alpha, 5alpha-THP and 3alpha-diol. J. Neuroendocrinol. 1999, 11:839-847.
14. Frye C.A. Neurosteroids' effects and mechanisms for social, cognitive, emotional, and physical functions. Psychoneuroendocrinology 2009, 34:143-161.
15. Furukawa A., Miyatake A., Ohnishi T., Ichikawa Y. Steroidogenic acute regulatory protein (StAR) transcripts constitutively expressed in the adult rat central nervous system: colocalization of StAR, cytochrome P-450SCC (CYP XIA1), and 3beta-hydroxysteroid dehydrogenase in the rat brain. J. Neurochem. 1998, 71:2231-2238.
16. Giuliani F.A., Yunes R., Mohn C.E., Laconi M., Rettori V., Cabrera R. Allopregnanolone induces LHRH and glutamate release through NMDA receptor modulation. Endocrine 2011, 40:21-26.
17. +-dependent 3 alpha-hydroxysteroid dehydrogenase from mouse liver cytosol. J. Biochem. 1988, 103:1027-1034.
18. Herd M.B., Belelli D., Lambert J.J. Neurosteroid modulation of synaptic and extrasynaptic GABAA receptors. Pharmacol. Ther. 2007, 116:20-34.
19. Hoog S.S., Pawlowski J.E., Alzari P.M., Penning T.M., Lewis M. Three-dimensional structure of rat liver 3 alpha-hydroxysteroid/dihydrodiol dehydrogenase: a member of the aldo-keto reductase superfamily. Proc. Natl. Acad. Sci. U.S.A 1994, 91:2517-2521.
20. Izquierdo I., Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 1997, 68:285-316.
21. Jez J.M., Penning T.M. The aldo-keto reductase (AKR) superfamily: an update. Chem. Biol. Interact. 2001, 130-132:499-525.
22. Johansson I.M., Birzniece V., Lindblad C., Olsson T., Bäckström T. Allopregnanolone inhibits learning in the Morris water maze. Brain Res. 2002, 934:125-131.
23. Karavolas H.J., Hodges D.R. Neuroendocrine metabolism of progesterone and related progestins. Ciba Found. Symp. 1990, 153:22-44. discussion 44-55.
24. Korol D.L., Unick K., Goosens K., Crane C., Gold P.E., Foster T.C. Estrogen effects on spatial performance and hippocampal physiology in female rats. Soc. Neurosci. Abstr. 1994, 20:1436.
25. Laconi M.R., Reggiani P.C., Penissi A., Yunes R., Cabrera R.J. Allopregnanolone modulates striatal dopaminergic activity of rats under different gonadal hormones conditions. Neurol. Res. 2007, 29:622-627.
26. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 1986, 23:1004-1007.
27. Melcangi R.C., Mensah-Nyagan A.G. Neurosteroids: measurement and pathophysiologic relevance. Neurochem. Int. 2008, 52:503-505.
28. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
29. Morrow A.L., Suzdak P.D., Paul S.M. Steroid hormone metabolites potentiate GABA receptor-mediated chloride ion flux with nanomolar potency. Eur. J. Pharmacol. 1987, 142:483-485.
30. Nanfaro F., Cabrera R., Bazzocchini V., Laconi M., Yunes R. Pregnenolone sulfate infused in lateral septum of male rats impairs novel object recognition memory. Pharmacol. Rep. 2010, 62:265-272.
31. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, University Press, Oxford.
32. Pawlowski J.E., Huizinga M., Penning T.M. Cloning and sequencing of the cDNA for rat liver 3 alpha-hydroxysteroid/dihydrodiol dehydrogenase. J. Biol. Chem. 1991, 266:8820-8825.
33. Penning T.M., Jin Y., Heredia V.V., Lewis M. Structure-function relationships in 3alpha-hydroxysteroid dehydrogenases: a comparison of the rat and human isoforms. J. Steroid Biochem. Mol. Biol. 2003, 85:247-255.
34. Quillfeldt J.A. Behavioral Methods to Study Learning and Memory in Rats 2006, vol. 21.
35. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. J. Neurochem. 1957, 20:11-21.
36. Takahashi M., Iwata N., Hara S., Mukai T., Takayama M., Endo T. Cyclic change in 3α-hydroxysteroid dehydrogenase in rat ovary during the estrous cycle. Biol. Reprod. 1995, 53:1265-1270.
37. Taleisnik S., Caligaris L., Astrada J.J. Effect of copulation on the release of pituitary gonadotropins in male and female rats. Endocrinology 1966, 79:49-54.
38. Vallée M., Mayo W., Darnaudéry M., Corpéchot C., Young J., Koehl M., Le Moal M., Baulieu E.E., Robel P., 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. 1997, 94:14865-21470.
39. Van Wimersma Greidanus T.B. Pregnene-type steroids and impairment of passive avoidance behavior in rats. Horm. Behav. 1977, 9:49-56.
40. Vianna M.R., Muller Igaz L., Coitinho A.S., Medina J.H., Izquierdo I. Memory extinction requires gene expression in rat hippocampus. Neurobiol. Learn. Mem. 2003, 79:199-203.
41. Walf A.A., Rhodes M.E., Frye C.A. Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats. Neurobiol. Learn. Mem. 2006, 86:35-46.
42. Warren S.G., Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behav. Neurosci. 1997, 111:259-266.
43. Zou L.B., Yamada K., Sasa M., Nakata Y., Nabeshima T. Effects of s1 receptor agonist SA4503 and neuroactive steroids on performance in a radial arm maze task in rats. Neuropharmacology 2000, 39:1617-1627.