Dehydroepiandrosterone sulfate prevents ischemia-induced impairment of long-term potentiation in rat hippocampal CA1 by up-regulating tyrosine phosphorylation of NMDA receptor

Neuropharmacology

Volumn 51, Issue 5, 2006, Pages 958-966

  Li, Zhen ^a   Zhou, Rong ^a   Cui, Shengzhong ^a   Xie, Guiqin ^a   Cai, Weiyan ^a   Sokabe, Masahiro ^b,c,d   Chen, Ling ^a,b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

Dehydroepiandrosterone sulfate (DHEAS); Ischemia; Long term potentiation; NMDA receptor; Sigma1 ( 1) receptor

Indexed keywords

2 [4 METHOXY 3 (2 PHENYLETHOXY)PHENYL] N,N DIPROPYLETHYLAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PRASTERONE SULFATE; PROGESTERONE;

ANALYTIC METHOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FOLLOW UP; HIPPOCAMPUS; ISCHEMIA; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; RAT; REPERFUSION INJURY; TRANSIENT ISCHEMIC ATTACK; UPREGULATION;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; ANISOLES; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; DEHYDROEPIANDROSTERONE SULFATE; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; IMMUNOPRECIPITATION; ISCHEMIA; LONG-TERM POTENTIATION; MALE; PHOSPHORYLATION; PROPYLAMINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; TYROSINE; UP-REGULATION;

EID: 33749526113     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2006.06.007     Document Type: Article

References (61)

1. Azuma T., Nagai Y., Saito T., Funauchi M., Matsubara T., and Sakoda S. The effect of dehydroepiandrosterone sulfate administration to patients with multi-infarct dementia. J. Neurol. Sci. 162 (1999) 69-73
2. Baulieu E.E., and Robel P. Dehydroepiandrosterone (DHEA) and dehydroepiandrosterone sulfate (DHEAS) as neuroactive neurosteroids. Proc. Natl. Acad. Sci. U.S.A 95 (1998) 4089-4091
3. Bendel O., Prunell G., Stenqvist A., Mathiesen T., Holmin S., Svendgaard N.A., and Euler G. Experimental subarachnoid hemorrhage induces changes in the levels of hippocampal NMDA receptor subunit mRNA. Brain Res. Mol. Brain Res. 13 (2005) 119-125
4. Bergeron R., de Montigny C., and Debonnel G. Potentiation of neuronal NMDA response induced by dehydroepiandrosterone and its suppression by progesterone: effects mediated via sigma receptors. J. Neurosci. 1 (1996) 1193-1202
5. Bi R., Rong Y., Bernard A., Khrestchatisky M., and Baudry M. Src-mediated tyrosine phosphorylation of NR2 subunits of N-methyl-d-aspartate receptors protects from calpain-mediated truncation of their C-terminal domains. J. Biol. Chem. 25 (2000) 26477-26483
6. 2+ injury 24 h following severe forebrain ischemia and reduces infarction following focal ischemia. J. Cereb. Blood Flow Metab. 14 (1994) 903-910
7. Chen J., Chopp M., and Li Y. Neuroprotective effects of progesterone after transient middle cerebral artery occlusion in rat. J. Neurol. Sci. 171 (1999) 24-30
8. 1) receptor: optical imaging study in rat hippocampal slices. Neuropharmacology 50 (2006) 380-392
9. Chen, L., Miyamoto, Y., Furuya, K., Dai, X.N., Mori, N., Sokabe, M., 2006b. Chronic DHEAS administration facilitates hippocampal long-term potentiation via an amplification of Src-dependent NMDA receptor signaling. Neuropharmacology, in press. doi:10.1016/j.neuropharm.2006.05.011.
10. Cheney D.L., Uzunov D., and Guidotti A. Pregnenolone sulfate antagonizes dizocilpine amnesia: role for allopregnanolone. Neuroreport 6 (1995) 1697-1700
11. Cheung H.H., Takagi N., Teves L., Logan R., Wallace M.C., and Gurd J.W. Altered association of protein tyrosine kinases with postsynaptic densities after transient cerebral ischemia in the rat brain. J. Cereb. Blood Flow Metab. 20 (2000) 505-512
12. Cheung H.H., Teves L., Wallace M.C., and Gurd J.W. Inhibition of protein kinase C reduces ischemia-induced tyrosine phosphorylation of the N-methyl-d-aspartate receptor. J. Neurochem. 86 (2003) 1441-1449
13. Collingridge G.L., and Bliss T.V. Memories of NMDA receptors and LTP. Trends Neurosci. 18 (1995) 54-56
14. Flood J.F., and Roberts E. Dehydroepiandrosterone sulfate improves memory in aging mice. Brain Res. 448 (1988) 178-181
15. Flood J.F., Smith G.E., and Roberts E. Dehydroepiandrosterone and its sulfate enhance memory retention in mice. Brain Res. 447 (1988) 269-278
16. Flood J.F., Farr S.A., Johnson D.A., Li P.K., and Morley J.E. Peripheral steroid sulfatase inhibition potentiates improvement of memory retention for hippocampally administered dehydroepiandrosterone sulfate but not pregnenolone sulfate. Psychoneuroendocrinology 24 (1999) 799-811
17. Grosshans D.R., Clayton D.A., Coultrap S.J., and Browning M.D. LTP leads to rapid sulface expression of NMDA but not AMPA receptors in adult rat CA1. Nat. Neurosci. 5 (2002) 27-33
18. Jiang N., Chopp M., Stein D., and Feit H. Progesterone is neuroprotective after transient middle cerebral artery occlusion in male rats. Brain Res. 735 (1996) 101-107
19. Johnson D.A., Wu T., Li P., and Maher T.J. The effect of steroid sulfatase inhibition on learning and spatial memory. Brain Res. 26 (2000) 286-290
20. Kalia L.V., and Salter M.W. Interactions between Src family protein tyrosine kinases and PSD-95. Neuropharmacology 45 (2003) 720-728
21. Kalia L.V., Gingrich J.R., and Salter M.W. Src in synaptic transmission and plasticity. Oncogene 23 (2004) 8007-8016
22. Kimonides V.G., Khatibi N.H., Svendsen C.N., Sofroniew M.V., and Herbert J. Dehydroepiandrosterone (DHEA) and DHEA-sulfate (DHEAS) protect hippocampal neurons against excitatory amino acid-induced neurotoxicity. Proc. Natl. Acad. Sci. U.S.A 95 (1998) 1852-1857
23. A receptors. Stroke 31 (2000) 1953-1957
24. Leblhuber F., Windhager E., Reisecker F., Steinparz F.X., and Dienstl E. Dehydroepiandrosterone sulfate in Alzheimer's disease. Lancet 336 (1990) 449-454
25. Li P.K., Rhodes M.E., Burke A.M., and Johnson D.A. Memory enhancement mediated by the steroid sulfatase inhibitor (p-O-sulfamoyl)-N-tetradecanoyl tyramine. Life Sci. 60 (1997) 45-51
26. Lu Y.M., Roder J.C., Davidow J., and Salter M.W. Src activation in the induction of long-term potentiation in CA1 hippocampal neurons. Science 279 (1998) 1363-1367
27. A receptor. Brain Res. 526 (1990) 143-146
28. Mao X., and Barger S.W. Neuroprotection by dehydroepiandrosterone-sulfate: role of an NFkB-like factor. Neuroreport 9 (1998) 759-763
29. Mathis C., Paul S.M., and Crawley J.N. The neurosteroid pregnenolone sulfate blocks NMDA antagonist-induced deficits in a passive avoidance memory task. Psychopharmacology 116 (1994) 201-206
30. Maurice T., and Privat A. SA4503, a novel cognitive enhancer with sigma (σ) receptor agonist properties, facilitates NMDA receptor-dependent learning in mice. Eur. J. Pharmacol. 328 (1997) 9-18
31. Maurice T., Junien J.L., and Privat A. Dehydroepiandrosterone sulfate attenuates dizocilpine-induced learning impairment in mice via σ1 receptors. Behav. Brain Res. 83 (1997) 159-164
32. Maurice T., Su T.P., and Privat A. Sigma (σ) receptor agonists and neurosteroids attenuate β-amyloid peptide-induced amnesia in 25-35 mice through a common mechanism. Neurosci. 83 (1998) 413-428
33. 1) receptor: Pharmacological evidence and therapeutic opportunities. Jpn. J. Pharmacol. 81 (1999) 125-155
34. Mayo W., Dellu F., Robel P., Cherkaoui J., Le Moal M., Baulieu E.E., and Simon H. Infusion of neurosteroids into the nucleus basalis magnocellularis affects cognitive processes in the rat. Brain Res. 607 (1993) 324-328
35. Meyer J.H., Lee S., Wittenberg G.F., Randall R.D., and Gruol D.L. Neurosteroid regulation of inhibitory synaptic transmission in the rat hippocampus in vitro. Neuroscience 90 (1999) 1177-1183
36. Monnet F.P., Mahe V., Robel P., and Baulieu E.E. Neurosteroids, via sigma receptors, modulate the [H]norepinephrine release evoked by N-methyl-d-aspartate in the rat hippocampus. Proc. Natl. Acad. Sci. U.S.A 92 (1995) 3774-3778
37. Mori K., Yoshioka M., Suda N., Togashi H., Matsumoto M., Ueno K.I., and Saito H. An incomplete cerebral ischemia produced a delayed dysfunction in the rat hippocampal system. Brain Res. 795 (1998) 221-226
38. 2+ signaling mediated by recombinant N-methyl-d-aspartate receptor expressed in Chinese hamster ovary cells. Neurosci. Lett. 282 (2000) 93-96
39. Nasman B., Oisson T., Bachstrom T., Eriksson S., Grankvist K., Viitanen M., and Bucht G. Serum dehydroepiandrosterone sulfate in Alzheimer's disease and in multi-infarct dementia. Biol. Psychiatry 30 (1991) 684-690
40. O'Dell T.J., Kandel E.R., and Grant S.G. Long-term potentiation in the hippocampus is blocked by tyrosine kinase inhibitors. Nature 10 (1991) 558-560
41. Okuyama S., Imagawa I., Sakagawa T., Nakazato A., Yamaguchi K., Katoh M., Yamada S., Araki H., and Otomo S. NE-100, a novel sigma receptor ligand: effect on phencyclidine-induced behaviors in rats, dogs and monkeys. Life Sci. 55 (1994) 133-138
42. Pei L., Li Y., Zhang G.Y., Cui Z.C., and Zhu Z.M. Mechanisms of regulation of tyrosine phosphorylation of NMDA receptor subunit 2B after cerebral ischemia/reperfusion. Acta Pharmacol. Sin. 21 (2000) 695-700
43. Pelkey K.A., Askalan R., Paul S., Kalia L.V., Nguyen T.H., Pitcher G.M., Salter M.W., and Lombroso P.J. Tyrosine phosphatase STEP is a tonic brake on induction of long-term potentiation. Neuron 28 (2002) 127-138
44. Rhodes M.E., Li P.K., Burke A.M., and Johnson D.A. Enhanced plasma DHEAS, brain acetylcholine and memory mediated by steroid sulfatase inhibition. Brain Res. 773 (1997) 28-32
45. Rong Y., Lu X., Bernard A., Khrestchatisky M., and Baudry M. Tyrosine phosphorylation of ionotropic glutamate receptors by Fyn or Src differentially modulates their susceptibility to calpain and enhances their binding to spectrin and PSD-95. J. Neurochem. 79 (2001) 382-390
46. Rostas J.A., Brent V.A., Voss K., Errington M.L., Bliss T.V., and Gurd J.W. Enhanced tyrosine phosphorylation of the 2B subunit of the N-methyl-d-aspartate receptor in long-term potentiation. Proc. Natl. Acad. Sci. U.S.A 17 (1996) 10452-10456
47. Salter M.W., and Kalia L.V. Src kinases: a hub for NMDA receptor regulation. Nature 5 (2004) 317-328
48. Schneider L.S., Hinsey M., and Lyness S. Plasma dehydroepiandrosterone sulfate in Alzheimer's disease. Biol. Psychiatry 31 (1992) 205-208
49. Simpkins K.L., Guttmann R.P., Dong Y., Chen Z., Sokol S., Neumar R.W., and Lynch D.R. Selective activation induced cleavage of the NR2B subunit by calpain. J. Neurosci. 10 (2003) 11322-11331
50. Su T.P., Wu X.Z., Cone E.J., Shukla K., Gund T.M., Dodge A.L., and Parish D.W. Sigma compounds derived from phencyclidine: identification of PRE-084, a new, selective sigma ligand. J. Pharmacol. Exp. Ther. 259 (1991) 543-548
51. Takagi N., Cheung H.H., Bissoon N., Teves L., Wallace M.C., and Gurd J.W. The effect of transient global ischemia on the interaction of Src and Fyn with the n-methyl-d-aspartate receptor and postsynaptic densities: possible involvement of Src homology 2 domains. J. Cereb. Blood Flow Metab. 19 (1999) 880-888
52. Takagi N., Logan R., Teves L., Wallace M.C., and Gurd J.W. Altered interaction between PSD-95 and the NMDA receptor following transient global ischemia. J. Neurochem. 74 (2000) 169-178
53. Todd N.V., Crockard H.A., Russel R.W., and Picozzi P. Cerebral blood flow in the four-vessel occlusion rat model. Stroke 15 (1984) 579-585
54. 1) receptors. Brain Res. 799 (1998) 64-77
55. Vallee M., Mayo W., Darnaudery M., Corpechot 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
56. Vallee M., Mayo W., and Le Moal M. Role of pregnenolone, dehydroepiandrosterone and their sulfate esters on learning and memory in cognitive aging. Brain Res. Rev. 37 (2001) 301-312
57. Wang Y.T., and Salter M.W. Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369 (1994) 233-235
58. Weill-Engerer S., David J.P., Sazdovitch V., Liere P., Eychenne B., Pianos A., Schumacher M., Delacourte A., Baulieu E.E., and Akwa Y. Neurosteroid quantification in human brain regions: comparison between Alzheimer's and nondemented patients. J. Clin. Endocrinol. Metab. 87 (2002) 5138-5143
59. Yanase T., Fukahori M., Taniguchi S., Nishi Y., Sakai Y., Takayanagi R., Haji M., and Nawata H. Serum dehydroepiandrosterone (DHEA) and DHEA-sulfate (DHEA-S) in Alzheimer's disease and in cerebrovascular dementia. Endocr. J. 43 (1996) 119-123
60. Yu X.M., Askalan R., Keil G.J., and Salter M.W. NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275 (1997) 674-678
61. Zalewska T., Ziemka-Nalecz M., and Domanska-Janik K. Transient forebrain ischemia effects interaction of Src, FAK, and PYK2 with the NR2B subunit of N-methyl-d-aspartate receptor in gerbil hippocampus. Brain Res. 3 (2005) 214-223