Neuroprotection by the synthetic neurosteroid enantiomers ent-PREGS and ent-DHEAS against Aβ25-35 peptide-induced toxicity in vitro and in vivo in mice

Psychopharmacology

Volumn 231, Issue 17, 2014, Pages 3293-3312

  El Bitar, Fadia ^a,b   Meunier, Johann ^c   Villard, Vanessa ^c   Alméras, Marion ^c   Krishnan, Kathiresan ^d   Covey, Douglas F ^d   Maurice, Tangui ^c   Akwa, Yvette ^a  

^a Universite Paris Sud   (France)

^b KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^c University of Montpellier   (France)

^d WASHINGTON UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Dehydroepiandrosterone sulphate; Enantiomer; Learning and memory; Memory; Neuroprotection; Neurosteroid; Oxidative stress; Pregnenolone sulphate; amyloid toxicity

Indexed keywords

AMYLOID BETA PROTEIN[25-35]; LIPID; PRASTERONE SULFATE; PREGNENOLONE SULFATE; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (25-35); NEUROPROTECTIVE AGENT; PEPTIDE FRAGMENT; PREGNENOLONE;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CELL VIABILITY; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; ENANTIOMER; FLOW CYTOMETRY; IN VITRO STUDY; IN VIVO STUDY; LIPID PEROXIDATION; MALE; MEMORY; MENTAL PERFORMANCE; MOUSE; NERVE CELL NECROSIS; NEUROBLASTOMA CELL LINE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PASSIVE AVOIDANCE; PRIORITY JOURNAL; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; AVOIDANCE BEHAVIOR; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; HUMAN; NEURITE; RAT; TUMOR CELL LINE;

AMYLOID BETA-PEPTIDES; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CELL LINE, TUMOR; CELL SURVIVAL; DEHYDROEPIANDROSTERONE SULFATE; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; IN VITRO TECHNIQUES; LIPID PEROXIDATION; MALE; MICE; NEURITES; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; PREGNENOLONE; RATS;

EID: 84906938704     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-014-3435-3     Document Type: Article

References (59)

1. Akan P, Kizildag S, Ormen M, Genc S, Oktem MA, Fadiloglu M (2009) Pregnenolone protects the PC-12 cell line against amyloid β peptide toxicity but its sulfate ester does not. Chem Biol Interact 177:65-70
2. Akwa Y, Ladurelle N, Covey DF, Baulieu EE (2001) The synthetic enantiomer of pregnenolone sulfate is very active on memory in rats and mice, even more so than its physiological neurosteroid counterpart: distinct mechanisms? Proc Natl Acad Sci U S A 98:14033-14037 (Pubitemid 33116019)
3. Behl C, Davis JB, Klier FG, Schubert D (1994) Amyloid β peptide induces necrosis rather than apoptosis. Brain Res 645:253-264 (Pubitemid 24140132)
4. Behl C (1997) Amyloid β-protein toxicity and oxidative stress in Alzheimer's disease. Cell Tissue Res 290:471-480
5. Blennow K, de Leon MJ, Zetterberg H (2006) Alzheimer's disease. Lancet 368:387-403 (Pubitemid 44108123)
6. Butterfield DA, Drake J, Pocernich C, Castegna A (2001) Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid β-peptide. Trends Mol Med 7:548-554 (Pubitemid 33127140)
7. Butterfield DA, Castegna A, Lauderback CM, Drake J (2002a) Evidence that amyloid β-peptide-induced lipid peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death. Neurobiol Aging 23:655-664 (Pubitemid 35217687)
8. Butterfield DA, Griffin S, Munch G, Pasinetti GM (2002b) Amyloid β-peptide and amyloid pathology are central to the oxidative stress and inflammatory cascades under which Alzheimer's disease brain exists. J Alzheimers Dis 4:193-201 (Pubitemid 35006051)
9. Compagnone NA, Mellon SH (1998) Dehydroepiandrosterone: a potential signalling molecule for neocortical organization during development. Proc Natl Acad Sci U S A 95:4678-4683 (Pubitemid 28207973)
10. Compagnone NA, Mellon SH (2000) Neurosteroids: biosynthesis and function of these novel neuromodulators. Front Neuroendocrinol 21:1-56 (Pubitemid 30105920)
11. Covey DF (2009) ent-Steroids: novel tools for studies of signaling pathways. Steroids 74:577-585
12. Covey DF, Evers AS, Mennerick S, Zorumski CF, Purdy RH (2001) Recent developments in structure-activity relationships for steroid modulators of GABAA receptors. Brain Res Brain Res Rev 37:91-97 (Pubitemid 34020723)
13. Deshpande A, Mina E, Glabe C, Busciglio J (2006) Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons. J Neurosci 26:6011-6018 (Pubitemid 44318367)
14. Ekinci FJ, Linsley MD, Shea TB (2000) β-amyloid-induced calcium influx induces apoptosis in culture by oxidative stress rather than tau phosphorylation. Brain Res Mol Brain Res 76:389-395 (Pubitemid 30179777)
15. El Bitar F, Dastugue B, Meiniel A (1999) Neuroblastoma B104 cell line as a model for analysis of neurite outgrowth and neuronal aggregation induced by Reissner's fiber material. Cell Tissue Res 298:233-242 (Pubitemid 29512075)
16. Farr SA, Banks WA, Uezu K, Gaskin FS, Morley JE (2004) DHEAS improves learning and memory in aged SAMP8 mice but not in diabetic mice. Life Sci 75:2775-2785 (Pubitemid 39349264)
17. Flood JF, Smith GE, Roberts E (1988) Dehydroepiandrosterone and its sulfate enhance memory retention in mice. Brain Res 447:269-278
18. Forloni G, Bugiani O, Tagliavini F, Salmona M (1996) Apoptosis-mediated neurotoxicity induced by β-amyloid and PrP fragments. Mol Chem Neuropathol 28:163-171 (Pubitemid 26275064)
19. 25-35-induced toxicity, lipid peroxidation and glucose utilization in human SK-N-SH neuroblastoma cells. Brain Res 778:158-165
20. Gursoy E, Cardounel A, Kalimi M (2001) Pregnenolone protects mouse hippocampal (HT-22) cells against glutamate and amyloid-β protein toxicity. Neurochem Res 26:15-21 (Pubitemid 32428808)
21. A mRNAs have functional receptors. J Neurosci 14:5429-5436
22. Hardy J, Gwinn-Hardy K (1998) Genetic classification of primary neurodegenerative disease. Science 282:1075-1079 (Pubitemid 28516229)
23. Harkany T, Hortobagyi T, Sasvari M, Konya C, Penke B, Luiten PG, Nyakas C (1999) Neuroprotective approaches in experimental models of β-amyloid neurotoxicity: relevance to Alzheimer's disease. Prog Neuropsychopharmacol Biol Psychiatry 23:963-1008 (Pubitemid 29468909)
24. Hermes-Lima M, Willmore WG, Storey KB (1995) Quantification of lipid peroxidation in tissue extracts based on Fe(III)xylenol orange complex formation. Free Radic Biol Med 19:271-280
25. Holscher C, Gengler S, Gault VA, Harriott P, Mallot HA (2007) Soluble β-amyloid[25-35] reversibly impairs hippocampal synaptic plasticity and spatial learning. Eur J Pharmacol 561:85-90 (Pubitemid 46435857)
26. Kaminsky YG, Marlatt MW, Smith MA, Kosenko EA (2010) Subcellular and metabolic examination of amyloid-β peptides in Alzheimer disease pathogenesis: evidence for Aβ25-35. Exp Neurol 221:26-37
27. Loo DT, Copani A, Pike CJ, Whittemore ER, Walencewicz AJ, Cotman CW (1993) Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc Natl Acad Sci U S A 90:7951-7955 (Pubitemid 23260832)
28. Malouf AT (1992) Effect of β-amyloid peptides on neurons in hippocampal slice cultures. Neurobiol Aging 13:543-551
29. Mark RJ, Blanc EM, Mattson MP (1996) Amyloid β-peptide and oxidative cellular injury in Alzheimer's disease. Mol Neurobiol 12:211-224 (Pubitemid 126718488)
30. Markowski M, Ungeheuer M, Bitran D, Locurto C (2001) Memory-enhancing effects of DHEAS in aged mice on a win-shift water escape task. Physiol Behav 72:521-525 (Pubitemid 32244414)
31. Mathis C, Vogel E, Cagniard B, Criscuolo F, Ungerer A (1996) The neurosteroid pregnenolone sulfate blocks deficits induced by a competitive NMDA antagonist in active avoidance and lever-press learning tasks in mice. Neuropharmacology 35:1057-1064 (Pubitemid 27008180)
32. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE (1992) β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12:376-389
33. Maurice T, Lockhart BP, Privat A (1996) Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction. Brain Res 706:181-193 (Pubitemid 26048681)
34. 1) receptor: biochemical and physiological evidences, consequences in neuroprotection. Pharmacol Biochem Behav 84:581-597
35. Maurice T, Junien JL, Privat A (1997) Dehydroepiandrosterone sulfate attenuates dizocilpine-induced learning impairment in mice via sigma 1-receptors. Behav Brain Res 83:159-164 (Pubitemid 27086630)
36. 25-35-amyloid peptide-induced amnesia in mice through a common mechanism. Neuroscience 83:413-428
37. 25-35 peptide-induced toxicity in mice involve an interaction with the sigma1 receptor. Br J Pharmacol 149:998-1012
38. Miranda S, Opazo C, Larrondo LF, Munoz FJ, Ruiz F, Leighton F (2000) The role of oxidative stress in the toxicity induced by amyloid β-peptide in Alzheimer's disease. Prog Neurobiol 62:633-648 (Pubitemid 30407138)
39. A receptor pharmacology of enantiomers of dehydroepiandrosterone sulfate, pregnenolone sulfate, and (3α, 5β)-3-hydroxypregnan-20-one sulfate. J Med Chem 41:2604-2613
40. Petit GH, Tobin C, Krishnan K, Moricard Y, Covey DF, Rondi-Reig L, Akwa Y (2011) Pregnenolone sulfate and its enantiomer: differential modulation of memory in a spatial discrimination task using forebrain NMDA receptor deficient mice. Eur Neuropsychopharmacol 21:211-215
41. 25-35 region to aggregation and neurotoxicity. J Neurochem 64:253-265
42. Sayre LM, Zelasko DA, Harris PL, Perry G, Salomon RG, Smith MA (1997) 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J Neurochem 68:2092-2097 (Pubitemid 27176147)
43. Schubert D, Brass B, Dumas JP (1986) Protein complexity of central nervous system cell lines. J Neurosci 6:2829-2836 (Pubitemid 16026062)
44. Schubert D, Heinemann S, Carlisle W, Tarikas H, Kimes B, Patrick J, Steinbach JH, Culp W, Brandt BL (1974) Clonal cell lines from the rat central nervous system. Nature 249:224-227
45. Selkoe DJ (1997) Alzheimer's disease: genotypes, phenotypes, and treatments. Science 275:630-631
46. Solovyan V, Bezvenyuk Z, Huotari V, Tapiola T, Suuronen T, Salminen A (1998) Distinct mode of apoptosis induced by genotoxic agent etoposide and serum withdrawal in neuroblastoma cells. Mol Brain Res 62:43-55 (Pubitemid 29023177)
47. 25-35 peptide induces impairment in short-term rather than long-term memory in rats. Brain Res Bull 61:197-205
48. A receptor subunit mRNAs in 13 cell lines. J Neurosci 14:5417-5428
49. Vallée M, Mayo W, Le Moal M (2001a) Role of pregnenolone, dehydroepiandrosterone and their sulfate esters on learning and memory in cognitive aging. Brain Res Brain Res Rev 37:301- 312
50. Vallée M, Shen W, Heinrichs SC, Zorumski CF, Covey DF, Koob GF, Purdy RH (2001b) Steroid structure and pharmacological properties determine the anti- amnesic effects of pregnenolone sulphate in the passive avoidance task in rats. Eur J Neurosci 14:2003 - 2010
51. 25-35-induced toxicity in mice. Neuropsychopharmacology 34:1552-1566
52. 2 toxicity in human neuroblastoma SK-N-SH cells. Mol Pharmacol 70:395-404
53. Weaver CE Jr, Wu FS, Gibbs TT, Farb DH (1998) Pregnenolone sulfate exacerbates NMDA-induced death of hippocampal neurons. Brain Res 803:129-136 (Pubitemid 28392138)
54. Weill-Engerer S, David JP, Sazdovitch V, Liere P, Eychenne B, Pianos A, Schumacher M, Delacourte A, Baulieu EE, Akwa Y (2002) Neurosteroid quantification in human brain regions: comparison between Alzheimer's and nondemented patients. J Clin Endocrinol Metab 87:5138-5143 (Pubitemid 35316357)
55. Xu B, Yang R, Chang F, Chen L, Xie G, Sokabe M (2012) Neurosteroid PREGS protects neurite growth and survival of newborn neurons in the hippocampal dentate gyrus of APPswe/PS1dE9 mice. Curr Alzheimer Res 9:361-372
56. 7nAChR-mediated neuroprotection. Neuropharmacology 63:1042-1050
57. Yankner BA, Duffy LK, Kirschner DA (1990) Neurotrophic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides. Science 250:279-282
58. Zussy C, Brureau A, Delair B, Marchal S, Keller E, Ixart G, Naert G, Meunier J, Chevallier N, Maurice T, Givalois L (2011) Time-course and regional analyses of the physiopathological changes induced after cerebral injection of an amyloid-β fragment in rats. Am J Pathol 179:315-334
59. Zwain IH, Yen SS (1999) Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140:3843-3852 (Pubitemid 30645442)