Treatment with dehydroepiandrosterone increases peripheral benzodiazepine receptors of mitochondria from cerebral cortex in D-galactose-induced aged rats

Basic and Clinical Pharmacology and Toxicology

Volumn 103, Issue 6, 2008, Pages 493-501

  Chen, Chunfu ^a,b   Lang, Senyang ^b   Zuo, Pingping ^c   Yang, Nan ^c   Wang, Xiangqing ^b  

^a SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG UNIVERSITY   (China)

^b CHINESE PLA GENERAL HOSPITAL   (China)

^c PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BENZODIAZEPINE RECEPTOR; GALACTOSE; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; PRASTERONE;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN MITOCHONDRION; CONTROLLED STUDY; DRUG EFFECT; FEMALE; LEARNING; MALE; MAZE TEST; MEMORY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR DENSITY; SENESCENCE;

AGING; ANIMALS; CEREBRAL CORTEX; COGNITION; DEHYDROEPIANDROSTERONE; FEMALE; GALACTOSE; MALE; MAZE LEARNING; MEMORY; MITOCHONDRIA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A;

RATTUS;

EID: 56049106837     PISSN: 17427835     EISSN: 17427843     Source Type: Journal    
DOI: 10.1111/j.1742-7843.2008.00288.x     Document Type: Article

References (87)

1. Racchi M, Balduzzi C, Corsini E. Dehydroepiandrosterone (DHEA) and the aging brain: flipping a coin in the 'fountain of youth'. CNS Drug Rev 2003 9 : 21 40.
2. Majewska MD. Neurosteroids: endogenous bimodal modulators of the GABA, receptor: mechanisms of action and physiological significance. Prog Neurobiol 1992 38 : 379 95.
3. Bologa L, Sharma J, Roberts E. Dehydroepiandrosterone and its sulfated derivative reduce neuronal death and enhance astrocytic differentiation in brain cell cultures. J Neurosci Res 1987 17 : 225 34.
4. Mathis C, Meziane H, Ungerer A. Models for the study of memory and neurosteroids. J Soc Biol 1999 193 : 299 306.
5. Kaasik A, Safiulina D, Kalda A, Zharkovsky A. Dehydroepiandrosterone with other neurosteroids preserve neuronal mitochondria from calcium overload. J Steroid Biochem Mol Biol 2003 87 : 97 103.
6. Basile AS, Skolnick P. Subcellular localization of peripheraltype binding sites for benzodiazepines in rat brain. J Neurochem 1986 46 : 305 8.
7. Anholt RRH, Pedersen PL, De Souza EB, Snyder SH. The peripheral-type benzodiazepine receptor-localization to the mitochondrial outer membrane. J Biol Chem 1986 261 : 576 83.
8. Lang SY. The role of peripheral benzodiazepine receptors (PBRs) in CNS pathophysiology. Curr Med Chem 2002 9 : 1411 5.
9. Casellas P, Galiegue S, Basile AS. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem Int 2002 40 : 475 86.
10. Hirsch T, Decaudin D, Susin SA, Marchetti P, Larochette N, Resche-Rigon M et al. PK11195, a ligand of the mitochondrial benzodiazepine receptor, facilitates the induction of apoptosis and reverses the induction of apoptosis and reverses Bcl-2-mediated cytoprotection. Exp Cell Res 1998 241 : 426 34.
11. Carayon P, Portier M, Dussossoy D, Bord A, Petitprêtre G, Canat X et al. Involvement of peripheral benzodiazepine receptors in the protection of hematopoietic cells against oxygen radical damage. Blood 1996 87 : 3170 8.
12. Bono F, Lamarche I, Prabonnaud V, Le Fur G, Herbert JM. Peripheral benzodiazepine receptor agonists exhibit potent antiapoptotic activities. Biochem Biophys Res Communun 1999 265 : 457 61.
13. Shang YZ, Gong MY, Zhou XX, Li ST, Wang BY. Improving effects of SSF on memory deficits and pathological changes of neural and immunological systems in senescent mice. Acta Pharmacol Sin 2001 22 : 1078 83.
14. Shen YX, Xu SY, Wei W, Sun XX, Yang J, Liu LH et al. Melatonin reduces memory changes and neural oxidative damage in mice treated with D-galactose. J Pineal Res 2002 32 : 173 8.
15. Xu XH, Zhang ZG. Effect of puerarin on learning-memory behavior and synaptic structure of hippocampus in the aging mice induced by D-galactose. Acta Pharmacol Sin 2002 37 : 1 4.
16. Ho SC, Liu JH, Wu RY. Establishment of the mimetic aging effect in mice caused by D-galactose. Biogerontology 2003 4 : 15 8.
17. Cui X, Wang LN, Zuo PP, Han ZT, Fang ZY, Li WB et al. D-galactose-caused life shortening in Drosophila melanogaster and Musca domestica is associated with oxidative stress. Biogerontology 2004 5 : 317 25.
18. Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants and the degenerative disease of aging. Proc Natl Acad Sci USA 1993 90 : 7915 22.
19. Nakamura H, Nakamura K, Yodoi J. Redox regulation of cellular activation. Annu Rev Immunol 1997 15 : 351 69.
20. Baulieu EE. Neurosteroids: a novel function of the brain. Psychoneuroendocrinology 1998 23 : 963 87.
21. Mao X, Barger SW. Neuroprotection by dehydroepiandrosterone-sulfate: role of an NF-kappaB-like factor. Neuroreport 1998 9 : 759 63.
22. Morris R. Developments of a water maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984 11 : 47 64.
23. Quattrone A, Pascale A, Nogues X, Zhao W, Gusev P, Pacini A et al. Posttranscriptional regulation of gene expression in learning by the neuronal ELAV-like mRNA-stabilizing proteins. Proc Natl Acad Sci USA 2001 98 : 11668 73.
24. Rogers DC, Hagan JJ. 5-HT6 receptor antagonists enhance retention of a water maze task in the rat. Psychopharmacology 2001 158 : 114 9.
25. Gray EG, Whittaker VP. The isolation of nerve endings from brain: an electron-microscopic study of cell fragments derived by homogenization and centrifugation. J Anat 1962 96 : 79 88.
26. Benavides J, Capdeville C, Dauphin F, Dubois A, Duverger D, Fage D et al. The quantification of brain lesions with an omega 3 site ligand: a critical analysis of animal models of cerebral ischaemia and neurodegeneration. Brain Res 1990 522 : 275 89.
27. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye binding. Anal Biochem 1976 72 : 248 54.
28. Warfield AS, Segal S. Myoinositol and phosphatidylinositol metabolism in synaptosomes from galactose-fed rats. Proc Natl Acad Sci USA 1978 75 : 4568 72.
29. Lei H, Wang B, Li WP, Yang Y, Zhou AW, Chen MZ. Anti-aging effect of astragalosides and its mechanism of action. Acta Pharmacol Sin 2003 24 : 230 34.
30. 2+-ATPase activity. Biochim Biophys Acta 1999 1437 : 257 64.
31. Diamond DM, Branch BJ, Fleshner M. The neurosteroid dehydroepiandrosterone sulfate (DHEAS) enhances hippocampal primed burst, but not long-term, potentiation. Neurosci Lett 1996 202 : 204 8.
32. Gavish M, Bachman I, Shoukrun R, Katz Y, Veenman L, Weisinger G et al. Enigma of the peripheral benzodiazepine receptor. Pharmacol Rev 1999 51 : 629 50.
33. Reddy DS, Kulkarni SK. Proconvulsant effects of neurosteroids pregnenolone sulfate and dehydroepiandrosterone sulfate in mice. Eur J Pharmacol 1998 345 : 55 9.
34. Komiskey HL, MacFarlan MF. Aging: effect on neuronal and non-neuronal benzodiazepine binding sites. Neurochcem Res 1983 8 : 1135 41.
35. Anholt RRH, De Souza EB, Oster-Granite MI, Snyder SH. The peripheral-type benzodiazepine receptor: autoradiographic localization in whole-body sections of neonatal rats. J Pharmacol Exp Ther 1985 233 : 517 26.
36. Fares F, Weizman A, Zlotogorski D, Gavish M. Ontogenetic development of peripheral benzodiazepine binding sites in rat brain, heart and lung. Brain Res 1987 408 : 381 4.
37. Daval JL, Deckert J, Nakajima T, Morgan PF, Marangos PJ. Regional ontogenetic profile of central and peripheral benzodiazepine receptors in the guinea pig brain. Neurosci Lett 1988 92 : 82 5.
38. Itzhak Y, Roig-Cantisano A, Norenberg MD. Ontogeny of peripheral-type benzodiazepine receptors in cultured astrocytes and brain from rat. Brain Res Dev Brain Res 1995 84 : 62 6.
39. Dalezios Y, Matsokis N. Brain benzodiazepine binding in aged rats. Neurochem Int 1998 32 : 213 7.
40. Xu XH, Zhao TQ. Effects of puerarin on D-galactose-induced memory deficits in mice. Acta Pharmacol Sin 2002 23 : 587 90.
41. Liu JH, Ho SC, Lai TH, Liu TH, Chi PY, Wu RY. Protective effects of Chinese herbs on D-galactose-induced oxidative damage. Clin Pharmacol 2003 25 : 447 52.
42. Wright G, Reichenbecher V. The effects of superoxide and the peripheral benzodiazepine receptor ligands on the mitochondrial processing of manganese-dependent superoxide dismutase. Exp Cell Res 1999 246 : 443 50.
43. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000 408 : 239 47.
44. Lehmann J, Weizman R, Pryce CR, Leschiner S, Allmann I, Feldon J et al. Peripheral benzodiazepine receptors in cerebral cortex, but not in internal organs, are increased following inescapable stress and subsequent avoidance/escape shuttle-box testing. Brain Res 1999 851 : 141 7.
45. Rago L, Kiivet RA, Harro G, Pold M. Central- and peripheral-type benzodiazepine receptors: similar regulation by stress and GABA receptor agonists. Pharmacol Biochem Behav 1989b 32 : 879 83.
46. Mennini T, Gobbi M, Caharuchinda C. Noise-induced opposite changes in central and peripheral benzodiazepine receptors in rat brain cortex. Neurosci Res Commun 1989 5 : 27 34.
47. Drugan RC, Basile AS, Crawley JN, Paul SM, Skolnick P. Inescapable shock reduces (3H)Ro 5-4864 binding to 'peripheral-type' benzodiazepine receptors in the rat. Pharmacol Biochem Behav 1986 24 : 1673 7.
48. Burgin R, Weizman R, Gavish M. Repeated swim stress and peripheral-type benzodiazepine receptors. Neuropsychobiology 1996 33 : 28 31.
49. Gavish M, Katz Y, Bar-Ami S, Weizman R. Biochemical, physiological, and pathological aspects of the peripheral benzodiazepine receptor. J Neurochem 1992 58 : 1589 601.
50. Soreni N, Apter A, Weizman A, Don-Tufeled O, Leschiner S, Karp L et al. Decreased platelet peripheral-type benzodiazepine receptors in adolescent inpatients with repeated suicide attempts. Biol Psychiatry 1999 46 : 484 8.
51. Nakamura K, Fukunishi I, Nakamoto Y, Iwahashi K, Yoshii M. Peripheral-type benzodiazepine receptors on platelets are correlated with the degrees of anxiety in normal human subjects. Psychopharmacology 2002 162 : 301 3.
52. Drugan RC, Holmes PV, Stringer AP. Sexual dimorphism of stress-induced changes in renal peripheral benzodiazepine receptor in rat. Neuropharmacology 1991 30 : 413 6.
53. Weizman R, Laor N, Karp L, Dagan E, Reiss A, Dar DE et al. Alteration of platelet benzodiazepine receptors by stress of war. Am J Psychiatry 1994 151 : 766 7.
54. Hirsch JD, Beyer CF, Malkowitz L, Beer B, Blume AJ. Mitochondrial benzodiazepine receptors mediate inhibition of mitochondrial respiratory control. Mol Pharmacol 1989 35 : 157 63.
55. Papadopoulos V, Amri H, Boujrad N, Cascio C, Culty M, Garnier M et al. Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids 1997 62 : 21 8.
56. Holmes PV, Drugan RC. Differential effects of anxiogenic central and peripheral benzodiazepine receptor ligands in tests of learning and memory. Psychopharmacology (Berl) 1991 104 : 249 54.
57. Corpechot C, Robel P, Axelson M, Sjovall J, Baulieu EE. Characterization and measurement of dehydroepiandrosterone sulfate in rat brain. Proc Natl Acad Sci USA 1981 78 : 4704 7.
58. Johnson DA, Rhodes ME, Boni RL, Li PK. Chronic steroid sulfatase inhibition by (p-O-sulfamoyl)-N-tetradecanoyl tyramine increases dehydroepiandrosterone sulfate in whole brain. Life Sci 1997 61 : 355 9.
59. Liere P, Pianos A, Eychenne B, Cambourg A, Liu S, Griffiths W et al. Novel lipoidal derivatives of pregnenolone and dehydroepiandrosterone and absence of their sulfated counterparts in rodent brain. J Lipid Res 2004 45 : 2287 302.
60. Papadopoulos V. Structure and function of the peripheral-type benzodiazepine receptor in steroidogenic cells. Proc Soc Exp Biol Med 1998 217 : 130 42.
61. Majewska MD, Demigoren S, Spivak CE, London ED. The neurosteroid dehydroepiandrosterone sulfate is an allosteric antagonist of the GABAA receptor. Brain Res 1990 526 : 143 6.
62. 2+ channel current in freshly isolated hippocampal CA1 neurons. Eur J Pharmacol 1991 202 : 269 72.
63. Flood JF, Morley JE, Roberts E. Memory-enhancing effects in male mice of pregnenolone and steroids metabolically derived from it. Proc Natl Acad Sci USA 1992 89 : 1567 71.
64. Ebeling P, Koivisto VA. Physiological importance of dehydroepiandrosterone. Lancet 1994 343 : 1479 81.
65. Flood JF, Farr SA, Johnson DA, Li PK, Morley JE. Peripheral steroid sulfatase inhibition potentiates improvement of memory retention for hippocampally administered dehydroepiandrosterone sulfate but not pregnenolone sulfate. Psychoneuroendocrinology 1999 24 : 799 811.
66. Roberts E, Bologa L, Flood JF, Smith GE. Effects of dehydroepiandrosterone and its sulfate on brain tissue in culture and on memory in mice. Brain Res 1987 406 : 357 62.
67. Yoo A, Harris J, Dubrovsky B. Dose-response study of dehydroepiandrosterone sulfate on dentate gyrus long-term potentiation. Exp Neurol 1996 137 : 151 6.
68. Aragno M, Parola S, Tamagno E, Brignardello E, Manti R, Danni O et al. Oxidative derangement in rat synaptosomes induced by hyperglycaemia: restorative effect of dehydroepiandrosterone treatment. Biochem Pharmacol 2000 60 : 389 95.
69. Bastianetto S, Ramassamy C, Poirier J, Quirion R. Dehydroepiandrosterone (DHEA) protects hippocampal cells from oxidative stress-induced damage. Brain Res Mol Brain Res 1999 66 : 35 41.
70. Morin C, Zini R, Simon N, Tillement JP. Dehydroepiandrosterone and alpha-estradiol limit the functional alterations of rat brain mitochondria submitted to different experimental stresses. Neuroscience 2002 115 : 415 24.
71. Waters SL, Miller GW, Aleo MD, Schnellmann RG. Neurosteroid inhibition of cell death. Am J Physiol 1997 273 : F869 76.
72. Zhu WJ, Vicini S. Neurosteroid prolongs GABAA channel deactivation by altering kinetics of desensitized states. J Neurosci 1997 17 : 4022 31.
73. Gavish M, Okun F, Weizman A, Youdim MB. Modulation of peripheral benzodiazepine binding sites following chronic estradiol treatment. Eur J Pharmacol 1986 127 : 147 51.
74. Bender AS, Norenberg MD. Effect of benzodiazepines and neurosteroids on ammonia-induced swelling in cultured astrocytes. J Neurosci Res 1998 54 : 673 80.
75. Asaba H, Hosoya K, Takanaga H, Ohtsuki S, Tamura E, Takizawa T et al. Blood-brain barrier is involved in the efflux transport of a neuroactive steroid, dehydroepiandrosterone sulfate, via organic anion transporting polypeptide 2. J Neurochem 2000 75 : 1907 16.
76. Guazzo EP, Kirkpatrick PJ, Goodyer IM, Shiers HM, Herbert J. Cortisol, dehydroepiandrosterone (DHEA), and DHEA sulfate in the cerebrospinal fluid of man: relation to blood levels and the effects of age. J Clin Endocrinol Metab 1996 81 : 3951 60.
77. Lhullier FL, Riera NG, Nicolaidis R, Junqueira D, Dahm KC, Cipriani F et al. Effect of DHEA glutamate release from synaptosomes of rats at different ages. Neurochem Res 2004 29 : 335 9.
78. Robel P, Young J, Corpechot C, Mayo W, Perché F, Haug M et al. Biosynthesis and assay of neurosteroids in rats and mice: functional correlates. J Steroid Biochem Mol Biol 1995 53 : 355 60.
79. Kimonides VG, Khatibi NH, Svendsen CN, Sofroniew MV, Herbert J. Dehydroepiandrosterone (DHEA) and DHEA-sulfate (DHEAS) protect hippocampal neurons against excitatory amino acid-induced neurotoxicity. Neurobiology 1998 95 : 1852 7.
80. Steel N. Dehydro-epiandrosterone and ageing. Age Ageing 1999 28 : 89 91.
81. Flood JF, Smith GE, Roberts E. Dehydroepiandrosterone and its sulfate enhance memory retention in mice. Brain Res 1988 447 : 269 78.
82. de la Torre JC, Nelson N, Sutherland RJ, Pappas BA. Reversal of ischemic-induced chronic memory dysfunction in aging rats with a free radical scavenger-glycolytic intermediate combination. Brain Res 1998 779 : 285 8.
83. Cheney JA, Weisser JD, Bareyre FM, Laurer HL, Saatman KE, Raghupathi R et al. The maxi-K channel opener BMS-204352 attenuates regional cerebral edema and neurologic motor impairment after experimental brain injury. J Cereb Blood Flow Metab 2001 21 : 396 403.
84. Maurice T, Su TP, Privat A. Sigma1 (sigma-1) receptor agonists and neurosteroids attenuate B25-35-amyloid peptide-induced amnesia in mice through a common mechanism. Neuroscience 1998 83 : 413 28.
85. Hoffman SW, Virmani S, Simkins RM, Stein DG. The delayed administration of dehydroepiandrosterone sulfate improves recovery of function after traumatic brain injury in rats. J Neurotrauma 2003 20 : 859 70.
86. Mo Q, Lu SF, Hu S, Simon NG. DHEA and DHEA sulfate differentially regulate neural androgen receptor and its transcriptional activity. Brain Res Mol Brain Res 2004 126 : 165 72.
87. Charalampopoulos I, Tsatsanis C, Dermitzaki E, Alexaki VI, Castanas E, Margioris AN et al. Dehydroepiandrosterone and allopregnanolone protect sympathoadrenal medulla cells against apoptosis via antiapoptotic Bcl-2 proteins. Proc Natl Acad Sci USA 2004 101 : 8209 14.