Effects of short-term hormonal replacement on learning and on basal forebrain ChAT and TrkA content in ovariectomized rats

Brain Research

Volumn 1375, Issue , 2011, Pages 77-84

  Espinosa Raya, Judith ^a,b   Plata Cruz, Noemí ^a   Neri Gómez, Teresa ^a   Camacho Arroyo, Ignacio ^b   Picazo, Ofir ^a  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Alzheimer; Basal forebrain; ChAT; Estrogens; Learning; Neurodegeneration; Ovariectomy; Progesterone; TrkA

Indexed keywords

CHOLINE ACETYLTRANSFERASE; ESTRADIOL; PROGESTERONE; PROTEIN TYROSINE KINASE A;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CHOLINERGIC NERVE CELL; COGNITION; CONTROLLED STUDY; DRUG MEGADOSE; ESTROGEN THERAPY; FEMALE; FOREBRAIN; LEARNING; LOW DRUG DOSE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN CONTENT; RAT; SHORT COURSE THERAPY; TASK PERFORMANCE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CHOLINE O-ACETYLTRANSFERASE; ESTRADIOL; FEMALE; HORMONE REPLACEMENT THERAPY; LEARNING; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; OVARIECTOMY; PROGESTERONE; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKA;

RATTUS;

EID: 79651469383     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.12.044     Document Type: Article

References (77)

1. C.C. Aguirre, and M. Baudry Progesterone reverses 17beta-estradiol- mediated neuroprotection and BDNF induction in cultured hippocampal slices Eur. J. Neurosci. 29 2009 447 454
2. I. Azcoitia, A. Sierra, S. Veiga, S. Honda, N. Harada, and L.M. Garcia-Segura Brain aromatase is neuroprotective J. Neurobiol. 47 2001 318 329 (Pubitemid 32467339)
3. H.A. Barton, M.E. Andersen, and B.C. Allen Dose-response characteristics of uterine responses in rats exposed to estrogen agonists Regul. Toxicol. Pharmacol. 28 1998 133 149 (Pubitemid 29076779)
4. B. Berse, I. Lopez-Coviella, and J.K. Blusztajn Activation of TrkA by nerve growth factor upregulates expression of the cholinergic gene locus but attenuates the response to ciliary neurotrophic growth factor Biochem. J. 342 1999 301 308 (Pubitemid 29425350)
5. B.B. Braden, J.S. Talboom, I.D. Crain, A.R. Simard, R.J. Lukas, L. Prokai, M.R. Scheldrup, B.L. Bowman, and H.A. Bimonte-Nelson Medroxyprogesterone acetate impairs memory and alters the GABAergic system in aged surgically menopausal rats Neurobiol. Learn. Mem. 93 2010 444 453
6. W. Cai, Y. Zhu, K. Furuya, Z. Li, M. Sokabe, and L. Chen Two different molecular mechanisms underlying progesterone neuroprotection against ischemic brain damage Neuropharmacology 55 2008 127 138
7. J.C. Carroll, E.R. Rosario, and C.J. Pike Progesterone blocks estrogen neuroprotection from kainate in middle-aged female rats Neurosci. Lett. 445 2008 229 232
8. J.C. Carroll, E.R. Rosario, A. Villamagna, and C.J. Pike Continuous and cyclic progesterone differentially interact with estradiol in the regulation of Alzheimer-like pathology in female 3xTransgenic-Alzheimer's disease mice Endocrinology 151 2010 2713 2722
9. T.R. Chakraborty, and A.C. Gore Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function Exp. Biol. Med. 229 2004 977 987 (Pubitemid 39431077)
10. Z. Chen, M.S. Simmons, R.T. Perry, H.W. Wiener, L.E. Harrell, and R.C. Go Genetic association of neurotrophic tyrosine kinase receptor type 2 (NTRK2) with Alzheimer's disease Am. J. Med. Genet. B Neuropsychiatr. Genet. 147 2008 363 369 (Pubitemid 351536802)
11. J.M. Daniel, and G.P. Dohanich Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory J. Neurosci. 21 2001 6949 6956 (Pubitemid 32781137)
12. M.W. Decker, and J.L. McGaugh The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory Synapse 7 1991 151 168
13. P. Dudchenko, and M. Sarter GABAergic control of basal forebrain cholinergic neurons and memory Behav. Brain Res. 42 1991 33 41
14. J. Espinosa-Raya, M. Espinoza-Fonseca, O. Picazo, and J. Trujillo-Ferrara Effect of a M1 allosteric modulator on scopolamine-induced amnesia Med. Chem. 3 2007 7 11 (Pubitemid 46062336)
15. C.A. Frye, C.K. Duffy, and A.A. Walf Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task Neurobiol. Learn. Mem. 88 2007 208 216 (Pubitemid 47223753)
16. R. Gabor, R. Nagle, D.A. Johnson, and R.B. Gibbs Estrogen enhances potassium-stimulated acetylcholine release in the rat hipoccampus Brain Res. 962 2003 244 247 (Pubitemid 36126343)
17. A.R. Genazzani, N. Pluchino, S. Luisi, and M. Luisi Estrogen, cognition and female ageing Hum. Reprod. Update 13 2007 175 187 (Pubitemid 46323194)
18. R.B. Gibbs Fluctuations in relative levels of choline acetyltransferase mRNA in different regions of the rat basal forebrain across the estrous cycle: effects of estrogen and progesterone J. Neurosci. 16 1996 1049 1055 (Pubitemid 26140861)
19. R.B. Gibbs Levels of TrkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement Brain Res. 787 1998 259 268 (Pubitemid 28197913)
20. R.B. Gibbs Impairment of basal forebrain cholinergic neurons associated with aging and long-term loss of ovarian function Exp. Neurol. 15 1998 289 302 (Pubitemid 28285909)
21. R.B. Gibbs Treatment with estrogen and progesterone affects relative levels of brain-derived neurotrophic factor mRNA and protein in different regions of the adult rat brain Brain Res. 844 1999 20 27 (Pubitemid 29490948)
22. R.B. Gibbs Effects of gonadal hormone replacement on measures of basal forebrain cholinergic function Neuroscience 101 2000 931 938
23. R.B. Gibbs Basal forebrain cholinergic neurons are necessary for estrogen to enhance acquisition of a delayed matching-to-position T-maze task Horm. Behav. 42 2002 245 257 (Pubitemid 35435618)
24. R.B. Gibbs Effects of ageing and long-term hormone replacement on cholinergic neurons in the medial septum and nucleus basalis magnocellularis of ovariectomized rats J. Neuroendocrinol. 15 2003 477 485 (Pubitemid 36582463)
25. R.B. Gibbs Estrogen therapy and cognition: a review of the cholinergic hypothesis Endocr. Rev. 31 2010 224 253
26. R.B. Gibbs, and P. Aggarwal Estrogen and basal forebrain cholinergic neurons: implications for brain aging and Alzheimer's disease-related cognitive decline Horm. Behav. 34 1998 98 111 (Pubitemid 28541752)
27. R.B. Gibbs, A. Hashash, and D.A. Johnson Effects of estrogen on potassium-stimulated acetylcholine release in the hippocampus and overlying cortex of adult rats Brain Res. 749 1997 143 146 (Pubitemid 27096467)
28. R.B. Gibbs, D. Wu, L.B. Hersh, and D.W. Pfaff Effects of estrogen replacement on the relative levels of choline acetyltransferase, TrkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats Exp. Neurol. 129 2004 70 80
29. M.C. Gonzalez Deniselle, L. Garay, S. Gonzalez, F. Saravia, F. Labombarda, R. Guennoun, M. Schumacher, and A.F. De Nicola Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating Wobbler motoneurons Exp. Neurol. 203 2007 406 414 (Pubitemid 46164803)
30. L.K. Gorman, K. Pang, K.M. Frick, B. Givens, and D.S. Olton Acetylcholine release in the hippocampus: effects of cholinergic and GABAergic compounds in the medial septal area Neurosci. Lett. 166 1994 199 202 (Pubitemid 24053828)
31. L.L. Harburger, A.S. Pechenino, A. Saadi, and K.M. Frick Post-training progesterone dose-dependently enhances object, but not spatial, memory consolidation Behav. Brain Res. 194 2008 174 180
32. V.W. Henderson, A. Paganini-Hill, C.K. Emanuel, M.E. Dunn, and J.G. Buckwalter Estrogen replacement therapy in older women: comparisons between Alzheimer's disease cases and nondemented control subjects Arch. Neurol. 51 1994 896 900 (Pubitemid 24286044)
33. R. Ito, B.J. Everitt, and T.W. Robbins The hippocampus and appetitive Pavlovian conditioning: effects of excitotoxic hippocampal lesions on conditioned locomotor activity and autoshaping Hippocampus 15 2005 713 721 (Pubitemid 41300822)
34. I.M. Johansson, V. Birzniece, C. Lindblad, T. Olsson, and T. Backstrom Allopregnanolone inhibits learning in the Morris water maze Brain Res. 934 2002 125 131 (Pubitemid 34304315)
35. P. Kaur, P.K. Jodhka, W.A. Underwood, C.A. Bowles, N.C. de Fiebre, C.M. de Fiebre, and M. Singh Progesterone increases brain-derived neurotrophic factor expression and protects against glutamate toxicity in a mitogen-activated protein kinase- and phosphoinositide-3 kinase-dependent manner in cerebral cortical explants J. Neurosci. Res. 85 2007 2441 2449 (Pubitemid 47204758)
36. P. Lanlua, F. Decorti, P.R.R. Gangula, K. Chung, G. Taglialatela, and C. Yallampalli Female steroid hormones modulate receptors for nerve growth factor in rat dorsal root ganglia Biol. Reprod. 64 2001 331 338 (Pubitemid 32044643)
37. A.D. Lawrence, and B.J. Sahakian Alzheimer disease, attention, and the cholinergic system Alzheimer Dis. Assoc. Disord. 9 1995 43 49
38. V.N. Luine Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats Exp. Neurol. 89 1985 484 490 (Pubitemid 15040918)
39. V.N. Luine, and B.S. McEwen Sex differences in cholinergic enzymes of diagonal band nuclei in the rat preoptic area Neuroendocrinology 36 1983 475 482 (Pubitemid 13092159)
40. V.N. Luine, R.I. Khylchevskaya, and B.S. McEwen Effect of gonadal steroids on activities of monoamine oxidase and choline acetylase in rat brain Brain Res. 86 1975 293 306
41. V.N. Luine, K.J. Renner, S. Heady, and K.J. Jones Age and sex-dependent decreases in ChAT in basal forebrain nuclei Neurobiol. Aging 7 1986 193 198 (Pubitemid 16021590)
42. L. Manuel-Apolinar, and A. Meneses 8-OH-DPAT facilitated memory consolidation and increased hippocampal and cortical cAMP production Behav. Brain Res. 148 2004 179 184 (Pubitemid 37543666)
43. A.L. Markowska, and A.V. Savonenko Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats J. Neurosci. 22 2002 10985 10995 (Pubitemid 36005175)
44. P.J. McMillan, C.A. Singer, and D.M. Dorsa The effects of ovariectomy and estrogen replacement on trkA and choline acetyltransferase mRNA expression in the basal forebrain of the adult female Sprague-Dawley rat J. Neurosci. 16 1996 1860 1865 (Pubitemid 26145963)
45. MED-Associates WMPC software 1999 v. 1.15 [Computer software]. St Albans, VT.
46. A. Meneses 5-HT system and cognition Neurosci. Biobehav. Rev. 23 1999 1111 1125
47. A. Meneses A pharmacological analysis of an associative learning task: 5-HT (1) to 5-HT (7) receptor subtypes function on a pavlovian/instrumental autoshaped memory Learn. Mem. 10 2003 363 372 (Pubitemid 37266681)
48. A. Meneses, and E. Hong Role of 5-HT1B, 5-HT2A and 5-HT2C receptors in learning Behav. Brain Res. 87 1997 105 110 (Pubitemid 27421553)
49. A. Meneses, and J.A. Terrón Role of 5-HT (1A) and 5-HT (7) receptors in the facilitatory response induced by 8-OH-DPAT on learning consolidation Behav. Brain Res. 121 2001 21 28 (Pubitemid 32223462)
50. J.L. Muir, K.J. Page, D.J. Sirinathsinghji, T.W. Robbins, and B.J. Everitt Excitotoxic lesions of the basal forebrain cholinergic neurons: effects on learning, memory and attention Behav. Brain Res. 57 1993 123 131 (Pubitemid 24027142)
51. J. Nilsen, and R.D. Brinton Impact of progestins on estradiol potentiation of the glutamate calcium response NeuroReport 13 2002 825 830 (Pubitemid 34492909)
52. T. Ohkura, K. Isse, K. Akazawa, M. Hamamoto, Y. Yaoi, and N. Hagino Evaluation of estrogen treatment in female patients with dementia of the Alzheimer type Endocr. J. 41 1994 361 371 (Pubitemid 24297493)
53. T. Ohkura, K. Isse, K. Akazawa, M. Hamamoto, Y. Yaoi, and N. Hagino Long-term estrogen replacement therapy in female patients with dementia of the Alzheimer type: 7 case reports Dementia 6 1995 99 107
54. D.S. Olton, and G.L. Wenk Dementia: Animal models of the cognitive impairments produced by degeneration of the basal forebrain cholinergic system H.Y. Meltzer, Psychopharmacology: The Third Generation of Progress 1987 Raven Press New York 941 953
55. M.B. Parent, and M.G. Baxter Septohippocampal acetylcholine: involved in but not necessary for learning and memory? Learn. Mem. 11 2004 9 20 (Pubitemid 38167053)
56. G. Paxinos, and C. Watson The rat brain in stereotaxic coordinates 1986 Academic Press San Diego
57. O. Picazo, I. Azcoitia, and L.M. Garcia-Segura Neuroprotective and neurotoxic effects of estrogens Brain Res. 990 2003 20 27 (Pubitemid 37244057)
58. J.H. Pirch Basal forebrain and frontal cortex neuron responses during visual discrimination in the rat Brain Res. Bull. 3 1993 73 83 (Pubitemid 23102828)
59. S. Reilly, and R.P. Grutzmacher Autoshaping in the rat: conditioned licking response to a stimulus that signals sucrose reinforcement Behav Processes. 59 2002 15 24 (Pubitemid 34667314)
60. B.B. Sherwin Estrogen and cognitive functioning in women Endocr. Rev. 24 2003 133 151 (Pubitemid 36515282)
61. P.J. Shughrue, P.J. Scrimo, and I. Merchenthaler Estrogen binding and estrogen receptor characterization (ERalpha and ERbeta) in the cholinergic neurons of the rat basal forebrain Neuroscience 96 2000 41 49 (Pubitemid 30103601)
62. S.A. Shumaker, C. Legault, S.R. Rapp, L. Thal, R.B. Wallace, J.K. Ockene, S.L. Hendrix, B.N. Jones III, A.R. Assaf, R.D. Jackson, J.M. Kotchen, S. Wassertheil-Smoller, and J. Wactawski-Wende Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a Randomized Controlled Trial JAMA 289 2003 2651 2662 (Pubitemid 37430136)
63. M. Singh, E.M. Meyer, W.J. Millard, and J.W. Simpkins Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats Brain Res. 644 1994 305 312 (Pubitemid 24127987)
64. M. Singh, E.M. Meyer, and J.W. Simpkins The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats Endocrinology 136 1995 2320 2324
65. F. Sohrabji, R.C. Miranda, and C.D. Toran-Allerand Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons J. Neurosci. 14 1994 459 471 (Pubitemid 24043906)
66. T. Steckler, and A. Sahgal The role of serotonergic-cholinergic interactions in the mediation of cognitive behaviour Behav. Brain Res. 67 1995 165 199
67. T. Steckler, J.S. Andrews, P. Marten, and J.D. Turner Effects of NBA lesions with two neurotoxins on spatial memory and autoshaping Pharmacol. Biochem. Behav. 44 1993 877 889
68. T. Steckler, A.B. Keith, R.G. Wiley, and A. Sahgal Cholinergic lesions by 192 IgG-saporin and short-term recognition memory: role of the septohippocampal projection Neuroscience 66 1995 101 114
69. J.O. Strom, E. Theodorsson, and A. Theodorsson Order of magnitude differences between methods for maintaining physiological 17beta-oestradiol concentrations in ovariectomized rats Scand. J. Clin. Lab. Invest. 68 2008 814 822
70. J.S. Talboom, B.J. Williams, E.R. Baxley, S.G. West, and H.A. Bimonte-Nelson Higher levels of estradiol replacement correlate with better spatial memory in surgically menopausal young and middle-aged rats Neurobiol. Learn. Mem. 90 2008 155 163
71. C.D. Toran-Allerand, R.C. Miranda, W.D. Bentham, F. Sohrabji, T.J. Brown, R.B. Hochberg, and N.J. MacLusky Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain Proc. Natl Acad. Sci. USA 89 1992 4668 4672
72. S. Veiga, I. Azcoitia, and L.M. Garcia-Segura Extragonadal synthesis of estradiol is protective against kainic acid excitotoxic damage to the hippocampus NeuroReport 16 2005 1599 1603 (Pubitemid 41783131)
73. G.L. Wenk The nucleus basalis magnocellularis cholinergic system: one hundred years of progress Neurobiol. Learn. Mem. 67 1997 85 95 (Pubitemid 27424463)
74. F.A. Wilson, and E.T. Rolls Neuronal responses related to reinforcement in the primate basal forebrain Brain Res. 509 1990 213 232
75. P.J. Winsauer, F.H. Rodriguez, A.E. Cha, and J.M. Moerschbaecher Full and partial 5-HT1A receptor agonists disrupt learning and performance in rats J. Pharmacol. Exp. Ther. 288 1999 335 347 (Pubitemid 29113508)
76. C.S. Woolley, and B.S. McEwen Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism J. Neurosci. 14 1994 7680 7687
77. J. Wu, Y. Zhu, and J. Wu Effects of estrogen and estrogenic compounds on cognition in ovariectomized rats Climacteric 11 2008 212 220