2012, Number 6
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Salud Mental 2012; 35 (6)
Regulación de la neurogénesis hipocámpica por los estrógenos: su relación con la depresión
Vega-Rivera NM, Fernández-Guasti JA, Ramírez-Rodríguez GB, Castro-García M, Estrada-Camarena E
Language: Spanish
References: 184
Page: 527-533
PDF size: 131.43 Kb.
ABSTRACT
Estrogens produce a wide range of biological effects throughout the
body, including the Central Nervous System (CNS). In the brain, besides
acting as neuroprotective agents, estrogens play an important
role in many neuronal processes and certain psychiatric disorders
such as depression.
The precise mechanism by which estrogens induce their positive
effects on depressive disorders has not been elucidated; however,
it is known that estrogens act on the CNS through the activation of
specific receptors. These actions occur in genomic and non-genomics
mechanisms through the modulation of synthesis and metabolism of
neurotransmitters, neuropeptides, neurosteroids and influencing the
morphological features of neurons and synaptic function. In addition,
it is known that estrogens can act as modulators of processes related
to neuroplasticity and neurogenesis.
Adult hippocampal neurogenesis is a neuroplastic process that
is affected by antidepressant drugs. These drugs increase the number
of new neurons following a temporal course that correlates within
the time in which antidepressants cause a behavioral improvement in
rodents and in humans. Interestingly, whereas the behavioral antidepressant
effects require 2-4 weeks to appear, after treatment initiation,
estrogen reduce the depressive-like behavior and induce cell proliferation
in terms of days. Thus, antidepressant drugs and the estrogens
replacement during the adulthood could influence in a similar manner
the new neuron formation.
Furthermore, recent works have indicated that the combination
of antidepressants plus estrogens could exert beneficial actions at lower
doses of estrogens (physiological range). This evidence is important
due to the combination of non-effective doses of antidepressants plus
estrogens could decrease the side-effects of both compounds, and facilitate
the behavioral action of antidepressant drugs shortening the
latency to onset their action.
The present review discusses recent information about the implication
of estrogens in depression, and on their effects as positive
regulators of new neuron formation in the adult hippocampus. In addition,
we will review the possible implication of last effect of estrogens
on their antidepressant effects.
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Sloan DM, Kornstein SG. Gender differences in depression and response to antidepressant treatment. Psychiatr Clin North Am 2003;26:581-594.
Marcus SM, Depression during pregnancy: rates, risks and consequences- Motherisk Update 2008. Can J Clin Pharmacol 2009;16:e15-22.
Kuiper GG, Shughrue PJ, Merchenthaler I, Gustafsson JA. The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol 1998;19:253-286.
Mehra RD, Sharma K, Nyakas C, Vij U. Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study. Brain Res 2005;1056:22-35.
Caraveo-Arduaga J, Colmenares E, Saldívar G. Estudio clínico-epidemiológico de los trastornos depresivos. Salud Mental 1999;22:7-17.
OMS. Cincuenta y cinco Asamblea Mundial de la Salud. Salud Mental: respeta al llamamiento a favor de la acción 2002. OMS. Programa Mundial de Acción en Salud Mental mhGAP.
Bello M, Puentes-Rosas E, Medina-Mora ME, Lozano R. [Prevalence and diagnosis of depression in Mexico]. Salud Publica Mex 2005;47(Supl 1):S4-11.
Halbreich U, Kahn LS. Role of estrogen in the aetiology and treatment of mood disorders. CNS Drugs 2001;15:797-817.
Hendrick V, Altshuler LL, Suri R. Hormonal changes in the postpartum and implications for postpartum depression. Psychosomatics 1998;39:93-101.
Woods NF, Smith-Dijulio K, Percival DB, Tao EY et al. Depressed mood during the menopausal transition and early postmenopause: observation from the Seattle Midlife Women´s Health Study. Menopause 2008;15:223-232.
Halbreich U, Endicott J, Goldstein S, Nee J. Premenstrual changes and changes in gonadal hormones. Acta Psychiatr Scand 1986;74:576-586.
Teixeira C, Figueiredo B, Conde A, Pacheco A et al. Anxiety and depression during pregnancy in women and men. J Affective Disorders 2009;119:142-148.
Ahokas A, Kaukoranta J, Wahlbeck K, Aito M. Estrogen deficiency in severe postpartum depression: successful treatment with sublingual physiologic 17beta-estradiol: a preliminary study. J Clin Psychiatry 2001;62:332-336.
Frye CA, Walf AA. Changes in progesterone metabolites in the hippocampus can modulate open field and forced swim test behavior of proestrous rats. Horm Behav 2002;41:306-315.
Frye CA, Wawrzycki J. Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats. Horm Behav 2003;44:319-326.
Galea LA, Wide JK, Barr AM. Estradiol alleviates depressive-like symptoms in a novel animal model of post-partum depression. Behav Brain Res 2001;122:1-9.
Estrada-Camarena E, López-Rubalcava C, Hernández-Aragón A, Mejía- Mauries S et al. Long-term ovariectomy modulates the antidepressant- like action of estrogens, but not of antidepressants. J Psychopharmacol 2011;25(10):1365-1377.
Lagunas N, Calmarza-Font I, Diz-Chaves Y, García-Segura LM. Longterm ovariectomy enhances anxiety and depressive-like behaviors in mice submitted to chronic unpredictable strees. Home Behav 2010;58(5):786-791.
Bernardi F, Cairoli S, D’Aurizio C, De Rosa A et al. [Double-blind comparative study of alprazolam (Xanax) and amitriptyline in the treatment of anxiety associated with depression]. Minerva Psichiatr 1988;29:203-210.
Romano-Torres M, Fernandez-Guasti A. Estradiol valerate elicits antidepressant- like effects in middle-aged female rats under chronic mild stress. Behav Pharmacol 2010;21:104-111.
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Nilssen O. [Dynamic mutations in hereditary neurodegenerative disorders]. Tidsskr Nor Laegeforen 1999;119:3021-3027.
Brake WG, Alves SE, Dunlop JC, Lee SJ et al. Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 2001;142:1284-1289.
McEwen B, Akama K, Alves S, Brake WG et al. Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc Natl Acad Sci USA 2001;98:7093-7100.
Lee SJ, Campomanes CR, Sikat PT, Greenfield AT et al. Estrogen induces phosphorylation of cyclic AMP response element binding (pCREB) in primary hippocampal cells in a time-dependent manner. Neuroscience 2004;124:549-560.
Osterlund M, Kuiper GG, Gustafsson JA, Hurd YL. Differential distribution and regulation of estrogen receptor-alpha and -beta mRNA within the female rat brain. Brain Res Mol Brain Res 1998;54:175-180.
Kuiper GG, Shughrue PJ, Merchenthaler I, Gustafsson JA. The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol 1998;19:253-286.
Osterlund MK, Hurd YL. Estrogen receptors in the human forebra in and the relation to neuropsychiatric disorders. Prog Neurobiol 2001;64:251-267.
Shughrue PJ, Lane MV, Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 1997;388:507-525.
Mehra RD, Sharma K, Nyakas C, Vij U. Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study. Brain Res 2005;1056:22-35.
Weiland NG, Orikasa C, Hayashi S, McEwen BS. Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J Comp Neurol 1997;388:603-612.
Milner TA, Ayoola K, Drake CT, Herrick SP et al. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 2005;491:81-95.
Herrick SP, Waters EM, Drake CT, McEwen BS et al. Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus. Brain Res 2006;1121:46-58.
Osterlund MK, Grandien K, Keller E, Hurd YL. The human brain has distinct regional expression patterns of estrogen receptor alpha mRNA isoforms derived from alternative promoters. J Neurochem 2000;75:1390-1397.
Cameron HA, Tanapat P, Gould E. Adrenal steroids and N-methyl- D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 1998;82:349-354.
Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004;27:447-452.
Tanapat P, Hastings NB, Reeves AJ, Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 1999;19:5792-5801.
Ormerod BK, Galea LA. Reproductive status influences the survival of new cells in the dentate gyrus of adult male meadow voles. Neurosci Lett 2003;346:25-28.
Barker JM, Galea LA. Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 2008;152:888-902.
Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965;124:319-335.
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Galea LA, Spritzer MD, Barker JM, Pawluski JL. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 2006;16:225-232.
Wise PM, Dubal DB, Wilson ME, Rau SW et al. Estradiol is a protective factor in the adult and aging brain: understanding of mechanisms derived from in vivo and in vitro studies. Brain Res Brain Res Rev 2001;37:313-319.
Tanapat P, Hastings NB, Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J Comp Neurol 2005;481:252-265.
Ormerod BK, Galea LA. Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: a possible regulatory role for estradiol. Neuroscience 2001;102:369-379.
Galea LA, McEwen BS. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 1999;89:955-964.
Perez-Martin M, Azcoitia I, Trejo JL, Sierra A et al. An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin- like growth factor-I in the dentate gyrus of adult female rat. Eur J Neurosci 2003;18:923-930.
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Estrada-Camarena E, Vega-Rivera NM, Berlanga C, Fernandez-Guasti A. Reduction in the latency of action of antidepressants by 17 betaestradiol in the forced swimming test. Psychopharmacology (Berl) 2008;201:351-360.
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Gutierrez-Lobos K, Scherer M, Anderer P, Katschnig H. The influence of age on the female/male ratio of treated incidence ratesin depression. BMC Psychiatry 2002;2:3.
Sloan DM, Kornstein SG. Gender differences in depression and response to antidepressant treatment. Psychiatr Clin North Am 2003;26:581-594.
Marcus SM, Depression during pregnancy: rates, risks and consequences-Motherisk Update 2008. Can J Clin Pharmacol 2009;16:e15-22.
Kuiper GG, Shughrue PJ, Merchenthaler I, Gustafsson JA. The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol 1998;19:253-286.
Mehra RD, Sharma K, Nyakas C, Vij U. Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study. Brain Res 2005;1056:22-35.
Caraveo-Arduaga J, Colmenares E, Saldívar G. Estudio clínico-epidemiológico de los trastornos depresivos. Salud Mental 1999;22:7-17.
OMS. Cincuenta y cinco Asamblea Mundial de la Salud. Salud Mental: respeta al llamamiento a favor de la acción 2002. OMS. Programa Mundial de Acción en Salud Mental mhGAP.
Bello M, Puentes-Rosas E, Medina-Mora ME, Lozano R. [Prevalence and diagnosis of depression in Mexico]. Salud Publica Mex 2005;47(Supl 1):S4-11.
Halbreich U, Kahn LS. Role of estrogen in the aetiology and treatment of mood disorders. CNS Drugs 2001;15:797-817.
Hendrick V, Altshuler LL, Suri R. Hormonal changes in the postpartum and implications for postpartum depression. Psychosomatics 1998;39:93-101.
Woods NF, Smith-Dijulio K, Percival DB, Tao EY et al. Depressed mood during the menopausal transition and early postmenopause: observation from the Seattle Midlife Women´s Health Study. Menopause 2008;15:223-232.
Halbreich U, Endicott J, Goldstein S, Nee J. Premenstrual changes and changes in gonadal hormones. Acta Psychiatr Scand 1986;74:576-586.
Teixeira C, Figueiredo B, Conde A, Pacheco A et al. Anxiety and depression during pregnancy in women and men. J Affective Disorders 2009;119:142-148.
Ahokas A, Kaukoranta J, Wahlbeck K, Aito M. Estrogen deficiency in severe postpartum depression: successful treatment with sublingual physiologic 17beta-estradiol: a preliminary study. J Clin Psychiatry 2001;62:332-336.
Frye CA, Walf AA. Changes in progesterone metabolites in the hippocampus can modulate open field and forced swim test behavior of proestrous rats. Horm Behav 2002;41:306-315.
Frye CA, Wawrzycki J. Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats. Horm Behav 2003;44:319-326.
Galea LA, Wide JK, Barr AM. Estradiol alleviates depressive-like symptoms in a novel animal model of post-partum depression. Behav Brain Res 2001;122:1-9.
Estrada-Camarena E, López-Rubalcava C, Hernández-Aragón A, Mejía- Mauries S et al. Long-term ovariectomy modulates the antidepressant- like action of estrogens, but not of antidepressants. J Psychopharmacol 2011;25(10):1365-1377.
Lagunas N, Calmarza-Font I, Diz-Chaves Y, García-Segura LM. Longterm ovariectomy enhances anxiety and depressive-like behaviors in mice submitted to chronic unpredictable strees. Home Behav 2010;58(5):786-791.
Bernardi F, Cairoli S, D’Aurizio C, De Rosa A et al. [Double-blind comparative study of alprazolam (Xanax) and amitriptyline in the treatment of anxiety associated with depression]. Minerva Psichiatr 1988;29:203-210.
Romano-Torres M, Fernandez-Guasti A. Estradiol valerate elicits antidepressant- like effects in middle-aged female rats under chronic mild stress. Behav Pharmacol 2010;21:104-111.
Rachman IM, Unnerstall JR, Pfaff DW, Cohen RS. Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test. Proc Natl Acad Sci USA 1998;95:13941-13946.
Estrada-Camarena E, Fernandez-Guasti A, Lopez-Rubalcava C. Antidepressant- like effect of different estrogenic compounds in the forced swimming test. Neuropsychopharmacology 2003;28:830-838.
Consiglio AR, Ramos ALLP, Henriques JAP, Picada JN. DNA brain damage after stress in rats. Progress in Neuro-Psychopharmacology Biological Psychiatry 2010;34:652-656.
Estrada-Camarena E, López-Rubalcava C, Hernandez-Aragon, Picazo O. Long-term modulates the antidepressant-like action of estrogens, but not of antidepressant. J Pharmacology 2011:1-13.
Williams CL, Stancel GMG. Estrógenos y progestágenos. En: Goodman, Gilman (eds.). Las bases farmacológicas de la terapéutica. México: McGraw-Hill Interamericana; 1996; pp. 1497-1529.
Alonso-Solis R, Abreu P, Lopez-Coviella I, Hernandez G et al. Gonadal steroid modulation of neuroendocrine transduction: a transynaptic view. Cell Mol Neurobiol 1996;16:357-382.
Nilssen O. [Dynamic mutations in hereditary neurodegenerative disorders]. Tidsskr Nor Laegeforen 1999;119:3021-3027.
Brake WG, Alves SE, Dunlop JC, Lee SJ et al. Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 2001;142:1284-1289.
McEwen B, Akama K, Alves S, Brake WG et al. Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc Natl Acad Sci USA 2001;98:7093-7100.
Lee SJ, Campomanes CR, Sikat PT, Greenfield AT et al. Estrogen induces phosphorylation of cyclic AMP response element binding (pCREB) in primary hippocampal cells in a time-dependent manner. Neuroscience 2004;124:549-560.
Osterlund M, Kuiper GG, Gustafsson JA, Hurd YL. Differential distribution and regulation of estrogen receptor-alpha and -beta mRNA within the female rat brain. Brain Res Mol Brain Res 1998;54:175-180.
Kuiper GG, Shughrue PJ, Merchenthaler I, Gustafsson JA. The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol 1998;19:253-286.
Osterlund MK, Hurd YL. Estrogen receptors in the human forebra in and the relation to neuropsychiatric disorders. Prog Neurobiol 2001;64:251-267.
Shughrue PJ, Lane MV, Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 1997;388:507-525.
Mehra RD, Sharma K, Nyakas C, Vij U. Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study. Brain Res 2005;1056:22-35.
Weiland NG, Orikasa C, Hayashi S, McEwen BS. Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J Comp Neurol 1997;388:603-612.
Milner TA, Ayoola K, Drake CT, Herrick SP et al. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 2005;491:81-95.
Herrick SP, Waters EM, Drake CT, McEwen BS et al. Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus. Brain Res 2006;1121:46-58.
Osterlund MK, Grandien K, Keller E, Hurd YL. The human brain has distinct regional expression patterns of estrogen receptor alpha mRNA isoforms derived from alternative promoters. J Neurochem 2000;75:1390-1397.
Cameron HA, Tanapat P, Gould E. Adrenal steroids and N-methyl- D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 1998;82:349-354.
Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004;27:447-452.
Tanapat P, Hastings NB, Reeves AJ, Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 1999;19:5792-5801.
Ormerod BK, Galea LA. Reproductive status influences the survival of new cells in the dentate gyrus of adult male meadow voles. Neurosci Lett 2003;346:25-28.
Barker JM, Galea LA. Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 2008;152:888-902.
Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965;124:319-335.
Zhao Z, Sun P, Chauhan N, Kaur J et al. Neuroprotection and neurogenesis: modulation of cornus ammonis 1 neuronal survival after transient forebrain ischemia by prior fimbria-fornix deafferentation. Neuroscience 2006;140:219-226.
Galea LA. Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Rev 2008;57:332-341.
Galea LA, Spritzer MD, Barker JM, Pawluski JL. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 2006;16:225-232.
Wise PM, Dubal DB, Wilson ME, Rau SW et al. Estradiol is a protective factor in the adult and aging brain: understanding of mechanisms derived from in vivo and in vitro studies. Brain Res Brain Res Rev 2001;37:313-319.
Tanapat P, Hastings NB, Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J Comp Neurol 2005;481:252-265.
Ormerod BK, Galea LA. Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: a possible regulatory role for estradiol. Neuroscience 2001;102:369-379.
Galea LA, McEwen BS. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 1999;89:955-964.
Perez-Martin M, Azcoitia I, Trejo JL, Sierra A et al. An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin- like growth factor-I in the dentate gyrus of adult female rat. Eur J Neurosci 2003;18:923-930.
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