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CNS & Neurological Disorders - Drug Targets


ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Research Article

The Role of Annexin A1 and Formyl Peptide Receptor 2/3 Signaling in Chronic Corticosterone-Induced Depression-Like behaviors and Impairment in Hippocampal-Dependent Memory

Author(s): Alessio Filippo Peritore, Rosalia Crupi, Maria Scuto, Enrico Gugliandolo, Rosalba Siracusa, Daniela Impellizzeri, Marika Cordaro, Ramona D’amico, Roberta Fusco, Rosanna Di Paola and Salvatore Cuzzocrea*

Volume 19, Issue 1, 2020

Page: [27 - 43] Pages: 17

DOI: 10.2174/1871527319666200107094732

Price: $65


Background: The activity of the Hypothalamic-Pituitary-Adrenal (HPA) axis is commonly dysregulated in stress-related psychiatric disorders. Annexin A1 (ANXA1), an endogenous ligand of Formyl Peptide Receptor (FPR) 2/3, is a member of the family of phospholipid- and calcium-binding proteins with a well-defined role in the delayed early inhibitory feedback of Glucocorticoids (GC) in the pituitary gland and implicated in the occurrence of behavioural disorders such as anxiety.

Objective: The present study aimed to evaluate the potential role of ANXA1 and its main receptor, as a cellular mediator of behavioural disorders, in a model of Corticosterone (CORT)-induced depression and subsequently, the possible correlation between the depressive state and impairment of hippocampal memory.

Methods: To induce the depression model, Wild-Type (WT), ANXA1 Knockout (KO), and FPR2/3 KO mice were exposed to oral administration of CORT for 28 days dissolved in drinking water. Following this, histological, biochemical and behavioural analyses were performed.

Results: FPR2/3 KO and ANXA1 KO mice showed improvement in anxiety and depression-like behaviour compared with WT mice after CORT administration. In addition, FPR2/3 KO and ANXA1 KO mice showed a reduction in histological alterations and neuronal death in hippocampal sections. Moreover, CORT+ FPR2/3 KO and ANXA1 KO, exhibited a higher expression of Brain-Derived Neurotrophic Factor (BDNF), phospho-ERK, cAMP response element-binding protein (pCREB) and a decrease in Serotonin Transporter Expression (SERT) compared to WT(CORT+) mice.

Conclusion: In conclusion, the absence of the ANXA1 protein, even more than the absence of its main receptor (FPR 2/3), was fundamental to the inhibitory action of GC on the HPA axis; it also maintained the hippocampal homeostasis by preventing neuronal damage associated with depression.

Keywords: Depression, corticosterone, annexin A1, formyl peptide receptor 2/3, glucorticoid, hippocampus.

Graphical Abstract
Hölscher, C. Time, space and hippocampal functions. Rev. Neurosci., 2003, 14(3), 253-284.
[] [PMID: 14513868]
LeDoux, J.E. Emotional memory systems in the brain. Behav. Brain Res., 1993, 58(1-2), 69-79.
[] [PMID: 8136051]
Baudry, A.; Mouillet-Richard, S.; Schneider, B.; Launay, J.M.; Kellermann, O. miR-16 targets the serotonin transporter: a new facet for adaptive responses to antidepressants. Science, 2010, 329(5998), 1537-1541.
[] [PMID: 20847275]
Nibuya, M.; Nestler, E.J.; Duman, R.S. Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J. Neurosci., 1996, 16(7), 2365-2372.
[] [PMID: 8601816]
Vaidya, V.A.; Marek, G.J.; Aghajanian, G.K.; Duman, R.S. 5-HT2A receptor-mediated regulation of brain-derived neurotrophic factor mRNA in the hippocampus and the neocortex. J. Neurosci., 1997, 17(8), 2785-2795.
[] [PMID: 9092600]
Coppell, A.L.; Pei, Q.; Zetterström, T.S. Bi-phasic change in BDNF gene expression following antidepressant drug treatment. Neuropharmacology, 2003, 44(7), 903-910.
[] [PMID: 12726822]
Lee, H.Y.; Kim, Y.K. Plasma brain-derived neurotrophic factor as a peripheral marker for the action mechanism of antidepressants. Neuropsychobiology, 2008, 57(4), 194-199.
[] [PMID: 18679038]
Govindarajan, A.; Rao, B.S.; Nair, D. Transgenic brain-derived neurotrophic factor expression causes both anxiogenic and antidepressant effects. Proc. Natl. Acad. Sci. USA, 2006, 103(35), 13208-13213.
[] [PMID: 16924103]
Siuciak, J.A.; Boylan, C.; Fritsche, M.; Altar, C.A.; Lindsay, R.M. BDNF increases monoaminergic activity in rat brain following intracerebroventricular or intraparenchymal administration. Brain Res., 1996, 710(1-2), 11-20.
[] [PMID: 8963648]
Gourley, S.L.; Wu, F.J.; Taylor, J.R. Corticosterone regulates pERK1/2 map kinase in a chronic depression model. Ann. N. Y. Acad. Sci., 2008, 1148, 509-514.
[] [PMID: 19120149]
McEwen, B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci., 1999, 22, 105-122.
[] [PMID: 10202533]
Duman, R.S.; Malberg, J.; Nakagawa, S. Regulation of adult neurogenesis by psychotropic drugs and stress. J. Pharmacol. Exp. Ther., 2001, 299(2), 401-407.
[PMID: 11602648]
Manji, H.K.; Drevets, W.C.; Charney, D.S. The cellular neurobiology of depression. Nat. Med., 2001, 7(5), 541-547.
[] [PMID: 11329053]
Manji, H.K.; Quiroz, J.A.; Sporn, J. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol. Psychiatry, 2003, 53(8), 707-742.
[] [PMID: 12706957]
Crupi, R.; Mazzon, E.; Marino, A. Hypericum perforatum treatment: effect on behaviour and neurogenesis in a chronic stress model in mice. BMC Complement. Altern. Med., 2011, 11, 7.
[] [PMID: 21272291]
Theogaraj, E.; John, C.D.; Christian, H.C.; Morris, J.F.; Smith, S.F.; Buckingham, J.C. Perinatal glucocorticoid treatment produces molecular, functional, and morphological changes in the anterior pituitary gland of the adult male rat. Endocrinology, 2005, 146(11), 4804-4813.
[] [PMID: 16099861]
Taylor, A.D.; Cowell, A.M.; Flower, J.; Buckingham, J.C. Lipocortin 1 mediates an early inhibitory action of glucocorticoids on the secretion of ACTH by the rat anterior pituitary gland in vitro. Neuroendocrinology, 1993, 58(4), 430-439.
[] [PMID: 7506818]
Buckingham, J.C.; Flower, R.J. Lipocortin 1: a second messenger of glucocorticoid action in the hypothalamo-pituitary-adrenocortical axis. Mol. Med. Today, 1997, 3(7), 296-302.
[] [PMID: 9257297]
Philip, J.G.; Flower, R.J.; Buckingham, J.C. Glucocorticoids modulate the cellular disposition of lipocortin 1 in the rat brain in vivo and in vitro. Neuroreport, 1997, 8(8), 1871-1876.
[] [PMID: 9223068]
Perretti, M.; Getting, S.J.; Solito, E.; Murphy, P.M.; Gao, J.L. Involvement of the receptor for formylated peptides in the in vivo anti-migratory actions of annexin 1 and its mimetics. Am. J. Pathol., 2001, 158(6), 1969-73.
[] [PMID: 11395373]
Ye, R.D.; Boulay, F.; Wang, J.M. International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol. Rev., 2009, 61(2), 119-161.
[] [PMID: 19498085]
Perretti, M.; D’Acquisto, F. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol., 2009, 9(1), 62-70.
[] [PMID: 19104500]
Dufton, N.; Perretti, M. Therapeutic anti-inflammatory potential of formyl-peptide receptor agonists. Pharmacol. Ther., 2010, 127(2), 175-88.
[] [PMID: 20546777]
Gallo, I.; Rattazzi, L.; Piras, G. Formyl peptide receptor as a novel therapeutic target for anxiety-related disorders. PLoS One, 2014, 9(12)e114626
[] [PMID: 25517119]
Hannon, R.; Croxtall, J.D.; Getting, S.J. Aberrant inflammation and resistance to glucocorticoids in annexin 1-/- mouse. FASEB J., 2003, 17(2), 253-255.
[] [PMID: 12475898]
Grassmé, H.; Jernigan, P.L.; Hoehn, R.S. Inhibition of acid sphingomyelinase by antidepressants counteracts stress-induced activation of P38-Kinase in Major Depression. Neurosignals, 2015, 23(1), 84-92.
[] [PMID: 26682751]
Casili, G.; Campolo, M.; Paterniti, I. Dimethyl fumarate attenuates neuroinflammation and neurobehavioral deficits induced by experimental traumatic brain injury. J. Neurotrauma, 2018, 35(13), 1437-1451.
[] [PMID: 29361881]
Santarelli, L.; Saxe, M.; Gross, C. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science, 2003, 301(5634), 805-9.
[] [PMID: 12907793]
Porsolt, R.D.; Bertin, A.; Blavet, N.; Deniel, M.; Jalfre, M. Immobility induced by forced swimming in rats: effects of agents which modify central catecholamine and serotonin activity. Eur. J. Pharmacol., 1979, 57(2-3), 201-10.
[] [PMID: 488159]
Mao, Q.Q.; Xian, Y.F.; Ip, S.P.; Tsai, S.H.; Che, C.T. Long-term treatment with peony glycosides reverses chronic unpredictable mild stress-induced depressive-like behavior via increasing expression of neurotrophins in rat brain. Behav. Brain Res., 2010, 210(2), 171-7.
[] [PMID: 20176057]
Botton, P.H.; Costa, M.S.; Ardais, A.P. Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice. Behav. Brain Res., 2010, 214(2), 254-9.
[] [PMID: 20553765]
Siracusa, R.; Impellizzeri, D.; Cordaro, M. Anti-inflammatory and neuroprotective effects of co-UltraPEALut in a mouse model of vascular dementia. Front. Neurol., 2017, 8, 233.
[] [PMID: 28634464]
Yin, J.B.; Wu, H.H.; Dong, Y.L. Neurochemical properties of BDNF-containing neurons projecting to rostral ventromedial medulla in the ventrolateral periaqueductal gray. Front. Neural Circuits, 2014, 8, 137.
[] [PMID: 25477786]
Esposito, E, D I, G B, et al. A new co-micronized composite containing palmitoylethanolamide and polydatin shows superior oral efficacy compared to their association in a rat paw model of carrageenan-induced inflammation. Eur. J. Pharmacol., 2016, 782:, 107-18.
[] [PMID: 27095683]
Cordaro, M.; Siracusa, R.; Crupi, R. 2-Pentadecyl-2-oxazoline reduces neuroinflammatory environment in the MPTP model of Parkinson disease. Mol. Neurobiol., 2018, 55(12), 9251-9266.
[] [PMID: 29656363]
Siracusa, R.; Impellizzeri, D.; Cordaro, M. Topical application of adelmidrol + trans-traumatic acid enhances skin wound healing in a streptozotocin-induced diabetic mouse model. Front. Pharmacol., 2018, 9, 871.
[] [PMID: 30190675]
John, C.D.; Christian, H.C.; Morris, J.F.; Flower, R.J.; Solito, E.; Buckingham, J.C. Annexin 1 and the regulation of endocrine function. Trends Endocrinol. Metab., 2004, 15(3), 103-109.
[] [PMID: 15046738]
Aoki, M.; Shimozuru, M.; Kikusui, T.; Takeuchi, Y.; Mori, Y. Sex differences in behavioral and corticosterone responses to mild stressors in ICR mice are altered by ovariectomy in peripubertal period. Zool. Sci., 2010, 27(10), 783-9.
[] [PMID: 20887175]
Márquez, C.; Nadal, R.; Armario, A. Influence of reactivity to novelty and anxiety on hypothalamic-pituitary-adrenal and prolactin responses to two different novel environments in adult male rats. Behav. Brain Res., 2006, 168(1), 13-22.
[] [PMID: 16303185]
Touma, C.; Bunck, M.; Glasl, L. Mice selected for high versus low stress reactivity: a new animal model for affective disorders. Psychoneuroendocrinology, 2008, 33(6), 839-62.
[] [PMID: 18502051]
File, S.E. Factors controlling measures of anxiety and responses to novelty in the mouse. Behav. Brain Res., 2001, 125(1-2), 151-157.
[] [PMID: 11682106]
Crawley, J.N. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res., 1999, 835(1), 18-26.
[] [PMID: 10448192]
Zhang, H.; Liu, B.; Wu, J.; Xu, C.; Tao, J.; Duan, X.; Cao, Y.; Dong, J. Icariin inhibits corticosterone-induced apoptosis in hypothalamic neurons via the PI3-K/Akt signaling pathway. Mol. Med. Rep., 2012, 6(5), 967-972.
[] [PMID: 22923091]
Levy, B.H.; Tasker, J.G. Synaptic regulation of the hypothalamic-pituitary-adrenal axis and its modulation by glucocorticoids and stress. Front. Cell. Neurosci., 2012, 6, 24.
[] [PMID: 22593735]
Rubin, R.T.; Poland, R.E.; Lesser, I.M.; Martin, D.J.; Blodgett, A.L.; Winston, R.A. Neuroendocrine aspects of primary endogenous depression. III. Cortisol secretion in relation to diagnosis and symptom patterns. Psychol. Med., 1987, 17(3), 609-619.
[] [PMID: 3628622]
Herbert, J. Cortisol and depression: three questions for psychiatry. Psychol. Med., 2013, 43(3), 449-469.
[] [PMID: 22564216]
Zameer, S.; Akhtar, M.; Vohora, D. Behavioral experimental paradigms for the evaluation of drug’s influence on cognitive functions: interpretation of associative, spatial/nonspatial and working memory. CNS Neurol. Disord. Drug Targets, 2019, 18(3), 185-204.
[] [PMID: 30648527]
Yu, J.Z.; Li, Y.H.; Liu, C.Y.; Wang, Q.; Gu, Q.F.; Wang, H.Q.; Zhang, G.X.; Xiao, B.G.; Ma, C.G. Multitarget therapeutic effect of fasudil in APP/PS1transgenic mice. CNS Neurol. Disord. Drug Targets, 2017, 16(2), 199-209.
[] [PMID: 27401064]
Al-Hakeim, H.K.; Al-Kufi, S.N.; Al-Dujaili, A.H.; Maes, M. Serum interleukin levels and insulin resistance in major depressive disorder. CNS Neurol. Disord. Drug Targets, 2018, 17(8), 618-625.
[] [PMID: 30033878]
Farkhondeh, T.; Samarghandian, S.; Samini, F.; Sanati, A.R. Protective effects of crocetin on depression-like behavior induced by immobilization in rat. CNS Neurol. Disord. Drug Targets, 2018, 17(5), 361-369.
[] [PMID: 29766828]
Vazquez, G.H.; Camino, S.; Tondo, L.; Baldessarini, R.J. Potential novel treatments for bipolar depression: ketamine, fatty acids, anti-inflammatory agents, and probiotics. CNS Neurol. Disord. Drug Targets, 2017, 16(8), 858-869.
[PMID: 28758582]
Murray, F.; Smith, D.W.; Hutson, P.H. Chronic low dose corticosterone exposure decreased hippocampal cell proliferation, volume and induced anxiety and depression like behaviours in mice. Eur. J. Pharmacol., 2008, 583(1), 115-127.
[] [PMID: 18289522]
Pan, Z.; Grovu, R.C.; Cha, D.S.; Carmona, N.E.; Subramaniapillai, M.; Shekotikhina, M.; Rong, C.; Lee, Y.; McIntyre, R.S. Pharmacological treatment of cognitive symptoms in major depressive disorder. CNS Neurol. Disord. Drug Targets, 2017, 16(8), 891-899.
[PMID: 28933261]
Gao, J.L.; Schneider, E.H.; Dimitrov, E.L.; Haun, F.; Pham, T.M.; Mohammed, A.H.; Usdin, T.B.; Murphy, P.M. Reduced fear memory and anxiety-like behavior in mice lacking formylpeptide receptor 1. Behav. Genet., 2011, 41(5), 724-733.
[] [PMID: 21484271]
Patel, H.B.; Kornerup, K.N.; Sampaio, A.L.; D’Acquisto, F.; Seed, M.P.; Girol, A.P.; Gray, M.; Pitzalis, C.; Oliani, S.M.; Perretti, M. The impact of endogenous annexin A1 on glucocorticoid control of inflammatory arthritis. Ann. Rheum. Dis., 2012, 71(11), 1872-1880.
[] [PMID: 22562975]
de Jong, R.; Leoni, G.; Drechsler, M.; Soehnlein, O. The advantageous role of annexin A1 in cardiovascular disease. Cell Adhes. Migr., 2017, 11(3), 261-274.
[] [PMID: 27860536]
Babbin, B.A.; Laukoetter, M.G.; Nava, P.; Koch, S.; Lee, W.Y.; Capaldo, C.T.; Peatman, E.; Severson, E.A.; Flower, R.J.; Perretti, M.; Parkos, C.A.; Nusrat, A. Annexin A1 regulates intestinal mucosal injury, inflammation, and repair. J. Immunol., 2008, 181(7), 5035-5044.
[] [PMID: 18802107]
Ansari, J.; Kaur, G.; Gavins, F.N.E. Therapeutic potential of annexin A1 in ischemia reperfusion injury. Int. J. Mol. Sci., 2018, 19(4)E1211
[] [PMID: 29659553]
Leasure, J.L.; Jones, M. Forced and voluntary exercise differentially affect brain and behavior. Neuroscience, 2008, 156(3), 456-465.
[] [PMID: 18721864]
Santos-Soto, I.J.; Chorna, N.; Carballeira, N.M.; Vélez-Bartolomei, J.G.; Méndez-Merced, A.T.; Chornyy, A.P.; Peña de Ortiz, S. Voluntary running in young adult mice reduces anxiety-like behavior and increases the accumulation of bioactive lipids in the cerebral cortex. PLoS One, 2013, 8(12)e81459
[] [PMID: 24349072]
Fediuc, S; Campbell, JE; Riddell, MC Effect of voluntary wheel running on circadian corticosterone release and on HPA axis responsiveness to restraint stress in Sprague-Dawley rats. J Appl Physiol (1985) 2006, 100(6), 1867-75.
Benaroya-Milshtein, N.; Hollander, N.; Apter, A.; Kukulansky, T.; Raz, N.; Wilf, A.; Yaniv, I.; Pick, C.G. Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur. J. Neurosci., 2004, 20(5), 1341-1347.
[] [PMID: 15341605]
Marashi, V.; Barnekow, A.; Ossendorf, E.; Sachser, N. Effects of different forms of environmental enrichment on behavioral, endocrinological, and immunological parameters in male mice. Horm. Behav., 2003, 43(2), 281-292.
[] [PMID: 12694638]
Olsson, I.A.; Dahlborn, K. Improving housing conditions for laboratory mice: a review of “environmental enrichment”. Lab. Anim., 2002, 36(3), 243-270.
[] [PMID: 12144738]
Lee, B.; Shim, I.; Lee, H.J.; Yang, Y.; Hahm, D.H. Effects of acupuncture on chronic corticosterone-induced depression-like behavior and expression of neuropeptide Y in the rats. Neurosci. Lett., 2009, 453(3), 151-156.
[] [PMID: 19429024]
Ali, SH. Madhana RM, KVA, et al.Resveratrol ameliorates depressive-like behavior in repeated corticosterone-induced depression in mice. Steroids, 2015, 101, 37-42.
[] [PMID: 26048446]
John, C.D.; Sahni, V.; Mehet, D.; Morris, J.F.; Christian, H.C.; Perretti, M.; Flower, R.J.; Solito, E.; Buckingham, J.C. Formyl peptide receptors and the regulation of ACTH secretion: targets for annexin A1, lipoxins, and bacterial peptides. FASEB J., 2007, 21(4), 1037-1046.
[] [PMID: 17218541]
Kurek, A.; Kucharczyk, M.; Detka, J.; Ślusarczyk, J.; Trojan, E.; Głombik, K.; Bojarski, B.; Ludwikowska, A.; Lasoń, W.; Budziszewska, B. Pro-apoptotic action of corticosterone in hippocampal organotypic cultures. Neurotox. Res., 2016, 30(2), 225-238.
[] [PMID: 27189478]
Solito, E.; McArthur, S.; Christian, H.; Gavins, F.; Buckingham, J.C.; Gillies, G.E. Annexin A1 in the brain--undiscovered roles? Trends Pharmacol. Sci., 2008, 29(3), 135-142.
[] [PMID: 18262660]
Parente, L.; Solito, E. Annexin 1: more than an anti-phospholipase protein. Inflamm. Res., 2004, 53(4), 125-132.
[] [PMID: 15060718]
Solito, E.; de Coupade, C.; Canaider, S.; Goulding, N.J.; Perretti, M. Transfection of annexin 1 in monocytic cells produces a high degree of spontaneous and stimulated apoptosis associated with caspase-3 activation. Br. J. Pharmacol., 2001, 133(2), 217-228.
[] [PMID: 11350857]
Xia, Q.; Li, X.; Zhou, H.; Zheng, L.; Shi, J. S100A11 protects against neuronal cell apoptosis induced by cerebral ischemia via inhibiting the nuclear translocation of annexin A1. Cell Death Dis., 2018, 9(6), 657.
[] [PMID: 29844306]
Coope, J. Is oestrogen therapy effective in the treatment of menopausal depression? J. R. Coll. Gen. Pract., 1981, 31(224), 134-140.
[PMID: 6268783]
Seeman, M.V. Psychopathology in women and men: focus on female hormones. Am. J. Psychiatry, 1997, 154(12), 1641-1647.
[] [PMID: 9396940]
Hayward, C.; Sanborn, K. Puberty and the emergence of gender differences in psychopathology. J. Adolesc. Health, 2002, 30(4)(Suppl.), 49-58.
[] [PMID: 11943575]
Shimizu, E.; Hashimoto, K.; Okamura, N.; Koike, K.; Komatsu, N.; Kumakiri, C.; Nakazato, M.; Watanabe, H.; Shinoda, N.; Okada, S.; Iyo, M. Alterations of serum levels of brain-derived neurotrophic factor (BDNF) in depressed patients with or without antidepressants. Biol. Psychiatry, 2003, 54(1), 70-75.
[] [PMID: 12842310]
Franklin, T.B.; Perrot-Sinal, T.S. Sex and ovarian steroids modulate brain-derived neurotrophic factor (BDNF) protein levels in rat hippocampus under stressful and non-stressful conditions. Psychoneuroendocrinology, 2006, 31(1), 38-48.
[] [PMID: 15996825]
Bai, Y.; Song, L.; Dai, G.; Xu, M.; Zhu, L.; Zhang, W.; Jing, W.; Ju, W. Antidepressant effects of magnolol in a mouse model of depression induced by chronic corticosterone injection. Steroids, 2018, 135, 73-78.
[] [PMID: 29555480]
Khan, H.; Khattak, S.; Mubarak, M.S.; Bawazeer, S.S.; Abu-Izneid, T.; Kamal, M.A. Aantidepressant potential of peptides: new insights as future therapeutic. CNS Neurol. Disord. Drug Targets, 2018, 17(1), 9-13.
[] [PMID: 28758584]
Guo, J.Q.; Deng, H.H.; Bo, X.; Yang, X.S. Involvement of BDNF/TrkB and ERK/CREB axes in nitroglycerin-induced rat migraine and effects of estrogen on these signals in the migraine. Biol. Open, 2017, 6(1), 8-16.
[] [PMID: 27875242]
Martinowich, K.; Lu, B. Interaction between BDNF and serotonin: role in mood disorders. Neuropsychopharmacology, 2008, 33(1), 73-83.
[] [PMID: 17882234]
Perucci, L.O.; Vieira, E.L.M.; Teixeira, A.L.; Gomes, K.B.; Dusse, L.M.; Sousa, L.P. Decreased plasma concentrations of brain-derived neurotrophic factor in preeclampsia. Clin. Chim. Acta, 2017, 464, 142-147.
[] [PMID: 27887959]
Kelly, A.; Laroche, S.; Davis, S. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J. Neurosci., 2003, 23(12), 5354-5360.
[] [PMID: 12832561]
Soulé, J.; Penke, Z.; Kanhema, T.; Alme, M.N.; Laroche, S.; Bramham, C.R. Object-place recognition learning triggers rapid induction of plasticity-related immediate early genes and synaptic proteins in the rat dentate gyrus. Neural Plast., 2008, 2008269097
[] [PMID: 19190776]
Chen, D.; Peng, C.; Xie, X.; Chen, Q.; Liu, H.; Zhang, S.; Wan, F.; Ao, H. Low dose of anisodine hydrobromide induced neuroprotective effects in chronic cerebral hypoperfusion rats. CNS Neurol. Disord. Drug Targets, 2017, 16(10), 1111-1119.
[] [PMID: 29076436]
Mann, J.J.; McBride, P.A.; Malone, K.M.; DeMeo, M.; Keilp, J. Blunted serotonergic responsivity in depressed inpatients. Neuropsychopharmacology, 1995, 13(1), 53-64.
[] [PMID: 8526971]
Bhagwagar, Z.; Whale, R.; Cowen, P.J. State and trait abnormalities in serotonin function in major depression. Br. J. Psychiatry, 2002, 180, 24-28.
[] [PMID: 11772847]
Graeff, F.G. Serotonergic systems. Psychiatr. Clin. North Am., 1997, 20(4), 723-739.
[] [PMID: 9443347]
Zhang, J.; Fan, Y.; Li, Y.; Zhu, H.; Wang, L.; Zhu, M.Y. Chronic social defeat up-regulates expression of the serotonin transporter in rat dorsal raphe nucleus and projection regions in a glucocorticoid-dependent manner. J. Neurochem., 2012, 123(6), 1054-1068.
[] [PMID: 23061525]
Moreno-Ramos, O.A.; Lattig, M.C.; González Barrios, A.F. Modeling of the hypothalamic-pituitary-adrenal axis-mediated interaction between the serotonin regulation pathway and the stress response using a Boolean approximation: a novel study of depression. Theor. Biol. Med. Model., 2013, 10, 59.
[] [PMID: 24093582]

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