Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
NeuroMolecular Medicine
Published in: NeuroMolecular Medicine 2/2015

01-06-2015 | Original Paper

Modification of Hippocampal Markers of Synaptic Plasticity by Memantine in Animal Models of Acute and Repeated Restraint Stress: Implications for Memory and Behavior

Authors: Shaimaa Nasr Amin, Ahmed Amro El-Aidi, Mohamed Mostafa Ali, Yasser Mahmoud Attia, Laila Ahmed Rashed

Published in: NeuroMolecular Medicine | Issue 2/2015

Login to get access

Abstract

Stress is any condition that impairs the balance of the organism physiologically or psychologically. The response to stress involves several neurohormonal consequences. Glutamate is the primary excitatory neurotransmitter in the central nervous system, and its release is increased by stress that predisposes to excitotoxicity in the brain. Memantine is an uncompetitive N-methyl D-aspartate glutamatergic receptors antagonist and has shown beneficial effect on cognitive function especially in Alzheimer’s disease. The aim of the work was to investigate memantine effect on memory and behavior in animal models of acute and repeated restraint stress with the evaluation of serum markers of stress and the expression of hippocampal markers of synaptic plasticity. Forty-two male rats were divided into seven groups (six rats/group): control, acute restraint stress, acute restraint stress with Memantine, repeated restraint stress, repeated restraint stress with Memantine and Memantine groups (two subgroups as positive control). Spatial working memory and behavior were assessed by performance in Y-maze. We evaluated serum cortisol, tumor necrotic factor, interleukin-6 and hippocampal expression of brain-derived neurotrophic factor, synaptophysin and calcium-/calmodulin-dependent protein kinase II. Our results revealed that Memantine improved spatial working memory in repeated stress, decreased serum level of stress markers and modified the hippocampal synaptic plasticity markers in both patterns of stress exposure; in ARS, Memantine upregulated the expression of synaptophysin and brain-derived neurotrophic factor and downregulated the expression of calcium-/calmodulin-dependent protein kinase II, and in repeated restraint stress, it upregulated the expression of synaptophysin and downregulated calcium-/calmodulin-dependent protein kinase II expression.
Literature
Adamec, R., Toth, M., Haller, J., Halasz, J., & Blundell, J. (2012). A comparison of activation patterns of cells in selected prefrontal cortical and amygdala areas of rats which are more or less anxious in response to predator exposure or submersion stress. Physiology & Behavior, 105(3), 628–638.CrossRef
Adlard, P., & Cotman, C. (2004). Voluntary exercise protects against stress-induced decreases in brain-derived neurotrophic factor protein expression. Neuroscience, 124(4), 985–992.
Adlard, P. A., Perreau, V. M., Engesser-Cesar, C., & Cotman, C. W. (2004). The time course of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neuroscience Letters, 363, 43–48.CrossRefPubMed
Alsina, B., Vu, T., & Cohen-Cory, S. (2001). Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nature Neuroscience, 4, 1093–1101.CrossRefPubMed
Altman, G .D. (2005). Comparing groups: Three or more independent groups of observations in practical statistics for medical research. London: Chapman and Hall.
Arai, K., Matsuki, N., Ikegaya, Y., & Nishiyama, N. (2001). Deterioration of spatial learning performances in lipopolysaccharide-treated mice. Japanese Journal of Pharmacology, 87, 195–201.CrossRefPubMed
Babic, S., Ondrejcakova, M., Bakos, J., Racekova, E., & Jezova, D. (2012). Cell proliferation in the hippocampus and in the heart is modified by exposure to repeated stress and treatment with memantine. Journal of Psychiatric Research, 46(4), 526–532.CrossRefPubMed
Bannerman, D. M., Rawlins, J. N., McHugh, S. B., Deacon, R. M., Yee, B. K., Bast, T., et al. (2004). Regional dissociations within the hippocampus–memory and anxiety. Neuroscience and Biobehavioral Reviews, 3, 273–283.CrossRef
Bannerman, D. M., Sprengel, R., Sanderson, D. J., McHugh, S. B., Rawlins, J. N., Monyer, H., et al. (2014). Hippocampal synaptic plasticity, spatial memory and anxiety. Nature Reviews Neuroscience, 15(3), 181–192.
Barco, A., Bailey, C. H., & Kandel, E. R. (2006). Common molecular mechanisms in explicit and implicit memory. Journal of Neurochemistry, 97, 1520–1533.CrossRefPubMed
Barde, Y. A. (1994). Neurotrophins: A family of proteins supporting the survival of neurons. Progress in Clinical and Biological Research, 390, 45–56.PubMed
Blanchard, R. J., & Blanchard, D. C. (1969). Crouching as an index of fear. Journal of Comparative and Physiological Psychology, 67, 370–375.CrossRefPubMed
Bolles, R. C., & Riley, A. L. (1973). Freezing as an avoidance response: Another look at the operant-respondent distinction. Learning and Motivation, 4(3), 268–275.
Bowman, R. E., Zrull, M. C., & Luine, V. N. (2001). Chronic restraint stress enhances radial arm maze performance in female rats. Brain Research, 904(2), 279–289.
Britton, D. R., Koob, G. F., Rivier, J., & Vale, W. (1982). Intraventricular corticotropin-releasing factor enhances behavioral effects of novelty. Life Sciences, 31, 363–367.CrossRefPubMed
Campos, A. C., Ferreira, F. R., da Silva, W. A., & Guimarães, F. S., Jr. (2013). Predator threat stress promotes long lasting anxiety-like behaviors and modulates synaptophysin and CB1 receptors expression in brain areas associated with PTSD symptoms. Neuroscience Letters, 15(533), 34–38.CrossRef
Chen, D. Y., Bambah-Mukku, D., Pollonini, G., & Alberini, C. M. (2012). Glucocorticoid receptors recruit the CaMKIIα-BDNF-CREB pathways to mediate memory consolidation. Nature Neuroscience, 15(12), 1707–1714.CrossRefPubMedCentralPubMed
Collingridge, G. L., Peineau, S., Howland, J. G., & Wang, Y. T. (2010). Longterm depression in the CNS. Nature Reviews Neuroscience, 11, 459–473.CrossRefPubMed
Conner, J. M., Lauterborn, J. C., Yan, Q., Gall, C. M., & Varon, S. (1997). Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: Evidence for anterograde axonal transport. Journal of Neuroscience, 17(2295e), 2313.
Coppell, A. L., Pei, Q., & Zetterstrom, T. S. (2003). Bi-phasic change in BDNF gene expression following antidepressant drug treatment. Neuropharmacology, 44, 903–910.CrossRefPubMed
Costa, A. C., Scott-McKean, J. J., & Stasko, M. R. (2008). Acute injections of the NMDA receptor antagonist memantine rescue performance deficits of the Ts65Dn mouse model of down syndrome on a fear conditioning test. Neuropsychopharmacology, 33(7), 1624–1632.CrossRefPubMed
Creeley, C., Wozniak, D. F., Labruyere, J., Taylor, G. T., & Olney, J. W. (2006). Low doses of memantine disrupt memory in adult rats. The Journal of Neuroscience, 26(15), 3923–3932.
Cull-Candy, S. (2007). NMDA receptors. Encyclopedia of life sciences.
Daniels, W. M. U., de Klerk Uys, J., van Vuuren, P., & Stein, D. J. (2008). The development of behavioral and endocrine abnormalities in rats after repeated exposure to direct and indirect stress. Neuropsychiatric Disease and Treatment 2, 451–464.
Deak, T., Meriwether, J. L., Fleshner, M., Spencer, R. L., Abouhamze, A., Moldawer, L. L., et al. (2004). Evidence that brief stress may induce the acute phase response in rats. American Journal of Physiology, 273(6 Pt 2), R1998–R2004.
Denmark, A., Tien, D., Wong, K., Chung, A., Cachat, J., Goodspeed, J., et al. (2010). The effects of chronic social defeat stress on mouse self-grooming behavior and its patterning. Behavioural Brain Research, 208(2), 553–559.
Diamond, D. M., Fleshner, M., & Rose, G. M. (1994). Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats. Behavioural Brain Research, 62, 1–9.CrossRefPubMed
Dubovicky, M., & Jezova, D. (2004). Effect of chronic emotional stress on habituation processes in open field in adult rats. Annals of the New York Academy of Sciences, 1018, 199e206.
Dunn, A. J., Swiergiel, A. H., & de Beaurepaire, R. (2005). Cytokines as mediators of depression: What can we learn from animal studies? Neuroscience and Biobehavioral Reviews, 29(4–5), 891–909.CrossRefPubMed
Eastwood, S. L., & Harrison, P. J. (2001). Synaptic pathology in the anterior cingulated cortex in schizophrenia and mood disorders. A review and a Western blot study of synaptophysin, GAP-43 and the complexins. Brain Research Bulletin, 55, 569–578.CrossRefPubMed
Edwards, K. M., Burns, V. E., Ring, C., & Carroll, D. (2006). Sex differences in the interleukin-6 response to acute psychological stress. Biological Psychology, 71, 236–239.CrossRefPubMed
Elenkov, I. J., Wilder, R. L., Chrousos, G. P., Vizi, E. S. (2000). The sympathetic nerve an integrative interface between two supersystems: The brain and the immune system. Pharmacological Reviews, 52, 595–638.
Farmer, J., Zhao, X., Van Praag, H., Wodtke, K., Gage, F. H., & Christie, B. R. (2004). Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience, 124, 71–79.CrossRefPubMed
Fink, C. C., & Meyer, T. (2002). Molecular mechanisms of CaMKII activation in neuronal plasticity. Current Opinion in Neurobiology, 12, 293–299.CrossRefPubMed
Gądek-Michalska, A., Tadeusz, J., Rachwalska, P., & Bugajski, J. (2013). Cytokines, prostaglandins and nitric oxide in the regulation of stress-response systems. Pharmacological Reports, 65(6), 1655–1662.CrossRefPubMed
Gaertner, T. R., Kolodziej, S. J., Wang, D., Kobayashi, R., Koomen, J. M., Stoops, J. K., & Waxham, M. N. (2004). Comparative analyses of the 3-dimensional structures and enzymatic properties of a, b, c, and isoforms of Ca2R-calmodulin dependent protein kinase II. Journal of Biological Chemistry, 279(12484), 12494.
Gardoni, F., Schrama, L. H., van Dalen, J. J., Gispen, W. H., Cattabeni, F., & Di Luca, M. (1999). αCaMKII binding to the C-terminal tail of NMDA receptor subunit NR2A and its modulation by autophosphorylation. FEBS Letters, 456, 394–398.CrossRefPubMed
Givalois, L., Naert, G., Rage, F., Ixart, G., Arancibia, S., & Tapia-Arancibia, L. (2004). A single brain-derived neurotrophic factor injection modifies hypothalamo-pituitary-adrenocortical axis activity in adult male rats. Molecular and Cellular Neuroscience, 27(3), 280–295.CrossRefPubMed
Gray, T. S. (1993). Amygdaloid CRF pathways: Role in autonomic, neuroendocrine and behavioural responses to stress. Annals of New York Academy of Sciences, 697, 53–60.CrossRef
Greengard, P., Valtorta, F., Czernik, A. J., & Benfenati, F. (1993). Synaptic vesicle phosphoproteins and regulation of synaptic function. Science, 259, 780–785.CrossRefPubMed
Gronli, J., Bramham, C., Murison, R., Kanhema, T., Fiske, E., Bjorvatn, B., et al. (2006). Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper. Pharmacology, Biochemistry and Behavior, 85, 842–849.CrossRefPubMed
Hansson, A. C., Sommer, W., Rimondini, R., Andbjer, B., Stromberg, I., & Fuxe, K. (2003). c-Fos reduces corticosterone-mediated effects on neurotrophic factor expression in the rat hippocampal CA1 region. Journal of Neuroscience, 23, 6013–6022.PubMed
Horner, W. G., Falkai, P., Chen, C., Arango, V., Mann, J. J., & Dwork, A. J. (1999). Synaptic and plasticity-associated proteins in anterior frontal cortex in severe mental illness. Neuroscience, 91, 1247–1255.CrossRef
Hudmon, A., & Schulman, H. (2002). Structure–function of the multifunctional Ca2 +/calmodulin-dependent protein kinase II. Biochemical Journal, 364, 593–611.CrossRefPubMedCentralPubMed
Hwa, L. S., Shimamoto, A., Nathanson, A. J., Tayeh, J., DeBold, J. F., & Miczek, K. A. (2013). Alcohol-withdrawal aggression: Glutamate and Nmda receptors in the Pfc. Behavioural Pharmacology, 24, e56.
Irwin, M., Hanger, R. L., & Jones, L. (1991). Sympathetic nervous system mediates central CRF induced suppression of natural killer cell cytotoxicity. Journal of Pharmacology and Experimental Therapeutics, 255, I 01–I 07.
Itami, C., Kimura, F., Kohno, T., Matsuoka, M., Ichikawa, M., Tsumoto, T., & Nakamura, S. (2003). Brain-derived neurotrophic factor-dependent unmasking of “silent” synapses in the developing mouse barrel cortex. Proceedings of the National Academy of Sciences USA, 100(22), 13069–13074.CrossRef
Jezova, D. (2005). Control of ACTH secretion by excitatory amino acids. Endocrine, 28(3), 287–293.
Jin, K., Xie, L., Mao, X. O., & Greenberg, D. A. (2006). Alzheimer’s disease drugs promote neurogenesis. Brain Research, 1085, 183–188.CrossRefPubMed
Kalueff, A. V., & Tuohimaa, P. (2005). The grooming analysis algorithm discriminates between different levels of anxiety in rats: Potential utility for neurobehavioural stress research. Journal of Neuroscience Methods, 143, 169–177.CrossRefPubMed
Kant, G. J., Leu, J. R., & Anderson, S. M. (1987). Effects of chronic stress on plasma corticosterone. ACTH and prolactin. Physiology Behavior, 40, 775–779.CrossRefPubMed
Katoh-Semba, R., Takeuchi, I. K., Inaguma, Y., Ichisaka, S., Hata, Y., Tsumoto, T., et al. (2001). Induction of brain-derived neurotrophic factor by convulsant drugs in the rat brain: Involvement of region-specific voltage-dependent calcium channels. Journal of Neurochemistry, 77, 71–83.CrossRefPubMed
Katz, R. J., Roth, K. A., & Carroll, B. J. (1981). Acute and chronic stress effects on open field activity in the rat: implications for a model of depression. Neuroscience and Biobehavioral Reviews, 5(2), 247–251.CrossRefPubMed
Kelleher, R. J., I. I. I., Govindarajan, A., & Tonegawa, S. (2004). Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron, 44, 59–73.CrossRefPubMed
Khalaj, L., Nejad, S. C., Mohammadi, M., Zadeh, S. S., Pour, M. H., Ahmadiani, A., et al. (2013). Gemfibrozil pretreatment proved protection against acute restraint stress-induced changes in the male rats’ hippocampus. Brain Research, 1527, 117–130.
Kim, J. J., & Diamond, D. M. (2002). The stressed hippocampus, synaptic plasticity and lost memories. Nature Reviews Neuroscience, 3(6):453–462.
Kirschbaum, C., Wolf, O. T., May, M., Wippich, W., & Hellhammer, D. H. (1996). Stress-and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sciences, 58(17):1475–1483.
Koo, J. W., Park, C. H., Choi, S. H., Kim, N. J., Kim, H., Choe, J. C., & Suh, Y. (2003). The post-natal environment can counteract pre-natal effects on cognitive ability, cell proliferation, and synaptic protein expression. FASEB Journal, 17, 1556–1558.PubMed
Kos, T., & Popik, P. (2005). A comparison of the predictive therapeutic and undesired side-effects of the NMDA receptor antagonist, memantine, in mice. Behavioural Pharmacology, 16(3), 155–161.
Kumar, A., Garg, R., & Prakash, A. K. (2010). Effect of St. John’s Wort (Hypericum perforatum) treatment on restraint stress-induced behavioral and biochemical alteration in mice. BMC complement. Alternative Medicine, 7, 10–18.
Lavric, A., Rippon, G., & Gray, J. R. (2003). Threat-evoked anxiety disrupts spatial working memory performance: An attentional account. Cognitive Therapy and Research, 27(5), 489–504.CrossRef
Lee, S. Y., Chen, S. L., Chang, Y. H., Chen, P. S., Huang, S. Y., Tzeng, N. S., et al. (2014). The effects of add-on low-dose memantine on cytokine levels in bipolar II depression: A 12-week double-blind, randomized controlled trial. Journal of Clinical Psychopharmacology, 34(3), 337–343.
Lin, K. Y., Cherng, C. G., Yang, F. R., Lin, L. C., Lu, R. B., & Yu, L. (2011). Memantine abolishes the formation of cocaine-induced conditioned place preference possibly via its IL-6-modulating effect in medial prefrontal cortex. Behavioural Brain Research, 220(1), 126–131.CrossRefPubMed
Lisman, J., Schulman, H., & Cline, H. (2002). The molecular basis of CaMKII function in synaptic and behavioural memory. Nature Reviews Neuroscience, 3, 175–190.CrossRefPubMed
Lisman, J., Yasuda, R., & Raghavachari, S. (2012). Mechanisms of CaMKII action in long-term potentiation. Nature Reviews Neuroscience, 13, 169–182.PubMedCentralPubMed
Lu, B. (2003). BDNF and activity-dependent synaptic modulation. Learning & Memory, 10, 86–98.CrossRef
Maekawa, M., Namba, T., Suzuki, E., Yuasa, S., Kohsaka, S., & Uchino, S. (2009). NMDA receptor antagonist memantine promotes cell proliferation and production of mature granule neurons in the adult hippocampus. Neuroscience Research, 63(4), 259–266.
Marsden, K. C., Shemesh, A., Bayer, K. U., & Carroll, R. C. (2010). Selective translocation of Ca2+/calmodulinprotein kinase IIalpha (CaMKIIalpha) to inhibitory synapses. Proceedings of National Academy of Sciences USA, 107(47), 20559–20564.CrossRef
Marvanová, M., Lakso, M., Pirhonen, J., Nawa, N., Hiroyoki, N., Wong, G., et al. (2001). The neuroprotective agent memantine induces brain-derived neurotrophic factor and trkb receptor expression in rat brain. Molecular and Cellular Neuroscience, 18, 247–258.
Masliah, E., Mallory, M., Hansen, L., DeTeresa, R., Alford, M., & Terry, R. D. (1994). Synaptic and neuritic alterations during the progression of Alzheimer’s disease. Neuroscience Letters, 174, 67–72.CrossRefPubMed
McEwen, B. S. (1999). Stress and hippocampal plasticity. Annual Review of Neuroscience, 22, 105–122.CrossRefPubMed
Mehta, A., Prabhakar, M., Kumar, P., Deshmukh, R., & Sharma, P. L. (2013). Excitotoxicity: Bridge to various triggers in neurodegenerative disorders. European Journal of Pharmacology, 698(1–3), 6–18.CrossRefPubMed
Mercier, S., Canini, F., Buguet, A., Cespuglio, R., Martin, S., & Bourdon, L. (2003). Behavioural changes after an acute stress: stressor and test types influences. Behavioural Brain Research, 139, 167–175.CrossRefPubMed
Mizuno, M., Yamada, K., Olariu, A., Nawa, H., & Nabeshima, T. (2000). Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. Journal of Neuroscience, 20, 7116–7121.PubMed
Murakami, S., Imbe, H., Morikawa, Y., Kubo, C., & Senba, E. (2005). Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neuroscience Research, 53(2), 129–139.CrossRefPubMed
Namba, T., Yabe, T., Gonda, Y., Ichikawa, N., Sanagi, T., et al. (2010). Pigment epithelium-derived factor up-regulation induced by memantine, an N-methyl-D-aspartate receptor antagonist, is involved in increased proliferation of hippocampal progenitor cells. Neuroscience, 167, 372–383.CrossRefPubMed
Nosek, K., Dennis, K., Andrus, B. M., Ahmadiyeh, N., Baum, A. E., Woods, L. C., & Redei, E. E. (2008). Context and strain-dependent behavioral response to stress. Behavioral and Brain Functions, 4, 23.CrossRefPubMedCentralPubMed
Novak, G., Fan, T., O’Dowd, B. F., & George, S. R. (2013). Postnatal maternal deprivation and pubertal stress have additive effects on dopamine D2 receptor and CaMKII beta expression in the striatum. International Journal of Developmental Neuroscience, 3, 189–195.CrossRef
Novelli, A., Basterrechea, M. P., & Fernandez-Sanchez, M. T. (2005). Glutamate and neurodegeneration. In: W. J. Schmidt & M. E. Reith (Eds.), Dopamine and Glutamate in Psychiatric disorders (pp 447–472). Totowa, NJ: Humana Press.
Padovan, C. M., & Guimaraes, F. S. (2004). Antidepressant-like effects of NMDA-receptor antagonist injected into the dorsal hippocampus of rats. Pharmacology, Biochemistry and Behavior, 77(1), 15–19.CrossRefPubMed
Pan, F. L. C., Song, J., Hong, J., Li, Q., Yu, H. I., & Chen, X. Y. (2006). Different duration of crowding and noise exposure effects on exploratory behavior, cellular immunity and hsp70 expression in rats. Stress Health, 22, 257–262.CrossRef
Phillips, H. S., Hains, J. M., Laramee, G. R., Rosenthal, A., & Winslow, J. W. (1990). Widespread expression of BDNF but not NT3 by target areas of basal forebrain cholinergic neurons. Science, 250, 290e294.
Popoli, M., Yan, Z., McEwen, B. S., & Sanacora, G. (2011). The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nature Reviews Neuroscience, 13(1), 22–37.PubMedCentralPubMed
Quan, M. N., Zhang, N., Wang, Y. Y., Zhang, T., & Yang, Z. (2011). Possible antidepressant effects and mechanisms of memantine in behaviors and synaptic plasticity of a depression rat model. Neuroscience, 182, 88–97.CrossRefPubMed
Ranjit, N., Diez-Roux, A. V., Shea, S., Cushman, M., Seeman, T., Jackson, S. A., & Ni, H. (2007). Psychosocial factors and inflammation in the multi-ethnic study of atherosclerosis. Archives of Internal Medicine, 167, 174–181.CrossRefPubMed
Rehm, H., Wiedenmann, B., & Betz, H. (1986). Molecular characterization of synaptophysin, a major calcium-binding protein of the synaptic vesicle membrane. EMBO Journal, 5, 535–541.PubMedCentralPubMed
Reul, J. M., & de Kloet, E. R. (1985). Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology, 117, 2505–2511.CrossRefPubMed
Rogóz, Z., Skuza, G., & Legutko, B. (2008). Repeated co-treatment with fluoxetine and amantadine induces brain-derived neurotrophic factor gene expression in rats. Pharmacology Reports, 60, 817–826.
Saha, R. N., Liu, X., & Pahan, K. (2006). Up-regulation of BDNF in astrocytes by TNF-alpha: A case for the neuroprotective role of cytokine. Journal of Neuroimmune Pharmacology, 1(3), 212–222.CrossRefPubMedCentralPubMed
Sapolsky, R. M., Krey, L. C., & McEwen, B. S. (1984). Stress down-regulates corticosterone receptors in a site-specific manner in the brain. Endocrinology, 114, 287–292.CrossRefPubMed
Schaaf, M. J., de Jong, J., de Kloet, E. R., & Vreugdenhil, E. (1998). Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Research, 813, 112–120.CrossRefPubMed
Seil, F. J., & Drake-Baumann, R. (2000). TrkB receptor ligands promote activity-dependent inhibitory synaptogenesis. Journal of Neuroscience, 20, 5367–5373.PubMed
Smith, M. A., Makino, S., Kvetnansky, R., & Post, R. M. (1995). Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. Journal of Neuroscience, 15, 1768–1777.PubMed
Smolinsky, A. N., Bergner, C. L., LaPorte, J. L., & Kalueff, A. V. (2009). Analysis of grooming behavior and its utility in studying animal stress, anxiety, and depression. Mood and anxiety related phenotypes in mice (pp. 21–36). New York: Humana Press.
Stanton, P. K., & Gage, A. T. (1996). Distinct synaptic loci of Ca2+/calmodulin-dependent protein kinase II necessary for long-term potentiation and depression. Journal of Neurophysiology, 76, 2097–2101.PubMed
Steimer, T., & Driscoll, P. (2003). Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low-(RLA) avoidance rats: Behavioral, neuroendocrine and developmental aspects. Stress, 6, 87–100.CrossRefPubMed
Suenaga, T., Morinobu, S., Kawano, K., Sawada, T., & Yamawaki, S. (2004). Influence of immobilization stress on the levels of CaMKII and phospho-CaMKII in the rat hippocampus. International Journal of Neuropsychopharmacology, 3, 299–309.CrossRef
Sun, C. Y., Qi, S. S., Lou, X. F., Sun, S. H., Wang, X., Dai, K. Y., et al. (2006). Changes of learning, memory and levels of CaMKII, CaM mRNA, CREB mRNA in the hippocampus of chronic multiple-stressed rats. Chinese Medical Journal, 119(2), 140–147.PubMed
Thome, J., Pesold, B., Baader, M., Hu, M., Gewirtz, J. C., Duman, R. S., & Henn, F. A. (2001). Stress differentially regulates synaptophysin and synaptotagmin expression in hippocampus. Biological Psychiatry, 50(10), 809–812.CrossRefPubMed
Thome, J., Sakai, N., Shin, K., Steffen, C., Zhang, Y. J., Impey, S., et al. (2000). cAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment. Journal of Neuroscience, 20, 4030–4036.PubMed
Tokarev, D., & Jezova, D. (1997). Effect of central administration of the non-NMDA receptor antagonist DNQX on ACTH and corticosterone release before and during immobilization stress. Methods and Findings in Experimental and Clinical Pharmacology, 19, 323–328.PubMed
Ueyama, T., Kawai, Y., Nemoto, K., Sekimoto, M., Tone, S., & Senba, E. (1997). Immobilization stress reduced the expression of neurotrophins and their receptors in the rat brain. Neuroscience Research, 28, 103–110.CrossRefPubMed
Van Erp, A. M. M., Kruk, M. R., Meelis, W., & Willekens-Bramer, D. C. (1994). Effect of environmental stressors on time course, viability and form of self-grooming in the rat: handling, social contact, defeat, novelty, restraint and fur moistening. Behavioural Brain Research, 65, 47–55.CrossRefPubMed
Volbracht, C., van Beek, J., Zhu, C., Blomgren, K., & Leist, M. (2006). Neuroprotective properties of memantine in different in vitro and in vivo models of excitotoxicity. European Journal of Neuroscience, 23, 2611–2622.CrossRefPubMed
Wiedenmann, B., & Franke, W. W. (1985). Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell, 41, 1017–1028.CrossRefPubMed
Xu, H., He, J., Richardson, J. S., & Li, X. M. (2004). The response of synaptophysin and microtubule-associated protein 1 to restraint stress in rat hippocampus and its modulation by venlafaxine. Journal of Neurochemistry, 91(6), 1380–1388.CrossRefPubMed
Yan, Q., Radeke, M. J., Matheson, C. R., Talvenheimo, J., Welcher, A. A., & Feinstein, S. C. (1997). Immunocytochemical localization of TrkB in the central nervous system of the adult rat. Journal of Comparative Neurology, 378, 135–157.CrossRefPubMed
Yuen, E. Y., Liu, W., Karatsoreos, I. N., Feng, J., McEwen, B. S., & Yan, Z. (2013). Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proceedings of the National Academy of Sciences, 106(33), 14075–14079.
Zelena, D., Mergl, Z., & Makara, G. B. (2005). Glutamate agonists activate the hypothalamic-pituitary-adrenal axis through hypothalamic paraventricular nucleus but not through vasopressinerg neurons. Brain Research, 1031, 185–193.CrossRefPubMed
Zhang, L., Zhang, H. Q., Liang, X. Y., Zhang, H. F., Zhang, T., & Liu, F. E. (2013). Melatonin ameliorates cognitive impairment induced by sleep deprivation in rats: Role of oxidative stress. BDNF and CaMKII. Behaviour Brain Research, 256, 72–81.CrossRef
Metadata
Title
Modification of Hippocampal Markers of Synaptic Plasticity by Memantine in Animal Models of Acute and Repeated Restraint Stress: Implications for Memory and Behavior
Authors
Shaimaa Nasr Amin
Ahmed Amro El-Aidi
Mohamed Mostafa Ali
Yasser Mahmoud Attia
Laila Ahmed Rashed
Publication date
01-06-2015
Publisher
Springer US
Published in
NeuroMolecular Medicine / Issue 2/2015
Print ISSN: 1535-1084
Electronic ISSN: 1559-1174
DOI
https://doi.org/10.1007/s12017-015-8343-0

Other articles of this Issue 2/2015

NeuroMolecular Medicine 2/2015 Go to the issue

Original Paper

A Dual Inhibitor of Cyclooxygenase and 5-Lipoxygenase Protects Against Kainic Acid-Induced Brain Injury

Original Paper

Unfolding the Promise of Translational Targeting in Neurodegenerative Disease

Original Paper

The Domain II S4-S5 Linker in Nav1.9: A Missense Mutation Enhances Activation, Impairs Fast Inactivation, and Produces Human Painful Neuropathy

Erratum

Erratum to: Genetic Association Between KIBRA Polymorphism and Alzheimer’s Disease with in a Japanese Population

Original Paper

A Candidate Gene Association Study Identifies DAPL1 as a Female-Specific Susceptibility Locus for Age-Related Macular Degeneration (AMD)

Original Paper

Genetic Association Between KIBRA Polymorphism and Alzheimer’s Disease with in a Japanese Population