Cytoskeletal changes in the hippocampus following restraint stress. Role of serotonin and microtubules
Abstract
The aetiology of depression is associated with depletion in central levels of serotonin (5-HT). Hence, a major effect of antidepressant drugs is to increase synaptic 5-HT levels. Stressful conditions have also been shown to affect neuronal plasticity and 5-HT neurotransmission in the hippocampus. Neuronal plasticity, which is typically referred to as a structural adaptation of neurons to functional requirements, requires more dynamic forms of microtubules (cytoskeletal component). The alpha-tubulin, which is the major component of microtubules, can be postranslationally modified and both the tyrosinated (tyr-tub) and acetylated (acet-tub) forms are considered markers of more dynamic or more stable microtubules, respectively. The aim of the present work was to investigate the expression of tyr-tub and acet-tub in the hippocampus of rats submitted to either acute (6 h for 1 day) or sub-chronic (6 h for 4 days every day) restraint stress. In addition, ex vivo hippocampal 5-HT levels were monitored by differential pulse voltammetry to analyse the influence of both stress conditions upon 5-HT levels. Our results showed that the expression of tyr-tub in the hippocampus was significantly decreased to 70 +/- 7% following sub-chronic restraint stress (P < 0.01). In contrast, acute and sub-chronic restraint stress increased the hippocampal expression of acet-tub to 139 +/- 11% and 145 +/- 11% of control, respectively. Finally, 5-HT levels were significantly increased (P < 0.05) to 142 +/- 15% and 135 +/- 11% following acute and sub-chronic restraint stress, respectively. The stress-induced cytoskeletal changes observed in the present study suggest that the microtubular network is a potential new pathway that may increase our understanding of stress-related events.
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Remodeling of hippocampal neurons by chronic stress and hibernation alters the acetylation of microtubule subunits that is consistent with a more stable cytoskeleton.
“the remodeling of hippocampal neurons by chronic stress and hibernation alters the acetylation of microtubule subunits that is consistent with a more stable cytoskeleton (Bianchi et al., 2003)”
From Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators (2008) · cites this paper as Bianchi et al., 2003
Cites
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
LAEMMLI, U. K. (1970) · Nature · doi:10.1038/227680a0 · Cited by 249,961 · see citing works
Murray, C. J. L., & López, A. D. (1997) · The Lancet · doi:10.1016/s0140-6736(96)07492-2 · Cited by 7,007 · see citing works
STRESS AND HIPPOCAMPAL PLASTICITY
McEwen, B. S. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.105 · Cited by 2,087 · see citing works
Glucocorticoids and Hippocampal Atrophy in Neuropsychiatric Disorders
Sapolsky, R. M. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.10.925 · Cited by 2,016 · see citing works
Transduction of psychosocial stress into the neurobiology of recurrent affective disorder
(1992) · American Journal of Psychiatry · doi:10.1176/ajp.149.8.999 · Cited by 1,848 · see citing works
Current advances and trends in the treatment of depression
Blier, P., & de Montigny, C. (1994) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(94)90315-8 · Cited by 1,113 · see citing works
Czéh, B., Michaelis, T., Watanabe, T., Frahm, J., de Biurrun, G., van Kampen, M., Bartolomucci, A., & Fuchs, E. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.211427898 · Cited by 1,090 · see citing works
Woolley, C. S., Gould, E., & McEwen, B. S. (1990) · Brain Research · doi:10.1016/0006-8993(90)90778-a · Cited by 1,020 · see citing works
Friston, K. J. (1998) · Schizophrenia Research · doi:10.1016/s0920-9964(97)00140-0 · Cited by 882 · see citing works
Magariños, A. M., McEwen, B. S., Flügge, G., & Fuchs, E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03534.1996 · Cited by 864 · see citing works
Magarin˜os, A. M., & McEwen, B. S. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00259-l · Cited by 863 · see citing works
Neuronal plasticity and survival in mood disorders
Duman, R. S., Malberg, J., Nakagawa, S., & D’Sa, C. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00935-5 · Cited by 652 · see citing works
Effects of adverse experiences for brain structure and function
McEwen, B. S. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00964-1 · Cited by 639 · see citing works
Azmitia, E. C. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00614-1 · Cited by 497 · see citing works
Wagstaff, A. J., Ormrod, D. J., & Spencer, C. M. (2001) · CNS Drugs · doi:10.2165/00023210-200115030-00006 · Cited by 395 · see citing works
Magariños, A. M., Deslandes, A., & McEwen, B. S. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00163-6 · Cited by 330 · see citing works
Serotonin, stress and corticoids
Chaouloff, F. (2000) · Journal of Psychopharmacology · doi:10.1177/026988110001400203 · Cited by 315 · see citing works
Gundersen, G. G., Khawaja, S., & Bulinski, J. C. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.1.251 · Cited by 309 · see citing works
Tubulin Post‐Translational Modifications
MacRae, T. H. (1997) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1997.00265.x · Cited by 291 · see citing works
Maris, R. W. (2002) · The Lancet · doi:10.1016/s0140-6736(02)09556-9 · Cited by 260 · see citing works
Possible mechanisms for atrophy of the human hippocampus
McEwen, B. S. (1997) · Molecular Psychiatry · doi:10.1038/sj.mp.4000254 · Cited by 243 · see citing works
Adell, A., CASANOVAS, J. M., & Artigas, F. (1997) · Neuropharmacology · doi:10.1016/s0028-3908(97)00048-8 · Cited by 229 · see citing works
The multitubulin hypothesis revisited: what have we learned?
Cleveland, D. W. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.104.3.381 · Cited by 215 · see citing works
Cambray-Deakin, M. A., & Burgoyne, R. D. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.104.6.1569 · Cited by 172 · see citing works
Magariños, A. M., Orchinik, M., & McEwen, B. S. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00882-8 · Cited by 163 · see citing works
Amat, J., Matus-Amat, P., Watkins, L. R., & Maier, S. F. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00368-0 · Cited by 158 · see citing works
Kennett, G. A., & Joseph, M. H. (1981) · Neuropharmacology · doi:10.1016/0028-3908(81)90039-3 · Cited by 148 · see citing works
Wright, I. K., Upton, N., & Marsden, C. A. (1992) · Psychopharmacology · doi:10.1007/bf02245882 · Cited by 135 · see citing works
Second Messenger‐Regulated Protein Kinases in the Brain
Popoli, M., Brunello, N., Pérez, J., & Racagni, G. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0740021.x · Cited by 122 · see citing works
Microtubule stability decreases axon elongation but not axoplasm production
Rochlin, M. W., Wickline, K. M., & Bridgman, P. C. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03236.1996 · Cited by 117 · see citing works
Vahabzadeh, A., & Fillenz, M. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00619.x · Cited by 117 · see citing works
Kuroda, Y., & McEwen, B. S. (1998) · Molecular Brain Research · doi:10.1016/s0169-328x(98)00130-2 · Cited by 114 · see citing works
Mueller, G. P., Twohy, C. P., Chen, H. T., Advis, J. P., & Meites, J. (1976) · Life Sciences · doi:10.1016/0024-3205(76)90183-1 · Cited by 109 · see citing works
Crespi, F., Martin, K. F., & Marsden, C. A. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90191-1 · Cited by 106 · see citing works
Massot, O., Rousselle, J. C., Fillion, M. P., Grimaldi, B., Cloëz-Tayarani, I., Fugelli, A., Prudhomme, N., Seguin, L., Rousseau, B., Plantefol, M., et al. (1996) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)09375-7 · Cited by 88 · see citing works
Cumming, R., Burgoyne, R. D., & Lytton, N. A. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.98.1.347 · Cited by 82 · see citing works
In vivo voltammetry with micro-biosensors for analysis of neurotransmitter release and metabolism
Crespi, F. (1990) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(90)90042-e · Cited by 66 · see citing works
Thorré, K., Chaouloff, F., Sarre, S., MEEUSEN, R. R., Ebinger, G., & Michotte, Y. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00841-x · Cited by 63 · see citing works
Are ω3 Fatty Acids Beneficial in Depression but Not Mania?
Su, K., Shen, W. W., & Huang, S. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.7.716 · Cited by 61 · see citing works
Bolaños, F. J., Manhães‐de‐Castro, R., Seguin, L., Cloëz-Tayarani, I., Monneret, V., Drieu, K., & Fillion, G. (1995) · European Journal of Pharmacology · doi:10.1016/0014-2999(95)00590-0 · Cited by 60 · see citing works
Effect of Stress on Serotonin Concentration and Tryptophan Hydroxylase Activity of Brain Nuclei
Palkovits, M., Brownstein, M. J., Kizer, J. S., Saavedra, J. M., & Kopin, I. J. (2008) · Neuroendocrinology · doi:10.1159/000122638 · Cited by 55 · see citing works
Social interaction increases 5-HT release and cAMP efflux in the rat ventral hippocampus in vivo
Cadogan, A., Kendall, D. A., Fink, H., & Marsden, C. A. (1994) · Behavioural Pharmacology · doi:10.1097/00008877-199406000-00007 · Cited by 38 · see citing works
Differential influences of different stressors upon midbrain raphe neurons in rats
Lee, E. H. Y., Lin, H. H., & Yin, H. M. (1987) · Neuroscience Letters · doi:10.1016/0304-3940(87)90506-4 · Cited by 27 · see citing works
Seguin, L., Seznec, J.-C., & Fillion, G. (1997) · Neuroscience Research · doi:10.1016/s0168-0102(96)01150-9 · Cited by 26 · see citing works
Characteristics of Microtubules at the Different Stages of Neuronal Differentiation and Maturation
Meininger, V., & Binet, S. (1989) · International review of cytology · doi:10.1016/s0074-7696(08)60858-x · Cited by 24 · see citing works
Bonnin, A., Grimaldi, B., Fillion, M., & Fillion, G. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01265-2 · Cited by 20 · see citing works
In vivo voltammetric methods for monitoring monoamine release and metabolism
Stamford, J., Crespi, F., & Marsden, C. A. (1992) · doi:10.1093/oso/9780199632442.003.0005 · Cited by 16 · see citing works
Contin, M. A., & Arce, C. A. (2000) · Neurochemical Research · doi:10.1023/a:1007579113813 · Cited by 13 · see citing works
The receptor tyrosine phosphatase CRYP? affects growth cone morphology
Mueller, B. K., Ledig, M. M., & Wahl, S. (2000) · Journal of Neurobiology · doi:10.1002/1097-4695(200008)44:2 · Cited by 12 · see citing works
Farina, Zedda, M., Bianchi, M., Marongiu, P., & Pl, D. R. (1999) · PubMed · Cited by 12 · see citing works
Aluminum promotes neuronal plasticity events in a mouse neuroblastoma cell line
Farina, V., Tapparo, A., Zedda, M., Gadau, S. D., & Lepore, G. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)02179-6 · Cited by 8 · see citing works
Serotonin and neuronal plasticity relationship: A new mechanism involved in depression?
Crespi, F., & Bianchi, M. (2002) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(02)80176-6 · Cited by 4 · see citing works
Expression of the microtubule‐associated protein stop in oligodendrocytes
Galiano, M. R., Soto, E. F., Pasquini, J. M., & Hallak, M. E. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.81.s1.21_4.x · Cited by 1 · see citing works
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Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · see citing works
McEwen, B. S. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.071 · Cited by 1,864 · see citing works
McEwen, B. S., & Gianaros, P. J. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05331.x · Cited by 1,715 · see citing works
Protective and damaging effects of stress mediators: central role of the brain
McEwen, B. S. (2006) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2006.8.4/bmcewen · Cited by 1,220 · see citing works
Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling
McEwen, B. S. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05568.x · Cited by 335 · see citing works
Repeated stress and structural plasticity in the brain
Radley, J. J., & Morrison, J. H. (2005) · Ageing Research Reviews · doi:10.1016/j.arr.2005.03.004 · Cited by 241 · see citing works
Fogaça, M. V., Campos, A. C., Coelho, L. D., Duman, R. S., & Guimarães, F. S. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.03.001 · Cited by 208 · see citing works
Depression after status epilepticus: behavioural and biochemical deficits and effects of fluoxetine
Mazarati, A., Siddarth, P., Baldwin, R. A., Shin, D., Caplan, R., & Sankar, R. (2008) · Brain · doi:10.1093/brain/awn117 · Cited by 202 · see citing works
Bianchi, M., Fone, K. C. F., Azmi, N., Heidbreder, C. A., Hagan, J. J., & Marsden, C. A. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05170.x · Cited by 191 · see citing works
The ever‐changing brain: Cellular and molecular mechanisms for the effects of stressful experiences
McEwen, B. S. (2012) · Developmental Neurobiology · doi:10.1002/dneu.20968 · Cited by 165 · see citing works
Remodeling of neuronal networks by stress
Fuchs, E. (2006) · Frontiers in bioscience · doi:10.2741/2004 · Cited by 127 · see citing works
Microtubule and microtubule associated protein anomalies in psychiatric disease
Marchisella, F., Coffey, E. T., & Hollós, P. (2016) · Cytoskeleton · doi:10.1002/cm.21300 · Cited by 122 · see citing works
Posttranslational modifications of α-tubulin in alzheimer disease
Zhang, F., Su, B., Wang, C., Siedlak, S. L., Mondragón‐Rodríguez, S., Lee, H., Wang, X., Perry, G. L., & Zhu, X. (2015) · Translational Neurodegeneration · doi:10.1186/s40035-015-0030-4 · Cited by 116 · see citing works
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Kroes, R. A., Panksepp, J., Burgdorf, J. S., Otto, N. J., & Moskal, J. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.076 · Cited by 101 · see citing works
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Alfonso, J., Frasch, A. C. C., & Flügge, G. (2005) · Reviews in the Neurosciences · doi:10.1515/revneuro.2005.16.1.43 · Cited by 80 · see citing works
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Priel, A., Tuszyński, J. A., & Woolf, N. J. (2009) · Journal of Biological Physics · doi:10.1007/s10867-009-9153-0 · Cited by 79 · see citing works
Yang, C., Wang, G., Wang, H., Liu, Z., & Wang, X. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.08.008 · Cited by 66 · see citing works
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Xu, H., He, J., Richardson, J. S., & Li, X. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02827.x · Cited by 61 · see citing works
Fluoxetine administration modulates the cytoskeletal microtubular system in the rat hippocampus
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Wong, G. T.-H., Chang, R. C., & Law, A. C.-K. (2012) · Ageing Research Reviews · doi:10.1016/j.arr.2012.08.004 · Cited by 56 · see citing works
McEwen, B. S. (2004) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2004.6.2/bmcewen · Cited by 54 · see citing works
Piubelli, C., Carboni, L., Becchi, S., Mathé, A. A., & Domenici, E. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.12.043 · Cited by 53 · see citing works
Ladurelle, N., Gabriel, C., Viggiano, A., Mocaër, E., Baulieu, E. E., & Bianchi, M. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2597-5 · Cited by 52 · see citing works
Lin, Y., Westenbroek, C., Bakker, P. L., Termeer, J., Liu, A., Li, X., & Horst, G. J. T. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn035 · Cited by 48 · see citing works
Fluoxetine-induced up-regulation of 14-3-3zeta and tryptophan hydroxylase levels in RBL-2H3 cells
Baik, S.-Y., Jung, K. H., Choi, M., Yang, B., Kim, S. H., Lee, J., Oh, D.-Y., Choi, I.-G., Chung, H., & Chai, Y. G. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.10.047 · Cited by 46 · see citing works
Jensen, S. K. G., Pangelinan, M., Björnholm, L., Klasnja, A., Leemans, A., Drakesmith, M., Evans, C. J., Barker, E. D., & Paus, T. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2017.10.033 · Cited by 44 · see citing works
Changes in tau phosphorylation levels in the hippocampus and frontal cortex following chronic stress
Yang, C., Guo, X.-L., Wang, G. H., Wang, H., Liu, Z. C., Liu, H., Zhu, Z., & Li, Y. (2014) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x20133275 · Cited by 40 · see citing works
Neurological Complications of Conventional and Novel Anticancer Treatments
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Park, S. H., Jang, S., Lee, S. W., Park, S., Sung, Y.-Y., & Kim, H. K. (2018) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2018.04.010 · Cited by 38 · see citing works
Deceivingly dynamic: Learning-dependent changes in stathmin and microtubules
Uchida, S., & Shumyatsky, G. P. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.07.011 · Cited by 36 · see citing works
Ejchel-Cohen, T. F., Wood, G. E., Wang, J., Barlow, K. B. L., Nóbrega, J. N., McEwen, B. S., & Young, L. T. (2006) · Brain Research · doi:10.1016/j.brainres.2006.03.062 · Cited by 36 · see citing works
Iliev, A. I., Djannatian, J. R., Opazo, F., Gerber, J., Nau, R., Mitchell, T. J., & Wouters, F. S. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06538.x · Cited by 35 · see citing works
Bio Molecular Considerations in Major Depression and Ischemic Cardiovascular Disease
Cocchi, M., & Tonello, L. (2010) · Central Nervous System Agents in Medicinal Chemistry · doi:10.2174/187152410791196378 · Cited by 33 · see citing works
Singh, H., Wray, N. H., Schappi, J. M., & Rasenick, M. M. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0016-x · Cited by 33 · see citing works
RetractedBianchi, M., Fone, K. C. F., Shah, A. J., Atkins, A. R., Dawson, L. A., Heidbreder, C. A., Hagan, J. J., & Marsden, C. A. (2009) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.06.005 · Cited by 29 · see citing works
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Proteomic investigation of the prefrontal cortex in the rat clomipramine model of depression
Gellén, B., Völgyi, K., Györffy, B. A., Darula, Z., Hunyadi‐Gulyás, É., Baracskay, P., Czurkó, A., Hernádi, I., Juhász, G. D., Dobolyi, Á., et al. (2016) · Journal of Proteomics · doi:10.1016/j.jprot.2016.06.027 · Cited by 23 · see citing works
Human depression: a new approach in quantitative psychiatry
Cocchi, M., Tonello, L., & Rasenick, M. M. (2010) · Annals of General Psychiatry · doi:10.1186/1744-859x-9-25 · Cited by 22 · see citing works
Progesterone and fluoxetine treatments of postpartum depressive‐like behavior in rat model
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Barbiero, I., Bianchi, M., & Kilstrup‐Nielsen, C. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.13033 · Cited by 16 · see citing works
Čolić, L., McDonnell, C., Li, M., Woelfer, M., Liebe, T., Kretzschmar, M., Speck, O., Schott, B. H., Bianchi, M., & Walter, M. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.10.021 · Cited by 15 · see citing works
Xiang, D., Sun, S., Wang, G., & Liu, Z. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.644663 · Cited by 14 · see citing works
Pangratz-Fuehrer, S., Bubna‐Littitz, H., Propst, F., & Reitsamer, H. A. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.018 · Cited by 14 · see citing works
Yao, L., Chen, J., Chen, H., Xiang, D., Yang, C., Xiao, L., Liu, W., Wang, H., Wang, G., Zhu, F., et al. (2016) · Europe PMC (PubMed Central) · Cited by 13 · see citing works
Sun, L., Wang, G., Wu, Z., Xie, Y., Zhou, L., Xiao, L., & Wang, H. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2021.173285 · Cited by 14 · see citing works
Raftogianni, A., Stamatakis, A., Papadopoulou, A., Vougas, K. N., Anagnostopoulos, A. K., Stylianopoulou, F., & Tsangaris, G. T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048337 · Cited by 10 · see citing works
Eskandari‐Sedighi, G., Riazi, G. H., Mahdavi, M. R. V., Cheraghi, T., Atarod, D., & Rafiei, S. (2014) · Journal of Molecular Neuroscience · doi:10.1007/s12031-014-0394-4 · Cited by 10 · see citing works
Possible target-related proteins of stress-resistant rats suggested by label-free proteomic analysis
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Woolf, N. J., Priel, A., & Tuszyński, J. A. (2009) · Biological and medical physics series · doi:10.1007/978-3-642-03584-5_5 · Cited by 8 · see citing works
Maltby, C. J., Klein, A. K., Paschen, E., Pinto, J., Dvořák, D., Hedde, J. R., Hanks, A. N., Bianchi, M., & Hughes, Z. A. (2026) · Journal of Psychopharmacology · doi:10.1177/02698811251395386 · Cited by 6 · see citing works
Sántha, P., Pákáski, M., Fodor, E. K., Fazekas, Ö. C., Kálmán, S., Kalman, J. L., Janka, Z., Szabó, G., & Kalman, J. L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073504 · Cited by 6 · see citing works
Chronic MAP4343 reverses escalated alcohol drinking in a mouse model of alcohol use disorder
Macedo, G. C., Kreifeldt, M., Goulding, S. P., Okhuarobo, A., Sidhu, H., & Contet, C. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01529-z · Cited by 6 · see citing works
Remodeling of Neural Networks by Stress
Czéh, B., & Fuchs, E. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-800951-2.00014-5 · Cited by 3 · see citing works
Evaluation of Antidepressant Effects of Zhuyeqing Liquor Using C. elegans as a Model
Cui, X., Shen, J., Yan, J., Li, C., Li, J., & Li, F. (2025) · Food Science & Nutrition · doi:10.1002/fsn3.71349 · Cited by 2 · see citing works
Tomàs-Roig, J., Ramasamy, S. S., Zbarsky, D., Havemann‐Reinecke, U., & Hoyer‐Fender, S. (2022) · PLoS ONE · doi:10.1371/journal.pone.0274352 · Cited by 1 · see citing works
Effects of Social Defeat Stress on Microtubule Regulating Proteins and Tubulin Polymerization
Le, T.-H., Oh, J.-M., Rami, F. Z., Li, L., Chun, S., & Chung, Y. (2023) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.23.1077 · Cited by 1 · see citing works
Argumedo, G. S., Ávila, M. A. M., Peraza, A. V., Zavala, M. A. G., Rojas, L., Gerardo, M., & Mejía, G. B. (2007)
The Effect of Exercise and Stress on Neurodegeneration in the Mouse Hippocampus
Kolobova, A., Fincher, D., & Patel, G. B. (2009)
Role of glutamate in neurodegenerative changes in the hippocampus caused by stress
Zach, P., Mrzílková, J., & Valeš, K. (2010) · Kontakt · doi:10.32725/kont.2010.012
Crespi, F. (2020) · Biomedical Journal of Scientific & Technical Research · doi:10.26717/bjstr.2020.30.004940
Cocchi, M., Tonello, L., & Gabrielli, F. (2014) · Open Journal of Depression · doi:10.4236/ojd.2014.31003
Arikawe, A. P., Oghene, O., Olusanya, A. W., Olumide, O., Dawodu, O. O., Babafemi, P., & Jaja, S. (2022) · African Journal of Endocrinology and Metabolism · doi:10.4103/ajem.ajem_2_23
Le, T.-H., Li, L., Rami, F. Z., Oh, J.-M., Chun, S., & Chung, Y. (2024) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.24.1212
Long, J.-D., Yao, S.-Y., Wu, W., Zan, G., Wang, Z.-W., Wei, X., Shu, X., Chen, Y., Ju, Y., Chen, J., et al. (2026) · Biological Psychiatry · doi:10.1016/j.biopsych.2026.06.001
Hu, T., Yan, L., Huang, C., Zhang, H., Guo, Y., Zhang, W. X., & Jiang, C. (2026) · Journal of Translational Internal Medicine · doi:10.1515/jtim-2026-0033
- Authors
- Bianchi, M., Heidbreder, C., & Crespi, F.
- Affiliations
- GlaxoSmithKline (Italy) (IT)
- Corresponding author
- Bianchi, Massimiliano
- Venue
- Synapse
- Publisher
- Wiley
- Published
- 2003-05-23
- Volume
- 49
- Issue
- 3
- Pages
- 188-194
- ISSN
- 0887-4476 (ISSN-L)
- 1098-2396
- OpenAlex
- W1969328491
- Cited by
- 72
- References
- 53
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 3 · 2021: 4 · 2020: 1 · 2019: 1 · 2018: 4 · 2017: 2 · 2016: 4 · 2015: 5 · 2014: 5 · 2013: 1 · 2012: 2
- FWCI
- 1.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Synapse (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- restraint stress, hippocampus, serotonin, microtubules, alpha-tubulin, tyrosinated tubulin, acetylated tubulin, cytoskeleton, neuroplasticity, depression, chronic stress, acute stress, serotonin levels
- MeSH terms
- Animals, Cytoskeleton, Hippocampus, Male, Microtubules, Restraint, Physical, Serotonin, Stress, Physiological, Blotting, Western, Rats, Wistar, Rats
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