Generic placeholder image

Central Nervous System Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5249
ISSN (Online): 1875-6166

Research Article

Tianeptine Affects the Improvement of Behavioral Defects, such as Schizophrenia, Caused by Maternal Immune Activation in the Mice Offspring

Author(s): Kooseung Jung* and Jun-Tack Kwon

Volume 23, Issue 3, 2023

Published on: 07 September, 2023

Page: [157 - 166] Pages: 10

DOI: 10.2174/1871524923666230905142700

Price: $65

Abstract

Background: Simultaneously with studies on animal models of fetal-induced maternal immune activation, related studies documented behavior, neurophysiological, and/or neurochemical disorders observed in some neuropsychiatric disorders, including autism and schizophrenia.

Objective: To investigate whether treatment tianeptine might ameliorate maternal immune activation (MIA)-induced behavioral deficits in the offspring.

Materials and Methods: The pregnant mice were injected through tail vein injection at a concentration of 5 mg/kg of polyriboinosinic-polyribocytidilic acid (polyI:C) and/or used saline as a vehicle. The injection was performed on the 9th day of pregnancy. Each group of MIA offspring was subjected to vehicle, clozapine, or tianeptine treatment.

Results: In prepulse inhibition (PPI) test, oral treatment with tianeptine ameliorated MIA-induced sensorimotor gating deficit. Most behavioral parameters of social interaction test (SIT), forced swimming test (FST), and open field test (OFT) were significantly changed in the MIA offspring. Tianeptine treatment significantly recovered behavioral changes observed in the SIT, OFT, and FST. In order to confirm expression level of neurodevelopmental proteins, immunohistochemical image analysis and Western blot were performed, and the medial prefrontal cortex (mPFC) was targeted. As a result, it was confirmed that the neurodevelopmental proteins were decreased, which was recovered after administration of tianeptine to MIA offspring.

Conclusion: Tianeptine might be useful for treating psychiatric disorders with neurodevelopmental issues.

Graphical Abstract

[1]
McEwen BS, Chattarji S, Diamond DM, et al. The neurobiological properties of tianeptine (Stablon): From monoamine hypothesis to glutamatergic modulation. Mol Psychiatry 2010; 15(3): 237-49.
[http://dx.doi.org/10.1038/mp.2009.80]
[2]
Lucassen PJ, Fuchs E, Czéh B. Antidepressant treatment with tianeptine reduces apoptosis in the hippocampal dentate gyrus and temporal cortex. Biol Psychiatry 2004; 55(8): 789-96.
[http://dx.doi.org/10.1016/j.biopsych.2003.12.014]
[3]
Della FP, Abelaira HM, Réus GZ, et al. Tianeptine exerts neuroprotective effects in the brain tissue of rats exposed to the chronic stress model. Pharmacol Biochem Behav 2012; 103(2): 395-402.
[http://dx.doi.org/10.1016/j.pbb.2012.09.018]
[4]
Plaisant F, Dommergues MA, Spedding M, et al. Neuroprotective properties of tianeptine: Interactions with cytokines. Neuropharmacology 2003; 44(6): 801-9.
[http://dx.doi.org/10.1016/S0028-3908(03)00066-2]
[5]
Castanon N, Médina C, Mormède C, Dantzer R. Chronic administration of tianeptine balances lipopolysaccharide-induced expression of cytokines in the spleen and hypothalamus of rats. Psychoneuroendocrinology 2004; 29(6): 778-90.
[http://dx.doi.org/10.1016/S0306-4530(03)00142-2]
[6]
Janda E, Visalli V, Colica C, et al. The protective effect of tianeptine on Gp120-induced apoptosis in astroglial cells: Role of GS and NOS, and NF-κB suppression. Br J Pharmacol 2011; 164(6): 1590-9.
[http://dx.doi.org/10.1111/j.1476-5381.2010.01172.x]
[7]
Canetta S, Sourander A, Surcel HM, et al. Elevated maternal C-reactive protein and increased risk of schizophrenia in a national birth cohort. Am J Psychiatry 2014; 171(9): 960-8.
[http://dx.doi.org/10.1176/appi.ajp.2014.13121579]
[8]
Brown AS, Sourander A, Hinkka-Yli-Salomäki S, McKeague IW, Sundvall J, Surcel H-M. Elevated maternal C-reactive protein and autism in a national birth cohort. Mol Psychiatry 2014; 19(2): 259-64.
[http://dx.doi.org/10.1038/mp.2012.197]
[9]
Fatemi SH, Reutiman TJ, Folsom TD, Lee S. Phosphodiesterase-4A expression is reduced in cerebella of patients with bipolar disorder. Psychiatr Genet 2008; 18(6): 282-8.
[http://dx.doi.org/10.1097/YPG.0b013e3283060fb8]
[10]
Meyer U, Feldon J, Fatemi SH. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci Biobehav Rev 2009; 33(7): 1061-79.
[http://dx.doi.org/10.1016/j.neubiorev.2009.05.001]
[11]
Meyer U, Feldon J, Schedlowski M, Yee BK. Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neurosci Biobehav Rev 2005; 29(6): 913-47.
[http://dx.doi.org/10.1016/j.neubiorev.2004.10.012]
[12]
Braff DL, Geyer MA, Swerdlow NR. Human studies of prepulse inhibition of startle: Normal subjects, patient groups, and pharmacological studies. Psychopharmacology 2001; 156(2-3): 234-58.
[http://dx.doi.org/10.1007/s002130100810]
[13]
Piontkewitz Y, Arad M, Weiner I. Tracing the development of psychosis and its prevention: What can be learned from animal models. Neuropharmacology 2012; 62(3): 1273-89.
[http://dx.doi.org/10.1016/j.neuropharm.2011.04.019]
[14]
Meyer U, Spoerri E, Yee BK, Schwarz MJ, Feldon J. Evaluating early preventive antipsychotic and antidepressant drug treatment in an infection-based neurodevelopmental mouse model of schizophrenia. Schizophr Bull 2010; 36(3): 607-23.
[http://dx.doi.org/10.1093/schbul/sbn131]
[15]
Won H, Kim YO, Lee H. Effect of valeriana fauriei extract on the neurodevelopmental proteins expression and behavioral patterns in maternal immune activation animal model. Korean J Med Crop Sci 2016; 24(5): 341-50.
[16]
Kim HJ, Won H. Effects of Panax ginseng C.A. Meyer extract on the offspring of adult mice with maternal immune activation. Mol Med Rep 2018; 18(4): 3834-42.
[17]
Council NR. Guide for the care and use of laboratory animals. Washington, DC, USA: National Academy Press 1996; p. 22.
[18]
Lee H, Lee M, Kim HK, Kim YO, Kwon JT, Kim HJ. Influence of clozapine on neurodevelopmental protein expression and behavioral patterns in animal model of psychiatric disorder induced by low-level of lead. Korean J Physiol Pharmacol 2019; 23(6): 467-74.
[http://dx.doi.org/10.4196/kjpp.2019.23.6.467]
[19]
Meyer U, Feldon J. Neural basis of psychosis-related behaviour in the infection model of schizophrenia. Behav Brain Res 2009; 204(2): 322-34.
[http://dx.doi.org/10.1016/j.bbr.2008.12.022]
[20]
Kuipers SD, Trentani A, van der Zee EA, den Boer JA. Chronic stress-induced changes in the rat brain: Role of sex differences and effects of long-term tianeptine treatment. Neuropharmacology 2013; 75: 426-36.
[http://dx.doi.org/10.1016/j.neuropharm.2013.08.018]
[21]
Jantas D, Krawczyk S, Lason W. The predominant protective effect of tianeptine over other antidepressants in models of neuronal apoptosis: The effect blocked by inhibitors of MAPK/ERK1/2 and PI3-K/Akt pathways. Neurotox Res 2014; 25(2): 208-25.
[http://dx.doi.org/10.1007/s12640-013-9430-3]
[22]
Sanchez-Mateo CC, Darias V, Albertos LM, Exposito-Orta MA. Psychopharmacological effects of tianeptine analogoushetero [2,1] benzothiazepine derivatives. Arzneimittelforschung 2003; 53: 12-20.
[23]
Muniz PS, Nardi AE. Refractory pain-depression syndrome treated with tianeptine: A case report. Aust N Z J Psychiatry 2004; 38(3): 176.
[http://dx.doi.org/10.1111/j.1440-1614.2004.01328.x]
[24]
Castanon N, Konsman JP, Médina C, Chauvet N, Dantzer R. Chronic treatment with the antidepressant tianeptine attenuates lipopolysaccharide-induced Fos expression in the rat paraventricular nucleus and HPA axis activation. Psychoneuroendocrinology 2003; 28(1): 19-34.
[http://dx.doi.org/10.1016/S0306-4530(02)00005-7]
[25]
Bitanihirwe BKY, Peleg-Raibstein D, Mouttet F, Feldon J, Meyer U. Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Neuropsychopharmacology 2010; 35(12): 2462-78.
[http://dx.doi.org/10.1038/npp.2010.129]
[26]
Meyer U, Nyffeler M, Engler A, et al. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci 2006; 26(18): 4752-62.
[http://dx.doi.org/10.1523/JNEUROSCI.0099-06.2006]
[27]
Lee H, Joo J, Nah SS, et al. Changes in Dpysl2 expression are associated with prenatally stressed rat offspring and susceptibility to schizophrenia in humans. Int J Mol Med 2015; 35(6): 1574-86.
[http://dx.doi.org/10.3892/ijmm.2015.2161]
[28]
Nakata K, Ujike H, Sakai A, et al. The human dihydropyrimidinase-related protein 2 gene on chromosome 8p21 is associated with paranoid-type schizophrenia. Biol Psychiatry 2003; 53(7): 571-6.
[http://dx.doi.org/10.1016/S0006-3223(02)01729-8]
[29]
Czéh B, Michaelis T, Watanabe T, et al. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci 2001; 98(22): 12796-801.
[http://dx.doi.org/10.1073/pnas.211427898]
[30]
Powchik P, Davidson M, Haroutunian V, et al. Postmortem studies in schizophrenia. Schizophr Bull 1998; 24(3): 325-41.
[http://dx.doi.org/10.1093/oxfordjournals.schbul.a033330]
[31]
Lewis DA, Glantz LA, Pierri JN, Sweet RA. Altered cortical glutamate neurotransmission in schizophrenia: Evidence from morphological studies of pyramidal neurons. Ann N Y Acad Sci 2003; 1003(1): 102-12.
[http://dx.doi.org/10.1196/annals.1300.007]
[32]
Barros CS, Calabrese B, Chamero P, et al. Impaired maturation of dendritic spines without disorganization of cortical cell layers in mice lacking NRG1/ErbB signaling in the central nervous system. Proc Natl Acad Sci 2009; 106(11): 4507-12.
[http://dx.doi.org/10.1073/pnas.0900355106]
[33]
Pappas GD, Kriho V, Pesold C. Reelin in the extracellular matrix and dendritic spines of the cortex and hippocampus: A comparison between wild type and heterozygous reeler mice by immunoelectron microscopy. J Neurocytol 2002; 30(5): 413-25.
[http://dx.doi.org/10.1023/A:1015017710332]
[34]
Silva-Gómez AB, Rojas D, Juárez I, Flores G. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 2003; 983(1-2): 128-36.
[http://dx.doi.org/10.1016/S0006-8993(03)03042-7]
[35]
Wagstaff AJ, Ormrod D, Spencer CM. tianeptine. CNS Drugs 2001; 15(3): 231-59.
[http://dx.doi.org/10.2165/00023210-200115030-00006]
[36]
Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 2000; 57(1): 65-73.
[http://dx.doi.org/10.1001/archpsyc.57.1.65]
[37]
Rosoklija G, Toomayan G, Ellis SP, et al. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: Preliminary findings. Arch Gen Psychiatry 2000; 57(4): 349-56.
[http://dx.doi.org/10.1001/archpsyc.57.4.349]
[38]
Moyer CE, Shelton MA, Sweet RA. Dendritic spine alterations in schizophrenia. Neurosci Lett 2015; 601: 46-53.
[http://dx.doi.org/10.1016/j.neulet.2014.11.042]
[39]
Critchlow HM, Maycox PR, Skepper JN, Krylova O. Clozapine and haloperidol differentially regulate dendritic spine formation and synaptogenesis in rat hippocampal neurons. Mol Cell Neurosci 2006; 32: 356-65.
[http://dx.doi.org/10.1016/j.mcn.2006.05.007]
[40]
Law AJ, Harrison PJ. The distribution and morphology of prefrontal cortex pyramidal neurons identified using anti-neurofilament antibodies SMI32, N200 and FNP7. Normative data and a comparison in subjects with schizophrenia, bipolar disorder or major depression. J Psychiatr Res 2003; 37(6): 487-99.
[http://dx.doi.org/10.1016/S0022-3956(03)00075-X]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy