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Neonatal Exposure to Bacterial Lipopolysaccharide Affects Behavior and Expression of Ionotropic Glutamate Receptors in the Hippocampus of Adult Rats after Psychogenic Trauma

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Abstract

According to the two-hit hypothesis of psychoneuropathology formation, infectious diseases and other pathological conditions occurring during the critical periods of early ontogenesis disrupt normal brain development and increase its susceptibility to stress experienced in adolescence and adulthood. It is believed that these disorders are associated with changes in the functional activity of the glutamatergic system in the hippocampus. Here, we studied expression of NMDA (GluN1, GluN2a, GluN2b) and AMPA (GluA1, GluA2) glutamate receptor subunits, as well as glutamate transporter EAAT2, in the ventral and dorsal regions of the hippocampus of rats injected with LPS during the third postnatal week and then subjected to predator stress (contact with a python) in adulthood. The tests were performed 25 days after the stress. It was found that stress altered protein expression in the ventral, but not in the dorsal hippocampus. Non-stressed LPS-treated rats displayed lower levels of the GluN2b protein in the ventral hippocampus vs. control animals. Stress significantly increased the content of GluN2b in the LPS-treated rats, but not in the control animals. Stress also affected differently the exploratory behavior of LPS-injected and control rats. Compared to the non-stressed animals, stressed control rats demonstrated a higher locomotor activity during the 1st min of the open field test, while the stressed LPS-injected rats displayed lower locomotor activity than the non-stressed rats. In addition, LPS-treated stressed and non-stressed rats spent more time in the open arms of the elevated plus maze and demonstrated reduced blood levels of corticosterone. To summarize the results of our study, exposure to bacterial LPS in the early postnatal ontogenesis affects the pattern of stress-induced changes in the behavior and hippocampal expression of genes coding for ionotropic glutamate receptor subunits after psychogenic trauma suffered in adulthood.

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Abbreviations

AMPA:

α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

EAAT2:

excitatory amino acid transporter 2

EPMT:

elevated plus maze test

LPS:

lipopolysaccharide, endotoxin

NMDA:

N-methyl-D-aspartate

OFT:

open field test

PTSD:

post-traumatic stress disorder

References

  1. Lee, R. S., Oswald, L. M., and Wand, G. S. (2018) Early life stress as a predictor of co-occurring alcohol use disorder and post-traumatic stress disorder, Alcohol. Res., 39, 147-159.

    PubMed  PubMed Central  Google Scholar 

  2. Fisher, P. A., Beauchamp, K. G., Roos, L. E., Noll, L. K., Flannery, J., and Delker, B. C. (2016) The neurobiology of intervention and prevention in early adversity, Annu. Rev. Clin. Psychol., 12, 331-357, https://doi.org/10.1146/annurev-clinpsy-032814-112855.

    Article  PubMed  Google Scholar 

  3. Van Camp, G., Cigalotti, J., Bouwalerh, H., Mairesse, J., Gatta, E., et al. (2018) Consequences of a double hit of stress during the perinatal period and midlife in female rats: mismatch or cumulative effect? Psychoneuroendocrinology, 93, 45-55, https://doi.org/10.1016/j.psyneuen.2018.04.004.

    Article  PubMed  Google Scholar 

  4. Jaric, I., Rocks, D., Cham, H., Herchek, A., and Kundakovic, M. (2019) Sex and estrous cycle effects on anxiety- and depression-related phenotypes in a two-hit developmental stress model, Front. Mol. Neurosci., 12, 74, https://doi.org/10.3389/fnmol.2019.00074.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Koss, K. J., and Gunnar, M. R. (2018) Annual research review: early adversity, the hypothalamic-pituitary-adrenocortical axis, and child psychopathology, J. Child Psychol. Psychiatry, 59, 327-346, https://doi.org/10.1111/jcpp.12784.

    Article  PubMed  Google Scholar 

  6. Dinel, A.-L., Joffre, C., Trifilieff, P., Aubert, A., Foury, A., Le Ruyet, P., and Layé, S. (2014) Inflammation early in life is a vulnerability factor for emotional behavior at adolescence and for lipopolysaccharide-induced spatial memory and neurogenesis alteration at adulthood, J. Neuroinflammation, 11, 155, https://doi.org/10.1186/s12974-014-0155-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Doenni, V. M., Song, C. M., Hill, M. N., and Pittman, Q. J. (2017) Early-life inflammation with LPS delays fear extinction in adult rodents, Brain. Behav. Immun., 63, 176-185, https://doi.org/10.1016/j.bbi.2016.11.022.

    Article  CAS  PubMed  Google Scholar 

  8. Lei, Y., Chen, C.-J., Yan, X.-X., Li, Z., and Deng, X.-H. (2017) Early-life lipopolysaccharide exposure potentiates forebrain expression of NLRP3 inflammasome proteins and anxiety-like behavior in adolescent rats, Brain Res., 1671, 43-54, https://doi.org/10.1016/j.brainres.2017.06.014.

    Article  CAS  PubMed  Google Scholar 

  9. Trofimov, A., Strekalova, T., Mortimer, N., Zubareva, O., Schwarz, A., et al. (2017) Postnatal LPS challenge impacts escape learning and expression of plasticity factors Mmp9 and Timp1 in rats: effects of repeated training, Neurotox. Res., 32, 175-186, https://doi.org/10.1007/s12640-017-9720-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Trofimov, A. N., Rotov, A. Y., Veniaminova, E. A., Fomalont, K., Schwarz, A. P., and Zubareva, O. E. (2020) Changes in behavior and the expression of ionotropic glutamate receptor genes in the brains of adult rats after neonatal administration of bacterial lipopolysaccharide, Neurosci. Behav. Physiol., 50, 1239-1248, https://doi.org/10.1007/s11055-020-01025-7.

    Article  CAS  Google Scholar 

  11. Zubareva, O. E., Postnikova, T. Y., Grifluk, A. V., Schwarz, A. P., Smolensky, I. V., et al. (2020) Exposure to bacterial lipopolysaccharide in early life affects the expression of ionotropic glutamate receptor genes and is accompanied by disturbances in long-term potentiation and cognitive functions in young rats, Brain. Behav. Immun., 90, 3-15, https://doi.org/10.1016/j.bbi.2020.07.034.

    Article  CAS  PubMed  Google Scholar 

  12. Walker, A. K., Nakamura, T., Byrne, R. J., Naicker, S., Tynan, R. J., et al. (2009) Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: implications for the double-hit hypothesis, Psychoneuroendocrinology, 34, 1515-1525, https://doi.org/10.1016/j.psyneuen.2009.05.010.

    Article  CAS  PubMed  Google Scholar 

  13. Walker, A. K., Nakamura, T., and Hodgson, D. M. (2010) Neonatal lipopolysaccharide exposure alters central cytokine responses to stress in adulthood in Wistar rats, Stress, 13, 506-515, https://doi.org/10.3109/10253890.2010.489977.

    Article  CAS  PubMed  Google Scholar 

  14. Harré, E.-M., Galic, M. A., Mouihate, A., Noorbakhsh, F., and Pittman, Q. J. (2008) Neonatal inflammation produces selective behavioural deficits and alters N-methyl-D-aspartate receptor subunit mRNA in the adult rat brain, Eur. J. Neurosci., 27, 644-653, https://doi.org/10.1111/j.1460-9568.2008.06031.x.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hansen, K. B., Yi, F., Perszyk, R. E., Furukawa, H., Wollmuth, L. P., et al. (2018) Structure, function, and allosteric modulation of NMDA receptors, J. Gen. Physiol., 150, 1081-1105, https://doi.org/10.1085/jgp.201812032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Liu, S., Lau, L., Wei, J., Zhu, D., Zou, S., et al. (2004) Expression of Ca2+-permeable AMPA receptor channels primes cell death in transient forebrain ischemia, Neuron, 43, 43-55, https://doi.org/10.1016/j.neuron.2004.06.017.

    Article  PubMed  Google Scholar 

  17. Wenzel, A., Fritschy, J. M., Mohler, H., and Benke, D. (1997) NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins, J. Neurochem., 68, 469-478, https://doi.org/10.1046/j.1471-4159.1997.68020469.x.

    Article  CAS  PubMed  Google Scholar 

  18. Babb, T. L., Mikuni, N., Najm, I., Wylie, C., Olive, M., et al. (2005) Pre- and postnatal expressions of NMDA receptors 1 and 2B subunit proteins in the normal rat cortex, Epilepsy Res., 64, 23-30, https://doi.org/10.1016/j.eplepsyres.2005.02.008.

    Article  CAS  PubMed  Google Scholar 

  19. Du Bois, T. M., and Huang, X.-F. (2007) Early brain development disruption from NMDA receptor hypofunction: relevance to schizophrenia, Brain Res. Rev., 53, 260-270, https://doi.org/10.1016/j.brainresrev.2006.09.001.

    Article  CAS  PubMed  Google Scholar 

  20. Lippman-Bell, J. J., Zhou, C., Sun, H., Feske, J. S., and Jensen, F. E. (2016) Early-life seizures alter synaptic calcium-permeable AMPA receptor function and plasticity, Mol. Cell. Neurosci., 76, 11-20, https://doi.org/10.1016/j.mcn.2016.08.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Yuan, T., and Bellone, C. (2013) Glutamatergic receptors at developing synapses: the role of GluN3A-containing NMDA receptors and GluA2-lacking AMPA receptors, Eur. J. Pharmacol., 719, 107-111, https://doi.org/10.1016/j.ejphar.2013.04.056.

    Article  CAS  PubMed  Google Scholar 

  22. Sweatt, J. D. (2016) Neural plasticity and behavior – sixty years of conceptual advances, J. Neurochem., 139, 179-199, https://doi.org/10.1111/jnc.13580.

    Article  CAS  PubMed  Google Scholar 

  23. Diering, G. H., and Huganir, R. L. (2018) The AMPA receptor code of synaptic plasticity, Neuron, 100, 314-329, https://doi.org/10.1016/j.neuron.2018.10.018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lisman, J. (2017) Glutamatergic synapses are structurally and biochemically complex because of multiple plasticity processes: long-term potentiation, long-term depression, short-term potentiation and scaling, Philos. Trans. R. Soc. Lond. B Biol. Sci., 372, https://doi.org/10.1098/rstb.2016.0260.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sarantis, K., Antoniou, K., Matsokis, N., and Angelatou, F. (2012) Exposure to novel environment is characterized by an interaction of D1/NMDA receptors underlined by phosphorylation of the NMDA and AMPA receptor subunits and activation of ERK1/2 signaling, leading to epigenetic changes and gene expression in rat hippocampus, Neurochem. Int., 60, 55-67, https://doi.org/10.1016/j.neuint.2011.10.018.

    Article  CAS  PubMed  Google Scholar 

  26. Barkus, C., McHugh, S. B., Sprengel, R., Seeburg, P. H., Rawlins, J. N. P., and Bannerman, D. M. (2010) Hippocampal NMDA receptors and anxiety: at the interface between cognition and emotion, Eur. J. Pharmacol., 626, 49-56, https://doi.org/10.1016/j.ejphar.2009.10.014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Pacheco, A., Aguayo, F. I., Aliaga, E., Muñoz, M., García-Rojo, G., et al. (2017) Chronic stress triggers expression of immediate early genes and differentially affects the expression of AMPA and NMDA subunits in dorsal and ventral hippocampus of rats, Front. Mol. Neurosci., 10, 244, https://doi.org/10.3389/fnmol.2017.00244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Costa-Nunes, J., Zubareva, O., Araújo-Correia, M., Valença, A., Schroeter, C. A., et al. (2014) Altered emotionality, hippocampus-dependent performance and expression of NMDA receptor subunit mRNAs in chronically stressed mice, Stress, 17, 108-116, https://doi.org/10.3109/10253890.2013.872619.

    Article  CAS  PubMed  Google Scholar 

  29. Furini, C., Myskiw, J., and Izquierdo, I. (2014) The learning of fear extinction, Neurosci. Biobehav. Rev., 47, 670-683, https://doi.org/10.1016/j.neubiorev.2014.10.016.

    Article  PubMed  Google Scholar 

  30. Matsumoto, Y., Morinobu, S., Yamamoto, S., Matsumoto, T., Takei, S., et al. (2013) Vorinostat ameliorates impaired fear extinction possibly via the hippocampal NMDA-CaMKII pathway in an animal model of posttraumatic stress disorder, Psychopharmacology (Berlin), 229, 51-62, https://doi.org/10.1007/s00213-013-3078-9.

    Article  CAS  Google Scholar 

  31. Réus, G. Z., Abelaira, H. M., Stringari, R. B., Fries, G. R., Kapczinski, F., and Quevedo, J. (2012) Memantine treatment reverses anhedonia, normalizes corticosterone levels and increases BDNF levels in the prefrontal cortex induced by chronic mild stress in rats, Metab. Brain Dis., 27, 175-182, https://doi.org/10.1007/s11011-012-9281-2.

    Article  CAS  PubMed  Google Scholar 

  32. Padovan, C. M., and Guimarães, F. S. (2004) Antidepressant-like effects of NMDA-receptor antagonist injected into the dorsal hippocampus of rats, Pharmacol. Biochem. Behav., 77, 15-19, https://doi.org/10.1016/j.pbb.2003.09.015.

    Article  CAS  PubMed  Google Scholar 

  33. Blacker, C. J., Millischer, V., Webb, L. M., Ho, A. M. C., Schalling, M., et al. (2020) EAAT2 as a research target in bipolar disorder and unipolar depression: a systematic review, Mol. Neuropsychiatry, 5, 44-59, https://doi.org/10.1159/000501885.

    Article  CAS  PubMed  Google Scholar 

  34. Zink, M., Vollmayr, B., Gebicke-Haerter, P. J., and Henn, F. A. (2010) Reduced expression of glutamate transporters vGluT1, EAAT2 and EAAT4 in learned helpless rats, an animal model of depression, Neuropharmacology, 58, 465-473, https://doi.org/10.1016/j.neuropharm.2009.09.005.

    Article  CAS  PubMed  Google Scholar 

  35. Zhang, X. H., Jia, N., Zhao, X. Y., Tang, G. K., Guan, L. X., et al. (2013) Involvement of pGluR1, EAAT2 and EAAT3 in offspring depression induced by prenatal stress, Neuroscience, 250, 333-341, https://doi.org/10.1016/j.neuroscience.2013.04.031.

    Article  CAS  PubMed  Google Scholar 

  36. Kovalenko, A. A., Zakharova, M. V., Nikitina, V. A., Schwarz, A. P., Karyakin, V. B., et al. (2018) Alterations in the expression of genes that encode subunits of ionotropic glutamate receptors and the glutamate transporter in brain structures of rats after psychogenic stress, Neurochem. J., 12, 135-141, https://doi.org/10.1134/S181971241802006X.

    Article  CAS  Google Scholar 

  37. Nasca, C., Bigio, B., Zelli, D., de Angelis, P., Lau, T., et al. (2017) Role of the Astroglial glutamate exchanger xCT in ventral hippocampus in resilience to stress, Neuron, 96, 402-413.e5, https://doi.org/10.1016/j.neuron.2017.09.020.

    Article  CAS  PubMed  Google Scholar 

  38. Beznin, G. V., Pshenichnaya, A. G., Kusov, A. G., and Tsikunov, S. G. (2012) Morphological and functional bases of behavioral deviations in the model of acute vital stress in rats, Med. Akadem. Zhurn., 12, 37-39.

    Google Scholar 

  39. Paxinos, G., and Watson, C. (2007) The Rat Brain in Stereotaxic Coordinates, 6th Edition, Academic Press.

  40. Kopec, A. M., Rivera, P. D., Lacagnina, M. J., Hanamsagar, R., and Bilbo, S. D. (2017) Optimized solubilization of TRIzol-precipitated protein permits Western blotting analysis to maximize data available from brain tissue, J. Neurosci. Methods, 280, 64-76, https://doi.org/10.1016/j.jneumeth.2017.02.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Harrington, C. R. (1990) Lowry protein assay containing sodium dodecyl sulfate in microtiter plates for protein determinations on fractions from brain tissue, Anal. Biochem., 186, 285-7, https://doi.org/10.1016/0003-2697(90)90081-j.

    Article  CAS  PubMed  Google Scholar 

  42. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680-685, https://doi.org/10.1038/227680a0.

    Article  CAS  PubMed  Google Scholar 

  43. Lei, T., Dong, D., Song, M., Sun, Y., Liu, X., and Zhao, H. (2020) Rislenemdaz treatment in the lateral habenula improves despair-like behavior in mice, Neuropsychopharmacology, 45, 1717-1724, https://doi.org/10.1038/s41386-020-0652-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Delawary, M., Tezuka, T., Kiyama, Y., Yokoyama, K., Inoue, T., et al. (2010) NMDAR2B tyrosine phosphorylation regulates anxiety-like behavior and CRF expression in the amygdala, Mol. Brain, 3, 37, https://doi.org/10.1186/1756-6606-3-37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Rahman, T., Zavitsanou, K., Purves-Tyson, T., Harms, L. R., Meehan, C., et al. (2017) Effects of immune activation during early or late gestation on N-methyl-d-aspartate receptor measures in adult rat offspring, Front. Psychiatry, 8, 77, https://doi.org/10.3389/fpsyt.2017.00077.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Tishkina, A., Stepanichev, M., Kudryashova, I., Freiman, S., Onufriev, M., et al. (2016) Neonatal proinflammatory challenge in male Wistar rats: effects on behavior, synaptic plasticity, and adrenocortical stress response, Behav. Brain Res., 304, 1-10, https://doi.org/10.1016/j.bbr.2016.02.001.

    Article  PubMed  Google Scholar 

  47. Onufriev, M. V., Freiman, S. V., Peregud, D. I., Kudryashova, I. V., Tishkina, A. O., et al. (2017) Neonatal proinflammatory stress induces accumulation of corticosterone and interleukin-6 in the hippocampus of juvenile rats: potential mechanism of synaptic plasticity impairments, Biochemistry (Moscow), 82, 275-281, https://doi.org/10.1134/S0006297917030051.

    Article  CAS  Google Scholar 

  48. Postnikova, T. Y., Griflyuk, A. V., Ergina, J. L., Zubareva, O. E., and Zaitsev, A. V. (2020) Administration of bacterial lipopolysaccharide during early postnatal ontogenesis induces transient impairment of long-term synaptic plasticity associated with behavioral abnormalities in young rats, Pharmaceuticals (Basel), 13, https://doi.org/10.3390/ph13030048.

    Article  CAS  Google Scholar 

  49. Onufriev, M. V., Uzakov, S. S., Freiman, S. V., Stepanichev, M. Y., Moiseeva, Y. V., et al. (2018) The Dorsal and ventral hippocampus have different reactivities to proinflammatory stress: corticosterone levels, cytokine expression, and synaptic plasticity, Neurosci. Behav. Physiol., 48, 1024-1031, https://doi.org/10.1007/s11055-018-0665-6.

    Article  CAS  Google Scholar 

  50. Benmhammed, H., El Hayek, S., Nassiri, A., Bousalham, R., Mesfioui, A., et al. (2019) Effects of lipopolysaccharide administration and maternal deprivation on anxiety and depressive symptoms in male and female Wistar rats: neurobehavioral and biochemical assessments, Behav. Brain Res., 362, 46-55, https://doi.org/10.1016/j.bbr.2019.01.005.

    Article  CAS  PubMed  Google Scholar 

  51. Sulakhiya, K., Keshavlal, G. P., Bezbaruah, B. B., Dwivedi, S., Gurjar, S. S., et al. (2016) Lipopolysaccharide induced anxiety- and depressive-like behaviour in mice are prevented by chronic pre-treatment of esculetin, Neurosci. Lett., 611, 106-111, https://doi.org/10.1016/j.neulet.2015.11.031.

    Article  CAS  PubMed  Google Scholar 

  52. Walker, F. R., March, J., and Hodgson, D. M. (2004) Endotoxin exposure in early life alters the development of anxiety-like behaviour in the Fischer 344 rat, Behav. Brain Res., 154, 63-69, https://doi.org/10.1016/j.bbr.2004.01.019.

    Article  CAS  PubMed  Google Scholar 

  53. Spencer, S. J., Heida, J. G., and Pittman, Q. J. (2005) Early life immune challenge – effects on behavioural indices of adult rat fear and anxiety, Behav. Brain Res., 164, 231-238, https://doi.org/10.1016/j.bbr.2005.06.032.

    Article  PubMed  Google Scholar 

  54. Custódio, C. S., Mello, B. S. F., Filho, A. J. M. C., de Carvalho Lima, C. N., Cordeiro, R. C., et al. (2018) Neonatal immune challenge with lipopolysaccharide triggers long-lasting sex- and age-related behavioral and immune/neurotrophic alterations in mice: relevance to autism spectrum disorders, Mol. Neurobiol., 55, 3775-3788, https://doi.org/10.1007/s12035-017-0616-1.

    Article  CAS  PubMed  Google Scholar 

  55. Fan, L.-W., Tien, L.-T., Mitchell, H. J., Rhodes, P. G., and Cai, Z. (2008) Alpha-phenyl-n-tert-butyl-nitrone ameliorates hippocampal injury and improves learning and memory in juvenile rats following neonatal exposure to lipopolysaccharide, Eur. J. Neurosci., 27, 1475-84, https://doi.org/10.1111/j.1460-9568.2008.06121.x.

    Article  PubMed  Google Scholar 

  56. Zoladz, P. R., and Diamond, D. M. (2016) Predator-based psychosocial stress animal model of PTSD: preclinical assessment of traumatic stress at cognitive, hormonal, pharmacological, cardiovascular and epigenetic levels of analysis, Exp. Neurol., 284, 211-219, https://doi.org/10.1016/j.expneurol.2016.06.003.

    Article  CAS  PubMed  Google Scholar 

  57. Zoladz, P. R., Park, C. R., Fleshner, M., and Diamond, D. M. (2015) Psychosocial predator-based animal model of PTSD produces physiological and behavioral sequelae and a traumatic memory four months following stress onset, Physiol. Behav., 147, 183-192, https://doi.org/10.1016/j.physbeh.2015.04.032.

    Article  CAS  PubMed  Google Scholar 

  58. Auxéméry, Y. (2012) Posttraumatic stress disorder (PTSD) as a consequence of the interaction between an individual genetic susceptibility, a traumatogenic event and a social context, Encephale, 38, 373-380, https://doi.org/10.1016/j.encep.2011.12.003.

    Article  PubMed  Google Scholar 

  59. Ding, X.-F., Li, Y.-H., Chen, J.-X., Sun, L.-J., Jiao, H.-Y., et al. (2017) Involvement of the glutamate/glutamine cycle and glutamate transporter GLT-1 in antidepressant-like effects of Xiao Yao san on chronically stressed mice, BMC Complement. Altern. Med., 17, 326, https://doi.org/10.1186/s12906-017-1830-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Shanks, N., Larocque, S., and Meaney, M. J. (1995) Neonatal endotoxin exposure alters the development of the hypothalamic-pituitary-adrenal axis: early illness and later responsivity to stress, J. Neurosci., 15, 376-384.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Zoladz, P. R., Fleshner, M., and Diamond, D. M. (2012) Psychosocial animal model of PTSD produces a long-lasting traumatic memory, an increase in general anxiety and PTSD-like glucocorticoid abnormalities, Psychoneuroendocrinology, 37, 1531-1545, https://doi.org/10.1016/j.psyneuen.2012.02.007.

    Article  CAS  PubMed  Google Scholar 

  62. Olff, M., Güzelcan, Y., de Vries, G.-J., Assies, J., and Gersons, B. P. R. (2006) HPA- and HPT-axis alterations in chronic posttraumatic stress disorder, Psychoneuroendocrinology, 31, 1220-1230, https://doi.org/10.1016/j.psyneuen.2006.09.003.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Spectrophotometric studies and visualization of membranes were carried out at the Center for the Shared Use of Scientific Equipment for Physiological, Biochemical, and Molecular Biology Research at the Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences.

Funding

The work was supported by the Russian Foundation for Basic Research (project no. 17-04-02116).

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Authors and Affiliations

  1. Institute of Experimental Medicine, 197376, Saint Petersburg, Russia

    Veronika A. Nikitina, Alexander N. Trofimov, Gleb V. Beznin & Sergei G. Tsikunov

  2. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, 194223, Saint Petersburg, Russia

    Maria V. Zakharova, Alexander P. Schwarz & Olga E. Zubareva

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  1. Veronika A. Nikitina
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Correspondence to Olga E. Zubareva.

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Nikitina, V.A., Zakharova, M.V., Trofimov, A.N. et al. Neonatal Exposure to Bacterial Lipopolysaccharide Affects Behavior and Expression of Ionotropic Glutamate Receptors in the Hippocampus of Adult Rats after Psychogenic Trauma. Biochemistry Moscow 86, 761–772 (2021). https://doi.org/10.1134/S0006297921060134

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