Pre-gestational stress reduces the ratio of 5-HIAA to 5-HT and the expression of 5-HT1A receptor and serotonin transporter in the brain of foetal rat
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BACKGROUND: Many studies have found that stress before or during pregnancy is linked to an increased incidence of behavioural disorders in offspring. However, few studies have investigated hypothalamic-pituitary-adrenal (HPA) axis activity and the serotonergic system as a consequence of pregestational stress. In the present study, we investigated the effect of pre-gestational stress on HPA axis activity in maternal rats and their foetuses and examined whether changes in HPA axis activity of maternal rats produced functional changes in the serotonergic system in the brain of foetuses. RESULTS: We used the behavioural tests to assess the model of chronic unpredictable stress (CUS) in maternal rats. We found the activity in the open field and sucrose consumption was lower for rats with CUS than for the controls. Body weight but not brain weight was higher for control foetuses than those from the CUS group. Serum corticosterone and corticotrophin-releasing hormone levels were significantly higher for mothers with CUS before pregnancy and their foetuses than for the controls. Levels of 5-hydroxytryptamine (5-HT) were higher in the hippocampus and hypothalamus of foetuses in the CUS group than in the controls, and 5-hydroxyindoleacetic acid (5-HIAA) levels were lower in the hippocampus in foetuses in the CUS group than in the control group. Levels of 5-HIAA in the hypothalamus did not differ between foetuses in the CUS group and in the control group. The ratio of 5-HIAA to 5-HT was significantly lower for foetuses in the CUS group than in the control group. Levels of 5-HT1A receptor were significantly lower in the foetal hippocampus in the CUS group than in the control group, with no significant difference in the hypothalamus. The levels of serotonin transporter (SERT) were lower in both the foetal hippocampus and foetal hypothalamus in the CUS group than in the control group. CONCLUSIONS: Our data demonstrate that pre-gestational stress alters HPA axis activity in maternal rats and their foetuses, which is associated with functional changes in 5-HT activity (5-HT, 5-HIAA and ratio of 5-HIAA to 5-HT), as well as the levels of the 5-HT1A receptor and SERT in the hippocampus and hypothalamus of foetuses.
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Pre-gestational and early-life stress with HPA activation is linked to an altered serotonergic system, leading to interruptions in brain development and cognition.
“Pre-gestational and early-life stress, with activation of the HPA axis, have been linked with an altered serotonergic system, leading to interruptions in brain development and cognition (218–220).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [220]
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Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
Chomczyński, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90021-2 · Cited by 47,092 · see citing works
Brain corticosteroid receptor balance in health and disease
de Kloet, E. R., Vreugdenhil, E., Oitzl, M. S., & Joëls, M. (1998) · Endocrine Reviews · doi:10.1210/edrv.19.3.0331 · Cited by 2,614 · see citing works
Brain corticosteroid receptor balance in health and disease
de Kloet, E. R. (1998) · Endocrine Reviews · doi:10.1210/er.19.3.269 · Cited by 2,614 · see citing works
Molecular, pharmacological and functional diversity of 5-HT receptors
Hoyer, D., Hannon, J. P., & Martin, G. R. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00746-8 · Cited by 1,869 · see citing works
Early-Life Blockade of the 5-HT Transporter Alters Emotional Behavior in Adult Mice
Ansorge, M. S., Zhou, M., Lira, A., Hen, R., & Gingrich, J. A. (2004) · Science · doi:10.1126/science.1101678 · Cited by 817 · see citing works
Prenatal stress and brain development
Charil, A., Laplante, D. P., Vaillancourt, C., & King, S. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.06.002 · Cited by 554 · see citing works
Is there a role for 5-HT1A agonists in the treatment of depression?
Blier, P., & Ward, N. M. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01643-8 · Cited by 529 · see citing works
The therapeutic role of 5-HT1A and 5-HT2A receptors in depression
Celada, P., Puig, M. V., Amargós‐Bosch, M., Adell, A., & Artigas, F. (2004) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0427 · Cited by 523 · see citing works
Lidov, H. G. W., & Molliver, M. E. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90077-6 · Cited by 483 · see citing works
Physiological stress reactivity in human pregnancy—a review
de Weerth, C., & Buitelaar, J. K. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.005 · Cited by 399 · see citing works
Barr, C. S., Newman, T. K., Shannon, C., Parker, C., Dvoskin, R. L., Becker, M. L., Schwandt, M., Champoux, M., Lesch, K. P., Goldman, D., et al. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.12.008 · Cited by 385 · see citing works
Immunocytochemical localization of serotonin1A receptors in the rat central nervous system
Kia, H. K., Miquel, M., Brisorgueil, M., Daval, G., Riad, M., Mestikawy, S. E., Hamon, M., & Verg�, D. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960205)365:2 · Cited by 378 · see citing works
Bonnin, A., & Levitt, P. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.10.005 · Cited by 311 · see citing works
Local circuit regulation of paraventricular nucleus stress integration
Herman, J. P., Tasker, J. G., Ziegler, D. R., & Cullinan, W. E. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00681-5 · Cited by 274 · see citing works
Commissiong, J. W. (1985) · Biochemical Pharmacology · doi:10.1016/0006-2952(85)90484-8 · Cited by 252 · see citing works
Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults
Entringer, S., Kumsta, R., Hellhammer, D. H., Wadhwa, P. D., & Wüst, S. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.11.006 · Cited by 251 · see citing works
HPA axis responsiveness to stress: implications for healthy aging
Aguilera, G. (2011) · Experimental Gerontology · doi:10.1016/j.exger.2010.08.023 · Cited by 250 · see citing works
Foster, C. E., Garber, J., & Durlak, J. A. (2007) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-007-9197-1 · Cited by 204 · see citing works
Kilpatrick, I. C., Jones, M. W., & Phillipson, O. T. (1986) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1986.tb08506.x · Cited by 195 · see citing works
Prenatal stress and neonatal rat brain development
van den Hove, D., Steinbusch, H. W. M., Scheepens, A., van de Berg, W. D. J., Kooiman, L. A. M., Boosten, B. J. G., Prickaerts, J., & Blanco, C. E. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.060 · Cited by 192 · see citing works
Li, Q., Wichems, C. H., Heils, A., de Kar, L. D. V., Lesch, K., & Murphy, D. L. (1999) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)35202-4 · Cited by 184 · see citing works
Hensler, J. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00395-5 · Cited by 168 · see citing works
Grippo, A. J., Sullivan, N. R., Damjanoska, K. J., Crane, J. W., Carrasco, G. A., Shi, J., Chen, Z., García, F., Muma, N. A., & de Kar, L. D. V. (2004) · Psychopharmacology · doi:10.1007/s00213-004-2103-4 · Cited by 152 · see citing works
Chronic social instability stress in female rats: A potential animal model for female depression
Herzog, C., Czéh, B., Corbach‐Söhle, S., Wuttke, W., Schulte‐Herbrüggen, O., Hellweg, R., Flügge, G., & Fuchs, E. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.01.059 · Cited by 142 · see citing works
Fujioka, T., Sakata, Y., Yamaguchi, K., Shibasaki, T., Kato, H., & Nakamura, S. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00073-1 · Cited by 134 · see citing works
Zhou, W., Cunningham, K. A., & Thomas, M. L. (2002) · Molecular Brain Research · doi:10.1016/s0169-328x(02)00134-1 · Cited by 130 · see citing works
Froger, N., Palazzo, E., Boni, C., Hanoun, N., Saurini, F., Joubert, C., Dutriez-Casteloot, I., Enache, M., Maccari, S., Barden, N., et al. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4132-03.2004 · Cited by 122 · see citing works
Tjurmina, O., Armando, I., Saavedra, J. M., Goldstein, D. S., & Murphy, D. L. (2002) · Endocrinology · doi:10.1210/en.2002-220416 · Cited by 117 · see citing works
Kapoor, A., Kostaki, A., Janus, C., & Matthews, S. G. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.08.018 · Cited by 109 · see citing works
Raap, D. K., DonCarlos, L. L., García, F., Muma, N. A., Wolf, W. A., Battaglia, G., & de Kar, L. D. V. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(99)00264-6 · Cited by 105 · see citing works
Programming of the Hypothalamo–Pituitary–Adrenal Axis: Serotonergic Involvement
Andrews, M. H., & Matthews, S. G. (2004) · Stress · doi:10.1080/10253890310001650277 · Cited by 99 · see citing works
Leitch, M. M., Ingram, C. D., Young, A. H., McQuade, R., & Gartside, S. E. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300016 · Cited by 93 · see citing works
Kasper, S. F., Tauscher, J. T., Willeit, M., Stamenkovic, M., Neumeister, A., Kufferle, B., Barnas, C., Stastny, J., Praschak-Rieder, N., Pezawas, L., et al. (2002) · The World Journal of Biological Psychiatry · doi:10.3109/15622970209150614 · Cited by 90 · see citing works
Bilbo, S. D., Newsum, N. J., Sprunger, D. B., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2006.10.005 · Cited by 88 · see citing works
Cintra, A., Solfrini, V., Bunnemann, B., Okret, S., Bortolotti, F., Gustafsson, J.-Å., & Fuxé, K. (2008) · Neuroendocrinology · doi:10.1159/000126480 · Cited by 88 · see citing works
Induction and expression of GluA1 (GluR‐A)‐independent LTP in the hippocampus
Romberg, C., Raffel, J., Martin, L., Sprengel, R., Seeburg, P. H., Rawlins, J. N. P., Bannerman, D. M., & Paulsen, O. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06677.x · Cited by 82 · see citing works
Slotkin, T. A., Kreider, M. L., Tate, C. A., & Seidler, F. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300892 · Cited by 81 · see citing works
Spinelli, S., Chefer, S. I., Carson, R. E., Jagoda, E. M., Lang, L., Heilig, M. A., Barr, C. S., Suomi, S. J., Higley, J. D., & Stein, E. A. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.12.030 · Cited by 77 · see citing works
Davidson, S., Prokonov, D., Taler, M., Maayan, R., Harell, D., Gil‐Ad, I., & Weizman, A. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e318193594a · Cited by 71 · see citing works
Huang, Y., Shi, X., Xu, H., Yang, H., Tian, C., Chen, S., & Chen, X. (2010) · Neurochemical Research · doi:10.1007/s11064-010-0152-0 · Cited by 68 · see citing works
Self-citationDremencov, E., Gur, E., Lerer, B., & Newman, M. E. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(03)00123-4 · Cited by 65 · see citing works
Li, Q., Holmes, A., Ma, L., de Kar, L. D. V., García, F., & Murphy, D. L. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3223-04.2004 · Cited by 65 · see citing works
Belay, H., Burton, C. L., Lovic, V., Meaney, M. J., Sokolowski, M., & Fleming, A. S. (2011) · Behavioral Neuroscience · doi:10.1037/a0022891 · Cited by 61 · see citing works
Gao, W., Paterson, J., Abbott, M., Carter, S., & Iusitini, L. (2007) · Australian & New Zealand Journal of Psychiatry · doi:10.1080/00048670701634929 · Cited by 59 · see citing works
Synaptic organization of the glomerular complexes in the lateral geniculate nucleus of Cebus monkey
Saavedra, J. P., & Vaccarezza, O. L. (1968) · Brain Research · doi:10.1016/0006-8993(68)90061-9 · Cited by 51 · see citing works
Li, H., Zhang, L., Fang, Z., Lin, L., Wu, C., & Huang, Q. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.12.017 · Cited by 40 · see citing works
Self-citationPieper, S., Out, D., Bakermans‐Kranenburg, M. J., & van IJzendoorn, M. H. (2011) · Journal of Traumatic Stress · doi:10.1002/jts.20659 · Cited by 36 · see citing works
Takano, H., Ito, H., Takahashi, H., Arakawa, R., Okumura, M., Kodaka, F., Otsuka, T., Kato, M., & Suhara, T. (2010) · Synapse · doi:10.1002/syn.20883 · Cited by 36 · see citing works
Stress through handling for vaginal screening, serotonin, and ACTH response to ether
Sfikakis, A. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02089-6 · Cited by 36 · see citing works
Acute rise in corticosterone facilitates 5-HT1A receptor-mediated behavioural responses
Meijer, O. C., Kortekaas, R., Oitzl, M. S., & de Kloet, E. R. (1998) · European Journal of Pharmacology · doi:10.1016/s0014-2999(98)00289-1 · Cited by 34 · see citing works
Uchida, T., Oki, Y., Yanagawa, Y., & Fukuda, A. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.12.010 · Cited by 27 · see citing works
Byers, J. P., Masters, K. L., Sarver, J. G., & Hassoun, E. A. (2006) · Toxicology · doi:10.1016/j.tox.2006.09.009 · Cited by 27 · see citing works
Slotkin, T. A., & Seidler, F. J. (2010) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2010.02.015 · Cited by 26 · see citing works
Bilobalide modulates serotonin-controlled behaviors in the nematode Caenorhabditis elegans
Brown, M. K., & Luo, Y. (2009) · BMC Neuroscience · doi:10.1186/1471-2202-10-62 · Cited by 17 · see citing works
Otten, W., Kanitz, E., Tuchscherer, M., Brüssow, K. ‐., & Nürnberg, G. (2007) · Theriogenology · doi:10.1016/j.theriogenology.2007.09.025 · Cited by 16 · see citing works
Dremencov, E., Gur, E., Lerer, B., & Newman, M. E. (2002) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(02)00227-0 · Cited by 16 · see citing works
Kim, S. J., Kang, J. I., Namkoong, K., & Song, D. (2011) · Neuropsychobiology · doi:10.1159/000327705 · Cited by 12 · see citing works
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- Dremencov E Gur E Lerer B Newman ME Effects of chronic antidepressants and electroconvulsive shock on serotonergic neurotransmission in the rat hypothalamus Prog Neuropsychopharmacol Biol Psychiatry 2002 26 6 1029 1034 10.1016/S0278-5846(02)00227-0 12452522 · DOI
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Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S., & Bale, T. L. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0914-13.2013 · Cited by 814 · see citing works
Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
Brummelte, S., Mc Glanaghy, E., Bonnin, A., & Oberlander, T. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2016.02.037 · Cited by 306 · see citing works
Effects of prenatal maternal stress on serotonin and fetal development
St‐Pierre, J., Laurent, L., King, S., & Vaillancourt, C. (2015) · Placenta · doi:10.1016/j.placenta.2015.11.013 · Cited by 129 · see citing works
Yu, Y., Wang, R., Chen, C., Du, X., Ruan, L., Sun, J., Li, J., Zhang, L., O’Donnell, J. M., Pan, J., et al. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.10.018 · Cited by 105 · see citing works
Serotonin and motherhood: From molecules to mood
Pawluski, J. L., Li, M., & Lonstein, J. S. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.03.001 · Cited by 98 · see citing works
Zaidan, H., Leshem, M., & Gaisler-Salomon, I. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.04.014 · Cited by 94 · see citing works
Gestational Factors throughout Fetal Neurodevelopment: The Serotonin Link
Hanswijk, S. I., Spoelder, M., Shan, L., Verheij, M. M. M., Muilwijk, O. G., Li, W., Liu, C., Kolk, S. M., & Homberg, J. R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165850 · Cited by 86 · see citing works
Sarro, E. C., Sullivan, R. M., & Barr, G. A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.10.064 · Cited by 77 · see citing works
Gemmel, M., Hazlett, M. F., Bögi, E., Lacalle, S. D., Hill, L. A., Kokras, N., Hammond, G. L., Dalla, C., Charlier, T. D., & Pawluski, J. L. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.07.480 · Cited by 56 · see citing works
Gemmel, M., Rayen, I., van Donkelaar, E. L., Loftus, T., Steinbusch, H. W. M., Kokras, N., Dalla, C., & Pawluski, J. L. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.03.068 · Cited by 56 · see citing works
Xia, B., Chen, C., Zhang, H., Xue, W., Tang, J., Tao, W., Wu, R., Ren, L., Wang, W., & Chen, G. (2016) · Scientific Reports · doi:10.1038/srep35042 · Cited by 45 · see citing works
Wang, J., Cheng, C., Xin, C., & Wang, Z. (2019) · Molecules · doi:10.3390/molecules24061105 · Cited by 44 · see citing works
Shi, H., Wu, D., Chen, R., Li, N., & Zhu, L. (2022) · Theranostics · doi:10.7150/thno.70370 · Cited by 40 · see citing works
Gemmel, M., Lacalle, S. D., Mort, S. C., Hill, L. A., Charlier, T. D., & Pawluski, J. L. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.10.009 · Cited by 39 · see citing works
Gemmel, M., Harmeyer, D., Bögi, E., Fillet, M., Hill, L. A., Hammond, G. L., Charlier, T. D., & Pawluski, J. L. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.11.038 · Cited by 33 · see citing works
5-HT2A and 5-HT2C receptors as hypothalamic targets of developmental programming in male rats
Martin‐Gronert, M. S., Stocker, C. J., Wargent, E. T., Cripps, R. L., Garfield, A. S., Jovanović, Z., D’Agostino, G., Yeo, G. S. H., Cawthorne, M. A., Arch, J. R. S., et al. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.023903 · Cited by 32 · see citing works
Lee, H., Kim, S., Jang, J., Park, H., & Lee, S. (2021) · Antioxidants · doi:10.3390/antiox10060895 · Cited by 31 · see citing works
Wang, S., Ni, Y., Guo, F., Sun, Z., Ahmed, A. A., & Zhao, R. (2013) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2013.11.005 · Cited by 31 · see citing works
Gemmel, M., Kokras, N., Dalla, C., & Pawluski, J. L. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.10.009 · Cited by 29 · see citing works
Czarzasta, K., Makowska‐Zubrycka, M., Kasarełło, K., Skital, V. M., Tyszkowska, K., Matusik, K., Jesion, A., Wojciechowska, M., Segiet, A., Wrzesień, R., et al. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.11.024 · Cited by 28 · see citing works
Huang, Y., Shen, Z., Hu, L., Xia, F., Li, Y., Zhuang, J., Chen, P., & Huang, Q. (2016) · Psychiatry Research · doi:10.1016/j.psychres.2016.10.005 · Cited by 22 · see citing works
Self-citationAzizi, N., Roshan‐Milani, S., Mahmoodkhani, M., Saboory, E., Gholinejad, Z., Abdollahzadeh, N., Sayyadi, H., & Chodari, L. (2019) · Stress · doi:10.1080/10253890.2019.1619075 · Cited by 22 · see citing works
Huang, Y., Chen, S., Xu, H., Yu, X., Lai, H., Ho, G., Huang, Q., & Shi, X. (2013) · BMC Neuroscience · doi:10.1186/1471-2202-14-67 · Cited by 21 · see citing works
Self-citationPawluski, J. L., & Gemmel, M. (2018) · HORMONES · doi:10.1007/s42000-018-0011-y · Cited by 21 · see citing works
Bielas, H., Arck, P., Bruenahl, C. A., Walitza, S., & Grünblatt, E. (2014) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2014.07.006 · Cited by 21 · see citing works
Mahmoodkhani, M., Saboory, E., Roshan‐Milani, S., Azizi, N., Karimipour, M., Rasmi, Y., & Gholinejad, Z. (2018) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2017.12.016 · Cited by 17 · see citing works
Ahmed, A. A., Musa, H. H., & Sifaldin, A. Z. (2016) · Asian Pacific Journal of Reproduction · doi:10.1016/j.apjr.2016.06.013 · Cited by 11 · see citing works
Jenkins, S., Harker, A., & Gibb, R. L. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.10.023 · Cited by 12 · see citing works
Huang, Y., Lai, H., Xu, H., Wu, W., Lai, X., Ho, G., Ma, L., & Chen, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082502 · Cited by 11 · see citing works
Self-citationBelovičová, K., Šimončičová, E., Viñas-Noguera, M., Dubovický, M., & Bögi, E. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112944 · Cited by 10 · see citing works
Jenkins, S., Harker, A., & Gibb, R. L. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113543 · Cited by 10 · see citing works
Huang, Y., Hu, L., Li, H., Huang, Y., Li, Y., Yang, J., Gu, J., & Xu, H. (2019) · Psychiatry Research · doi:10.1016/j.psychres.2019.112497 · Cited by 10 · see citing works
Self-citationSex differences in the vulnerability of the hippocampus to prenatal stress
Soti, M., Ranjbar, H., Kohlmeier, K. A., & Shabani, M. (2022) · Developmental Psychobiology · doi:10.1002/dev.22305 · Cited by 10 · see citing works
Zhang, X., Zhang, H., Tan, R., Peng, J. C., Liang, X. L., Liu, Q., Wang, M., & Yu, X. (2012) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2012/670362 · Cited by 9 · see citing works
Xie, J., Qin, X., Shu, L., Li, P., Liu, Z., Zhu, P., Tao, F., & Huang, K. (2021) · Brain Research · doi:10.1016/j.brainres.2021.147562 · Cited by 8 · see citing works
Zhang, X. G., Zhang, H., Liang, X. L., Liu, Q., Wang, H. Y., Cao, B., Cao, J., Liu, S., Long, Y. J., Xie, W., et al. (2016) · Genetics and Molecular Research · doi:10.4238/gmr.15039009 · Cited by 7 · see citing works
Sasváriová, M., Kaprinay, B. T., Salvaras, L., Belovičová, K., Bögi, E., Knezl, V., Barteková, M., Stankovičová, T., & Dubovický, M. (2018) · European Pharmaceutical Journal · doi:10.2478/afpuc-2018-0007 · Cited by 7 · see citing works
Vásquez, F. D. J. J., Guerrero, D. M., Rubio‐Osornio, M., Rubio, C., Orozco-Suárez, S. A., & Retana‐Márquez, S. (2020) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2020-029 · Cited by 7 · see citing works
Pre-pregnancy stress induces maternal vascular dysfunction during pregnancy and postpartum
Gemmel, M., Stumpp, L., Gallaher, M. J., & Powers, R. W. (2023) · Reproductive Sciences · doi:10.1007/s43032-023-01248-2 · Cited by 6 · see citing works
Guerrero, D. M., Vásquez, F. D. J. J., Rubio‐Osornio, M., Rubio, C., Orozco-Suárez, S. A., & Retana‐Márquez, S. (2020) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2020-037 · Cited by 5 · see citing works
Bögi, E., Belovičová, K., Csatlósová, K., & Dubovický, M. (2017) · Interdisciplinary Toxicology · doi:10.1515/intox-2017-0005 · Cited by 5 · see citing works
Sajdel, E. M. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817933-8.00007-4 · Cited by 4 · see citing works
Azizi, N., Heidari, M., Saboory, E., Abdollahzade, N., & Roshan‐Milani, S. (2024) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2024.03.007 · Cited by 4 · see citing works
Hoppanová, L., Filipova, A., Bukatová, S., Ondáčová, K., Tomko, M., Jurkovičová-Tarabová, B., Dubovický, M., Dremencov, E., & Lacinová, Ľ. (2025) · Scientia Pharmaceutica · doi:10.3390/scipharm93020017 · Cited by 4 · see citing works
Roles of serotonin in the fetal brain
Zhao, Q., & Bonnin, A. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-444-64125-0.00024-4 · Cited by 3 · see citing works
Chronic Ultrasound Prenatal Stress Altered the Brain’s Neurochemical Systems in Newborn Rats
Abramova, O. V., Zorkina, Y., Ka, P., Ushakova, V. M., Morozova, A. Y., Zubkov, E. A., Pavlova, O., Storozheva, Z. I., Gurina, O. I., & Chekhonin, V. P. (2024) · Neural Plasticity · doi:10.1155/2024/3829941 · Cited by 3 · see citing works
Analysis of membrane transport mechanisms of endogenous substrates using chromatographic techniques
Yamaguchi, H., & Mano, N. (2019) · Biomedical Chromatography · doi:10.1002/bmc.4495 · Cited by 2 · see citing works
Perspectives on Behavioral Development
Jenkins, S. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804036-2.00002-9 · Cited by 1 · see citing works
Developmental and psychoneuroimmunological mechanisms in depression
Pujol-Lopez, Y. (2015) · doi:10.26481/dis.20151030yp
Bowe, C., Thomas, C. J., & Mackey, P. (2025) · Child and Adolescent Social Work Journal · doi:10.1007/s10560-025-01027-9
- Authors
- Huang, Y., Xu, H., Li, H., Yang, H., Chen, Y., & Shi, X.
- Affiliations
- Shantou University (CN)
- Guangdong Province Women and Children Hospital (CN)
- Corresponding author
- Chen, Yunbin
- Shi, Xuechuan
- Venue
- BMC Neuroscience
- Published
- 2012-02-28
- Volume
- 13
- Issue
- 1
- Pages
- 22-22
- ISSN
- 1471-2202 (ISSN-L)
- PMC
- PMC3311061
- OpenAlex
- W2048234240
- Cited by
- 55
- References
- 58
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 2 · 2022: 2 · 2021: 6 · 2020: 5 · 2019: 5 · 2018: 6 · 2017: 6 · 2016: 8 · 2015: 2 · 2014: 1 · 2013: 6 · 2012: 2
- FWCI
- 1.47
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Natural Science Foundation of China (31140016)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- chronic unpredictable mild stress, hypothalamic-pituitary-adrenal axis, serotonergic system, 5-HT1A receptor, serotonin transporter, fetal brain, hippocampus, hypothalamus, corticosterone, corticotropin-releasing factor, maternal stress, rat model, sucrose intake, open field
- MeSH terms
- Analysis of Variance, Animals, Body Weight, Brain, Chromatography, High Pressure Liquid, Corticosterone, Corticotropin-Releasing Hormone, Embryo, Mammalian, Female, Food Preferences, Hydroxyindoleacetic Acid, Male, Maternal Behavior, Pregnancy, Prenatal Exposure Delayed Effects, Serotonin, Time Factors, Rats, Sprague-Dawley, Gene Expression Regulation, Developmental, Receptor, Serotonin, 5-HT1A, Serotonin Plasma Membrane Transport Proteins, Rats
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