Gestational Factors throughout Fetal Neurodevelopment: The Serotonin Link

Hanswijk, Sabrina I.; Spoelder, Marcia; Shan, Ling; Verheij, Michel M. M.; Muilwijk, Otto G.; Li, Weizhuo; Liu, Chunqing; Kolk, Sharon M.; Homberg, Judith R.

doi:10.3390/ijms21165850

Cited by 87Maternal Mental Health During Pregnancy and PostpartumNeurotransmitter Receptor Influence on BehaviorTryptophan and brain disorders

Gestational Factors throughout Fetal Neurodevelopment: The Serotonin Link

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Hanswijk, Sabrina I., Spoelder, Marcia, Shan, Ling, Verheij, Michel M. M., Muilwijk, Otto G., Li, Weizhuo, Liu, Chunqing, Kolk, Sharon M. +1 more·2020·International Journal of Molecular Sciences

DOI 10.3390/ijms21165850PMC PMC7461571

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Abstract

Serotonin (5-HT) is a critical player in brain development and neuropsychiatric disorders. Fetal 5-HT levels can be influenced by several gestational factors, such as maternal genotype, diet, stress, medication, and immune activation. In this review, addressing both human and animal studies, we discuss how these gestational factors affect placental and fetal brain 5-HT levels, leading to changes in brain structure and function and behavior. We conclude that gestational factors are able to interact and thereby amplify or counteract each other’s impact on the fetal 5-HT-ergic system. We, therefore, argue that beyond the understanding of how single gestational factors affect 5-HT-ergic brain development and behavior in offspring, it is critical to elucidate the consequences of interacting factors. Moreover, we describe how each gestational factor is able to alter the 5-HT-ergic influence on the thalamocortical- and prefrontal-limbic circuitry and the hypothalamo-pituitary-adrenocortical-axis. These alterations have been associated with risks to develop attention deficit hyperactivity disorder, autism spectrum disorders, depression, and/or anxiety. Consequently, the manipulation of gestational factors may be used to combat pregnancy-related risks for neuropsychiatric disorders.

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Serotonin exerts a significant trophic and modulatory function in neurodevelopmental processes such as proliferation, migration, and differentiation in cortical areas, including the PFC.
“It has become widely accepted that serotonin exerts a significant trophic and modulatory function in neurodevelopmental processes such as proliferation, migration and differentiation in cortical areas, including the PFC [119, 123, 125–129].”
From Development of prefrontal cortex (2022) · cites this paper as [125]
Section 2 says serotonin is involved in neuronal proliferation and migration during development, and §2.1 describes its role in cortical migration, including serotoninergic fibers in the medial PFC. The passages do not establish the claimed role in differentiation, so the full list of processes is not supported. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Treatments against maternal depression such as SSRIs can cause substantial structural damage to prefrontal subdomains.
“treatments against maternal depression such as SSRIs can cause substantial structural damage to prefrontal subdomains [125, 128].”
From Development of prefrontal cortex (2022) · cites this paper as [125]
Section 3.4 reports decreased dendritic complexity in the medial prefrontal cortex and describes possible reductions in prefrontal neuron complexity after SSRI exposure. It does not characterize these changes as substantial structural damage, and it presents the proposed mechanisms cautiously, largely in the context of offspring studies. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Maternal stress itself can be detrimental to brain development in general and the developing PFC in particular.
“Although maternal stress itself can be detrimental to brain development in general and the developing PFC in particular (for review see [125])”
From Development of prefrontal cortex (2022) · cites this paper as [125]

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The Association Between Antenatal Exposure to Selective Serotonin Reuptake Inhibitors and Autism
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Maternal postpartum corticosterone and fluoxetine differentially affect adult male and female offspring on anxiety-like behavior, stress reactivity, and hippocampal neurogenesis
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Serotonin transporter gene polymorphisms: Effect on serotonin transporter availability in the brain of suicide attempters
Bah, J., Lindström, M., Westberg, L., Mannerås, L., Ryding, E., Henningsson, S., Melke, J., Rosén, I., Träskman‐Bendz, L., & Eriksson, E. (2008) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2007.07.004 · Cited by 67 · see citing works
Effects of prenatal protein malnutrition and neonatal stress on CNS responsiveness
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Combined effect of maternal serotonin transporter genotype and prenatal stress in modulating offspring social interaction in mice
Jones, K. L., Smith, R. M., Edwards, K. S., Givens, B. S., Tilley, M. R., & Beversdorf, D. Q. (2010) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2010.05.002 · Cited by 67 · see citing works
Prenatal protein malnutrition effects on the serotonergic system in the hippocampal formation: An immunocytochemical, ligand binding, and neurochemical study
Blatt, G. J., Chen, J., Rosene, D. L., Volicer, L., & Galler, J. R. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90025-6 · Cited by 67 · see citing works
Prenatal antidepressant exposure and the risk of autism spectrum disorders in children. Are we looking at the fall of Gods?
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Effects of maternal stress and perinatal fluoxetine exposure on behavioral outcomes of adult male offspring
Kiryanova, V., Meunier, S., Vecchiarelli, H. A., Hill, M. N., & Dyck, R. H. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.064 · Cited by 67 · see citing works
Behavioural outcomes of perinatal maternal fluoxetine treatment
McAllister, B. B., Kiryanova, V., & Dyck, R. H. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.09.024 · Cited by 66 · see citing works
The Presynaptic Component of the Serotonergic System is Required for Clozapine's Efficacy
Yadav, P. N., Abbas, A. I., Farrell, M. S., Setola, V., Sciaky, N., Huang, X., Kroeze, W. K., Crawford, L. K., Piel, D., Keiser, M. J., et al. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.195 · Cited by 66 · see citing works
Developmental Influence of the Serotonin Transporter on the Expression of Npas4 and GABAergic Markers: Modulation by Antidepressant Treatment
Guidotti, G., Calabrese, F., Auletta, F., Olivier, J., Racagni, G., Homberg, J. R., & Riva, M. A. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.252 · Cited by 66 · see citing works
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Prenatal selective serotonin reuptake inhibitor use and the risk of autism spectrum disorder in children: A systematic review and meta-analysis
Kaplan, Y. C., Arslan, E. K., Acar, S., & Sözmen, K. (2016) · Reproductive Toxicology · doi:10.1016/j.reprotox.2016.09.013 · Cited by 66 · see citing works
The 5-Hydroxytryptamine signaling map: an overview of serotonin-serotonin receptor mediated signaling network
Sahu, A., Gopalakrishnan, L., Gaur, N., Chatterjee, O., Mol, P., Modi, P. K., Dagamajalu, S., Advani, J., Jain, S., & Prasad, T. S. K. (2018) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-018-0482-2 · Cited by 66 · see citing works
Identification of kynurenine pathway enzyme mRNAs and metabolites in human placenta: Up-regulation by inflammatory stimuli and with clinical infection
Manuelpillai, U., Ligam, P., Smythe, G. A., Wallace, E. M., Hirst, J. J., & Walker, D. W. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.06.090 · Cited by 65 · see citing works
Disruption of Transient Serotonin Accumulation by Non-Serotonin-Producing Neurons Impairs Cortical Map Development
Chen, X., Ye, R., Gargus, J. J., Blakely, R., Dobrenis, K., & Sze, J. Y. (2015) · Cell Reports · doi:10.1016/j.celrep.2014.12.033 · Cited by 65 · see citing works
Neonatal S100B Protein Levels After Prenatal Exposure to Selective Serotonin Reuptake Inhibitors
Pawluski, J. L., Galea, L. A. M., Brain, U., Papsdorf, M., & Oberlander, T. F. (2009) · Pediatrics · doi:10.1542/peds.2009-0442 · Cited by 65 · see citing works
Perinatal selective serotonin reuptake inhibitor medication (SSRI) effects on social behaviors, neurodevelopment and the epigenome
Gemmel, M., Bögi, E., Ragan, C. M., Hazlett, M. F., Dubovický, M., van den Hove, D., Oberlander, T. F., Charlier, T. D., & Pawluski, J. L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.04.023 · Cited by 65 · see citing works
Excess of serotonin affects neocortical pyramidal neuron migration
Riccio, O., Jacobshagen, M., Golding, B., Vutskits, L., Jabaudon, D., Hornung, J., & Dayer, A. G. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.49 · Cited by 63 · see citing works
The serotonin 1A receptor gene as a genetic and prenatal maternal environmental factor in anxiety
Gleason, G., Liu, B., Bruening, S., Zupan, B., Auerbach, A. D., Mark, W. H., Oh, J.-E., Toth, J. G., Lee, F., & Tóth, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914805107 · Cited by 62 · see citing works
In utero ethanol exposure decreased the density of serotonin neurons. Maternal ipsapirone treatment exerted a protective effect
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Serotonergic Stimulation of the Rat Hypothalamo‐Pituitary‐Adrenal Axis: Interaction between 5‐HT1A and 5‐HT2A Receptors
Mikkelsen, J. D., Hay‐Schmidt, A., & KISS, A. J. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1296.007 · Cited by 62 · see citing works
Maternal immune activation epigenetically regulates hippocampal serotonin transporter levels
Reisinger, S. N., Kong, E., Khan, D., Schulz, S., Ronovsky, M., Berger, S., Horvath, O., Cabatic, M., Berger, A., & Pollak, D. D. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.02.007 · Cited by 62 · see citing works
Transplacental Nutrient Transport Mechanisms of Intrauterine Growth Restriction in Rodent Models and Humans
Winterhager, E., & Gellhaus, A. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00951 · Cited by 59 · see citing works
Decreased Cortical Serotonin in Neonatal Rabbits Exposed to Endotoxin <i>in Utero</i>
Kannan, S., Saadani-Makki, F., Balakrishnan, B., Dai, H., Chakraborty, P. K., Janisse, J., Muzik, O., Romero, R., & Chugani, D. C. (2011) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2010.156 · Cited by 58 · see citing works
Genetic and pharmacological manipulations of the serotonergic system in early life: neurodevelopmental underpinnings of autism-related behavior
Kinast, K., Peeters, D., Kolk, S. M., Schubert, D., & Homberg, J. R. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00072 · Cited by 57 · see citing works
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Perinatal exposure to the selective serotonin reuptake inhibitor citalopram alters spatial learning and memory, anxiety, depression, and startle in Sprague‐Dawley rats
Sprowles, J. L. N., Wendel, J. R. H., Gutierrez, A., Bailey, R. A., Jablonski, S. A., Williams, M. T., & Vorhees, C. V. (2016) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2016.08.007 · Cited by 57 · see citing works
Attention-Deficit/Hyperactivity Disorder Symptoms in Offspring of Mothers With Impaired Serotonin Production
Halmøy, A., Johansson, S., Winge, I., McKinney, J. A., Knappskog, P. M., & Haavik, J. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.124 · Cited by 56 · see citing works
Prenatal exposure to selective serotonin reuptake inhibitors (SSRI) increases aggression and modulates maternal behavior in offspring mice
Svirsky, N., Levy, S., & Avitsur, R. (2015) · Developmental Psychobiology · doi:10.1002/dev.21356 · Cited by 56 · see citing works
Perinatal fluoxetine effects on social play, the HPA system, and hippocampal plasticity in pre-adolescent male and female rats: Interactions with pre-gestational maternal stress
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
Effect of Time-Dependent Selective Serotonin Reuptake Inhibitor Antidepressants During Pregnancy on Behavioral, Emotional, and Social Development in Preschool-Aged Children
Lupattelli, A., Wood, M. E., Ystrøm, E., Skurtveit, S. O., Handal, M., & Nordeng, H. (2017) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2017.12.010 · Cited by 56 · see citing works
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
Huang, Y., Xu, H., Li, H., Yang, H., Chen, Y., & Shi, X. (2012) · BMC Neuroscience · doi:10.1186/1471-2202-13-22 · Cited by 55 · see citing works
Perinatal vs Genetic Programming of Serotonin States Associated with Anxiety
Altieri, S. C., Yang, H., O'Brien, H. J., Redwine, H. M., Şentürk, D., Hensler, J. G., & Andrews, A. M. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.331 · Cited by 55 · see citing works
Serotonin transporter protects the placental cells against apoptosis in caspase 3‐independent pathway
Hadden, C., Fahmi, T., Cooper, A., Savenka, A. V., Lupashin, V. V., Roberts, D. J., Maroteaux, L., Mouzon, S. H., & Kilic, F. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25812 · Cited by 55 · see citing works
Long‐term consequences of neonatal fluoxetine exposure in adult rats
Ko, M., Lee, L. J., Li, Y., & Lee, L. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22185 · Cited by 54 · see citing works
The genetics of selective serotonin reuptake inhibitors
Kroeze, Y., Zhou, H., & Homberg, J. R. (2012) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2012.08.015 · Cited by 54 · see citing works
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SSRIs and SNRIs (SRI) in Pregnancy: Effects on the Course of Pregnancy and the Offspring: How Far Are We from Having All the Answers?
Ornoy, A., & Koren, G. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20102370 · Cited by 54 · see citing works
The impact of maternal high-fat diet consumption on neural development and behavior of offspring
Sullivan, E. L., Nousen, E. K., Chamlou, K. A., & Grove, K. L. (2012) · International Journal of Obesity Supplements · doi:10.1038/ijosup.2012.15 · Cited by 53 · see citing works
Lack of serotonin reuptake during brain development alters rostral raphe-prefrontal network formation
Witteveen, J. S., Middelman, A., van Hulten, J. A., Martens, G. J. M., Homberg, J. R., & Kolk, S. M. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00143 · Cited by 53 · see citing works
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Maternal Inflammation Results in Altered Tryptophan Metabolism in Rabbit Placenta and Fetal Brain
Williams, M. A., Zhang, Z., Nance, E., Drewes, J., Lesniak, W. G., Singh, S., Chugani, D., Rangaramanujam, K. M., Graham, D. R. M., & Kannan, S. (2017) · Developmental Neuroscience · doi:10.1159/000471509 · Cited by 53 · see citing works
Distinct effects of perinatal exposure to fluoxetine or methylmercury on parvalbumin and perineuronal nets, the markers of critical periods in brain development
Umemori, J., Winkel, F., Ċastrén, E., & Karpova, N. N. (2015) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2015.05.006 · Cited by 52 · see citing works

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Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
“Although maternal stress itself can be detrimental to brain development in general and the developing PFC in particular (for review see [125]), treatments against maternal depression such as SSRIs can cause substantial structural damage to prefrontal subdomains [125, 128].”
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Preclinical animal models of mental illnesses to translate findings from the bench to the bedside: Molecular brain mechanisms and peripheral biomarkers associated to early life stress or immune challenges
Cattane, N., Vernon, A. C., Borsini, A., Scassellati, C., Endres, D., Capuron, L., Tamouza, R., Benros, M. E., Leza, J. C., Pariante, C. M., et al. (2022) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2022.02.002 · Cited by 64 · see citing works
Placental CRH as a Signal of Pregnancy Adversity and Impact on Fetal Neurodevelopment
Kassotaki, I., Valsamakis, G., Mastorakos, G. P., & Grammatopoulos, D. K. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.714214 · Cited by 62 · see citing works
Autism spectrum disorders pathogenesis: Toward a comprehensive model based on neuroanatomic and neurodevelopment considerations
Béopoulos, A., Géa, M., Fasano, A., & Iris, F. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.988735 · Cited by 52 · see citing works
The relationship between pesticide exposure during critical neurodevelopment and autism spectrum disorder: A narrative review
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Developmental Neurotoxicity and Behavioral Screening in Larval Zebrafish with a Comparison to Other Published Results
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The Serotonin-Immune Axis in Preeclampsia
Gumusoglu, S. B., Scroggins, S. M., Vignato, J. A., Santillan, D. A., & Santillan, M. K. O. (2021) · Current Hypertension Reports · doi:10.1007/s11906-021-01155-4 · Cited by 43 · see citing works
The combination of fluoxetine and environmental enrichment reduces postpartum stress-related behaviors through the oxytocinergic system and HPA axis in mice
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Sensor behavior of transition-metals (X = Ag, Au, Pd, and Pt) doped Zn11-X-O12 nanostructured materials for the detection of serotonin
Louis, H., Patrick, M., Amodu, I. O., Benjamin, I., Ikot, I. J., Iniama, G. E., & Adeyinka, A. S. (2022) · Materials Today Communications · doi:10.1016/j.mtcomm.2022.105048 · Cited by 38 · see citing works
Fetal cannabidiol (CBD) exposure alters thermal pain sensitivity, problem-solving, and prefrontal cortex excitability
Swenson, K. S., Wulschner, L. E. G., Hoelscher, V. M., Folts, L. M., Korth, K. M., Oh, W. C., & Bates, E. A. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02130-y · Cited by 36 · see citing works
Serotonin-related rodent models of early-life exposure relevant for neurodevelopmental vulnerability to psychiatric disorders
Adjimann, T. S., Argañaraz, C., & Soiza‐Reilly, M. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01388-6 · Cited by 32 · see citing works
Comprehensive Review of the Impact of Maternal Stress on Fetal Development
Tadanki, D., Kaza, P., Meisinger, E., Syed, A., Johnson, A., Bainbridge, G., Cho, M., Anigbogu, C., & Gupta, G. (2025) · Pediatric Discovery · doi:10.1002/pdi3.70004 · Cited by 33 · see citing works
Targeting the brain 5-HT7 receptor to prevent hypomyelination in a rodent model of perinatal white matter injuries
Bokobza, C., Jacquens, A., Guenoun, D., Bianco, B., Galland, A., Pispisa, M., Cruz, A., Zinni, M., Faivre, V., Roumier, A., et al. (2022) · Journal of Neural Transmission · doi:10.1007/s00702-022-02556-8 · Cited by 23 · see citing works
Early Pregnancy Exposure to Ambient Air Pollution among Late-Onset Preeclamptic Cases Is Associated with Placental DNA Hypomethylation of Specific Genes and Slower Placental Maturation
Engström, K., Mandakh, Y., Garmire, L. X., Masoumi, Z. T., Isaxon, C., Malmqvist, E., Erlandsson, L., & Hansson, S. R. (2021) · Toxics · doi:10.3390/toxics9120338 · Cited by 23 · see citing works
Differential Serotonin Uptake Mechanisms at the Human Maternal–Fetal Interface
Baković, P., Kesić, M., Horvatiček, M., George, M., Perić, M., Bečeheli, I., Čičin‐Šain, L., Desoyé, G., Wadsack, C., Panzenboeck, U., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22157807 · Cited by 21 · see citing works
Identification and prediction model of placenta-brain axis genes associated with neurodevelopmental delay in moderate and late preterm children
Zhu, Y., Zhang, Y., Jin, Y., Jin, H., Huang, K., Tong, J., Gan, H., Rui, C., Lv, J., Wang, X., et al. (2023) · BMC Medicine · doi:10.1186/s12916-023-03023-1 · Cited by 20 · see citing works
Dysregulation of mTOR signaling mediates common neurite and migration defects in both idiopathic and 16p11.2 deletion autism neural precursor cells
Prem, S., Dev, B., Peng, C., Mehta, M., Alibutud, R., Connacher, R., Thomas, M. S., Zhou, X., Matteson, P. G., Xing, J., et al. (2024) · eLife · doi:10.7554/elife.82809 · Cited by 19 · see citing works
Melatonin ameliorates hypertension in hypertensive pregnant mice and suppresses the hypertension-induced decrease in Ca2+-activated K+ channels in uterine arteries
Sun, Y., Wang, C., Zhang, N., & Liu, F. (2021) · Hypertension Research · doi:10.1038/s41440-021-00675-5 · Cited by 18 · see citing works
Maternal Western-style diet reduces social engagement and increases idiosyncratic behavior in Japanese macaque offspring
Mitchell, A. J., Khambadkone, S. G., Dunn, G. A., Bagley, J. L., Tamashiro, K. L., Fair, D. A., Gustafsson, H., & Sullivan, E. L. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.07.004 · Cited by 16 · see citing works
Maternal Metabolic State and Fetal Sex and Genotype Modulate Methylation of the Serotonin Receptor Type 2A Gene (HTR2A) in the Human Placenta
Horvatiček, M., Perić, M., Bečeheli, I., Klasić, M., Žutić, M., Kesić, M., Desoyé, G., Radoš, S. N., Ivanišević, M., Hranilović, D., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10020467 · Cited by 15 · see citing works
Sex differences in offspring risk and resilience following 11β-hydroxylase antagonism in a rodent model of maternal immune activation
Martz, J., Shelton, M. A., Geist, L., Seney, M. L., & Kentner, A. C. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01771-5 · Cited by 12 · see citing works
Gestational administration of Bifidobacterium dentium results in intergenerational modulation of inflammatory, metabolic, and social behavior
Galley, J. D., King, M. K., Rajasekera, T. A., Batabyal, A., Woodke, S. T., & Gur, T. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.08.006 · Cited by 11 · see citing works
Gestational CBD Shapes Insular Cortex in Adulthood
Iezzi, D., Cáceres-Rodríguez, A., Pereira-Silva, J., Chavis, P., & Manzoni, O. J. (2024) · Cells · doi:10.3390/cells13171486 · Cited by 11 · see citing works
Socio-affective communication in Tph2-deficient rat pups: communal nesting aggravates growth retardation despite ameliorating maternal affiliation deficits
Wang, T., Homberg, J. R., Boreggio, L., Samina, M. C. F., Castro, R. C. R., Kolk, S. M., Alenina, N. V., Bäder, M., Dai, J., & Wöhr, M. (2024) · Molecular Autism · doi:10.1186/s13229-024-00629-x · Cited by 11 · see citing works
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Maternal Gestational Diabetes Influences DNA Methylation in the Serotonin System in the Human Placenta
Song, J. Y., Lee, K. E., Byeon, E. J., Choi, J., Kim, S. J., & Shin, J. E. (2022) · Life · doi:10.3390/life12111869 · Cited by 10 · see citing works
Placental Remote Control of Fetal Metabolism: Trophoblast mTOR Signaling Regulates Liver IGFBP-1 Phosphorylation and IGF-1 Bioavailability
Rosario, F. J., Chopra, A., Biggar, K. K., Powell, T. L., Gupta, M. B., & Jansson, T. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087273 · Cited by 10 · see citing works
Maternal anxiety‐driven modulation of fetal limbic connectivity designs a backbone linking neonatal brain functional topology to socio‐emotional development in early childhood
Canini, M., Pecco, N., Caglioni, M., Katušić, A., Išasegi, I. Ž., Oprandi, C., Scifo, P., Pozzoni, M., Lorioli, L., Garbetta, G., et al. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25207 · Cited by 10 · see citing works
Methylation of serotonin regulating genes in cord blood cells: association with maternal metabolic parameters and correlation with methylation in peripheral blood cells during childhood and adolescence
Bečeheli, I., Horvatiček, M., Perić, M., Nikolić, B., Holuka, C., Klasić, M., Ivanišević, M., Starčević, M., Desoyé, G., Hranilović, D., et al. (2024) · Clinical Epigenetics · doi:10.1186/s13148-023-01610-w · Cited by 9 · see citing works
Prenatal Stress Modulates Placental and Fetal Serotonin Levels and Determines Behavior Patterns in Offspring of Mice
Melnikova, V. I., Лифанцева, Н. В., Voronova, S. N., & Bondarenko, N. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252413565 · Cited by 9 · see citing works
Vilazodone exposure during pregnancy: Effects on embryo-fetal development, pregnancy outcomes and fetal neurotoxicity by BDNF/Bax-Bcl2/5-HT mediated mechanisms
Agrawal, P., Singh, P., & Singh, K. P. (2024) · NeuroToxicology · doi:10.1016/j.neuro.2024.10.012 · Cited by 8 · see citing works
Serotonergic mechanisms associated with experimental models of hypoxia: A systematic review
Carneiro, I. B. C., Toscano, A. E., da Cunha, M. D. S. B., Lacerda, D. C., Pontes, P. B., Manhães‐de‐Castro, R., Deiró, T. C. B. D. J., & Medeiros, J. M. B. (2022) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10226 · Cited by 8 · see citing works
Postnatal exposure to fluoxetine led to cognitive‐emotional alterations and decreased parvalbumin positive neurons in the hippocampus of juvenile Wistar rats
Meurer, Y. D. S. R., Linhares, S. S. G., Lima, A. D. C., de Aquino, A. C. Q., Brandão, L. E. M., Nôga, D. A., Campêlo, C. L. D. C., Lima, R. H., Cavalcante, J. S., Engelberth, R. C. G. J., et al. (2021) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10139 · Cited by 8 · see citing works
Metformin inhibits OCT3-mediated serotonin transport in the placenta
Váchalová, V., Kumnova, F., Synova, T., Anandam, K. Y., Abad, C., Karahoda, R., & Štaud, F. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.117399 · Cited by 7 · see citing works
Prenatal Stress and Adaptive Behavior of Offspring: The Role of Placental Serotonin
Бондаренко, Н. С., Voronova, S. N., Voronezhskaya, E. E., & Melnikova, V. I. (2022) · Doklady Biochemistry and Biophysics · doi:10.1134/s160767292202003x · Cited by 7 · see citing works
Ascorbic acid derived carbon dots promote circadian rhythm and contribute to attention deficit hyperactivity disorder
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Authors: Hanswijk, S. I., Spoelder, M., Shan, L., Verheij, M. M. M., Muilwijk, O. G., Li, W., Liu, C., Kolk, S. M., & Homberg, J. R.
Affiliations: Radboud University Medical Center (NL)
Netherlands Institute for Neuroscience (NL)
Dalian Medical University (CN)
Radboud University Nijmegen (NL)
Corresponding author: Homberg, Judith R.
ORCID: Hanswijk, Sabrina I.
Spoelder, Marcia
Shan, Ling
Verheij, Michel M. M.
Liu, Chunqing
Kolk, Sharon M.
Homberg, Judith R.
Venue: International Journal of Molecular Sciences
Publisher: MDPI AG
Published: 2020-08-14
Volume: 21
Issue: 16
Pages: 5850
ISSN: 1422-0067 (ISSN-L)
DOI: 10.3390/ijms21165850
PMC: PMC7461571
OpenAlex: W3049210532
Cited by: 86
References: 313
Citations by year: 2026: 16 · 2025: 14 · 2024: 14 · 2023: 12 · 2022: 15 · 2021: 14 · 2020: 1
FWCI: 1.80
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: International Journal of Molecular Sciences (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (submittedVersion, other-oa)
Radboud Repository (Radboud University) (submittedVersion)
Radboud Repository (Radboud University) (submittedVersion, other-oa)
Funders: Koninklijke Nederlandse Akademie van Wetenschappen (5305CDP09)
H2020 Marie Skłodowska-Curie Actions (707404)
Era-Net NEURON (RESPOND)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: serotonin, fetal brain development, gestational factors, maternal diet, maternal stress, maternal medication use, immune activation, maternal genotype, serotonergic system, thalamocortical circuits, hypothalamic-pituitary-adrenal axis, attention deficit hyperactivity disorder, autism spectrum disorder, depression, anxiety, neuropsychiatric disorders
MeSH terms: Animals, Behavior, Animal, Brain, Female, Fetus, Humans, Pregnancy, Serotonin, Stress, Physiological, Fetal Development

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Gestational Factors throughout Fetal Neurodevelopment: The Serotonin Link

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