Serotonin transporter transgenic (SERTcre) mouse line reveals developmental targets of serotonin specific reuptake inhibitors (SSRIs)
Open accessAbstract
The serotonin transporter gene (SLC6A4; synonyms, SERT, 5-HTT) is expressed much more broadly during development than in adulthood. To obtain a full picture of all sites of SERT expression during development we used a new mouse model where Cre recombinase was inserted into the gene encoding the serotonin transporter. Two reporter mouse lines, ROSA26R and the Tau(mGFP), allowed to map all the cells that express SERT at any point during development. Combined LacZ histochemistry and GFP immunolabelling showed neuronal cell bodies and axon fiber tracts. Earliest recombination in embryos was visible in the periphery in the heart and liver by E10.5 followed by recombination in the brain in raphe serotonergic neurons by E12.5. Further, recombination in non-serotonin neurons was visible in the choroid plexus, roof plate, and neural crest derivatives; by E15.5, recombination was found in the dorsal thalamus, cingulate cortex, CA3 field of the hippocampus, retinal ganglion cells, superior olivary nucleus and cochlear nucleus. Postnatally, SERT mediated recombination was visible in the medial prefrontal cortex and layer VI neurons in the isocortex. Recombined cells were co-labelled with Neu-N, but not with GAD67, and were characterized by long range projections (corpus callosum, fornix, thalamocortical). This fate map of serotonin transporter expressing cells emphasizes the broad expression of SERT in non-serotonin neurons during development and clarifies the localization of SERT expression in the hippocampus and limbic cortex. The identification of targets of SSRIs and serotonin releasers during embryonic and early postnatal life helps understanding the very diverse physiological consequences of administration of these drugs during development.
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Receptors, transporters as well as synthesizing enzymes are already expressed (~E10 rodent and week 4-5 human) even when the actual axonal projections have not yet arrived in the PFC.
“Receptors, transporters as well as synthesizing enzymes are already expressed (~E10 rodent and week 4–5 human) even when the actual axonal projections have not yet arrived in the PFC [236–240].”
From Development of prefrontal cortex (2022) · cites this paper as [237]
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Self-citationPostnatal Growth Defects in Mice with Constitutive Depletion of Central Serotonin
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Self-citationMillard, S. J., Weston–Green, K., & Newell, K. A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.06.008 · Cited by 81 · see citing works
“Developmental SERT expression on non- serotonergic neurons in the rodent brain ceases in the first two weeks of postnatal life (equivalent to birth in humans (Semple et al., 2013), and is localised to serotonergic neurons in the mature brain (Narboux-Nême et al., 2008).”
BackgroundHippocampal HDAC4 Contributes to Postnatal Fluoxetine-Evoked Depression-Like Behavior
Sarkar, A., Chachra, P., Kennedy, P., Pena, C. J., Desouza, L. A., Nestler, E. J., & Vaidya, V. A. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.73 · Cited by 79 · see citing works
“A possible reason for the differential effects of fluoxetine at these two ages could be the distinct patterns of serotonin transporter expression in the postnatal vs adult brain (Narboux-Nême et al, 2008).”
BackgroundSerotonylation and Transamidation of Other Monoamines
Muma, N. A., & Mi, Z. (2015) · ACS Chemical Neuroscience · doi:10.1021/cn500329r · Cited by 75 · see citing works
Serotonin-related pathways and developmental plasticity: relevance for psychiatric disorders
Dayer, A. G. (2014) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2014.16.1/adayer · Cited by 71 · see citing works
Soiza‐Reilly, M., Meye, F. J., Olusakin, J., Telley, L., Petit, E., Chen, X., Mameli, M., Jabaudon, D., Sze, J.-Y., & Gaspar, P. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0260-9 · Cited by 71 · see citing works
Self-citationde León-Reyes, N. S., Mederos, S., Varela, I., Weiss, L. A., Perea, G., Galazo, M. J., & Nieto, M. (2019) · Nature Communications · doi:10.1038/s41467-019-12495-w · Cited by 67 · see citing works
Rewiring of the Serotonin System in Major Depression
Vahid-Ansari, F., & Albert, P. R. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.802581 · Cited by 73 · see citing works
“Using 5-HTT-cre mice to drive reporter gene expression, labeling was seen in dorsal thalamus, cingulate cortex, hippocampal CA3 neurons, retinal ganglion cells, superior olivary and cochlear nuclei during embryonic development and postnatally in medial prefrontal cortex (97).”
MethodJha, S. C., Meltzer-Brody, S., Steiner, R. J., Cornea, E., Woolson, S., Ahn, M., Verde, A. R., Hamer, R. M., Zhu, H., Styner, M., et al. (2016) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2016.05.004 · Cited by 66 · see citing works
Development of Serotonergic Fibers in the Post-Natal Mouse Brain
Maddaloni, G., Bertero, A., Pratelli, M., Barsotti, N., Boonstra, A., Giorgi, A. U. D., Migliarini, S., & Pasqualetti, M. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00202 · Cited by 71 · see citing works
“Furthermore, SERT is transiently expressed in non-serotonergic neurons in the developing brain (Lebrand et al., 1998; Narboux-Nême et al., 2008).”
BackgroundLeptin Does Not Directly Affect CNS Serotonin Neurons to Influence Appetite
Lam, D. D., Leinninger, G. M., Louis, G. W., Garfield, A. S., Marston, O. J., Leshan, R. L., Scheller, E. L., Christensen, L., Donato, J., Xia, J., et al. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.03.016 · Cited by 69 · see citing works
“onto the conditional Leprfl background and the ROSA26-reporter alleles that express EGFP/EYFP following cre-dependent excision (Mao et al., 1999; McMinn et al., 2005; Narboux-Neme et al., 2008).”
BackgroundExcess 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
“cortical anlage receives the innervation of thalamo-cortical axons that express high levels of SERT allowing them to actively reuptake serotonin from the extracellular space.(31,32)”
BackgroundMarek, G. J. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_480 · Cited by 63 · see citing works
“…htr2a gene rescue experiment for the thalamus appears to have been compromised by the use of a promoter that is weakly expressed in the midline and intralaminar thalamic nuclei compared to a robust expression in the primary sensory thalamic nuclei (Lebrand et al. 1996; Narboux-Neme et al. 2008).”
BackgroundCalabrese, F., Guidotti, G., Middelman, A., Racagni, G., Homberg, J. R., & Riva, M. A. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8449-z · Cited by 60 · see citing works
New insights into how serotonin selective reuptake inhibitors shape the developing brain
Gingrich, J. A., Malm, H., Ansorge, M. S., Brown, A., Sourander, A., Suri, D., Teixeira, C. M., Caffrey Cagliostro, M. K., Mahadevia, D., & Weissman, M. M. (2017) · Birth Defects Research · doi:10.1002/bdr2.1085 · Cited by 53 · see citing works
“…other systems as well, because the transient ectopic expression of 5-HT transporter during development is also observed in other sensory, thalamic, hippocampal, hypothalamic, and prefrontal cortical neurons throughout development in rodents (Lebrand et al., 1996, 1998; Narboux-Neme et al., 2008).”
BackgroundKoch, S. M., Cruz, C. G. D., Hnasko, T. S., Edwards, R. H., Huberman, A. D., & Ullian, E. M. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.045 · Cited by 60 · see citing works
“The direct contributions of synaptic transmission to this process, however, remain unclear.”
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
“This spanned virtually all stages of brain 5-HT development (Hansson et al., 1998; Homberg et al., 2010; Johnston and Coyle 1980; Lauder and Bloom 1975; Narboux-Neme et al., 2008; Olivier et al., 2011; Zhou et al., 2000).”
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
“Apart from being expressed in 5-HT neurons, the 5-HTT is also transiently expressed in non-aminergic neurons, belonging to many topographically distinct brain areas (Lebrand et al., 1998; Zhou et al., 2000; Narboux-Neme et al., 2008; Kalueff et al., 2010).”
BackgroundInfluentialAscl1 Is Required for the Development of Specific Neuronal Subtypes in the Enteric Nervous System
Memic, F., Knoflach, V., Sadler, R., Tegerstedt, G., Sundström, E., Guillemot, F., Pachnis, V., & Marklund, U. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0202-16.2016 · Cited by 53 · see citing works
“However, SERT has been shown to be expressed in nonserotonergic cells in other parts of the developing PNS and in the CNS (Narboux-Nême et al., 2008; Chen et al., 2015).”
BackgroundZhang, Z., Rasmussen, L., Saraswati, M., Koehler, R., Robertson, C., & Kannan, S. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2017.5450 · Cited by 49 · see citing works
Wiring and Volume Transmission: An Overview of the Dual Modality for Serotonin Neurotransmission
Gianni, G., & Pasqualetti, M. (2023) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.3c00648 · Cited by 44 · see citing works
Belmer, A., Klenowski, P. M., Patkar, O. L., & Bartlett, S. E. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1278-x · Cited by 47 · see citing works
“To determine whether the proportion of putative excitatory/inhibitory synapses contributed to the number excitatory/inhibitory triads identified in each brain region, we performed Pearson correlation analysis on their respective ratios within the brain areas analyzed.”
BackgroundMethodTrowbridge, S., Narboux‐Nême, N., & Gaspar, P. (2011) · The Anatomical Record · doi:10.1002/ar.21248 · Cited by 45 · see citing works
Self-citationLiu, Y., Shan, L., Liu, T., Li, J., Chen, Y., Sun, C., Yang, C., Bian, X., Niu, Y., Zhang, C., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.02.010 · Cited by 45 · see citing works
Pelosi, B., Migliarini, S., Pacini, G., Pratelli, M., & Pasqualetti, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104318 · Cited by 47 · see citing works
Arakawa, H., Suzuki, A., Zhao, S., Tsytsarev, V., Lo, F., Hayashi, Y., Itohara, S., Iwasato, T., & Erzurumlu, R. S. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1663-14.2014 · Cited by 45 · see citing works
“most part similar between Tg208 and Tg810 (n 90 in total) and similar to those previously reported for 5-HTTCre knock-in mice, in which an allele of endogenous 5-HTT gene is inserted and disrupted by the Cre recombinase gene (Zhuang et al., 2005; Narboux-Nême et al., 2008).”
BackgroundResultReisoli, E., Lucchini, S. D., Nardi, I., & Ori, M. (2010) · Development · doi:10.1242/dev.041079 · Cited by 44 · see citing works
“A specific population of neuroepithelial cells in Xenopus gills has also been shown to contain 5-HT (Saltys et al., 2006) and 5-HT uptake sites have been described in mammalian branchial arches and cranial NCCs (Shuey et al., 1993; Hansson et al., 1999; Narboux-Neme et al., 2008).”
BackgroundYu, F., Huang, S., Zhang, H., Ye, H., Chi, H., Zou, Y., Lv, R., & Zheng, X.-B. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i12.3451 · Cited by 43 · see citing works
Diaz, S. L., Narboux‐Nême, N., Trowbridge, S., Scotto‐Lomassese, S., Kleine Borgmann, F. B., Jessberger, S., Giros, B., Maroteaux, L., Deneris, E., & Gaspar, P. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12297 · Cited by 41 · see citing works
Self-citationThalamic neuronal specification and early circuit formation
Gezelius, H., & López‐Bendito, G. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22460 · Cited by 41 · see citing works
“The Sert gene has been used as a driver to generate various mouse lines with selective activity in principal neurons of the thalamus (Narboux-Nême et al., 2008; Arakawa et al., 2014; Mizuno et al., 2014).”
MethodFluoxetine Suppresses Glutamate- and GABA-Mediated Neurotransmission by Altering SNARE Complex
Lazarevic, V., Mantas, I., Flais, I., & Svenningsson, P. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174247 · Cited by 39 · see citing works
“It was shown that SERT is transiently expressed during early postnatal days in the cortical layer VI, layer II of retrosplenial cortex, and CA3 of HPC [30,31].”
BackgroundComprehensive topographical map of the serotonergic fibers in the male mouse brain
Awasthi, J. R., Tamada, K., Overton, E. T. N., & Takumi, T. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.25027 · Cited by 37 · see citing works
The role of teratogens in neural crest development
Cerrizuela, S., Vega‐López, G. A., & Aybar, M. J. (2020) · Birth Defects Research · doi:10.1002/bdr2.1644 · Cited by 38 · see citing works
Laurent, L., Huang, C., Ernest, S. R., Bérard, A., Vaillancourt, C., & Hales, B. F. (2016) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.23537 · Cited by 33 · see citing works
Effect of the 5-HT4 receptor and serotonin transporter on visceral hypersensitivity in rats
Chi, Y., Liu, X., Hua-Hong, W., Li, J., & Li, Y.-X. (2012) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2012007500122 · Cited by 32 · see citing works
Thalamus mediates neocortical Down state transition via GABAB-receptor-targeting interneurons
Hay, Y. A., Deperrois, N., Fuchsberger, T., Quarrell, T. M., Koerling, A.-L., & Paulsen, O. (2021) · Neuron · doi:10.1016/j.neuron.2021.06.030 · Cited by 30 · see citing works
Divergent Roles of Central Serotonin in Adult Hippocampal Neurogenesis
Song, N., Huang, Y., Yu, X., Lang, B., Ding, Y., & Zhang, L. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00185 · Cited by 32 · see citing works
“In Sert-Cre mice, however, Cre recombinase expression is not limited in 5-HTergic neurons (Narboux-Neme et al., 2008), and this may lead to Vmat2 deletion in other neurons.”
BackgroundSprowles, J. L. N., Wendel, J. R. H., Gutierrez, A., Bailey, R. A., Jablonski, S. A., Williams, M. T., & Vorhees, C. V. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.06.004 · Cited by 31 · see citing works
“SERT is transiently expressed in some regions as early as embryonic day (E) 11 and aids organization of neuronal connectivity by maintaining 5-HT near target receptors (Gaspar et al., 2003; Homberg et al., 2010; Narboux-Neme et al., 2008; Olivier et al., 2011a).”
BackgroundRORα Coordinates Thalamic and Cortical Maturation to Instruct Barrel Cortex Development
Vitalis, T., Dauphinot, L., Gressèns, P., Potier, M., Mariani, J., & Gaspar, P. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx262 · Cited by 28 · see citing works
Self-citationMinireview: A Skeleton in Serotonin’s Closet?
Kawai, M., & Rosen, C. J. (2010) · Endocrinology · doi:10.1210/en.2010-0499 · Cited by 29 · see citing works
Garcia, L. P., Witteveen, J. S., Middelman, A., van Hulten, J. A., Martens, G. J. M., Homberg, J. R., & Kolk, S. M. (2019) · Molecular Neurobiology · doi:10.1007/s12035-018-1105-x · Cited by 28 · see citing works
“Narboux-Nème and colleagues [60] elegantly showed a transient 5-HTTexpression within layers II, V, and VI of the mPFC at E15.”
The relationship between the placental serotonin pathway and fetal growth restriction
Ranzil, S., Walker, D. W., Borg, A. J., Wallace, E. M., Ebeling, P. R., & Murthi, P. (2018) · Biochimie · doi:10.1016/j.biochi.2018.12.016 · Cited by 28 · see citing works
The deletion of the microtubule‐associated STOP protein affects the serotonergic mouse brain network
Fournet, V., Jany, M., Fabre, V., Chali, F., Orsal, D., Schweitzer, A., Andrieux, A., Messanvi, F., Bruno Giros, A., Hamon, M., et al. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07064.x · Cited by 28 · see citing works
Bonnin, A., Zhang, L., Blakely, R., & Levitt, P. R. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.35 · Cited by 27 · see citing works
Warkus, E. L. L., & Marikawa, Y. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy143 · Cited by 27 · see citing works
Vyas, P., Wu, J. S., Jimenez, A., Glowatzki, E., & Fuchs, P. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-41770-5 · Cited by 26 · see citing works
Zhou, X., Lu, J. Y.-F., Darling, R. D., Simpson, K. L., Zhu, X., Wang, F., Yu, L., Sun, X., Merzenich, M. M., & Lin, R. C. S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1416582111 · Cited by 26 · see citing works
“Serotonin is also known to take up (via norepinephrine transporter) 5-HT transiently in the noradrenergic locus coeruleus (LC) system during early development (31, 33), and it is again likely that noradrenergic circuitry may be affected by CTM exposure.”
BackgroundUnraveling new roles for serotonin receptor 2B in development: key findings from Xenopus
Ori, M., Lucchini, S. D., Marras, G., & Nardi, I. (2013) · The International Journal of Developmental Biology · doi:10.1387/ijdb.130204mo · Cited by 25 · see citing works
“In mice uptake of 5-HT during early development is first observed in non-neural tissues such as the heart, the liver, the cranial mesenchyme, the migrating cranial neural crest cells (NCCs), dorsal ganglia and retinal ganglion cells (Lauder and Zimmerman, 1988; Narboux-Nème et al., 2008).”
BackgroundOlusakin, J., Moutkine, I., Dumas, S., Ponimaskin, E. G., Païzanis, E., Soiza‐Reilly, M., & Gaspar, P. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0775-z · Cited by 24 · see citing works
“While SERT is expressed exclusively in the 5-HT-producing neurons of the raphe nuclei in adult brain, it has a broader expression during fetal and early postnatal life in rodents [12, 13] and primates including humans [[14, 15]; http://www.”
BackgroundSelf-citationHeart valve cardiomyocytes of mouse embryos express the serotonin transporter SERT
Pavone, L. M., Spina, A., Muto, R. L., Santoro, D., Mastellone, V., & Avallone, L. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.09.152 · Cited by 23 · see citing works
Self-citationThalamic adenylyl cyclase 1 is required for barrel formation in the somatosensory cortex
Suzuki, A., Lee, L., Hayashi, Y., Muglia, L. M., Itohara, S., Erzurumlu, R. S., & Iwasato, T. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.043 · Cited by 23 · see citing works
“043 thalamus and raphe during early postnatal development (Allen-Developing-Mouse-Brain-Atlas; Lebrand et al., 1998; Narboux-Neme et al., 2008).”
BackgroundInfluentialWhitaker‐Azmitia, P. M. (2010) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(10)70086-2 · Cited by 23 · see citing works
Molecular biology of serotonergic systems in avian brains
Fujita, T., Aoki, N., Mori, C., Homma, K. J., & Yamaguchi, S. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1226645 · Cited by 21 · see citing works
“It should be noted that Sert is transiently expressed in non-serotonergic neurons in several brain regions during development (Lebrand et al., 1996; Narboux-Nême et al., 2008).”
BackgroundDopamine–mediated immunomodulation affects choroid plexus function
Castellani, G., Contarini, G., Mereu, M., Albanesi, E., Devroye, C., D’Amore, C., Ferretti, V., Martin, S. D., & Papaleo, F. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.06.006 · Cited by 22 · see citing works
Serotonin activates cell survival and apoptotic death responses in cultured epithelial thyroid cells
Cerulo, G., Tafuri, S., Pasquale, V. D., Rea, S., Romano, S., Costagliola, A., Morte, R. D., Avallone, L., & Pavone, L. M. (2014) · Biochimie · doi:10.1016/j.biochi.2014.06.020 · Cited by 21 · see citing works
“The transporter SERT is targeted by many antidepressant drugs, including the selective serotonin reuptake inhibitors (SSRI), and psycho-stimulants such as cocaine, amphetamine and related drugs [14].”
BackgroundSelf-citationPinheiro, I. L., da Silva, A. I., Reginato, A., Silva‐Filho, R., Galindo, L. C. M., de Matos, R. J. B., Ferraz, J. C., Toscano, A. E., Milanski, M., Manhães‐de‐Castro, R., et al. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.07.038 · Cited by 21 · see citing works
“The use of SSRIs during gestation or childhood can modify properties of neurons expressing SERT through changes in their specific transcription or changes in their gene expression [37].”
Grieb, Z. A., & Ragan, C. M. (2019) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2019.07.239 · Cited by 21 · see citing works
Kast, R. J., Wu, H.-H., Williams, P., Gaspar, P., & Levitt, P. (2017) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00020 · Cited by 20 · see citing works
Self-citationSerotonergic regulation of bipolar cell survival in the developing cerebral cortex
Wong, F. K., Selten, M. M., Rosés-Novella, C., Sreenivasan, V., Pallas‐Bazarra, N., Serafeimidou‐Pouliou, E., Hanusz-Godoy, A., Oozeer, F., Edwards, R. H., & Marín, Ó. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111037 · Cited by 19 · see citing works
Hou, G., & Zhang, Z.-W. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00353 · Cited by 20 · see citing works
“The hyperpolarization-activated current (Ih) plays important roles in the regulation of neuronal intrinsic excitability during development and in adult (Robinson and Siegelbaum, 2003; Bender and Baram, 2008; Biel et al., 2009; Noam et al., 2011).”
BackgroundPrenatal antidepressant exposure and sex differences in neonatal corpus callosum microstructure
Campbell, K. S. J., Williams, L. J., Björnson, B., Weik, E., Brain, U. M., GRUNAU, R. E., Miller, S. P., & Oberlander, T. F. (2021) · Developmental Psychobiology · doi:10.1002/dev.22125 · Cited by 19 · see citing works
Beyond Gene Inactivation: Evolution of Tools for Analysis of Serotonergic Circuitry
Hainer, C., Mosienko, V., Koutsikou, S., Crook, J. J., Gloss, B. R., Kasparov, S., Lumb, B. M., & Alenina, N. V. (2015) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00045 · Cited by 18 · see citing works
Murray, K. D., Liu, X.-B., King, A. N., Luu, J. D., & Cheng, H.-J. (2020) · eNeuro · doi:10.1523/eneuro.0030-20.2020 · Cited by 19 · see citing works
“CreERT2 recombinase activity in Gli1-CreERT2;TaumGFP mice leads to expression of membrane localized EGFP (Narboux-Nême et al., 2008; Dondzillo et al., 2010; Gangarossa et al., 2012).”
Assali, A., Magueresse, C. L., Bennis, M., Nicol, X., Gaspar, P., & Rebsam, A. (2017) · Scientific Reports · doi:10.1038/s41598-017-03361-0 · Cited by 18 · see citing works
Self-citationIn Utero Exposure to Citalopram Mitigates Maternal Stress Effects on Fetal Brain Development
Velasquez, J. C., Zhao, Q., Chan, Y., Galindo, L. C. M., Simasotchi, C., Wu, D., Hou, Z., Herod, S. M., Oberlander, T. F., Gil, S., et al. (2019) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.9b00180 · Cited by 18 · see citing works
ErbB4 knockdown in serotonergic neurons in the dorsal raphe induces anxiety-like behaviors
Zhang, S.-R., Wu, J., Chen, H. H., Luo, R., Chen, W., Tang, L., Li, X., Yang, J., & Gao, T. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0601-7 · Cited by 17 · see citing works
Maternal Pharmacokinetics and Fetal Disposition of (±)-Citalopram during Mouse Pregnancy
Velasquez, J. C., Goeden, N., Herod, S. M., & Bonnin, A. (2016) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00287 · Cited by 17 · see citing works
Dudok, J. J., Groffen, A. J. A., Toonen, R. F. G., & Verhage, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028137 · Cited by 16 · see citing works
“However, SERT is also transiently expressed in some other brain regions during development, such as the thalamocortical neurons [16,17].”
Backgroundde Leeuw, V. C., Hessel, E. V. S., Pennings, J. L. A., Hodemaekers, H. M., Wackers, P. F. K., van Oostrom, C. T. M., & Piersma, A. H. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.09.014 · Cited by 16 · see citing works
Kurahashi, H., Kunisawa, K., Tanaka, K. F., Kubota, H., Hasegawa, M., Miyachi, M., Moriya, Y., Hasegawa, Y., Nagai, T., Saito, K., et al. (2024) · Neuropsychopharmacology · doi:10.1038/s41386-024-02004-z · Cited by 15 · see citing works
Cortical influences of serotonin and glutamate on layer V pyramidal neurons
Marek, G. J., & Schoepp, D. D. (2021) · Progress in brain research · doi:10.1016/bs.pbr.2020.11.002 · Cited by 15 · see citing works
Fate Map of Serotonin Transporter‐Expressing Cells in Developing Mouse Thyroid
Spina, A., Rea, S., Pasquale, V. D., Mastellone, V., Avallone, L., & Pavone, L. M. (2011) · The Anatomical Record · doi:10.1002/ar.21353 · Cited by 15 · see citing works
“During development, SERT is expressed much more broadly than in adults in several non-serotonin neurons of the brain and in neural crest derivatives (Hansson et al., 1999; Narboux-Nême et al., 2008).”
BackgroundSelf-citationPavone, L. M., & Norris, R. A. (2013) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-013-9606-8 · Cited by 15 · see citing works
“[6] suggest that blocking 5-HT uptake during pregnancy could affect fetal valve development and may provide an explanation for why selective serotonin reuptake inhibitors (SSRIs) have been associated with increased risk of cardiac malformations [26].”
Self-citationThe teratogenic effects of sertraline in mice
Cabrera, R. M., Lin, Y. L., Law, E., Kim, J., & Wlodarczyk, B. J. (2020) · Birth Defects Research · doi:10.1002/bdr2.1660 · Cited by 14 · see citing works
Perinatal SSRI exposure impacts innate fear circuit activation and behavior in mice and humans
Zanni, G., van Dijk, M. T., Cagliostro, M. K. C., Sepúlveda, P., Pini, N., Rose, A. L., Kesin, A. L., Lugo-Candelas, C. I., Gonçalves, P. D., MacKay, A. S., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-58785-4 · Cited by 13 · see citing works
Sánchez, N., Juárez-Balarezo, J., Olhaberry, M., Oneto, H. G., Muzard, A., Mardonez, M. J., Franco, P., Barrera, F., & Gaete, M. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.632766 · Cited by 13 · see citing works
Serotonin regulates contractile activity of the uterus in non-pregnant rabbits
Lychkova, A. E., Pasquale, V. D., Avallone, L., Puzikov, A. M., & Pavone, L. M. (2014) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2014.05.006 · Cited by 13 · see citing works
Self-citationImpact of selective serotonin reuptake inhibitors on neural crest stem cell formation
Vichier-Guerre, C., Parker, M. M., Pomerantz, Y., Finnell, R. H., & Cabrera, R. M. (2017) · Toxicology Letters · doi:10.1016/j.toxlet.2017.08.012 · Cited by 12 · see citing works
Baudat, M., de Kort, A. R., van den Hove, D., & Joosten, E. A. J. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15544 · Cited by 10 · see citing works
“In the PFC, SERT is expressed in glutamatergic pyramidal neurons between P 0 and P 10 (Narboux-Nême et al., 2008; Soiza-Reilly et al., 2019).”
BackgroundSex differences in serotonergic control of rat social behaviour
Poceviciute, I., Kasperaviciute, K., Buišas, R., Rukšėnas, O., & Vengeliene, V. (2023) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2023.173533 · Cited by 11 · see citing works
- Authors
- Narboux-Nême, N., Pavone, L. M., Avallone, L., Zhuang, X., & Gaspar, P.
- Affiliations
- University of Naples Federico II (IT)
- University of Chicago (US)
- Venue
- Neuropharmacology
- Publisher
- Elsevier BV
- Published
- 2008-11
- Volume
- 55
- Issue
- 6
- Pages
- 994-1005
- ISSN
- 0028-3908 (ISSN-L)
- OpenAlex
- W2013740680
- Cited by
- 148
- References
- 72
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 4 · 2023: 5 · 2022: 3 · 2021: 13 · 2020: 16 · 2019: 11 · 2018: 9 · 2017: 14 · 2016: 10 · 2015: 6 · 2014: 11 · 2013: 6 · 2012: 6
- FWCI
- 3.46
- Type
- journal article
- Language
- en
- Open access
- Licence
- Locations
- Neuropharmacology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- INFM-OAR (INFN Catania) (submittedVersion, other-oa)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
- Funders
- European Commission (201714)
- Agence Nationale de la Recherche
- Institut National de la Santé et de la Recherche Médicale
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- serotonin transporter, selective serotonin reuptake inhibitors, developmental gene expression, Cre recombinase, fate mapping, embryonic development, choroid plexus, neural crest derivatives, hippocampus, limbic cortex, medial prefrontal cortex, axonal projections
- MeSH terms
- Animals, Embryo, Mammalian, Mice, Transgenic, Neurons, Raphe Nuclei, Serotonin, tau Proteins, Selective Serotonin Reuptake Inhibitors, Gene Expression Regulation, Developmental, Integrases, Green Fluorescent Proteins, Serotonin Plasma Membrane Transport Proteins, Mice
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