The Thalamus Regulates Retinoic Acid Signaling and Development of Parvalbumin Interneurons in Postnatal Mouse Prefrontal Cortex

Larsen, Rachel A.; Proue, Alatheia; Scott, Earl Parker; Christiansen, Matthew; Nakagawa, Yasushi

doi:10.1523/eneuro.0018-19.2019

Cited by 24 publications

(20 citation statements)

References 146 publications

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“…Interestingly, there is a ventro-lateral and dorso-lateral expansion of ALDH1A3 expression in the mid-fetal primate neocortex, similar to the expansion of PFC-MD connectivity in primates, and a posterior shift of Cyp26b1 expression, co-incident with posterior expansion of the primate PFC. Long-range connectivity with the thalamus has previously been shown to be integral for specification of the primary and secondary sensory cortex 11 , and was recently reported to regulate Cyp26b1 in the mouse frontal cortex 38 . Of note, mid-fetal cortical development in human and macaque, and equivalent perinatal/neonatal development in mice, is a critical period for laminar and areal specification of neurons, onset of dendritic growth and synaptogenesis, axon pathfinding, and ingression of thalamocortical axons 28 .…”

Section: Resultsmentioning

confidence: 97%

“…RA is a diffusible biologically active derivative of vitamin A previously implicated in neurogenesis, differentiation and synaptic function of cortical neurons 24, 25, 29, 30, 33–38 . RA is also known to exert a trophic influence on nascent neurons to promote axon and dendritic outgrowth 33, 35, 39, 40 as well as synaptogenesis 35, 41 .…”

Section: Introductionmentioning

confidence: 99%

“…Whereas heterozygotes appear normal and are fertile, mice with constitutive deletion of Cyp26b1 exhibited various body malformations and died perinatally. Nevertheless, it has been previously shown that the genetic deletion of Cyp26b1 in mice resulted in expansion of RA signaling in multiple organs prenatally 54 and the postnatal mouse mPFC 38 . Consistent with previous findings in humans 32 and mice 38 , CYP26B1 is upregulated in M1C compared to the PFC during human mid-fetal development (Fig.…”

Section: Introductionmentioning

confidence: 99%

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Regulation of Prefrontal Patterning, Connectivity and Synaptogenesis by Retinoic Acid

Shibata

Pattabiraman

Lorente-Galdós

et al. 2019

Preprint

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33The prefrontal cortex (PFC) and its reciprocal connections with the mediodorsal 34 thalamus (MD) are crucial for cognitive flexibility and working memory 1-4 and are 35 thought to be altered in several disorders such as autism spectrum disorder 5, 6 36 and schizophrenia 6-9 . While developmental mechanisms governing regional 37 patterning of the rodent cerebral cortex have been characterized 10-15 , the 38 mechanisms underlying the development of PFC-MD connectivity and the lateral 39 expansion of PFC with distinct granular layer 4 in anthropoid primates 16-23 have 40 not been elucidated. Here we report increased concentration of retinoic acid (RA), 41 a signaling molecule involved in brain development and function 24,25 in the 42 prospective PFC areas of human and macaque, compared to mouse, during mid-43 fetal development, a crucial period for cortical circuit assembly. In addition, we 44 observed the lateral expansion of RA synthesizing enzyme, ALDH1A3, 45 expression in mid-fetal macaque and human frontal cortex, compared to mouse. 46 Furthermore, we found that enrichment of RA signaling is restricted to the 47 prospective PFC by CYP26B1, a gene encoding an RA-catabolizing enzyme 48 upregulated in the mid-fetal motor cortex. Gene deletion in mice revealed that RA 49 signaling through anteriorly upregulated RA receptors, Rxrg and Rarb, and 50 Cyp26b1-dependent catabolism is required for the proper molecular patterning 51 of PFC and motor areas, the expression of the layer 4 marker RORB, intra-PFC 52 synaptogenesis, and the development of reciprocal PFC-MD connectivity. 53

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Section: Resultsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Regulation of Prefrontal Patterning, Connectivity and Synaptogenesis by Retinoic Acid

Shibata

Pattabiraman

Lorente-Galdós

et al. 2019

Preprint

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“…This is not surprising given that the mammalian frontal cortex is one of the few brain regions where RA is synthesized (Wagner et al, 2006). Interestingly, the RA-degrading enzyme CYP26B1 is also found to regulate parvalbumin (PV)-expressing interneurons in the mouse medial PFC, and RA signaling has thus been suggested to play a crucial role in establishing connections between the thalamus and PFC (Larsen et al, 2019). Importantly, abnormal reductions in retinoid signaling were already found in the prefrontal cortex of depressed patients (Qi et al, 2015).…”

Section: Retinoid and The Orbitofrontal Cortex (Ofc/ventromedial Prefmentioning

confidence: 99%

Retinoic acid and depressive disorders: Evidence and possible neurobiological mechanisms

Dam

Wang

et al. 2020

Neuroscience & Biobehavioral Reviews

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The retinoid family members, including vitamin A and derivatives like 13-cis-retinoic acid (ITT) and all-trans retinoic acid (ATRA), are essential for normal functioning of the developing and adult brain. When vitamin A intake is excessive, however, or after ITT treatment, increased risks have been reported for depression and suicidal ideation. Here, we review pre-clinical and clinical evidences supporting association between retinoids and depressive disorders and discuss several possible underlying neurobiological mechanisms. Clinical evidences include case reports and studies from healthcare databases and government agency sources. Preclinical studies further confirmed that RA treatment induces hyperactivity of the hypothalamus-pituitary-adrenal (HPA) axis and typical depressive-like behaviors. Notably, the molecular components of the RA signaling are widely expressed throughout adult brain. We further discuss three most important brain systems, hippocampus, hypothalamus and orbitofrontal cortex, as major brain targets of RA. Finally, we highlight altered monoamine systems in the pathophysiology of RA-associated depression. A better understanding of the neurobiological mechanisms underlying RA-associated depression will provide new insights in its etiology and development of effective intervention strategies.

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“…CYP26B1) [240,247], and the already mentioned sensitivity of the dopamine neurotransmitter system, particularly D2R, to RA interference (see "Affective disorders -altered mood, depression, and suicide" section) [outlined in 246]. Besides the dopamine system, also γ-amino butyric acid (GABA)-ergic interneurons in the prefrontal cortex, whose aberrant development is associated with neurological disorders including schizophrenia, have been shown to be sensitive to RA [248].…”

Section: Schizophreniamentioning

confidence: 99%

Highlighting the gaps in hazard and risk assessment of unregulated Endocrine Active Substances in surface waters: retinoids as a European case study

et al. 2021

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Regulatory hazard and risk assessment of endocrine-active substances currently specifies four modes of action: interference with sex hormone (oestrogen, androgen) pathways, steroidogenesis, and thyroid hormone signalling. This does not encompass the full complexity of the endocrine system and its extended interfaces with environmental pollutants that can potentially disrupt the carefully maintained balance. Here we take the retinoid signalling pathway as a European case study for both, under- and unregulated endocrine pathways and outline the different levels of interference, discuss their adversity, and indicate crosstalk to other signalling pathways. Retinoid compounds already exist in drinking water sources, occur naturally in cyanobacterial blooms and/or enter surface waters via wastewater discharge, where they pose a potential hazard to the environment and human health - a situation that can be expected to worsen due to water shortages induced by climate-change and population growth. We briefly review relevant aspects of current endocrine disruptor (ED) testing for regulatory purposes and then expand upon the needs for inclusion of disruption of retinoid signalling in (ED) regulatory safety assessment contributing to adverse health outcomes that include cognitive function and neurological disease. An overview of developmental effects of retinoid signalling disruption across species highlights critical processes and potential crosstalk with other signalling pathways. A focused weight of evidence-based evaluation of the biologically plausible associations between neurological disorders and altered retinoid signalling highlights the evidence gaps. We show that monitoring only a limited number of anthropogenic priority chemicals in water is insufficient to address the environmental risks of retinoid signalling disruption. To comprehensively assess impacts on the endpoints, processes, and pathways of the endocrine system that are most vulnerable to chemical interference we need further investigation of the true mixture composition in environmental matrices. On a weight of evidence-basis this information can then be integrated into a reliable, inclusive, quantitative approach that ultimately accommodates all the critical pathways. By focusing on the retinoid signalling pathway, we intend to improve the scope and relevance of an integrated approach for the risk assessment of endocrine disruptors.

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The Thalamus Regulates Retinoic Acid Signaling and Development of Parvalbumin Interneurons in Postnatal Mouse Prefrontal Cortex

Abstract: Visual Abstract

Cited by 24 publications

References 146 publications

Regulation of Prefrontal Patterning, Connectivity and Synaptogenesis by Retinoic Acid

Regulation of Prefrontal Patterning, Connectivity and Synaptogenesis by Retinoic Acid

Retinoic acid and depressive disorders: Evidence and possible neurobiological mechanisms

Highlighting the gaps in hazard and risk assessment of unregulated Endocrine Active Substances in surface waters: retinoids as a European case study

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