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      Tangential Intrahypothalamic Migration of the Mouse Ventral Premamillary Nucleus and Fgf8 Signaling

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          Abstract

          The tuberal hypothalamic ventral premamillary nucleus (VPM) described in mammals links olfactory and metabolic cues with mating behavior and is involved in the onset of puberty. We offer here descriptive and experimental evidence on a migratory phase in the development of this structure in mice at E12.5–E13.5. Its cells originate at the retromamillary area (RM) and then migrate tangentially rostralward, eschewing the mamillary body, and crossing the molecularly distinct perimamillary band, until they reach a definitive relatively superficial ventral tuberal location. Corroborating recent transcriptomic studies reporting a variety of adult glutamatergic cell types in the VPM, and different projections in the adult, we found that part of this population heterogeneity emerges already early in development, during tangential migration, in the form of differential gene expression properties of at least 2–3 mixed populations possibly derived from subtly different parts of the RM. These partly distribute differentially in the core and shell parts of the final VPM. Since there is a neighboring acroterminal source of Fgf8, and Fgfr2 is expressed at the early RM, we evaluated a possible influence of Fgf8 signal on VPM development using hypomorphic Fgf8 neo/null embryos. These results suggested a trophic role of Fgf8 on RM and all cells migrating tangentially out of this area (VPM and the subthalamic nucleus), leading in hypomorphs to reduced cellularity after E15.5 without alteration of the migrations proper.

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          Forebrain gene expression domains and the evolving prosomeric model.

          The prosomeric model attributes morphological meaning to gene expression patterns and other data in the forebrain. It divides this territory into the same transverse segments (prosomeres) and longitudinal zones in all vertebrates. The axis and longitudinal zones of this model are widely accepted but controversy subsists about the number of prosomeres and their nature as segments. We describe difficulties encountered in establishing continuity between prosomeric limits postulated in the hypothalamus and intra-telencephalic limits. Such difficulties throw doubt on the intersegmental nature of these limits. We sketch a simplified model, in which the secondary prosencephalon (telencephalon plus hypothalamus) is a complex protosegment not subdivided into prosomeres, which exhibits patterning singularities. By contrast, we continue to postulate that prosomeres p1-p3 (i.e. the pretectum, thalamus and prethalamus) are the caudal forebrain.
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            A genomic atlas of mouse hypothalamic development.

            The hypothalamus is a central regulator of many behaviors that are essential for survival, such as temperature regulation, food intake and circadian rhythms. However, the molecular pathways that mediate hypothalamic development are largely unknown. To identify genes expressed in developing mouse hypothalamus, we performed microarray analysis at 12 different developmental time points. We then conducted developmental in situ hybridization for 1,045 genes that were dynamically expressed over the course of hypothalamic neurogenesis. We identified markers that stably labeled each major hypothalamic nucleus over the entire course of neurogenesis and constructed a detailed molecular atlas of the developing hypothalamus. As a proof of concept of the utility of these data, we used these markers to analyze the phenotype of mice in which Sonic Hedgehog (Shh) was selectively deleted from hypothalamic neuroepithelium and found that Shh is essential for anterior hypothalamic patterning. Our results serve as a resource for functional investigations of hypothalamic development, connectivity, physiology and dysfunction.
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              An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination.

              We describe a strategy for generating an allelic series of mutations at a given locus that requires the production of only one targetted mouse line. The 'allelogenic' mouse line we produced carries a hypomorphic allele of Fgf8, which can be converted to a null allele by mating to cre transgenic animals. The hypomorphic allele can also be reverted to wild-type by mating the allelogenic mice to flp transgenic animals, thereby generating a mouse line suitable for Cre-induced tissue-specific knockout experiments. Analysis of embryos carrying different combinations of these alleles revealed requirements for Fgf8 gene function during gastrulation, as well as cardiac, craniofacial, forebrain, midbrain and cerebellar development.
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                Author and article information

                Contributors
                Journal
                Front Cell Dev Biol
                Front Cell Dev Biol
                Front. Cell Dev. Biol.
                Frontiers in Cell and Developmental Biology
                Frontiers Media S.A.
                2296-634X
                19 May 2021
                2021
                : 9
                : 676121
                Affiliations
                [1] 1Department of Human Anatomy and Psychobiology, School of Medicine, University of Murcia , Murcia, Spain
                [2] 2Biomedical Research Institute of Murcia (IMIB-Arrixaca) , Murcia, Spain
                [3] 3Instituto de Neurociencias de Alicante, CSIC, Universidad Miguel Hernández , Alicante, Spain
                Author notes

                Edited by: Shamik Sen, Indian Institute of Technology Bombay, India

                Reviewed by: Enrique Lanuza, University of Valencia, Spain; Lidija Radenovic, University of Belgrade, Serbia

                *Correspondence: Luis Puelles, puelles@ 123456um.es

                This article was submitted to Cell Adhesion and Migration, a section of the journal Frontiers in Cell and Developmental Biology

                Article
                10.3389/fcell.2021.676121
                8170039
                34095148
                c35e9750-c6a6-4157-a58b-783e9dcda229
                Copyright © 2021 López-González, Alonso, García-Calero, de Puelles and Puelles.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 04 March 2021
                : 15 April 2021
                Page count
                Figures: 14, Tables: 0, Equations: 0, References: 78, Pages: 26, Words: 0
                Funding
                Funded by: Fundación Séneca 10.13039/100007801
                Funded by: Ministerio de Economía y Competitividad 10.13039/501100003329
                Funded by: Ministerio de Economía y Competitividad 10.13039/501100003329
                Categories
                Cell and Developmental Biology
                Original Research

                neuronal tangential migration,ventral premamillary nucleus (vpm),fgf8,hypothalamus,organotypic cultures,retromamillary area (rm),dorsal premamillary nucleus (dpm),perimamillary band

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