Anatomical location of mature GnRH neurons corresponds with their birthdate in the developing mouse

Jasoni, Christine L.; Porteous, Robert; Herbison, Allan E.

doi:10.1002/dvdy.21869

Cited by 33 publications

(42 citation statements)

References 37 publications

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“…To establish mRNA expression patterns for CXCR7, CXCL12, and CXCR4 in the nasal area of wild-type mice, we used pregnant C57BL/6 mice purchased from Charles River. Embryos of transgenic CXCR7-eGFP and CXCR4-eGFP mice (The Gene Expression Nervous System Atlas project GENSAT; http://www.gensat.org/index.html), and transgenic mice expressing CXCL12-RFP under control of the CXCL12 promoter (Bhattacharyya et al, 2008), bred on CD1 background, were used for immunohistochemistry. CXCL12 Ϫ/Ϫ , CXCR7 Ϫ/Ϫ , and CXCR4 Ϫ/Ϫ embryos were obtained by mating heterozygous mice (Nagasawa et al, 1996;Zou et al, 1998;Sierro et al, 2007), which were on C57BL/6 background.…”

Section: Methodsmentioning

confidence: 99%

“…The mechanisms that guide the migration of GnRH neurons are complex, as they encounter different molecular environments during their migratory journey. Thus, their migration is affected by a wide range of factors (Cariboni et al, 2007b;Wierman et al, 2011;Giacobini and Prevot, 2013) including the chemokine CXCL12 (Schwarting et al, 2006;Toba et al, 2008;Casoni et al, 2012), which has an established role in directed cell migration (Tiveron and Cremer, 2008;Lewellis and Knaut, 2012). CXCL12 has been observed in the nasal mesenchyme (NM), whereas its receptor, CXCR4, has been localized in migrating GnRH neurons and olfactory/vomeronasal nerve axons.…”

Section: Introductionmentioning

confidence: 99%

“…Recent work established CXCR7 as the second CXCL12 receptor (Balabanian et al, 2005;Burns et al, 2006). Unlike CXCR4, however, CXCR7 fails to signal through G␣ i proteins and does not facilitate cell migration in response to CXCL12, suggesting that it is an atypical chemokine receptor (Burns et al, 2006;Boldajipour et al, 2008;Rajagopal et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…Unlike CXCR4, however, CXCR7 fails to signal through G␣ i proteins and does not facilitate cell migration in response to CXCL12, suggesting that it is an atypical chemokine receptor (Burns et al, 2006;Boldajipour et al, 2008;Rajagopal et al, 2010). CXCR7 has a 10-fold higher binding affinity to CXCL12 than CXCR4, and its property to rapidly internalize CXCL12 and to degrade large amounts of extracellular chemokine has led to the concept that it acts as a scavenger to control the levels of the chemokine Naumann et al, 2010;Hoffmann et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…CXCR7 has a 10-fold higher binding affinity to CXCL12 than CXCR4, and its property to rapidly internalize CXCL12 and to degrade large amounts of extracellular chemokine has led to the concept that it acts as a scavenger to control the levels of the chemokine Naumann et al, 2010;Hoffmann et al, 2012). In this context, studies in zebrafish (Boldajipour et al, 2008) and mice (Sánchez-Alcaniz et al, 2011) have demonstrated that CXCR7 indeed plays a role in cell migration by regulating CXCL12 pro-tein levels available to CXCR4-expressing cells in the process of migration.…”

Section: Introductionmentioning

confidence: 99%

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CXC Chemokine Receptor 7 (CXCR7) Affects the Migration of GnRH Neurons by Regulating CXCL12 Availability

et al. 2013

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Gonadotropin-releasing hormone (GnRH) neurons are neuroendocrine cells, located in the hypothalamus, that play an essential role in mammalian reproduction. These neurons originate in the nasal placode and migrate during embryonic development, in association with olfactory/vomeronasal nerves, first in the nose, then through the cribriform plate to enter the forebrain, before settling in the hypothalamus. One of the molecules required for their early migration in the nose is the chemokine CXCL12, which is expressed in the embryonic nasal mesenchyme in an increasing ventral to dorsal gradient, presumably guiding GnRH neurons toward the forebrain. Mice lacking CXCR4, the receptor for CXCL12, exhibit defective GnRH cell movement and a significant reduction in their number, suggesting that CXCL12/CXCR4 signaling is important in the migration and survival of these neurons. Here, we investigated the role of the more recently identified second CXCL12 receptor, CXCR7, in GnRH neuron development. We demonstrate that CXCR7 is expressed along the migratory path of GnRH neurons in the nasal cavity and, although not expressed by GnRH neurons, it affects their migration as indicated by the ectopic accumulation of these cells in the nasal compartment in CXCR7 Ϫ/Ϫ mice. Absence of CXCR7 caused abnormal accumulation of CXCL12-RFP at CXCR4-positive sites in the nasal area of CXCL12-RFP-transgenic mice and excessive CXCL12-dependent intracellular clustering of CXCR4 in GnRH neurons, suggesting internalization. These findings imply that CXCR7 regulates CXCL12 availability by acting as a scavenger along the migratory path of GnRH neurons and, thus, influences the migration of these cells in a noncell-autonomous manner.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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CXC Chemokine Receptor 7 (CXCR7) Affects the Migration of GnRH Neurons by Regulating CXCL12 Availability

et al. 2013

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Diversity within olfactory sensory derivatives revealed by the contribution of Dbx1 lineages

Causeret

Fayon

Moreau

et al. 2023

J of Comparative Neurology

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In vertebrates, the embryonic olfactory epithelium contains progenitors that will give rise to distinct classes of neurons, including olfactory sensory neurons (OSNs; involved in odor detection), vomeronasal sensory neurons (VSNs; responsible for pheromone sensing), and gonadotropin-releasing hormone (GnRH) neurons that control the hypothalamic-pituitary-gonadal axis. Currently, these three neuronal lineages are usually believed to emerge from uniform pools of progenitors. Here, we found that the homeodomain transcription factor Dbx1 is expressed by neurogenic progenitors in the developing and adult mouse olfactory epithelium. We demonstrate that Dbx1 itself is dispensable for neuronal fate specification and global organization of the olfactory sensory system. Using lineage tracing, we characterize the contribution of Dbx1 lineages to OSN, VSN, and GnRH neuron populations and reveal an unexpected degree of diversity. Furthermore, we demonstrate that Dbx1-expressing progenitors remain neurogenic in the absence of the proneural gene Ascl1. Our work therefore points to the existence of distinct neurogenic programs in Dbx1-derived and other olfactory lineages.

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Olfactory ensheathing cells form the microenvironment of migrating GnRH‐1 neurons during mouse development

Geller

Kolasa

Tillet

et al. 2013

Glia

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During development, GnRH-1 neurons differentiate extracerebraly from the nasal placode and migrate from the vomeronasal organ to the forebrain along vomeronasal and terminal nerves. Numerous studies have described the influence of different molecules on the migration of GnRH-1 neurons, however, the role of microenvironment cells remains poorly understood. This study used GFAP-GFP transgenic mice to detect glial cells at early developmental stages. Using nasal explant cultures, the comigration of glial cells with GnRH-1 neurons was clearly demonstrated. This in vitro approach showed that glial cells began migrating from the explants before GnRH-1 neurons. They remained ahead of the GnRH-1 migratory front and stopped migrating after the GnRH-1 neurons. The association of these glial cells with the axons combined with gene expression analysis of GFAP-GFP sorted cells enabled them to be identified as olfactory ensheathing cells (OEC). Immunohistochemical analysis revealed the presence of multiple glial cell-type markers showing several OEC subpopulations surrounding GnRH-1 neurons. Moreover, these OEC expressed genes whose products are involved in the migration of GnRH-1 neurons, such as Nelf and Semaphorin 4. In situ data confirmed that the majority of the GnRH-1 neurons were associated with glial cells along the vomeronasal axons in nasal septum and terminal nerves in the nasal forebrain junction as early as E12.5. Overall, these data demonstrate an OEC microenvironment for migrating GnRH-1 neurons during mouse development. The fact that this glial cell type precedes GnRH-1 neurons and encodes for molecules involved in their nasal migration suggests that it participates in the GnRH-1 system ontogenesis.

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Anatomical location of mature GnRH neurons corresponds with their birthdate in the developing mouse

Cited by 33 publications

References 37 publications

CXC Chemokine Receptor 7 (CXCR7) Affects the Migration of GnRH Neurons by Regulating CXCL12 Availability

CXC Chemokine Receptor 7 (CXCR7) Affects the Migration of GnRH Neurons by Regulating CXCL12 Availability

Diversity within olfactory sensory derivatives revealed by the contribution of Dbx1 lineages

Olfactory ensheathing cells form the microenvironment of migrating GnRH‐1 neurons during mouse development

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