Balance between BDNF and Semaphorins gates the innervation of the mammary gland

Shalom, Hadas Sar; Goldner, Ron; Golan-Vaishenker, Yarden; Yaron, Avraham

doi:10.7554/elife.41162

Cited by 7 publications

(5 citation statements)

References 41 publications

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“…Here, we provide data to support a need for communication between RPE and retinal progenitors via Sema6d/Plxna1a, and implicating cell-cell contact mediated signaling in optic cup morphogenesis. The expression of SEMA6s in other embryonic tissues ( Xu et al, 2000 ; Toyofuku et al, 2004a ; Koestner et al, 2008 ; Shalom et al, 2019 ) suggests they may play similar roles in mediating cell-cell and/or cell-ECM interactions that underlie morphogenesis of other embryonic tissues.…”

Section: Discussionmentioning

confidence: 99%

Retinal Pigment Epithelium and Neural Retinal Progenitors Interact via Semaphorin 6D to Facilitate Optic Cup Morphogenesis

Cechmanek

Hehr

McFarlane

2021

eNeuro

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Cell movement propels embryonic tissues to acquire shapes required for mature function.The movements are driven both by acto-myosin signaling, and by cells interacting with the extracellular matrix. Unknown is whether cell-cell interactions within a tissue are also required, and the molecular mechanisms by which such communication might occur. Here we use the developing visual system of zebrafish as a model to understand the role cell-cell communication plays in tissue morphogenesis in the embryonic nervous system. We identify that cell-cell mediated contact between two distinct cell populations, progenitors of the neural retina and retinal pigment epithelium, facilitates epithelial flow to produce the mature cupped retina. We identify for the first time the need in eye morphogenesis for distinct populations of progenitors to interact, and suggest a novel role for a member of a key developmental signaling family, the transmembrane Semaphorin6d, as mediating communication between distinct cell types to control tissue morphogenesis. Significance Statement:We identify that cell-cell communication between neural progenitors in the embryonic eye and their non-neural, retinal pigmented epithelial cell neighbours promotes the cell movements which are required to form a cupped retina that mediates vision. We also reveal the repulsive guidance molecule Semaphorin6d as the molecular mechanism that allows these two distinct cell populations to work together to orchestrate optic cup morphogenesis.

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Section: Discussionmentioning

confidence: 99%

Retinal Pigment Epithelium and Neural Retinal Progenitors Interact via Semaphorin 6D to Facilitate Optic Cup Morphogenesis

Cechmanek

Hehr

McFarlane

2021

eNeuro

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“…SEMA3F signals through NRP1 and NRP2 coreceptors that form heteroprotein complexes with the plexin (PLXN) family of receptors, mainly the PLXN A type, and therefore transduce signals intracellularly [21]. Interestingly, SEMA3F through NRP2 has been described as a promoter of postnatal mammary gland morphogenesis [22]. Although SEMA3F has been extensively reported to act as a tumor suppressor element by inhibiting cell migration in the context of metastasis [23][24][25][26], two recent publications point to a prometastatic role of SEMA3F in hepatocarcinoma [27,28], thus suggesting that SEMA3F is a suitable poor prognosis marker.…”

Section: Introductionmentioning

confidence: 99%

The SEMA3F-NRP1/NRP2 axis is a key factor in the acquisition of invasive traits in in situ breast ductal carcinoma

Moragas,

Fernandez-Nogueira,

Recalde-Percaz

et al. 2024

Preprint

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Background: A better understanding of ductal carcinoma in situ (DCIS) is urgently needed to identify these preinvasive lesions as distinct clinical entities. Semaphorin 3F (SEMA3F) is a soluble axonal guidance molecule, and its coreceptors Neuropilin 1 (NRP1) and NRP2 are strongly expressed in invasive epithelial BC cells. Methods: We utilized two cell line models to represent the progression from a healthy state to the mild-aggressive or ductal carcinoma in situ (DCIS) stage and, ultimately, to invasive cell lines. Additionally, we employed in vivo models and conducted analyses on patient databases to ensure the translational relevance of our results. Results: We revealed SEMA3F as a promoter of invasion during the DCIS-to-invasive ductal carcinoma (IDC) transition in breast cancer (BC) through the action of NRP1 and NRP2. In epithelial cells, SEMA3F activates epithelial mesenchymal transition (EMT), whereas it promotes extracellular matrix degradation and basal membrane and myoepithelial cell layer breakdown. Conclusions:Together with our patient database data, these proof-of-concept results reveal new SEMA3F-mediated mechanisms occurring in the most common preinvasive BC lesion, DCIS, and represent potent and direct activation of its transition to invasion. Moreover, and of clinical and therapeutic relevance, the effects of SEMA3F can be blocked directly through both its receptors and coreceptors, thus preventing invasion and keeping DCIS lesions in the preinvasive state.

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“…Moreover, BDNF is associated with numerous neuropsychiatric disorders, such as depression, bipolar disorder, schizophrenia, addiction, and various neurodevelopmental conditions ( Autry and Monteggia, 2012 ; Wang et al, 2022 ). In recent years the functions of BDNF have been demonstrated in various non-neural tissues, including the heart ( Donovan et al, 2000 ; Fulgenzi et al, 2015 ; Li et al, 2022 ), lung ( Paris et al, 2020 ), skin ( Rutlin et al, 2014 ), mammary gland ( Liu et al, 2012 ; Sar Shalom et al, 2019 ), and skeletal muscle ( Delezie et al, 2019 ; Ahuja et al, 2021 ). Furthermore, BDNF regulates blood insulin levels ( Yang et al, 2019 ; Fulgenzi et al, 2020 ), and BDNF signaling is important in kidney development ( García-Suárez et al, 2006 ; Endlich et al, 2018 ) and serves as a potential marker for chronic kidney disease ( Afsar and Afsar, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Revisiting the expression of BDNF and its receptors in mammalian development

Esvald

Tuvikene

Kiir

et al. 2023

Front. Mol. Neurosci.

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Brain-derived neurotrophic factor (BDNF) promotes the survival and functioning of neurons in the central nervous system and contributes to proper functioning of many non-neural tissues. Although the regulation and role of BDNF have been extensively studied, a rigorous analysis of the expression dynamics of BDNF and its receptors TrkB and p75NTR is lacking. Here, we have analyzed more than 3,600 samples from 18 published RNA sequencing datasets, and used over 17,000 samples from GTEx, and ~ 180 samples from BrainSpan database, to describe the expression of BDNF in the developing mammalian neural and non-neural tissues. We show evolutionarily conserved dynamics and expression patterns of BDNF mRNA and non-conserved alternative 5′ exon usage. Finally, we also show increasing BDNF protein levels during murine brain development and BDNF protein expression in several non-neural tissues. In parallel, we describe the spatiotemporal expression pattern of BDNF receptors TrkB and p75NTR in both murines and humans. Collectively, our in-depth analysis of the expression of BDNF and its receptors gives insight into the regulation and signaling of BDNF in the whole organism throughout life.

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Balance between BDNF and Semaphorins gates the innervation of the mammary gland

Cited by 7 publications

References 41 publications

Retinal Pigment Epithelium and Neural Retinal Progenitors Interact via Semaphorin 6D to Facilitate Optic Cup Morphogenesis

Retinal Pigment Epithelium and Neural Retinal Progenitors Interact via Semaphorin 6D to Facilitate Optic Cup Morphogenesis

The SEMA3F-NRP1/NRP2 axis is a key factor in the acquisition of invasive traits in in situ breast ductal carcinoma

Revisiting the expression of BDNF and its receptors in mammalian development

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