ECB-ART-51191
Dev Neurobiol
2023 Jan 01;831-2:3-27. doi: 10.1002/dneu.22902.
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microRNA-124 regulates Notch and NeuroD1 to mediate transition states of neuronal development.
Konrad KD
,
Song JL
.
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MicroRNAs regulate gene expression by destabilizing target mRNA and/or inhibiting translation in animal cells. The ability to mechanistically dissect miR-124's function during specification, differentiation, and maturation of neurons during development within a single system has not been accomplished. Using the sea urchin embryo, we take advantage of the manipulability of the embryo and its well-documented gene regulatory networks (GRNs). We incorporated NeuroD1 as part of the sea urchin neuronal GRN and determined that miR-124 inhibition resulted in aberrant gut contractions, swimming velocity, and neuronal development. Inhibition of miR-124 resulted in an increased number of cells expressing transcription factors (TFs) associated with progenitor neurons and a concurrent decrease of mature and functional neurons. Results revealed that in the early blastula/gastrula stages, miR-124 regulates undefined factors during neuronal specification and differentiation. In the late gastrula/larval stages, miR-124 regulates Notch and NeuroD1 during the transition between neuronal differentiation and maturation. Overall, we have improved the neuronal GRN and identified miR-124 to play a prolific role in regulating various transitions of neuronal development.
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References [+] :
Amador-Arjona,
SOX2 primes the epigenetic landscape in neural precursors enabling proper gene activation during hippocampal neurogenesis.
2015, Pubmed
Amador-Arjona, SOX2 primes the epigenetic landscape in neural precursors enabling proper gene activation during hippocampal neurogenesis. 2015, Pubmed
Ambasudhan, Direct reprogramming of adult human fibroblasts to functional neurons under defined conditions. 2011, Pubmed
Angerer, SoxB1 downregulation in vegetal lineages of sea urchin embryos is achieved by both transcriptional repression and selective protein turnover. 2005, Pubmed , Echinobase
Angerer, The evolution of nervous system patterning: insights from sea urchin development. 2011, Pubmed , Echinobase
Aquino-Nunez, cnd-1/NeuroD1 Functions with the Homeobox Gene ceh-5/Vax2 and Hox Gene ceh-13/labial To Specify Aspects of RME and DD Neuron Fate in Caenorhabditis elegans. 2020, Pubmed
Arenas-Mena, Spatial expression of Hox cluster genes in the ontogeny of a sea urchin. 2000, Pubmed , Echinobase
Audouard, The Onecut transcription factor HNF-6 regulates in motor neurons the formation of the neuromuscular junctions. 2012, Pubmed
Bartel, MicroRNAs: target recognition and regulatory functions. 2009, Pubmed
Bartel, Metazoan MicroRNAs. 2018, Pubmed
Boutin, NeuroD1 induces terminal neuronal differentiation in olfactory neurogenesis. 2010, Pubmed
Braun, Wnt signaling is required at distinct stages of development for the induction of the posterior forebrain. 2003, Pubmed
Burke, Sea urchin neural development and the metazoan paradigm of neurogenesis. 2014, Pubmed , Echinobase
Burke, Neuron-specific expression of a synaptotagmin gene in the sea urchin Strongylocentrotus purpuratus. 2006, Pubmed , Echinobase
Buznikov, The pre-nervous serotonergic system of developing sea urchin embryos and larvae: pharmacologic and immunocytochemical evidence. 2005, Pubmed , Echinobase
Chen, miR-124 function during Ciona intestinalis neuronal development includes extensive interaction with the Notch signaling pathway. 2011, Pubmed
Cho, The role of BETA2/NeuroD1 in the development of the nervous system. 2004, Pubmed
DeBello, Synaptotagmin and neurotransmitter release. 1993, Pubmed
Devlin, The pharmacology of gamma-aminobutyric acid and acetylcholine receptors at the echinoderm neuromuscular junction. 2001, Pubmed , Echinobase
Garner, Neurogenesis in sea urchin embryos and the diversity of deuterostome neurogenic mechanisms. 2016, Pubmed , Echinobase
Gustafson, Post-translational regulation by gustavus contributes to selective Vasa protein accumulation in multipotent cells during embryogenesis. 2011, Pubmed , Echinobase
Huang, The neuronal differentiation factor NeuroD1 downregulates the neuronal repellent factor Slit2 expression and promotes cell motility and tumor formation of neuroblastoma. 2011, Pubmed
Jiao, miR-124 promotes proliferation and differentiation of neuronal stem cells through inactivating Notch pathway. 2017, Pubmed
Kamath, Transcriptional profile of NeuroD expression in a human fetal astroglial cell line. 2005, Pubmed
Katow, Serotonin stimulates [Ca2+]i elevation in ciliary ectodermal cells of echinoplutei through a serotonin receptor cell network in the blastocoel. 2007, Pubmed , Echinobase
Kengaku, Basic fibroblast growth factor induces differentiation of neural tube and neural crest lineages of cultured ectoderm cells from Xenopus gastrula. 1993, Pubmed
Kimmel, Stages of embryonic development of the zebrafish. 1995, Pubmed
Kozuka, miR-124 dosage regulates prefrontal cortex function by dopaminergic modulation. 2019, Pubmed
Krupke, Eph-Ephrin signaling and focal adhesion kinase regulate actomyosin-dependent apical constriction of ciliary band cells. 2014, Pubmed , Echinobase
Leguia, Synaptotagmin I is involved in the regulation of cortical granule exocytosis in the sea urchin. 2006, Pubmed , Echinobase
Lewis, Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. 2005, Pubmed
Litsiou, A balance of FGF, BMP and WNT signalling positions the future placode territory in the head. 2005, Pubmed
Liu, MiR-124 regulates early neurogenesis in the optic vesicle and forebrain, targeting NeuroD1. 2011, Pubmed
Makeyev, The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. 2007, Pubmed
Mao, Substituting mouse transcription factor Pou4f2 with a sea urchin orthologue restores retinal ganglion cell development. 2016, Pubmed , Echinobase
Masoudi, Unconventional function of an Achaete-Scute homolog as a terminal selector of nociceptive neuron identity. 2018, Pubmed
Materna, Diversification of oral and aboral mesodermal regulatory states in pregastrular sea urchin embryos. 2013, Pubmed , Echinobase
Matsuda, Pioneer Factor NeuroD1 Rearranges Transcriptional and Epigenetic Profiles to Execute Microglia-Neuron Conversion. 2019, Pubmed
McClay, Neurogenesis in the sea urchin embryo is initiated uniquely in three domains. 2018, Pubmed , Echinobase
Mellott, Notch signaling patterns neurogenic ectoderm and regulates the asymmetric division of neural progenitors in sea urchin embryos. 2017, Pubmed , Echinobase
Minokawa, Expression patterns of four different regulatory genes that function during sea urchin development. 2004, Pubmed , Echinobase
Morrow, NeuroD regulates multiple functions in the developing neural retina in rodent. 1999, Pubmed
Oliveri, Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. 2006, Pubmed , Echinobase
Otim, SpHnf6, a transcription factor that executes multiple functions in sea urchin embryogenesis. 2004, Pubmed , Echinobase
Pataskar, NeuroD1 reprograms chromatin and transcription factor landscapes to induce the neuronal program. 2016, Pubmed
Pérez, Hunchback prevents notch-induced apoptosis in the serotonergic lineage of Drosophila Melanogaster. 2022, Pubmed
Perillo, A pancreatic exocrine-like cell regulatory circuit operating in the upper stomach of the sea urchin Strongylocentrotus purpuratus larva. 2016, Pubmed , Echinobase
Perillo, New Neuronal Subtypes With a "Pre-Pancreatic" Signature in the Sea Urchin Stongylocentrotus purpuratus. 2018, Pubmed , Echinobase
Puligilla, Sox2 induces neuronal formation in the developing mammalian cochlea. 2010, Pubmed
Rajasethupathy, Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. 2009, Pubmed
Range, Canonical and non-canonical Wnt signaling pathways define the expression domains of Frizzled 5/8 and Frizzled 1/2/7 along the early anterior-posterior axis in sea urchin embryos. 2018, Pubmed , Echinobase
Range, LvNumb works synergistically with Notch signaling to specify non-skeletal mesoderm cells in the sea urchin embryo. 2008, Pubmed , Echinobase
Remsburg, Analysis of microRNA functions. 2019, Pubmed , Echinobase
Rentzsch, FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. 2008, Pubmed
Reuter, Identification of an evolutionarily conserved domain in Neurod1 favouring enteroendocrine versus goblet cell fate. 2022, Pubmed
Rozen, Primer3 on the WWW for general users and for biologist programmers. 2000, Pubmed
Schneider, NIH Image to ImageJ: 25 years of image analysis. 2012, Pubmed
Sethi, Multicolor labeling in developmental gene regulatory network analysis. 2014, Pubmed , Echinobase
Siebel, Notch Signaling in Development, Tissue Homeostasis, and Disease. 2017, Pubmed
Slota, Developmental origin of peripheral ciliary band neurons in the sea urchin embryo. 2020, Pubmed , Echinobase
Slota, Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus. 2019, Pubmed , Echinobase
Song, Select microRNAs are essential for early development in the sea urchin. 2012, Pubmed , Echinobase
Squires, Serotonin and its metabolism in basal deuterostomes: insights from Strongylocentrotus purpuratus and Xenoturbella bocki. 2010, Pubmed , Echinobase
Staton, Use of target protector morpholinos to analyze the physiological roles of specific miRNA-mRNA pairs in vivo. 2011, Pubmed
Stepicheva, microRNAs regulate β-catenin of the Wnt signaling pathway in early sea urchin development. 2015, Pubmed , Echinobase
Stepicheva, High throughput microinjections of sea urchin zygotes. 2014, Pubmed , Echinobase
Stepicheva, microRNA-31 modulates skeletal patterning in the sea urchin embryo. 2015, Pubmed , Echinobase
Toch, Onecut-dependent Nkx6.2 transcription factor expression is required for proper formation and activity of spinal locomotor circuits. 2020, Pubmed
Torii, Two-dimensional spatial patterning in developmental systems. 2012, Pubmed
Truman, Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster. 2010, Pubmed
Tutukova, The Role of Neurod Genes in Brain Development, Function, and Disease. 2021, Pubmed
van der Raadt, ONECUT transcription factors induce neuronal characteristics and remodel chromatin accessibility. 2019, Pubmed
Vega Thurber, Apoptosis in early development of the sea urchin, Strongylocentrotus purpuratus. 2007, Pubmed , Echinobase
Wada, Modification of ciliary beating in sea urchin larvae induced by neurotransmitters: beat-plane rotation and control of frequency fluctuation. 1997, Pubmed , Echinobase
Wang, Positive feedback between RNA-binding protein HuD and transcription factor SATB1 promotes neurogenesis. 2015, Pubmed
Wei, Neurogenic gene regulatory pathways in the sea urchin embryo. 2016, Pubmed , Echinobase
Wei, Direct development of neurons within foregut endoderm of sea urchin embryos. 2011, Pubmed , Echinobase
Weng, Drosophila miR-124 regulates neuroblast proliferation through its target anachronism. 2012, Pubmed
Wessel, Sequential expression of germ-layer specific molecules in the sea urchin embryo. 1985, Pubmed , Echinobase
Wessel, How to grow a gut: ontogeny of the endoderm in the sea urchin embryo. 1999, Pubmed , Echinobase
Yaguchi, Zinc finger homeobox is required for the differentiation of serotonergic neurons in the sea urchin embryo. 2012, Pubmed , Echinobase
Yaguchi, Cooperative Wnt-Nodal Signals Regulate the Patterning of Anterior Neuroectoderm. 2016, Pubmed , Echinobase
Yaguchi, Sea urchin larvae utilize light for regulating the pyloric opening. 2021, Pubmed , Echinobase
Yaguchi, Expression of tryptophan 5-hydroxylase gene during sea urchin neurogenesis and role of serotonergic nervous system in larval behavior. 2003, Pubmed , Echinobase
Yaguchi, A Wnt-FoxQ2-nodal pathway links primary and secondary axis specification in sea urchin embryos. 2008, Pubmed , Echinobase
Yaguchi, TGFβ signaling positions the ciliary band and patterns neurons in the sea urchin embryo. 2010, Pubmed , Echinobase
Yaguchi, Specification of ectoderm restricts the size of the animal plate and patterns neurogenesis in sea urchin embryos. 2006, Pubmed , Echinobase
Yaguchi, Fez function is required to maintain the size of the animal plate in the sea urchin embryo. 2011, Pubmed , Echinobase
Yamazaki, Krüppel-like is required for nonskeletogenic mesoderm specification in the sea urchin embryo. 2008, Pubmed , Echinobase
Yu, MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. 2008, Pubmed
Zaharieva, Concentration and Localization of Coexpressed ELAV/Hu Proteins Control Specificity of mRNA Processing. 2015, Pubmed