22 results on '"Cell type diversity"'
Search Results
2. High-resolution transcriptional landscape of xeno-free human induced pluripotent stem cell-derived cerebellar organoids
- Author
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Esther B. E. Becker, Samuel Nayler, Devika Agarwal, Fabiola Curion, and Rory Bowden
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Science ,Induced Pluripotent Stem Cells ,Cell ,Cell Culture Techniques ,Biology ,Article ,Cell Line ,Transcriptome ,Purkinje Cells ,In vivo ,Cerebellum ,Gene expression ,medicine ,Organoid ,Animals ,Humans ,Transcriptomics ,Induced pluripotent stem cell ,Gene ,Aged ,Matrigel ,Multidisciplinary ,Gene Expression Profiling ,Computational Biology ,Cell type diversity ,Cell Differentiation ,Cell biology ,Organoids ,Drug Combinations ,medicine.anatomical_structure ,nervous system ,Neuronal development ,Medicine ,Female ,Proteoglycans ,Collagen ,Laminin ,Biomarkers - Abstract
Current protocols for producing cerebellar neurons from human pluripotent stem cells (hPSCs) often rely on animal co-culture and mostly exist as monolayers, limiting their capability to recapitulate the complex processes in the developing cerebellum. Here, we employed a robust method, without the need for mouse co-culture to generate three-dimensional cerebellar organoids from hPSCs that display hallmarks of in vivo cerebellar development. Single-cell profiling followed by comparison to human and mouse cerebellar atlases revealed the presence and maturity of transcriptionally distinct populations encompassing major cerebellar cell types. Encapsulation with Matrigel aimed to provide more physiologically-relevant conditions through recapitulation of basement-membrane signalling, influenced both growth dynamics and cellular composition of the organoids, altering developmentally relevant gene expression programmes. We identified enrichment of cerebellar disease genes in distinct cell populations in the hPSC-derived cerebellar organoids. These findings ascertain xeno-free human cerebellar organoids as a unique model to gain insight into cerebellar development and its associated disorders.
- Published
- 2021
3. Single-cell atlas of early human brain development highlights heterogeneity of human neuroepithelial cells and early radial glia
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Maximilian Haeussler, Ugomma C. Eze, Aparna Bhaduri, Arnold R. Kriegstein, and Tomasz J. Nowakowski
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0301 basic medicine ,Resource ,1.1 Normal biological development and functioning ,Neurogenesis ,Population ,Ependymoglial Cells ,Neuroepithelial Cells ,Hindbrain ,Developmental neurogenesis ,Biology ,Regenerative Medicine ,03 medical and health sciences ,0302 clinical medicine ,Neural Stem Cells ,Stem Cell Research - Nonembryonic - Human ,Underpinning research ,Cortex (anatomy) ,medicine ,Psychology ,Animals ,Humans ,education ,Pediatric ,Cerebral Cortex ,education.field_of_study ,Neurology & Neurosurgery ,Cerebrum ,General Neuroscience ,Neurosciences ,Cell type diversity ,Human brain ,Stem Cell Research ,Neural stem cell ,Neuroepithelial cell ,030104 developmental biology ,medicine.anatomical_structure ,nervous system ,Neurological ,Stem Cell Research - Nonembryonic - Non-Human ,Cognitive Sciences ,Single-Cell Analysis ,Neuroscience ,030217 neurology & neurosurgery - Abstract
The human cortex comprises diverse cell types that emerge from an initially uniform neuroepithelium that gives rise to radial glia, the neural stem cells of the cortex. To characterize the earliest stages of human brain development, we performed single-cell RNA-sequencing across regions of the developing human brain, including the telencephalon, diencephalon, midbrain, hindbrain and cerebellum. We identify nine progenitor populations physically proximal to the telencephalon, suggesting more heterogeneity than previously described, including a highly prevalent mesenchymal-like population that disappears once neurogenesis begins. Comparison of human and mouse progenitor populations at corresponding stages identifies two progenitor clusters that are enriched in the early stages of human cortical development. We also find that organoid systems display low fidelity to neuroepithelial and early radial glia cell types, but improve as neurogenesis progresses. Overall, we provide a comprehensive molecular and spatial atlas of early stages of human brain and cortical development., Eze et al. use single-cell sequencing and immunohistochemical validation to create an atlas of early human brain development. In the telencephalon, they discover a diversity of progenitor subtypes, including two that are enriched in humans.
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- 2021
4. Distinct subtypes of proprioceptive dorsal root ganglion neurons regulate adaptive proprioception in mice
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Channabasavaiah B. Gurumurthy, Konstantinos Meletis, Charles Petitpré, Saida Hadjab, Simone Wanderoy, Yiqiao Wang, Francois Lallemend, Anil Sharma, Paula Fontanet, Haohao Wu, Jorge L. Ruas, Paulo R. Jannig, Ole Kiehn, J. Alexander Heimel, Carmelo Bellardita, Rolen M. Quadros, Kylie K. Y. Cheung, Yang Xuan, and Netherlands Institute for Neuroscience (NIN)
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Motor Neurons/classification ,Male ,0301 basic medicine ,Gene Expression ,General Physics and Astronomy ,Mice ,Motor network ,0302 clinical medicine ,Dorsal root ganglion ,Feedback, Sensory ,Ganglia, Spinal ,Nerve Tissue Proteins/genetics ,Spinal Cord/cytology ,Motor Neurons ,Multidisciplinary ,Cell type diversity ,LIM Domain Proteins ,Proprioceptive function ,Sensory input ,medicine.anatomical_structure ,Spinal Cord ,Calbindin 1 ,Core Binding Factor Alpha 2 Subunit ,Sensory processing ,Core Binding Factor Alpha 3 Subunit/genetics ,Single-Cell Analysis ,Co-Repressor Proteins ,animal structures ,Co-Repressor Proteins/genetics ,Sensory Receptor Cells ,Science ,Lectins, C-Type/genetics ,Mice, Transgenic ,Nerve Tissue Proteins ,Sensory system ,Biology ,Article ,General Biochemistry, Genetics and Molecular Biology ,03 medical and health sciences ,Physical Conditioning, Animal ,medicine ,Animals ,Ganglia, Spinal/cytology ,Lectins, C-Type ,Transcriptomics ,Feedback, Sensory/physiology ,Calcium-Binding Proteins/genetics ,Proprioception ,Core Binding Factor Alpha 2 Subunit/genetics ,Calcium-Binding Proteins ,General Chemistry ,LIM Domain Proteins/genetics ,Cellular neuroscience ,Mice, Inbred C57BL ,Sensory Physiology ,Core Binding Factor Alpha 3 Subunit ,030104 developmental biology ,nervous system ,Sensory Receptor Cells/classification ,Increased motor activity ,Calbindin 1/genetics ,Neuroscience ,Proprioception/physiology ,030217 neurology & neurosurgery - Abstract
Proprioceptive neurons (PNs) are essential for the proper execution of all our movements by providing muscle sensory feedback to the central motor network. Here, using deep single cell RNAseq of adult PNs coupled with virus and genetic tracings, we molecularly identify three main types of PNs (Ia, Ib and II) and find that they segregate into eight distinct subgroups. Our data unveil a highly sophisticated organization of PNs into discrete sensory input channels with distinct spatial distribution, innervation patterns and molecular profiles. Altogether, these features contribute to finely regulate proprioception during complex motor behavior. Moreover, while Ib- and II-PN subtypes are specified around birth, Ia-PN subtypes diversify later in life along with increased motor activity. We also show Ia-PNs plasticity following exercise training, suggesting Ia-PNs are important players in adaptive proprioceptive function in adult mice., Molecular diversity of proprioceptive neuron types (Ia, Ib and II PNs) is unclear. Here, the authors characterized the functional organization and development of eight subtypes of PNs in mice. Importantly, Ia subtypes are plastic, suggesting a role in adaptive proprioception during motor behavior.
- Published
- 2021
5. Single-cell delineation of lineage and genetic identity in the mouse brain
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Rachel C. Bandler, Ilaria Vitali, Ryan N. Delgado, May C. Ho, Elena Dvoretskova, Josue S. Ibarra Molinas, Paul W. Frazel, Maesoumeh Mohammadkhani, Robert Machold, Sophia Maedler, Shane A. Liddelow, Tomasz J. Nowakowski, Gord Fishell, and Christian Mayer
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Multidisciplinary ,Neurogenesis ,Brain ,Embryonic Development ,Mitosis ,Cell type diversity ,Cell Differentiation ,Article ,Mice ,Neural Stem Cells ,Animals ,Cell Lineage ,GABAergic Neurons ,Transcriptome ,Cell fate and cell lineage - Abstract
During neurogenesis, mitotic progenitor cells lining the ventricles of the embryonic mouse brain undergo their final rounds of cell division, giving rise to a wide spectrum of postmitotic neurons and glia1,2. The link between developmental lineage and cell-type diversity remains an open question. Here we used massively parallel tagging of progenitors to track clonal relationships and transcriptomic signatures during mouse forebrain development. We quantified clonal divergence and convergence across all major cell classes postnatally, and found diverse types of GABAergic neuron that share a common lineage. Divergence of GABAergic clones occurred during embryogenesis upon cell-cycle exit, suggesting that differentiation into subtypes is initiated as a lineage-dependent process at the progenitor cell level., Single-cell RNA sequencing with parallel tagging of progenitor cells is used to track clonal relationships and transcriptomic signatures during development of the mouse forebrain.
- Published
- 2022
6. Combined microRNA and mRNA detection in mammalian retinas by in situ hybridization chain reaction
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Ryan M. Welchko, Robert C. Thompson, Shunbin Xu, Huanqing Zhang, Pei Zhuang, and David L. Turner
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0301 basic medicine ,In situ ,lcsh:Medicine ,In situ hybridization ,Article ,Retina ,Mice ,03 medical and health sciences ,0302 clinical medicine ,microRNA ,medicine ,Animals ,RNA, Messenger ,lcsh:Science ,In Situ Hybridization ,Regulation of gene expression ,Messenger RNA ,Multidisciplinary ,Chemistry ,lcsh:R ,Cell type diversity ,RNA ,3. Good health ,Cell biology ,MicroRNAs ,Amacrine Cells ,030104 developmental biology ,medicine.anatomical_structure ,miRNAs ,lcsh:Q ,human activities ,030217 neurology & neurosurgery ,Function (biology) - Abstract
Improved in situ hybridization methods for mRNA detection in tissues have been developed based on the hybridization chain reaction (HCR). We show that in situ HCR methods can be used for the detection of microRNAs in tissue sections from mouse retinas. In situ HCR can be used for the detection of two microRNAs simultaneously or for the combined detection of microRNA and mRNA. In addition, miRNA in situ HCR can be combined with immunodetection of proteins. We use these methods to characterize cells expressing specific microRNAs in the mouse retina. We find that miR-181a is expressed in amacrine cells during development and in adult retinas, and it is present in both GABAergic and glycinergic amacrine cells. The detection of microRNAs with in situ HCR should facilitate studies of microRNA function and gene regulation in the retina and other tissues.
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- 2020
7. Coordination of two enhancers drives expression of olfactory trace amine-associated receptors
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Zhengrong Xu, Longzhi Tan, Clemens Riegler, Mustafa Talay, Cheng Yang, X. Sunney Xie, Wanqing Wu, Hui Yang, Cheng Tang, Mark Johnson, Xiaona Huo, Hongqiang Bao, Kristian J. Herrera, Stephen D. Liberles, Florian Engert, Gilad Barnea, Qian Li, Aimei Fei, Yalei Kong, and Griffin Hartmann
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Male ,0301 basic medicine ,Science ,Transgene ,General Physics and Astronomy ,Olfactory receptors ,Biology ,Receptors, Odorant ,Olfactory Receptor Neurons ,Article ,General Biochemistry, Genetics and Molecular Biology ,Receptors, G-Protein-Coupled ,Animals, Genetically Modified ,Mice ,03 medical and health sciences ,0302 clinical medicine ,Olfactory Mucosa ,Gene expression ,Animals ,Epigenetics ,Enhancer ,Receptor ,Gene ,Trace amine ,Zebrafish ,Trace amine-associated receptor ,Cell fate and cell lineage ,Multidisciplinary ,Epigenetics and plasticity ,Optical Imaging ,Cell type diversity ,General Chemistry ,respiratory system ,Cell biology ,Mice, Inbred C57BL ,Smell ,Enhancer Elements, Genetic ,030104 developmental biology ,Gene Expression Regulation ,Female ,030217 neurology & neurosurgery - Abstract
Olfactory sensory neurons (OSNs) are functionally defined by their expression of a unique odorant receptor (OR). Mechanisms underlying singular OR expression are well studied, and involve a massive cross-chromosomal enhancer interaction network. Trace amine-associated receptors (TAARs) form a distinct family of olfactory receptors, and here we find that mechanisms regulating Taar gene choice display many unique features. The epigenetic signature of Taar genes in TAAR OSNs is different from that in OR OSNs. We further identify that two TAAR enhancers conserved across placental mammals are absolutely required for expression of the entire Taar gene repertoire. Deletion of either enhancer dramatically decreases the expression probabilities of different Taar genes, while deletion of both enhancers completely eliminates the TAAR OSN populations. In addition, both of the enhancers are sufficient to drive transgene expression in the partially overlapped TAAR OSNs. We also show that the TAAR enhancers operate in cis to regulate Taar gene expression. Our findings reveal a coordinated control of Taar gene choice in OSNs by two remote enhancers, and provide an excellent model to study molecular mechanisms underlying formation of an olfactory subsystem., In our nose, some neuron subpopulations express a family of trace amine associated receptors (TAARs, smelling e.g., rotten fish). Fei et al. identify two conserved enhancers across placental mammals named TAAR enhancer 1 and 2 that coordinately regulate expression of the entire Taar gene repertoire.
- Published
- 2021
8. Intracellular trafficking of Notch orchestrates temporal dynamics of Notch activity in the fly brain
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Makoto Sato, Xujun Han, Rie Takayama, Masaharu Nagayama, Shin-Ichiro Ei, Miaoxing Wang, Yoshitaro Tanaka, Tetsuo Yasugi, and Chuyan Liu
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0301 basic medicine ,animal structures ,Endosome ,Science ,Neurogenesis ,Notch signaling pathway ,General Physics and Astronomy ,Developmental neurogenesis ,Endosomes ,General Biochemistry, Genetics and Molecular Biology ,Article ,03 medical and health sciences ,0302 clinical medicine ,Neuroblast ,Downregulation and upregulation ,Animals ,Drosophila Proteins ,Neural stem cells ,Multidisciplinary ,Receptors, Notch ,Chemistry ,rab4 GTP-Binding Proteins ,fungi ,Intracellular Signaling Peptides and Proteins ,Cell type diversity ,Brain ,Gene Expression Regulation, Developmental ,rab7 GTP-Binding Proteins ,Cell Differentiation ,General Chemistry ,Cell biology ,Neuroepithelial cell ,Protein Transport ,030104 developmental biology ,Drosophila melanogaster ,nervous system ,rab GTP-Binding Proteins ,Differentiation ,Gene Knockdown Techniques ,embryonic structures ,030217 neurology & neurosurgery ,Intracellular ,Function (biology) ,Neural patterning ,Signal Transduction ,Transcription Factors - Abstract
While Delta non-autonomously activates Notch in neighboring cells, it autonomously inactivates Notch through cis-inhibition, the molecular mechanism and biological roles of which remain elusive. The wave of differentiation in the Drosophila brain, the ‘proneural wave’, is an excellent model for studying Notch signaling in vivo. Here, we show that strong nonlinearity in cis-inhibition reproduces the second peak of Notch activity behind the proneural wave in silico. Based on this, we demonstrate that Delta expression induces a quick degradation of Notch in late endosomes and the formation of the twin peaks of Notch activity in vivo. Indeed, the amount of Notch is upregulated and the twin peaks are fused forming a single peak when the function of Delta or late endosomes is compromised. Additionally, we show that the second Notch peak behind the wavefront controls neurogenesis. Thus, intracellular trafficking of Notch orchestrates the temporal dynamics of Notch activity and the temporal patterning of neurogenesis., During Drosophila development, two peaks of Notch activity propagate across the neuroepithelium to generate neuroblasts. Here, the authors show Notch cis-inhibition under the control of intracellular Notch trafficking establishes these two peaks, which temporally control neurogenesis in the brain.
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- 2021
9. Biotransformation of Chemicals at the Water–Sediment Interface─Toward a Robust Simulation Study Setup
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Carolin Seller, Mark Honti, Kathrin Fenner, Birge D. Özel Duygan, University of Zurich, and Fenner, Kathrin
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10120 Department of Chemistry ,Environmental Engineering ,phenotypic microbial community composition ,cell type diversity ,Interface (Java) ,OECD 308/309 studies ,2301 Environmental Science (miscellaneous) ,Water sediment ,Environmental Science (miscellaneous) ,micropollutants ,Environmental sciences ,2312 Water Science and Technology ,2305 Environmental Engineering ,Biotransformation ,Environmental chemistry ,540 Chemistry ,water−sediment systems ,Environmental science ,GE1-350 ,biotransformation ,chemical persistence ,Water Science and Technology - Published
- 2021
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10. Single-cell transcriptomics reveals cell type diversity of human prostate.
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Chen Y, Zhang P, Liao J, Cheng J, Zhang Q, Li T, Zhang H, Jiang Y, Zhang F, Zeng Y, Mo L, Yan H, Liu D, Zhang Q, Zou C, Wei GH, and Mo Z
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- Male, Humans, Transcriptome genetics, Cellular Senescence genetics, Fibroblasts metabolism, Cell Transformation, Neoplastic, Prostate metabolism, Prostate pathology, Prostatic Neoplasms genetics, Prostatic Neoplasms metabolism, Prostatic Neoplasms pathology
- Abstract
Extensive studies have been performed to describe the phenotypic changes occurring during malignant transformation of the prostate. However, the cell types and associated changes that contribute to the development of prostate diseases and cancer remain elusive, largely due to the heterogeneous composition of prostatic tissues. Here, we conduct a comprehensive evaluation of four human prostate tissues by single-cell RNA sequencing (scRNA-seq) to analyze their cellular compositions. We identify 18 clusters of cell types, each with distinct gene expression profiles and unique features; of these, one cluster of epithelial cells (Ep) is found to be associated with immune function. In addition, we characterize a special cluster of fibroblasts and aberrant signaling changes associated with prostate cancer (PCa). Moreover, we provide insights into the epithelial changes that occur during the cellular senescence and aging. These results expand our understanding of the unique functional associations between the diverse prostatic cell types and the contributions of specific cell clusters to the malignant transformation of prostate tissues and PCa development., Competing Interests: Conflict of interest The authors have no competing interests to declare., (Copyright © 2022 Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, and Genetics Society of China. Published by Elsevier Ltd. All rights reserved.)
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- 2022
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11. Onecut-dependent Nkx6.2 transcription factor expression is required for proper formation and activity of spinal locomotor circuits
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Olivier Schakman, Xiuqian Mu, Frédéric Clotman, Audrey Harris, Elena Kondratskaya, Stéphanie Debrulle, María Hidalgo-Figueroa, Nicolas Dauguet, Jean-Luc Boulland, Alexander Gow, Mathilde Toch, Fadel Tissir, Joel C. Glover, Charlotte Baudouin, Psicología, and UCL - SSS/IONS/CEMO - Pôle Cellulaire et moléculaire
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0301 basic medicine ,Spinal neuron ,Population ,lcsh:Medicine ,Gene Expression ,Developmental neurogenesis ,Mice, Transgenic ,Biology ,Neural circuits ,Article ,Mice ,03 medical and health sciences ,0302 clinical medicine ,medicine ,Animals ,lcsh:Science ,Author Correction ,education ,Transcription factor ,Homeodomain Proteins ,Motor Neurons ,education.field_of_study ,Multidisciplinary ,lcsh:R ,Cell type diversity ,Gene Expression Regulation, Developmental ,Motor neuron ,Spinal cord ,Cell biology ,030104 developmental biology ,medicine.anatomical_structure ,Spinal Cord ,nervous system ,embryonic structures ,ISL1 ,Neuronal development ,lcsh:Q ,Neuron ,Locomotion ,030217 neurology & neurosurgery ,Onecut Transcription Factors ,Transcription Factors - Abstract
In the developing spinal cord, Onecut transcription factors control the diversification of motor neurons into distinct neuronal subsets by ensuring the maintenance of Isl1 expression during differentiation. However, other genes downstream of the Onecut proteins and involved in motor neuron diversification have remained unidentified. In the present study, we generated conditional mutant embryos carrying specific inactivation of Onecut genes in the developing motor neurons, performed RNA-sequencing to identify factors downstream of Onecut proteins in this neuron population, and employed additional transgenic mouse models to assess the role of one specific Onecut-downstream target, the transcription factor Nkx6.2. Nkx6.2 expression was up-regulated in Onecut-deficient motor neurons, but strongly downregulated in Onecut-deficient V2a interneurons, indicating an opposite regulation of Nkx6.2 by Onecut factors in distinct spinal neuron populations. Nkx6.2-null embryos, neonates and adult mice exhibited alterations of locomotor pattern and spinal locomotor network activity, likely resulting from defective survival of a subset of limb-innervating motor neurons and abnormal migration of V2a interneurons. Taken together, our results indicate that Nkx6.2 regulates the development of spinal neuronal populations and the formation of the spinal locomotor circuits downstream of the Onecut transcription factors.
- Published
- 2020
12. Antidepressant–like effects of fish, krill oils and Vit B12 against exposure to stress environment in mice models: current status and pilot study
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Sima Kianpour Rad, Abolfazl Movafagh, Soheila Kianpour Rad, and Parastoo Mojtahed Zadeh-Ardabili
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0301 basic medicine ,Male ,medicine.medical_specialty ,Imipramine ,Antioxidant ,medicine.medical_treatment ,lcsh:Medicine ,Pilot Projects ,Drug development ,medicine.disease_cause ,Krill oil ,Antioxidants ,Article ,03 medical and health sciences ,chemistry.chemical_compound ,Mice ,0302 clinical medicine ,Fish Oils ,Stress, Physiological ,Internal medicine ,medicine ,Animals ,Author Correction ,lcsh:Science ,Depressive Disorder ,Multidisciplinary ,Chemistry ,Depression ,lcsh:R ,Cell type diversity ,Glutathione ,Fish oil ,Tail suspension test ,Antidepressive Agents ,Disease Models, Animal ,Oxidative Stress ,Vitamin B 12 ,030104 developmental biology ,Endocrinology ,lcsh:Q ,Dietary Proteins ,030217 neurology & neurosurgery ,Oxidative stress ,Stress, Psychological ,medicine.drug ,Behavioural despair test ,Euphausiacea ,Neuroscience - Abstract
Oxidative stress has significant role in pathophysiology of any kind of depression through actions of free radicals, non-radical molecules, and unbalancing antioxidant systems in body. In the current study, antidepressant responses of fish oil (FO), Neptune krill oil (NKO), vitamin B12 (Vit B12), and also imipramine (IMP) as the reference were studied. Natural light was employed to induce stress in the animals followed by oral administration of the drugs for 14 days. The antidepressant effect was assessed by tail suspension test (TST) and forced swimming test (FST), antioxidant enzymes and oxidative stress markers were then measured in the brain tissue of the animals. The administration of FO and NKO could significantly reduce the immobility of the animals; while, increasing climbing and swimming time compared to the normal saline in CUS-control group in TST and FST, similarly to IMP but not with Vit B12. Vit B12 could not effect on SOD activity and H2O2 level, but, cause decrease of the malondialdihydric (MDA) level and CAT activity, as well as increased the GPx and GSH activities. The rest treatments led to decrease of MDA, H2O2 levels and CAT activity and increase of GPx, SOD, GSH activities.
- Published
- 2019
13. Early dorsomedial tissue interactions regulate gyrification of distal neocortex
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Igor Y. Iskusnykh, Victor V. Chizhikov, Nikolai Fattakhov, Shubha Tole, Achira Roy, Kathleen J. Millen, Ashwin S. Shetty, Ekaterina Y. Steshina, and Anne G. Lindgren
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Male ,0301 basic medicine ,Science ,Mesenchyme ,LIM-Homeodomain Proteins ,Neuroepithelial Cells ,General Physics and Astronomy ,Lissencephaly ,Developmental neurogenesis ,Neocortex ,Biology ,Article ,General Biochemistry, Genetics and Molecular Biology ,Mesoderm ,Mice ,03 medical and health sciences ,0302 clinical medicine ,medicine ,Animals ,lcsh:Science ,Gyrification ,Mice, Knockout ,Regulation of gene expression ,Multidisciplinary ,Wnt signaling pathway ,Neural tube ,Cell type diversity ,Gene Expression Regulation, Developmental ,General Chemistry ,medicine.disease ,Mice, Inbred C57BL ,Wnt Proteins ,Neuroepithelial cell ,030104 developmental biology ,medicine.anatomical_structure ,Female ,lcsh:Q ,Neuroscience ,030217 neurology & neurosurgery ,Signal Transduction ,Transcription Factors - Abstract
The extent of neocortical gyrification is an important determinant of a species’ cognitive abilities, yet the mechanisms regulating cortical gyrification are poorly understood. We uncover long-range regulation of this process originating at the telencephalic dorsal midline, where levels of secreted Bmps are maintained by factors in both the neuroepithelium and the overlying mesenchyme. In the mouse, the combined loss of transcription factors Lmx1a and Lmx1b, selectively expressed in the midline neuroepithelium and the mesenchyme respectively, causes dorsal midline Bmp signaling to drop at early neural tube stages. This alters the spatial and temporal Wnt signaling profile of the dorsal midline cortical hem, which in turn causes gyrification of the distal neocortex. Our study uncovers early mesenchymal-neuroepithelial interactions that have long-range effects on neocortical gyrification and shows that lissencephaly in mice is actively maintained via redundant genetic regulation of dorsal midline development and signaling., The contribution of long-range signaling to cortical gyrification remains poorly understood. In this study, authors demonstrate that the combined genetic loss of transcription factors Lmx1a and Lmx1b, expressed in the telencephalic dorsal midline neuroepithelium and head mesenchyme, respectively, induces gyrification in the mouse neocortex
- Published
- 2019
14. Brain-specific homeobox Bsx specifies identity of pineal gland between serially homologous photoreceptive organs in zebrafish
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Mano, Hiroaki, Asaoka, Yoichi, Kojima, Daisuke, and Fukada, Yoshitaka
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Rhodopsin ,endocrine system ,PAX6 Transcription Factor ,Medicine (miscellaneous) ,Biology ,Pineal Gland ,Article ,Retina ,General Biochemistry, Genetics and Molecular Biology ,Animals, Genetically Modified ,03 medical and health sciences ,Pineal gland ,0302 clinical medicine ,Cellular neuroscience ,Gene expression ,medicine ,Animals ,Promoter Regions, Genetic ,lcsh:QH301-705.5 ,Zebrafish ,Gene ,030304 developmental biology ,Homeodomain Proteins ,0303 health sciences ,Otx Transcription Factors ,Cell type diversity ,Gene Expression Regulation, Developmental ,Zebrafish Proteins ,biology.organism_classification ,Cell biology ,medicine.anatomical_structure ,lcsh:Biology (General) ,nervous system ,Trans-Activators ,Homeobox ,Ectopic expression ,Evolutionary developmental biology ,General Agricultural and Biological Sciences ,hormones, hormone substitutes, and hormone antagonists ,030217 neurology & neurosurgery ,Transcription Factors - Abstract
The pineal gland functioning as a photoreceptive organ in non-mammalian species is a serial homolog of the retina. Here we found that Brain-specific homeobox (Bsx) is a key regulator conferring individuality on the pineal gland between the two serially homologous photoreceptive organs in zebrafish. Bsx knock-down impaired the pineal development with reduced expression of exorh, the pineal-specific gene responsible for the photoreception, whereas it induced ectopic expression of rho, a retina-specific gene, in the pineal gland. Bsx remarkably transactivated the exorh promoter in combination with Otx5, but not with Crx, through its binding to distinct subtypes of PIRE, a DNA cis-element driving Crx/Otx-dependent pineal-specific gene expression. These results demonstrate that the identity of pineal photoreceptive neurons is determined by the combinatorial code of Bsx and Otx5, the former confers the pineal specificity at the tissue level and the latter determines the photoreceptor specificity at the cellular level., Hiroaki Mano et al. show that brain-specific homeobox, Bsx, is a regulator in pineal gland development. They show that Bsx depletion in zebrafish reduces the expression of a pineal-specific gene responsible for photoreception, affecting the identity of pineal photoreceptive neurons.
- Published
- 2019
15. Transient Callosal Projections of L4 Neurons Are Eliminated for the Acquisition of Local Connectivity
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Maria J. Galazo, Ignacio Varela, Linnea A. Weiss, Gertrudis Perea, N. S. De León Reyes, S. Mederos, Marta Nieto, León, Reyes N.S. De, Mederos, S., Weiss, L.A., Galazo, M.J., Nieto, M., León, Reyes N.S. De [0000-0002-4070-5983], Mederos, S. [0000-0003-0960-9974], Weiss, L.A. [0000-0002-7593-7821], Galazo, M.J. [0000-0003-1909-7765], and Nieto, M. [0000-0002-8349-8435]
- Subjects
0301 basic medicine ,Sensory Receptor Cells ,Science ,Green Fluorescent Proteins ,General Physics and Astronomy ,Mice, Transgenic ,Sensory system ,Biology ,Somatosensory system ,Corpus callosum ,Article ,General Biochemistry, Genetics and Molecular Biology ,Corpus Callosum ,03 medical and health sciences ,0302 clinical medicine ,Thalamus ,Neural Pathways ,medicine ,Animals ,Transient (computer programming) ,lcsh:Science ,Cell fate and cell lineage ,Mice, Knockout ,Neurons ,Microscopy, Confocal ,Multidisciplinary ,Genetic interventions ,Axon and dendritic guidance ,Cell type diversity ,Development of the nervous system ,Somatosensory Cortex ,General Chemistry ,Axons ,Mice, Inbred C57BL ,030104 developmental biology ,medicine.anatomical_structure ,Animals, Newborn ,nervous system ,Cerebral cortex ,Excitatory postsynaptic potential ,lcsh:Q ,Neuron ,Neuroscience ,030217 neurology & neurosurgery - Abstract
Interhemispheric axons of the corpus callosum (CC) facilitate the higher order functions of the cerebral cortex. According to current views, callosal and non-callosal fates are determined early after a neuron's birth, and certain populations, such as cortical layer (L) 4 excitatory neurons of the primary somatosensory (S1) barrel, project only ipsilaterally. Using a novel axonal-retrotracing strategy and GFP-targeted visualization of Rorb+ neurons, we instead demonstrate that L4 neurons develop transient interhemispheric axons. Locally restricted L4 connectivity emerges when exuberant contralateral axons are refined in an area- and layer-specific manner during postnatal development. Surgical and genetic interventions of sensory circuits demonstrate that refinement rates depend on distinct inputs from sensory-specific thalamic nuclei. Reductions in input-dependent refinement result in mature functional interhemispheric hyperconnectivity, demonstrating the plasticity and bona fide callosal potential of L4 neurons. Thus, L4 neurons discard alternative interhemispheric circuits as instructed by thalamic input. This may ensure optimal wiring., This work was funded by grants from MINECO SAF2014-52119-R, BFU2016-81887-REDT, PCIN-2015-176-C02-02/ERA-Net Neuron (Era-Net,MINECO), MCIU/AEI/FEDER, UE SAF2017-83117-R.
- Published
- 2019
16. Regulation of retinal interneuron subtype identity by the Iroquois homeobox gene Irx6.
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Star, Erin N., Minyan Zhu, Zhiwei Shi, Haiquan Liu, Pashmforoush, Mohammad, Sauve, Yves, Bruneau, Benoit G., and Chow, Robert L.
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- *
NEURONS , *NEURAL circuitry , *TRANSCRIPTION factors , *TACHYKININS , *RETINAL diseases , *INTERPHOTORECEPTOR matrix - Abstract
Interneuronal subtype diversity lies at the heart of the distinct molecular properties and synaptic connections that shape the formation of the neuronal circuits that are necessary for the complex spatial and temporal processing of sensory information. Here, we investigate the role of Irx6, a member of the Iroquois homeodomain transcription factor family, in regulating the development of retinal bipolar interneurons. Using a knock-in reporter approach, we show that, in the mouse retina, Irx6 is expressed in type 2 and 3a OFF bipolar interneurons and is required for the expression of cell type-specific markers in these cells, likely through direct transcriptional regulation. In Irx6 mutant mice, presumptive type 3a bipolar cells exhibit an expansion of their axonal projection domain to the entire OFF region of the inner plexiform layer, and adopt molecular features of both type 2 and 3a bipolar cells, highlighted by the ectopic upregulation of neurokinin 3 receptor (Nk3r) and Vsx1. These findings reveal Irx6 as a key regulator of type 3a bipolar cell identity that prevents these cells from adopting characteristic features of type 2 bipolar cells. Analysis of the Irx6;Vsx1 double null retina suggests that the terminal differentiation of type 2 bipolar cells is dependent on the combined expression of the transcription factors Irx6 and Vsx1, but also points to the existence of Irx6;Vsx1-independent mechanisms in regulating OFF bipolar subtype-specific gene expression. This work provides insight into the generation of neuronal subtypes by revealing a mechanism in which opposing, yet interdependent, transcription factors regulate subtype identity. [ABSTRACT FROM AUTHOR]
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- 2012
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17. A GABAergic Maf-expressing interneuron subset regulates the speed of locomotion in Drosophila
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Babski, H., Jovanic, Tihana, Surel, C., Yoshikawa, S., Zwart, M., Valmier, J., Thomas, J., Enriquez, J., Carroll, P., Garces, A., Institut des Neurosciences de Montpellier - Déficits sensoriels et moteurs (INM), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM), Institut des Neurosciences Paris-Saclay (NeuroPSI), Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), Décision et processus Bayesiens / Decision and Bayesian Computation, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), The Salk Institute for Biological Studies, School of Psychology & Neuroscience, University of St Andrews [Scotland], Institut de Génomique Fonctionnelle de Lyon (IGFL), École normale supérieure - Lyon (ENS Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS), Institut des Neurosciences de Montpellier (INM), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), École normale supérieure de Lyon (ENS de Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), ANR-17-CE37-0019,DECISIONSEQ,Base neuronale de la prise de decision et de sequences compartementales(2017), Centre National de la Recherche Scientifique (CNRS), Institut des Neurosciences de Paris-Saclay (Neuro-PSI), University of St Andrews. School of Psychology and Neuroscience, University of St Andrews. Centre for Biophotonics, and University of St Andrews. Institute of Behavioural and Neural Sciences
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Embryo, Nonmammalian ,Maf Transcription Factors, Large ,Chemistry(all) ,MESH: Drosophila ,QH301 Biology ,[SDV]Life Sciences [q-bio] ,[SDV.NEU.NB]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Neurobiology ,MESH: gamma-Aminobutyric Acid ,Animals, Genetically Modified ,Drosophila Proteins ,MESH: Animals ,MESH: Gene Silencing ,lcsh:Science ,gamma-Aminobutyric Acid ,R2C ,[SDV.NEU.PC]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Psychology and behavior ,musculoskeletal, neural, and ocular physiology ,MESH: Maf Transcription Factors, Large ,Cell type diversity ,[SDV.NEU.SC]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Cognitive Sciences ,MESH: Interneurons ,MESH: Gene Expression Regulation ,MESH: Motor Activity ,Larva ,Drosophila ,Spinal Nerve Roots ,BDC ,Locomotion ,MESH: Spinal Nerve Roots ,animal structures ,MESH: Drosophila Proteins ,Science ,NDAS ,MESH: Locomotion ,Motor Activity ,Physics and Astronomy(all) ,Article ,MESH: Animals, Genetically Modified ,QH301 ,Interneurons ,Proto-Oncogene Proteins ,[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN] ,Developmental biology ,Animals ,Gene Silencing ,Biochemistry, Genetics and Molecular Biology(all) ,fungi ,MESH: Embryo, Nonmammalian ,MESH: Proto-Oncogene Proteins ,Gene Expression Regulation ,nervous system ,lcsh:Q ,MESH: Larva - Abstract
Interneurons (INs) coordinate motoneuron activity to generate appropriate patterns of muscle contractions, providing animals with the ability to adjust their body posture and to move over a range of speeds. In Drosophila larvae several IN subtypes have been morphologically described and their function well documented. However, the general lack of molecular characterization of those INs prevents the identification of evolutionary counterparts in other animals, limiting our understanding of the principles underlying neuronal circuit organization and function. Here we characterize a restricted subset of neurons in the nerve cord expressing the Maf transcription factor Traffic Jam (TJ). We found that TJ+ neurons are highly diverse and selective activation of these different subtypes disrupts larval body posture and induces specific locomotor behaviors. Finally, we show that a small subset of TJ+ GABAergic INs, singled out by the expression of a unique transcription factors code, controls larval crawling speed., Spinal interneurons (IN) coordinate motoneuron activity to modulate locomotion behavior. Here, the authors characterize a subset of IN subtypes expressing the Maf transcription factor Traffic Jam (TJ) and report the distinct effects of their activation on body posture and locomotion in Drosophila larvae.
- Published
- 2019
18. A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity.
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Levy, Shani, Elek, Anamaria, Grau-Bové, Xavier, Menéndez-Bravo, Simón, Iglesias, Marta, Tanay, Amos, Mass, Tali, and Sebé-Pedrós, Arnau
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SCLERACTINIA , *SYMBIOSIS , *CORAL reefs & islands , *MARINE ecology , *COLONIAL animals (Marine invertebrates) , *CORALS , *CORAL bleaching , *SKELETON - Abstract
Stony corals are colonial cnidarians that sustain the most biodiverse marine ecosystems on Earth: coral reefs. Despite their ecological importance, little is known about the cell types and molecular pathways that underpin the biology of reef-building corals. Using single-cell RNA sequencing, we define over 40 cell types across the life cycle of Stylophora pistillata. We discover specialized immune cells, and we uncover the developmental gene expression dynamics of calcium-carbonate skeleton formation. By simultaneously measuring the transcriptomes of coral cells and the algae within them, we characterize the metabolic programs involved in symbiosis in both partners. We also trace the evolution of these coral cell specializations by phylogenetic integration of multiple cnidarian cell type atlases. Overall, this study reveals the molecular and cellular basis of stony coral biology. [Display omitted] • Whole-organism single-cell analysis of the stony coral Stylophora pistillata • Skeleton formation and symbiosis-associated gene expression dynamics • Identification of immune cell programs in Stylophora pistillata • Conserved broad cell type identities across cnidarian lineages Over 40 cell types across the life cycle of Stylophora pistillata , a stony coral, are identified through the use of single-cell RNA sequencing. From this reference atlas, the molecular pathways underpinning coral reef building, specialized immune cells, and the metabolic programs involved in symbiosis between coral and algae partners are described. [ABSTRACT FROM AUTHOR]
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- 2021
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19. Mass spectrometry quantitation of proteins from small pools of developing auditory and vestibular cells
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Dongseok Choi, David P. Corey, Ashok P. Reddy, Deborah I. Scheffer, Larry L. David, Peter G. Barr-Gillespie, and Jocelyn F. Krey
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0301 basic medicine ,Statistics and Probability ,Data Descriptor ,Proteome ,Cell ,Proteomic analysis ,Sensory system ,Library and Information Sciences ,Mass spectrometry ,Education ,Hair Cells, Vestibular ,Mice ,03 medical and health sciences ,Hair Cells, Auditory ,Inner ear ,Organelle ,otorhinolaryngologic diseases ,medicine ,Animals ,Cochlea ,Vestibular system ,Chemistry ,Cell type diversity ,Computer Science Applications ,Cell biology ,030104 developmental biology ,medicine.anatomical_structure ,sense organs ,Statistics, Probability and Uncertainty ,Information Systems - Abstract
Hair cells of the inner ear undergo postnatal development that leads to formation of their sensory organelles, synaptic machinery, and in the case of cochlear outer hair cells, their electromotile mechanism. To examine how the proteome changes over development from postnatal days 0 through 7, we isolated pools of 5000 Pou4f3-Gfp positive or negative cells from the cochlea or utricles; these cell pools were analysed by data-dependent and data-independent acquisition (DDA and DIA) mass spectrometry. DDA data were used to generate spectral libraries, which enabled identification and accurate quantitation of specific proteins using the DIA datasets. DIA measurements were extremely sensitive; we were able to detect proteins present at less than one part in 100,000 from only 312 hair cells. The DDA and DIA datasets will be valuable for accurately quantifying proteins in hair cells and non-hair cells over this developmental window.
- Published
- 2018
20. Integration of temporal and spatial patterning generates neural diversity
- Author
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Claire Bertet, Kevin P. White, June Ng, Lionel Senderowicz, Urfa Arain, Clara Koo, Claude Desplan, Xin Li, Zhenqing Chen, Rudy Behnia, Ted Erclik, Alberto Del Valle Rodriguez, Nicolas Nègre, Ryan Baumert, Maximilien Courgeon, New York University, New York University [New York] (NYU), NYU System (NYU)-NYU System (NYU), Beijing University of Posts ans Telecommunications (BUPT), Institut de Biologie du Développement de Marseille (IBDM), Aix Marseille Université (AMU)-Collège de France (CdF (institution))-Centre National de la Recherche Scientifique (CNRS), Department of Biology, Northern Arizona University [Flagstaff], New York University [Abu Dhabi], NYU System (NYU), University of Chicago, Institute for Genomics and Systems Biology - Department of Human Genetics, National Institutes of Health (NIH) [R01 EY017916], Canadian Institutes of Health Research (CIHR), Natural Sciences and Engineering Research Council of Canada (NSERC) [RGPIN-2015-06457], Robert Leet and Clara Guthrie Patterson Trust Postdoctoral Fellowship, EMBO [ALTF 680-2009], HFSPO [LT000077/2010-L], and NIH [U01HG004264]
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Male ,0301 basic medicine ,Neuropil ,Time Factors ,Biodiversité et Ecologie ,[SDV]Life Sciences [q-bio] ,[SDV.NEU.NB]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Neurobiology ,Cell Movement ,neurone ,[SDV.BDD]Life Sciences [q-bio]/Development Biology ,Neurons ,Multidisciplinary ,biology ,Pupa ,Brain ,Cell type diversity ,Cell Differentiation ,Anatomy ,drosophila ,Neural stem cell ,Neuroepithelial cell ,Drosophila melanogaster ,medicine.anatomical_structure ,Female ,Neural patterning ,Neurogenesis ,Developmental neurogenesis ,[SDV.BC]Life Sciences [q-bio]/Cellular Biology ,Article ,Biodiversity and Ecology ,03 medical and health sciences ,Spatio-Temporal Analysis ,Neuroblast ,medicine ,Animals ,Medulla ,Body Patterning ,diversité ,Neural stem cells ,Optic Lobe, Nonmammalian ,moelle ,[SDV.BDD.MOR]Life Sciences [q-bio]/Development Biology/Morphogenesis ,biology.organism_classification ,030104 developmental biology ,nervous system ,Retinotopy ,Neuron ,[SDE.BE]Environmental Sciences/Biodiversity and Ecology ,Neuroscience - Abstract
International audience; In the Drosophila optic lobes, 800 retinotopically organized columns in the medulla act as functional units for processing visual information. The medulla contains over 80 types of neuron, which belong to two classes: uni-columnar neurons have a stoichiometry of one per column, while multi-columnar neurons contact multiple columns. Here we show that combinatorial inputs from temporal and spatial axes generate this neuronal diversity: all neuroblasts switch fates over time to produce different neurons; the neuroepithelium that generates neuroblasts is also subdivided into six compartments by the expression of specific factors. Uni-columnar neurons are produced in all spatial compartments independently of spatial input; they innervate the neuropil where they are generated. Multi-columnar neurons are generated in smaller numbers in restricted compartments and require spatial input; the majority of their cell bodies subsequently move to cover the entire medulla. The selective integration of spatial inputs by a fixed temporal neuroblast cascade thus acts as a powerful mechanism for generating neural diversity, regulating stoichiometry and the formation of retinotopy.
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- 2017
21. Cell-Type Specificity of Genomic Imprinting in Cerebral Cortex.
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Laukoter, Susanne, Pauler, Florian M., Beattie, Robert, Amberg, Nicole, Hansen, Andi H., Streicher, Carmen, Penz, Thomas, Bock, Christoph, and Hippenmeyer, Simon
- Subjects
- *
GENOMIC imprinting , *CEREBRAL cortex , *CEREBRAL cortex development , *PLANT gene silencing , *GENE expression , *MAMMAL genomes , *CHROMOSOMES - Abstract
In mammalian genomes, a subset of genes is regulated by genomic imprinting, resulting in silencing of one parental allele. Imprinting is essential for cerebral cortex development, but prevalence and functional impact in individual cells is unclear. Here, we determined allelic expression in cortical cell types and established a quantitative platform to interrogate imprinting in single cells. We created cells with uniparental chromosome disomy (UPD) containing two copies of either the maternal or the paternal chromosome; hence, imprinted genes will be 2-fold overexpressed or not expressed. By genetic labeling of UPD, we determined cellular phenotypes and transcriptional responses to deregulated imprinted gene expression at unprecedented single-cell resolution. We discovered an unexpected degree of cell-type specificity and a novel function of imprinting in the regulation of cortical astrocyte survival. More generally, our results suggest functional relevance of imprinted gene expression in glial astrocyte lineage and thus for generating cortical cell-type diversity. • Uniform allelic expression of imprinted genes in major forebrain cell types • Cortical cell-type-specific expression levels of imprinted genes • Cell-type-specific transcriptional responses in uniparental chromosome disomy (UPD) • Cortical cell-type-specific phenotype in cells with UPD Laukoter et al. analyze prevalence and functional impact of genomic imprinting, an epigenetic phenomenon resulting in the silencing of one parental allele, in cerebral cortex development at the single-cell level. They find a high degree of cell-type specificity and a novel function of imprinting in cortical astrocyte development. [ABSTRACT FROM AUTHOR]
- Published
- 2020
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22. A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity
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Marta Iglesias, Arnau Sebé-Pedrós, Simón Menéndez-Bravo, Amos Tanay, Anamaria Elek, Shani Levy, Tali Mass, and Xavier Grau-Bové
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Cnidaria ,invertebrate immunity ,cell type diversity ,Coral ,Stylophora pistillata ,General Biochemistry, Genetics and Molecular Biology ,Article ,Transcriptome ,03 medical and health sciences ,0302 clinical medicine ,Symbiosis ,Algae ,evolution ,scRNA-seq ,Animals ,Marine ecosystem ,14. Life underwater ,Phylogeny ,Coralls ,Ecosystem ,030304 developmental biology ,0303 health sciences ,geography ,geography.geographical_feature_category ,biology ,Sequence Analysis, RNA ,Coral Reefs ,fungi ,Immunity ,technology, industry, and agriculture ,Calcinosis ,Coral reef ,biochemical phenomena, metabolism, and nutrition ,biology.organism_classification ,biomineralization ,Anthozoa ,Evolutionary biology ,population characteristics ,dinoflagellates ,Single-Cell Analysis ,030217 neurology & neurosurgery ,Genètica ,geographic locations - Abstract
Summary Stony corals are colonial cnidarians that sustain the most biodiverse marine ecosystems on Earth: coral reefs. Despite their ecological importance, little is known about the cell types and molecular pathways that underpin the biology of reef-building corals. Using single-cell RNA sequencing, we define over 40 cell types across the life cycle of Stylophora pistillata. We discover specialized immune cells, and we uncover the developmental gene expression dynamics of calcium-carbonate skeleton formation. By simultaneously measuring the transcriptomes of coral cells and the algae within them, we characterize the metabolic programs involved in symbiosis in both partners. We also trace the evolution of these coral cell specializations by phylogenetic integration of multiple cnidarian cell type atlases. Overall, this study reveals the molecular and cellular basis of stony coral biology., Graphical abstract, Highlights • Whole-organism single-cell analysis of the stony coral Stylophora pistillata • Skeleton formation and symbiosis-associated gene expression dynamics • Identification of immune cell programs in Stylophora pistillata • Conserved broad cell type identities across cnidarian lineages, Over 40 cell types across the life cycle of Stylophora pistillata, a stony coral, are identified through the use of single-cell RNA sequencing. From this reference atlas, the molecular pathways underpinning coral reef building, specialized immune cells, and the metabolic programs involved in symbiosis between coral and algae partners are described.
- Full Text
- View/download PDF
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