scholarly journals From spiral cleavage to bilateral symmetry: The developmental cell lineage of the annelid brain

2018 ◽  
Author(s):  
Pavel Vopalensky ◽  
Maria Antonietta Tosches ◽  
Kaia Achim ◽  
Mette Handberg-Thorsager ◽  
Detlev Arendt
Keyword(s):  
Nervous System ◽  
Marine Invertebrates ◽  
Rotational Symmetry ◽  
Cell Lineage ◽  
Bilateral Symmetry ◽  
Cell Types ◽  
Spiral Cleavage ◽  
Larval Brain ◽  
Larval Stages ◽  
Extensive Cell

AbstractThe spiral cleavage pattern is characteristic for Spiralia (Lophotrochozoa), a large assembly of marine invertebrates. In most cases, spiral cleavage produces freely swimming, trochophora-type larvae with a simple nervous system that controls ciliary locomotion. These larvae acquire bilateral symmetry, as manifested for example in the larval brain. The transition from the rotational symmetry of spiral cleavage into the bilateral adult body has not yet been understood. Here, we present the developmental cell lineage of the brain of the annelid Platynereis dumerilii from the zygote until the mid-trochophore stage (~30 hpf), in combination with a gene expression atlas for several embryonic and larval stages. Comparison of multiple embryos reveals a highly stereotypical development and an invariant cell lineage of the differentiated cell types. In addition, we observe a fundamental subdivision of the larval brain into a highly proliferative dorsolateral region and an early differentiating ventromedial region that gives rise to the apical nervous system. The transition from rotational to bilateral symmetry progresses gradually from the lateral to the central regions. Strikingly, the spiral-to-bilateral transition does not involve extensive cell migration. Rather, corresponding cells in different spiral quadrants acquire highly divergent identities in line with their bilateral position.

scholarly journals From spiral cleavage to bilateral symmetry: the developmental cell lineage of the annelid brain

BMC Biology ◽  
2019 ◽  
Vol 17 (1) ◽  
Author(s):  
Pavel Vopalensky ◽  
Maria Antonietta Tosches ◽  
Kaia Achim ◽  
Mette Handberg-Thorsager ◽  
Detlev Arendt
Keyword(s):  
Gene Expression ◽  
Cell Lineage ◽  
Cholinergic Neurons ◽  
Bilateral Symmetry ◽  
Specific Cell ◽  
Cleavage Pattern ◽  
Spiral Cleavage ◽  
Sensory Organs ◽  
Larval Brain ◽  
Larval Stages

Abstract Background During early development, patterns of cell division—embryonic cleavage—accompany the gradual restriction of blastomeres to specific cell fates. In Spiralia, which include annelids, mollusks, and flatworms, “spiral cleavage” produces a highly stereotypic, spiral-like arrangement of blastomeres and swimming trochophore-type larvae with rotational (spiral) symmetry. However, starting at larval stages, spiralian larvae acquire elements of bilateral symmetry, before they metamorphose into fully bilateral juveniles. How this spiral-to-bilateral transition occurs is not known and is especially puzzling for the early differentiating brain and head sensory organs, which emerge directly from the spiral cleavage pattern. Here we present the developmental cell lineage of the Platynereis larval episphere. Results Live-imaging recordings from the zygote to the mid-trochophore stage (~ 30 hpf) of the larval episphere of the marine annelid Platynereis dumerilii reveal highly stereotypical development and an invariant cell lineage of early differentiating cell types. The larval brain and head sensory organs develop from 11 pairs of bilateral founders, each giving rise to identical clones on the right and left body sides. Relating the origin of each bilateral founder pair back to the spiral cleavage pattern, we uncover highly divergent origins: while some founder pairs originate from corresponding cells in the spiralian lineage on each body side, others originate from non-corresponding cells, and yet others derive from a single cell within one quadrant. Integrating lineage and gene expression data for several embryonic and larval stages, we find that the conserved head patterning genes otx and six3 are expressed in bilateral founders representing divergent lineage histories and giving rise to early differentiating cholinergic neurons and head sensory organs, respectively. Conclusions We present the complete developmental cell lineage of the Platynereis larval episphere, and thus the first comprehensive account of the spiral-to-bilateral transition in a developing spiralian. The bilateral symmetry of the head emerges from pairs of bilateral founders, similar to the trunk; however, the head founders are more numerous and show striking left-right asymmetries in lineage behavior that we relate to differential gene expression.

scholarly journals Expansion and long-range differentiation of the NKT cell lineage in mice expressing CD1d exclusively on cortical thymocytes

2005 ◽  
Vol 202 (2) ◽  
pp. 239-248 ◽  
Author(s):  
Datsen G. Wei ◽  
Hyunji Lee ◽  
Se-Ho Park ◽  
Lucie Beaudoin ◽  
Luc Teyton ◽  
...  
Keyword(s):  
Cell Lineage ◽  
Cell Types ◽  
Interferon Γ ◽  
Interleukin 4 ◽  
Thymic Epithelial Cells ◽  
Nkt Cell ◽  
Extensive Cell ◽  
Cell Type Specific ◽  
Necessary And Sufficient ◽  
Antigen Presenting

Unlike conventional major histocompatibility complex–restricted T cells, Vα14-Jα18 NKT cell lineage precursors engage in cognate interactions with CD1d-expressing bone marrow–derived cells that are both necessary and sufficient for their thymic selection and differentiation, but the nature and sequence of these interactions remain partially understood. After positive selection mediated by CD1d-expressing cortical thymocytes, the mature NKT cell lineage undergoes a series of changes suggesting antigen priming by a professional antigen-presenting cell, including extensive cell division, acquisition of a memory phenotype, the ability to produce interleukin-4 and interferon-γ, and the expression of a panoply of NK receptors. By using a combined transgenic and chimeric approach to restrict CD1d expression to cortical thymocytes and to prevent expression on other hematopoietic cell types such as dendritic cells, macrophages, or B cells, we found that, to a large extent, expansion and differentiation events could be imparted by a single-cognate interaction with CD1d-expressing cortical thymocytes. These surprising findings suggest that, unlike thymic epithelial cells, cortical thymocytes can provide unexpected, cell type–specific signals leading to lineage expansion and NKT cell differentiation.

Eutely, cell lineage, and fate within the ascidian larval nervous system: determinacy or to be determined?

2005 ◽  
Vol 83 (1) ◽  
pp. 184-195 ◽  
Author(s):  
Ian A Meinertzhagen
Keyword(s):  
Nervous System ◽  
Cell Lineage ◽  
Cell Types ◽  
Cell Number ◽  
Fixed Number ◽  
Wild Type ◽  
Halocynthia Roretzi ◽  
Cell Fates ◽  
Larval Nervous System ◽  
Larval Hatching

The larval central nervous system (CNS) of the ascidian Ciona intestinalis (L., 1767) arises from an embryonic neural plate and contains sufficiently few cells, about 330, to enable definitive counts. On the basis of such counts, there is evidence both for cell constancy (eutely) in the larval CNS and for small variations in the overall numbers of cells and among defined cell types within this total. However, evidence for the range of such deviations and the existence of a true phenotypic wild type are lacking. The record of cell lineage, i.e., the mitotic ancestry of each cell, and the fates of some of these cells have recently received increased documentation in both the genus Ciona and Halocynthia roretzi (von Drasche, 1884). Relatively few generations of cells, between 10 and 14, form the entire CNS in C. intestinalis, and cell death does not occur prior to larval hatching. The tiny complement of larval CNS cells can therefore be seen as the product of a small fixed number of determinate cleavages, and variations in cell number as the product of minor deviations in this mitotic ancestry. Within these lineage records, some cell fates have already been identified, but knowledge of most is lacking because the cells lack markers or other identifying features. Nevertheless, this tiny nervous system offers the prospect that all its cells can one day be identified, and their developmental histories and larval functions analyzed, cell by cell.

scholarly journals Intact Drosophila Whole Brain Cellular Quantitation reveals Sexual Dimorphism

2021 ◽  
Author(s):  
Wei Jiao ◽  
Gard Spreemann ◽  
Evelyne Ruchti ◽  
Soumya Banerjee ◽  
Ying Shi ◽  
...  
Keyword(s):  
Nervous System ◽  
Sexual Dimorphism ◽  
Topological Analysis ◽  
Molecular Genetic ◽  
Cell Types ◽  
Larval Brain ◽  
Gene And Protein Expression ◽  
The Central Nervous System ◽  
The Brain ◽  
Sophisticated Analysis

Establishing with precision the quantity and identity of the cell types of the brain is a prerequisite for a detailed compendium of gene and protein expression in the central nervous system. Currently however, strict quantitation of cell numbers has been achieved only for the nervous system of C.elegans. Here we describe the development of a synergistic pipeline of molecular genetic, imaging, and computational technologies designed to allow high-throughput, precise quantitation with cellular resolution of reporters of gene expression in intact whole tissues with complex cellular constitutions such as the brain. We have deployed the approach to determine with exactitude the number of functional neurons and glia in the entire intact Drosophila larval brain, revealing fewer neurons and many more glial cells than previously estimated. Moreover, we discover an unexpected divergence between the sexes at this juvenile developmental stage, with female brains having significantly more neurons than males. Topological analysis of our data establishes that this sexual dimorphism extends to deeper features of brain organisation. Our methodology enables robust and accurate quantification of the number and positioning of cells within intact organs, facilitating sophisticated analysis of cellular identity, diversity, and expression characteristics.

scholarly journals Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution

2015 ◽  
Vol 370 (1684) ◽  
pp. 20150286 ◽  
Author(s):  
Detlev Arendt ◽  
Elia Benito-Gutierrez ◽  
Thibaut Brunet ◽  
Heather Marlow
Keyword(s):  
Nervous System ◽  
Bilateral Symmetry ◽  
Cell Types ◽  
Division Of Labour ◽  
The Body ◽  
System Evolution ◽  
Lateral Body ◽  
Ventral Neural Tube ◽  
Body Sizes ◽  
Nervous System Evolution

Prerequisite for tracing nervous system evolution is understanding of the body plan, feeding behaviour and locomotion of the first animals in which neurons evolved. Here, a comprehensive scenario is presented for the diversification of cell types in early metazoans, which enhanced feeding efficiency and led to the emergence of larger animals that were able to move. Starting from cup-shaped, gastraea-like animals with outer and inner choanoflagellate-like cells, two major innovations are discussed that set the stage for nervous system evolution. First, the invention of a mucociliary sole entailed a switch from intra- to extracellular digestion and increased the concentration of nutrients flowing into the gastric cavity. In these animals, an initial nerve net may have evolved via division of labour from mechanosensory-contractile cells in the lateral body wall, enabling coordinated movement of the growing body that involved both mucociliary creeping and changes of body shape. Second, the inner surface of the animals folded into metameric series of gastric pouches, which optimized nutrient resorption and allowed larger body sizes. The concomitant acquisition of bilateral symmetry may have allowed more directed locomotion and, with more demanding coordinative tasks, triggered the evolution of specialized nervous subsystems. Animals of this organizational state would have resembled Ediacarian fossils such as Dickinsonia and may have been close to the cnidarian–bilaterian ancestor. In the bilaterian lineage, the mucociliary sole was used mostly for creeping, or frequently lost. One possible remnant is the enigmatic Reissner's fibre in the ventral neural tube of cephalochordates and vertebrates.

Seq Your Destiny: Neural Crest Fate Determination in the Genomic Era

2021 ◽  
Vol 55 (1) ◽  
Author(s):  
Shashank Gandhi ◽  
Marianne E. Bronner
Keyword(s):  
Nervous System ◽  
Neural Crest ◽  
Cell Lineage ◽  
Cell Types ◽  
The Body ◽  
Annual Review ◽  
Publication Date ◽  
Developmental Potential ◽  
Migratory Patterns ◽  
Modern Genomic

Neural crest stem/progenitor cells arise early during vertebrate embryogenesis at the border of the forming central nervous system. They subsequently migrate throughout the body, eventually differentiating into diverse cell types ranging from neurons and glia of the peripheral nervous system to bones of the face, portions of the heart, and pigmentation of the skin. Along the body axis, the neural crest is heterogeneous, with different subpopulations arising in the head, neck, trunk, and tail regions, each characterized by distinct migratory patterns and developmental potential. Modern genomic approaches like single-cell RNA- and ATAC-sequencing (seq) have greatly enhanced our understanding of cell lineage trajectories and gene regulatory circuitry underlying the developmental progression of neural crest cells. Here, we discuss how genomic approaches have provided new insights into old questions in neural crest biology by elucidating transcriptional and posttranscriptional mechanisms that govern neural crest formation and the establishment of axial level identity. Expected final online publication date for the Annual Review of Genetics, Volume 55 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Cell lineage in the developing neural tube

1998 ◽  
Vol 76 (6) ◽  
pp. 1051-1068 ◽  
Author(s):  
Anjali J Kalyani ◽  
Mahendra S Rao
Keyword(s):  
Spinal Cord ◽  
Nervous System ◽  
Cell Lineage ◽  
Cell Types ◽  
Cell Type ◽  
Developmental Potential ◽  
Environmental Signals ◽  
Cell Type Specific ◽  
Multiple Species ◽  
Sequential Restriction

Acquisition of cell type specific properties in the spinal cord is a process of sequential restriction in developmental potential. A multipotent stem cell of the nervous system, the neuroepithelial cell, generates central nervous system and peripheral nervous system derivatives via the generation of intermediate lineage restricted precursors that differ from each other and from neuroepithelial cells. Intermediate lineage restricted neuronal and glial precursors termed neuronal restricted precursors and glial restricted precursors, respectively, have been identified. Differentiation is influenced by extrinsic environmental signals that are stage and cell type specific. Analysis in multiple species illustrates similarities between chick, rat, mouse, and human cell differentiation. The utility of obtaining these precursor cell types for gene discovery, drug screening, and therapeutic applications is discussed.Key words: stem cells, oligodendrocytes, astrocytes, neurons, spinal cord.

scholarly journals Stem cell differentiation trajectories inHydraresolved at single-cell resolution

2018 ◽  
Author(s):  
Stefan Siebert ◽  
Jeffrey A. Farrell ◽  
Jack F. Cazet ◽  
Yashodara L. Abeykoon ◽  
Abby S. Primack ◽  
...  
Keyword(s):  
Nervous System ◽  
Stem Cell ◽  
Cell Differentiation ◽  
Cell Lineage ◽  
Stem Cell Differentiation ◽  
Cell Types ◽  
Differentiated Cells ◽  
Nervous System Function ◽  
Stem Cell Populations ◽  
Molecular Description

AbstractThe adultHydrapolyp continuously renews all of its cells using three separate stem cell populations, but the genetic pathways enabling homeostatic tissue maintenance are not well understood. We used Drop-seq to sequence transcriptomes of 24,985 singleHydracells and identified the molecular signatures of a broad spectrum of cell states, from stem cells to terminally differentiated cells. We constructed differentiation trajectories for each cell lineage and identified the transcription factors expressed along these trajectories, thus creating a comprehensive molecular map of all developmental lineages in the adult animal. We unexpectedly found that neuron and gland cell differentiation transits through a common progenitor state, suggesting a shared evolutionary history for these secretory cell types. Finally, we have built the first gene expression map of theHydranervous system. By producing a comprehensive molecular description of the adultHydrapolyp, we have generated a resource for addressing fundamental questions regarding the evolution of developmental processes and nervous system function.

scholarly journals Selective deletion of SHIP-1 in hematopoietic cells in mice leads to severe lung inflammation involving ILC2 cells

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Xujun Ye ◽  
Fengrui Zhang ◽  
Li Zhou ◽  
Yadong Wei ◽  
Li Zhang ◽  
...  
Keyword(s):  
Lung Inflammation ◽  
Airway Remodeling ◽  
Pulmonary Inflammation ◽  
Hematopoietic Cells ◽  
Cell Lineage ◽  
Allergic Inflammation ◽  
Cell Types ◽  
Lymphoid Cells ◽  
Whole Body

AbstractSrc homology 2 domain–containing inositol 5-phosphatase 1 (SHIP-1) regulates the intracellular levels of phosphotidylinositol-3, 4, 5-trisphosphate, a phosphoinositide 3–kinase (PI3K) product. Emerging evidence suggests that the PI3K pathway is involved in allergic inflammation in the lung. Germline or induced whole-body deletion of SHIP-1 in mice led to spontaneous type 2-dominated pulmonary inflammation, demonstrating that SHIP-1 is essential for lung homeostasis. However, the mechanisms by which SHIP-1 regulates lung inflammation and the responsible cell types are still unclear. Deletion of SHIP-1 selectively in B cells, T cells, dendritic cells (DC) or macrophages did not lead to spontaneous allergic inflammation in mice, suggesting that innate immune cells, particularly group 2 innate lymphoid cells (ILC2 cells) may play an important role in this process. We tested this idea using mice with deletion of SHIP-1 in the hematopoietic cell lineage and examined the changes in ILC2 cells. Conditional deletion of SHIP-1 in hematopoietic cells in Tek-Cre/SHIP-1 mice resulted in spontaneous pulmonary inflammation with features of type 2 immune responses and airway remodeling like those seen in mice with global deletion of SHIP-1. Furthermore, when compared to wild-type control mice, Tek-Cre/SHIP-1 mice displayed a significant increase in the number of IL-5/IL-13 producing ILC2 cells in the lung at baseline and after stimulation by allergen Papain. These findings provide some hints that PI3K signaling may play a role in ILC2 cell development at baseline and in response to allergen stimulation. SHIP-1 is required for maintaining lung homeostasis potentially by restraining ILC2 cells and type 2 inflammation.

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