scholarly journals The architecture of cell differentiation in choanoflagellates and sponge choanocytes

2018 ◽  
Author(s):  
Davis Laundon ◽  
Ben Larson ◽  
Kent McDonald ◽  
Nicole King ◽  
Pawel Burkhardt
Keyword(s):  
Cell Differentiation ◽  
Cell Biology ◽  
Animal Cell ◽  
Cell Activity ◽  
Cell Types ◽  
Cell Contact ◽  
Last Common Ancestor ◽  
Animal Kingdom ◽  
Variable Nature ◽  
Salpingoeca Rosetta

SUMMARYCollar cells are ancient animal cell types which are conserved across the animal kingdom [1] and their closest relatives, the choanoflagellates [2]. However, little is known about their ancestry, their subcellular architecture, or how they differentiate. The choanoflagellate Salpingoeca rosetta [3] expresses genes necessary for animal multicellularity and development [4] and can alternate between unicellular and multicellular states [3,5], making it a powerful model to investigate the origin of animal multicellularity and mechanisms underlying cell differentiation [6,7]. To compare the subcellular architecture of solitary collar cells in S. rosetta with that of multicellular “rosettes” and collar cells in sponges, we reconstructed entire cells in 3D through transmission electron microscopy on serial ultrathin sections. Structural analysis of our 3D reconstructions revealed important differences between single and colonial choanoflagellate cells, with colonial cells exhibiting a more amoeboid morphology consistent with relatively high levels of macropinocytotic activity. Comparison of multiple reconstructed rosette colonies highlighted the variable nature of cell sizes, cell-cell contact networks and colony arrangement. Importantly, we uncovered the presence of elongated cells in some rosette colonies that likely represent a distinct and differentiated cell type. Intercellular bridges within choanoflagellate colonies displayed a variety of morphologies and connected some, but not all, neighbouring cells. Reconstruction of sponge choanocytes revealed both ultrastructural commonalities and differences in comparison to choanoflagellates. Choanocytes and colonial choanoflagellates are typified by high amoeboid cell activity. In both, the number of microvilli and volumetric proportion of the Golgi apparatus are comparable, whereas choanocytes devote less of their cell volume to the nucleus and mitochondria than choanoflagellates and more of their volume to food vacuoles. Together, our comparative reconstructions uncover the architecture of cell differentiation in choanoflagellates and sponge choanocytes and constitute an important step in reconstructing the cell biology of the last common ancestor of the animal kingdom.

scholarly journals The origin of animal multicellularity and cell differentiation

2017 ◽  
Author(s):  
Thibaut Brunet ◽  
Nicole King
Keyword(s):  
Developmental Biology ◽  
Extracellular Matrix ◽  
Cell Differentiation ◽  
Cell Biology ◽  
Common Ancestor ◽  
Cell Types ◽  
Last Common Ancestor ◽  
Matrix Synthesis ◽  
Genomic Landscape ◽  
Stem Lineage

AbstractHow animals evolved from their single-celled ancestors over 600 million years ago is poorly understood. Comparisons of genomes from animals and their closest relatives – choanoflagellates, filastereans and ichthyosporeans – have recently revealed the genomic landscape of animal origins. However, the cell and developmental biology of the first animals have been less well examined. Using principles from evolutionary cell biology, we reason that the last common ancestor of animals and choanoflagellates (the ‘Urchoanozoan’) used a collar complex - a flagellum surrounded by a microvillar collar – to capture bacterial prey. The origin of animal multicellularity likely occurred through the modification of pre-existing mechanisms for extracellular matrix synthesis and regulation of cytokinesis. The progenitors of animals likely developed clonally through serial division of flagellated cells, giving rise to sheets of cells that folded into spheres by a morphogenetic process comparable to that seen in modern choanoflagellate rosettes and calcareous sponge embryos. Finally, we infer that cell differentiation evolved in the animal stem-lineage by a combination of three mechanisms: division of labor from ancient plurifunctional cell types, conversion of temporally segregated phenotypes into spatially segregated cell types, and functional innovation.

scholarly journals Transfection of choanoflagellates illuminates their cell biology and the ancestry of animal septins

2018 ◽  
Vol 29 (25) ◽  
pp. 3026-3038 ◽  
Author(s):  
David S. Booth ◽  
Heather Szmidt-Middleton ◽  
Nicole King
Keyword(s):  
Cell Biology ◽  
Fluorescent Protein ◽  
Animal Cell ◽  
Single Cells ◽  
Dna Delivery ◽  
Cytoskeletal Proteins ◽  
Model Organisms ◽  
Protein Markers ◽  
Foreign Genes ◽  
Salpingoeca Rosetta

As the closest living relatives of animals, choanoflagellates offer unique insights into animal origins and core mechanisms underlying animal cell biology. However, unlike traditional model organisms, such as yeast, flies, and worms, choanoflagellates have been refractory to DNA delivery methods for expressing foreign genes. Here we report a robust method for expressing transgenes in the choanoflagellate Salpingoeca rosetta, overcoming barriers that have previously hampered DNA delivery and expression. To demonstrate how this method accelerates the study of S. rosetta cell biology, we engineered a panel of fluorescent protein markers that illuminate key features of choanoflagellate cells. We then investigated the localization of choanoflagellate septins, a family of GTP-binding cytoskeletal proteins that are hypothesized to regulate multicellular rosette development in S. rosetta. Fluorescently tagged septins localized to the basal poles of S. rosetta single cells and rosettes in a pattern resembling septin localization in animal epithelia. The establishment of transfection in S. rosetta and its application to the study of septins represent critical advances in the use of S. rosetta as an experimental model for investigating choanoflagellate cell biology, core mechanisms underlying animal cell biology, and the origin of animals.

scholarly journals Conserved epigenetic regulatory logic infers genes governing cell identity

2019 ◽  
Author(s):  
Woo Jun Shim ◽  
Enakshi Sinniah ◽  
Jun Xu ◽  
Burcu Vitrinel ◽  
Michael Alexanian ◽  
...  
Keyword(s):  
Cell Differentiation ◽  
Cell Biology ◽  
Peer Review Process ◽  
Cell Types ◽  
Computational Method ◽  
Cell Identity ◽  
Genome Wide ◽  
Fundamental Goal ◽  
A Genome ◽  
Wide Range

SUMMARYDetermining genes orchestrating cell differentiation in development and disease remains a fundamental goal of cell biology. This study establishes a genome-wide metric based on the gene-repressive tri-methylation of histone 3 lysine 27 (H3K27me3) across hundreds of diverse cell types to identify genetic regulators of cell differentiation. We introduce a computational method, TRIAGE, that uses discordance between gene-repressive tendency and expression to identify genetic drivers of cell identity. We apply TRIAGE to millions of genome-wide single-cell transcriptomes, diverse omics platforms, and eukaryotic cells and tissue types. Using a wide range of data, we validate TRIAGE’s performance for identifying cell-type specific regulatory factors across diverse species including human, mouse, boar, bird, fish, and tunicate. Using CRISPR gene editing, we use TRIAGE to experimentally validate RNF220 as a regulator of Ciona cardiopharyngeal development and SIX3 as required for differentiation of endoderm in human pluripotent stem cells. A record of this paper’s Transparent Peer Review process is included in the Supplemental Information.

scholarly journals Pluripotency and the origin of animal multicellularity

2019 ◽  
Author(s):  
Shunsuke Sogabe ◽  
William L. Hatleberg ◽  
Kevin M. Kocot ◽  
Tahsha E. Say ◽  
Daniel Stoupin ◽  
...  
Keyword(s):  
Stem Cells ◽  
Animal Cell ◽  
Cell Types ◽  
The Body ◽  
Sponge Cell ◽  
Limited Capacity ◽  
Cell Type ◽  
Animal Kingdom ◽  
Amphimedon Queenslandica ◽  
State Changes

The most widely held, but rarely tested, hypothesis for the origin of animals is that they evolved from a unicellular ancestor with an apical cilium surrounded by a microvillar collar that structurally resembled present-day sponge choanocytes and choanoflagellates1–4. Here we test this traditional view of the origin of the animal kingdom by comparing the transcriptomes, fates and behaviours of the three primary sponge cell types – choanocytes, pluripotent mesenchymal archeocytes and epithelial pinacocytes – with choanoflagellates and other unicellular holozoans. Unexpectedly, we find the transcriptome of sponge choanocytes is the least similar to the transcriptomes of choanoflagellates and is significantly enriched in genes unique to either animals or to sponges alone. In contrast, pluripotent archeocytes upregulate genes controlling cell proliferation and gene expression, as in other metazoan stem cells and in the proliferating stages of two closely-related unicellular holozoans, including a colonial choanoflagellate. In the context of the body plan of the sponge, Amphimedon queenslandica, we show that choanocytes appear late in development and are the result of a transdifferentiation event. They exist in a metastable state and readily transdifferentiate into archeocytes, which can differentiate into a range of other cell types. These sponge cell type conversions are similar to the temporal cell state changes that occur in many unicellular holozoans5. Together, these analyses offer no support for the homology of sponge choanocytes and choanoflagellates, nor for the view that the first multicellular animals were simple balls of cells with limited capacity to differentiate. Instead, our results are consistent with the first animal cell being able to transition between multiple states in a manner similar to modern transdifferentiating and stem cells.

scholarly journals Alternative Splicing Modulates Stem Cell Differentiation

2009 ◽  
Vol 18 (9) ◽  
pp. 1029-1038 ◽  
Author(s):  
Ru-Huei Fu ◽  
Shih-Ping Liu ◽  
Chen-Wei Ou ◽  
Hsiu-Hui Yu ◽  
Kuo-Wei Li ◽  
...  
Keyword(s):  
Stem Cells ◽  
Stem Cell ◽  
Alternative Splicing ◽  
Cell Differentiation ◽  
Cell Biology ◽  
Single Gene ◽  
Stem Cell Differentiation ◽  
Cell Types ◽  
Regulatory Elements ◽  
Multiple Transcripts

Stem cells have the surprising potential to develop into many different cell types. Therefore, major research efforts have focused on transplantation of stem cells and/or derived progenitors for restoring depleted diseased cells in degenerative disorders. Understanding the molecular controls, including alternative splicing, that arise during lineage differentiation of stem cells is crucial for developing stem cell therapeutic approaches in regeneration medicine. Alternative splicing to allow a single gene to encode multiple transcripts with different protein coding sequences and RNA regulatory elements increases genomic complexities. Utilizing differences in alternative splicing as a molecular marker may be more sensitive than simply gene expression in various degrees of stem cell differentiation. Moreover, alternative splicing maybe provide a new concept to acquire induced pluripotent stem cells or promote cell–cell transdifferentiation for restorative therapies and basic medicine researches. In this review, we highlight the recent advances of alternative splicing regulation in stem cells and their progenitors. It will hopefully provide much needed knowledge into realizing stem cell biology and related applications.

scholarly journals Choanoflagellate transfection illuminates their cell biology and the ancestry of animal septins

2018 ◽  
Author(s):  
David S. Booth ◽  
Heather Szmidt-Middleton ◽  
Nicole King
Keyword(s):  
Cell Biology ◽  
Fluorescent Protein ◽  
Animal Cell ◽  
Single Cells ◽  
Dna Delivery ◽  
Cytoskeletal Proteins ◽  
Model Organisms ◽  
Protein Markers ◽  
Foreign Genes ◽  
Salpingoeca Rosetta

ABSTRACTAs the closest living relatives of animals, choanoflagellates offer unique insights into animal origins and core mechanisms underlying animal cell biology. However, unlike traditional model organisms, such as yeast, flies and worms, choanoflagellates have been refractory to DNA delivery methods for expressing foreign genes. Here we report the establishment of a robust method for expressing transgenes in the choanoflagellate Salpingoeca rosetta, overcoming barriers that have previously hampered DNA delivery and expression. To demonstrate how this method accelerates the study of S. rosetta cell biology, we engineered a panel of fluorescent protein markers that illuminate key features of choanoflagellate cells. We then investigated the localization of choanoflagellate septins, a family of GTP-binding cytoskeletal proteins that are hypothesized to regulate the multicellular rosette development in S. rosetta. Fluorescently tagged septins localized to the basal pole of S. rosetta single cells and rosettes in a pattern resembling septin localization in animal epithelia. The establishment of transfection in S. rosetta and its application to the study of septins represent critical advances in the growth of S. rosetta as an experimental model for investigating choanoflagellate cell biology, core mechanisms underlying animal cell biology, and the origin of animals.

Adenosine Analogues as Opposite Modulators of the Cisplatin Resistance of Ovarian Cancer Cells

2019 ◽  
Vol 19 (4) ◽  
pp. 473-486 ◽  
Author(s):  
Katarzyna Bednarska-Szczepaniak ◽  
Damian Krzyżanowski ◽  
Magdalena Klink ◽  
Marek Nowak
Keyword(s):  
Cell Cycle ◽  
Ovarian Cancer ◽  
Cancer Cells ◽  
Cancer Cell ◽  
Cell Biology ◽  
Immune Cell ◽  
Immunosuppressive Agents ◽  
Cell Activity ◽  
Ovarian Cancer Cells ◽  
Adenosine Analogues

Background: Adenosine released by cancer cells in high amounts in the tumour microenvironment is one of the main immunosuppressive agents responsible for the escape of cancer cells from immunological control. Blocking adenosine receptors with adenosine analogues and restoring immune cell activity is one of the methods considered to increase the effectiveness of anticancer therapy. However, their direct effects on cancer cell biology remain unclear. Here, we determined the effect of adenosine analogues on the response of cisplatinsensitive and cisplatin-resistant ovarian cancer cells to cisplatin treatment. Methods: The effects of PSB 36, DPCPX, SCH58261, ZM 241385, PSB603 and PSB 36 on cisplatin cytotoxicity were determined against A2780 and A2780cis cell lines. Quantification of the synergism/ antagonism of the compounds cytotoxicity was performed and their effects on the cell cycle, apoptosis/necrosis events and cisplatin incorporation in cancer cells were determined. Results: PSB 36, an A1 receptor antagonist, sensitized cisplatin-resistant ovarian cancer cells to cisplatin from low to high micromolar concentrations. In contrast to PSB 36, the A2AR antagonist ZM 241385 had the opposite effect and reduced the influence of cisplatin on cancer cells, increasing their resistance to cisplatin cytotoxicity, decreasing cisplatin uptake, inhibiting cisplatin-induced cell cycle arrest, and partly restoring mitochondrial and plasma membrane potentials that were disturbed by cisplatin. Conclusion: Adenosine analogues can modulate considerable sensitivity to cisplatin of ovarian cancer cells resistant to cisplatin. The possible direct beneficial or adverse effects of adenosine analogues on cancer cell biology should be considered in the context of supportive chemotherapy for ovarian cancer.

scholarly journals Multiple Roles for Cholinergic Signaling from the Perspective of Stem Cell Function

2021 ◽  
Vol 22 (2) ◽  
pp. 666
Author(s):  
Toshio Takahashi
Keyword(s):  
Stem Cells ◽  
Stem Cell ◽  
Cell Function ◽  
Cell Activity ◽  
Embryonic Stem ◽  
Cholinergic Neurons ◽  
Cell Types ◽  
Proliferative Potential ◽  
True Nature ◽  
Cholinergic Signaling

Stem cells have extensive proliferative potential and the ability to differentiate into one or more mature cell types. The mechanisms by which stem cells accomplish self-renewal provide fundamental insight into the origin and design of multicellular organisms. These pathways allow the repair of damage and extend organismal life beyond that of component cells, and they probably preceded the evolution of complex metazoans. Understanding the true nature of stem cells can only come from discovering how they are regulated. The concept that stem cells are controlled by particular microenvironments, also known as niches, has been widely accepted. Technical advances now allow characterization of the zones that maintain and control stem cell activity in several organs, including the brain, skin, and gut. Cholinergic neurons release acetylcholine (ACh) that mediates chemical transmission via ACh receptors such as nicotinic and muscarinic receptors. Although the cholinergic system is composed of organized nerve cells, the system is also involved in mammalian non-neuronal cells, including stem cells, embryonic stem cells, epithelial cells, and endothelial cells. Thus, cholinergic signaling plays a pivotal role in controlling their behaviors. Studies regarding this signal are beginning to unify our understanding of stem cell regulation at the cellular and molecular levels, and they are expected to advance efforts to control stem cells therapeutically. The present article reviews recent findings about cholinergic signaling that is essential to control stem cell function in a cholinergic niche.

scholarly journals Morphological and Ultrastructural Characterization of Hemocytes in an Insect Model, the Hematophagous Dipetalogaster maxima (Hemiptera: Reduviidae)

Insects ◽  
2021 ◽  
Vol 12 (7) ◽  
pp. 640
Author(s):  
Natalia R. Moyetta ◽  
Fabián O. Ramos ◽  
Jimena Leyria ◽  
Lilián E. Canavoso ◽  
Leonardo L. Fruttero
Keyword(s):  
Cell Biology ◽  
Cell Types ◽  
Transmission Electron ◽  
Ultrastructural Characterization ◽  
Current Classification ◽  
Contrast Microscopy ◽  
First Time ◽  
Controversial Aspect

Hemocytes, the cells present in the hemolymph of insects and other invertebrates, perform several physiological functions, including innate immunity. The current classification of hemocyte types is based mostly on morphological features; however, divergences have emerged among specialists in triatomines, the insect vectors of Chagas’ disease (Hemiptera: Reduviidae). Here, we have combined technical approaches in order to characterize the hemocytes from fifth instar nymphs of the triatomine Dipetalogaster maxima. Moreover, in this work we describe, for the first time, the ultrastructural features of D. maxima hemocytes. Using phase contrast microscopy of fresh preparations, five hemocyte populations were identified and further characterized by immunofluorescence, flow cytometry and transmission electron microscopy. The plasmatocytes and the granulocytes were the most abundant cell types, although prohemocytes, adipohemocytes and oenocytes were also found. This work sheds light on a controversial aspect of triatomine cell biology and physiology setting the basis for future in-depth studies directed to address hemocyte classification using non-microscopy-based markers.

scholarly journals Desmosomal Molecules In and Out of Adhering Junctions: Normal and Diseased States of Epidermal, Cardiac and Mesenchymally Derived Cells

2010 ◽  
Vol 2010 ◽  
pp. 1-12 ◽  
Author(s):  
Sebastian Pieperhoff ◽  
Mareike Barth ◽  
Steffen Rickelt ◽  
Werner W. Franke
Keyword(s):  
Cell Biology ◽  
Cell Types ◽  
Cell Junctions ◽  
Surface Molecules ◽  
Transmembrane Glycoprotein ◽  
Current Cell ◽  
Plakophilin 2 ◽  
Definition Of ◽  
Adhering Junctions ◽  
Cell Cell

Current cell biology textbooks mention only two kinds of cell-to-cell adhering junctions coated with the cytoplasmic plaques: the desmosomes (maculae adhaerentes), anchoring intermediate-sized filaments (IFs), and the actin microfilament-anchoring adherens junctions (AJs), including both punctate (puncta adhaerentia) and elongate (fasciae adhaerentes) structures. In addition, however, a series of other junction types has been identified and characterized which contain desmosomal molecules but do not fit the definition of desmosomes. Of these special cell-cell junctions containing desmosomal glycoproteins or proteins we review the composite junctions (areae compositae) connecting the cardiomyocytes of mature mammalian hearts and their importance in relation to human arrhythmogenic cardiomyopathies. We also emphasize the various plakophilin-2-positive plaques in AJs (coniunctiones adhaerentes) connecting proliferatively active mesenchymally-derived cells, including interstitial cells of the heart and several soft tissue tumor cell types. Moreover, desmoplakin has also been recognized as a constituent of the plaques of thecomplexus adhaerentesconnecting certain lymphatic endothelial cells. Finally, we emphasize the occurrence of the desmosomal transmembrane glycoprotein, desmoglein Dsg2, out of the context of any junction as dispersed cell surface molecules in certain types of melanoma cells and melanocytes. This broadening of our knowledge on the diversity of AJ structures indicates that it may still be too premature to close the textbook chapters on cell-cell junctions.

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