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 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 A flagellate-to-amoeboid switch in the closest living relatives of animals

2020 ◽  
Author(s):  
Thibaut Brunet ◽  
Marvin Albert ◽  
William Roman ◽  
Danielle C. Spitzer ◽  
Nicole King
Keyword(s):  
Epithelial Cells ◽  
Common Ancestor ◽  
Cell Types ◽  
Cell Phenotype ◽  
Last Common Ancestor ◽  
Animal Evolution ◽  
Amoeboid Motility ◽  
History Of ◽  
Different Cell Types ◽  
Amoeboid Cells

The evolution of different cell types was a key process of early animal evolution1–3. Two fundamental cell types, epithelial cells and amoeboid cells, are broadly distributed across the animal tree of life4,5 but their origin and early evolution are unclear. Epithelial cells are polarized, have a fixed shape and often bear an apical cilium and microvilli. These features are shared with choanoflagellates – the closest living relatives of animals – and are thought to have been inherited from their last common ancestor with animals1,6,7. The deformable amoeboid cells of animals, on the other hand, seem strikingly different from choanoflagellates and instead evoke more distantly related eukaryotes, such as diverse amoebae – but it has been unclear whether that similarity reflects common ancestry or convergence8. Here, we show that choanoflagellates subjected to spatial confinement differentiate into an amoeboid phenotype by retracting their flagella and microvilli, generating blebs, and activating myosin-based motility. Choanoflagellate cell crawling is polarized by geometrical features of the substrate and allows escape from confined microenvironments. The confinement-induced amoeboid switch is conserved across diverse choanoflagellate species and greatly expands the known phenotypic repertoire of choanoflagellates. The broad phylogenetic distribution of the amoeboid cell phenotype across animals9–14 and choanoflagellates, as well as the conserved role of myosin, suggests that myosin-mediated amoeboid motility was present in the life history of their last common ancestor. Thus, the duality between animal epithelial and crawling cells might have evolved from a temporal phenotypic switch between flagellate and amoeboid forms in their single-celled ancestors3,15,16.

scholarly journals A Single Mechanism of Biogenesis, Initiated and Directed by PIWI Proteins, Explains piRNA Production in Most Animals

2018 ◽  
Author(s):  
Ildar Gainetdinov ◽  
Cansu Colpan ◽  
Amena Arif ◽  
Katharine Cecchini ◽  
Phillip D. Zamore
Keyword(s):  
Gene Expression ◽  
Common Ancestor ◽  
Cell Types ◽  
Unified Model ◽  
Last Common Ancestor ◽  
Single Model ◽  
Regulate Gene Expression ◽  
Single Mechanism ◽  
Regulate Gene

SummaryIn animals, piRNAs guide PIWI-proteins to silence transposons and regulate gene expression. The mechanisms for making piRNAs have been proposed to differ among cell types, tissues, and animals. Our data instead suggest a single model that explains piRNA production in most animals. piRNAs initiate piRNA production by guiding PIWI proteins to slice precursor transcripts. Next, PIWI proteins direct the stepwise fragmentation of the sliced precursor transcripts, yielding tail-to-head strings of phased pre-piRNAs. Our analyses detect evidence for this piRNA biogenesis strategy across an evolutionarily broad range of animals including humans. Thus, PIWI proteins initiate and sustain piRNA biogenesis by the same mechanism in species whose last common ancestor predates the branching of most animal lineages. The unified model places PIWI-clade Argonautes at the center of piRNA biology and suggests that the ancestral animal—the Urmetazoan—used PIWI proteins both to generate piRNA guides and to execute piRNA function.

scholarly journals Spatial cell disparity in the colonial choanoflagellateSalpingoeca rosetta

2019 ◽  
Author(s):  
Benjamin Naumann ◽  
Pawel Burkhardt
Keyword(s):  
Plasma Membrane ◽  
Cell Differentiation ◽  
Common Ancestor ◽  
Single Cells ◽  
Traditional View ◽  
Published Data ◽  
Specific Cell ◽  
Last Common Ancestor ◽  
Membrane Contacts ◽  
Spatial Cell

AbstractChoanoflagellates are the closest unicellular relatives of animals (Metazoa). These tiny protists display complex life histories that include sessile as well as different pelagic stages. Some choanoflagellates have the ability to form colonies as well. Up until recently, these colonies have been described to consist of mostly identical cells showing no spatial cell differentiation, which supported the traditional view that spatial cell differentiation, leading to specific cell types in animals, evolved after the split of the last common ancestor of the Choanoflagellata and Metazoa. The recent discovery of single cells in colonies of the choanoflagellateSalpingoeca rosettathat exhibit unique cell morphologies challenges this traditional view. We have now reanalyzed TEM serial sections, aiming to determine the degree of similarity ofS. rosettacells within a rosette colony. We investigated cell morphologies and nuclear, mitochondrial and food vacuole volumes of 40 individual cells from four differentS. rosettarosette colonies and compared our findings to previously published data on sponge choanocytes. Our analysis show that cells in a choanoflagellate colony differ from each other in respect to cell morphology and content ratios of nuclei, mitochondria and food vacuoles. Furthermore, cell disparity withinS. rosettacolonies is higher compared to cell disparity within sponge choanocytes. Moreover, we discovered the presence of plasma membrane contacts between colonial cells in addition to already described intercellular bridges and filo-/pseudopodial contacts. Our findings indicate that the last common ancestor of Choanoflagellata and Metazoa might have possessed plasma membrane contacts and spatial cell disparity during colonial life history stages.

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 The Biogenetic Law and the Gastraea Theory: From Ernst Haeckel´s Discoveries to Contemporary Views

2020 ◽  
Author(s):  
Georgy S. Levit ◽  
Uwe Hoßfeld ◽  
Benjamin Naumann ◽  
Paul Lukas ◽  
Lennart Olsson
Keyword(s):  
Common Ancestor ◽  
Present Situation ◽  
Cell Types ◽  
Molecular Data ◽  
Last Common Ancestor ◽  
Ernst Haeckel ◽  
Biogenetic Law ◽  
Glass Model ◽  
Further Development ◽  
Gastraea Theory

More than 150 years ago, in 1866, Ernst Haeckel published a book in two volumes called "Generelle Morphologie der Organismen" (General Morphology of Organisms) in the first volume of which he formulated his Biogenetic law, famously stating that ontogeny recapitulates phylogeny (Rieppel 2019). Here we describe Haeckel´s original idea as first formulated in the “Generelle Morphologie der Organismen” and later further developed in other publications until the present situation in which molecular data are used to test the "hour-glass model", which can be seen as a modern version of the biogenetic law. We also tell the story about his discovery, while travelling in Norway, of an unknown organism, Magosphaera planula, that was important in that it helped to precipitate his ideas into what was to become the Gastraea theory. We also follow the further development and reformulations of the Gastraea theory by other scientists, notably the Russian school (Levit, 2007). Ilya Metchnikov developed the Phagocytella hypothesis for the origin of metazoans based on studies of a colonial flagellate. Alexey Zakhvatin focused on deducing the ancestral life cycle and the cell types of the last common ancestor of all metazoans, and Mikhailov recently pursued this line of research further.

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.

CELL AND TISSUE THERAPY OF HEART

2019 ◽  
pp. 77-84
Keyword(s):  
Extracellular Matrix ◽  
Cell Types ◽  
Heart Tissue ◽  
Decellularized Extracellular Matrix ◽  
Tissue Therapy ◽  
Essential Components ◽  
Long Time ◽  
Different Populations ◽  
A Site ◽  
Recipient Tissue

The strategy of heart tissue engineering is simple enough: first remove all the cells from a organ then take the protein scaffold left behind and repopulate it with stem cells immunologically matched to the patient in need. While various suc- cessful methods for decellularization have been developed, and the feasibility of using decellularized whole hearts and extracellular matrix to support cells has been demonstrated, the reality of creating whole hearts for transplantation and of clinical application of decellularized extracellular matrix-based scaffolds will require much more research. For example, further investigations into how lineage-restricted progenitors repopulate the decellularized heart and differentiate in a site-specific manner into different populations of the native heart would be essential. The scaffold heart does not have to be human. Pig hearts carries all the essential components of the extracellular matrix. Through trial and error, scaling up the concentration, timing and pressure of the detergents, researchers have refined the decellularization process on hundreds of hearts and other organs, but this is only the first step. Further, the framework must be populated with human cells. Most researchers in the field use a mixture of two or more cell types, such as endothelial precursor cells to line blood vessels and muscle progenitors to seed the walls of the chambers. The final challenge is one of the hardest: vasculariza- tion, placing a engineered heart into a living animal, integration with the recipient tissue, and keeping it beating for a long time. Much remains to be done before a bioartificial heart is available for transplantation in humans.

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