The origin and evolution of cell types

Arendt, Detlev; Musser, Jacob M.; Baker, Clare V. H.; Bergman, Aviv; Cepko, Connie; Erwin, Douglas H.; Pavličev, Mihaela; Schlosser, Gerhard; Widder, Stefanie; Laubichler, Manfred D.; Wagner, Günter P.

doi:10.1038/nrg.2016.127

Cited by 656 publications

(672 citation statements)

References 162 publications

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“…The PPE also gives rise to mechanosensing hair cells of lateral lines in the trunk of anamniote vertebrates and those in vertebrate inner ears (1). The development of the mechanosensing hair cells in vertebrates and that of the mechanosensory neurons in worm and fly both depend on Atoh1/lin-32 (22,38). On the contrary, Ciona BTNs and vertebrate DRG neurons require Neurogenin/ngn-1 (9).…”

Section: Discussionmentioning

confidence: 99%

Conserved gene regulatory module specifies lateral neural borders across bilaterians

Zhao

Horie

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The lateral neural plate border (NPB), the neural part of the vertebrate neural border, is composed of central nervous system (CNS) progenitors and peripheral nervous system (PNS) progenitors. In invertebrates, PNS progenitors are also juxtaposed to the lateral boundary of the CNS. Whether there are conserved molecular mechanisms determining vertebrate and invertebrate lateral neural borders remains unclear. Using single-cell-resolution gene-expression profiling and genetic analysis, we present evidence that orthologs of the NPB specification module specify the invertebrate lateral neural border, which is composed of CNS and PNS progenitors. First, like in vertebrates, the conserved neuroectoderm lateral border specifier Msx/vab-15 specifies lateral neuroblasts in Caenorhabditis elegans. Second, orthologs of the vertebrate NPB specification module (Msx/vab-15, Pax3/7/pax-3, and Zic/ref-2) are significantly enriched in worm lateral neuroblasts. In addition, like in other bilaterians, the expression domain of Msx/vab-15 is more lateral than those of Pax3/7/pax-3 and Zic/ref-2 in C. elegans. Third, we show that Msx/vab-15 regulates the development of mechanosensory neurons derived from lateral neural progenitors in multiple invertebrate species, including C. elegans, Drosophila melanogaster, and Ciona intestinalis. We also identify a novel lateral neural border specifier, ZNF703/tlp-1, which functions synergistically with Msx/vab-15 in both C. elegans and Xenopus laevis. These data suggest a common origin of the molecular mechanism specifying lateral neural borders across bilaterians.C. elegans | neural plate border | neural border | Msx/vab-15 | ZNF703/tlp-1 T he vertebrate neural border is a transient embryonic domain located between the neural plate and nonneurogenic ectoderm from late gastrulation to early neurulation. The neural border is composed of the lateral neural plate border (NPB) and preplacode ectoderm (PPE) subdomains (1, 2). The NPB and PPE give rise to the neural crest and placode, respectively, both of which undergo epithelial-to-mesenchymal transition/delamination, migrate in prototypical paths, and give rise to the peripheral nervous system (PNS) and many other cell types (3, 4). However, the NPB and PPE also have many different features (5). For example, the PPE is confined to the anterior half of embryos and does not contribute to the central nervous system (CNS), whereas the NPB is the lateral border of the whole neural plate and consists not only of progenitors for the PNS but also those for the CNS in the dorsal neural tube. The juxtaposed localization of the CNS neuroectoderm and PNS progenitors also occurs in the trunk of invertebrate embryos such as nematodes, arthropods, annelids, and urochordates (6-9), reminiscent of vertebrate NPB. In Caenorhabditis elegans, lateral neuroblasts (P, Q, and V5 cells) are located between the embryonic CNS and skin from the birth of these cells (10). In addition, worm lateral neuroblasts possess several key cellular and developmental features of vertebra...

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Section: Discussionmentioning

confidence: 99%

Conserved gene regulatory module specifies lateral neural borders across bilaterians

Zhao

Horie

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…This allows investigation into the genetic repertoire being used in a cell type as well as potentially revealing cell lineages and subpopulations within a cell type (Shapiro et al, 2013;Dueck et al, 2016). Cell type specific transcriptomes are also important for understanding cell behaviour and identity within an organism, with recent studies suggesting these datasets also hold the potential of revealing cell type evolutionary histories (Achim and Arendt, 2014;Arendt et al, 2016). In sponges, a recent study sequenced cell type specific transcriptomes of choanocytes, archeocytes and a mixture of other cell types in the freshwater sponge E. fluviatilis (Alié et al, 2015).…”

Section: Cell Type Transcriptomes and Their Use In Comparative Analysesmentioning

confidence: 99%

“…The comparison here is between one cell type within an organism (sponge choanocytes) and a unicellular organism (choanoflagellates). Homologous cells are defined as "cell types that trace back to the same cell type in a common ancestor" (Wagner, 2014;Arendt et al, 2016). When this definition is applied to sponge choanocytes and choanoflagellates, the common ancestor in this case, is the last common ancestor (LCA) between metazoan and choanoflagellate lineages.…”

Section: The Proposed Homology Between Sponge Choanocytes and Choanofmentioning

confidence: 99%

“…Having said this, these results do not necessarily reject their suggested homology, as all of these observed differences could be the product of at least 900 million years (Hedges et al, 2004;Tweedt and Erwin, 2015) of independent evolution. As mentioned in Chapter 3, further investigation of deeply conserved genes and regulatory networks shared between sponges and choanoflagellates is required to determine if the core regulatory complexes (CoRCs) of sponge choanocytes and choanoflagellates have shared components (Wagner, 2014;Arendt et al, 2016).…”

Section: The Proposed Homology Between Sponge Choanocytes and Choanofmentioning

confidence: 99%

“…convergence with choanoflagellates) cannot be determined yet. In studies observing cell type evolution within and between species, it is crucial to identify the cell type-specific core regulatory complex (CoRC) (Wagner, 2014;Arendt et al, 2016). The CoRC consists of the repertoire of transcription factors and the surrounding regulatory mechanisms, allowing homologous cell types to be recognizable throughout evolution due to the strong evolutionary conservation of these core regulatory mechanisms (Wagner, 2014).…”

Section: Cell Type Transcriptomes Enriched In Genes Indicative Of Thementioning

confidence: 99%

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The biology of choanocytes and choanocyte chambers and their role in the sponge stem cell system

Sogabe¹

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Metazoan multicellularity required the evolution of cellular processes such as cell differentiation, cell-cell adhesion and communication, along with complex gene regulatory networks and the emergence of a stem cell system. Choanocytes, the collared feeding cells in sponges, have been extensively compared to choanoflagellates, the closest sister group to metazoans due to their morphological similarities and their capacity to form multicellular structures. Recently available genomic and transcriptomic data alongside observational studies on the multicellular colonies in choanoflagellate Salpingoeca rosetta, revealed many genes shared with metazoans are upregulated only when the S. rosetta cells form colonies, while there has been little progress made on understanding the development of sponge choanocyte chambers. Choanocytes have also been suggested as playing a part in the sponge stem cell system, but again, there is limited knowledge on their general biology. To expand our understanding on this unique feeding cell that has potential stem cell capacities as well as a long-suggested homology with a closely related unicellular holozoan, I investigated molecular mechanisms underlying the development and maintenance of choanocyte chambers in the demosponge Amphimedon queenslandica.During my PhD, I have documented the formation and maintenance of choanocyte chambers in detail using cell trackers and proliferation assays, showing their dynamic nature in the sponge body as part of the stem cell system. Contrary to previous studies in sponges as well as choanoflagellates, I found that choanocyte chamber development is not always clonal, and a chamber is not always comprised of a clonal cell population. After metamorphosis, choanocytes in these chambers are also capable of dedifferentiating into archeocytes, which can subsequently differentiate into multiple cell types including new choanocyte chambers. I propose that choanocyte chambers in A. queenslandica are playing a central role in the stem cell system, increasing and maintaining the stem cell population. I have also identified genes uniquely expressed in choanocytes, as well as archeocytes (primary stem cells) and pinacocytes (epithelial cells) by manually isolating these cell types from adult sponges, which was sequenced using CEL-Seq. From this, I have obtained a reliable transcriptome for three major cell types comprising the sponge body plan. A number of analyses on the A. queenslandica choanocyte transcriptome and publicly available choanoflagellate datasets, show no strong evidence of a shared gene repertoire between choanocytes and choanoflagellates. This thesis provides a detailed documentation of choanocyte chambers and their biology in the sponge body, along with developing a number of lab-based III techniques and cell-type specific transcriptomes to be utilized for further investigation on the sponge stem cell system and the evolution of metazoan multicellularity.

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Single‐Cell Transcriptomics

Ballouz¹

2020

Encyclopedia of Life Sciences

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Single‐cell transcriptomics is an emerging field with a variety of applications, from revealing tissue heterogeneity and cell identity to deepening our understanding of complex biological systems. Single‐cell RNA‐sequencing assays the transcriptome of individual cells, allowing for a refined resolution of transcription compared to the averaged profiles from bulk RNA‐sequencing. Advances in the technology have resulted in a surplus of protocols, computational methods and studies. Multiple experimental approaches to isolate and sequence single cells provide many levels of coverage and throughput, allowing for the growth of computational pipelines and methods to assess and analyse this plethora. These advances will allow for the transcriptional documentation of all cells and cell types, which brings forth yet unknown opportunities for understanding all cellular life. Key Concepts Single‐cell transcriptomics has revolutionised the field of functional genomics, allowing for the evaluation of the transcriptome at cellular resolution. Novel technologies have made it simple to sequence 1000s–10 000s of cells at a time. Computational methods continue to advance in order to analyse and integrate the millions of cell samples. Cellular temporal resolutions, rather than bulk averages, have allowed for lineage tracing to study development and differentiation, the discovery of subpopulations and rare cell types to assess tissue heterogeneity, with particular applications to disease. Technical and biological noise still remains a major challenge, along with computational scalability and costs. Integration of transcriptional information along with genomic, epigenomic and spatial data at the single‐cell level will expand our understanding further.

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The origin and evolution of cell types

Cited by 656 publications

References 162 publications

Conserved gene regulatory module specifies lateral neural borders across bilaterians

Conserved gene regulatory module specifies lateral neural borders across bilaterians

The biology of choanocytes and choanocyte chambers and their role in the sponge stem cell system

Single‐Cell Transcriptomics

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