Biology subjects

Rentzsch, F.

Publications and source records attributed to Rentzsch, F..

9 recordsLinked to original sources

bioRxiv2025

Ectopic head regeneration after nervous system ablation in a sea anemone

Some animals are able to regenerate all missing cell types and large body parts after bisection, a phenomenon called whole-body regeneration. Many of these animals regenerate the correct tissues and structures with remarkable fidelity according to the original polarity of the body, reflecting positional information present in the remaining tissue. Understanding the cellular and molecular basis of this positional information is a central question in regeneration biology. In planarians and acoels, muscle cells have been shown to carry such positional information, but where this information originates and whether this function is conserved in other highly regenerative animals, is not well understood. Here we use the cnidarian Nematostella vectensis to address the role of the nervous system in whole-body regeneration. We generated a transgenic line for conditional ablation of neurons and first showed that Nematostella can repeatedly regenerate its nervous system. Bisection experiments following nervous system ablation showed that all head fragments regenerate a second head instead of a foot, whereas foot fragments correctly regenerate the missing head. We further found that regenerating head fragments of nervous system-ablated animals increase the expression of Wnt signaling genes that in wildtype animals are only upregulated in regenerating foot fragments. These molecular changes and the initiation of ectopic head regeneration precede the re-appearance of neurons, suggesting that the nervous system does not directly control whether a head or foot will be regenerated. Instead, we propose a model in which the nervous system provides positional information to the tissue of the body column, and that this information allows foot regeneration by suppressing a default program for head regeneration.

developmental biology↗

bioRxiv2022

NvPrdm14d-expressing neural progenitor cells contribute to non-ectodermal neurogenesis in Nematostella vectensis

Neurogenesis has been studied extensively in the ectoderm, from which most animals generate the majority of their neurons. Neurogenesis from non-ectodermal tissue is, in contrast, poorly understood. Here we use the cnidarian Nematostella vectensis as a model to provide new insights into the molecular regulation of non-ectodermal neurogenesis. We show that the transcription factor NvPrdm14d is expressed in a subpopulation of NvSoxB(2)-expressing endodermal progenitor cells and their NvPOU4-expressing progeny. Using a new transgenic reporter line, we show that NvPrdm14d-expressing cells give rise to neurons in the body wall and in close vicinity of the longitudinal retractor muscles. RNA-sequencing of NvPrdm14d::GFP-expressing cells and gene knockdown experiments provide candidate genes for the development and function of these neurons. Together, the identification of a population of endoderm-specific neural progenitor cells and of previously undescribed putative motoneurons in Nematostella provide new insights into the regulation of non-ectodermal neurogenesis.

developmental biology↗

bioRxiv2021

The chromatin-regulating CoREST complex is animal specific and essential for development in the cnidarian Nematostella vectensis

Chromatin-modifying proteins are key players in the regulation of development and cell differentiation in animals. Many individual chromatin modifiers, however, predate the evolution of animal multicellularity and how they became integrated into the regulatory networks underlying development is unclear. Here we show that CoREST is an animal-specific protein that assembles a conserved, vertebrate-like histone-modifying complex including Lsd1 and HDAC1/2 in the sea anemone Nematostella vectensis. We further show that NvCoREST expression overlaps fully with that of NvLsd1 throughout development. NvCoREST mutants, generated using CRISPR-Cas9, reveal essential roles during development and for the differentiation of cnidocytes, thereby phenocopying NvLsd1 mutants. We also show that this requirement is cell autonomous using a cell-type-specific rescue approach. Together, this shows that the evolution of CoREST allowed the formation of a chromatin-modifying complex that was present before the last common cnidarian-bilaterian ancestor and thus represents an ancient component of the animal developmental toolkit.

evolutionary biology↗

bioRxiv2021

Insm1-expressing neurons and secretory cells develop from a common pool of progenitors in the sea anemone Nematostella vectensis

Neurons are highly specialized cells present in nearly all animals, but their evolutionary origin and relationship to other cell types is not well understood. We use here the sea anemone Nematostella vectensis as a model system for early-branching animals to gain fresh insights into the evolutionary history of neurons. We generated a transgenic reporter line to show that the transcription factor NvInsm1 is expressed in post-mitotic cells that give rise to various types of neurons and secretory cells. Expression analyses, double transgenics and gene knockdown experiments show that the NvInsm1-expressing neurons and secretory cells derive from a common pool of NvSoxB(2)-positive progenitor cells. These findings, together with the requirement for Insm1 for the development of neurons and endocrine cells in vertebrates, support a close evolutionary relationship of neurons and secretory cells.

developmental biology↗

bioRxiv2020

Histone demethylase Lsd1 is required for the differentiation of neural cells in the cnidarian Nematostella vectensis

The evolution of multicellularity was accompanied by the emergence of processes to regulate cell fate, identity and differentiation in a robust and faithful manner. Chromatin regulation has emerged as a key process in development and yet its contribution to the evolution of such processes is largely unexplored. Chromatin is regulated by a diverse set of proteins, which themselves are tightly regulated in order to play cell/ tissue-specific functions. Using the cnidarian Nematostella vectensis, a model for basal metazoans, we explore the function of one such chromatin regulator, Lysine specific demethylase 1 (Lsd1). We generated an endogenously tagged allele and show that the expression of NvLsd1 is developmentally regulated and higher in differentiated neural cells than their progenitors. We further show, using a CRISPR/Cas9 generated mutant that loss of NvLsd1 leads to several distinct developmental abnormalities. Strikingly, NvLsd1 loss leads to the almost complete loss of differentiated cnidocytes, cnidarian-specific neural cells, which we show to be the result of a cell-autonomous requirement for NvLsd1. Together this suggests that complex regulation of developmental processes by chromatin modifying proteins predates the split of the cnidarian and bilaterian lineages, approximately 600 million years ago, and may constitute an ancient feature of animal development.

developmental biology↗

bioRxiv2020

Muscle cell type diversification driven by extensive gene duplications

The evolutionary mechanisms underlying the emergence of new cell types are still unclear. Here, we address the origin and diversification of muscle cells in the diploblastic sea anemone Nematostella vectensis. We discern two fast and two slow-contracting muscle cell populations in Nematostella differing by extensive sets of paralogous genes. The regulatory gene set of the slow cnidarian muscles and the bilaterian cardiac muscle are remarkably similar. By contrast, the two fast muscles differ substantially from each other, while driving the same set of paralogous structural protein genes. Our data suggest that extensive gene duplications and co-option of individual effector modules may have played an important role in cell type diversification during metazoan evolution. One Sentence SummaryThe study of the simple sea anemone suggests a molecular mechanism for cell type evolution and morphological complexity.

developmental biology↗

bioRxiv2020

The genetic basis for PRC1 complex diversity emerged early in animal evolution

Polycomb group proteins are essential regulators of developmental processes across animals. Despite their importance, studies on Polycomb are often restricted to classical model systems and, as such, little is known about the evolution of these important chromatin regulators. Here we focus on Polycomb Repressive Complex 1 (PRC1) and trace the evolution of core components of canonical and non-canonical PRC1 complexes in animals. Previous work suggested that a major expansion in the number of PRC1 complexes occurred in the vertebrate lineage. Here we show that the expansion of the PCGF protein family, an essential step for the establishment of the large diversity of PRC1 complexes found in vertebrates, predates the bilaterian-cnidarian ancestor. This means that the genetic repertoire necessary to form all major vertebrate PRC1 complexes emerged early in animal evolution, over 550 million years ago. We further show that PCGF5, a gene conserved in cnidarians and vertebrates but lost in all other studied groups, is expressed in the nervous system in the sea anemone Nematostella vectensis, similar to its mammalian counterpart. Together this work provides an evolutionary framework to understand PRC1 complex diversity and evolution and establishes Nematostella as a promising model system in which this can be further explored.

evolutionary biology↗

bioRxiv2020

NvPOU4/Brain3 functions as a terminal selector gene in the nervous system of the cnidarian Nematostella vectensis

Terminal selectors are transcription factors that control the morphological, physiological and molecular features that characterize distinct cell types. Here we use expression analyses and a transgenic reporter line to show that NvPOU4 is expressed in post-mitotic cells that give rise to a diverse set of neural cell types in the sea anemone Nematostella vectensis. We generated a loss-of-function allele by CRISPR/Cas9 and used additional transgenic reporter lines to show that the initial specification of neural cells is not affected in the NvPOU4 mutants. Analyses of transcriptomes derived from the mutants and from different neural cell populations revealed that NvPOU4 is required for the execution of the terminal differentiation program of these neural cells. These findings suggest that POU4 genes have ancient functions as terminal selectors for morphologically and functionally highly disparate types of neurons and they provide experimental support for the relevance of terminal selectors for understanding the evolution of cell types.

developmental biology↗

bioRxiv2017

Evolutionary proteomics uncovers ciliary signaling components

Cilia are organelles specialized for movement and signaling. To infer when during animal evolution signaling pathways became associated with cilia, we characterized the proteomes of cilia from three organisms: sea urchins, sea anemones and choanoflagellates. From these ciliomes, we identified 437 high confidence ciliary candidate proteins conserved in mammals, including known regulators of Hh, GPCR and TRP channel signaling. The phylogenetic profiles of their ciliary association indicate that the Hh and GPCR pathways were linked to cilia before the origin of bilateria and TRP channels before the origin of animals. We demonstrated that some of the candidates not previously implicated in ciliary biology localized to cilia and further investigated ENKUR, a TRP channel-interacting protein that we identified in the cilia of all three organisms. In animals, ENKUR is expressed by cells with motile cilia, ENKUR localizes to cilia in diverse organisms and, in both Xenopus laevis and mice, ENKUR is required for patterning the left/right axis. Moreover, mutation of ENKUR causes situs inversus in humans. Thus, proteomic profiling of cilia from diverse eukaryotes defines a conserved ciliary proteome, reveals ancient connections to Hh, GPCR and TRP channel signaling, and uncovers a novel ciliary protein that controls vertebrate development and human disease.

evolutionary biology↗