Journal of Developmental Biology

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11 pages, 2009 KiB

Open AccessArticle

The Hox Gene egl-5 Acts as a Terminal Selector for VD13 Development via Wnt Signaling

by Meagan Kurland, Bryn O’Meara, Dana K. Tucker and Brian D. Ackley

J. Dev. Biol. 2020, 8(1), 5; https://doi.org/10.3390/jdb8010005 - 3 Mar 2020

Cited by 3 | Viewed by 4199

Abstract

Nervous systems are comprised of diverse cell types that differ functionally and morphologically. During development, extrinsic signals, e.g., growth factors, can activate intrinsic programs, usually orchestrated by networks of transcription factors. Within that network, transcription factors that drive the specification of features specific [...] Read more.

Nervous systems are comprised of diverse cell types that differ functionally and morphologically. During development, extrinsic signals, e.g., growth factors, can activate intrinsic programs, usually orchestrated by networks of transcription factors. Within that network, transcription factors that drive the specification of features specific to a limited number of cells are often referred to as terminal selectors. While we still have an incomplete view of how individual neurons within organisms become specified, reporters limited to a subset of neurons in a nervous system can facilitate the discovery of cell specification programs. We have identified a fluorescent reporter that labels VD13, the most posterior of the 19 inhibitory GABA (γ-amino butyric acid)-ergic motorneurons, and two additional neurons, LUAL and LUAR. Loss of function in multiple Wnt signaling genes resulted in an incompletely penetrant loss of the marker, selectively in VD13, but not the LUAs, even though other aspects of GABAergic specification in VD13 were normal. The posterior Hox gene, egl-5, was necessary for expression of our marker in VD13, and ectopic expression of egl-5 in more anterior GABAergic neurons induced expression of the marker. These results suggest egl-5 is a terminal selector of VD13, subsequent to GABAergic specification. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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10 pages, 10138 KiB

Open AccessArticle

Nematode Autotomy Requires Molting and Entails Tissue Healing without Obvious Regeneration

by Jonathan Hodgkin

J. Dev. Biol. 2019, 7(4), 21; https://doi.org/10.3390/jdb7040021 - 23 Nov 2019

Cited by 2 | Viewed by 4328

Abstract

Autotomy in C. elegans, which results in the severing of the body into two fragments, has been observed as a response to late larval worm-star formation after exposure to a bacterial surface pathogen. It was found that autotomy can occur in both [...] Read more.

Autotomy in C. elegans, which results in the severing of the body into two fragments, has been observed as a response to late larval worm-star formation after exposure to a bacterial surface pathogen. It was found that autotomy can occur in both hermaphroditic and gonochoristic nematode species, and during either the L3 or the L4 molt. Severing was hypothesized to be driven by a ‘balloon-twisting’ mechanism during molting but was found to be independent of lethargus-associated flipping. Extensive healing and apparent tissue fusion were seen at the site of scission. No obvious regeneration of lost body parts was seen in either L4 or adult truncated worms. A variety of mutants defective in processes of cell death, healing, regeneration, responses to damage, stress or pathogens were found to be competent to autotomize. Mutants specifically defective in autotomy have yet to be found. Autotomy may represent a modification of the essential normal process of molting. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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13 pages, 2868 KiB

Open AccessArticle

Integrins Have Cell-Type-Specific Roles in the Development of Motor Neuron Connectivity

by Devyn Oliver, Emily Norman, Heather Bates, Rachel Avard, Monika Rettler, Claire Y. Bénard, Michael M. Francis and Michele L. Lemons

J. Dev. Biol. 2019, 7(3), 17; https://doi.org/10.3390/jdb7030017 - 27 Aug 2019

Cited by 2 | Viewed by 6951

Abstract

Formation of the nervous system requires a complex series of events including proper extension and guidance of neuronal axons and dendrites. Here we investigate the requirement for integrins, a class of transmembrane cell adhesion receptors, in regulating these processes across classes of C. [...] Read more.

Formation of the nervous system requires a complex series of events including proper extension and guidance of neuronal axons and dendrites. Here we investigate the requirement for integrins, a class of transmembrane cell adhesion receptors, in regulating these processes across classes of C. elegans motor neurons. We show α integrin/ina-1 is expressed by both GABAergic and cholinergic motor neurons. Despite this, our analysis of hypomorphic ina-1(gm144) mutants indicates preferential involvement of α integrin/ina-1 in GABAergic commissural development, without obvious involvement in cholinergic commissural development. The defects in GABAergic commissures of ina-1(gm144) mutants included both premature termination and guidance errors and were reversed by expression of wild type ina-1 under control of the native ina-1 promoter. Our results also show that α integrin/ina-1 is important for proper outgrowth and guidance of commissures from both embryonic and post-embryonic born GABAergic motor neurons, indicating an ongoing requirement for integrin through two phases of GABAergic neuron development. Our findings provide insights into neuron-specific roles for integrin that would not be predicted based solely upon expression analysis. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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15 pages, 3642 KiB

Open AccessFeature PaperArticle

The Chromatin Remodeler LET-418/Mi2 is Required Cell Non-Autonomously for the Post-Embryonic Development of Caenorhabditis elegans

by Makhabbat Saudenova and Chantal Wicky

J. Dev. Biol. 2019, 7(1), 1; https://doi.org/10.3390/jdb7010001 - 24 Dec 2018

Cited by 5 | Viewed by 4591

Abstract

Chromatin condition is crucial for the cells to respond to their environment. In C. elegans, post-embryonic development is accompanied by the exit of progenitor cells from quiescence in response to food. The chromatin protein LET-418/Mi2 is required for this transition in development [...] Read more.

Chromatin condition is crucial for the cells to respond to their environment. In C. elegans, post-embryonic development is accompanied by the exit of progenitor cells from quiescence in response to food. The chromatin protein LET-418/Mi2 is required for this transition in development indicating that proper chromatin structure in cells of the freshly hatched larvae is important to respond to food. However, the identity of the tissue or cells where LET-418/Mi2 is required, as well as the developmental signals that it is modulating have not been elucidated. By restoring the activity of LET-418/Mi2 in specific tissues, we demonstrate that its activity in the intestine and the hypodermis is able to promote in a cell non-autonomous manner the exit of blast cells from quiescence and further development. Furthermore, we identify the IIS (insulin/insulin-like growth factor signaling) pathway to be one of the signaling pathways that is conveying LET-418/Mi2 cell non-autonomous effect on development. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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Review

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26 pages, 2305 KiB

Open AccessReview

C. elegans Apical Extracellular Matrices Shape Epithelia

by Jennifer D. Cohen and Meera V. Sundaram

J. Dev. Biol. 2020, 8(4), 23; https://doi.org/10.3390/jdb8040023 - 6 Oct 2020

Cited by 32 | Viewed by 7299

Abstract

Apical extracellular matrices (aECMs) coat exposed surfaces of epithelia to shape developing tissues and protect them from environmental insults. Despite their widespread importance for human health, aECMs are poorly understood compared to basal and stromal ECMs. The nematode Caenorhabditis elegans contains a variety [...] Read more.

Apical extracellular matrices (aECMs) coat exposed surfaces of epithelia to shape developing tissues and protect them from environmental insults. Despite their widespread importance for human health, aECMs are poorly understood compared to basal and stromal ECMs. The nematode Caenorhabditis elegans contains a variety of distinct aECMs, some of which share many of the same types of components (lipids, lipoproteins, collagens, zona pellucida domain proteins, chondroitin glycosaminoglycans and proteoglycans) with mammalian aECMs. These aECMs include the eggshell, a glycocalyx-like pre-cuticle, both collagenous and chitin-based cuticles, and other understudied aECMs of internal epithelia. C. elegans allows rapid genetic manipulations and live imaging of fluorescently-tagged aECM components, and is therefore providing new insights into aECM structure, trafficking, assembly, and functions in tissue shaping. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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18 pages, 1660 KiB

Open AccessReview

A Series of Tubes: The C. elegans Excretory Canal Cell as a Model for Tubule Development

by Matthew Buechner, Zhe Yang and Hikmat Al-Hashimi

J. Dev. Biol. 2020, 8(3), 17; https://doi.org/10.3390/jdb8030017 - 7 Sep 2020

Cited by 4 | Viewed by 7710

Abstract

Formation and regulation of properly sized epithelial tubes is essential for multicellular life. The excretory canal cell of C. elegans provides a powerful model for investigating the integration of the cytoskeleton, intracellular transport, and organismal physiology to regulate the developmental processes of tube [...] Read more.

Formation and regulation of properly sized epithelial tubes is essential for multicellular life. The excretory canal cell of C. elegans provides a powerful model for investigating the integration of the cytoskeleton, intracellular transport, and organismal physiology to regulate the developmental processes of tube extension, lumen formation, and lumen diameter regulation in a narrow single cell. Multiple studies have provided new understanding of actin and intermediate filament cytoskeletal elements, vesicle transport, and the role of vacuolar ATPase in determining tube size. Most of the genes discovered have clear homologues in humans, with implications for understanding these processes in mammalian tissues such as Schwann cells, renal tubules, and brain vasculature. The results of several new genetic screens are described that provide a host of new targets for future studies in this informative structure. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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18 pages, 1202 KiB

Open AccessFeature PaperReview

Recent Advances in the Genetic, Anatomical, and Environmental Regulation of the C. elegans Germ Line Progenitor Zone

by Kacy Gordon

J. Dev. Biol. 2020, 8(3), 14; https://doi.org/10.3390/jdb8030014 - 22 Jul 2020

Cited by 5 | Viewed by 5291

Abstract

The C. elegans germ line and its gonadal support cells are well studied from a developmental genetics standpoint and have revealed many foundational principles of stem cell niche biology. Among these are the observations that a niche-like cell supports a self-renewing stem cell [...] Read more.

The C. elegans germ line and its gonadal support cells are well studied from a developmental genetics standpoint and have revealed many foundational principles of stem cell niche biology. Among these are the observations that a niche-like cell supports a self-renewing stem cell population with multipotential, differentiating daughter cells. While genetic features that distinguish stem-like cells from their differentiating progeny have been defined, the mechanisms that structure these populations in the germ line have yet to be explained. The spatial restriction of Notch activation has emerged as an important genetic principle acting in the distal germ line. Synthesizing recent findings, I present a model in which the germ stem cell population of the C. elegans adult hermaphrodite can be recognized as two distinct anatomical and genetic populations. This review describes the recent progress that has been made in characterizing the undifferentiated germ cells and gonad anatomy, and presents open questions in the field and new directions for research to pursue. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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17 pages, 1217 KiB

Open AccessReview

Game of Tissues: How the Epidermis Thrones C. elegans Shape

by Cátia A. Carvalho and Limor Broday

J. Dev. Biol. 2020, 8(1), 7; https://doi.org/10.3390/jdb8010007 - 9 Mar 2020

Cited by 10 | Viewed by 4536

Abstract

The versatility of epithelial cell structure is universally exploited by organisms in multiple contexts. Epithelial cells can establish diverse polarized axes within their tridimensional structure which enables them to flexibly communicate with their neighbors in a 360° range. Hence, these cells are central [...] Read more.

The versatility of epithelial cell structure is universally exploited by organisms in multiple contexts. Epithelial cells can establish diverse polarized axes within their tridimensional structure which enables them to flexibly communicate with their neighbors in a 360° range. Hence, these cells are central to multicellularity, and participate in diverse biological processes such as organismal development, growth or immune response and their misfunction ultimately impacts disease. During the development of an organism, the first task epidermal cells must complete is the formation of a continuous sheet, which initiates its own morphogenic process. In this review, we will focus on the C. elegans embryonic epithelial morphogenesis. We will describe how its formation, maturation, and spatial arrangements set the final shape of the nematode C. elegans. Special importance will be given to the tissue-tissue interactions, regulatory tissue-tissue feedback mechanisms and the players orchestrating the process. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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23 pages, 4154 KiB

Open AccessReview

Axin Family of Scaffolding Proteins in Development: Lessons from C. elegans

by Avijit Mallick, Shane K. B. Taylor, Ayush Ranawade and Bhagwati P. Gupta

J. Dev. Biol. 2019, 7(4), 20; https://doi.org/10.3390/jdb7040020 - 15 Oct 2019

Cited by 13 | Viewed by 6685

Abstract

Scaffold proteins serve important roles in cellular signaling by integrating inputs from multiple signaling molecules to regulate downstream effectors that, in turn, carry out specific biological functions. One such protein, Axin, represents a major evolutionarily conserved scaffold protein in metazoans that participates in [...] Read more.

Scaffold proteins serve important roles in cellular signaling by integrating inputs from multiple signaling molecules to regulate downstream effectors that, in turn, carry out specific biological functions. One such protein, Axin, represents a major evolutionarily conserved scaffold protein in metazoans that participates in the WNT pathway and other pathways to regulate diverse cellular processes. This review summarizes the vast amount of literature on the regulation and functions of the Axin family of genes in eukaryotes, with a specific focus on Caenorhabditis elegans development. By combining early studies with recent findings, the review is aimed to serve as an updated reference for the roles of Axin in C. elegans and other model systems. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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15 pages, 1136 KiB

Open AccessReview

How Weird is The Worm? Evolution of the Developmental Gene Toolkit in Caenorhabditis elegans

by Emily A. Baker and Alison Woollard

J. Dev. Biol. 2019, 7(4), 19; https://doi.org/10.3390/jdb7040019 - 28 Sep 2019

Cited by 6 | Viewed by 9502

Abstract

Comparative developmental biology and comparative genomics are the cornerstones of evolutionary developmental biology. Decades of fruitful research using nematodes have produced detailed accounts of the developmental and genomic variation in the nematode phylum. Evolutionary developmental biologists are now utilising these data as a [...] Read more.

Comparative developmental biology and comparative genomics are the cornerstones of evolutionary developmental biology. Decades of fruitful research using nematodes have produced detailed accounts of the developmental and genomic variation in the nematode phylum. Evolutionary developmental biologists are now utilising these data as a tool with which to interrogate the evolutionary basis for the similarities and differences observed in Nematoda. Nematodes have often seemed atypical compared to the rest of the animal kingdom—from their totally lineage-dependent mode of embryogenesis to their abandonment of key toolkit genes usually deployed by bilaterians for proper development—worms are notorious rule breakers of the bilaterian handbook. However, exploring the nature of these deviations is providing answers to some of the biggest questions about the evolution of animal development. For example, why is the evolvability of each embryonic stage not the same? Why can evolution sometimes tolerate the loss of genes involved in key developmental events? Lastly, why does natural selection act to radically diverge toolkit genes in number and sequence in certain taxa? In answering these questions, insight is not only being provided about the evolution of nematodes, but of all metazoans. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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18 pages, 1946 KiB

Open AccessFeature PaperReview

Novel Technological Advances in Functional Connectomics in C. elegans

by Elizabeth M. DiLoreto, Christopher D. Chute, Samantha Bryce and Jagan Srinivasan

J. Dev. Biol. 2019, 7(2), 8; https://doi.org/10.3390/jdb7020008 - 23 Apr 2019

Cited by 12 | Viewed by 6042

Abstract

The complete structure and connectivity of the Caenorhabditis elegans nervous system (“mind of a worm”) was first published in 1986, representing a critical milestone in the field of connectomics. The reconstruction of the nervous system (connectome) at the level of synapses provided a [...] Read more.

The complete structure and connectivity of the Caenorhabditis elegans nervous system (“mind of a worm”) was first published in 1986, representing a critical milestone in the field of connectomics. The reconstruction of the nervous system (connectome) at the level of synapses provided a unique perspective of understanding how behavior can be coded within the nervous system. The following decades have seen the development of technologies that help understand how neural activity patterns are connected to behavior and modulated by sensory input. Investigations on the developmental origins of the connectome highlight the importance of role of neuronal cell lineages in the final connectivity matrix of the nervous system. Computational modeling of neuronal dynamics not only helps reconstruct the biophysical properties of individual neurons but also allows for subsequent reconstruction of whole-organism neuronal network models. Hence, combining experimental datasets with theoretical modeling of neurons generates a better understanding of organismal behavior. This review discusses some recent technological advances used to analyze and perturb whole-organism neuronal function along with developments in computational modeling, which allows for interrogation of both local and global neural circuits, leading to different behaviors. Combining these approaches will shed light into how neural networks process sensory information to generate the appropriate behavioral output, providing a complete understanding of the worm nervous system. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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13 pages, 1038 KiB

Open AccessReview

Regulation of Actin Dynamics in the C. elegans Somatic Gonad

by Charlotte A. Kelley and Erin J Cram

J. Dev. Biol. 2019, 7(1), 6; https://doi.org/10.3390/jdb7010006 - 20 Mar 2019

Cited by 11 | Viewed by 5514

Abstract

The reproductive system of the hermaphroditic nematode C. elegans consists of a series of contractile cell types—including the gonadal sheath cells, the spermathecal cells and the spermatheca–uterine valve—that contract in a coordinated manner to regulate oocyte entry and exit of the fertilized embryo [...] Read more.

The reproductive system of the hermaphroditic nematode C. elegans consists of a series of contractile cell types—including the gonadal sheath cells, the spermathecal cells and the spermatheca–uterine valve—that contract in a coordinated manner to regulate oocyte entry and exit of the fertilized embryo into the uterus. Contraction is driven by acto-myosin contraction and relies on the development and maintenance of specialized acto-myosin networks in each cell type. Study of this system has revealed insights into the regulation of acto-myosin network assembly and contractility in vivo. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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21 pages, 2352 KiB

Open AccessReview

The Signaling Network Controlling C. elegans Vulval Cell Fate Patterning

by Hanna Shin and David J. Reiner

J. Dev. Biol. 2018, 6(4), 30; https://doi.org/10.3390/jdb6040030 - 11 Dec 2018

Cited by 15 | Viewed by 6577

Abstract

EGF, emitted by the Anchor Cell, patterns six equipotent C. elegans vulval precursor cells to assume a precise array of three cell fates with high fidelity. A group of core and modulatory signaling cascades forms a signaling network that demonstrates plasticity during the [...] Read more.

EGF, emitted by the Anchor Cell, patterns six equipotent C. elegans vulval precursor cells to assume a precise array of three cell fates with high fidelity. A group of core and modulatory signaling cascades forms a signaling network that demonstrates plasticity during the transition from naïve to terminally differentiated cells. In this review, we summarize the history of classical developmental manipulations and molecular genetics experiments that led to our understanding of the signals governing this process, and discuss principles of signal transduction and developmental biology that have emerged from these studies. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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18 pages, 2069 KiB

Open AccessFeature PaperReview

G Proteins and GPCRs in C. elegans Development: A Story of Mutual Infidelity

by Daniel Matúš and Simone Prömel

J. Dev. Biol. 2018, 6(4), 28; https://doi.org/10.3390/jdb6040028 - 25 Nov 2018

Cited by 3 | Viewed by 6386

Abstract

Many vital processes during C. elegans development, especially the establishment and maintenance of cell polarity in embryogenesis, are controlled by complex signaling pathways. G protein-coupled receptors (GPCRs), such as the four Frizzled family Wnt receptors, are linchpins in regulating and orchestrating several of [...] Read more.

Many vital processes during C. elegans development, especially the establishment and maintenance of cell polarity in embryogenesis, are controlled by complex signaling pathways. G protein-coupled receptors (GPCRs), such as the four Frizzled family Wnt receptors, are linchpins in regulating and orchestrating several of these mechanisms. However, despite being GPCRs, which usually couple to G proteins, these receptors do not seem to activate classical heterotrimeric G protein-mediated signaling cascades. The view on signaling during embryogenesis is further complicated by the fact that heterotrimeric G proteins do play essential roles in cell polarity during embryogenesis, but their activity is modulated in a predominantly GPCR-independent manner via G protein regulators such as GEFs GAPs and GDIs. Further, the triggered downstream effectors are not typical. Only very few GPCR-dependent and G protein-mediated signaling pathways have been unambiguously defined in this context. This unusual and highly intriguing concept of separating GPCR function and G-protein activity, which is not restricted to embryogenesis in C. elegans but can also be found in other organisms, allows for essential and multi-faceted ways of regulating cellular communication and response. Although its relevance cannot be debated, its impact is still poorly discussed, and C. elegans is an ideal model to understand the underlying principles. Full article

(This article belongs to the Special Issue Caenorhabditis elegans - A Developmental Genetic Model System)

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