Feedback regulation of BMP signaling by<i>Caenorhabditis elegans</i>cuticle collagens

Madaan, Uday; Faure, Lionel; Chowdhury, Albar; Ahmed, Shahrear; Ciccarelli, Emma J.; Gumienny, Tina L.; Savage-Dunn, Cathy

doi:10.1091/mbc.e19-07-0390

Cited by 16 publications

(8 citation statements)

References 40 publications

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“…Direct or indirect targets of TGFβ -regulated Smad transcription factors include the collagen genes rol-6 , col-41 , col-141 , and col-142 , whose loss and/or overexpression also impacts body size [ 141 ]. Interestingly, mutations in some collagens also reduce expression levels of the TGFβ ligand DBL-1, suggesting a positive feedback loop whereby cuticle structure maintains proper TGFβ signaling [ 142 ]. Relationships between TGFβ signaling and extracellular matrix organization also have been found in mammalian systems [ 143 ], and C. elegans could be a good system for understanding some of these connections.…”

Section: Collagen-based Cuticles and The Molt Cyclementioning

confidence: 99%

C. elegans Apical Extracellular Matrices Shape Epithelia

Cohen

Sundaram

2020

JDB

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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.

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Section: Collagen-based Cuticles and The Molt Cyclementioning

confidence: 99%

C. elegans Apical Extracellular Matrices Shape Epithelia

Cohen

Sundaram

2020

JDB

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“…The integrity or function of the cuticle may also be sensed by other tissues, implying complex systemic regulation of cuticle composition and function. For example, altered collagen levels can affect the level of the neuronally expressed BMP signal DBL-1 34 , which acts via SMADs in the epidermis to regulate cuticle collagen expression 35 . These observations suggest the operation of a feedback pathway that senses cuticle function; the precise mechanism of such feedback is not yet clear but could involve mechanosensing by neurons.…”

Section: The Aecm As a Signaling Center: Interactions Between The mentioning

confidence: 99%

Form and function of the apical extracellular matrix: new insights from Caenorhabditis elegans, Drosophila melanogaster, and the vertebrate inner ear

Zheng¹,

Adams²,

Chisholm³

2020

Fac Rev

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Apical extracellular matrices (aECMs) are the extracellular layers on the apical sides of epithelia. aECMs form the outer layer of the skin in most animals and line the luminal surface of internal tubular epithelia. Compared to the more conserved basal ECMs (basement membranes), aECMs are highly diverse between tissues and between organisms and have been more challenging to understand at mechanistic levels. Studies in several genetic model organisms are revealing new insights into aECM composition, biogenesis, and function and have begun to illuminate common principles and themes of aECM organization. There is emerging evidence that, in addition to mechanical or structural roles, aECMs can participate in reciprocal signaling with associated epithelia and other cell types. Studies are also revealing mechanisms underlying the intricate nanopatterns exhibited by many aECMs. In this review, we highlight recent findings from well-studied model systems, including the external cuticle and ductal aECMs of Caenorhabditis elegans, Drosophila melanogaster , and other insects and the internal aECMs of the vertebrate inner ear.

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“…Moreover, collagen genes have been shown to be regulated by TGF-β signaling (Madaan et al . 2018, 2020), and this pathway may regulate body morphology in part through controlling the expression of such exoskeletal factors. Thus, it is possible that these divergent transcriptional dynamics in collagen genes may promote the evolution of elongated body size in C. inopinata .…”

Section: Discussionmentioning

confidence: 99%

Widespread changes in gene expression accompany body size evolution in nematodes

Woodruff,

Willis,

Johnson

et al. 2023

Preprint

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Body size is a fundamental trait that drives multiple evolutionary and ecological patterns.Caenorhabditis inopinatais a fig-associated nematode that is exceptionally large relative to other members of the genus, includingC. elegans. We previously showed thatC. inopinatais large primarily due to postembryonic cell size expansion that occurs during the larval-to-adult transition. Here, we describe gene expression patterns inC. elegansandC. inopinatathroughout this developmental period to understand the transcriptional basis of body size change. We performed RNA-seq in both species across the L3, L4, and adult stages. Most genes are differentially expressed across all developmental stages, consistent withC. inopinata’s divergent ecology and morphology. We also used a model comparison approach to identify orthologs with divergent dynamics across this developmental period between the two species. This included genes connected to neurons, behavior, stress response, developmental timing, and small RNA/chromatin regulation. Multiple hypodermal collagens were also observed to harbor divergent developmental dynamics across this period, and genes important for molting and body morphology were also detected. Genes associated with TGF-β signaling revealed idiosyncratic and unexpected transcriptional patterns given their role in body size regulation inC. elegans. Widespread transcriptional divergence between these species is unexpected and may be a signature of the ecological and morphological divergence ofC. inopinata. Alternatively, transcriptional turnover may be the rule in theCaenorhabditisgenus, indicative of widespread developmental system drift among species. This work lays the foundation for future functional genetic studies interrogating the bases of body size evolution in this group.

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Feedback regulation of BMP signaling byCaenorhabditis eleganscuticle collagens

Cited by 16 publications

References 40 publications

C. elegans Apical Extracellular Matrices Shape Epithelia

C. elegans Apical Extracellular Matrices Shape Epithelia

Form and function of the apical extracellular matrix: new insights from Caenorhabditis elegans, Drosophila melanogaster, and the vertebrate inner ear

Widespread changes in gene expression accompany body size evolution in nematodes

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