A multi-layered and dynamic apical extracellular matrix shapes the vulva lumen in<i>Caenorhabditis elegans</i>

Cohen, Jozef; Sparacio, Alessandro P.; Belfi, Alexandra C.; Forman-Rubinsky, Rachel; Hall, David H.; Maul-Newby, Hannah M.; Frand, Alison R.; Sundaram, Meera V.

doi:10.1101/2020.04.14.041483

Cited by 9 publications

(10 citation statements)

References 91 publications

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“…10B). We previously noted and reported an accumulation of unusually large vesicles in vulF vulva cells of this same specimen (Cohen et al, 2020). In contrast, similar vesicles were not observed in seam syncytia of ten wild-type specimens, including four other late L4s (Fig.…”

Section: Resultssupporting

confidence: 55%

“…To examine the timing and patterns of provisional matrix deposition, we visualized the lipocalin LPR-3 and the ZP-domain proteins LET-653, FBN-1, and NOAH-1 using functional translational fusions expressed from the endogenous loci or from extrachromosomal transgenes (Cohen et al, 2020; Vuong-Brender et al, 2017) (Methods) (Fig. 7A).…”

Section: Resultsmentioning

confidence: 99%

“…For synchronization, gravid worms were allowed to lay eggs during limited time windows or were bleached to isolate eggs and hatchlings arrested in starvation-induced L1 diapause and were released from diapause by plating on NGM seeded with E. coli OP50-1. The precise stages of L4 worms were further determined based on the shape of the vulva (Cohen et al, 2020; Mok et al, 2015).…”

Section: Methodsmentioning

confidence: 99%

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A transient apical extracellular matrix relays cytoskeletal patterns to shape permanent acellular ridges on the surface of adult C. elegans

Katz

Barker

Maul-Newby

et al. 2021

Preprint

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Apical extracellular matrices can form protruding structures such as denticles, ridges, scales, or teeth on the surfaces of epithelia. The mechanisms that shape these structures remain poorly understood. Here, we show how the actin cytoskeleton and a provisional matrix work together to sculpt acellular longitudinal alae ridges in the cuticle of adult C. elegans. Transient actomyosin-dependent constriction of the underlying lateral epidermis accompanies deposition of the provisional matrix at the earliest stages of alae formation. Actin is required to pattern the provisional matrix into longitudinal bands that are initially offset from the pattern of longitudinal actin filaments. These bands appear ultrastructurally as alternating regions of adhesion and separation within laminated provisional matrix layers. The provisional matrix is required to establish these demarcated zones of adhesion and separation, which ultimately give rise to alae ridges and their intervening valleys, respectively. Provisional matrix proteins shape the alae ridges and valleys but are not present within the final structure. We propose a morphogenetic mechanism wherein cortical actin patterns are relayed mechanically to the laminated provisional matrix to set up distinct zones of matrix layer separation and accretion that shape a permanent and acellular matrix structure.

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Section: Resultssupporting

confidence: 55%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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A transient apical extracellular matrix relays cytoskeletal patterns to shape permanent acellular ridges on the surface of adult C. elegans

Katz

Barker

Maul-Newby

et al. 2021

Preprint

Self Cite

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“…Because the identified EV proteome contained 13% of the entire C. elegans proteome, we reasoned that the captured EV cargo candidates likely originated from multiple cellular sources and not solely from the ciliated EV-releasing neurons (EVNs). Nematodes produce EVs from the plasma membrane of embryonic cells [24], epithelial cells and cuticle [25], reproductive tract [26,27], nervous system [11, 28,29], and intestine [30]. In these reports, compelling evidence for tissue-specific EV biogenesis was obtained using electron microscopy, whereas EV cargo composition remains unknown.…”

Section: Integration With Cell-specific Transcriptomic Datasetsmentioning

confidence: 99%

Tracking extracellular vesicle (EV) cargo as a platform for studying EVomics, signaling, and targeting in vivo

Nikonorova

Wang

Cope

et al. 2021

Preprint

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Extracellular vesicle (EV)-based signaling is a challenge to study, due to EV small size, heterogeneity, and limited information on cargo content in vivo. We present Caenorhabditis elegans as a discovery platform that allows single EV tracking from source to target tissue in living animals. We enriched ciliary EVs using GFP-tagged PKD-2 cargo followed by mass spectrometry analysis to identify 2,888 cargo candidates. By integrating our dataset with single-cell transcriptomic data, we identified EV cargo produced by individual neurons and other cell and tissue types. A single cilium produces multiple EVs with distinct protein content. Ciliary EVs carry nucleic acid binding proteins. We observed transfer of EV cargo from the male reproductive tract to the hermaphrodite uterus during mating, a direct demonstration of animal-to-animal EV targeting.

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“…Traditionally, the time of molting is equated with lethargus, a period of relative behavioral quiescence, when animals stop feeding. For simplicity we will follow this tradition here, but note that additional events required for successful molting precede lethargus (Cohen et al, 2020; Cohen and Sundaram, 2020); (Tsiairis and Großhans, 2021).…”

Section: Introductionmentioning

confidence: 99%

The Grainyhead/LSF transcription factor GRH-1 is rhythmically required for molting

Meeuse

Nahar

Braun

et al. 2022

Preprint

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Molting, that is, the synthesis and shedding of a cuticular exoskeleton, is a defining characteristic of ecdysozoa. In nematodes such as C. elegans, molts rhythmically terminate each of four larval stages. The molting cycle is tightly coupled to the rhythmic expression of thousands of genes. The mechanisms that support the regular molting cycle and oscillatory gene expression have remained largely elusive. Here, we performed an RNAi-based screen for transcription factors required for molting to identify potential components of a molting clock. We find that depletion of GRH-1, BLMP-1, NHR-23, NHR-25, MYRF-1 or BED-3 impairs progression through the molting cycle. We characterize GRH-1, a Grainyhead/LSF transcription factor whose functions in C. elegans development have remained largely unexplored, but whose orthologues in other animals are known to be key epithelial cell fate regulators. We show that GRH-1 depletion causes a dose-dependent extension of molt duration, with severe depletion causing defects in cuticle formation and shedding, and larval death. GRH-1 is required repetitively, during a specific time window prior to each larval molt. This rhythmic activity is consistent with the rhythmic accumulation of GRH-1 protein. These features are consistent with GRH-1 functioning as a key component, or high-level output, of the a gene regulatory network that controls molting. As its mammalian orthologues, as well as those of BLMP-1 and NHR-23, have been implicated in rhythmic homeostatic skin regeneration in mouse, the mechanisms underlying rhythmic C. elegans molting may be conserved beyond nematodes.

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A multi-layered and dynamic apical extracellular matrix shapes the vulva lumen inCaenorhabditis elegans

Cited by 9 publications

References 91 publications

A transient apical extracellular matrix relays cytoskeletal patterns to shape permanent acellular ridges on the surface of adult C. elegans

A transient apical extracellular matrix relays cytoskeletal patterns to shape permanent acellular ridges on the surface of adult C. elegans

Tracking extracellular vesicle (EV) cargo as a platform for studying EVomics, signaling, and targeting in vivo

The Grainyhead/LSF transcription factor GRH-1 is rhythmically required for molting

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