Multi-tissue patterning drives anterior morphogenesis of the C. elegans embryo

Grimbert, Stéphanie; Mastronardi, Karina; Richard, Victoria; Christensen, Ryan; Law, Chris; Zardoui, Khashayar; Fay, David S.; Piekny, Alisa

doi:10.1016/j.ydbio.2020.12.003

Cited by 3 publications

(6 citation statements)

References 64 publications

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“…Thus the author of this study concludes that the physical attachment of AM pores to epidermis and interconnection of AM cells is enabled by apical junctions. Additionally, the results show that anterior migration of the epidermal sheet is encasing the anterior region of the embryos head, which is confirmed by very recent findings (Grimbert, S. et al, 2020). The author of the study in hands thereby suggests, that anterior epidermis migration drives the translocation of AM pores, which are attached to the epidermal sheet and AM dendrite tips by CeAJ.…”

Section: Discussionsupporting

confidence: 83%

“…Importantly, the data of the study in hands show co-occurrence of dendrite elongation with epidermal head enclosure, which is reaffirmed by very recent findings from (Grimbert, S. et al, 2020).…”

Section: Apical Constriction Affects Pore Migration and Pharynx Devel...supporting

confidence: 85%

“…Remarkably, the findings exhibit the establishment of an arcade-pharynx funnel, which seems to gain its shape by apical constriction within the arcade cells (Figure3.11A).It is thereby assumed that the connection between mouth opening and pharynx is most likely established through apical constriction within the arcade cells. Very recent findings confirm the conclusion that embryonic head morphogenesis includes the anterior positioning of pharyngeal cells (through apical constriction) and epidermal cells (through head enclosure), adding a role for neuroblasts(Grimbert, S. et al, 2020). Moreover, this dissertation suggests that RPN.6.1 might play a role for successful interconnection of the mouth opening to the pharynx via arcade cells, since the results show lack of pharynx-mouth connection after RPN-6.1 depletion (Figure3.8).…”

supporting

confidence: 81%

“…Auch kürzlich veröffentlichte Studien ordnen Sensillen als Teil der Epidermis ein und vermuten Gemeinsamkeiten bei der Morphogenese (Low, I. I. et al, 2019). Darüber hinaus wird der in vorliegender Arbeit dokumentierte Vorgang der Kopfumschließung durch aktuelle Ergebnisse zur Entwicklung der anterioren Kopfregion bekräftigt (Grimbert, S. et al, 2020). Eindeutig ist die neuronale Elongation der AM-Sensillen dem morphogenetischen Mechanismus Schleppen von Dendriten ("dendrite towing") zuzuordnen, welcher auf der Definition durch (Gilmour, D. et al, 2004) A: Epidermale Bedeckung des Kopfbereiches führt zu "dendrite towing" und hierdurch die Morphogenese der Amphidsensillen (AM).…”

Section: Die Vorliegende Arbeit Bringt Die Erkenntnis Zutage Dass Die...unclassified

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Coupling between epidermis and amphid morphogenesis during embryonic development of C. elegans

Kunz¹

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Sensory organs are fundamental for survival of animal populations, since the detection of environmental stimuli is crucial for localization of nourishment, predators or mating partners. In nematodes, the amphid (AM) sensilla are the largest sensory organs for detection of chemical compounds. This study investigates how the AM sensilla acquire their special elongated shape during lima-bean to 1.5-fold embryonic stages of C. elegans head development. The dissertation also examines events facilitating the morphogenesis of other head sensilla (IL/OL/CEP) and addresses aspects of general embryonic head morphogenesis. Using high resolution live-cell imaging techniques with different combinations of markers highlighting specific tissues, this study shows that epidermal head enclosure, migration of AM socket cells (pores) and translocation of AM dendrite tips are coupled processes, facilitating the elongation of AM dendrites. Importantly, during AM dendrite elongation the AM neural cell bodies are staying stationary. Manipulation through conducting UV-Laser ablation (epidermis close to pore/pore) and RPN-6.1 dsRNA interference resulted in compromised AM pore migration and impaired dendrite elongation. This leads to the conclusion that AM pores need to be physically attached (through C. elegans apical junctions, CeAJ) to the migrating epidermal sheet and to AM dendrite tips for successful AM morphogenesis. This study infers that RPN-6.1 plays an important role for correct AM pore morphogenesis and AM pore to AM dendrite tip attachment. Our results lead to the conclusion that head enclosure drives AM pore migration and AM dendrite elongation with AM neural cell bodies staying stationary. Thereby, CeAJ are interconnecting AM dendrite tips to AM pores and CeAJ link the sensillar ending to the migrating epidermis. Thus, migration of attached target tissue (pore), with neural cell bodies staying stationary (constituting an abutment), creates a pulling force facilitating AM dendrite elongation. This passive neurite elongation procedure is coined dendrite towing in this study. Additionally, this study discovers that translocation of IL, OL and CEP head sensilla pores is influenced by apical constriction. This conclusion was made based on the findings that IL/OL/CEP pores migrate towards the prospective mouth anterior to the epidermal leading edge, separated from AM pores and irrespective of highly impaired AM sensilla morphogenesis after strong RPN-6.1 depletion. Also, concurrent with translocation of IL/OL/CEP pores, bottle-shaped cells occur and non-muscle-myosin and apical polarity factors are getting enriched at the anterior most part of the head, indicating de-novo manifestation of apical constriction. It is furthermore assumed that apical constriction in arcade cells might contribute to early pharynx development. All in all, this study reveals two force-generating events: Head enclosure-driven AM sensilla morphogenesis via dendrite towing and, otherwise, apical constriction-facilitated translocation of IL/OL/CEP sensilla pores. These events can get separated by graded depletion of the proteasome activator RPN-6.1.

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Section: Discussionsupporting

confidence: 83%

Section: Apical Constriction Affects Pore Migration and Pharynx Devel...supporting

confidence: 85%

supporting

confidence: 81%

Section: Die Vorliegende Arbeit Bringt Die Erkenntnis Zutage Dass Die...unclassified

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Coupling between epidermis and amphid morphogenesis during embryonic development of C. elegans

Kunz¹

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“…The nematode Caenorhabditis elegans is a useful model in which to study various aspects of development including the morphogenesis of embryos and organs. Whereas certain aspects of C. elegans embryonic morphogenesis-such as gastrulation (Goldstein and Nance, 2020), embryonic elongation (Vuong-Brender et al, 2016), and dorsoventral enclosure (Chisholm and Hardin, 2005;Chisholm and Hsiao, 2012)-have been reasonably well described, the development and morphogenesis of the anterior embryo, in particular the epidermis and its integration with the oral cavity, have just begun to be characterized in detail (Grimbert et al, 2021;Portereiko and Mango, 2001).…”

Section: Introductionmentioning

confidence: 99%

Pathways that affect anterior morphogenesis inC. elegansembryos

Balasubramaniam

Topalidou

Kelley

et al. 2023

Preprint

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During embryogenesis the nascent Caenorhabditis elegans epidermis secretes an apical extracellular matrix (aECM) that serves as an external stabilizer, preventing deformation of the epidermis by mechanical forces exerted during morphogenesis. We showed that two conserved proteins linked to this process, SYM-3/FAM102A and SYM-4/WDR44, colocalize to intracellular and membrane-associated puncta and likely function together in a complex. Proteomics data also suggested potential roles for FAM102A and WDR44 family proteins in intracellular trafficking, consistent with their localization patterns. Nonetheless, we found no evidence to support a clear function for SYM-3 or SYM-4 in the apical deposition of two aECM components, FBN-1 and NOAH. Surprisingly, loss of MEC-8/RBPMS2, a conserved splicing factor and regulator of fbn-1, had little effect on the abundance or deposition of FBN-1 to the aECM. Using a focused screening approach, we identified 32 additional proteins that likely contribute to the structure and function of the embryonic aECM. Lastly, we examined morphogenesis defects in embryos lacking mir-51 microRNA family members, which display a related embryonic phenotype to mec-8; sym double mutants. Collectively, our findings add to our knowledge of pathways controlling embryonic morphogenesis.

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Effectors of anterior morphogenesis in C. elegans embryos

et al. 2023

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During embryogenesis the nascent Caenorhabditis elegans epidermis secretes an apical extracellular matrix (aECM) that serves as an external stabilizer, preventing deformation of the epidermis by mechanical forces exerted during morphogenesis. At present, the factors that contribute to aECM function are mostly unknown, including the aECM components themselves, their posttranslational regulators, and the pathways required for their secretion. Here we showed that two proteins previously linked to aECM function, SYM-3/FAM102A and SYM-4/WDR44, colocalize to intracellular and membrane-associated puncta and likely function in a complex. Proteomics experiments also suggested potential roles for SYM-3/FAM102A and SYM-4/WDR44 family proteins in intracellular trafficking. Nonetheless, we found no evidence to support a clear function for SYM-3 or SYM-4 in the apical deposition of two aECM components, NOAH-1 and FBN-1. Moreover, loss of a key splicing regulator of fbn-1, MEC-8/RBPMS2, had surprisingly little effect on the abundance or deposition of FBN-1. Using a focused screening approach, we identified 32 additional proteins that likely contribute to the structure and function of the embryonic aECM. We also characterized morphogenesis defects in embryos lacking mir-51 microRNA family members, which display a similar phenotype to mec-8; sym double mutants. Collectively, these findings add to our knowledge of factors controlling embryonic morphogenesis.

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Multi-tissue patterning drives anterior morphogenesis of the C. elegans embryo

Cited by 3 publications

References 64 publications

Coupling between epidermis and amphid morphogenesis during embryonic development of C. elegans

Coupling between epidermis and amphid morphogenesis during embryonic development of C. elegans

Pathways that affect anterior morphogenesis inC. elegansembryos

Effectors of anterior morphogenesis in C. elegans embryos

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