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PreprintCited by 23Marine Invertebrate Physiology and EcologyMarine Sponges and Natural ProductsCellular Mechanics and Interactions

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Molecular profiling of sponge deflation reveals an ancient relaxant-inflammatory response

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Ruperti, Fabian, Becher, Isabelle, Stokkermans, Anniek, Wang, Ling, Marschlich, Nick, Potel, Clement, Maus, Emanuel, Stein, Frank, Drotleff, Bernhard, Schippers, Klaske, Nickel, Michael, Prevedel, Robert, Musser, Jacob M, Savitski, Mikhail M, Arendt, Detlev·2023·Current Biology
DOI 10.1101/2023.08.02.551666PMC PMC10418225

Preprint — published as 10.1016/j.cub.2023.12.021 · Paper page

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Abstract

A hallmark of animals is the coordination of whole-body movement. Neurons and muscles are central to this, yet coordinated movements also exist in sponges that lack these cell types. Sponges are sessile animals with a complex canal system for filter-feeding. They undergo whole-body movements resembling “contractions” that lead to canal closure and water expulsion. Here, we combine 3D optical coherence microscopy, pharmacology, and functional proteomics to elucidate anatomy, molecular physiology, and control of these movements. We find them driven by the relaxation of actomyosin stress fibers in epithelial canal cells, which leads to whole-body deflation via collapse of the incurrent and expansion of the excurrent system, controlled by an Akt/NO/PKG/A pathway. A concomitant increase in reactive oxygen species and secretion of proteinases and cytokines indicate an inflammation-like state reminiscent of vascular endothelial cells experiencing oscillatory shear stress. This suggests an ancient relaxant-inflammatory response of perturbed fluid-carrying systems in animals. Highlights: Sponge deflation is driven by tension release in actomyosin stress fibers of epithelial pinacocytes Akt kinase/Nitric oxide/Protein kinase G/A regulate actomyosin relaxation Agitation-induced deflation coincides with an inflammatory state The sponge relaxant-inflammatory response is evolutionary related to similar responses in the vertebrate vascular system

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Metadata

Authors
Ruperti, F., Becher, I., Stokkermans, A., Wang, L., Marschlich, N., Potel, C., Maus, E., Stein, F., Drotleff, B., Schippers, K., Nickel, M., Prevedel, R., Musser, J. M., Savitski, M. M., & Arendt, D.
Affiliations
  • Heidelberg University (DE)
  • European Molecular Biology Laboratory (DE)
  • Hubrecht Institute for Developmental Biology and Stem Cell Research (NL)
  • Yale University (US)
Corresponding author
  • Wang, Ling
  • Musser, Jacob M
  • Savitski, Mikhail M
  • Arendt, Detlev
ORCID
Venue
Current Biology
Publisher
openRxiv
Published
2023-08-02
Volume
34
Issue
2
Pages
361-375.e9
ISSN
0960-9822 (ISSN-L)
DOI
10.1101/2023.08.02.551666
PMC
PMC10418225
OpenAlex
W4390579554
Cited by
23
References
1
Citations by year
2026: 6 · 2025: 7 · 2024: 7 · 2023: 3
FWCI
6.29
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Current Biology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Lirias (submittedVersion)
  • PubMed Central (submittedVersion, cc-by-nc)
Funders
  • European Molecular Biology Laboratory
  • Paul G. Allen Frontiers Group
  • European Commission (664726, HORIZON2020, 788921, 764840, 101094250, 864027)
  • Horizon 2020 Framework Programme
  • HORIZON EUROPE Framework Programme (101094250/IMAGINE)
  • European Research Council
  • Horizon 2020
  • H2020 European Research Council (788921, 864027 / Brillouin4Life)
  • H2020 Marie Skłodowska-Curie Actions (764840, HORIZON-INFRA-2022-TECH-01, HORIZON2020, 664726)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
Keywords
mechanotransduction, epithelial cell junctions, reactive oxygen species, antioxidant depletion, proteinase secretion, cytokines, granulin, paracrine signaling, whole-body coordination, mechanosensitive signaling, thermal proteome profiling, phosphoproteomics, metabolomics, sponges

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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