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

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 +7 more·2024·Current Biology

Published version of a preprint

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 live 3D optical coherence microscopy, pharmacology, and functional proteomics to elucidate the sequence and detail of shape changes, the tissues and molecular physiology involved, and the control of these movements. Morphometric analysis and targeted perturbation suggest that the movement is 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 canal system. Thermal proteome profiling and quantitative phosphoproteomics confirm the control of cellular relaxation by an Akt/NO/PKG/PKA pathway. Agitation-induced deflation leads to differential phosphorylation of proteins forming epithelial cell junctions, implying their mechanosensitive role. Unexpectedly, untargeted metabolomics detect a concomitant decrease in antioxidant molecules during deflation, reflecting an increase in reactive oxygen species. Together with the secretion of proteinases, cytokines, and granulin, this indicates an inflammation-like state of the deflating sponge reminiscent of vascular endothelial cells experiencing oscillatory shear stress. These results suggest the conservation of an ancient relaxant-inflammatory response of perturbed fluid-carrying systems in animals and offer a possible mechanism for whole-body coordination through diffusible paracrine signals and mechanotransduction.

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Authors
Ruperti, F., Becher, I., Stokkermans, A., Wang, L., Marschlich, N., Potel, C., Maus, E., Stein, F., Drotleff, B., Schippers, K. J., 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
Venue
Current Biology
Publisher
Elsevier BV
Published
2024-01
Volume
34
Issue
2
Pages
361-375.e9
ISSN
0960-9822 (ISSN-L)
OpenAlex
W4390579554
Cited by
23
References
206
Citations by year
2026: 6 · 2025: 7 · 2024: 7 · 2023: 3
FWCI
6.29
Type
journal article
Language
en
Open access
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
  • ERC (864027 / Brillouin4Life, 788921)
  • The Paul G Allen Frontiers Group
  • Horizon Europe (101094250 /IMAGINE)
  • Horizon 2020
  • H2020 Marie Skłodowska-Curie Actions (664726, HORIZON-INFRA-2022-TECH-01, 764840)
  • Horizon 2020 Framework Programme
  • European Molecular Biology Laboratory
  • European Research Council
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › 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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