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

Autor:	Ruperti F; Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany; Collaboration for joint Ph.D. degree between EMBL and Heidelberg University, Faculty of Biosciences 69117 Heidelberg, Germany., Becher I; Genome Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany., Stokkermans A; Hubrecht Institute, 3584 CT Utrecht, the Netherlands., Wang L; Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany. Electronic address: ling.wang@embl.de., Marschlich N; Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany; Centre for Organismal Studies (COS), University of Heidelberg, 69120 Heidelberg, Germany., Potel C; Genome Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany., Maus E; Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany., Stein F; Proteomics Core Facility, European Molecular Biology Laboratory, 69117 Heidelberg, Germany., Drotleff B; Metabolomics Core Facility, European Molecular Biology Laboratory, 69117 Heidelberg, Germany., Schippers KJ; Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany., Nickel M; Bionic consulting Dr. Michael Nickel, 71686 Remseck am Neckar, Germany., Prevedel R; Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany; Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany., Musser JM; Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06520, USA. Electronic address: jacob.musser@yale.edu., Savitski MM; Genome Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany; Proteomics Core Facility, European Molecular Biology Laboratory, 69117 Heidelberg, Germany. Electronic address: mikhail.savitski@embl.de., Arendt D; Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany; Centre for Organismal Studies (COS), University of Heidelberg, 69120 Heidelberg, Germany. Electronic address: detlev.arendt@embl.de.
Jazyk:	angličtina
Zdroj:	Current biology : CB [Curr Biol] 2024 Jan 22; Vol. 34 (2), pp. 361-375.e9. Date of Electronic Publication: 2024 Jan 04.
DOI:	10.1016/j.cub.2023.12.021
Abstrakt:	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. Competing Interests: Declaration of interests M.N. is the founder of bionic consulting Dr. Michael Nickel. (Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.)
Databáze:	MEDLINE
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