Extracellular matrix remodeling through endocytosis and resurfacing of Tenascin-R

2021 | journal article; research paper. A publication of Göttingen

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​Extracellular matrix remodeling through endocytosis and resurfacing of Tenascin-R​
Dankovich, T. M.; Kaushik, R.; Olsthoorn, L. H. M.; Petersen, G. C.; Giro, P. E.; Kluever, V. & Agüi-Gonzalez, P.  et al.​ (2021) 
Nature Communications12(1) art. 7129​.​ DOI: https://doi.org/10.1038/s41467-021-27462-7 

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Dankovich, Tal M.; Kaushik, Rahul; Olsthoorn, Linda H. M.; Petersen, Gabriel Cassinelli; Giro, Philipp Emanuel; Kluever, Verena; Agüi-Gonzalez, Paola ; Grewe, Katharina; Bao, Guobin ; Beuermann, Sabine; Rizzoli, Silvio O. 
Abstract The brain extracellular matrix (ECM) consists of extremely long-lived proteins that assemble around neurons and synapses, to stabilize them. The ECM is thought to change only rarely, in relation to neuronal plasticity, through ECM proteolysis and renewed protein synthesis. We report here an alternative ECM remodeling mechanism, based on the recycling of ECM molecules. Using multiple ECM labeling and imaging assays, from super-resolution optical imaging to nanoscale secondary ion mass spectrometry, both in culture and in brain slices, we find that a key ECM protein, Tenascin-R, is frequently endocytosed, and later resurfaces, preferentially near synapses. The TNR molecules complete this cycle within ~3 days, in an activity-dependent fashion. Interfering with the recycling process perturbs severely neuronal function, strongly reducing synaptic vesicle exo- and endocytosis. We conclude that the neuronal ECM can be remodeled frequently through mechanisms that involve endocytosis and recycling of ECM proteins.
Issue Date
Nature Communications 
EXC 2067: Multiscale Bioimaging 
SFB 1190: Transportmaschinen und Kontaktstellen zellulärer Kompartimente 
SFB 1190 | P09: Proteinsortierung in der Synapse: Prinzipien und molekulare Organisation 
SFB 1286: Quantitative Synaptologie 
SFB 1286 | A03: Dynamische Analyse der Remodellierung der extrazellulären Matrix (ECM) als Mechanismus der Synapsenorganisation und Plastizität 
Working Group
RG Rizzoli (Quantitative Synaptology in Space and Time) 



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