Extracellular matrix remodeling through endocytosis and resurfacing of Tenascin-R

Tal M. Dankovich (), Rahul Kaushik, Linda H. M. Olsthoorn, Gabriel Cassinelli Petersen, Philipp Emanuel Giro, Verena Kluever, Paola Agüi-Gonzalez, Katharina Grewe, Guobin Bao, Sabine Beuermann, Hannah Abdul Hadi, Jose Doeren, Simon Klöppner, Benjamin H. Cooper, Alexander Dityatev and Silvio O. Rizzoli ()
Additional contact information
Tal M. Dankovich: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Rahul Kaushik: Molecular Neuroplasticity, German Center for Neurodegenerative Diseases (DZNE)
Linda H. M. Olsthoorn: International Max Planck Research School for Neuroscience
Gabriel Cassinelli Petersen: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Philipp Emanuel Giro: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Verena Kluever: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Paola Agüi-Gonzalez: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Katharina Grewe: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Guobin Bao: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Sabine Beuermann: Max Planck Institute for Experimental Medicine
Hannah Abdul Hadi: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Jose Doeren: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Simon Klöppner: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
Benjamin H. Cooper: Max Planck Institute for Experimental Medicine
Alexander Dityatev: Molecular Neuroplasticity, German Center for Neurodegenerative Diseases (DZNE)
Silvio O. Rizzoli: University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging

Nature Communications, 2021, vol. 12, issue 1, 1-23

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-27462-7

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