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Extracellular matrix remodeling through endocytosis and resurfacing of Tenascin-R

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Listed:
  • Tal M. Dankovich

    (University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
    International Max Planck Research School for Neuroscience)

  • Rahul Kaushik

    (Molecular Neuroplasticity, German Center for Neurodegenerative Diseases (DZNE)
    Center for Behavioral Brain Sciences (CBBS))

  • Linda H. M. Olsthoorn

    (International Max Planck Research School for Neuroscience
    Max Planck Institute for Biophysical Chemistry)

  • 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
    University Medical Center Göttingen, Institute of Pharmacology and Toxicology)

  • 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)
    Center for Behavioral Brain Sciences (CBBS)
    Medical Faculty, Otto von Guericke University)

  • Silvio O. Rizzoli

    (University Medical Center Göttingen, Institute for Neuro- and Sensory Physiology, Excellence Cluster Multiscale Bioimaging
    Biostructural Imaging of Neurodegeneration (BIN) Center)

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.

Suggested Citation

  • 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 &, 2021. "Extracellular matrix remodeling through endocytosis and resurfacing of Tenascin-R," Nature Communications, Nature, vol. 12(1), pages 1-23, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27462-7
    DOI: 10.1038/s41467-021-27462-7
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    1. Eugenio F. Fornasiero & Sunit Mandad & Hanna Wildhagen & Mihai Alevra & Burkhard Rammner & Sarva Keihani & Felipe Opazo & Inga Urban & Till Ischebeck & M. Sadman Sakib & Maryam K. Fard & Koray Kirli &, 2018. "Precisely measured protein lifetimes in the mouse brain reveal differences across tissues and subcellular fractions," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    2. Sinem K. Saka & Alf Honigmann & Christian Eggeling & Stefan W. Hell & Thorsten Lang & Silvio O. Rizzoli, 2014. "Multi-protein assemblies underlie the mesoscale organization of the plasma membrane," Nature Communications, Nature, vol. 5(1), pages 1-14, December.
    3. Sinem K. Saka & Angela Vogts & Katharina Kröhnert & François Hillion & Silvio O Rizzoli & Johannes T. Wessels, 2014. "Correlated optical and isotopic nanoscopy," Nature Communications, Nature, vol. 5(1), pages 1-8, May.
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    1. Christian Hoffmann & Jakob Rentsch & Taka A. Tsunoyama & Akshita Chhabra & Gerard Aguilar Perez & Rajdeep Chowdhury & Franziska Trnka & Aleksandr A. Korobeinikov & Ali H. Shaib & Marcelo Ganzella & Gr, 2023. "Synapsin condensation controls synaptic vesicle sequestering and dynamics," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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