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Release of astroglial vimentin by extracellular vesicles: Modulation of binding and internalization of C3 transferase in astrocytes and neurons

Artikel i vetenskaplig tidskrift
Författare A. Adolf
A. Rohrbeck
A. Munster-Wandowski
Malin Johansson
Hans-Georg Kuhn
M. A. Kopp
B. Brommer
J. M. Schwab
I. Just
G. Ahnert-Hilger
M. Holtje
Publicerad i Glia
Volym 67
Nummer/häfte 4
Sidor 703-717
ISSN 0894-1491
Publiceringsår 2019
Publicerad vid Institutionen för neurovetenskap och fysiologi, sektionen för klinisk neurovetenskap
Sidor 703-717
Språk en
Länkar dx.doi.org/10.1002/glia.23566
Ämnesord astrocytes, axonotrophic, C3 transferase, exosomes, vimentin, spinal-cord-injury, central-nervous-system, membrane-vesicles, cell-surface, exosomes, growth, integrin, rho, recruitment, exoenzyme, Neurosciences & Neurology
Ämneskategorier Neurovetenskaper

Sammanfattning

Clostridium botulinum C3 transferase (C3bot) ADP-ribosylates rho proteins to change cellular functions in a variety of cell types including astrocytes and neurons. The intermediate filament protein vimentin as well as transmembrane integrins are involved in internalization of C3bot into cells. The exact contribution, however, of these proteins to binding of C3bot to the cell surface and subsequent cellular uptake remains to be unraveled. By comparing primary astrocyte cultures derived from wild-type with Vim(-/-) mice, we demonstrate that astrocytes lacking vimentin exhibited a delayed ADP-ribosylation of rhoA concurrent with a blunted morphological response. This functional impairment was rescued by the extracellular excess of recombinant vimentin. Binding assays using C3bot harboring a mutated integrin-binding RGD motif (C3bot-G89I) revealed the involvement of integrins in astrocyte binding of C3bot. Axonotrophic effects of C3bot are vimentin dependent and postulate an underlying mechanism entertaining a molecular cross-talk between astrocytes and neurons. We present functional evidence for astrocytic release of vimentin by exosomes using an in vitro scratch wound model. Exosomal vimentin+ particles released from wild-type astrocytes promote the interaction of C3bot with neuronal membranes. This effect vanished when culturing Vim(-/-) astrocytes. Specificity of these findings was confirmed by recombinant vimentin propagating enhanced binding of C3bot to synaptosomes from rat spinal cord and mouse brain. We hypothesize that vimentin+ exosomes released by reactive astrocytes provide a novel molecular mechanism constituting axonotrophic (neuroprotective) and plasticity augmenting effects of C3bot after spinal cord injury.

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