Inhibition of the autophagic protein ULK1 attenuates axonal degeneration in vitro and in vivo, enhances translation, and modulates splicing

Björn Friedhelm Vahsen, Vinicius Toledo Ribas, Jonas Sundermeyer, Alexander Boecker, Vivian Dambeck, Christof Lenz, Orr Shomroni, Lucas Caldi Gomes, Lars Tatenhorst, Elisabeth Barski, Anna Elisa Roser, Uwe Michel, Henning Urlaub, Gabriela Salinas, Mathias Bähr, Jan Christoph Koch, Paul Lingor

Research output: Contribution to journalArticlepeer-review

33 Scopus citations

Abstract

Axonal degeneration is a key and early pathological feature in traumatic and neurodegenerative disorders of the CNS. Following a focal lesion to axons, extended axonal disintegration by acute axonal degeneration (AAD) occurs within several hours. During AAD, the accumulation of autophagic proteins including Unc-51 like autophagy activating kinase 1 (ULK1) has been demonstrated, but its role is incompletely understood. Here, we study the effect of ULK1 inhibition in different models of lesion-induced axonal degeneration in vitro and in vivo. Overexpression of a dominant negative of ULK1 (ULK1.DN) in primary rat cortical neurons attenuates axotomy-induced AAD in vitro. Both ULK1.DN and the ULK1 inhibitor SBI-0206965 protect against AAD after rat optic nerve crush in vivo. ULK1.DN additionally attenuates long-term axonal degeneration after rat spinal cord injury in vivo. Mechanistically, ULK1.DN decreases autophagy and leads to an mTOR-mediated increase in translational proteins. Consistently, treatment with SBI-0206965 results in enhanced mTOR activation. ULK1.DN additionally modulates the differential splicing of the degeneration-associated genes Kif1b and Ddit3. These findings uncover ULK1 as an important mediator of axonal degeneration in vitro and in vivo, and elucidate its function in splicing, defining it as a putative therapeutic target.

Original languageEnglish
Pages (from-to)2810-2827
Number of pages18
JournalCell Death and Differentiation
Volume27
Issue number10
DOIs
StatePublished - 1 Oct 2020
Externally publishedYes

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