eprintid: 10032511 rev_number: 32 eprint_status: archive userid: 608 dir: disk0/10/03/25/11 datestamp: 2017-11-09 14:51:13 lastmod: 2021-09-25 23:06:06 status_changed: 2017-11-09 14:51:13 type: article metadata_visibility: show creators_name: Rott, R creators_name: Szargel, R creators_name: Shani, V creators_name: Hamza, H creators_name: Savyon, M creators_name: Abd Elghani, F creators_name: Bandopadhyay, R creators_name: Engelender, S title: SUMOylation and ubiquitination reciprocally regulate α-synuclein degradation and pathological aggregation ispublished: pub divisions: UCL divisions: B02 divisions: C07 divisions: D07 divisions: F84 keywords: Parkinson’s disease, α-synuclein, SUMOylatio, nubiquitination, aggregation note: This version is the author accepted manuscript. For information on re-use, please refer to the publisher’s terms and conditions. abstract: α-Synuclein accumulation is a pathological hallmark of Parkinson’s disease (PD). Ubiquitinated α-synuclein is targeted to proteasomal or lysosomal degradation. Here, we identify SUMOylation as a major mechanism that counteracts ubiquitination by different E3 ubiquitin ligases and regulates α-synuclein degradation. We report that PIAS2 promotes SUMOylation of α-synuclein, leading to a decrease in α-synuclein ubiquitination by SIAH and Nedd4 ubiquitin ligases, and causing its accumulation and aggregation into inclusions. This was associated with an increase in α-synuclein release from the cells. A SUMO E1 inhibitor, ginkgolic acid, decreases α-synuclein levels by relieving the inhibition exerted on α-synuclein proteasomal degradation. α-Synuclein disease mutants are more SUMOylated compared with the wild-type protein, and this is associated with increased aggregation and inclusion formation. We detected a marked increase in PIAS2 expression along with SUMOylated α-synuclein in PD brains, providing a causal mechanism underlying the up-regulation of α-synuclein SUMOylation in the disease. We also found a significant proportion of Lewy bodies in nigral neurons containing SUMO1 and PIAS2. Our observations suggest that SUMOylation of α-synuclein by PIAS2 promotes α-synuclein aggregation by two mutually reinforcing mechanisms. First, it has a direct proaggregatory effect on α-synuclein. Second, SUMOylation facilitates α-synuclein aggregation by blocking its ubiquitin-dependent degradation pathways and promoting its accumulation. Therefore, inhibitors of α-synuclein SUMOylation provide a strategy to reduce α-synuclein levels and possibly aggregation in PD. date: 2017-12-12 date_type: published publisher: National Academy of Sciences official_url: https://doi.org/10.1073/pnas.1704351114 oa_status: green full_text_type: other language: eng primo: open primo_central: open_green verified: verified_manual elements_id: 1506570 doi: 10.1073/pnas.1704351114 lyricists_name: Bandopadhyay, Rina lyricists_id: RBAND40 actors_name: Dewerpe, Marie actors_id: MDDEW97 actors_role: owner full_text_status: public publication: Proceedings of the National Academy of Sciences of the United States of America volume: 114 number: 50 pagerange: 13176-13181 issn: 0027-8424 citation: Rott, R; Szargel, R; Shani, V; Hamza, H; Savyon, M; Abd Elghani, F; Bandopadhyay, R; Rott, R; Szargel, R; Shani, V; Hamza, H; Savyon, M; Abd Elghani, F; Bandopadhyay, R; Engelender, S; - view fewer <#> (2017) SUMOylation and ubiquitination reciprocally regulate α-synuclein degradation and pathological aggregation. Proceedings of the National Academy of Sciences of the United States of America , 114 (50) pp. 13176-13181. 10.1073/pnas.1704351114 <https://doi.org/10.1073/pnas.1704351114>. Green open access document_url: https://discovery.ucl.ac.uk/id/eprint/10032511/1/Bandopadhyay_Rott%20PNAS%20oct%2030%2017.pdf