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Yamamoto, Hayashi; Fujioka, Yuko; Suzuki, Sho W.; Noshiro, Daisuke; Suzuki, Hironori; Kondo-Kakuta, Chika; Kimura, Yayoi; Hirano, Hisashi; Ando, Toshio; Noda, Nobuo N.; Ohsumi, Yoshinori
Developmental cell, 07/2016, Letnik: 38, Številka: 1Journal Article
Autophagosome formation in yeast entails starvation-induced assembly of the pre-autophagosomal structure (PAS), in which multiple Atg1 complexes (composed of Atg1, Atg13, and the Atg17-Atg29-Atg31 subcomplex) are initially engaged. However, the molecular mechanisms underlying the multimeric assembly of these complexes remain unclear. Using structural and biological techniques, we herein demonstrate that Atg13 has a large intrinsically disordered region (IDR) and interacts with two distinct Atg17 molecules using two binding regions in the IDR. We further reveal that these two binding regions are essential not only for Atg1 complex assembly in vitro, but also for PAS organization in vivo. These findings underscore the structural and functional significance of the IDR of Atg13 in autophagy initiation: Atg13 provides intercomplex linkages between Atg17-Atg29-Atg31 complexes, thereby leading to supramolecular self-assembly of Atg1 complexes, in turn accelerating the initial events of autophagy, including autophosphorylation of Atg1, recruitment of Atg9 vesicles, and phosphorylation of Atg9 by Atg1. Display omitted •An essential autophagy factor Atg13 has a large intrinsically disordered region (IDR)•The IDR of Atg13 contains two distinct regions binding intermolecularly to Atg17•Tethering two Atg17 molecules by Atg13 leads to supramolecular Atg1 complex assembly•The Atg13-mediated supramolecular assembly is responsible for autophagy initiation Yamamoto et al. uncover insights into early steps of yeast autophagosome assembly, where autophagy-related (Atg) proteins localize to a perivacuolar site to organize the pre-autophagosomal structure (PAS). Atg13, via an intrinsically disordered region, provides a flexible linkage between two Atg17 molecules to mediate multimeric Atg1 complex self-assembly for PAS organization.
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