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      Autophagy in the context of the cellular membrane-trafficking system: the enigma of Atg9 vesicles

      review-article
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      Publication date (Electronic):
      Journal: Biochemical Society Transactions
      Publisher: Portland Press Ltd.
      Keywords: autophagy, endoplasmic reticulum, trafficking

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          Abstract

          Macroautophagy is an intracellular degradation system that involves the de novo formation of membrane structures called autophagosomes, although the detailed process by which membrane lipids are supplied during autophagosome formation is yet to be elucidated. Macroautophagy is thought to be associated with canonical membrane trafficking, but several mechanistic details are still missing. In this review, the current understanding and potential mechanisms by which membrane trafficking participates in macroautophagy are described, with a focus on the enigma of the membrane protein Atg9, for which the proximal mechanisms determining its movement are disputable, despite its key role in autophagosome formation.

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          Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum

          Elizabeth L. Axe, Simon A. Walker, Maria Manifava … (2008)
          Autophagy is the engulfment of cytosol and organelles by double-membrane vesicles termed autophagosomes. Autophagosome formation is known to require phosphatidylinositol 3-phosphate (PI(3)P) and occurs near the endoplasmic reticulum (ER), but the exact mechanisms are unknown. We show that double FYVE domain–containing protein 1, a PI(3)P-binding protein with unusual localization on ER and Golgi membranes, translocates in response to amino acid starvation to a punctate compartment partially colocalized with autophagosomal proteins. Translocation is dependent on Vps34 and beclin function. Other PI(3)P-binding probes targeted to the ER show the same starvation-induced translocation that is dependent on PI(3)P formation and recognition. Live imaging experiments show that this punctate compartment forms near Vps34-containing vesicles, is in dynamic equilibrium with the ER, and provides a membrane platform for accumulation of autophagosomal proteins, expansion of autophagosomal membranes, and emergence of fully formed autophagosomes. This PI(3)P-enriched compartment may be involved in autophagosome biogenesis. Its dynamic relationship with the ER is consistent with the idea that the ER may provide important components for autophagosome formation.
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            A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation.

            Mitsuko Hayashi-Nishino, Naonobu Fujita, Takeshi Noda … (2009)
            Autophagy is a bulk degradation process in eukaryotic cells and has fundamental roles in cellular homeostasis.The origin and source of autophagosomal membranes are long-standing questions in the field. Using electron microscopy, we show that, in mammalian culture cells, the endoplasmic reticulum (ER) associates with early autophagic structures called isolation membranes (IMs). Overexpression of an Atg4B mutant, which causes defects in autophagosome formation, induces the accumulation of ER-IM complexes. Electron tomography revealed that the ER-IM complex appears as a subdomain of the ER that formed a cradle encircling the IM, and showed that both ER and isolation membranes are interconnected.
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              3D tomography reveals connections between the phagophore and endoplasmic reticulum.

              Päivi Ylä-Anttila, Helena Vihinen, Eija Jokitalo … (2009)
              Autophagosomes have been reported to form in the vicinity of the endoplasmic reticulum (ER). In many cases, the phagophore membrane is observed between two cisternae of rough ER, but it is not known whether these two membranes are directly connected. To investigate the relationship of the phagophore membrane and the ER, we used electron microscopic tomography of serum and amino acid starved normal rat kidney cells. The cells were fixed in glutaraldehyde and reduced osmium tetroxide and embedded in Epon. Dual axis tilt image series were acquired from two successive 250-nm sections. To analyze the three-dimensional (3D) morphology of phagophores and the associated rough ER, 3D tomograms were used to model the ER and phagophore membranes. The tomographic reconstructions revealed connections between the phagophore/autophagosome membrane and the closely located ER cisternae, especially with the ER located inside the autophagosome. The connections were typically formed by narrow extensions from the phagophore/autophagosome to the ER. This finding has potential implications on the origin of autophagosome membranes, and on the mechanism of phagophore membrane extension. In addition, we observed lipid droplets in very close contact with the phagophores/autophagosomes.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Biochem Soc Trans
                Journal ID (iso-abbrev): Biochem. Soc. Trans
                Journal ID (hwp): ppbiost
                Journal ID (publisher-id): BST
                Title: Biochemical Society Transactions
                Publisher: Portland Press Ltd.
                ISSN (Print): 0300-5127
                ISSN (Electronic): 1470-8752
                Publication date (Print): 15 December 2017
                Publication date (Electronic): 17 November 2017
                Volume: 45
                Issue: 6
                Pages: 1323-1331
                Affiliations
                Center for Frontier Oral Science, Graduate School of Dentistry, Osaka University, Osaka 565-0871, Japan
                Author notes
                Correspondence: Takeshi Noda ( takenoda@ 123456dent.osaka-u.ac.jp )
                Article
                Publisher ID: BST-45-1323
                DOI: 10.1042/BST20170128
                PMC ID: 5730941
                PubMed ID: 29150528
                SO-VID: ec4f9841-9a76-4db6-82f7-b38f31924b1f
                Copyright © © 2017 The Author(s)
                License:

                This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution License 4.0 (CC BY-NC-ND).

                History
                Date received : 22 July 2017
                Date revision received : 11 October 2017
                Date accepted : 16 October 2017
                Categories
                Subject: Review Articles
                Subject: Review Article
                Subject: 27
                Subject: 24
                Subject: 23

                ScienceOpen disciplines: Biochemistry
                Keywords: autophagy,endoplasmic reticulum,trafficking
                Data availability:
                ScienceOpen disciplines: Biochemistry
                Keywords: autophagy, endoplasmic reticulum, trafficking

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