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      Development of Research into Autophagic Lysosome Reformation

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          Abstract

          Autophagy is a lysosome-dependent degradation process that is essential for maintaining cellular homeostasis. In recent years, more studies have focused on the late stages of autophagy. Our group discovered and studied the terminal step of autophagy, namely autophagic lysosome reformation (ALR). ALR is the process that regenerates functional lysosomes from autolysosomes, thus maintaining lysosome homeostasis. ALR involves clathrin-mediated membrane budding from autolysosomes, elongation of membrane tubules along microtubules with the pulling force provided by the motor protein KIF5B, proto-lysosome scission by dynamin 2, and finally maturation of proto-lysosomes to functional lysosomes. In this review, we will summarize progress in unveiling the molecular mechanisms underlying ALR and its potential pathophysiological roles.

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          Spinster is required for autophagic lysosome reformation and mTOR reactivation following starvation.

          Christina McPhee, E H Baehrecke, Lei Huang … (2011)
          Autophagy is a conserved cellular process to degrade and recycle cytoplasmic components. During autophagy, lysosomes fuse with an autophagosome to form an autolysosome. Sequestered components are degraded by lysosomal hydrolases and presumably released into the cytosol by lysosomal efflux permeases. Following starvation-induced autophagy, lysosome homeostasis is restored by autophagic lysosome reformation (ALR) requiring activation of the "target of rapamycin" (TOR) kinase. Spinster (Spin) encodes a putative lysosomal efflux permease with the hallmarks of a sugar transporter. Drosophila spin mutants accumulate lysosomal carbohydrates and enlarged lysosomes. Here we show that defects in spin lead to the accumulation of enlarged autolysosomes. We find that spin is essential for mTOR reactivation and lysosome reformation following prolonged starvation. Further, we demonstrate that the sugar transporter activity of Spin is essential for ALR.
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            Clathrin.

            Tomas Kirchhausen (1999)
            Clathrin was discovered nearly 25 years ago. Since then, a large number of other proteins that participate in the process by which clathrin-coated vesicles retrieve synaptic membranes or take up endocytic receptors have been identified. The functional relationships among these disparate components remain, in many cases, obscure. High-resolution structures of parts of clathrin, determined by X-ray crystallography, and lower-resolution images of assembled coats, determined by electron cryomicroscopy, now provide the information necessary to integrate various lines of evidence and to design experiments that test specific mechanistic notions. This review summarizes and illustrates the recent structural results and outlines what is known about coated-vesicle assembly in the context of this information.
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              Spastic paraplegia proteins spastizin and spatacsin mediate autophagic lysosome reformation.

              Jaerak Chang, Seongju Lee, Craig Blackstone (2014)
              Autophagy allows cells to adapt to changes in their environment by coordinating the degradation and recycling of cellular components and organelles to maintain homeostasis. Lysosomes are organelles critical for terminating autophagy via their fusion with mature autophagosomes to generate autolysosomes that degrade autophagic materials; therefore, maintenance of the lysosomal population is essential for autophagy-dependent cellular clearance. Here, we have demonstrated that the two most common autosomal recessive hereditary spastic paraplegia gene products, the SPG15 protein spastizin and the SPG11 protein spatacsin, are pivotal for autophagic lysosome reformation (ALR), a pathway that generates new lysosomes. Lysosomal targeting of spastizin required an intact FYVE domain, which binds phosphatidylinositol 3-phosphate. Loss of spastizin or spatacsin resulted in depletion of free lysosomes, which are competent to fuse with autophagosomes, and an accumulation of autolysosomes, reflecting a failure in ALR. Moreover, spastizin and spatacsin were essential components for the initiation of lysosomal tubulation. Together, these results link dysfunction of the autophagy/lysosomal biogenesis machinery to neurodegeneration.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Mol Cells
                Journal ID (iso-abbrev): Mol. Cells
                Journal ID (publisher-id): ksmcb
                Title: Molecules and Cells
                Publisher: Korean Society for Molecular and Cellular Biology
                ISSN (Print): 1016-8478
                ISSN (Electronic): 0219-1032
                Publication date (Print): 31 January 2018
                Publication date (Electronic): 23 January 2018
                Volume: 41
                Issue: 1
                Pages: 45-49
                Affiliations
                State Key Laboratory of Membrane Biology, Tsinghua University-Peking University Joint Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing 100084, China
                Author notes
                Article
                Publisher ID: molce-41-1-45
                DOI: 10.14348/molcells.2018.2265
                PMC ID: 5792712
                PubMed ID: 29370688
                SO-VID: a56d40b0-bb52-42c6-8c0f-57799b265dbf
                Copyright © © The Korean Society for Molecular and Cellular Biology. All rights reserved.
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/.

                History
                Date received : 23 October 2017
                Date accepted : 30 November 2017
                Categories
                Subject: Minireview

                Keywords: autophagic lysosome reformation (alr),autophagy,in vitro reconstitution,membrane deformation,phospholipid
                Data availability:
                Keywords: autophagic lysosome reformation (alr), autophagy, in vitro reconstitution, membrane deformation, phospholipid

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