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Research Paper

WIPI2 positively regulates mitophagy by promoting mitochondrial recruitment of VCP

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References

  • Mizushima N. A brief history of autophagy from cell biology to physiology and disease. Nat Cell Biol. 2018 May;20(5):521–527.
  • Dikic I, Elazar Z. Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol. 2018 Jun;19(6):349–364.
  • Lu G, Wang L, Zhou J, et al. A destiny for degradation: interplay between cullin-RING E3 ligases and autophagy. Trends Cell Biol. 2021 Jun;31(6):432–444. DOI:10.1016/j.tcb.2021.01.005.
  • Killackey SA, Philpott DJ, Girardin SE. Mitophagy pathways in health and disease. J Cell Biol. 2020 Nov 2;219(11): DOI: 10.1083/jcb.202004029.
  • Aman Y, Schmauck-Medina T, Hansen M, et al. Autophagy in healthy aging and disease. Nature Aging. 2021 Aug 01;1(8):634–650. DOI: 10.1038/s43587-021-00098-4.
  • Fang EF, Hou Y, Palikaras K, et al. Mitophagy inhibits amyloid-beta and tau pathology and reverses cognitive deficits in models of Alzheimer’s disease. Nat Neurosci. 2019 Mar;22(3):401–412. DOI:10.1038/s41593-018-0332-9.
  • Pickles S, Vigie P, Youle RJ. Mitophagy and quality control mechanisms in mitochondrial maintenance. Curr Biol. 2018 Feb 19;28(4):R170–R185.
  • Wang L, Qi H, Tang Y, et al. Post-translational modifications of key machinery in the control of mitophagy. Trends Biochem Sci. 2020 Jan;45(1):58–75. DOI:10.1016/j.tibs.2019.08.002.
  • Kane LA, Lazarou M, Fogel AI, et al. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol. 2014 Apr 28;205(2):143–153.
  • Koyano F, Okatsu K, Kosako H, et al. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature. 2014 Jun 5;510(7503):162–166.
  • Kazlauskaite A, Kondapalli C, Gourlay R, et al. Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem J. 2014 May 15;460(1):127–139.
  • Shiba-Fukushima K, Imai Y, Yoshida S, et al. PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci Rep. 2012;2:1002.
  • Kondapalli C, Kazlauskaite A, Zhang N, et al. PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol. 2012 May;2(5):120080. DOI:10.1098/rsob.120080.
  • Ordureau A, Sarraf SA, Duda DM, et al. Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis. Mol Cell. 2014 Nov 6 56(3):360–375. DOI: 10.1016/j.molcel.2014.09.007.
  • Polson HE, de Lartigue J, Rigden DJ, et al. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy. 2010 May;6(4):506–522. DOI:10.4161/auto.6.4.11863.
  • Dooley HC, Razi M, Polson HE, et al. WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell. 2014 Jul 17;55(2):238–252.
  • Lu G, Yi J, Gubas A, et al. Suppression of autophagy during mitosis via CUL4-RING ubiquitin ligases-mediated WIPI2 polyubiquitination and proteasomal degradation. Autophagy. 2019 Nov;15(11):1917–1934. DOI:10.1080/15548627.2019.1596484.
  • Wan W, You Z, Zhou L, et al. mTORC1-regulated and HUWE1-mediated WIPI2 degradation controls autophagy Flux. Mol Cell. 2018 Oct 18;72(2):303–315 e6.
  • Stavoe AK, Gopal PP, Gubas A, et al. Expression of WIPI2B counteracts age-related decline in autophagosome biogenesis in neurons. Elife. 2019 Jul16;8:e44219.
  • Thurston TL, Boyle KB, Allen M, et al. Recruitment of TBK1 to cytosol-invading salmonella induces WIPI2-dependent antibacterial autophagy. EMBO J. 2016 Aug 15;35(16):1779–1792.
  • Martinez-Martin N, Maldonado P, Gasparrini F, et al. A switch from canonical to noncanonical autophagy shapes B cell responses. Science. 2017 Feb 10 355(6325):641–647. DOI: 10.1126/science.aal3908.
  • Heo JM, Harper NJ, Paulo JA, et al. Integrated proteogenetic analysis reveals the landscape of a mitochondrial-autophagosome synapse during PARK2-dependent mitophagy. Sci Adv. 2019 Nov;5(11):eaay4624. DOI:10.1126/sciadv.aay4624.
  • Heo JM, Ordureau A, Paulo JA, et al. The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote mitophagy. Mol Cell. 2015 Oct 1;60(1):7–20.
  • Wong YC, Holzbaur EL. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc Natl Acad Sci U S A. 2014 Oct 21;111(42):E4439–48.
  • Lazarou M, Sliter DA, Kane LA, et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 2015 Aug 20;524(7565):309–314.
  • Ahmed MR, Zhan X, Song X, et al. Ubiquitin ligase parkin promotes Mdm2-arrestin interaction but inhibits arrestin ubiquitination. Biochemistry. 2011 May 10;50(18):3749–3763.
  • Sun N, Yun J, Liu J, et al. Measuring In Vivo mitophagy. Mol Cell. 2015 Nov 19;60(4):685–696.
  • Fang EF, Palikaras K, Sun N, et al. In vitro and in vivo detection of mitophagy in human cells, C. elegans, and mice. J Vis Exp. 2017 Nov 22;(129):e56301.
  • Tanaka A, Cleland MM, Xu S, et al. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol. 2010 Dec 27;191(7):1367–1380.
  • Bento AC, Bippes CC, Kohler C, et al. UBXD1 is a mitochondrial recruitment factor for p97/VCP and promotes mitophagy. Sci Rep. 2018 Aug 17;8(1):12415.
  • McLelland GL, Goiran T, Yi W, et al. Mfn2 ubiquitination by PINK1/parkin gates the p97-dependent release of ER from mitochondria to drive mitophagy. Elife. 2018 Apr 20;7: DOI:10.7554/eLife.32866.
  • Mengus C, Neutzner M, Bento A, et al. VCP/p97 cofactor UBXN1/SAKS1 regulates mitophagy by modulating MFN2 removal from mitochondria. Autophagy. 2021;9:1–20.
  • Guo X, Sun X, Hu D, et al. VCP recruitment to mitochondria causes mitophagy impairment and neurodegeneration in models of Huntington’s disease. Nat Commun. 2016 Aug 26;7(1):12646.
  • Niwa H, Ewens CA, Tsang C, et al. The role of the N-domain in the ATPase activity of the mammalian AAA ATPase p97/VCP. J Biol Chem. 2012 Mar 9;287(11):8561–8570.
  • Sato Y, Tsuchiya H, Yamagata A, et al. Structural insights into ubiquitin recognition and Ufd1 interaction of Npl4. Nat Commun. 2019 Dec 13;10(1):5708.
  • van den Boom J, Meyer H. VCP/p97-mediated unfolding as a principle in protein homeostasis and signaling. Mol Cell. 2018 Jan 18;69(2):182–194.
  • Kimura Y, Fukushi J, Hori S, et al. Different dynamic movements of wild-type and pathogenic VCPs and their cofactors to damaged mitochondria in a Parkin-mediated mitochondrial quality control system. Genes Cells. 2013 Dec;18(12):1131–1143. DOI:10.1111/gtc.12103.
  • Magnaghi P, D’Alessio R, Valsasina B, et al. Covalent and allosteric inhibitors of the ATPase VCP/p97 induce cancer cell death. Nat Chem Biol. 2013 Sep;9(9):548–556. DOI:10.1038/nchembio.1313.
  • Kim NC, Tresse E, Kolaitis RM, et al. VCP is essential for mitochondrial quality control by PINK1/Parkin and this function is impaired by VCP mutations. Neuron. 2013 Apr 10;78(1):65–80.
  • Wang ZH, Clark C, Geisbrecht ER. Drosophila clueless is involved in Parkin-dependent mitophagy by promoting VCP-mediated Marf degradation. Hum Mol Genet. 2016 May 15;25(10):1946–1964.
  • Yoshii SR, Kishi C, Ishihara N, et al. Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J Biol Chem. 2011 Jun 3;286(22):19630–19640.
  • Pasquier B. SAR405, a PIK3C3/Vps34 inhibitor that prevents autophagy and synergizes with MTOR inhibition in tumor cells. Autophagy. 2015 Apr 3;11(4):725–726.
  • Wei Y, Chiang WC, Sumpter R Jr., et al. Prohibitin 2 is an inner mitochondrial membrane mitophagy receptor. Cell. 2017 Jan 12;168(1–2):224–238 e10.
  • Liang JR, Martinez A, Lane JD, et al. USP30 deubiquitylates mitochondrial Parkin substrates and restricts apoptotic cell death. EMBO Rep. 2015 May;16(5):618–627. DOI:10.15252/embr.201439820.
  • Heiskanen KM, Bhat MB, Wang HW, et al. Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells. J Biol Chem. 1999 Feb 26;274(9):5654–5658.
  • Gottlieb E, Armour SM, Harris MH, et al. Mitochondrial membrane potential regulates matrix configuration and cytochrome c release during apoptosis. Cell Death Differ. 2003 Jun;10(6):709–717. DOI:10.1038/sj.cdd.4401231.
  • Wang C. A sensitive and quantitative mKeima assay for mitophagy via FACS. Curr Protoc Cell Biol. 2020 Mar;86(1):e99.
  • Ordureau A, Paulo JA, Zhang J, et al. Global landscape and dynamics of parkin and USP30-dependent ubiquitylomes in iNeurons during mitophagic signaling. Mol Cell. 2020 Mar 5;77(5):1124–1142 e10.
  • Ju JS, Fuentealba RA, Miller SE, et al. Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J Cell Biol. 2009 Dec 14;187(6):875–888.
  • Tresse E, Salomons FA, Vesa J, et al. VCP/p97 is essential for maturation of ubiquitin-containing autophagosomes and this function is impaired by mutations that cause IBMPFD. Autophagy. 2010 Feb;6(2):217–227. DOI:10.4161/auto.6.2.11014.
  • Hill SM, Wrobel L, Ashkenazi A, et al. VCP/p97 regulates Beclin-1-dependent autophagy initiation. Nat Chem Biol. 2021 Apr;17(4):448–455. DOI:10.1038/s41589-020-00726-x.
  • Bock FJ, Tait SWG. Mitochondria as multifaceted regulators of cell death. Nat Rev Mol Cell Biol. 2020 Feb;21(2):85–100.
  • Matsuda N, Sato S, Shiba K, et al. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol. 2010 Apr 19;189(2):211–221.
  • Carroll RG, Hollville E, Martin SJ. Parkin sensitizes toward apoptosis induced by mitochondrial depolarization through promoting degradation of Mcl-1. Cell Rep. 2014 Nov 20;9(4):1538–1553.
  • Akabane S, Matsuzaki K, Yamashita S, et al. Constitutive activation of PINK1 protein leads to proteasome-mediated and non-apoptotic cell death independently of mitochondrial autophagy. J Biol Chem. 2016 Jul 29;291(31):16162–16174.
  • Lautrup S, Sinclair DA, Mattson MP, et al. NAD(+) in brain aging and neurodegenerative disorders. Cell Metab. 2019 Oct 1;30(4):630–655.
  • Kobro-Flatmoen A, Lagartos-Donate MJ, Aman Y, et al. Re-emphasizing early Alzheimer’s disease pathology starting in select entorhinal neurons, with a special focus on mitophagy. Ageing Res Rev. 2021 May;67:101307.
  • Hulsmann J, Kravic B, Weith M, et al. AP-SWATH reveals direct involvement of VCP/p97 in integrated stress response signaling through facilitating CReP/PPP1R15B degradation. Mol Cell Proteomics. 2018 Jul;17(7):1295–1307. DOI:10.1074/mcp.RA117.000471.
  • Ritz D, Vuk M, Kirchner P, et al. Endolysosomal sorting of ubiquitylated caveolin-1 is regulated by VCP and UBXD1 and impaired by VCP disease mutations. Nat Cell Biol. 2011 Aug 7;13(9):1116–1123.
  • Ran FA, Hsu PD, Wright J, et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013 Nov;8(11):2281–2308. DOI:10.1038/nprot.2013.143.
  • Aarreberg LD, Esser-Nobis K, Driscoll C, et al. Interleukin-1beta induces mtDNA release to activate innate immune signaling via cGAS-STING. Mol Cell. 2019 May 16;74(4):801–815 e6.
  • Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006 Dec;224(Pt 3):213–232.
  • Stauffer W, Sheng H, Lim HN. EzColocalization: an ImageJ plugin for visualizing and measuring colocalization in cells and organisms. Sci Rep. 2018 Oct 25; 8(1):15764. DOI: 10.1038/s41598-018-33592-8.