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Research Paper

A conserved requirement for RME-8/DNAJC13 in neuronal autophagic lysosome reformation

ORCID Icon, , ORCID Icon, , ORCID Icon & ORCID Icon
Pages 792-808 | Received 09 Mar 2023, Accepted 02 Oct 2023, Published online: 09 Nov 2023

References

  • Yu L, McPhee CK, Zheng L, et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature. 2010;465(7300):942–946. doi: 10.1038/nature09076
  • Rong Y, Liu M, Ma L, et al. Clathrin and phosphatidylinositol-4,5-bisphosphate regulate autophagic lysosome reformation. Nat Cell Biol. 2012;14(9):924–934. doi: 10.1038/ncb2557
  • Schulze RJ, Weller SG, Schroeder B, et al. Lipid droplet breakdown requires dynamin 2 for vesiculation of autolysosomal tubules in hepatocytes. J Cell Bio. 2013;203(2):315–326. doi: 10.1083/jcb.201306140
  • Du W, Su Q, Chen Y, et al. Kinesin 1 drives autolysosome tubulation. Dev Cell. 2016;37(4):326–336. doi: 10.1016/j.devcel.2016.04.014
  • Eramo MJ, Gurung R, Mitchell CA, et al. Bidirectional interconversion between PtdIns4P and PtdIns(4,5)P2 is required for autophagic lysosome reformation and protection from skeletal muscle disease. Autophagy. 2021;17(5):1287–1289. doi: 10.1080/15548627.2021.1916195
  • Munson MJ, Allen GF, Toth R, et al. mTOR activates the VPS 34– UVRAG complex to regulate autolysosomal tubulation and cell survival. EMBO J. 2015;34(17):2272–2290. doi: 10.15252/embj.201590992
  • Boland B, Kumar A, Lee S, et al. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in alzheimer’s disease. J Neurosci. 2008;28(27):6926. doi: 10.1523/JNEUROSCI.0800-08.2008
  • Maday S, Holzbaur EL. Compartment-specific regulation of autophagy in primary neurons. J Neurosci. 2016;36(22):5933–5945. doi: 10.1523/JNEUROSCI.4401-15.2016
  • Takalo M, Salminen A, Soininen H, et al. Protein aggregation and degradation mechanisms in neurodegenerative diseases. Am J Neurodegener Dis. 2013;2(1):1–14.
  • Tan C-C, Yu J-T, Tan M-S, et al. Autophagy in aging and neurodegenerative diseases: implications for pathogenesis and therapy. Neurobiol Aging. 2014;35(5):941–957. doi: 10.1016/j.neurobiolaging.2013.11.019
  • Chang J, Lee S, Blackstone C. Spastic paraplegia proteins spastizin and spatacsin mediate autophagic lysosome reformation. J Clin Investig. 2014;124(12):5249–5262. doi: 10.1172/JCI77598
  • Francis V, Alshafie W, Kumar R, et al. The ARSACS disease protein sacsin controls lysosomal positioning and reformation by regulating microtubule dynamics. J Biol Chem. 2022;298(9):298(9. doi: 10.1016/j.jbc.2022.102320
  • Vilarino-Guell C, Rajput A, Milnerwood AJ, et al. DNAJC13 mutations in Parkinson disease. Hum Mol Genet. 2014;23(7):1794–1801. doi: 10.1093/hmg/ddt570
  • Appel-Cresswell S, Rajput AH, Sossi V, et al. Clinical, positron emission tomography, and pathological studies of DNAJC13 p.N855S parkinsonism. Mov Disord. 2014;29(13):1684–1687. doi: 10.1002/mds.26019
  • Norris A, McManus CT, Wang S, et al. Mutagenesis and structural modeling implicate RME-8 IWN domains as conformational control points. PLoS Genet. 2022;18(10):e1010296. doi: 10.1371/journal.pgen.1010296
  • Spillantini MG, Schmidt ML, Lee VM-Y, et al. α-synuclein in Lewy bodies. Nature. 1997;388(6645):839–840. doi: 10.1038/42166
  • Rajput A, Ross JP, Bernales CQ, et al. VPS35 and DNAJC13 disease-causing variants in essential tremor. Eur J Hum Genet. 2015;23(6):887–888. doi: 10.1038/ejhg.2014.164
  • Grant B, Hirsh D, Kimble J. Receptor-mediated endocytosis in the caenorhabditis elegans oocyte. Mol Biol Cell. 1999;10(12):4311–4326. doi: 10.1091/mbc.10.12.4311
  • Zhang Y, Grant B, Hirsh D, et al. RME-8, a conserved J-Domain protein, is required for endocytosis in caenorhabditis elegans. Mol Biol Cell. 2001;12(7):2011–2021. doi: 10.1091/mbc.12.7.2011
  • Greener T, Grant B, Zhang Y, et al. Caenorhabditis elegans auxilin: a J-domain protein essential for clathrin-mediated endocytosis in vivo. Nat Cell Biol. 2001;3(2):215–219. doi: 10.1038/35055137
  • Xhabija B, Taylor GS, Fujibayashi A, et al. Receptor mediated endocytosis 8 is a novel PI(3)P binding protein regulated by myotubularin-related 2. FEBS Lett. 2011;585(12):1722–1728. doi: 10.1016/j.febslet.2011.04.016
  • Norris A, Grant BD. Endosomal microdomains: formation and function. Curr Opinion Cell Biol. 2020;65:86–95. doi: 10.1016/j.ceb.2020.02.018
  • Shi A, Sun L, Banerjee R, et al. Regulation of endosomal clathrin and retromer-mediated endosome to Golgi retrograde transport by the J-domain protein RME-8. EMBO J. 2009;28(21):3290–3302. doi: 10.1038/emboj.2009.272
  • Norris A, Tammineni P, Wang S, et al. SNX-1 and RME-8 oppose the assembly of HGRS-1/ESCRT-0 degradative microdomains on endosomes. Proc Natl Acad Sci U S A. 2017;114(3):E307–E316. doi: 10.1073/pnas.1612730114
  • Raiborg C, Wesche J, Malerød L, Stenmark H. Flat clathrin coats on endosomes mediate degradative protein sorting by scaffolding Hrs in dynamic microdomains. Journal of Cell Science. 2006;119(12):2414–2424. doi: 10.1242/jcs.02978
  • Hurley JH. The ESCRT complexes. Crit Rev Biochem Mol Biol. 2010;45(6):463–487. doi: 10.3109/10409238.2010.502516
  • Hurley JH, Hanson PI. Membrane budding and scission by the ESCRT machinery: it’s all in the neck. Nat Rev Mol Cell Biol. 2010;11(8):556–566. doi: 10.1038/nrm2937
  • Wollert T, Hurley JH. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature. 2010;464(7290):864–869. doi: 10.1038/nature08849
  • Popoff V, Mardones GA, Bai SK, et al. Analysis of articulation between Clathrin and retromer in retrograde Sorting on early endosomes. Traffic. 2009;10(12):1868–1880. doi: 10.1111/j.1600-0854.2009.00993.x
  • Gagliardi M, Annesi G, Procopio R, et al. DNAJC13 mutation screening in patients with Parkinson’s disease from South Italy. parkinsonism relat Disord. 2018;55:134–137. doi: 10.1016/j.parkreldis.2018.06.004
  • Gustavsson EK, Trinh J, Guella I, et al. DNAJC13 genetic variants in parkinsonism. Mov Disord. Mov Disord. 2015;30(2):273–278. doi: 10.1002/mds.26064
  • Lorenzo-Betancor O, Ogaki K, Soto‐Ortolaza AI, et al. DNAJC13 p.Asn855Ser mutation screening in Parkinson’s disease and pathologically confirmed Lewy body disease patients. Eur J Neurol. 2015;22(9):1323–1325. doi: 10.1111/ene.12770
  • Yoshida S, Hasegawa T, Suzuki M, et al. Parkinson’s disease-linked DNAJC13 mutation aggravates alpha-synuclein-induced neurotoxicity through perturbation of endosomal trafficking. Hum Mol Genet. 2018;27(5):823–836. doi: 10.1093/hmg/ddy003
  • Schafer WR. Mechanosensory molecules and circuits in C. elegans. Pflugers Arch - Eur J Physiol. 2015;467(1):39–48. doi: 10.1007/s00424-014-1574-3
  • Hamelin M, Scott IM, Way JC, et al. The mec-7 beta-tubulin gene of caenorhabditis elegans is expressed primarily in the touch receptor neurons. EMBO J. 1992;11(8):2885–2893. doi: 10.1002/j.1460-2075.1992.tb05357.x
  • Lőrincz P, Juhász G. Autophagosome-lysosome fusion. J Mol Biol. 2020;432(8):2462–2482. doi: 10.1016/j.jmb.2019.10.028
  • Nguyen JA, Yates RM. Better together: Current insights into phagosome-lysosome fusion. Front Immunol. 2021;12:12. doi: 10.3389/fimmu.2021.636078
  • Malik BR, Maddison DC, Smith GA, et al. Autophagic and endo-lysosomal dysfunction in neurodegenerative disease. Mol Brain. 2019;12(1):100. doi: 10.1186/s13041-019-0504-x
  • McGrath MJ, Eramo MJ, Gurung R, et al. Defective lysosome reformation during autophagy causes skeletal muscle disease. J Clin Invest. 2021;131(1). doi: 10.1172/JCI135124
  • Serra-Vinardell J, Sandler MB, De Pace R, et al. LYST deficiency impairs autophagic lysosome reformation in neurons and alters lysosome number and size. Cell Mol Life Sci. 2023;80(2):53. doi: 10.1007/s00018-023-04695-x
  • Cao Y, Klionsky DJ. Physiological functions of Atg6/Beclin 1: a unique autophagy-related protein. Cell Res. 2007;17(10):839–849. doi: 10.1038/cr.2007.78
  • Kihara A, Noda T, Ishihara N, et al. Two distinct Vps34 phosphatidylinositol 3–kinase complexes function in autophagy and carboxypeptidase Y Sorting inSaccharomyces cerevisiae. J Cell Bio. 2001;152(3):519–530. doi: 10.1083/jcb.152.3.519
  • Ruck A, Attonito J, Garces KT, et al. The Atg6/Vps30/Beclin 1 ortholog BEC-1 mediates endocytic retrograde transport in addition to autophagy in C. elegans. Autophagy. 2011;7(4):386–400. doi: 10.4161/auto.7.4.14391
  • Clark SG, Shurland D-L, Meyerowitz EM, et al. A dynamin GTPase mutation causes a rapid and reversible temperature-inducible locomotion defect in C. elegans. Proc Natl Acad Sci, USA. 1997;94(19):10438–10443. doi: 10.1073/pnas.94.19.10438
  • Xhabija B, Vacratsis PO. Receptor-mediated endocytosis 8 utilizes an N-terminal phosphoinositide-binding motif to regulate endosomal clathrin dynamics. J Biol Chem. 2015;290(35):21676–21689. doi: 10.1074/jbc.M115.644757
  • Hu Y, Reggiori F. Molecular regulation of autophagosome formation. Biochem Soc Trans. 2022;50(1):55–69. doi: 10.1042/BST20210819
  • Nishimura T, Tamura N, Kono N, et al. Autophagosome formation is initiated at phosphatidylinositol synthase-enriched ER subdomains. EMBO J. 2017;36(12):1719–1735. doi: 10.15252/embj.201695189
  • Tian E, Wang F, Han J, et al. Epg-1 functions in autophagy-regulated processes and may encode a highly divergent Atg13 homolog in C. elegans. Autophagy. 2009;5(5):608–615. doi: 10.4161/auto.5.5.8624
  • Lu Q, Yang P, Huang X, et al. The WD40 repeat PtdIns(3)P-Binding protein EPG-6 regulates progression of omegasomes to autophagosomes. Dev Cell. 2011;21(2):343–357. doi: 10.1016/j.devcel.2011.06.024
  • Yang P, Zhang H. The coiled-coil domain protein EPG-8 plays an essential role in the autophagy pathway in C. elegans. Autophagy. 2011;7(2):159–165. doi: 10.4161/auto.7.2.14223
  • Kuma A, Matsui M, Mizushima N. LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy: caution in the interpretation of LC3 localization. Autophagy. 2007;3(4):323–328. doi: 10.4161/auto.4012
  • Zhang H, Chang JT, Guo B, et al. Guidelines for monitoring autophagy in caenorhabditis elegans. Autophagy. 2015;11(1):9–27. doi: 10.1080/15548627.2014.1003478
  • Krüger U, Wang Y, Kumar S, et al. Autophagic degradation of tau in primary neurons and its enhancement by trehalose. Neurobiol Aging. 2012;33(10):2291–2305. doi: 10.1016/j.neurobiolaging.2011.11.009
  • Feng T, Tammineni P, Agrawal C, et al. Autophagy-mediated regulation of BACE1 protein trafficking and degradation. J Biol Chem. 2017;292(5):1679–1690. doi: 10.1074/jbc.M116.766584
  • Umezawa H, Aoyagi T, Morishima H, et al. Pepstatin, a new pepsin inhibitor produced by Actinomycetes. J Antibiot (Tokyo). 1970;23(5):259–262. doi: 10.7164/antibiotics.23.259
  • Kleina LG, Grubman MJ. Antiviral effects of a thiol protease inhibitor on foot-and-mouth disease virus. J Virol. 1992;66(12):7168–7175. doi: 10.1128/jvi.66.12.7168-7175.1992
  • Stavoe AKH, Holzbaur ELF. Autophagy in neurons. Annu Rev Cell Dev Biol. 2019;35:477–500. doi: 10.1146/annurev-cellbio-100818-125242
  • Ferguson SM. Neuronal lysosomes. Neurosci Lett. 2019;697:1–9. doi: 10.1016/j.neulet.2018.04.005
  • Hirst J, Hesketh GG, Gingras A-C, et al. Rag GTPases and phosphatidylinositol 3-phosphate mediate recruitment of the AP-5/SPG11/SPG15 complex. J Cell Bio. 2021;220(2). doi: 10.1083/jcb.202002075
  • Eisenberg E, Greene L E. Multiple Roles of Auxilin and Hsc70 in Clathrin‐Mediated Endocytosis. Traffic. 2007;8(6):640–646. doi: 10.1111/j.1600-0854.2007.00568.x
  • Ken Sato AN, Sato M, Barth D. Grant. C. elegans as a model for membrane traffic. WormBook: the online review of C. elegans Biology [internet]. 2018.
  • Kirchhausen T, Harrison SC. Protein organization in clathrin trimers. Cell. 1981;23(3):755–761. doi: 10.1016/0092-8674(81)90439-6
  • Chen Y, Yu L. Scissors for autolysosome tubules. EMBO J. 2015;34(17):2217–2218. doi: 10.15252/embj.201592519
  • Lenk GM, Meisler MH. Chapter fourteen - mouse models of PI(3,5)P2 deficiency with impaired lysosome function. In: Conn PM, editor. Methods in enzymology. Elsevier: Academic Press; 2014. pp. 245–260. https://www.sciencedirect.com/science/article/pii/B9780123979261000147?casa_token=3fe8fQfZrlcAAAAA:VoWEihZSOe7ynPROpzk2AgI5b5ZkhpLQr4kNXzmRi_zxuMYFM5N5NkJbPRD-kioagemZx2Td
  • Rivero-Ríos P, Weisman LS. Roles of PIKfyve in multiple cellular pathways. Curr Opinion Cell Biol. 2022;76:102086. doi: 10.1016/j.ceb.2022.102086
  • Klein DE, Lee A, Frank DW, et al. The pleckstrin homology domains of dynamin isoforms require oligomerization for high affinity phosphoinositide binding. J Biol Chem. 1998;273(42):27725–27733. doi: 10.1074/jbc.273.42.27725
  • Yarar D, Surka MC, Leonard MC, et al. SNX9 activities are regulated by multiple phosphoinositides through both PX and BAR domains. Traffic. 2008;9(1):133–146. doi: 10.1111/j.1600-0854.2007.00675.x
  • Lu N, Shen Q, Mahoney TR, et al. Three sorting nexins drive the degradation of apoptotic cells in response to PtdIns(3)P signaling. Mol Biol Cell. 2011;22(3):354–374. doi: 10.1091/mbc.e10-09-0756
  • Lu N, Shen Q, Mahoney TR, et al. Two PI 3-kinases and one PI 3-phosphatase together establish the cyclic waves of phagosomal PtdIns(3)P critical for the degradation of apoptotic cells. PLoS Biol. 2012;10(1):e1001245. doi: 10.1371/journal.pbio.1001245
  • Cheng S, Wang K, Zou W, et al. PtdIns(4,5)P₂ and PtdIns3P coordinate to regulate phagosomal sealing for apoptotic cell clearance. J Cell Bio. 2015;210(3):485–502. doi: 10.1083/jcb.201501038
  • Zhou C, Wu Z, Du W, et al. Recycling of autophagosomal components from autolysosomes by the recycler complex. Nat Cell Biol. 2022;24(4):497–512. doi: 10.1038/s41556-022-00861-8
  • Besemer AS, Maus J, Ax MDA, et al. Receptor-mediated endocytosis 8 (RME-8)/DNAJC13 is a novel positive modulator of autophagy and stabilizes cellular protein homeostasis. Cell Mol Life Sci. 2021;78(2):645–660. doi: 10.1007/s00018-020-03521-y
  • Brenner S. The genetics of caenorhabditis elegans. Genetics. 1974;77(1):71–94. doi: 10.1093/genetics/77.1.71
  • Frokjaer-Jensen C, Wayne Davis M, Hopkins CE, et al. Single-copy insertion of transgenes in caenorhabditis elegans. Nat Genet. 2008;40(11):1375–1383. doi: 10.1038/ng.248
  • Cai Q, Lu L, Tian J-H, et al. Snapin-regulated late endosomal transport is critical for efficient autophagy-lysosomal function in neurons. Neuron. 2010;68(1):73–86. doi: 10.1016/j.neuron.2010.09.022
  • Cai Q, Zakaria H, Simone A, et al. Spatial Parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr Biol. 2012;22(6):545–552. doi: 10.1016/j.cub.2012.02.005
  • Ye X, Cai Q. Snapin-mediated BACE1 retrograde transport is essential for its degradation in lysosomes and regulation of APP processing in neurons. Cell Rep. 2014;6(1):24–31. doi: 10.1016/j.celrep.2013.12.008
  • Ye X, Sun X, Starovoytov V, et al. Parkin-mediated mitophagy in mutant hAPP neurons and Alzheimer’s disease patient brains. Hum Mol Genet. 2015;24(10):2938–2951. doi: 10.1093/hmg/ddv056
  • Ye X, Feng T, Tammineni P, et al. Regulation of synaptic Amyloid-β generation through BACE1 retrograde transport in a mouse model of Alzheimer’s disease. J Neurosci. 2017;37(10):2639–2655. doi: 10.1523/JNEUROSCI.2851-16.2017
  • Tammineni P, Jeong YY, Feng T, et al. Impaired axonal retrograde trafficking of the retromer complex augments lysosomal deficits in Alzheimer’s disease neurons. Hum Mol Genet. 2017;26(22):4352–4366. doi: 10.1093/hmg/ddx321
  • Han S, Zhang M, Jeong YY, et al. The role of mitophagy in the regulation of mitochondrial energetic status in neurons. Autophagy. 2021;17(12):4182–4201. doi: 10.1080/15548627.2021.1907167
  • Han S, Jeong YY, Sheshadri P, et al. Mitophagy regulates integrity of mitochondria at synapses and is critical for synaptic maintenance. EMBO Rep. 2020;21(9):e49801. doi: 10.15252/embr.201949801
  • Jeong YY, Han S, Jia N, et al. Broad activation of the Parkin pathway induces synaptic mitochondrial deficits in early tauopathy. Brain. 2022;145(1):305–323. doi: 10.1093/brain/awab243

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