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Research Paper

Chloroquine treatment induces secretion of autophagy-related proteins and inclusion of Atg8-family proteins in distinct extracellular vesicle populations

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Pages 2547-2560 | Received 23 Mar 2021, Accepted 04 Feb 2022, Published online: 28 Feb 2022

References

  • Levy JMM, Towers CG, Thorburn A. Targeting autophagy in cancer. Nat Rev Cancer. 2017;17(9):528–542.
  • He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009;43(1):67–93.
  • Ponpuak M, Mandell MA, Kimura T, et al. Secretory autophagy. Curr Opin Cell Biol. 2015;35:106–116.
  • Rebecca VW, Amaravadi RK. Emerging strategies to effectively target autophagy in cancer. Oncogene. 2016;35(1):1–11.
  • Dolgin E. Anticancer autophagy inhibitors attract ‘resurgent’ interest. Nat Rev Drug Discov. 2019;18(6):408–410.
  • Chude CI, Amaravadi RK. Targeting autophagy in cancer: update on clinical trials and novel inhibitors. Int J Mol Sci. 2017;18(6):1279.
  • Maes H, Kuchnio A, Peric A, et al. Tumor vessel normalization by chloroquine independent of autophagy. Cancer Cell. 2014;26(2):190–206.
  • van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213–228.
  • Yáñez-Mó M, Siljander PR-M, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4(1):27066.
  • El Andaloussi S,Mager, I,Breakefield, X. O, et al. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov. 2013;12(5):347–357.
  • Hoshino A, Costa-Silva, B, Shen, T. L, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;1–19. DOI:10.1038/nature15756.
  • Xu J, Camfield R, Gorski SM. The interplay between exosomes and autophagy – partners in crime. J Cell Sci. 2018;131(15):jcs215210.
  • Eitan E, Suire C, Zhang S, et al. Impact of lysosome status on extracellular vesicle content and release. Ageing Res. Rev. 2016; 1–10. DOI:10.1016/j.arr.2016.05.001.
  • Fussi N, Höllerhage M, Chakroun T, et al. Exosomal secretion of α-synuclein as protective mechanism after upstream blockage of macroautophagy. Cell Death Dis. 2018;9(7): DOI:10.1038/s41419-018-0816-2.
  • Leidal AM, Huang, HH, Marsh, T, et al. The LC3-conjugation machinery specifies the loading of RNA-binding proteins into extracellular vesicles. Nat Cell Bio. 2020;22(2):187–199.
  • Hughes CS, Foehr, S, Garfield, D. A, et al. Ultrasensitive proteome analysis using paramagnetic bead technology. Mol Syst Biol. 2014;10(10):757.
  • Kohtala S, Theilmann W, Suomi T. PECA: probe-level expression change averaging. ACS Chemical Neuroscience. 2016;7(6):749–756.
  • Mauthe M, Orhon I, Rocchi C, et al. Chloroquine inhibits autophagic flux by decreasing autophagosome-lysosome fusion. Autophagy. 2018;14(8):1435–1455.
  • Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy. 2011;7(3):279–296.
  • Mancias JD, Wang X, Gygi SP, et al. Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature. 2014;509(7498):105–109.
  • Sarraf SA, Shah HV, Kanfer G, et al. Selective autophagic clearance of protein aggregates is mediated by the autophagy receptor, TAX1BP1. bioRxiv. 2019;558767. DOI:10.1101/558767.
  • Kirkin V, Rogov VV. A diversity of selective autophagy receptors determines the specificity of the autophagy pathway. Mol Cell. 2019;76(2):268–285.
  • Xie X, Li F, Wang Y, et al. Molecular basis of ubiquitin recognition by the autophagy receptor CALCOCO2. Autophagy. 2015;11(10):1775–1789.
  • 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.
  • Guo H, Chitiprolu M, Roncevic L, et al. Atg5 disassociates the V1V0-ATPase to promote exosome production and tumor metastasis independent of canonical macroautophagy. Dev Cell. 2017;43(6):716–730.e7.
  • Lystad AH, Carlsson SR, de la Ballina LR, et al. Distinct functions of ATG16L1 isoforms in membrane binding and LC3B lipidation in autophagy-related processes. Nat Cell Bio. 2019;21(3):372–383.
  • Agrotis A, von Chamier L, Oliver H, et al. Human ATG4 autophagy proteases counteract attachment of ubiquitin-like LC3/GABARAP proteins to other cellular proteins. J Biol Chem. 2019;294(34):jbc.AC119.009977.
  • Agrotis A, Pengo N, Burden JJ, et al. Redundancy of human ATG4 protease isoforms in autophagy and LC3/GABARAP processing revealed in cells. Autophagy. 2019;00:1–22.
  • Kraft C, Peter M, Hofmann K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat Cell Bio. 2010;12(9):836–841.
  • Tauro BJ, Greening DW, Mathias RA, et al. Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids. Mol Cell Proteomics. 2013;12(3):587–598.
  • Colombo M, Moita C, van Niel G, et al. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci. 2013;126(Pt 24):5553–5565.
  • Jeppesen DK, Fenix AM, Franklin JL, et al. Reassessment of exosome composition. Cell. 2019;177(2):428–445.e18.
  • Baietti MF, Zhang Z, Mortier E, et al. Syndecan–syntenin–ALIX regulates the biogenesis of exosomes. Nat Cell Bio. 2012;14(7):677–685.
  • Fletcher K, Ulferts, R, Jacquin, E, et al. The WD40 domain of ATG16L1 is required for its non‐canonical role in lipidation of LC3 at single membranes. EMBO J. 2018;e97840. DOI:10.15252/embj.201797840.
  • Russell RC, Tian Y, Yuan H, et al. ULK1 induces autophagy by phosphorylating beclin-1 and activating VPS34 lipid kinase. Nat Cell Bio. 2013;15(7):741–750.
  • Zachari M, Ganley IG, Lane JD. The mammalian ULK1 complex and autophagy initiation. Essays Biochem. 2017;61(6):585–596.
  • Ohnstad AE, Delgado, JM, North, BJ, et al. Receptor‐mediated clustering of FIP200 bypasses the role of LC3 lipidation in autophagy. EMBO J. 2020;39(24):1–20.
  • Minakaki G, Menges, S, Kittel, A, et al. Autophagy inhibition promotes SNCA/alpha-synuclein release and transfer via extracellular vesicles with a hybrid autophagosome-exosome-like phenotype. Autophagy. 2017;8627:1–61.
  • Latifkar A, Ling L, Hingorani A, et al. Loss of sirtuin 1 alters the secretome of breast cancer cells by impairing lysosomal integrity. Dev Cell. 2019;49(3):393–408.e7.
  • Sahu R, Kaushik S, Clement CC, et al. Microautophagy of cytosolic proteins by late endosomes. Dev Cell. 2011;20(1):131–139.
  • Mukherjee A, Patel B, Koga H, et al. Selective endosomal microautophagy is starvation-inducible in drosophila. Autophagy. 2016;12(11):1984–1999.
  • Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016;113(8):E968–77.
  • Mathieu M, Menges, S, Kittel, A, et al. Specificities of exosome versus small ectosome secretion revealed by live intracellular tracking and synchronized extracellular vesicle release of CD9 and CD63. bioRxiv. 2020;2020(10.27.323766). DOI:10.1101/2020.10.27.323766
  • Florey O, Gammoh N, Kim SE, et al. V-ATPase and osmotic imbalances activate endolysosomal LC3 lipidation. Autophagy. 2015;11(1):88–99.
  • Jacquin E, Leclerc-Mercier S, Judon C, et al. Pharmacological modulators of autophagy activate a parallel noncanonical pathway driving unconventional LC3 lipidation. Autophagy. 2017;13(5):854–867.
  • Durgan J, Lystad AH, Sloan, K, et al. Non-canonical autophagy drives alternative ATG8 conjugation to phosphatidylserine. Mol Cell. 2021;81(9):2031–2040.e8.
  • Patel KK, Miyoshi H, Beatty WL, et al. Autophagy proteins control goblet cell function by potentiating reactive oxygen species production. EMBO J. 2013;32(24):3130–3144.
  • Zhang M, Kenny SJ, Ge L, et al. Translocation of interleukin-1β into a vesicle intermediate in autophagy- mediated secretion. Elife. 2015;4. 10.7554/eLife.11205
  • Bachurski D, Schuldner, M, Nguyen, PH, et al. Extracellular vesicle measurements with nanoparticle tracking analysis – an accuracy and repeatability comparison between NanoSight NS300 and ZetaView. J Extracell Vesicles. 2019;8(1):1596016.
  • Xu R, Ji Z, Xu C, et al. The clinical value of using chloroquine or hydroxychloroquine as autophagy inhibitors in the treatment of cancers. Medicine (Baltimore). 2018;97(46):e12912.
  • Maycotte P, Aryal S, Cummings CT, et al. Chloroquine sensitizes breast cancer cells to chemotherapy independent of autophagy. Autophagy. 2012;8(2):200–212.
  • Shurtleff MJ, Temoche-Diaz MM, Karfilis KV, et al. Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction. Elife. 2016;5:1–23.
  • Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–675.
  • Bolte S, Cordelières FP. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 2006;224(3):213–232.
  • Perez-Riverol Y, Csordas A, Bai J, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47(D1):D442–D450.
  • R Core Team. . R: A Language and Environment for Statistical Computing. https://www.R-project.org/. Vienna, Austria: R Foundation for Statistical Computing; 2016, .
  • Thomas PD, Campbell MJ, Kejariwal A. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res. 2003;13(9):2129–2141.
  • Yu G, Wang L-G, Han Y, et al. clusterProfiler: an R package for comparing biological themes among gene clusters. Omi A J Integr Biol. 2012;16(5):284–287.
  • Jacomin A-C, Samavedam S, Promponas V, et al. iLIR database: a web resource for LIR motif-containing proteins in eukaryotes. Autophagy. 2016;12(10):1945–1953.
  • Van Deun J, Mestdagh, P, Agostinis, P, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Methods. 2017;14(3):228–232.
  • Théry C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the international society for extracellular vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7(1):1535750.

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