3,470
Views
38
CrossRef citations to date
0
Altmetric
Reviews

Mechanism of cargo sorting into small extracellular vesicles

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 8186-8201 | Received 18 Jun 2021, Accepted 03 Sep 2021, Published online: 18 Oct 2021

References

  • 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.
  • Anand S, Samuel M, Kumar S, et al. Ticket to a bubble ride: cargo sorting into exosomes and extracellular vesicles. Biochim Biophys Acta Proteins Proteom. 2019;1867(12):140203.
  • Kowal J, Tkach M, Thery C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol. 2014;29:116–125.
  • Harada Y, Suzuki T, Fukushige T, et al. Generation of the heterogeneity of extracellular vesicles by membrane organization and sorting machineries. Biochim Biophys Acta Gen Subj. 2019;1863(4):681–691.
  • Pathan M, Fonseka P, Chitti SV, et al. Vesiclepedia 2019: a compendium of RNA, proteins, lipids and metabolites in extracellular vesicles. Nucleic Acids Res. 2019;47(D1):D516–d519.
  • Keerthikumar S, Chisanga D, Ariyaratne D, et al. ExoCarta: a Web-Based Compendium of Exosomal Cargo. J Mol Biol. 2016;428(4):688–692.
  • Li SP, Lin ZX, Jiang XY, et al. Exosomal cargo-loading and synthetic exosome-mimics as potential therapeutic tools. Acta Pharmacol Sin. 2018;39(4):542–551.
  • Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature. 2009;458(7237):445–452.
  • Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010;73(10):1907–1920.
  • Futter CE, White IJ. Annexins and endocytosis. Traffic. 2007;8(8):951–958.
  • Li Y, Zheng Q, Bao C, et al. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res. 2015;25(8):981–984.
  • Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523(7559):177–182.
  • Li Y, Gao Y, Gong C, et al. A33 antibody-functionalized exosomes for targeted delivery of doxorubicin against colorectal cancer. Nanomedicine. 2018;14(7):1973–1985.
  • Wang X, Xiang Z, Liu Y, et al. Exosomes derived from Vδ2-T cells control Epstein-Barr virus-associated tumors and induce T cell antitumor immunity. Sci Transl Med. 2020;12(563):563.
  • Jurisic V, Srdic-Rajic T, Konjevic G, et al. TNF-α induced apoptosis is accompanied with rapid CD30 and slower CD45 shedding from K-562 cells. J Membr Biol. 2011;239(3):115–122.
  • Jurisic V, Radenkovic S, Konjevic G. The Actual Role of LDH as Tumor Marker, Biochemical and Clinical Aspects. In: Scatena R, editor. Advances in Cancer Biomarkers: from biochemistry to clinic for a critical revision. Dordrecht: Springer Netherlands; 2015. p. 115–124.
  • Jean-Toussaint R, Tian Y, Chaudhuri AD, et al. Proteome characterization of small extracellular vesicles from spared nerve injury model of neuropathic pain. J Proteomics. 2020;211:103540.
  • Abriel H, Loffing J, Rebhun JF, et al. Defective regulation of the epithelial Na+ channel by Nedd4 in Liddle’s syndrome. J Clin Invest. 1999;103(5):667–673.
  • Villarroya-Beltri C, Baixauli F, Gutierrez-Vazquez C, et al. Sorting it out: regulation of exosome loading. Semin Cancer Biol. 2014;28:3–13.
  • Goel P, Manning JA, Kumar S. NEDD4-2 (NEDD4L): the ubiquitin ligase for multiple membrane proteins. Gene. 2015;557(1):1–10.
  • Henne WM, Buchkovich NJ, Emr SD. The ESCRT pathway. Dev Cell. 2011;21(1):77–91.
  • Migliano SM, Teis D. ESCRT and Membrane Protein Ubiquitination. Prog Mol Subcell Biol. 2018;57:107–135.
  • Welchman RL, Gordon C, Mayer RJ. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat Rev Mol Cell Biol. 2005;6(8):599–609.
  • Geiss-Friedlander R, Melchior F. Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol. 2007;8(12):947–956.
  • Kunadt M, Eckermann K, Stuendl A, et al. Extracellular vesicle sorting of alpha-Synuclein is regulated by sumoylation. Acta Neuropathol. 2015;129(5):695–713.
  • Emmanouilidou E, Melachroinou K, Roumeliotis T, et al. Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J Neurosci. 2010;30(20):6838–6851.
  • Ageta H, Ageta-Ishihara N, Hitachi K, et al. UBL3 modification influences protein sorting to small extracellular vesicles. Nat Commun. 2018;9(1):3936.
  • DemoryBeckler M, Higginbotham JN, Franklin JL, et al. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Mol Cell Proteomics. 2013;12(2):343–355.
  • Shearwin-Whyatt L, Dalton HE, Foot N, et al. Regulation of functional diversity within the Nedd4 family by accessory and adaptor proteins. Bioessays. 2006;28(6):617–628.
  • Putz U, Howitt J, Lackovic J, et al. Nedd4 family-interacting protein 1 (Ndfip1) is required for the exosomal secretion of Nedd4 family proteins. J Biol Chem. 2008;283(47):32621–32627.
  • Anand S, Foot N, Ang CS, et al. Arrestin-Domain Containing Protein 1 (Arrdc1) Regulates the Protein Cargo and Release of Extracellular Vesicles. Proteomics. 2018;18(17):e1800266.
  • Feng Z, Hensley L, McKnight KL, et al. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature. 2013;496(7445):367–371.
  • Jiang W, Ma P, Deng L, et al. Hepatitis A virus structural protein pX interacts with ALIX and promotes the secretion of virions and foreign proteins through exosome-like vesicles. J Extracell Vesicles. 2020;9(1):1716513.
  • Larios J, Mercier V, Roux A, et al. ALIX-and ESCRT-III-dependent sorting of tetraspanins to exosomes. J Cell Biol. 2020;219(3):3.
  • Vild CJ, Li Y, Guo EZ, et al. A novel mechanism of regulating the ATPase VPS4 by its cofactor LIP5 and the endosomal sorting complex required for transport (ESCRT)-III protein CHMP5. J Biol Chem. 2015;290(11):7291–7303.
  • Roche JV, Nesverova V, Olsson C, et al. Structural Insights into AQP2 Targeting to Multivesicular Bodies. Int J Mol Sci. 2019;20(21):21.
  • Han Q, Lv L, Wei J, et al. Vps4A mediates the localization and exosome release of beta-catenin to inhibit epithelial-mesenchymal transition in hepatocellular carcinoma. Cancer Lett. 2019;457:47–59.
  • Giannelli G, Koudelkova P, Dituri F, et al. Role of epithelial to mesenchymal transition in hepatocellular carcinoma. J Hepatol. 2016;65(4):798–808.
  • Heuberger J, Birchmeier W. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol. 2010;2(2):a002915.
  • Stuffers S, Sem Wegner C, Stenmark H, et al. Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic. 2009;10(7):925–937.
  • De Gassart A, Geminard C, Fevrier B, et al. Lipid raft-associated protein sorting in exosomes. Blood. 2003;102(13):4336–4344.
  • Parolini I, Sargiacomo M, Lisanti MP, et al. Signal transduction and glycophosphatidylinositol-linked proteins (lyn, lck, CD4, CD45, G proteins, and CD55) selectively localize in Triton-insoluble plasma membrane domains of human leukemic cell lines and normal granulocytes. Blood. 1996;87(9):3783–3794.
  • Trajkovic K, Hsu C, Chiantia S, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319(5867):1244–1247.
  • Escola JM, Kleijmeer MJ, Stoorvogel W, et al. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem. 1998;273(32):20121–20127.
  • Pols MS, Klumperman J. Trafficking and function of the tetraspanin CD63. Exp Cell Res. 2009;315(9):1584–1592.
  • Hurwitz SN, Nkosi D, Conlon MM, et al. CD63 Regulates Epstein-Barr Virus LMP1 Exosomal Packaging, Enhancement of Vesicle Production, and Noncanonical NF-kappaB Signaling. J Virol. 2017;91(5):5.
  • Dogrammatzis C, Deschamps T, Kalamvoki M. Biogenesis of Extracellular Vesicles during Herpes Simplex Virus 1 Infection: role of the CD63 Tetraspanin. J Virol. 2019;93(2):2.
  • Mazurov D, Barbashova L, Filatov A. Tetraspanin protein CD9 interacts with metalloprotease CD10 and enhances its release via exosomes. Febs J. 2013;280(5):1200–1213.
  • Barrena S, Almeida J, Yunta M, et al. Aberrant expression of tetraspanin molecules in B-cell chronic lymphoproliferative disorders and its correlation with normal B-cell maturation. Leukemia. 2005;19(8):1376–1383.
  • Turchinovich A, Weiz L, Langheinz A, et al. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011;39(16):7223–7233.
  • Mittelbrunn M, Sanchez-Madrid F. Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol. 2012;13(5):328–335.
  • Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A. 2010;107(14):6328–6333.
  • Chen C, Luo Y, He W, et al. Exosomal long noncoding RNA LNMAT2 promotes lymphatic metastasis in bladder cancer. J Clin Invest. 2020;130(1):404–421.
  • Liu R, Li X, Zhu W, et al. Cholangiocyte-Derived Exosomal Long Noncoding RNA H19 Promotes Hepatic Stellate Cell Activation and Cholestatic Liver Fibrosis. Hepatology. 2019;70(4):1317–1335.
  • Zhu L, Li J, Gong Y, et al. Exosomal tRNA-derived small RNA as a promising biomarker for cancer diagnosis. Mol Cancer. 2019;18(1):74.
  • Andreeva OE, Shchegolev YY, Scherbakov AM, et al. Secretion of Mutant DNA and mRNA by the Exosomes of Breast Cancer Cells. Molecules. 2021;26(9):9.
  • Batagov AO, Kurochkin IV. Exosomes secreted by human cells transport largely mRNA fragments that are enriched in the 3ʹ-untranslated regions. Biol Direct. 2013;8(1):12.
  • Mendell JT. MicroRNAs: critical regulators of development, cellular physiology and malignancy. Cell Cycle. 2005;4(9):1179–1184.
  • Guduric-Fuchs J, O’Connor A, Camp B, et al. Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics. 2012;13(1):357.
  • Alexander M, Hu R, Runtsch MC, et al. Exosome-delivered microRNAs modulate the inflammatory response to endotoxin. Nat Commun. 2015;6(1):7321.
  • Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, et al. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013;4(1):2980.
  • Wu B, Su S, Patil DP, et al. Molecular basis for the specific and multivariant recognitions of RNA substrates by human hnRNP A2/B1. Nat Commun. 2018;9(1):420.
  • Han ZJ, Feng YH, Gu BH, et al. The post-translational modification, SUMOylation, and cancer (Review). Int J Oncol. 2018;52(4):1081–1094.
  • Pérez-Boza J, Boeckx A, Lion M, et al. hnRNPA2B1 inhibits the exosomal export of miR-503 in endothelial cells. Cell Mol Life Sci. 2020;77(21):4413–4428.
  • Santangelo L, Giurato G, Cicchini C, et al. The RNA-Binding Protein SYNCRIP Is a Component of the Hepatocyte Exosomal Machinery Controlling MicroRNA Sorting. Cell Rep. 2016;17(3):799–808.
  • Kwon E, Todorova K, Wang J, et al. The RNA-binding protein YBX1 regulates epidermal progenitors at a posttranscriptional level. Nat Commun. 2018;9(1):1734.
  • 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:e19276.
  • Ismail N, Wang Y, Dakhlallah D, et al. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood. 2013;121(6):984–995.
  • Lin F, Zeng Z, Song Y, et al. YBX-1 mediated sorting of miR-133 into hypoxia/reoxygenation-induced EPC-derived exosomes to increase fibroblast angiogenesis and MEndoT. Stem Cell Res Ther. 2019;10(1):263.
  • Wei WJ, Mu SR, Heiner M, et al. YB-1 binds to CAUC motifs and stimulates exon inclusion by enhancing the recruitment of U2AF to weak polypyrimidine tracts. Nucleic Acids Res. 2012;40(17):8622–8636.
  • Teng Y, Ren Y, Hu X, et al. MVP-mediated exosomal sorting of miR-193a promotes colon cancer progression. Nat Commun. 2017;8(1):14448.
  • Schrier M, Severijnen LA, Reis S, et al. Transport kinetics of FMRP containing the I304N mutation of severe fragile X syndrome in neurites of living rat PC12 cells. Exp Neurol. 2004;189(2):343–353.
  • De Diego Otero Y, Severijnen LA, van Cappellen G, et al. Transport of fragile X mental retardation protein via granules in neurites of PC12 cells. Mol Cell Biol. 2002;22(23):8332–8341.
  • McDaniel K, Herrera L, Zhou T, et al. The functional role of microRNAs in alcoholic liver injury. J Cell Mol Med. 2014;18(2):197–207.
  • Shen J, Huang CK, Yu H, et al. The role of exosomes in hepatitis, liver cirrhosis and hepatocellular carcinoma. J Cell Mol Med. 2017;21(5):986–992.
  • Wozniak AL, Long A, Jones-Jamtgaard KN, et al. Hepatitis C virus promotes virion secretion through cleavage of the Rab7 adaptor protein RILP. Proc Natl Acad Sci U S A. 2016;113(44):12484–12489.
  • Wozniak AL, Adams A, KE K, et al. The RNA binding protein FMR1 controls selective exosomal miRNA cargo loading during inflammation. J Cell Biol. 2020;219(10):10.
  • Meister G. Argonaute proteins: functional insights and emerging roles. Nat Rev Genet. 2013;14(7):447–459.
  • McKenzie AJ, Hoshino D, Hong NH, et al. KRAS-MEK Signaling Controls Ago2 Sorting into Exosomes. Cell Rep. 2016;15(5):978–987.
  • Müller M, Fazi F, Ciaudo C. Argonaute Proteins: from Structure to Function in Development and Pathological Cell Fate Determination. Front Cell Dev Biol. 2019;7:360.
  • Leidal AM, Huang HH, Marsh T, et al. The LC3-conjugation machinery specifies the loading of RNA-binding proteins into extracellular vesicles. Nat Cell Biol. 2020;22(2):187–199.
  • Kaur J, Debnath J. Autophagy at the crossroads of catabolism and anabolism. Nat Rev Mol Cell Biol. 2015;16(8):461–472.
  • Kosaka N, Iguchi H, Yoshioka Y, et al. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010;285(23):17442–17452.
  • Kosaka N, Iguchi H, Hagiwara K, et al. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J Biol Chem. 2013;288(15):10849–10859.
  • Singh R, Pochampally R, Watabe K, et al. Exosome-mediated transfer of miR-10b promotes cell invasion in breast cancer. Mol Cancer. 2014;13(1):256.
  • Cha DJ, Franklin JL, Dou Y, et al. KRAS-dependent sorting of miRNA to exosomes. Elife. 2015;4:e07197.
  • Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9(6):654–659.
  • Mofatteh M, Bullock SL. SnapShot: subcellular mRNA Localization. Cell. 2017;169(1):178–178.e171.
  • Bolukbasi MF, Mizrak A, Ozdener GB, et al. miR-1289 and “Zipcode”-like Sequence Enrich mRNAs in Microvesicles. Mol Ther Nucleic Acids. 2012;1:e10.
  • Yanshina DD, Kossinova OA, Gopanenko AV, et al. Structural features of the interaction of the 3ʹ-untranslated region of mRNA containing exosomal RNA-specific motifs with YB-1, a potential mediator of mRNA sorting. Biochimie. 2018;144:134–143.
  • Peters DL, Pretorius PJ. Origin, translocation and destination of extracellular occurring DNA–a new paradigm in genetic behaviour. Clin Chim Acta. 2011;412(11–12):806–811.
  • Lázaro-Ibáñez E, Lässer C, Shelke GV, et al. DNA analysis of low- and high-density fractions defines heterogeneous subpopulations of small extracellular vesicles based on their DNA cargo and topology. J Extracell Vesicles. 2019;8(1):1656993.
  • Balaj L, Lessard R, Dai L, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun. 2011;2(1):180.
  • Yokoi A, Villar-Prados A, Oliphint PA, et al. Mechanisms of nuclear content loading to exosomes. Sci Adv. 2019;5(11):eaax884911
  • Thakur BK, Zhang H, Becker A, et al. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 2014;24(6):766–769.
  • Fenech M. Cytokinesis-block micronucleus cytome assay. Nat Protoc. 2007;2(5):1084–1104.
  • Skotland T, Sandvig K, Llorente A. Lipids in exosomes: current knowledge and the way forward. Prog Lipid Res. 2017;66:30–41.
  • Haraszti RA, Didiot M-C, Sapp E, et al. High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources. J Extracell Vesicles. 2016;5(1):1.
  • Hannun YA, Obeid LM. Sphingolipids and their metabolism in physiology and disease. Nat Rev Mol Cell Biol. 2018;19(3):175–191.
  • Crescitelli R, Lässer C, Jang SC, et al. Subpopulations of extracellular vesicles from human metastatic melanoma tissue identified by quantitative proteomics after optimized isolation. J Extracell Vesicles. 2020;9(1):1722433.
  • Greening DW, Xu R, Ji H, et al. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods Mol Biol. 2015;1295:179–209.
  • Monguió-Tortajada M, Gálvez-Montón C, Bayes-Genis A, et al. Extracellular vesicle isolation methods: rising impact of size-exclusion chromatography. Cell Mol Life Sci. 2019;76(12):2369–2382.