Skip to main content
SpringerLink
Log in

Biogenesis of Extracellular Vesicles

  • Chapter
  • First Online:
New Frontiers: Extracellular Vesicles

Part of the book series: Subcellular Biochemistry ((SCBI,volume 97))

Abstract

Extracellular vesicles (EVs) refer to vesicles that are released by cells into the extracellular space. EVs mediate cell-to-cell communication via delivery of functional biomolecules between host and recipient cells. EVs can be categorised based on their mode of biogenesis and secretion and include apoptotic bodies, ectosomes or shedding microvesicles and exosomes among others. EVs have gained immense interest in recent years owing to their implications in pathophysiological conditions. Indeed, EVs have been proven useful in clinical applications as potential drug delivery vehicles and as source of diagnostic biomarkers. Despite the growing body of evidence supporting the clinical benefits, the processes involved in the biogenesis of EVs are poorly understood. Hence, it is critical to gain a deeper understanding of the underlying molecular machineries that ultimately govern the biogenesis and secretion of EVs. This chapter discusses the current knowledge on molecular mechanisms involved in the biogenesis of various subtypes of EVs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, Norman M, Neve EP, Scheynius A, Gabrielsson S (2007) Exosomes with immune modulatory features are present in human breast milk. J Immunol 179(3):1969–1978

    Article  CAS  PubMed  Google Scholar 

  • Agromayor M, Soler N, Caballe A, Kueck T, Freund SM, Allen MD, Bycroft M, Perisic O, Ye Y, McDonald B, Scheel H, Hofmann K, Neil SJD, Martin-Serrano J, Williams RL (2012) The UBAP1 subunit of ESCRT-I interacts with ubiquitin via a SOUBA domain. Structure 20(3):414–428

    Article  CAS  PubMed  Google Scholar 

  • Albrecht C, McVey JH, Elliott JI, Sardini A, Kasza I, Mumford AD, Naoumova RP, Tuddenham EG, Szabo K, Higgins CF (2005) A novel missense mutation in ABCA1 results in altered protein trafficking and reduced phosphatidylserine translocation in a patient with Scott syndrome. Blood 106(2):542–549

    Article  CAS  PubMed  Google Scholar 

  • Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, Rak J (2008) Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 10(5):619–624

    Article  CAS  PubMed  Google Scholar 

  • Anand S, Foot N, Ang CS, Gembus KM, Keerthikumar S, Adda CG, Mathivanan S, Kumar S (2018) Arrestin-domain containing protein 1 (Arrdc1) regulates the protein cargo and release of extracellular vesicles. Proteomics. https://doi.org/10.1002/pmic.201800266

  • Anand S, Samuel M, Kumar S, Mathivanan S (2019) Ticket to a bubble ride: cargo sorting into exosomes and extracellular vesicles. Biochim Biophys Acta Proteins Proteom. https://doi.org/10.1016/j.bbapap.2019.02.005

  • Ando J, Kinoshita M, Cui J, Yamakoshi H, Dodo K, Fujita K, Murata M, Sodeoka M (2015) Sphingomyelin distribution in lipid rafts of artificial monolayer membranes visualized by Raman microscopy. Proc Natl Acad Sci 112(15):4558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andreu Z, Yáñez-Mó M (2014) Tetraspanins in extracellular vesicle formation and function. Front Immunol 5:442

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD (2002a) Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell 3(2):271–282

    Article  CAS  PubMed  Google Scholar 

  • Babst M, Katzmann DJ, Snyder WB, Wendland B, Emr SD (2002b) Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell 3(2):283–289

    Article  CAS  PubMed  Google Scholar 

  • Bache KG, Brech A, Mehlum A, Stenmark H (2003a) Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J Cell Biol 162(3):435–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bache KG, Raiborg C, Mehlum A, Stenmark H (2003b) STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J Biol Chem 278(14):12513–12521

    Article  CAS  PubMed  Google Scholar 

  • Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, Zimmermann P, David G (2012) Syndecan–syntenin–ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14(7):677–685

    Article  CAS  PubMed  Google Scholar 

  • Bari R, Guo Q, Xia B, Zhang YH, Giesert EE, Levy S, Zheng JJ, Zhang XA (2011) Tetraspanins regulate the protrusive activities of cell membrane. Biochem Biophys Res Commun 415(4):619–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barreiro O, Yáñez-Mó M, Sala-Valdés M, Gutiérrez-López MD, Ovalle S, Higginbottom A, Monk PN, Cabañas C, Sánchez-Madrid F (2005) Endothelial tetraspanin microdomains regulate leukocyte firm adhesion during extravasation. Blood 105(7):2852–2861

    Article  CAS  PubMed  Google Scholar 

  • Berditchevski F (2001) Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci 114(23):4143–4151

    Article  CAS  PubMed  Google Scholar 

  • Bevers EM, Williamson PL (2016) Getting to the outer leaflet: physiology of Phosphatidylserine exposure at the plasma membrane. Physiol Rev 96(2):605–645

    Article  CAS  PubMed  Google Scholar 

  • Boere J, Malda J, van de Lest CHA, van Weeren PR, Wauben MHM (2018) Extracellular vesicles in joint disease and therapy. Front Immunol 9:2575–2575

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Borrelli DA, Yankson K, Shukla N, Vilanilam G, Ticer T, Wolfram J (2018) Extracellular vesicle therapeutics for liver disease. J Control Release 273:86–98

    Article  CAS  PubMed  Google Scholar 

  • Boucheix C, Rubinstein E (2001) Tetraspanins. Cell Mol Life Sci 58(9):1189–1205

    Article  CAS  PubMed  Google Scholar 

  • Boukouris S, Mathivanan S (2015) Exosomes in bodily fluids are a highly stable resource of disease biomarkers. Proteomics Clin Appl 9(3–4):358–367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brisson C, Azorsa DO, Jennings LK, Moog S, Cazenave JP, Lanza F (1997) Co-localization of CD9 and GPIIb-IIIa (alpha IIb beta 3 integrin) on activated platelet pseudopods and alpha-granule membranes. Histochem J 29(2):153–165

    Article  CAS  PubMed  Google Scholar 

  • Brzozowski JS, Bond DR, Jankowski H, Goldie BJ, Burchell R, Naudin C, Smith ND, Scarlett CJ, Larsen MR, Dun MD, Skelding KA, Weidenhofer J (2018) Extracellular vesicles with altered tetraspanin CD9 and CD151 levels confer increased prostate cell motility and invasion. Sci Rep 8(1):8822

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carnino JM, Lee H, Jin Y (2019) Isolation and characterization of extracellular vesicles from Broncho-alveolar lavage fluid: a review and comparison of different methods. Respir Res 20(1):240

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Caruso S, Poon IKH (2018) Apoptotic cell-derived extracellular vesicles: more than just debris. Front Immunol 9:1486

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Castro BM, Prieto M, Silva LC (2014) Ceramide: a simple sphingolipid with unique biophysical properties. Prog Lipid Res 54:53–67

    Article  CAS  PubMed  Google Scholar 

  • Chairoungdua A, Smith DL, Pochard P, Hull M, Caplan MJ (2010) Exosome release of β-catenin: a novel mechanism that antagonizes Wnt signaling. J Cell Biol 190(6):1079–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charras GT, Yarrow JC, Horton MA, Mahadevan L, Mitchison TJ (2005) Non-equilibration of hydrostatic pressure in blebbing cells. Nature 435(7040):365–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charras GT, Coughlin M, Mitchison TJ, Mahadevan L (2008) Life and times of a cellular bleb. Biophys J 94(5):1836–1853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charrin S, Le Naour F, Labas V, Billard M, Le Caer JP, Emile JF, Petit MA, Boucheix C, Rubinstein E (2003) EWI-2 is a new component of the tetraspanin web in hepatocytes and lymphoid cells. Biochem J 373(Pt 2):409–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charrin S, le Naour F, Silvie O, Milhiet PE, Boucheix C, Rubinstein E (2009) Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J 420(2):133–154

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Sun X, Scicluna BJ, Coleman BM, Hill AF (2014) Characterization and deep sequencing analysis of exosomal and non-exosomal miRNA in human urine. Kidney Int 86(2):433–444

    Article  CAS  PubMed  Google Scholar 

  • Chitti SV, Fonseka P, Mathivanan S (2018) Emerging role of extracellular vesicles in mediating cancer cachexia. Biochem Soc Trans 46(5):1129–1136

    Article  CAS  PubMed  Google Scholar 

  • Chiu R, Novikov L, Mukherjee S, Shields D (2002) A caspase cleavage fragment of p115 induces fragmentation of the Golgi apparatus and apoptosis. J Cell Biol 159(4):637–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chivet M, Javalet C, Laulagnier K, Blot B, Hemming FJ, Sadoul R (2014) Exosomes secreted by cortical neurons upon glutamatergic synapse activation specifically interact with neurons. J Extracell Vesicles 3:24722–24722

    Article  PubMed  Google Scholar 

  • Chuo ST-Y, Chien JC-Y, Lai CP-K (2018) Imaging extracellular vesicles: current and emerging methods. J Biomed Sci 25(1):91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coller HA (2014) Is cancer a metabolic disease? Am J Pathol 184(1):4–17

    Article  PubMed  PubMed Central  Google Scholar 

  • Colombo M, Moita C, van Niel G, Kowal J, Vigneron J, Benaroch P, Manel N, Moita LF, Théry C, Raposo G (2013) Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci 126(24):5553–5565

    CAS  PubMed  Google Scholar 

  • Colombo M, Raposo G, Théry C (2014) Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 30(1):255–289

    Article  CAS  PubMed  Google Scholar 

  • Curtiss M, Jones C, Babst M (2007) Efficient cargo sorting by ESCRT-I and the subsequent release of ESCRT-I from multivesicular bodies requires the subunit Mvb12. Mol Biol Cell 18(2):636–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • da Rocha-Azevedo B, Schmid SL (2015) Migrasomes: a new organelle of migrating cells. Cell Res 25(1):1–2

    Article  PubMed  CAS  Google Scholar 

  • Di Vizio D, Kim J, Hager MH, Morello M, Yang W, Lafargue CJ, True LD, Rubin MA, Adam RM, Beroukhim R, Demichelis F, Freeman MR (2009) Oncosome formation in prostate Cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res 69(13):5601

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Di Vizio D, Morello M, Dudley AC, Schow PW, Adam RM, Morley S, Mulholland D, Rotinen M, Hager MH, Insabato L, Moses MA, Demichelis F, Lisanti MP, Wu H, Klagsbrun M, Bhowmick NA, Rubin MA, D'Souza-Schorey C, Freeman MR (2012) Large oncosomes in human prostate cancer tissues and in the circulation of mice with metastatic disease. Am J Pathol 181(5):1573–1584

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Edgar JR, Eden ER, Futter CE (2014) Hrs- and CD63-dependent competing mechanisms make different sized endosomal intraluminal vesicles. Traffic (Copenhagen, Denmark) 15(2):197–211

    Article  CAS  Google Scholar 

  • Erwig LP, Henson PM (2008) Clearance of apoptotic cells by phagocytes. Cell Death Differ 15(2):243–250

    Article  CAS  PubMed  Google Scholar 

  • Essandoh K, Yang L, Wang X, Huang W, Qin D, Hao J, Wang Y, Zingarelli B, Peng T, Fan G-C (2015) Blockade of exosome generation with GW4869 dampens the sepsis-induced inflammation and cardiac dysfunction. Biochim Biophys Acta (BBA) Mol Basis Dis 1852(11):2362–2371

    Article  CAS  Google Scholar 

  • Fabrikant G, Lata S, Riches JD, Briggs JA, Weissenhorn W, Kozlov MM (2009) Computational model of membrane fission catalyzed by ESCRT-III. PLoS Comput Biol 5(11):e1000575

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fonseka P, Liem M, Ozcitti C, Adda CG, Ang CS, Mathivanan S (2019) Exosomes from N-Myc amplified neuroblastoma cells induce migration and confer chemoresistance to non-N-Myc amplified cells: implications of intra-tumor heterogeneity. J Extracell Vesicles 8(1):1597614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frankel EB, Shankar R, Moresco JJ, Yates JR, Volkmann N, Audhya A (2017) Ist1 regulates ESCRT-III assembly and function during multivesicular endosome biogenesis in Caenorhabditis elegans embryos. Nat Commun 8(1):1439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedman JR, Dibenedetto JR, West M, Rowland AA, Voeltz GK (2013) Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature. Mol Biol Cell 24(7):1030–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gangoda L, Boukouris S, Liem M, Kalra H, Mathivanan S (2015) Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic? Proteomics 15(2–3):260–271

    Article  CAS  PubMed  Google Scholar 

  • Gavrilescu LC, Denkers EY (2003) Apoptosis and the balance of homeostatic and pathologic responses to protozoan infection. Infect Immun 71(11):6109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorvel JP, Chavrier P, Zerial M, Gruenberg J (1991) rab5 controls early endosome fusion in vitro. Cell 64(5):915–925

    Article  CAS  PubMed  Google Scholar 

  • Grange C, Skovronova R, Marabese F, Bussolati B (2019) Stem cell-derived extracellular vesicles and kidney regeneration. Cell 8(10):1240

    Article  CAS  Google Scholar 

  • Guix FX, Sannerud R, Berditchevski F, Arranz AM, Horré K, Snellinx A, Thathiah A, Saido T, Saito T, Rajesh S, Overduin M, Kumar-Singh S, Radaelli E, Corthout N, Colombelli J, Tosi S, Munck S, Salas IH, Annaert W, De Strooper B (2017) Tetraspanin 6: a pivotal protein of the multiple vesicular body determining exosome release and lysosomal degradation of amyloid precursor protein fragments. Mol Neurodegener 12(1):25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hankins HM, Baldridge RD, Xu P, Graham TR (2015) Role of flippases, scramblases and transfer proteins in phosphatidylserine subcellular distribution. Traffic (Copenhagen, Denmark) 16(1):35–47

    Article  CAS  Google Scholar 

  • Hannafon BN, Ding WQ (2013) Intercellular communication by exosome-derived microRNAs in cancer. Int J Mol Sci 14(7):14240–14269

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Harding C, Heuser J, Stahl P (1983) Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 97(2):329–339

    Article  CAS  PubMed  Google Scholar 

  • Hemler ME (2005) Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 6(10):801–811

    Article  CAS  PubMed  Google Scholar 

  • Hessvik NP, Øverbye A, Brech A, Torgersen ML, Jakobsen IS, Sandvig K, Llorente A (2016) PIKfyve inhibition increases exosome release and induces secretory autophagy. Cell Mol Life Sci 73(24):4717–4737

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Zucker B, Zhang S, Elias S, Zhu Y, Chen H, Ding T, Li Y, Sun Y, Lou J, Kozlov MM, Yu L (2019) Migrasome formation is mediated by assembly of micron-scale tetraspanin macrodomains. Nat Cell Biol 21(8):991–1002

    Article  CAS  PubMed  Google Scholar 

  • Israels SJ, McMillan-Ward EM (2007) Platelet tetraspanin complexes and their association with lipid rafts. Thromb Haemost 98(5):1081–1087

    CAS  PubMed  Google Scholar 

  • Jahn R, Scheller RH (2006) SNAREs—engines for membrane fusion. Nat Rev Mol Cell Biol 7(9):631–643

    Article  CAS  PubMed  Google Scholar 

  • Janmey PA, Kinnunen PKJ (2006) Biophysical properties of lipids and dynamic membranes. Trends Cell Biol 16(10):538–546

    Article  CAS  PubMed  Google Scholar 

  • Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262(19):9412–9420

    Article  CAS  PubMed  Google Scholar 

  • Kalra H, Drummen GPC, Mathivanan S (2016) Focus on extracellular vesicles: introducing the next small big thing. Int J Mol Sci 17(2):170

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kalra H, Gangoda L, Fonseka P, Chitti SV, Liem M, Keerthikumar S, Samuel M, Boukouris S, Al Saffar H, Collins C, Adda CG, Ang CS, Mathivanan S (2019) Extracellular vesicles containing oncogenic mutant beta-catenin activate Wnt signalling pathway in the recipient cells. J Extracell Vesicles 8(1):1690217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Shibata H, Suzuki H, Nara A, Ishidoh K, Kominami E, Yoshimori T, Maki M (2003) The ALG-2-interacting protein Alix Associates with CHMP4b, a human homologue of yeast Snf7 that is involved in multivesicular body sorting. J Biol Chem 278(40):39104–39113

    Article  CAS  PubMed  Google Scholar 

  • Katzmann DJ, Babst M, Emr SD (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved Endosomal protein sorting complex, ESCRT-I. Cell 106(2):145–155

    Article  CAS  PubMed  Google Scholar 

  • Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Morley S, Le M, Bedoret D, Umetsu DT, Di Vizio D, Freeman MR (2014) Enhanced shedding of extracellular vesicles from amoeboid prostate cancer cells: potential effects on the tumor microenvironment. Cancer Biol Ther 15(4):409–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koniusz S, Andrzejewska A, Muraca M, Srivastava AK, Janowski M, Lukomska B (2016) Extracellular vesicles in physiology, pathology, and therapy of the immune and central nervous system, with focus on extracellular vesicles derived from mesenchymal stem cells as therapeutic tools. Front Cell Neurosci 10:109–109

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kowal J, Tkach M, Thery C (2014) Biogenesis and secretion of exosomes. Curr Opin Cell Biol 29:116–125

    Article  CAS  PubMed  Google Scholar 

  • Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, Dingli F, Loew D, Tkach M, Théry C (2016) Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci 113(8):E968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kutateladze TG (2006) Phosphatidylinositol 3-phosphate recognition and membrane docking by the FYVE domain. Biochim Biophys Acta 1761(8):868–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lachenal G, Pernet-Gallay K, Chivet M, Hemming FJ, Belly A, Bodon G, Blot B, Haase G, Goldberg Y, Sadoul R (2011) Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol Cell Neurosci 46(2):409–418

    Article  CAS  PubMed  Google Scholar 

  • Lachmann J, Barr FA, Ungermann C (2012) The Msb3/Gyp3 GAP controls the activity of the Rab GTPases Vps21 and Ypt7 at endosomes and vacuoles. Mol Biol Cell 23(13):2516–2526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee TH, D’Asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J (2011) Microvesicles as mediators of intercellular communication in cancer: the emerging science of cellular ‘debris’. Semin Immunopathol 33(5):455–467

    Article  PubMed  Google Scholar 

  • Lee JH, Cho HS, Lee JJ, Jun SY, Ahn JH, Min JS, Yoon JY, Choi MH, Jeon SJ, Lim JH, Jung CR, Kim DS, Kim HT, Factor VM, Lee YH, Thorgeirsson SS, Kim CH, Kim NS (2016) Plasma glutamate carboxypeptidase is a negative regulator in liver cancer metastasis. Oncotarget 7(48):79774–79786

    Article  PubMed  PubMed Central  Google Scholar 

  • Leverrier Y, Ridley AJ (2001) Apoptosis: caspases orchestrate the ROCK `n' bleb. Nat Cell Biol 3(4):E91–E92

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Wang Y, Wu H, Zhang L, Yang P, Li Z (2014) GRP78 enhances the glutamine metabolism to support cell survival from glucose deficiency by modulating the β-catenin signaling. Oncotarget 5(14):5369–5380

    Article  PubMed  PubMed Central  Google Scholar 

  • Liem M, Ang CS, Mathivanan S (2017) Insulin mediated activation of PI3K/Akt signalling pathway modifies the proteomic cargo of extracellular vesicles. Proteomics 17(23–24):1600371

    Article  CAS  Google Scholar 

  • Lu Z, Zhang C, Zhai Z (2005) Nucleoplasmin regulates chromatin condensation during apoptosis. Proc Natl Acad Sci USA 102(8):2778–2783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E, Buchanan M, Hosein AN, Basik M, Wrana JL (2012) Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 151(7):1542–1556

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Li Y, Peng J, Wu D, Zhao X, Cui Y, Chen L, Yan X, Du Y, Yu L (2015) Discovery of the migrasome, an organelle mediating release of cytoplasmic contents during cell migration. Cell Res 25(1):24–38

    Article  CAS  PubMed  Google Scholar 

  • Malerød L, Stuffers S, Brech A, Stenmark H (2007) Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8(11):1617–1629

    Article  PubMed  CAS  Google Scholar 

  • Margolis L, Sadovsky Y (2019) The biology of extracellular vesicles: the known unknowns. PLoS Biol 17(7):e3000363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masvekar R, Mizrahi J, Park J, Williamson PR, Bielekova B (2019) Quantifications of CSF apoptotic bodies do not provide clinical value in multiple sclerosis. Front Neurol 10:1241

    Article  PubMed  PubMed Central  Google Scholar 

  • Mazurov D, Barbashova L, Filatov A (2013) Tetraspanin protein CD9 interacts with metalloprotease CD10 and enhances its release via exosomes. FEBS J 280(5):1200–1213

    Article  CAS  PubMed  Google Scholar 

  • McConnell RE, Higginbotham JN, Shifrin DA Jr, Tabb DL, Coffey RJ, Tyska MJ (2009) The enterocyte microvillus is a vesicle-generating organelle. J Cell Biol 185(7):1285–1298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCullough J, Fisher RD, Whitby FG, Sundquist WI, Hill CP (2008) ALIX-CHMP4 interactions in the human ESCRT pathway. Proc Natl Acad Sci USA 105(22):7687–7691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menck K, Sönmezer C, Worst TS, Schulz M, Dihazi GH, Streit F, Erdmann G, Kling S, Boutros M, Binder C, Gross JC (2017) Neutral sphingomyelinases control extracellular vesicles budding from the plasma membrane. J Extracell Vesicles 6(1):1378056–1378056

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Michael A, Bajracharya SD, Yuen PST, Zhou H, Star RA, Illei GG, Alevizos I (2010) Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis 16(1):34–38

    Article  CAS  PubMed  Google Scholar 

  • Minciacchi VR, Freeman MR, Di Vizio D (2015a) Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol 40:41–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minciacchi VR, You S, Spinelli C, Morley S, Zandian M, Aspuria PJ, Cavallini L, Ciardiello C, Reis Sobreiro M, Morello M, Kharmate G, Jang SC, Kim DK, Hosseini-Beheshti E, Tomlinson Guns E, Gleave M, Gho YS, Mathivanan S, Yang W, Freeman MR, Di Vizio D (2015b) Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles. Oncotarget 6(13):11327–11341

    Article  PubMed  PubMed Central  Google Scholar 

  • Minciacchi VR, Spinelli C, Reis-Sobreiro M, Cavallini L, You S, Zandian M, Li X, Mishra R, Chiarugi P, Adam RM, Posadas EM, Viglietto G, Freeman MR, Cocucci E, Bhowmick NA, Di Vizio D (2017) MYC mediates large Oncosome-induced fibroblast reprogramming in prostate Cancer. Cancer Res 77(9):2306–2317

    Article  CAS  PubMed  Google Scholar 

  • Mondal A, Ashiq KA, Phulpagar P, Singh DK, Shiras A (2019) Effective visualization and easy tracking of extracellular vesicles in glioma cells. Biol Proc Online 21(1):4

    Article  CAS  Google Scholar 

  • Morello M, Minciacchi VR, de Candia P, Yang J, Posadas E, Kim H, Griffiths D, Bhowmick N, Chung LW, Gandellini P, Freeman MR, Demichelis F, Di Vizio D (2013) Large oncosomes mediate intercellular transfer of functional microRNA. Cell Cycle 12(22):3526–3536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muralidharan-Chari V, Clancy J, Plou C, Romao M, Chavrier P, Raposo G, D’Souza-Schorey C (2009) ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 19(22):1875–1885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muralidharan-Chari V, Clancy JW, Sedgwick A, D’Souza-Schorey C (2010) Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 123:1603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy DE, de Jong OG, Brouwer M, Wood MJ, Lavieu G, Schiffelers RM, Vader P (2019) Extracellular vesicle-based therapeutics: natural versus engineered targeting and trafficking. Exp Mol Med 51(3):1–12

    Article  CAS  PubMed  Google Scholar 

  • Nabhan JF, Hu R, Oh RS, Cohen SN, Lu Q (2012) Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc Natl Acad Sci USA 109(11):4146–4151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nickerson DP, Russell MRG, Lo SY, Chapin HC, Milnes J, Merz AJ (2012) Termination of isoform-selective Vps21/Rab5 signaling at endolysosomal organelles by Msb3/Gyp3. Traffic 13(10):1411–1428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nojima H, Konishi T, Freeman CM, Schuster RM, Japtok L, Kleuser B, Edwards MJ, Gulbins E, Lentsch AB (2016) Chemokine receptors, CXCR1 and CXCR2, differentially regulate exosome release in hepatocytes. PLoS One 11(8):e0161443

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oppel F, Müller N, Schackert G, Hendruschk S, Martin D, Geiger KD, Temme A (2011) SOX2-RNAi attenuates S-phase entry and induces RhoA-dependent switch to protease-independent amoeboid migration in human glioma cells. Mol Cancer 10:137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oram JF, Vaughan AM (2000) ABCA1-mediated transport of cellular cholesterol and phospholipids to HDL apolipoproteins. Curr Opin Lipidol 11(3):253–260

    Article  CAS  PubMed  Google Scholar 

  • Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, Seabra MC, Darchen F, Amigorena S, Moita LF, Thery C (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12(1):19–30

    Article  CAS  PubMed  Google Scholar 

  • Paluch E, Sykes C, Prost J, Bornens M (2006) Dynamic modes of the cortical actomyosin gel during cell locomotion and division. Trends Cell Biol 16(1):5–10

    Article  CAS  PubMed  Google Scholar 

  • Pan BT, Johnstone RM (1983) Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33(3):967–978

    Article  CAS  PubMed  Google Scholar 

  • Pathan M, Fonseka P, Chitti SV, Kang T, Sanwlani R, Van Deun J, Hendrix A, Mathivanan S (2019) Vesiclepedia 2019: a compendium of RNA, proteins, lipids and metabolites in extracellular vesicles. Nucleic Acids Res 47(D1):D516–d519

    Article  CAS  PubMed  Google Scholar 

  • Perez-Hernandez D, Gutiérrez-Vázquez C, Jorge I, López-Martín S, Ursa A, Sánchez-Madrid F, Vázquez J, Yáñez-Mó M (2013) The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes. J Biol Chem 288(17):11649–11661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen SH, Odintsova E, Haigh TA, Rickinson AB, Taylor GS, Berditchevski F (2011) The role of tetraspanin CD63 in antigen presentation via MHC class II. Eur J Immunol 41(9):2556–2561

    Article  CAS  PubMed  Google Scholar 

  • Piper RC, Katzmann DJ (2007) Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol 23:519–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pornillos O, Higginson DS, Stray KM, Fisher RD, Garrus JE, Payne M, He G-P, Wang HE, Morham SG, Sundquist WI (2003) HIV gag mimics the Tsg101-recruiting activity of the human Hrs protein. J Cell Biol 162(3):425–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porter KR, Claude A, Fullam EF (1945) A study of tissue culture cells by electron microscopy: methods and preliminary observations. J Exp Med 81(3):233–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010) Identification of the switch in early-to-late endosome transition. Cell 141(3):497–508

    Article  CAS  PubMed  Google Scholar 

  • Potolicchio I, Carven GJ, Xu X, Stipp C, Riese RJ, Stern LJ, Santambrogio L (2005) Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J Immunol 175(4):2237

    Article  CAS  PubMed  Google Scholar 

  • Puri N, Roche PA (2006) Ternary SNARE complexes are enriched in lipid rafts during mast cell exocytosis. Traffic 7(11):1482–1494

    Article  CAS  PubMed  Google Scholar 

  • Qazi H, Shi Z-D, Song JW, Cancel LM, Huang P, Zeng Y, Roberge S, Munn LL, Tarbell JM (2016) Heparan sulfate proteoglycans mediate renal carcinoma metastasis. Int J Cancer 139(12):2791–2801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183(3):1161–1172

    Article  CAS  PubMed  Google Scholar 

  • Rauch S, Martin-Serrano J (2011) Multiple interactions between the ESCRT machinery and arrestin-related proteins: implications for PPXY-dependent budding. J Virol 85(7):3546–3556

    Article  CAS  PubMed  Google Scholar 

  • Richardson MM, Jennings LK, Zhang XA (2011) Tetraspanins and tumor progression. Clin Exp Metastasis 28(3):261–270

    Article  CAS  PubMed  Google Scholar 

  • Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122(5):735–749

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Boulan E, Kreitzer G, Müsch A (2005) Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 6(3):233–247

    Article  CAS  PubMed  Google Scholar 

  • Rubinstein E, Le Naour F, Lagaudrière-Gesbert C, Billard M, Conjeaud H, Boucheix C (1996) CD9, CD63, CD81, and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA integrins. Eur J Immunol 26(11):2657–2665

    Article  CAS  PubMed  Google Scholar 

  • Sakaidani Y, Nomura T, Matsuura A, Ito M, Suzuki E, Murakami K, Nadano D, Matsuda T, Furukawa K, Okajima T (2011) O-linked-N-acetylglucosamine on extracellular protein domains mediates epithelial cell–matrix interactions. Nat Commun 2(1):583

    Article  PubMed  CAS  Google Scholar 

  • Sanwlani R, Fonseka P, Chitti SV, Mathivanan S (2020) Milk-derived extracellular vesicles in inter-organism, cross-species communication and drug delivery. Proteomes 8(2)

    Google Scholar 

  • Schmidt O, Teis D (2012) The ESCRT machinery. Curr Biol 22(4):R116–R120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schöneberg J, Lee I-H, Iwasa JH, Hurley JH (2017) Reverse-topology membrane scission by the ESCRT proteins. Nat Rev Mol Cell Biol 18(1):5–17

    Article  PubMed  CAS  Google Scholar 

  • Seo MY, Rhee K (2018) Caspase-mediated cleavage of the centrosomal proteins during apoptosis. Cell Death Dis 9(5):571

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharanek A, Burban A, Burbank M, Le Guevel R, Li R, Guillouzo A, Guguen-Guillouzo C (2016) Rho-kinase/myosin light chain kinase pathway plays a key role in the impairment of bile canaliculi dynamics induced by cholestatic drugs. Sci Rep 6:24709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Son F, Umphred-Wilson K, Shim JH, Adoro S (2019) Assessment of ESCRT protein CHMP5 activity on client protein ubiquitination by immunoprecipitation and Western blotting. Methods Mol Biol 1998:219–226

    Article  CAS  PubMed  Google Scholar 

  • Ståhl A-L, Johansson K, Mossberg M, Kahn R, Karpman D (2019) Exosomes and microvesicles in normal physiology, pathophysiology, and renal diseases. Pediatr Nephrol (Berlin, Germany) 34(1):11–30

    Article  Google Scholar 

  • Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10(8):513–525

    Article  CAS  PubMed  Google Scholar 

  • Stipp CS, Kolesnikova TV, Hemler ME (2001) EWI-2 is a major CD9 and CD81 partner and member of a novel Ig protein subfamily. J Biol Chem 276(44):40545–40554

    Article  CAS  PubMed  Google Scholar 

  • Stipp CS, Kolesnikova TV, Hemler ME (2003) Functional domains in tetraspanin proteins. Trends Biochem Sci 28(2):106–112

    Article  CAS  PubMed  Google Scholar 

  • Strack B, Calistri A, Craig S, Popova E, Göttlinger HG (2003) AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114(6):689–699

    Article  CAS  PubMed  Google Scholar 

  • Stuffers S, Sem Wegner C, Stenmark H, Brech A (2009) Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic 10(7):925–937

    Article  CAS  PubMed  Google Scholar 

  • Surman M, Stępień E, Hoja-Łukowicz D, Przybyło M (2017) Deciphering the role of ectosomes in cancer development and progression: focus on the proteome. Clin Exp Metastasis 34(3):273–289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki J, Umeda M, Sims PJ, Nagata S (2010) Calcium-dependent phospholipid scrambling by TMEM16F. Nature 468(7325):834–838

    Article  CAS  PubMed  Google Scholar 

  • Suzuki J, Denning DP, Imanishi E, Horvitz HR, Nagata S (2013) Xk-related protein 8 and CED-8 promote phosphatidylserine exposure in apoptotic cells. Science 341(6144):403

    Article  CAS  PubMed  Google Scholar 

  • Svitkina T (2018) The actin cytoskeleton and actin-based motility. Cold Spring Harb Perspect Biol 10(1):a018267

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takahashi H, Mayers JR, Wang L, Edwardson JM, Audhya A (2015) Hrs and STAM function synergistically to bind ubiquitin-modified cargoes in vitro. Biophys J 108(1):76–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor AC, Robbins E (1963) Observations on microextensions from the surface of isolated vertebrate cells. Dev Biol 7:660–673

    Article  Google Scholar 

  • Teo H, Perisic O, González B, Williams RL (2004) ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Dev Cell 7(4):559–569

    Article  CAS  PubMed  Google Scholar 

  • Teo H, Gill DJ, Sun J, Perisic O, Veprintsev DB, Vallis Y, Emr SD, Williams RL (2006) ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes. Cell 125(1):99–111

    Article  CAS  PubMed  Google Scholar 

  • Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R, Antoniou A, Arab T, Archer F, Atkin-Smith GK, Ayre DC, Bach J-M, Bachurski D, Baharvand H, Balaj L, Baldacchino S, Bauer NN, Baxter AA, Bebawy M, Beckham C, Bedina Zavec A, Benmoussa A, Berardi AC, Bergese P, Bielska E, Blenkiron C, Bobis-Wozowicz S, Boilard E, Boireau W, Bongiovanni A, Borràs FE, Bosch S, Boulanger CM, Breakefield X, Breglio AM, Brennan MÁ, Brigstock DR, Brisson A, Broekman MLD, Bromberg JF, Bryl-Górecka P, Buch S, Buck AH, Burger D, Busatto S, Buschmann D, Bussolati B, Buzás EI, Byrd JB, Camussi G, Carter DRF, Caruso S, Chamley LW, Chang Y-T, Chen C, Chen S, Cheng L, Chin AR, Clayton A, Clerici SP, Cocks A, Cocucci E, Coffey RJ, Cordeiro-da-Silva A, Couch Y, Coumans FAW, Coyle B, Crescitelli R, Criado MF, D’Souza-Schorey C, Das S, Datta Chaudhuri A, de Candia P, De Santana EF, De Wever O, del Portillo HA, Demaret T, Deville S, Devitt A, Dhondt B, Di Vizio D, Dieterich LC, Dolo V, Dominguez Rubio AP, Dominici M, Dourado MR, Driedonks TAP, Duarte FV, Duncan HM, Eichenberger RM, Ekström K, El Andaloussi S, Elie-Caille C, Erdbrügger U, Falcón-Pérez JM, Fatima F, Fish JE, Flores-Bellver M, Försönits A, Frelet-Barrand A, Fricke F, Fuhrmann G, Gabrielsson S, Gámez-Valero A, Gardiner C, Gärtner K, Gaudin R, Gho YS, Giebel B, Gilbert C, Gimona M, Giusti I, Goberdhan DCI, Görgens A, Gorski SM, Greening DW, Gross JC, Gualerzi A, Gupta GN, Gustafson D, Handberg A, Haraszti RA, Harrison P, Hegyesi H, Hendrix A, Hill AF, Hochberg FH, Hoffmann KF, Holder B, Holthofer H, Hosseinkhani B, Hu G, Huang Y, Huber V, Hunt S, Ibrahim AG-E, Ikezu T, Inal JM, Isin M, Ivanova A, Jackson HK, Jacobsen S, Jay SM, Jayachandran M, Jenster G, Jiang L, Johnson SM, Jones JC, Jong A, Jovanovic-Talisman T, Jung S, Kalluri R, Kano S-i, Kaur S, Kawamura Y, Keller ET, Khamari D, Khomyakova E, Khvorova A, Kierulf P, Kim KP, Kislinger T, Klingeborn M, Klinke DJ, Kornek M, Kosanović MM, Kovács ÁF, Krämer-Albers E-M, Krasemann S, Krause M, Kurochkin IV, Kusuma GD, Kuypers S, Laitinen S, Langevin SM, Languino LR, Lannigan J, Lässer C, Laurent LC, Lavieu G, Lázaro-Ibáñez E, Le Lay S, Lee M-S, Lee YXF, Lemos DS, Lenassi M, Leszczynska A, Li ITS, Liao K, Libregts SF, Ligeti E, Lim R, Lim SK, Linē A, Linnemannstöns K, Llorente A, Lombard CA, Lorenowicz MJ, Lörincz ÁM, Lötvall J, Lovett J, Lowry MC, Loyer X, Lu Q, Lukomska B, Lunavat TR, Maas SLN, Malhi H, Marcilla A, Mariani J, Mariscal J, Martens-Uzunova ES, Martin-Jaular L, Martinez MC, Martins VR, Mathieu M, Mathivanan S, Maugeri M, McGinnis LK, McVey MJ, Meckes DG, Meehan KL, Mertens I, Minciacchi VR, Möller A, Møller Jørgensen M, Morales-Kastresana A, Morhayim J, Mullier F, Muraca M, Musante L, Mussack V, Muth DC, Myburgh KH, Najrana T, Nawaz M, Nazarenko I, Nejsum P, Neri C, Neri T, Nieuwland R, Nimrichter L, Nolan JP, Nolte-‘t Hoen ENM, Noren Hooten N, O’Driscoll L, O’Grady T, O’Loghlen A, Ochiya T, Olivier M, Ortiz A, Ortiz LA, Osteikoetxea X, Østergaard O, Ostrowski M, Park J, Pegtel DM, Peinado H, Perut F, Pfaffl MW, Phinney DG, Pieters BCH, Pink RC, Pisetsky DS, Pogge von Strandmann E, Polakovicova I, Poon IKH, Powell BH, Prada I, Pulliam L, Quesenberry P, Radeghieri A, Raffai RL, Raimondo S, Rak J, Ramirez MI, Raposo G, Rayyan MS, Regev-Rudzki N, Ricklefs FL, Robbins PD, Roberts DD, Rodrigues SC, Rohde E, Rome S, Rouschop KMA, Rughetti A, Russell AE, Saá P, Sahoo S, Salas-Huenuleo E, Sánchez C, Saugstad JA, Saul MJ, Schiffelers RM, Schneider R, Schøyen TH, Scott A, Shahaj E, Sharma S, Shatnyeva O, Shekari F, Shelke GV, Shetty AK, Shiba K, Siljander PRM, Silva AM, Skowronek A, Snyder OL, Soares RP, Sódar BW, Soekmadji C, Sotillo J, Stahl PD, Stoorvogel W, Stott SL, Strasser EF, Swift S, Tahara H, Tewari M, Timms K, Tiwari S, Tixeira R, Tkach M, Toh WS, Tomasini R, Torrecilhas AC, Tosar JP, Toxavidis V, Urbanelli L, Vader P, van Balkom BWM, van der Grein SG, Van Deun J, van Herwijnen MJC, Van Keuren-Jensen K, van Niel G, van Royen ME, van Wijnen AJ, Vasconcelos MH, Vechetti IJ, Veit TD, Vella LJ, Velot É, Verweij FJ, Vestad B, Viñas JL, Visnovitz T, Vukman KV, Wahlgren J, Watson DC, Wauben MHM, Weaver A, Webber JP, Weber V, Wehman AM, Weiss DJ, Welsh JA, Wendt S, Wheelock AM, Wiener Z, Witte L, Wolfram J, Xagorari A, Xander P, Xu J, Yan X, Yáñez-Mó M, Yin H, Yuana Y, Zappulli V, Zarubova J, Žėkas V, Zhang J-y, Zhao Z, Zheng L, Zheutlin AR, Zickler AM, Zimmermann P, Zivkovic AM, Zocco D, Zuba-Surma EK (2018) 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 7(1):1535750

    Article  PubMed  PubMed Central  Google Scholar 

  • Tomasoni S, Longaretti L, Rota C, Morigi M, Conti S, Gotti E, Capelli C, Introna M, Remuzzi G, Benigni A (2013) Transfer of growth factor receptor mRNA via exosomes unravels the regenerative effect of mesenchymal stem cells. Stem Cells Dev 22(5):772–780

    Article  CAS  PubMed  Google Scholar 

  • Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brugger B, Simons M (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319(5867):1244–1247

    Article  CAS  PubMed  Google Scholar 

  • Tu Y, Zhao L, Billadeau DD, Jia D (2020) Endosome-to-TGN trafficking: organelle-vesicle and organelle-organelle interactions. Front Cell Dev Biol 8:163–163

    Article  PubMed  PubMed Central  Google Scholar 

  • Upadhya D, Shetty AK (2019) Extracellular vesicles as therapeutics for brain injury and disease. Curr Pharm Des 25(33):3500–3505

    Article  CAS  PubMed  Google Scholar 

  • van Niel G, Charrin S, Simoes S, Romao M, Rochin L, Saftig P, Marks MS, Rubinstein E, Raposo G (2011) The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev Cell 21(4):708–721

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Villarroya-Beltri C, Baixauli F, Gutiérrez-Vázquez C, Sánchez-Madrid F, Mittelbrunn M (2014) Sorting it out: regulation of exosome loading. Semin Cancer Biol 28:3–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei Y, Wang D, Jin F, Bian Z, Li L, Liang H, Li M, Shi L, Pan C, Zhu D, Chen X, Hu G, Liu Y, Zhang C-Y, Zen K (2017) Pyruvate kinase type M2 promotes tumour cell exosome release via phosphorylating synaptosome-associated protein 23. Nat Commun 8(1):14041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wickman GR, Julian L, Mardilovich K, Schumacher S, Munro J, Rath N, Zander SA, Mleczak A, Sumpton D, Morrice N, Bienvenut WV, Olson MF (2013) Blebs produced by actin–myosin contraction during apoptosis release damage-associated molecular pattern proteins before secondary necrosis occurs. Cell Death Diff 20(10):1293–1305

    Article  CAS  Google Scholar 

  • Wilkinson S, Paterson HF, Marshall CJ (2005) Cdc42-MRCK and Rho-ROCK signalling cooperate in myosin phosphorylation and cell invasion. Nat Cell Biol 7(3):255–261

    Article  CAS  PubMed  Google Scholar 

  • Wollert T, Hurley JH (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464(7290):864–869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH (2009) Membrane scission by the ESCRT-III complex. Nature 458(7235):172–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu D, Xu Y, Ding T, Zu Y, Yang C, Yu L (2017) Pairing of integrins with ECM proteins determines migrasome formation. Cell Res 27(11):1397–1400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Lai Y, Hua Z-C (2019) Apoptosis and apoptotic body: disease message and therapeutic target potentials. Biosci Rep 39(1):BSR20180992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yáñez-Mó M, Barreiro O, Gordon-Alonso M, Sala-Valdés M, Sánchez-Madrid F (2009) Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 19(9):434–446

    Article  PubMed  CAS  Google Scholar 

  • Yáñez-Mó M, Gutiérrez-López MD, Cabañas C (2011) Functional interplay between tetraspanins and proteases. Cell Mol Life Sci 68(20):3323–3335

    Article  PubMed  CAS  Google Scholar 

  • Yang D, Hurley JH (2010) Structural role of the Vps4-Vta1 interface in ESCRT-III recycling. Structure (London, England: 1993) 18(8):976–984

    Article  CAS  Google Scholar 

  • Yang L, Peng X, Li Y, Zhang X, Ma Y, Wu C, Fan Q, Wei S, Li H, Liu J (2019) Long non-coding RNA HOTAIR promotes exosome secretion by regulating RAB35 and SNAP23 in hepatocellular carcinoma. Mol Cancer 18(1):78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuana Y, Sturk A, Nieuwland R (2013) Extracellular vesicles in physiological and pathological conditions. Blood Rev 27(1):31–39

    Article  CAS  PubMed  Google Scholar 

  • Zacks MA, Garg N (2006) Recent developments in the molecular, biochemical and functional characterization of GPI8 and the GPI-anchoring mechanism [review]. Mol Membr Biol 23(3):209–225

    Article  PubMed  CAS  Google Scholar 

  • Zappulli V, Friis KP, Fitzpatrick Z, Maguire CA, Breakefield XO (2016) Extracellular vesicles and intercellular communication within the nervous system. J Clin Invest 126(4):1198–1207

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Michaelson JE, Moshiach S, Sachs N, Zhao W, Sun Y, Sonnenberg A, Lahti JM, Huang H, Zhang XA (2011) Tetraspanin CD151 maintains vascular stability by balancing the forces of cell adhesion and cytoskeletal tension. Blood 118(15):4274–4284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Freitas D, Kim HS, Fabijanic K, Li Z, Chen H, Mark MT, Molina H, Martin AB, Bojmar L, Fang J, Rampersaud S, Hoshino A, Matei I, Kenific CM, Nakajima M, Mutvei AP, Sansone P, Buehring W, Wang H, Jimenez JP, Cohen-Gould L, Paknejad N, Brendel M, Manova-Todorova K, Magalhães A, Ferreira JA, Osório H, Silva AM, Massey A, Cubillos-Ruiz JR, Galletti G, Giannakakou P, Cuervo AM, Blenis J, Schwartz R, Brady MS, Peinado H, Bromberg J, Matsui H, Reis CA, Lyden D (2018) Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation. Nat Cell Biol 20(3):332–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Higginbotham JN, Jeppesen DK, Yang Y-P, Li W, McKinley ET, Graves-Deal R, Ping J, Britain CM, Dorsett KA, Hartman CL, Ford DA, Allen RM, Vickers KC, Liu Q, Franklin JL, Bellis SL, Coffey RJ (2019) Transfer of functional cargo in exomeres. Cell Reports 27(3):940–954.e946

    Article  CAS  PubMed  Google Scholar 

  • Zhao K, Bleackley M, Chisanga D, Gangoda L, Fonseka P, Liem M, Kalra H, Al Saffar H, Keerthikumar S, Ang CS, Adda CG, Jiang L, Yap K, Poon IK, Lock P, Bulone V, Anderson M, Mathivanan S (2019a) Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling. Commun Biol 2:305

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao X, Lei Y, Zheng J, Peng J, Li Y, Yu L, Chen Y (2019b) Identification of markers for migrasome detection. Cell Discov 5:27–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Q, Yamakuchi M, Lowenstein CJ (2015) SNAP23 regulates endothelial exocytosis of von Willebrand Factor. PLoS One 10(8):e0118737

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, Ricciardi-Castagnoli P, Raposo G, Amigorena S (1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell derived exosomes. Nat Med 4(5):594–600

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry and Genetics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Victoria, Australia

    Taeyoung Kang, Ishara Atukorala & Suresh Mathivanan

Authors
  1. Taeyoung Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ishara Atukorala
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suresh Mathivanan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suresh Mathivanan .

Editor information

Editors and Affiliations

  1. Department of Biochemistry and Genetics La Trobe Institute for Molecular Science, La Trobe University, Melbourne, VIC, Australia

    Suresh Mathivanan

  2. Department of Biochemistry and Genetics La Trobe Institute for Molecular Science, La Trobe University, Melbourne, VIC, Australia

    Pamali Fonseka

  3. Department of Biochemistry and Genetics La Trobe Institute for Molecular Science, La Trobe University, Melbourne, VIC, Australia

    Christina Nedeva

  4. Department of Biochemistry and Genetics La Trobe Institute for Molecular Science, La Trobe University, Melbourne, VIC, Australia

    Ishara Atukorala

Rights and permissions

Reprints and permissions

Copyright information

© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kang, T., Atukorala, I., Mathivanan, S. (2021). Biogenesis of Extracellular Vesicles. In: Mathivanan, S., Fonseka, P., Nedeva, C., Atukorala, I. (eds) New Frontiers: Extracellular Vesicles. Subcellular Biochemistry, vol 97. Springer, Cham. https://doi.org/10.1007/978-3-030-67171-6_2

Download citation

Publish with us

Policies and ethics

Search

Navigation