Exosomes purified from a single cell type have diverse morphology

Journal of Extracellular Vesicles

Volumn 6, Issue 1, 2017, Pages

  Zabeo, Davide ^a   Cvjetkovic, Aleksander ^a   Lässer, Cecilia ^a   Schorb, Martin ^b   Lötvall, Jan ^a   Höög, Johanna L ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Cryo electron microscopy; density gradient; extracellular vesicles; HMC 1; multivesicular bodies; spikes

Indexed keywords

ARTICLE; BIODIVERSITY; BODY FLUID; CELL COMMUNICATION; CELL FUNCTION; CELL ISOLATION; CELL STRUCTURE; CELL SUBPOPULATION; CELL VACUOLE; CELL VIABILITY; CELLULAR DISTRIBUTION; CLASSIFICATION; COATED VESICLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; DOUBLE VESICLE; ELECTRON DENSE VESICLE; EXOSOME; HMC-1 CELL LINE; HUMAN; HUMAN CELL; INCOMPLETE VESICLE; LARGE TUBULE; MORPHOLOGICAL TRAIT; OVAL VESICLE; PLEOMORPHIC VESICLE; PURIFICATION; SINGLE CELL ANALYSIS; SINGLE VESICLE; SMALL DOUBLE VESICLE; SMALL TUBULE; TRIPLE VESICLE;

EID: 85035133358     PISSN: None     EISSN: 20013078     Source Type: Journal    
DOI: 10.1080/20013078.2017.1329476     Document Type: Article

References (55)

1. Brown L, Wolf JM, Prados-Rosales R, et al. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat Rev Microbiol. 2015;13(10):1–11.
2. Schwechheimer C, Kuehn MJ., Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol. 2015;13(10):605–619.
3. Colombo M, Raposo G, Thery C., Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255–289.
4. An Q, Van Bel AJ, Huckelhoven R. Do plant cells secrete exosomes derived from multivesicular bodies? Plant Signal Behav. 2007;2(1):4–7.
5. Stanly C, Fiume I, Capasso G, et al. Isolation of exosome-like vesicles from plants by ultracentrifugation on sucrose/deuterium oxide (D2O) density cushions. Methods Mol Biol. 2016;1459:259–269.
6. Valadi H, Ekstrom 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.
7. Greening DW, Gopal SK, Mathias RA, et al. Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Semin Cell Dev Biol. 2015;40:60–71.
8. Abd Elmageed ZY, Yang Y, Thomas R, et al. Neoplastic reprogramming of patient-derived adipose stem cells by prostate cancer cell-associated exosomes. Stem Cells. 2014;32(4):983–997.
9. Sung BH, Ketova T, Hoshino D, et al. Directional cell movement through tissues is controlled by exosome secretion. Nat Commun. 2015;6:7164.
10. Al-Nedawi K, Meehan B, Micallef J, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008;10(5):619–624.
11. Yuana Y, Koning RI, Kuil ME, et al. Cryo-electron microscopy of extracellular vesicles in fresh plasma. J Extracell Vesicles. 2013;2:21494.
12. Arraud N, Linares R, Tan S, et al. Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thromb Haemost. 2014;12(5):614–627.
13. Zonneveld MI, Brisson AR, Van Herwijnen MJ, et al. Recovery of extracellular vesicles from human breast milk is influenced by sample collection and vesicle isolation procedures. J Extracell Vesicles. 2014;3:24215.
14. Lasser C, Alikhani VS, Ekstrom K, et al. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J Transl Med. 2011;9:9.
15. Hoog JL, Lotvall J. Diversity of extracellular vesicles in human ejaculates revealed by cryo-electron microscopy. J Extracell Vesicles. 2015;4:28680.
16. Poliakov A, Spilman M, Dokland T, et al. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate. 2009;69(2):159–167.
17. Ronquist G, Brody I, Gottfries A, et al. An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid: part I. Andrologia. 1978;10(4):261–272.
18. Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164(6):1226–1232.
19. Taylor DD, Homesley HD, Doellgast GJ. Binding of specific peroxidase-labeled antibody to placental-type phosphatase on tumor-derived membrane fragments. Cancer Res. 1980;40(11):4064–4069.
20. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373–383.
21. Crescitelli R, Lasser C, Szabo TG, et al. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles. 2013;2:20677.
22. Hanson PI, Cashikar A. Multivesicular body morphogenesis. Annu Rev Cell Dev Biol. 2012;28:337–362.
23. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol. 1983;97(2):329–339.
24. Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183(3):1161–1172.
25. Gardiner C, Di Vizio D, Sahoo S, et al. Techniques used for the isolation and characterization of extracellular vesicles: results of a worldwide survey. J Extracell Vesicles. 2016;5:32945.
26. Momen-Heravi F, Balaj L, Alian S, et al. Current methods for the isolation of extracellular vesicles. Biol Chem. 2013;394(10):1253–1262.
27. Thery C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;Chapter 3:Unit 3 22.
28. Brenner S, Horne RW. A negative staining method for high resolution electron microscopy of viruses. Biochim Biophys Acta. 1959;34:103–110.
29. Coleman BM, Hanssen E, Lawson VA, et al. Prion-infected cells regulate the release of exosomes with distinct ultrastructural features. Faseb J. 2012;26(10):4160–4173.
30. Bosch S, De Beaurepaire L, Allard M, et al. Trehalose prevents aggregation of exosomes and cryodamage. Sci Rep. 2016;6:36162.
31. Van Niel G, Bergam P, Di Cicco A, et al. Apolipoprotein E regulates amyloid formation within endosomes of pigment cells. Cell Rep. 2015;13(1):43–51.
32. Shelke GV, Lasser C, Gho YS, et al. Importance of exosome depletion protocols to eliminate functional and RNA-containing extracellular vesicles from fetal bovine serum. J Extracell Vesicles. 2014;3:24783.
33. Cvjetkovic A, Lotvall J, Lasser C. The influence of rotor type and centrifugation time on the yield and purity of extracellular vesicles. J Extracell Vesicles. 2014;3:23111.
34. Perktold A, Zechmann B, Daum G, et al. Organelle association visualized by three-dimensional ultrastructural imaging of the yeast cell. FEMS Yeast Res. 2007;7(4):629–638.
35. McDowall AW, Smith JM, Dubochet J. Cryo-electron microscopy of vitrified chromosomes in situ. Embo J. 1986;5(6):1395–1402.
36. Hoog JL, Lacomble S, O’Toole ET, et al. Modes of flagellar assembly in Chlamydomonas reinhardtii and Trypanosoma brucei. Elife. 2014;3:e01479.
37. Dubochet J, Sartori Blanc N. The cell in absence of aggregation artifacts. Micron. 2001;32(1):91–99.
38. Hoog JL, Lacomble S, Bouchet-Marquis C, et al. 3D architecture of the trypanosoma brucei flagella connector, a mobile transmembrane junction. Plos Negl Trop Dis. 2016;10(1):e0004312.
39. Hoog JL, Gluenz E, Vaughan S, et al. Ultrastructural investigation methods for Trypanosoma brucei. Methods Cell Biol. 2010;96:175–196.
40. Hawes P, Netherton, CL, Mueller M, et al. Rapid freeze-substitution preserves membranes in high-pressure frozen tissue culture cells. J Microsc. 2007;226(Pt 2):182–189.
41. Dubochet J, Adrian M, Chang, JJ, et al. Cryo-electron microscopy of vitrified specimens. Q Rev Biophys. 1988;21(2):129–228.
42. Orlov I, Myasnikov, AG, Andronov L, et al. The integrative role of cryo electron microscopy in molecular and cellular structural biology. Biol Cell. 2017;109(2):81–93.
43. Kremer, JR, Mastronarde, DN, McIntosh, JR. Computer visualization of three-dimensional image data using IMOD. J Struct Biol. 1996;116(1):71–76.
44. Zeev-Ben-Mordehai T, Vasishtan D, Siebert, CA, et al. The full-length cell-cell fusogen EFF-1 is monomeric and upright on the membrane. Nat Commun. 2014;5:3912.
45. Lasser C, Shelke, GV, Yeri A, et al. Two distinct extracellular RNA signatures released by a single cell type identified by microarray and next-generation sequencing. RNA Biol. 2017;14(1):58–72.
46. Baranyai T, Herczeg K, Onodi Z, et al. Isolation of exosomes from blood plasma: qualitative and quantitative comparison of ultracentrifugation and size exclusion chromatography methods. Plos One. 2015;10(12):e0145686.
47. Wernersson S, Pejler G. Mast cell secretory granules: armed for battle. Nat Rev Immunol. 2014;14(7):478–494.
48. Henningsson F, Hergeth S, Cortelius R, et al. A role for serglycin proteoglycan in granular retention and processing of mast cell secretory granule components. Febs J. 2006;273(21):4901–4912.
49. Butterfield, JH, Weiler D, Dewald G, et al. Establishment of an immature mast cell line from a patient with mast cell leukemia. Leuk Res. 1988;12(4):345–355.
50. Rohlich P, Anderson P, Uvnas B. Electron microscope observations on compounds 48-80-induced degranulation in rat mast cells. Evidence for sequential exocytosis of storage granules. J Cell Biol. 1971;51(21):465–483.
51. Meyer, GK, Neetz A, Brandes G, et al. Clostridium difficile toxins A and B directly stimulate human mast cells. Infect Immun. 2007;75(8):3868–3876.
52. Balletta A, Lorenz D, Rummel A, et al. Human mast cell line-1 (HMC-1) cells exhibit a membrane capacitance increase when dialysed with high free-Ca(2+) and GTPgammaS containing intracellular solution. Eur J Pharmacol. 2013;720(1–3):227–236.
53. Frost A, Perera R, Roux A, et al. Structural basis of membrane invagination by F-BAR domains. Cell. 2008;132(5):807–817.
54. McMahon, HT, Gallop, JL. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature. 2005;438(7068):590–596.
55. Ford, MG, Mills, IG, Peter, BJ, et al. Curvature of clathrin-coated pits driven by epsin. Nature. 2002;419(6905):361–366.