A review of exosome separation techniques and characterization of B16-F10 mouse melanoma exosomes with AF4-UV-MALS-DLS-TEM

Analytical and Bioanalytical Chemistry

Volumn 406, Issue 30, 2014, Pages 7855-7866

  Petersen, Kevin E ^a   Manangon, Eliana ^b   Hood, Joshua L ^c   Wickline, Samuel A ^c   Fernandez, Diego P ^b   Johnson, William P ^b   Gale, Bruce K ^a  

^a Department of Electrical and Computer Engineering   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Dynamic light scattering; Exosomes; Field flow fractionation; Multi angle light scattering; Separation

Indexed keywords

CELL CULTURE; DERMATOLOGY; DISEASES; DYNAMIC LIGHT SCATTERING; FRACTIONATION; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; LIGHT TRANSMISSION; LIQUID CHROMATOGRAPHY; ONCOLOGY; SEPARATION; TRANSMISSIONS;

CANCER; EXOSOMES; FIELD FLOW FRACTIONATION; FLOW FIELD FLOW FRACTIONATIONS; MULTI-ANGLE LIGHT SCATTERINGS; SEPARATION AND CHARACTERIZATIONS; TRANSMISSION ELECTRON MICROGRAPH; ULTRAVIOLET ABSORBANCE;

SIZE SEPARATION;

ANIMAL; EXOSOME; FIELD FLOW FRACTIONATION; LIGHT; MELANOMA; MOUSE; PATHOLOGY; PROCEDURES; RADIATION SCATTERING; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE; ULTRAVIOLET SPECTROPHOTOMETRY;

ANIMALS; CELL LINE, TUMOR; EXOSOMES; FRACTIONATION, FIELD FLOW; LIGHT; MELANOMA; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; SCATTERING, RADIATION; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 84914153712     PISSN: 16182642     EISSN: 16182650     Source Type: Journal    
DOI: 10.1007/s00216-014-8040-0     Document Type: Article

References (55)

1. Schorey JS, Bhatnagar S (2008) Exosome function: from tumor immunology to pathogen biology. Traffic (Copenhagen, Denmark) 9(6):871-881. doi: 10.1111/j.1600-0854.2008.00734.x
2. Hood JL, Wickline SA (2012) A systematic approach to exosome-based translational nanomedicine. Wiley Interdiscip Rev Nanomed Nanobiotechnol 4(4):458-467. doi: 10.1002/wnan.1174
3. D'Souza-Schorey C, Clancy JW (2012) Tumor-derived microvesicles: shedding light on novel microenvironment modulators and prospective cancer biomarkers. Genes Dev 26(12):1287-1299. doi: 10.1101/gad.192351.112
4. Thery C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9(8):581-593. doi: 10.1038/nri2567
5. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, Garcia-Santos G, Ghajar C, Nitadori-Hoshino A, Hoffman C, Badal K, Garcia BA, Callahan MK, Yuan J, Martins VR, Skog J, Kaplan RN, Brady MS, Wolchok JD, Chapman PB, Kang Y, Bromberg J, Lyden D (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18(6):883-891. doi: 10.1038/nm.2753
6. Sokolova V, Ludwig AK, Hornung S, Rotan O, Horn PA, Epple M, Giebel B (2011) Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surf B Biointerfaces 87(1):146-150. doi: 10.1016/j.colsurfb.2011.05.013
7. Gyorgy B, Szabo TG, Pasztoi M, Pal Z, Misjak P, Aradi B, Laszlo V, Pallinger E, Pap E, Kittel A, Nagy G, Falus A, Buzas EI (2011) Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci: CMLS 68(16):2667-2688. doi: 10.1007/s00018-011-0689-3
8. van der Pol E, Boing AN, Harrison P, Sturk A, Nieuwland R (2012) Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev 64(3):676-705. doi: 10.1124/pr.112.005983
9. Hood JL, Pan H, Lanza GM, Wickline SA (2009) Paracrine induction of endothelium by tumor exosomes. Lab Investig; J Technical Methods and Pathology 89(11):1317-1328. doi: 10.1038/labinvest.2009.94
10. Weitz DA Dynamic Light Scattering (QLS, PCS). http://weitzlab.seas.harvard.edu/links/tutorials/dynamiclightscattering.pdf. Accessed 24 Apr 2014
11. Bobrie A, Colombo M, Raposo G, Thery C (2011) Exosome secretion: molecular mechanisms and roles in immune responses. Traffic (Copenhagen, Denmark) 12(12):1659-1668. doi: 10.1111/j.1600-0854.2011.01225.x
12. van der Pol E, Hoekstra AG, Sturk A, Otto C, van Leeuwen TG, Nieuwland R (2010) Optical and non-optical methods for detection and characterization of microparticles and exosomes. J Thromb Haemost: JTH 8(12):2596-2607. doi: 10.1111/j.1538-7836.2010.04074.x
13. Hood JL, San RS, Wickline SA (2011) Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 71(11):3792-3801. doi: 10.1158/0008-5472.can-10-4455
14. MuDie;ller G (2012) Novel tools for the study of cell type-specific exosomes and microvesicles. J Bioanal Biomed 4(4):46-60. doi: 10.4172/1948-593X.1000063
15. Hood JL, Scott MJ, Wickline SA (2013) Maximizing exosome colloidal stability following electroporation. Anal Biochem 448C:41-49. doi: 10.1016/j.ab.2013.12.001
16. 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
17. Carayon K, Chaoui K, Ronzier E, Lazar I, Bertrand-Michel J, Roques V, Balor S, Terce F, Lopez A, Salome L, Joly E (2011) Proteolipidic composition of exosomes changes during reticulocyte maturation. J Biol Chem 286(39):34426-34439. doi: 10.1074/jbc.M111.257444
18. 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. doi: 10.1038/ncb1725
19. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10(12):1470-1476. doi: 10.1038/ncb1800
20. Safaei R, Larson BJ, Cheng TC, Gibson MA, Otani S, Naerdemann W, Howell SB (2005) Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol Cancer Ther 4(10):1595-1604. doi: 10.1158/1535-7163.mct-05-0102
21. Mathivanan S, Simpson RJ (2009) ExoCarta: a compendium of exosomal proteins and RNA. Proteomics 9(21):4997-5000. doi: 10.1002/pmic.200900351
22. Mathivanan S, Fahner CJ, Reid GE, Simpson RJ (2012) ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res 40(Database issue):D1241-D1244. doi: 10.1093/nar/gkr828
23. Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P, Bond VC, Borras FE, Breakefield X, Budnik V, Buzas E, Camussi G, Clayton A, Cocucci E, Falcon-Perez JM, Gabrielsson S, Gho YS, Gupta D, Harsha HC, Hendrix A, Hill AF, Inal JM, Jenster G, Kramer-Albers EM, Lim SK, Llorente A, Lotvall J, Marcilla A, Mincheva-Nilsson L, Nazarenko I, Nieuwland R, Nolte-'t Hoen EN, Pandey A, Patel T, Piper MG, Pluchino S, Prasad TS, Rajendran L, Raposo G, Record M, Reid GE, Sanchez-Madrid F, Schiffelers RM, Siljander P, Stensballe A, Stoorvogel W, Taylor D, Thery C, Valadi H, van Balkom BW, Vazquez J, Vidal M, Wauben MH, Yanez-Mo M, Zoeller M, Mathivanan S (2012) Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol 10(12):e1001450. doi: 10.1371/journal.pbio.1001450
24. Thery C, Amigorena S, Raposo G, Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Current protocols in cell biology//editorial board, Juan S Bonifacino [et al.] Chapter 3:Unit 3.22. doi: 10.1002/0471143030.cb0322s30
25. Taylor D, Zacharias W, Gercel-Taylor C (2011) Exosome Isolation for Proteomic Analyses and RNA Profiling. In: Simpson RJ, Greening DW (eds) Serum/Plasma Proteomics, vol 728. Methods in Molecular Biology. Humana, pp 235-246. doi: 10.1007/978-1-61779-068-3-15
26. Chen C, Skog J, Hsu CH, Lessard RT, Balaj L, Wurdinger T, Carter BS, Breakefield XO, Toner M, Irimia D (2010) Microfluidic isolation and transcriptome analysis of serum microvesicles. Lab Chip 10(4):505-511. doi: 10.1039/b916199f
27. Raj DAA, Fiume I, Capasso G, Pocsfalvi G (2012) Urinary exosomes for protein biomarker research. In: Man TK, Prof (ed) Proteomics - human diseases and protein functions. In Tech, pp 49-64
28. Lesieur S, Grabielle-Madelmont C, Paternostre M, Ollivon M (1993) Study of size distribution and stability of liposomes by high performance gel exclusion chromatography. Chem Phys Lipids 64(1):57-82
29. Ruysschaert T, Marque A, Duteyrat JL, Lesieur S, Winterhalter M, Fournier D (2005) Liposome retention in size exclusion chromatography. BMC Biotechnol 5:11. doi: 10.1186/1472-6750-5-11
30. Ingebrigtsen L, Brandl M (2002) Determination of the size distribution of liposomes by SEC fractionation, and PCS analysis and enzymatic assay of lipid content. AAPS PharmSciTech 3(2):E7. doi: 10.1208/pt030207
31. Lai RC, Arslan F, Lee MM, Sze NS, Choo A, Chen TS, Salto-Tellez M, Timmers L, Lee CN, El Oakley RM, Pasterkamp G, de Kleijn DP, Lim SK (2010) Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res 4(3):214-222. doi: 10.1016/j.scr.2009.12.003
32. Oshima K, Aoki N, Kato T, Kitajima K, Matsuda T (2002) Secretion of a peripheral membrane protein, MFG-E8, as a complex with membrane vesicles. Eur J Biochem FEBS 269(4):1209-1218
33. Chen TS, Arslan F, Yin Y, Tan SS, Lai RC, Choo AB, Padmanabhan J, Lee CN, de Kleijn DP, Lim SK (2011) Enabling a robust scalable manufacturing process for therapeutic exosomes through oncogenic immortalization of human ESC-derived MSCs. J Transl Med 9:47. doi: 10.1186/1479-5876-9-47
34. Rekker K, Saare M, Roost AM, Kubo AL, Zarovni N, Chiesi A, Salumets A, Peters M (2014) Comparison of serum exosome isolation methods for microRNA profiling. Clin Biochem 47(1-2):135-138. doi: 10.1016/j.clinbiochem.2013.10.020
35. Yamada T, Inoshima Y, Matsuda T, Ishiguro N (2012) Comparison of methods for isolating exosomes from bovine milk. J Vet Med Sci///Japanese Society of Veterinary Science 74(11):1523-1525
36. Cheruvanky A, Zhou H, Pisitkun T, Kopp JB, Knepper MA, Yuen PS, Star RA (2007) Rapid isolation of urinary exosomal biomarkers using a nanomembrane ultrafiltration concentrator. Am J Physiol Renal Physiol 292(5):F1657-F1661. doi: 10.1152/ajprenal.00434.2006
37. Merchant ML, Powell DW, Wilkey DW, Cummins TD, Deegens JK, Rood IM, McAfee KJ, Fleischer C, Klein E, Klein JB (2010) Microfiltration isolation of human urinary exosomes for characterization by MS. Proteomics Clin Appl 4(1):84-96. doi: 10.1002/prca.200800093
38. Oh S, Kang D, Ahn SM, Simpson RJ, Lee BH, Moon MH (2007) Miniaturized asymmetrical flow field-flow fractionation: application to biological vesicles. J Sep Sci 30(7):1082-1087
39. Kang D, Oh S, Ahn S-M, Lee B-H, Moon MH (2008) Proteomic analysis of exosomes from human neural stem cells by flow field-flow fractionation and nanoflow liquid chromatography-tandem mass spectrometry. J Proteome Res 7(8):3475-3480
40. Lasser C, Eldh M, Lotvall J (2012) Isolation and characterization of RNA-containing exosomes. J Visualized Experiments: JoVE 59:e3037. doi: 10.3791/3037
41. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9(6):654-659. doi: 10.1038/ncb1596
42. Jorgensen M, Baek R, Pedersen S, Sondergaard EK, Kristensen SR, Varming K (2013) Extracellular Vesicle (EV) Array: microarray capturing of exosomes and other extracellular vesicles for multiplexed phenotyping. J Extracellular Vesicles 2. doi: 10.3402/jev.v2i0.20920
43. Tauro BJ, Greening DW, Mathias RA, Ji H, Mathivanan S, Scott AM, Simpson RJ (2012) Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods (San Diego, Calif) 56(2):293-304. doi: 10.1016/j.ymeth.2012.01.002
44. Wahlund KG, Giddings JC (1987) Properties of an asymmetrical flow field-flow fractionation channel having one permeable wall. Anal Chem 59(9):1332-1339
45. Qureshi RN, Kok WT (2011) Application of flow field-flow fractionation for the characterization of macromolecules of biological interest: a review. Anal Bioanal Chem 399(4):1401-1411. doi: 10.1007/s00216-010-4278-3
46. Korgel BA, van Zanten JH, Monbouquette HG (1998) Vesicle size distributions measured by flow field-flow fractionation coupled with multiangle light scattering. Biophys J 74(6):3264-3272. doi: 10.1016/s0006-3495(98)78033-6
47. Paulaitis M, Guzman N, Agarwal K, Saji M (2010) Poster Session 3 - tumor cell and molecular biology: MicroRNAs Abstract P3-09-04: exosome-specific microRNA signatures in combination with characteristic surface markers on the circulating exosomes themselves provide new insights in the EMT. Cancer Res 70 (24). doi: 10.1158/0008-5472.SABCS10-P3-09-04
48. Roda B, Zattoni A, Reschiglian P, Moon MH, Mirasoli M, Michelini E, Roda A (2009) Field-flow fractionation in bioanalysis: a review of recent trends. Anal Chim Acta 635(2):132-143. doi: 10.1016/j.aca.2009.01.015
49. Mitrus I, Bryndza E, Kazura M, Smagur A, Sochanik A, Cichon T, Szala S (2012) Properties of B16-F10 murine melanoma cells subjected to metabolic stress conditions. Acta Biochim Pol 59(3):363-366
50. Wyatt Technology Corporation (2010) DYNAMICS User's Guide. In., Version 7.1 (M1400 Rev. K) edn., pp Ch8-8, Appendix A
51. Wyatt Technology Corporation (2008) Astra V User's Guide. In, vol Version 5.3.4 (M1000 Rev. H). pp Appendix D-F
52. Belnap D (2013) Negative Stain Procedure. http://www.cores.utah.edu/wp-content/uploads/2013/06/negative-stain.pdf. Accessed 13 Nov 2013
53. Wyatt Technology Corporation (2011) Introduction to light scattering. Light Scattering University. Santa Barbara California
54. Pencer J, White GF, Hallett FR (2001) Osmotically induced shape changes of large unilamellar vesicles measured by dynamic light scattering. Biophys J 81(5):2716-2728. doi: 10.1016/s0006-3495(01)75914-0
55. Pencer J, Hallett FR (2003) Effects of vesicle size and shape on static and dynamic light scattering measurements. Langmuir 19(18):7488-7497. doi: 10.1021/la0345439