Isolation of human salivary extracellular vesicles by iodixanol density gradient ultracentrifugation and their characterizations

References

• Wong DT. Salivary diagnostics powered by nanotechnologies, proteomics and genomics. J Am Dent Assoc. 2006; 137: 313–21.
   PubMed Web of Science ®Google Scholar
• Pfaffe T, Cooper-White J, Beyerlein P, Kostner K, Punyadeera C. Diagnostic potential of saliva: current state and future applications. Clin Chem. 2011; 57: 675–87.
   PubMed Web of Science ®Google Scholar
• Humphrey SP, Williamson RT. A review of saliva: normal composition, flow, and function. J Prosthet Dent. 2001; 85: 162–9.
   PubMed Web of Science ®Google Scholar
• Deutsch O, Fleissig Y, Zaks B, Krief G, Aframian DJ, Palmon A. An approach to remove alpha amylase for proteomic analysis of low abundance biomarkers in human saliva. Electrophoresis. 2008; 29: 4150–7.
   PubMed Web of Science ®Google Scholar
• Krief G, Deutsch O, Gariba S, Zaks B, Aframian DJ, Palmon A. Improved visualization of low abundance oral fluid proteins after triple depletion of alpha amylase, albumin and IgG. Oral Dis. 2011; 17: 45–52.
   PubMed Web of Science ®Google Scholar
• Wong DT. Salivary extracellular noncoding RNA: emerging biomarkers for molecular diagnostics. Clin Ther. 2015; 37: 540–51.
   Web of Science ®Google Scholar
• Lötvall J, Hill AF, Hochberg F, Buzas EI, Di Vizio D, Gardiner C, etal. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles. 2014; 3: 26913, doi: http://dx.doi.org/10.3402/jev.v3.26913.
   Google Scholar
• Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, etal. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015; 4: 27066, doi: http://dx.doi.org/10.3402/jev.v4.27066.
   Google Scholar
• Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007; 9: 654–9.
   PubMed Web of Science ®Google Scholar
• El Andaloussi S, Mager I, Breakefield XO, Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov. 2013; 12: 347–57.
   PubMed Web of Science ®Google Scholar
• Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009; 9: 581–93.
   PubMed Web of Science ®Google Scholar
• Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, etal. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008; 10: 1470–6.
   PubMed Web of Science ®Google Scholar
• Rupp AK, Rupp C, Keller S, Brase JC, Ehehalt R, Fogel M, etal. Loss of EpCAM expression in breast cancer derived serum exosomes: role of proteolytic cleavage. Gynecol Oncol. 2011; 122: 437–46.
   PubMed Web of Science ®Google Scholar
• Gyorgy B, Modos K, Pallinger E, Paloczi K, Pasztoi M, Misjak P, etal. Detection and isolation of cell-derived microparticles are compromised by protein complexes resulting from shared biophysical parameters. Blood. 2011; 117: e39–48.
   PubMed Web of Science ®Google Scholar
• Alvarez ML, Khosroheidari M, Kanchi Ravi R, Distefano JK. Comparison of protein, microRNA, and mRNA yields using different methods of urinary exosome isolation for the discovery of kidney disease biomarkers. Kidney Int. 2012; 82: 1024–32.
   PubMed Web of Science ®Google Scholar
• Chen C, Skog J, Hsu C-H, Lessard RT, Balaj L, Wurdinger T, etal. Microfluidic isolation and transcriptome analysis of serum microvesicles. Lab Chip. 2010; 10: 505–11.
   PubMed Web of Science ®Google Scholar
• Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006. Chapter 3:Unit 3 22.
   PubMedGoogle Scholar
• Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, etal. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996; 183: 1161–72.
   PubMed Web of Science ®Google Scholar
• Rani S, O'Brien K, Kelleher FC, Corcoran C, Germano S, Radomski MW, etal. Isolation of exosomes for subsequent mRNA, MicroRNA, and protein profiling. Methods Mol Biol. 2011; 784: 181–95.
   PubMedGoogle Scholar
• Raj DA, Fiume I, Capasso G, Pocsfalvi G. A multiplex quantitative proteomics strategy for protein biomarker studies in urinary exosomes. Kidney Int. 2012; 81: 1263–72.
   PubMed Web of Science ®Google Scholar
• Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, Norman M, etal. Exosomes with immune modulatory features are present in human breast milk. J Immunol. 2007; 179: 1969–78.
   PubMed Web of Science ®Google Scholar
• Harrington MG, Fonteh AN, Oborina E, Liao P, Cowan RP, McComb G, etal. The morphology and biochemistry of nanostructures provide evidence for synthesis and signaling functions in human cerebrospinal fluid. Cerebrospinal Fluid Res. 2009; 6: 10.
   PubMedGoogle Scholar
• Berckmans RJ, Sturk A, van Tienen LM, Schaap MC, Nieuwland R. Cell-derived vesicles exposing coagulant tissue factor in saliva. Blood. 2011; 117: 3172–80.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Begne M, Lu B, Han X, Hagen FK, Hand AR, Melvin JE, etal. Proteomic analysis of human parotid gland exosomes by multidimensional protein identification technology (MudPIT). J Proteome Res. 2009; 8: 1304–14.
   PubMed Web of Science ®Google Scholar
• Michael A, Bajracharya SD, Yuen PS, Zhou H, Star RA, Illei GG, etal. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 2010; 16: 34–8.
   PubMed Web of Science ®Google Scholar
• Sharma S, Rasool HI, Palanisamy V, Mathisen C, Schmidt M, Wong DT, etal. Structural-mechanical characterization of nanoparticle exosomes in human saliva, using correlative AFM, FESEM, and force spectroscopy. ACS Nano. 2010; 4: 1921–6.
   PubMed Web of Science ®Google Scholar
• Lässer C, Alikhani VS, Ekstrom K, Eldh M, Paredes PT, Bossios A, etal. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J Transl Med. 2011; 9: 9.
   PubMed Web of Science ®Google Scholar
• Sharma S, Gillespie B, Palanisamy V, Gimzewski JK. Quantitative nanostructural and single-molecule force spectroscopy biomolecular analysis of human saliva-derived exosomes. Langmuir. 2011; 27: 14394–400.
   PubMed Web of Science ®Google Scholar
• Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One. 2012; 7: e30679.
   PubMed Web of Science ®Google Scholar
• Ogawa Y, Taketomi Y, Murakami M, Tsujimoto M, Yanoshita R. Small RNA transcriptomes of 2 types of exosomes in human whole saliva determined by next generation sequencing. Biol Pharm Bull. 2013; 36: 66–75.
   PubMed Web of Science ®Google Scholar
• Lau C, Kim Y, Chia D, Spielmann N, Eibl G, Elashoff D, etal. Role of pancreatic cancer-derived exosomes in salivary biomarker development. J Biol Chem. 2013; 288: 26888–97.
   PubMed Web of Science ®Google Scholar
• Zlotogorski-Hurvitz A, Dayan D, Chaushu G, Korvala J, Salo T, Sormunen R, etal. Human saliva-derived exosomes: comparing methods of isolation. J Histochem Cytochem. 2015; 63: 181–9.
   PubMed Web of Science ®Google Scholar
• Yang J, Wei F, Schafer C, Wong DT. Detection of tumor cell-specific mRNA and protein in exosome-like microvesicles from blood and saliva. PLoS One. 2014; 9: e110641.
   PubMed Web of Science ®Google Scholar
• Gorur A, Balci Fidanci S, Dogruer Unal N, Ayaz L, Akbayir S, Yildirim Yaroglu H, etal. Determination of plasma microRNA for early detection of gastric cancer. Mol Biol Rep. 2013; 40: 2091–6.
   PubMed Web of Science ®Google Scholar
• Jang JS, Simon VA, Feddersen RM, Rakhshan F, Schultz DA, Zschunke MA, etal. Quantitative miRNA expression analysis using fluidigm microfluidics dynamic arrays. BMC Genomics. 2011; 12: 144.
   PubMed Web of Science ®Google Scholar
• Cantin R, Diou J, Belanger D, Tremblay AM, Gilbert C. Discrimination between exosomes and HIV-1: purification of both vesicles from cell-free supernatants. J Immunol Methods. 2008; 338: 21–30.
   PubMed Web of Science ®Google Scholar
• Neves JS, Perez SA, Spencer LA, Melo RC, Weller PF. Subcellular fractionation of human eosinophils: isolation of functional specific granules on isoosmotic density gradients. J Immunol Methods. 2009; 344: 64–72.
   Web of Science ®Google Scholar
• Perez-Gonzalez R, Gauthier SA, Kumar A, Levy E. The exosome-secretory pathway transports amyloid precursor protein carboxyl terminal fragments from the cell into the brain extracellular space. J Biol Chem. 2012; 287: 43108–15.
   PubMed Web of Science ®Google Scholar
• Cvjetkovic A, Lötvall J, Lässer C. The influence of rotor type and centrifugation time on the yield and purity of extracellular vesicles. J Extracell Vesicles. 2014; 3: 23111, doi: http://dx.doi.org/10.3402/jev.v3.23111.
   Google Scholar
• Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosomes: current perspectives. Proteomics. 2008; 8: 4083–99.
   PubMed Web of Science ®Google Scholar
• Katsuda T, Kosaka N, Ochiya T. The roles of extracellular vesicles in cancer biology: toward the development of novel cancer biomarkers. Proteomics. 2014; 14: 412–25.
   PubMed Web of Science ®Google Scholar
• Rantonen PJ, Meurman JH. Viscosity of whole saliva. Acta Odontol Scand. 1998; 56: 210–4.
   PubMed Web of Science ®Google Scholar
• Mayanagi T, Kurosawa R, Ohnuma K, Ueyama A, Ito K, Takahashi J. Purification of mouse primordial germ cells by Nycodenz. Reproduction. 2003; 125: 667–75.
   Web of Science ®Google Scholar
• Graham J, Ford T, Rickwood D. The preparation of subcellular organelles from mouse liver in self-generated gradients of iodixanol. Anal Biochem. 1994; 220: 367–73.
   PubMed Web of Science ®Google Scholar
• Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, etal. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 2012; 14: 677–85.
   PubMed Web of Science ®Google Scholar
• Tauro BJ, Mathias RA, Greening DW, Gopal SK, Ji H, Kapp EA, etal. Oncogenic H-ras reprograms Madin-Darby canine kidney (MDCK) cell-derived exosomal proteins following epithelial-mesenchymal transition. Mol Cell Proteomics. 2013; 12: 2148–59.
   PubMed Web of Science ®Google Scholar
• Aalberts M, van Dissel-Emiliani FM, van Adrichem NP, van Wijnen M, Wauben MH, Stout TA, etal. Identification of distinct populations of prostasomes that differentially express prostate stem cell antigen, annexin A1, and GLIPR2 in humans. Biol Reprod. 2012; 86: 82.
   PubMed Web of Science ®Google Scholar
• Palanisamy V, Sharma S, Deshpande A, Zhou H, Gimzewski J, Wong DT. Nanostructural and transcriptomic analyses of human saliva derived exosomes. PLoS One. 2010; 5: e8577.
   PubMed Web of Science ®Google Scholar
• Zlotogorski-Hurvitz A, Dayan D, Chaushu G, Salo T, Vered M. Morphological and molecular features of oral fluid-derived exosomes: oral cancer patients versus healthy individuals. J Cancer Res Clin Oncol. 2015; 142: 101–10.
   Web of Science ®Google Scholar
• Hardij J, Cecchet F, Berquand A, Gheldof D, Chatelain C, Mullier F, etal. Characterisation of tissue factor-bearing extracellular vesicles with AFM: comparison of air-tapping-mode AFM and liquid Peak Force AFM. J Extracell Vesicles. 2013; 2: 21045, doi: http://dx.doi.org/10.3402/jev.v2i0.21045.
   Google Scholar
• Ashcroft BA, de Sonneville J, Yuana Y, Osanto S, Bertina R, Kuil ME, etal. Determination of the size distribution of blood microparticles directly in plasma using atomic force microscopy and microfluidics. Biomed Microdevices. 2012; 14: 641–9.
   PubMed Web of Science ®Google Scholar
• Leong HS, Podor TJ, Manocha B, Lewis JD. Validation of flow cytometric detection of platelet microparticles and liposomes by atomic force microscopy. J Thromb Haemost. 2011; 9: 2466–76.
   Web of Science ®Google Scholar
• Uesugi A, Kozaki K, Tsuruta T, Furuta M, Morita K, Imoto I, etal. The tumor suppressive microRNA miR-218 targets the mTOR component Rictor and inhibits AKT phosphorylation in oral cancer. Cancer Res. 2011; 71: 5765–78.
   PubMed Web of Science ®Google Scholar
• Li A, Omura N, Hong SM, Vincent A, Walter K, Griffith M, etal. Pancreatic cancers epigenetically silence SIP1 and hypomethylate and overexpress miR-200a/200b in association with elevated circulating miR-200a and miR-200b levels. Cancer Res. 2010; 70: 5226–37.
   PubMed Web of Science ®Google Scholar
• Shantikumar S, Caporali A, Emanueli C. Role of microRNAs in diabetes and its cardiovascular complications. Cardiovasc Res. 2012; 93: 58393.
   Web of Science ®Google Scholar
• Tijsen AJ, Pinto YM, Creemers EE. Circulating microRNAs as diagnostic biomarkers for cardiovascular diseases. Am J Physiol Heart Circ Physiol. 2012; 303: H1085–95.
   PubMed Web of Science ®Google Scholar
• Wang Y, Li L, Moore BT, Peng XH, Fang X, Lappe JM, etal. MiR-133a in human circulating monocytes: a potential biomarker associated with postmenopausal osteoporosis. PLoS One. 2012; 7: e34641.
   PubMed Web of Science ®Google Scholar
• Alevizos I, Illei GG. MicroRNAs in Sjogren's syndrome as a prototypic autoimmune disease. Autoimmun Rev. 2010; 9: 618–21.
   PubMed Web of Science ®Google Scholar
• Bousquet M, Harris MH, Zhou B, Lodish HF. MicroRNA miR-125b causes leukemia. Proc Natl Acad Sci USA. 2010; 107: 21558–63.
   PubMed Web of Science ®Google Scholar
• Bandyopadhyay S, Friedman RC, Marquez RT, Keck K, Kong B, Icardi MS, etal. Hepatitis C virus infection and hepatic stellate cell activation downregulate miR-29: miR-29 overexpression reduces hepatitis C viral abundance in culture. J Infect Dis. 2011; 203: 1753–62.
   PubMed Web of Science ®Google Scholar
• Yuana Y, Boing AN, Grootemaat AE, van der Pol E, Hau CM, Cizmar P, etal. Handling and storage of human body fluids for analysis of extracellular vesicles. J Extracell Vesicles. 2015; 4: 29260, doi: http://dx.doi.org/10.3402/jev.v4.29260.
   Google Scholar
• Linares R, Tan S, Gounou C, Arraud N, Brisson AR. High-speed centrifugation induces aggregation of extracellular vesicles. J Extracell Vesicles. 2015; 4: 29509, doi: http://dx.doi.org/10.3402/jev.v4.29509.
   Google Scholar