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Extraction of redox extracellular vesicles using exclusion-based sample preparation

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A Correction to this article was published on 02 October 2024

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Abstract

Studying specific subpopulations of cancer-derived extracellular vesicles (EVs) could help reveal their role in cancer progression. In cancer, an increase in reactive oxygen species (ROS) happens which results in lipid peroxidation with a major product of 4-hydroxynonenal (HNE). Adduction by HNE causes alteration to the structure of proteins, leading to loss of function. Blebbing of EVs carrying these HNE-adducted proteins as a cargo or carrying HNE-adducted on EV membrane are methods for clearing these molecules by the cells. We have referred to these EVs as Redox EVs. Here, we utilize a surface tension-mediated extraction process, termed exclusion-based sample preparation (ESP), for the rapid and efficient isolation of intact Redox EVs, from a mixed population of EVs derived from human glioblastoma cell line LN18. After optimizing different parameters, two populations of EVs were analyzed, those isolated from the sample (Redox EVs) and those remaining in the original sample (Remaining EVs). Electron microscopic imaging was used to confirm the presence of HNE adducts on the outer leaflet of Redox EVs. Moreover, the population of HNE-adducted Redox EVs shows significantly different characteristics to those of Remaining EVs including smaller size EVs and a more negative zeta potential EVs. We further treated glioblastoma cells (LN18), radiation-resistant glioblastoma cells (RR-LN18), and normal human astrocytes (NHA) with both Remaining and Redox EV populations. Our results indicate that Redox EVs promote the growth of glioblastoma cells, likely through the production of H2O2, and cause injury to normal astrocytes. In contrast, Remaining EVs have minimal impact on the viability of both glioblastoma cells and NHA cells. Thus, isolating a subpopulation of EVs employing ESP-based immunoaffinity could pave the way for a deeper mechanistic understanding of how subtypes of EVs, such as those containing HNE-adducted proteins, induce biological changes in the cells that take up these EVs.

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  1. Dehghan Banadaki M., Rummel N. G., Backus S., Butterfield A.D., St. Clair D.K., Campbell J.M., Zhong W., Mayer K., Berry S.M., Chaiswing L., Extraction of redox extracellular vesicles using exclusion-based samples preparation. SfRBM 2023 & SFRRI 21st Biennial Meeting, Poster Presentation, Punta del Este, Uruguay, 2023.

References

  1. Möller A, Lobb RJ. The evolving translational potential of small extracellular vesicles in cancer. Nat Rev Cancer. 2020;20:697–709. https://doi.org/10.1038/s41568-020-00299-w.

    Article  CAS  PubMed  Google Scholar 

  2. Miller CE, Xu F, Zhao Y, Luo W, Zhong W, Meyer K, et al. Hydrogen peroxide promotes the production of radiation-derived EVs containing mitochondrial proteins. Antioxidants. 2022;11:2119. https://doi.org/10.3390/antiox11112119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kinoshita T, Yip KW, Spence T, Liu F-F. MicroRNAs in extracellular vesicles: potential cancer biomarkers. J Hum Genet. 2017;62:67–74. https://doi.org/10.1038/jhg.2016.87.

    Article  CAS  PubMed  Google Scholar 

  4. Greening DW, Xu R, Ji H, Tauro BJ, Simpson RJ. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods, 2015, p. 179–209. https://doi.org/10.1007/978-1-4939-2550-6_15.

  5. Havers M, Broman A, Lenshof A, Laurell T. Advancement and obstacles in microfluidics-based isolation of extracellular vesicles. Anal Bioanal Chem. 2023;415:1265–85. https://doi.org/10.1007/s00216-022-04362-3.

    Article  CAS  PubMed  Google Scholar 

  6. Nguyen A, Turko IV. Isolation protocols and mitochondrial content for plasma extracellular vesicles. Anal Bioanal Chem. 2023;415:1299–304. https://doi.org/10.1007/s00216-022-04465-x.

    Article  CAS  PubMed  Google Scholar 

  7. Oliveira-Rodríguez M, López-Cobo S, Reyburn HT, Costa-García A, López-Martín S, Yáñez-Mó M, et al. Development of a rapid lateral flow immunoassay test for detection of exosomes previously enriched from cell culture medium and body fluids. J Extracell Vesicles. 2016;5:31803. https://doi.org/10.3402/jev.v5.31803.

    Article  CAS  PubMed  Google Scholar 

  8. Sharma P, Ludwig S, Muller L, Hong CS, Kirkwood JM, Ferrone S, et al. Immunoaffinity-based isolation of melanoma cell-derived exosomes from plasma of patients with melanoma. J Extracell Vesicles. 2018;7:1435138. https://doi.org/10.1080/20013078.2018.1435138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Yoshioka Y, Kosaka N, Konishi Y, Ohta H, Okamoto H, Sonoda H, et al. Ultra-sensitive liquid biopsy of circulating extracellular vesicles using ExoScreen. Nat Commun. 2014;5:3591. https://doi.org/10.1038/ncomms4591.

    Article  CAS  PubMed  Google Scholar 

  10. Fang S, Tian H, Li X, Jin D, Li X, Kong J, et al. Clinical application of a microfluidic chip for immunocapture and quantification of circulating exosomes to assist breast cancer diagnosis and molecular classification. PLoS One. 2017;12:e0175050. https://doi.org/10.1371/journal.pone.0175050.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Zhang P, He M, Zeng Y. Ultrasensitive microfluidic analysis of circulating exosomes using a nanostructured graphene oxide/polydopamine coating. Lab Chip. 2016;16:3033–42. https://doi.org/10.1039/C6LC00279J.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ni F, Zhu Q, Li H, Liu F, Chen H. Efficient preparation of high-purity and intact mesenchymal stem cell–derived extracellular vesicles. Anal Bioanal Chem. 2024;416:1797–808. https://doi.org/10.1007/s00216-024-05193-0.

    Article  CAS  PubMed  Google Scholar 

  13. Ströhle G, Gan J, Li H. Affinity-based isolation of extracellular vesicles and the effects on downstream molecular analysis. Anal Bioanal Chem. 2022;414:7051–67. https://doi.org/10.1007/s00216-022-04178-1.

    Article  CAS  PubMed  Google Scholar 

  14. Sato H, Shibata M, Shimizu T, Shibata S, Toriumi H, Ebine T, et al. Differential cellular localization of antioxidant enzymes in the trigeminal ganglion. Neuroscience. 2013;248:345–58. https://doi.org/10.1016/j.neuroscience.2013.06.010.

    Article  CAS  PubMed  Google Scholar 

  15. Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, et al. Oxidative stress: harms and benefits for human health. Oxid Med Cell Longev. 2017;2017:1–13. https://doi.org/10.1155/2017/8416763.

    Article  CAS  Google Scholar 

  16. Dalleau S, Baradat M, Guéraud F, Huc L. Cell death and diseases related to oxidative stress:4-hydroxynonenal (HNE) in the balance. Cell Death Differ. 2013;20:1615–30. https://doi.org/10.1038/cdd.2013.138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chiarpotto* E, Domenicotti* C, Paola D, Vitali A, Nitti M, Pronzato MA, et al. Regulation of rat hepatocyte protein kinase C ? isoenzymes by the lipid peroxidation product 4-hydroxy-2,3-nonenal: a signaling pathway to modulate vesicular transport of glycoproteins. Hepatology 1999;29:1565–72. https://doi.org/10.1002/hep.510290510.

  18. Uchida K, Toyokuni S, Nishikawa K, Kawakishi S, Oda H, Hiai H, et al. Michael addition-type 4-hydroxy-2-nonenal adducts in modified low-density lipoproteins: markers for atherosclerosis. Biochemistry. 1994;33:12487–94. https://doi.org/10.1021/bi00207a016.

    Article  CAS  PubMed  Google Scholar 

  19. Poli G, Schaur RJ, Siems WG, Leonarduzzi G. 4-Hydroxynonenal: a membrane lipid oxidation product of medicinal interest. Med Res Rev. 2008;28:569–631. https://doi.org/10.1002/med.20117.

    Article  CAS  PubMed  Google Scholar 

  20. Subramaniam R, Roediger F, Jordan B, Mattson MP, Keller JN, Waeg G, et al. The lipid peroxidation product, 4-hydroxy-2-trans-nonenal, alters the conformation of cortical synaptosomal membrane proteins. J Neurochem. 2002;69:1161–9. https://doi.org/10.1046/j.1471-4159.1997.69031161.x.

    Article  Google Scholar 

  21. Butterfield DA, Halliwell B. Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease. Nat Rev Neurosci. 2019;20:148–60. https://doi.org/10.1038/s41583-019-0132-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Barrera G. Oxidative stress and lipid peroxidation products in cancer progression and therapy. ISRN Oncol. 2012;2012:1–21. https://doi.org/10.5402/2012/137289.

    Article  CAS  Google Scholar 

  23. Bader Lange ML, Cenini G, Piroddi M, Mohmmad Abdul H, Sultana R, Galli F, et al. Loss of phospholipid asymmetry and elevated brain apoptotic protein levels in subjects with amnestic mild cognitive impairment and Alzheimer disease. Neurobiol Dis. 2008;29:456–64. https://doi.org/10.1016/j.nbd.2007.11.004.

    Article  CAS  PubMed  Google Scholar 

  24. Firl N, Kienberger H, Hauser T, Rychlik M. Determination of the fatty acid profile of neutral lipids, free fatty acids and phospholipids in human plasma. Clinical Chemistry and Laboratory Medicine (CCLM). 2013;51:799–810. https://doi.org/10.1515/cclm-2012-0203.

    Article  CAS  PubMed  Google Scholar 

  25. Morel O, Jesel L, Freyssinet J-M, Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol. 2011;31:15–26. https://doi.org/10.1161/ATVBAHA.109.200956.

    Article  CAS  PubMed  Google Scholar 

  26. Ho J, Chaiswing L, Clair DK. Extracellular vesicles and cancer therapy: insights into the role of oxidative stress. Antioxidants. 2022;11:1194. https://doi.org/10.3390/antiox11061194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zhang S, Eitan E, Wu T-Y, Mattson MP. Intercellular transfer of pathogenic α-synuclein by extracellular vesicles is induced by the lipid peroxidation product 4-hydroxynonenal. Neurobiol Aging. 2018;61:52–65. https://doi.org/10.1016/j.neurobiolaging.2017.09.016.

    Article  CAS  PubMed  Google Scholar 

  28. Szweda LI, Uchida K, Tsai L, Stadtman ER. Inactivation of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Selective modification of an active-site lysine. J Biol Chem. 1993;268:3342–7.

    Article  CAS  PubMed  Google Scholar 

  29. Sukati S, Ho J, Chaiswing L, Sompol P, Pandit H, Wei W, et al. Extracellular vesicles released after cranial radiation: an insight into an early mechanism of brain injury. Brain Res. 2022;1782: 147840. https://doi.org/10.1016/j.brainres.2022.147840.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Rummel NG, Chaiswing L, Bondada S, Clair DK, Butterfield DA. Chemotherapy-induced cognitive impairment: focus on the intersection of oxidative stress and TNFα. Cell Molecular Life Sci. 2021;78:6533–40. https://doi.org/10.1007/s00018-021-03925-4.

    Article  CAS  Google Scholar 

  31. Malloci M, Perdomo L, Veerasamy M, Andriantsitohaina R, Simard G, Martínez MC. Extracellular vesicles: mechanisms in human health and disease. Antioxid Redox Signal. 2019;30:813–56. https://doi.org/10.1089/ars.2017.7265.

    Article  CAS  PubMed  Google Scholar 

  32. Ricklefs FL, Wollmann K, Salviano-Silva A, Drexler R, Maire CL, Kaul MG, et al. Circulating extracellular vesicles as biomarker for diagnosis, prognosis, and monitoring in glioblastoma patients. Neuro Oncol. 2024;26:1280–91. https://doi.org/10.1093/neuonc/noae068.

    Article  PubMed  Google Scholar 

  33. Osti D, Del Bene M, Rappa G, Santos M, Matafora V, Richichi C, et al. Clinical significance of extracellular vesicles in plasma from glioblastoma patients. Clin Cancer Res. 2019;25:266–76. https://doi.org/10.1158/1078-0432.CCR-18-1941.

    Article  CAS  PubMed  Google Scholar 

  34. Sidhom K, Obi PO, Saleem A. A review of exosomal isolation methods: is size exclusion chromatography the best option? Int J Mol Sci. 2020;21:6466. https://doi.org/10.3390/ijms21186466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. De Sousa KP, Rossi I, Abdullahi M, Ramirez MI, Stratton D, Inal JM. Isolation and characterization of extracellular vesicles and future directions in diagnosis and therapy. WIREs Nanomed Nanobiotechnol. 2023;15:e1835. https://doi.org/10.1002/wnan.1835.

    Article  CAS  Google Scholar 

  36. Morales-Kastresana A, Musich TA, Welsh JA, Telford W, Demberg T, Wood JCS, et al. High-fidelity detection and sorting of nanoscale vesicles in viral disease and cancer. J Extracell Vesicles. 2019;8:1597603. https://doi.org/10.1080/20013078.2019.1597603.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Berry SM, Chin EN, Jackson SS, Strotman LN, Goel M, Thompson NE, et al. Weak protein–protein interactions revealed by immiscible filtration assisted by surface tension. Anal Biochem. 2014;447:133–40. https://doi.org/10.1016/j.ab.2013.10.038.

    Article  CAS  PubMed  Google Scholar 

  38. Casavant BP, Guckenberger DJ, Beebe DJ, Berry SM. Efficient sample preparation from complex biological samples using a sliding lid for immobilized droplet extractions. Anal Chem. 2014;86:6355–62. https://doi.org/10.1021/ac500574t.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Berry SM, Pezzi HM, Williams ED, Loeb JM, Guckenberger DJ, Lavanway AJ, et al. Using exclusion-based sample preparation (ESP) to reduce viral load assay cost. PLoS One. 2015;10: e0143631. https://doi.org/10.1371/journal.pone.0143631.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Sperger JM, Strotman LN, Welsh A, Casavant BP, Chalmers Z, Horn S, et al. Integrated analysis of multiple biomarkers from circulating tumor cells enabled by exclusion-based analyte isolation. Clin Cancer Res. 2017;23:746–56. https://doi.org/10.1158/1078-0432.CCR-16-1021.

    Article  PubMed  Google Scholar 

  41. Strike W, Amirsoleimani A, Olaleye A, Noble A, Lewis K, Faulkner L, et al. Development and validation of a simplified method for analysis of SARS-CoV-2 RNA in University Dormitories. ACS ES&T Water. 2022;2:1984–91. https://doi.org/10.1021/acsestwater.2c00044.

    Article  CAS  Google Scholar 

  42. Torabi S, Amirsoleimani A, DehghanBanadaki M, Strike WD, Rockward A, Noble A, et al. Stabilization of SARS-CoV-2 RNA in wastewater via rapid RNA extraction. Sci Total Environ. 2023;878: 162992. https://doi.org/10.1016/j.scitotenv.2023.162992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. DehghanBanadaki M, Torabi S, Rockward A, Strike WD, Noble A, Keck JW, et al. Simple SARS-CoV-2 concentration methods for wastewater surveillance in low resource settings. Sci Total Environ. 2024;912: 168782. https://doi.org/10.1016/j.scitotenv.2023.168782.

    Article  CAS  Google Scholar 

  44. Moussavi-Harami SF, Annis DS, Ma W, Berry SM, Coughlin EE, Strotman LN, et al. Characterization of molecules binding to the 70K N-terminal region of fibronectin by IFAST purification coupled with mass spectrometry. J Proteome Res. 2013;12:3393–404. https://doi.org/10.1021/pr400225p.

    Article  CAS  PubMed  Google Scholar 

  45. Goel S, Chin EN, Fakhraldeen SA, Berry SM, Beebe DJ, Alexander CM. Both LRP5 and LRP6 receptors are required to respond to physiological Wnt ligands in mammary epithelial cells and fibroblasts. J Biol Chem. 2012;287:16454–66. https://doi.org/10.1074/jbc.M112.362137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. DehghanBanadaki M, Torabi S, Strike WD, Noble A, Keck JW, Berry SM. Improving wastewater-based epidemiology performance through streamlined automation. J Environ Chem Eng. 2023;11: 109595. https://doi.org/10.1016/j.jece.2023.109595.

    Article  CAS  Google Scholar 

  47. Nguyen U, Squaglia N, Boge A, Fung PA. The simple WesternTM: a gel-free, blot-free, hands-free Western blotting reinvention. Nat Methods. 2011;8:v–vi. https://doi.org/10.1038/nmeth.f.353.

    Article  CAS  Google Scholar 

  48. Hill JL, McIver KB, Katzer K, Foster MT. Capillary western immunoassay optimization of estrogen related factors in human subcutaneous adipose tissue. Methods Protoc. 2022;5:34. https://doi.org/10.3390/mps5020034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell. 2016;30:836–48. https://doi.org/10.1016/j.ccell.2016.10.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Chiaradia E, Tancini B, Emiliani C, Delo F, Pellegrino RM, Tognoloni A, et al. Extracellular vesicles under oxidative stress conditions: biological properties and physiological roles. Cells. 2021;10:1763. https://doi.org/10.3390/cells10071763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kim W, Lee S, Seo D, Kim D, Kim K, Kim E, et al. Cellular stress responses in radiotherapy. Cells. 2019;8:1105. https://doi.org/10.3390/cells8091105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Chaiswing L, Weiss HL, Jayswal RD, Clair DK, Kyprianou N. Profiles of radioresistance mechanisms in prostate cancer. Crit Rev Oncog. 2018;23:39–67. https://doi.org/10.1615/CritRevOncog.2018025946.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Matsumura S, Minamisawa T, Suga K, Kishita H, Akagi T, Ichiki T, et al. Subtypes of tumour cell-derived small extracellular vesicles having differently externalized phosphatidylserine. J Extracell Vesicles. 2019;8:1579541. https://doi.org/10.1080/20013078.2019.1579541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Nagata S, Suzuki J, Segawa K, Fujii T. Exposure of phosphatidylserine on the cell surface. Cell Death Differ. 2016;23:952–61. https://doi.org/10.1038/cdd.2016.7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Welsh JA, Goberdhan DCI, O’Driscoll L, Buzas EI, Blenkiron C, Bussolati B, et al. Minimal information for studies of extracellular vesicles (MISEV2023): from basic to advanced approaches. J Extracell Vesicles. 2024;13: e12404. https://doi.org/10.1002/jev2.12404.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Saha B, Evers TH, Prins MWJ. How antibody surface coverage on nanoparticles determines the activity and kinetics of antigen capturing for biosensing. Anal Chem. 2014;86:8158–66. https://doi.org/10.1021/ac501536z.

    Article  CAS  PubMed  Google Scholar 

  57. Lennicke C, Rahn J, Lichtenfels R, Wessjohann LA, Seliger B. Hydrogen peroxide – production, fate and role in redox signaling of tumor cells. Cell Communication Signal. 2015;13:39. https://doi.org/10.1186/s12964-015-0118-6.

    Article  CAS  Google Scholar 

  58. Park I, Hwang J, Kim YM, Ha J, Park OJ. Differential modulation of AMPK signaling pathways by low or high levels of exogenous reactive oxygen species in colon cancer cells. Ann N Y Acad Sci. 2006;1091:102–9. https://doi.org/10.1196/annals.1378.059.

    Article  CAS  PubMed  Google Scholar 

  59. Borovic S, Cipak A, Meinitzer A, Kejla Z, Perovic D, Waeg G, et al. Differential sensitivity to 4-hydroxynonenal for normal and malignant mesenchymal cells. Redox Rep. 2007;12:50–4. https://doi.org/10.1179/135100007X162194.

    Article  CAS  PubMed  Google Scholar 

  60. Wei H, Malcor J-DM, Harper MT. Lipid rafts are essential for release of phosphatidylserine-exposing extracellular vesicles from platelets. Sci Rep 2018;8:9987. https://doi.org/10.1038/s41598-018-28363-4.

  61. Flannagan RS, Canton J, Furuya W, Glogauer M, Grinstein S. The phosphatidylserine receptor TIM4 utilizes integrins as coreceptors to effect phagocytosis. Mol Biol Cell. 2014;25:1511–22. https://doi.org/10.1091/mbc.e13-04-0212.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Zhong H, Yin H. Role of lipid peroxidation derived 4-hydroxynonenal (4-HNE) in cancer: focusing on mitochondria. Redox Biol. 2015;4:193–9. https://doi.org/10.1016/j.redox.2014.12.011.

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported, in part, by (1) NIH grants R01 CA251663 (L.C.), P20 GM148326 (L.C.), and R01 CA217934 (D.A.B. and D.S.) and (2) pilot funding to L.C and S.M.B. by Markey Cancer Center support grant (P30 CA177558). S.M.B., M.D.B., and S.B. were supported by NIH grants 1U01DA053903-01 and P30 ES026529, CDC contract BAA 75D301-20-R-68024, and NSF grant 2154934. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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  1. Mohammad Dehghan Banadaki and Nicole G. Rummel contributed equally to this work.

Authors and Affiliations

  1. Department of Mechanical Engineering, University of Kentucky, Lexington, KY, 40506, USA

    Mohammad Dehghan Banadaki, Spencer Backus & Scott M. Berry

  2. Department of Chemistry, University of Kentucky, Lexington, KY, 40506, USA

    Nicole G. Rummel & David Allan Butterfield

  3. Markey Cancer Center, University of Kentucky, Lexington, KY, 40536, USA

    Nicole G. Rummel, David Allan Butterfield, Daret K. St. Clair, James M. Campbell & Luksana Chaiswing

  4. Department of Toxicology and Cancer Biology, University of Kentucky, Lexington, KY, 40536, USA

    Daret K. St. Clair, James M. Campbell & Luksana Chaiswing

  5. Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, 53706, USA

    Weixiong Zhong & Kristy Mayer

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Contributions

M.D.B., N.R.: Writing—original draft. D.A.B., D.S., S.M.B., L.C.: Writing—review and editing. M.D.B., N.R., J.M.C., S.B.: Investigation. M.D.B., N.R., J.M.C., S.B., N.R.,W.Z., K.M.: Methodology. M.D.B., N.R.: Validation. M.D.B., N.R.,W.Z., K.M.: Formal analysis. M.D.B., N.R., and L.C.: Visualization. S.M.B and L.C.: Conceptualization. D.A.B., D.S., S.M.B., L.C.: Project administration. S.M.B., L.C.: Supervision. S.M.B., L.C.: Funding acquisition.

Corresponding authors

Correspondence to Scott M. Berry or Luksana Chaiswing.

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The authors declare the following competing financial interest: Scott Berry has an ownership interest in Salus Discovery, LLC, which has licensed the ESP technology described in the text. All other authors declare no conflict of interest.

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The original online version of this article was revised: The original version of this article unfortunately contained a mistake since the y-Axis of Figure 6 A is missing negative symbol. Zeta potential is a negative value.

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Banadaki, M.D., Rummel, N.G., Backus, S. et al. Extraction of redox extracellular vesicles using exclusion-based sample preparation. Anal Bioanal Chem 416, 6317–6331 (2024). https://doi.org/10.1007/s00216-024-05518-z

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