Proteomic analysis of plasma-derived extracellular vesicles: pre- and postprandial comparisons.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
03 10 2024
Historique:
received: 15 05 2024
accepted: 24 09 2024
medline: 4 10 2024
pubmed: 4 10 2024
entrez: 3 10 2024
Statut: epublish

Résumé

Extracellular vesicles (EVs) are key in intercellular communication, carrying biomolecules like nucleic acids, lipids, and proteins. This study investigated postprandial characteristics and proteomic profiles of blood-derived EVs in healthy individuals. Twelve participants fasted overnight before baseline assessments. After consuming a controlled isocaloric meal, EVs were isolated for proteomic and flow cytometric analysis. Plasma triacylglyceride levels confirmed fasting completion, while protein concentrations in plasma and EVs were monitored for postprandial stability. Proteomic analysis identified upregulated proteins related to transport mechanisms and epithelial/endothelial functions postprandially, indicating potential roles in physiological responses to nutritional intake. Enrichment analyses revealed vesicle-related pathways and immune system processes. Flow cytometry showed increased expression of CD324 on CD9

Identifiants

pubmed: 39363010
doi: 10.1038/s41598-024-74228-4
pii: 10.1038/s41598-024-74228-4
doi:

Substances chimiques

Proteome 0

Types de publication

Journal Article Comparative Study

Langues

eng

Sous-ensembles de citation

IM

Pagination

23032

Informations de copyright

© 2024. The Author(s).

Références

Kumar, M. A. et al. Extracellular vesicles as tools and targets in therapy for diseases. Signal Transduct. Targ. Ther.9, 1–41 (2024).
Shah, R., Patel, T. & Freedman, J. E. Circulating extracellular vesicles in human disease. N. Engl. J. Med.379, 958–966 (2018).
pubmed: 30184457 doi: 10.1056/NEJMra1704286
Lyu, C., Sun, H., Sun, Z., Liu, Y. & Wang, Q. Roles of exosomes in immunotherapy for solid cancers. Cell Death Dis.2024(15), 1–21 (2024).
Buzas, E. I. The roles of extracellular vesicles in the immune system. Nat. Rev. Immunol.23, 236–250 (2022).
pubmed: 35927511 pmcid: 9361922 doi: 10.1038/s41577-022-00763-8
Van Niel, G., D’Angelo, G. & Raposo, G. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol.19, 213–228 (2018).
pubmed: 29339798 doi: 10.1038/nrm.2017.125
Dixson, A. C., Dawson, T. R., Di Vizio, D. & Weaver, A. M. Context-specific regulation of extracellular vesicle biogenesis and cargo selection. Nat. Rev. Mol. Cell Biol.2023(24), 454–476 (2023).
doi: 10.1038/s41580-023-00576-0
Lässer, C., Jang, S. C. & Lötvall, J. Subpopulations of extracellular vesicles and their therapeutic potential. Mol. Aspects Med.60, 1–14 (2018).
pubmed: 29432782 doi: 10.1016/j.mam.2018.02.002
Dong, L. et al. Comprehensive evaluation of methods for small extracellular vesicles separation from human plasma, urine and cell culture medium. J. Extracell Vesicles10, e12044 (2020).
pubmed: 33489012 doi: 10.1002/jev2.12044
Sharma, P. et al. A comprehensive proteomic profiling of urinary exosomes and the identification of early non-invasive biomarker in patients with coronary artery disease. J. Proteomics293, 105059 (2024).
pubmed: 38151158 doi: 10.1016/j.jprot.2023.105059
Dutta, S., Hornung, S., Taha, H. B. & Bitan, G. Biomarkers for parkinsonian disorders in CNS-originating EVs: promise and challenges. Acta Neuropathol.145, 515–540 (2023).
pubmed: 37012443 pmcid: 10071251 doi: 10.1007/s00401-023-02557-1
Gebara, N. et al. Single extracellular vesicle analysis in human amniotic fluid shows evidence of phenotype alterations in preeclampsia. J. Extracell Vesicles11, e12217 (2022).
pubmed: 35582873 pmcid: 9115584 doi: 10.1002/jev2.12217
Alić, V. K. et al. Extracellular vesicles from human cerebrospinal fluid are effectively separated by sepharose CL-6B-comparison of four gravity-flow size exclusion chromatography methods. Biomedicines10, 785 (2022).
doi: 10.3390/biomedicines10040785
Karimi, N., Dalirfardouei, R., Dias, T., Lötvall, J. & Lässer, C. Tetraspanins distinguish separate extracellular vesicle subpopulations in human serum and plasma - Contributions of platelet extracellular vesicles in plasma samples. J. Extracell Vesicles11, e12213 (2022).
pubmed: 35524458 pmcid: 9077141 doi: 10.1002/jev2.12213
Royo, F., Théry, C., Falcón-Pérez, J. M., Nieuwland, R. & Witwer, K. W. Methods for separation and characterization of extracellular vesicles: Results of a worldwide survey performed by the ISEV rigor and standardization subcommittee. Cells9, 1955 (2020).
pubmed: 32854228 pmcid: 7563174 doi: 10.3390/cells9091955
Nieuwland, R. & Siljander, P. R. M. A beginner’s guide to study extracellular vesicles in human blood plasma and serum. J. Extracell Vesicles13, e12400 (2024).
pubmed: 38193375 pmcid: 10775135 doi: 10.1002/jev2.12400
Lucien, F. et al. MIBlood-EV: Minimal information to enhance the quality and reproducibility of blood extracellular vesicle research. J. Extracell Vesicles12, e12385 (2023).
pubmed: 38063210 doi: 10.1002/jev2.12385
Welsh, J. A. et al. A compendium of single extracellular vesicle flow cytometry. J. Extracell Vesicles12, 12299 (2023).
doi: 10.1002/jev2.12299
Zhang, Y. et al. Advances in therapeutic applications of extracellular vesicles. Int. J. Nanomed.18, 3285 (2023).
doi: 10.2147/IJN.S409588
Ferreira, A. C. et al. Postprandial hypertriglyceridemia increases circulating levels of endothelial cell microparticles. Circulation110, 3599–3603 (2004).
pubmed: 15569844 doi: 10.1161/01.CIR.0000148820.55611.6B
Liang, Y., Lehrich, B. M., Zheng, S. & Lu, M. Emerging methods in biomarker identification for extracellular vesicle-based liquid biopsy. J. Extracell Vesicles10, e12090 (2021).
pubmed: 34012517 pmcid: 8114032 doi: 10.1002/jev2.12090
Sódar, B. W. et al. Low-density lipoprotein mimics blood plasma-derived exosomes and microvesicles during isolation and detection. Sci. Rep.6, 24316 (2016).
pubmed: 27087061 pmcid: 4834552 doi: 10.1038/srep24316
Jamaly, S. et al. Impact of preanalytical conditions on plasma concentration and size distribution of extracellular vesicles using nanoparticle tracking analysis. Sci. Rep.8 (2018).
Nasu, M., Khadka, V. S., Jijiwa, M., Kobayashi, K. & Deng, Y. Exploring optimal biomarker sources: A comparative analysis of exosomes and whole plasma in fasting and non-fasting conditions for liquid biopsy applications. Int J Mol Sci25, 371 (2023).
pubmed: 38203541 pmcid: 10779159 doi: 10.3390/ijms25010371
Welsh, J. A. et al. Minimal information for studies of extracellular vesicles (MISEV2023): From basic to advanced approaches. J Extracell Vesicles13, e12404 (2024).
pubmed: 38326288 pmcid: 10850029 doi: 10.1002/jev2.12404
Garza, A. P. et al. Initial and ongoing tobacco smoking elicits vascular damage and distinct inflammatory response linked to neurodegeneration. Brain Behav. Immun. Health28, 100597 (2023).
pubmed: 36817509 pmcid: 9931921 doi: 10.1016/j.bbih.2023.100597
Burkhart, J. M. et al. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood120, e73–e82 (2012).
pubmed: 22869793 doi: 10.1182/blood-2012-04-416594
Kadir, R. R. A., Alwjwaj, M. & Bayraktutan, U. Protein kinase C-β distinctly regulates blood-brain barrier-forming capacity of brain microvascular endothelial cells and outgrowth endothelial cells. Metab Brain Dis.37, 1815 (2022).
pubmed: 35763197 pmcid: 9283364 doi: 10.1007/s11011-022-01041-1
Newton, A. C. Protein kinase C: structure, function, and regulation. J. Biol. Chem. https://doi.org/10.1074/jbc.270.48.28495 (1995).
doi: 10.1074/jbc.270.48.28495 pubmed: 7493995
Mørk, M. et al. Postprandial increase in blood plasma levels of tissue factor-bearing (and other) microvesicles measured by flow cytometry: Fact or artifact?. TH Open2, 147–157 (2018).
doi: 10.1055/s-0038-1642021
Michelsen, A. E. et al. Elevated levels of platelet microparticles in carotid atherosclerosis and during the postprandial state. Thromb. Res.123, 881–886 (2009).
pubmed: 19073340 doi: 10.1016/j.thromres.2008.10.016
Utar, V. et al. Post - prandial rise of microvesicles in peripheral blood of healthy human donors. Lipids Health Dis.10, 11 (2011).
Yates, A. G. et al. In sickness and in health: The functional role of extracellular vesicles in physiology and pathology in vivo: Part I: Health and normal physiology. J. Extracell Vesicles11, e12190 (2022).
pubmed: 35041301 pmcid: 8765328 doi: 10.1002/jev2.12190
Staufer, O. et al. Vesicle induced receptor sequestration: Mechanisms behind extracellular vesicle-based protein signaling. Adv. Sci.9, 2200201 (2022).
doi: 10.1002/advs.202200201
Klemetti, M. M. et al. Lipid profile of circulating placental extracellular vesicles during pregnancy identifies foetal growth restriction risk. J. Extracell Vesicles13, 12413 (2024).
doi: 10.1002/jev2.12413
Fortunato, D. et al. Selective isolation of extracellular vesicles from minimally processed human plasma as a translational strategy for liquid biopsies. Biomark. Res.10, 1–24 (2022).
doi: 10.1186/s40364-022-00404-1
Pospichalova, V. et al. Simplified protocol for flow cytometry analysis of fluorescently labeled exosomes and microvesicles using dedicated flow cytometer. J. Extracell Vesicles. https://doi.org/10.3402/jev.v4.25530 (2015).
doi: 10.3402/jev.v4.25530 pubmed: 25833224 pmcid: 4382613
Chang, X. et al. Extracellular vesicles with possible roles in gut intestinal tract homeostasis and IBD. Mediat. Inflamm.1, 1945832 (2020).
Maltseva, D. V., Poloznikov, A. A. & Artyushenko, V. G. Selective changes in expression of integrin α-subunits in the intestinal epithelial caco-2 cells under conditions of hypoxia and microcirculation. Bull. Russ. State Med. Univ. https://doi.org/10.24075/BRSMU.2020.078 (2020).
doi: 10.24075/BRSMU.2020.078
Spazierer, D. et al. Epiplakin gene analysis in mouse reveals a single exon encoding a 725-kDa protein with expression restricted to epithelial tissues. J. Biol. Chem.278, 31657–31666 (2003).
pubmed: 12791695 doi: 10.1074/jbc.M303055200
Niessen, P. et al. Smoothelin-A is essential for functional intestinal smooth muscle contractility in mice. Gastroenterology129, 1592–1601 (2005).
pubmed: 16285958 doi: 10.1053/j.gastro.2005.08.018
Isayama, K., Rini, D. M., Yamamoto, Y. & Suzuki, T. Propionate regulates tight junction barrier by increasing endothelial-cell selective adhesion molecule in human intestinal Caco-2 cells. Exp. Cell Res.425, 113528 (2023).
pubmed: 36842619 doi: 10.1016/j.yexcr.2023.113528
Scalise, A. A., Kakogiannos, N., Zanardi, F., Iannelli, F. & Giannotta, M. The blood–brain and gut–vascular barriers: From the perspective of claudins. Tissue Barriers9, 1926190 (2021).
pubmed: 34152937 pmcid: 8489939 doi: 10.1080/21688370.2021.1926190
Qian, F. et al. Analysis and biomedical applications of functional cargo in extracellular vesicles. ACS Nano16, 19980–20001 (2022).
pubmed: 36475625 doi: 10.1021/acsnano.2c11298
Salomon, C. et al. Extracellular vesicles and their emerging roles as cellular messengers in endocrinology: An endocrine society scientific statement. Endocr. Rev.43, 441–468 (2022).
pubmed: 35552682 pmcid: 10686249 doi: 10.1210/endrev/bnac009
Zhang, X. et al. Extracellular vesicles in the treatment and diagnosis of breast cancer: A status update. Front. Endocrinol. (Lausanne)14, 1202493 (2023).
pubmed: 37534210 doi: 10.3389/fendo.2023.1202493
Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem.72, 248–254 (1976).
pubmed: 942051 doi: 10.1016/0003-2697(76)90527-3
Hughes, C. S. et al. Single-pot, solid-phase-enhanced sample preparation for proteomics experiments. Nat. Protoc.14, 68–85 (2019).
pubmed: 30464214 doi: 10.1038/s41596-018-0082-x

Auteurs

Alejandra P Garza (AP)

Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-Von-Guericke University, Magdeburg, Germany.

Elisa Wider-Eberspächer (E)

Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-Von-Guericke University, Magdeburg, Germany.

Lorena Morton (L)

Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-Von-Guericke University, Magdeburg, Germany.

Marco van Ham (M)

Cellular Proteome Research Group, Helmholtz Centre for Infection Research, Braunschweig, Germany.

Éva Pállinger (É)

Department of Genetics, Cell- and Immunobiology, Semmelweis University, Budapest, Hungary.

Edit I Buzás (EI)

Department of Genetics, Cell- and Immunobiology, Semmelweis University, Budapest, Hungary.
HCEMM SU Extracellular Vesicle Research Group, Budapest, Hungary.
HUN-REN-SU Translational Extracellular Vesicle Research Group, Budapest, Hungary.

Lothar Jänsch (L)

Cellular Proteome Research Group, Helmholtz Centre for Infection Research, Braunschweig, Germany.

Ildiko R Dunay (IR)

Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-Von-Guericke University, Magdeburg, Germany. ildiko.dunay@med.ovgu.de.
Center for Behavioral Brain Sciences, Magdeburg, Germany. ildiko.dunay@med.ovgu.de.
Center for Intervention and Research on Adaptive and Maladaptive Brain Circuits Underlying Mental Health (C-I-R-C), Jena-Magdeburg-Halle, Germany. ildiko.dunay@med.ovgu.de.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH