Biological insight into the extracellular vesicles in women with and without gestational diabetes.
Extracellular vesicles
Flow cytometry
Gestational diabetes
Gestational weight gain
Metabolism
Journal
Journal of endocrinological investigation
ISSN: 1720-8386
Titre abrégé: J Endocrinol Invest
Pays: Italy
ID NLM: 7806594
Informations de publication
Date de publication:
Jan 2021
Jan 2021
Historique:
received:
28
12
2019
accepted:
16
04
2020
pubmed:
27
4
2020
medline:
5
10
2021
entrez:
27
4
2020
Statut:
ppublish
Résumé
Gestational diabetes mellitus (GDM) is the most common metabolic disorder in pregnancy, with increasing prevalence worldwide and still unclear pathogenic mechanisms. Extracellular vesicles (EVs) are emerging as potential biomarkers of disease-specific pathways in metabolic disorders, but their potential role in GDM is not fully understood. Therefore, the main aim of this study was to evaluate the link between EVs and hyperglycaemia during pregnancy. We assessed 50 GDM women and 50 controls at the third trimester of pregnancy in whom we collected demographic characteristics and clinical and anthropometric parameters. In addition, the circulating total EVs (tEVs) and their subpopulations were assessed using flow cytometry. The levels of tEVs and EVs subtypes, expressed as median and interquartile range, were not significantly different between two groups; however, adipocyte-derived EVs (aEVs) concentration, expressed as percentage, was higher in controls than in GDM women (p = 0.045). In addition, a significant correlation was observed between aEVs (%) and third trimester total cholesterol (p = 0.022) within the GDM group. Furthermore, a significant correlation between endothelial-derived EVs (eEVs) and platelet-derived EVs (pEVs) within both groups was found, as well as a significant relation between aEVs and pEVs. These data, although preliminary, represent the starting point for further studies to determine the role of circulating EVs in GDM.
Identifiants
pubmed: 32335856
doi: 10.1007/s40618-020-01262-0
pii: 10.1007/s40618-020-01262-0
doi:
Substances chimiques
Biomarkers
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
49-61Références
American Diabetes Association (ADA) (2019) Standards of medical care in diabetes—2019. Diabetes Care 42(Suppl 1):S165–S172
doi: 10.2337/dc19-S014
Hod M, Kapur A, Sacks A et al (2015) The international Federation of Gynecology and Obstetrics (FIGO) Initiative on gestational diabetes mellitus: a pragmatic guide for diagnosis, management, and care. Int J Gynecol Obstet 131(Suppl 3):S173–S211
doi: 10.1016/S0020-7292(15)30033-3
Burlina S, Dalfra MG, Lapolla A (2018) Clinical and biochemical approach to predicting post-pregnancy metabolic decompensation. Diabetes Res Clin Pract 145:178–183
doi: 10.1016/j.diabres.2018.02.035
Franzago M, Fraticelli F, Stuppia L, Vitacolonna E (2019) Nutrigenetics, epigenetics and gestational diabetes: consequences in mother and child. Epigenetics 14(3):215–235. https://doi.org/10.1080/15592294.2019.1582277
doi: 10.1080/15592294.2019.1582277
pubmed: 30865571
pmcid: 6557546
Hedderson MM, Gunderson EP, Ferrara A (2010) Gestational weight gain and risk of gestational diabetes mellitus. Obstet Gynecol 115(3):597–604
doi: 10.1097/AOG.0b013e3181cfce4f
Ding M, Chavarro J, Olsen S, Lin Y, Ley SH, Bao W, Rawal S, Grunnet LG, Thuesen ACB, Mills JL, Yeung E, Hinkle SN, Zhang W, Vaag A, Liu A, Hu FB, Zhang C (2018) Genetic variants of gestational diabetes mellitus: a study of 112 SNPs among 8722 women in two independent populations. Diabetologia 61(8):1758–1768. https://doi.org/10.1007/s00125-018-4637-8
doi: 10.1007/s00125-018-4637-8
pubmed: 29947923
pmcid: 6701842
Franzago M, Fraticelli F, Nicolucci A, Celentano C, Liberati M, Stuppia L, Vitacolonna E (2017) Molecular analysis of a genetic variants panel related to nutrients and metabolism: association with susceptibility to gestational diabetes and cardiometabolic risk in affected women. J Diabetes Res 2017:4612623. https://doi.org/10.1155/2017/4612623
doi: 10.1155/2017/4612623
pubmed: 28133617
pmcid: 5241477
Franzago M, Fraticelli F, Marchetti D, Celentano C, Liberati M, Stuppia L, Vitacolonna E (2018) Nutrigenetic variants and cardio-metabolic risk in women with or without gestational diabetes. Diabetes Res Clin Pract 137:64–71. https://doi.org/10.1016/j.diabres.2018.01.001 (Epub 2018 Jan 8)
doi: 10.1016/j.diabres.2018.01.001
pubmed: 29325775
Franzago M, Fraticelli F, Di Nicola M, Bianco F, Marchetti D, Celentano C, Liberati M, De Caterina R, Stuppia L, Vitacolonna E (2018) Early subclinical atherosclerosis in gestational diabetes: the predictive role of routine biomarkers and nutrigenetic variants. J Diabetes Res 2018:9242579. https://doi.org/10.1155/2018/9242579
doi: 10.1155/2018/9242579
pubmed: 30671483
pmcid: 6323479
Martínez MC, Andriantsitohaina R (2017) Extracellular vesicles in metabolic syndrome. Circ Res 120(10):1674–1686. https://doi.org/10.1161/CIRCRESAHA.117.309419.Review
doi: 10.1161/CIRCRESAHA.117.309419.Review
pubmed: 28495997
Shah R, Patel T, Freedman JE (2018) Circulating extracellular vesicles in human disease. N Engl J Med 379(22):2180–2181
pubmed: 30485772
Kranendonk ME, de Kleijn DP, Kalkhoven E, Kanhai DA, Uiterwaal CS, van derGraaf Y, Pasterkamp G, Visseren FL, on behalf of the SMART Study Group (2014) Extracellular vesicle markers in relation to obesity and metabolic complications in patients with manifest cardiovascular disease. Cardiovasc Diabetol 13:37. https://doi.org/10.1186/1475-2840-13-37
doi: 10.1186/1475-2840-13-37
pubmed: 24498934
pmcid: 3918107
Alexandru N, Badila E, Weiss E, Cochior D, Stępień E, Georgescu A (2016) Vascular complications in diabetes: microparticles and microparticle associated microRNAs as active players. Biochem Biophys Res Commun 472:1–10. https://doi.org/10.1016/j.bbrc.2016.02.038
doi: 10.1016/j.bbrc.2016.02.038
pubmed: 26891868
Freeman DW, Noren Hooten N, Eitan E, Green J, Mode NA, Bodogai M, Zhang Y, Lehrmann E, Zonderman AB, Biragyn A, Egan J, Becker KG, Mattson MP, Ejiogu N, Evans MK (2018) Altered extracellular vesicle concentration, cargo, and function in diabetes. Diabetes 67:2377–2388. https://doi.org/10.2337/db17-1308
doi: 10.2337/db17-1308
pubmed: 29720498
pmcid: 6198336
Margolis L, Sadovsky Y (2019) The biology of extracellular vesicles: the known unknowns. PLoS Biol 17(7):e3000363. https://doi.org/10.1371/journal.pbio.3000363 (eCollection 2019 Jul)
doi: 10.1371/journal.pbio.3000363
pubmed: 31318874
pmcid: 6667152
van Niel G, Charrin S, Simoes S, Romao M, Rochin L, Saftig P, Marks MS, Rubinstein E, Raposo G (2011) The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev Cell 21(4):708–721. https://doi.org/10.1016/j.devcel.2011.08.019 (Epub 2011 Sep 29)
doi: 10.1016/j.devcel.2011.08.019
pubmed: 21962903
pmcid: 3199340
Andreu Z, Yáñez-Mó M (2014) Tetraspanins in extracellular vesicle formation and function. Front Immunol 5:442. https://doi.org/10.3389/fimmu.2014.00442 (eCollection 2014)
doi: 10.3389/fimmu.2014.00442
pubmed: 25278937
pmcid: 4165315
Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 273(32):20121–20127
doi: 10.1074/jbc.273.32.20121
Buschow SI, Nolte-'t Hoen EN, van Niel G, Pols MS, ten Broeke T, Lauwen M, Ossendorp F, Melief CJ, Raposo G, Wubbolts R, Wauben MH, Stoorvogel W (2009) MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways. Traffic 10(10):1528–1542. https://doi.org/10.1111/j.1600-0854.2009.00963.x (Epub 2009 Jul 14)
doi: 10.1111/j.1600-0854.2009.00963.x
pubmed: 19682328
Pieragostino D, Cicalini I, Lanuti P, Ercolino E, di Ioia M, Zucchelli M, Zappacosta R, Miscia S, Marchisio M, Sacchetta P, Onofrj M, Del Boccio P (2018) Enhanced release of acid sphingomyelinase-enriched exosomes generates a lipidomics signature in CSF of multiple sclerosis patients. Sci Rep 8(1):3071. https://doi.org/10.1038/s41598-018-21497-5
doi: 10.1038/s41598-018-21497-5
pubmed: 29449691
pmcid: 5814401
Nazarenko I, Rana S, Baumann A, McAlear J, Hellwig A, Trendelenburg M, Lochnit G, Preissner KT, Zöller M (2010) Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 70(4):1668–1678. https://doi.org/10.1158/0008-5472.CAN-09-2470 (Epub 2010 Feb 2)
doi: 10.1158/0008-5472.CAN-09-2470
pubmed: 20124479
Villarroya-Beltri C, Baixauli F, Gutiérrez-Vázquez C, Sánchez-Madrid F, Mittelbrunn M (2014) Sorting it out: regulation of exosome loading. Semin Cancer Biol 28:3–13. https://doi.org/10.1016/j.semcancer.2014.04.009
doi: 10.1016/j.semcancer.2014.04.009
pubmed: 24769058
pmcid: 4640178
Gutiérrez-López MD, Gilsanz A, Yáñez-Mó M, Ovalle S, Lafuente EM, Domínguez C, Monk PN, González-Alvaro I, Sánchez-Madrid F, Cabañas C (2011) The sheddase activity of ADAM17/TACE is regulated by the tetraspanin CD9. Cell Mol Life Sci 68(19):3275–3292. https://doi.org/10.1007/s00018-011-0639-0 (Epub 2011 Mar 2)
doi: 10.1007/s00018-011-0639-0
pubmed: 21365281
Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E, Buchanan M, Hosein AN, Basik M, Wrana JL (2012) Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 151(7):1542–1556. https://doi.org/10.1016/j.cell.2012.11.024
doi: 10.1016/j.cell.2012.11.024
pubmed: 23260141
Mazurov D, Barbashova L, Filatov A (2013) Tetraspanin protein CD9 interacts with metalloprotease CD10 and enhances its release via exosomes. FEBS J 280(5):1200–1213. https://doi.org/10.1111/febs.12110
doi: 10.1111/febs.12110
pubmed: 23289620
Pillaiyar T, Manickam M, Jung SH (2017) Recent development of signaling pathways inhibitors of melanogenesis. Cell Signal 40:99–115. https://doi.org/10.1016/j.cellsig.2017.09.004 (Epub 2017 Sep 12)
doi: 10.1016/j.cellsig.2017.09.004
pubmed: 28911859
Brocco D, Lanuti P, Simeone P, Bologna G, Pieragostino D, Cufaro MC, Graziano V, Peri M, Di Marino P, De Tursi M, Grassadonia A, Rapposelli IG, Pierdomenico L, Ercolino E et al (2019) Circulating cancer stem cell-derived extracellular vesicles as a novel biomarker for clinical outcome evaluation. J Oncol 2019:5879616. https://doi.org/10.1155/2019/5879616 (eCollection 2019)
doi: 10.1155/2019/5879616
pubmed: 31827511
pmcid: 6885781
Rossi C, Cicalini I, Cufaro MC, Agnifili L, Mastropasqua L, Lanuti P, Marchisio M, De Laurenzi V (2019) Multi-omics approach for studying tears in treatment-naïve glaucoma patients. Int J Mol Sci. https://doi.org/10.3390/ijms20164029
doi: 10.3390/ijms20164029
pubmed: 31906232
pmcid: 6981573
Ciardiello C, Leone A, Lanuti P, Roca MS, Moccia T, Minciacchi VR, Minopoli M, Gigantino V, De Cecio R, Rippa M, Petti L, Capone F, Vitagliano C, Milone MR, Pucci B, Lombardi R, Iannelli F, Di Gennaro E, Bruzzese F, Marchisio M et al (2019) Large oncosomes overexpressing integrin alpha-V promote prostate cancer adhesion and invasion via AKT activation. J Exp Clin Cancer Res 38(1):317. https://doi.org/10.1186/s13046-019-1317-6
doi: 10.1186/s13046-019-1317-6
pubmed: 31319863
pmcid: 6639931
Zhang Y, Zhao C, Wei Y, Yang S, Cui C, Yang J, Zhang J, Qiao R (2018) Increased circulating microparticles in women with preeclampsia. Int J Lab Hematol 40(3):352–358. https://doi.org/10.1111/ijlh.12796
doi: 10.1111/ijlh.12796
pubmed: 29520961
Minciacchi VR, You S, Spinelli C, Morley S, Zandian M, Aspuria PJ, Cavallini L, Ciardiello C, Reis Sobreiro M, Morello M, Kharmate G, Jang SC, Kim DK, Hosseini-Beheshti E, Tomlinson Guns E, Gleave M, Gho YS, Mathivanan S (2015) Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles. Oncotarget 6(13):11327–11341
doi: 10.18632/oncotarget.3598
Vagner T, Spinelli C, Minciacchi VR, Balaj L, Zandian M, Conley A et al (2018) Large extracellular vesicles carry most of the tumour DNA circulating in prostate cancer patient plasma. J Extracell Vesicles 7(1):1505403. https://doi.org/10.1080/20013078.2018.1505403 (eCollection 2018)
doi: 10.1080/20013078.2018.1505403
pubmed: 30108686
pmcid: 6084494
Cufaro MC, Pieragostino D, Lanuti P, Rossi C, Cicalini I, Federici L et al (2019) Extracellular vesicles and their potential use in monitoring cancer progression and therapy: the contribution of proteomics. J Oncol 2019:1639854. https://doi.org/10.1155/2019/1639854 (eCollection 2019)
doi: 10.1155/2019/1639854
pubmed: 31281356
pmcid: 6590542
Bologna G, Lanuti P, D'Ambrosio P, Tonucci L, Pierdomenico L et al (2014) Water-soluble platinum phthalocyanines as potential antitumor agents. Biometals 27(3):575–589. https://doi.org/10.1007/s10534-014-9730-y (Epub 2014 Apr 4)
doi: 10.1007/s10534-014-9730-y
pubmed: 24699848
Poon IKH, Parkes MAF, Jiang L, Atkin-Smith GK, Tixeira R, Gregory CD, Ozkocak DC et al (2019) Moving beyond size and phosphatidylserine exposure: evidence for a diversity of apoptotic cell-derived extracellular vesicles in vitro. J Extracell Vesicles 8(1):1608786. https://doi.org/10.1080/20013078.2019.1608786 (eCollection 2019)
doi: 10.1080/20013078.2019.1608786
pubmed: 31069027
pmcid: 6493268
Kakarla R, Hur J, Kim YJ, Kim J, Chwae YJ (2020) Apoptotic cell-derived exosomes: messages from dying cells. Exp Mol Med 52(1):1–6. https://doi.org/10.1038/s12276-019-0362-8 (Epub 2020 Jan 9)
doi: 10.1038/s12276-019-0362-8
pubmed: 31915368
pmcid: 7000698
Coumans FAW, Brisson AR, Buzas EI, Dignat-George F, Drees EEE, El-Andaloussi S, Emanueli C, Gasecka A et al (2017) Methodological guidelines to study extracellular vesicles. Circ Res 120(10):1632–1648. https://doi.org/10.1161/CIRCRESAHA.117.309417
doi: 10.1161/CIRCRESAHA.117.309417
pubmed: 28495994
pmcid: 28495994
Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R, Antoniou A, Arab T, Archer F, Atkin-Smith GK, Ayre DC, Bach JM, Bachurski D, Baharvand H, Balaj L (2018) Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the international society for extracellular vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles 7(1):1535750. https://doi.org/10.1080/20013078.2018.1535750 (eCollection 2018)
doi: 10.1080/20013078.2018.1535750
pubmed: 30637094
pmcid: 30637094
Boukouris S, Mathivanan S (2015) Exosomes in bodily fluids are a highly stable resource of disease biomarkers. Proteom Clin Appl 9(3–4):358–367. https://doi.org/10.1002/prca.201400114 (Epub 2015 Mar 19)
doi: 10.1002/prca.201400114
Lv Y, Tan J, Miao Y, Zhang Q (2019) The role of microvesicles and its active molecules in regulating cellular biology. J Cell Mol Med 23(12):7894–7904. https://doi.org/10.1111/jcmm.14667 (Epub 2019 Sep 27)
doi: 10.1111/jcmm.14667
pubmed: 31559684
pmcid: 6850934
van Niel G, D'Angelo G, Raposo G (2018) Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 19(4):213–228. https://doi.org/10.1038/nrm.2017.125 (Epub 2018 Jan 17)
doi: 10.1038/nrm.2017.125
Dignat-George F, Boulanger CM (2011) The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 31:27
doi: 10.1161/ATVBAHA.110.218123
Lanuti P, Santilli F, Marchisio M, Pierdomenico L, Vitacolonna E, Santavenere E, Iacone A, Davì G, Romano M, Miscia S (2012) A novel flow cytometric approach to distinguish circulating endothelial cells from endothelial microparticles: relevance for the evaluation of endothelial dysfunction. J Immunol Methods 380(1–2):16–22. https://doi.org/10.1016/j.jim.2012.03.007 (Epub 2012 Mar 31)
doi: 10.1016/j.jim.2012.03.007
pubmed: 22484509
Markiewicz M, Richard E, Marks N, Ludwicka-Bradley A (2013) Impact of endothelial microparticles on coagulation, inflammation, and angiogenesis in age-related vascular diseases. J Aging Res 2013:734509
doi: 10.1155/2013/734509
Chironi GN, Boulanger CM, Simon A, Dignat-George F, Freyssinet JM, Tedgui A (2009) Endothelial microparticles in diseases. Cell Tissue Res 335(1):143–151
doi: 10.1007/s00441-008-0710-9
Burger D, Schock S, Thompson CS, Montezano AC, Hakim AM, Touyz RM (2013) Microparticles: biomarkers and beyond. Clin Sci (Lond) 124(7):423–441. https://doi.org/10.1042/CS20120309 (Review)
doi: 10.1042/CS20120309
Garcia-Contreras M, Brooks RW, Boccuzzi L, Robbins PD, Ricordi C (2017) Exosomes as biomarkers and therapeutic tools for type 1 diabetes mellitus. Eur Rev Med Pharmacol Sci 21(12):2940–2956
pubmed: 28682421
Al-Qaissi A, Papageorgiou M, Deshmukh H, Madden LA, Rigby A, Kilpatrick ES, Atkin SL, Sathyapalan T (2019) Effects of acute insulin induced hypoglycaemia on endothelial microparticles in adults with and without type 2 diabetes. Diabetes Obes Metab 21(3):533–540. https://doi.org/10.1111/dom.13548
doi: 10.1111/dom.13548
pubmed: 30264480
Huang-Doran I, Zhang CY, Vidal-Puig A (2017) Extracellular vesicles: novel mediators of cell communication in metabolic disease. Trends Endocrinol Metab 28(1):3–18. https://doi.org/10.1016/j.tem.2016.10.003
doi: 10.1016/j.tem.2016.10.003
pubmed: 27810172
Sáez T, Toledo F, Sobrevia L (2019) Impaired signalling pathways mediated by extracellular vesicles in diabesity. Mol Asp Med 66:13–20. https://doi.org/10.1016/j.mam.2018.12.001
doi: 10.1016/j.mam.2018.12.001
Grande R, Dovizio M, Marcone S, Szklanna PB, Bruno A, Ebhardt HA, Cassidy H, Ní Áinle F, Caprodossi A, Lanuti P, Marchisio M, Mingrone G, Maguire PB, Patrignani P (2019) Platelet-derived microparticles from obese individuals: characterization of number, size, proteomics, and crosstalk with cancer and endothelial cells. Front Pharmacol 10:7. https://doi.org/10.3389/fphar.2019.00007
doi: 10.3389/fphar.2019.00007
pubmed: 30723407
pmcid: 6349702
Jayabalan N, Lai A, Ormazabal V, Adam S, Guanzon D, Palma C, Scholz-Romero K, Lim R, Jansson T, McIntyre HD, Lappas M, Salomon C (2019) Adipose tissue exosomal proteomic profile reveals a role on placenta glucose metabolism in gestational diabetes mellitus. J Clin Endocrinol Metab 104(5):1735–1752. https://doi.org/10.1210/jc.2018-01599
doi: 10.1210/jc.2018-01599
pubmed: 30517676
Redman CW, Sargent IL (2008) Circulating microparticles in normal pregnancy and pre-eclampsia. Placenta 29(Suppl A):S73–S77. https://doi.org/10.1016/j.placenta.2007.11.016 (Epub 2008 Jan 14)
doi: 10.1016/j.placenta.2007.11.016
pubmed: 18192006
Salomon C, Scholz-Romero K, Sarker S, Sweeney E, Kobayashi M, Correa P, Longo S, Duncombe G, Mitchell MD, Rice GE, Illanes SE (2016) Gestational diabetes mellitus is associated with changes in the concentration and bioactivity of placenta-derived exosomes in maternal circulation across gestation. Diabetes 65(3):598–609. https://doi.org/10.2337/db15-0966
doi: 10.2337/db15-0966
pubmed: 26718504
Chiarello DI, Salsoso R, Toledo F, Mate A, Vázquez CM, Sobrevia L (2018) Foetoplacental communication via extracellular vesicles in normal pregnancy and preeclampsia. Mol Asp Med 60:69–80. https://doi.org/10.1016/j.mam.2017.12.002 (Epub 2017 Dec 13)
doi: 10.1016/j.mam.2017.12.002
International Association of Diabetes, and Pregnancy Study Groups Consensus Panel, Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, Damm P, Dyer AR, Leiva AD, Hod M, Kitzmiler JL, Lowe LP, McIntyre HD, Oats JJ, Omori Y, Schmidt MI (2010) International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 33(3):676–682
doi: 10.2337/dc09-1848
Pieragostino D, Lanuti P, Cicalini I, Cufaro MC, Ciccocioppo F, Ronci M, Simeone P, Onofrj M, van der Pol E, Fontana A, Marchisio M, Del Boccio P (2019) Proteomics characterization of extracellular vesicles sorted by flow cytometry reveals a disease-specific molecular cross-talk from cerebrospinal fluid and tears in multiple sclerosis. J Proteom 204:103403. https://doi.org/10.1016/j.jprot.2019.103403
doi: 10.1016/j.jprot.2019.103403
de Rond L, Coumans FAW, Nieuwland R, van Leeuwen TG, van der Pol E (2018) Deriving extracellular vesicle size from scatter intensities measured by flow cytometry. Curr Protoc Cytom 86(1):e43. https://doi.org/10.1002/cpcy.43
doi: 10.1002/cpcy.43
pubmed: 30168659
Lanuti P, Simeone P, Rotta G, Almici C, Avvisati G, Azzaro R, Bologna G, Budillon A, Di Cerbo M, Di Gennaro E, Di Martino ML, Diodato A, Doretto P, Ercolino E, Falda A et al (2018) A standardized flow cytometry network study for the assessment of circulating endothelial cell physiological ranges. Sci Rep 8(1):5823. https://doi.org/10.1038/s41598-018-24234-0
doi: 10.1038/s41598-018-24234-0
pubmed: 29643468
pmcid: 5895616
Maecker HT, Trotter J (2006) Flow cytometry controls, instrument setup, and the determination of positivity. Cytometry A 69(9):1037–1042. https://doi.org/10.1002/cyto.a.20333
doi: 10.1002/cyto.a.20333
pubmed: 16888771
Cossarizza A, Chang HD, Radbruch A, Acs A, Adam D, Adam-Klages S, Agace WW, Aghaeepour N, Akdis M, Allez M, Almeida LN, Alvisi G, Anderson G, Andrä I, Annunziato F, Anselmo A, Bacher P, Baldari CT, Bari S, Barnaba V, Barros-Martins J, Battistini L, Bauer W, Baumgart S, Baumgarth N et al (2019) Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition). Eur J Immunol 49(10):1457–1973. https://doi.org/10.1002/eji.201970107
doi: 10.1002/eji.201970107
pubmed: 7350392
pmcid: 7350392
Kuo WP, Tigges JC, Toxavidis V (2017) Red blood cells: a source of extracellular vesicles. Methods Mol Biol 1660:15–22. https://doi.org/10.1007/978-1-4939-7253-1_2
doi: 10.1007/978-1-4939-7253-1_2
pubmed: 28828644
Kandzija N, Zhang W, Motta-Mejia C, Mhlomi V, McGowan-Downey J, James T, Cerdeira AS, Tannetta D, Sargent I, Redman CW, Bastie CC, Vatish M (2019) Placental extracellular vesicles express active dipeptidyl peptidase IV; levels are increased in gestational diabetes mellitus. J Extracell Vesicles 8(1):1617000. https://doi.org/10.1080/20013078.2019.1617000 (eCollection 2019)
doi: 10.1080/20013078.2019.1617000
pubmed: 31164969
pmcid: 6534242
Xia Y, Zheng L, Zou X, Wang J, Zhong J, Zhong T (2019) Extracellular vesicles in type 2 diabetes mellitus: key roles in pathogenesis, complications, and therapy. J Extracell Vesicles 8(1):1625677
doi: 10.1080/20013078.2019.1625677
Boulanger CM, Amabile N, Tedgui A (2006) Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease. Hypertension 48(2):180–186
doi: 10.1161/01.HYP.0000231507.00962.b5
Akbar N, Azzimato V, Choudhury RP, Aouadi M (2019) Extracellular vesicles in metabolic disease. Diabetologia 62(12):2179–2187. https://doi.org/10.1007/s00125-019-05014-5
doi: 10.1007/s00125-019-05014-5
pubmed: 31690986
pmcid: 6861353
Jayabalan N, Nair S, Nuzhat Z, Rice GE, Zuñiga FA, Sobrevia L, Leiva A, Sanhueza C, Gutiérrez JA, Lappas M, Freeman DJ, Salomon C (2017) Cross talk between adipose tissue and placenta in obese and gestational diabetes mellitus pregnancies via exosomes. Front Endocrinol (Lausanne) 8:239. https://doi.org/10.3389/fendo.2017.00239 (eCollection 2017)
doi: 10.3389/fendo.2017.00239
Kranendonk ME, Visseren FL, van Herwaarden JA, Nolte-'t Hoen EN, de Jager W, Wauben MH, Kalkhoven E (2014) Effect of extracellular vesicles of human adipose tissue on insulin signaling in liver and muscle cells. Obesity (Silver Spring) 22(10):2216–2223. https://doi.org/10.1002/oby.20847 (Epub 2014 Jul 17)
doi: 10.1002/oby.20847
Ying W, Riopel M, Bandyopadhyay G, Dong Y, Birmingham A, Seo JB, Ofrecio JM, Wollam J, Hernandez-Carretero A, Fu W, Li P, Olefsky JM (2017) Adipose tissue macrophage-derived exosomal miRNAs can modulate in vivo and in vitro insulin sensitivity. Cell 171(2):372–384.e12
doi: 10.1016/j.cell.2017.08.035
Nair S, Jayabalan N, Guanzon D, Palma C, Scholz-Romero K, Elfeky O, Zuñiga F, Ormazabal V, Diaz E, Rice GE, Duncombe G, Jansson T, McIntyre HD, Lappas M, Salomon C (2018) Human placental exosomes in gestational diabetes mellitus carry a specific set of miRNAs associated with skeletal muscle insulin sensitivity. Clin Sci (Lond) 132(22):2451–2467. https://doi.org/10.1042/CS20180487 (Print 2018 Nov 30)
doi: 10.1042/CS20180487
Meziani F, Tesse A, David E, Martinez MC, Wangensten R, Schneider F, Andriantsitohaina R (2006) Shed membrane particles from pre-eclamptic women generate vascular wall inflammation and blunt vascular contractility. Am J Pathol 169:1473–1483
doi: 10.2353/ajpath.2006.051304
Sabapatha A, Gercel-Taylor C, Taylor DD (2006) Specific isolation of placenta-derived exosomes from the circulation of pregnant women and their immunoregulatory consequences. Am J Reprod Immunol 56:345–355
doi: 10.1111/j.1600-0897.2006.00435.x
Salomon C, Torres MJ, Kobayashi M et al (2014) A gestational profile of placental exosomes in maternal plasma and their effects on endothelial cell migration. PLoS ONE 9:e98667
doi: 10.1371/journal.pone.0098667
Mitchell MD, Peiris HN, Kobayashi M, Koh YQ, Duncombe G, Illanes SE, Rice GE, Salomon C (2015) Placental exosomes in normal and complicated pregnancy. Am J Obstet Gynecol 213(4 Suppl):S173–S181. https://doi.org/10.1016/j.ajog.2015.07.001
doi: 10.1016/j.ajog.2015.07.001
pubmed: 26428497
Yang C, Song G, Lim W (2019) Effects of extracellular vesicles on placentation and pregnancy disorders. Reproduction. https://doi.org/10.1530/REP-19-0147 (2019 Jun 1)
doi: 10.1530/REP-19-0147
pubmed: 31756167
pmcid: 6826174
Rice GE, Scholz-Romero K, Sweeney E, Peiris H, Kobayashi M, Duncombe G, Mitchell MD, Salomon C (2015) The effect of glucose on the release and bioactivity of exosomes from first trimestertrophoblast cells. J Clin Endocrinol Metab 100(10):E1280–E1288. https://doi.org/10.1210/jc.2015-2270 (Epub 2015 Aug 4)
doi: 10.1210/jc.2015-2270
pubmed: 26241326
Elfeky O, Longo S, Lai A, Rice GE, Salomon C (2017) Influence of maternal BMI on the exosomal profile during gestation and their role on maternal systemic inflammation. Placenta 50:60–69. https://doi.org/10.1016/j.placenta.2016.12.020 (Epub 2016 Dec 21)
doi: 10.1016/j.placenta.2016.12.020
pubmed: 28161063
Luo SS, Ishibashi O, Ishikawa G, Ishikawa T, Katayama A, Mishima T, Takizawa T, Shigihara T, Goto T, Izumi A, Ohkuchi A, Matsubara S, Takeshita T, Takizawa T (2009) Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol Reprod 81(4):717–729. https://doi.org/10.1095/biolreprod.108.075481
doi: 10.1095/biolreprod.108.075481
pubmed: 19494253
Gillet V, Ouellet A, Stepanov Y, Rodosthenous RS, Croft EK, Brennan K, Abdelouahab N, Baccarelli A, Takser L (2019) miRNA profiles in extracellular vesicles from serum early in pregnancies complicated by gestational diabetes mellitus. J Clin Endocrinol Metab 104(11):5157–5169. https://doi.org/10.1210/jc.2018-02693
doi: 10.1210/jc.2018-02693
pubmed: 31058973
pmcid: 6760296
Jayabalan N, Lai A, Nair S, Guanzon D, Scholz-Romero K, Palma C, McIntyre HD, Lappas M, Salomon C (2019) Quantitative proteomics by SWATH-MS suggest an association between circulating exosomesand maternal metabolic changes in gestational diabetes mellitus. Proteomics 19(1–2):e1800164. https://doi.org/10.1002/pmic.201800164
doi: 10.1002/pmic.201800164
pubmed: 30536821