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Vol 94, No 10 (2023)
Research paper
Published online: 2022-11-21
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Microvesicles released from ectopic endometrial foci as a potential biomarker of endometriosis

Magdalena Kajdos1, Jacek Szymanski2, Hanna Jerczynska2, Tomasz Stetkiewicz1, Jacek R. Wilczynski3
·
Pubmed: 36448351
·
Ginekol Pol 2023;94(10):780-791.
Affiliations
  1. Department of Gynecology and Gynecological Oncology, Polish Mother Memorial Hospital Research Institute, Lodz, Poland, Poland
  2. Central Research Laboratory of Medical University in Lodz, Poland, Poland
  3. Department of Operative and Oncological Gynecology of Medical University in Lodz, Poland, Poland

open access

Vol 94, No 10 (2023)
ORIGINAL PAPERS Gynecology
Published online: 2022-11-21

Abstract

Objectives: Angiogenesis is engaged in endometriosis. It is regulated by regulatory factors and cytokines, transported in microvesicles. The purpose was to investigate the presence of MVs with vascular endothelial growth factor (VEGF) and metalloproteinase-9 (MMP-9) in peripheral blood and peritoneal fluid of women operated on for endometrioma or teratoma Material and methods: Microvesicles (MVs) were determined in blood samples and peritoneal fluid samples collected from women aged 20–60 years operated on for endometriosis (test group) and teratoma (control group). The final investigations were performed on 47 patients, who qualified for the study based on the meticulous inclusion criteria. MVs were analyzed by flow cytometry (FACS) using annexin V, antibodies for molecules characteristic of cells from endometriosis foci (keratin 18 (K18), CD105, CD146), and antibodies for intraepithelial vascular growth factor VEGF and metalloproteinase-9 (MMP-9). The sample was double “reading” using flow cytometry (FACSCantoII).  Results: Cytometry analysis confirmed MVs’ presence in plasma and peritoneal fluid collected from patients with both endometriosis and teratomas. A statistically significant higher level of AnnexinV (+) MVs were observed in plasma samples of endometriosis patients. In the control group, there was a higher percentage of double-positive VEGF (+)/MMP-9 (+) and single MMP-9 (+) positive MVs in the serum. In the peritoneal fluid higher frequency of double-positive VEGF (+)/MMP-9 (+) MVs were found in the control group. However, the amount of VEGF (+) / MMP-9 (+) MVs object did not enable to differentiate between the test and control groups. The study was the first, in which MVs were confirmed in plasma and peritoneal fluid in benign adnexa tumors.  Conclusions: Microvesicles are present in peripheral blood and peritoneal fluid samples collected from patients with endometriosis and teratomas. Microvesicles with proangiogenic factors (VEGF and MMP-9) are more abundant in blood and peritoneal fluid samples from patients with teratomas.

Abstract

Objectives: Angiogenesis is engaged in endometriosis. It is regulated by regulatory factors and cytokines, transported in microvesicles. The purpose was to investigate the presence of MVs with vascular endothelial growth factor (VEGF) and metalloproteinase-9 (MMP-9) in peripheral blood and peritoneal fluid of women operated on for endometrioma or teratoma Material and methods: Microvesicles (MVs) were determined in blood samples and peritoneal fluid samples collected from women aged 20–60 years operated on for endometriosis (test group) and teratoma (control group). The final investigations were performed on 47 patients, who qualified for the study based on the meticulous inclusion criteria. MVs were analyzed by flow cytometry (FACS) using annexin V, antibodies for molecules characteristic of cells from endometriosis foci (keratin 18 (K18), CD105, CD146), and antibodies for intraepithelial vascular growth factor VEGF and metalloproteinase-9 (MMP-9). The sample was double “reading” using flow cytometry (FACSCantoII).  Results: Cytometry analysis confirmed MVs’ presence in plasma and peritoneal fluid collected from patients with both endometriosis and teratomas. A statistically significant higher level of AnnexinV (+) MVs were observed in plasma samples of endometriosis patients. In the control group, there was a higher percentage of double-positive VEGF (+)/MMP-9 (+) and single MMP-9 (+) positive MVs in the serum. In the peritoneal fluid higher frequency of double-positive VEGF (+)/MMP-9 (+) MVs were found in the control group. However, the amount of VEGF (+) / MMP-9 (+) MVs object did not enable to differentiate between the test and control groups. The study was the first, in which MVs were confirmed in plasma and peritoneal fluid in benign adnexa tumors.  Conclusions: Microvesicles are present in peripheral blood and peritoneal fluid samples collected from patients with endometriosis and teratomas. Microvesicles with proangiogenic factors (VEGF and MMP-9) are more abundant in blood and peritoneal fluid samples from patients with teratomas.

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Keywords

endometriosis; microvesicles; angiogenesis; VEGF MMP-9

About this article
Title

Microvesicles released from ectopic endometrial foci as a potential biomarker of endometriosis

Journal

Ginekologia Polska

Issue

Vol 94, No 10 (2023)

Article type

Research paper

Pages

780-791

Published online

2022-11-21

Page views

712

Article views/downloads

539

DOI

10.5603/GP.a2022.0096

Pubmed

36448351

Bibliographic record

Ginekol Pol 2023;94(10):780-791.

Keywords

endometriosis
microvesicles
angiogenesis
VEGF MMP-9

Authors

Magdalena Kajdos
Jacek Szymanski
Hanna Jerczynska
Tomasz Stetkiewicz
Jacek R. Wilczynski

References (108)
  1. Giusti I, D'Ascenzo S, Dolo V. Microvesicles as potential ovarian cancer biomarkers. Biomed Res Int. 2013; 2013: 703048.
  2. Stern RC, Dash R, Bentley RC, et al. Malignancy in endometriosis: frequency and comparison of ovarian and extraovarian types. Int J Gynecol Pathol. 2001; 20(2): 133–139.
  3. D’Alterio M, Saponara S, Agus M, et al. Medical and surgical interventions to improve the quality of life for endometriosis patients: a systematic review. Gynecol Surg. 2021; 18(1).
  4. Hadfield RM, Mardon HJ, Barlow DH, et al. Endometriosis in monozygotic twins. Fertil Steril. 1997; 68(5): 941–942.
  5. Lauchlan SC. The secondary Müllerian system. Obstet Gynecol Surv. 1972; 27(3): 133–146.
  6. Inal JM, Kosgodage U, Azam S, et al. Blood/plasma secretome and microvesicles. Biochim Biophys Acta. 2013; 1834(11): 2317–2325.
  7. Meckes DG, Raab-Traub N. Microvesicles and viral infection. J Virol. 2011; 85(24): 12844–12854.
  8. Jayachandran M, Litwiller RD, Owen WG, et al. Characterization of blood borne microparticles as markers of premature coronary calcification in newly menopausal women. Am J Physiol Heart Circ Physiol. 2008; 295(3): H931–H938.
  9. D'Souza-Schorey C, Clancy JW. Tumor-derived microvesicles: shedding light on novel microenvironment modulators and prospective cancer biomarkers. Genes Dev. 2012; 26(12): 1287–1299.
  10. Frey GH. The Familial Occurrence of Endometriosis. Am J Obstet Gynecol. 1957; 73(2): 418–421.
  11. Gardiner L. Endometriosis. Obstet Gynecol. 1953; 1: 615.
  12. Ranney B. Endometriosis. IV. Hereditary tendency. Obstet Gynecol. 1971; 37(5): 734–737.
  13. Practise Committee of American Society for Reproductive Medicine. Endometriosis and infertility. Fertility and Sterility. 2006; 86(5): S156–S160.
  14. Bulun SE. Endometriosis. N Engl J Med. 2009; 360(3): 268–279.
  15. Hu Z, Mamillapalli R, Taylor HS. Increased circulating miR-370-3p regulates steroidogenic factor 1 in endometriosis. Am J Physiol Endocrinol Metab. 2019; 316(3): E373–E382.
  16. Saha R, Pettersson HJ, Svedberg P, et al. Heritability of endometriosis. Fertil Steril. 2015; 104(4): 947–952.
  17. Wilczyński JR. Angiogeneza w ogniskach endometrozy. In: Radowicki S, Szyłło K. ed. Endometrioza. Diagnostyka i leczenie. Elsevier Urban & Partner, Wrocław 2013: 47–55.
  18. Kyama CM, Debrock S, Mwenda JM, et al. Potential involvement of the immune system in the development of endometriosis. Reprod Biol Endocrinol. 2003; 1: 123.
  19. McLaren J, Prentice A, Charnock-Jones DS, et al. Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids. J Clin Invest. 1996; 98(2): 482–489.
  20. Tariverdian N, Theoharides TC, Siedentopf F, et al. Neuroendocrine-immune disequilibrium and endometriosis: an interdisciplinary approach. Semin Immunopathol. 2007; 29(2): 193–210.
  21. Gargett CE, Masuda H. Adult stem cells in the endometrium. Mol Hum Reprod. 2010; 16(11): 818–834.
  22. Shifren JL. Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis. Journal of Clinical Endocrinology & Metabolism. 1996; 81(8): 3112–3118.
  23. Mueller M, Lebovic D, Garrett E, et al. Neutrophils infiltrating the endometrium express vascular endothelial growth factor: potential role in endometrial angiogenesis. Fertil Steril. 2000; 74(1): 107–112.
  24. Merrill JA. Endometrial induction of endometriosis across Millipore filters. Am J Obstet Gynecol. 1966; 94: 780–790.
  25. Antoniou AC, Easton DF. Models of genetic susceptibility to breast cancer. Oncogene. 2006; 25(43): 5898–5905.
  26. Radowicki S, Szyłło K. Endometrioza. Diagnostyka i leczenie. Elsevier Urban & Partner, Wrocław 2013: 6–18.
  27. Forehand JR, Johnston RB, Bomalski JS. Phospholipase A2 activity in human neutrophils. J Immunol. 1993; 151: 4918–4925.
  28. Garcia-Velasco J, Arici A. Interleukin-8 stimulates the adhesion of endometrial stromal cells to fibronectin. Fertil Steril. 1999; 72(2): 336–340.
  29. Koninckx PR, Kennedy SH, Barlow DH. Pathogenesis of Endometriosis: The Role of Peritoneal Fluid. Gynecol Obstet Invest. 1999; 47(Suppl. 1): 23–33.
  30. Maathuis JB, Van Look PF, Michie EA. Changes in volume, total protein and ovarian steroid concentrations of peritoneal fluid throughout the human menstrual cycle. J Endocrinol. 1978; 76(1): 123–133.
  31. Syrop CH, Halme J. Peritoneal fluid environment and infertility. Fertil Steril. 1987; 48(1): 1–9.
  32. Polak G, Kotarski J. The role of peritoneal fluid in pathogenesis of endometriosis, Endometriosis. Diagnosis and Treatment. 2013: 1–5.
  33. van der Linden PJ. Theories on the pathogenesis of endometriosis. Hum Reprod. 1996; 11 Suppl 3: 53–65.
  34. Taylor RN, Yu J, Torres PB, et al. Mechanistic and therapeutic implications of angiogenesis in endometriosis. Reprod Sci. 2009; 16(2): 140–146.
  35. Laganà AS, Garzon S, Götte M, et al. The Pathogenesis of Endometriosis: Molecular and Cell Biology Insights. Int J Mol Sci. 2019; 20(22).
  36. Die epithelialen Eierstocksgeschwülste, insbesondere die Kystome. Archiv für Gynäekologie. 1870; 1(2): 252–316.
  37. Miyazaki K, Dyson MT, Coon V JS, et al. Generation of Progesterone-Responsive Endometrial Stromal Fibroblasts from Human Induced Pluripotent Stem Cells: Role of the WNT/CTNNB1 Pathway. Stem Cell Reports. 2018; 11(5): 1136–1155.
  38. Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol. 1967; 13(3): 269–288.
  39. Moen MH, Magnus P. The familial risk of endometriosis. Acta Obstet Gynecol Scand. 1993; 72(7): 560–564.
  40. Simpson J, Elias S, Malinak L, et al. Heritable aspects of endometriosis. Am J Obstet Gynecol. 1980; 137(3): 327–331.
  41. Maliniak LR, Elias S, Simpson JL. Heritable aspects of endometriosis. II. Clinical characteristics of familial endometriosis. Am J Obstet Gynecol. 1980; 137: 332–338.
  42. Reis RD, Sá MS, Moura MDe, et al. Familial risk among patient with endometriosis. J Assist Reprod Genet. 1999; 16(9): 500–503.
  43. Kashima K, Ishimaru T, Okamura H, et al. Familial risk among Japanese patients with endometriosis. Int J Gynaecol Obstet. 2003; 84(1): 61–64.
  44. Stefansson H, Geirsson RT, Steinthorsdottir V, et al. Genetic factors contribute to the risk of developing endometriosis. Hum Reprod. 2002; 17(3): 555–559.
  45. Zondervan KT, Weeks DE, Colman R, et al. Familial aggregation of endometriosis in a large pedigree of rhesus macaques. Hum Reprod. 2004; 19(2): 448–455.
  46. Albertsen HM, Chettier R, Farrington P, et al. Genome-wide association study link novel loci to endometriosis. PLoS One. 2013; 8(3): e58257.
  47. Simpson RJ, Lim JWe, Moritz RL, et al. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics. 2009; 6(3): 267–283.
  48. Hugel B, Martínez MC, Kunzelmann C, et al. Membrane microparticles: two sides of the coin. Physiology (Bethesda). 2005; 20: 22–27.
  49. Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007; 9(6): 654–659.
  50. Skog J, Würdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008; 10(12): 1470–1476.
  51. Pisetsky DS, Gauley J, Ullal AJ. Microparticles as a source of extracellular DNA. Immunol Res. 2011; 49(1-3): 227–234.
  52. Irungu S, Mavrelos D, Worthington J, et al. Discovery of non-invasive biomarkers for the diagnosis of endometriosis. Clin Proteomics. 2019; 16: 14.
  53. Ballard K, Lowton K, Wright J. What's the delay? A qualitative study of women's experiences of reaching a diagnosis of endometriosis. Fertil Steril. 2006; 86(5): 1296–1301.
  54. Hadfield R, Mardon H, Barlow D, et al. Delay in the diagnosis of endometriosis: a survey of women from the USA and the UK. Hum Reprod. 1996; 11(4): 878–880.
  55. Husby GK, Haugen RS, Moen MH. Diagnostic delay in women with pain and endometriosis. Acta Obstet Gynecol Scand. 2003; 82(7): 649–653.
  56. Becker C, Bokor A, Heikinheimo O, et al. ESHRE guideline: endometriosis. Human Reproduction Open. 2022; 2022(2).
  57. Wu CY, Wu JD, Chen CC. The Association of Ovarian Teratoma and Anti-N-Methyl-D-Aspartate Receptor Encephalitis: An Updated Integrative Review. Int J Mol Sci. 2021; 22(20).
  58. Kyama C, Debrock S, Mwenda J, et al. Potential involvement of the immune system in the development of endometriosis. Reprod Biol Endocrinol. 2003; 1(1): 123.
  59. Machado DE, Berardo PT, Palmero CY, et al. Higher expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 (Flk-1) and metalloproteinase-9 (MMP-9) in a rat model of peritoneal endometriosis is similar to cancer diseases. J Exp Clin Cancer Res. 2010; 29: 4.
  60. Witwer KW, Buzás EI, Bemis LT, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013; 2.
  61. Van Deun J, Mestdagh P, Sormunen R, et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles. 2014; 3.
  62. Dziechciowski M, Zapala B, Skotniczny K, et al. Diagnostic and prognostic relevance of microparticles in peripheral and uterine blood of patients with endometrial cancer. Ginekol Pol. 2018; 89(12): 682–687.
  63. Mancuso P, Calleri A, Cassi C, et al. Circulating endothelial cells as a novel marker of angiogenesis. Adv Exp Med Biol. 2003; 522: 83–97.
  64. Beerepoot LV, Mehra N, Vermaat JSP, et al. Increased levels of viable circulating endothelial cells are an indicator of progressive disease in cancer patients. Ann Oncol. 2004; 15(1): 139–145.
  65. Mancuso P, Burlini A, Pruneri G, et al. Resting and activated endothelial cells are increased in the peripheral blood of cancer patients. Blood. 2001; 97(11): 3658–3661.
  66. Nielsen CT, Østergaard O, Stener L, et al. Increased IgG on cell-derived plasma microparticles in systemic lupus erythematosus is associated with autoantibodies and complement activation. Arthritis Rheum. 2012; 64(4): 1227–1236.
  67. Biró E, Nieuwland R, Tak PP, et al. Activated complement components and complement activator molecules on the surface of cell-derived microparticles in patients with rheumatoid arthritis and healthy individuals. Ann Rheum Dis. 2007; 66(8): 1085–1092.
  68. van Eijk IC, Tushuizen ME, Sturk A, et al. Circulating microparticles remain associated with complement activation despite intensive anti-inflammatory therapy in early rheumatoid arthritis. Ann Rheum Dis. 2010; 69(7): 1378–1382.
  69. Renner B, Klawitter J, Goldberg R, et al. Cyclosporine induces endothelial cell release of complement-activating microparticles. J Am Soc Nephrol. 2013; 24(11): 1849–1862.
  70. Yin W, Ghebrehiwet B, Peerschke EIB. Expression of complement components and inhibitors on platelet microparticles. Platelets. 2008; 19(3): 225–233.
  71. Yáñez-Mó M, Siljander PRM, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015; 4: 27066.
  72. Hargett LA, Bauer NN. On the origin of microparticles: From "platelet dust" to mediators of intercellular communication. Pulm Circ. 2013; 3(2): 329–340.
  73. Cordazzo C, Neri T, Petrini S, et al. Angiotensin II induces the generation of procoagulant microparticles by human mononuclear cells via an angiotensin type 2 receptor-mediated pathway. Thromb Res. 2013; 131(4): e168–e174.
  74. Preston RA, Jy W, Jimenez JJ, et al. Effects of severe hypertension on endothelial and platelet microparticles. Hypertension. 2003; 41(2): 211–217.
  75. Voukalis C, Shantsila E, Lip GYH. Microparticles and cardiovascular diseases. Ann Med. 2019; 51(3-4): 193–223.
  76. Hsu CY, Huang PH, Chiang CH, et al. Increased circulating endothelial apoptotic microparticle to endothelial progenitor cell ratio is associated with subsequent decline in glomerular filtration rate in hypertensive patients. PLoS One. 2013; 8(7): e68644.
  77. Huang PH, Huang SS, Chen YH, et al. Increased circulating CD31+/annexin V+ apoptotic microparticles and decreased circulating endothelial progenitor cell levels in hypertensive patients with microalbuminuria. J Hypertens. 2010; 28(8): 1655–1665.
  78. Ayers L, Kohler M, Harrison P, et al. Measurement of circulating cell-derived microparticles by flow cytometry: sources of variability within the assay. Thromb Res. 2011; 127(4): 370–377.
  79. Young TN, Rodriguez GC, Rinehart AR, et al. Characterization of gelatinases linked to extracellular matrix invasion in ovarian adenocarcinoma: purification of matrix metalloproteinase 2. Gynecol Oncol. 1996; 62(1): 89–99.
  80. Dolo V, D'Ascenzo S, Violini S, et al. Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin Exp Metastasis. 1999; 17(2): 131–140.
  81. Horstman LL, Jy W, Jimenez JJ, et al. Measuring circulating cell-derived microparticles. J Thromb Haemost. 2004; 2(10): 1842–1851.
  82. van der Pol E, Hoekstra AG, Sturk A, et al. Optical and non-optical methods for detection and characterization of microparticles and exosomes. J Thromb Haemost. 2010; 8(12): 2596–2607.
  83. Dey-Hazra E, Hertel B, Kirsch T, et al. Detection of circulating microparticles by flow cytometry: influence of centrifugation, filtration of buffer, and freezing. Vasc Health Risk Manag. 2010; 6: 1125–1133.
  84. Chandler WL, Yeung W, Tait JF. A new microparticle size calibration standard for use in measuring smaller microparticles using a new flow cytometer. J Thromb Haemost. 2011; 9(6): 1216–1224.
  85. Horstman LL, Jy W, Jimenez JJ, et al. Measuring circulating cell-derived microparticles. J Thromb Haemost. 2004; 2(10): 1842–1851.
  86. Daniel L, Fakhouri F, Joly D, et al. Increase of circulating neutrophil and platelet microparticles during acute vasculitis and hemodialysis. Kidney Int. 2006; 69(8): 1416–1423.
  87. Lynch SF, Ludlam CA. Plasma microparticles and vascular disorders. Br J Haematol. 2007; 137(1): 36–48.
  88. Erdbruegger U, Grossheim M, Hertel B, et al. Diagnostic role of endothelial microparticles in vasculitis. Rheumatology (Oxford). 2008; 47(12): 1820–1825.
  89. Shah MD, Bergeron AL, Dong JF, et al. Flow cytometric measurement of microparticles: pitfalls and protocol modifications. Platelets. 2008; 19(5): 365–372.
  90. Buschmann D, Kirchner B, Hermann S, et al. Erratum: Evaluation of serum extracellular vesicle isolation methods for profiling miRNAs by Next-Generation Sequencing. J Extracell Vesicles. 2019; 8(1): 1581487.
  91. Filella M, Zhang J, Newman M, et al. Analytical applications of photon correlation spectroscopy for size distribution measurements of natural colloidal suspensions: capabilities and limitations. Colloids Surf A Physicochem Eng Asp. 1997; 120(1-3): 27–46.
  92. Joop K, Berckmans R, Nieuwland R, et al. Microparticles from Patients with Multiple Organ Dysfunction Syndrome and Sepsis Support Coagulation through Multiple Mechanisms. Thrombosis and Haemostasis. 2017; 85(05): 810–820.
  93. Nozaki T, Sugiyama S, Sugamura K, et al. Prognostic value of endothelial microparticles in patients with heart failure. Eur J Heart Fail. 2010; 12(11): 1223–1228.
  94. Zhang EG, Smith SK, Charnock-Jones DS. Expression of CD105 (endoglin) in arteriolar endothelial cells of human endometrium throughout the menstrual cycle. Reproduction. 2002; 124(5): 703–711.
  95. Gold LI, Saxena B, Mittal KR, et al. Increased expression of transforming growth factor β isoforms and basic fibroblast growth factor in complex hyperplasia and adenocarcinoma of the endometrium: evidence for paracrine and autocrine action. Cancer Resaerch. 1994; 54: 2347–2358.
  96. Ghosh AK, Secreto CR, Knox TR, et al. Circulating microvesicles in B-cell chronic lymphocytic leukemia can stimulate marrow stromal cells: implications for disease progression. Blood. 2010; 115(9): 1755–1764.
  97. György B, Szabó TG, Turiák L, et al. Improved flow cytometric assessment reveals distinct microvesicle (cell-derived microparticle) signatures in joint diseases. PLoS One. 2012; 7(11): e49726.
  98. Liu R, Klich I, Ratajczak J, et al. Erythrocyte-derived microvesicles may transfer phosphatidylserine to the surface of nucleated cells and falsely 'mark' them as apoptotic. Eur J Haematol. 2009; 83(3): 220–229.
  99. Connor DE, Exner T, Ma DD, et al. The majority of circulating platelet-derived microparticles fail to bind annexin V, lack phospholipid-dependent procoagulant activity and demonstrate greater expression of glycoprotein Ib. Thromb Haemost. 2010; 103(5): 1044–1052.
  100. Boulanger CM, Amabile N, Tedgui A. Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease. Hypertension. 2006; 48(2): 180–186.
  101. Amabile N, Guérin AP, Tedgui A, et al. Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. J Am Soc Nephrol. 2005; 16(11): 3381–3388.
  102. Budoni M, Fierabracci A, Luciano R, et al. The Immunosuppressive Effect of Mesenchymal Stromal Cells on B Lymphocytes is Mediated by Membrane Vesicles. Cell Transplant. 2013; 22(2): 369–379.
  103. Ng YH, Rome S, Jalabert A, et al. Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS One. 2013; 8(3): e58502.
  104. Harp D, Driss A, Mehrabi S, et al. Exosomes derived from endometriotic stromal cells have enhanced angiogenic effects in vitro. Cell Tissue Res. 2016; 365(1): 187–196.
  105. Tao H, Chen X, Wei A, et al. Comparison of Teratoma Formation between Embryonic Stem Cells and Parthenogenetic Embryonic Stem Cells by Molecular Imaging. Stem Cells Int. 2018; 2018: 7906531.
  106. Shomali N, Hemmatzadeh M, Yousefzadeh Y, et al. Exosomes: Emerging biomarkers and targets in folliculogenesis and endometriosis. J Reprod Immunol. 2020; 142: 103181.
  107. Ito T, Sun Li, Henriquez R, et al. A Carbon Nanotube-Based Coulter Nanoparticle Counter. Acc Chem Res. 2004; 37(12): 937–945.
  108. Saleh OA, Sohn LL. Quantitative sensing of nanoscale colloids using a microchip Coulter counter. Rev Sci Instrum. 2001; 72(12): 4449–4451.

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