Биологические мембраны: Журнал мембранной и клеточной биологии, 2022, T. 39, № 6, стр. 431-439

Прокоагулянтные свойства внеклеточных везикул при нормальной и патологической беременности

Е. М. Кольцова ab*, А. А. Мартьянов abc, Н. А. Подоплелова ab

a Национальный медицинский исследовательский центр детской гематологии, онкологии и иммунологии им. Дмитрия Рогачева
117997 Москва, Россия

b Центр теоретических проблем физико-химической фармакологии РАН
109029 Москва, Россия

c Институт биохимической физики им. Н.М. Эмануэля РАН
119334 Москва, Россия

* E-mail: ekaterina_koltsova@bk.ru

Поступила в редакцию 25.11.2021
После доработки 16.04.2022
Принята к публикации 17.04.2022

Аннотация

Внеклеточные везикулы – это двухслойные мембранные липидные структуры без ядер, которые высвобождаются из различных клеток в результате физиологических и метаболических изменений. Они играют важную роль в межклеточной коммуникации посредством передачи широкого спектра биоактивных молекул, способствуя регуляции различных физиологических и патологических процессов. Внеклеточные везикулы могут обладать прокоагулянтными свойствами вследствие наличия фосфатидилсерина, ускоряющего реакции свертывания, на внешнем слое мембраны, а также экспрессии тканевого фактора, активирующего свертывание по внешнему пути, на поверхности некоторых везикул. В большом количестве клинических и экспериментальных исследований показано, что при различных патологиях и специфических физиологических состояниях, включая состояние беременности, концентрации внеклеточных везикул существенно превышают концентрации у здоровых добровольцев, что теоретически может являться одним из факторов развития гиперкоагуляционных состояний. Данный обзор будет сосредоточен на описании прокоагулянтных свойств внеклеточных везикул различного происхождения при нормальной и патологической беременности.

Ключевые слова: гемостаз, везикулы, беременность, плацента, тромбин, гиперкоагуляция

Список литературы

  1. Théry C., Witwer K.W., Aikawa E., Alcaraz M.J., Anderson J.D., Andriantsitohaina R., Antoniou A., Arab T., Archer F., Atkin-Smith G.K., Ayre D.C., Bach J.M., Bachurski D., Baharvand H., Balaj L., et al. 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

  2. Yáñez-Mó M., Siljander P.R., Andreu Z., Zavec A.B., Borràs F.E., Buzas E.I., Buzas K., Casal E., Cappello F., Carvalho J., Colás E., Cordeiro-da Silva A., Fais S., Falcon-Perez J.M., Ghobrial I.M., et al. 2015. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. vesicles. 4 (2015), 27066. https://doi.org/10.3402/jev.v4.27066

  3. Colombo M., Raposo G., Théry C. 2014. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30, 255–289. https://doi.org/10.1146/annurev-cellbio-101512-122326

  4. Rojalin T., Phong B., Koster H.J., Carney R.P. 2019. Nanoplasmonic approaches for sensitive detection and molecular characterization of extracellular vesicles. Front. Chem. 7, 279. https://doi.org/10.3389/fchem.2019.00279

  5. Raposo G., Stoorvogel W. 2013. Extracellular vesicles: Exosomes, microvesicles, and friends. J. Cell Biol. 200 (4), 373–383. https://doi.org/10.1083/jcb.201211138

  6. Bebelman M.P., Smit M.J., Pegtel D.M., Baglio S.R. 2018. Biogenesis and function of extracellular vesicles in cancer. Pharmacol. Ther. 188, 1–11. https://doi.org/10.1016/j.pharmthera.2018.02.013

  7. Cretoiu D., Xu J., Xiao J., Cretoiu S.M. 2016. Telocytes and their extracellular vesicles-evidence and hypotheses. Int. J. Mol. Sci. 17 (8), 1322. https://doi.org/10.3390/ijms17081322

  8. Wickman G., Julian L., Olson M.F. 2012. How apoptotic cells aid in the removal of their own cold dead bodies. Cell Death Differ. 19 (5), 735–742. https://doi.org/10.1038/cdd.2012.25

  9. Tannetta D., Dragovic R., Alyahyaei Z., Southcombe J. 2014. Extracellular vesicles and reproduction–promotion of successful pregnancy. Cell. Mol. Immunol. 11 (6), 548–563. https://doi.org/10.1038/cmi.2014.42

  10. Burnett L.A., Nowak R.A. 2016. Exosomes mediate embryo and maternal interactions at implantation and during pregnancy. Front. Biosci. 8 (1), 79–96. https://doi.org/10.2741/s448

  11. Chiarello D.I., Salsoso R., Toledo F., Mate A., Vázquez C.M., Sobrevia L. 2018. Foetoplacental communication via extracellular vesicles in normal pregnancy and preeclampsia. Mol. Aspects Med. 60, 69–80. https://doi.org/10.1016/j.mam.2017.12.002

  12. Sheller-Miller S., Choi K., Choi C., Menon R. 2019. Cyclic-recombinase-reporter mouse model to determine exosome communication and function during pregnancy. Am. J. Obstet. Gynecol. 221 (5), 502.e1–502.e12. https://doi.org/10.1016/j.ajog.2019.06.010

  13. Han C., Han L., Huang P., Chen Y., Wang Y., Xue F. 2019. Syncytiotrophoblast-derived extracellular vesicles in pathophysiology of preeclampsia. Front. Physiol. 10, 1236. https://doi.org/10.3389/fphys.2019.01236

  14. James-Allan L.B., Devaskar S.U. 2021. Extracellular vesicles and their role in gestational diabetes mellitus. Placenta. 113, 15–22. https://doi.org/10.1016/j.placenta.2021.02.012

  15. Menon R, Shahin H. 2021. Extracellular vesicles in spontaneous preterm birth. Am. J. Reprod. Immunol. 85(2), 139–148. https://doi.org/10.1111/aji.13353

  16. Weiss R., Gröger M., Rauscher S., Fendl B., Eichhorn T., Fischer M.B., Spittler A., Weber V. 2018. Differential interaction of platelet-derived extracellular vesicles with leukocyte subsets in human whole blood. Sci. Rep. 8 (1), 6598. https://doi.org/10.1038/s41598-018-25047-x

  17. Arraud N., Linares R., Tan S., Gounou C., Pasquet J.M., Mornet S., Brisson A.R. 2014. Extracellular vesicles from blood plasma: Determination of their morphology, size, phenotype and concentration. J. Thromb. Haemost. 12 (5), 614–627. https://doi.org/10.1111/jth.12554

  18. Koltsova E.M., Sorokina M.A., Pisaryuk A.S., Povalyaev N.M., Ignatova A.A., Polokhov D.M., Kotova E.O., Balatskiy A.V., Ataullakhanov F.I., Panteleev M.A., Kobalava Z.D., Balandina A.N. 2021. Hypercoagulation detected by routine and global laboratory hemostasis assays in patients with infective endocarditis. PLoS One. 16 (12), e0261429. https://doi.org/10.1371/journal.pone.0261429

  19. Combes V., Simon A.C., Grau G.E., Arnoux D., Camoin L., Sabatier F., Mutin M., Sanmarco M., Sampol J., Dignat-George F. 1999. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J. Clin. Invest. 104 (1), 93–102. https://doi.org/10.1172/JCI4985

  20. Dickhout A., Koenen R.R. 2018. Extracellular vesicles as biomarkers in cardiovascular disease: Chances and risks. Front. Cardiovasc. Med. 5, 113. https://doi.org/10.3389/fcvm.2018.00113

  21. Dignat-George F., Boulanger C.M. 2011. The many faces of endothelial microparticles. Arterioscler. Thromb. Vasc. Biol. 31(1), 27–33. https://doi.org/10.1161/ATVBAHA.110.218123

  22. Sedgwick A.E., D’Souza-Schorey C. 2018. The biology of extracellular microvesicles. Traffic. 19 (5), 319–327. https://doi.org/10.1111/tra.12558

  23. Thangaraju K., Neerukonda S.N., Katneni U., Buehler P.W. 2020. Extracellular vesicles from red blood cells and their evolving roles in health, coagulopathy and therapy. Int. J. Mol. Sci. 22 (1), 153. https://doi.org/10.3390/ijms22010153

  24. Gamonet C., Desmarets M., Mourey G., Biichle S., Aupet S., Laheurte C., François A., Resch E., Bigey F., Binda D., Bardiaux L., Naegelen C., Marpaux N., Delettre F.A., Saas P., Morel P., Tiberghien P., Lacroix J., Capellier G., Vidal C., Garnache-Ottou F. 2020. Processing methods and storage duration impact extracellular vesicle counts in red blood cell units. Blood Adv. 4 (21), 5527–5539. https://doi.org/10.1182/bloodadvances.2020001658

  25. Jy W., Ricci M., Shariatmadar S., Gomez-Marin O., Horstman L.H., Ahn Y.S. 2011. Microparticles in stored red blood cells as potential mediators of transfusion complications. Transfusion. 51 (4), 886–893. https://doi.org/10.1111/j.1537-2995.2011.03099.x

  26. Giesen P.L.A., Rauch U., Bohrmann B., Kling D., Roqué M., Fallon J.T., Badimon J.J., Himber J., Riederer M.A., Nemerson Y. 1999. Blood-borne tissue factor: Another view of thrombosis. Proc. Natl. Acad. Sci. USA. 96 (5), 2311–2315. https://doi.org/10.1073/pnas.96.5.2311

  27. Reddy E.C., Rand M.L. 2020. Procoagulant phosphatidylserine-exposing platelets in vitro and in vivo. Front Cardiovasc. Med. 7 (15), 15. https://doi.org/10.3389/fcvm.2020.00015

  28. Mackman N. 2009. The many faces of tissue factor. J. Thromb. Haemost. 7, 136–139. https://doi.org/10.1111/j.1538-7836.2009.03368.x

  29. Ruf W., Dorfleutner A., Riewald M. 2003. Specificity of coagulation factor signaling. J. Thromb. Haemost. 1 (7), 1495–1503. https://doi.org/10.1046/j.1538-7836.2003.00300.x

  30. Monroe D.M., Key N.S. 2007. The tissue factor-factor VIIa complex: Procoagulant activity, regulation, and multitasking. J. Thromb. Haemost. 5(6), 1097–1105. https://doi.org/10.1111/j.1538-7836.2007.02435.x

  31. Butenas S., Orfeo T., Mann K.G. 2009. Tissue factor in coagulation: Which? Where? When? Arterioscler. Thromb. Vasc. Biol. 29 (12), 1989–1996. https://doi.org/10.1161/ATVBAHA.108.177402

  32. Mackman N., Tilley R.E., Key N.S. 2007. Role of the extrinsic pathway of blood coagulation in hemostasis and thrombosis. Arterioscler. Thromb. Vasc. Biol. 27 (8), 1687–1693. https://doi.org/10.1161/ATVBAHA.107.141911

  33. Andrews A.M., Rizzo V. 2016. Microparticle-induced activation of the vascular endothelium requires caveolin-1/caveolae. PLoS One. 11 (2), e0149272. https://doi.org/10.1371/journal.pone.0149272

  34. Shustova O.N., Antonova O.A., Golubeva N.V., Khaspekova S.G., Yakushkin V.V., Aksuk S.A., Alchinova I.B., Karganov M.Y., Mazurov A.V. 2017. Differential procoagulant activity of microparticles derived from monocytes, granulocytes, platelets and endothelial cells: Impact of active tissue factor. Blood Coagul. Fibrinolysis. 28 (5), 373–382. https://doi.org/10.1097/MBC.0000000000000609

  35. Yang A., Chen F., He C., Zhou J., Lu Y., Dai J., Birge R.B., Wu Y. 2017. The procoagulant activity of apoptotic cells is mediated by interaction with factor XII. Front. Immunol. 8, 1188. https://doi.org/10.3389/fimmu.2017.01188

  36. Bretelle F., Sabatier F., Desprez D., Camoin L., Grunebaum L., Combes V., D’Ercole C., Dignat-George F. 2003. Circulating microparticles: A marker of procoagulant state in normal pregnancy and pregnancy complicated by preeclampsia or intrauterine growth restriction. Thromb. Haemost. 89 (3), 486–492. https://doi.org/10.1055/s-0037-1613378

  37. Alijotas-Reig J., Palacio-Garcia C., Farran-Codina I., Zarzoso C., Cabero-Roura L., Vilardell-Tarres M. 2011. Circulating cell-derived microparticles in women with pregnancy loss. Am. J. Reprod. Immunol. 66 (3), 199–208. https://doi.org/10.1111/j.1600-0897.2010.00972.x

  38. Radu C.M., Campello E., Spiezia L., Dhima S., Visentin S., Gavasso S., Woodhams B., Cosmi E., Simioni P. 2015. Origin and levels of circulating microparticles in normal pregnancy: A longitudinal observation in healthy women. Scand. J. Clin. Lab. Invest. 75 (6), 487–495. https://doi.org/10.3109/00365513.2015.1052551

  39. 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

  40. Alijotas-Reig J., Palacio-Garcia C., Llurba E., Vilardell-Tarres M. 2013. Cell-derived microparticles and vascular pregnancy complications: A systematic and comprehensive review. Fertil. Steril. 99 (2), 441–449. https://doi.org/10.1016/j.fertnstert.2012.10.009

  41. Aharon A., Brenner B. 2011. Microparticles and pregnancy complications. Thromb. Res. 127, S67–S71. https://doi.org/10.1016/S0049-3848(11)70019-6

  42. Burton G.J., Fowden A.L. 2015. The placenta: A multifaceted, transient organ. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 370 (1663), 20140066. https://doi.org/10.1098/rstb.2014.0066

  43. Huppertz B., Kadyrov M., Kingdom J.C.P. 2006. Apoptosis and its role in the trophoblast. Am. J. Obstet. Gynecol. 195 (1), 29–39. https://doi.org/10.1016/j.ajog.2005.07.039

  44. Haider S., Meinhardt G., Saleh L., Kunihs V., Gamperl M., Kaindl U., Ellinger A., Burkard T.R., Fiala C., Pollheimer J., Mendjan S., Latos P.A., Knöfler M. 2018. Self-renewing trophoblast organoids recapitulate the developmental program of the early human placenta. Stem Cell Reports. 11 (2), 537–551. https://doi.org/10.1016/j.stemcr.2018.07.004

  45. Moffett A., Loke C. 2006. Immunology of placentation in eutherian mammals. Nat. Rev. Immunol. 6 (8), 584–594. https://doi.org/10.1038/nri1897

  46. Askelund K.J., Chamley L.W. 2011. Trophoblast deportation part I: Review of the evidence demonstrating trophoblast shedding and deportation during human pregnancy. Placenta. 32 (10), 716–723. https://doi.org/10.1016/j.placenta.2011.07.081

  47. Holland O., Kroneis T., El-Heliebi A., McDowell-Hook M., Stone P., Sedlmayr P., Chamley L. 2017. Detection of fetal sex, aneuploidy and a microdeletion from single placental syncytial nuclear aggregates. Fetal Diagn. Ther. 41 (1), 32–40. https://doi.org/10.1159/000445112

  48. Johansen M., Redman C.W., Wilkins T., Sargent I.L. 1999. Trophoblast deportation in human pregnancy – its relevance for pre-eclampsia. Placenta. 20 (7), 531–539. https://doi.org/10.1053/plac.1999.0422

  49. Reverdiau P., Jarousseau A.C., Thibault G., Khalfoun B., Watier H., Lebranchu Y., Bardos P., Gruel Y. 1995. Tissue factor activity of syncytiotrophoblast plasma membranes and tumoral trophoblast cells in culture. Thromb. Haemost. 73 (1), 49–54. https://doi.org/10.1055/s-0038-1653724

  50. Teng Y.C., Lin Q.De., Lin J.H., Ding C.W., Zuo Y. 2009. Coagulation and fibrinolysis related cytokine imbalance in preeclampsia: The role of placental trophoblasts. J. Perinat. Med. 37 (4), 343–348. https://doi.org/10.1515/JPM.2009.060

  51. Aharon A., Brenner B., Katz T., Miyagi Y., Lanir N. 2004. Tissue factor and tissue factor pathway inhibitor levels in trophoblast cells: Implications for placental hemostasis. Thromb. Haemost. 92 (4), 776–786. https://doi.org/10.1160/TH04-01-0033

  52. Lakasing L., Campa J.S., Poston R., Khamashta M.A., Poston L. 1999. Normal expression of tissue factor, thrombomodulin, and annexin V in placentas from women with antiphospholipid syndrome. Am. J. Obstet. Gynecol. 181 (1), 180–189. https://doi.org/10.1016/s0002-9378(99)70457-6

  53. Faulk W.P., Labarrere C.A., Carson S.D. 1990. Tissue factor: Identification and characterization of cell types in human placentae. Blood. 76(1), 86–96.

  54. Teng Y., Jiang R., Lin Q., Ding C., Ye Z. 2010. The relationship between plasma and placental tissue factor, and tissue factor pathway inhibitors in severe pre-eclampsia patients. Thromb. Res. 126 (1), e41–e45. https://doi.org/10.1016/j.thromres.2010.02.012

  55. Gardiner C., Tannetta D.S., Simms C.A., Harrison P., Redman C.W.G., Sargent I.L. 2011. Syncytiotrophoblast microvesicles released from pre-eclampsia placentae exhibit increased tissue factor activity. PLoS One. 6 (10), e26313. https://doi.org/10.1371/journal.pone.0026313

  56. Ng E.K.O., Leung T.N., Tsui N.B.Y., Lau T.K., Panesar N.S., Chiu R.W.K., Lo Y.M.D. 2003. The concentration of circulating corticotropin-releasing hormone mRNA in maternal plasma is increased in preeclampsia. Clin. Chem. 49 (5), 727–731. https://doi.org/10.1373/49.5.727

  57. Freeman D.J., Tham K., Brown E.A., Rumley A., Lowe G.D., Greer I.A. 2008. Fetal corticotrophin-releasing hormone mRNA, but not phosphatidylserine-exposing microparticles, in maternal plasma are associated with factor VII activity in pre-eclampsia. J. Thromb. Haemost. 6 (3), 421–427. https://doi.org/10.1111/j.1538-7836.2007.02882.x

  58. Goswami D., Tannetta D.S., Magee L.A., Fuchisawa A., Redman C.W.G., Sargent I.L., von Dadelszen P. 2006. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta. 27 (1), 56–61. https://doi.org/10.1016/j.placenta.2004.11.007

  59. Knight M., Redman C.W.G., Linton E.A., Sargent I.L. 1998. Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies. Br. J. Obstet. Gynaecol. 105 (6), 632–640. https://doi.org/10.1111/j.1471-0528.1998.tb10178.x

  60. Lok C.A.R, Van Der Post J.A.M, Sargent I.L., Hau C.M., Sturk A., Boer K., Nieuwland R. 2008. Changes in microparticle numbers and cellular origin during pregnancy and preeclampsia. Hypertens. Pregnancy. 27 (4), 344–360. https://doi.org/10.1080/10641950801955733

  61. Huppertz B., Frank H.G., Kingdom J.C., Reister F., Kaufmann P. 1998. Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta. Histochem. Cell Biol. 110 (5), 495–508. https://doi.org/10.1007/s004180050311

  62. Owens A.P. 3rd, Mackman N. 2012. Microparticles in hemostasis and thrombosis. 108 (10), 1284–1297. https://doi.org/10.1161/CIRCRESAHA.110.233056

  63. Fazel A., Vincenot A., Malassiné A., Soncin F., Gaus-sem P., Alsat E., Evain-Brion D. 1998. Increase in expression and activity of thrombomodulin in term human syncytiotrophoblast microvilli. Placenta. 19 (4), 261–268. https://doi.org/10.1016/s0143-4004(98)90057-1

  64. Lanir N., Aharon A., Brenner B. 2003. Haemostatic mechanisms in human placenta. Best Pract. Res. Clin. Haematol. 16 (2), 183–195. https://doi.org/10.1016/s1521-6926(02)00098-1

  65. Štok U., Čučnik S., Sodin-Šemrl S., Žigon P. 2021. Extracellular vesicles and antiphospholipid syndrome: State-of-the-art and future challenges. Int. J. Mol. Sci. 22 (9), 4689. https://doi.org/10.3390/ijms22094689

  66. Goulopoulou S., Davidge S.T. 2015. Molecular mechanisms of maternal vascular dysfunction in preeclampsia. Trends Mol. Med. 21 (2), 88–97. https://doi.org/10.1016/j.molmed.2014.11.009

  67. Tannetta D.S., Dragovic R.A., Gardiner C., Redman C.W., Sargent I.L. 2013. Characterisation of syncytiotrophoblast vesicles in normal pregnancy and pre-eclampsia: Expression of Flt-1 and endoglin. PLoS One. 8 (2), e56754. https://doi.org/10.1371/journal.pone.0056754

  68. Lok C.A.R., Böing A.N., Sargent I.L., Sooranna S.R., van der Post J.A.M., Nieuwland R., Sturk A. 2008. Circulating platelet-derived and placenta-derived microparticles expose Flt-1 in preeclampsia. Reprod. Sci. 15 (10), 1002–1010. https://doi.org/10.1177/1933719108324133

  69. Cronqvist T., Tannetta D., Mörgelin M., Belting M., Sargent I., Familari M., Hansson S.R. 2017. Syncytiotrophoblast derived extracellular vesicles transfer functional placental miRNAs to primary human endothelial cells. Sci. Rep. 7 (1), 4558. https://doi.org/10.1038/s41598-017-04468-0

  70. Tannetta D.S., Hunt K., Jones C.I., Davidson N., Coxon C.H., Ferguson D., Redman C.W., Gibbins J.M., Sargent I.L., Tucker K.L. 2015. Syncytiotrophoblast extracellular vesicles from pre-eclampsia placentas differentially affect platelet function. PLoS One. 10 (11), e0142538. https://doi.org/10.1371/journal.pone.0142538

  71. Tannetta D., Masliukaite I., Vatish M., Redman C., Sargent I. 2017. Update of syncytiotrophoblast derived extracellular vesicles in normal pregnancy and preeclampsia. J. Reprod. Immunol. 119, 98–106. https://doi.org/10.1016/j.jri.2016.08.008

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