The role of platelet microvesicles in the pathogenesis of preeclampsia

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Abstract

Among the diverse picture of preeclampsia, the hematological component, thrombocytopenia, attracts attention. Platelets are able to form microvesicles by “budding” the plasma membrane from the cell surface during apoptosis, stimulation, and also in a small amount in normal conditions. The membrane of these particles has a negative charge and contains phospholipids and an integral glycoprotein on the outer monolayer, due to which platelet microvesicles are involved in the process of blood coagulation and angiogenesis. Microvesicles are of platelet origin, they were first discovered in the middle of the last century in England when describing the phenomenon of plasma and serum coagulation in the absence of platelets in them. The number of platelet microvesicles dynamically changes during the formation of preeclampsia in pregnant women and in women with risk factors for the development of preeclampsia, which include obesity, arterial hypertension, diabetes mellitus, antiphospholipid syndrome. Exposure to these risk factors for preeclampsia before pregnancy leads to a change in the concentration of cells that produce microvesicles, which in turn can create conditions favorable for the development of preeclampsia during pregnancy. A special risk group are women with a history of preeclampsia. Taking into account the direct role of microvesicles in the processes of angiogenesis and blood coagulation, the study of these particles will allow a more detailed study of the pathophysiological aspects of the preeclampsia development, which will expand the possibilities for early prediction of this pathology and improvement of perinatal outcomes.

About the authors

Svetlana А. Galeeva

Bashkir State University

Author for correspondence.
Email: Svetagaleeva04@gmail.com
ORCID iD: 0000-0002-6911-3367

Postgrad. Stud., Depart. of Obstetrics and Gynecology with the IDPO course

Russian Federation, Ufa, Russia

Nadzhiba А. Tadzhiboeva

Bashkir State University

Email: najibatojiboeva@gmail.com
ORCID iD: 0000-0002-1863-3784

Postgrad. Stud., Depart. of Obstetrics and Gynecology with the IDPO course

Russian Federation, Ufa, Russia

References

  1. Yi HY, Jeong SY, Kim SH, Kim Y, Choi SJ, Oh SY, Roh CR, Kim JH. Indications and characteristics of obstetric patients admitted to theintensive care unit: a 22-year review in a tertiary care center. Obstet Gynecol Sci. 2018;61(2):209–219. doi: 10.5468/ogs.2018.61.2.209.
  2. Katsuragi S, Tanaka H, Hasegawa J, Nakamura M, Kanayama N, Nakata M, Murakoshi T, Yoshimatsu J, Osato K, Tanaka K, Sekizawa A, Ishiwata I, Ikeda T. On behalf of the Maternal Death Exploratory Committee in Japan and Japan Association of Obstetricians and Gynecologists. Analysis of preventability of hypertensive disorder in pregnancy-related maternal death using the nationwide registration system of maternal deaths in Japan. J Matern Fetal Neonatal Med. 2018;31(16):2097–2104. doi: 10.1080/14767058.2017.1336222.
  3. Navolotskaya VK, Lyashko ES, Shifman EM, Konysheva OV, Kulikov AV, Arustamyan RR, Pylaeva NYu. Possibilities for prediction of preeclampsia complications (a review). Problemy reproduktsii. 2019;25(1):87–96. (In Russ.) doi: 10.17116/repro20192501187.
  4. Khodzhaeva ZS, Akatyeva AS, Kholin AM, Safonova AD, Vavina OV, Muminova KT. Molecular determinants of the development of early and late preeclampsia. Akusherstvo i ginekologiya. 2014;(6):14–19. (In Russ.)
  5. Valensise H, Vasapollo B, Gagliardi G, Novelli GP. Early and late preeclampsia: Two different maternal hemodynamic states in the latent phase of the disease. Hypertension. 2011;52(5):873–880. doi: 10.1161/HYPERTENSIONAHA.108.117358.
  6. Lisonkova S, Sabr Y, Mayer C, Young C, Skoll A, Joseph KS. Maternal morbidity associated with early-onset and late-onset preeclampsia. Obstet Gynecol. 2014;124(4):771–781. doi: 10.1097/AOG.0000000000000472.
  7. Vodneva DN, Romanova VV, Dubova EA, Pavlov KA, Shmakov RG, Shchegolev AI. The clinical and morpholo¬gical features of early- and late-onset preeclampsia. Akusherstvo i ginekologiya. 2014;(2):35–40. (In Russ.)
  8. Perni U, Cristina Sison C, Sharma V, Helseth G, Hawfield A, Suthanthiran M, August Ph. Angiogenic factors in superimposed preeclampsia. A longitudinal study of wo¬men with chronic hypertension during pregnancy. Hypertension. 2012;59:740–746. doi: 10.1161/hypertensionaha.111.181735.
  9. Ivanets TYu, Alekseyeva ML, Loginova NS, Kolodko VG, Nasonova DM, Khasiyanova ZSh. The placental growth factor and fms-similar tyrosine kinase-1 as mar¬kers of preeclampsy in dynamics of pregnancy. Klinicheskaya la¬boratornaya diagnostika. 2013;(8):14–17. (In Russ.)
  10. Starodub¬tseva NL, Popov IA, Nikolayev EN, Ivanets TYu, Alekseyeva ML, Loginova NS, Nikolaeva AV, Vavina OV, Sukhikh GT. Search for reproducible biomarkers for the diagnosis of preeclmpsia. Akusherstvo i ginekologiya. 2013;(2):10–17. (In Russ.)
  11. Skovorodina TV, Vishnyakova PA, Shmakov RG, Vysokikh MYu. Rol' mitokhondrial'nykh markerov v patogeneze preeklampsii i otsenka effektivnosti respiratornoy terapii v lechenii preeklampsii. Akusherstvo i ginekologiya. 2017;(6):5–9. (In Russ.) doi: 10.18565/aig.2017.6.5-9.
  12. Kirsanova TV, Vinogradova MA. New in the differential diagnosis of diffe¬rent variants of thrombotic microangiopathies in obstetrics. Meditsinskiy sovet. 2021;(3):98–105. (In Russ.) doi: 10.21518/2079-701X-2021-3-98-105.
  13. Fatkullina IB. Hemostasis indexes in pregnancy complicated by preeclampsia and chronic hypertension. Vestnik of the Buryat State University. 2010;(12): 158-161. (In Russ.)
  14. Kosterina AV. Some issues of diagnostics and treatment of anemia and thrombocytopenia in pregnancy. Prakticheskaya me¬ditsina. 2017;(8):81–84. (In Russ.)
  15. Zubairov DM, Zubairova LD. Mikrovezikuly v krovi. Funktsii i ih rol' v tromboobrazovanii. (Microvesicles in blood. Functions and their role in thrombus formation.) Moscow: GEOTAR-Media; 2009. 168 p. (In Russ.)
  16. Kubatiev AA, Borovaya TG, Zhukovitskaya VG, Adreevskaya SG, Shevlyagina NV. Platelet microparticles: formation and properties. Patogenez. 2017;15(2):4–13. (In Russ) doi: 10.25557/GM.2017.2.7296.
  17. Panteleev MA, Abaeva AA, Balandina AN, Belyaev AV, Nechipurenko DYu, Obydennyi SI, Sveshnikova AN, Shibeko AM, Ataullakhanov FI. Extracellular vesicles of blood plasma: content, origin, and pro¬perties. Biochemistry (Moscow) Supplement. Series A: membrane and cell biology. 2017;11(3):155–161. doi: 10.1134/S1990747817030060.
  18. O’Brien JR. The platelet-like activity of serum. Br J Haematol. 1955;1(2):223–228.
  19. Wolf P. The nature and significance of platelet pro¬ducts in human plasma. Br J Haematol. 1967;13(3):269–288. doi: 10.1111/j.1365-2141.1967.tb08741.
  20. Momot AP, Tsarigorodtseva NO, Fedo¬rov DV, Bishevski KM, Vostrikova NV, Klimova EE. Platelet microvesicles and their role in providing hemostatic capacity (literature review). Sibirskiy nauchnyy meditsinskiy zhurnal. 2020;40(2):4–14. (In Russ.) doi: 10.15372/SSMJ20200201.
  21. Paltsyn AA. Platelet microparticles. Patologicheskaya fiziologiya i eksperimentalnaya terapiya. 2017;61(1):99–105. (In Russ.) doi: 10.25557/0031-2991.2017.01.99-105.
  22. Italiano JEJr, Mairuhu TA, Flaumenhaft R. Clini¬cal relevance of microparticles from platelets and megakaryocytes. Curr Opin Hematol. 2010;17(6):578–584. doi: 10.1097/MOH.0b013e32833e77ee.
  23. Terekhina VYu. The role of extracellular microvesicles of endothelial origin in the development of preeclampsia. Scientist (Russia). 2020;(4):5. (In Russ.)
  24. Lacroix R, Plawinski L, Robert S, Doeuvre L, Saba¬tier F, Martinez de Lizarrondo S, Mezzapesa A, Anfosso F, Leroyer AS, Poullin P, Jourde N, Njock MS, Boulanger CM, Angles-Cano E, Dignat-George F. Leukocyte- and endothelial-derived microparticles: A circulating source for fibrinolysis. Haematologica. 2012;97(12):1864–1872.
  25. Kim HK, Song KS, Chung JH, Lee KR, Lee SN. Platelet microparticles induce angiogenesis in vitro. Br J Haematol. 2004;124(3):376–384. doi: 10.1046/j.1365-2141.2003.04773.x.
  26. Faille D, El-Assaad F, Mitchell AJ, Alessi MC, Chimini G, Fusai T, Grau GE, Combes V. Endocytosis and ¬intracellular processing of platelet microparticles by brain endothelial cells. J Cell Mol Med. 2012;16(8):1731–1738. doi: 10.1111/j.1582- 4934.2011.01434.x.
  27. Goubran HA, Burnouf T, Stakiw J, Seghatchian J. Platelet microparticle: a sensitive physiological “fine tu¬ning” balancing factor in health and disease. Transfus Apher Sci. 2015;52(1):12–18. doi: 10.1016/j.transci.2014.12.01.
  28. Sinauridze EI, Kireev DA, Popenko NY, Pichugin AV, Panteleev MA, Krymskaya OV, Ataullakhanov FI. Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb Haemost. 2007;97(3):425–434.
  29. Burnier L, Fontana P, Kwak BR, Angelillo Scherrer A. Cell-derived microparticles in haemostasis and vascular medicine. Thromb Haemost. 2009;101(3):439–451. doi: 10.1160/TH08-08-0521.
  30. Leroyer AS, Anfosso F, Lacroix R, Sabatier F, Simoncini S, Njock SM, Jourde N, Brunet P, Camoin-Jau L, Sampol J, Dignat-George F. Endothelial-derived microparticles: Biological conveyors at the crossroad of inflammation, thrombosis and angiogenesis. Thromb Haemost. 2010;104(3):456–463. doi: 10.1160/TH10-02-0111.
  31. Perez-Casal M, Downey C, Cutillas-Moreno B, Zuzel M, Fukudome K, Hock Toh C. Microparticle-associa¬ted endothelial protein C receptor and the induction of cytoprotective and anti-inflammatory effects. Haematologica. 2009;94(3):387–394. doi: 10.3324/haematol.13547.
  32. Germain SJ, Sacks GP, Sooranna SR, Sargent IL, Redman CW. Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circula-ting syncytiotrophoblast microparticles. J Immunol. 2007;178(9):5949–5956.
  33. Stepanian A, Bourguignat L, Hennou S, Coupaye M, Hajage D, Salomon L, Alessi MC, Msika S, de Prost D. Microparticle increase in severe obesity: not related to metabolic syndrome and unchanged after massive weight loss. Obesity (Silver Spring). 2013;21(11):2236–2243.
  34. Tramontano AF, Lyubarova R, Tsiakos J, Palaia T, Deleon JR, Ragolia L. Circulating endothelial microparticles in diabetes mellitus. Mediators Inflamm. 2010;2010:250476. doi: 10.1155/2010/250476.
  35. Zhang X, McGeoch SC, Johnstone AM, Holtrop G, Sneddon AA, MacRury SM, Megson IL, Pearson DW, Abraham P, De Roos B, Lobley GE, O’Kennedy N. Platelet-derived microparticle count and surface molecule expression differ between subjects with and without type 2 diabetes, independently of obesity status. J Thromb Thrombolysis. 2014;37(4):455–463.
  36. Macey MG, Bevan S, Alam S, Verghese L, Agra¬wal S, Beski S, Thuraisingham R, MacCallum PK. Platelet activation and endogenous thrombin potential in pre-eclampsia. Thromb Res. 2010;125(3):e76–e81. doi: 10.1016/j.thromres.2009.09.013.
  37. Lok CA, van der Post JA, Sargent IL, Hau CM, Sturk A, Boer K, Nieuwland R. Changes in microparticle numbers and cellular origin during pregnancy and preeclampsia. Hypertens Pregnancy. 2008;27(4):344–360.
  38. Marques FK, Campos FM, Filho OA, Carvalho AT, Dusse LM, Gomes KB. Circulating microparticles in severe preeclampsia. Clin Chim Acta. 2012;414:253–258.
  39. Kerkeshko GO, Korenevsky AV, Sokolov DI, Selkov SA. The role of interactions between trophoblastderived extracellular microvesicles, immune cells and endothelium in pathogenesis of pre-eclampsia. Medical Immunology (Russia). 2018;20(4):485–514. (In Russ.) doi: 10.15789/1563-0625-2018-4-485-514.
  40. Gomzikova MO, Gaifullina RF, Mustafin IG, Chernov VM, Miftahova ZR, Galya¬vich AS, Rizvanov AA. Membrane microvesicles: biological properties and involvement in pathogenesis of diseases. Geny & Kletki. 2013;8(1):6–11. (In Russ.)
  41. Ailamazyan EK, Stepanova OI, Selkov SA, Sokolov DI. Cells of immune system of mother аnd trophoblast cells: constructive cooperation for the sake of achievement of the joint purpose. Vestnik RAMN. 2013;68(11):12–21. (In Russ.) doi: 10.15690/vramn.v68i11.837.
  42. Morgoyeva AA, Tsakhilova SG, Sakvarelidze NYu, Zikova AS, Olisayeva IV. The role of extracellular vesicles in the development of endothelial dysfunction in preeclampsia. Effektivnaya farmakoterapiya. 2021;17(32)8–12. (In Russ.) doi: 10.33978/2307-3586-2021-17-32-8-12.
  43. Roberts JM, Redman CW. Pre-eclampsia: more than pregnancy-induced hypertension. Lancet. 1993;341(8858):1447–1451.
  44. Roberts JM, Escudero C. The placenta in preeclampsia. Pregnancy Hypertens. 2012;2(2):72–83.
  45. Zhou Y, Gormley MJ, Hunkapiller NM, Kapidzic M, Stolyarov Y, Feng V, Nishida M, Drake PM, Bianco K, Wang F, McMaster MT, Fisher SJ. Reversal of gene dysregulation in cultured cytotrophoblasts reveals possible causes of preeclampsia. J Clin Invest. 2013;123(7):2862–2872. doi: 10.1172/JCI66966.
  46. Caniggia I, Winter J, Lye SJ, Post M. Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia. Placenta. 2000;21(Suppl A):S25–S30.
  47. Gilani SI, Weissgerber TL, Garovic VD, Jayachandran M. Preeclampsia and extracellular vesicles. Curr Hypertens Rep. 2016;18(9):68.
  48. Kambe S, Yoshitake H, Yuge K, Ishida Y, Moksed Ali M, Takizawa T, Kuwata T, Ohkuchi A, Matsubara Sh, Suzuki M, Takeshita T, Saito Sh, Takizawa T. Human exosomal placentaassociated miR-517a-3p modulates the expression of PRKG1 mRNA in Jurkat cells. Biol Reprod. 2014;91(5):129. doi: 10.1095/biolreprod.114.121616.
  49. Komaki M, Numata Y, Morioka C, Honda I, Tooi M, Yokoyama N, Ayame H, Iwasaki K, Taki A, Oshima N, Morita I. Exosomes of human placenta-derived mesenchymal stem cells stimulate angiogenesis. Stem Cell Res Ther. 2017;8(1):219. doi: 10.1186/s13287-017-0660-9.
  50. Mouillet JF, Ouyang Y, Bayer A, Coyne СВ, Sadovsky Y. The role of trophoblastic microRNAs in placental viral infection. Int J Dev Biol. 2014;58(2–4):281–289. doi: 10.1387/ijdb.130349ys.
  51. Lisonkova S, Joseph KS. Incidence of preeclampsia: risk factors and outcomes associated with early-versus late-onset disease. Am J Obstet Gynecol. 2013;209(6):544.
  52. Barton JR, Sibai BM. Prediction and prevention of recurrent preeclampsia. Obstet Gynecol. 2008;112(2 Pt 1):359–372.
  53. Akulenko LV, Dzansolova AV, Mugadova ZV, Balios LV, Sozaeva LG, Kuznetsov VM. The likely role of prooxidant and antioxidant genes in the development of preeclampsia. Problemy reprodukcii. 2017;23(2):84–87. (In Russ.) doi: 10.17116/repro201723284-87.
  54. Kan NE, Bednyagin LA, Dolgushina NV, Tyutyunnik VL, Hovhaeva PA, Sergunina OA, Tyutyunnik NV, Amiraslanov EYu. Clinical and anamnestic risk factors for preeclampsia in pregnant women. Akusherstvo i ginekologiya. 2016;(6):39–44. (In Russ.) doi: 10.18565/aig.2016.6.39-44.
  55. Pinheiro MB, Gomes KB, Dusse LM. Fibrinolytic system in preeclampsia. Clin Chim Acta. 2013;416:67–71. doi: 10.1016/j.cca.2012.10.060.
  56. Townsley DM. Hematologic complications of pregnancy. Semin Hematol. 2013;50(3):222–231. doi: 10.1053/j.seminhematol.2013.06.004.
  57. Ghoshal K, Bhattacharyya M. Overview of platelet physiology: Its hemostatic and nonhemostatic role in di¬sease pathogenesis. Scientific World Journal. 2014;2014:1–16. doi: 10.1155/2014/781857.
  58. McCrae KR. Thrombocytopenia in pregnancy: differential diagnosis, pathogenesis, and management. Blood Rev. 2003;17(1):7–14. PMID: 12490206.
  59. Frölich MA, Datta S, Corn SB. Thrombopoietin in normal pregnancy and preeclampsia. Am J Obstet Gynecol. 1998;179(1):100–104. PMID: 9704772.
  60. Pogorelov VM, Kozinec GI, Makarov IO, Toche¬nov AV, Rykunova OV. Trombocyte parametrs in normal pregnancy and gestosis. Akusherstvo, ginekologiya i reproduktsiya. 2012;6(3):28–33. (In Russ.)
  61. Felfernig-Boehm D, Salat A, Vogl SE, Murabito M, Felfernig M, Schmidt D, Mittlboeck M, Husslein P, Mueller MR. Early detection of preeclampsia by determination of platelet aggregability. Thromb Res. 2000;98(2):139–146. doi: 10.1016/s0049-3848(99)00224-8.
  62. Madazli R, Benian A, Gümüştaş K, Uzun H, Ocak V, Aksu F. Lipid peroxidation and antioxidants in preeclampsia. Eur J Obstet Gynecol Reprod Biol. 1999;85(2):205–208. doi: 10.1016/s0301-2115(99)00023-8.
  63. Hayashi M, Kiumi F, Hoshimoto K, Ohkura T. Platelet aggregation response and adenosine triphosphate secretion after abdominal total hysterectomy. Int J Clin Pract. 2003;57(6):461–466. PMID: 12918883.
  64. Lazarov R, Konijnenberg A, van der Post JA, Sturk А, Boer K. Preeclampsia not (yet) predictable from the blood platelet count. Ned Tijdschr Geneeskd. 1999;143(1):10–13. PMID: 10086090.
  65. Borzova NYu, Gerasimov AM, Skripkina IYu, Kuzmenko GN. Katepsin d role in gestosis pathogenesis. Vestnik novykh meditsinskikh tekhnologiy. 2009;16(3):54–56. (In Russ.)
  66. Rinehart BK, Terrone DA, May WL, Magann EF, Isler CM, Martin JrJN. Change in platelet count predicts eventual maternal outcome with syndrome of hemolysis, ele¬vated liver enzymes and low platelet count. J Matern Fetal. 2001;10(1):28–34. PMID: 11332416.
  67. Bakunovich AV, Bulanova KYa. Structural and functional alterations of platelets in pregnant women with preeclampsia. Journal of the Belarusian State University. Ecology. 2018;(4):76–83. (In Russ.)
  68. Ponomareva AA, Nevzorova TA, Mordakhanova ER, Andrianova IA, Litvinov RI. Structural characterization of platelets and platelet microvesicles. Cell and tissue biology. 2016;10(3):217–226. doi: 10.1134/S1990519X1603010X.
  69. Zubairova LD. Mikrovezikuly krovi v patogeneze ostroy gemostaticheskoy reaktsii. Avtoreferat dissertatsii doktora meditsinskikh nauk. (Blood microvesicles in the pathogenesis of acute hemostatic reaction. Abstract of the diss. of a Dr. Med. Scien¬ces.) Kazan'; 2008. 34 р. (In Russ.)
  70. Makatsariya AD, Bitsadze VO, Akinshina SV. Tyazhelye formy preeklampsii kak proyavlenie tromboticheskoy mikroangiopatii. Akusherstvo i ginekologiya. 2017;(4):21–26. (In Russ.) doi: 10.18565/aig.2017.4.21-6.

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