The role of placental macrophages in physiological pregnancy and preeclampsia

DOI

https://dx.doi.org/10.18565/aig.2022.4.5-12

Vishnyakova P.A., Elchaninov A.V., Kiseleva V.V., Muminova K.T., Khodzhaeva Z.S., Eremina I.Z., Fatkhudinov T.Kh.
1) Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia, Moscow, Russia; 2) Peoples’ Friendship University of Russia, Ministry of Science and Higher Education of the Russian Federation (RUDN University), Moscow, Russia; 3) A.P. Avtsyn Research Institute of Human Morphology, Moscow, Russia

Preeclampsia (PE) is a multisystem pregnancy complication that is the leading cause of maternal and perinatal morbidity and mortality. Today, a large body of data has been accumulated, suggesting that an abnormal maternal immune response in PE is manifested, among other things, as a change in the functional activity of the monocyte-macrophage system, the most important unit of innate immunity. The cause of abnormal placentation underlying PE, especially early PE, may be dysfunction of placental immune cells, namely macrophages. The macrophages are one of the main cellular constituents of the decidua, the maternal component of the placenta, and also play an important role in the development of the fetal part of the placenta, per se being one of the first immune cells of a baby. Depending on their functional state, the macrophages can either stimulate or suppress inflammation, angiogenesis, and the proliferation of neighboring cells. According to the concept of binary polarization, there are two states of macrophages: classically activated macrophages (M1) produce proinflammatory cytokines and reactive oxygen/nitrogen species. The other type of macrophages (M2) produces anti-inflammatory cytokines and is involved in the elimination of inflammation.
Conclusion: Turning to the key differential markers of macrophages, this review attempts to summarize the current data on the functioning of the monocyte-macrophage system in physiological pregnancy and PE.

preeclampsia

macrophages

inflammation

phenotype

polarization

Full text (in Russian)

Conde-Agudelo A., Villar J., Lindheimer M. World Health Organization S-systematic review of screening tests for preeclampsia. Obstet. Gynecol. 2004; 104(6): 1367-91. https://dx.doi.org/10.1097/01.AOG.0000147599.47713.5d.
Вишнякова П.А., Кан. Н.Е., Ходжаева З.С., Высоких М.Ю. Митохондрии плаценты в норме и при преэклампсии. Акушерство и гинекология. 2017; 5: 5-8. [Vishnyakova P.A., Kan N.E., Khodzhaeva Z.S., Vysokikh M.Yu. Mitochondria placenta in the norm and during preeclampsia. Obstetrics and Gynecology. 2017; 5: 5-8. (in Russian)]. https://dx.doi.org/10.18565/aig.2017.5.5-8.
Зарипова Л.Р., Галина Т.В., Голикова Т.П., Гондаренко А.С. Прогнозирование и ранняя диагностика преэклампсии. Вестник РУДН. 2012; 6: 15-22. [Zaripova L.R., Galina T.V., Golikova T.P., Gondarenko A.S. Prediction and early diagnosis of pre-eclampsia. Bulletin of RUDN University. 2012; 6: 15-22. (in Russian)].
World Health Organization. WHO recommendations for prevention and treatment of pre-eclampsia and eclampsia. Geneva: World Health Organization; 2011. Available at: http://www.ncbi.nlm.nih.gov/books/NBK140561/ Accessed May 23, 2016.
Duley L. The global impact of pre-eclampsia and eclampsia. Semin. Perinatol. 2009; 33(3): 130-7. https://dx.doi.org/10.1053/j.semperi.2009.02.010.
Steegers E.A.P., von Dadelszen P., Duvekot J.J., Pijnenborg R. Pre-eclampsia. Lancet. 2010; 376(9741): 631-44. https://dx.doi.org/10.1016/S0140-6736(10)60279-6.
Vishnyakova P., Elchaninov A., Fatkhudinov T., Sukhikh G. Role of the monocyte–macrophage system in normal pregnancy and preeclampsia. Int. J. Mol. Sci. 2019; 20(15): 3695. https://dx.doi.org/10.3390/ijms20153695.
Mills C.D. Anatomy of a discovery: M1 and M2 macrophages. Front. Immunol. 2015; 6: 212. https://dx.doi.org/10.3389/fimmu.2015.00212
Yao Y., Xu X.H., Jin L. Macrophage polarization in physiological and pathological pregnancy. Front. Immunol. 2019; 10: 792. https://dx.doi.org/10.3389/FIMMU.2019.00792/BIBTEX.
Novak M.L., Koh T.J. Macrophage phenotypes during tissue repair. J. Leukoc. Biol. 2013; 93(6): 875-81. https://dx.doi.org/10.1189/JLB.1012512.
White M.J.V., Gomer R.H. Trypsin, tryptase, and thrombin polarize macrophages towards a pro-fibrotic M2a phenotype. PLoS One. 2015; 10(9): e0138748. https://dx.doi.org/10.1371/JOURNAL.PONE.0138/
Wang L.X., Zhang S.X., Wu H.J., Rong X.L., Guo J. M2b macrophage polarization and its roles in diseases. J. Leukoc. Biol. 2019; 106(2): 345-8. https://dx.doi.org/10.1002/JLB.3RU1018-37
Zulu M.Z., Martinez F.O., Gordon S., Gray C.M. The elusive role of placental macrophages: the Hofbauer cell. J. Innate Immun. 2019; 11(6): 447-56. https://dx.doi.org/10.1159/000497416.
Heikkinen J., Möttönen M., Komi J., Alanen A., Lassila O. Phenotypic characterization of human decidual macrophages. Clin. Exp. Immunol. 2003; 131(3): 498-505. https://dx.doi.org/10.1046/J.1365-2249.2003.02092.X.
Chazaud B. Macrophages: Supportive cells for tissue repair and regeneration. Immunobiology. 2014; 219(3): 172-8. https://dx.doi.org/10.1016/j.imbio.2013.09.001.
Perdiguero E.G., Geissmann F. The development and maintenance of resident macrophages. Nat. Immunol. 2016; 17(1): 2-8. https://dx.doi.org/10.1038/ni.3341.
Hoeffel G., Ginhoux F. Fetal monocytes and the origins of tissue-resident macrophages. Cell. Immunol. 2018; 330: 5-15. https://dx.doi.org/10.1016/j.cellimm.2018.01.001.
Kim J.S., Romero R., Kim M.R., Kim Y.M., Friel L., Espinoza J., Kim C.J. Involvement of hofbauer cells and maternal T cells in villitis of unknown aetiology. Histopathology. 2008; 52(4): 457-64. https://dx.doi.org/10.1111/J.1365-2559.2008.02964.X.
Kim M.J., Romero R., Kim C.J., Tarca A.L., Chhauy S., LaJeunesse C. et al. Villitis of unknown etiology is associated with a distinct pattern of chemokine up-regulation in the feto-maternal and placental compartments: implications for conjoint maternal allograft rejection and maternal anti-fetal graft-versus-host disease. J. Immunol. 2009; 182(6): 3919-27. https://dx.doi.org/10.4049/jimmunol.0803834.
Takahashi K., Naito M., Katabuchi H., Higashi K. Development, differentiation, and maturation of macrophages in the chorionic villi of mouse placenta with special reference to the origin of Hofbauer cells. J. Leukoc. Biol. 1991; 50(1): 57-68. https://dx.doi.org/10.1002/JLB.50.1.57.
Seval Y., Korgun E.T., Demir R. Hofbauer cells in early human placenta: possible implications in vasculogenesis and angiogenesis. Placenta. 2007; 28(8-9): 841-5. https://dx.doi.org/10.1016/J.PLACENTA.2007.01.010.
Hoeffel G., Chen J., Lavin Y., Low D., Almeida F.F., See P. et al. C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity. 2015; 42(4): 665-78. https://dx.doi.org/10.1016/j.immuni.2015.03.011.
Sun F., Wang S., Du M. Functional regulation of decidual macrophages during pregnancy. J. Reprod. Immunol. 2021; 143: 103264. https://dx.doi.org/10.1016/J.JRI.2020.103264.
Murray P.J. Macrophage polarization. Annu. Rev. Physiol. 2017; 79: 541-66. https://dx.doi.org/10.1146/annurev-physiol-022516-034339.
Murray P.J., Wynn T.A. Obstacles and opportunities for understanding macrophage polarization. J. Leukoc. Biol. 2011; 89(4): 557-63. https://dx.doi.org/10.1189/jlb.0710409.
Martinez F.O., Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Reports. 2014; 6: 13. https://dx.doi.org/10.12703/P6-13.
Pepe G., Locati M., Della Torre S., Mornata F., Cignarella A., Maggi A., Vegeto E. The estrogen–macrophage interplay in the homeostasis of the female reproductive tract. Hum. Reprod. Update. 2018; 24(6): 652-72. https://dx.doi.org/10.1093/humupd/dmy026.
Tagliani E., Shi C., Nancy P., Tay C.S., Pamer E.G., Erlebacher A. Coordinate regulation of tissue macrophage and dendritic cell population dynamics by CSF-1. J. Exp. Med. 2011; 208(9): 1901-16. https://dx.doi.org/10.1084/JEM.20110866.
Hashimoto D., Chow A., Noizat C., Teo P., Beasley M.B., Leboeuf M. et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity. 2013; 38(4): 792-804. https://dx.doi.org/10.1016/j.immuni.2013.04.004.
Jenkins S.J., Ruckerl D., Thomas G.D., Hewitson J.P., Duncan S., Brombacher F. et al. IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1. J. Exp. Med. 2013; 210(11): 2477-91. https://dx.doi.org/10.1084/JEM.20121999.
Jackson-Jones L.H., Rückerl D., Svedberg F., Duncan S., Maizels R.M., Sutherland T.E. et al. IL-33 delivery induces serous cavity macrophage proliferation independent of interleukin-4 receptor alpha. Eur. J. Immunol. 2016; 46(10): 2311-21. https://dx.doi.org/10.1002/EJI.201646442.
Pepe G., Braga D., Renzi T.A., Villa A., Bolego C., D'Avila F. et al. Self-renewal and phenotypic conversion are the main physiological responses of macrophages to the endogenous estrogen surge. Sci. Rep. 2017; 7: 44270. https://dx.doi.org/ 10.1038/srep44270.
Senokuchi T., Matsumura T., Sakai M., Matsuo T., Yano M., Kiritoshi S. et al. Extracellular signal-regulated kinase and p38 mitogen-activated protein kinase mediate macrophage proliferation induced by oxidized low-density lipoprotein. Atherosclerosis. 2004; 176(2): 233-45. https://dx.doi.org/10.1016/j.atherosclerosis.2004.05.019.
Ishii N., Matsumura T., Kinoshita H., Motoshima H., Kojima K., Tsutsumi A. et al. Activation of AMP-activated protein kinase suppresses oxidized low-density lipoprotein-induced macrophage proliferation. J. Biol. Chem. 2009; 284(50): 34561-9. https://dx.doi.org/10.1074/jbc.M109.028043.
Biwa T., Hakamata H., Sakai M., Miyazaki A., Suzuki H., Kodama T. et al. Induction of murine macrophage growth by oxidized low density lipoprotein is mediated by granulocyte macrophage colony-stimulating factor. J. Biol. Chem. 1998; 273(43): 28305-13. https://dx.doi.org/10.1074/jbc.273.43.28305.
Villa A., Rizzi N., Vegeto E., Ciana P., Maggi A. Estrogen accelerates the resolution of inflammation in macrophagic cells. Sci. Rep. 2015; 5(1): 15224. https://dx.doi.org/10.1038/srep15224.
Cousins F.L., Kirkwood P.M., Saunders P.T.K., Gibson D.A. Evidence for a dynamic role for mononuclear phagocytes during endometrial repair and remodelling. Sci. Rep. 2016; 6(1): 36748. https://dx.doi.org/10.1038/srep36748.
Hunt J.S., Robertson S.A. Uterine macrophages and environmental programming for pregnancy success. J. Reprod. Immunol. 1996; 32(1): 1-25. https://dx.doi.org/10.1016/s0165-0378(96)88352-5.
Wira C.R., Fahey J.V., Rodriguez-Garcia M., Shen Z., Patel M.V. Regulation of mucosal immunity in the female reproductive tract: the role of sex hormones in immune protection against sexually transmitted pathogens. Am. J. Reprod. Immunol. 2014; 72(2): 236-58. https://dx.doi.org/10.1111/aji.12252.
Thiruchelvam U., Dransfield I., Saunders P.T.K., Critchley H.O.D. The importance of the macrophage within the human endometrium. J. Leukoc. Biol. 2013; 93(2): 217-25. https://dx.doi.org/10.1189/jlb.0712327.
Lash G.E., Pitman H., Morgan H.L., Innes B.A., Agwu C.N., Bulmer J.N. Decidual macrophages: key regulators of vascular remodeling in human pregnancy. J. Leukoc. Biol. 2016; 100(2): 315-25. https://dx.doi.org/10.1189/jlb.1A0815-351R.
Smith S.D., Dunk C.E., Aplin J.D., Harris L.K., Jones R.L. Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy. Am. J. Pathol. 2009; 174(5): 1959-71. https://dx.doi.org/10.2353/ajpath.2009.080995.
Hazan A.D., Smith S.D., Jones R.L., Whittle W., Lye S.J., Dunk C.E. Vascular-leukocyte interactions. Am. J. Pathol. 2010; 177(2): 1017-30. https://dx.doi.org/10.2353/ajpath.2010.091105.
Chen Q., Guo F., Jin H.Y., Lau S., Stone P., Chamley L. Phagocytosis of apoptotic trophoblastic debris protects endothelial cells against activation. Placenta. 2012; 33(7): 548-53. https://dx.doi.org/10.1016/j.placenta.2012.03.007.
Katabuchi H., Yih S., Ohba T., Matsui K., Takahashi K., Takeya M., Okamura H. Characterization of macrophages in the decidual atherotic spiral artery with special reference to the cytology of foam cells. Med. Electron Microsc. 2003; 36(4): 253-62. https://dx.doi.org/10.1007/S00795-003-0223-2.
Reister F., Frank H.G., Heyl W., Kosanke G., Huppertz B., Schröder W. et al. The distribution of macrophages in spiral arteries of the placental bed in pre-eclampsia differs from that in healthy patients. Placenta. 1999; 20(2-3): 229-33. https://dx.doi.org/10.1053/PLAC.1998.0373.
Berkane N., Liere P., Oudinet J.P., Hertig A., Lefèvre G., Pluchino N. et al. From pregnancy to preeclampsia: a key role for estrogens. Endocr. Rev. 2017; 38(2): 123-44. https://dx.doi.org/10.1210/er.2016-1065.
Napso T., Yong H.E.J., Lopez-Tello J., Sferruzzi-Perri A.N. The role of placental hormones in mediating maternal adaptations to support pregnancy and lactation. Front. Physiol. 2018; 9: 1091. https://dx.doi.org/10.3389/fphys.2018.01091.
Schmidt M., Kreutz M., Löffler G., Schölmerich J., Straub R.H. Conversion of dehydroepiandrosterone to downstream steroid hormones in macrophages. J. Endocrinol. 2000; 164(2): 161-9.
Tang Z., Tadesse S., Norwitz E., Mor G., Abrahams V.M., Guller S. Isolation of hofbauer cells from human term placentas with high yield and purity. Am. J. Reprod. Immunol. 2011; 66(4): 336-48. https://dx.doi.org/10.1111/j.1600-0897.2011.01006.x.
Salas S.P., Marshall G., Gutiérrez B.L., Rosso P. Time course of maternal plasma volume and hormonal changes in women with preeclampsia or fetal growth restriction. Hypertension. 2006; 47(2): 203-8. https://dx.doi.org/10.1161/01.HYP.0000200042.64517.19.
Hertig A., Liere P., Chabbert-Buffet N., Fort J., Pianos A., Eychenne B. et al. Steroid profiling in preeclamptic women: Evidence for aromatase deficiency. Am. J. Obstet. Gynecol. 2010; 203(5): 477.e1-477.e9. https://dx.doi.org/10.1016/j.ajog.2010.06.011.
Bussen S., Bussen D. Influence of the vascular endothelial growth factor on the development of severe pre-eclampsia or HELLP syndrome. Arch. Gynecol. Obstet. 2011; 284(3): 551-7. https://dx.doi.org/10.1007/s00404-010-1704-x.
Jobe S.O., Tyler C.T., Magness R.R. Aberrant synthesis, metabolism, and plasma accumulation of circulating estrogens and estrogen metabolites in preeclampsia implications for vascular dysfunction. Hypertension. 2013; 61(2): 480-7. https://dx.doi.org/10.1161/HYPERTENSIONAHA.111.201624.
Yin G., Zhu X., Guo C., Yang Y., Han T., Chen L. et al. Differential expression of estradiol and estrogen receptor α in severe preeclamptic pregnancies compared with normal pregnancies. Mol. Med. Rep. 2013; 7(3): 981-5. https://dx.doi.org/10.3892/mmr.2013.1262.
Vishnyakova P., Poltavets A., Nikitina M., Midiber K., Mikhaleva L., Muminova K. et al. Expression of estrogen receptor α by decidual macrophages in preeclampsia. Biomedicines. 2021; 9(2): 1-13. https://dx.doi.org/10.3390/biomedicines9020191.
Zhang Y., Wang T., Shen Y., Wang X., Baker P.N., Zhao A. 2-Methoxyestradiol deficiency is strongly related to hypertension in early onset severe pre-eclampsia. Pregnancy Hypertens. 2014; 4(3): 215-9. https://dx.doi.org/10.1016/j.preghy.2014.04.004.
Açıkgöz Ş., Bayar U.O., Can M., Güven B., Mungan G., Doğan S., Sümbüloğlu V. Levels of oxidized LDL, estrogens, and progesterone in placenta tissues and serum paraoxonase activity in preeclampsia. Mediators Inflamm. 2013; 2013: 862982. https://dx.doi.org/10.1155/2013/862982.
Bussen S., Rieger L., Sütterlin M., Dietl J. Plasma VEGF levels are increased in women with severe preeclampsia or HELLP syndrome. Z. Geburtshilfe Neonatol. 2003; 207(3): 101-6. https://dx.doi.org/10.1055/s-2003-40977.
Lang T.J. Estrogen as an immunomodulatory. Clin. Immunol. 2004; 113(3): 224-30. https://dx.doi.org/10.1016/J.CLIM.2004.05.011.
Kloc M., ed. Macrophages origin, functions and biointervention. Cham: Springer Nature; 2017. https://dx.doi.org/10.1007/978-3-319-54090-0_3.
Thomas J.R., Appios A., Zhao X., Dutkiewicz R., Donde M., Lee C.Y.C. et al. Phenotypic and functional characterization of first-trimester human placental macrophages, Hofbauer cells. J. Exp. Med. 2020; 218(1): e20200891. https://dx.doi.org/10.1084/jem.20200891.
Kim S.Y., Romero R., Tarca A.L., Bhatti G., Kim C.J., Lee J. et al. Methylome of fetal and maternal monocytes and macrophages at the feto-maternal interface. Am. J. Reprod. Immunol. 2012; 68(1): 8-27. https://dx.doi.org/10.1111/j.1600-0897.2012.01108.x.
Yang S.W., Cho E.H., Choi S.Y., Lee Y.K., Park J.H., Kim M.K. et al. DC-SIGN expression in Hofbauer cells may play an important role in immune tolerance in fetal chorionic villi during the development of preeclampsia. J. Reprod. Immunol. 2017; 124: 30-7. https://dx.doi.org/10.1016/j.jri.2017.09.012.
Tang Z., Buhimschi I.A., Buhimschi C.S., Tadesse S., Norwitz E., Niven-Fairchild T. et al. Decreased levels of folate receptor-β and reduced numbers of fetal macrophages (Hofbauer cells) in placentas from pregnancies with severe pre-eclampsia. Am. J. Reprod. Immunol. 2013; 70(2): 104-15. https://dx.doi.org/10.1111/aji.12112.
Ma Y., Ye Y., Zhang J., Ruan C.C., Gao P.J. Immune imbalance is associated with the development of preeclampsia. Medicine (Baltimore). 2019; 98(14): e15080. https://dx.doi.org/10.1097/MD.0000000000015080.
Than N.G., Erez O., Wildman D.E., Tarca A.L., Edwin S.S., Abbas A. et al. Severe preeclampsia is characterized by increased placental expression of galectin-1. J. Matern. Fetal Neonatal Med. 2008; 21(7): 429-42. https://dx.doi.org/10.1080/14767050802041961.
Perucci L.O., Corrêa M.D., Dusse L.M., Gomes K.B., Sousa L.P. Resolution of inflammation pathways in preeclampsia-a narrative review. Immunol. Res. 2017; 65(4): 774-89. https://dx.doi.org/10.1007/S12026-017-8921-3.
Przybyl L., Haase N., Golic M., Rugor J., Solano M.E., Arck P.C. et al. CD74-downregulation of placental macrophage-trophoblastic interactions in preeclampsia. Circ. Res. 2016; 119(1): 55-68. https://dx.doi.org/10.1161/CIRCRESAHA.116.308304.
Evsen M.S., Kalkanli S., Deveci E., Sak M.E., Ozler A., Baran O. et al. Human placental macrophages (Hofbauer cells) in severe preeclampsia complicated by HELLP syndrome: immunohistochemistry of chorionic villi. Anal. Quant. Cytopathol. Histopathol. 2013; 35(5): 283-8.
Aggarwal R., Jain A.K., Mittal P., Kohli M., Jawanjal P., Rath G. Association of pro- and anti-inflammatory cytokines in preeclampsia. J. Clin. Lab. Anal. 2019; 33(4): e22834. https://dx.doi.org/10.1002/jcla.22834.
Williams P.J., Bulmer J.N., Searle R.F., Innes B.A., Robson S.C. Altered decidual leucocyte populations in the placental bed in pre-eclampsia and foetal growth restriction: a comparison with late normal pregnancy. Reproduction. 2009; 138(1): 177-84. https://dx.doi.org/10.1530/rep-09-0007.
Bürk M.R., Troeger C., Brinkhaus R., Holzgreve W., Hahn S. Severely reduced presence of tissue macrophages in the basal plate of pre-eclamptic placentae. Placenta. 2001; 22(4): 309-16. https://dx.doi.org/10.1053/plac.2001.0624.
Milosevic-Stevanovic J., Krstic M., Radovic-Janosevic D., Popovic J., Tasic M., Stojnev S. Number of decidual natural killer cells & macrophages in pre-eclampsia. Indian J. Med. Res. 2016; 144(6): 823-30. https://dx.doi.org/10.4103/ijmr.IJMR_776_15.
Al-Khafaji L.A., Al-Yawer M.A. Localization and counting of CD68-labelled macrophages in placentas of normal and preeclamptic women. AIP Conference Proceedings. 2017; 1888: 20011. https://dx.doi.org/10.1063/1.5004289.
Schonkeren D., van der Hoorn M.L., Khedoe P., Swings G., van Beelen E., Claas F. et al. Differential distribution and phenotype of decidual macrophages in preeclamptic versus control pregnancies. Am. J. Pathol. 2011; 178(2): 709-17. https://dx.doi.org/10.1016/j.ajpath.2010.10.011.
Vishnyakova P., Poltavets A., Nikitina M., Muminova K., Potapova A., Vtorushina V. et al. Preeclampsia: inflammatory signature of decidual cells in early manifestation of disease. Placenta. 2021; 104: 277-83. https://dx.doi.org/10.1016/j.placenta.2021.01.011.

Received 12.01.2022

Accepted 21.02.2022

Polina A. Vishnyakova, PhD, Senior Researcher, Laboratory of Regenerative Medicine, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of the Russian Federation; Assistant of the Department of Histology, Cytology and Embryology, Medical Institute, RUDN University, p_vishnyakova@oparina4.ru, https://orcid.org/0000-0001-8650-8240, 117997, Russia, Moscow, Ac. Oparina str., 4.
Andrey V. Elchaninov, Dr. Med. Sci., Head of the Laboratory of Regenerative Medicine, Academician V.I. Kulakov National Medical Research Center for Obstetrics,
Gynecology and Perinatology, Ministry of Health of the Russian Federation, elchandrey@yandex.ru, https://orcid.org/0000-0002-2392-4439,
117997, Russia, Moscow, Ac. Oparina str., 4.
Viktoria V. Kiseleva, Junior Researcher, Laboratory of Regenerative Medicine, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of the Russian Federation, victoria.kurnosova.1991@gmail.com, https://orcid.org/0000-0002-3001-4820,
117997, Russia, Moscow, Ac. Oparina str., 4.
Kamilla T. Muminova, Ph.D., Researcher of 1st Department of Obstetric Pathology of Pregnancy, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology, Perinatology, Ministry of Health of the Russian Federation, k_muminova@oparina4.ru, https://orcid.org/0000-0003-2708-4366,
117997, Russia, Moscow, Ac. Oparina str., 4.
Zulfiya S. Khodzhaeva, Dr. Med. Sci., Professor, Deputy Director for Research, Institute of Obstetrics, Academician V.I. Kulakov National Medical Research Center
for Obstetrics, Gynecology, Perinatology, Ministry of Health of the Russian Federation, zkhodjaeva@mail.ru, https://orcid.org/0000-0001-8159-3714,
117997, Russia, Moscow, Ac. Oparina str., 4.
Irina Z. Eremina, Ph.D., Associate Professor, Head of Educational Part of the Department of Histology, Cytology and Embryology, Medical Institute of the RUDN University, eremina_iz@rudn.university, 117997, Russia, Moscow, Miklukho-Maklaya str., 8.
Timur Kh. Fatkhudinov, Dr. Med. Sci., Deputy Director, A.P. Avtsyn Research Institute of Human Morphology; Head of the Department of Histology,
Cytology and Embryology, Deputy Director for Research, Medical Institute of the RUDN University, tfat@yandex.ru, https://orcid.org/0000-0002-6498-5764,
117997, Russia, Moscow, Miklukho-Maklaya str., 8.

Authors’ contributions: Vishnyakova P.A., Elchaninov A.V., Kiseleva V.V., Muminova K.T., Khodzhaeva Z.S., Eremina I.Z., Fatkhudinov T.Kh. – literature analysis; data summation; writing the article.
Conflicts of interest: The authors declare that there are no conflicts of interest.
Funding: The investigation has been conducted within the framework of State Assignment No. 121032500100-3. This has been also supported by the Russian Federation President’s grant MK-1573.2022.3 for young Russian scientists, candidates of sciences.
For citation: Vishnyakova P.A., Elchaninov A.V., Kiseleva V.V.,
Muminova K.T., Khodzhaeva Z.S., Eremina I.Z., Fatkhudinov T.Kh. The role of placental macrophages in physiological pregnancy and preeclampsia.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2022; 4: 5-12 (in Russian)
https://dx.doi.org/10.18565/aig.2022.4.5-12

The role of placental macrophages in physiological pregnancy and preeclampsia

Vishnyakova P.A., Elchaninov A.V., Kiseleva V.V., Muminova K.T., Khodzhaeva Z.S., Eremina I.Z., Fatkhudinov T.Kh.

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