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Bogdanova I.M.

Avtsyn Research Institute of Human Morphology of the Petrovsky Russian Scientific Center of Surgery

Artemieva K.A.

Avtsyn Research Institute of Human Morphology of the Petrovsky Russian Scientific Center of Surgery

Boltovskaya M.N.

Avtsyn Research Institute of Human Morphology of the Petrovsky Russian Scientific Center of Surgery

Nizyaeva N.V.

Avtsyn Research Institute of Human Morphology of the Petrovsky Russian Scientific Center of Surgery

Kulikov I.A.

Vidnovsky Perinatal Center

Functional cytokine redundancy in pregnancy

Authors:

Bogdanova I.M., Artemieva K.A., Boltovskaya M.N., Nizyaeva N.V., Kulikov I.A.

More about the authors

Journal: Russian Journal of Human Reproduction. 2024;30(6): 73‑80

DOI: 10.17116/repro20243006173

Views: 438

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Table of contents

FUNCTIONAL CYTOKINE REDUNDANCY IN PREGNANCY
FUNCTIONAL CYTOKINE REDUNDANCY IN PREGNANCY

To cite this article:

Bogdanova IM, Artemieva KA, Boltovskaya MN, Nizyaeva NV, Kulikov IA. Functional cytokine redundancy in pregnancy. Russian Journal of Human Reproduction. 2024;30(6):73‑80. (In Russ.)
https://doi.org/10.17116/repro20243006173

 
 
Подписка 2025-2 (Russian Journal of Human Reproduction)
 
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The development of pregnancy depends on complex interrelated processes of adaptation of the maternal immune system to pregnancy, aimed at creating a tolerant environment that is favorable for the developing embryo and at the same time protecting the mother and fetus from infections. Utero-placental zone and secrete a large panel of cytokines with pro-inflammatory and anti-inflammatory activity. Cytokines are key effector mediators that determine the successful course and outcome of pregnancy. at all stages of the gestational process. T-helper (Th1) and Th2 cells secrete cytokines with pro-inflammatory (tumor necrosis factor-α, interferon-γ, interleukin (IL)-1) and anti-inflammatory (IL-4, IL-5, IL-6, IL-10, IL-13 and granulocyte-macrophage colony-stimulating factor) properties that regulate immune functions in utero-placental zone. Cytokines are involved in maintaining a balance between the inflammatory and anti-inflammatory response and are required for the induction of maternal-fetal tolerance to a semi-allogeneic fetus, placental formation, and for adequate trophoblast invasion and neovascularization. The aim of the review is to analyze the current data on the complementary and overlapping roles of cytokines in human pregnancy and to characterize the fundamental cytokines involved in key steps of the reproductive process.

Keywords:

pregnancy
cytokines
placenta
immune tolerance
inflammation

Authors:

Bogdanova I.M.

Avtsyn Research Institute of Human Morphology of the Petrovsky Russian Scientific Center of Surgery

Artemieva K.A.

Avtsyn Research Institute of Human Morphology of the Petrovsky Russian Scientific Center of Surgery

Boltovskaya M.N.

Avtsyn Research Institute of Human Morphology of the Petrovsky Russian Scientific Center of Surgery

Nizyaeva N.V.

Avtsyn Research Institute of Human Morphology of the Petrovsky Russian Scientific Center of Surgery

Kulikov I.A.

Vidnovsky Perinatal Center

Received:

25.01.2024

Accepted:

31.10.2024

List of references:

  1. Ali S, Majid S, Niamat Ali M, Taing S. Evaluation of T cell cytokines and their role in recurrent miscarriage. International Immunopharmacology. 2020;82:106347. https://doi.org/10.1016/j.intimp.2020.106347
  2. Mor G. Introduction to the immunology of pregnancy. Immunological Reviews. 2022;308(1):5-8.  https://doi.org/10.1111/imr.13102
  3. Kervancioglu Demirci E, Salamonsen LA, Gauster M. The role of CX3CL1 in fetal-maternal interaction during human gestation. Cell Adhesion and Migration. 2016;10(1-2):189-96.  https://doi.org/10.1080/19336918.2015.1089378
  4. Munro SK, Balakrishnan B, Lissaman AC, Gujral P, Ponnampalam AP. Cytokines and pregnancy: Potential regulation by histone deacetylases. Molecular Reproduction and Development. 2021;88(5): 321-337.  https://doi.org/10.1002/mrd.23430
  5. Lin JX, Leonard WJ. Fine-tuning cytokine signals. Annual Review of Immunology. 2019;37:295-324.  https://doi.org/10.1146/annurev-immunol-042718-041447
  6. Mor G, Aldo P, Alvero AB. The unique immunological and microbial aspects of pregnancy. Nature Reviews Immunology. 2017;17(8): 469-482.  https://doi.org/10.1038/nri.2017.64
  7. Yang X, Tian Y, Zheng L, Luu T, Kwak-Kim J. The update immune-regulatory role of pro- and anti-inflammatory cytokines in recurrent pregnancy losses. International Journal of Molecular Sciences. 2022;24(1):132.  https://doi.org/10.3390/ijms24010132
  8. Wang M, Zhai X, Li J, Guan J, Xu S, Li Y, Zhu H. The role of cytokines in predicting the response and adverse events related to immune checkpoint inhibitors. Frontiers in Immunology. 2021;12: 670391. https://doi.org/10.3389/fimmu.2021.670391
  9. Meyyazhagan A Kuchi Bhotla H, Pappuswamy M, Tsibizova V, Al Qasem M, Di Renzo GC. Cytokine see-saw across pregnancy, its related complexities and consequences. International Journal of Gynecology and Obstetrics. 2023;160(2):516-525.  https://doi.org/10.1002/ijgo.14333
  10. Mor G, Cardenas I, Abrahams V, Guller S. Inflammation and pregnancy: the role of the immune system at the implantation site. Annals of the New York Academy of Sciences. 2011;1221(1):80-87.  https://doi.org/10.1111/j.1749-6632.2010.05938.x
  11. Ramhorst R, Fraccaroli L, Aldo P, Alvero AB, Cardenas I, Leirós CP, Mor G. Modulation and recruitment of inducible regulatory T cells by first trimester trophoblast cells. American Journal of Reproductive Immunology. 2012;67(1):17-27.  https://doi.org/10.1111/j.1600-0897.2011.01056.x
  12. Zenclussen AC, Hämmerling GJ. Cellular regulation of the uterine microenvironment that enables embryo implantation. Frontiers in Immunology. 2015;6:321.  https://doi.org/10.3389/fimmu.2015.00321
  13. Pantos K, Grigoriadis S, Maziotis E Pistola K, Xystra P, Pantou A, Kokkali G, Pappas A, Lambropoulou M, Sfakianoudis K, Simopoulou M. The role of interleukins in recurrent implantation failure: a comprehensive review of the literature. International Journal of Molecular Sciences. 2022;23(4):2198. https://doi.org/10.3390/ijms23042198
  14. Østensen M, Förger F, Villiger PM. Cytokines and pregnancy in rheumatic disease. Annals of the New York Academy of Sciences. 2006;1069:353-363.  https://doi.org/10.1196/annals.1351.033
  15. Saito S. Cytokine network at the feto-maternal interface. American Journal of Reproductive Immunology. 2000;47(2):87-103.  https://doi.org/10.1016/s0165-0378(00)00060-7
  16. Romero R, Espinoza J, Gonçalves LF, Kusanovic JP, Friel LA, Nien JK. Inflammation in preterm and term labour and delivery. Seminars in Fetal Neonatal Medicine. 2006;11(5):317-326.  https://doi.org/10.1016/j.siny.2006.05.001
  17. Vignali DA, Kuchroo VK. IL-12 family cytokines: immunological playmakers. Nature Immunology. 2012;13(8):722-728.  https://doi.org/10.1038/ni.2366
  18. You Y, Stelzl P, Joseph DN, Aldo PB, Maxwell AJ, Dekel N, Liao A, Whirledge S, Mor G. TNF-α regulated endometrial stroma secretome promotes trophoblast invasion. Frontiers in Immunology. 2021;12:737401. https://doi.org/10.3389/fimmu.2021.737401
  19. Haider S, Knöfler M. Human tumour necrosis factor: physiological and pathological roles in placenta and endometrium. Placenta. 2009;30(2):111-123.  https://doi.org/10.1016/j.placenta.2008.10.012
  20. Hefler LA, Tempfer CB, Unfried G, Schneeberger C, Lessl K, Nagele F, Huber JC. A polymorphism of the interleukin-1beta gene and idiopathic recurrent miscarriage. Fertility and Sterility. 2001; 76(2):377-379.  https://doi.org/10.1016/s0015-0282(01)01914-8
  21. Nilkaeo A, Bhuvanath S. Interleukin-1 modulation of human placental trophoblast proliferation. Mediators of Inflammation. 2006; 2006(2):79359. https://doi.org/10.1155/MI/2006/79359
  22. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions.
  23. Journal of Leukocyte Biology. 2004;75(2):163-189.  https://doi.org/10.1189/jlb.0603252
  24. Karmakar S, Dhar R, Das C. Inhibition of cytotrophoblastic (JEG-3) cell invasion by interleukin 12 involves an interferon gamma-mediated pathway.
  25. Journal of Biological Chemistry. 2004;279(53):55297-55307. https://doi.org/10.1074/jbc.M407013200
  26. Murphy SP, Tayade C, Ashkar AA, Hatta K, Zhang J, Croy BA. Interferon gamma in successful pregnancies. Biology of Reproduction. 2009;80(5):848-859.  https://doi.org/10.1095/biolreprod.108.07335
  27. Trinchieri G, Pflanz S, Kastelein RA. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity. 2003;19(5):641-644.  https://doi.org/10.1016/s1074-7613(03)00296-6
  28. Pongcharoen S, Somran J, Sritippayawan S, Niumsup P, Chanchan P, Butkhamchot P, Tatiwat P, Kunngurn S, Searle RF. Interleukin-17 expression in the human placenta. Placenta. 2007;28(1):59-63.  https://doi.org/10.1016/j.placenta.2006.01.016
  29. Piccinni MP, Raghupathy R, Saito S, Szekeres-Bartho J. Cytokines, hormones and cellular regulatory mechanisms favoring successful reproduction. Frontiers in Immunology. 2021;12:717808. https://doi.org/10.3389/fimmu.2021.717808
  30. Ruiz de Morales JMG, Puig L, Daudén E, Cañete JD, Pablos JL, Martín AO, Juanatey CG, Adán A, Montalbán X, Borruel N, Ortí G, Holgado-Martín E, García-Vidal C, Vizcaya-Morales C, Martín-Vázquez V, González-Gay MÁ. Critical role of interleukin (IL)-17 in inflammatory and immune disorders: An updated review of the evidence focusing in controversies. Autoimmunity Reviews. 2020; 19(1):102429. https://doi.org/10.1016/j.autrev.2019.102429
  31. Murakami M, Kamimura D, Hirano T. Pleiotropy and specificity: Insights from the interleukin 6 family of cytokines. Immunity. 2019;50(4):812-831.  https://doi.org/10.1016/j.immuni.2019.03.027
  32. Rose-John S. Interleukin-6 family cytokines. Cold Spring Harbor Perspectives in Biology. 2018;10(2):a028415. https://doi.org/10.1101/cshperspect.a028415
  33. Vilotić A, Nacka-Aleksić M, Pirković A, Bojić-Trbojević Ž, Dekanski D, Jovanović Krivokuća M. IL-6 and IL-8: An overview of their roles in healthy and pathological pregnancies. International Journal of Molecular Sciences. 2022;23(23):14574. https://doi.org/10.3390/ijms232314574
  34. Brosnahan MM, Miller DC, Adams M, Antczak DF. IL-22 is expressed by the invasive trophoblast of the equine (Equus caballus) chorionic girdle. Journal of Immunology. 2012;188(9):4181-4187. https://doi.org/10.4049/jimmunol.1103509
  35. Wang Y, Xu B, Li MQ, Li DJ, Jin LP. IL-22 secreted by decidual stromal cells and NK cells promotes the survival of human trophoblasts. International Journal of Clinical and Experimental Pathology. 2013;6(9):1781-1790.
  36. Cheng SB, Sharma S. Interleukin-10: a pleiotropic regulator in pregnancy. American Journal of Reproductive Immunology. 2015;73(6): 487-500.  https://doi.org/10.1111/aji.12329
  37. Sabat R, Grütz G, Warszawska K, Kirsch S, Witte E, Wolk K, Geginat J. Biology of interleukin-10. Cytokine Growth Factor Reviews. 2010;21(5):331-344.  https://doi.org/10.1016/j.cytogfr.2010.09.002
  38. Pandey M, Chauhan M, Awasthi S. Interplay of cytokines in preterm birth. Indian Journal of Medical Research. 2017;146(3):316-327.  https://doi.org/10.4103/ijmr.IJMR_1624_14
  39. Wang H, Wang LL, Zhao SJ, Lin XX, Liao AH. IL-10: A bridge between immune cells and metabolism during pregnancy. American Journal of Reproductive Immunology. 2022;154:103750. https://doi.org/10.1016/j.jri.2022.103750
  40. Paiva P, Menkhorst E, Salamonsen L, Dimitriadis E. Leukemia inhibitory factor and interleukin-11: critical regulators in the establishment of pregnancy. Cytokine Growth Factor Reviews. 2009; 20(4):319-28.  https://doi.org/10.1016/j.cytogfr.2009.07.001
  41. Dimitriadis E, Robb L, Salamonsen LA. Interleukin 11 advances progesterone-induced decidualization of human endometrial stromal cells. Molecular Human Reproduction. 2002;8(7):636-643.  https://doi.org/10.1093/molehr/8.7.636
  42. Markert UR, Morales-Prieto DM, Fitzgerald JS. Understanding the link between the IL-6 cytokine family and pregnancy: implications for future therapeutics. Expert Review of Clinical Immunology. 2011;7(5):603-609.  https://doi.org/10.1586/eci.11.60
  43. Winship A, Correia J, Krishnan T, Menkhorst E, Cuman C, Zhang JG, Nicola NA, Dimitriadis E. Blocking endogenous leukemia inhibitory factor during placental development in mice leads to abnormal placentation and pregnancy loss. Scientific Reports. 2015;5:13237. https://doi.org/10.1038/srep13237
  44. Prossler J, Chen Q, Chamley L, James JL. The relationship between TGFβ, low oxygen and the outgrowth of extravillous trophoblasts from anchoring villi during the first trimester of pregnancy. Cytokine. 2014;68(1):9-15.  https://doi.org/10.1016/j.cyto.2014.03.001
  45. Jones RL, Stoikos C, Findlay JK, Salamonsen LA. TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction. 2006;132(2):217-232.  https://doi.org/10.1530/rep.1.01076
  46. Li Y, Yan J, Chang HM, Chen ZJ, Leung PCK. Roles of TGF-β Superfamily Proteins in Extravillous Trophoblast Invasion. Trends in Endocrinology and Metabolism. 2021;32(3):170-189.  https://doi.org/10.1016/j.tem.2020.12.005
  47. Ni N, Li Q. TGFβ superfamily signaling and uterine decidualization. Reproductive Biology and Endocrinology. 2017;15(1):84.  https://doi.org/10.1186/s12958-017-0303-0
  48. Trinh QD, Pham NTK, Takada K, Ushijima H, Komine-Aizawa S, Hayakawa S. Roles of TGF-β1 in viral infection during pregnancy: Research update and perspectives. International Journal of Molecular Sciences. 2023;24(7):6489. https://doi.org/10.3390/ijms24076489
  49. Gusniev SA, Polner SA, Mikhaleva LM, Ilina NI, Esakova AP, Kurbacheva OM, Shilovskiy IP, Khaitov MR. Influence of interleukin-33 gene expression on clinical and morphological characteristics of the nasal mucosa in allergic rhinitis. Immunologiya. 2021;42(1):68-79. (In Russ.). https://doi.org/10.33029/0206-4952-2021-42-1-68-79
  50. Smithgall MD, Comeau MR, Yoon BR, Kaufman D, Armitage R, Smith DE. IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. International Immunology. 2008;20(8):1019-1030. https://doi.org/10.1093/intimm/dxn060
  51. Gajardo Carrasco T, Morales RA, Pérez F, Terraza C, Yáñez L, Campos-Mora M, Pino-Lagos K. Alarmin’ immunologists: IL-33 as a putative target for modulating T cell-dependent responses. Frontiers in Immunology. 2015;6:232.  https://doi.org/10.3389/fimmu.2015.00232
  52. Salker MS, Nautiyal J, Steel JH, Webster Z, Sućurović S, Nicou M, Singh Y, Lucas ES, Murakami K, Chan YW, James S, Abdallah Y, Christian M, Croy BA, Mulac-Jericevic B, Quenby S, Brosens JJ. Disordered IL-33/ST2 activation in decidualizing stromal cells prolongs uterine receptivity in women with recurrent pregnancy loss. PLoS One. 2012;7(12):e52252. https://doi.org/10.1371/journal.pone.0052252
  53. Chatterjee P, Chiasson VL, Bounds KR, Mitchell BM. Regulation of the anti-inflammatory cytokines interleukin-4 and interleukin-10 during pregnancy. Frontiers in Immunology. 2014;5:253.  https://doi.org/10.3389/fimmu.2014.00253

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