Mast cell involvement in physiological and preeclampsia complicated pregnancy
AbstractMast cells (MCs) are multifunctional tissue-resident cells generated from hematopoietic precursors in the bone marrow, migrate through the circulatory system to the periphery, where they settle on the mucosal surface and in the connective tissue of many organs and complete differentiation and maturation. The phenotypic characteristics of MCs and their functional activity are determined by the local microenvironment. MCs are key inducers and modulators of allergic, anaphylactic and other inflammatory reactions. MCs secrete a wide range of preformed or newly synthesized biologically active products with pro- and anti-inflammatory properties in response to multiple stimuli. Upon activation, MCs secrete histamine, leukotrienes and prostanoids, as well as proteases and a variety of cytokines and chemokines. The wide tissue distribution and ability to respond to many different stimuli suggests the involvement of MCs in many physiological and pathological processes in the body. Data from experimental studies on rodents indicate the involvement of uterine MCs in the processes of blastocyst implantation and placenta formation. An important role of MCs in the processes of remodeling of the uterine spiral arteries, as well as in creating a maternal microenvironment tolerant for the fetus, has also been shown. However to date few studies have been devoted to the contribution of MCs to the pathogenesis of obstetric pathologies including preeclampsia (PE). This review focuses on analyzes the role of MCs in various physiological and pathological conditions, including key pathogenetic mechanisms of preeclampsia.
Keywords:review; mast cells; inflammation; pregnancy; preeclampsia
For citation: Bogdanova I.M., Artemyeva K.A., Boltovskaya M.N., Kondashevskaya M.V., Nizyaeva N.V. Mast cell involvement in physiological and preeclampsia complicated pregnancy. Immunologiya. 2022; 43 (6): 736–45. DOI: https://doi.org/10.33029/0206-4952-2022-43-6-736-745 (in Russain)
Funding. The study was carried out within the framework of State assignment of A.P. Avtsyn RIHM of «B.V. Petrovsky NRCS», MSHE of Russia (No 122030200534-4).
Conflict of interests. The authors declare no conflict of interests.
Authors’ contribution. Concept and design of the review – Bogdanova I.M., Nizyaeva N.V., Kondashevskaya M.V.; literature collection and analysis – Bogdanova I.M., Artemyeva K.A., Nizyaeva N.V.; text writing – Bogdanova I.M.; literature analysis and text editing – Boltovskaya M.N.
References
1. Okayama Y., Kawakami T. Development, migration, and survival of mast cells. Immunol. Res. 2006; 34 (2): 97–115. DOI: https://doi.org/10.1385/IR:34:2:97
2. Kalesnikoff J., Galli S.J. New developments in mast cell biology. Nat. Immunol. 2008; 9 (11): 1215–23. DOI: https://doi.org/10.1038/ni.f.216
3. Komi D.E.A., Mortaz E., Amani S., Tiotiu A., Folkerts G., Adcock I.M. The role of mast cells in IgE -independent lung diseases. Clin. Rev. Allergy Immunol. 2020; 58 (3): 377–87. DOI: https://doi.org/10.1007/s12016-020-08779-5
4. Redegeld F.A., Yu V., Kumari S., Charles N., Blank U. Non-IgE mediated mast cell activation. Immunol. Rev. 2018; 282 (1): 87–113. DOI: https://doi.org/10.1111/imr.12629
5. Woidacki K., Jensen F., Zenclussen A.C. Mast cells as novel mediators of reproductive processes. Front. Immunol. 2013; 4: 29. DOI: https://doi.org/10.3389/fimmu.2013.00029
6. Woidacki K., Meyer N., Schumacher A., Goldschmidt A., Maurer M., Zenclussen A.C. Transfer of regulatory T cells into abortion-prone mice promotes the expansion of uterine mast cells and normalizes early pregnancy angiogenesis. Sci. Rep. 2015; 5: 13938. DOI: https://doi.org/10.1038/srep13938
7. Meyer N., Woidacki K., Knöfler M., Meinhardt G., Nowak D., Velicky P., Pollheimer J., Zenclussen A.C. Chymase-producing cells of the innate immune system are required for decidual vascular remodeling and fetal growth. Sci. Rep. 2017; 7: 45106. DOI: https://doi.org/10.1038/srep45106
8. Matsuno T., Toyoshima S., Sakamoto-Sasaki T., Kashiwakura J.I., Matsuda A., Watanabe Y., Azuma H., Kawana K., Yamamoto T., Okayama Y. Characterization of human decidual mast cells and establishment of a culture system. Allergol. Int. 2018; 67S: S18–24. DOI: https://doi.org/10.1016/j.alit.2018.05.001
9. Wernersson S., Pejler G. Mast cell secretory granules: armed for battle. Nat. Rev. Immunol. 2014; 14 (7): 478–94. DOI: https://doi.org/10.1038/nri3690
10. Elieh Ali Komi D, Wöhrl S, Bielory L. Mast cell biology at molecular level: a comprehensive review. Clin. Rev. Allergy Immunol. 2020; 58 (3): 342–65. DOI: https://doi.org/10.1007/s12016-019-08769-2
11. Krishnaswamy G., Ajitawi O., Chi D.S. The human mast cell: an overview. Methods Mol. Biol. 2006; 315: 13–34. DOI: https://doi.org/10.1385/1-59259-967-2:013
12. Pastwińska J., Żelechowska P., Walczak-Drzewiecka A., Brzezińska-Błaszczyk E., Dastych J. The art of mast cell adhesion. Cells. 2020; 9 (12): 2664. DOI: https://doi.org/10.3390/cells9122664
13. Metcalfe D.D., Boyce J.A. Mast cell biology in evolution. J. Allergy Clin. Immunol. 2006; 117 (6): 1227–9. DOI: https://doi.org/10.1016/j.jaci.2006.03.031
14. Gusel’nikova V.V., Polevshchikov A.V. Thymic mast cells: at three-way crossroads. Immunologiya. 2021; 42 (4): 327–36. DOI: https://doi.org/10/33029/0206-4952-2021-42-4-327-336 (in Russian)
15. Krystel-Whittemore M., Dileepan K.N., Wood J.G. Mast cell: a multi-functional master cell. Front. Immunol. 2016; 6: 620. DOI: https://doi.org/10.3389/fimmu.2015.00620
16. Varricchi G., Rossi F.W., Galdiero M.R., Granata F., Criscuolo G., Spadaro G., de Paulis A., Marone G. Physiological roles of mast cells: collegium internationale allergologicum update 2019. Int. Arch. Allergy Immunol. 2019; 179 (4): 247–61. DOI: https://doi.org/10.1159/000500088
17. Amin K. The role of mast cells in allergic inflammation. Respir. Med. 2012; 106 (1): 9–14. DOI: https://doi.org/10.1016/j.rmed.2011.09.007
18. Sobiepanek A., Kuryk Ł., Garofalo M., Kumar S., Baran J., Musolf P., Siebenhaar F., Fluhr J.W., Kobiela T., Plasenzotti R., Kuchler K., Staniszewska M. The multifaceted roles of mast cells in immune homeostasis, infections and cancers. Int. J. Mol. Sci. 2022; 23 (4): 2249. DOI: https://doi.org/10.3390/ijms23042249
19. Krishnaswamy G., Kelley J., Johnson D., Youngberg G., Stone W., Huang S.K., Bieber J., Chi D.S. The human mast cell: functions in physiology and disease. Front. Biosci. 2001; 6: D1109–27. DOI: https://doi.org/10.2741/krishnas
20. Aneman I., Pienaar D., Suvakov S., Simic T. P., Garovic V. D., McClements L. Mechanisms of key innate immune cells in early- and late-onset preeclampsia. Front. Immunol. 2020; 11: 1864. DOI: https://doi.org/10. 3389/fimmu.2020.01864
21. Sotnikova N.Yu., Farzalieva A.V., Borzova N.Yu., Voronin D.N., Kroshkina N.V. Characteristics of monocyte differentiation and CD163 expression in women with pointed early mission. Immunologiya. 2022; 43 (6): 714–21. DOI: https://doi.org/10.33029/0206-4952-2021-42-6-714-721 (in Russian)
22. Artemieva K.A., Bogdanova I.M., Stepanova I.I., Stepanov A.A., Tikhonova N.B., Boltovskaya M.N., Kalyuzhin O.V., Zemlyakov A.E. Production of transforming growth factor β and interleukin-10 in the mouse spleen at early stage of gestation in models of spontaneous and muramylpeptide-dependent abortions. Immunologiya. 2021;42(2):131–9. DOI: https://doi.org/10.33029/0206-4952-2021-42-2-131-139 (in Russian)
23. De Falco S. The discovery of placenta growth factor and its biological activity. Exp. Mol. Med. 2012; 44 (1): 1–9. DOI: https://doi.org/10.3858/emm.2012.44.1.025
24. Faas M.M., de Vos P. Innate immune cells in the placental bed in healthy pregnancy and preeclampsia. Placenta. 2018; 69: 125–33. DOI: https://doi.org/10.1016/j/placenta.2018.04.012
25. Szewczyk G., Pyzlak M., Klimkiewicz J., Smiertka W., Miedzińska-Maciejewska M., Szukiewicz D. Mast cells and histamine: do they influence placental vascular network and development in preeclampsia? Mediators Inflamm. 2012; 2012: 307189. DOI: https://doi.org/10.1155/2012/307189
26. Maynard S.E., Karumanchi S.A. Angiogenic factors and preeclampsia. Semin. Nephrol. 2011; 31 (1): 33–46. DOI: https://doi.org/10.1016/j.semnephrol.2010.10.004
27. Seki H. Balance of antiangiogenic and angiogenic factors in the context of the etiology of preeclampsia. Acta Obstet. Gynecol. Scand. 2014; 93 (10): 959–64. DOI: https://doi.org/10.1111/aogs.12473
28. Venkatesha S., Toporsian M., Lam C., Hanai J., Mammoto T., Kim Y.M., Bdolah Y., Lim K.H., Yuan H.T., Libermann T.A., Stillman I.E., Roberts D., D’Amore P.A., Epstein F.H., Sellke F.W., Romero R, Sukhatme V.P., Letarte M., Karumanchi S.A. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat. Med. 2006; 12 (6): 642–9. DOI: https://doi.org/10.1038/nm1429
29. Purcell W.M., Hanahoe T.H. A novel source of mast cells: the human placenta. Agents Actions. 1991; 33 (1–2): 8–12. DOI: https://doi.org/10.1007/BF01993113
30. Szukiewicz D., Szukiewicz A., Maslinska D., Gujski M., Poppe P., Mazurek-Kantor J. Mast cell number, histamine concentration and placental vascular response to histamine in preeclampsia. Inflamm. Res. 1999; 48 (suppl 1): S39–40. DOI: https://doi.org/10.1007/s000110050390
31. Norrby K. Mast cells and angiogenesis. APMIS. 2002; 110 (5): 355–71. DOI: https://doi.org/10.1034/j.1600-0463.2002.100501.x
32. Moon T.C., Befus A.D., Kulka M. Mast cell mediators: their differential release and the secretory pathways involved. Front. Immunol. 2014; 5: 569. DOI: https://doi.org/10.3389/fimmu.2014.00569
33. Dvorak H.F., Nagy J.A., Feng D., Brown L.F., Dvorak A.M. Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr. Top. Microbiol. Immunol. 1999; 237: 97–132. DOI: https://doi.org/10.1007/978-3-642-59953-8_6
34. Linfert D., Chowdhry T., Rabb H. Lymphocytes and ischemia-reperfusion injury. Transplant. Rev. (Orlando). 2009; 23 (1): 1–10. DOI: https://doi.org/10.1016/j.trre.2008.08.003
35. Hung T.H., Burton G.J. Hypoxia and reoxigenation: a possible mechanisms for placental oxidative stress in preeclampsia. Taiwan J. Obstet. Gynecol. 2006; 45 (3): 189–200. DOI: https://doi.org/10.1016/S1028-4559(09)60224-2
36. Yang M.Q., Ma Y.Y., Ding J., Li J.Y. The role of mast cells in ischemia and reperfusion injury. Inflamm. Res. 2014; 63 (11): 899–905. DOI: https://doi.org/10.1007/s00011-014-0763-z
37. Andoh A., Kimura T., Fukuda M., Araki Y., Fujiyama Y., Bamba T. Rapid intestinal ischaemia-reperfusion injury is suppressed in genetically mast cell-deficient Ws/Ws rats. Clin. Exp. Immunol. 1999; 116 (1): 90–3. DOI: https://doi.org/10.1046/j.1365-2249.1999.00851.x
38. Irani R.A., Xia Y. The functional role of the renin-angiotensin system in pregnancy and preeclampsia. Placenta. 2008; 29 (9): 763–71. DOI: https://doi.org/10.1016/j.placenta.2008.06.011
39. Silver R.B., Reid A.C., Mackins C.J., Askwith T., Schaefer U., Herzlinger D., Levi R. Mast cells: a unique source of renin. Proc. Natl Acad. Sci. USA. 2004; 101 (37): 13 607–12. DOI: https://doi.org/10.1073/pnas.0403208101
40. Peters H., Unger T. Mast cells and the power of local RAS activation. Nephrol. Dial. Transplant. 2007; 22 (1): 40–2. DOI: https://doi.org/10.1093/ndt/gfl544
41. 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. DOI: https://doi.org/10.1530/REP-09-0007
42. Bilinski M.J., Thorne J.G., Oh M.J., Leonard S., Murrant C., Tayade C., Croy B.A. Uterine NK cells in murine pregnancy. Reprod. Biomed. Online. 2008; 16 (2): 218–26. DOI: https://doi.org/10.1016/s1472-6483(10)60577-9
43. Plaks V., Birnberg T., Berkutzki T., Sela S., BenYashar A., Kalchenko V., Mor G., Keshet E., Dekel N., Neeman M., Jung S. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Invest. 2008; 118 (12): 3954–65. DOI: https://doi.org/10.1172/JCI36682
44. Schumacher A., Heinze K., Witte J., Poloski E., Linzke N., Woidacki K., Zenclussen A.C. Human chorionic gonadotropin as a central regulator of pregnancy immune tolerance. J. Immunol. 2013; 190 (6): 2650–8. DOI: https://doi.org/10.4049/jimmunol.1202698
45. Munoz-Suano A., Hamilton A.B., Betz A.G. Gimme shelter: the immune system during pregnancy. Immunol. Rev. 2011; 241 (1): 20–38. DOI: https://doi.org/10.1111/j.1600-065X.2011.01002.x
46. Miller D., Motomura K., Galaz J., Gershater M., Lee E.D., Romero R., Gomez-Lopez N. Cellular immune responses in the pathophysiology of preeclampsia. J. Leukoc. Biol. 2022; 111 (1): 237–60. DOI: https://doi.org/10.1002/JLB.5RU.1120-787RR
47. LaMarca B., Cornelius D., Wallace K. Elucidating immune mechanisms causing hypertension during pregnancy. Physiology (Bethesda). 2013; 28 (4): 225–33. DOI: https://doi.org/10.1152/physiol.00006.2013
48. Toldi G., Molvarec A., Stenczer B., Müller V., Eszes N., Bohács A., Bikov A., Rigó J. Jr., Vásárhelyi B., Losonczy G., Tamási L. Peripheral T(h)1/T(h)2/T(h)17/regulatory T-cell balance in asthmatic pregnancy. Int. Immunol. 2011; 23 (11): 669–77. DOI: https://doi.org/10.1093/intimm/dxr074
49. Darmochwal-Kolarz D., Kludka-Sternik M., Tabarkiewicz J., Kolarz B., Rolinski J., Leszczynska-Gorzelak B., Oleszczuk J. The predominance of Th17 lymphocytes and decreased number and function of Treg cells in preeclampsia. J. Reprod. Immunol. 2012; 93 (2): 75–81. DOI: https://doi.org/10.1016/j.jri.2012.01.006
50. Collier A.Y., Smith L.A., Karumanchi S.A. Review of the immune mechanisms of preeclampsia and the potential of immune modulating therapy. Hum. Immunol. 2021; 82 (5): 362–70. DOI: https://doi.org/10.1016/j.humimm.2021.01.004
51. Voronova O.V., Milovanov A.P., Mikhaleva L.M. Integration approach to study placental vessels in preeclampsia. Klinicheskaya i eksperimental’naya morfologiya. 2022; 11 (3): 30–44. DOI: https://doi.org/10.31088/CEM2022.11.3.30-44 (in Russian)
52. De Filippo K., Dudeck A., Hasenberg M., Nye E., van Rooijen N., Hartmann K., Gunzer M., Roers A., Hogg N. Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation. Blood. 2013; 121 (24): 4930–7. DOI: https://doi.org/10.1182/blood-2013-02-486217
53. Forward N.A., Furlong S.J., Yang Y., Lin T.J., Hoskin D.W. Mast cells down-regulate CD4+CD25+ T regulatory cell suppressor function via histamine H1 receptor interaction. J. Immunol. 2009; 183 (5): 3014–22. DOI: https://doi.org/10.4049/jimmunol.0802509
54. Caughey G.H. Mast cell tryptases and chymases in inflammation and host defense. Immunol. Rev. 2007; 217: 141–54. DOI: https://doi.org/10.1111/j.1600-065X.2007.00509.x
55. Mitani R., Maeda K., Fukui R., Endo S., Saijo Y., Shinokara K. Kamada M., Irahara M., Yamano S., Nakaya Y., Aono T. Production of human mast cell chymase in human myometrium and placenta in cases of normal pregnancy and preeclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 2002; 101 (2): 155–60. DOI: https://doi.org/10.1016/s0301-2115(01)00546-2
56. Broekhuizen M., Hitzerd E., van den Bosch T.P.P., Dumas J., Verdijk R.M., van Rijn B.B., Danser A.H.J., van Eijck C.H.J., Reiss I.K.M., Mustafa D.A.M. The placental innate immune system is altered in early-onset preeclampsia, but not in late-onset preeclampsia. Front. Immunol. 2021; 12: 780043. DOI: https://doi.org/10.3389/fimmu.2021.780043
57. Lampiasi N. Interactions between macrophages and mast cells in the female reproductive system. Int. J. Mol. Sci. 2022; 23 (10): 5414. DOI: https://doi.org/10.3390/ijms23105414