CELLS OF IMMUNE SYSTEM OF MOTHER АND TROPHOBLAST CELLS: CONSTRUCTIVE COOPERATION FOR THE SAKE OF ACHIEVEMENT OF THE JOINT PURPOSE

Cover Page


Cite item

Full Text

Abstract

In the present review modern data about change of morfo-functional properties of a trophoblast during pregnancy, and also about influence of the cytokines produced by cells of a microenvironment, including leucocytes of mother, on a functional state of trophoblast is cited. Features of interaction between trophoblast and immune cells of mother are described within physiological pregnancy and within pregnancy complicated by preeclampsia.

 

About the authors

E. K. Ailamazyan

D.O. Ott Research Institute of Obstetrics and Gynecology North-West Branch under the Russian Academy of Medical Sciences, St. Petersburg, Russian Federation

Author for correspondence.
Email: iag@ott.ru
PhD, professor, academician of RAMS, Honoured scientist of Russian Federation, Director of FSBI “D. O. Ott Research Institute of Obstetrics and Gynecology”, Russian Academy of Medical Sciences. Address: 3, Mendeleevskaya line, St. Petersburg, RF, 199034, tel.: (812) 325-32-20 Russian Federation

O. I. Stepanova

D.O. Ott Research Institute of Obstetrics and Gynecology North-West Branch under the Russian Academy of Medical Sciences, St. Petersburg, Russian Federation

Email: alzas@mail.ru
MD, research scientist of Laboratory of Immunology of FSBI “D. O. Ott Research Institute of Obstetrics and Gynecology”, Russian Academy of Medical Sciences. Address: 3, Mendeleevskaya line, St. Petersburg, RF, 199034, tel.: (812) 323-75-45 Russian Federation

S. A. Sel'kov

D.O. Ott Research Institute of Obstetrics and Gynecology North-West Branch under the Russian Academy of Medical Sciences, St. Petersburg, Russian Federation

Email: elkovsa@mail.ru
PhD, professor, Head of Laboratory of Immunology of FSBI “D. O. Ott Research Institute of Obstetrics and Gynecology”, Russian Academy of Medical Sciences. Address: 3, Mendeleevskaya line, St. Petersburg, RF, 199034, tel.: (812) 323-75-45 Russian Federation

D. I. Sokolov

D.O. Ott Research Institute of Obstetrics and Gynecology North-West Branch under the Russian Academy of Medical Sciences, St. Petersburg, Russian Federation

Email: falcojugger@yandex.ru
PhD, leading research scientist of Laboratory of Immunology of FSBI “D. O. Ott Research Institute of Obstetrics and Gynecology”, Russian Academy of Medical Sciences. Address: 3, Mendeleevskaya line, St. Petersburg, RF, 199034, tel.: (812) 323-75-45, (812) 328-98-50 Russian Federation

References

  1. Huppertz B. The anatomy of the normal placenta. J. Clin. Pathol. 2008; 61 (12): 1296-1302.
  2. James J.L., Carter A.M., Chamley L.W. Human placentation from nidation to 5 weeks of gestation. Part I: What do we know about formative placental development following implantation? Placenta. 2012; 33 (5): 327-334.
  3. Dolzhikov A.A., Zabolotnaya S.V. Prikladnaya morfologiya dlya studentov i vrachei: morfologiya posleda cheloveka [Practical Morphology for Students and Doctors: Morphology of Homan Secundines]. Belgorod, 2005. p. 41.
  4. Fitzgerald J.S., Poehlmann T.G., Schleussner E., Markert U.R. Trophoblast invasion: the role of intracellular cytokine signalling via signal transducer and activator of transcription 3 (STAT3). Hum. Reprod Update. 2008; 14 (4): 335-344.
  5. Cartwright J.E., Fraser R., Leslie K., Wallace A.E., James J.L. Remodelling at the maternal-fetal interface: relevance to human pregnancy disorders. Reproduction. 2010; 140 (6): 803-813.
  6. Tapia A., Salamonsen L.A., Manuelpillai U., Dimitriadis E. Leukemia inhibitory factor promotes human first trimester extravillous trophoblast adhesion to extracellular matrix and secretion of tissue inhibitor of metalloproteinases-1 and -2. Hum. Reprod. 2008; 23 (8): 1724-1732.
  7. Kaufmann P., Black S., Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol. Reprod. 2003; 69 (1): 1-7.
  8. Mori M., Ishikawa G., Luo S.S., Mishima T., Goto T., Robinson J.M., et al. The cytotrophoblast layer of human chorionic villi becomes thinner but maintains its structural integrity during gestation. Biol. Reprod. 2007; 76 (1): 164-172.
  9. Longtine M.S., Chen B., Odibo A.O., Zhong Y., Nelson D.M. Caspase-mediated apoptosis of trophoblasts in term human placental villi is restricted to cytotrophoblasts and absent from the multinucleated syncytiotrophoblast. Reproduction. 2012; 143 (1): 107-121.
  10. Achache H., Revel A. Endometrial receptivity markers, the journey to successful embryo implantation. Hum. Reprod Update. 2006; 12 (6): 731-746.
  11. Staun-Ram E., Shalev E. Human trophoblast function during the implantation process. Reprod Biol. Endocrinol. 2005; 3: 56.
  12. Al-Nasiry S., Spitz B., Hanssens M., Luyten C., Pijnenborg R. Differential effects of inducers of syncytialization and apoptosis on BeWo and JEG-3 choriocarcinoma cells. Hum. Reprod. 2006; 21 (1): 193-201.
  13. Silva R., D'Amico G., Hodivala-Dilke K.M., Reynolds L.E. Integrins: the keys to unlocking angiogenesis. Arterioscler Thromb. Vasc. Biol. 2008; 28 (10): 1703-1713.
  14. Ferretti C., Bruni L., Dangles-Marie V., Pecking A.P., Bellet D. Molecular circuits shared by placental and cancer cells, and their implications in the proliferative, invasive and migratory capacities of trophoblasts. Hum. Reprod Update. 2007; 13 (2): 121-141.
  15. Kabir-Salmani M., Shiokawa S., Akimoto Y., Sakai K., Iwashita M. The role of alpha(5)beta(1)-integrin in the IGF-I-induced migration of extravillous trophoblast cells during the process of implantation. Mol. Hum. Reprod. 2004; 10 (2): 91-97.
  16. Wallace A.E., Fraser R., Cartwright J.E. Extravillous trophoblast and decidual natural killer cells: a remodelling partnership. Hum. Reprod Update. 2012; 18 (4): 458-471.
  17. Wu X., Jin L.P., Yuan M.M., Zhu Y., Wang M.Y., Li D.J. Human first-trimester trophoblast cells recruit CD56brightCD16- NK cells into decidua by way of expressing and secreting of CXCL12/stromal cell-derived factor 1. J. Immunol. 2005; 175 (1): 61-68.
  18. Lash G.E., Schiessl B., Kirkley M., Innes B.A., Cooper A., Searle R.F., et al. Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J. Leukoc Biol. 2006; 80 (3): 572-580.
  19. van Gils J.M., Zwaginga J.J., Hordijk P.L. Molecular and functional interactions among monocytes, platelets, and endothelial cells and their relevance for cardiovascular diseases. J. Leukoc Biol. 2009; 85 (2): 195-204.
  20. Gomez-Lopez N., Guilbert L.J., Olson D.M. Invasion of the leukocytes into the fetal-maternal interface during pregnancy. J. Leukoc Biol. 2010; 88 (4): 625-633.
  21. Cao G., Savani R.C., Fehrenbach M., Lyons C., Zhang L., Coukos G., et al. Involvement of endothelial CD44 during in vivo angiogenesis. Am. J. Pathol. 2006; 169 (1): 325-336.
  22. Horita H., Kuroda E., Hachisuga T., Kashimura M., Yamashita U. Induction of prostaglandin E2 production by leukemia inhibitory factor promotes migration of first trimester extravillous trophoblast cell line, HTR-8/SVneo. Hum. Reprod. 2007; 22 (7): 1801-1809.
  23. Straszewski-Chavez S.L., Abrahams V.M., Mor G. The role of apoptosis in the regulation of trophoblast survival and differentiation during pregnancy. Endocr. Rev. 2005; 26 (7): 877-897.
  24. Hirota Y., Osuga Y., Hasegawa A., Kodama A., Tajima T., Hamasaki K., et al. Interleukin (IL)-1beta stimulates migration and survival of first-trimester villous cytotrophoblast cells through endometrial epithelial cell-derived IL-8. Endocrinology. 2009; 150 (1): 350-356.
  25. Jaleel M.A., Tsai A.C., Sarkar S., Freedman P.V., Rubin L.P. Stromal cell-derived factor-1 (SDF-1) signalling regulates human placental trophoblast cell survival. Mol. Hum. Reprod. 2004; 10 (12): 901-909.
  26. Fukushima K., Miyamoto S., Tsukimori K., Kobayashi H., Seki H., Takeda S., et al. Tumor necrosis factor and vascular endothelial growth factor induce endothelial integrin repertories, regulating endovascular differentiation and apoptosis in a human extravillous trophoblast cell line. Biol. Reprod. 2005; 73 (1): 172-179.
  27. Forbes K., Westwood M. Maternal growth factor regulation of human placental development and fetal growth. J. Endocrinol. 2010; 207 (1): 1-16.
  28. Handwerger S., Aronow B. Dynamic changes in gene expression during human trophoblast differentiation. Recent Prog. Horm. Res. 2003; 58: 263-281.
  29. Leduc K., Bourassa V., Asselin E., Leclerc P., Lafond J., Reyes-Moreno C. Leukemia inhibitory factor regulates differentiation of trophoblastlike BeWo cells through the activation of JAK/STAT and MAPK3/1 MAP kinase-signaling pathways. Biol. Reprod. 2012; 86 (2): 54.
  30. Zhou W.H., Du M.R., Dong L., Yu J., Li D.J. Chemokine CXCL12 promotes the cross-talk between trophoblasts and decidual stromal cells in human first-trimester pregnancy. Hum. Reprod. 2008; 23 (12): 2669-2679.
  31. Prutsch N., Fock V., Haslinger P., Haider S., Fiala C., Pollheimer J., et al. The role of interleukin-1beta in human trophoblast motility. Placenta. 2012; 33 (9): 696-703.
  32. Dominguez F., Martinez S., Quinonero A., Loro F., Horcajadas J.A., Pellicer A., et al. CXCL10 and IL-6 induce chemotaxis in human trophoblast cell lines. Mol. Hum. Reprod. 2008; 14 (7): 423-430.
  33. Lash G.E., Otun H.A., Innes B.A., Kirkley M., De Oliveira L., Searle R.F., et al. Interferon-gamma inhibits extravillous trophoblast cell invasion by a mechanism that involves both changes in apoptosis and protease levels. FASEB J. 2006; 20 (14): 2512-2518.
  34. Paiva P., Salamonsen L.A., Manuelpillai U., Walker C., Tapia A., Wallace E.M., et al. Interleukin-11 promotes migration, but not proliferation, of human trophoblast cells, implying a role in placentation. Endocrinology. 2007; 148 (11): 5566-5572.
  35. Nagamatsu T., Schust D.J. The immunomodulatory roles of macrophages at the maternal-fetal interface. Reprod Sci. 2010; 17 (3): 209-218.
  36. van Mourik M.S., Macklon N.S., Heijnen C.J. Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment. J. Leukoc Biol. 2009; 85 (1): 4-19.
  37. Lash G.E., Otun H.A., Innes B.A., Percival K., Searle R.F., Robson S.C., et al. Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age. Hum. Reprod. 2010; 25 (5): 1137-1145.
  38. Murphy S.P., Tayade C., Ashkar A.A., Hatta K., Zhang J., Croy B.A. Interferon gamma in successful pregnancies. Biol. Reprod. 2009; 80 (5): 848-859.
  39. Laresgoiti-Servitje E., Gomez-Lopez N., Olson D.M. An immunological insight into the origins of pre-eclampsia. Hum Reprod Update. 2010; 16 (5): 510-524.
  40. Sakaguchi S., Wing K., Onishi Y., Prieto-Martin P., Yamaguchi T. Regulatory T cells: how do they suppress immune responses? Int. Immunol. 2009; 21 (10): 1105-1111.
  41. Guerin L.R., Prins J.R., Robertson S.A. Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment? Hum. Reprod Update. 2009; 15 (5): 517-535.
  42. Carosella E.D., Gregori S., LeMaoult J. The tolerogenic interplay(s) among HLA-G, myeloid APCs, and regulatory cells. Blood. 2011; 118 (25): 6499-6505.
  43. Li C., Houser B.L., Nicotra M.L., Strominger J.L. HLA-G homodimer-induced cytokine secretion through HLA-G receptors on human decidual macrophages and natural killer cells. Proc. Natl. Acad. Sci U S A. 2009; 106 (14): 5767-5772.
  44. Salamone G., Fraccaroli L., Gori S., Grasso E., Paparini D., Geffner J., et al. Trophoblast cells induce a tolerogenic profile in dendritic cells. Hum. Reprod. 2012; 27 (9): 2598-2606.
  45. Gorczynski R.M., Lee L., Boudakov I. Augmented Induction of CD4+CD25+ Treg using monoclonal antibodies to CD200R. Transplantation. 2005; 79 (9): 1180-11803.
  46. Nagamatsu T., Schust D.J., Sugimoto J., Barrier B.F. Human decidual stromal cells suppress cytokine secretion by allogenic CD4+ T cells via PD-1 ligand interactions. Hum Reprod. 2009; 24 (12): 3160-3171.
  47. Taglauer E.S., Trikhacheva A.S., Slusser J.G., Petroff M.G. Expression and function of PDCD1 at the human maternal-fetal interface. Biol Reprod. 2008; 79 (3): 562-569.
  48. D'Addio F., Riella L.V., Mfarrej B.G., Chabtini L., Adams L.T., Yeung M., et al. The link between the PDL1 costimulatory pathway and Th17 in fetomaternal tolerance. J Immunol. 2011; 187 (9): 4530-4541.
  49. Sokolov D.I., Sel'kov S.A. Immunologicheskii kontrol' formirovaniya sosudistoi seti platsenty [Immunological Monitoring of Placenta’s Vasculature Formation]. St. Petersburg, Izdatel'stvo N-L, 2012. p. 206.
  50. Harris L.K., Clancy O.H., Myers J.E., Baker P.N. Plasma from women with preeclampsia inhibits trophoblast invasion. Reprod Sci. 2009; 16 (11): 1082-1090.
  51. Irwin J.C., Suen L.F., Martina N.A., Mark S.P., Giudice L.C. Role of the IGF system in trophoblast invasion and pre-eclampsia. Hum. Reprod. 1999; 14 Suppl 2: 90-96.
  52. Renaud S.J., Macdonald-Goodfellow S.K., Graham C.H. Coordinated regulation of human trophoblast invasiveness by macrophages and interleukin 10. Biol. Reprod. 2007; 76 (3): 448-454.
  53. Germain S.J., Sacks G.P., Sooranna S.R., Sargent I.L., Redman C.W. Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles. J. Immunol. 2007; 178 (9): 5949-5956.
  54. Serov V.N. Gestoz — bolezn' adaptatsii [Gestational Toxicosis - Adaptation Disease]. Novosibirsk, RIPEL plyus, 2001. p. 208.
  55. Spierings D.C., de Vries E.G., Vellenga E., van den Heuvel F.A., Koornstra J.J., Wesseling J., et al. Tissue distribution of the death ligand TRAIL and its receptors. J. Histochem Cytochem. 2004; 52 (6): 821-31.
  56. Schiessl B., Innes B.A., Bulmer J.N., Otun H.A., Chadwick T.J., Robson S.C., et al. Localization of angiogenic growth factors and their receptors in the human placental bed throughout normal human pregnancy. Placenta. 2009; 30 (1): 79-87.
  57. Lomunova M.A., Talaev V.Yu. Trophoblast cells of human placenta: the way of their maturation and interaction with the immune system. Immunologiya = Immunology. 2007; 28(1): 50–58.
  58. Scaife P.J., Bulmer J.N., Robson S.C., Innes B.A., Searle R.F. Effector activity of decidual CD8+ T lymphocytes in early human pregnancy. Biol. Reprod. 2006; 75 (4): 562-567.
  59. Chen L.M., Liu B., Zhao H.B., Stone P., Chen Q., Chamley L. IL-6, TNFalpha and TGFbeta promote nonapoptotic trophoblast deportation and subsequently causes endothelial cell activation. Placenta. 2010; 31 (1): 75-80.
  60. Ketlinskii S.A., Cimbirtsev A.S. Tsitokiny [Cytokines]. St. Petersburg, Foliant, 2008. p. 522.
  61. Hannan N.J., Paiva P., Dimitriadis E., Salamonsen L.A. Models for study of human embryo implantation: choice of cell lines? Biol. Reprod. 2010; 82 (2): 235-245.
  62. Piao H.L., Wang S.C., Tao Y., Zhu R., Sun C., Fu Q., et al. Cyclosporine A enhances Th2 bias at the maternal-fetal interface in early human pregnancy with aid of the interaction between maternal and fetal cells. PLoS One. 2012; 7 (9): e45275.
  63. Wu H.X., Guo P.F., Jin L.P., Liang S.S., Li D.J. Functional regulation of thymic stromal lymphopoietin on proliferation and invasion of trophoblasts in human first-trimester pregnancy. Hum. Reprod. 2010; 25 (5): 1146-52.
  64. Ochoa-Reparaz J., Rynda A., Ascon M.A., Yang X., Kochetkova I., Riccardi C., et al. IL-13 production by regulatory T cells protects against experimental autoimmune encephalomyelitis independently of autoantigen. J. Immunol. 2008; 181 (2): 954-68.
  65. Han J., Li L., Hu J., Yu L., Zheng Y., Guo J., et al. Epidermal growth factor stimulates human trophoblast cell migration through Rho A and Rho C activation. Endocrinology. 2010; 151 (4): 1732-42.
  66. Andraweera P.H., Dekker G.A., Roberts C.T. The vascular endothelial growth factor family in adverse pregnancy outcomes. Hum. Reprod Update. 2012; 18 (4): 436-457.
  67. Kalkunte S.S., Mselle T.F., Norris W.E., Wira C.R., Sentman C.L., Sharma S. Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J. Immunol. 2009; 182 (7): 4085-4092.
  68. Fest S., Aldo P.B., Abrahams V.M., Visintin I., Alvero A., Chen R., et al. Trophoblast-macrophage interactions: a regulatory network for the protection of pregnancy. Am. J. Reprod Immunol. 2007; 57 (1): 55-66.
  69. Jovanovic M., Stefanoska I., Radojcic L., Vicovac L. Interleukin-8 (CXCL8) stimulates trophoblast cell migration and invasion by increasing levels of matrix metalloproteinase (MMP)2 and MMP9 and integrins alpha5 and beta1. Reproduction. 2010; 139 (4): 789-798.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 1970 "Paediatrician" Publishers LLC



This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies