Acetylcholine contributes to control the physiological inflammatory response during the peri-implantation period

Background: Maternal antigen-presenting cells attracted to the pregnant uterus interact with trophoblast cells and modulate their functional profile to favour immunosuppressant responses. Non-neuronal cholinergic system is expressed in human cytotrophoblast cells and in immune cells with homeostatic...

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Autor principal: Paparini, D.
Otros Autores: Gori, S., Grasso, E., Scordo, W., Calo, G., Pérez Leirós, C., Ramhorst, R., Salamone, G.
Formato: Capítulo de libro
Lenguaje:Inglés
Publicado: Blackwell Publishing Ltd 2015
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Acceso en línea:Registro en Scopus
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Sumario:Background: Maternal antigen-presenting cells attracted to the pregnant uterus interact with trophoblast cells and modulate their functional profile to favour immunosuppressant responses. Non-neuronal cholinergic system is expressed in human cytotrophoblast cells and in immune cells with homeostatic regulatory functions. Aim: The aim of this work was to evaluate whether non-neuronal acetylcholine conditions maternal monocyte and DC migration and activation profiles. Methods: We used an in vitro model resembling maternal-placental interface represented by the co-culture of human trophoblast cells (Swan-71 cell line) and monocytes or DC. Results: When cytotrophoblast cells were treated with neostigmine (Neo) to concentrate endogenous acetylcholine levels, monocyte migration was increased. In parallel, high levels of IL-10 and decreased levels of TNF-α were observed upon interaction of maternal monocytes with trophoblast cells. This effect was synergized by Neo and was prevented by atropine, a muscarinic acetylcholine receptor antagonist. Similarly, trophoblast cells increased the migration of DC independently of Neo treatment; however, enhanced IL-10 and MCP-1 synthesis in trophoblast-DC co-cultures with no changes in TNF-α and IL-6 was observed. In fact, there were no changes in HLA-DR, CD86 or CD83 expression. Finally, trophoblast cells treated with Neo increased the expression of two antigen-presenting cells attracting chemokines, MCP-1, MIP-1α and RANTES through muscarinic receptors, and it was prevented by atropine. Conclusions: Our present results support a novel role of acetylcholine synthesized by trophoblast cells to modulate antigen-presenting cell migration and activation favouring an immunosuppressant profile that contributes to immune homeostasis maintenance at the maternal-foetal interface. © 2015 Scandinavian Physiological Society. Published by John Wiley & Sons Ltd.
Bibliografía:Abrahams, V.M., Kim, Y.M., Straszewski, S.L., Romero, R., Mor, G., Macrophages and apoptotic cell clearance during pregnancy (2004) Am J Reprod Immunol, 51, pp. 275-282
Aluvihare, V.R., Kallikourdis, M., Betz, A.G., Tolerance, suppression and the fetal allograft (2005) J Mol Med (Berl), 83, pp. 88-96
Aplin, J.D., Straszewski-Chavez, S.L., Kalionis, B., Dunk, C., Morrish, D., Forbes, K., Baczyk, D., Knöfler, M., Trophoblast differentiation: progenitor cells, fusion and migration - a workshop report (2006) Placenta, 27, pp. S141-S143
Bhuiyan, M.B., Murad, F., Fant, M.E., The placental cholinergic system: localization to the cytotrophoblast and modulation of nitric oxide (2006) Cell Commun Signal, 4, p. 4
Biswas, S., Chittezhath, M., Shalova, I., Lim, J.-Y., Macrophage polarization and plasticity in health and disease (2012) Immunol Res, 53, pp. 11-24
Blois, S.M., Ilarregui, J.M., Tometten, M., Garcia, M., Orsal, A.S., Cordo-Russo, R., Toscano, M.A., Handjiski, B., A pivotal role for galectin-1 in fetomaternal tolerance (2007) Nat Med, 13, pp. 1450-1457
Borovikova, L.V., Ivanova, S., Zhang, M., Yang, H., Botchkina, G.I., Watkins, L.R., Wang, H., Tracey, K.J., Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin (2000) Nature, 405, pp. 458-462
Dekel, N., Gnainsky, Y., Granot, I., Mor, G., Inflammation and implantation (2010) Am J Reprod Immunol, 63, pp. 17-21
Dominguez, F., Yáñez-Mó, M., Sanchez-Madrid, F., Simon, C., Embryonic implantation and leukocyte transendothelial migration: different processes with similar players? (2005) FASEB J, 19, pp. 1056-1060
Fest, S., Aldo, P.B., Abrahams, V.M., Visintin, I., Alvero, A., Chen, R., Chavez, S.L., Mor, G., Trophoblast-macrophage interactions: a regulatory network for the protection of pregnancy (2007) Am J Reprod Immunol, 57, pp. 55-66
Fraccaroli, L., Alfieri, J., Leiros, C., Ramhorst, R., Immunomodulatory effects of chemokines during the early implantation window (2009) Front Biosci, 1, pp. 288-298
Fraccaroli, L., Alfieri, J., Larocca, L., Calafat, M., Mor, G., Perez Leirós, C., Ramhorst, R., A potential tolerogenic immune mechanism in a trophoblast cell line through the activation of chemokine-induced T cell death and regulatory T cell modulation (2009) Hum Reprod, 24, pp. 166-175
Girardi, G., Yarilin, D., Thurman, J.M., Holers, V.M., Salmon, J.E., Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction (2006) J Exp Med, 203, pp. 2165-2175
Gomez-Lopez, N., Guilbert, L., Olson, D.M., Invasion of the leukocytes into the fetal-maternal interface during pregnancy (2010) J Leukoc Biol, 88, pp. 625-633
Grando, S.A., Kawashima, K., Kirkpatrick, C.J., Meurs, H., Wessler, I., The non-neuronal cholinergic system: basic science, therapeutic implications and new perspectives (2012) Life Sci, 91, pp. 969-972
Grasso, E., Paparini, D., Hauk, V., Salamone, G., Leiros, C.P., Ramhorst, R., Differential migration and activation profile of monocytes after trophoblast interaction (2014) PLoS ONE, 9, pp. 1-10
Harris, L.K., IFPA Gabor Than Award lecture: transformation of the spiral arteries in human pregnancy: key events in the remodelling timeline (2011) Placenta, 32, pp. 154-158
Huang, Y., Zhu, X., Du, M., Li, D.-J., Human trophoblasts recruited T lymphocytes and monocytes into decidua by secretion of chemokine CXCL16 and interaction with CXCR6 in the first-trimester pregnancy (2008) J Immunol, 180, pp. 2367-2375
Jiang, X., Bar, H.Y., Yan, J., Jones, S., Brannon, P.M., West, A.A., Perry, C.A., Caudill, M.A., A higher maternal choline intake among third-trimester pregnant women lowers placental and circulating concentrations of the antiangiogenic factor fms-like tyrosine kinase-1 (sFLT1) (2013) FASEB J, 27, pp. 1245-1253
Kwak-Kim, J., Park, J., Ahn, H., Kim, J., Gilman-Sachs, A., Immunological modes of pregnancy loss (2010) Am J Reprod Immunol, 63, pp. 611-623
Laskarin, G., Kämmerer, U., Rukavina, D., Thomson, A.W., Fernandez, N., Blois, S.M., Antigen-presenting cells and materno-fetal tolerance: an emerging role for dendritic cells (2007) Am J Reprod Immunol, 58, pp. 255-267
Leber, A., Teles, A., Zenclussen, A.C., Regulatory T cells and their role in pregnancy (2010) Am J Reprod Immunol, 63, pp. 445-459
Liu, T., Xie, C., Chen, X., Zhao, F., Liu, A.M., Cho, D.B., Chong, J.Y.P., Role of muscarinic receptor activation in regulating immune cell activity in nasal mucosa (2010) Allergy, 65, pp. 969-977
Mor, G., Inflammation and pregnancy: the role of toll-like receptors in trophoblast-immune interaction (2008) Ann N Y Acad Sci, 1127, pp. 121-128
Mor, G., Cardenas, I., The immune system in pregnancy: a unique complexity (2010) Am J Reprod Immunol, 63, pp. 425-433
Mor, G., Straszewski-Chavez, S.L., Abrahams, V., Macrophage-trophoblast interactions (2006) Methods Mol Med, 122, pp. 149-163
Mosser, D.M., Edwards, J.P., Exploring the full spectrum of macrophage activation (2008) Nat Rev Immunol, 8, pp. 958-969
Nagamatsu, T., Schust, D., The contribution of macrophages to normal and pathological pregnancies (2010) Am J Reprod Immunol, 63, pp. 460-471
Olubadewo, J.O., Rama Sastry, B.V., Human placental cholinergic system: stimulation-secretion coupling for release of acetylcholine from isolated placental villus (1978) J Pharmacol Exp Ther, 204, pp. 433-445
Pérez Leirós, C., Ramhorst, R., Tolerance induction at the early maternal-placental interface through selective cell recruitment and targeting by immune polypeptides (2013) Am J Reprod Immunol, 69, pp. 359-368
Plaks, V., Birnberg, T., Berkutzki, T., Sela, S., Benyashar, A., Kalchenko, V., Mor, G., Jung, S., Uterine DCs are crucial for decidua formation during embryo implantation in mice (2008) J Clin Invest, 118, pp. 3954-3965
Redman, C., Sargent, I., Immunology of pre-eclampsia (2010) Am J Reprod Immunol, 63, pp. 534-543
Renaud, S., Graham, C., The role of macrophages in utero-placental interactions during normal and pathological pregnancy (2008) Immunol Invest, 37, pp. 535-564
Salamone, G., Lombardi, G., Gori, S., Nahmod, K., Jancic, C., Amaral, M.M., Vermeulen, M., Geffner, J., Cholinergic modulation of dendritic cell function (2011) J Neuroimmunol, 236, pp. 47-56
Salamone, G., Fraccaroli, L., Gori, S., Grasso, E., Paparini, D., Geffner, J., Leirós, C.P., Ramhorst, R., Trophoblast cells induce a tolerogenic profile in dendritic cells (2012) Hum Reprod, 27, pp. 2598-2606
Sastry, B., Janson, V., Cholinergic markers in transformed trophoblast cells: BeWo and JAr cells (1997) Cell Mol Biol, 43, pp. 559-565
Satyanarayana, M., A correlative review of acetylcholine synthesis in relation to histopathology of the human syncytiotrophoblast (1986) Acta Obstet Gynecol Scand, 65, pp. 567-572
Sica, A., Mantovani, A., Macrophage plasticity and polarization: in vivo veritas (2012) J Clin Invest, 122, pp. 787-795
Straszewski-Chavez, S.L., Abrahams, V.M., Alvero, A.B., Aldo, P.B., Ma, Y., Guller, S., Romero, R., Mor, G., The isolation and characterization of a novel telomerase immortalized first trimester trophoblast cell line, Swan 71 (2009) Placenta, 30, pp. 939-948
Tayebati, S., Sabbatini, M., Zaccheo, D., Amenta, F., Muscarinic cholinergic receptor subtypes expression by human placenta (1997) Neurosci Lett, 221, pp. 208-212
Tayebati, S., Vitaioli, L., Zaccheo, D., Amenta, F., Autoradiographic localisation of muscarinic cholinergic receptor subtypes in human placenta (1998) Neurosci Lett, 247, pp. 167-170
Terness, P., Kallikourdis, M., Betz, A.G., Tolerance signaling molecules and pregnancy: IDO, galectins, and the renaissance of regulatory T cells (2007) Am J Reprod Immunol, 58, pp. 238-254
Thaxton, J., Sharma, S., Interleukin-10: a multi-faceted agent of pregnancy (2010) Am J Reprod Immunol, 63, pp. 482-491
Wessler, I., Kirkpatrick, C.J., Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans (2008) Br J Pharmacol, 154, pp. 1558-1571
Wessler, I., Michel-Schmidt, R., Brochhausen, C., Kirkpatrick, C.J., Subcellular distribution of choline acetyltransferase by immunogold electron microscopy in non-neuronal cells: placenta, airways and murine embryonic stem cells (2012) Life Sci, 91, pp. 977-980
ISSN:17481708
DOI:10.1111/apha.12494