Artículo

Paparini, D.; Gori, S.; Grasso, E.; Scordo, W.; Calo, G.; Pérez Leirós, C.; Ramhorst, R.; Salamone, G. "Acetylcholine contributes to control the physiological inflammatory response during the peri-implantation period" (2015) Acta Physiologica. 214(2):237-247
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

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.

Registro:

Documento: Artículo
Título:Acetylcholine contributes to control the physiological inflammatory response during the peri-implantation period
Autor:Paparini, D.; Gori, S.; Grasso, E.; Scordo, W.; Calo, G.; Pérez Leirós, C.; Ramhorst, R.; Salamone, G.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, IQUIBICEN-CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Medicina Experimental-IMEX-CONICET, Academia Nacional de Medicina, Buenos Aires, Argentina
Servicio de Medicina Transfusional, Hospital Italiano de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Dendritic cells; Monocytes; Non-neuronal acetylcholine; Trophoblast cells; acetylcholine; atropine; CD83 antigen; CD86 antigen; HLA DR antigen; interleukin 10; interleukin 6; macrophage inflammatory protein 1alpha; monocyte chemotactic protein 1; muscarinic receptor; neostigmine; RANTES; tumor necrosis factor alpha; acetylcholine; antigen presenting cell; Article; cell interaction; coculture; controlled study; cytokine production; cytotrophoblast; dendritic cell; female; human; human cell; immunomodulation; in vitro study; inflammation; leukocyte activation; leukocyte migration; monocyte; nidation; placenta; priority journal; protein expression; protein synthesis; swan 71 cell line; trophoblast; cell separation; cytology; immunology; inflammation; metabolism; nidation; pregnancy; procedures; trophoblast; Acetylcholine; Cell Separation; Coculture Techniques; Embryo Implantation; Female; Humans; Inflammation; Placenta; Pregnancy; Trophoblasts
Año:2015
Volumen:214
Número:2
Página de inicio:237
Página de fin:247
DOI: http://dx.doi.org/10.1111/apha.12494
Título revista:Acta Physiologica
Título revista abreviado:Acta Physiol.
ISSN:17481708
CAS:acetylcholine, 51-84-3, 60-31-1, 66-23-9; atropine, 51-55-8, 55-48-1; macrophage inflammatory protein 1alpha, 155075-84-6; neostigmine, 114-80-7, 588-17-0, 59-99-4, 8048-84-8; Acetylcholine
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_17481708_v214_n2_p237_Paparini

Referencias:

  • 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

Citas:

---------- APA ----------
Paparini, D., Gori, S., Grasso, E., Scordo, W., Calo, G., Pérez Leirós, C., Ramhorst, R.,..., Salamone, G. (2015) . Acetylcholine contributes to control the physiological inflammatory response during the peri-implantation period. Acta Physiologica, 214(2), 237-247.
http://dx.doi.org/10.1111/apha.12494
---------- CHICAGO ----------
Paparini, D., Gori, S., Grasso, E., Scordo, W., Calo, G., Pérez Leirós, C., et al. "Acetylcholine contributes to control the physiological inflammatory response during the peri-implantation period" . Acta Physiologica 214, no. 2 (2015) : 237-247.
http://dx.doi.org/10.1111/apha.12494
---------- MLA ----------
Paparini, D., Gori, S., Grasso, E., Scordo, W., Calo, G., Pérez Leirós, C., et al. "Acetylcholine contributes to control the physiological inflammatory response during the peri-implantation period" . Acta Physiologica, vol. 214, no. 2, 2015, pp. 237-247.
http://dx.doi.org/10.1111/apha.12494
---------- VANCOUVER ----------
Paparini, D., Gori, S., Grasso, E., Scordo, W., Calo, G., Pérez Leirós, C., et al. Acetylcholine contributes to control the physiological inflammatory response during the peri-implantation period. Acta Physiol. 2015;214(2):237-247.
http://dx.doi.org/10.1111/apha.12494