Artículo

Ramhorst, R.; Calo, G.; Paparini, D.; Vota, D.; Hauk, V.; Gallino, L.; Merech, F.; Grasso, E.; Leirós, C.P. "Control of the inflammatory response during pregnancy: Potential role of VIP as a regulatory peptide" (2019) Annals of the New York Academy of Sciences. 1437(1):15-21
El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

A network of cell–cell communications through contact and soluble factors supports the maternal–placental interaction and provides a suitable environment for fetal growth. Trophoblast cells take center stage at these loops: they interact with maternal leukocytes to sustain the varying demands of gestation, and they synthesize hormones, cytokines among other factors that contribute to the maintenance of immune homeostasis. Here, we discuss vasoactive intestinal peptide (VIP) and its potential as a regulatory neuropeptide in pregnancy. VIP is synthesized by trophoblast cells; it regulates trophoblast cell function and interaction with the major immune cell populations present in the pregnant uterus. VIP activity produces an anti-inflammatory microenvironment by modulating the functional profile of monocytes, macrophages, and regulatory T cells. Trophoblast VIP inhibits neutrophil extracellular trap formation and accelerates neutrophil apoptosis, enabling their silent clearance by phagocytic cells. The effects of VIP on the trophoblast–immune interaction are consistent with its regulatory role throughout pregnancy for immune homeostasis maintenance. These observations may provide new clues for pharmacological targeting of pregnancy complications associated with exacerbated inflammation. © 2018 New York Academy of Sciences.

Registro:

Documento: Artículo
Título:Control of the inflammatory response during pregnancy: Potential role of VIP as a regulatory peptide
Autor:Ramhorst, R.; Calo, G.; Paparini, D.; Vota, D.; Hauk, V.; Gallino, L.; Merech, F.; Grasso, E.; Leirós, C.P.
Filiación:Laboratory of Immunopharmacology, Department of Biological Chemistry, School of Sciences, University of Buenos Aires, Buenos Aires, Argentina
IQUIBICEN-CONICET, Ciudad Universitaria, Buenos Aires, Argentina
Palabras clave:Immune homeostasis; Pregnancy; Trophoblast cell lines; Vasoactive intestinal polypeptide; vasoactive intestinal polypeptide; apoptosis; cell population; disease control; extracellular trap; homeostasis; human; inflammation; macrophage; monocyte; neutrophil; phagocyte; pregnancy; pregnancy complication; regulatory T lymphocyte; Review; trophoblast
Año:2019
Volumen:1437
Número:1
Página de inicio:15
Página de fin:21
DOI: http://dx.doi.org/10.1111/nyas.13632
Título revista:Annals of the New York Academy of Sciences
Título revista abreviado:Ann. New York Acad. Sci.
ISSN:00778923
CODEN:ANYAA
CAS:vasoactive intestinal polypeptide, 37221-79-7
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00778923_v1437_n1_p15_Ramhorst

Referencias:

  • Racicot, K., Kwon, J.Y., Aldo, P., Understanding the complexity of the immune system during pregnancy (2014) Am. J. Reprod. Immunol., 72, pp. 107-116
  • Harris, L., Aplin, J.D., Vascular remodeling and extracellular matrix breakdown in the uterine spiral arteries during pregnancy (2007) Reprod. Sci., 14, pp. 28-34
  • Smith, S.D., Dunk, C.E., Aplin, J.D., Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy (2009) Am. J. Pathol., 174, pp. 1959-1971
  • Mor, G., Cardenas, I., The immune system in pregnancy: A unique complexity (2010) Am. J. Reprod. Immunol., 63, pp. 425-433
  • Prabhudas, M., Bonney, E., Caron, K., Immune mechanisms at the maternal–fetal interface: Perspectives and challenges (2015) Nat. Immunol., 16, pp. 328-334
  • Munoz-Suano, A., Hamilton, A.B., Betz, A.G., Gimme shelter: The immune system during pregnancy (2011) Immunol. Rev., 241, pp. 20-38
  • Fest, S., Aldo, P.B., Abrahams, V.M., Trophoblast– macrophage interactions: A regulatory network for the protection of pregnancy (2007) Am. J. Reprod. Immunol., 57, pp. 55-66
  • Romero, R., Dey, S.K., Fisher, S.J., Preterm labor: One syndrome, many causes (2014) Science, 345, pp. 760-765
  • Huppertz, B., Weiss, G., Moser, G., Trophoblast invasion and oxygenation of the placenta: Measurements versus presumptions (2014) J. Reprod. Immunol., 101-102, pp. 74-79
  • Khong, Y., Brosens, I., Defective deep placentation (2011) Best Pract. Res. Clin. Obstet. Gynaecol., 25, pp. 301-311
  • Brosens, I., Pijnenborg, R., Vercruysse, L., The “Great Obstetrical Syndromes” are associated with disorders of deep placentation (2008) Am. J. Obstet. Gynecol., 204, pp. 193-201
  • Huppertz, B., Placental origins of preeclampsia: Challenging the current hypothesis (2008) Hypertension, 51, pp. 970-975
  • Redman, C.W.G., Sargent, I.L., Immunology of preeclampsia (2010) Am. J. Reprod. Immunol., 63, pp. 534-543
  • Gülmezoglu, A.M., Lawrie, T.A., Hezelgrave, N., Interventions to reduce maternal and newborn morbidity and mortality (2015) Reproductive, Maternal, Newborn, and Child Health: Disease Control Priorities, pp. 115-136. , 3rd ed. R.E. Black, R. Laxminarayan, M. Temmerman & N. Walker, Eds., Washington, DC: The International Bank for Reconstruction and Development/The World Bank
  • Petty, H.R., Kindzelskii, A.L., Espinoza, J., Trophoblast contact deactivates human neutrophils (2006) J. Immunol., 176, pp. 3205-3514
  • Gomez-Lopez, N., Guilbert, L.J., Olson, D.M., Invasion of the leukocytes into the fetal–maternal interface during pregnancy (2010) J. Leukoc. Biol., 88, pp. 625-633
  • Ramhorst, R., Grasso, E., Paparini, D., Decoding the chemokine network that links leukocytes with decidual cells and the trophoblast during early implantation (2016) Cell Adh. Migr., 10, pp. 197-207
  • Abrahams, V.M., Kim, Y.M., Straszewski, S.L., Macrophages and apoptotic cell clearance during pregnancy (2004) Am. J. Reprod. Immunol., 51, pp. 275-282
  • Straszewski-Chavez, S.L., Abrahams, V.M., Mor, G., The role of apoptosis in the regulation of trophoblast survival and differentiation during pregnancy (2005) Endocr. Rev., 26, pp. 877-897
  • Nagamatsu, T., Schust, D.J., The immunomodulatory roles of macrophages at the maternal–fetal interface (2010) Reprod. Sci., 17, pp. 209-218
  • Faas, M.M., de Vos, P., Uterine NK cells and macrophages in pregnancy (2017) Placenta, 56, pp. 44-52
  • Choudhury, R.H., Dunk, C.E., Lye, S.J., Extrav-illous trophoblast and endothelial cell crosstalk mediates leukocyte infiltration to the early remodeling decidual spiral arteriole wall (2017) J. Immunol., 198, pp. 4115-4128
  • Plaks, V., Birnberg, T., Berkutzki, T., Uterine DCs are crucial for decidua formation during embryo implantation in mice (2008) J. Clin. Invest., 118, pp. 3954-3965
  • Zenclussen, A.C., Gerlof, K., Zenclussen, M.L., Abnormal T-cell reactivity against paternal antigens in spontaneous abortion: Adoptive transfer of pregnancy-induced CD4 + CD25 + T regulatory cells prevents fetal rejection in a murine abortion model (2005) Am. J. Pathol., 166, pp. 811-822
  • Aluvihare, V.R., Kallikourdis, M., Betz, A.G., Regulatory T cells mediate maternal tolerance to the fetus (2004) Nat. Immunol., 5, pp. 266-271
  • Schumacher, A., Zenclussen, A.C., Regulatory T cells: Regulators of life (2014) Am. J. Reprod. Immunol., 72, pp. 158-170
  • Sacks, G.P., Studena, K., Sargent, K., Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis (1998) Am. J. Obstet. Gynecol., 179, pp. 80-86
  • Aly, A.S., Khandelwal, M., Zhao, J., Neutrophils are stimulated by syncytiotrophoblast microvillous membranes to generate superoxide radicals in women with preeclampsia (2004) Am. J. Obstet. Gynecol., 190, pp. 252-258
  • Tsukimori, K., Maeda, H., Ishida, K., The superoxide generation of neutrophils in normal and preeclamptic pregnancies (1993) Obstet. Gynecol., 81, pp. 536-540
  • Amsalem, H., Kwan, M., Hazan, A., Identification of a novel neutrophil population: Proangiogenic granulocytes in second-trimester human decidua (2014) J. Immunol., 193, pp. 3070-3079
  • Brinkmann, V., Reichard, U., Goosmann, C., Neutrophil extracellular traps kill bacteria (2004) Science, 303, pp. 1532-1535
  • Papayannopoulos, V., Zychlinsky, A., NETs: A new strategy for using old weapons (2009) Trends Immunol, 30, pp. 513-521
  • Hakkim, A., Furnrohr, B.G., Amann, K., Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis (2010) Proc. Natl. Acad. Sci. USA, 107, pp. 9813-9818
  • Fuchs, T.A., Brill, A., Duerschmied, D., Extracellular DNA traps promote thrombosis (2010) Proc. Natl. Acad. Sci. USA, 107, pp. 15880-15885
  • Gupta, A.K., Hasler, P., Holzgreve, W., Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia (2005) Hum. Immunol., 66, pp. 1146-1154
  • Walsh, S.W., Wang, Y., Trophoblast and placental villous core production of lipid peroxides, thromboxane, and prostacyclin in preeclampsia (1995) J. Clin. Endocrinol. Metab., 80, pp. 1888-1893
  • Hahn, S., Giaglis, S., Hoesli, I., Neutrophil NETs in reproduction: From infertility to preeclampsia and the possibility of fetal loss (2012) Front. Immunol., 3, p. 362
  • Mellembakken, J.R., Aukrust, P., Olafsen, M.K., Activation of leukocytes during the uteroplacental passage in preeclampsia (2002) Hypertension, 39, pp. 155-160
  • Said, S.I., The discovery of VIP: Initially looked for in the lung, isolated from intestine, and identified as a neuropeptide (2007) Peptides, 28, pp. 1620-1621
  • Waschek, J.A., VIP and PACAP: Neuropeptide modulators of CNS inflammation, injury, and repair (2013) Br. J. Pharmacol., 169, pp. 512-523
  • Gomariz, R.P., Gutiérrez-Cañas, I., Arranz, A., Peptides targeting Toll-like receptor signalling pathways for novel immune therapeutics (2010) Curr. Pharm. Des., 16, pp. 1063-1080
  • Symes, A., Lewis, S., Corpus, L., STAT proteins participate in the regulation of the vasoactive intestinal peptide gene by the ciliary neurotrophic factor family of cytokines (1994) Mol. Endocrinol., 8, pp. 1750-1763
  • Hahm, S.H., Eiden, L.E., Two separate cis-active elements of the vasoactive intestinal peptide gene mediate constitutive and inducible transcription by binding different sets of AP-1 proteins (1999) J. Biol. Chem., 274, pp. 25588-25593
  • Jones, E.A., Conover, J., Symes, A.J., Identification of a novel gp130-responsive site in the vasoactive intestinal peptide cytokine response element (2000) J. Biol. Chem., 275, pp. 36013-36020
  • Vogiagis, D., Salamonsen, L.A., The role of leukaemia inhibitory factor in the establishment of pregnancy (1999) J. Endocrinol., 160, pp. 181-190
  • Poehlmann, T.G., Fitzgerald, J.S., Meissner, A., Trophoblast invasion: Tuning through LIF, signalling via Stat3 (2005) Placenta, 26, pp. S37-S41. , Suppl. A
  • Hill, J.M., McCune, S.K., Alvero, R.J., Maternal vasoactive intestinal peptide and the regulation of embryonic growth in the rodent (1996) J. Clin. Invest., 97, pp. 202-208
  • Spong, C.Y., Lee, S.J., McCune, S.K., Maternal regulation of embryonic growth: The role of vasoactive intestinal peptide (1999) Endocrinology, 140, pp. 917-924
  • Hauk, V., Azzam, S., Calo, G., Vasoactive intestinal peptide induces an immunosuppressant microenvironment in the maternal–fetal interface of non-obese diabetic mice and improves early pregnancy outcome (2014) Am. J. Reprod. Immunol., 71, pp. 120-130
  • Gressens, P., Hill, J.M., Gozes, I., Growth factor function of vasoactive intestinal peptide in whole cultured mouse embryos (1993) Nature, 362, pp. 155-158
  • Passemard, S., El Ghouzzi, V., Nasser, H., VIP blockade leads to microcephaly in mice via disruption of Mcph1–Chk1 signaling (2011) J. Clin. Invest., 121, pp. 3071-3087
  • Gallino, L., Calo, G., Hauk, V., VIP treatment prevents embryo resorption by modulating efferocytosis and activation profile of maternal macrophages in the CBAxDBA resorption prone model (2016) Sci. Rep., 6
  • Marzioni, D., Fiore, G., Giordano, A., Placental expression of substance P and vasoactive intestinal peptide: Evidence for a local effect on hormone release (2005) J. Clin. Endocrinol. Metab., 90, pp. 2378-2383
  • Deutsch, P.J., Sun, Y., Kroog, G.S., Vasoactive intestinal peptide increases intracellular cAMP and gonadotropin-alpha gene activity in JEG-3 syncytial trophoblasts. Constraints posed by desensitization (1990) J. Biol. Chem., 265, pp. 10274-10281
  • Fraccaroli, L., Alfieri, J., Larocca, L., VIP modulates the pro-inflammatory maternal response, inducing tolerance to trophoblast cells (2009) Br. J. Pharmacol., 156, pp. 116-126
  • Fraccaroli, L., Grasso, E., Hauk, V., VIP boosts regulatory T cell induction by trophoblast cells in an in vitro model of trophoblast–maternal leukocyte interaction (2015) J. Leukoc. Biol., 98, pp. 49-58
  • Vota, D., Paparini, D., Hauk, V., Vasoactive intestinal peptide modulates trophoblast-derived cell line function and interaction with phagocytic cells through autocrine pathways (2016) Sci. Rep., 6
  • Paparini, D., Grasso, E., Calo, G., Trophoblast cells primed with vasoactive intestinal peptide enhance monocyte migration and apoptotic cell clearance through αvβ3 integrin portal formation in a model of maternal–placental interaction (2015) Mol. Hum. Reprod., 21, pp. 930-941
  • Calo, G., Sabbione, F., Vota, D., Trophoblast cells inhibit neutrophil extracellular trap formation and enhance apoptosis through vasoactive intestinal peptide-mediated pathways (2017) Hum. Reprod., 32, pp. 55-64

Citas:

---------- APA ----------
Ramhorst, R., Calo, G., Paparini, D., Vota, D., Hauk, V., Gallino, L., Merech, F.,..., Leirós, C.P. (2019) . Control of the inflammatory response during pregnancy: Potential role of VIP as a regulatory peptide. Annals of the New York Academy of Sciences, 1437(1), 15-21.
http://dx.doi.org/10.1111/nyas.13632
---------- CHICAGO ----------
Ramhorst, R., Calo, G., Paparini, D., Vota, D., Hauk, V., Gallino, L., et al. "Control of the inflammatory response during pregnancy: Potential role of VIP as a regulatory peptide" . Annals of the New York Academy of Sciences 1437, no. 1 (2019) : 15-21.
http://dx.doi.org/10.1111/nyas.13632
---------- MLA ----------
Ramhorst, R., Calo, G., Paparini, D., Vota, D., Hauk, V., Gallino, L., et al. "Control of the inflammatory response during pregnancy: Potential role of VIP as a regulatory peptide" . Annals of the New York Academy of Sciences, vol. 1437, no. 1, 2019, pp. 15-21.
http://dx.doi.org/10.1111/nyas.13632
---------- VANCOUVER ----------
Ramhorst, R., Calo, G., Paparini, D., Vota, D., Hauk, V., Gallino, L., et al. Control of the inflammatory response during pregnancy: Potential role of VIP as a regulatory peptide. Ann. New York Acad. Sci. 2019;1437(1):15-21.
http://dx.doi.org/10.1111/nyas.13632