Artículo

Fraccaroli, L.; Alfieri, J.; Larocca, L.; Calafat, M.; Roca, V.; Lombardi, E.; Ramhorst, R.; Leirós, C.P. "VIP modulates the pro-inflammatory maternal response, inducing tolerance to trophoblast cells" (2009) British Journal of Pharmacology. 156(1):116-126
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Abstract:

Background and purpose: Successful embryo implantation is followed by a local pro-inflammatory and Th1 response, subsequently controlled by a Th2 response. Vasoactive intestinal peptide (VIP) has anti-inflammatory effects and promotes tolerogenic/Th2 responses while favouring embryonic development. We investigated the potential regulatory role of VIP on human trophoblast cells, maternal pro-inflammatory responses and trophoblast-maternal leukocyte interactions. Experimental approach: We tested VIP effects directly on a trophoblast cell line (Swan 71 cells) and after co-culture with maternal peripheral blood mononuclear cells (PBMCs) as models of the feto-maternal dialogue. We also co-cultured maternal and paternal PBMCs to test effects of endogenous VIP on maternal alloresponses. Key results: Swan 71 cells express VPAC 1 receptors and VIP induced their proliferation and the expression of leukaemia inhibitor factor, a pro-implantatory marker. After interaction with trophoblast cells, VIP increased Foxp3, the proportion of CD4+CD25+Foxp3+ cells within maternal PBMCs and transforming growth factor β expression. Also, during the trophoblast-maternal PBMCs interaction, VIP reduced pro-inflammatory mediators [interleukin (IL)-6, monocyte chemoattractant protein 1, nitric oxide], while increasing IL-10. Trophoblast cells produced VIP which dose-dependently suppressed allomaternal responses, accompanied by reduced expression of the T cell transcription factor, T-bet. Conclusions and implications: Vasoactive intestinal peptide induced pro-implantatory markers and trophoblast cell proliferation, while controlling the initial pro-inflammatory response, by increasing maternal regulatory T cells and anti-inflammatory cytokines. As an autocrine regulatory peptide VIP might contribute to fetal survival through two mechanisms; a direct trophic effect on trophoblast cells and an immunomodulatory effect that favours tolerance to fetal antigens. © 2008 The British Pharmacological Society.

Registro:

Documento: Artículo
Título:VIP modulates the pro-inflammatory maternal response, inducing tolerance to trophoblast cells
Autor:Fraccaroli, L.; Alfieri, J.; Larocca, L.; Calafat, M.; Roca, V.; Lombardi, E.; Ramhorst, R.; Leirós, C.P.
Filiación:Laboratory of Immunopharmacology, Ciudad Universitaria, University of Buenos Aires, Int. Guiraldes 2160, Pabellón 2 Piso 4, Buenos Aires (C1428EHA), Argentina
Immunopharmacology Laboratory, School of Sciences, University of Buenos Aires, Buenos Aires, Argentina
Immunogenetics Laboratory, School of Medicine, University of Buenos Aires, Buenos Aires, Argentina
Instituto de Fertilidad, IFER, Buenos Aires, Argentina
Palabras clave:Early pregnancy; Human implantation; Tolerance and pregnancy; VIP; interleukin 10; interleukin 6; leukemia inhibitory factor; monocyte chemotactic protein 1; nitric oxide; nitrite; transcription factor FOXP3; transcription factor T bet; transforming growth factor beta; vasoactive intestinal polypeptide; vasoactive intestinal polypeptide antagonist; vasoactive intestinal polypeptide receptor; autacoid; interleukin 10; vasoactive intestinal polypeptide receptor; antiinflammatory activity; article; CD4+ CD25+ T lymphocyte; cell line; cell proliferation; coculture; controlled study; dose response; flow cytometry; human; human cell; immunological tolerance; immunomodulation; inflammation; nidation; peripheral blood mononuclear cell; priority journal; protein expression; reverse transcription polymerase chain reaction; statistical analysis; Swan 71 cell; trophoblast; Western blotting; drug antagonism; drug effect; female; immunological tolerance; immunology; metabolism; mononuclear cell; nidation; pregnancy; Cell Line; Cell Proliferation; Coculture Techniques; Dose-Response Relationship, Drug; Embryo Implantation; Female; Humans; Immune Tolerance; Inflammation Mediators; Interleukin-10; Leukocytes, Mononuclear; Pregnancy; Receptors, Vasoactive Intestinal Peptide; Trophoblasts; Vasoactive Intestinal Peptide
Año:2009
Volumen:156
Número:1
Página de inicio:116
Página de fin:126
DOI: http://dx.doi.org/10.1111/j.1476-5381.2008.00055.x
Título revista:British Journal of Pharmacology
Título revista abreviado:Br. J. Pharmacol.
ISSN:00071188
CODEN:BJPCB
CAS:nitric oxide, 10102-43-9; nitrite, 14797-65-0; vasoactive intestinal polypeptide, 37221-79-7; Inflammation Mediators; Interleukin-10, 130068-27-8; Receptors, Vasoactive Intestinal Peptide; Vasoactive Intestinal Peptide, 37221-79-7
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00071188_v156_n1_p116_Fraccaroli

Referencias:

  • Abad, C., Martinez, C., Juarranz, M.G., Arranz, A., Receta, J., Delgado, M., Therapeutic effects of vasoactive intestinal peptide in the trinitrobenzene sulfonic acid mice model of Crohn's disease (2003) Gastroenterol, 124, pp. 961-971
  • Abrahams, V., Visitin, I., Aldo, P., Guller, S., Romero, R., Mor, G., A role for TLRs in the regulation of immune cell migration by first trimester trophoblast cells (2005) J Immunol, 176, pp. 8096-8104
  • Alexander, S.P.H., Mathie, A., Peters, J.A., Guide to Receptors and Channels (GRAC), 3rd edition (2008) Br J Pharmacol, 153 (2), pp. 1-209. , Suppl
  • Aluvihare, V., Kallikourdis, M., Betz, A.G., Regulatory T cells mediate maternal tolerance to the fetus (2004) Nat Immunol, 5, pp. 266-271
  • Aplin, J.D., Straszewski-Chavez, S.L., Kalions, B., Dunk, C., Morrish, D., Forbes, K., Trophoblast differentiation: Progenitor cells, fusion and migration (2006) Placenta, 27, p. 141. , A workshop report. Suppl. A
  • Armstrong, B.D., Hu, Z., Abad, C., Yamamoto, M., Rodriguez, W.I., Cheng, J., Lymphocyte regulation of neuropeptide gene expression after neuronal injury (2003) J Neurosci Res, 15, pp. 240-247
  • Arranz, A., Juarranz, Y., Leceta, J., Gomariz, R.P., Martínez, C., VIP balances innate and adaptive immune responses induced by specific stimulation of TLR2 and TLR4 (2008) Peptides, 29, pp. 948-956
  • Arruvito, L., Sanz, M., Banham, A., Fainboim, L., Expansion of CD4+CD25+FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: Implications for human reproduction (2007) J Immunol, 178, pp. 2572-2578
  • Auchincloss Jr., H., Sachs, D.H., Xenogeneic transplantation (1998) Annu Rev Immunol, 16, pp. 433-470
  • Blois, S.M., Ilarregui, J.M., Tometten, M., Garcia, M., Orsa, L.A.S., Cordo-Russo, R., Toscano, M.A., Arck, P.C., A pivotal role for galectin-1 in fetomaternal tolerance (2007) Nat Med, 13, pp. 1450-1457
  • Bulletti, C., Flamigni, C., De Ziegler, D., Implantation markers and endometriosis (2005) Reprod Biomed Online, 11, pp. 464-468
  • Bulmer, J.N., Sunderland, C., Immunological characterization of lymphoid cell populations in the early human placental bed (1984) Immunology, 52, pp. 349-357
  • Chaouat, G., Zourbas, S., Ostoij, S., Lappree-Delage, G., Dubanchet, S., Ledee, N., A brief review of recent data on some cytokine expressions at the materno-fetal interface which might challenge the classical Th1/Th2 dichotomy (2002) J Reprod Immunol, 53, pp. 241-253
  • Chaouat, G., Ledee-Bataille, N., Dubanchet, S., Zourbas, S., Sandra, O., Martal, J., TH1/TH2 paradigm in pregnancy: Paradigm lost? Cytokines in pregnancy/early abortion: Reexamining the TH1/TH2 paradigm (2004) Int Arch Allergy Immunol, 134, pp. 93-119
  • Chaouat, G., Dubanchet, S., Ledée, N., Cytokines: Important for implantation? (2007) J Assist Reprod Genet, 24, pp. 491-505
  • Chorny, A., Gonzalez-Rey, E., Fernandez Martin, A., Ganea, D., Delgado, M., Vasointestinal peptide induces regulatory dendritic cells that prevent acute graft-host disease while maintaining the graft-versus tumor response (2006) Blood, 107, pp. 3787-3794
  • Clark, D.A., Chaouat, G., Gorczynsk, G., Thinking outside the box: Mechanisms of environmental selective pressures on the outcome of the materno-fetal relationship (2002) Am J Reprod Immunol, 47, pp. 275-282
  • Clark, K.E., Mills, E.G., Stys, S.J., Seeds, A.E., Effects of vasoactive polypeptides on the uterine vasculature (1981) Am J Obstet and Gynecol, 139, pp. 182-188
  • Delgado, M., Munoz-Elias, E.J., Gomariz, R.P., Ganea, D., Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide enhance IL-10 production by murine macrophages: In vitro and in vivo studies (1999) Journal of Immunology, 162 (3), pp. 1707-1716
  • Delgado, M., Abad, C., Martinez, C., Receta, J., Gomariz, R.P., Vasoactive intestinal peptide prevents experimental arthritis by downregulating both autoimmune and inflammatory components of the disease (2001) Nat Med, 7, pp. 563-568
  • Delgado, M., Abad, C., Martinez, C., Juarranz, M.G., Vasoactive intestinal peptide in the immune system: Potential therapeutic role in inflammatory and autoimmune diseases (2002) J Mol Med, 80, pp. 16-24
  • Deon, D., Ahmed, S., Tai, K., Scaletta, N., Herrero, C., Lee, I.H., Cross-talk between IL-1 and IL-6 signaling pathways in rheumatoid arthritis synovial fibroblasts (2001) J Immunol, 1, pp. 5395-5403
  • Dimitriadis, E., White, C.A., Jones, R.L., Salamonsen, L.A., Cytokines, chemokines and growth factors in endometrium related to implantation (2005) Hum Reprod Update, 11, pp. 613-630
  • Ding, A.H., Nathan, C.F., Stuehr, D.J., Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production (1988) J Immunol, 141, pp. 2404-2412
  • Domínguez, F., Martínez, S., Quiñonero, A., Loro, F., Horcajadas, J.A., Pellicer, A., CXCL10 and IL-6 induce chemotaxis in human trophoblast cell lines (2008) Mol Hum Reprod, 14, pp. 423-430
  • Ekström, J., Mansson, B., Tobin, G., Vasoactive intestinal peptide evokes secretion of fluid and protein from rat salivary glands and the development of supersensitivity (1983) Acta Physiol Scand, 199, pp. 169-175
  • Fest, S., Aldo, P., Abrahams, V.M., Alvero, I., Chen, R., Chavez, S.L., Trophoblast-macrophage Interactions: A Regulatory network for the protection of pregnancy (2000) Am J Reprod Immunol, 5, pp. 55-66
  • Gomariz, R.P., Martinez, C., Abadd, C., Leceta, J., Delgado, M., Immunology of VIP: A review and therapeutical perspectives (2001) Curr Pharm des, 7, pp. 89-111
  • Gonzalez-Rey, E., Anderson, P., Delgado, M., Emerging roles of vasoactive intestinal peptide: A new approach for autoimmune therapy (2007) Ann Rheum Dis, 66, pp. 70-76
  • Gressens, P., Paindaveine, B., Hill, J.M., Evrard, P., Brenneman, D.E., Vasoactive intestinal peptide shortens both G1 and S phases of neural cell cycle in whole postimplantation cultured mouse embryos (1998) Eur J Neurosci, 10, pp. 1734-1742
  • Gutiérrez-Cañas, I., Rodríguez-Henche, N., Bolaños, O., Carmena, M.J., Prieto, J.C., Juarranz, M.G., VIP and PACAP are autocrine factors that protect the androgen-independent prostate cancer cell line PC-3 from apoptosis induced by serum withdrawal (2003) Br J Pharmacol, 139, pp. 1050-1058
  • Gutiérrez-Cañas, I., Juarranz, Y., Santiago, B., Arranz, A., Martinez, C., Galindo, M., VIP down-regulates TLR4 expression and TLR4-mediated chemokine production in human rheumatoid synovial fibroblasts (2006) Rheumatology, 45, pp. 527-532
  • Henson, P.M., Bratton, D.L., Fadok, V.A., The phosphatidylserine receptor: A crucial molecular switch? (2001) Nat Rev Mol Cell Biol, 2, pp. 627-633
  • Inoue, Y., Kaku, K., Kaneko, T., Yanahara, N., Kanno, T., Vasoactive intestinal peptide binding to specific receptors on rat parotid acinar cells induces amylase secretion accompanied by cyclic adenosine 3′-5′-monophosphate (1985) Endocrinology, 116, pp. 686-692
  • Jovanovic, A., Jovanovic, S., Tulic, I., Grbovic, L., Predominant role for nitric oxide in the relaxation induced by vasoactive intestinal polypeptide in human uterine artery (1998) Mol Hum Reprod, 4, pp. 71-76
  • Kawano, Y., Fukuda, J., Nasu, K., Matsumoto, H., Narahara, H., Miyakawa, I., Synergistic effect of interleukin (IL)-1alpha and ceramide analogue on the production of IL-6, IL-8, and macrophage colony-stimulating factor by endometrial stromal cells (2004) Fertil Steril, 3, pp. 1043-1047
  • Killedar, S.J., Eckenrode, S.E., McIndoe, R.A., She, J.X., Nguyen, C.Q., Peck, A.B., Early pathogenic events associated with Sjögren's syndrome (SjS)-like disease of the NOD mouse using microarray analysis (2006) Lab Invest, 86, pp. 1243-1260
  • Larocca, L., Calafat, M., Roca, V., Franchi, A.M., Leirós, C.P., VIP limits LPS-induced nitric oxide production through IL-10 in NOD mice macrophages (2007) Int Immunopharmacol, 10, pp. 1343-1349
  • Larocca, L., Ramhorst, R., Roca, V., Calafat, M., Aisemberg, J., Franchi, A., Pérez-Leirós, Neuroimmune-endocrine interactions during early pregnancy in an autoimmune context: Focus on macrophage activation (2008) Neuroimmunemodulation, 15, pp. 84-90
  • Mauri, C., Williams, R.O., Walmsley, M., Feldmann, M., Relationship between Th1/Th2 cytokine patterns ans arthritogenic response in collagen-induced arthritis (1996) Eur J Immunol, 26, pp. 1511-1520
  • Paria, B., Reese, J., Das, S., Dey, S., Deciphering the cross talk of implantation: Advances and challenges (2002) Science, 296, pp. 2185-2188
  • Piccinni, M.P., Role of T-cell cytokines in decidua and in cumulus oophorus during pregnancy (2007) Gynecol Obstet Invest, 64, pp. 144-148
  • Pregi, N., Vittori, D., Pérez, G., Pérez Leirós, C., Nesse, A., Effect of erythropoietin on staurosporine-induced apoptosis and differentiation of SH-SY5Y neuroblastoma cells (2006) Biochim Biophys Acta, 1763, pp. 238-246
  • Rosignoli, F., Torraoba, M., Juarranz, J., Garcia-Gomez, M., Martinez, C., Gomariz, R.P., VIP and tolerance induction in autoimmunity (2006) Ann N y Acad Sci, 1070, pp. 525-530
  • Rugeles, M.T., Shearer, G.M., Alloantigen recognition in utero: Dual advantage for the fetus? (2004) Trends Immunol, 25, pp. 348-352
  • Saito, S., Cytokine network at feto-maternal interface (2000) J Reprod Immunol, 47, pp. 87-103
  • Sherman, L.A., Chattopadhyay, S., The molecular basis of allorecognition (1993) Annu Rev Immunol, 11, pp. 385-402
  • Song, H., Lim, H., Evidence for heterodimeric association of leukemia inhibitory factor (LIF) receptor and gp130 in the mouse uterus for LIF signaling during blastocyst implantation (2006) Reproduction, 131, pp. 341-349
  • Spong, C.Y., Lee, S.J., McCune, S.K., Gibney, G., Abebe, D.T., Alvero, R., Brenneman, D.E., Hill, J.M., Maternal regulation of embryonic growth: The role of vasoactive intestinal peptide (1999) Endocrinology, 140 (2), pp. 917-924. , DOI 10.1210/en.140.2.917
  • Sreedharan, S.P., Huang, J.X., Cheung, M.C., Goetzl, E.J., Structure, expression, and chromosomal localization of the type i human vasoactive intestinal peptide receptor gene (1995) Proc Natl Acad Sci USA, 92, pp. 2939-2943
  • Terness, P., Kallikourdis, M., Betz, A.G., Rabinovich, G.A., Saito, S., Clark, D.A., Tolerance signaling molecules and pregnancy: IDO, galectins, and the renaissance of regulatory T cells (2007) Am J Reprod Immunol, 58, pp. 238-254
  • Thellin, O., Coumans, B., Zorzi, W., Igout, A., Heinen, A., Tolerance to the foeto-placental 'graft': Ten ways to support a child for nine months (2000) Curr Opin Immunol, 12, pp. 731-737
  • Wheeler, S., Eardley, J.E., McNulty, K.F., Sutcliffe, C.P., Morrison, J.D., An investigation into the relative merits of pituitary adenylate cyclase-activating polypeptide (PACAP-27) and vasoactive intestinal polypeptide as vagal neuro-transmitters in exocrine pancreas of rats (1997) Exp Physiol, 82, pp. 729-747

Citas:

---------- APA ----------
Fraccaroli, L., Alfieri, J., Larocca, L., Calafat, M., Roca, V., Lombardi, E., Ramhorst, R.,..., Leirós, C.P. (2009) . VIP modulates the pro-inflammatory maternal response, inducing tolerance to trophoblast cells. British Journal of Pharmacology, 156(1), 116-126.
http://dx.doi.org/10.1111/j.1476-5381.2008.00055.x
---------- CHICAGO ----------
Fraccaroli, L., Alfieri, J., Larocca, L., Calafat, M., Roca, V., Lombardi, E., et al. "VIP modulates the pro-inflammatory maternal response, inducing tolerance to trophoblast cells" . British Journal of Pharmacology 156, no. 1 (2009) : 116-126.
http://dx.doi.org/10.1111/j.1476-5381.2008.00055.x
---------- MLA ----------
Fraccaroli, L., Alfieri, J., Larocca, L., Calafat, M., Roca, V., Lombardi, E., et al. "VIP modulates the pro-inflammatory maternal response, inducing tolerance to trophoblast cells" . British Journal of Pharmacology, vol. 156, no. 1, 2009, pp. 116-126.
http://dx.doi.org/10.1111/j.1476-5381.2008.00055.x
---------- VANCOUVER ----------
Fraccaroli, L., Alfieri, J., Larocca, L., Calafat, M., Roca, V., Lombardi, E., et al. VIP modulates the pro-inflammatory maternal response, inducing tolerance to trophoblast cells. Br. J. Pharmacol. 2009;156(1):116-126.
http://dx.doi.org/10.1111/j.1476-5381.2008.00055.x