Artículo

Grasso, E.; Gori, S.; Paparini, D.; Soczewski, E.; Fernández, L.; Gallino, L.; Salamone, G.; Martinez, G.; Irigoyen, M.; Ruhlmann, C.; Pérez Leirós, C.; Ramhorst, R. "VIP induces the decidualization program and conditions the immunoregulation of the implantation process" (2018) Molecular and Cellular Endocrinology. 460:63-72
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Abstract:

The decidualization process involves phenotype and functional changes on endometrial cells and the modulation of mediators with immunoregulatory properties as the vasoactive intestinal peptide (VIP). We investigate VIP contribution to the decidualization program and to immunoregulation throughout the human embryo implantation process. The decidualization of Human endometrial stromal cell line (HESC) with Medroxyprogesterone-dibutyryl-cAMP increased VIP/VPAC-receptors system. In fact, VIP could induce decidualization increasing differentiation markers (IGFBP1, PRL, KLF13/KLF9 ratio, CXCL12, CXCL8 and CCL2) and allowing Blastocyst-like spheroids (BLS) invasion in an in vitro model of embryo implantation. Focus on the tolerogenic effects, decidualized cells induced a semi-mature profile on maternal dendritic cells; restrained CD4+ cells recruitment while increased regulatory T-cells recruitment. Interestingly, the human blastocyst conditioned media from developmentally impaired embryos diminished the invasion and T-regulatory cells recruitment in these settings. These evidences suggest that VIP contributes to the implantation process inducing decidualization, allowing BLS invasion and favoring a tolerogenic micro-environment. © 2017 Elsevier B.V.

Registro:

Documento: Artículo
Título:VIP induces the decidualization program and conditions the immunoregulation of the implantation process
Autor:Grasso, E.; Gori, S.; Paparini, D.; Soczewski, E.; Fernández, L.; Gallino, L.; Salamone, G.; Martinez, G.; Irigoyen, M.; Ruhlmann, C.; Pérez Leirós, C.; Ramhorst, R.
Filiación:Immunopharmacology Laboratory, School of Sciences, University of Buenos Aires, IQUIBICEN-CONICET, Argentina
Institute of Experimental Medicine IMEX-CONICET, National Academy of Sciences, Buenos Aires, Argentina
Instituto de Fertilidad San Isidro, Buenos Aires, Argentina
Palabras clave:Decidualization; Immunoregulation; Implantation; VIP; cysteine rich protein 61; dibutyrylcytidine 3',5' phosphate; interleukin 8; medroxyprogesterone; membrane protein; monocyte chemotactic protein 1; prolactin; protein KLF13; stromal cell derived factor 1; unclassified drug; vasoactive intestinal polypeptide; vasoactive intestinal polypeptide receptor; biological marker; vasoactive intestinal polypeptide; Article; blastocyst; CD4+ T lymphocyte; controlled study; decidualization; dendritic cell; human; human cell; immunoregulation; in vitro study; nidation; priority journal; protein expression; regulatory T lymphocyte; stromal cell line; tumor spheroid; biological model; cell line; conditioned medium; cytology; decidua; drug effect; endometrium; female; immunological tolerance; immunology; metabolism; nidation; pharmacology; stroma cell; trophoblast; tumor microenvironment; Biomarkers; Blastocyst; Cell Line; Cellular Microenvironment; Culture Media, Conditioned; Decidua; Embryo Implantation; Endometrium; Female; Humans; Immune Tolerance; Models, Biological; Stromal Cells; Trophoblasts; Vasoactive Intestinal Peptide
Año:2018
Volumen:460
Página de inicio:63
Página de fin:72
DOI: http://dx.doi.org/10.1016/j.mce.2017.07.006
Título revista:Molecular and Cellular Endocrinology
Título revista abreviado:Mol. Cell. Endocrinol.
ISSN:03037207
CODEN:MCEND
CAS:dibutyrylcytidine 3',5' phosphate, 64649-87-2; interleukin 8, 114308-91-7; medroxyprogesterone, 520-85-4; prolactin, 12585-34-1, 50647-00-2, 9002-62-4; vasoactive intestinal polypeptide, 37221-79-7; Biomarkers; Culture Media, Conditioned; Vasoactive Intestinal Peptide
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03037207_v460_n_p63_Grasso

Referencias:

  • Abrahams, V.M., Visintin, I., Aldo, P.B., 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., 175, pp. 8096-8104
  • Bartsch, O., Bartlick, B., Ivell, R., Phosphodiesterase 4 inhibition synergizes with relaxin signaling to promote decidualization of human endometrial stromal cells (2004) J. Clin. Endocrinol. Metab., 89, pp. 324-334
  • Brosens, J.J., Hayashi, N., White, J.O., Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells (1999) Endocrinology, 140, pp. 4809-4820
  • Brosens, J.J., Parker, M.G., McIndoe, A., Pijnenborg, R., Brosens, I.A., A role for menstruation in preconditioning the uterus for successful pregnancy (2009) Am. J. Obstet. Gynecol., 200, p. 615. , e1–6
  • Brosens, J.J., Salker, M.S., Teklenburg, G., Nautiyal, J., Salter, S., Lucas, E.S., Steel, J.H., Macklon, N.S., Uterine selection of human embryos at implantation (2015) Sci. Rep., 4, p. 3894
  • Couvineau, A., Laburthe, M., VPAC receptors: structure, molecular pharmacology and interaction with accessory proteins (2012) Br. J. Pharmacol., 166, pp. 42-50
  • Dey, S.K., Lim, H., Das, S.K., Reese, J., Paria, B.C., Daikoku, T., Wang, H., Molecular cues to implantation (2004) Endocr. Rev., 25, pp. 341-373
  • Dimitriadis, E., Nie, G., Hannan, N.J., Paiva, P., Salamonsen, L.A., Local regulation of implantation at the human fetal-maternal interface (2010) Int. J. Dev. Biol., 54, pp. 313-322
  • 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
  • Du, M.R., Wang, S.C., Li, D.J., The integrative roles of chemokines at the maternal-fetal interface in early pregnancy (2014) Cell Mol. Immunol., 11, pp. 438-448
  • Ekström, J., Månsson, B., Tobin, G., Vasoactive intestinal peptide evoked secretion of fluid and protein from rat salivary glands and the development of supersensitivity (1983) Acta Physiol. Scand., 119, pp. 169-175
  • 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) Br. J. Pharmacol., 156, pp. 116-126
  • Fraccaroli, L., Alfieri, J., Leiros, C.P., Ramhorst, R., Immunomodulatory effects of chemokines during the early implantation window (2009) Front. Biosci. (Elite Ed.), 1, pp. 288-298
  • Fraccaroli, L., Grasso, E., Hauk, V., Cortelezzi, M., Calo, G., Pérez Leirós, C., Ramhorst, R., Defects in the vasoactive intestinal peptide (VIP)/VPAC system during early stages of the placental-maternal leucocyte interaction impair the maternal tolerogenic response (2012) Clin. Exp. Immunol., 170, pp. 310-320
  • Fraccaroli, L., Grasso, E., Zeitler, E., Lombardi, E., Gogorza, S., Etchepareborda, J.J., Nagle, C., Ramhorst, R., Modulation of maternal LIF producers T cells by trophoblast and paternal antigens (2011) Am. J. Reprod. Immunol., 65, pp. 133-145
  • Gardner, D.K., Lane, M., Stevens, J., Schlenker, T., Schoolcraft, W.B., Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer (2000) Fertil. Steril., 73, pp. 1155-1158
  • Gellersen, B., Brosens, I.A., Brosens, J.J., Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives (2007) Semin. Reprod. Med., 25, pp. 445-453
  • Gellersen, B., Brosens, J., Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair (2003) J. Endocrinol., 178, pp. 357-372
  • 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
  • Gonzalez-Rey, E., Delgado, M., Vasoactive intestinal peptide and regulatory T-cell induction: a new mechanism and therapeutic potential for immune homeostasis (2007) Trends Mol. Med., 13, pp. 241-251
  • Grasso, E., Paparini, D., Agüero, M., Mor, G., Pérez Leirós, C., Ramhorst, R., VIP contribution to the decidualization program: regulatory T cell recruitment (2014) J. Endocrinol., 221, pp. 121-131
  • Grohmann, U., Tolerance, DCs and tryptophan: much ado about IDO (2003) Trends Immunol., 24, pp. 242-248
  • Guerin, L.R., Prins, J.R., Robertson, S.A., Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment? (2009) Hum. Reprod. Update, 15, pp. 517-535
  • Krikun, G., Mor, G., Alvero, A., Guller, S., Schatz, F., Sapi, E., Rahman, M., Lockwood, C.J., A novel immortalized human endometrial stromal cell line with normal progestational response (2004) Endocrinology, 145, pp. 2291-2296
  • Kwak-Kim, J., Yang, K.M., Gilman-Sachs, A., Recurrent pregnancy loss: a disease of inflammation and coagulation (2009) J. Obstet. Gynaecol. Res., 35, pp. 609-622
  • Larregina, A.T., Falo, L.D., Changing paradigms in cutaneous immunology: adapting with dendritic cells (2005) J. Invest. Dermatol, 124, pp. 1-12
  • Leceta, J., Gomariz, R.P., Martinez, C., Carrión, M., Arranz, A., Juarranz, Y., Vasoactive intestinal peptide regulates Th17 function in autoimmune inflammation (2007) Neuroimmunomodulation, 14, pp. 134-138
  • Lin, Y., Xu, L., Jin, H., Zhong, Y., Di, J., Lin, Q., CXCL12 enhances exogenous CD4+CD25+ T cell migration and prevents embryo loss in non-obese diabetic mice (2009) Fertil. Steril., 91, pp. 2687-2696
  • Mellor, A.L., Munn, D.H., IDO expression by dendritic cells: tolerance and tryptophan catabolism (2004) Nat. Rev. Immunol., 4, pp. 762-774
  • Mesiano, S., Wang, Y., Norwitz, E.R., Progesterone receptors in the human pregnancy uterus: do they hold the key to birth timing? (2011) Reprod. Sci., 18, pp. 6-19
  • Mor, G., Cardenas, I., The immune system in pregnancy: a unique complexity (2010) Am. J. Reprod. Immunol., 63, pp. 425-433
  • Morelli, A.E., Thomson, A.W., Tolerogenic dendritic cells and the quest for transplant tolerance (2007) Nat. Rev. Immunol., 7, pp. 610-621
  • Morelli, A.E., Thomson, A.W., Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction (2003) Immunol. Rev., 196, pp. 125-146
  • Nancy, P., Tagliani, E., Tay, C.-S., Asp, P., Levy, D.E., Erlebacher, A., Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface (2012) Science, 336, pp. 1317-1321
  • Ou, X., O'Leary, H.A., Broxmeyer, H.E., Implications of DPP4 modification of proteins that regulate stem/progenitor and more mature cell types (2013) Blood, 122, pp. 161-169
  • Pabona, J.M.P., Zeng, Z., Simmen, F.A., Simmen, R.C.M., Functional differentiation of uterine stromal cells involves cross-regulation between bone morphogenetic protein 2 and Kruppel-like factor (KLF) family members KLF9 and KLF13 (2010) Endocrinology, 151, pp. 3396-3406
  • 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
  • Ramhorst, R., Fraccaroli, L., Aldo, P., Alvero, A.B., Cardenas, I., Leirós, C.P., Mor, G., Modulation and recruitment of inducible regulatory T cells by first trimester trophoblast cells (2012) Am. J. Reprod. Immunol., 67, pp. 17-27
  • Ramhorst, R., Grasso, E., Paparini, D., Hauk, V., Gallino, L., Calo, G., Vota, D., Pérez Leirós, C., Decoding the chemokine network that links leukocytes with decidual cells and the trophoblast during early implantation (2016) Cell Adh. Migr, 10, pp. 197-207
  • Reis e Sousa, C., Dendritic cells in a mature age (2006) Nat. Rev. Immunol., 6, pp. 476-483
  • Ren, L., Liu, Y.-Q., Zhou, W.-H., Zhang, Y.-Z., Trophoblast-derived chemokine CXCL12 promotes CXCR4 expression and invasion of human first-trimester decidual stromal cells (2012) Hum. Reprod., 27, pp. 366-374
  • Salker, M., Teklenburg, G., Molokhia, M., Lavery, S., Trew, G., Aojanepong, T., Mardon, H.J., Brosens, J.J., Natural selection of human embryos: impaired decidualization of endometrium disables embryo-maternal interactions and causes recurrent pregnancy loss (2010) PLoS One, 5
  • Stoikos, C.J., Harrison, C.A., Salamonsen, L.A., Dimitriadis, E., A distinct cohort of the TGFbeta superfamily members expressed in human endometrium regulate decidualization (2008) Hum. Reprod., 23, pp. 1447-1456
  • 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
  • Tan, C.W., Lee, Y.H., Tan, H.H., Lau, M.S.K., Choolani, M., Griffith, L., Chan, J.K.Y., CD26/DPPIV down-regulation in endometrial stromal cell migration in endometriosis (2014) Fertil. Steril., 102, pp. 167-177. , e9
  • Teklenburg, G., Salker, M., Heijnen, C., Macklon, N.S., Brosens, J.J., The molecular basis of recurrent pregnancy loss: impaired natural embryo selection (2010) Mol. Hum. Reprod., 16, pp. 886-895
  • Teklenburg, G., Salker, M., Molokhia, M., Lavery, S., Trew, G., Aojanepong, T., Mardon, H.J., Macklon, N.S., Natural selection of human embryos: decidualizing endometrial stromal cells serve as sensors of embryo quality upon implantation (2010) PLoS One, 5, p. e10258
  • Teles, A., Schumacher, A., Kühnle, M.-C., Linzke, N., Thuere, C., Reichardt, P., Tadokoro, C.E., Zenclussen, A.C., Control of uterine microenvironment by foxp3(+) cells facilitates embryo implantation (2013) Front. Immunol., 4, p. 158
  • 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
  • Weiss, G., Goldsmith, L.T., Taylor, R.N., Bellet, D., Taylor, H.S., Inflammation in reproductive disorders (2009) Reprod. Sci., 16, pp. 216-229
  • Yoshinaga, K., Research on blastocyst implantation essential factors (BIEFs) (2010) Am. J. Reprod. Immunol., 63, pp. 413-424

Citas:

---------- APA ----------
Grasso, E., Gori, S., Paparini, D., Soczewski, E., Fernández, L., Gallino, L., Salamone, G.,..., Ramhorst, R. (2018) . VIP induces the decidualization program and conditions the immunoregulation of the implantation process. Molecular and Cellular Endocrinology, 460, 63-72.
http://dx.doi.org/10.1016/j.mce.2017.07.006
---------- CHICAGO ----------
Grasso, E., Gori, S., Paparini, D., Soczewski, E., Fernández, L., Gallino, L., et al. "VIP induces the decidualization program and conditions the immunoregulation of the implantation process" . Molecular and Cellular Endocrinology 460 (2018) : 63-72.
http://dx.doi.org/10.1016/j.mce.2017.07.006
---------- MLA ----------
Grasso, E., Gori, S., Paparini, D., Soczewski, E., Fernández, L., Gallino, L., et al. "VIP induces the decidualization program and conditions the immunoregulation of the implantation process" . Molecular and Cellular Endocrinology, vol. 460, 2018, pp. 63-72.
http://dx.doi.org/10.1016/j.mce.2017.07.006
---------- VANCOUVER ----------
Grasso, E., Gori, S., Paparini, D., Soczewski, E., Fernández, L., Gallino, L., et al. VIP induces the decidualization program and conditions the immunoregulation of the implantation process. Mol. Cell. Endocrinol. 2018;460:63-72.
http://dx.doi.org/10.1016/j.mce.2017.07.006