Leptin promotes HLA-G expression on placental trophoblasts via the MEK/Erk and PI3K signaling pathways

Introduction The development of the human haemochorial placenta requires complex regulatory mechanisms to protect invasive trophoblast cells from cytotoxic responses elicited by maternal immune cells. Leptin, the adipocyte derived hormone encoded by the Lep gene, is synthesized by placental trophobl...

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Autor principal: Barrientos, G.
Otros Autores: Toro, A., Moschansky, P., Cohen, M., Garcia, M.G, Rose, M., Maskin, B., Sánchez-Margalet, V., Blois, S.M, Varone, C.L
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Lenguaje:Inglés
Publicado: W.B. Saunders Ltd 2015
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100 1 |a Barrientos, G. 
245 1 0 |a Leptin promotes HLA-G expression on placental trophoblasts via the MEK/Erk and PI3K signaling pathways 
260 |b W.B. Saunders Ltd  |c 2015 
270 1 0 |m Blois, S.M.; Charité Center 12 Internal Medicine and Dermatology, Reproductive Medicine Research Group, Medicine UniversityGermany 
506 |2 openaire  |e Política editorial 
504 |a Red-Horse, K., Zhou, Y., Genbacev, O., Prakobphol, A., Foulk, R., McMaster, M., Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface (2004) J Clin Invest, 114 (6), pp. 744-754 
504 |a Hutter, H., Hammer, A., Dohr, G., Hunt, J.S., HLA expression at the maternal-fetal interface (1998) Dev Immunol, 6 (34), pp. 197-204 
504 |a Solier, C., Aguerre-Girr, M., Lenfant, F., Campan, A., Berrebi, A., Rebmann, V., Secretion of pro-apoptotic intron 4-retaining soluble HLA-G1 by human villous trophoblast (2002) Eur J Immunol, 32 (12), pp. 3576-3586 
504 |a Apps, R., Gardner, L., Sharkey, A.M., Holmes, N., Moffett, A., A homodimeric complex of HLA-G on normal trophoblast cells modulates antigen-presenting cells via LILRB1 (2007) Eur J Immunol, 37 (7), pp. 1924-1937 
504 |a Chen, L.J., Han, Z.Q., Zhou, H., Zou, L., Zou, P., Inhibition of HLA-G expression via RNAi abolishes resistance of extravillous trophoblast cell line TEV-1 to NK lysis (2010) Placenta, 31 (6), pp. 519-527 
504 |a McMaster, M.T., Librach, C.L., Zhou, Y., Lim, K.H., Janatpour, M.J., Demars, R., Human placental HLA-G expression is restricted to differentiated cytotrophoblasts (1995) J Immunol, 154 (8), pp. 3771-3778 
504 |a Liu, X., Gu, W., Li, X., HLA-G regulates the invasive properties of JEG-3 choriocarcinoma cells by controlling STAT3 activation (2013) Placenta, 34 (11), pp. 1044-1052 
504 |a McCormick, J., Whitley, G.S., Le Bouteiller, P., Cartwright, J.E., Soluble HLA-G regulates motility and invasion of the trophoblast-derived cell line SGHPL-4 (2009) Hum Reprod (Oxford, England), 24 (6), pp. 1339-1345 
504 |a Fons, P., Chabot, S., Cartwright, J.E., Lenfant, F., L'Faqihi, F., Giustiniani, J., Soluble HLA-G1 inhibits angiogenesis through an apoptotic pathway and by direct binding to CD160 receptor expressed by endothelial cells (2006) Blood, 108 (8), pp. 2608-2615 
504 |a Rajagopalan, S., Long, E.O., Cellular senescence induced by CD158d reprograms natural killer cells to promote vascular remodeling (2012) Proc Natl Acad Sci U S A, 109 (50), pp. 20596-20601 
504 |a Moschos, S., Chan, J.L., Mantzoros, C.S., Leptin and reproduction: A review (2002) Fertil Steril, 77 (3), pp. 433-444 
504 |a Masuzaki, H., Ogawa, Y., Isse, N., Satoh, N., Okazaki, T., Shigemoto, M., Human obese gene expression. Adipocyte-specific expression and regional differences in the adipose tissue (1995) Diabetes, 44 (7), pp. 855-858 
504 |a Campfield, L.A., Smith, F.J., Guisez, Y., Devos, R., Burn, P., Recombinant mouse OB protein: Evidence for a peripheral signal linking adiposity and central neural networks (1995) Sci (New York, N Y), 269 (5223), pp. 546-549 
504 |a Henson, M.C., Swan, K.F., O'Neil, J.S., Expression of placental leptin and leptin receptor transcripts in early pregnancy and at term (1998) Obstet Gynecol, 92 (6), pp. 1020-1028 
504 |a Ashworth, C.J., Hoggard, N., Thomas, L., Mercer, J.G., Wallace, J.M., Lea, R.G., Placental leptin (2000) Rev Reprod, 5 (1), pp. 18-24 
504 |a Gambino, Y.P., Maymo, J.L., Perez-Perez, A., Duenas, J.L., Sanchez-Margalet, V., Calvo, J.C., 17Beta-estradiol enhances leptin expression in human placental cells through genomic and nongenomic actions (2010) Biol Reprod, 83 (1), pp. 42-51 
504 |a Maymo, J.L., Perez, A.P., Gambino, Y., Calvo, J.C., Sanchez-Margalet, V., Varone, C.L., Review: Leptin gene expression in the placenta-regulation of a key hormone in trophoblast proliferation and survival (2011) Placenta, 32, pp. S146-S153 
504 |a Maymo, J.L., Perez Perez, A., Sanchez-Margalet, V., Duenas, J.L., Calvo, J.C., Varone, C.L., Up-regulation of placental leptin by human chorionic gonadotropin (2009) Endocrinology, 150 (1), pp. 304-313 
504 |a Grosfeld, A., Turban, S., Andre, J., Cauzac, M., Challier, J.C., Hauguel-De Mouzon, S., Transcriptional effect of hypoxia on placental leptin (2001) FEBS Lett, 502 (3), pp. 122-126 
504 |a Perez-Perez, A., Maymo, J., Duenas, J.L., Goberna, R., Calvo, J.C., Varone, C., Leptin prevents apoptosis of trophoblastic cells by activation of MAPK pathway (2008) Arch Biochem Biophys, 477 (2), pp. 390-395 
504 |a Magarinos, M.P., Sanchez-Margalet, V., Kotler, M., Calvo, J.C., Varone, C.L., Leptin promotes cell proliferation and survival of trophoblastic cells (2007) Biol Reprod, 76 (2), pp. 203-210 
504 |a Chardonnens, D., Cameo, P., Aubert, M.L., Pralong, F.P., Islami, D., Campana, A., Modulation of human cytotrophoblastic leptin secretion by interleukin-1alpha and 17beta-oestradiol and its effect on HCG secretion (1999) Mol Hum Reprod, 5 (11), pp. 1077-1082 
504 |a Cameo, P., Bischof, P., Calvo, J.C., Effect of leptin on progesterone, human chorionic gonadotropin, and interleukin-6 secretion by human term trophoblast cells in culture (2003) Biol Reprod, 68 (2), pp. 472-477 
504 |a Basak, S., Duttaroy, A.K., Leptin induces tube formation in first-trimester extravillous trophoblast cells (2012) Eur J Obstet Gynecol Reprod Biol, 164 (1), pp. 24-29 
504 |a Castellucci, M., De Matteis, R., Meisser, A., Cancello, R., Monsurro, V., Islami, D., Leptin modulates extracellular matrix molecules and metalloproteinases: Possible implications for trophoblast invasion (2000) Mol Hum Reprod, 6 (10), pp. 951-958 
504 |a Gonzalez, R.R., Devoto, L., Campana, A., Bischof, P., Effects of leptin, interleukin-1alpha, interleukin-6, and transforming growth factor-beta on markers of trophoblast invasive phenotype: Integrins and metalloproteinases (2001) Endocrine, 15 (2), pp. 157-164 
504 |a Lam, Q.L., Lu, L., Role of leptin in immunity (2007) Cell Mol Immunol, 4 (1), pp. 1-13 
504 |a Fernandez-Riejos, P., Najib, S., Santos-Alvarez, J., Martin-Romero, C., Perez-Perez, A., Gonzalez-Yanes, C., Role of leptin in the activation of immune cells (2010) Mediat Inflamm, 2010, p. 568343 
504 |a Sanchez-Margalet, V., Martin-Romero, C., Santos-Alvarez, J., Goberna, R., Najib, S., Gonzalez-Yanes, C., Role of leptin as an immunomodulator of blood mononuclear cells: Mechanisms of action (2003) Clin Exp Immunol, 133 (1), pp. 11-19 
504 |a Laivuori, H., Gallaher, M.J., Collura, L., Crombleholme, W.R., Markovic, N., Rajakumar, A., Relationships between maternal plasma leptin, placental leptin mRNA and protein in normal pregnancy, pre-eclampsia and intrauterine growth restriction without pre-eclampsia (2006) Mol Hum Reprod, 12 (9), pp. 551-556 
504 |a Herse, F., Dechend, R., Harsem, N.K., Wallukat, G., Janke, J., Qadri, F., Dysregulation of the circulating and tissue-based renin-angiotensin system in preeclampsia (2007) Hypertension, 49 (3), pp. 604-611 
504 |a Shen, Y., Wang, Q., Zhao, Q., Zhou, J., Leptin promotes the immune escape of lung cancer by inducing proinflammatory cytokines and resistance to apoptosis (2009) Mol Med Rep, 2 (2), pp. 295-299 
504 |a Fenton, J.I., Hursting, S.D., Perkins, S.N., Hord, N.G., Leptin induces an Apc genotype-associated colon epithelial cell chemokine production pattern associated with macrophage chemotaxis and activation (2007) Carcinogenesis, 28 (2), pp. 455-464 
504 |a Tirado-Gonzalez, I., Freitag, N., Barrientos, G., Shaikly, V., Nagaeva, O., Strand, M., Galectin-1 influences trophoblast immune evasion and emerges as a predictive factor for the outcome of pregnancy (2013) Mol Hum Reprod, 19 (1), pp. 43-53 
504 |a Cohen, M., Bischof, P., Coculture of decidua and trophoblast to study proliferation and invasion (2009) Methods Mol Biol (Clifton, NJ), 550, pp. 63-72 
504 |a Ramhorst, R., Fraccaroli, L., Aldo, P., Alvero, A.B., Cardenas, I., Leiros, C.P., Modulation and recruitment of inducible regulatory T cells by first trimester trophoblast cells (2012) Am J Reprod Immunol, 67 (1), pp. 17-27 
504 |a Straszewski-Chavez, S.L., Abrahams, V.M., Alvero, A.B., Aldo, P.B., Ma, Y., Guller, S., The isolation and characterization of a novel telomerase immortalized first trimester trophoblast cell line, Swan 71 (2009) Placenta, 30 (11), pp. 939-948 
504 |a Perez-Perez, A., Maymo, J., Gambino, Y., Duenas, J.L., Goberna, R., Varone, C., Leptin stimulates protein synthesis-activating translation machinery in human trophoblastic cells (2009) Biol Reprod, 81 (5), pp. 826-832 
504 |a Masuzaki, H., Ogawa, Y., Sagawa, N., Hosoda, K., Matsumoto, T., Mise, H., Nonadipose tissue production of leptin: Leptin as a novel placenta-derived hormone in humans (1997) Nat Med, 3 (9), pp. 1029-1033 
504 |a Atawi, F.A., Warsy, A.S., Babay, Z., Addar, M., Leptin concentration during different stages of pregnancy (2004) Clin Exp Obstet Gynecol, 31 (3), pp. 211-216 
504 |a Hardie, L., Trayhurn, P., Abramovich, D., Fowler, P., Circulating leptin in women: A longitudinal study in the menstrual cycle and during pregnancy (1997) Clin Endocrinol, 47 (1), pp. 101-106 
504 |a Hoggard, N., Crabtree, J., Allstaff, S., Abramovich, D.R., Haggarty, P., Leptin secretion to both the maternal and fetal circulation in the ex vivo perfused human term placenta (2001) Placenta, 22 (4), pp. 347-352 
504 |a Apps, R., Murphy, S.P., Fernando, R., Gardner, L., Ahad, T., Moffett, A., Human leucocyte antigen (HLA) expression of primary trophoblast cells and placental cell lines, determined using single antigen beads to characterize allotype specificities of anti-HLA antibodies (2009) Immunology, 127 (1), pp. 26-39 
504 |a Chauhan, M., Balakrishnan, M., Yallampalli, U., Endsley, J., Hankins, G.D., Theiler, R., Adrenomedullin 2/intermedin regulates HLA-G in human trophoblasts (2011) Biol Reprod, 85 (6), pp. 1232-1239 
504 |a Le Bouteiller, P., HLA-G in human early pregnancy: Control of uterine immune cell activation and likely vascular remodeling (2014) Biomed J, , Epub ahead of print 
504 |a Favier, B., Lemaoult, J., Lesport, E., Carosella, E.D., ILT2/HLA-G interaction impairs NK-cell functions through the inhibition of the late but not the early events of the NK-cell activating synapse (2010) FASEB J, 24 (3), pp. 689-699 
504 |a Zhong, M., Weng, X., Liang, Z., Lu, S., Li, J., Chen, X., Dimerization of soluble HLA-G by IgG-Fc fragment augments ILT2-mediated inhibition of T-cell alloresponse (2009) Transplantation, 87 (1), pp. 8-15 
504 |a Naji, A., Menier, C., Morandi, F., Agaugue, S., Maki, G., Ferretti, E., Binding of HLA-G to ITIM-bearing Ig-like transcript 2 receptor suppresses B cell responses (2014) J Immunol, 192 (4), pp. 1536-1546 
504 |a Fournel, S., Aguerre-Girr, M., Huc, X., Lenfant, F., Alam, A., Toubert, A., Cutting edge: Soluble HLA-G1 triggers CD95/CD95 ligand-mediated apoptosis in activated CD8+ cells by interacting with CD8 (2000) J Immunol, 164 (12), pp. 6100-6104 
504 |a Contini, P., Ghio, M., Merlo, A., Poggi, A., Indiveri, F., Puppo, F., Apoptosis of antigen-specific T lymphocytes upon the engagement of CD8 by soluble HLA class i molecules is Fas ligand/Fas mediated: Evidence for the involvement of p56lck, calcium calmodulin kinase II, and calcium-independent protein kinase C signaling pathways and for NF-kappaB and NF-AT nuclear translocation (2005) J Immunol, 175 (11), pp. 7244-7254 
504 |a Proll, J., Bensussan, A., Goffin, F., Foidart, J.M., Berrebi, A., Le Bouteiller, P., Tubal versus uterine placentation: Similar HLA-G expressing extravillous cytotrophoblast invasion but different maternal leukocyte recruitment (2000) Tissue Antigens, 56 (6), pp. 479-491 
504 |a Perez-Perez, A., Gambino, Y., Maymo, J., Goberna, R., Fabiani, F., Varone, C., MAPK and PI3K activities are required for leptin stimulation of protein synthesis in human trophoblastic cells (2010) Biochem Biophys Res Commun, 396 (4), pp. 956-960 
504 |a Fitzgerald, J.S., Busch, S., Wengenmayer, T., Foerster, K., De La Motte, T., Poehlmann, T.G., Signal transduction in trophoblast invasion (2005) Chem Immunol Allergy, 88, pp. 181-199 
504 |a Wang, H., Cheng, H., Shao, Q., Dong, Z., Xie, Q., Zhao, L., Leptin-promoted human extravillous trophoblasts invasion is MMP14 dependent and requires the crosstalk between notch1 and PI3K/Akt signaling (2014) Biol Reprod, 90 (4), p. 78 
504 |a Iikuni, N., Lam, Q.L., Lu, L., Matarese, G., La Cava, A., Leptin and inflammation (2008) Curr Immunol Rev, 4 (2), pp. 70-79 
504 |a Carosella, E.D., Moreau, P., Aractingi, S., Rouas-Freiss, N., HLA-G: A shield against inflammatory aggression (2001) Trends Immunol, 22 (10), pp. 553-555 
504 |a Rizzo, R., Bortolotti, D., Baricordi, O.R., Fainardi, E., New insights into HLA-G and inflammatory diseases (2012) Inflamm Allergy Drug Targets, 11 (6), pp. 448-463 
504 |a Appel, S., Turnwald, E.M., Alejandre-Alcazar, M.A., Ankerne, J., Rother, E., Janoschek, R., Leptin does not induce an inflammatory response in the murine placenta (2014) Horm Metab Res, 46 (6), pp. 384-389 
520 3 |a Introduction The development of the human haemochorial placenta requires complex regulatory mechanisms to protect invasive trophoblast cells from cytotoxic responses elicited by maternal immune cells. Leptin, the adipocyte derived hormone encoded by the Lep gene, is synthesized by placental trophoblasts and exerts pleiotropic effects on the immune system, including the promotion of inflammation and the activation of T cell responses. Methods To address its possible involvement in the modulation of maternal immune responses during pregnancy, we investigated the effect of leptin on the expression of the class Ib histocompatibility antigen HLA-G as one of the chief immunosuppressive strategies used by trophoblast cells. Results In vitro incubation of the trophoblast derived Swan 71 and JEG-3 cell lines with 25-50 ng/ml recombinant leptin significantly boosted HLA-G mRNA and protein expression, and this effect was abrogated upon pharmacological inhibition of the PI3K-Akt and MEK-Erk signaling pathways. A similar stimulatory effect of leptin was observed in term placental tissue explants, though 10-fold higher doses were required for stimulation. Further, JEG-3 cells treated with a leptin antisense oligodeoxynucleotide displayed decreased HLA-G expression levels, which were partially recovered by addition of stimulating doses of exogenous hormone. Immunofluorescence and qPCR analysis confirmed leptin biosynthesis in placental tissue, further showing that invasive extravillous trophoblast cells were a main source of this hormone during the first trimester of normal pregnancies. Discussion Taken together, our results show that leptin acts as an autocrine/paracrine signal promoting HLA-G expression in placental trophoblasts suggesting an important role in the regulation of immune evasion mechanisms at the fetal maternal interface. © 2015 Elsevier Ltd. All rights reserved.  |l eng 
536 |a Detalles de la financiación: Agencia Nacional de Promoción Científica y Tecnológica 
536 |a Detalles de la financiación: Deutscher Akademischer Austausch Dienst Kairo 
536 |a Detalles de la financiación: Universidad de Buenos Aires 
536 |a Detalles de la financiación: Secretaría de Ciencia y Técnica, Universidad de Buenos Aires, 2010-01/2123 
536 |a Detalles de la financiación: Consejo Nacional de Investigaciones Científicas y Técnicas 
536 |a Detalles de la financiación: PIP 2010-247 
536 |a Detalles de la financiación: Fritz Thyssen Stiftung, Az. 10.10.2.125 
536 |a Detalles de la financiación: Agencia Nacional de Promoción Científica y Tecnológica, PICT 2008-0425 
536 |a Detalles de la financiación: The authors are especially grateful to Christine Wuillemin (Cohen's group) and Dr. I. Tirado-González (Blois's group) for their excellent technical assistance. This work was supported by grants from Universidad de Buenos Aires [UBACYT, 2010-01/2123 ], Agencia Nacional de Promoción Científica y Tecnológica [ ANPCyT PICT 2008-0425 ] and Consejo Nacional de Investigaciones Científicas y Técnicas [ CONICET PIP 2010-247 ] to C. L. V.; and the Fritz Thyssen Stiftung [Az. 10.10.2.125 ] and Charité Stiftung to S.M.B. G.B. is a postdoctoral fellow of CONICET and was granted a Reinvitation fellowship from the Deutscher Akademischer Austausch Dienst (DAAD). Appendix A 
593 |a Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IQUIBICEN CONICET, Buenos Aires, Argentina 
593 |a Charité Center 12 Internal Medicine and Dermatology, Reproductive Medicine Research Group, Medicine University, Berlin, Germany 
593 |a Laboratoire d'Hormonologie, Department of Gynaecology and Obstetrics, Geneva, Switzerland 
593 |a Gene Therapy Laboratory, Facultad de Ciencias Biomédicas, Universidad Austral, Derqui-Buenos Aires, Argentina 
593 |a Hospital Nacional Profesor Alejandro Posadas, Buenos Aires, Argentina 
593 |a Departamento de Bioquímica Médica y Biología Molecular, Hospital Universitario Virgen Macarena, Universidad de Sevilla, Sevilla, Spain 
690 1 0 |a HLA-G 
690 1 0 |a LEPTIN 
690 1 0 |a SIGNAL TRANSDUCTION 
690 1 0 |a 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE 
690 1 0 |a 2 MORPHOLINO 8 PHENYLCHROMONE 
690 1 0 |a HLA G ANTIGEN 
690 1 0 |a LEPTIN 
690 1 0 |a MITOGEN ACTIVATED PROTEIN KINASE KINASE 
690 1 0 |a PHOSPHATIDYLINOSITOL 3 KINASE 
690 1 0 |a PROTEIN KINASE B 
690 1 0 |a RECOMBINANT LEPTIN 
690 1 0 |a ANTISENSE OLIGODEOXYNUCLEOTIDE 
690 1 0 |a HLA G ANTIGEN 
690 1 0 |a LEPTIN 
690 1 0 |a PHOSPHATIDYLINOSITOL 3 KINASE 
690 1 0 |a PROTEIN KINASE INHIBITOR 
690 1 0 |a RECOMBINANT PROTEIN 
690 1 0 |a ANTIGEN EXPRESSION 
690 1 0 |a ARTICLE 
690 1 0 |a CHORIOCARCINOMA CELL LINE 
690 1 0 |a CONTROLLED STUDY 
690 1 0 |a EMBRYO 
690 1 0 |a EXPLANT 
690 1 0 |a FEMALE 
690 1 0 |a FIRST TRIMESTER PREGNANCY 
690 1 0 |a GENE EXPRESSION 
690 1 0 |a HORMONE ACTION 
690 1 0 |a HUMAN 
690 1 0 |a HUMAN CELL 
690 1 0 |a IMMUNE EVASION 
690 1 0 |a IMMUNE RESPONSE 
690 1 0 |a IMMUNOFLUORESCENCE 
690 1 0 |a IMMUNOMODULATION 
690 1 0 |a IN VITRO STUDY 
690 1 0 |a PRIORITY JOURNAL 
690 1 0 |a PROTEIN EXPRESSION 
690 1 0 |a REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION 
690 1 0 |a SIGNAL TRANSDUCTION 
690 1 0 |a SYNCYTIOTROPHOBLAST 
690 1 0 |a TROPHOBLAST 
690 1 0 |a UPREGULATION 
690 1 0 |a WESTERN BLOTTING 
690 1 0 |a ADULT 
690 1 0 |a ANTAGONISTS AND INHIBITORS 
690 1 0 |a CELL LINE 
690 1 0 |a CHEMISTRY 
690 1 0 |a CYTOLOGY 
690 1 0 |a DRUG EFFECTS 
690 1 0 |a GENE EXPRESSION REGULATION 
690 1 0 |a GENE SILENCING 
690 1 0 |a GENETICS 
690 1 0 |a IMMUNOLOGY 
690 1 0 |a METABOLISM 
690 1 0 |a PREGNANCY 
690 1 0 |a REPRODUCTION 
690 1 0 |a THIRD TRIMESTER PREGNANCY 
690 1 0 |a TISSUE CULTURE TECHNIQUE 
690 1 0 |a TROPHOBLAST 
690 1 0 |a ADULT 
690 1 0 |a CELL LINE 
690 1 0 |a FEMALE 
690 1 0 |a GENE EXPRESSION REGULATION, DEVELOPMENTAL 
690 1 0 |a GENE SILENCING 
690 1 0 |a HLA-G ANTIGENS 
690 1 0 |a HUMANS 
690 1 0 |a LEPTIN 
690 1 0 |a MAP KINASE SIGNALING SYSTEM 
690 1 0 |a OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE 
690 1 0 |a PHOSPHATIDYLINOSITOL 3-KINASE 
690 1 0 |a PLACENTATION 
690 1 0 |a PREGNANCY 
690 1 0 |a PREGNANCY TRIMESTER, FIRST 
690 1 0 |a PREGNANCY TRIMESTER, THIRD 
690 1 0 |a PROTEIN KINASE INHIBITORS 
690 1 0 |a RECOMBINANT PROTEINS 
690 1 0 |a SIGNAL TRANSDUCTION 
690 1 0 |a TISSUE CULTURE TECHNIQUES 
690 1 0 |a TROPHOBLASTS 
650 1 7 |2 spines  |a PLACENTA 
650 1 7 |2 spines  |a PLACENTA 
700 1 |a Toro, A. 
700 1 |a Moschansky, P. 
700 1 |a Cohen, M. 
700 1 |a Garcia, M.G. 
700 1 |a Rose, M. 
700 1 |a Maskin, B. 
700 1 |a Sánchez-Margalet, V. 
700 1 |a Blois, S.M. 
700 1 |a Varone, C.L. 
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