Artículo

Blidner, A.G.; Rabinovich, G.A. "'Sweetening' Pregnancy: Galectins at the Fetomaternal Interface" (2013) American Journal of Reproductive Immunology. 69(4):369-382
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Abstract:

Successful mammalian pregnancy relies upon acceptance of a semi-allogeneic fetus by the maternal immune system. Lessons learned from studies on protective immunity to microbial infections and tumours, prevention of autoimmunity, and allograft rejection have contributed to delineate the mechanisms leading to T-cell tolerance at the fetomaternal interface. Recent observations highlight the contribution of galectins, a family of endogenous glycan-binding proteins, to critical biological events occurring during mammalian gestation, including immune cell tolerance, inflammation, implantation, and angiogenesis. These multifunctional lectins can hierarchically control a cascade of immunoregulatory events including the expansion, recruitment, and function of regulatory T cells, the promotion of tolerogenic dendritic cells, and the execution of T-cell death programs. In addition, galectins can control cell adhesion and signaling events critical for implantation and are involved in fundamental processes linking tissue hypoxia to angiogenesis. In an attempt to integrate the regulatory roles of galectins to immunological and vascular programs operating during pregnancy. Here we outline the regulated expression and function of individual members of the galectin family within the fetoplacental unit and their biological implications for the development and preservation of successful pregnancies. © 2013 John Wiley & Sons A/S.

Registro:

Documento: Artículo
Título:'Sweetening' Pregnancy: Galectins at the Fetomaternal Interface
Autor:Blidner, A.G.; Rabinovich, G.A.
Filiación:Instituto de Oncología Ángel H. Roffo, Universidad de Buenos Aires, Buenos Aires, Argentina
Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental (IBYME), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
Laboratorio de Glicómica Funcional, IQUIBICEN-CONICET, Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Angiogenesis; Fetomaternal tolerance; Galectins; Immune privilege; Implantation; Pregnancy; ecalectin; galectin; galectin 1; galectin 10; galectin 12; galectin 13; galectin 14; galectin 15; galectin 2; galectin 3; galectin 4; galectin 7; galectin 8; glycan; hypoxia inducible factor 1alpha; immunoglobulin enhancer binding protein; Janus kinase 2; lectin; unclassified drug; vasculotropin receptor 3; fetoplacental unit; homeostasis; human; nonhuman; pregnancy; priority journal; protein expression; protein function; review; Cell Adhesion; Cell Communication; Cell Hypoxia; Dendritic Cells; Embryo Implantation; Female; Fetus; Galectins; Humans; Immune Tolerance; Neovascularization, Physiologic; Pregnancy; Signal Transduction; T-Lymphocytes, Regulatory
Año:2013
Volumen:69
Número:4
Página de inicio:369
Página de fin:382
DOI: http://dx.doi.org/10.1111/aji.12090
Handle:http://hdl.handle.net/20.500.12110/paper_10467408_v69_n4_p369_Blidner
Título revista:American Journal of Reproductive Immunology
Título revista abreviado:Am. J. Reprod. Immunol.
ISSN:10467408
CODEN:AAJID
CAS:galectin 1, 258495-34-0; galectin 3, 208128-56-7; galectin 8, 220452-97-1; Galectins
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_10467408_v69_n4_p369_Blidner.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_10467408_v69_n4_p369_Blidner

Referencias:

  • 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
  • Chaouat, G., Petitbarat, M., Dubanchet, S., Rahmati, M., Ledée, N., Tolerance to the foetal allograft? (2010) Am J Reprod Immunol, 63, pp. 624-636
  • Blois, S.M., Joachim, R., Kandil, J., Margni, R., Tometten, M., Klapp, B.F., Arck, P.C., Depletion of CD8+ cells abolishes the pregnancy protective effect of progesterone substitution with dydrogesterone in mice by altering the Th1/Th2 cytokine profile (2004) J Immunol, 172, pp. 5893-5899
  • Chaouat, G., The Th1/Th2 paradigm: still important in pregnancy? (2007) Semin Immunopathol, 29, pp. 95-113
  • Aluvihare, V.R., Kallikourdis, M., Betz, A.G., Regulatory T cells mediate maternal tolerance to the fetus (2004) Nat Immunol, 5, pp. 266-271
  • Zenclussen, A.C., Gerlof, K., Zenclussen, M.L., Sollwedel, A., Bertoja, A.Z., Ritter, T., Kotsch, K., Volk, H.D., 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
  • Kallikourdis, M., Andersen, K.G., Welch, K.A., Betz, A.G., Alloantigen-enhanced accumulation of CCR5+ 'effector' regulatory T cells in the gravid uterus (2007) Proc Natl Acad Sci U S A., 104, pp. 594-599
  • Fainboim, L., Arruvito, L., Mechanisms involved in the expansion of Tregs during pregnancy: role of IL-2/STAT5 signalling (2011) J Reprod Immunol, 88, pp. 93-98
  • Koopman, L.A., Kopcow, H.D., Rybalov, B., Boyson, J.E., Orange, J.S., Schatz, F., Masch, R., Strominger, J.L., Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential (2003) J Exp Med, 198, pp. 1201-1212
  • Guleria, I., Khosroshahi, A., Ansari, M.J., Habicht, A., Azuma, M., Yagita, H., Noelle, R.J., Sayegh, M.H., A critical role for the programmed death ligand 1 in fetomaternal tolerance (2005) J Exp Med, 202, pp. 231-237
  • Kayisli, U.A., Selam, B., Guzeloglu-Kayisli, O., Demir, R., Arici, A., Human chorionic gonadotropin contributes to maternal immunotolerance and endometrial apoptosis by regulating Fas-Fas ligand system (2003) J Immunol, 171, pp. 2305-2313
  • Phillips, T.A., Ni, J., Pan, G., Ruben, S.M., Wei, Y.F., Pace, J.L., Hunt, J.S., TRAIL (Apo-2L) and TRAIL receptors in human placentas: implications for immune privilege (1999) J Immunol, 162, pp. 6053-6059
  • Tariverdian, N., Theoharides, T.C., Siedentopf, F., Gutiérrez, G., Jeschke, U., Rabinovich, G.A., Blois, S.M., Arck, P.C., Neuroendocrine-immune disequilibrium and endometriosis: an interdisciplinary approach (2007) Semin Immunopathol, 29, pp. 193-210
  • Arck, P.C., Gilhar, A., Bienenstock, J., Paus, R., The alchemy of immune privilege explored from a neuroimmunological perspective (2008) Curr Opin Pharmacol, 8, pp. 480-489
  • 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
  • Arck, P., Hansen, P.J., Mulac Jericevic, B., Piccinni, M.P., Szekeres-Bartho, J., Progesterone during pregnancy: endocrine-immune cross talk in mammalian species and the role of stress (2007) Am J Reprod Immunol, 58, pp. 268-279
  • Arruvito, L., Giulianelli, S., Flores, A.C., Paladino, N., Barboza, M., Lanari, C., Fainboim, L., NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis (2008) J Immunol, 180, pp. 5746-5753
  • Zenclussen, A.C., Schumacher, A., Zenclussen, M.L., Wafula, P., Volk, H.D., Immunology of pregnancy: cellular mechanisms allowing fetal survival within the maternal uterus (2007) Expert Rev Mol Med, 9, pp. 1-14
  • Nakamura, K., Sheps, S., Arck, P.C., Stress and reproductive failure: past notions, present insights and future directions (2008) J Assist Reprod Genet, 25, pp. 47-62
  • Oreshkova, T., Dimitrov, R., Mourdjeva, M., A cross-talk of decidual stromal cells, trophoblast, and immune cells: a prerequisite for the success of pregnancy (2012) Am J Reprod Immunol, 68, pp. 366-373
  • Rabinovich, G.A., Croci, D.O., Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer (2012) Immunity, 36, pp. 322-335
  • Meseguer, M., Pellicer, A., Simón, C., MUC1 and endometrial receptivity (1998) Mol Hum Reprod, 4, pp. 1089-1098
  • Toscano, M.A., Ilarregui, J.M., Bianco, G.A., Campagna, L., Croci, D.O., Salatino, M., Rabinovich, G.A., Dissecting the pathophysiologic role of endogenous lectins: glycan-binding proteins with cytokine-like activity? (2007) Cytokine Growth Factor Rev, 18, pp. 57-71
  • Rabinovich, G.A., Toscano, M.A., Jackson, S.S., Vasta, G.R., Functions of cell surface galectin-glycoprotein lattices (2007) Curr Opin Struct Biol, 17, pp. 513-520
  • Dam, T.K., Brewer, C.F., Lectins as pattern recognition molecules: the effects of epitope density in innate immunity (2010) Glycobiology, 20, pp. 270-279
  • Dennis, J.W., Nabi, I.R., Demetriou, M., Metabolism, cell surface organization, and disease (2009) Cell, 139, pp. 1229-1241
  • Rabinovich, G.A., Toscano, M.A., Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation (2009) Nat Rev Immunol, 9, pp. 338-352
  • Liu, F.T., Rabinovich, G.A., Galectins: regulators of acute and chronic inflammation (2010) Ann N Y Acad Sci, 1183, pp. 158-182
  • Yang, R.Y., Rabinovich, G.A., Liu, F.T., Galectins: structure, function and therapeutic potential (2008) Expert Rev Mol Med, 10, pp. e17
  • Hirabayashi, J., Hashidate, T., Arata, Y., Nishi, N., Nakamura, T., Hirashima, M., Urashima, T., Kasai, K., Oligosaccharide specificity of galectins: a search by frontal affinity chromatography (2002) Biochim Biophys Acta, 1572, pp. 232-254
  • Stowell, S.R., Arthur, C.M., Mehta, P., Slanina, K.A., Blixt, O., Leffler, H., Smith, D.F., Cummings, R.D., Galectin-1, -2, and -3 exhibit differential recognition of sialylated glycans and blood group antigens (2008) J Biol Chem, 283, pp. 10109-10123
  • Di Lella, S., Sundblad, V., Cerliani, J.P., Guardia, C.M., Estrin, D.A., Vasta, G.R., Rabinovich, G.A., When galectins recognize glycans: from biochemistry to physiology and back again (2011) Biochemistry, 50, pp. 7842-7857
  • Rabinovich, G.A., Daly, G., Dreja, H., Tailor, H., Riera, C.M., Hirabayashi, J., Chernajovsky, Y., Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis (1999) J Exp Med, 190, pp. 385-398
  • Toscano, M.A., Commodaro, A.G., Ilarregui, J.M., Bianco, G.A., Liberman, A., Serra, H.M., Hirabayashi, J., Rabinovich, G.A., Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2- and T regulatory-mediated anti-inflammatory responses (2006) J Immunol, 176, pp. 6323-6332
  • Toscano, M.A., Bianco, G.A., Ilarregui, J.M., Croci, D.O., Correale, J., Hernandez, J.D., Zwirner, N.W., Rabinovich, G.A., Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death (2007) Nat Immunol, 8, pp. 825-834
  • Perone, M.J., Bertera, S., Shufesky, W.J., Divito, S.J., Montecalvo, A., Mathers, A.R., Larregina, A.T., Morelli, A.E., Suppression of autoimmune diabetes by soluble galectin-1 (2009) J Immunol, 182, pp. 2641-2653
  • Starossom, S.C., Mascanfroni, I.D., Imitola, J., Cao, L., Raddassi, K., Hernandez, S.F., Bassil, R., Rabinovich, G.A., Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration (2012) Immunity, 37, pp. 249-263
  • Seropian, I.M., Cerliani, J.P., Toldo, S., Van Tassell, B.W., Ilarregui, J.M., González, G.E., Matoso, M., Rabinovich, G.A., Galectin-1 controls cardiac inflammation and ventricular remodeling during acute myocardial infarction (2013) Am J Pathol, 182, pp. 29-40
  • Rubinstein, N., Alvarez, M., Zwirner, N.W., Toscano, M.A., Ilarregui, J.M., Bravo, A., Mordoh, J., Rabinovich, G.A., Targeted inhibition of galectin-1 gene expression in tumor cells results in heightened T cell-mediated rejection; a potential mechanism of tumor-immune privilege (2004) Cancer Cell, 5, pp. 241-251
  • Juszczynski, P., Ouyang, J., Monti, S., Rodig, S.J., Takeyama, K., Abramson, J., Chen, W., Shipp, M.A., The AP1-dependent secretion of galectin-1 by Reed Sternberg cells fosters immune privilege in classical Hodgkin lymphoma (2007) Proc Natl Acad Sci U S A., 104, pp. 13134-13139
  • Banh, A., Zhang, J., Cao, H., Bouley, D.M., Kwok, S., Kong, C., Giaccia, A.J., Le, Q.T., Tumor galectin-1 mediates tumor growth and metastasis through regulation of T-cell apoptosis (2011) Cancer Res, 71, pp. 4423-4431
  • Soldati, R., Berger, E., Zenclussen, A.C., Jorch, G., Lode, H.N., Salatino, M., Rabinovich, G.A., Fest, S., Neuroblastoma triggers an immunoevasive program involving galectin-1-dependent modulation of T cell and dendritic cell compartments (2012) Int J Cancer, 131, pp. 1131-1141
  • Dalotto-Moreno, T., Croci, D.O., Cerliani, J.P., Martinez-Allo, V.C., Dergan-Dylon, S., Mendez Huergo, S.P., Stupirski, J.C., Salatino, M., Targeting galectin-1 overcomes breast cancer associated immunosuppression and prevents metastatic disease (2013) Cancer Res, 73, pp. 1107-1117
  • Ilarregui, J.M., Croci, D.O., Bianco, G.A., Toscano, M.A., Salatino, M., Vermeulen, M.E., Geffner, J.R., Rabinovich, G.A., Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10 (2009) Nat Immunol, 10, pp. 981-991
  • Liu, S.D., Lee, S., La Cava, A., Motran, C.C., Hahn, B.H., Miceli, M.C., Galectin-1-induced down-regulation of T lymphocyte activation protects (NZB × NZW) F1 mice fromlupus-like disease (2011) Lupus, 20, pp. 473-484
  • Rabinovich, G.A., Ariel, A., Hershkoviz, R., Hirabayashi, J., Kasai, K.I., Lider, O., Specific inhibition of T-cell adhesion to extracellular matrix and proinflammatory cytokine secretion by human recombinant galectin-1 (1999) Immunology, 97, pp. 100-106
  • Norling, L.V., Sampaio, A.L., Cooper, D., Perretti, M., Inhibitory control of endothelial galectin-1 on in vitro and in vivo lymphocyte trafficking (2008) FASEB J, 22, pp. 682-690
  • He, J., Baum, L.G., Galectin interactions with extracellular matrix and effects on cellular function (2006) Methods Enzymol, 417, pp. 247-256
  • van der Leij, J., van den Berg, A., Harms, G., Eschbach, H., Vos, H., Zwiers, P., van Weeghel, R., Visser, L., Strongly enhanced IL-10 production using stable galectin-1 homodimers (2007) Mol Immunol, 44, pp. 506-513
  • Stowell, S.R., Qian, Y., Karmakar, S., Koyama, N.S., Dias-Baruffi, M., Leffler, H., McEver, R.P., Cummings, R.D., Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion (2008) J Immunol, 180, pp. 3091-3102
  • Cedeno-Laurent, F., Opperman, M., Barthel, S.R., Kuchroo, V.K., Dimitroff, C.J., Galectin-1 triggers an immunoregulatory signature in Th cells functionally defined by IL-10 expression (2012) J Immunol, 188, pp. 3127-3137
  • Rabinovich, G.A., Ilarregui, J.M., Conveying glycan information into T-cell homeostatic programs: a challenging role for galectin-1 in inflammatory and tumor microenvironments (2009) Immunol Rev, 230, pp. 144-159
  • Than, N.G., Romero, R., Kim, C.J., McGowen, M.R., Papp, Z., Wildman, D.E., Galectins: guardians of eutherian pregnancy at the maternal-fetal interface (2012) Trends Endocrinol Metab, 23, pp. 23-31
  • Phillips, B., Knisley, K., Weitlauf, K.D., Dorsett, J., Lee, V., Weitlauf, H., Differential expression of two beta-galactoside-binding lectins in the reproductive tracts of pregnant mice (1996) Biol Reprod, 55, pp. 548-558
  • Dettin, L., Rubinstein, N., Aoki, A., Rabinovich, G.A., Maldonado, C.A., Regulated expression and ultrastructural localization of galectin-1, a proapoptotic beta-galactoside-binding lectin, during spermatogenesis in rat testis (2003) Biol Reprod, 68, pp. 51-59
  • Maquoi, E., van den Brûle, F.A., Castronovo, V., Foidart, J.M., Changes in the distribution pattern of galectin-1 and galectin-3 in human placenta correlates with the differentiation pathways of trophoblasts (1997) Placenta, 18, pp. 433-439
  • Iglesias, M.M., Rabinovich, G.A., Ivanovic, V., Sotomayor, C., Wolfenstein-Todel, C., Galectin-1 from ovine placenta-amino-acid sequence, physicochemical properties and implications in T-cell death (1998) Eur J Biochem, 252, pp. 400-407
  • Bozić, M., Petronijević, M., Milenković, S., Atanacković, J., Lazić, J., Vićovac, L.J., Galectin-1 and galectin-3 in the trophoblast of the gestational trophoblastic disease (2004) Placenta, 25, pp. 797-802
  • von Wolff, M., Wang, X., Gabius, H.J., Strowitzki, T., Galectin fingerprinting in human endometrium and decidua during the menstrual cycle and in early gestation (2005) Mol Hum Reprod, 11, pp. 189-194
  • Dong, M., Ding, G., Zhou, J., Wang, H., Zhao, Y., Huang, H., The effect of trophoblasts on T lymphocytes: possible regulatory effector molecules-a proteomic analysis (2008) Cell Physiol Biochem, 21, pp. 463-472
  • Tirado-González, I., Freitag, N., Barrientos, G., Shaikly, V., Nagaeva, O., Strand, M., Kjellberg, L., Blois, S.M., Galectin-1 influences trophoblast immune evasion and emerges as a predictive factor for the outcome of pregnancy (2013) Mol Hum Reprod, 19, pp. 43-53
  • Garín, M.I., Chu, C.C., Golshayan, D., Cernuda-Morollón, E., Wait, R., Lechler, R.I., Galectin-1: a key effector of regulation mediated by CD4+ CD25+ T cells (2007) Blood, 109, pp. 2058-2065
  • Fuertes, M.B., Molinero, L.L., Toscano, M.A., Ilarregui, J.M., Rubinstein, N., Fainboim, L., Zwirner, N.W., Rabinovich, G.A., Regulated expression of galectin-1 during T-cell activation involves Lck and Fyn kinases and signaling through MEK1/ERK, p38 MAP kinase and p70S6 kinase (2004) Mol Cell Biochem, 267, pp. 177-185
  • Rabinovich, G.A., Castagna, L., Landa, C., Riera, C.M., Sotomayor, C., Regulated expression of a 16-kd galectin-like protein in activated rat macrophages (1996) J Leukoc Biol, 59, pp. 363-370
  • Karimi, K., Arck, P.C., Natural Killer cells: keepers of pregnancy in the turnstile of the environment (2010) Brain Behav Immun, 24, pp. 339-347
  • Bevan, B.H., Kilpatrick, D.C., Liston, W.A., Hirabayashi, J., Kasai, K., Immunohistochemical localization of a beta-D-galactoside-binding lectin at the human maternofetal interface (1994) Histochem J, 26, pp. 582-586
  • Ramhorst, R.E., Giribaldi, L., Fraccaroli, L., Toscano, M.A., Stupirski, J.C., Romero, M.D., Durand, E.S., Rabinovich, G.A., Galectin-1 confers immune privilege to human trophoblast: implications in recurrent fetal loss (2012) Glycobiology, 22, pp. 1374-1386
  • Poirier, F., Timmons, P.M., Chan, C.T., Guénet, J.L., Rigby, P.W., Expression of the L14 lectin during mouse embryogenesis suggests multiple roles during pre- and post-implantation development (1992) Development, 115, pp. 143-155
  • Poirier, F., Robertson, E.J., Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin (1993) Development, 119, pp. 1229-1236
  • Blois, S.M., Ilarregui, J.M., Tometten, M., Garcia, M., Orsal, 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
  • Kopcow, H.D., Rosetti, F., Leung, Y., Allan, D.S., Kutok, J.L., Strominger, J.L., T cell apoptosis at the maternal-fetal interface in early human pregnancy, involvement of galectin-1 (2008) Proc Natl Acad Sci USA, 105, pp. 18472-18477
  • Woidacki, K., Popovic, M., Metz, M., Schumacher, A., Linzke, N., Teles, A., Poirier, F., Zenclussen, A.C., Mast cells rescue implantation defects caused by c-kit deficiency (2013) Cell Death Dis, 4, pp. e462
  • Than, N.G., Romero, R., Erez, O., Weckle, A., Tarca, A.L., Hotra, J., Abbas, A., Wildman, D.E., Emergence of hormonal and redox regulation of galectin-1 in placental mammals: implication in maternal-fetal immune tolerance (2008) Proc Natl Acad Sci USA, 105, pp. 15819-15824
  • Hirota, Y., Burnum, K.E., Acar, N., Rabinovich, G.A., Daikoku, T., Dey, S.K., Galectin-1 markedly reduces the incidence of resorptions in mice missing immunophilin FKBP52 (2012) Endocrinology, 153, pp. 2486-2493
  • Jeschke, U., Reimer, T., Bergemann, C., Wiest, I., Schulze, S., Friese, K., Walzel, H., Binding of galectin-1 (gal-1) on trophoblast cells and inhibition of hormone production of trophoblast tumor cells in vitro by gal-1 (2004) Histochem Cell Biol, 121, pp. 501-508
  • Kolundžić, N., Bojić-Trbojević, Z., Kovačević, T., Stefanoska, I., Kadoya, T., Vićovac, L., Galectin-1 is part of human trophoblast invasion machinery-a functional study in vitro (2011) PLoS ONE, 6, pp. e28514
  • Fischer, I., Weber, M., Kuhn, C., Fitzgerald, J.S., Schulze, S., Friese, K., Walzel, H., Jeschke, U., Is galectin-1 a trigger for trophoblast cell fusion?: the MAP-kinase pathway and syncytium formation in trophoblast tumour cells BeWo (2011) Mol Hum Reprod, 17, pp. 747-757
  • Thijssen, V.L., Barkan, B., Shoji, H., Aries, I.M., Mathieu, V., Deltour, L., Hackeng, T.M., Griffioen, A.W., Tumor cells secrete galectin-1 to enhance endothelial cell activity (2010) Cancer Res, 70, pp. 6216-6224
  • Mathieu, V., de Lassalle, E.M., Toelen, J., Mohr, T., Bellahcène, A., Van Goietsenoven, G., Verschuere, T., Feron, O., Galectin-1 in melanoma biology and related neo-angiogenesis processes (2012) J Invest Dermatol, 132, pp. 2245-2254
  • Croci, D.O., Salatino, M., Rubinstein, N., Cerliani, J.P., Cavallin, L.E., Leung, H.J., Ouyang, J., Rabinovich, G.A., Disrupting galectin-1 interactions with N-glycans suppresses hypoxia-driven angiogenesis and tumorigenesis in Kaposi's sarcoma (2012) J Exp Med, 209, pp. 1985-2000
  • Laderach, D.J., Gentilini, L.D., Giribaldi, L., Delgado, V.C., Nugnes, L., Croci, D.O., Al Nakouzi, N., Rabinovich, G.A., A unique galectin signature in human prostate cancer progression suggests galectin-1 as a key target for treatment of advanced disease (2013) Cancer Res, 73, pp. 86-96
  • Zhao, X.Y., Zhao, K.W., Jiang, Y., Zhao, M., Chen, G.Q., Synergistic induction of galectin-1 by CCAAT/enhancer binding protein alpha and hypoxia-inducible factor 1alpha and its role in differentiation of acute myeloid leukemic cells (2011) J Biol Chem, 286, pp. 36808-36819
  • Cooper, D., Norling, L.V., Perretti, M., Novel insights into the inhibitory effects of Galectin-1 on neutrophil recruitment under flow (2008) J Leukoc Biol, 83, pp. 1459-1466
  • Vasta, G.R., Ahmed, H., Nita-Lazar, M., Banerjee, A., Pasek, M., Shridhar, S., Guha, P., Fernández-Robledo, J.A., Galectins as self/non-self recognition receptors in innate and adaptive immunity: an unresolved paradox (2012) Front Immunol, 3, p. 199
  • Pacienza, N., Pozner, R.G., Bianco, G.A., D'Atri, L.P., Croci, D.O., Negrotto, S., Malaver, E., Schattner, M., The immunoregulatory glycan-binding protein galectin-1 triggers human platelet activation (2008) FASEB J, 22, pp. 1113-1123
  • Lobsanov, Y.D., Gitt, M.A., Leffler, H., Barondes, S.H., Rini, J.M., X-ray crystal structure of the human dimeric S-Lac lectin, L-14-II, in complex with lactose at 2.9-A resolution (1993) J Biol Chem, 268, pp. 27034-27038
  • Paclik, D., Berndt, U., Guzy, C., Dankof, A., Danese, S., Holzloehner, P., Rosewicz, S., Sturm, A., Galectin-2 induces apoptosis of lamina propria T lymphocytes and ameliorates acute and chronic experimental colitis in mice (2008) J Mol Med (Berl), 86, pp. 1395-1406
  • Paclik, D., Lohse, K., Wiedenmann, B., Dignass, A.U., Sturm, A., Galectin-2 and -4, but not galectin-1, promote intestinal epithelial wound healing in vitro through a TGF-beta-independent mechanism (2008) Inflamm Bowel Dis, 14, pp. 1366-1372
  • Ochieng, J., Green, B., Evans, S., James, O., Warfield, P., Modulation of the biological functions of galectin-3 by matrix metalloproteinases (1998) Biochim Biophys Acta, 1379, pp. 97-106
  • Pasquini, L.A., Millet, V., Hoyos, H.C., Giannoni, J.P., Croci, D.O., Marder, M., Liu, F.T., Pasquini, J.M., Galectin-3 drives oligodendrocyte differentiation to control myelin integrity and function (2011) Cell Death Differ, 18, pp. 1746-1756
  • Sundblad, V., Croci, D.O., Rabinovich, G.A., Regulated expression of galectin-3, a multifunctional glycan-binding protein, in haematopoietic and non-haematopoietic tissues (2011) Histol Histopathol, 26, pp. 247-265
  • Markowska, A.I., Liu, F.T., Panjwani, N., Galectin-3 is an important mediator of VEGF- and bFGF-mediated angiogenic response (2010) J Exp Med, 207, pp. 1981-1993
  • Liu, F.T., Rabinovich, G.A., Galectins as modulators of tumour progression (2005) Nat Rev Cancer, 5, pp. 29-41
  • Cao, Z., Said, N., Amin, S., Wu, H.K., Bruce, A., Garate, M., Hsu, D.K., Panjwani, N., Galectins-3 and -7, but not galectin-1, play a role in re-epithelialization of wounds (2002) J Biol Chem, 277, pp. 42299-42305
  • Yang, H., Lei, C., Zhang, W., Expression of galectin-3 in mouse endometrium and its effect during embryo implantation (2012) Reprod Biomed Online, 24, pp. 116-122
  • Lee, V.H., Lee, A.B., Phillips, E.B., Roberts, J.K., Weitlauf, H.M., Spatio-temporal pattern for expression of galectin-3 in the murine utero-placental complex: evidence for differential regulation (1998) Biol Reprod, 58, pp. 1277-1282
  • Froehlich, R., Hambruch, N., Haeger, J.D., Dilly, M., Kaltner, H., Gabius, H.J., Pfarrer, C., Galectin fingerprinting detects differences in expression profiles between bovine endometrium and placentomes as well as early and late gestational stages (2012) Placenta, 33, pp. 195-201
  • Crider-Pirkle, S., Billingsley, P., Faust, C., Hardy, D.M., Lee, V., Weitlauf, H., Cubilin, a binding partner for galectin-3 in the murine utero-placental complex (2002) J Biol Chem, 277, pp. 15904-15912
  • Iglesias, M.M., Rabinovich, G.A., Ambrosio, A.L., Castagna, L.F., Sotomayor, C.E., Wolfenstein-Todel, C., Purification of galectin-3 from ovine placenta: developmentally regulated expression and immunological relevance (1998) Glycobiology, 8, pp. 59-65
  • Troncoso, M.F., Elola, M.T., Croci, D.O., Rabinovich, G.A., Integrating structure and function of 'tandem-repeat' galectins (2012) Front Biosci (Schol Ed), 4, pp. 864-887
  • Delacour, D., Gouyer, V., Zanetta, J.P., Drobecq, H., Leteurtre, E., Grard, G., Moreau-Hannedouche, O., Huet, G., Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells (2005) J Cell Biol, 169, pp. 491-501
  • Hokama, A., Mizoguchi, E., Sugimoto, K., Shimomura, Y., Tanaka, Y., Yoshida, M., Rietdijk, S.T., Mizoguchi, A., Induced reactivity of intestinal CD4(+) T cells with an epithelial cell lectin, galectin-4, contributes to exacerbation of intestinal inflammation (2004) Immunity, 20, pp. 681-693
  • Nishida, A., Nagahama, K., Imaeda, H., Ogawa, A., Lau, C.W., Kobayashi, T., Hisamatsu, T., Mizoguchi, A., Inducible colitis-associated glycome capable of stimulating the proliferation of memory CD4+ T cells (2012) J Exp Med, 209, pp. 2383-2394
  • Arikawa, T., Simamura, E., Shimada, H., Nishi, N., Tatsuno, T., Ishigaki, Y., Tomosugi, N., Shoji, H., Expression pattern of Galectin 4 in rat placentation (2012) Placenta, 33, pp. 885-887
  • Leonidas, D.D., Vatzaki, E.H., Vorum, H., Celis, J.E., Madsen, P., Acharya, K.R., Structural basis for the recognition of carbohydrates by human galectin-7 (1998) Biochemistry, 37, pp. 13930-13940
  • Kuwabara, I., Kuwabara, Y., Yang, R.Y., Schuler, M., Green, D.R., Zuraw, B.L., Hsu, D.K., Liu, F.T., Galectin-7 (PIG1) exhibits pro-apoptotic function through JNK activation and mitochondrial cytochrome c release (2002) J Biol Chem, 277, pp. 3487-3497
  • Bidon-Wagner, N., Le Pennec, J.P., Human galectin-8 isoforms and cancer (2004) Glycoconj J, 19, pp. 557-563
  • Zick, Y., Eisenstein, M., Goren, R.A., Hadari, Y.R., Levy, Y., Ronen, D., Role of galectin-8 as a modulator of cell adhesion and cell growth (2004) Glycoconj J, 19, pp. 517-526
  • Nishi, N., Shoji, H., Seki, M., Itoh, A., Miyanaka, H., Yuube, K., Hirashima, M., Nakamura, T., Galectin-8 modulates neutrophil function via interaction with integrin alphaM (2003) Glycobiology, 13, pp. 755-763
  • Stowell, S.R., Arthur, C.M., Dias-Baruffi, M., Rodrigues, L.C., Gourdine, J.P., Heimburg-Molinaro, J., Ju, T., Cummings, R.D., Innate immune lectins kill bacteria expressing blood group antigen (2010) Nat Med, 16, pp. 295-301
  • Cattaneo, V., Tribulatti, M.V., Campetella, O., Galectin-8 tandem-repeat structure is essential for T-cell proliferation but not for co-stimulation (2011) Biochem J, 434, pp. 153-160
  • Romaniuk, M.A., Tribulatti, M.V., Cattaneo, V., Lapponi, M.J., Molinas, F.C., Campetella, O., Schattner, M., Human platelets express and are activated by galectin-8 (2010) Biochem J, 432, pp. 535-547
  • Delgado, V.M., Nugnes, L.G., Colombo, L.L., Troncoso, M.F., Fernández, M.M., Malchiodi, E.L., Frahm, I., Elola, M.T., Modulation of endothelial cell migration and angiogenesis: a novel function for the "tandem-repeat" lectin galectin-8 (2011) FASEB J, 25, pp. 242-254
  • Kolundžić, N., Bojić-Trbojević, Z., Radojčić, L., Petronijević, M., Vićovac, L.J., Galectin-8 is expressed by villous and extravillous trophoblast of the human placenta (2011) Placenta, 32, pp. 909-911
  • Chabot, S., Kashio, Y., Seki, M., Shirato, Y., Nakamura, K., Nishi, N., Nakamura, T., Hirashima, M., Regulation of galectin-9 expression and release in Jurkat T cell line cells (2002) Glycobiology, 12, pp. 111-118
  • Zhu, C., Anderson, A.C., Schubart, A., Xiong, H., Imitola, J., Khoury, S.J., Zheng, X.X., Kuchroo, V.K., The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity (2005) Nat Immunol, 6, pp. 1245-1252
  • Anderson, A.C., Anderson, D.E., Bregoli, L., Hastings, W.D., Kassam, N., Lei, C., Chandwaskar, R., Hafler, D.A., Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells (2007) Science, 318, pp. 1141-1143
  • Oomizu, S., Arikawa, T., Niki, T., Kadowaki, T., Ueno, M., Nishi, N., Yamauchi, A., Hirashima, M., Galectin-9 suppresses Th17 cell development in an IL-2-dependent but Tim-3-independent manner (2012) Clin Immunol, 143, pp. 51-58
  • Ohtsubo, K., Takamatsu, S., Minowa, M.T., Yoshida, A., Takeuchi, M., Marth, J.D., Dietary and genetic control of glucose transporter 2 glycosylation promotes insulin secretion in suppressing diabetes (2005) Cell, 123, pp. 1307-1321
  • Popovici, R.M., Krause, M.S., Germeyer, A., Strowitzki, T., von Wolff, M., Galectin-9: a new endometrial epithelial marker for the mid- and late-secretory and decidual phases in humans (2005) J Clin Endocrinol Metab, 90, pp. 6170-6176
  • Heusschen, R., Freitag, N., Tirado-González, I., Barrientos, G., Moschansky, P., Muñoz-Fernández, R., Leno-Durán, E., Blois, S.M., Profiling Lgals9 splice variant expression at the fetal-maternal interface: implications in normal and pathological pregnancy (2013) Biol Reprod, 88, p. 22
  • Swaminathan, G.J., Leonidas, D.D., Savage, M.P., Ackerman, S.J., Acharya, K.R., Selective recognition of mannose by the human eosinophil Charcot-Leyden crystal protein (galectin-10): a crystallographic study at 1.8 A resolution (1999) Biochemistry, 38, pp. 13837-13843
  • Kubach, J., Lutter, P., Bopp, T., Stoll, S., Becker, C., Huter, E., Richter, C., Jonuleit, H., Human CD4+ CD25+ regulatory T cells: proteome analysis identifies galectin-10 as a novel marker essential for their anergy and suppressive function (2007) Blood, 110, pp. 1550-1558
  • Guardia, C.M., Gauto, D.F., Di Lella, S., Rabinovich, G.A., Martí, M.A., Estrin, D.A., An integrated computational analysis of the structure, dynamics, and ligand binding interactions of the human galectin network (2011) J Chem Inf Model, 51, pp. 1918-1930
  • Yang, R.Y., Hsu, D.K., Yu, L., Chen, H.Y., Liu, F.T., Galectin-12 is required for adipogenic signaling and adipocyte differentiation (2004) J Biol Chem, 279, pp. 29761-29766
  • Yang, R.Y., Yu, L., Graham, J.L., Hsu, D.K., Lloyd, K.C., Havel, P.J., Liu, F.T., Ablation of a galectin preferentially expressed in adipocytes increases lipolysis, reduces adiposity, and improves insulin sensitivity in mice (2011) Proc Natl Acad Sci USA, 108, pp. 18696-18701
  • Than, N.G., Pick, E., Bellyei, S., Szigeti, A., Burger, O., Berente, Z., Janaky, T., Sumegi, B., Functional analyses of placental protein 13/galectin-13 (2004) Eur J Biochem, 271, pp. 1065-1078
  • Balogh, A., Pozsgay, J., Matkó, J., Dong, Z., Kim, C.J., Várkonyi, T., Sammar, M., Than, N.G., Placental protein 13 (PP13/galectin-13) undergoes lipid raft-associated subcellular redistribution in the syncytiotrophoblast in preterm preeclampsia and HELLP syndrome (2011) Am J Obstet Gynecol, 205, p. 156. , e1-156.e14
  • Kliman, H.J., Sammar, M., Grimpel, Y.I., Lynch, S.K., Milano, K.M., Pick, E., Bejar, J., Gonen, R., Placental protein 13 and decidual zones of necrosis: an immunologic diversion that may be linked to preeclampsia (2012) Reprod Sci, 19, pp. 16-30
  • Burger, O., Pick, E., Zwickel, J., Klayman, M., Meiri, H., Slotky, R., Mandel, S., Gonen, R., Placental protein 13 (PP-13): effects on cultured trophoblasts, and its detection in human body fluids in normal and pathological pregnancies (2004) Placenta, 25, pp. 608-622
  • Young, A.R., Barcham, G.J., Kemp, J.M., Dunphy, J.L., Nash, A., Meeusen, E.N., Functional characterization of an eosinophil-specific galectin, ovine galectin-14 (2009) Glycoconj J, 26, pp. 423-432
  • Lewis, S.K., Farmer, J.L., Burghardt, R.C., Newton, G.R., Johnson, G.A., Adelson, D.L., Bazer, F.W., Spencer, T.E., Galectin 15 (LGALS15): a gene uniquely expressed in the uteri of sheep and goats that functions in trophoblast attachment (2007) Biol Reprod, 77, pp. 1027-1036
  • Satterfield, M.C., Bazer, F.W., Spencer, T.E., Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus (2006) Biol Reprod, 75, pp. 289-296
  • Gray, C.A., Adelson, D.L., Bazer, F.W., Burghardt, R.C., Meeusen, E.N., Spencer, T.E., Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm (2004) Proc Natl Acad Sci USA, 101, pp. 7982-7987
  • Mor, G., Cardenas, I., The immune system in pregnancy: a unique complexity (2010) Am J Reprod Immunol, 63, pp. 425-433
  • Liu, A.X., Jin, F., Zhang, W.W., Zhou, T.H., Zhou, C.Y., Yao, W.M., Qian, Y.L., Huang, H.F., Proteomic analysis on the alteration of protein expression in the placental villous tissue of early pregnancy loss (2006) Biol Reprod, 75, pp. 414-420
  • Molvarec, A., Blois, S.M., Stenczer, B., Toldi, G., Tirado-Gonzalez, I., Ito, M., Shima, T., Saito, S., Peripheral blood galectin-1-expressing T and natural killer cells in normal pregnancy and preeclampsia (2011) Clin Immunol, 139, pp. 48-56
  • Than, N.G., Erez, O., Wildman, D.E., Tarca, A.L., Edwin, S.S., Abbas, A., Hotra, J., Romero, R., Severe preeclampsia is characterized by increased placental expression of galectin-1 (2008) J Matern Fetal Neonatal Med, 21, pp. 429-442
  • Than, N.G., Kim, S.S., Abbas, A., Han, Y.M., Hotra, J., Tarca, A.L., Erez, O., Romero, R., Chorioamnionitis and increased galectin-1 expression in PPROM -an anti-inflammatory response in the fetal membranes? (2008) Am J Reprod Immunol, 60, pp. 298-311
  • Jeschke, U., Mayr, D., Schiessl, B., Mylonas, I., Schulze, S., Kuhn, C., Friese, K., Walzel, H., Expression of galectin-1, -3 (gal-1, gal-3) and the Thomsen-Friedenreich (TF) antigen in normal, IUGR, preeclamptic and HELLP placentas (2007) Placenta, 28, pp. 1165-1173
  • Odibo, A.O., Zhong, Y., Goetzinger, K.R., Odibo, L., Bick, J.L., Bower, C.R., Nelson, D.M., First-trimester placental protein 13, PAPP-A, uterine artery Doppler and maternal characteristics in the prediction of pre-eclampsia (2011) Placenta, 32, pp. 598-602
  • Cowans, N.J., Stamatopoulou, A., Khalil, A., Spencer, K., PP13 as a marker of pre-eclampsia: a two platform comparison study (2011) Placenta, 32, pp. S37-S41

Citas:

---------- APA ----------
Blidner, A.G. & Rabinovich, G.A. (2013) . 'Sweetening' Pregnancy: Galectins at the Fetomaternal Interface. American Journal of Reproductive Immunology, 69(4), 369-382.
http://dx.doi.org/10.1111/aji.12090
---------- CHICAGO ----------
Blidner, A.G., Rabinovich, G.A. "'Sweetening' Pregnancy: Galectins at the Fetomaternal Interface" . American Journal of Reproductive Immunology 69, no. 4 (2013) : 369-382.
http://dx.doi.org/10.1111/aji.12090
---------- MLA ----------
Blidner, A.G., Rabinovich, G.A. "'Sweetening' Pregnancy: Galectins at the Fetomaternal Interface" . American Journal of Reproductive Immunology, vol. 69, no. 4, 2013, pp. 369-382.
http://dx.doi.org/10.1111/aji.12090
---------- VANCOUVER ----------
Blidner, A.G., Rabinovich, G.A. 'Sweetening' Pregnancy: Galectins at the Fetomaternal Interface. Am. J. Reprod. Immunol. 2013;69(4):369-382.
http://dx.doi.org/10.1111/aji.12090