Artículo

Davicino, R.C.; Méndez-Huergo, S.P.; Eliçabe, R.J.; Stupirski, J.C.; Autenrieth, I.; Di Genaro, M.S.; Rabinovich, G.A. "Galectin-1-driven tolerogenic programs aggravate yersinia enterocolitica infection by repressing antibacterial immunity" (2017) Journal of Immunology. 199(4):1382-1392
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Yersinia enterocolitica is an enteropathogenic bacterium that causes gastrointestinal disorders, as well as extraintestinal manifestations. To subvert the host's immune response, Y. enterocolitica uses a type III secretion system consisting of an injectisome and effector proteins, called Yersinia outer proteins (Yops), that modulate activation, signaling, and survival of immune cells. In this article, we show that galectin-1 (Gal-1), an immunoregulatory lectin widely expressed in mucosal tissues, contributes to Y. enterocolitica pathogenicity by undermining protective antibacterial responses. We found higher expression of Gal-1 in the spleen and Peyer's patches of mice infected orogastrically with Y. enterocolitica serotype O:8 compared with noninfected hosts. This effect was prevented when mice were infected with Y. enterocolitica lacking YopP or YopH, two critical effectors involved in bacterial immune evasion. Consistent with a regulatory role for this lectin during Y. enterocolitica pathogenesis, mice lacking Gal-1 showed increased weight and survival, lower bacterial load, and attenuated intestinal pathology compared with wild-type mice. These protective effects involved modulation of NF-kB activation, TNF production, and NO synthesis in mucosal tissue and macrophages, as well as systemic dysregulation of IL-17 and IFN-γ responses. In vivo neutralization of these proinflammatory cytokines impaired bacterial clearance and eliminated host protection conferred by Gal-1 deficiency. Finally, supplementation of recombinant Gal-1 in mice lacking Gal-1 or treatment of wild-type mice with a neutralizing anti-Gal-1 mAb confirmed the immune inhibitory role of this endogenous lectin during Y. enterocolitica infection. Thus, targeting Gal-1-glycan interactions may contribute to reinforce antibacterial responses by reprogramming innate and adaptive immune mechanisms. Copyright © 2017 by The American Association of Immunologists, Inc.

Registro:

Documento: Artículo
Título:Galectin-1-driven tolerogenic programs aggravate yersinia enterocolitica infection by repressing antibacterial immunity
Autor:Davicino, R.C.; Méndez-Huergo, S.P.; Eliçabe, R.J.; Stupirski, J.C.; Autenrieth, I.; Di Genaro, M.S.; Rabinovich, G.A.
Filiación:División de Inmunología, Facultad de Química, Bioquímica y Farmacia, Universidad Nacional de San Luis e Instituto Multidisciplinario de Investigaciones Biológicas, Consejo Nacional de Investigaciones Científicas y Técnicas, San Luis, C5700, Argentina
Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas, Vuelta de Obligado 2490, Buenos Aires, C1428, Argentina
Department of Clinical Microbiology and Hygiene, Tubingen University Hospital, Tubingen, 72076, Germany
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, C1428, Argentina
Palabras clave:bacterial protein; galectin 1; gamma interferon; immunoglobulin enhancer binding protein; interleukin 17; nitric oxide; outer membrane protein; protein tyrosine phosphatase; tumor necrosis factor; yopH protein, Yersinia; YopP protein, Yersinia; animal; antagonists and inhibitors; bacterial load; biosynthesis; blood; deficiency; genetics; host pathogen interaction; immunology; intestine; metabolism; microbiology; mouse; pathology; Peyer patch; spleen; Yersinia enterocolitica; Yersinia infection; Animals; Bacterial Load; Bacterial Outer Membrane Proteins; Bacterial Proteins; Galectin 1; Host-Pathogen Interactions; Interferon-gamma; Interleukin-17; Intestines; Mice; NF-kappa B; Nitric Oxide; Peyer's Patches; Protein Tyrosine Phosphatases; Spleen; Tumor Necrosis Factor-alpha; Yersinia enterocolitica; Yersinia Infections
Año:2017
Volumen:199
Número:4
Página de inicio:1382
Página de fin:1392
DOI: http://dx.doi.org/10.4049/jimmunol.1700579
Título revista:Journal of Immunology
Título revista abreviado:J. Immunol.
ISSN:00221767
CODEN:JOIMA
CAS:galectin 1, 258495-34-0; gamma interferon, 82115-62-6; nitric oxide, 10102-43-9; protein tyrosine phosphatase, 79747-53-8, 97162-86-2; Bacterial Outer Membrane Proteins; Bacterial Proteins; Galectin 1; Interferon-gamma; Interleukin-17; NF-kappa B; Nitric Oxide; Protein Tyrosine Phosphatases; Tumor Necrosis Factor-alpha; yopH protein, Yersinia; YopP protein, Yersinia
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00221767_v199_n4_p1382_Davicino

Referencias:

  • Koornhof, H.J., Smego, R.A., Jr., Nicol, M., Yersiniosis (1999) II: The Pathogenesis of Yersinia Infections. Eur. J. Clin. Microbiol. Infect. Dis., 18, pp. 87-112
  • Köberle, M., Klein-Gunther, A., Schutz, M., Fritz, M., Berchtold, S., Tolosa, E., Autenrieth, I.B., Bohn, E., Yersinia enterocolitica targets cells of the innate and adaptive immune system by injection of Yops in a mouse infection model (2009) PLoS Pathog., 5, p. e1000551
  • Autenrieth, S.E., Warnke, P., Wabnitz, G.H., Lucero Estrada, C., Pasquevich, K.A., Drechsler, D., Gunter, M., Beer-Hammer, S., Depletion of dendritic cells enhances innate antibacterial host defense through modulation of phagocyte homeostasis (2012) PLoS Pathog., 8, p. e1002552
  • DePaolo, R.W., Kamdar, K., Khakpour, S., Sugiura, Y., Wang, W., Jabri, B., A specific role for TLR1 in protective T(H)17 immunity during mucosal infection (2012) J. Exp. Med., 209, pp. 1437-1444
  • Eliçabe, R.J., Cargnelutti, E., Serer, M.I., Stege, P.W., Valdez, S.R., Toscano, M.A., Rabinovich, G.A., Genaro, M.S.D.I., Lack of TNFR p55 results in heightened expression of IFN-g and IL-17 during the development of reactive arthritis (2010) J. Immunol., 185, pp. 4485-4495
  • Sugiura, Y., Kamdar, K., Khakpour, S., Young, G., Karpus, W.J., DePaolo, R.W., TLR1-induced chemokine production is critical for mucosal immunity against Yersinia enterocolitica (2013) Mucosal Immunol., 6, pp. 1101-1109
  • Tumitan, A.R., Monnazzi, L.G., Ghiraldi, F.R., Cilli, E.M., Medeiros De Machado, B.M., Pattern of macrophage activation in Yersinia-resistant and Yersinia-susceptible strains of mice (2007) Microbiol. Immunol., 51, pp. 1021-1028
  • Eliçabe, R.J., Arias, J.L., Rabinovich, G.A., Genaro, M.S.D.I., TNFRp55 modulates IL-6 and nitric oxide responses following Yersinia lipopolysaccharide stimulation in peritoneal macrophages (2011) Immunobiology., 216, pp. 1322-1330
  • Cornelis, G.R., The type III secretion injectisome (2006) Nat. Rev. Microbiol., 4, pp. 811-825
  • Galán, J.E., Wolf-Watz, H., Protein delivery into eukaryotic cells by type III secretion machines (2006) Nature, 444, pp. 567-573
  • Viboud, G.I., Bliska, J.B., Yersinia outer proteins: Role in modulation of host cell signaling responses and pathogenesis (2005) Annu. Rev. Microbiol., 59, pp. 69-89
  • Thiefes, A., Wolf, A., Doerrie, A., Grassl, G.A., Matsumoto, K., Autenrieth, I., Bohn, E., Kracht, M., The Yersinia enterocolitica effector YopP inhibits host cell signalling by inactivating the protein kinase TAK1 in the IL-1 signalling pathway (2006) EMBO Rep., 7, pp. 838-844
  • Mittal, R., Peak-Chew, S.Y., McMahon, H.T., Acetylation of MEK2 and i kappa B kinase (IKK) activation loop residues by YopJ inhibits signaling (2006) Proc. Natl. Acad. Sci. USA, 103, pp. 18574-18579
  • Autenrieth, S.E., Soldanova, I., Rösemann, R., Gunst, D., Zahir, N., Kracht, M., Ruckdeschel, K., Autenrieth, I.B., Yersinia enterocolitica YopP inhibits MAP kinase-mediated antigen uptake in dendritic cells (2007) Cell. Microbiol., 9, pp. 425-437
  • Erfurth, S.E., Gröbner, S., Kramer, U., Gunst, D.S., Soldanova, I., Schaller, M., Autenrieth, I.B., Borgmann, S., Yersinia enterocolitica induces apoptosis and inhibits surface molecule expression and cytokine production in murine dendritic cells (2004) Infect. Immun., 72, pp. 7045-7054
  • Ruckdeschel, K., Mannel, O., Richter, K., Jacobi, C.A., Trulzsch, K., Rouot, B., Heesemann, J., Yersinia outer protein P of Yersinia enterocolitica simultaneously blocks the nuclear factor-kappa B pathway and exploits lipopolysaccharide signaling to trigger apoptosis in macrophages (2001) J. Immunol., 166, pp. 1823-1831
  • Gerke, C., Falkow, S., Chien, Y.H., The adaptor molecules LAT and SLP-76 are specifically targeted by Yersinia to inhibit T cell activation (2005) J. Exp. Med., 201, pp. 361-371
  • Alonso, A., Bottini, N., Bruckner, S., Rahmouni, S., Williams, S., Schoenberger, S.P., Mustelin, T., Lck dephosphorylation at Tyr-394 and inhibition of T cell antigen receptor signaling by Yersinia phosphatase YopH (2004) J. Biol. Chem., 279, pp. 4922-4928
  • Méndez-Huergo, S.P., Blidner, A.G., Rabinovich, G.A., Galectins: Emerging regulatory checkpoints linking tumor immunity and angiogenesis (2017) Curr. Opin. Immunol., 45, pp. 8-15
  • 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
  • Perone, M.J., Bertera, S., Tawadrous, Z.S., Shufesky, W.J., Piganelli, J.D., Baum, L.G., Trucco, M., Morelli, A.E., Dendritic cells expressing transgenic galectin-1 delay onset of autoimmune diabetes in mice (2006) J. Immunol., 177, pp. 5278-5289
  • 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
  • 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
  • Croci, D.O., Cerliani, J.P., Dalotto-Moreno, T., Méndez-Huergo, S.P., Mascanfroni, I.D., Dergan-Dylon, S., Toscano, M.A., Ouyang, J., Glycosylation-dependent lectin-receptor interactions preserve angiogenesis in anti-VEGF refractory tumors (2014) Cell, 156, pp. 744-758
  • Rutkowski, M.R., Stephen, T.L., Svoronos, N., Allegrezza, M.J., Tesone, A.J., Perales-Puchalt, A., Brencicova, E., Cadungog, M.G., Microbially driven TLR5-dependent signaling governs distal malignant progression through tumor-promoting inflammation (2015) Cancer Cell, 27, pp. 27-40
  • Tesone, A.J., Rutkowski, M.R., Brencicova, E., Svoronos, N., Perales-Puchalt, A., Stephen, T.L., Allegrezza, M.J., Wickramasinghe, J., Satb1 overexpression drives tumor-promoting activities in cancerassociated dendritic cells (2016) Cell Reports, 14, pp. 1774-1786
  • Ge, X.N., Ha, S.G., Greenberg, Y.G., Rao, A., Bastan, I., Blidner, A.G., Rao, S.P., Sriramarao, P., Regulation of eosinophilia and allergic airway inflammation by the glycan-binding protein galectin-1 (2016) Proc. Natl. Acad. Sci. USA, 113, pp. E4837-E4846
  • Poncini, C.V., Ilarregui, J.M., Batalla, E.I., Engels, S., Cerliani, J.P., Cucher, M.A., Van Kooyk, Y., Rabinovich, G.A., Trypanosoma cruzi infection imparts a regulatory program in dendritic cells and T cells via galectin-1-dependent mechanisms (2015) J. Immunol., 195, pp. 3311-3324
  • 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
  • Correa, S.G., Sotomayor, C.E., Aoki, M.P., Maldonado, C.A., Rabinovich, G.A., Opposite effects of galectin-1 on alternative metabolic pathways of L-arginine in resident, inflammatory, and activated macrophages (2003) Glycobiology, 13, pp. 119-128
  • Barrionuevo, P., Beigier-Bompadre, M., Ilarregui, J.M., Toscano, M.A., Bianco, G.A., Isturiz, M.A., Rabinovich, G.A., A novel function for galectin-1 at the crossroad of innate and adaptive immunity: Galectin-1 regulates monocyte/macrophage physiology through a nonapoptotic ERK-dependent pathway (2007) J. Immunol., 178, pp. 436-445
  • Starossom, S.C., Mascanfroni, I.D., Imitola, J., Cao, L., Raddassi, K., Hernandez, S.F., Bassil, R., Delacour, D., Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration (2012) Immunity, 37, pp. 249-263
  • 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
  • Dalotto-Moreno, T., Croci, D.O., Cerliani, J.P., Martinez-Allo, V.C., Dergan-Dylon, S., Méndez-Huergo, S.P., Stupirski, J.C., Toscano, M.A., Targeting galectin-1 overcomes breast cancer-associated immunosuppression and prevents metastatic disease (2013) Cancer Res., 73, pp. 1107-1117
  • Baum, L.G., Garner, O.B., Schaefer, K., Lee, B., Microbe-host interactions are positively and negatively regulated by galectin-glycan interactions (2014) Front. Immunol., 5, p. 284
  • Cerliani, J.P., Blidner, A.G., Toscano, M.A., Croci, D.O., Rabinovich, G.A., Translating the 'sugar code' into immune and vascular signaling programs (2017) Trends Biochem. Sci., 42, pp. 255-273
  • Suryawanshi, A., Cao, Z., Thitiprasert, T., Zaidi, T.S., Panjwani, N., Galectin-1-mediated suppression of Pseudomonas aeruginosa-induced corneal immunopathology (2013) J. Immunol., 190, pp. 6397-6409
  • Curciarello, R., Steele, A., Cooper, D., MacDonald, T.T., Kruidenier, L., Kudo, T., The role of galectin-1 and galectin-3 in the mucosal immune response to Citrobacter rodentium infection (2014) PLoS One, 9, p. e107933
  • Nita-Lazar, M., Banerjee, A., Feng, C., Amin, M.N., Frieman, M.B., Chen, W.H., Cross, A.S., Vasta, G.R., Desialylation of airway epithelial cells during influenza virus infection enhances pneumococcal adhesion via galectin binding (2015) Mol. Immunol., 65, pp. 1-16
  • Muglia, C., Mercer, N., Toscano, M.A., Schattner, M., Pozner, R., Cerliani, J.P., Gobbi, R.P., Docena, G.H., The glycan-binding protein galectin-1 controls survival of epithelial cells along the crypt-villus axis of small intestine (2011) Cell Death Dis., 2, p. e163
  • Vasta, G.R., Roles of galectins in infection (2009) Nat. Rev. Microbiol., 7, pp. 424-438
  • Chen, H.Y., Weng, I.C., Hong, M.H., Liu, F.T., Galectins as bacterial sensors in the host innate response (2014) Curr. Opin. Microbiol., 17, pp. 75-81
  • Adkins, I., Köberle, M., Gröbner, S., Bohn, E., Autenrieth, I.B., Borgmann, S., Yersinia outer proteins E, H, P, and T differentially target the cytoskeleton and inhibit phagocytic capacity of dendritic cells (2007) Int. J. Med. Microbiol., 297, pp. 235-244
  • Autenrieth, I.B., Tingle, A., Reske-Kunz, A., Heesemann, J., T lymphocytes mediate protection against Yersinia enterocolitica in mice: Characterization of murine T-cell clones specific for y (1992) Enterocolitica. Infect. Immun., 60, pp. 1140-1149
  • Autenrieth, I.B., Beer, M., Bohn, E., Kaufmann, S.H., Heesemann, J., Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: An essential role for gamma interferon (1994) Infect. Immun., 62, pp. 2590-2599
  • Rabinovich, G., 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
  • Ouyang, J., Juszczynski, P., Rodig, S.J., Green, M.R., O'Donnell, E., Currie, T., Armant, M., Rabinovich, G.A., Viral induction and targeted inhibition of galectin-1 in EBV+ posttransplant lymphoproliferative disorders (2011) Blood, 117, pp. 4315-4322
  • Croci, D.O., Salatino, M., Rubinstein, N., Cerliani, J.P., Cavallin, L.E., Leung, H.J., Ouyang, J., Domaica, C.I., 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
  • Bastón, J.I., Baranão, R.I., Ricci, A.G., Bilotas, M.A., Olivares, C.N., Singla, J.J., Gonzalez, A.M., Meresman, G.F., Targeting galectin-1-induced angiogenesis mitigates the severity of endometriosis (2014) J. Pathol., 234, pp. 329-337
  • Ruckdeschel, K., Deuretzbacher, A., Haase, R., Crosstalk of signalling processes of innate immunity with Yersinia Yop effector functions (2008) Immunobiology, 213, pp. 261-269
  • Echeverry, A., Saijo, S., Schesser, K., Adkins, B., Yersinia enterocolitica promotes robust mucosal inflammatory T-cell immunity in murine neonates (2010) Infect. Immun., 78, pp. 3595-3608
  • Motran, C.C., Molinder, K.M., Liu, S.D., Poirier, F., Miceli, M.C., Galectin-1 functions as a Th2 cytokine that selectively induces Th1 apoptosis and promotes Th2 function (2008) Eur. J. Immunol., 38, pp. 3015-3027
  • De La Fuente, H., Cruz-Adalia, A., Martinez Del Hoyo, G., Cibrián-Vera, D., Bonay, P., Pérez-Hernández, D., Vázquez, J., Ramirez-Huesca, M., The leukocyte activation receptor CD69 controls T cell differentiation through its interaction with galectin-1 (2014) Mol. Cell. Biol., 34, pp. 2479-2487
  • Keir, M.E., Butte, M.J., Freeman, G.J., Sharpe, A.H., PD-1 and its ligands in tolerance and immunity (2008) Annu. Rev. Immunol., 26, pp. 677-704
  • Rabinovich, G.A., Iglesias, M.M., Modesti, N.M., Castagna, L.F., Wolfenstein-Todel, C., Riera, C.M., Sotomayor, C.E., Activated rat macrophages produce a galectin-1-like protein that induces apoptosis of T cells: Biochemical and functional characterization (1998) J. Immunol., 160, pp. 4831-4840
  • Toscano, M.A., Campagna, L., Molinero, L.L., Cerliani, J.P., Croci, D.O., Ilarregui, J.M., Fuertes, M.B., Zwirner, N.W., Nuclear factor (NF)-kB controls expression of the immunoregulatory glycan-binding protein galectin-1 (2011) Mol. Immunol., 48, pp. 1940-1949
  • Zunĩga, E., Rabinovich, G.A., Iglesias, M.M., Gruppi, A., Regulated expression of galectin-1 during B-cell activation and implications for T-cell apoptosis (2001) J. Leukoc. Biol., 70, pp. 73-79
  • 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
  • Blois, S.M., Ilarregui, J.M., Tometten, M., Garcia, M., Orsal, A.S., Cordo-Russo, R., Toscano, M.A., Handjiski, B., A pivotal role for galectin-1 in fetomaternal tolerance (2007) Nat. Med., 13, pp. 1450-1457
  • Ramhorst, R.E., Giribaldi, L., Fraccaroli, L., Toscano, M.A., Stupirski, J.C., Romero, M.D., Durand, E.S., Sedlmayr, P., Galectin-1 confers immune privilege to human trophoblast: Implications in recurrent fetal loss (2012) Glycobiology, 22, pp. 1374-1386
  • Ouellet, M., Mercier, S., Pelletier, I., Bounou, S., Roy, J., Hirabayashi, J., Sato, S., Tremblay, M.J., Galectin-1 acts as a soluble host factor that promotes HIV-1 infectivity through stabilization of virus attachment to host cells (2005) J. Immunol., 174, pp. 4120-4126
  • Toledo, K.A., Fermino, M.L., Andrade, C.C., Riul, T.B., Alves, R.T., Muller, V.D., Russo, R.R., Dias-Baruffi, M., Galectin-1 exerts inhibitory effects during DENV-1 infection (2014) PLoS One, 9, p. e112474
  • Okumura, C.Y., Baum, L.G., Johnson, P.J., Galectin-1 on cervical epithelial cells is a receptor for the sexually transmitted human parasite Trichomonas vaginalis (2008) Cell. Microbiol., 10, pp. 2078-2090
  • Garner, O.B., Aguilar, H.C., Fulcher, J.A., Levroney, E.L., Harrison, R., Wright, L., Robinson, L.R., Haslam, S.M., Endothelial galectin-1 binds to specific glycans on nipah virus fusion protein and inhibits maturation, mobility, and function to block syncytia formation (2010) PLoS Pathog., 6, p. e1000993
  • Benatar, A.F., Garća, G.A., Bua, J., Cerliani, J.P., Postan, M., Tasso, L.M., Scaglione, J., Gómez, K.A., Galectin-1 prevents infection and damage induced by Trypanosoma cruzi on cardiac cells (2015) PLoS Negl. Trop. Dis., 9, p. e0004148
  • Nothaft, H., Szymanski, C.M., Protein glycosylation in bacteria: Sweeter than ever (2010) Nat. Rev. Microbiol., 8, pp. 765-778
  • Valguarnera, E., Kinsella, R.L., Feldman, M.F., Sugar and spice make bacteria not nice: Protein glycosylation and its influence in pathogenesis (2016) J. Mol. Biol., 428, pp. 3206-3220
  • Goto, Y., Uematsu, S., Kiyono, H., Epithelial glycosylation in gut homeostasis and inflammation (2016) Nat. Immunol., 17, pp. 1244-1251
  • Matteoli, G., Fahl, E., Warnke, P., Muller, S., Bonin, M., Autenrieth, I.B., Bohn, E., Role of IFN-gamma and IL-6 in a protective immune response to Yersinia enterocolitica in mice (2008) BMC Microbiol., 8, p. 153
  • Pasztoi, M., Bonifacius, A., Pezoldt, J., Kulkarni, D., Niemz, J., Yang, J., Teich, R., Rohde, M., Yersinia pseudotuberculosis supports Th17 differentiation and limits de novo regulatory T cell induction by directly interfering with T cell receptor signalling (2017) Cell. Mol. Life Sci.
  • Carlos, I.Z., Silva Monnazzi, L.G., Falcaõ, D.P., Medeiros De Machado, B.M., TNF-A, H2O2 and NO response of peritoneal macrophages to Yersinia enterocolitica O:3 derivatives (2004) Microbes Infect., 6, pp. 207-212
  • Monnazzi, L.G., Carlos, I.Z., De Medeiros, B.M., Influence of Yersinia pseudotuberculosis outer proteins (Yops) on interleukin-12, tumor necrosis factor alpha and nitric oxide production by peritoneal macrophages (2004) Immunol. Lett., 94, pp. 91-98
  • 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
  • Toegel, S., Weinmann, D., André, S., Walzer, S.M., Bilban, M., Schmidt, S., Chiari, C., Gabius, H.J., Galectin-1 couples glycobiology to inflammation in osteoarthritis through the activation of an NF-kB-regulated gene network (2016) J. Immunol., 196, pp. 1910-1921
  • Cargnelutti, E., Arias, J.L., Valdez, S.R., Rabinovich, G.A., Genaro, M.S.D.I., TNFRp55 controls regulatory T cell responses in Yersinia-induced reactive arthritis (2013) Immunol. Cell Biol., 91, pp. 159-166

Citas:

---------- APA ----------
Davicino, R.C., Méndez-Huergo, S.P., Eliçabe, R.J., Stupirski, J.C., Autenrieth, I., Di Genaro, M.S. & Rabinovich, G.A. (2017) . Galectin-1-driven tolerogenic programs aggravate yersinia enterocolitica infection by repressing antibacterial immunity. Journal of Immunology, 199(4), 1382-1392.
http://dx.doi.org/10.4049/jimmunol.1700579
---------- CHICAGO ----------
Davicino, R.C., Méndez-Huergo, S.P., Eliçabe, R.J., Stupirski, J.C., Autenrieth, I., Di Genaro, M.S., et al. "Galectin-1-driven tolerogenic programs aggravate yersinia enterocolitica infection by repressing antibacterial immunity" . Journal of Immunology 199, no. 4 (2017) : 1382-1392.
http://dx.doi.org/10.4049/jimmunol.1700579
---------- MLA ----------
Davicino, R.C., Méndez-Huergo, S.P., Eliçabe, R.J., Stupirski, J.C., Autenrieth, I., Di Genaro, M.S., et al. "Galectin-1-driven tolerogenic programs aggravate yersinia enterocolitica infection by repressing antibacterial immunity" . Journal of Immunology, vol. 199, no. 4, 2017, pp. 1382-1392.
http://dx.doi.org/10.4049/jimmunol.1700579
---------- VANCOUVER ----------
Davicino, R.C., Méndez-Huergo, S.P., Eliçabe, R.J., Stupirski, J.C., Autenrieth, I., Di Genaro, M.S., et al. Galectin-1-driven tolerogenic programs aggravate yersinia enterocolitica infection by repressing antibacterial immunity. J. Immunol. 2017;199(4):1382-1392.
http://dx.doi.org/10.4049/jimmunol.1700579