Artículo

Fermino, M.L.; Dias, F.C.; Lopes, C.D.; Souza, M.A.; Cruz, A.K.; Liu, F.-T.; Chammas, R.; Roque-Barreira, M.C.; Rabinovich, G.A.; Bernardes, E.S. "Galectin-3 negatively regulates the frequency and function of CD4 + CD25 + Foxp3 + regulatory T cells and influences the course of Leishmania major infection" (2013) European Journal of Immunology. 43(7):1806-1817
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:

Galectin-3, an endogenous glycan-binding protein, plays essential roles during microbial infection by modulating innate and adaptive immunity. However, the role of galectin-3 within the CD4 + CD25 + Foxp3 + T regulatory (T REG ) cell compartment has not yet been explored. Here, we found, in a model of Leishmania major infection, that galectin-3 deficiency increases the frequency of peripheral T REG cells both in draining lymph nodes (LNs) and sites of infection. These observations correlated with an increased severity of the disease, as shown by increased footpad swelling and parasite burden. Galectin-3-deficient (Lgals3 -/- ) T REG cells displayed higher CD103 expression, showed greater suppressive capacity, and synthesized higher amounts of IL-10 compared with their wild-type (WT) counterpart. Furthermore, both T REG cells and T effector (T EFF ) cells from Lgals3 -/- mice showed higher expression of Notch1 and the Notch target gene Hes-1. Interestingly, Notch signaling components were also altered in both T REG and T EFF cells from uninfected Lgals3 -/- mice. Thus, endogenous galectin-3 regulates the frequency and function of CD4 + CD25 + Foxp3 + T REG cells and alters the course of L. major infection. © 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.

Registro:

Documento: Artículo
Título:Galectin-3 negatively regulates the frequency and function of CD4 + CD25 + Foxp3 + regulatory T cells and influences the course of Leishmania major infection
Autor:Fermino, M.L.; Dias, F.C.; Lopes, C.D.; Souza, M.A.; Cruz, A.K.; Liu, F.-T.; Chammas, R.; Roque-Barreira, M.C.; Rabinovich, G.A.; Bernardes, E.S.
Filiación:Departamento de Biologia Celular e Molecular, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil
Departamento de Imunologia, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Uberlândia, MG, Brazil
Department of Dermatology, University of California Davis, School of Medicine, CA, United States
Departamento de Radiologia e Oncologia, Faculdade de Medicina, Universidade de São Paulo, SP, Brazil
Cancer Institute of the State of Sao Paulo (ICESP), Center for Translational Research in Oncology (CTO), São Paulo, SP, Brazil
Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental (IBYME), Consejo Nacional de Investigaciones Cientificas y Técnicas, Buenos Aires, Argentina
Laboratorio de Glicómica Estructural y Funcional, Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
School of Medicine of University of São Paulo, Av. Dr. Arnaldo no. 455, 01246903, São Paulo, SP, Brazil
Palabras clave:Galectin-3; IL-10; Leishmania major; Notch signaling; T regulatory (Treg) cells; CD103 antigen; galectin 3; gamma interferon; interleukin 10; interleukin 4; Notch1 receptor; transcription factor FOXP3; transcription factor HES 1; animal experiment; animal model; animal tissue; antigen expression; article; CD4+ CD25+ T lymphocyte; controlled study; disease course; disease severity; effector cell; flow cytometry; immunohistochemistry; in vitro study; Leishmania major; leishmaniasis; lymph node; lymphocyte function; mouse; negative feedback; nonhuman; parasite load; priority journal; regulatory T lymphocyte; wild type; Galectin-3; IL-10; Leishmania major; Notch signaling; T regulatory (Treg) cells; Animals; Disease Models, Animal; Flow Cytometry; Forkhead Transcription Factors; Galectin 3; Immunohistochemistry; Leishmania major; Leishmaniasis, Cutaneous; Mice; Mice, Inbred BALB C; Mice, Knockout; Real-Time Polymerase Chain Reaction; Receptors, Notch; Reverse Transcriptase Polymerase Chain Reaction; T-Lymphocytes, Regulatory
Año:2013
Volumen:43
Número:7
Página de inicio:1806
Página de fin:1817
DOI: http://dx.doi.org/10.1002/eji.201343381
Título revista:European Journal of Immunology
Título revista abreviado:Eur. J. Immunol.
ISSN:00142980
CODEN:EJIMA
CAS:CD103 antigen, 269047-90-7; galectin 3, 208128-56-7; gamma interferon, 82115-62-6; Forkhead Transcription Factors; Galectin 3; Receptors, Notch
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00142980_v43_n7_p1806_Fermino

Referencias:

  • Vasta, G.R., Roles of galectins in infection (2009) Nat. Rev. Microbiol., 7, pp. 424-438
  • Rabinovich, G.A., Croci, D.O., Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer (2012) Immunity, 36, pp. 322-335
  • Leffler, H., Carlsson, S., Hedlund, M., Qian, Y., Poirier, F., Introduction to galectins (2004) Glycoconj. J., 19, pp. 433-440
  • Acosta-Rodríguez, E.V., Montes, C.L., Motrán, C.C., Zuniga, E.I., Liu, F.T., Rabinovich, G.A., Gruppi, A., Galectin-3 mediates IL-4-induced survival and differentiation of B cells: functional cross-talk and implications during Trypanosoma cruzi infection (2004) J. Immunol., 172, pp. 493-502
  • Bernardes, E.S., Silva, N.M., Ruas, L.P., Mineo, J.R., Loyola, A.M., Hsu, D.K., Liu, F.T., Toxoplasma gondii infection reveals a dual role for galectin-3 on innate and adaptive immune response (2006) Am. J. Pathol., 168, pp. 1910-1920
  • Ferraz, L.C., Bernardes, E.S., Oliveira, A.F., Ruas, L.P., Fermino, M.L., Soares, S.G., Loyola, A.M., Lack of galectin-3 alters the balance of innate immune cytokines and confers resistance to Rhodococcus equi (2008) Eur. J. Immunol., 38, pp. 2762-2775
  • Ruas, L.P., Bernardes, E.S., Fermino, M.L., de Oliveira, L.L., Hsu, D.K., Liu, F.T., Chammas, R., Lack of galectin-3 drives response to Paracoccidioides brasiliensis toward a Th2-biased immunity (2009) PLoS ONE, 4, pp. e4519
  • Breuilh, L., Vanhoutte, F., Fontaine, J., van Stijn, C.M., Tillie-Leblond, I., Capron, M., Faveeuw, C., Galectin-3 modulates immune and inflammatory responses during helminthic infection: impact of galectin-3 deficiency on the functions of dendritic cells (2007) Infect. Immun., 75, pp. 5148-5157
  • Vignali, D.A., Collison, L.W., Workman, C.J., How regulatory T cells work (2008) Nat. Rev. Immunol., 8, pp. 523-532
  • 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
  • Kubach, J., Lutter, P., Bopp, T., Stoll, S., Becker, C., Huter, E., Richter, C., 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
  • Ocklenburg, F., Moharregh-Khiabani, D., Geffers, R., Janke, V., Pfoertner, S., Garritsen, H., Groebe, L., UBD, a downstream element of FOXP3, allows the identification of LGALS3, a new marker of human regulatory T cells (2006) Lab. Invest., 86, pp. 724-737
  • Jiang, H.R., Al Rasebi, Z., Mensah-Brown, E., Shahin, A., Xu, D., Goodyear, C.S., Fukada, S.Y., Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis (2009) J. Immunol., 182, pp. 1167-1173
  • Sacks, D., Noben-Trauth, N., The immunology of susceptibility and resistance to Leishmania major in mice (2002) Nat. Rev. Immunol, 2, pp. 845-858
  • Xu, D., Liu, H., Komai-Koma, M., Campbell, C., McSharry, C., Alexander, J., Liew, F.Y., CD4 + CD25 + regulatory T cells suppress differentiation and functions of Th1 and Th2 cells, Leishmania major infection, and colitis in mice (2003) J. Immunol., 170, pp. 394-399
  • Aseffa, A., Gumy, A., Launois, P., MacDonald, H.R., Louis, J.A., Tacchini-Cottier, F., The early IL-4 response to Leishmania major and the resulting Th2 cell maturation steering progressive disease in BALB/c mice are subject to the control of regulatory CD4 + CD25 + T cells (2002) J. Immunol., 169, pp. 3232-3241
  • Suffia, I., Reckling, S.K., Salay, G., Belkaid, Y., A role for CD103 in the retention of CD4 + CD25 + T REG and control of Leishmania major infection (2005) J. Immunol., 174, pp. 5444-5455
  • Liu, D., Zhang, T., Marshall, A.J., Okkenhaug, K., Vanhaesebroeck, B., Uzonna, J.E., The p110delta isoform of phosphatidylinositol 3-kinase controls susceptibility to Leishmania major by regulating expansion and tissue homing of regulatory T cells (2009) J. Immunol., 183, pp. 1921-1933
  • Asano, N., Watanabe, T., Kitani, A., Fuss, I.J., Strober, W., Notch1 signaling and regulatory T cell function (2008) J. Immunol., 180, pp. 2796-2804
  • Hoyne, G.F., Le Roux, I., Corsin-Jimenez, M., Tan, K., Dunne, J., Forsyth, L.M., Dallman, M.J., Serrate1-induced notch signalling regulates the decision between immunity and tolerance made by peripheral CD4(+) T cells (2000) Int. Immunol., 12, pp. 177-185
  • Yvon, E.S., Vigouroux, S., Rousseau, R.F., Biagi, E., Amrolia, P., Dotti, G., Wagner, H.J., Overexpression of the Notch ligand, Jagged-1, induces alloantigen-specific human regulatory T cells (2003) Blood, 102, pp. 3815-3821
  • Radtke, F., Fasnacht, N., Macdonald, H.R., Notch signaling in the immune system (2010) Immunity, 32, pp. 14-27
  • 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
  • Dhirapong, A., Lleo, A., Leung, P., Gershwin, M.E., Liu, F.T., The immunological potential of galectin-1 and -3 (2009) Autoimmun. Rev., 8, pp. 360-363
  • Joo, H.G., Goedegebuure, P.S., Sadanaga, N., Nagoshi, M., von Bernstorff, W., Eberlein, T.J., Expression and function of galectin-3, a beta-galactoside-binding protein in activated T lymphocytes (2001) J. Leukoc. Biol., 69, pp. 555-564
  • Hsu, D.K., Chen, H.Y., Liu, F.T., Galectin-3 regulates T-cell functions (2009) Immunol. Rev., 230, pp. 114-127
  • Chen, H.Y., Fermin, A., Vardhana, S., Weng, I.C., Lo, K.F., Chang, E.Y., Maverakis, E., Galectin-3 negatively regulates TCR-mediated CD4 + T-cell activation at the immunological synapse (2009) Proc. Natl. Acad. Sci. USA, 106, pp. 14496-14501
  • Iellem, A., Mariani, M., Lang, R., Recalde, H., Panina-Bordignon, P., Sinigaglia, F., D'Ambrosio, D., Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells (2001) J. Exp. Med., 194, pp. 847-853
  • Fisson, S., Darrasse-Jèze, G., Litvinova, E., Septier, F., Klatzmann, D., Liblau, R., Salomon, B.L., Continuous activation of autoreactive CD4 + CD25 + regulatory T cells in the steady state (2003) J. Exp. Med., 198, pp. 737-746
  • Ermann, J., Hoffmann, P., Edinger, M., Dutt, S., Blankenberg, F.G., Higgins, J.P., Negrin, R.S., Only the CD62L+ subpopulation of CD4+CD25+ regulatory T cells protects from lethal acute GVHD (2005) Blood, 105, pp. 2220-2226
  • Robinson, P.W., Green, S.J., Carter, C., Coadwell, J., Kilshaw, P.J., Studies on transcriptional regulation of the mucosal T-cell integrin alphaEbeta7 (CD103) (2001) Immunology, 103, pp. 146-154
  • Noben-Trauth, N., Lira, R., Nagase, H., Paul, W.E., Sacks, D.L., The relative contribution of IL-4 receptor signaling and IL-10 to susceptibility to Leishmania major (2003) J. Immunol., 170, pp. 5152-5158
  • Kane, M.M., Mosser, D.M., The role of IL-10 in promoting disease progression in leishmaniasis (2001) J. Immunol., 166, pp. 1141-1147
  • Nagase, H., Jones, K.M., Anderson, C.F., Noben-Trauth, N., Despite increased CD4+Foxp3+ cells within the infection site, BALB/c IL-4 receptor-deficient mice reveal CD4+Foxp3-negative T cells as a source of IL-10 in Leishmania major susceptibility (2007) J. Immunol., 179, pp. 2435-2444
  • Belkaid, Y., Piccirilo, A.C., Mendez, S., Shevack, E., Sacks, D.L., CD4+CD25 +regulatory T cells control Leishmania major persistence and immunity (2002) Nature, 420, pp. 502-507
  • Belkaid, Y., Hoffmann, K.F., Mendez, S., Kamhawi, S., Udey, M.C., Wynn, T.A., Sacks, D.L., The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure (2001) J. Exp. Med., 194, pp. 1497-1506
  • Ronet, C., Hauyon-La Torre, Y., Revaz-Breton, M., Mastelic, B., Tacchini-Cottier, F., Louis, J., Launois, P., Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production (2010) J. Immunol., 184, pp. 886-894
  • Bhaumik, P., St-Pierre, G., Milot, V., St-Pierre, C., Sato, S., Galectin-3 facilitates neutrophil recruitment as an innate immune response to a parasitic protozoa cutaneous infection (2013) J. Immunol, 190, pp. 630-640
  • Anastasi, E., Campese, A.F., Bellavia, D., Bulotta, A., Balestri, A., Pascucci, M., Checquolo, S., Expression of activated Notch-3 in transgenic mice enhances generation of T regulatory cells and protects against experimental autoimmune diabetes (2003) J. Immunol., 171, pp. 4504-4511
  • Ou-Yang, H.F., Zhang, H.W., Wu, C.G., Zhang, P., Zhang, J., Li, J.C., Hou, L.H., Notch signaling regulates the FOXP3 promoter through RBP-J- and Hes1-dependent mechanisms (2009) Mol. Cell. Biochem., 320, pp. 109-114
  • Samon, J.B., Champhekar, A., Minter, L.M., Telfer, J.C., Miele, L., Fauq, A., Das, P., Notch-1 and TGF-β1 cooperatively regulate Foxp3 expression and the maintenance of peripheral regulatory T cells (2008) Blood, 112, pp. 1813-1821
  • Rutz, S., Janke, M., Kassner, N., Hohnstein, T., Krueger, M., Scheffold, A., Notch regulates IL-10 production by T helper 1 cells (2008) Proc. Natl. Acad. Sci. USA, 105, pp. 3497-3502
  • Hue, S., Kared, H., Mehwish, Y., Mouhamad, S., Balbo, M., Levy, Y., Notch activation on effector T cells increases their sensitivity to T REG cell-mediated suppression through upregulation of TGF-βRII expression (2012) Eur. J. Immunol., 42, pp. 1796-1803
  • Reinhard, K., Huber, M., Wostl, C., Hellhund, A., Toboldt, A., Abass, E., Casper, B., c-Rel promotes type 1 and type 17 immune responses during Leishmania major infection (2011) Eur. J. Immunol., 41, pp. 1388-1398
  • Hsu, D.K., Yang, R.Y., Yu, L., Pan, Z., Salomon, D.R., Fung-Leung, W.P., Liu, F.T., Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses (2000) Am. J. Pathol., 156, pp. 1073-1083
  • Louis, J., Moedder, E., Behin, R., Engers, H., Recognition of protozoan parasite antigens by murine T lymphocytes. I. Induction of specific T lymphocyte-dependent proliferative response to Leishmania tropica (1979) Eur. J. Immunol., 9, pp. 841-847
  • Nicolas, L., Prina, E., Lang, T., Milon, G., Real-time PCR for detection and quantitation of leishmania in mouse tissues (2002) J. Clin. Microbiol., 40, pp. 1666-1669
  • Ho, M.K., Springer, T.A., Mac-2, a novel 32,000 Mr mouse macrophage subpopulation-specific antigen defined by monoclonal antibodies (1982) J. Immunol., 128, pp. 1221-1228
  • Scott-Browne, J.P., Shafiani, S., Tucker-Heard, G., Ishida-Tsubota, K., Fontenot, J.D., Rudensky, A.Y., Bevan, M.J., Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis (2007) J. Exp. Med., 204, pp. 2159-2169
  • Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method (2001) Methods, 25, pp. 402-408

Citas:

---------- APA ----------
Fermino, M.L., Dias, F.C., Lopes, C.D., Souza, M.A., Cruz, A.K., Liu, F.-T., Chammas, R.,..., Bernardes, E.S. (2013) . Galectin-3 negatively regulates the frequency and function of CD4 + CD25 + Foxp3 + regulatory T cells and influences the course of Leishmania major infection. European Journal of Immunology, 43(7), 1806-1817.
http://dx.doi.org/10.1002/eji.201343381
---------- CHICAGO ----------
Fermino, M.L., Dias, F.C., Lopes, C.D., Souza, M.A., Cruz, A.K., Liu, F.-T., et al. "Galectin-3 negatively regulates the frequency and function of CD4 + CD25 + Foxp3 + regulatory T cells and influences the course of Leishmania major infection" . European Journal of Immunology 43, no. 7 (2013) : 1806-1817.
http://dx.doi.org/10.1002/eji.201343381
---------- MLA ----------
Fermino, M.L., Dias, F.C., Lopes, C.D., Souza, M.A., Cruz, A.K., Liu, F.-T., et al. "Galectin-3 negatively regulates the frequency and function of CD4 + CD25 + Foxp3 + regulatory T cells and influences the course of Leishmania major infection" . European Journal of Immunology, vol. 43, no. 7, 2013, pp. 1806-1817.
http://dx.doi.org/10.1002/eji.201343381
---------- VANCOUVER ----------
Fermino, M.L., Dias, F.C., Lopes, C.D., Souza, M.A., Cruz, A.K., Liu, F.-T., et al. Galectin-3 negatively regulates the frequency and function of CD4 + CD25 + Foxp3 + regulatory T cells and influences the course of Leishmania major infection. Eur. J. Immunol. 2013;43(7):1806-1817.
http://dx.doi.org/10.1002/eji.201343381