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Abstract:

Along with the discovery of tumor-driven inflammatory pathways, there has been a considerable progress over the past 10 years in understanding the mechanisms leading to cancer immunosurveillance and immunoediting. Several regulatory pathways, typically involved in immune cell homeostasis, are co-opted by cancer cells to thwart the development of effective antitumor responses. These regulatory circuits include the engagement of inhibitory checkpoint pathways (CTLA-4, PD-1/PD-L1, LAG-3 and TIM-3), secretion of immunosuppressive cytokines (TGF-β, IL-10), and expansion and/or recruitment of myeloid or lymphoid regulatory cell populations. Elucidation of these pathways has inspired the design and implementation of novel immunotherapeutic modalities, which have already generated clinical benefits in an important number of cancer patients. Galectins, a family of glycan-binding proteins widely expressed in the tumor microenvironment (TME), have emerged as key players in immune evasion programs that differentially control the fate of effector and regulatory lymphoid and myeloid cell populations. How do galectins translate glycan-containing information into cellular programs that control immune regulatory cancer networks? Here, we uncover the selective roles of individual members of the galectin family in cancer-promoting inflammation, immunosuppression, and angiogenesis. Moreover, we highlight the relevance of corresponding glycosylated ligands and counter-receptors and the emerging function of these lectins as biological liaisons connecting commensal microbiota, systemic inflammation, and distal tumor growth. Understanding the molecular and cellular components of galectin-driven regulatory circuits, the implications of different glycosylation pathways in their functions and their clinical relevance in human cancer might lead to the development of new therapeutic approaches in a broad range of tumor types. © 2016 Elsevier Ltd

Registro:

Documento: Artículo
Título:Shaping the Immune Landscape in Cancer by Galectin-Driven Regulatory Pathways
Autor:Rabinovich, G.A.; Conejo-García, J.R.
Filiación:Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental (IBYME), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Vuelta de Obligado 2490, Buenos Aires, C1428, Argentina
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Buenos Aires, C1428, Argentina
Tumor Microenvironment and Metastasis Program, The Wistar Institute, Philadelphia, PA 19104, United States
Palabras clave:Cancer; Galectins; Glycans; Immunotherapy; Tumor Immunity; activated leukocyte cell adhesion molecule; B lymphocyte receptor; CD45 antigen; CD7 antigen; cytokine receptor; cytotoxic T lymphocyte antigen 4; ecalectin; galectin; galectin 1; galectin 10; galectin 3; galectin 8; glycan; glycolipid; glycoprotein; interleukin 10; interleukin 15; interleukin 2; interleukin 4; lag 3 protein; leukosialin; n acetylglucosaminyltransferase; natural killer cell receptor NKG2D; programmed death 1 ligand 1; protein; T lymphocyte receptor; tim 3 protein; transforming growth factor beta; unclassified drug; unindexed drug; vasculotropin receptor 2; galectin; ligand; angiogenesis; antigen presenting cell; apoptosis; bone marrow cell; breast cancer; cancer patient; carbohydrate synthesis; CD8+ T lymphocyte; cell adhesion; cell differentiation; cell migration; chronic lymphatic leukemia; classical Hodgkin lymphoma; commensal; cross linking; cutaneous T cell lymphoma; cytokine production; cytokine release; cytotoxic T lymphocyte; endothelium cell; epithelial mesenchymal transition; fibroblast; glycosylation; human; immune evasion; immunocompetent cell; immunosuppressive treatment; immunosurveillance; inflammation; inflammatory cell; inflammatory infiltrate; Kaposi sarcoma; lung adenocarcinoma; lymphoid cell; malignant neoplastic disease; melanoma; mycosis fungoides; natural killer cell; non small cell lung cancer; nonhuman; ovary cancer; pancreas adenocarcinoma; priority journal; prostate carcinoma; protein protein interaction; regulatory T lymphocyte; Review; Sezary syndrome; T cell lymphoma; Th1 cell; Th17 cell; tumor growth; tumor immunity; tumor microenvironment; upregulation; animal; immunology; neoplasm; signal transduction; Animals; Galectins; Glycosylation; Humans; Ligands; Neoplasms; Signal Transduction; Tumor Microenvironment
Año:2016
Volumen:428
Número:16
Página de inicio:3266
Página de fin:3281
DOI: http://dx.doi.org/10.1016/j.jmb.2016.03.021
Título revista:Journal of Molecular Biology
Título revista abreviado:J. Mol. Biol.
ISSN:00222836
CODEN:JMOBA
CAS:galectin 1, 258495-34-0; galectin 3, 208128-56-7; galectin 8, 220452-97-1; interleukin 2, 85898-30-2; leukosialin, 123897-54-1; n acetylglucosaminyltransferase, 9054-49-3; protein, 67254-75-5; Galectins; Ligands
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00222836_v428_n16_p3266_Rabinovich

Referencias:

  • Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation (2011) Cell., 144, pp. 646-674
  • Trinchieri, G., Cancer and inflammation: an old intuition with rapidly evolving new concepts (2012) Annu. Rev. Immunol., 30, pp. 677-706
  • Balkwill, F.R., Mantovani, A., Cancer-related inflammation: common themes and therapeutic opportunities (2012) Semin. Cancer Biol., 22, pp. 33-40
  • Mantovani, A., Molecular pathways linking inflammation and cancer (2010) Curr. Mol. Med., 10, pp. 369-373
  • Gubin, M.M., Schreiber, R.D., CANCER. the odds of immunotherapy success (2015) Science., 350, pp. 158-159
  • Rabinovich, G.A., Gabrilovich, D., Sotomayor, E.M., Immunosuppressive strategies that are mediated by tumor cells (2007) Annu. Rev. Immunol., 25, pp. 267-296
  • Mariño, K., Bones, J., Kattla, J.J., Rudd, P.M., A systematic approach to protein glycosylation analysis: a path through the maze (2010) Nat. Chem. Biol., 6, pp. 713-723
  • Elola, M.T., Blidner, A.G., Ferragut, F., Bracalente, C., Rabinovich, G.A., Assembly, organization and regulation of cell-surface receptors by lectin–glycan complexes (2015) Biochem. J., 469, pp. 1-16
  • van Kooyk, Y., Rabinovich, G.A., Protein–glycan interactions in the control of innate and adaptive immune responses (2008) Nat. Immunol., 9, pp. 593-601
  • Blidner, A.G., Mendez-Huergo, S.P., Cagnoni, A.J., Rabinovich, G.A., Re-wiring regulatory cell networks in immunity by galectin–glycan interactions (2015) FEBS Lett., 589, pp. 3407-3418
  • Pinho, S.S., Reis, C.A., Glycosylation in cancer: mechanisms and clinical implications (2015) Nat. Rev. Cancer., 15, pp. 540-555
  • Rabinovich, G.A., Croci, D.O., Regulatory circuits mediated by lectin–glycan interactions in autoimmunity and cancer (2012) Immunity., 36, pp. 322-335
  • Croci, D.O., Cerliani, J.P., Pinto, N.A., Morosi, L.G., Rabinovich, G.A., Regulatory role of glycans in the control of hypoxia-driven angiogenesis and sensitivity to anti-angiogenic treatment (2014) Glycobiology., 24, pp. 1283-1290
  • Hakomori, S., Glycosylation defining cancer malignancy: new wine in an old bottle (2002) Proc. Natl. Acad. Sci. U. S. A., 99, pp. 10231-10233
  • Bassaganas, S., Allende, H., Cobler, L., Ortiz, M.R., Llop, E., de Bolos, C., Peracaula, R., Inflammatory cytokines regulate the expression of glycosyltransferases involved in the biosynthesis of tumor-associated sialylated glycans in pancreatic cancer cell lines (2015) Cytokine., 75, pp. 197-206
  • Higai, K., Miyazaki, N., Azuma, Y., Matsumoto, K., Interleukin-1beta induces sialyl Lewis X on hepatocellular carcinoma HuH-7 cells via enhanced expression of ST3Gal IV and FUT VI gene (2006) FEBS Lett., 580, pp. 6069-6075
  • Azuma, Y., Murata, M., Matsumoto, K., Alteration of sugar chains on alpha(1)-acid glycoprotein secreted following cytokine stimulation of HuH-7 cells in vitro (2000) Clin. Chim. Acta., 294, pp. 93-103
  • Nolz, J.C., Harty, J.T., IL-15 regulates memory CD8 + T cell O-glycan synthesis and affects trafficking (2014) J. Clin. Invest., 124, pp. 1013-1026
  • Carlow, D.A., Corbel, S.Y., Williams, M.J., Ziltener, H.J., IL-2, -4, and -15 differentially regulate O-glycan branching and P-selectin ligand formation in activated CD8 T cells (2001) J. Immunol., 167, pp. 6841-6848
  • Lau, K.S., Dennis, J.W., N-glycans in cancer progression (2008) Glycobiology., 18, pp. 750-760
  • Miwa, H.E., Song, Y., Alvarez, R., Cummings, R.D., Stanley, P., The bisecting GlcNAc in cell growth control and tumor progression (2012) Glycoconj. J., 29, pp. 609-618
  • Kimura, T., Finn, O.J., MUC1 immunotherapy is here to stay (2013) Expert. Opin. Biol. Ther., 13, pp. 35-49
  • Bull, C., den Brok, M.H., Adema, G.J., Sweet escape: sialic acids in tumor immune evasion (2014) Biochim. Biophys. Acta., 1846, pp. 238-246
  • Dam, T.K., Brewer, C.F., Multivalent lectin–carbohydrate interactions energetics and mechanisms of binding (2010) Adv. Carbohydr. Chem. Biochem., 63, pp. 139-164
  • Cummings, R.D., Esko, J.D., Principles of Glycan Recognition (2009) Essentials of Glycobiology, , A. Varki R.D. Cummings J.D. Esko H.H. Freeze P. Stanley C.R. Bertozzi G.W. Hart M.E.,. Etzler 2nd edit. Cold Spring Harbor NY (Chapter 27; ISBN-13: 9780879697709)
  • Brewer, C.F., Miceli, M.C., Baum, L.G., Clusters, bundles, arrays and lattices: novel mechanisms for lectin–saccharide-mediated cellular interactions (2002) Curr. Opin. Struct. Biol., 12, pp. 616-623
  • Thiemann, S., Baum, L.G., Galectins and immune responses—just how do they do those things they do? (2016) Annu. Rev. Immunol., , (Feb 22. Epub ahead of print)
  • Liu, F.T., Rabinovich, G.A., Galectins as modulators of tumour progression (2005) Nat. Rev. Cancer, 5, pp. 29-41
  • Lahm, H., Andre, S., Hoeflich, A., Fischer, J.R., Sordat, B., Kaltner, H., Wolf, E., Gabius, H.J., Comprehensive galectin fingerprinting in a panel of 61 human tumor cell lines by RT-PCR and its implications for diagnostic and therapeutic procedures (2001) J. Cancer Res. Clin. Oncol., 127, pp. 375-386
  • Langbein, S., Brade, J., Badawi, J.K., Hatzinger, M., Kaltner, H., Lensch, M., Gene-expression signature of adhesion/growth-regulatory tissue lectins (galectins) in transitional cell cancer and its prognostic relevance (2007) Histopathology., 51, pp. 681-690
  • Remmelink, M., de Leval, L., Decaestecker, C., Duray, A., Crompot, E., Sirtaine, N., Quantitative immunohistochemical fingerprinting of adhesion/growth-regulatory galectins in salivary gland tumours: divergent profiles with diagnostic potential (2011) Histopathology., 58, pp. 543-556
  • Laderach, D.J., Gentilini, L.D., Giribaldi, L., Delgado, V.C., Nugnes, L., Croci, D.O., 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
  • Schulkens, I.A., Heusschen, R., van den Boogaart, V., van Suylen, R.J., Dingemans, A.M., Griffioen, A.W., Thijssen, V.L., Galectin expression profiling identifies galectin-1 and Galectin-9Delta5 as prognostic factors in stage I/II non-small cell lung cancer (2014) PLoS One., 9 (9). , e107988
  • El Leithy, A.A., Helwa, R., Assem, M.M., Hassan, N.H., Expression profiling of cancer-related galectins in acute myeloid leukemia (2015) Tumour Biol., 36, pp. 7929-7939
  • Thijssen, V.L., Barkan, B., Shoji, H., Aries, I.M., Mathieu, V., Deltour, L., Tumor cells secrete galectin-1 to enhance endothelial cell activity (2010) Cancer Res., 70, pp. 6216-6224
  • Croci, D.O., Salatino, M., Rubinstein, N., Cerliani, J.P., Cavallin, L.E., Leung, H.J., 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
  • Croci, D.O., Cerliani, J.P., Dalotto-Moreno, T., Mendez-Huergo, S.P., Mascanfroni, I.D., Dergan-Dylon, S., Glycosylation-dependent lectin-receptor interactions preserve angiogenesis in anti-VEGF refractory tumors (2014) Cell., 156, pp. 744-758
  • Bacigalupo, M.L., Manzi, M., Espelt, M.V., Gentilini, L.D., Compagno, D., Laderach, D.J., Galectin-1 triggers epithelial–mesenchymal transition in human hepatocellular carcinoma cells (2015) J. Cell. Physiol., 230, pp. 1298-1309
  • Liu, F.T., Patterson, R.J., Wang, J.L., Intracellular functions of galectins (2002) Biochim. Biophys. Acta., 1572, pp. 263-273
  • Elad-Sfadia, G., Haklai, R., Balan, E., Kloog, Y., Galectin-3 augments K-Ras activation and triggers a Ras signal that attenuates ERK but not phosphoinositide 3-kinase activity (2004) J. Biol. Chem., 279, pp. 34922-34930
  • Su, Y.C., Davuluri, G.V., Chen, C.H., Shiau, D.C., Chen, C.C., Chen, C.L., Lin, Y.S., Chang, C.P., Galectin-1-induced autophagy facilitates cisplatin resistance of hepatocellular carcinoma (2016) PLoS One., 11. , e0148408
  • Hirabayashi, J., Kasai, K.I., Evolution of animal lectins (1998) Prog. Mol. Subcell. Biol., 19, pp. 45-88
  • Nickel, W., The mystery of nonclassical protein secretion. a current view on cargo proteins and potential export routes (2003) Eur. J. Biochem., 270, pp. 2109-2119
  • Hirabayashi, J., Hashidate, T., Arata, Y., Nishi, N., Nakamura, T., Hirashima, M., Oligosaccharide specificity of galectins: a search by frontal affinity chromatography (2002) Biochim. Biophys. Acta., 1572, pp. 232-254
  • Blixt, O., Head, S., Mondala, T., Scanlan, C., Huflejt, M.E., Alvarez, R., Bryan, M.C., Printed covalent glycan array for ligand profiling of diverse glycan binding proteins (2004) Proc. Natl. Acad. Sci. U. S. A., 101, pp. 17033-17038
  • Nagae, M., Nishi, N., Nakamura-Tsuruta, S., Hirabayashi, J., Wakatsuki, S., Kato, R., Structural analysis of the human galectin-9 N-terminal carbohydrate recognition domain reveals unexpected properties that differ from the mouse orthologue (2008) J. Mol. Biol., 375, pp. 119-135
  • 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
  • Toscano, M.A., Bianco, G.A., Ilarregui, J.M., Croci, D.O., Correale, J., Hernandez, J.D., Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death (2007) Nat. Immunol., 8, pp. 825-834
  • Amano, M., Galvan, M., He, J., Baum, L.G., The ST6Gal I sialyltransferase selectively modifies N-glycans on CD45 to negatively regulate galectin-1-induced CD45 clustering, phosphatase modulation, and T cell death (2003) J. Biol. Chem., 278, pp. 7469-7475
  • Stowell, S.R., Arthur, C.M., Mehta, P., Slanina, K.A., Blixt, O., Leffler, H., Galectin-1, -2, and -3 exhibit differential recognition of sialylated glycans and blood group antigens (2008) J. Biol. Chem., 283, pp. 10109-10123
  • Ideo, H., Matsuzaka, T., Nonaka, T., Seko, A., Yamashita, K., Galectin-8-N-domain recognition mechanism for sialylated and sulfated glycans (2011) J. Biol. Chem., 286, pp. 11346-11355
  • 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, p. 15406
  • Stillman, B.N., Hsu, D.K., Pang, M., Brewer, C.F., Johnson, P., Liu, F.T., Baum, L.G., Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death (2006) J. Immunol., 176, pp. 778-789
  • Wang, J., Lu, Z.H., Gabius, H.J., Rohowsky-Kochan, C., Ledeen, R.W., Wu, G., Cross-linking of GM1 ganglioside by galectin-1 mediates regulatory T cell activity involving TRPC5 channel activation: possible role in suppressing experimental autoimmune encephalomyelitis (2009) J. Immunol., 182, pp. 4036-4045
  • Kouo, T., Huang, L., Pucsek, A.B., Cao, M., Solt, S., Armstrong, T., Jaffee, E., Galectin-3 shapes antitumor immune responses by suppressing CD8 + T cells via LAG-3 and inhibiting expansion of plasmacytoid dendritic cells (2015) Cancer Immunol. Res., 3, pp. 412-423
  • Carcamo, C., Pardo, E., Oyanadel, C., Bravo-Zehnder, M., Bull, P., Caceres, M., Galectin-8 binds specific beta1 integrins and induces polarized spreading highlighted by asymmetric lamellipodia in Jurkat T cells (2006) Exp. Cell Res., 312, pp. 374-386
  • Eshkar Sebban, L., Ronen, D., Levartovsky, D., Elkayam, O., Caspi, D., Aamar, S., The involvement of CD44 and its novel ligand galectin-8 in apoptotic regulation of autoimmune inflammation (2007) J. Immunol., 179, pp. 1225-1235
  • Zhu, C., Anderson, A.C., Schubart, A., Xiong, H., Imitola, J., Khoury, S.J., The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity (2005) Nat. Immunol., 6, pp. 1245-1252
  • Wu, C., Thalhamer, T., Franca, R.F., Xiao, S., Wang, C., Hotta, C., Galectin-9–CD44 interaction enhances stability and function of adaptive regulatory T cells (2014) Immunity., 41, pp. 270-282
  • Thiemann, S., Man, J.H., Chang, M.H., Lee, B., Baum, L.G., Galectin-1 regulates tissue exit of specific dendritic cell populations (2015) J. Biol. Chem., 290, pp. 22662-22677
  • Ilarregui, J.M., Croci, D.O., Bianco, G.A., Toscano, M.A., Salatino, M., Vermeulen, M.E., 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
  • Fulcher, J.A., Chang, M.H., Wang, S., Almazan, T., Hashimi, S.T., Eriksson, A.U., Galectin-1 co-clusters CD43/CD45 on dendritic cells and induces cell activation and migration through Syk and protein kinase C signaling (2009) J. Biol. Chem., 284, pp. 26860-26870
  • Starossom, S.C., Mascanfroni, I.D., Imitola, J., Cao, L., Raddassi, K., Hernandez, S.F., Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration (2012) Immunity., 37, pp. 249-263
  • Hsieh, S.H., Ying, N.W., Wu, M.H., Chiang, W.F., Hsu, C.L., Wong, T.Y., Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells (2008) Oncogene., 27, pp. 3746-3753
  • Jouve, N., Despoix, N., Espeli, M., Gauthier, L., Cypowyj, S., Fallague, K., The involvement of CD146 and its novel ligand Galectin-1 in apoptotic regulation of endothelial cells (2013) J. Biol. Chem., 288, pp. 2571-2579
  • 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
  • Delgado, V.M., Nugnes, L.G., Colombo, L.L., Troncoso, M.F., Fernandez, M.M., Malchiodi, E.L., Modulation of endothelial cell migration and angiogenesis: a novel function for the “tandem-repeat” lectin galectin-8 (2011) FASEB J., 25, pp. 242-254
  • 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
  • Tesone, A.J., Rutkowski, M.R., Brencicova, E., Svoronos, N., Perales-Puchalt, A., Stephen, T.L., Satb1 overexpression drives tumor-promoting activities in cancer-associated dendritic cells (2016) Cell Rep., 14, pp. 1774-1786
  • Fuertes, M.B., Molinero, L.L., Toscano, M.A., Ilarregui, J.M., Rubinstein, N., Fainboim, L., 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
  • Zuñiga, 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
  • Garin, M.I., Chu, C.C., Golshayan, D., Cernuda-Morollon, 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
  • 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. U. S. A., 105, pp. 18472-18477
  • Dyer, K.D., Rosenberg, H.F., Transcriptional regulation of galectin-10 (eosinophil Charcot–Leyden crystal protein): a GC box (-44 to -50) controls butyric acid induction of gene expression (2001) Life Sci., 69, pp. 201-212
  • Kubach, J., Lutter, P., Bopp, T., Stoll, S., Becker, C., Huter, E., 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
  • Thijssen, V.L., Heusschen, R., Caers, J., Griffioen, A.W., Galectin expression in cancer diagnosis and prognosis: a systematic review (2015) Biochim. Biophys. Acta., 1855, pp. 235-247
  • Mendez-Huergo, S.P., Maller, S.M., Farez, M.F., Marino, K., Correale, J., Rabinovich, G.A., Integration of lectin-glycan recognition systems and immune cell networks in CNS inflammation (2014) Cytokine Growth Factor Rev., 25, pp. 247-255
  • Rubinstein, N., Alvarez, M., Zwirner, N., Toscano, M., Ilarregui, J., Bravo, 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
  • Cedeno-Laurent, F., Opperman, M.J., Barthel, S.R., Hays, D., Schatton, T., Zhan, Q., He, X., Dimitroff, C.J., Metabolic inhibition of galectin-1-binding carbohydrates accentuates antitumor immunity (2012) J. Investig. Dermatol., 132, pp. 410-420
  • Rostoker, R., Yaseen, H., Schif-Zuck, S., Lichtenstein, R.G., Rabinovich, G.A., Ariel, A., Galectin-1 induces 12/15-lipoxygenase expression in murine macrophages and favors their conversion toward a pro-resolving phenotype (2013) Prostaglandins Other Lipid Mediat., 107, pp. 85-94
  • 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
  • He, J., Baum, L.G., Endothelial cell expression of galectin-1 induced by prostate cancer cells inhibits T-cell transendothelial migration (2006) Lab. Investig., 86, pp. 578-590
  • Juszczynski, P., Ouyang, J., Monti, S., Rodig, S.J., Takeyama, K., Abramson, J., 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
  • Gandhi, M.K., Moll, G., Smith, C., Dua, U., Lambley, E., Ramuz, O., Galectin-1 mediated suppression of Epstein–Barr virus specific T-cell immunity in classic Hodgkin lymphoma (2007) Blood., 110, pp. 1326-1329
  • Ouyang, J., Juszczynski, P., Rodig, S.J., Green, M.R., O'Donnell, E., Currie, T., Viral induction and targeted inhibition of galectin-1 in EBV + posttransplant lymphoproliferative disorders (2011) Blood., 117, pp. 4315-4322
  • Banh, A., Zhang, J., Cao, H., Bouley, D.M., Kwok, S., Kong, C., Tumor galectin-1 mediates tumor growth and metastasis through regulation of T-cell apoptosis (2011) Cancer Res., 71, pp. 4423-4431
  • Kuo, P.L., Huang, M.S., Cheng, D.E., Hung, J.Y., Yang, C.J., Chou, S.H., Lung cancer-derived galectin-1 enhances tumorigenic potentiation of tumor-associated dendritic cells by expressing heparin-binding EGF-like growth factor (2012) J. Biol. Chem., 287, pp. 9753-9764
  • Soldati, R., Berger, E., Zenclussen, A.C., Jorch, G., Lode, H.N., Salatino, M., 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., Targeting galectin-1 overcomes breast cancer-associated immunosuppression and prevents metastatic disease (2013) Cancer Res., 73, pp. 1107-1117
  • Ito, K., Scott, S.A., Cutler, S., Dong, L.F., Neuzil, J., Blanchard, H., Ralph, S.J., Thiodigalactoside inhibits murine cancers by concurrently blocking effects of galectin-1 on immune dysregulation, angiogenesis and protection against oxidative stress (2011) Angiogenesis., 14, pp. 293-307
  • Martinez-Bosch, N., Fernandez-Barrena, M.G., Moreno, M., Ortiz-Zapater, E., Munne-Collado, J., Iglesias, M., Galectin-1 drives pancreatic carcinogenesis through stroma remodeling and Hedgehog signaling activation (2014) Cancer Res., 74, pp. 3512-3524
  • Tang, D., Gao, J., Wang, S., Yuan, Z., Ye, N., Chong, Y., Apoptosis and anergy of T cell induced by pancreatic stellate cells-derived galectin-1 in pancreatic cancer (2015) Tumour Biol., 36, pp. 5617-5626
  • Verschuere, T., Toelen, J., Maes, W., Poirier, F., Boon, L., Tousseyn, T., Glioma-derived galectin-1 regulates innate and adaptive antitumor immunity (2014) Int. J. Cancer., 134, pp. 873-884
  • Baker, G.J., Chockley, P., Yadav, V.N., Doherty, R., Ritt, M., Sivaramakrishnan, S., Natural killer cells eradicate galectin-1-deficient glioma in the absence of adaptive immunity (2014) Cancer Res., 74, pp. 5079-5090
  • Rutkowski, M.R., Stephen, T.L., Svoronos, N., Allegrezza, M.J., Tesone, A.J., Perales-Puchalt, A., Microbially driven TLR5-dependent signaling governs distal malignant progression through tumor-promoting inflammation (2015) Cancer Cell., 27, pp. 27-40
  • Croci, D.O., Morande, P.E., Dergan-Dylon, S., Borge, M., Toscano, M.A., Stupirski, J.C., Nurse-like cells control the activity of chronic lymphocytic leukemia B cells via galectin-1 (2013) Leukemia., 27, pp. 1413-1416
  • Cedeno-Laurent, F., Watanabe, R., Teague, J.E., Kupper, T.S., Clark, R.A., Dimitroff, C.J., Galectin-1 inhibits the viability, proliferation, and Th1 cytokine production of nonmalignant T cells in patients with leukemic cutaneous T-cell lymphoma (2012) Blood., 119, pp. 3534-3538
  • Roberts, A.A., Amano, M., Felten, C., Galvan, M., Sulur, G., Pinter-Brown, L., Galectin-1-mediated apoptosis in mycosis fungoides: the roles of CD7 and cell surface glycosylation (2003) Mod. Pathol., 16, pp. 543-551
  • Rappl, G., Abken, H., Muche, J.M., Sterry, W., Tilgen, W., Andre, S., CD4 + CD7- leukemic T cells from patients with Sezary syndrome are protected from galectin-1-triggered T cell death (2002) Leukemia., 16, pp. 840-845
  • Lykken, J.M., Horikawa, M., Minard-Colin, V., Kamata, M., Miyagaki, T., Poe, J.C., Tedder, T.F., Galectin-1 drives lymphoma CD20 immunotherapy resistance: validation of a preclinical system to identify resistance mechanisms (2016) Blood., , (pii: blood-2015-11-681130. Epub ahead of print)
  • Demotte, N., Stroobant, V., Courtoy, P.J., Van Der Smissen, P., Colau, D., Luescher, I.F., Restoring the association of the T cell receptor with CD8 reverses anergy in human tumor-infiltrating lymphocytes (2008) Immunity., 28, pp. 414-424
  • Demotte, N., Wieers, G., Van Der Smissen, P., Moser, M., Schmidt, C., Thielemans, K., A galectin-3 ligand corrects the impaired function of human CD4 and CD8 tumor-infiltrating lymphocytes and favors tumor rejection in mice (2010) Cancer Res., 70, pp. 7476-7488
  • Peng, W., Wang, H.Y., Miyahara, Y., Peng, G., Wang, R.F., Tumor-associated galectin-3 modulates the function of tumor-reactive T cells (2008) Cancer Res., 68, pp. 7228-7236
  • Fukumori, T., Takenaka, Y., Yoshii, T., Kim, H.R., Hogan, V., Inohara, H., CD29 and CD7 mediate galectin-3-induced type II T-cell apoptosis (2003) Cancer Res., 63, pp. 8302-8311
  • Tsuboi, S., Sutoh, M., Hatakeyama, S., Hiraoka, N., Habuchi, T., Horikawa, Y., A novel strategy for evasion of NK cell immunity by tumours expressing core2 O-glycans (2011) EMBO J., 30, pp. 3173-3185
  • Wang, W., Guo, H., Geng, J., Zheng, X., Wei, H., Sun, R., Tian, Z., Tumor-released Galectin-3, a soluble inhibitory ligand of human NKp30, plays an important role in tumor escape from NK cell attack (2014) J. Biol. Chem., 289, pp. 33311-33319
  • Sakuishi, K., Jayaraman, P., Behar, S.M., Anderson, A.C., Kuchroo, V.K., Emerging Tim-3 functions in antimicrobial and tumor immunity (2011) Trends Immunol., 32, pp. 345-349
  • Li, H., Wu, K., Tao, K., Chen, L., Zheng, Q., Lu, X., Tim-3/galectin-9 signaling pathway mediates T-cell dysfunction and predicts poor prognosis in patients with hepatitis B virus-associated hepatocellular carcinoma (2012) Hepatology., 56, pp. 1342-1351
  • Kang, C.W., Dutta, A., Chang, L.Y., Mahalingam, J., Lin, Y.C., Chiang, J.M., Apoptosis of tumor infiltrating effector TIM-3 + CD8 + T cells in colon cancer (2015) Sci. Rep., 5, p. 15659
  • Dardalhon, V., Anderson, A.C., Karman, J., Apetoh, L., Chandwaskar, R., Lee, D.H., Tim-3/galectin-9 pathway: regulation of Th1 immunity through promotion of CD11b + Ly-6G + myeloid cells (2010) J. Immunol., 185, pp. 1383-1392
  • Nagahara, K., Arikawa, T., Oomizu, S., Kontani, K., Nobumoto, A., Tateno, H., Galectin-9 increases Tim-3 + dendritic cells and CD8 + T cells and enhances antitumor immunity via galectin-9–Tim-3 interactions (2008) J. Immunol., 181, pp. 7660-7669
  • Oomizu, S., Arikawa, T., Niki, T., Kadowaki, T., Ueno, M., Nishi, N., Galectin-9 suppresses Th17 cell development in an IL-2-dependent but Tim-3-independent manner (2012) Clin. Immunol., 143, pp. 51-58
  • Leitner, J., Rieger, A., Pickl, W.F., Zlabinger, G., Grabmeier-Pfistershammer, K., Steinberger, P., TIM-3 does not act as a receptor for galectin-9 (2013) PLoS Pathog., 9. , e1003253
  • Chiba, S., Baghdadi, M., Akiba, H., Yoshiyama, H., Kinoshita, I., Dosaka-Akita, H., Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1 (2012) Nat. Immunol., 13, pp. 832-842
  • Madireddi, S., Eun, S.Y., Lee, S.W., Nemčovičová, I., Mehta, A.K., Zajonc, D.M., Galectin-9 controls the therapeutic activity of 4-1BB-targeting antibodies (2014) J. Exp. Med., 211, pp. 1433-1448
  • Bunt, S.K., Yang, L., Sinha, P., Clements, V.K., Leips, J., Ostrand-Rosenberg, S., Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression (2007) Cancer Res., 67, pp. 10019-10026
  • Sinha, P., Clements, V.K., Fulton, A.M., Ostrand-Rosenberg, S., Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells (2007) Cancer Res., 67, pp. 4507-4513
  • Eruslanov, E., Daurkin, I., Ortiz, J., Vieweg, J., Kusmartsev, S., Pivotal Advance: Tumor-mediated induction of myeloid-derived suppressor cells and M2-polarized macrophages by altering intracellular PGE(2) catabolism in myeloid cells (2010) J. Leukoc. Biol., 88, pp. 839-848
  • Takizawa, H., Boettcher, S., Manz, M.G., Demand-adapted regulation of early hematopoiesis in infection and inflammation (2012) Blood., 119, pp. 2991-3002
  • Ostrand-Rosenberg, S., Sinha, P., Myeloid-derived suppressor cells: linking inflammation and cancer (2009) J. Immunol., 182, pp. 4499-4506
  • Gabrilovich, D.I., Ostrand-Rosenberg, S., Bronte, V., Coordinated regulation of myeloid cells by tumours (2012) Nat. Rev. Immunol., 12, pp. 253-268
  • Youn, J.I., Nagaraj, S., Collazo, M., Gabrilovich, D.I., Subsets of myeloid-derived suppressor cells in tumor-bearing mice (2008) J. Immunol., 181, pp. 5791-5802
  • Rutkowski, M.R., Conejo-Garcia, J.R., TLR5 signaling, commensal microbiota and systemic tumor promoting inflammation: the three parcae of malignant progression (2015) Oncoimmunology., 4 (8). , e1021542
  • Rutkowski, M.R., Conejo-Garcia, J.R., Size does not matter: commensal microorganisms forge tumor-promoting inflammation and antitumor immunity (2015) Oncoscience., 2, pp. 239-246
  • Movahedi, K., Guilliams, M., Van den Bossche, J., Van den Bergh, R., Gysemans, C., Beschin, A., Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity (2008) Blood., 111, pp. 4233-4244
  • Novak, R., Dabelic, S., Dumic, J., Galectin-1 and galectin-3 expression profiles in classically and alternatively activated human macrophages (2012) Biochim. Biophys. Acta., 1820, pp. 1383-1390
  • Cubillos-Ruiz, J.R., Silberman, P.C., Rutkowski, M.R., Chopra, S., Perales-Puchalt, A., Song, M., ER stress sensor XBP1 controls antitumor immunity by disrupting dendritic cell homeostasis (2015) Cell., 161, pp. 1527-1538
  • Scarlett, U., Rutkowski, M., Rauwerdink, A., Fields, J., Escovar-Fadul, X., Baird, J., Ovarian cancer progression is controlled by phenotypic changes in dendritic cells (2012) J. Exp. Med., 209, pp. 495-506
  • Tuddenham, S., Sears, C.L., The intestinal microbiome and health (2015) Curr. Opin. Infect. Dis., 28, pp. 464-470
  • Furusawa, Y., Obata, Y., Fukuda, S., Endo, T., Nakato, G., Takahashi, D., Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells (2013) Nature., 504, pp. 446-450
  • Arpaia, N., Campbell, C., Fan, X., Dikiy, S., van der Veeken, J., Deroos, P., Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation (2013) Nature., 504, pp. 451-455
  • Chappert, P., Bouladoux, N., Naik, S., Schwartz, R., Specific gut commensal flora locally alters T cell tuning to endogenous ligands (2013) Immunity., 38, pp. 1198-1210
  • Duan, J., Chung, H., Troy, E., Kasper, D., Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing gamma/delta T cells (2010) Cell Host Microbe., 7, pp. 140-150
  • Ivanov, I.I., Frutos Rde, L., Manel, N., Yoshinaga, K., Rifkin, D.B., Sartor, R.B., Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine (2008) Cell Host Microbe., 4, pp. 337-349
  • Wei, B., Wingender, G., Fujiwara, D., Chen, D.Y., McPherson, M., Brewer, S., Commensal microbiota and CD8 + T cells shape the formation of invariant NKT cells (2010) J. Immunol., 184, pp. 1218-1226
  • Iida, N., Dzutsev, A., Stewart, C.A., Smith, L., Bouladoux, N., Weingarten, R.A., Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment (2013) Science., 342, pp. 967-970
  • Viaud, S., Saccheri, F., Mignot, G.G., Yamazaki, T., Daillére, R., Hannani, D., The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide (2013) Science., 342, pp. 971-976
  • Sivan, A., Corrales, L., Hubert, N., Williams, J.B., Aquino-Michaels, K., Earley, Z.M., Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy (2015) Science, 110, pp. 1084-1089
  • Vetizou, M., Pitt, J.M., Daillere, R., Lepage, P., Waldschmitt, N., Flament, C., Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota (2015) Science., 350, pp. 1079-1084
  • Rabinovich, G.A., Thijssen, V.L., Introduction to special issue: Galectins go with the flow (2014) Glycobiology., 24, p. 885
  • Thijssen, V.L., Griffioen, A.W., Galectin-1 and − 9 in angiogenesis: a sweet couple (2014) Glycobiology., 24, pp. 915-920
  • Funasaka, T., Raz, A., Nangia-Makker, P., Galectin-3 in angiogenesis and metastasis (2014) Glycobiology., 24, pp. 886-891
  • Troncoso, M.F., Ferragut, F., Bacigalupo, M.L., Cardenas Delgado, V.M., Nugnes, L.G., Gentilini, L., Galectin-8: a matricellular lectin with key roles in angiogenesis (2014) Glycobiology., 24, pp. 907-914
  • Le, Q.T., Shi, G., Cao, H., Nelson, D.W., Wang, Y., Chen, E.Y., Galectin-1: a link between tumor hypoxia and tumor immune privilege (2005) J. Clin. Oncol., 23, pp. 8932-8941
  • 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
  • Mathieu, V., de Lassalle, E.M., Toelen, J., Mohr, T., Bellahcene, A., Van Goietsenoven, G., Galectin-1 in melanoma biology and related neoangiogenesis processes (2012) J. Investig. Dermatol., 132, pp. 2245-2254
  • Carlini, M.J., Roitman, P., Nunez, M., Pallotta, M.G., Boggio, G., Smith, D., Clinical relevance of galectin-1 expression in non-small cell lung cancer patients (2014) Lung Cancer., 84, pp. 73-78
  • Rabinovich, G.A., Cumashi, A., Bianco, G.A., Ciavardelli, D., Iurisci, I., D'Egidio, M., Synthetic lactulose amines: novel class of anticancer agents that induce tumor-cell apoptosis and inhibit galectin-mediated homotypic cell aggregation and endothelial cell morphogenesis (2006) Glycobiology., 16, pp. 210-220
  • Tejler, J., Tullberg, E., Frejd, T., Leffler, H., Nilsson, U.J., Synthesis of multivalent lactose derivatives by 1,3-dipolar cycloadditions: selective galectin-1 inhibition (2006) Carbohydr. Res., 341, pp. 1353-1362
  • Giguere, D., Bonin, M.A., Cloutier, P., Patnam, R., St-Pierre, C., Sato, S., Roy, R., Synthesis of stable and selective inhibitors of human galectins-1 and -3 (2008) Bioorg. Med. Chem., 16, pp. 7811-7723
  • Iurisci, I., Cumashi, A., Sherman, A.A., Tsvetkov, Y.E., Tinari, N., Piccolo, E., Consorzio Interuniversitario Nazionale Per la, B.-O., Synthetic inhibitors of galectin-1 and -3 selectively modulate homotypic cell aggregation and tumor cell apoptosis (2009) Anticancer Res., 29, pp. 403-410
  • Stannard, K.A., Collins, P.M., Ito, K., Sullivan, E.M., Scott, S.A., Gabutero, E., Darren Grice, I., Ralph, S.J., Galectin inhibitory disaccharides promote tumour immunity in a breast cancer model (2010) Cancer Lett., 299, pp. 95-110
  • Thijssen, V.L., Postel, R., Brandwijk, R.J., Dings, R.P., Nesmelova, I., Satijn, S., Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy (2006) Proc. Natl. Acad. Sci. U. S. A., 103, pp. 15975-15980
  • Dings, R.P., Miller, M.C., Nesmelova, I., Astorgues-Xerri, L., Kumar, N., Serova, M., Antitumor agent calixarene 0118 targets human galectin-1 as an allosteric inhibitor of carbohydrate binding (2012) J. Med. Chem., 55, pp. 5121-5129
  • Dings, R.P., Kumar, N., Miller, M.C., Loren, M., Rangwala, H., Hoye, T.R., Mayo, K.H., Structure-based optimization of angiostatic agent 6DBF7, an allosteric antagonist of galectin-1 (2013) J. Pharmacol. Exp. Ther., 344, pp. 589-599
  • Astorgues-Xerri, L., Riveiro, M.E., Tijeras-Raballand, A., Serova, M., Rabinovich, G.A., Bieche, I., OTX008, a selective small-molecule inhibitor of galectin-1, downregulates cancer cell proliferation, invasion and tumour angiogenesis (2014) Eur. J. Cancer., 50, pp. 2463-2477
  • Nangia-Makker, P., Hogan, V., Honjo, Y., Baccarini, S., Tait, L., Bresalier, R., Raz, A., Inhibition of human cancer cell growth and metastasis in nude mice by oral intake of modified citrus pectin (2002) J. Natl. Cancer Inst., 94, pp. 1854-1862

Citas:

---------- APA ----------
Rabinovich, G.A. & Conejo-García, J.R. (2016) . Shaping the Immune Landscape in Cancer by Galectin-Driven Regulatory Pathways. Journal of Molecular Biology, 428(16), 3266-3281.
http://dx.doi.org/10.1016/j.jmb.2016.03.021
---------- CHICAGO ----------
Rabinovich, G.A., Conejo-García, J.R. "Shaping the Immune Landscape in Cancer by Galectin-Driven Regulatory Pathways" . Journal of Molecular Biology 428, no. 16 (2016) : 3266-3281.
http://dx.doi.org/10.1016/j.jmb.2016.03.021
---------- MLA ----------
Rabinovich, G.A., Conejo-García, J.R. "Shaping the Immune Landscape in Cancer by Galectin-Driven Regulatory Pathways" . Journal of Molecular Biology, vol. 428, no. 16, 2016, pp. 3266-3281.
http://dx.doi.org/10.1016/j.jmb.2016.03.021
---------- VANCOUVER ----------
Rabinovich, G.A., Conejo-García, J.R. Shaping the Immune Landscape in Cancer by Galectin-Driven Regulatory Pathways. J. Mol. Biol. 2016;428(16):3266-3281.
http://dx.doi.org/10.1016/j.jmb.2016.03.021