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Galectins and their ligands: negative regulators of anti-tumor immunity

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Abstract

Cytotoxic CD8+ T cells are major players of anti-tumor immune responses, as their functional activity can limit tumor growth and progression. Data show that cytotoxic T cells efficiently control the proliferation of tumor cells through major histocompatibility complex class I-mediated mechanisms; nevertheless, the presence of tumor-infiltrating CD8+ T cells in lesional tissue does not always correlate with better prognosis and increased survival of cancer patients. Similarly, adoptive transfer of tumor-specific cytotoxic T cells has only shown marginal improvement in life spans of patients with metastatic disease. In this report, we discuss experimental evidence showing that expression of tumor-derived galectins, galectin (Gal)-1, Gal-3 and Gal-9, and concomitant presence of their ligands on the surface of anti-tumor immunocytes directly compromise anti-tumor CD8+ T cell immune responses and, perhaps, undermine the promise of adoptive CD8+ T cell immunotherapy. Furthermore, we describe novel strategies designed to counteract Gal-1-, Gal-3- and Gal-9-mediated effects and highlight their targeting potential for creating more effective anti-tumor immune responses. We believe that Gal and their ligands represent an efficacious targeted molecular paradigm that warrants clinical evaluation.

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References

  1. Liu, F.T., Rabinovich, G.A.: Galectins as modulators of tumour progression. Nat. Rev. 1, 29–41 (2005)

    Article  CAS  Google Scholar 

  2. Camby, I., Le Mercier, M., Lefranc, F., Kiss, R.: Galectin-1: a small protein with major functions. Glycobiology 11, 137R–157R (2006)

    Article  Google Scholar 

  3. Zhu, C., Anderson, A.C., Schubart, A., Xiong, H., Imitola, J., Khoury, S.J., Zheng, X.X., Strom, T.B., Kuchroo, V.K.: The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 12, 1245–1252 (2005)

    Article  Google Scholar 

  4. Dhirapong, A., Lleo, A., Leung, P., Gershwin, M.E., Liu, F.T.: The immunological potential of galectin-1 and -3. Autoimmun. Rev. 5, 360–363 (2009)

    Article  Google Scholar 

  5. Saussez, S., Glinoer, D., Chantrain, G., Pattou, F., Carnaille, B., Andre, S., Gabius, H.J., Laurent, G.: Serum galectin-1 and galectin-3 levels in benign and malignant nodular thyroid disease. Thyroid 7, 705–712 (2008)

    Article  Google Scholar 

  6. Szoke, T., Kayser, K., Baumhakel, J.D., Trojan, I., Furak, J., Tiszlavicz, L., Horvath, A., Szluha, K., Gabius, H.J., Andre, S.: Prognostic significance of endogenous adhesion/growth-regulatory lectins in lung cancer. Oncology 2, 167–174 (2005)

    Google Scholar 

  7. Liang, M.Y., Lu, Y.M., Zhang, Y., Zhang, S.L.: Serum galectin-9 in cervical cancer. Zhonghua yi xue za zhi. 39, 2783–2785 (2008)

    Google Scholar 

  8. Zhu, C., Anderson, A.C., Kuchroo, V.K.: TIM-3 and its regulatory role in immune responses. Current topics in microbiology and immunology. 1–15

  9. Rodriguez-Manzanet, R., DeKruyff, R., Kuchroo, V.K., Umetsu, D.T.: The costimulatory role of TIM molecules. Immunol. Rev. 1, 259–270 (2009)

    Article  Google Scholar 

  10. Sakuishi, K., Apetoh, L., Sullivan, J.M., Blazar, B.R., Kuchroo, V.K., Anderson, A.C.: Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J. Exp. Med. 10, 2187–2194 (2010)

    Article  Google Scholar 

  11. Zhou, Q., Munger, M.E., Veenstra, R.G., Weigel, B.J., Hirashima, M., Munn, D.H., Murphy, W.J., Azuma, M., Anderson, A.C., Kuchroo, V.K., et al.: Coexpression of Tim-3 and PD-1 identifies a CD8+ T-cell exhaustion phenotype in mice with disseminated acute myelogenous leukemia. Blood 17, 4501–4510 (2011)

    Article  Google Scholar 

  12. 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. Nat. Immunol. 9, 981–991 (2009)

    Article  Google Scholar 

  13. Demotte, N., Wieers, G., Van Der Smissen, P., Moser, M., Schmidt, C., Thielemans, K., Squifflet, J.L., Weynand, B., Carrasco, J., Lurquin, C., et al.: A galectin-3 ligand corrects the impaired function of human CD4 and CD8 tumor-infiltrating lymphocytes and favors tumor rejection in mice. Cancer Res. 19, 7476–7488 (2010)

    Article  Google Scholar 

  14. Lopez-Lucendo, M.F., Solis, D., Andre, S., Hirabayashi, J., Kasai, K., Kaltner, H., Gabius, H.J., Romero, A.: Growth-regulatory human galectin-1: crystallographic characterisation of the structural changes induced by single-site mutations and their impact on the thermodynamics of ligand binding. J. Mol. Biol. 4, 957–970 (2004)

    Article  Google Scholar 

  15. Nickel, W.: Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 8, 607–614 (2005)

    Article  Google Scholar 

  16. Paz, A., Haklai, R., Elad-Sfadia, G., Ballan, E., Kloog, Y.: Galectin-1 binds oncogenic H-Ras to mediate Ras membrane anchorage and cell transformation. Oncogene 51, 7486–7493 (2001)

    Article  Google Scholar 

  17. Leppanen, A., Stowell, S., Blixt, O., Cummings, R.D.: Dimeric galectin-1 binds with high affinity to alpha2,3-sialylated and non-sialylated terminal N-acetyllactosamine units on surface-bound extended glycans. J. Biol. Chem. 7, 5549–5562 (2005)

    Google Scholar 

  18. Perillo, N.L., Pace, K.E., Seilhamer, J.J., Baum, L.G.: Apoptosis of T cells mediated by galectin-1. Nature 6558, 736–739 (1995)

    Article  Google Scholar 

  19. Cedeno-Laurent, F., Dimitroff, C.J.: Galectin-1 research in T cell immunity: past, present and future. Clin. Immunol. 2, 107–116 (2012)

    Article  Google Scholar 

  20. Jung, E.J., Moon, H.G., Cho, B.I., Jeong, C.Y., Joo, Y.T., Lee, Y.J., Hong, S.C., Choi, S.K., Ha, W.S., Kim, J.W., et al.: Galectin-1 expression in cancer-associated stromal cells correlates tumor invasiveness and tumor progression in breast cancer. Int. J. Cancer 11, 2331–2338 (2007)

    Article  Google Scholar 

  21. Nagy, N., Legendre, H., Engels, O., Andre, S., Kaltner, H., Wasano, K., Zick, Y., Pector, J.C., Decaestecker, C., Gabius, H.J., et al.: Refined prognostic evaluation in colon carcinoma using immunohistochemical galectin fingerprinting. Cancer 8, 1849–1858 (2003)

    Article  Google Scholar 

  22. Rubinstein, N., Alvarez, M., Zwirner, N.W., Toscano, M.A., Ilarregui, J.M., Bravo, A., Mordoh, J., Fainboim, L., Podhajcer, O.L., 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. Cancer Cell. 3, 241–251 (2004)

    Article  Google Scholar 

  23. 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. Eur. J. Immunol. 11, 3015–3027 (2008)

    Article  Google Scholar 

  24. van der Leij, J., van den Berg, A., Harms, G., Eschbach, H., Vos, H., Zwiers, P., van Weeghel, R., Groen, H., Poppema, S., Visser, L.: Strongly enhanced IL-10 production using stable galectin-1 homodimers. Mol. Immunol. 4, 506–513 (2007)

    Article  Google Scholar 

  25. Juszczynski, P., Ouyang, J., Monti, S., Rodig, S.J., Takeyama, K., Abramson, J., Chen, W., Kutok, J.L., Rabinovich, G.A., Shipp, M.A.: The AP1-dependent secretion of galectin-1 by Reed Sternberg cells fosters immune privilege in classical Hodgkin lymphoma. Proc. Natl. Acad. Sci. U. S. A. 32, 13134–13139 (2007)

    Article  Google Scholar 

  26. 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. J. Immunol. 7, 3127–3137 (2012)

    Article  Google Scholar 

  27. Cedeno-Laurent, F., Opperman, M.J., Barthel, S.R., Hays, D., Schatton, T., Zhan, Q., He, X., Matta, K.L., Supko, J.G., Frank, M.H., et al.: Metabolic inhibition of galectin-1-binding carbohydrates accentuates antitumor immunity. J. Investig. Dermatol. 2, 410–420 (2012)

    Article  Google Scholar 

  28. Zacarias Fluck, M.F., Hess, L., Salatino, M., Croci, D.O., Stupirski, J.C., Di Masso, R.J., Roggero, E., Rabinovich, G.A., Scharovsky, O.G.: The aggressiveness of murine lymphomas selected in vivo by growth rate correlates with galectin-1 expression and response to cyclophosphamide. Cancer Immunol. Immunother (2011)

  29. Banh, A., Zhang, J., Cao, H., Bouley, D.M., Kwok, S., Kong, C., Giaccia, A.J., Koong, A.C., Le, Q.T.: Tumor Galectin-1 Mediates Tumor Growth and Metastasis through Regulation of T-Cell Apoptosis. Cancer Res. 13, 4423–4431 (2011)

    Article  Google Scholar 

  30. Tang, D., Yuan, Z., Xue, X., Lu, Z., Zhang, Y., Wang, H., Chen, M., An, Y., Wei, J., Zhu, Y., et al.: High expression of Galectin-1 in pancreatic stellate cells plays a role in the development and maintenance of an immunosuppressive microenvironment in pancreatic cancer. International journal of cancer. (2011).

  31. 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. Int. J. Cancer (2011)

  32. Dumic, J., Dabelic, S., Flogel, M.: Galectin-3: an open-ended story. Biochim. Biophys. Acta 4, 616–635 (2006)

    Article  Google Scholar 

  33. Raz, A., Pazerini, G., Carmi, P.: Identification of the metastasis-associated, galactoside-binding lectin as a chimeric gene product with homology to an IgE-binding protein. Cancer Res. 13, 3489–3493 (1989)

    Google Scholar 

  34. Varki, A., Cummings, R., Esko, J.D.: Essentials of Glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press, New York (2009)

    Google Scholar 

  35. Akahani, S., Nangia-Makker, P., Inohara, H., Kim, H.R., Raz, A.: Galectin-3: a novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res. 23, 5272–5276 (1997)

    Google Scholar 

  36. Bi, S., Earl, L.A., Jacobs, L., Baum, L.G.: Structural features of galectin-9 and galectin-1 that determine distinct T cell death pathways. J. Biol. Chem. 18, 12248–12258 (2008)

    Article  Google Scholar 

  37. Yu, F., Finley Jr., R.L., Raz, A., Kim, H.R.: Galectin-3 translocates to the perinuclear membranes and inhibits cytochrome c release from the mitochondria. A role for synexin in galectin-3 translocation. J. Biol. Chem. 18, 15819–15827 (2002)

    Article  Google Scholar 

  38. Yang, R.Y., Hsu, D.K., Liu, F.T.: Expression of galectin-3 modulates T-cell growth and apoptosis. Proc. Natl. Acad. Sci. U. S. A. 13, 6737–6742 (1996)

    Article  Google Scholar 

  39. 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. J. Biol. Chem. 33, 34922–34930 (2004)

    Article  Google Scholar 

  40. Davidson, P.J., Davis, M.J., Patterson, R.J., Ripoche, M.A., Poirier, F., Wang, J.L.: Shuttling of galectin-3 between the nucleus and cytoplasm. Glycobiology 5, 329–337 (2002)

    Article  Google Scholar 

  41. Park, J.W., Voss, P.G., Grabski, S., Wang, J.L., Patterson, R.J.: Association of galectin-1 and galectin-3 with Gemin4 in complexes containing the SMN protein. Nucleic Acids Res. 17, 3595–3602 (2001)

    Article  Google Scholar 

  42. Morris, S., Ahmad, N., Andre, S., Kaltner, H., Gabius, H.J., Brenowitz, M., Brewer, F.: Quaternary solution structures of galectins-1, -3, and −7. Glycobiology 3, 293–300 (2004)

    Google Scholar 

  43. Fukumori, T., Takenaka, Y., Yoshii, T., Kim, H.R., Hogan, V., Inohara, H., Kagawa, S., Raz, A.: CD29 and CD7 mediate galectin-3-induced type II T-cell apoptosis. Cancer Res. 23, 8302–8311 (2003)

    Google Scholar 

  44. 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. J. Immunol. 2, 778–789 (2006)

    Google Scholar 

  45. Liu, T.Y., Chen, C.Y., Tien, H.F., Lin, C.W.: Loss of CD7, independent of galectin-3 expression, implies a worse prognosis in adult T-cell leukaemia/lymphoma. Histopathology 2, 214–220 (2009)

    Article  Google Scholar 

  46. Rappl, G., Abken, H., Muche, J.M., Sterry, W., Tilgen, W., Andre, S., Kaltner, H., Ugurel, S., Gabius, H.J., Reinhold, U.: CD4+CD7- leukemic T cells from patients with Sezary syndrome are protected from galectin-1-triggered T cell death. Leukemia 5, 840–845 (2002)

    Article  Google Scholar 

  47. Iurisci, I., Tinari, N., Natoli, C., Angelucci, D., Cianchetti, E., Iacobelli, S.: Concentrations of galectin-3 in the sera of normal controls and cancer patients. Clin. Cancer Res. 4, 1389–1393 (2000)

    Google Scholar 

  48. van den Brule, F., Califice, S., Castronovo, V.: Expression of galectins in cancer: a critical review. Glycoconj. J. 7–9, 537–542 (2004)

    Google Scholar 

  49. Newlaczyl, A.U., Yu, L.G.: Galectin-3 - A jack-of-all-trades in cancer. Cancer Lett. 2, 123–128 (2011)

    Article  Google Scholar 

  50. Byrd, J.C., Bresalier, R.S.: Mucins and mucin binding proteins in colorectal cancer. Cancer Metastasis Rev. 1–2, 77–99 (2004)

    Article  Google Scholar 

  51. Peng, W., Wang, H.Y., Miyahara, Y., Peng, G., Wang, R.F.: Tumor-associated galectin-3 modulates the function of tumor-reactive T cells. Cancer Res. 17, 7228–7236 (2008)

    Article  Google Scholar 

  52. Radosavljevic, G., Jovanovic, I., Majstorovic, I., Mitrovic, M., Lisnic, V.J., Arsenijevic, N., Jonjic, S., Lukic, M.L.: Deletion of galectin-3 in the host attenuates metastasis of murine melanoma by modulating tumor adhesion and NK cell activity. Clin. Exp. Metastasis 5, 451–462 (2011)

    Article  Google Scholar 

  53. Wei, J., Barr, J., Kong, L.Y., Wang, Y., Wu, A., Sharma, A.K., Gumin, J., Henry, V., Colman, H., Sawaya, R., et al.: Glioma-associated cancer-initiating cells induce immunosuppression. Clin. Cancer Res. 2, 461–473 (2010)

    Article  Google Scholar 

  54. Tsuboi, S., Sutoh, M., Hatakeyama, S., Hiraoka, N., Habuchi, T., Horikawa, Y., Hashimoto, Y., Yoneyama, T., Mori, K., Koie, T., et al.: A novel strategy for evasion of NK cell immunity by tumours expressing core2 O-glycans. EMBO J. 15, 3173–3185 (2011)

    Article  Google Scholar 

  55. Dunphy, J.L., Barcham, G.J., Bischof, R.J., Young, A.R., Nash, A., Meeusen, E.N.: Isolation and characterization of a novel eosinophil-specific galectin released into the lungs in response to allergen challenge. J. Biol. Chem. 17, 14916–14924 (2002)

    Article  Google Scholar 

  56. Matsumoto, R., Matsumoto, H., Seki, M., Hata, M., Asano, Y., Kanegasaki, S., Stevens, R.L., Hirashima, M.: Human ecalectin, a variant of human galectin-9, is a novel eosinophil chemoattractant produced by T lymphocytes. J. Biol. Chem. 27, 16976–16984 (1998)

    Article  Google Scholar 

  57. Hirashima M: Ecalectin/galectin-9, a novel eosinophil chemoattractant: its function and production. Int. Arch Allergy Immunol. 6–9 (2000)

  58. Elahi S, Dinges WL, Lejarcegui N, Laing KJ, Collier AC, Koelle DM, McElrath MJ, Horton H: Protective HIV-specific CD8+ T cells evade Treg cell suppression. Nat. Med. 8, 989–995

  59. Imaizumi, T., Kumagai, M., Sasaki, N., Kurotaki, H., Mori, F., Seki, M., Nishi, N., Fujimoto, K., Tanji, K., Shibata, T., et al.: Interferon-gamma stimulates the expression of galectin-9 in cultured human endothelial cells. J. Leukoc. Biol. 3, 486–491 (2002)

    Google Scholar 

  60. Oikawa, T., Kamimura, Y., Akiba, H., Yagita, H., Okumura, K., Takahashi, H., Zeniya, M., Tajiri, H., Azuma, M.: Preferential involvement of Tim-3 in the regulation of hepatic CD8+ T cells in murine acute graft-versus-host disease. J. Immunol. 7, 4281–4287 (2006)

    Google Scholar 

  61. Seki, M., Oomizu, S., Sakata, K.M., Sakata, A., Arikawa, T., Watanabe, K., Ito, K., Takeshita, K., Niki, T., Saita, N., et al.: Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clinical immunology (Orlando, Fla. 1, 78–88 (2008).

    Google Scholar 

  62. McMahan, R.H., Golden-Mason, L., Nishimura, M.I., McMahon, B.J., Kemper, M., Allen, T.M., Gretch, D.R., Rosen, H.R.: Tim-3 expression on PD-1+ HCV-specific human CTLs is associated with viral persistence, and its blockade restores hepatocyte-directed in vitro cytotoxicity. J. Clin. Investigation 12, 4546–4557

  63. Ngiow, S.F., von Scheidt, B., Akiba, H., Yagita, H., Teng, M.W., Smyth, M.J.: Anti-TIM3 antibody promotes T cell IFN-gamma-mediated antitumor immunity and suppresses established tumors. Cancer Res. 10, 3540–3551

  64. Fourcade, J., Sun, Z., Benallaoua, M., Guillaume, P., Luescher, I.F., Sander, C., Kirkwood, M., Kuchroo, V., Zarour, H.M.: Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J. Exp. Med. 10, 2175–2186

  65. Ouyang, J., Juszczynski, P., Rodig, S.J., Green, M.R., O’Donnell, E., Currie, T., Armant, M., Takeyama, K., Monti, S., Rabinovich, G.A., et al.: Viral induction and targeted inhibition of galectin-1 in EBV+posttransplant lymphoproliferative disorders. Blood 16, 4315–4322 (2011)

    Article  Google Scholar 

  66. Klibi, J., Niki, T., Riedel, A., Pioche-Durieu, C., Souquere, S., Rubinstein, E., Le Moulec, S., Guigay, J., Hirashima, M., Guemira, F., et al.: Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood 9, 1957–1966 (2009)

    Article  Google Scholar 

  67. Stannard, K.A., Collins, P.M., Ito, K., Sullivan, E.M., Scott, S.A., Gabutero, E., Darren Grice, I., Low, P., Nilsson, U.J., Leffler, H., et al.: Galectin inhibitory disaccharides promote tumour immunity in a breast cancer model. Cancer Lett. 2, 95–110 (2010)

    Article  Google Scholar 

  68. 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. Angiogenesis. (2011)

  69. 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. Bioorg. Med. Chem. 16, 7811–7823 (2008)

    Article  PubMed  CAS  Google Scholar 

  70. Rabinovich, G.A., Cumashi, A., Bianco, G.A., Ciavardelli, D., Iurisci, I., D’Egidio, M., Piccolo, E., Tinari, N., Nifantiev, N., Iacobelli, S.: Synthetic lactulose amines: novel class of anticancer agents that induce tumor-cell apoptosis and inhibit galectin-mediated homotypic cell aggregation and endothelial cell morphogenesis. Glycobiology 3, 210–220 (2006)

    Google Scholar 

  71. Barthel, S.R., Antonopoulos, A., Cedeno-Laurent, F., Schaffer, L., Hernandez, G., Patil, S.A., North, S.J., Dell, A., Matta, K.L., Neelamegham, S., et al.: Peracetylated 4-fluoro-glucosamine reduces the content and repertoire of N- and O-glycans without direct incorporation. J. Biol. Chem. 24, 21717–21731 (2011)

    Article  Google Scholar 

  72. Woynarowska, B., Skrincosky, D.M., Haag, A., Sharma, M., Matta, K., Bernacki, R.J.: Inhibition of lectin-mediated ovarian tumor cell adhesion by sugar analogs. J. Biol. Chem. 36, 22797–22803 (1994)

    Google Scholar 

  73. Yan, Y.P., Lang, B.T., Vemuganti, R., Dempsey, R.J.: Galectin-3 mediates post-ischemic tissue remodeling. Brain research. 116–124 (2009)

  74. Pace, K.E., Hahn, H.P., Pang, M., Nguyen, J.T., Baum, L.G.: CD7 delivers a pro-apoptotic signal during galectin-1-induced T cell death. J. Immunol. 5, 2331–2334 (2000)

    Google Scholar 

  75. 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. J. Biol. Chem. 9, 7469–7475 (2003)

    Article  Google Scholar 

  76. 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. J. Immunol. 5, 3091–3102 (2008)

    Google Scholar 

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  1. Department of Dermatology, Brigham and Women’s Hospital, HIM, Rm. 662, 77 Avenue Louis Pasteur, Boston, MA, 02115, USA

    Filiberto Cedeno-Laurent & Charles J. Dimitroff

  2. Harvard Medical School, Boston, MA, 02115, USA

    Filiberto Cedeno-Laurent & Charles J. Dimitroff

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Cedeno-Laurent, F., Dimitroff, C.J. Galectins and their ligands: negative regulators of anti-tumor immunity. Glycoconj J 29, 619–625 (2012). https://doi.org/10.1007/s10719-012-9379-0

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