Targeting galectin-1 overcomes breast cancer-associated immunosuppression and prevents metastatic disease

Cancer Research

Volumn 73, Issue 3, 2013, Pages 1107-1117

  Dalotto Moreno, Tomás ^a   Croci, Diego O ^a   Cerliani, Juan P ^a   Martinez Allo, Verónica C ^a   Dergan Dylon, Sebastián ^a   Méndez Huergo, Santiago P ^a   Stupirski, Juan C ^a   Mazal, Daniel ^c   Osinaga, Eduardo ^d   Toscano, Marta A ^a   Sundblad, Victoria ^a   Rabinovich, Gabriel A ^a,b   Salatino, Mariana ^a,e  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Centro Hospitalario Pereira Rossell   (Uruguay)

^d DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^e INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST BIOPSY; BREAST CANCER; BREAST HYPERPLASIA; CANCER GRADING; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; IMMUNE DEFICIENCY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; LYMPHOCYTE FUNCTION; MALE; METASTASIS INHIBITION; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REGULATORY T LYMPHOCYTE; SPLEEN; TUMOR GROWTH; UPREGULATION; WILD TYPE;

ANIMALS; BREAST NEOPLASMS; FEMALE; GALECTIN 1; IMMUNE TOLERANCE; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; T-LYMPHOCYTES, REGULATORY;

EID: 84873449312     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-2418     Document Type: Article

References (50)

1. Ruffell B, DeNardo DG, Affara NI, Coussens LM. Lymphocytes in cancer development: polarization towards pro-tumor immunity. Cytokine Growth Factor Rev 2010;21:3-10.
2. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565-70.
3. Rabinovich GA, Croci DO. Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer. Immunity 2012;36: 322-35.
4. Liu FT, Rabinovich GA. Galectins as modulators of tumour progression. Nat Rev Cancer 2005;5:29-41.
5. Salatino M, Rabinovich GA. Fine-tuning antitumor responses through the control of galectin-glycan interactions: an overview. Meth Mol Biol 2011;677:355-74.
6. Thijssen VL, Barkan B, Shoji H, Aries IM, Mathieu V, Deltour L, et al. Tumor cells secrete galectin-1 to enhance endothelial cell activity. Cancer Res 2010;70:6216-24.
7. Rotblat B, Niv H, Andre S, Kaltner H, Gabius HJ, Kloog Y. Galectin-1 (L11A) predicted from a computed galectin-1 farnesyl-binding pocket selectively inhibits Ras-GTP. Cancer Res 2004;64:3112-8.
8. Salatino M, Croci DO, Bianco GA, Ilarregui JM, Toscano MA, Rabinovich GA. Galectin-1 as a potential therapeutic target in autoimmune disorders and cancer. Expert Opin Biol Ther 2008;8:45-57.
9. Rubinstein N, Alvarez M, Zwirner NW, Toscano MA, Ilarregui JM, Bravo A, et al. 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 2004;5:241-51.
10. Banh A, Zhang J, Cao H, Bouley DM, Kwok S, Kong C, et al. Tumor galectin-1 mediates tumor growth and metastasis through regulation of T-cell apoptosis. Cancer Res 2011;71:4423-31.
11. Kuo PL, Huang MS, Cheng DE, Hung JY, Yang CJ, Chou SH. Lung cancer-derived galectin-1 enhances tumorigenic potentiation of tumor-associated dendritic cells by expressing heparin-binding EGF-like growth factor. J Biol Chem 2012;287:9753-64.
12. Juszczynski P, Ouyang J, Monti S, Rodig SJ, Takeyama K, Abramson J, et al. 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 2007;104:13134-9.
13. Gandhi MK, Moll G, Smith C, Dua U, Lambley E, Ramuz O, et al. Galectin-1 mediated suppression of Epstein-Barr virus specific T-cell immunity in classic Hodgkin lymphoma. Blood 2007;110: 1326-9.
14. Soldati R, Berger E, Zenclussen AC, Jorch G, Lode HN, Salatino M, et al. Neuroblastoma triggers an immunoevasive program involving galectin-1-dependent modulation of T cell and dendritic cell compartments. Int J Cancer 2012;131:1131-41.
15. Le QT, Shi G, Cao H, Nelson DW, Wang Y, Chen EY, et al. Galectin-1: a link between tumor hypoxia and tumor immune privilege. J Clin Oncol 2005;23:8932-41.
16. Tang D, Yuan Z, Xue X, Lu Z, Zhang Y, Wang H, 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. Int J Cancer 2012;130: 2337-48.
17. Kovacs-Solyom F, Blasko A, Fajka-Boja R, Katona RL, Vegh L, Novak J, et al. Mechanism of tumor cell-induced T-cell apoptosis mediated by galectin-1. Immunol Lett 2010;127:108-18.
18. Cedeno-Laurent F, Watanabe R, Teague JE, Kupper TS, Clark RA, Dimitroff CJ. Galectin-1 inhibits the viability, proliferation, and Th1 cytokine production of nonmalignant T cells in patients with leukemic cutaneous T-cell lymphoma. Blood 2012;119:3534-8.
19. Kreunin P, Yoo C, Urquidi V, Lubman DM, Goodison S. Proteomic profiling identifies breast tumor metastasis-associated factors in an isogenic model. Proteomics 2007;7:299-312.
20. Xu SG, Yan PJ, Shao ZM. Differential proteomic analysis of a highly metastatic variant of human breast cancer cells using two-dimensional differential gel electrophoresis. J Cancer Res Clin Oncol 2010; 136:1545-56.
21. Jung EJ, Moon HG, Cho BI, Jeong CY, Joo YT, Lee YJ, et al. Galectin-1 expression in cancer-associated stromal cells correlates tumor invasiveness and tumor progression in breast cancer. Int J Cancer 2007;120:2331-8.
22. Toscano MA, Bianco GA, Ilarregui JM, Croci DO, Correale J, Hernandez JD, et al. Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat Immunol 2007;8:825-34.
23. Toscano MA, Commodaro AG, Ilarregui JM, Bianco GA, Liberman A, Serra HM, et al. Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2- and T regulatory-mediated anti-inflammatory responses. J Immunol 2006;176:6323-32.
24. He J, Baum LG. Endothelial cell expression of galectin-1 induced by prostate cancer cells inhibits T-cell transendothelial migration. Lab Invest 2006;86:578-90.
25. Norling LV, Sampaio AL, Cooper D, Perretti M. Inhibitory control of endothelial galectin-1 on in vitro and in vivo lymphocyte trafficking. FASEB J 2008;22:682-90.
26. Ilarregui JM, Croci DO, Bianco GA, Toscano MA, Salatino M, Vermeulen ME, et al. Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat Immunol 2009;10:981-91.
27. Cedeno-Laurent F, Opperman M, Barthel SR, Kuchroo VK, Dimitroff CJ. Galectin-1 triggers an immunoregulatory signature in Th cells functionally defined by IL-10 expression. J Immunol 2012;188: 3127-37.
28. + T cells to block their TCR-mediated ERK activity and proliferation. Brain Behav Immun 2009;23:1028-37.
29. Garin MI, Chu CC, Golshayan D, Cernuda-Morollon E, Wait R, Lechler RI. Galectin-1: a key effector of regulation mediated by CD4+CD25+T cells. Blood 2007;109:2058-65.
30. Pulaski BA, Ostrand-Rosenberg S. Mouse 4T1 breast tumor model. Curr Prot Immunol 2001;20:20.
31. Yamaguchi T, Hirota K, Nagahama K, Ohkawa K, Takahashi T, Nomura T, et al. Control of immune responses by antigen-specific regulatory T cells expressing the folate receptor. Immunity 2007;27:145-59.
32. Croci D, Salatino M, Rubinstein N, Cerliani JP, Cavallin LE, Howard JL, et al. Disrupting galectin-1 interactions with Nglycans suppresses hypoxia-driven angiogenesis and tumorigenesis in Kaposi's sarcoma. J Exp Med 2012;209:1985-2000.
33. Olkhanud PB, Baatar D, Bodogai M, Hakim F, Gress R, Anderson RL, et al. Breast cancer lung metastasis requires expression of chemokine receptor CCR4 and regulatory T cells. Cancer Res 2009;69:5996-6004.
34. Pedroza-Gonzalez A, Xu K, Wu TC, Aspord C, Tindle S, Marches F, et al. Thymic stromal lymphopoietin fosters human breast tumor growth by promoting type 2 inflammation. J Exp Med 2011; 208:479-90.
35. Danna EA, Sinha P, Gilbert M, Clements VK, Pulaski BA, Ostrand-Rosenberg S. Surgical removal of primary tumor reverses tumorinduced immunosuppression despite the presence of metastatic disease. Cancer Res 2004;64:2205-11.
36. Olkhanud PB, Damdinsuren B, Bodogai M, Gress RE, Sen R, Wejksza K, et al. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4(+) T cells to T-regulatory cells. Cancer Res 2011;71:3505-15.
37. Chuck MI, Zhu M, Shen S, Zhang W. The role of the LAT-PLC-gamma1 interaction in T regulatory cell function. J Immunol 2010;184:2476-86.
38. Shen S, Chuck MI, Zhu M, Fuller DM, Yang CW, Zhang W. The importance of LAT in the activation, homeostasis, and regulatory function of T cells. J Biol Chem 2010;285:35393-405.
39. Croci DO, Salatino M. Tumor immune escape mechanisms that operate during metastasis. Curr Pharm Biotechnol 2011;12:1923-36.
40. Ito K, Ralph SJ. Inhibiting galectin-1 reduces murine lung metastasis with increased CD4(+) and CD8 (+) T cells and reduced cancer cell adherence. Clin Exp Metastasis 2012;29:561-72.
41. Ito K, Scott SA, Cutler S, Dong LF, Neuzil J, Blanchard H, et al. Thiodigalactoside inhibits murine cancers by concurrently blocking effects of galectin-1 on immune dysregulation, angiogenesis and protection against oxidative stress. Angiogenesis 2011;14: 293-307.
42. Daroqui CM, Ilarregui JM, Rubinstein N, Salatino M, Toscano MA, Vazquez P, et al. Regulation of galectin-1 expression by transforming growth factor beta1 in metastatic mammary adenocarcinoma cells: implications for tumor-immune escape. Cancer Immunol Immunother 2007;56:491-9.
43. Gromov P, Gromova I, Bunkenborg J, Cabezon T, Moreira JM, Timmermans-Wielenga V, et al. Up-regulated proteins in the fluid bathing the tumour cell microenvironment as potential serological markers for early detection of cancer of the breast. Mol Oncol 2010;4:65-89.
44. Zhang W, Sommers CL, Burshtyn DN, Stebbins CC, DeJarnette JB, Trible RP, et al. Essential role of LAT in T cell development. Immunity 1999;10:323-32.
45. Sommers CL, Park CS, Lee J, Feng C, Fuller CL, Grinberg A, et al. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science 2002;296:2040-3.
46. Aguado E, Richelme S, Nunez-Cruz S, Miazek A, Mura AM, Richelme M, et al. Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science 2002;296:2036-40.
47. Koonpaew S, Shen S, Flowers L, Zhang W. LAT-mediated signaling in CD4+CD25+ regulatory T cell development. J Exp Med 2006;203: 119-29.
48. Chung CD, Patel VP, Moran M, Lewis LA, Miceli MC. Galectin-1 induces partial TCR zeta-chain phosphorylation and antagonizes processive TCR signal transduction. J Immunol 2000;165: 3722-9.
49. Stannard KA, Collins PM, Ito K, Sullivan EM, Scott SA, Gabutero E, et al. Galectin inhibitory disaccharides promote tumour immunity in a breast cancer model. Cancer Lett 2010;299:95-110.
50. Delaine T, Cumpstey I, Ingrassia L, Le Mercier M, Okechukwu P, Leffler H, et al. Galectin-inhibitory thiodigalactoside ester derivatives have antimigratory effects in cultured lung and prostate cancer cells. J Med Chem 2008;51:8109-14.