Abstract:
Galectins, a family of glycan-binding proteins, influence tumor progression by modulating interactions between tumor, endothelial, stromal, and immune cells. Despite considerable progress in identifying the roles of individual galectins in tumor biology, an integrated portrait of the galectin network in different tumor microenvironments is still missing. We undertook this study to analyze the "galectin signature" of the human prostate cancer microenvironment with the overarching goal of selecting novel-molecular targets for prognostic and therapeutic purposes. In examining androgen-responsive and castration-resistant prostate cancer cells and primary tumors representing different stages of the disease, we found that galectin-1 (Gal-1) was the most abundantly expressed galectin in prostate cancer tissue and was markedly upregulated during disease progression. In contrast, all other galectins were expressed at lower levels: Gal-3, -4, -9, and -12 were downregulated during disease evolution, whereas expression of Gal-8 was unchanged. Given the prominent regulation of Gal-1 during prostate cancer progression and its predominant localization at the tumor-vascular interface, we analyzed the potential role of this endogenous lectin in prostate cancer angiogenesis. In human prostate cancer tissue arrays, Gal-1 expression correlated with the presence of blood vessels, particularly in advanced stages of the disease. Silencing Gal-1 in prostate cancer cells reduced tumor vascularization without altering expression of other angiogenesis-related genes. Collectively, our findings identify a dynamically regulated "galectin-specific signature" that accompanies disease evolution in prostate cancer, and they highlight a major role for Gal-1 as a tractable target for antiangiogenic therapy in advanced stages of the disease. ©2012 AACR.
Registro:
Documento: |
Artículo
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Título: | A unique galectin signature in human prostate cancer progression suggests galectin-1 as a key target for treatment of advanced disease |
Autor: | Laderach, D.J.; Gentilini, L.D.; Giribaldi, L.; Delgado, V.C.; Nugnes, L.; Croci, D.O.; Al Nakouzi, N.; Sacca, P.; Casas, G.; Mazza, O.; Shipp, M.A.; Vazquez, E.; Chauchereau, A.; Kutok, J.L.; Rodig, S.J.; Elola, M.T.; Compagno, D.; Rabinovich, G.A. |
Filiación: | Laboratorio de Glicómica Estructural y Funcional, IQUIBICEN-CONICET, UBA, C1428, Ciudad de Buenos Aires, Argentina Apoptosis y Cancer, IQUIBICEN-CONICET, Universidad de Buenos Aires, Argentina Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental (IBYME-CONICET), Argentina Instituto de Química y Fisicoquímica Biológicas (IQUIFIB, CONICET), Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Argentina División Anatomía Patológica, Hospital Alemán, Argentina División Urología, Hospital Nacional de Clínicas José de San Martín, Ciudad de Buenos Aires, Argentina Institut Gustave Roussy-INSERM U981, Villejuif, France Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, United States Department of Pathology, Brigham and Women's Hospital, Boston, MA, United States Instituto de Biología y Medicina Experimental (IBYME/CONICET), C1428 Ciudad de Buenos Aires, Argentina Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental (IBYME-CONICET), Vuelta de Obligado 2490, C1428, Ciudad de Buenos Aires, Argentina
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Palabras clave: | ecalectin; galectin; galectin 1; galectin 12; galectin 3; galectin 4; galectin 8; monoclonal antibody; unclassified drug; advanced cancer; animal experiment; animal model; antiangiogenic therapy; article; cancer cell; cancer classification; cancer growth; cancer patient; cancer staging; controlled study; correlation analysis; drug targeting; enzyme activity; enzyme regulation; human; human cell; human tissue; major clinical study; male; molecular evolution; mouse; nonhuman; outcome assessment; priority journal; prostate cancer; protein expression; tumor localization; tumor vascularization; Aged; Disease Progression; Galectin 1; Humans; Immunoblotting; Immunohistochemistry; Male; Middle Aged; Molecular Targeted Therapy; Neovascularization, Pathologic; Prostatic Neoplasms; Real-Time Polymerase Chain Reaction; Reverse Transcriptase Polymerase Chain Reaction; Tissue Array Analysis; Transcriptome; Tumor Microenvironment |
Año: | 2013
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Volumen: | 73
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Número: | 1
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Página de inicio: | 86
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Página de fin: | 96
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DOI: |
http://dx.doi.org/10.1158/0008-5472.CAN-12-1260 |
Título revista: | Cancer Research
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Título revista abreviado: | Cancer Res.
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ISSN: | 00085472
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CODEN: | CNREA
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CAS: | galectin 1, 258495-34-0; galectin 3, 208128-56-7; galectin 8, 220452-97-1; Galectin 1
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Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00085472_v73_n1_p86_Laderach |
Referencias:
- Jemal, A., Bray, F., Center, M.M., Ferlay, J., Ward, E., Forman, D., Global cancer statistics (2011) CA Cancer J Clin, 61, pp. 69-90
- Logothetis, C.J., Navone, N.M., Lin, S.H., Understanding the biology of bone metastases: Key to the effective treatment of prostate cancer (2008) Clin Cancer Res, 14, pp. 1599-1602
- Denmeade, S.R., Isaacs, J.T., A history of prostate cancer treatment (2002) Nat Rev Cancer, 2, pp. 389-396
- Rillahan, C.D., Paulson, J.C., Glycan microarrays for decoding the glycome (2011) Annu Rev Biochem, 80, pp. 797-823
- Dube, D.H., Bertozzi, C.R., Glycans in cancer and inflammation - Potential for therapeutics and diagnostics (2005) Nat Rev Drug Discov, 4, pp. 477-488
- Liu, F.T., Rabinovich, G.A., Galectins as modulators of tumour progression (2005) Nat Rev Cancer, 5, pp. 29-41
- Rabinovich, G.A., Croci, D.O., Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer (2012) Immunity, 36, pp. 322-335
- Levy, R., Biran, A., Poirier, F., Raz, A., Kloog, Y., Galectin-3 mediates crosstalk between K-Ras and Let-7c tumor suppressor microRNA (2011) PLoS ONE, 6, pp. e27490
- Ellerhorst, J., Troncoso, P., Xu, X.C., Lee, J., Lotan, R., Galectin-1 and galectin-3 expression in human prostate tissue and prostate cancer (1999) Urol Res, 27, pp. 362-367
- Van Den Brule, F.A., Waltregny, D., Liu, F.T., Castronovo, V., Alteration of the cytoplasmic/nuclear expression pattern of galectin-3 correlates with prostate carcinoma progression (2000) Int J Cancer, 89, pp. 361-367
- Van Den Brule, F.A., Waltregny, D., Castronovo, V., Increased expression of galectin-1 in carcinoma-associated stroma predicts poor outcome in prostate carcinoma patients (2001) J Pathol, 193, pp. 80-87
- Valenzuela, H.F., Pace, K.E., Cabrera, P.V., White, R., Porvari, K., Kaija, H., O-glycosylation regulates LNCaP prostate cancer cell susceptibility to apoptosis induced by galectin-1 (2007) Cancer Res, 67, pp. 6155-6162
- He, J., Baum, L.G., Endothelial cell expression of galectin-1 induced by prostate cancer cells inhibits T-cell transendothelial migration (2006) Lab Invest, 86, pp. 578-590
- Ellerhorst, J.A., Stephens, L.C., Nguyen, T., Xu, X.C., Effects of galectin-3 expression on growth and tumorigenicity of the prostate cancer cell line LNCaP (2002) Prostate, 50, pp. 64-70
- Glinsky, V.V., Glinsky, G.V., Glinskii, O.V., Huxley, V.H., Turk, J.R., Mossine, V.V., Intravascular metastatic cancer cell homotypic aggregation at the sites of primary attachment to the endothelium (2003) Cancer Res, 63, pp. 3805-3811
- Clausse, N., Van Den Brule, F., Waltregny, D., Garnier, F., Castronovo, V., Galectin-1 expression in prostate tumor-associated capillary endothelial cells is increased by prostate carcinoma cells and modulates heterotypic cell-cell adhesion (1999) Angiogenesis, 3, pp. 317-325
- Fukumori, T., Oka, N., Takenaka, Y., Nangia-Makker, P., Elsamman, E., Kasai, T., Galectin-3 regulates mitochondrial stability and antiapoptotic function in response to anticancer drug in prostate cancer (2006) Cancer Res, 66, pp. 3114-3119
- Merseburger, A.S., Kramer, M.W., Hennenlotter, J., Simon, P., Knapp, J., Hartmann, J.T., Involvement of decreased Galectin-3 expression in the pathogenesis and progression of prostate cancer (2008) Prostate, 68, pp. 72-77
- Ahmed, H., Banerjee, P.P., Vasta, G.R., Differential expression of galectins in normal, benign and malignant prostate epithelial cells: Silencing of galectin-3 expression in prostate cancer by its promoter methylation (2007) Biochem Biophys Res Commun, 358, pp. 241-246
- Wang, Y., Nangia-Makker, P., Tait, L., Balan, V., Hogan, V., Pienta, K.J., Regulation of prostate cancer progression by galectin-3 (2009) Am J Pathol, 174, pp. 1515-1523
- Su, Z.Z., Lin, J., Shen, R., Fisher, P.E., Goldstein, N.I., Fisher, P.B., Surface-epitope masking and expression cloning identifies the human prostate carcinoma tumor antigen gene PCTA-1 a member of the galectin gene family (1996) Proc Natl Acad Sci U S A, 93, pp. 7252-7257
- Zick, Y., Eisenstein, M., Goren, R.A., Hadari, Y.R., Levy, Y., Ronen, D., Role of galectin-8 as a modulator of cell adhesion and cell growth (2004) Glycoconj J, 19, pp. 517-526
- Rubinstein, N., Alvarez, M., Zwirner, N.W., Toscano, M.A., Ilarregui, J.M., 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
- 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
- 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
- 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
- Compagno, D., Merle, C., Morin, A., Gilbert, C., Mathieu, J.R., Bozec, A., SIRNA-directed in vivo silencing of androgen receptor inhibits the growth of castration-resistant prostate carcinomas (2007) PLoS ONE, 2, pp. e1006
- Wiznerowicz, M., Trono, D., Conditional suppression of cellular genes: Lentivirus vector-mediated drug-inducible RNA interference (2003) J Virol, 77, pp. 8957-8961
- Gopalkrishnan, R.V., Roberts, T., Tuli, S., Kang, D., Christiansen, K.A., Fisher, P.B., Molecular characterization of prostate carcinoma tumor antigen-1, PCTA-1, a human galectin-8 related gene (2000) Oncogene, 19, pp. 4405-4416
- Le Mercier, M., Fortin, S., Mathieu, V., Roland, I., Spiegl-Kreinecker, S., Haibe-Kains, B., Galectin 1 proangiogenic and promigratory effects in the Hs683 oligodendroglioma model are partly mediated through the control of BEX2 expression (2009) Neoplasia, 11, pp. 485-496
- 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
- Karlou, M., Tzelepi, V., Efstathiou, E., Therapeutic targeting of the prostate cancer microenvironment (2010) Nat Rev Urol, 7, pp. 494-509
- 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., Chen, T.T., Xia, L., Guo, M., Xu, Y., Yue, F., Hypoxia inducible factor-1mediatesexpressionof galectin-1: Thepotential role inmigration/invasion of colorectal cancer cells (2010) Carcinogenesis, 31, pp. 1367-1375
- Ramsay, A.K., Leung, H.Y., Signalling pathways in prostate carcinogenesis: Potentials for molecular-targeted therapy (2009) Clin Sci, 117, pp. 209-228. , Lond
- 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
- Califice, S., Castronovo, V., Bracke, M., Van Den Brule, F., Dual activities of galectin-3 in human prostate cancer: Tumor suppression of nuclear galectin-3 vs tumor promotion of cytoplasmic galectin-3 (2004) Oncogene, 23, pp. 7527-7536
- Lahm, H., André, S., Hoeflich, A., Fischer, J.R., Sordat, B., Kaltner, H., 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
- Thijssen, V.L., Hulsmans, S., Griffioen, A.W., The galectin profile of the endothelium: Altered expression and localization in activated and tumor endothelial cells (2008) Am J Pathol, 172, pp. 545-553
- Baum, L.G., Seilhamer, J.J., Pang, M., Levine, W.B., Beynon, D., Berliner, J.A., Synthesis of an endogeneous lectin, galectin-1, by human endothelial cells is up-regulated by endothelial cell activation (1995) Glycoconj J, 12, pp. 63-68
- Saussez, S., Camby, I., Toubeau, G., Kiss, R., Galectins as modulators of tumor progression in head and neck squamous cell carcinomas (2007) Head Neck, 29, pp. 874-884
- Lotan, R., Belloni, P.N., Tressler, R.J., Lotan, D., Xu, X.C., Nicolson, G.L., Expression of galectins on microvessel endothelial cells and their involvement in tumour cell adhesion (1994) Glycoconj J, 11, pp. 462-468
- 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
- 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
- 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
- Nangia-Makker, P., Honjo, Y., Sarvis, R., Akahani, S., Hogan, V., Pienta, K.J., Galectin-3 induces endothelial cell morphogenesis and angiogenesis (2000) Am J Pathol, 156, pp. 899-909
- 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
Citas:
---------- APA ----------
Laderach, D.J., Gentilini, L.D., Giribaldi, L., Delgado, V.C., Nugnes, L., Croci, D.O., Al Nakouzi, N.,..., Rabinovich, G.A.
(2013)
. A unique galectin signature in human prostate cancer progression suggests galectin-1 as a key target for treatment of advanced disease. Cancer Research, 73(1), 86-96.
http://dx.doi.org/10.1158/0008-5472.CAN-12-1260---------- CHICAGO ----------
Laderach, D.J., Gentilini, L.D., Giribaldi, L., Delgado, V.C., Nugnes, L., Croci, D.O., et al.
"A unique galectin signature in human prostate cancer progression suggests galectin-1 as a key target for treatment of advanced disease"
. Cancer Research 73, no. 1
(2013) : 86-96.
http://dx.doi.org/10.1158/0008-5472.CAN-12-1260---------- MLA ----------
Laderach, D.J., Gentilini, L.D., Giribaldi, L., Delgado, V.C., Nugnes, L., Croci, D.O., et al.
"A unique galectin signature in human prostate cancer progression suggests galectin-1 as a key target for treatment of advanced disease"
. Cancer Research, vol. 73, no. 1, 2013, pp. 86-96.
http://dx.doi.org/10.1158/0008-5472.CAN-12-1260---------- VANCOUVER ----------
Laderach, D.J., Gentilini, L.D., Giribaldi, L., Delgado, V.C., Nugnes, L., Croci, D.O., et al. A unique galectin signature in human prostate cancer progression suggests galectin-1 as a key target for treatment of advanced disease. Cancer Res. 2013;73(1):86-96.
http://dx.doi.org/10.1158/0008-5472.CAN-12-1260