Galectin-1 Triggers Epithelial-Mesenchymal Transition in Human Hepatocellular Carcinoma Cells

Journal of Cellular Physiology

Volumn 230, Issue 6, 2015, Pages 1298-1309

  Bacigalupo, María L ^a   Manzi, Malena ^a   Espelt, María V ^a   Gentilini, Lucas D ^a   Compagno, Daniel ^a   Laderach, Diego J ^a   Wolfenstein Todel, Carlota ^a   Rabinovich, Gabriel A ^a,b   Troncoso, María F ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; COMPLEMENTARY DNA; CYCLIN D1; GALECTIN 1; LYMPHOID ENHANCER FACTOR 1; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; UVOMORULIN; VIMENTIN; WNT PROTEIN; CADHERIN; CTNNB1 PROTEIN, HUMAN; LGALS1 PROTEIN, HUMAN;

ANCHORAGE INDEPENDENT GROWTH; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; CELL NUCLEUS; CELL POLARITY; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLAST; FLUORESCENCE MICROSCOPY; GAIN OF FUNCTION MUTATION; GENE OVEREXPRESSION; HEPG2 CELL LINE; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; LOSS OF FUNCTION MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; TRANSCRIPTION INITIATION; UPREGULATION; WESTERN BLOTTING; WNT SIGNALING PATHWAY; DOWN REGULATION; LIVER TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

GASTROPODA;

BETA CATENIN; CADHERINS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; GALECTIN 1; HUMANS; LIVER NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; UP-REGULATION;

EID: 84923310890     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24865     Document Type: Article

References (48)

1. Anspach FB, Hilbeck O. 1995. Removal of endotoxins by affinity sorbents. J Chromatogr A 711:81-92.
2. Bacigalupo ML, Manzi M, Rabinovich GA, Troncoso MF. 2013. Hierarchical and selective roles of galectins in hepatocarcinogenesis, liver fibrosis and inflammation of hepatocellular carcinoma. World J Gastroenterol 19:8831-8849.
3. Camby I, Decaestecker C, Lefranc F, Kaltner H, Gabius HJ, Kiss R. 2005. Galectin-1 knocking down in human U87 glioblastoma cells alters their gene expression pattern. Biochem Biophys Res Commun 335:27-35.
4. Cokakli M, Erdal E, Nart D, Yilmaz F, Sagol O, Kilic M, Karademir S, Atabey N. 2009. Differential expression of Caveolin-1 in hepatocellular carcinoma: Correlation with differentiation state, motility and invasion. BMC Cancer 9:65.
5. Couraud PO, Casentini-Borocz D, Bringman TS, Griffith J, McGrogan M, Nedwin GE. 1989. Molecular cloning, characterization, and expression of a human 14-kDa lectin. J Biol Chem 264: 1310-1316.
6. Croci DO, Cerliani JP, Dalotto-Moreno T, Mendez-Huergo SP, Mascanfroni ID, Dergan-Dylon S, Toscano MA, Caramelo JJ, Garcia-Vallejo JJ, Ouyang J, Mesri EA, Junttila MR, Bais C, Shipp MA, Salatino M, Rabinovich GA. 2014. Glycosylation-dependent lectin-receptor interactions preserve angiogenesis in anti-VEGF refractory tumors. Cell 156:744-758.
7. Croci DO, Salatino M, Rubinstein N, Cerliani JP, Cavallin LE, Leung HJ, Ouyang J, Ilarregui JM, Toscano MA, Domaica CI, Croci MC, Shipp MA, Mesri EA, Albini A, Rabinovich GA. 2012. Disrupting galectin-1 interactions with N-glycans suppresses hypoxia-driven angiogenesis and tumorigenesis in Kaposi's sarcoma. J Exp Med 209:1985-2000.
8. Chung EJ, Sung YK, Farooq M, Kim Y, Im S, Tak WY, Hwang YJ, Kim YI, Han HS, Kim JC, Kim MK. 2002. Gene expression profile analysis in human hepatocellular carcinoma by cDNA microarray. Mol Cells 14:382-387.
9. Dalotto-Moreno T, Croci DO, Cerliani JP, Martinez-Allo VC, Dergan-Dylon S, Mendez-Huergo SP, Stupirski JC, Mazal D, Osinaga E, Toscano MA, Sundblad V, Rabinovich GA, Salatino M. 2013. Targeting galectin-1 overcomes breast cancer-associated immunosuppression and prevents metastatic disease. Cancer Res 73:1107-1117.
10. de La Coste A, Romagnolo B, Billuart P, Renard CA, Buendia MA, Soubrane O, Fabre M, Chelly J, Beldjord C, Kahn A, Perret C. 1998. Somatic mutations of the beta-catenin gene are frequent in mouse and human hepatocellular carcinomas. Proc Natl Acad Sci U S A 95:8847-8851.
11. de Lope CR, Tremosini S, Forner A, Reig M, Bruix J. 2012. Management of HCC. J Hepatol 56:S75-S87.
12. Demydenko D, Berest I. 2009. Expression of galectin-1 in malignant tumors. Exp Oncol 31:74-79.
13. Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B, van Beijnum JR, Griffioen AW, Vink J, Krimpenfort P, Peterse JL, Cardiff RD, Berns A, Jonkers J. 2006. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10:437-449.
14. Elola MT, Wolfenstein-Todel C, Troncoso MF, Vasta GR, Rabinovich GA. 2007. Galectins: matricellular glycan-binding proteins linking cell adhesion, migration, and survival. Cell Mol Life Sci 64:1679-1700.
15. Espelt MV, Croci DO, Bacigalupo ML, Carabias P, Manzi M, Elola MT, Munoz MC, Dominici FP, Wolfenstein-Todel C, Rabinovich GA, Troncoso MF. 2011. Novel roles of galectin-1 in hepatocellular carcinoma cell adhesion, polarization, and in vivo tumor growth. Hepatology 53:2097-2106.
16. Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, Mills GB, Kobayashi R, Hunter T, Lu Z. 2007. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem 282:11221-11229.
17. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. 2010. Int J Cancer Estimates of worldwide burden of cancer in 2008: GLOBOCAN 127:2893-2917.
18. Firrincieli D, Boissan M, Chignard N. 2010. Epithelial-mesenchymal transition in the liver. Gastroenterol Clin Biol 34:523-528.
19. Grille SJ, Bellacosa A, Upson J, Klein-Szanto AJ, van Roy F, Lee-Kwon W, Donowitz M, Tsichlis PN, Larue L. 2003. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res 63:2172-2178.
20. Heuberger J, Birchmeier W. 2010. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2:a002915.
21. Ito K, Stannard K, Gabutero E, Clark AM, Neo SY, Onturk S, Blanchard H, Ralph SJ. 2012. Galectin-1 as a potent target for cancer therapy: Role in the tumor microenvironment. Cancer Metastasis Rev 31:763-778.
22. Kondoh N, Hada A, Ryo A, Shuda M, Arai M, Matsubara O, Kimura F, Wakatsuki T, Yamamoto M. 2003. Activation of Galectin-1 gene in human hepatocellular carcinoma involves methylation-sensitive complex formations at the transcriptional upstream and downstream elements. Int J Oncol 23:1575-1583.
23. Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B, Clevers H. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275:1784-1787.
24. Laderach DJ, Gentilini LD, Giribaldi L, Delgado VC, Nugnes L, Croci DO, Al Nakouzi N, Sacca P, Casas G, Mazza O, Shipp MA, Vazquez E, Chauchereau A, Kutok JL, Rodig SJ, Elola MT, Compagno D, Rabinovich GA. 2013. A unique galectin signature in human prostate cancer progression suggests galectin-1 as a key target for treatment of advanced disease. Cancer Res 73:86-96.
25. Lim MJ, Ahn J, Yi JY, Kim MH, Son AR, Lee SL, Lim DS, Kim SS, Kang MA, Han Y, Song JY. 2014. Induction of galectin-1 by TGF-beta1 accelerates fibrosis through enhancing nuclear retention of Smad2. Experimental cell research 326:125-135.
26. Liu S, Tobias R, McClure S, Styba G, Shi Q, Jackowski G. 1997. Removal of endotoxin from recombinant protein preparations. Clin Biochem 30:455-463.
27. Nieto MA. 2011. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 27:347-376.
28. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. 2008. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 68: 3645-3654.
29. Ose R, Oharaa O, Nagase T. 2012. Galectin-1 and Galectin-3 Mediate Protocadherin-24-Dependent Membrane Localization of beta-catenin in Colon Cancer Cell Line HCT116. Curr Chem Genomics 6:18-26.
30. Paz A, Haklai R, Elad-Sfadia G, Ballan E, Kloog Y. 2001. Galectin-1 binds oncogenic H-Ras to mediate Ras membrane anchorage and cell transformation. Oncogene 20:7486-7493.
31. Potikha T, Stoyanov E, Pappo O, Frolov A, Mizrahi L, Olam D, Shnitzer-Perlman T, Weiss I, Barashi N, Peled A, Sass G, Tiegs G, Poirier F, Rabinovich GA, Galun E, Goldenberg D. 2013. Interstrain differences in chronic hepatitis and tumor development in a murine model of inflammation-mediated hepatocarcinogenesis. Hepatology 58:192-204.
32. Rimerman RA, Gellert-Randleman A, Diehl JA. 2000. Wnt1 and MEK1 cooperate to promote cyclin D1 accumulation and cellular transformation. J Biol Chem 275:14736-14742.
33. Rubinstein N, Alvarez M, Zwirner NW, Toscano MA, Ilarregui JM, Bravo A, Mordoh J, Fainboim L, Podhajcer OL, Rabinovich GA. 2004. 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 5:241-251.
34. Sanchez-Tillo E, Liu Y, de Barrios O, Siles L, Fanlo L, Cuatrecasas M, Darling DS, Dean DC, Castells A, Postigo A. 2012. EMT-activating transcription factors in cancer: Beyond EMT and tumor invasiveness. Cell Mol Life Sci 69:3429-3456.
35. Shimura T, Takenaka Y, Fukumori T, Tsutsumi S, Okada K, Hogan V, Kikuchi A, Kuwano H, Raz A. 2005. Implication of galectin-3 in Wnt signaling. Cancer Res 65:3535-3537.
36. Spano D, Russo R, Di Maso V, Rosso N, Terracciano LM, Roncalli M, Tornillo L, Capasso M, Tiribelli C, Iolascon A. 2010. Galectin-1 and its involvement in hepatocellular carcinoma aggressiveness. Mol Med 16:102-115.
37. Tanos B, Rodriguez-Boulan E. 2008. The epithelial polarity program: machineries involved and their hijacking by cancer. Oncogene 27:6939-6957.
38. Thiery JP, Acloque H, Huang RY, Nieto MA. 2009. Epithelial-mesenchymal transitions in development and disease. Cell 139:871-890.
39. Troncoso MF, Iglesias MM, Isecke R, Todel CW, Brossmer R. 2000. Specificity of the binding site of the sialic acid-binding lectin from ovine placenta, deduced from interactions with synthetic analogues. Glycoconj J 17:705-711.
40. van Zijl F, Zulehner G, Petz M, Schneller D, Kornauth C, Hau M, Machat G, Grubinger M, Huber H, Mikulits W. 2009. Epithelial-mesenchymal transition in hepatocellular carcinoma. Future Oncol 5:1169-1179.
41. Villanueva A, Hernandez-Gea V, Llovet JM. 2013. Medical therapies for hepatocellular carcinoma: a critical view of the evidence. Nat Rev Gastroenterol Hepatol 10:34-42.
42. Whiteman EL, Liu CJ, Fearon ER, Margolis B. 2008. The transcription factor snail represses Crumbs3 expression and disrupts apico-basal polarity complexes. Oncogene 27:3875-3879.
43. Wodarz A, Nathke I. 2007. Cell polarity in development and cancer. Nat Cell Biol 9:1016-1024.
44. Wu H, Chen P, Liao R, Li YW, Yi Y, Wang JX, Sun TW, Zhou J, Shi YH, Yang XR, Jin JJ, Cheng YF, Fan J, Qiu SJ. 2012. Overexpression of galectin-1 is associated with poor prognosis in human hepatocellular carcinoma following resection. J Gastroenterol Hepatol 27:1312-1319.
45. Wu MH, Hong TM, Cheng HW, Pan SH, Liang YR, Hong HC, Chiang WF, Wong TY, Shieh DB, Shiau AL, Jin YT, Chen YL. 2009. Galectin-1-mediated tumor invasion and metastasis, up-regulated matrix metalloproteinase expression, and reorganized actin cytoskeletons. Mol Cancer Res 7:311-318.
46. Yang MH, Chen CL, Chau GY, Chiou SH, Su CW, Chou TY, Peng WL, Wu JC. 2009. Comprehensive analysis of the independent effect of twist and snail in promoting metastasis of hepatocellular carcinoma. Hepatology 50:1464-1474.
47. Yang RY, Rabinovich GA, Liu FT. 2008. Galectins: structure, function and therapeutic potential. Expert Rev Mol Med 10:e 17.
48. Zhai B, Yan HX, Liu SQ, Chen L, Wu MC, Wang HY. 2008. Reduced expression of E-cadherin/catenin complex in hepatocellular carcinomas. World J Gastroenterol 14:5665-5673.