Inhibition of Wnt-2 and galectin-3 synergistically destabilizes β-catenin and induces apoptosis in human colorectal cancer cells

International Journal of Cancer

Volumn 121, Issue 6, 2007, Pages 1175-1181

  Shi, Yihui ^a   He, Biao ^a   Kuchenbecker, Kristopher M ^a   You, Liang ^a   Xu, Zhidong ^a   Mikami, Iwao ^a   Yagui Beltran, Adam ^a   Clement, Genevieve ^a   Lin, Yu Ching ^a   Okamoto, Junichi ^a   Bravo, Dawn T ^a   Jablons, David M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Galectin 3; Human colorectal cancer; Wnt signaling pathway; Wnt 2

Indexed keywords

APC PROTEIN; AXIN; BETA CATENIN; GALECTIN 3; SMALL INTERFERING RNA; T CELL FACTOR PROTEIN; WNT PROTEIN; WNT2 PROTEIN;

APC GENE; APOPTOSIS; ARTICLE; AXIN1 GENE; CANCER CELL; COLORECTAL CANCER; CONTROLLED STUDY; CTNNB1 GENE; GENE; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REPORTER GENE; SIGNAL TRANSDUCTION;

APOPTOSIS; BETA CATENIN; BLOTTING, WESTERN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; GALECTIN 3; GENE EXPRESSION; HUMANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; WNT2 PROTEIN;

EID: 34548079518     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22848     Document Type: Article

References (42)

1. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990;61:759-67.
2. Fodde R, Smits R, Clevers H. APC, signal transduction and genetic instability in colorectal cancer. Nat Rev Cancer 2001;1:55-67.
3. Taketo MM. Shutting down Wnt signal-activated cancer. Nat Genet 2004;36:320-2.
4. -/- colon carcinoma. Science 1997;275:1784-7.
5. Liu W, Dong X, Mai M, Seelan RS, Taniguchi K, Krishnadath KK, Halling KC, Cunningham JM, Boardman LA, Qian C, Christensen E, Schmidt SS, et al. Mutations in AXIN2 cause colorectal cancer with defective mismatch repair by activating β-catenin/TCF signalling. Nat Genet 2000;26:146-7.
6. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science 1997;275:1787-90.
7. Holcombe RF, Marsh JL, Waterman ML, Lin F, Milovanovic T, Truong T. Expression of Wnt ligands and frizzled receptors in colonic mucosa and in colon carcinoma. Mol Pathol 2002;55:220-6.
8. Katoh M. Frequent up-regulation of WNT2 in primary gastric cancer and colorectal cancer. Int J Oncol 2001;19:1003-7.
9. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, Chen WD, Pretlow TP, Yang B, Akiyama Y, Van Engeland M, Toyota M, Tokino T, et al. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 2004;36: 417-22.
10. He B, Reguart N, You L, Mazieres J, Xu Z, Lee AY, Mikami I, McCormick F, Jablons DM. Blockade of Wnt-1 signaling induces apoptosis in human colorectal cancer cells containing downstream mutations. Oncogene 2005;24:3054-8.
11. Suzuki H, Gabrielson E, Chen W, Anbazhagan R, van Engeland M, Weijenberg MP, Herman JG, Baylin SB. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 2002;31:141-9.
12. Caldwell GM, Jones C, Gensberg K, Jan S, Hardy RG, Byrd P, Chughtai S, Wallis Y, Matthews GM, Morton DG. The Wnt antagonist sFRP1 in colorectal tumorigenesis. Cancer Res 2004;64:883-8.
13. Aguilera O, Fraga MF, Ballestar E, Paz MF, Herranz M, Espada J, Garcia JM, Munoz A, Esteller M, Gonzalez-Sancho JM. Epigenetic inactivation of the Wnt antagonist DICKKOPF-1 (DKK-1) gene in human colorectal cancer. Oncogene 2006;25:4116-21.
14. Akahani S, Nangia-Makker P, Inohara H, Kim HR, Raz A. Galectin-3: a novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res 1997;57:5272-6.
15. Davidson PJ, Davis MJ, Patterson RJ, Ripoche MA, Poirier F, Wang JL. Shuttling of galectin-3 between the nucleus and cytoplasm. Glycobiology 2002;12:329-37.
16. Inohara H, Raz A. Functional evidence that cell surface galectin-3 mediates homotypic cell adhesion. Cancer Res 1995;55:3267-71.
17. van den Brule F, Califice S, Castronovo V. Expression of galectins in cancer: a critical review. Glycoconj J 2004;19:537-42.
18. Califice S, Castronovo V, van den Brule F. Galectin-3 and cancer (Review). Int J Oncol 2004;25:983-92.
19. Liu FT, Rabinovich GA. Galectins as modulators of tumour progression. Nat Rev Cancer 2005;5:29-41.
20. Irimura T, Matsushita Y, Sutton RC, Carralero D, Ohannesian DW, Cleary KR, Ota DM, Nicolson GL, Lotan R. Increased content of an endogenous lactose-binding lectin in human colorectal carcinoma progressed to metastatic stages. Cancer Res 1991;51:387-93.
21. Schoeppner HL, Raz A, Ho SB, Bresalier RS. Expression of an endogenous galactose-binding lectin correlates with neoplastic progression in the colon. Cancer 1995;75:2818-26.
22. Nakamura M, Inufusa H, Adachi T, Aga M, Kurimoto M, Nakatani Y, Wakano T, Nakajima A, Hida JI, Miyake M, Shindo K, Yasutomi M. Involvement of galectin-3 expression in colorectal cancer progression and metastasis. Int J Oncol 1999;15:143-8.
23. Castronovo V, Campo E, van den Brule FA, Claysmith AP, Cioce V, Liu FT, Fernandez PL, Sobel ME. Inverse modulation of steady-state messenger RNA levels of two non-integrin laminin-binding proteins in human colon carcinoma. J Natl Cancer Inst 1992;84:1161-9.
24. Lotz MM, Andrews CW, Jr, Korzelius CA, Lee EC, Steele GD, Jr, Clarke A, Mercurio AM. Decreased expression of Mac-2 (carbohydrate binding protein 35) and loss of its nuclear localization are associated with the neoplastic progression of colon carcinoma. Proc Natl Acad Sci USA 1993;90:3466-70.
25. Shimura T, Takenaka Y, Tsutsumi S, Hogan V, Kikuchi A, Raz A. Galectin-3, a novel binding partner of β-catenin. Cancer Res 2004;64: 6363-7.
26. Shu SY, Rosenberg SA. Adoptive immunotherapy of newly induced murine sarcomas. Cancer Res 1985;45:1657-62.
27. You L, He B, Xu Z, Uematsu K, Mazieres J, Fujii N, Mikami I, Reguart N, McIntosh JK, Kashani-Sabet M, McCormick F, Jablons DM. An anti-Wnt-2 monoclonal antibody induces apoptosis in malignant melanoma cells and inhibits tumor growth. Cancer Res 2004;64: 5385-9.
28. Li L, Mao J, Sun L, Liu W, Wu D. Second cysteine-rich domain of Dickkopf-2 activates canonical Wnt signaling pathway via LRP-6 independently of dishevelled. J Biol Chem 2002;277:5977-81.
29. Elbashir SM, Harborth J, Weber K, Tuschl T. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 2002;26:199-213.
30. Uematsu K, Kanazawa S, You L, He B, Xu Z, Li K, Peterlin BM, McCormick F, Jablons DM. Wnt pathway activation in mesothelioma: evidence of dishevelled overexpression and transcriptional activity of β-catenin. Cancer Res 2003;63:4547-51.
31. Boutros M, Mlodzik M. Dishevelled: at the crossroads of divergent intracellular signaling pathways. Mech Dev 1999;83:27-37.
32. Tetsu O, McCormick F. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999;398:422-6.
33. Lin HM, Pestell RG, Raz A, Kim HR. Galectin-3 enhances cyclin D(1) promoter activity through SP1 and a cAMP-responsive element in human breast epithelial cells. Oncogene 2002;21:8001-10.
34. Shimura T, Takenaka Y, Fukumori T, Tsutsumi S, Okada K, Hogan V, Kikuchi A, Kuwano H, Raz A. Implication of galectin-3 in Wnt signaling. Cancer Res 2005;65:3535-7.
35. Kim PJ, Plescia J, Clevers H, Fearon ER, Altieri DC. Survivin and molecular pathogenesis of colorectal cancer. Lancet 2003;362:205-9.
36. Yang RY, Hsu DK, Liu FT. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci USA 1996;93:6737-42.
37. Kim HR, Lin HM, Biliran H, Raz A. Cell cycle arrest and inhibition of anoikis by galectin-3 in human breast epithelial cells. Cancer Res 1999;59:4148-54.
38. Moon BK, Lee YJ, Battle P, Jessup JM, Raz A, Kim HR. Galectin-3 protects human breast carcinoma cells against nitric oxide-induced apoptosis: implication of galectin-3 function during metastasis. Am J Pathol 2001;159:1055-60.
39. Hanada M, Aime-Sempe C, Sato T, Reed JC. Structure-function analysis of Bcl-2 protein. Identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax. J Biol Chem 1995;270:11962-9.
40. Nakahara S, Oka N, Raz A. On the role of galectin-3 in cancer apoptosis. Apoptosis 2005;10:267-75.
41. Houghton JA, Harwood FG, Gibson AA, Tillman DM. The fas signaling pathway is functional in colon carcinoma cells and induces apoptosis. Clin Cancer Res 1997;3:2205-9.
42. Ciccolini J, Peillard L, Evrard A, Cuq P, Aubert C, Pelegrin A, Formento P, Milano G, Catalin J. Enhanced antitumor activity of 5-fluorouracil in combination with 2′-deoxyinosine in human colorectal cell lines and human colon tumor xenografts. Clin Cancer Res 2000;6: 1529-35.