Genetic assessment of the importance of galectin-3 in cancer initiation, progression, and dissemination in mice

Glycobiology

Volumn 19, Issue 1, 2009, Pages 68-75

  Eude le Parco, Isabelle ^a   Gendronneau, Gaëlle ^a   Dang, Tien ^a   Delacour, Delphine ^a   Thijssen, Victor I ^b   Edelmann, Winfried ^c   Peuchmaur, Michel ^d   Poirier, Françoise ^a  

^a INSTITUT JACQUES MONOD   (France)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

Apc mutations; Galectin 3 knock out mice; Metastasis; PyMT transgenic; Tumor progression

Indexed keywords

GALECTIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER GENETICS; CANCER GROWTH; CONTROLLED STUDY; DISEASE COURSE; GENE FUNCTION; GENE MUTATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; INTESTINE CANCER; LUNG CARCINOGENESIS; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ANIMALS; DISEASE PROGRESSION; GALECTIN 3; GENOTYPE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; NEOPLASM METASTASIS; NEOPLASMS, EXPERIMENTAL;

ANIMALIA; MUS;

EID: 57649207937     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwn105     Document Type: Article

References (66)

1. Andre S, Kojima S, Yamazaki N, Fink C, Kaltner H, Kayser K, Gabius HJ. 1999. Galectins-1 and -3 and their ligands in tumor biology. Non-uniform properties in cell-surface presentation and modulation of adhesion to matrix glycoproteins for various tumor cell lines, in biodistribution of free and liposome-bound galectins and in their expression by breast and colorectal carcinomas with/without metastatic propensity. J Cancer Res Clin Oncol. 125:461-474.
2. Barondes SH, Cooper DN, Gitt MA, Leffler H. 1994. Galectins: Structure and function of a large family of animal lectins. J Biol Chem. 269:20807-20810.
3. Bichara M, Attmane-Elakeb A, Brown D, Essig M, Karim Z, Muffat-Joly M, Micheli L, Eude-Le Parco I, Cluzeaud F, Peuchmaur M, et al. 2006. Exploring the role of galectin 3 in kidney function: A genetic approach. Glycobiology. 16:36-45.
4. Boivin GP, Washington K, Yang K, Ward JM, Pretlow TP, Russell R, Besselsen DG, Godfrey VL, Doetschman T, Dove WF, et al. 2003. Pathology of mouse models of intestinal cancer: Consensus report and recommendations. Gastroenterology. 124:762-777.
5. Bresalier RS, Mazurek N, Sternberg LR, Byrd JC, Yunker CK, Nangia-Makker P, Raz A. 1998. Metastasis of human colon cancer is altered by modifying expression of the beta-galactoside-binding protein galectin 3. Gastroenterology. 115:287-296.
6. Castronovo V, Van Den Brule FA, Jackers P, Clausse N, Liu FT, Gillet C, Sobel ME. 1996. Decreased expression of galectin-3 is associated with progression of human breast cancer. J Pathol. 179:43-48.
7. Colnot C, Fowlis D, Ripoche MA, Bouchaert I, Poirier F. 1998. Embryonic implantation in galectin 1/galectin 3 double mutant mice. Dev Dyn. 211:306-313.
8. Colnot C, Sidhu SS, Balmain N, Poirier F. 2001. Uncoupling of chondrocyte death and vascular invasion in mouse galectin 3 nullmutant bones. Dev Biol. 229:203-214.
9. Cooper DN, Barondes SH. 1999. God must love galectins; he made so many of them. Glycobiology. 9:979-984.
10. Danguy A, Camby I, Kiss R. 2002. Galectins and cancer. Biochim Biophys Acta. 1572:285-293.
11. Delacour D, Cramm-Behrens CI, Drobecq H, Le Bivic A, Naim HY, Jacob R. 2006. Requirement for galectin-3 in apical protein sorting. Curr Biol 16:408-414.
12. Delacour D, Jacob R. 2006. Apical protein transport. Cell Mol Life Sci. 63:2491-2505.
13. Delacour D, Koch A, Ackermann W, Eude-Le Parco I, Elsasser HP, Poirier F, Jacob R. 2008. Loss of galectin-3 impairs membrane polarisation of mouse enterocytes in vivo. J Cell Sci. 121:458-465.
14. Dumic J, Dabelic S, Flogel M. 2006. Galectin-3: An open-ended story. Biochim Biophys Acta. 1760:616-635.
15. 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.
16. Fodde R, Edelmann W, Yang K, van Leeuwen C, Carlson C, Renault B, Breukel C, Alt E, Lipkin M, Khan PM, et al. 1994. A targeted chain-termination mutation in the mouse Apc gene results in multiple intestinal tumors. Proc Natl Acad Sci USA. 91:8969-8973.
17. Gendronneau G, Sidhu SS, Delacour D, Dang T, Calonne C, Houzelstein D, Magnaldo T, Poirier F. 2008. Galectin-7 in the control of epidermal homeostasis after injury. Mol Biol Cell. Epub ahead of print October 1, 2008.
18. Gillenwater A, Xu XC, el-Naggar AK, Clayman GL, Lotan R. 1996. Expression of galectins in head and neck squamous cell carcinoma. Head Neck. 18:422-432.
19. Min/+ mice. Genetics. 144:1769-1776.
20. Granovsky M, Fata J, Pawling J, Muller WJ, Khokha R, Dennis JW. 2000. Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nat Med. 6:306-312.
21. Guy CT, Cardiff RD, Muller WJ. 1992. Induction of mammary tumors by expression of polyomavirus middle T oncogene: A transgenic mouse model for metastatic disease. Mol Cell Biol. 12:954-961.
22. Hakomori S. 2002. Glycosylation de.ning cancer malignancy: New wine in an old bottle. Proc Natl Acad Sci USA. 99:10231-10233.
23. Heyer J, Yang K, Lipkin M, Edelmann W, Kucherlapati R. 1999. Mouse models for colorectal cancer. Oncogene. 18:5325-5333.
24. Hirabayashi J, Kasai K. 1993. The family of metazoan metal-independent beta- galactoside-binding lectins: Structure, function and molecular evolution. Glycobiology. 3:297-304.
25. Hittelet A, Legendre H, Nagy N, Bronckart Y, Pector JC, Salmon I, Yeaton P, Gabius HJ, Kiss R, Camby I. 2003. Upregulation of galectins-1 and -3 in human colon cancer and their role in regulating cell migration. Int J Cancer. 103:370-379.
26. Honjo Y, Nangia-Makker P, Inohara H, Raz A. 2001. Down-regulation of galectin-3 suppresses tumorigenicity of human breast carcinoma cells. Clin Cancer Res. 7:661-668.
27. Houzelstein D, Goncalves IR, Fadden AJ, Sidhu SS, Cooper DN, Drickamer K, Leffler H, Poirier F. 2004. Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol. 21:1177-1187.
28. Hsu DK, Dowling CA, Jeng KC, Chen JT, Yang RY, Liu FT. 1999. Galectin-3 expression is induced in cirrhotic liver and hepatocellular carcinoma. Int J Cancer. 81:519-526.
29. Hughes RC. 2001. Galectins as modulators of cell adhesion. Biochimie 83:667-676.
30. Idikio H. 1998. Galectin-3 expression in human breast carcinoma: Correlation with cancer histologic grade. Int J Oncol. 12:1287-1290.
31. Irimura T, Matsushita Y, Sutton RC, Carralero D, Ohannesian DW, Cleary KR, Ota DM, Nicolson GL, Lotan R. 1991. Increased content of an endogenous lactose-binding lectin in human colorectal carcinoma progressed to metastatic stages. Cancer Res. 51:387-393.
32. John CM, Lef.er H, Kahl-Knutsson B, Svensson I, Jarvis GA. 2003. Truncated galectin-3 inhibits tumor growth and metastasis in orthotopic nude mouse model of human breast cancer. Clin Cancer Res. 9:2374-2383.
33. Johnson KD, Glinskii OV, Mossine VV, Turk JR, Mawhinney TP, Anthony DC, Henry CJ, Huxley VH, Glinsky GV, Pienta KJ, et al. 2007. Galectin-3 as a potential therapeutic target in tumors arising from malignant endothelia. Neoplasia. 9:662-670.
34. Kim YJ, Varki A. 1997. Perspectives on the significance of altered glycosylation of glycoproteins in cancer. Glycoconj J. 14:569-576.
35. Konstantinov KN, Robbins BA, Liu FT. 1996. Galectin-3, a beta-galactoside-binding animal lectin, is a marker of anaplastic large-cell lymphoma. Am J Pathol. 148:25-30.
36. Lahm H, Andre S, Hoeflich A, Kaltner H, Siebert HC, Sordat B, von der Lieth CW, Wolf E, Gabius HJ. 2004. Tumor galectinology: Insights into the complex network of a family of endogenous lectins. Glycoconj J 20:227-238.
37. Lee EC, Woo HJ, Korzelius CA, Steele GD Jr, Mercurio AM. 1991. Carbohydrate-binding protein 35 is the major cell-surface laminin-binding protein in colon carcinoma. Arch Surg. 126:1498-1502.
38. Legendre H, Decaestecker C, Nagy N, Hendlisz A, Schuring MP, Salmon I, Gabius HJ, Pector JC, Kiss R. 2003. Prognostic values of galectin-3 and the macrophage migration inhibitory factor (MIF) in human colorectal cancers. Mod Pathol. 16:491-504.
39. Liu FT, Patterson RJ, Wang JL. 2002. Intracellular functions of galectins. Biochim Biophys Acta. 1572:263-273.
40. Liu FT, Rabinovich GA. 2005. Galectins as modulators of tumour progression. Nat Rev Cancer. 5:29-41.
41. Lotan R, Ito H, Yasui W, Yokozaki H, Lotan D, Tahara E. 1994. Expression of a 31-kDa lactoside-binding lectin in normal human gastric mucosa and in primary and metastatic gastric carcinomas. Int J Cancer. 56:474-480.
42. Lotz MM, Andrews CW Jr, Korzelius CA, Lee EC, Steele GD Jr, Clarke A, Mercurio AM. 1993. 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. 90:3466-3470.
43. Miller SA, Dykes DD, Polesky HF. 1988. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 16:1215.
44. Moser AR, Pitot HC, Dove WF. 1990. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science. 247:322-324.
45. Nakahara S, Oka N, Raz A. 2005. On the role of galectin-3 in cancer apoptosis. Apoptosis. 10:267-275.
46. Nakamura M, Inufusa H, Adachi T, Aga M, Kurimoto M, Nakatani Y, Wakano T, Nakajima A, Hida JI, Miyake M, et al. 1999. Involvement of galectin-3 expression in colorectal cancer progression and metastasis. Int J Oncol. 15:143-148.
47. Nangia-Makker P, Honjo Y, Sarvis R, Akahani S, Hogan V, Pienta KJ, Raz A. 2000. Galectin-3 induces endothelial cell morphogenesis and angiogenesis. Am J Pathol. 156:899-909.
48. Nieminen J, Kuno A, Hirabayashi J, Sato S. 2007. Visualization of galectin-3 oligomerization on the surface of neutrophils and endothelial cells using fluorescence resonance energy transfer. J Biol Chem. 282:1374-1383.
49. Nieminen J, St-Pierre C, Bhaumik P, Poirier F, Sato S. 2008. Role of galectin-3 in leukocyte recruitment in a murine model of lung infection by Streptococcus pneumoniae. J Immunol. 180:2466-2473.
50. Ochieng J, Furtak V, Lukyanov P. 2004. Extracellular functions of galectin-3. Glycoconj J. 19:527-535.
51. Pacis RA, Pilat MJ, Pienta KJ, Wojno K, Raz A, Hogan V, Cooper CR. 2000. Decreased galectin-3 expression in prostate cancer. Prostate. 44:118-123.
52. Perillo NL, Marcus ME, Baum LG. 1998. Galectins: Versatile modulators of cell adhesion, cell proliferation, and cell death. J Mol Med. 76, 402-412.
53. Sano H, Hsu DK, Apgar JR, Yu L, Sharma BB, Kuwabara I, Izui S, Liu FT. 2003. Critical role of galectin-3 in phagocytosis by macrophages. J Clin Invest. 112:389-397.
54. Schoeppner HL, Raz A, Ho SB, Bresalier RS. 1995. Expression of an endogenous galactose-binding lectin correlates with neoplastic progression in the colon. Cancer. 75:2818-2826.
55. Schrage A, Loddenkemper C, Erben U, Lauer U, Hausdorf G, Jungblut PR, Johnson J, Knolle PA, Zeitz M, Hamann A, et al. 2008. Murine CD146 is widely expressed on endothelial cells and is recognized by the monoclonal antibody ME-9F1. Histochem Cell Biol. 129:441-451.
56. 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.
57. Shimura T, Takenaka Y, Tsutsumi S, Hogan V, Kikuchi A, Raz A. 2004. Galectin-3, a novel binding partner of beta-catenin. Cancer Res. 64:6363-6367.
58. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, Gould KA, Dove WF. 1992. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science. 256:668-670.
59. Takenaka Y, Fukumori T, Raz A. 2004. Galectin-3 and metastasis. Glycoconj J. 19:543-549.
60. Thijssen VL, Postel R, Brandwijk RJ, Dings RP, Nesmelova I, Satijn S, Verhofstad N, Nakabeppu Y, Baum LG, Bakkers J, et al. 2006. Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc Natl Acad Sci USA. 103:15975-15980.
61. Toscano MA, Bianco GA, Ilarregui JM, Croci DO, Correale J, Hernandez JD, Zwirner NW, Poirier F, Riley EM, Baum LG, et al. 2007. Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat Immunol. 8:825-834.
62. Tsuboi K, Shimura T, Masuda N, Ide M, Tsutsumi S, Yamaguchi S, Asao T, Kuwano H. 2007. Galectin-3 expression in colorectal cancer: Relation to invasion and metastasis. Anticancer Res. 27:2289-2296.
63. Van Den Brule F, Califice S, Castronovo V. 2004. Expression of galectins in cancer: A critical review. Glycoconj J. 19:537-542.
64. Van Den Brule FA, Buicu C, Berchuck A, Bast RC, Deprez M, Liu FT, Cooper DN, Pieters C, Sobel ME, Castronovo V. 1996. Expression of the 67-kD laminin receptor, galectin-1, and galectin-3 in advanced human uterine adenocarcinoma. Hum Pathol. 27:1185-1191.
65. Xu XC, el-Naggar AK, Lotan R. 1995. Differential expression of galectin-1 and galectin-3 in thyroid tumors. Potential diagnostic implications. Am J Pathol. 147:815-822.
66. Yang WC, Mathew J, Velcich A, Edelmann W, Kucherlapati R, Lipkin M, Yang K, Augenlicht LH. 2001. Targeted inactivation of the p21(WAF1/cip1) gene enhances Apc-initiated tumor formation and the tumor-promoting activity of a Western-style high-risk diet by altering cell maturation in the intestinal mucosal. Cancer Res. 61:565-569.