Upregulation of galectins-1 and -3 in human colon cancer and their role in regulating cell migration

International Journal of Cancer

Volumn 103, Issue 3, 2003, Pages 370-379

  Hittelet, Axel ^a   Legendre, Hugues ^b   Nagy, Nathalie ^a   Bronckart, Yves ^c   Pector, Jean Claude ^b   Salmon, Isabelle ^a   Yeaton, Paul ^d   Gabius, Hans Joachim ^e   Kiss, Robert ^c   Camby, Isabelle ^c  

^a ERASME HOSPITAL   (Belgium)

^b JULES BORDET INSTITUTE   (Belgium)

^c FREE UNIVERSITY OF BRUSSELS   (Belgium)

^d UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cell migration; Colon cancer; Dysplasia; Galectin 1; Galectin 3; In vitro cell line; In vivo xenograft; Integrin

Indexed keywords

BETA GALACTOSIDE; EPITOPE; GALECTIN 1; GALECTIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CANCER CELL CULTURE; CANCER GROWTH; CELL MIGRATION; COLON CANCER; COMPUTER ASSISTED DIAGNOSIS; CONNECTIVE TISSUE; CONTROLLED STUDY; DYSPLASIA; EPITHELIUM CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; TUMOR XENOGRAFT; UPREGULATION; VIDEORECORDING;

ADENOCARCINOMA; ADENOMA; ANIMALS; CELL MOVEMENT; COLONIC NEOPLASMS; DNA PRIMERS; GALECTIN 1; GALECTIN 2; HUMANS; IMMUNOENZYME TECHNIQUES; LECTINS; MICE; MICE, NUDE; MICROSCOPY, FLUORESCENCE; MICROSCOPY, PHASE-CONTRAST; NEOPLASM STAGING; NEOPLASM TRANSPLANTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; UP-REGULATION;

EID: 0037454758     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.10843     Document Type: Article

References (52)

1. Gabius HJ. Biologic information transfer beyond the genetic code: The sugar code. Naturwissenschaften 2000;87:108-21.
2. Raz A, Lotan R. Endogenous galactoside-binding lectins: A new class of functional tumor cell surface molecules related to metastasis. Cancer Metastasis Rev 1987;6:433-52.
3. Barondes SH, Cooper DN, Gitt MA, Leffler H. Galectins. Structure and function of a large family of animal lectins. J Biol Chem 1994; 269:20807-10.
4. Itzkowitz SH. Galectins: Multipurpose carbohydrate-binding proteins implicated in tumor biology. Gastroenterology 1997;113:2003-5.
5. Kaltner H, Stierstorfer B. Animal lectins as cell adhesion molecules. Acta Anat (Basel) 1998;161:162-79.
6. Perillo NL, Marcus ME, Baum LG. Galectins: Versatile modulators of cell adhesion, cell proliferation, and cell death. J Mol Med 1998;76:402-12.
7. Hughes RC. Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim Biophys Acta 1999;1473:172-85.
8. Rabinovich GA. Galectins: An evolutionarily conserved family of animal lectins with multifunctional properties; a trip from the gene to clinical therapy. Cell Death Differ 1999;6:711-21.
9. André S, Kojima S, Yamazaki N, Fink C, Kayser K, Gabius HJ. Galectin-1 and -3 and their ligands in tumor biology. J Cancer Res Clin Oncol 1999;125:461-74.
10. Bresalier RS, Mazurek N, Sternberg LR, Byrd JC, Yunker CK, Nangia-Makker P, Raz A. Metastasis of human colon cancer is altered by modifying expression of the β-galactoside-binding protein galectin-3. Gastroenterology 1998;115:287-96.
11. Sanjuan X, Fernandez PL, Castells A, Castronovo V, Van den Brule F, Liu FT, Cadresa A, Campo E. Differential expression of galectin-3 and galectin-1 in colorectal cancer progression. Gastroenterology 1997;113:1906-15.
12. 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.
13. 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.
14. 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 metastasis stages. Cancer Res 1991;51:387-93.
15. Brinck U, Korabiowska M, Bosbach R, Gabius HJ. Detection of inflammation- and neoplasia-associated alterations in human large intestine using plant/invertebrate lectins, galectin-1 and neoglycoproteins. Acta Anat (Basel) 1998;161:219-33.
16. Nagy N, Bronckart Y, Camby I, Legendre H, Lahm H, Kaltner H, Hadari Y, Van Ham P, Yeaton P, Pector JC, Zick Y, Salmon I, et al. Galectin-8 expression decreases in cancer compared with normal and dysplastic human colon tissue and acts significantly on human colon cancer cell migration as a suppressor, Gut 2002;50:392-401.
17. Bronckart Y, Nagy N, Decaestecker C, Bouckaert Y, Remmelink M, Gielen I, Hittelet A, Darro F, Pector JC, Yeaton P, Danguy A, Kiss R, et al. Grading dysplasia in colorectal adenomas by means of the quantitative binding pattern determination of Arachis hypogaea, Dolichos biflorus, Amaranthus caudatus, Maackia amurensis and Sambucus nigra agglutinins. Hum Pathol 1999;30:1178-91.
18. Beahrs OH, Henson DE, Hutter RVP, Kennedy BS. eds. American Joint Committee on Cancer. Manual for Staging of Cancer, 4th Ed. Philadelphia: JB Lippincott, 1992. 81-2.
19. Darro F, Kruczynski A, Etiévant C, Martinez J, Pasteels JL, Kiss R. Characterization of the differentiation of human colorectal cancer cell lines by means of Voronoi diagrams. Cytometry 1993;14:783-92.
20. Darro F, Camby I, Kruczynski A, Pasteels JL, Martinez J, Kiss R. Characterization of the influence of anti-gastrin, anti-epidermal growth factor, anti-oestradiol, and antiluteinizing hormone releasing hormone antibodies on the proliferation of 27 cell lines from the gastrointestinal tract. Gut 1995;36:220-30.
21. Kiss R, Camby I, Duckworth C, DeDecker R, Salmon I, Pasteels JL, Danguy A, Yeaton P. In vitro influence of Phaseolus vulgaris, Griffonia simplicifolia, concanavalin A, wheat germ, and peanut agglutinins on HCT-15, LoVo, and SW837 human colorectal cancer cell growth. Gut 1997;40:253-61.
22. Jannot MC, Kruczynski A, Limouzy A, Dangou JM, Selves J, Delsol G, Martinez J, Kiss R. Spontaneous evolution of cytoplasmic lectin binding and nuclear size and deoxyribonucleic acid content in human colorectal cancers grafted onto nude mice. Lab Invest 1993;68:446-55.
23. Gabius HJ. Influence of type of linkage and spacer on the interaction of β-galactoside-binding proteins with immobilized affinity ligands. Anal Biochem 1990;189:91-4.
24. Kaltner H, Lips KS, Reuter G, Lippert S, Sinowatz F, Gabius HJ. Quantitation and histochemical localization of galectin-1 and galectin-1-reactive glycoconjugates in fetal development of bovine organs. Histol Histopathol 1997;12:945-60.
25. Siebert HC, Adar R, Arango R, Burchert M, Kaltner H, Kayser G, Tajkhorshid E, von der Lieth CW, Kaptein R, Sharon N, Vliegenthart JF, Gabius HJ. Involvement of laser photo CIDNP (chemically induced dynamic nuclear polarization)-reactive amino-acid side chains in ligand binding by galactoside-specific lectins in solution. Eur J Biochem 1997;249:27-38.
26. Camby I, Belot B, Rorive S, Lefranc F, Maurage CA, Lahm A, Kaltner H, Hadari Y, Ruchoux MM, Brotchi J, Zick Y, Salmon I, et al. Galectins are differentially expressed in supratentorial pilocytic astrocytomas, astrocytomas, anaplastic astrocytomas and glioblastomas, and significantly modulate tumor astrocyte migration. Brain Pathol 2001;11:12-26.
27. Kaltner H, Seyrek K, Heck A, Sinowatz F, Gabius HJ. Galectin-1 and galectin-3 in fetal development of bovine respiratory and digestive tracts. Comparison of cell type-specific expression profiles and subcellular localization. Cell Tissue Res 2002;307:35-46.
28. Nagy N, Brenner C, Markadieu N, Chaboteaux C, Camby I, Schafer BW, Pochet R, Heizmann CW, Salmon I, Kiss R, Decaestecker C. S100A2, a putative tumor suppressor gene, regulates in vitro squamous cell carcinoma migration. Lab Invest 2001;81:599-612.
29. DeHauwer C, Camby I, Darro F, Decaestecker C, Gras T, Salmon I, Kiss R, Van Ham P. Dynamic characterization of glioblastoma cell motility. Biochem Biophys Res Commun 1997;232:267-72.
30. DeHauwer C, Camby I, Darro F, Migeotte I, Decaestecker C, Verbeek C, Danguy A, Brotchi J, Salmon I, Van Ham P, Kiss R. Gastrin inhibits motility, decreases cell death and increases cell proliferation in human glioblastoma cell lines. J Neurobiol 1998;37:373-82.
31. Lahm H, Andre S, Hoeflich A, Fischer JR, Sordat B, Kaltner H, Wolf E, Gabius HJ, Comprehensive galectin fingerprinting in a panel of 61 human tumor cell lines by RT-PCR and its implications for diagnostic and therapeutic procedures. J Cancer Res Clin Oncol 2001;127;375-86.
32. Ohannesian DW, Lotan D, Thomas P, Jessup JM, Fukuda M, Gabius HJ, Lotan R. Carcinoembryonic antigen and other glycoconjugates act as ligands for galectin-3 in human colon carcinoma cells. Cancer Res 1995;55:2191-9.
33. Lotz MM, Andrews CW, Korzelius CA, Lee EC, Steele GD, Clarke A, Mercurio AM. Decreased expression of Mac-2 (carbohydrate binding protein 35) and loss of its nuclear localization are associated with neoplastic progression of colon carcinoma. Proc Natl Acad Sci USA 1993;90:3466-70.
34. van den Brule FA, Waltregny D, Castronovo V. Increased expression of galectin-1 in carcinoma-associated stroma predicts poor outcome in prostate carcinoma patients. J Pathol 2001;193:80-7.
35. Hughes RC. Galectins as modulators of cell adhesion. Biochimie 2001;83:667-76.
36. Inohara H, Raz A. Functional evidence that cell surface galectin-3 mediates homotypic cell adhesion. Cancer Res 1995;55:3267-371.
37. Mahanthappa NK, Cooper DNW, Barondes SH, Schwarting GA. Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism. Development 1994;120:1373-84.
38. 1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture. J Biol Chem 1998;273:11205-11.
39. Zhou Q, Cummings RD. L-14 lectin recognition of laminin and its promotion of in vitro cell adhesion. Arch Biochem Biophys 1993; 300:6-17.
40. Levy Y, Arbel-Goren R, Hadari YR, et al. Galectin-8 functions as a matricellular modulator of cell adhesion. J Biol Chem 2001;276:31285-95.
41. Gumbiner BM. Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 1996;84:345-57.
42. Cooper DN. Galectin-1: Secretion and modulation of cell interactions with laminin. Trends Glycosci Glycotechnol 1997;9:57-67.
43. Delbrouck C, Doyen I, Belot N, Decaestecker C, Ghanooni R, de Lavareille A, Kaltner H, Choufani G, Danguy A, Vandenhoven G, Gabius HJ, Hassid S, Kiss R. Galectin-1 is overexpressed in nasal polyps under budesonide and inhibits eosinophil migration. Lab Invest 2002;82:147-58.
44. Moiseeva EP, Spring EL, Baron JH, de Bono DP. Galectin 1 modulates attachment, spreading and migration of cultured vascular smooth muscle cells via interactions with cellular receptors and components of extracellular matrix. J Vasc Res 1999;36:47-58.
45. Camby I, Belot N, Lefranc F, Sadeghi N, de Launoit Y, Kaltner H, Musette S, Darro F, Danguy A, Salmon I, Gabius HJ, Kiss R.Galectin-1 modulates human glioblastoma cell migration into the brain though modifications to the actin cytoskeleton and the levels of expression of small GTPases. J Neuropathol Exp Neurol 2002;61:585-96.
46. LeMarer N, Hughes RC. Effects of the carbohydrate-binding protein galectin-3 on the invasiveness of human breast carcinoma cells. J Cell Physiol 1996;168:51-8.
47. Murray GI, Duncan ME, O'Neil P, Melvin WT, Fothergill JE. Matrix metalloproteinase-1 is associated with poor prognosis in colorectal cancer. Nat Med 1996;2:461-2.
48. Zeng ZS, Cohen AM, Guillem JG. Loss of basement membrane type IV collagen is associated with increased expression of metalloproteinases 2 and 9 (MMP-2 and MMP-9) during human colorectal tumorigenesis. Carcinogenesis 1999;20:749-55.
49. Garbett EA, Reed MW, Brown NJ. Proteolysis in human breast and colorectal cancer. Br J Cancer 1999;81:287-93.
50. Adachi Y, Yamamoto H, Itoh F, Hinoda Y, Okada Y, Imai K. Contribution of matrilysin (MMP-7) to the metastatic pathway of human colorectal cancers. Gut 1999;45:252-8.
51. Ochieng J, Green B, Evans S, James O, Warfield P. Modulation of the biologic functions of galectin-3 by matrix metalloproteinases. Biochim Biophys Acta 1998;1379:97-106.
52. Ochieng J, Fridman R, Nangia-Makker P, Kleiner DE, Liotta LA, Stetler-Stevenson WG, Raz A. Galectin-3 is a novel substrate for human matrix metalloproteinases-2 and -9. Biochemistry 1994;33:14109-14.