Introducing α(1,2)-linked fucose into hepatocarcinoma cells inhibits vasculogenesis and tumor growth

International Journal of Cancer

Volumn 121, Issue 8, 2007, Pages 1680-1689

  Mathieu, Sylvie ^a   Gerolami, René ^a   Luis, José ^b   Carmona, Sylvie ^a   Kol, Ossarath ^c   Crescence, Lydie ^a   Garcia, Stéphane ^a   Borentain, Patrick ^a   El Battari, Assou ^a  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

Author keywords

Antitumor; E selectin; Sialyl Lewis; Vasculogenesis; (1,2) fucosyltransferase I

Indexed keywords

ALPHA 1,2 FUCOSYLTRANSFERASE 1; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FUCOSYLTRANSFERASE; SIALYL LEWIS X ANTIGEN; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CELL ADHESION; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GROWTH INHIBITION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MOLECULAR INTERACTION; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR VOLUME;

EID: 34548668411     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22797     Document Type: Article

References (45)

1. Lowe JB. Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr Opin Cell Biol 2003;15:531-8.
2. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994;76:301-14.
3. Kannagi R. Molecular mechanism for cancer-associated induction of sialyl Lewis X and sialyl Lewis A expression-the Warburg effect revisited. Glycoconj J 2004;20:353-64.
4. Borsig L, Wong R, Hynes RO, Varki NM, Varki A. Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc Natl Acad Sci USA 2002;99:2193-8.
5. Taverna D, Moher H, Crowley D, Borsig L, Varki A, Hynes RO. Increased primary tumor growth in mice null for β3- or β3/β5-integrins or selectins. Proc Natl Acad Sci USA 2004;101:763-8.
6. Yu Y, Moulton KS, Khan MK, Vineberg S, Boye E, Davis VM, O'Donnell PE, Bischoff J, Milstone DS. E-selectin is required for the antiangiogenic activity of endostatin. Proc Natl Acad Sci USA 2004;101:8005-10.
7. Nguyen M, Strubel NA, Bischoff J. A role for sialyl Lewis-X/A glycoconjugates in capillary morphogenesis. Nature 1993;365:267-9.
8. Koike T, Kimura N, Miyazaki K, Yabuta T, Kumamoto K, Takenoshita S, Chen J, Kobayashi M, Hosokawa M, Taniguchi A, Kojima T, Ishida N, et al. Hypoxia induces adhesion molecules on cancer cells: a missing link between Warburg effect and induction of selectin-ligand carbohydrates. Proc Natl Acad Sci USA 2004;101:8132-7.
9. Koch AE, Halloran MM, Haskell CJ, Shah MR, Polverini PJ. Angiogenesis mediated by soluble forms of E-selectin and vascular cell adhesion molecule-1. Nature 1995;376:517-19.
10. Tei K, Kawakami-Kimura N, Taguchi O, Kumamoto K, Higashiyama S, Taniguchi N, Toda K, Kawata R, Hisa Y, Kannagi R. Roles of cell adhesion molecules in tumor angiogenesis induced by cotransplantation of cancer and endothelial cells to nude rats. Cancer Res 2002;62:6289-96.
11. Mathieu S, Prorok M, Benoliel AM, Uch R, Langlet C, Bongrand P, Gerolami R, El-Battari A. Transgene expression of α(1,2)-fucosyltransferase-I (FUT1) in tumor cells selectively inhibits sialyl-Lewis x expression and binding to E-selectin without affecting synthesis of sialyl-Lewis a or binding to P-selectin. Am J Pathol 2004;164:371-83.
12. Oriol R. Genetic control of the fucosylation of ABH precursor chains. Evidence for new epistatic interactions in different cells and tissues. J Immunogenet 1990;17:235-45.
13. Mitoma J, Petryniak B, Hiraoka N, Yeh JC, Lowe JB, Fukuda M. Extended core 1 and core 2 branched O-glycans differentially modulate sialyl Lewis X-type L-selectin ligand activity. J Biol Chem 2003;278:9953-61.
14. Prorok-Hamon M, Notel F, Mathieu S, Langlet C, Fukuda M, El-Battari A. N-glycans of core2 β(1,6)-N-acetylglucosaminyltransferase-I (C2GnT-I) but not those of α(1,3)-fucosyltransferase-VII (FucT-VII) are required for the synthesis of functional P-selectin glycoprotein ligand-1 (PSGL-1): effects on P-, L- and E-selectin binding. Biochem J 2005;391:491-502.
15. Rigot V, Lehmann M, Andre F, Daemi N, Marvaldi J, Luis J. Integrin ligation and PKC activation are required for migration of colon carcinoma cells. J Cell Sci 1998;111(Pt 20):3119-27.
16. Donovan D, Brown NJ, Bishop ET, Lewis CE. Comparison of three in vitro human angiogenesis assays with capillaries formed in vivo. Angiogenesis 2001;4:113-21.
17. Remacle-Bonnet M, Garrouste F, Baillat G, Andre F, Marvaldi J, Pommier G. Membrane rafts segregate pro- from anti-apoptotic insulin-like growth factor-I receptor signaling in colon carcinoma cells stimulated by members of the tumor necrosis factor superfamily. Am J Pathol 2005;167:761-73.
18. Leist M, Gantner F, Bohlinger I, Tiegs G, Germann PG, Wendel A. Tumor necrosis factor-induced hepatocyte apoptosis precedes liver failure in experimental murine shock models. Am J Pathol 1995;146:1220-34.
19. Osborne CK, Hobbs K, Clark GM. Effect of estrogens and antiestrogens on growth of human breast cancer cells in athymic nude mice. Cancer Res 1985;45:584-90.
20. El-Battari A, Prorok M, Angata K, Mathieu S, Zerfaoui M, Ong E, Suzuki M, Lombardo D, Fukuda M. Different glycosyltransferases are differentially processed for secretion, dimerization, and autoglycosylation. Glycobiology 2003;13:941-53.
21. Zanetta JP, Timmerman P, Leroy Y. Gas-liquid chromatography of the heptafluorobutyrate derivatives of the O-methyl-glycosides on capillary columns: a method for the quantitative determination of the monosaccharide composition of glycoproteins and glycolipids. Glycobiology 1999;9:255-66.
22. Pons A, Richet C, Robbe C, Herrmann A, Timmerman P, Huet G, Leroy Y, Carlstedt I, Capon C, Zanetta JP. Sequential GC/MS analysis of sialic acids, monosaccharides, and amino acids of glycoproteins on a single sample as heptafluorobutyrate derivatives. Biochemistry 2003;42:8342-53.
23. Prieto PA, Larsen RD, Cho M, Rivera HN, Shilatifard A, Lowe JB, Cummings RD, Smith DF. Expression of human H-type α1,2-fucosyltransferase encoding for blood group H(O) antigen in Chinese hamster ovary cells. Evidence for preferential fucosylation and truncation of polylactosamine sequences. J Biol Chem 1997;272:2089-97.
24. Du MH, Spohr U, Lemieux RU. The recognition of three different epitopes for the H-type 2 human blood group determinant by lectins of Ulex europaeus, Galactia tenuiflora and Psophocarpus tetragonolobus (winged bean). Glycoconj J 1994;11:443-61.
25. Yamamoto K, Konami Y, Irimura T. Sialic acid-binding motif of Maackia amurensis lectins. J Biochem (Tokyo) 1997;121:756-61.
26. Kannagi R, Izawa M, Koike T, Miyazaki K, Kimura N. Carbohydrate-mediated cell adhesion in cancer metastasis and angiogenesis. Cancer Sci 2004;95:377-84.
27. Hakomori S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res 1996;56:5309-18.
28. Wang QY, Guo P, Duan LL, Shen ZH, Chen HL. α-1,3- Fucosyltransferase-VII stimulates the growth of hepatocarcinoma cells via the cyclin-dependent kinase inhibitor p27Kip1. Cell Mol Life Sci 2005;62:171-8.
29. Liu F, Qi HL, Zhang Y, Zhang XY, Chen HL. Transfection of the c-erbB2/neu gene upregulates the expression of sialyl Lewis X, α1,3- fucosyltransferase VII, and metastatic potential in a human hepatocarcinoma cell line. Eur J Biochem 2001;268:3501-12.
30. Staber PB, Linkesch W, Zauner D, Beham-Schmid C, Guelly C, Schauer S, Sill H, Hoefler G. Common alterations in gene expression and increased proliferation in recurrent acute myeloid leukemia. Oncogene 2004;23:894-904.
31. Lehmann M, El Battari A, Abadie B, Martin JM, Marvaldi J. Role of α v β5 and α v β6 integrin glycosylation in the adhesion of a colonic adenocarcinoma cell line (HT29-D4). J Cell Biochem 1996;61:266-77.
32. Samih N, Hovsepian S, Notel F, Prorok M, Zattara-Cannoni H, Mathieu S, Lombardo D, Fayet G, El-Battari A. The impact of N- and O-glycosylation on the functions of Glut-1 transporter in human thyroid anaplastic cells. Biochim Biophys Acta 2003;1621:92-101.
33. Miyashita K, Shiraki K, Fuke H, Inoue T, Yamanaka Y, Yamaguchi Y, Yamamoto N, Ito K, Sugimoto K, Nakano T. The cyclin-dependent kinase inhibitor flavopiridol sensitizes human hepatocellular carcinoma cells to TRAIL-induced apoptosis. Int J Mol Med 2006;18:249-56.
34. Goupille C, Marionneau S, Bureau V, Hallouin F, Meichenin M, Rocher J, Le Pendu J. α1,2Fucosyltransferase increases resistance to apoptosis of rat colon carcinoma cells. Glycobiology 2000;10:375-82.
35. Burdick MM, Chu JT, Godar S, Sackstein R. HCELL is the major E- and L-selectin ligand expressed on LS174T colon carcinoma cells. J Biol Chem 2006;281:13899-905.
36. Gao C, Guo H, Downey L, Marroquin C, Wei J, Kuo PC. Osteopontin-dependent CD44v6 expression and cell adhesion in HepG2 cells. Carcinogenesis 2003;24:1871-8.
37. de Graffenried CL, Bertozzi CR. The roles of enzyme localisation and complex formation in glycan assembly within the Golgi apparatus. Curr Opin Cell Biol 2004;16:356-63.
38. Colley KJ. Golgi localization of glycosyltransferases: more questions than answers. Glycobiology 1997;7:1-13.
39. Kohler JJ, Bertozzi CR. Regulating cell surface glycosylation by small molecule control of enzyme localization. Chem Biol 2003;10:1303-11.
40. Opat AS, Houghton F, Gleeson PA. Medial Golgi but not late Golgi glycosyltransferases exist as high molecular weight complexes. Role of luminal domain in complex formation and localization. J Biol Chem 2000;275:11836-45.
41. Zerfaoui M, Fukuda M, Langlet C, Mathieu S, Suzuki M, Lombardo D, El-Battari A. The cytosolic and transmembrane domains of the β1,6 N-acetylglucosaminyltransferase (C2GnT) function as a cis to medial/Golgi-targeting determinant. Glycobiology 2002;12:15-24.
42. Goupille C, Hallouin F, Meflah K, Le Pendu J. Increase of rat colon carcinoma cells tumorigenicity by α(1-2) fucosyltransferase gene transfection. Glycobiology 1997;7:221-9.
43. Yazawa S, Nishimura T, Ide M, Asao T, Okamura A, Tanaka S, Takai I, Yagihashi Y, Saniabadi AR, Kochibe N. Tumor-related expression of α1,2fucosylated antigens on colorectal carcinoma cells and its suppression by cell-mediated priming using sugar acceptors for α1, 2fucosyltransferase. Glycobiology 2002;12:545-53.
44. Vajkoczy P, Blum S, Lamparter M, Mailhammer R, Erber R, Engelhardt B, Vestweber D, Hatzopoulos AK. Multistep nature of microvascular recruitment of ex vivo-expanded embryonic endothelial progenitor cells during tumor angiogenesis. J Exp Med 2003;197:1755-65.
45. Brandner B, Kurkela R, Vihko P, Kungl AJ. Investigating the effect of VEGF glycosylation on glycosaminoglycan binding and protein unfolding. Biochem Biophys Res Commun 2006;340:836-9.