Transfection of α(1,3)fucosyltransferase antisense sequences impairs the proliferative and tumorigenic ability of human colon carcinoma cells

Molecular Carcinogenesis

Volumn 27, Issue 4, 2000, Pages 280-288

  Hiller, Kara M ^a   Mayben, John P ^a   Bendt, Katharine M ^a   Manousos, George A ^a   Senger, Kate ^a   Cameron, H Scott ^a   Weston, Brent W ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Antisense; Colon cancer; Fucosyltransferase; Proliferation

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; FUCOSYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CARCINOGENICITY; CELL PROLIFERATION; COLON CARCINOGENESIS; COLON CARCINOMA; CONTROLLED STUDY; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL;

ANIMALS; CELL DIVISION; COLONIC NEOPLASMS; FUCOSYLTRANSFERASES; HUMANS; MICE; MICE, NUDE; OLIGONUCLEOTIDES, ANTISENSE; TRANSFECTION; TUMOR CELLS, CULTURED;

ANIMALIA; MUS MUSCULUS;

EID: 0034027333     PISSN: 08991987     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2744(200004)27:4<280::AID-MC6>3.0.CO;2-L     Document Type: Article

References (80)

1. x determinant of myeloid and tumor cells. Science 1990;250:1132-1135.
2. Srinivas U, Pahlsson P, Lundblad A. E-selectin/sialyl Lewis a-dependent adhesion of colon cancer cells is inhibited differently by antibodies against E-selectin ligands. Scand J Immunol 1996;44:197-203.
3. Fukuda M. Possible roles of tumor-associated carbohydrate antigens. Cancer Res 1996;56:2237-2244.
4. Nakamori S, Kameyama M, Imaoka S, et al. Increased expression of sialyl Lewis x antigen correlates with poor survival in patients with colorectal carcinoma. Cancer Res 1993;53:3632-3637.
5. Hoff S, Irimura T, Matsushita Y, Ota D, Cleary K, Hakamori S. Metastatic potential of colon carcinoma. Expression of ABO/Lewis-related antigens. Arch Surg 1990;125: 206-209.
6. x expression in gastric carcinoma correlates with venous invasion and poor outcome. Gastroenterology 1998;114:462-470.
7. a in lung cancer. J Thorac Cardiovasc Surg 1994;108:329-336.
8. a antigen. Int J Cancer 1996;69:290-294.
9. Pleskow DK, Berger HJ, Gyves J, Allen E, McLean A, Podolsky DK. Evaluation of a serologic marker, CA19-9, in the diagnosis of pancreatic cancer. Ann Intern Med 1989; 110:704-709.
10. Herlyn M, Sears HF, Verrill H, Koprowski H. Increased sensitivity in detecting tumor-associated antigens in sera of patients with colorectal carcinoma. J Immunol Methods 1984;75:15-21.
11. Kuusela P, Jalanko H, Roberts P, et al. Comparison of CA 19-9 and carcinoembryonic antigen (CEA) levels in the serum of patients with colorectal diseases. Br J Cancer 1984;49:135-139.
12. Kuijipers T. Terminal glycosyltransferase activity: a selective role in cell adhesion. Blood 1993;81:873-882.
13. Candelier JJ, Mollicone R, Mennesson B, et al. Alpha-3-fucosyltransferases and their glycoconjugate antigen products in the developing human kidney. Lab Invest 1993; 69:449-459.
14. Stroup GB, Anumula KR, Kline TF, Caltabiano MM. Identification and characterization of two distinct alpha(1-3)-L-fucosyltransferase activities in human colon carcinoma. Cancer Res 1990;50:6787-6792.
15. Mollicone R, Candelier JJ, Mennesson B, Couillin P, Venot AP, Oriol R. Five specificity patterns of (1-3)-α-L-fucosyltransferase activity defined by use of synthetic oligosaccharide acceptors. Carbohydr Res 1992;228:265-276.
16. Macher BA, Holmes EH, Swiedler SJ, Stults CLM, Srnka CA. Human α(1,3)fucosyltransferases. Glycobiology 1991;6: 577-584.
17. Mollicone R, Candelier J, Reguigne I, Couillin P, Fletcher A, Oriol R. Molecular genetics of α-L-fucosyltransferase genes (H, Se, Le, FUT4, FUT5, and FUT6). Transfus Clin Biol 1994; 2:91-97.
18. Kukowska-Latallo JF, Larsen RD, Nair RP, Lowe JB. A cloned human cDNA determines expression of a mouse stage-specific embryonic antigen and the Lewis blood group α(1,3/1,4)fucosyltransferase. Genes Devel 1990;4: 1288-1303.
19. Goelz SE, Hession C, Goff D, et al. ELFT: A gene that directs the expression of an ELAM-1 ligand. Cell 1990;63: 1349-1356.
20. Lowe JB, Kukowska-Latallo JF, Nair RP, et al. Molecular cloning of a human fucosyltransferase gene that determines expression of the Lewis x and Vim-2 epitopes but not ELAM-1-dependent cell adhesion. J Biol Chem 1991;266: 17467-17477.
21. Kumar R, Potvin B, Muller WA, Stanley P. Cloning of a human α(1,3)-fucosyltranferase gene that encodes ELFT but does not confer ELAM-1 recognition on Chinese hamster ovary cell transfectants. J Biol Chem 1991;266: 21777-21783.
22. Weston BW, Nair RP, Larsen RD, Lowe JB. Isolation of a novel human α(1,3)fucosyltransferase gene and molecular comparison to the human Lewis blood group α(1,3/1,4)fucosyltransferase. J Biol Chem 1992;267: 4152-4160.
23. Weston BW, Smith PL, Kelly RJ, Lowe JB. Molecular cloning of a fourth member of a human α(1,3)fucosyltransferase gene family. J Biol Chem 1992;267:24575-24584.
24. Koszdin KL, Bowen BR. The cloning and expression of a human α-1,3 fucosyltransferase capable of forming the E-selectin ligand. Biochem Biophys Res Commun 1992;187: 152-157.
25. Sasaki K, Kurata K, Funayama K, et al. Expression cloning of a novel α(1,3)-fucosyltransferase that is involved in biosynthesis of the sialyl Lewis x carbohydrate determinants in leukocytes. J Biol Chem 1994;269:14730-14737.
26. Natsuka S, Gersten K, Zenita K, Kannagi R, Lowe JB Molecular cloning of a cDNA encoding a novel human leukocyte α-1,3-fucosyltransferase capable of synthesizing the sialyl Lewis x determinant. J Biol Chem 1994;269: 16789-16794.
27. Kaneko M, Kudo T, Iwasaki H, et al. κ-1,3-Fucosyl-transferase IX (Fuc-TIX) is very highly conserved between human and mouse; molecular cloning, characterization and tissue destribution of human Fuc-TIX. FEBS Lett 1999;452: 237-242.
28. Cameron HS, Szczepaniak DA, Weston BW. Expression of human chromosome 19p α(1,3)fucosyltransferase genes in normal tissues: alternative splicing, polyadenylation, and isoforms. J Biol Chem 1995;270:20112-20122.
29. Yago K, Zenita K, Ginya H, et al. Expression of alpha-(1,3)-fucosyltransferases which synthesize sialyl Le(x) and sialyl Le(a), the carbohydrate ligands for E-and P-selectins in human malignant cell lines. Cancer Res 1993;53: 5559-5565.
30. Mannori G, Crottet P, Cecconi O, et al. Differential colon cancer cell adhesion to E-, P-, and L-selectin: Role of mucin-type glycoproteins. Cancer Res 1995;55:4425-4431.
31. Baeckstrom D, Zhang K, Asker N, Ruetschi U, Ek M, Hansson GC. Expression of the leukocyte-associated sialoglycoprotein CD43 by a colon carcinoma cell line. J Biol Chem 1995; 270:13688-13692.
32. Zhang K, Baeckstrom D, Brevinge H, Hansson GC. Comparison of sialyl-Lewis-a-carrying CD43 and MUC1 mucins secreted from a colon carcinoma cell line for E-selectin binding and inhibition of leukocyte adhesion. Tumor Biol 1997;18:175-187.
33. Feizi T. Demonstration by monoclonal antibodies that carbohydrate structures of glycoproteins and glycolipids are oncodevelopmental antigens. Nature 1985;314:53-57.
34. Hakomori S. Glycosphingolipids as differentiation-dependent, tumor-associated markers and as regulators of cell proliferation. Trends Biochem Sci 1984;9:453-456.
35. Hakomori S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res 1996;56:5309-5318.
36. a antigen with the metastatic potential human colon cancer cells. Anticancer Res 1997;17:3505-3512.
37. Takada A, Ohmori K, Taohasho N, et al. Adhesion of human cancer cells to vascular endothelium mediated by a carbohydrate antigen, sialyl Lewis A. Biochem Biophys Res Commun 1991;179:713-719.
38. Takada A, Ohmori K, Yoneda T, et al. Contribution of carbohydrate antigens sialyl Lewis A and sialyl Lewis X to adhesion of human cancer cells to vascular endothelium. Cancer Res 1993;53:354-361.
39. Sawada R, Tsuboi S, Fukuda M. Differential E-selectin-dependent adhesion efficiency in sublines of a human colon cancer exhibiting distinct metastatic potentials. J Biol Chem 1994;269:1425-1431.
40. Chen CJ, Li LJ, Maruya A, Shively JE. In vitro and in vivo footprint analysis of the promoter of carcinoembryonic antigen in colon carcinoma cells: Effects of interferon treatment. Cancer Res 1995;55:3873-3882.
41. Grimm T, Johnson JP. Ectopic expression of carcinoembryonic antigen by a melanoma cell leads to changes in the transcription of two additional cell adhesion molecules. Cancer Res 1995;55:3254-3257.
42. Obrink B. CEA adhesion molecules: Multifunctional proteins with signal-regulatory properties. Curr Opin Cell Biol 1997; 9:616-626.
43. Zbar AP, Lemoine NR, Wadhwa M, Thomas H, Snary D, Kmiot WA. Biological therapy: Approaches in colorectal cancer. Br J Cancer 1998;77:683-693.
44. Stanners CP, DeMarte L, Rojas M, Gold P, Fuks A. Opposite functions for two classes of genes of the human carcinoembryonic antigen family. Tumor Biol 1995:16:23-31.
45. Weston BW, Hiller KM, Mayben JM, et al. Expression of human α(1,3)fucosyltransferase antisense sequences inhibits selectin-mediated adhesion and liver metastases of colon carcinoma cells. Cancer Res 1999;59:2127-2135.
46. Mollicone R, Reguigne I, Kelly RJ, et al. Molecular basis for Lewis α(1,3/1,4)fucosyltransferase gene deficiency in Lewis negative Indonesian pedigrees. J Biol Chem 1994;269: 20987-20994.
47. Majuri ML, Niemela R, Tiisala S, Renkonen O, Renkonen R. Expression and function of alpha 2,3-sialyl-and alpha 1,3/ 1,4-fucosyltransferases in colon adenocarcinorna cell lines: role in synthesis of E-selectin counter-receptors. Int J Cancer 1995;63:551-559.
48. Ono M, Sakamoto M, Ino Y, et al. Cancer cell morphology at the invasive front and expression of cell adhesion-related carbohydrate in the primary lesion of patients with colorectal carcinoma with liver metastasis Cancer 1996;78: 1179-1186.
49. Kuo TH, Kubota T, Watanabe, et al. Liver colonization completence governs colon cancer metastasis. Proc Natl Acad Sci USA 1995;92:12085-12089.
50. Lasky L. Selectins: interpreters of cell-specific carbohydrate information during inflammation. Science 1992;258: 964-969.
51. Sass PM. The involvement of selectins in cell adhesion, tumor progression, and metastasis. Cancer Invest 1998;16: 322-328.
52. McEver RP. Selectin-mediated interactions during inflammation and metastasis. Glycoconjugate J 1997;14: 585-591.
53. Nowacki MP, Janik P, Nowacki PM. Inflammation and metastases. Med Hypotheses 1996;47:193-195.
54. Yamada N, Chung Y-S, Maeda K, et al. Increased expression of sialyl Lewis A and sialyl Lewis X in liver metastases of human colorectal carcinoma. Invasion Metastasis 1995;15: 95-102.
55. Yamada N, Chung YS, Takatsuka S, et al. Increased sialyl Lewis A expression and fucosyltransferase activity with acquisition of a high metastatic capacity in a colon cancer cell line. Br J Cancer 1997;76:582-587.
56. Nguyen M, Strubel NA, Bischoff J. A role for sialyl Lewis-x/a glycoconjugates in capillary morphogenesis. Nature 1993; 365:267-269.
57. Coffey RJ, Goustin AS, Soderquist AM, et al. Transforming growth factor α and β expression in human colon cancer lines: implications for an autocrine model. Cancer Res 1987; 47:4590-4594.
58. Barnard JA, Beauchamp RD, Coffey RJ, Moses HL. Regulation of intestinal epithelial growth by transforming growth factor type β. Proc Natl Acad Sci USA 1989;86: 1578-1582.
59. Balaji KC, Koul H, Mitra S, et al. Antiproliferative effects of c-myc antisense oligonucleotide in prostate cancer cells: a novel therapy in prostate cancer. Urology 1997;50: 1007-1015.
60. Buckhaults P, Chem L, Fregien N, Pierce M. Transcriptional regulation of N-acetylglucosaminyltransferase V by the src oncogene. J Biol Chem 1997;272:19575-19581.
61. Wojciechowicz DC, Park PY, Paty PB. Beta 1-6 branching of N-linked carbohydrate is associated with K-ras mutation in human colon carcinoma cell lines. Biochem Biophys Res Comm 1995;212:758-766.
62. DeJong KP, Stellema R, Karrenbeld A, et al. Clinical relevance of transforming growth factor α, epidermal growth factor receptor, p53, and ki67 in colorectal liver metastases and corresponding primary tumors. Hepatology 1998;28:971-979.
63. Snow DM, Hart GW. Nuclear and cytoplasmic glycosylation. Int Rev Cytol 1998;181:43-74.
64. DeGiovanni C, Landuzzi L, Frabetti F, et al. Antisense epidermal growth factor receptor transfection impairs the proliferative ability of human rhabdomyosarcoma cells. Cancer Res 1996;56:3898-3901.
65. Singh P, Owlia A, Varro A, Dai B, Rajaraman S, Wood T. Gastrin gene expression is required for the proliferation and tumorigenicity of human colon cancer cells. Cancer Res 1996;56:4111-4115.
66. Russell L, Waring P, Beaver JP. Increased cell surface exposure of fucose residues is a late event in apoptosis. Biochem Biophys Res Commun 1998;250:449-453.
67. Nakada H, Inoue M, Yamashina I. Metabolic changes of E-selectin caused by the binding of a mucin carrying sialyl Lewis a antigens. Biochem Biophys Res Commun 1997;234: 559-563.
68. Furie B, Furie B. Leukocyte crosstalk at the vascular wall. Thromb Haemost 1997;78:306-309.
69. Kim YJ Borsig L, Varki NM, Varki A. P-selectin deficiency attenuates tumor growth and metastasis. Proc Natl Acad Sci USA 1998;95:9325-9330.
70. Bry L, Falk PG, Gordan JL. Genetic engineering of carbohydrate biosynthetic pathways in transgenic mice demonstrates cell cycle-associated regulation of glycoconjugate production in small intestinal epithelial cells. Proc Natl Acad Sci USA 1996;93:1161-1166.
71. Hilton E, Chandrasekaran V, Rindos P, Isenberg HD. Association of recurrent candidal vaginitis with inheritance of Lewis blood group antigens. J Infect Dis 1995;172: 1616-1619.
72. Green D, Jarrett O, Ruth KJ, Folsom AR, Liu K. Relationship among Lewis phenotype, clotting factors, and other cardiovascular risk factors in young adults. J Lab Clin Med 1995;125:334-339.
73. Mollicone R, Reguigne I, Fletcher A, et al. Molecular basis for plasma α(1,3) fucosyltransferase gene deficiency (FUT6). J Biol Chem 1994;269:12662-12671.
74. Martin-Satue M, Marrugat R, Cancelas JA, Blanco J. Enhanced expression of α(1,3)fucosyltransferase genes correlates with E-selectin-mediated adhesion and metastatic potential of human lung adenocarcinoma cells. Cancer Res 1998;58:1544-1550.
75. Mas E, Pasqualini E, Caillol N, et al. Fucosyltransferase activities in human pancreatic tissue: Comparative study between cancer tissues and established tumoral cell lines. Glycobiology 1998;8:605-613.
76. Gewirtz AM, Stein CA, Glazer PM. Facilitating oligonucleotide delivery: helping antisense deliver on its promise. Proc Natl Acad Sci USA 1996;93:3161-3163.
77. Narayanan R. Harnessing the power of antisense technology for combination chemotherapy. J Natl Cancer Inst 1997;89: 107-108.
78. Philips JA, Craig SJ, Bayley D, Christian RA, Geary R, Nicklin PL. Pharmacokinetics, metabolism, and elimination of a 20-mer phosphorothioate oligodeoxynucleotide(CGP 69846A) after intravenous and subcutaneous administration. Biochem Pharmacol 1997;54:657-668.
79. Hughes JA, Aronsohn AI, Avrutskaya AV, Juliano RL. Evaluation of adjuvants that enhance the effectiveness of antisense oligodeoxynucleotides. Pharm Res 1995;13: 404-410.
80. Lewis JG, Lin KY, Kothavale A, et al. A serum-resistant cytofectin for cellular delivery of antisense oligodeoxynucleotides and plasmid DNA. Proc Natl Acad Sci USA 1996; 93:3176-3181.