De-N-acetyl-gangliosides in humans: Unusual subcellular distribution of a novel tumor antigen

Cancer Research

Volumn 59, Issue 6, 1999, Pages 1337-1346

  Chammas, Roger ^a   Sonnenburg, Justin L ^a   Watson, Nicki E ^a   Tai, Tadashi ^b   Farquhar, Marilyn G ^a   Varki, Nissi M ^a   Varki, Ajit ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Tokyo Metropolitan Inst Technol   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GANGLIOSIDE; GLYCOSPHINGOLIPID; TUMOR ANTIGEN;

ANTIGEN DETECTION; ARTICLE; CELLULAR DISTRIBUTION; DIAGNOSTIC VALUE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LYMPHOMA; MELANOMA; PRIORITY JOURNAL; TUMOR DIAGNOSIS;

ANTIGENS, NEOPLASM; ANTIGENS, SURFACE; CARCINOMA; CELL CYCLE; CELL MEMBRANE; GANGLIOSIDES; HUMANS; LYMPHOMA; LYSOSOMES; MELANOMA; NEOPLASMS; SUBCELLULAR FRACTIONS; TISSUE DISTRIBUTION;

EID: 0033559608     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (84)

1. Van Echten, G., and Sandhoff, K. Ganglioside metabolism. Enzymology, topology, and regulation. J. Biol. Chem., 268: 5341-5344, 1993.
2. Zeller, C. B., and Marchase, R. B. Gangliosides as modulators of cell function. Am. J. Physiol. Cell Physiol., 262: C1341-C1355, 1992.
3. Maggio, B. The surface behavior of glycosphingolipids in biomembranes: a new frontier of molecular ecology. Prog. Biophys. Mol. Biol., 62: 55-117, 1994.
4. Karlsson, K. A. Microbial recognition of target-cell glycoconjugates. Curr. Opin. Struct. Biol., 5: 622-635, 1995.
5. Hakomori, S., and Igarashi, Y. Functional role of glycosphingolipids in cell recognition and signaling. J. Biochem. (Tokyo), 118: 1091-1103, 1995.
6. Hakomori, S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res., 56: 5309-5318, 1996.
7. R having tetraosyl to octaosyl core. Biochemistry. 35: 758-769, 1996.
8. Stroud, M. R., Handa, K., Salyan, M. E. K., Ito, K., Levery, S. B., Hakomori, S., Reinhold, B. B., and Reinhold, V. N. Monosialogangliosides of human myelogenous leukemia HL60 cells and normal human leukocytes. 2. Characterization of E-selectin binding fractions, and structural requirements for physiological binding to E-selectin. Biochemistry. 35: 770-778, 1996.
9. Collins, B. E., Yang, L. J. S., Mukhopadhyay, G., Filbin, M. T., Kiso, M., Hasegawa, A., and Schnaar, R. L. Sialic acid specificity of myelin-associated glycoprotein binding. J. Biol. Chem., 272: 1248-1255, 1997.
10. Collins, B. E., Kiso, M., Hasegawa, A., Tropak, M. B., Roder, J. C., Crocker, P. R., and Schnaar, R. L. Binding specificities of the sialoadhesin family of I-type lectins. Sialic acid linkage and substructure requirements for binding of myelin-associated glycoprotein, Schwann cell myelin protein, and sialoadhesin. J. Biol. Chem., 272: 16889-16895, 1997.
11. D3 synthase). J. Biol. Chem., 269: 15950-15956, 1994.
12. Nara, K., Watanabe, Y., Maruyama, K., Kasahara, K., Nagai, Y., and Sanai, Y. Expression cloning of a CMP-NeuAc:NeuAcα2-3Galβ1-4Glcβ1-1'Cer α2,8-sialyltransferase (GD3 synthase) from human melanoma cells. Proc. Natl. Acad. Sci. USA, 91: 7952-7956, 1994.
13. Yamashiro, S., Okada, M., Haraguchi, M., Furukawa, K., Lloyd, K. O., and Shiku, H. Expression of α2,8-sialyltransferase (GD3 synthase) gene in human cancer cell lines: high level expression in melanomas and up-regulation in activated T lymphocytes. Glycoconjugate J., 12: 894-900, 1995.
14. D3, a prominent ganglioside of human melanoma. Detection and characterisation by mouse monoclonal antibody. J. Exp. Med., 155: 1133-1147, 1982.
15. Siddiqui, B., Buehler, J., DeGregorio, M. W., and Macher, B. A. Differential expression of ganglioside GD3 by human leukocytes and leukemia cells. Cancer Res., 44: 5262-5265, 1984.
16. Real, F. X., Houghton, A. N., Albino, A. P., Cordon-Cardo, C., Melamed, M. R., Oettgen, H. F., and Old, L. J. Surface antigens of melanomas and melanocytes defined by mouse monoclonal antibodies: specificity analysis and comparison of antigen expression in cultured cells and tissues. Cancer Res., 45: 4401-4411, 1985.
17. D3 ganglioside: a phase I trial in patients with malignant melanoma. Proc. Natl. Acad. Sci. USA, 82: 1242-1246, 1985.
18. Houghton, A. N., and Scheinberg, D. A. Monoclonal antibodies: potential applications to the treatment of cancer. Semin. Oncol., 13: 165-179, 1986.
19. Vadhan Raj, S., Cordon Cardo, C., Carswell, E., Mintzer, D., Dantis, L., Duteau, C., Templeton, M. A., Oettgen, H. F., Old, L. J., and Houghton, A. N. Phase I trial of a mouse monoclonal antibody against GD3 ganglioside in patients with melanoma: induction of inflammatory responses at tumor sites. J. Clin. Oncol., 6, 1636-1648, 1988.
20. Soiffer, R. J., Chapman, P. B., Murray, C., Williams. L., Unger, P., Collins, H., Houghton, A. N., and Ritz, J. Administration of R24 monoclonal antibody and low-dose interleukin 2 for malignant melanoma. Clin. Cancer Res., 3: 17-24, 1997.
21. Zhang, S. L., Cordon-Cardo, C., Zhang, H. S., Reuter, V. E., Adluri, S., Hamilton, W. B., Lloyd, K. O., and Livingston, P. O. Selection of tumor antigens as targets for immune attack using immunohistochemistry. 1. Focus on gangliosides. Int. J. Cancer, 73: 42-49, 1997.
22. Sen, G., Chakraborty, M., Foon, K. A., Reisfeld, R. A., and Bhattacharya-Chatterjee, M. Induction of IgG antibodies by an anti-idiotype antibody mimicking disialoganglioside GD2. J. Immunother., 21: 75-83, 1998.
23. Yu, A. L., Uttenreuther-Fischer, M. M., Huang, C. S., Tsui, C. C., Gillies, S. D., Reisfeld, R. A., and Kung, F. H. Phase I trial of a human-mouse chimeric anti-disialoganglioside monoclonal antibody ch14.18 in patients with refractory neuroblastoma and osteosarcoma. J. Clin. Oncol., 16: 2169-2180, 1998.
24. Zhang, H., Zhang, S. L., Cheung, N. K. V., Ragupathi, G., and Livingston, P. O. Antibodies against GD2 ganglioside can eradicate syngeneic cancer micrometastases. Cancer Res., 58: 2844-2849, 1998.
25. Schauer, R. Sialic Acids. Chemistry, Metabolism and Function, Cell Biology Monographs, Volume 10. New York: Springer-Verlag, 1982.
26. Varki, A. Diversity in the sialic acids. Glycobiology, 2: 25-40, 1992.
27. D3, by human melanoma cells creates a unique antigenic determinant. Science (Washington DC), 225: 844-846, 1984.
28. Kniep, B., Flegel, W. A., Northoff, H., and Rieber, E. P. CDw60 glycolipid antigens of human leukocytes: structural characterization and cellular distribution. Blood. 82: 1776-1786, 1993.
29. Hanai, N., Dohi, T., Nores, G. A., and Hakomori, S. A novel ganglioside, de-N-acetyl-GM3, acting as a strong promoter for epidermal growth factor receptor kinase and as a stimulator for cell growth. J. Biol. Chem., 263: 6296-6301, 1988.
30. Manzi, A. E., Sjoberg, E. R., Diaz, S., and Varki, A. Biosynthesis and turnover of O-acetyl and N-acetyl groups in the gangliosides of human melanoma cells. J. Biol. Chem., 265: 13091-13103, 1990.
31. Sjoberg, E. R., Chammas, R., Ozawa, H., Kawashima, I., Khoo, K-H., Morris, H. R., Dell, A., Tai, T., and Varki, A. Expression of de-N-acetyl-gangliosides in human melanoma cells is induced by genistein or nocodazole. J. Biol. Chem., 270: 2921-2930, 1995.
32. Higa, H. H., Rogers, G. N., and Paulson, J. C. Influenza virus hemagglutinins differentiate between receptor determinants bearing N-acetyl-, N-glycolyl-, and N,O-diacetylneuraminic acids. Virology, 144: 279-282, 1985.
33. Kelm, S., Schauer, R., Manuguerra, J-C., Gross, H-J., and Crocker, P. R. Modifications of cell surface sialic acids modulate cell adhesion mediated by sialoadhesin and CD22. Glycoconjugate J., 11: 576-585, 1994.
34. Powell, L. D., and Varki, A. I-type lectins. J. Biol. Chem., 270: 14243-14246, 1995.
35. Meri, S., and Pangburn, M. K. Discrimination between activators and nonactivators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H. Proc. Natl. Acad. Sci. USA, 87: 3982-3986, 1990.
36. Michalek, M. T., Mold, C., and Bremer, E. G. Inhibition of the alternative pathway of human complement by structural analogues of sialic acid. J. Immunol., 140: 1588-1594, 1988.
37. Shi, W. X., Chammas, R., Varki, N. M., Powell, L., and Varki, A. Sialic acid 9-O-acetylation on murine erythroleukemia cells affects complement activation, binding to I-type lectins, and tissue homing. J. Biol. Chem., 271: 31526-31532, 1996.
38. M3 directly enhances serine phosphorylation of epidermal growth factor receptor, independently of receptor-receptor interaction. J. Biol. Chem., 269: 1959-1965, 1994
39. Dekan, G., Miettinen, A., Schnabel, E., and Farquhar, M. G. Binding of monoclonal antibodies to glomerular endothelium, slit membranes, and epithelium after in vivo injection: localization of antigens and bound IgGs by immunoelectron microscopy. Am. J. Pathol. 137: 913-927, 1990.
40. Van Lenten, L., and Ashwell, G. Studies on the chemical and enzymatic modification of glycoproteins. J. Biol. Chem., 246: 1889-1894, 1971.
41. Bobbit, J. M. Periodate oxidation of carbohydrates. Adv. Carbohyde. Chem. Biochem., 6: 1-41, 1956.
42. Krishna, M., and Varki, A. 9-O-Acetylation of sialomucins: a novel marker of murine CD4 T cells that is regulated during maturation and activation. J. Exp. Med., 185: 1997-2013, 1997
43. Schmid, I., Uittenbogaart, C. H., and Giorgi, J. V. A gentle fixation and permeabilization method for combined cell surface and intracellular staining with improved precision in DNA quantification. Cytometry, 12: 279-285, 1991.
44. Butor, C., Diaz, S., and Varki, A. High level O-acetylation of sialic acids on N-linked oligosaccharides of rat liver membranes. Differential subcellular distribution of 7-and 9-O-acetyl groups and of enzymes involved in their regulation. J. Biol. Chem., 268: 10197-10206, 1993.
45. Joseph, K. C., Stieber, A., and Gonatas, N. K. Endocytosis of cholera toxin in GERL-like structures of murine neuroblastoma cells pretreated with GM1 ganglioside. Cholera toxin internalization into neuroblastoma GERL. J. Cell Biol., 81: 543-554, 1979.
46. Gonatas, J., Stieber, A., Olsnes, S., and Gonatas, N. K. Pathways involved in fluid phase and adsorptive endocytosis in neuroblastoma. J. Cell Biol., 87: 579-588, 1980.
47. Schneider, Y. J., Tulkens, P., de Duve, C., and Trouet, A. Fate of plasma membrane during endocytosis. I. Uptake and processing of anti-plasma membrane and control immunoglobulins by cultured fibroblasts. J. Cell Biol., 82: 449-465, 1979.
48. Schwarz, A., and Futerman, A. H. Determination of the localization of gangliosides using anti-ganglioside antibodies: comparison of fixation methods. J. Histochem. Cytochem., 45: 611-618, 1997.
49. Urmacher, C., Cordon-Cardo, C., and Houghton, A. N. Tissue distribution of GD3 ganglioside detected by mouse monoclonal antibody R24. Am. J. Dermatopathol., 11: 577-581, 1989.
50. Dippold, W. G., Dienes, H. P., Knuth, A., and Meyer zum, and Buschenfelde, K. H. Immunohistochemical localization of ganglioside GD3 in human malignant melanoma, epithelial tumors, and normal tissues. Cancer Res., 45: 3699-3705, 1985.
51. Graus, F., Cordon-Cardo, C. Houghton, A. N., Melamed, M. R., and Old, L. J. Distribution of the ganglioside GD3 in the human nervous system detected by R24 mouse monoclonal antibody. Brain Res., 324: 190-194, 1984.
52. Prokazova, N. V., and Bergelson, L. D. Gangliosides and atherosclerosis. Lipids, 29: 1-5, 1994.
53. Hara, A., and Taketomi, T. Characterization and changes of glycosphingolipids in the aorta of the Watanabe hereditable hyperlipidemic rabbit. J. Biochem. (Tokyo), 109: 904-908, 1991.
54. Lloyd, K. O., Gordon, C. M., Thampoe, I. J., and DiBenedetto, C. Cell surface accessibility of individual gangliosides in malignant melanoma cells to antibodies is influenced by the total ganglioside composition of the cells. Cancer Res., 52: 4948-4953, 1992.
55. Macala, L. J., and Yohe, H. C. In situ accessibility of murine macrophage gangliosides. Glycobiology, 5: 67-75, 1995.
56. Kurins Gillard, B., Heath, J. P., Thurmon, L. T., and Marcus, D. M. Association of glycosphingolipids with intermediate filaments of human umbilical vein endothelial cells. Exp. Cell Res., 192: 433-444, 1991.
57. Gillard, B. K., Thurmon, L. T., and Marcus, D. M. Association of glycosphingolipids with intermediate filaments of mesenchymal, epithelial, glial, and muscle cells. Cell Motil. Cytoskeleton. 21: 255-271, 1992.
58. Gillard, B. K., Thurmon, L. T., and Marcus, D. M. Variable subcellular localization of glycosphingolipids. Glycobiology, 3: 57-67, 1993.
59. Shogomori, H., Chiba, K., and Hoshi, M. Association of the major ganglioside in sea urchin eggs with yolk lipoproteins. Glycobiology, 7: 391-398, 1997.
60. Tatewaki, K., Yamaki, T., Maeda, Y., Tobioka, H., Piao, H. Z. Yu, H. W., Ibayashi, Y., Sawada, N., and Hashi, K. Cell density regulates crypticity of GM3 ganglioside on human glioma cells. Exp. Cell Res., 233: 145-154, 1997.
61. Van Genderen, I. L., van Meer, G., Slot, J. W., Geuze, H. J., and Voorhout, W. F. Subcellular localization of Forssman glycolipid in epithelial MDCK cells by immunoelectron microscopy alter freeze-substitution. J. Cell Biol., 115: 1009-1019, 1991.
62. Gonatas, N. K. Contributions to the physiology and pathology of the Golgi apparatus. Am. J. Pathol., 145: 751-761, 1994.
63. Sandhoff, K., and Koller, T. Topology of glycosphingolipid degradation. Trends Cell Biol., 6: 98-103, 1996.
64. Peters, M. W., Barber, K. R., and Grant, C. W. Lateral distribution of gangliosides in bilayer membranes: lipid and ionic effects. J. Neurosci., 12: 343-353, 1984.
65. Rock, P., Allietta, M., Young, W. W., Jr., Thompson, T. E., and Tillack, T. W. Organization of glycosphingolipids in phosphatidylcholine bilayers: use of antibody molecules and Fab fragments as morphologic markers. Biochemistry, 29: 8484-8490, 1990.
66. Simons, K., and Ikonen, E. Functional rafts in cell membranes. Nature (Lond.), 387: 569-572, 1997.
67. Brown, D. A., and Rose, J. K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68: 533-544, 1992.
68. Kniep, B., Cinek, T., Angelisovà, P., and Horejsí. V. Association of the GPI-anchored leucocyte surface glycoproteins with ganglioside GM3. Biochem. Biophys. Res. Commun., 203: 1069-1075, 1994.
69. Parton, R. G. Caveolae and caveolins. Curr. Opin. Cell Biol., 8: 542-548, 1996.
70. 1 is concentrated in caveolae. J. Histochem. Cytochem., 42: 155-166, 1994.
71. Sakakibara, K., Momoi, T., Uchida, T., and Nagai, Y. Evidence for association of glycosphingolipid with a colchicine-sensitive microtubule-like cytoskeletal structure of cultured cells. Nature (Lond.), 293: 76-78, 1981.
72. Gillard, B. K., Clement, R. G., and Marcus, D. M. Variations among cell lines in the synthesis of sphingolipids in de novo and recycling pathways. Glycobiology. 8: 885-890, 1998.
73. Gillard, B. K., Thurmon, L. T., Harrell, R. G., Capetanaki, Y., Saito, M., Yu. R. K., and Marcus, D. M. Biosynthesis of glycosphingolipids is reduced in the absence of a vimentin intermediate filament network. J. Cell Sci., 107: 3545-3555, 1994.
74. Gillard, B. K., Clement, R., Colucci-Guyon, E., Babinet, C., Schwarzmann, G . Taki, T., Kasama, T., and Marcus, D. M. Decreased synthesis of glycosphingolipids in cells lacking vimentin intermediate filaments. Exp. Cell Res., 242: 561-572, 1998.
75. Kniep, B., and Skubitz, K. M. Subcellular localization of glycosphingolipids in human neutrophils. J. Leukocyte Biol., 63: 83-88, 1998.
76. Gordon, C. M., and Lloyd, K. O. Endocytosis and recycling of gangliosides in a human melanoma cell line: inhibitory effect of Brefeldin A and monensin. Arch. Biochem. Biophys., 315: 339-344, 1994.
77. Chang, F. M., Li, R. X., and Ladisch, S. Shedding of gangliosides by human medulloblastoma cells. Exp. Cell Res., 234: 341-346, 1997.
78. D3 in adhesion plaques and on the surface of human melanoma cells. Proc. Natl. Acad. Sci. USA, 81: 5767-5771, 1984.
79. Valentino, L. A., and Ladisch, S. Circulating tumor gangliosides enhance platelet activation. Blood, 83: 2872-2877, 1994.
80. Bergelson, L. D. Serum gangliosides as endogenous immunomodulators. Immunol. Today, 16: 483-486, 1995.
81. Tubaro, E., Borelli, G. P., Belogi, L., Cavallo, G., Santoni, A., and Maniniero, F. Effect of a new de-N-acetyl-lysoglycosphingolipid on some tumour models. Eur. J. Pharmacol., 294: 555-563, 1995.
82. Wieser, J. R., Heisner, A., Stehling, P., Oesch, F., and Reutter, W. In vivo modulated N-acyl side chain of N-acetylneuraminic acid modulates the cell contact-dependent inhibition of growth. FEBS Lett., 385: 170-173, 1996.
83. De Maria, R., Lenti, L., Malisan, F., D'Agostino, F., Tomassini, B., Zeuner, A., Rippo, M. R., and Testi, R. Requirement for GD3 ganglioside in CD95-and ceramide-induced apoptosis. Science (Washington DC), 277: 1652-1655, 1997.
84. Mitsuoka, C., Ohmori, K., Kimura, N., Kanamori, A., Komba, S., Ishida, H., Kiso, M., and Kannagi, R. Regulation of selectin binding activity by cyclization of sialic acid moiety of carbohydrate ligands on human leukocytes. Proc. Natl. Acad. Sci. USA, in press, 1999.