Intracellular targeting of the endoplasmic reticulum/nuclear envelope by retrograde transport may determine cell hypersensitivity to verotoxin via globotriaosyl ceramide fatty acid isoform traffic

Journal of Cellular Physiology

Volumn 177, Issue 4, 1998, Pages 646-660

  Arab, Sara ^a   Lingwood, Clifford A ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLOBOTRIAOSYLCERAMIDE; VEROTOXIN;

ANIMAL CELL; ARTICLE; ASTROCYTOMA; BETA CHAIN; CELL COMPARTMENTALIZATION; CELL MEMBRANE TRANSPORT; DRUG RECEPTOR BINDING; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENZYME INACTIVATION; FATTY ACID TRANSPORT; GENE TARGETING; INTERNALIZATION; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; RAT; RIBOSOME SUBUNIT;

ASTROCYTOMA; BACTERIAL TOXINS; BIOLOGICAL TRANSPORT; BRAIN NEOPLASMS; BUTYRATES; CARCINOMA; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; FEMALE; GLYCOLIPIDS; HUMANS; MEMBRANE LIPIDS; MOLECULAR STRUCTURE; NUCLEAR ENVELOPE; OVARIAN NEOPLASMS; RECOMBINANT FUSION PROTEINS; SHIGA-LIKE TOXIN I; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; TUMOR CELLS, CULTURED;

EID: 0031773458     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199812)177:4<646::AID-JCP15>3.0.CO;2-B     Document Type: Article

References (74)

1. Abe, A., Shayman, J.A., and Radin, N. S. (1996) A novel enzyme that catalyzes the esterification of N-acetylsphingosine. J. Biol. Chem., 271:14383-14389.
2. Arab, S., and Lingwood, C.A. (1996) Influence of phospholipid chain length on verotoxin/globotriaosyl ceramide binding in model membranes: Comparison of a surface bilayer film and liposomes. Glycoconj. J., 13:159-166.
3. Arab, S., Russel, E., Chapman, W., Rosen, B., and Lingwood, C. (1997) Expression of the verotoxin receptor glycolipid, globotriaosylceramide, in ovarian hyperplasias. Oncol. Res., 9:553-563.
4. Arab, S., Murakami, M., Dirks, P., Boyd, B., Hubbard, S., Lingwood, C., and Rutka, J. (1998) Verotoxins inhibit the growth of and induce apoptosis in human astrocytoma cells. J Neurooncol. (in press).
5. Baldini, N., Scotlandi, K., Serra, M., Shikita, T., Zini, N., Ognibene, A., Santi, S., Ferracini, R., and Maraldi, N.M. (1995) Nuclear immunolocalization of P-glycoprotein in multidrug-resistant cell lines showing similar mechanisms of doxorubicin distribution. Eur. J. Cell Biol., 68:226-239.
6. Bates, S.E., Mickley, L., Chen, Y., Richert, N., Rudick, J., Biedler, J., and Fojo, A. (1989) Expression of a drug resistance gene in human neuroblastoma cell lines: Modulation by retenoic acid-induced differentiation. Mol. Cell. Biol., 9:4337-4344.
7. Bates, S.E., Currier, S.J., Alvarez, M., and Fojo, A.T. (1992) Modulation of P-glycoprotein phosphorylation and drug transport by sodium butyrate. Biochemistry, 31:6366-6372.
8. Boulanger, J., Petric, M., Lingwood, C.A., Law, H., Roscoe, M., and Karmali, M. (1990) Neutralization receptor-based immunoassay (NeutrELISA) for detection of neutralizing antibodies to Escherichia coli verocytotoxin 1. J. Clin. Microbiol., 28:2830-2833.
9. Boulanger, J., Huesca, M., Arab, S., and Lingwood, C.A. (1994) Universal method for the facile production of glycolipid/lipid matrices for the affinity purification of binding Uganda. Anal. Biochem., 217:1-6.
10. Boyd, B., and Lingwood, C.A. (1989) Verotoxin receptor glycolipid in human renal tissue. Nephron, 57:207-210.
11. Boyd, B., Zhiuyan, Z., Magnusson, G., and Lingwood, C.A. (1994) Lipid modulation of glycolipid receptor function: Presentation of galactose α1-4 galactose disaccharide for verotoxin binding in natural and synthetic glycolipids. Eur. J. Biochem., 223:873-878.
12. Bradley, G., Naik, M., and Ling, V. (1989) P-glycoprotein expression in multidrug-resistant human ovarian carcinoma cell lines. Cancer Res., 49:2790-2796.
13. Burger, K., van der Bijl, P., and van Meer, G. (1996) Topology of sphingolipid galactosyl transferase in ER and Golgi:transbilayer movement of monohexyl sphingolipids is required for higher glycosphingolipid biosynthesis. J. Cell Biol., 133:15-28.
14. Cohen, A., Madrid-Marina, V., Estrov, Z., Freedman, M., Lingwood, C.A., and Dosch, H.-M. (1990) Expression of glycolipid receptors to Shiga-like toxin on human B lymphocytes: A mechanism for the failure of long-lived antibody response to dysenteric disease. Int. Immunol., 2:1-8.
15. Eiklid, K., and Olsnes, S. (1980) Interaction of Shigella cytotoxin with receptors on sensitive and insensitive cells. J. Recept. Res., 1:199-213.
16. Endo, Y., Tsurugi, K., Yutsudo, T., Takeda, Y., Ogasawara, K., and Igarashi, K. (1988) Site of the action of a vero toxin (VT2) from Escherichia coli O157:H7 and a Shiga toxin on eukaryotic ribosomes. Eur. J. Biochem., 171:45-50.
17. Farkas-Himsley, H., Rosen, B., Hill, R., Arab, S., and Lingwood, C.A. (1995) Bacterial colicin active against tumour cells in vitro and in vivo is verotoxin 1. Proc. Natl. Acad. Sci. USA, 92:6996-7000.
18. Cannon, V.P.J., and Gyles, C.L. (1990) Characteristics of the Shigalike toxin produced by Escherichia coli associated with porcine edema disease. Vet. Microbiol., 24:89-100.
19. Gillard, B.K., Thurman, L.T., Harrell, R.G., Capentanaki, Y., Saito, M., Yu, R.K., and Marcus, D.M. (1994) Biosynthesis of glycosphingolipids is reduced in the absence of a vimentin; intermediate filament network. J. Cell Sci., 107:3545-3555.
20. Griffin, P.M. (1995) In: Infections of the Gastrointestinal Tract. M.J. Blaser, P.D. Smith, J.I. Ravdin, H.B. Greenberg, and R.L. Guerrant, eds., Raven Press, New York, pp. 739-761.
21. Haas, I.G. (1994) BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum. Experientia, 50:1012-1020.
22. Head, S., Karmali, M., and Lingwood, C.A. (1991) Preparation of VT1 and VT2 hybrid toxins from their purified dissociated subunits: Evidence for B subunit modulation of A subunit function. J. Biol. Chem., 266:3617-3621.
23. Inokuchi, J.-L, and Radin, N.S. (1987) Preparation of the active isomer of 1-phenyl-2-decanoylamino-3-morpholino-1-propanol, inhibitor of murine glucocerebroside synthetase. J. Lipid Res., 28:565-571.
24. Inward, C.D., Williams, J., Chant, I., Crocker, J., Milford, D.V., Rose, P.E., and Taylor, C.M. (1995) Verocytotoxin-1 induces apoptosis in vero cells. J. Infect., 30:213-218.
25. Jacewicz, M., Feldman, H.A., Donohue-Rolfe, A., Balasubramanian, K.A., and Keusch, G.T. (1989) Pathogenesis of Shigella diarrhea. XIV Analysis of Shiga toxin receptors on cloned HeLa cells. J. Infect. Dis., 159:881-889.
26. Jacewicz, M.S., Acheson, D.W.K., Mobassaleh, M., Donohue-Rolfe, A., Balasubramanian, K.A., and Keusch, G.T. (1995) Maturational regulation of globotriaosylceramide, the Shiga-like toxin 1 receptor, in cultured human gut epithelial cells. J. Clin. Invest., 96:1328-1335.
27. Jans, D. (1994) Nuclear signaling pathways for polypeptide ligands and their membrane receptors? FASEB J., 8:841-847.
28. Johannes, L., Tenza, D., Anthoy, C., and Goud, B. (1997) Retrograde transport of KDEL-bearing B-fragment of Shiga toxin. J. Biol. Chem., 272:19554-19561.
29. Kappeler, F., Itin, C., Schindler, R., and Hauri, H.P. (1994) A dual role for COOH-terminal lysine residues in pre-Golgi retention and endocytosis of ERGIC-53. J. Biol. Chem., 269:6279-6281.
30. Kappeler, F., Klopfenstein D.R.C., Foguet, M., Paccaud, J.-P., and Hauri, H.-P. (1997) The recycling of Ergic-53 in the early secretory pathway. J. Biol. Chem., 272:31801-31808.
31. Keusch, G.T., Acheson, D.W.K., Aaldering, L., Erban, J., and Jacewicz, M.S. (1996) Comparison of the effects of Shiga-like toxin 1 cytokine-and butyrate pretreated human umbilical and Saphenous vein endothelial cells. J. Infect. Dis., 173:1164-1170.
32. Khine, A.A., and Lingwood, C.A. (1994) Capping and receptor mediated endocytosis of cell bound verotoxin (Shiga-like toxin) 1: Chemical identification of an amino acid in the B subunit necessary for efficient receptor glycolipid binding and cellular internafization. J. Cell Physiol., 161:319-332.
33. Khine, A.A., Firtel, M., and Lingwood, C.A. (1998) CD77-dependent retrograde transport of CD19 to the nuclear membrane: Functional relationship between CD77 and CD19 during germinal center B-cell apoptosis. J. Cell. Physiol., 176:281-292.
34. Kiarash, A., Boyd, B., and Lingwood, C.A. (1994) Glycosphingolipid receptor function is modified by fatty acid content: Verotoxin 1 and verotoxin 2c preferentially recognize different globotriaosyl ceramide fatty acid homologues. J. Biol. Chem., 269:11138-11146.
35. Kim, J.H., Johannes, L., Goud, B., Antony, C., Lingwood, C.A., Daneman, R., and Grinstein, S. (1998) Non-invasive measurement of the pH of the endoplasmic reticulum at rest and during calcium release. Proc. Natl. Acad. Sci. USA, 95:2997-3002.
36. Kim, J.H., Lingwood, C.A., Williams, D.B., Furuya, W., Manolson, M.F., and Grinstein, S. (1996) Dynamic measurement of the pH of the Golgi complex in living cells using retrograde transport of the verotoxin receptor. J. Cell. Biol., 134:1387-1399.
37. Krenik, K.D., Kephart, G.M., Offord, K.P., Dunnette, S.L., and Gleich, G.J. (1989) Comparison of antifading agents used in immunofluorescence. J. Immunol, Methods, 117:91-97.
38. Kueng, W., Silber, E., and Eppenberger, U. (1989) Quantification of cells cultured on 96-well plates. Anal. Biochem., 182:16-19.
39. Lavie, Y., Cao, H., Bursten, S.L., Giuliano, A.E., and Cabot, M.C. (1996) Accumulation Of glucosylceramides in multidrug-resistant cancer cells. J. Biol. Chem., 271:19530-19536.
40. Lingwood, C.A. (1994) Verotoxin-binding in human renal sections. Nephron, 66:21-28.
41. Lingwood, C.A. (1996) Aglycone modulation of glycolipid receptor function. Glycoconj. J., 13:495-503.
42. Lingwood, C.A., Law, H., Richardson, S., Petric, M., Brunton, J.L., DeGrandis, S., and Karmali, M. (1987) Glycolipid binding of purified and recombinant Escherichia coli-produced verotoxin in vitro. J. Biol. Chem., 262:8834-8839.
43. Louise, C.B., Kaye, S-A., Boyd, B., Lingwood, C.A., and Obrig, T.G. (1995a) Shiga toxin-associated hemolytic uremic syndrome: Effect of sodium butyrate on sensitivity of human umbilical vein endothelial cells to Shiga toxin. Infect. Immun., 63:2765-2769.
44. Louise, C.B., Moran, T.P., Lingwood, C.A., Del Vecchio, P.J., Culp, D.J., and Obrig, T.G. (1995b) "Binding of [125I]Shiga-like toxin-1 to human endothelial cells: Implications for the pathogenesis of Shiga toxin-associated hemolytic uremic syndrome." Endothelium, 3:159-170.
45. Maloney, M.D., and Lingwood, C.A. (1994) CD19 has a potential CD77 (globotriaosyl ceramide)-binding site with sequence similarity to verotoxin B-subunits: Implications of molecular mimicry for B cell adhesion and enterohemorrhagic Escherichia coli pathogenesis. J. Exp. Med., 780:191-201.
46. Mangeney, M., Lingwood, C.A., Caillou, B., Taga, S., Tursz, T., and Wiels, J. (1993) Apoptosis induced in Burkitt's lymphoma cells via Gb3/CD77, a glycolipid antigen. Cancer Res., 53:5314-5319.
47. Molinari, A., Calcabrini, A., Meschini, S., Stringaro, A., Del Bufalo, D., Cianfriglia, M., and Arancia, G. (1998) Detection of P-glycoprotein in the Golgi apparatus of drug-untreated human melanoma cells. Int. J. Cancer, 75:885-893.
48. Myher, J.J., Kuksis, A., and Pind, S. (1989) Molecular species of glycerolipids and sphingomyelins of human erythrocytes: Improved method of analysis. Lipids, 24:396-407.
49. Newburg, D., Chaturvedi, P., Lopez, E., Devoto, S., Feyad, A., and Cleary, T. (1993) Susceptibility to hemolytic-uremic syndrome relates to erythrocyte glycosphingolipid patterns. J. Infect. Dis., 168: 476-479.
50. Nyholm, P., Magnusson, G., Zheng, Z., Norel, R., Birnington-Boyd, B., and Lingwood C.A (1996) Two distinct binding sites for globotriaosyl ceramide on verotoxihs; Molecular modelling and confirmation by analogue studies and a new glycolipid receptor for all verotoxins. Chem. Biol., 3:263-275.
51. Olsnes, S., van Deurs, B., and Sandvig, K. (1993) Protein toxins acting on intracellular targets: Cellular uptake and translocation to the cytosol. Med. Microbiol. Immunol., 182:51-61.
52. Pellizzari, A., Pang, H., and Lingwood, C.A. (1992) Binding of verocytotoxin 1 to its receptor is influenced by differences in receptor fatty acid content. Biochemistry, 31:1363-1370.
53. Petric, M., Karmali, M.A., Richardson, S., and Cheung, R. (1987) Purification and biological properties of Escherichia coli verocytotoxin. FEMS Microbiol. Letts., 47:63-68.
54. Ponten, J., and MacIntyre, E. (1986) Long-term culture of normal anq neoplastic human glia. Pathol. Microbiol. Scand., 81:791-805.
55. Pulczynski, S., Boesen, A.M., and Jensen, O.M. (1993) Antibody-induced modulation and intracellular transport of CD10 and CD19 antigens in human B-cell lines: An immunofluorescence and immunoelectron microscopy study. Blood, 81:1549-1557.
56. Ramotar, K., Boyd, B., Tyrrell, G., Gariepy, J., Lingwood, C.A., and Brunton, J. (1990) Characterization of Shiga-like toxin 1 B subunit purified from overproducing clones of the SLT-1 B cistron. Biochem. J., 272:805-811.
57. Robinson, L.A., Hurley, R.M., Lingwood, C.A., and Matsell, D.G. (1995) Escherichia coli verotoxin binding to human paediatric glomerular mesangial cells. Pediatr. Nephrol., 9:700-704.
58. Rowe, P., Orrbine, E., Wells, G., and McLaine, P. (1991) Epidemiology of the hemolytic-uremic syndrome in Canadian children from 1986-1988. J. Pediatr., 119:218-224.
59. Rutka, J., Giblin, J., Hoifodt, H., Dougherty, D., Bell, C., McCullough, J., Davis, R., Wilson, C., and Rosenblum, M. (1986) Establishment and characterization of a cell Line from a human gliosarcoma. Cancer Res., 46:5893-5902.
60. Rutka, J.T., Giblin, J.R., Dougherty, D.Y., Liu, H.C., McCulloch, J.R Bell, C.W., Stern R.S., Wilson, C.B., and Rosenblum, M.L. (1987) Establishment and characterization of five cell lines derived from human malignant gliomas. Acta Neuropathol. (Berl.), 75:92-103.
61. Sandvig, K., Garred, O., Prydz, K., Kozlov, J., Hansen, S., and van Deurs, B. (1992) Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum. Nature, 358:510-512.
62. Sandvig, K., Garred, O., HoIlm, P.K., and van Deurs, B. (1993) Endocytosis and intracellular transport of protein toxins. Biochem. Soc Trans., 21:707-711.
63. Sandvig, K., Garred, O., van Helvoort, A., van Meer, G., and van Deurs, B. (1996) Importance of glycolipid synthesis for butyric acidinduced sensitization to Shiga toxin and intracellular sorting Of toxin in A431 cells. Mol. Biol. Cell, 7:1391-1404.
64. Sandvig, K., Prydz, K., Ryd, M., and van Deurs, B. (1991) Endocytosis and intracellular transport of the glycolipid-binding ligand Shiga toxin in polarized MDCK cells. J. Cell. Biol., 113:553-562.
65. Sandvig, K., Ryd, M., Garred, O., Schweda, E., and Holm, P.K. (1994) Retrograde transport from the Golgi complex to the ER of both Shiga toxin and the nontoxic Shiga B-fragment is regulated by butyric acid and cAMP. J. Cell Biol., 126:53-64.
66. Sandvig, K., and Van Deurs, B. (1996) Endocytosis, intracellular transport, and cytotroxic actin of Shiga toxin and ricin. Physiol. Rev., 76:949-966.
67. Saxena, S.K., O'Brien, A.D., and Ackerman, E.J. (1989) Shiga toxin, Shiga-like toxin II variant, and ricin are all single-site RNA N-glycosidases of 28 S RNA when microinjected into Xenopus oocytes. J. Biol. Chem., 264:596-601.
68. Stachowiak, M., Maher, P., Mordechai, E., and Stachowiak, E. (1996) Nuclear accumulation of fibroblast growth factor receptors is regulated by multiple signals in adrenal medullary cells. Mol. Biol. Cell, 7:1299-1317.
69. St. Hilaire, P.M., Boyd, M.K., and Toone, E.J. (1994) Interaction of the Shiga-like toxin type 1 B-subunit with its carbohydrate receptor. Biochemistry, 33:14452-14463.
70. Stirling, J.W., and Graff, P.S. (1995) Antigen unmasking for immunoelectron microscopy: Labeling is improved by treating with sodium ethoxide or sodium metaperiodate, then heating on retrieval medium. J. Histochem. Cytochem., 43:115-123.
71. van Helvoort, A., Smith, A., Sprong, H., Fritzsche, I., Schinkel, A., Borst, P., and van Meer, G. (1996) MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidyl choline. Cell, 87:507-517.
72. Waddell, T., Head, S., Petric, M., Cohen, A., and Lingwood, C.A. (1988) Globotriosyl ceramide is specifically recognized by the E. coli verocytotoxin 2. Biochem. Biophys. Res. Commun., 152:674-679.
73. Westermark, B., Ponten, J., and Hugosson, R. (1973) Determinants for the establishment of permanent tissue culture lines from human gliomas. Acta. Pathol. Microbiol. Scand., 81:791-805.
74. Willingham, M., Richert, N.D., Cornwell, M.M., Tsuruo, T., Hamada, H., Gottesman, M.M., and Pastan, I.H. (1987) Immunocytochemical localization of P170 at the plasma membrane of multidrug-resistant human cells. J. Histochem. Cytochem., 35:1451-1456.