Glycosphingolipids in vascular endothelial cells: Relationship of heterogeneity in Gb3Cer/CD77 receptor expression with differential Shiga toxin 1 cytotoxicity

Glycoconjugate Journal

Volumn 25, Issue 4, 2008, Pages 291-304

  Schweppe, Christian H ^a   Bielaszewska, Martina ^a   Pohlentz, Gottfried ^a   Friedrich, Alexander W ^a   Büntemeyer, Heino ^b   Alexander Schmidt, M ^a   Kim, Kwang S ^c   Peter Katalinić, Jasna ^a   Karch, Helge ^a   Müthing, Johannes ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b BIELEFELD UNIVERSITY   (Germany)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

EA.hy 926 cells; Glycolipids; Glycosyltransferases; HBMECs

Indexed keywords

FATTY ACID; GLOBOTRIAOSYLCERAMIDE; GLYCOSPHINGOLIPID; VEROTOXIN 1;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; BINDING ASSAY; BRAIN CELL; CELL CULTURE; CELL HETEROGENEITY; CELL LINE; CYTOTOXICITY; ELECTROSPRAY; ENDOTHELIUM CELL; GENETIC HETEROGENEITY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MORTALITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOLID; SPECIES; TIME OF FLIGHT MASS SPECTROMETRY; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

BRAIN; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CHROMATOGRAPHY, THIN LAYER; ENDOTHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOSPHINGOLIPIDS; GLYCOSYLTRANSFERASES; HUMANS; IMMUNOHISTOCHEMISTRY; NANOTECHNOLOGY; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SHIGA TOXIN 1; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRIHEXOSYLCERAMIDES;

EID: 41149089223     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-007-9091-7     Document Type: Article

References (75)

1. Sandvig, K.: Shiga toxins. Toxicon. 39, 1629-1635 (2001)
2. Karch, H., Tarr, P.I., Bielaszewska, M.: Enterohaemorrhagic Escherichia coli in human medicine. Int. J. Med. Microbiol. 295, 405-418 (2005)
3. 3. Biochemistry 37, 1777-1788 (1998)
4. Lingwood, C.A.: Role of verotoxin receptors in pathogenesis. Trends Microbiol. 4, 147-153 (1996)
5. Sandvig, K., Garred, Ø., Prydz, K., Kozlov, J.V., Hansen, S.H., van Deurs, B.: Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum. Nature 358, 510-512 (1992)
6. Endo, Y., Tsurugi, K., Yutsudo, T., Takeda, Y., Ogasawara, T., Igarashi, K.: Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and Shiga toxin on eukaryotic ribosomes. Eur. J. Biochem. 171, 45-50 (1988)
7. Garred, Ø., van Deurs, B., Sandvig, K.: Furin-induced cleavage and activation of Shiga toxin. J. Biol. Chem. 270, 10817-10821 (1995)
8. Stults, C.L., Sweeley, C.C., Macher, B.A.: Glycosphingolipids: structure, biological source, and properties. Methods Enzymol. 179, 167-214 (1989)
9. Müthing, J.: Mammalian glycosphingolipids. In: Freiser-Reid, B., Tatsuka, K., Thiem, J. (eds.) Glycoscience: Chemistry and Chemical Biology, vol. 3, pp. 2220-2249. Springer-Verlag, Heidelberg, Germany (2001)
10. Schnaar, R.L.: Glycosphingolipids in cell surface recognition. Glycobiology 1, 477-485 (1991)
11. Feizi, T.: Carbohydrate-mediated recognition systems in innate immunity. Immunol. Rev. 173, 79-88 (2000)
12. Schlossmacher, M.G., Cullen, V., Müthing, J.: The glucocerebrosidase gene and Parkinson's disease in Ashkenazi Jews. N. Engl. J. Med. 352, 728-731 (2005)
13. Karlsson, K.A.: Animal glycosphingolipids as membrane attachment sites for bacteria. Annu. Rev. Biochem. 58, 309-350 (1989)
14. Teneberg, S., Ångström, J., Ljungh, Å.: Carbohydrate recognition by enterohemorrhagic Escherichia coli: characterization of a novel glycosphingolipid from cat small intestine. Glycobiology. 14, 187-196 (2004)
15. Miller-Podraza, H., Lanne, B., Ångström, J., Teneberg, S., Milh, M.A., Jovall, P.Å., Karlsson, H., Karlsson, K.A.: Novel binding epitope for Helicobacter pylori found in neolacto carbohydrate chains: structure and cross-binding properties. J. Biol. Chem. 280, 19695-19703 (2005)
16. Nakamura, K., Suzuki, M., Inagaki, F., Yamakawa, T., Suzuki, A.: A new ganglioside showing choleragenoid-binding activity in mouse spleen. J. Biochem. 101, 825-835 (1987)
17. Stins, M.F., Gilles, F., Kim, K.S.: Selective expression of adhesion molecules on human brain microvascular endothelial cells. J. Neuroimmunol. 76, 81-90 (1997)
18. Edgell, C.J.S., McDonald, C.C., Graham, J.B.: Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc. Natl. Acad. Sci. U.S.A. 80, 3734-3737 (1983)
19. Kim, K.S.: Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nat. Rev. Neurosci. 4, 376-385 (2003)
20. Bielaszewska, M., Karch, H.: Consequences of enterohaemorrhagic Escherichia coli infection for the vascular endothelium. Thromb. Haemost. 94, 312-318 (2005)
21. Kim, K.J., Chung, J.W., Kim, K.S.: 67-kDa laminin receptor promotes internalization of cytotoxic necrotizing factor 1-expressing Escherichia coli K1 into human brain microvascular endothelial cells. J. Biol. Chem. 280, 1360-1368 (2005)
22. Shin, S., Kim, K.S.: RhoA and Rac1 contribute to type III group B streptococcal invasion of human brain microvascular endothelial cells. Biochem. Biophys. Res. Commun. 345, 538-542 (2006)
23. Khan, N.A., Kim, Y., Shin, S., Kim, K.S.: FimH-mediated Escherichia coli K1 invasion of human brain microvascular endothelial cells. Cell. Microbiol. 9, 169-178 (2007)
24. 2/M arrest, inhibition of proliferation, and death of human endothelial cells. Infect. Immun. 73, 552-562 (2005)
25. Kügler, S., Böcker, K., Heusipp, G., Greune, L., Kim, K.S., Schmidt, M.A.: Pertussis toxin transiently affects barrier integrity, organelle organization and transmigration of monocytes in a human brain microvascular endothelial cell barrier model. Cell. Microbiol. 9, 619-632 (2007)
26. Emeis, J.J., Edgell, C.J.S.: Fibrinolytic properties of a human endothelial hybrid cell line (Ea.hy 926). Blood 71, 1669-1675 (1988)
27. Schönherr, E., Schaefer, L., O'Connell, B.C., Kresse, H.: Matrix metalloproteinase expression by endothelial cells in collagen lattices changes during co-culture with fibroblasts and upon induction of decorin expression. J. Cell. Physiol. 187, 37-47 (2001)
28. Strazynski, M., Eble, J.A., Kresse, H., Schönherr, E.: Interleukin (IL)-6 and IL-10 induce decorin mRNA in endothelial cells, but interaction with fibrillar collagen is essential for its translocation. J. Biol. Chem. 279, 21266-21270 (2004)
29. Kainulainen, V., Nelimarkka, L., Järveläinen, H., Laato, M., Jalkanen, M., Elenius, K.: Suppression of syndecan-1 expression in endothelial cells by tumor necrosis factor-α. J. Biol. Chem. 271, 18759-18766 (1996)
30. Obrig, T.O., Del Vecchio, P.J., Brown, J.E., Moran, T.P., Rowland, B.M., Judge, T.K., Rothman, S.W.: Direct cytotoxic action of Shiga toxin on human vascular endothelial cells. Infect. Immun. 56, 2373-2378 (1988)
31. Kaye, S.A., Louise, C.B., Boyd, B., Lingwood, C.A., Obrig, T.G.: Shiga toxin-associated hemolytic uremic syndrome: interleukin-1β enhancement of Shiga toxin cytotoxicity toward human vascular endothelial cells in vitro. Infect. Immun. 61, 3886-3891 (1993)
32. Gillard, B.K., Jones, M.A., Marcus, D.M.: Glycosphingolipids of human umbilical vein endothelial cells and smooth muscle cells. Arch. Biochem. Biophys. 256, 435-445 (1987)
33. Müthing, J., Duvar, S., Heitmann, D., Hanisch, F.G., Neumann, U., Lochnit, G., Geyer, R., Peter-Katalinić, J.: Isolation and structural characterization of glycosphingolipids of in vitro propagated human umbilical vein endothelial cells. Glycobiology 9, 459-468 (1999)
34. Kanda, T., Ariga, T., Kubodera, H., Jin, H.L., Owada, K., Kasama, T., Yamawaki, M., Mizusawa, H.: Glycosphingolipid composition of primary cultured human brain microvascular endothelial cells. J. Neurosci. Res. 78, 141-150 (2004)
35. Van de Kar, N.C.A.J., Monnens, L.A.H., Karmali, M.A., van Hinsbergh, V.W.M.: Tumor necrosis factor and interleukin-1 induce expression of the verocytotoxin receptor globotriaosylceramide on human endothelial cells: implications for the pathogenesis of the hemolytic uremic syndrome. Blood 80, 2755-2764 (1992)
36. Ramegowda, B., Samuel, J.E., Tesh, V.L.: Interaction of Shiga toxins with human brain microvascular endothelial cells: cytokines as sensitizing agents. J. Infect. Dis. 180, 1205-1213 (1999)
37. 3 and sensitivity to Shiga toxin. Infect. Immun. 69, 1889-1894 (2001)
38. Stricklett, P.K., Hughes, A.K., Ergonul, Z., Kohan, D.E.: Molecular basis for up-regulation by inflammatory cytokines of Shiga toxin 1 cytotoxicity and globotriaosylceramide expression. J. Infect. Dis. 186, 976-982 (2002)
39. Ergonul, Z., Hughes, A.K., Kohan, D.E.: Induction of apoptosis of human brain microvascular endothelial cells by Shiga toxin. J. Infect. Dis. 187, 154-158 (2003)
40. Duvar, S., Peter-Katalinić, J., Hanisch, F.G., Müthing, J.: Isolation and structural characterization of glycosphingolipids of in vitro propagated bovine aortic endothelial cells. Glycobiology 7, 1099-1109 (1997)
41. 2 incubator. Cytotechnology 14, 1-9 (1994)
42. Meisen, I., Friedrich, A.W., Karch, H., Witting, U., Peter- Katalinić, J., Müthing, J.: Application of combined high-performance thin-layer chromatography immunostaining and nanoelectrospray ionisation quadrupole time-of-flight tandem mass spectrometry to the structural characterization of high- and low-affinity binding ligands of Shiga toxin 1. Rapid Commun. Mass Spectrom. 19, 3659-3665 (2005)
43. Kasai, M., Iwamori, M., Nagai, Y., Okumura, K., Tada, T.: A glycolipid on the surface of mouse natural killer cells. Eur. J. Immunol. 10, 175-180 (1980)
44. Müthing, J., Burg, M., Möckel, B., Langer, M., Metelmann-Strupat, W., Werner, A., Neumann, U., Peter-Katalinić, J., Eck, J.: Preferential binding of the anticancer drug rViscumin (recombinant mistletoe lectin) to terminally α2-6-sialylated neolacto-series gangliosides. Glycobiology 12, 485-497 (2002)
45. Müthing, J., Meisen, I., Kniep, B., Haier, J., Senninger, N., Neumann, U., Langer, M., Witthohn, K., Milosević, J., Peter-Katalinić, J.: Tumor-associated CD75s gangliosides and CD75s-bearing glycoproteins with Neu5Acα2-6Galβ1-4GlcNAc residues are receptors for the anticancer drug rViscumin. FASEB J. 19, 103-105 (2005)
46. k UDP-galactose: Galβ1-4Glcβ1-1Cer α1,4-galactosyltransferase. J. Biol. Chem. 275, 16723-16729 (2000)
47. Müthing, J., Meisen, I., Bulau, P., Langer, M., Witthohn, K., Lentzen, H., Neumann, U., Peter-Katalinić, J.: Mistletoe lectin I is a sialic acid-specific lectin with strict preference to gangliosides and glycoproteins with terminal Neu5Acα2-6Galβ1-4GlcNAc residues. Biochemistry 43, 2996-3007 (2004)
48. Müthing, J., Unland, F., Heitmann, D., Orlich, M., Hanisch, F.G., Peter-Katalinić, J., Knäuper, V., Tschesche, H., Kelm, S., Schauer, R., Lehmann, J.: Different binding capacities of influenza A and Sendai viruses to gangliosides from human granulocytes. Glycoconj. J. 10, 120-126 (1993)
49. Müthing, J.: TLC in structure and recognition studies of glycosphingolipids. In: Hounsell, E.F. (ed.) Methods in Molecular Biology, pp. 183-195. Humana, Totawa, NJ (1998)
50. Meisen, I., Peter-Katalinić, J., Müthing, J.: Direct analysis of silica gel extracts from immunostained glycosphingolipids by nanoelectrospray ionization quadrupole time-of-flight mass spectrometry. Anal. Chem. 76, 2248-2255 (2004)
51. Meisen, I., Peter-Katalinić, J., Müthing, J.: Discrimination of neolacto-series gangliosides with α2-3- and α2-6-linked N-acetylneuraminic acid by nanoelectrospray ionization low-energy collision-induced dissociation tandem quadrupole TOF MS. Anal. Chem. 75, 5719-5725 (2003)
52. Domon, B., Costello, C.E.: A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconj. J. 5, 397-409 (1988)
53. Domon, B., Costello, C.E.: Structure elucidation of glycosphingolipids and gangliosides using high-performance tandem mass spectrometry. Biochemistry 27, 1534-1543 (1988)
54. Obrig, T.G., Louise, C.B., Lingwood, C.A., Boyd, B., Barley-Maloney, L., Daniel, T.O.: Endothelial heterogeneity in Shiga toxin receptors and responses. J. Biol. Chem. 268, 15484-15488 (1993)
55. Ohmi, K., Kiyokawa, N., Takeda, T., Fujimoto, J.: Human microvascular endothelial cells are strongly sensitive to Shiga toxins. Biochem. Biophys. Res. Commun. 251, 137-141 (1998)
56. Jacewicz, M., Acheson, D.W.K., Binion, D.G., West, G.A., Lincicome, L.L., Fiocchi, C., Keusch, G.T.: Responses of human intestinal microvascular endothelial cells to Shiga toxins 1 and 2 and pathogenesis of hemorrhagic colitis. Infect. Immun. 67, 1439-1444 (1999)
57. Rösner, H., Greis, Ch., Rodemann, H.P.: Density-dependent expression of ganglioside GM3 by human skin fibroblasts in an all-or-none fashion, as a possible modulator of cell growth in vitro. Exp. Cell Res. 190, 161-169 (1990)
58. Boyd, B., Magnusson, G., Zhiuyan, Z., Lingwood, C.A.: Lipid modulation of glycolipid receptor function. Eur. J. Biochem. 223, 873-878 (1994)
59. Kiarash, A., Boyd, B., Lingwood, C.A.: Glycosphingolipid receptor function is modified by fatty acid content. J. Biol. Chem. 269, 11138-11146 (1994)
60. Binnington, B., Lingwood, D., Nutikka, A., Lingwood, C.A.: Effect of globotriaosylceramide fatty acid α-hydroxylation on the binding by verotoxin 1 and verotoxin 2. Neurochem. Res. 27, 807-813 (2002)
61. Sandvig, K., Ryd, M., Garred, Ø., Schweda, E., Holm, P.K., van Deurs, B.: 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 (1994)
62. Sekino, T., Kiyokawa, N., Taguchi, T., Takenouchi, H., Matsui, J., Tang, W.R., Suzuki, T., Nakajima, H., Saito, M., Ohmi, K., Katagiri, Y.U., Okita, H., Nakao, H., Takeda, T., Fujimoto, J.: Characterization of a Shiga-toxin 1-resistant stock of Vero cells. Microbiol. Immunol. 48, 377-387 (2004)
63. Hakomori, S.I.: Cell adhesion/recognition and signal transduction through glycosphingolipid microdomain. Glycoconj. J. 17, 143-151 (2000)
64. Sonnino, S., Prinetti, A., Mauri, L., Chigorno, V., Tettamanti, G.: Dynamic and structural properties of sphingolipids as driving forces for the formation of membrane domains. Chem. Rev. 106, 2111-2125 (2006)
65. Fantini, J., Maresca, M., Hammache, D., Yahi, N., Delézay, O.: Glycosphingolipid (GSL) microdomains as attachment platforms for host pathogens and their toxins on intestinal epithelial cells: activation of signal transduction pathways and perturbations of intestinal absorption and secretion. Glycoconj. J. 17, 173-179 (2000)
66. 5 subunit bacterial toxins. Biochim. Biophys. Acta 1746, 314-321 (2005)
67. Falguières, T., Mallard, F., Baron, C., Hanau, D., Lingwood, C., Goud, B., Salamero, J., Johannes, L.: Targeting of Shiga toxin B-subunit to retrograde transport route in association with detergent-resistant membranes. Mol. Biol. Cell 12, 2453-2468 (2001)
68. Smith, D.C., Sillence, D.J., Falguières, T., Jarvis, R.M., Johannes, L., Lord, J.M., Platt, F.M., Roberts, L.M.: The association of Shiga-like toxin with detergent-resistant membranes is modulated by glucosylceramide and is an essential requirement in the endoplasmic reticulum for a cytotoxic effect. Mol. Biol. Cell 17, 1375-1387 (2006)
69. Falguières, T., Römer, W., Amessou, M., Afonso, C., Wolf, C., Tabet, J.C., Lamaze, C., Johannes, L.: Functionally different pools of Shiga toxin receptor, globotriaosyl ceramide, in HeLa cells. FEBS J. 273, 5205-5218 (2006)
70. Tarr, P.I., Gordon, C.A., Chandler, W.L.: Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365, 1073-1086 (2005)
71. Karmali, M.A.: Prospects for preventing serious systemic toxemic complications of Shiga toxin producing Escherichia coli infections using Shiga toxin receptor analogues. J. Infect. Dis. 189, 355-359 (2004)
72. Müthing, J., Čačić, M.: Glycosphingolipid expression in human skeletal and heart muscle assessed by immunostaining thin-layer chromatography. Glycoconj. J. 14, 19-28 (1997)
73. Bethke, U., Müthing, J., Schauder, B., Conradt, P., Mühlradt, P.F.: An improved semi-quantitative enzyme immunostaining procedure for glycosphingolipid antigens on high performance thin layer chromatograms. J. Immunol. Methods 89, 111-116 (1986)
74. Markotić, A., Čulić, V., Kurir, T., Meisen, I., Büntemeyer, H., Boraska, V., Zemunik, T., Petri, N., Mesarić, M., Peter-Katalinić, J., Müthing, J.: Oxygenation alters ganglioside expression in rat liver following partial hepatectomy. Biochem. Biophys. Res. Commun. 330, 131-141 (2005)
75. Chester, M.A.: IUPAC-IUB Joint Commission on Biochemical Nomenclature. Nomenclature of glycolipids. Recommendations 1997. Glycoconj. J. 16, 1-6 (1999)