Mammalian cell ganglioside-binding specificities of E. coli enterotoxins LT-IIb and variant LT-IIb(T13I)

Glycobiology

Volumn 20, Issue 1, 2010, Pages 41-54

  Berenson, Charles S ^a   Nawar, Hesham F ^a   Yohe, Herbert C ^b,c   Castle, Sherry A ^d   Ashline, David J ^d   Reinhold, Vernon N ^d   Hajishengallis, George ^e   Connell, Terry D ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b Department of Veterans Affairs Regional Office White River Junction   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d University of New Hampshire   (United States)

^e University of Louisville School of Medicine   (United States)

Author keywords

Enterotoxins; Ganglioside; Glycosphingolipid; Macrophage; Sialic acid

Indexed keywords

CERAMIDE; ESCHERICHIA COLI ENTEROTOXIN; ESCHERICHIA COLI ENTEROTOXIN LT IIB; GANGLIOSIDE; GANGLIOSIDE GD 1A; GANGLIOSIDE GD 1B; GANGLIOSIDE GM1A; GANGLIOSIDE GM2; GANGLIOSIDE GM3; ISOLEUCINE; PERIODATE; PROTEINASE K; SIALIC ACID; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTHROBACTER; ARTICLE; CLOSTRIDIUM PERFRINGENS; CONTROLLED STUDY; ENZYME DEGRADATION; ESCHERICHIA COLI; FLOW CYTOMETRY; IMMUNOBLOTTING; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION;

ANIMALS; BACTERIAL TOXINS; CELL LINE; CERAMIDES; CLOSTRIDIUM PERFRINGENS; ENTEROTOXINS; EPITOPES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GANGLIOSIDES; GLYCOSPHINGOLIPIDS; INFLAMMATION; MACROPHAGES; MASS SPECTROMETRY; MICE; N-ACETYLNEURAMINIC ACID; PROTEIN BINDING;

ESCHERICHIA COLI; MAMMALIA; MURINAE;

EID: 70849094217     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwp141     Document Type: Article

References (42)

1. Arnsmeier SL, Paller AS. 1995. Chemiluminescence detection of gangliosides by thin-layer chromatography. J Lipid Res. 36:911-915.
2. Bennett V, Cuatrecasas P. 1975. Mechanism of activation of adenylate cyclase by Vibrio cholerae enterotoxin. J Membr Biol. 22:29-52.
3. Berenson CS, Gallery MA, Smigiera JM, Rasp RH. 2002. The role of ceramide of human macrophage gangliosides in activation of human macrophages. J Leukoc Biol. 72:492-502.
4. Berenson CS, Rasp RH, Gau JT, Ryan JL, Yohe HC. 2001. Differences in splenic B-lymphocyte ganglioside expression and accessibility in normal and endotoxin-hyporesponsive mice. J Leukoc Biol. 69:969-976.
5. Berenson CS, Sayles KB, Huang J, Reinhold VN, Garlipp MA, Yohe HC. 2005. Nontypeable Haemophilus influenzae-binding gangliosides of human respiratory (HEp-2) cells have a requisite lacto/neolacto core structure. FEMS Immunol Med Microbiol. 45:171-182.
6. Berenson CS, Yohe HC, Ryan JL. 1989. Factors mediating lipopolysaccharide-induced ganglioside expression in murine peritoneal macrophages. J Leukoc Biol. 45:221-230.
7. Byres E, Paton AW, Paton JC, Löfling JC, Smith DF, Wilce MC, Talbot UM, Chong DC, Yu H, Huang S, et al. 2008. Incorporation of a non-human glycan mediates human susceptibility to a bacterial toxin. Nature. 456:648-652.
8. Campanero-Rhodes MA, Smith A, Chai W, Sonnino S, Mauri L, Childs RA, Zhang Y, Ewers H, Helenius A, Imberty A, et al. 2007. N-Glycolyl GM1 ganglioside as a receptor for simian virus 40. J Virol. 81:12846-12858.
9. Ciucanu I, Costello CE. 2003. Elimination of oxidative degradation during the per-O-methylation of carbohydrates. J Am Chem Soc 125:16213-16219.
10. Ciucanu I, Kerek F. 1984. A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res. 131:209-217.
11. Connell TD, Holmes RK. 1995. Mutational analysis of the ganglioside-binding activity of the type II Escherichia coli heat-labile enterotoxin LT-IIb. Mol Microbiol. 16:21-31.
12. Crocker PR, Varki A. 2001. Siglecs, sialic acids and innate immunity. Trends Immunol. 22:337-342.
13. Fakih MG, Murphy TF, Pattoli MA, Berenson CS. 1997. Specific binding of Haemophilus influenzae to minor gangliosides of human respiratory epithelial cells. Infect Immun. 65:1695-1700.
14. Fukuta S, Magnani JL, Twiddy EM, Holmes RK, Ginsburg V. 1988. Comparison of the carbohydrate-binding specificities of cholera toxin and Escherichia coli heat-labile enterotoxins LTh-I, LT-IIa, and LT-IIb. Infect Immun. 56:1748-1753.
15. Hajishengallis G, Tapping RI, Martin MH, Nawar H, Lyle EA, Russell MW, Connell TD. 2005. Toll-like receptor 2 mediates cellular activation by the B subunits of type II heat-labile enterotoxins. Infect Immun. 73:1343-1349.
16. Hakomori S. 2000. Traveling for the glycosphingolipid path. Glycoconj J. 17:627-647.
17. Iwabuchi K, Prinetti A, Sonnino S, Mauri L, Kobayashi T, Ishii K, Kaga N, Murayama K, Kurihara H, Nakayama H, et al. 2008. Involvement of very long fatty acid-containing lactosylceramide in lactosylceramide-mediated superoxide generation and migration in neutrophils. Glycoconj J. 25:357-374.
18. Kato I, Naiki M. 1976. Ganglioside and rabbit erythrocyte membrane receptor for staphylococcal alpha-toxin. Infect Immun. 13:289-291.
19. Kronke M. 1999. Biophysics of ceramide signaling: Interaction with proteins and phase transition of membranes. Chem Phys Lipids. 101:109-121.
20. Li S-C, DeGasperi R, Muldrey JE, Li Y-T. 1986. A unique glycosphingolipid-splitting enzyme (ceramide glycanase from leech) cleaves the linkage between the oligosaccharide and the ceramide. Biochem Biophys Res Commun. 141:346-352.
21. Liang S, Wang M, Tapping RI, Stepensky V, Nawar HF, Triantafilou M, Triantafilou K, Connell TD, Hajishengallis G. 2007. Ganglioside GD1a is an essential coreceptor for Toll-like receptor 2 signaling in response to the B subunit of type IIb enterotoxin. J Biol Chem. 282:7532-7542.
22. Macala LJ, Yohe HC. 1995. In situ accessibility of murine macrophage gangliosides. Glycobiology. 5:67-75.
23. Magnani JL, Smith DF, Ginsburg V. 1980. Detection of gangliosides that bind cholera toxin: Direct binding of 125I-labeled toxin to thin-layer chromatograms. Anal Biochem. 109:399-402.
24. Martin MJ, Rayner JC, Gagneux P, Barnwell JW, Varki A. 2005. Evolution of human-chimpanzee differences in malaria susceptibility: Relationship to human genetic loss of N-glycolylneuraminic acid. Proc Natl Acad Sci. 102:12819-12824.
25. Nawar HF, Arce S, Russell MW, Connell TD. 2005. Mucosal adjuvant properties of mutant LT-IIa and LT-IIb enterotoxins that exhibit altered ganglioside-binding activities. Infect Immun. 73: 1330-1342.
26. Orlandi PA, Critchley DR, Fishman PH. 1994. The heat-labile enterotoxin of Escherichia coli binds to polylactosaminoglycan-containing receptors in CaCo-2 human intestinal epithelial cells. Biochemistry 33:12886-12895.
27. Osborne JC, Moss J, Fishman PH, Nakaya S. 1982. Specificity in protein-membrane associations: The interactions of gangliosides with Escherichia coli heat-labile enterotoxin and choleragen. Biophys J 37:168-169.
28. Reinhold BB, Chan S-Y, Chan S, Reinhold VN. 1994. Profiling glycosphingolipid structural detail: Periodate oxidation, electrospray, collision-induced dissociation and tandem mass spectrometry. Org Mass Spectrom. 29:736-746.
29. Schengrund C-L. 1995. Evidence that molecules on the surface of one cell can adhere to the oligosaccharide portion of gangliosides on the surface of another cell. Biol Signals. 4:1-13.
30. Simpson LL, Rapport MM. 1971a. The binding of botulinum toxin tomembrane lipids: Phospholipids and proteolipid. J Neurochem. 18:1761-1767.
31. Simpson LL, Rapport MM. 1971b. The binding of botulinum toxin tomembrane lipids: Sphingolipids, steroids and fatty acids. J Neurochem. 18:1751-1759.
32. Sonnino S, Prinetti A, Nakayama H, Yangida M, Ogawa H, Iwabuchi K. 2009. Role of very long fatty acid-containing glycosphingolipids in membrane organization and cell signaling: The model of lactosylceramide in neutrophils. Glycoconj J. 26:615-621.
33. Stoeckel K, Schwab M, Thoenen H. 1977. Role of gangliosides in the uptake and retrograde axonal transport of cholera and tetanus toxin as compared to nerve growth factor and wheat germ agglutinin. Brain Res 132:273-285.
34. Svennerholm, L. 1963. Chromatographic separation of human brain gangliosides. J Neurochem. 10:613-623.
35. van Ginkel FW, Jackson RJ, Yoshino N, Hagiwara Y,Metzger DJ, Connell TD, Vu HL, Martin M, Fujihashi K, McGhee JR. 2005. Enterotoxin-based mucosal adjuvants alter antigen trafficking and induce inflammatory responses in the nasal tract. Infect Immun. 73:6892-6902.
36. Varki A. 2009. Multiple changes in sialic acid biology during human evolution. Glycoconj J. 26:231-245.
37. Varki NM, Varki A. 2007. Diversity in cell surface sialic acid presentations: Implications for biology and disease. Lab Invest. 87:851-857.
38. Virkola R, Parkkinen J, Hacker J, Korhonen TK. 1993. Sialyloligosaccharide chains of laminin as an extracellular matrix target for S fimbriae of Escherichia coli. Infect Immun. 61:4480-4484.
39. Yohe HC, Cuny CL, Macala LJ, Saito M, McMurray WJ, Ryan JL. 1991. The presence of sialidase-sensitive sialosylgangliotetraosyl ceramide (GM1b) in stimulated murine macrophages. Deficiency of GM1b in Escherichia coli-activated macrophages from the C3H/HeJ mouse. J Immunol. 146:1900-1908.
40. Yohe HC, Ryan JL. 1986. Ganglioside expression in macrophages from endotoxin responder and nonresponder mice. J Immunol. 137:3921-3927.
41. Yohe HC, Wallace PK, Berenson CS, Ye S, Reinhold BB, Reinhold VN. 2001. The major glycolipids of human peripheral blood monocytes/macrophages; absence of ganglio series structures. Glycobiology. 11:831-841.
42. Yohe HC, Ye S, Reinhold BB, Reinhold VN. 1997. Structural characterization of the disialogangliosides of murine peritoneal macrophages. Glycobiology. 7:1215-1227.