Rafts and related glycosphingolipid-enriched microdomains in the intestinal epithelium: Bacterial targets linked to nutrient absorption

Advanced Drug Delivery Reviews

Volumn 56, Issue 6, 2004, Pages 779-794

  Taïeb, Nadira ^a   Yahi, Nouara ^a   Fantini, Jacques ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Adhesin; Bacteria; Ceramide; CH interactions; Cholesterol; Glycosphingolipid; Intestinal absorption; Lipid raft; Nutrient; Toxin

Indexed keywords

ABSORPTION; BACTERIA; BIOCHEMISTRY; BIOLOGICAL MEMBRANES; CHOLESTEROL; LIPIDS;

LIPID RAFTS; PATHOGENS; PLASMA MEMBRANES; RAFT-PATHOGEN INTERACTIONS;

CONTROLLED DRUG DELIVERY;

ADAMANTANE; ADHESIN; ANTIINFECTIVE AGENT; CERAMIDE; GLYCOSPHINGOLIPID; MEMBRANE PROTEIN; OLIGOSACCHARIDE; SPHINGOSINE; TOXIN;

ABSORPTION; BACTERIUM ADHERENCE; BINDING AFFINITY; BINDING SITE; BIOPHYSICS; CAVEOLA; CELL MEMBRANE; CHEMICAL ANALYSIS; DRUG CONJUGATION; DRUG DESIGN; DRUG SYNTHESIS; HUMAN; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE FUNCTION; MEDICAL RESEARCH; NONHUMAN; NUTRIENT; PATHOGENESIS; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SURFACE PROPERTY;

EID: 18844471722     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.addr.2003.09.007     Document Type: Article

References (84)

1. Fantini J., Garmy N., Mahfoud R., Yahi N. Lipid rafts: structure, function and role in HIV, Alzheimer's and prion diseases. Expert Rev. Mol. Med. 2002;. (20 December, http://www.expertreviews.org/02005392h.htm ).
2. Brown D.A., London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275:2000;17221-17224.
3. Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 387:1997;569-572.
4. Sprong H., van der Sluijs P., van Meer G. How proteins move lipids and lipids move proteins. Nat. Rev. 2:2001;504-513.
5. Kasahara K., Sanai Y. Functional roles of glycosphingolipids in signal transduction via lipid rafts. Glycoconj. J. 17:2000;153-162.
6. Duncan M.J., Shin J.-S., Abraham S.N. Microbial entry through caveolae: variations on a theme. Cell. Microbiol. 4:2002;783-791.
7. Mahfoud R., Garmy N., Maresca M., Yahi N., Puigserver A., Fantini J. Identification of a common sphingolipid-binding domain in Alzheimer, prion, and HIV-1 proteins. J. Biol. Chem. 277:2002;11292-11296.
8. Smart E.J., Graf G.A., McNiven M.A., Sessa W.C., Engelman J.A., Scherer P.E., Okamoto T., Lisanti M.P. Caveolins, liquid-ordered domains, and signal transduction. Mol. Cell. Biol. 19:1999;7289-7304.
9. Hakomori S.-I. Cell adhesion/recognition and signal transduction through glycosphingolipid microdomain. Glycoconj. J. 17:2000;143-151.
10. Norkin L.C. Caveolae in the uptake and targeting of infectious agents and secreted toxins. Adv. Drug Deliv. Rev. 49:2001;301-315.
11. Brown R.E. Sphingolipid organization in biomembranes: what physical studies of model membrane reveal. J. Cell. Sci. 111:1998;1-9.
12. Rietveld A., Simons K. The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim. Biophys. Acta. 1376:1998;467-479.
13. Fantini J. How sphingolipids bind and shape proteins: molecular basis of lipid-protein interactions in lipid shells, rafts and related biomembrane domains. Cell. Mol. Life Sci. 60:2003;1027-1032.
14. Hammache D., Yahi N., Maresca M., Piéroni G., Fantini J. Human erythrocyte glycosphingolipids as alternative cofactors for human immunodeficiency virus type 1 (HIV-1) entry: evidence for CD4-induced interactions between HIV-1 gp120 and reconstituted membrane microdomains of glycosphingolipids (Gb3 and GM3). J. Virol. 73:1999;5244-5248.
15. Prieschl E.L., Baumruker T. Sphingolipids: second messengers, mediators and raft constituents in signaling. Immunol. Today. 21:2000;555-560.
16. Drevot P., Langlet C., Guo X.J., Bernard A.M., Colard O., Chauvin J.P., lasserre R., He H.T. TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 15:2000;1899-1908.
17. Benting J. Acyl and alkyl chain length of GPI-anchors is critical for raft association in vitro. FEBS Lett. 462:1999;47-50.
18. Pike L.J., Han X., Chung K.-N., Gross R.W. Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry. 41:2002;2075-2088.
19. Edidin M. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32:2003;257-283.
20. Bock J., Gulbins E. The transmembranous domain of CD40 determines CD40 partitioning into lipid rafts. FEBS Lett. 534:2003;169-174.
21. Anderson R.G.W., Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science. 296:2002;1821-1825.
22. Cook D.G., Fantini J., Spitalnik S.L., Gonzalez-Scarano F. Binding of HIV-1 gp120 to galactosylceramide: relationship to the V3 loop. Virology. 201:1994;206-214.
23. van der Goot F.G., Harder T. Raft membrane domains; from a liquid-ordered membrane phase to a site of pathogen attack. Semin. Immunol. 13:2001;89-97.
24. Haywood A. Virus receptors: binding, adhesion strengthening, and changes in viral structure. J. Virol. 68:1994;1-5.
25. Montecucco C. How do tetanus and botulinum toxins bind to neuronal membranes? Trends Biochem. Sci. 11:1986;314-317.
26. Fantini J., Hammache D., Piéroni G., Yahi N. Role of glycosphingolipid microdomains in CD4-dependent HIV-1 fusion. Glycoconj. J. 17:2000;199-204.
27. Hug P., Lin H.-M.J., Korte T., Xiao X., Dimitrov D.S., Wang J.M., Puri A., Blumenthal R. Glycosphingolipids promote entry of a broad range of human immunodeficiency virus type 1 isolates into cells expressing CD4, CXCR4, and/or CCR5. J. Virol. 74:2000;6377-6385.
28. Yahi N., Baghdiguian S., Moreau H., Fantini J. Galactosyl ceramide (or a closely related molecule) is the receptor for human immunodeficiency virus type 1 on human colon epithelial HT29 cells. J. Virol. 66:1992;4848-4854.
29. Meng G., Wei X., Wu X., Sellers M.T., Decker J.M., Moldoveanu Z., Orenstein J.M., Graham M.F., Kappes J.C., Mestecky J., Shaw G.M., Smith P.D. Primary intestinal epithelial cells selectively transfer R5 HIV-1 to CCR5+ cells. Nat. Med. 8:2002;150-156.
30. Fantini J., Maresca M., Hammache D., Yahi N., Delézay O. Glycosphingolipid (GSL) microdomain 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. 17:2000;173-179.
31. Hoey D.E.E., Sharp L., Currie C., Lingwood C.A., Gally D.L., Smith D.G.E. Verotoxin 1 binding to intestinal crypt epithelial cells results in localization to lysosomes and abrogation of toxicity. Cell. Microbiol. 5:2003;85-97.
32. Ma B., Elkayam T., Wolfson H., Nussinov R. Protein-protein interactions: structurally conserved residues distinguish between binding sites and exposed protein surfaces. Proc. Natl. Acad. Sci. U. S. A. 100:2003;5772-5777.
33. McGaughey G.B., Gagné M., Rappé A.K. π-Stacking interactions. Alive and well in proteins. J. Biol. Chem. 273:1998;15458-15463.
34. Weis W.I., Drickamer K. Structural basis of lectin-carbohydrate interactions. Ann. Rev. Biochem. 65:1996;441-473.
35. Nishio M., Umezawa Y., Hirota M., Takeuchi Y. The CH/π interaction: significance in molecular recognition. Tetrahedron. 51:1995;8665-8701.
36. Paul P.K.C. Aromatic ring-aliphatic ring stacking in organic crystal structures. Cryst. Eng. 5:2002;3-8.
37. Kiarash A., Boyd B., Lingwood C.A. 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. 269:1994;11138-11146.
38. Jones D.H., Lingwood C.A., Barber K.R., Grant C.W.M. Globoside as a membrane receptor: a consideration of oligosaccharide communication with the hydrophobic domain. Biochemistry. 36:1997;8539-8547.
39. Mahfoud R., Mylvaganam M., Lingwood C.A., Fantini J. A novel soluble anlog of the HIV-1 fusion cofactor, globotriaosylceramide (Gb3), eliminates the cholesterol requirement for high affinity gp120/Gb3 interaction. J. Lipid Res. 43:2002;1670-1679.
40. Radhakrishnan A., Anderson T.G., McConnell H.M. Condensed complexes, rafts, and the chemical activity of cholesterol in membranes. Proc. Natl. Acad. Sci. U. S. A. 97:2000;12422-12427.
41. Alouf J.E. Cholesterol-binding cytolytic protein toxins. Int. J. Med. Microbiol. 290:2000;351-356.
42. Hammache D., Piéroni G., Maresca M., Ivaldi S., Yahi N., Fantini J. Reconstitution of sphingolipid-cholesterol plasma membrane microdomains for studies of virus-glycolipid interactions. Methods Enzymol. 312:2000;495-506.
43. Corbeil D., Röper K., Fargeas C.A., Joester A., Huttner W.B. Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic. 2:2001;82-91.
44. Milhiet P.E., Giocondi M.-C., Le Grimellec C. Cholesterol is not crucial for the existence of microdomains in kidney brush border membrane models. J. Biol. Chem. 277:2002;875-878.
45. Braccia A., Villani M., Immerdal L., Niels-Christiansen L.-L., Nystrom B.T., Hansen G.H., Danielsen E.M. Microvillar membrane domains exist at physiological temperature. Role of galectin-4 as lipid raft stabilizer revealed by 'superrafts'. J. Biol. Chem. 278:2003;15679-15684.
46. Nylhom P.G., Pasher I., Sundell S. The effect of hydrogen bonds on the conformation of glycosphingolipids. Methylated and unmethylated cerebroside studied by X ray single crystal analysis and model calculations. Chem. Phys. Lipids. 52:1990;1-10.
47. Fantini J., Cook D.G., Nathanson N., Spitalnik S.L., Gonzalez-Scarano F. Infection of colonic epithelial cell lines by type 1 human immunodeficiency virus is associated with cell surface expression of galactosyl ceramide, a potential alternative gp120 receptor. Proc. Natl. Acad. Sci. U. S. A. 90:1993;2700-2704.
48. Karlsson K.A. Animal glycosphingolipids as membrane attachment sites for bacteria. Ann. Rev. Biochem. 58:1989;309-350.
49. Tang W., Seino K., Ito M., Konishi T., Senda H., Makuuchi M., Kojima N., Mizuochi T. Requirement of ceramide for adhesion of Helicobacter pylori to glycosphingolipids. FEBS Lett. 504:2001;31-35.
50. Nusrat A., Parkos C.A., Verkade P., Foley C.S., Liang T.W., Innis-Whitehouse W., Eastburn K.K., Madara J.L. Tight junctions are membrane microdomains. J. Cell. Sci. 113:2000;1771-1781.
51. Nusrat A., von Eichel-Streiber C., Turner J.R., Verkade P., Madara J.L., Parkos C.A. Clostridium difficile toxins disrupt epithelial barrier function by altering membrane microdomain localization of tight junction proteins. Infect. Immun. 69:2001;1329-1336.
52. Simons K., van Meer G. Lipid sorting in epithelial cells. Biochemistry. 27:1988;6197-6202.
53. Danielsen E.M. Involvement of detergent-insoluble complexes in the intracellular transport of intestinal brush border enzymes. Biochemistry. 34:1995;1596-1605.
54. Hansen G.H., Niels-Christiansen L.-L., Thorsen E., Immerdal L., Danielsen E.M. Cholesterol depletion of enterocytes. Effect on the Golgi complex and apical membrane trafficking. J. Biol. Chem. 275:2000;5136-5142.
55. Steven V.L., Tang J. Fumonisin B1-induced sphingolipid depletion inhibits vitamin uptake via the glycosylphosphatidylinositol-anchored folate receptor. J. Biol. Chem. 272:1997;18020-18025.
56. Lu L., Walker W.A. Pathologic and physiologic interactions of bacteria with the gastrointestinal epithelium. Am. J. Clin. Nutr. 73:2001;1124S-1130S.
57. Clayton F., Kotler D.P., Kuwada S.K., Morgan T., Stepan C., Kuang J., Le J., Fantini J. Gp120-induced Bob/GPR15 activation. A possible cause of HIV enteropathy. Am. J. Pathol. 159:2001;1933-1939.
58. Maresca M., Mahfoud R., Garmy N., Kotler D.P., Fantini J., Clayton F. The virotoxin model of HVI-1 enteropathy: involvement of GPR15/Bob and galactosylceramide in the cytopathic effects induced by HIV-1 gp120 in the HT-29-D4 intestinal cell line. J. Biomed. Sci. 10:2003;156-166.
59. Popoff M.R. Interactions between bacterial toxins and intestinal cells. Toxicon. 36:1998;665-685.
60. Fasano A. Toxins and the gut: role in human disease. Gut. 50:2002;iii9-iii14.
61. Sansonetti P. Host-pathogen interactions: the seduction of molecular cross-talk. Gut. 50:2002;iii2-iii8.
62. Catron D.M., Sylverster M.D., Lange Y., Kadekoppala M., Jones B.D., Monack D.M., Falkow S., Haldar K. The Salmonella-containing vacuole is a major site of intracellular cholesterol accumulation and recruits the GPI-anchored protein CD55. Cell. Microbiol. 4:2002;315-328.
63. Lafont F., Tran Van Nhieu G., Hanada K., Sansonetti P., van der Groot F.G. Initial steps of Shigella infection depend on the cholesterol/sphingolipid raf-mediated CD44-lpaB interaction. EMBO J. 21:2002;4449-4457.
64. Philpott D.J., McKay D.M., Sherman P.M., Perdue M.H. Infection of T84 cells with enteropathogenic Escherichia coli alters barrier and transport functions. Am. J. Physiol. 270:1996;G634-G645.
65. Jung H.C., Eckmann L., Yang S.K., Panja A., Fierer J., Morzycka-Wrobleska E., Kagnoff M.F. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Invest. 95:1995;55-65.
66. Hedlund M., Duang R.D., Nilsson A., Svanborg C. Sphingomyelin, glycosphingolipids and ceramide signalling in cells exposed to P-fimbriated Escherichia coli. Mol. Microbiol. 29:1998;1297-1306.
67. Fantini J. Synthetic analogs of glycolipids for studies of virus-glycolipid interactions. Methods Enzymol. 311:2000;626-638.
68. Yarema K.J., Bertozzi C.R. Chemical approaches to glycobiology and emerging carbohydrate-based therapeutic agents. Curr. Opin. Chem. Biol. 2:1998;49-61.
69. Zopf D., Roth S. Oligosaccharide anti-infective agents. Lancet. 347:1996;1017-1021.
70. Mylvaganam M., Lingwood C.A. Adamantyl globotriaosyl ceramide: a monovalent soluble mimic which inhibits verotoxin binding to its glycolipid receptor. Biochem. Biophys. Res. Commun. 257:1999;391-394.
71. Simon P.M., Goode P.L., Mobasseri A., Zopf D. Inhibition of Helicobacter pylori binding to gastrointestinal epithelial cells by sialic-acid containing oligosaccharides. Infect. Immun. 65:1997;750-757.
72. Kitov P.I., Sadowska J.M., Mulvey G., Armstrong G.D., Ling H., Pannu N.S., Read R.R.J., Bundle D.R. Shiga-like toxins are neutralized by tailored multivalent carbohydrate ligands. Nature. 403:2000;669-672.
73. Fantini J., Hammache D., Delézay O., Yahi N., André- Barrès C., Rico-Lattes I., Lattes A. Synthetic soluble analogs of galactosylceramide (GalCer) bind to the V3 domain of HIV-1 gp120 and inhibit HIV-1-induced fusion and entry. J. Biol. Chem. 272:1997;7245-7252.
74. Kozaki S., Kamata Y., Watarai S., Nishiki T.I., Mochida S. Ganglioside GT1b as a complementary receptor component for Clostridium botulinum neurotoxins. Microb. Pathog. 25:1998;91-99.
75. Swaminatahn S., Eswaramoorthy S. Structural analysis of the catalytic and binding sites of Clostridium botulinum neurotoxin B. Nat. Struct. Biol. 7:2000;693-699.
76. Jacewicz M.S., Clausen H., Nudelman E., Donohuerolfe A., Keusch G.T. Pathogenesis of Shigella diarrhea: II. Isolation of a Shigella toxin-binding glycolipid from rabbit jejunum and Hela cells and its identification as globotriaosylceramide. J. Exp. Med. 163:1986;1391-1404.
77. Lingwood C.A. Verotoxins and their glycolipid receptors. Adv. Lipid Res. 25:1993;189-211.
78. Merritt E.A., Sarfaty S., Feil I.K., Hol W.G.J. Structural foundation for the design of receptor anatagonists targeting Escherichia coli heat-labile enterotoxin. Structure. 5:1997;1485-1499.
79. Lencer W.I. Microbes and microbial toxins: paradigms for microbial-mucosal interactions: V. Cholera: invasion of the intestinal epithelial barrier by a stably folded toxin. Am. J. Physiol. 280:2001;G781-G786.
80. Backenson B., Coleman J., Benach J. Borrelia burgdorferi shows specificity of binding to glycosphingolipids. Infect. Immun. 63:1995;2811-2817.
81. Krivan H.C., Roberts D.D., Ginsburg V. Many pulmonary pathogenic bacteria bind specifically to the carbohydrate sequence GalNAc beta 1-4Gal found in some glycolipids. Proc. Natl. Acad. Sci. U. S. A. 85:1988;6157-6161.
82. Gatfield J., Pieters J. Essential role for cholesterol in entry of mycobacteria into macrophages. Science. 288:2000;1647-1650.
83. Jenkins J., Pickersgill R. The architecture of parallel β-helices and related folds. Prog. Biophys. Mol. Biol. 77:2001;111-175.
84. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling. Electrophoresis. 18:1997;2714-2723.