Heterogeneity of detergent-insoluble membranes from human intestine containing caveolin-1 and ganglioside G(M)1

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 278, Issue 6 41-6, 2000, Pages

  Badizadegan, Kamran ^a,d   Dickinson, Bonny L ^a   Wheeler, Heidi E ^a   Blumberg, Richard S ^a,c   Holmes, Randall K ^b   Lencer, Wayne I ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c HARVARD UNIVERSITY   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Caveolae; Cholera toxin; Toxigenic diarrhea

Indexed keywords

CAVEOLIN; CHOLERA TOXIN; DETERGENT; GANGLIOSIDE GM1;

ARTICLE; CELL HETEROGENEITY; CELL MEMBRANE; CONTROLLED STUDY; DIARRHEA; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE; MOLECULAR RECOGNITION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RECEPTOR BINDING;

EID: 0033932139     PISSN: 01931857     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpgi.2000.278.6.g895     Document Type: Article

References (51)

1. Anderson RG. The caveolae membrane system. Annu Rev Biochem 67: 199-225, 1998.
2. Balk SP, Burke S, Polischuk JE, Frantz ME, Yang L, Porcelli S, Colgan SP, and Blumberg RS. Beta 2-microglobulin-independent MHC class Ib molecule expressed by human intestinal epithelium. Science 265: 259-262, 1994.
3. Bastiaens PI, Majoul IV, Verveer PJ, Soling HD, and Jovin TM. Imaging the intracellular trafficking and state of the AB5 quaternary structure of cholera toxin. EMBO J 15: 4246-4253, 1996.
4. Blumberg RS, Terhorst C, Bleicher P, McDermott FV, Allan CH, Landau SB, Trier JS, and Balk SP. Expression of a nonpolymorphic MHC class I-like molecule, CD1D, by human intestinal epithelial cells. J Immunol 147: 2518-2524, 1991.
5. Bradbury NA, Clark JA, Watkins SC, Widnell CC, Smith HI, and Bridges RJ. Characterization of the internalization pathways for the cystic fibrosis transmembrane conductance regulator. Am J Physiol Lung Cell Mol Physiol 276: L659-L668, 1999.
6. +-ATPase-coated endocytic vesicles in intercalated cells. J Histochem Cytochem 46: 205-214, 1998.
7. Brown DA and London E. Functions of lipid rafts in biological membranes. Ann Rev Cell Dev Biol 14: 111-136, 1998.
8. Connell TD and Holmes RK. Characterization of hybrid toxins produced in Escherichia coli by assembly of A and B polypeptides from type I and type II heat-labile enterotoxins. Infect Immun 60: 1653-1661, 1992.
9. Engelman JA, Wykoff CC, Yasuhara S, Song KS, Okamoto T, and Lisanti MP. Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J Biol Chem 272: 16374-16381, 1997.
10. Engelman JA, Zhang X, Galbiati F, Volonte D, Sotgia F, Pestell RG, Minetti C, Scherer PE, Okamoto T, and Lisanti MP. Molecular genetics of the caveolin gene family: implications for human cancers, diabetes, Alzheimer disease, and muscular dystrophy. Am J Hum Genet 63: 1578-1587, 1998.
11. Field FJ, Born E, Murthy S, and Mathur SN. Caveolin is present in intestinal cells: role in cholesterol trafficking? J Lipid Res 39: 1938-1950, 1998.
12. Fra AM, Masserini M, Palestini P, Sonnino S, and Simons K. A photo-reactive derivative of ganglioside GM1 specifically cross-links VIP21-caveolin on the cell surface. FEBS Lett 375: 11-14, 1995.
13. Fra AM, Williamson E, Simons K, and Parton RG. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci USA 92: 8655-8659, 1995.
14. Fukuta S, Magnani JL, Twiddy EM, Holmes RK, and Ginsburg V. 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, 1988.
15. Holmes RK, Jobling MG, and Connell TD. Cholera toxin and related enterotoxins of gram-negative bacteria. In: Bacterial Toxins and Virulence Factors in Disease, edited by Moss J, Iglewski B, Vaughan M, and Tu AT. New York: Dekker, 1995, p. 225-255.
16. Holmes RK and Twiddy EM. Characterization of monoclonal antibodies that react with unique and cross-reacting determinants of cholera enterotoxin and its subunits. Infect Immun 42: 914-923, 1983.
17. Holmes RK, Twiddy EM, Pickett CL, Marcus H, Jobling MG, and Petitjean FMJ. The Escherichia coli/Vibrio cholera family of enterotoxins. In: Symposium on Molecular Mode of Action of Selected Microbial Toxins in Foods and Feeds, edited by Pohland AE, Dowell VR, and Richard JL. New York: Plenum, 1990, p. 91-102.
18. Iwabuchi K, Handa K, and Hakomori S. Separation of "glycosphingolipid signaling domain" from caveolin-containing membrane fraction in mouse melanoma B16 cells and its role in cell adhesion coupled with signaling. J Biol Chem 273: 33766-33773, 1998.
19. Lee SW, Reimer CL, Oh P, Campbell DB, and Schnitzer JE. Tumor cell growth inhibition by caveolin re-expression in human breast cancer cells. Oncogene 16: 1391-1397, 1998.
20. Lencer WI, Constable C, Moe S, Jobling MG, Webb HM, Ruston S, Madara JL, Hirst TR, and Holmes RK. Targeting of cholera toxin and Escherichia coli heat labile toxin in polarized epithelia: role of COOH-terminal KDEL. J Cell Biol 131: 951-962, 1995.
21. Lencer WI, de Almeida JB, Moe S, Stow JL, Ausiello DA, and Madara JL. Entry of cholera toxin into polarized human intestinal epithelial cells. Identification of an early brefeldin A sensitive event required for A1-peptide generation. J Clin Invest 92: 2941-2951, 1993.
22. Lencer WI, Delp C, Neutra MR, and Madara JL. Mechanism of cholera toxin action on a polarized human intestinal epithelial cell line: role of vesicular traffic. J Cell Biol 117: 1197-1209, 1992.
23. Lencer WI, Hirst TR, and Holmes RK. Membrane traffic and the cellular uptake of cholera toxin. Biochim Biophys Acta 1450: 177-190, 1999.
24. Lencer WI, Moe S, Rufo PA, and Madara JL. Transcytosis of cholera toxin subunits across model human intestinal epithelia. Proc Natl Acad Sci USA 92: 10094-10098, 1995.
25. Li S, Galbiati F, Volonte D, Sargiacomo M, Engelman JA, Das K, Scherer PE, and Lisanti MP. Mutational analysis of caveolin-induced vesicle formation. Expression of caveolin-1 recruits caveolin-2 to caveolae membranes. FEBS Lett 434: 127-134, 1998.
26. Majoul IV, Bastiaens PI, and Soling HD. Transport of an external Lys-Asp-Glu-Leu (KDEL) protein from the plasma membrane to the endoplasmic reticulum: studies with cholera toxin in Vero cells. J Cell Biol 133: 777-789, 1996.
27. Mayor S, Rothberg KG, and Maxfield FR. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science 264: 1948-1951, 1994.
28. Mirre C, Monlauzeur L, Garcia M, Delgrossi MH, and Le Bivic A. Detergent-resistant membrane microdomains from Caco-2 cells do not contain caveolin. Am J Physiol Cell Physiol 271: C887-C894, 1996.
29. Nabeyama A and Leblond CP. "Caveolated cells" characterized by deep surface invaginations and abundant filaments in mouse gastro-intestinal epithelia. Am J Anat 140: 147-165, 1974.
30. Newman GR, Campbell L, von Ruhland C, Jasani B, and Gumbleton M. Caveolin and its cellular and subcellular immunolocalisation in lung alveolar epithelium: implications for alveolar epithelial type I cell function. Cell Tissue Res 295: 111-120, 1999.
31. Okamoto T, Schlegel A, Scherer PE, and Lisanti MP. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem 273: 5419-5422, 1998.
32. Orlandi PA. Protein-disulfide isomerase-mediated reduction of the A subunit of cholera toxin in a human intestinal cell line. J Biol Chem 272: 4591-4599, 1997.
33. Orlandi PA and Fishman PH. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 141: 905-915, 1998.
34. Orlandi PA and Fishman PH. Orientation of cholera toxin bound to target cells. J Biol Chem 268: 17038-17044, 1993.
35. Parton RG. Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J Histochem Cytochem 42: 155-166, 1994.
36. Peters KR, Carley WW, and Palade GE. Endothelial plasmalemmal vesicles have a characteristic striped bipolar surface structure. J Cell Biol 101: 2233-2238, 1985.
37. Pickett CL, Twiddy EM, Coker C, and Holmes RK. Cloning, nucleotide sequence, and hybridization studies of the type IIb heat-labile enterotoxin gene of Escherichia coli. J Bacteriol 171: 4945-4952, 1989.
38. Rietveld A and Simons K. The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim Biophys Acta 1376: 467-479, 1998.
39. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, and Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 68: 673-682, 1992.
40. Roy S, Luetterforst R, Harding A, Apolloni A, Etheridge M, Stang E, Rolls B, Hancock JF, and Parton RG. Dominant-negative caveolin inhibits H-ras function by disrupting cholesterol-rich plasma membrane domains. Nat Cell Biol 1: 98-105, 1999.
41. Scheel J, Srinivasan J, Honnert U, Henske A, and Kurzchalia TV. Involvement of caveolin-1 in meiotic cell-cycle progression in C. elegans. Nat Cell Biol 1: 127-129, 1999.
42. Schlegel A, Volonte D, Engelman JA, Galbiati F, Mehta P, Zhang XL, Scherer PE, and Lisanti MP. Crowded little caves: structure and function of caveolae. Cell Signal 10: 457-463, 1998.
43. Schnitzer JE, McIntosh DP, Dvorak AM, Liu J, and Oh P. Separation of caveolae from associated microdomains of GPI-anchored proteins. Science 269: 1435-1439, 1995.
44. Seriwatana J, Echeverria P, Taylor DN, Rasrinaul L, Brown JE, Peiris JS, and Clayton CL. Type II heat-labile enterotoxin-producing Escherichia coli isolated from animals and humans. Infect Immun 56: 1158-1161, 1988.
45. Shaul PW and Anderson RG. Role of plasmalemmal caveolae in signal transduction. Am J Physiol Lung Cell Mol Physiol 275: L843-L851, 1998.
46. Simons K and Ikonen E. Functional rafts in cell membranes. Nature 387: 569-572, 1997.
47. Spangler BD. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev 56: 622-647, 1992.
48. Stan RV, Roberts WG, Predescu D, Ihida K, Saucan L, Ghitescu L, and Palade GE. Immunoisolation and partial characterization of endothelial plasmalemmal vesicles (caveolae). Mol Biol Cell 8: 595-605, 1997.
49. Vogel U, Sandvig K, and van Deurs B. Expression of caveolin-1 and polarized formation of invaginated caveolae in Caco-2 and MDCKII cells. J Cell Sci 111: 825-832, 1998.
50. Waugh MG, Lawson D, Tan SK, and Hsuan JJ. Phosphatidylinositol 4-phosphate synthesis in immunoisolated caveolae-like vesicles and low buoyant density non-caveolar membranes. J Biol Chem 273: 17115-17121, 1998.
51. Wolf AA, Jobling MG, Wimer-Mackin S, Ferguson-Maltzman M, Madara JL, Holmes RK, and Lencer WI. Ganglioside structure dictates signal transduction by cholera toxin and association with caveolae-like membrane domains in polarized epithelia. J Cell Biol 141: 917-927, 1998.