Cholesterol-sensitive modulation of transcytosis

Molecular Biology of the Cell

Volumn 18, Issue 6, 2007, Pages 2057-2071

  Leyt, Julieta ^a   Melamed Book, Naomi ^a   Vaerman, Jean Pierre ^b   Cohen, Shulamit ^a   Weiss, Aryeh M ^a,c   Aroeti, Benjamin ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b DE DUVE INSTITUTE   (Belgium)

^c BAR ILAN UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CYCLODEXTRIN; CAVEOLIN 1; CHOLESTEROL; DETERGENT; IMMUNOGLOBULIN A; TRANSFERRIN RECEPTOR; TYROSINE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; DEPOLARIZATION; ENDOCYTOSIS; ENDOSOME; HUMAN; INTERNALIZATION; LIPID RAFT; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCYTOSIS;

ANIMALS; BETA-CYCLODEXTRINS; CAVEOLIN 1; CELL LINE; CELL POLARITY; CHOLESTEROL; DOGS; ENDOCYTOSIS; ENDOSOMES; HUMANS; IMMUNOGLOBULIN A; LIGANDS; MEMBRANE MICRODOMAINS; RAB GTP-BINDING PROTEINS; RECEPTORS, FC; RECEPTORS, TRANSFERRIN; SIGNAL TRANSDUCTION;

EID: 34250353156     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-08-0735     Document Type: Article

References (71)

1. Adam, M., Rodriguez, A., Turbide, C., Larrick, J., Meighen, E., and Johnstone, R. M. (1984). In vitro acylation of the transferrin receptor. J. Biol. Chem. 259, 15460-15463.
2. Apodaca, G., Katz, L. A., and Mostov, K. E. (1994). Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125, 67-86.
3. Aroeti, B., Kosen, P. A., Kuntz, I. D., Cohen, F. E., and Mostov, K. E. (1993). Mutational and secondary structural analysis of the basolateral sorting signal of the polymeric immunoglobulin receptor. J. Cell Biol. 123, 1149-1160.
4. Aroeti, B., and Mostov, K. E. (1994). Polarized sorting of the polymeric immunoglobulin receptor in the exocytotic and endocytotic pathways is controlled by the same amino acids. EMBO J. 13, 2297-2304.
5. Barroso, M., and Sztul, E. S. (1994). Basolateral to apical transcytosis in polarized cells is indirect and involves BFA and trimeric G protein sensitive passage through the apical endosome. J. Cell Biol. 124, 83-100.
6. Batista, A., Millan, J., Mittelbrunn, M., Sanchez-Madrid, F., and Alonso, M. A. (2004). Recruitment of transferrin receptor to immunological synapse in response to TCR engagement. J. Immunol. 172, 6709-6714.
7. Bomsel, M., and Mostov, K. (1992). Role of heterotrimeric G proteins in membrane traffic. Mol. Biol. Cell 3, 1317-1328.
8. Breitfeld, P., Casanova, J. E., Harris, J. M., Simister, N. E., and Mostov, K. E. (1989). Expression and analysis of the polymeric immunoglobulin receptor. Methods Cell Biol. 32, 329-337.
9. Brown, D. A., and Rose, J. K. (1992). Sorting of GPl-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544.
10. Brown, P. S., Wang, E., Aroeti, B., Chapin, S. J., Mostov, K. E., and Dunn, K. W. (2000). Definition of distinct compartments in polarized Madin-Darby canine kidney (MDCK) cells for membrane-volume sorting, polarized sorting and apical recycling. Traffic 1, 124-140.
11. Burgos, P. V., Klattenhoff, C., de la Fuente, E., Rigotti, A., and Gonzalez, A. (2004). Cholesterol depletion induces PKA-mediated basolateral-to-apical transcytosis of the scavenger receptor class B type I in MDCK cells. Proc. Natl. Acad. Sci. USA 101, 3845-3850.
12. Bush, W. S., Ihrke, G., Robinson, J. M., and Kenworthy, A. K. (2006). Antibody-specific detection of caveolin-1 in subapical compartments of MDCK cells. Histochem. Cell Biol. 126, 27-34.
13. Casanova, J. E., Apodaca, G., and Mostov, K. E. (1991). An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell 66, 65-75.
14. Casanova, J. E., Wang, X., Kumar, R., Bharrur, S. G., Navarre, J., Woodrum, J. E., Altschuler, Y., Ray, G. S., and Goldenring, J. R. (1999). Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 10, 47-61.
15. De Marco, M. C., Martin-Belmonte, F., Kremer, L., Albar, J. P., Correas, I., Vaerman, J. P., Marazuela, M., Byrne, J. A., and Alonso, M. A. (2002). MAL2, a novel raft protein of the MAL family, is an essential component of the machinery for transcytosis in hepatoma HepG2 cells. J. Cell Biol. 159, 37-44.
16. Foster, L. J., De Hoog, C. L., and Mann, M. (2003). Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. USA 100, 5813-5818.
17. Gagescu, R., Demaurex, N., Parton, R. G., Hunziker, W., Huber, L. A., and Gruenberg, J. (2000). The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol. Biol. Cell 11, 2775-2791.
18. Gan, Y., McGraw, T. E., and Rodriguez-Boulan, E. (2002). The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane. Nat. Cell Biol. 4, 605-609.
19. Gibson, A., Futter, C. E., Maxwell, S., Allchin, E. H., Shipman, M., Kraehenbuhl, J. P., Domingo, D., Odorizzi, G., Trowbridge, I. S., and Hopkins, C. R. (1998). Sorting mechanisms regulating membrane protein traffic in the apical transcytotic pathway of polarized MDCK cells. J. Cell Biol. 143, 81-94.
20. Giffroy, D., Langendries, A., Maurice, M., Daniel, F., Lardeux, B., Courtoy, P. J., and Vaerman, J. P. (1998). In vivo stimulation of polymeric Ig receptor transcytosis by circulating polymeric IgA in rat liver. Int. Immunol. 10, 347-354.
21. Graf, G. A., Matveev, S. V., and Smart, E. J. (1999). Class B scavenger receptors, caveolae and cholesterol homeostasis. Trends Cardiovasc. Med. 9, 221-225.
22. Grimmer, S., Iversen, T. G., van Deurs, B., and Sandvig, K. (2000). Endosome to Golgi transport of ricin is regulated by cholesterol. Mol. Biol. Cell 11, 4205-4216.
23. Hansen, G. H., Niels-Christiansen, L. L., Immerdal, L., Hunziker, W., Kenny, A. J., and Danielsen, E. M. (1999). Transcytosis of immunoglobulin A in the mouse enterocyte occurs through glycolipid raft- and rab17-containing compartments. Gastroenterology 116, 610-622.
24. Hao, M., Lin, S. X., Karylowski, O. J., Wustner, D., McGraw, T. E., and Maxfield, F. R. (2002). Vesicular and non-vesicular sterol transport in living cells. The endocytic recycling compartment is a major sterol storage organelle. J. Biol. Chem. 277, 609-617.
25. Harder, T., Scheiffele, P., Verkade, P., and Simons, K. (1998). Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141, 929-942.
26. Ikonen, E., and Parton, R. G. (2000). Caveolins and cellular cholesterol balance. Traffic 1, 212-217.
27. Inoue, H. et al. (2002). Lipid rafts as the signaling scaffold for NK cell activation: tyrosine phosphorylation and association of LAT with phosphatidylinositol 3-kinase and phospholipase C-gamma following CD2 stimulation. Eur. J. Immunol. 32, 2188-2198.
28. Jing, S. Q., and Trowbridge, I. S. (1987). identification of the intermolecular disulfide bonds of the human transferrin receptor and its lipid-attachment site. EMBO J. 6, 327-331.
29. Kilsdonk, E. P., Yancey, P. G., Stoudt, G. W., Bangerter, F. W., Johnson, W. J., Phillips, M. C., and Rothblat, G. H. (1995). Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 270, 17250-17256.
30. Kim, Y. N., Dam, P., and Bertics, P. J. (2002). Caveolin-1 phosphorylation in human squamous and epidermoid carcinoma cells: dependence on ErbB1 expression and Src activation. Exp. Cell Res. 280, 134-147.
31. Lachmanovich, E., Shvartsman, D. E., Malka, Y., Botvin, C., Henis, Y. I., and Weiss, A. M. (2003). Co-localization analysis of complex formation among membrane proteins by computerized fluorescence microscopy: application to immunofluorescence co-patching studies. J. Microsc. 212, 122-131.
32. Lamm, M. E., Nedrud, J. G., Kaetzel, C. S., and Mazanec, M. B. (1995). IgA and mucosal defense. Apmis 103, 241-246.
33. Lawrence, C. M., Ray, S., Babyonyshev, M., Galluser, R., Borhani, D. W., and Harrison, S. C. (1999). Crystal structure of the ectodomain of human transferrin receptor. Science 286, 779-782.
34. Lee, H., Woodman, S. E., Engelman, J. A., Volonte, D., Galbiati, F., Kaufman, H. L., Lublin, D. M., and Lisanti, M. P. (2001). Palmitoylation of caveolin-1 at a single site (Cys-156) controls its coupling to the c-Src tyrosine kinase: targeting of dually acylated molecules (GPI-linked, transmembrane, or cytoplasmic) to caveolae effectively uncouples c-Src and caveolin-1 (TYR-14). J. Biol. Chem. 276, 35150-35158.
35. Li, S., Seitz, R., and Lisanti, M. P. (1996). Phosphorylation of caveolin by src tyrosine kinases. The alpha-isoform of caveolin is selectively phosphorylated by v-Src in vivo. J. Biol. Chem. 271, 3863-3868.
36. Lu, M. L., Schneider, M. C., Zheng, Y., Zhang, X., and Richie, J. P. (2001). Caveolin-1 interacts with androgen receptor. A positive modulator of androgen receptor mediated transactivation. J. Biol. Chem. 276, 13442-13451.
37. Luton, F., Cardone, M. H., Zhang, M., and Mostov, K. E. (1998). Role of tyrosine phosphorylation in ligand-induced regulation of transcytosis of the polymeric Ig receptor. Mol. Biol. Cell 9, 1787-1802.
38. Luton, F., and Mostov, K. E. (1999). Transduction of basolateral-to- apical signals across epithelial cells: ligand-stimulated transcytosis of the polymeric immunoglobulin receptor requires two signals. Mol. Biol. Cell 10, 1409-1427.
39. Luton, F., Verges, M., Vaerman, J. P., Sudol, M., and Mostov, K. E. (1999). The SRC family protein tyrosine kinase p62yes controls polymeric IgA transcytosis in vivo. Mol. Cell 4, 627-632.
40. Martin, S., and Parton, R. G. (2005). Caveolin, cholesterol, and lipid bodies. Semin. Cell Dev. Biol. 16, 163-174.
41. Maxfield, F. R., and Wustner, D. (2002). Intracellular cholesterol transport. J. Clin. Invest. 110, 891-898.
42. Maxfield, F. R., and Yamashiro, D. J. (1987). Endosome acidification and the pathways of receptor-mediated endocytosis. Adv. Exp. Med. Biol. 225, 189-198.
43. Mayor, S., Sabharanjak, S., and Maxfield, F. R. (1998). Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO J. 17, 4626-4638.
44. Melkonian, K. A., Ostermeyer, A. G., Chen, J. Z., Roth, M. G., and Brown, D. A. (1999). Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 274, 3910-3917.
45. Moffett, S., Brown, D. A., and Linder, M. E. (2000). Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 275, 2191-2198.
46. Mostov, K., Apodaca, G., Aroeti, B., and Okamoto, C. (1992). Plasma membrane protein sorting in polarized epithelial cells. J. Cell Biol. 116, 577-583.
47. Mundy, D. I., Machleidt, T., Ying, Y. S., Anderson, R. G., and Bloom, G. S. (2002). Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J. Cell Sci. 115, 4327-4339.
48. Nadler, M. J., Hu, X. E., Cassady, J. M., and Geahlen, R. L. (1994). Posttranslational acylation of the transferrin receptor in LSTRA cells with myristate, palmitate and stearate: evidence for distinct acyltransferases. Biochim. Biophys. Acta 1213, 100-106.
49. Naslavsky, N., Stein, R., Yanai, A., Friedlander, G., and Taraboulos, A. (1997). Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J. Biol. Chem. 272, 6324-6331.
50. Nyasae, L. K., Hubbard, A. L., and Tuma, P. L. (2003). Transcytotic efflux from early endosomes is dependent on cholesterol and glycosphingolipids in polarized hepatic cells. Mol. Biol. Cell 14, 2689-2705.
51. Okamoto, C. T., Shia, S. P., Bird, C., Mostov, K. E., and Roth, M. G. (1992). The cytoplasmic domain of the polymeric immunoglobulin receptor contains two internalization signals that are distinct from its basolateral sorting signal. J. Biol. Chem. 267, 9925-9932.
52. Okamoto, C. T., Song, W., Bomsel, M., and Mostov, K. E. (1994). Rapid Internalization of the polymeric immunoglobulin receptor requires phosphorylated serine 726. J. Biol. Chem. 269, 15676-15682.
53. Okamoto, T., Schlegel, A., Scherer, P. E., and Lisanti, M. P. (1998). Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J. Biol. Chem. 273, 5419-5422.
54. Orlichenko, L., Huang, B., Krueger, E., and McNiven, M. A. (2006). Epithelial growth factor-induced phosphorylation of caveolin 1 at tyrosine 14 stimulates caveolae formation in epithelial cells. J. Biol. Chem. 281, 4570-4579.
55. Orzech, E., Schlessinger, K., Weiss, A., Okamoto, C. T., and Aroeti, B. (1999). Interactions of the AP-1 Golgi adaptor with the polymeric immunoglobulin receptor and their possible role in mediating BFA-sensitive basolateral targeting from the trans-Golgi network. J. Biol. Chem. 274, 2201-2215.
56. Padbilewicz, B., and Mellman, I. (1990). ATP and cytosol requirements for transferrin recycling in intact and disrupted MDCK cells. EMBO J. 9, 3477-3487.
57. Rodal, S. K., Skretting, G., Garred, O., Vilhardt, F., van Deurs, B., and Sandvig, K. (1999). Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 10, 961-974.
58. Rojas, R., and Apodaca, G. (2002). Immunoglobulin transport across polarized epithelial cells. Nat. Rev. Mol. Cell Biol. 3, 944-955.
59. Sarnataro, D., Nitsch, L., Hunziker, W., and Zurzolo, C. (2000). Detergent insoluble microdomains are not involved in transcytosis of polymeric Ig receptor in FRT and MDCK cells. Traffic 1, 794-802.
60. Scheiffele, P., Roth, M. G., and Simons, K. (1997). Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16, 5501-5508.
61. Shvartsman, D. E., Kotler, M., Tall, R. D., Roth, M. G., and Henis, Y. I. (2003). Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts. J. Cell Biol. 163, 879-888.
62. Simons, K., and Toomre, D. (2000). Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39.
63. Singer, K. L., and Mostov, K. E. (1998). Dimerization of the polymeric immunoglobulin receptor controls its transcytotic trafficking. Mol. Biol. Cell 9, 901-915.
64. Solari, R., Kuhn, L., and Kraehenbuhl, J.-P. (1985). Antibodies recognizing different domains of the polymeric immunoglobulin receptor. J. Biol. Chem. 260, 1141-1145.
65. Song, W., Bomsel, M., Casanova, J., Vaerman, J. P., and Mostov, K. (1994). Stimulation of transcytosis of the polymeric immunoglobulin receptor by dimeric IgA. Proc. Natl. Acad. Sci. USA 91, 163-166.
66. Subtil, A., Gaidarov, I., Kobylarz, K., Lampson, M. A., Keen, J. H., and McGraw, T. E. (1999). Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. USA 96, 6775-6780.
67. Wang, E., Brown, P. S., Aroeti, B., Chapin, S. J., Mostov, K. E., and Dunn, K. W. (2000). Apical and basolateral endocytic pathways of MDCK cells meet in acidic common endosomes distinct from a nearly-neutral apical recycling endosome. Traffic 1, 480-493.
68. Waugh, M. G., Minogue, S., Anderson, J. S., dos Santos, M., and Hsuan, J. J. (2001). Signalling and non-caveolar rafts. Biochem. Soc. Trans. 29, 509-511.
69. White, S., Miller, K., Hopkins, C., and Trowbridge, I. S. (1992). Monoclonal antibodies against defined epitopes of the human transferrin receptor cytoplasmic tail. Biochim. Biophys. Acta 1136, 28-34.
70. Wustner, D., Herrmann, A., Hao, M., and Maxfield, F. R. (2002). Rapid nonvesicular transport of sterol between the plasma membrane domains of polarized hepatic cells. J. Biol. Chem. 277, 30325-30336.
71. Yancey, P. G., Rodrigueza, W. V., Kilsdonk, E. P., Stoudt, G. W., Johnson, W. J., Phillips, M. C., and Rothblat, G. H. (1996). Cellular cholesterol efflux mediated by cyclodextrins. Demonstration of kinetic pools and mechanism of efflux. J. Biol. Chem. 271, 16026-16034.