Delivery of raft-associated, GPI-anchored proteins to the apical surface of polarized MDCK cells by a transcytotic pathway

Nature Cell Biology

Volumn 6, Issue 4, 2004, Pages 297-307

  Polishchuk, Roman ^a,b   Di Pentima, Alessio ^b   Lippincott Schwartz, Jennifer ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b Ist di Ric Farmacol Mario Negri ^*  (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CELL PROTEIN; CLATHRIN; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE PROTEIN;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CELL ASSAY; CELL POLARITY; CELL SURFACE; CONTROLLED STUDY; ENDOCYTOSIS; EPITHELIUM CELL; EXOCYTOSIS; HUMAN; HUMAN CELL; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEIN TRANSPORT; TIGHT JUNCTION; TRANS GOLGI NETWORK; TRANSCYTOSIS;

ANIMALS; BIOLOGICAL MARKERS; CELL LINE; CELL POLARITY; CRICETINAE; DOGS; ENDOCYTOSIS; EPITHELIAL CELLS; EXOCYTOSIS; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; HYDROLYZABLE TANNINS; KIDNEY; MEMBRANE FUSION; MEMBRANE MICRODOMAINS; MICROSCOPY, ELECTRON; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; TRANS-GOLGI NETWORK; TRANSPORT VESICLES;

ANIMALIA;

EID: 2342599664     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1109     Document Type: Article

References (50)

1. Rodriguez-Boulan, E. & Powell, S. K. Polarity of epithelial and neuronal cells. Annu. Rev. Cell Biol. 8, 395-427 (1992).
2. Mostov, K. E., Verges, M. & Altschuler, Y. Membrane traffic in polarized epithelial cells. Curr. Opin. Cell Biol. 12, 483-490 (2000).
3. Keller, P. & Simons, K. Post-Golgi biosynthetic trafficking. J. Cell Sci. 110, 3001-3009 (1997).
4. Matter, K. & Mellman, I. Mechanisms of cell polarity: sorting and transport in epithelial cells. Curr. Opin. Cell Biol. 6, 545-554 (1994).
5. Nelson, W. J. & Yeaman, C. Protein trafficking in the exocytic pathway of polarized epithelial cells. Trends Cell. Biol. 11, 483-486 (2001).
6. Fiedler, K. & Simons, K. The role of N-glycans in the secretory pathway. Cell 81, 309-312 (1995).
7. Rodriguez-Boulan, E. & Gonzalez, A. Glycans in post-Golgi apical targeting: sorting signals or structural props? Trends Cell Biol. 9, 291-294 (1999).
8. Harder, T. & Simons, K. Caveolae, DIGs, and the dynamics of sphingolipid cholesterol microdomains. Curr. Opin. Cell Biol. 9, 534-542 (1997).
9. Simons, K. & Ikonen, E. Functional rafts in cell membranes. Nature 387, 569-572 (1997).
10. Casanova, J. E., Apodaca, G. & Mostov, K. E. An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell 66, 65-75 (1991).
11. Hunziker, W., Harter, C., Matter, K. & Mellman, I. Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell. 66, 907-920 (1991).
12. Folsch, H., Ohno, H., Bonifacino, J. S. & Mellman, I. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 99, 189-198 (1999).
13. Gan, Y., McGraw, T. E. & Rodriguez-Boulan, E. The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane. Nature Cell Biol. 4, 605-609 (2002).
14. Traub, L. M. & Apodaca, G. AP-1B: polarized sorting at the endosome. Nature Cell Biol. 5, 1045-1047 (2003).
15. Maier, O., Ait Slimane, T. & Hoekstra, D. Membrane domains and polarized trafficking of sphingolipids. Semin. Cell Dev. Biol. 12, 149-161 (2001).
16. Nichols, B. J. et al. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153, 529-541 (2001).
17. Sabharanjak, S., Sharma, P., Parton, R. G. & Mayor, S. GP1-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell 2, 411-423 (2002).
18. Slimane, T. A., Trugnan, G. & Van Ijzendoorn, S. C. Hoekstra. D. Raft-mediated trafficking of apical resident proteins occurs in both direct and transcytotic pathways in polarized hepatic cells: role of distinct lipid microdomains. Mol. Biol. Cell 14, 611-624 (2003).
19. Hirschberg, K. et al. Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells. J. Cell Biol. 143, 1485-1503 (1998).
20. Keller, P., Toomre, D., Diaz, E., White, J. & Simons, K. Multicolour imaging of post-Golgi sorting and trafficking in live cells. Nature Cell Biol. 3, 140-149 (2001).
21. Schmoranzer, J., Goulian, M., Axelrod, D. & Simon, S. M. Imaging constitutive exocytosis with total internal reflection fluorescence microscopy. J. Cell Biol. 149, 23-32 (2000).
22. Kreitzer, G. et al. Three-dimensional analysis of post-Golgi carrier exocytosis in epithelial cells. Nature Cell Biol. 5, 126-136 (2003).
23. Kreitzer, G., Marmorstein, A., Okamoto, P., Vallee, R. & Rodriguez-Boulan, E. Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein. Nature Cell Biol. 2, 125-127 (2000).
24. Ihrke, G. & Hubbard, A. L. Control of vesicle traffic in hepatocytes. Prog. Liver Dis. 13, 63-99 (1995).
25. Presley, J. F. et al. Dissection of COPI and Arf1 dynamics in vivo and role in Golgi membrane transport. Nature 417, 187-193 (2002).
26. Matlin, K. S. & Simons, K. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell 34, 233-243 (1983).
27. Polishchuk, R. S. et al. Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J. Cell Biol. 148, 45-58 (2000).
28. Yeaman, C. et al. Protein kinase D regulates basolateral membrane protein exit from trans-Golgi network. Nature Cell Biol. 6, 106-112 (2004).
29. Barnard, R. J., Morgan, A. & Burgoyne, R. D. Stimulation of NSF ATPase activity by α-SNAP is required for SNARE complex disassembly and exocytosis. J. Cell Biol. 139, 875-883 (1997).
30. Low, S. H. et al. The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells. J. Cell Biol. 141, 1503-1513 (1998).
31. Newman, T. M., Tian, M. & Gomperts, B. D. Ultrastructural characterization of tannic acid-arrested degranulation of permeabilized guinea pig eosinophils stimulated with GTP-γ-S. Eur. J. Cell Biol. 70, 209-220 (1996).
32. Brown, D. A., Crise, B. & Rose, J. K. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science 245, 1499-1501 (1989).
33. Lisanti, M. P., Caras, I. W., Davitz, M. A. & Rodriguez-Boulan, E. A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells. J. Cell Biol. 109, 2145-2156 (1989).
34. Brown, D. A. & Rose, J. K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544 (1992).
35. Fiedler, K., Kobayashi, T., Kurzchalia, T. V. & Simons, K. Glycosphingolipid-enriched, detergent-insoluble complexes in protein sorting in epithelial cells. Biochemistry 32, 6365-6373 (1993).
36. Friedrichson, T. & Kurzchalia, T. V. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394, 802-805 (1998).
37. Scheiffele, P. et al. Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J. Cell Biol. 140, 795-806 (1998).
38. Parton, R. G. Caveolae - from ultrastructure to molecular mechanisms. Nature Rev. Mol. Cell Biol. 4, 162-167 (2003).
39. Peters, P. J. et al. Trafficking of prion proteins through a caveolae-mediated endosomal pathway. J. Cell Biol. 162, 703-717 (2003).
40. Mostov, K. E. & Deitcher, D. L. Polymeric immunoglobulin receptor expressed in MDCK cells transcytoses IgA. Cell 46, 613-621 (1986).
41. Apodaca, G., Katz, L. A. & Mostov, K. E. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125, 67-86 (1994).
42. Zurzolo, C., Lisanti, M. P., Caras, I. W., Nitsch, L. & Rodriguez-Boulan, E. Glycosylphosphatidylinositol-anchored proteins are preferentially targeted to the basolateral surface in Fischer rat thyroid epithelial cells. J. Cell Biol. 121, 1031-1039 (1993).
43. Lipardi, C. et al. Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI)-anchored proteins in epithelial cells. J. Cell Biol. 140, 617-626 (1998).
44. Louvard D. Apical membrane aminopeptidase appears at site of cell-cell contact in cultured kidney epithelial cells. Proc. Natl Acad. Sci. USA 77, 4132-4136 (1980).
45. Grindstaff, K. K. et al. Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 93, 731-740 (1998).
46. Benting, J. H., Rietveld, A. G. & Simons, K. N-Glycans mediate the apical sorting of a GPI-anchored, raft-associated protein in Madin-Darby canine kidney cells. J. Cell Biol. 146, 313-320 (1999).
47. Pang, S., Urquhart, P. & Hooper, N. M. N-Glycans, not the GPI anchor, mediate the apical targeting of a naturally glycosylated, GPI-anchored protein in polarised epithelial cells. J. Cell Sci. (in the press).
48. Yeaman, C. et al. The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells. J. Cell Biol. 139, 929-940 (1997).
49. Polishchuk, F. V., Di Pentima, A., Luini, A. & Polishchuk, R. S. Mechanism of constitutive export from the Golgi: bulk flow via the formation, protrusion, and en bloc cleavage of large trans-Golgi network tubular domains. Mol. Biol. Cell 14, 4470-4485 (2003).
50. Rodriguez-Boulan, E. et al. Methods to estimate the polarized distribution of surface antigens in cultured epithelial cells. Methods Cell Biol. 32, 37-56 (1989).