Caveolin-1 is not essential for biosynthetic apical membrane transport

Molecular and Cellular Biology

Volumn 25, Issue 22, 2005, Pages 10087-10096

  Manninen, Aki ^a   Verkade, Paul ^a   Le Lay, Soazig ^a   Torkko, Juha ^a   Kasper, Michael ^c   Füllekrug, Joachim ^b   Simons, Kai ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; GLYCOSYLPHOSPHATIDYLINOSITOL; INFLUENZA VIRUS HEMAGGLUTININ;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CELL MEMBRANE TRANSPORT; COMPLEX FORMATION; DOG; EPITHELIUM CELL; FIBROBLAST; GOLGI COMPLEX; KIDNEY CELL; LIPID COMPOSITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN TARGETING; RNA INTERFERENCE; SYNTHESIS;

ADENOVIRIDAE; ANIMALS; BIOLOGICAL TRANSPORT; BIOTIN; BIOTINYLATION; CAVEOLIN 1; CAVEOLIN 2; CELL LINE; CELL MEMBRANE; CHOLESTEROL; DOGS; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROBLASTS; GLYCOSYLPHOSPHATIDYLINOSITOLS; GOLGI APPARATUS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNOHISTOCHEMISTRY; KINETICS; MEMBRANE MICRODOMAINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; RETROVIRIDAE; RNA INTERFERENCE; TEMPERATURE; TIME FACTORS; TRANSGENES;

ANIMALIA; CANIS FAMILIARIS; INFLUENZA VIRUS;

EID: 27644505702     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.22.10087-10096.2005     Document Type: Article

References (65)

1. Alfieri, J. A., A. D. Martin, J. Takeda, G. Kondoh, D. G. Myles, and P. Primakoff. 2003. Infertility in female mice with an oocyte-specific knockout of GPI-anchored proteins. S. Cell Sci. 116:2149-2155.
2. Balcarova-Stander, J., S. E. Pfeiffer, S. D. Fuller, and K. Simons. 1984. Development of cell surface polarity in the epithelial Madin-Darby canine kidney (MDCK) cell line. EMBO J. 3:2687-2694.
3. 2+ influx channels by regulating plasma membrane localization of TRPC1. J. Biol. Chem. 278:27208-27215.
4. Brown, D. A., B. Crise, and J. K. Rose. 1989. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science 245:1499-1501.
5. Cheong, K. H., D. Zacchetti, E. E. Schneeberger, and K. Simons. 1999. VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells. Proc. Natl. Acad. Sci. USA 96:6241-6248.
6. Cohen, A. W., R. Hnasko, W. Schubert, and M. P. Lisanti. 2004. Role of caveolae and caveolins in health and disease. Physiol. Rev. 84:1341-1379.
7. Delacour, D., V. Gouyer, J. P. Zanetta, H. Drobecq, E. Leteurtre, G. Grard, O. Moreau-Hannedouche, E. Maes, A. Pons, S. Andre, A. Le Bivic, H. J. Gabius, A. Manninen, K. Simons, and G. Huet. 2005. Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J. Cell Biol. 169:491-501.
8. de Marco, M. C., F. Martin-Belmonte, L. Kremer, J. P. Albar, I. Correas, J. P. Vaerman, M. Marazuela, J. A. Byrne, and M. A. Alonso. 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.
9. Diep, D. B., K. L. Nelson, S. M. Raja, E. N. Pleshak, and J. T. Buckley. 1998. Glycosylphosphatidylinositol anchors of membrane glycoproteins are binding determinants for the channel-forming toxin aerolysin. J. Biol. Chem. 273:2355-2360.
10. Drab, M., P. Verkade, M. Elger, M. Kasper, M. Lohn, B. Lauterbach, J. Menne, C. Lindschau, F. Mende, F. C. Luft, A. Schedl, H. Haller, and T. V. Kurzchalia. 2001. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293:2449-2452.
11. Etienne-Manneville, S., and A. Hall. 2003. Cell polarity: Par6, aPKC and cytoskeletal crosstalk. Curr. Opin. Cell Biol. 15:67-72.
12. Fiedler, K., F. Lafont, R. G. Parton, and K. Simons. 1995. Annexin XIIIb: a novel epithelial specific annexin is implicated in vesicular traffic to the apical plasma membrane. J. Cell Biol. 128:1043-1053.
13. Fielding, C. J., and P. E. Fielding. 2000. Cholesterol and caveolae: structural and functional relationships. Biochim. Biophys. Acta 1529:210-222.
14. Fivaz, M., F. Vilbois, S. Thurnheer, C. Pasquali, L. Abrami, P. E. Bickel, R. G. Parton, and F. G. Van Der Goot. 2002. Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J. 21:3989-4000.
15. Fra, A. M., E. Williamson, K. Simons, and R. G. Parton. 1995. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl. Acad. Sci. USA 92:8655-8659.
16. Fujimoto, T., H. Kogo, K. Ishiguro, K. Tauchi, and R. Nomura. 2001. Caveolin-2 is targeted to lipid droplets, a new "membrane domain" in the cell. J. Cell Biol. 152:1079-1085.
17. Fujimoto, T., H. Kogo, R. Nomura, and T. Une. 2000. Isoforms of caveolin-1 and caveolar structure. J. Cell Sci. 113:3509-3517.
18. Fullekrug, J., P. Scheiffele, and K. Simons. 1999. VIP36 localisation to the early secretory pathway. J. Cell Sci. 112:2813-2821.
19. Fullekrug, J., and K. Simons. 2004. Lipid rafts and apical membrane traffic. Ann. N. Y. Acad. Sci. 1014:164-169.
20. Gilbert, T., A. Le Bivic, A. Quaroni, and E. Rodriguez-Boulan. 1991. Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells. J. Cell Biol. 113:275-288.
21. Gumbiner, B., and K. Simons. 1986. A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of a uvomorulin-like polypeptide. J. Cell Biol. 102:457-468.
22. Hara-Kuge, S., A. Seko, O. Shimada, H. Tosaka-Shimada, and K. Yamashita. 2004. The binding of VIP36 and alpha-amylase in the secretory vesicles via high-mannose type glycans. Glycobiology 14:739-744.
23. Kawagoe, K., D. Kitamura, M. Okabe, I. Taniuchi, M. Ikawa, T. Watanabe, T. Kinoshita, and J. Takeda. 1996. Olycosylphosphatidylinositol-anchor-deficient mice: implications for clonal dominance of mutant cells in paroxysmal nocturnal hemoglobinuria. Blood 87:3600-3606.
24. Keller, P., D. Toomre, E. Diaz, J. White, and K. Simons. 2001. Multicolour imaging of post-Golgi sorting and trafficking in live cells. Nat. Cell Biol. 3:140-149.
25. Kurzchalia, T. V., P. Dupree, R. G. Parton, R. Kellner, H. Virta, M. Lehnert, and K. Simons. 1992. VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J. Cell Biol. 118:1003-1014.
26. Lafont, F., J. K. Burkhardt, and K. Simons. 1994. Involvement of microtubule motors in basolateral and apical transport in kidney cells. Nature 372:801-803.
27. Lafont, F., S. Lecat, P. Verkade, and K. Simons. 1998. Annexin XIIIb associates with lipid microdomains to function in apical delivery. J. Cell Biol. 142:1413-1427.
28. Lahtinen, U., M. Honsho, R. G. Parton, K. Simons, and P. Verkade. 2003. Involvement of caveolin-2 in caveolar biogenesis in MDCK cells. FEBS Lett. 538:85-88.
29. Linstedt, A. D., and H. P. Hauri. 1993. Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol. Biol. Cell 4:679-693.
30. Lipardi, C., R. Mora, V. Colomer, S. Paladino, L. Nitsch, E. Rodriguez-Boulan, and C. Zurzolo. 1998. Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI)-anchored proteins in epithelial cells. J. Cell Biol. 140:617-626.
31. Liu, P., M. Rudick, and R. G. Anderson. 2002. Multiple functions of caveolin-1. J. Biol. Chem. 277:41295-41298.
32. Matlin, K. S., and K. Simons. 1983. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell 34:233-243.
33. Meder, D., A. Shevchenko, K. Simons, and J. Fullekrug. 2005. Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells. J. Cell Biol. 168:303-313.
34. Monier, S., R. G. Parton, F. Vogel, J. Behlke, A. Henske, and T. V. Kurzchalia. 1995. VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol. Biol. Cell. 6:911-927.
35. Mora, R., V. L. Bonilha, A. Marmorstein, P. E. Scherer, D. Brown, M. P. Lisanti, and E. Rodriguez-Boulan. 1999. Caveolin-2 localizes to the golgi complex but redistributes to plasma membrane, caveolae, and rafts when co-expressed with caveolin-1. J. Biol. Chem. 274:25708-25717.
36. Mostov, K., T. Su, and M. ter Beest. 2003. Polarized epithelial membrane traffic: conservation and plasticity. Nat. Cell Biol. 5:287-293.
37. Murata, M., J. Peranen, R. Schreiner, F. Wieland, T. V. Kurzchalia, and K. Simons. 1995. VIP21/caveolin is a cholesterol-binding protein. Proc. Natl. Acad. Sci. USA 92:10339-10343.
38. Nakatsu, F., and H. Ohno. 2003. Adaptor protein complexes as the key regulators of protein sorting in the post-Golgi network. Cell Struct. Funct. 28:419-429.
39. Nelson, W. J. 2003. Adaptation of core mechanisms to generate cell polarity. Nature 422:766-774.
40. Nozaki, M., K. Ohishi, N. Yamada, T. Kinoshita, A. Nagy, and J. Takeda. 1999. Developmental abnormalities of glycosylphosphatidylinositol-anchor- deficient embryos revealed by Cre/loxP system. Lab. Investig. 79:293-299.
41. Ojakian, G. K., and R. Schwimmer. 1988. The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells. J. Cell Biol. 107:2377-2387.
42. Ostermeyer, A. G., J. M. Paci, Y. Zeng, D. M. Lublin, S. Munro, and D. A. Brown. 2001. Accumulation of caveolin in the endoplasmic reticulum redirects the protein to lipid storage droplets. J. Cell Biol. 152:1071-1078.
43. Parolini, I., M. Sargiacomo, F. Galbiati, G. Rizzo, F. Grignani, J. A. Engelman, T. Okamoto, T. Ikezu, P. E. Scherer, R. Mora, E. Rodriguez-Boulan, C. Peschle, and M. P. Lisanti. 1999. Expression of caveolin-1 is required for the transport of caveolin-2 to the plasma membrane. Retention of caveolin-2 at the level of the golgi complex. J. Biol. Chem. 274:25718-25725.
44. Pelkmans, L., T. Burli, M. Zerial, and A. Helenius. 2004. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118:767-780.
45. Pelkmans, L., and A. Helenius. 2002. Endocytosis via caveolae. Traffic 3:311-320.
46. Pelkmans, L., D. Puntener, and A. Helenius. 2002. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296:535-539.
47. Pol, A., R. Luetterforst, M. Lindsay, S. Heino, E. Ikonen, and R. G. Parton. 2001. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J. Cell Biol. 152:1057-1070.
48. Pol, A., S. Martin, M. A. Fernandez, C. Ferguson, A. Carozzi, R. Luetterforst, C. Enrich, and R. G. Parton. 2004. Dynamic and regulated association of caveolin with lipid bodies: modulation of lipid body motility and function by a dominant negative mutant. Mol. Biol. Cell. 15:99-110.
49. Pol, A., S. Martin, M. A. Fernandez, M. Ingelmo-Torres, C. Ferguson, C. Enrich, and R. G. Parton. 2005. Cholesterol and fatty acids regulate dynamic caveolin trafficking through the golgi complex and between the cell surface and lipid bodies. Mol. Biol. Cell 16:2091-2105.
50. Puertollano, R., F. Martin-Belmonte, J. Millan, M. C. de Marco, J. P. Albar, L. Kremer, and M. A. Alonso. 1999. The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. J. Cell Biol. 145:141-151.
51. Razani, B., T. P. Combs, X. B. Wang, P. G. Frank, D. S. Park, R. G. Russell, M. Li, B. Tang, L. A. Jelicks, P. E. Scherer, and M. P. Lisanti. 2002. Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J. Biol. Chem. 277:8635-8647.
52. Razani, B., J. A. Engelman, X. B. Wang, W. Schubert, X. L. Zhang, C. B. Marks, F. Macaluso, R. G. Russell, M. Li, R. G. Pestell, D. Di Vizio, H. Hou, Jr., B. Kneitz, G. Lagaud, G. J. Christ, W. Edelmann, and M. P. Lisanti. 2001. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J. Biol. Chem. 276:38121-38138.
53. Rodriguez-Boulan, E., G. Kreitzer, and A. Musch. 2005. Organization of vesicular trafficking in epithelia. Nat. Rev. Mol. Cell. Biol. 6:233-247.
54. Rothberg, K. G., J. E. Heuser, W. C. Donzell, Y. S. Ying, J. R. Glenney, and R. G. Anderson. 1992. Caveolin, a protein component of caveolae membrane coats. Cell 68:673-682.
55. Saemann, M. D., T. Weichhart, W. H. Horl, and G. J. Zlabinger. 2005. Tamm-Horsfall protein: a multilayered defence molecule against urinary tract infection. Eur. J. Clin. Investig. 35:227-235.
56. Scheiffele, P., P. Verkade, A. M. Fra, H. Virta, K. Simons, and E. Ikonen. 1998. Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J. Cell Biol. 140:795-806.
57. Schuck, S., A. Manninen, M. Honsho, J. Fullekrug, and K. Simons. 2004. Generation of single and double knockdowns in polarized epithelial cells by retrovirus-mediated RNA interference. Proc. Natl. Acad. Sci. USA 101:4912-4917.
58. Schuck, S., and K. Simons. 2004. Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane. J. Cell Sci. 117:5955-5964.
59. Simons, K., and W. L. Vaz. 2004. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33:269-295.
60. Sotgia, F., B. Razani, G. Bonuccelli, W. Schubert, M. Battista, H. Lee, F. Capozza, A. L. Schubert, C. Minetti, J. T. Buckley, and M. P. Lisanti. 2002. Intracellular retention of glycosylphosphatidyl inositol-linked proteins in caveolin-deficient cells. Mol. Cell. Biol. 22:3905-3926.
61. Tarutani, M., S. Itami, M. Okabe, M. Ikawa, T. Tezuka, K. Yoshikawa, T. Kinoshita, and J. Takeda. 1997. Tissue-specific knockout of the mouse Pig-a gene reveals important roles for GPI-anchored proteins in skin development. Proc. Natl. Acad. Sci. USA 94:7400-7405.
62. Verkade, P., T. Harder, F. Lafont, and K. Simons. 2000. Induction of caveolae in the apical plasma membrane of Madin-Darby canine kidney cells. J. Cell Biol. 148:727-739.
63. Wyse, B. D., I. A. Prior, H. Qian, I. C. Morrow, S. Nixon, C. Muncke, T. V. Kurzchalia, W. G. Thomas, R. G. Parton, and J. F. Hancock. 2003. Caveolin interacts with the angiotensin I1 type 1 receptor during exocytic transport but not at the plasma membrane. J. Biol. Chem. 278:23738-23746.
64. Yoshimori, T., P. Keller, M. G. Roth, and K. Simons. 1996. Different biosynthetic transport routes to the plasma membrane in BHK and CHO cells. J. Cell Biol. 133:247-256.
65. Zhao, Y. Y., Y. Liu, R. V. Stan, L. Fan, Y. Gu, N. Dalton, P. H. Chu, K. Peterson, J. Ross, Jr., and K. R. Chien. 2002. Defects in caveolin-1 cause dilated cardiomyopathy and pulmonary hypertension in knockout mice. Proc. Natl. Acad. Sci. USA 99:11375-11380.