Molecular characterization of caveolin association with the Golgi complex: Identification of a cis-Golgi targeting domain in the caveolin molecule

Journal of Cell Biology

Volumn 145, Issue 7, 1999, Pages 1443-1459

  Luetterforst, Robert ^a   Stang, Espen ^a,c   Zorzi, Natasha ^a   Carozzi, Amanda ^a   Way, Michael ^b   Parton, Robert G ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Caveolae; Caveolin; Complex; Golgi; Palmitoylation; Targeting

Indexed keywords

AMINO ACID; CAVEOLIN; GREEN FLUORESCENT PROTEIN; MUTANT PROTEIN; PROTEIN ANTIBODY;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; FIBROBLAST; GOLGI COMPLEX; HAMSTER; IMMUNOFLUORESCENCE; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN TARGETING;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; CAVEOLIN 1; CAVEOLIN 3; CAVEOLINS; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; CONSERVED SEQUENCE; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; GOLGI APPARATUS; HUMANS; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MICROSCOPY, IMMUNOELECTRON; MOLECULAR SEQUENCE DATA; NOCODAZOLE; PALMITIC ACID; PROTEIN BINDING; PROTEIN SORTING SIGNALS; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; TRANSFECTION;

ANIMALIA; CRICETINAE;

EID: 0033612537     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.7.1443     Document Type: Article

References (80)

1. Anderson, R.G. 1998. The caveolae membrane system. Annu. Rev. Biochem. 67:199-225.
2. Anderson, R.G.W. 1993. Plasmalemmal caveolae and GPI-anchored proteins. Curr. Opin. Cell Biol. 5:647-652.
3. Anderson, H.A., Y. Chen, and L.C. Norkin. 1996. Bound simian virus 40 trans-locates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol. Biol. Cell. 7:1825-1834.
4. Bist, A., P.E. Fielding, and C.J. Fielding. 1997. Two sterol regulatory element-like sequences mediate up-regulation of caveolin gene transcription in response to low density lipoprotein free cholesterol. Proc. Natl. Acad. Sci. USA. 94:10693-10698.
5. Bordier, C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1604-1607.
6. Chapman, R.E., and S. Munro. 1994. Retrieval of trans Golgi network proteins from the cell surface requires endosomal acidification. EMBO (Eur. Mol. Biol. Organ.) J. 13:2305-2312.
7. Chavrier, P., R.G. Parton, H.P. Hauri, K. Simons, and M. Zerial. 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell. 62:317-329.
8. Conrad, P.A., E.J. Smart, Y.S. Ying, R.G. Anderson, and G.S. Bloom. 1995. Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J. Cell Biol. 131:1421-1433.
9. Dietzen, D.J., W.R. Hastings, and D.M. Lublin. 1995. Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae. J. Biol. Chem. 270:6838-6842.
10. 2-terminal region of the 65-kDa isoform of glutamic acid decarboxylase. J. Biol. Chem. 270:2241-2246.
11. Dupree, P., R.G. Parton, G. Raposo, T.V. Kurzchalia, and K. Simons. 1993. Caveolae and sorting in the trans-Golgi network of epithelial cells. EMBO (Eur. Mol. Biol. Organ.) J. 12:1597-1605.
12. Feron, O., J.B. Michel, K. Sase, and T. Michel. 1998. Dynamic regulation of endothelial nitric oxide synthase: complementary roles of dual acylation and caveolin interactions. Biochemistry. 37:193-200.
13. Fielding, P.E., and C.J. Fielding. 1995. Plasma membrane caveolae mediate the efflux of cellular free cholesterol. Biochemistry. 34:14288-14292.
14. Fielding, C.J., and P.E. Fielding. 1997. Intracellular cholesterol transport. J. Lipid Res. 38:1503-1521.
15. Fielding, C.J., A. Bist, and P.E. Fielding. 1997. Caveolin mRNA levels are up-regulated by free cholesterol and down-regulated by oxysterols in fibroblast monolayers. Proc. Natl. Acad. Sci. USA. 94:3753-3758.
16. Fra, A.M., M. Masserini, P. Palestini, S. Sonnino, and K. Simons. 1995a. A photo-reactive derivative of ganglioside GM1 specifically cross-links VIP21-caveolin on the cell surface. FEBS Lett. 375:11-14.
17. Fra, A.M., E. Williamson, K. Simons, and R.G. Parton. 1994. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269:30745-30748.
18. Fra, A.M., E. Williamson, K. Simons, and R.G. Parton. 1995b. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl. Acad. Sci. USA. 92:8655-8659.
19. Glenney, J.R. 1989. Tyrosine phosphorylation of a 22-kDa protein is correlated with phosphorylation by Rous sarcoma virus. J. Biol. Chem. 264:20163-20166.
20. Glenney, J.J., and D. Soppet. 1992. Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc. Natl. Acad. Sci. USA. 89:10517-10521.
21. Gorodinsky, A., and D. A. Harris. 1995. Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin. J. Cell Biol. 129:619-627.
22. Griffiths, G., M. Ericsson, J. Krijnse-Locker, T. Nilsson, B. Goud, H.D. Soling, B.L. Tang, S.H. Wong, and W. Hong. 1994. Localization of the Lys, Asp, Glu, Leu tetrapeptide receptor to the Golgi complex and the intermediate compartment in mammalian cells. J. Cell Biol. 127:1557-1574.
23. Gruenberg, J., G. Griffiths, and K.E. Howell. 1989. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle function in vitro. J. Cell Biol. 108:1301-1316.
24. Hailstones, D., L.S. Sleer, R.G. Parton, and K.K. Stanley. 1998. Regulation of caveolin and caveolae by cholesterol in MDCK cells. J. Lipid Res. 39:369-379.
25. Keller, P., and K. Simons. 1998. Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140:1357-1367.
26. Kobayashi, T., E. Stang, P. de Moerloose, R.G. Parton, and J. Gruenberg. 1998. A lipid antigen associated with the anti-phospholipid syndrome regulates endosome structure/function. Nature. 392:193-197.
27. Koleske, A.J., D. Baltimore, and M.P. Lisanti. 1995. Reduction of caveolin and caveolae in oncogenically transformed cells. Proc. Natl. Acad. Sci. USA. 92: 1381-1385.
28. Kreis, T. 1990. Role of microtubules in the organisation of the Golgi apparatus. Cell Motil. Cytoskel. 15:67-70.
29. 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.
30. Levine, T.P., and S. Munro. 1998. The pleckstrin homology domain of oxysterol-binding protein recognises a determinant specific to Golgi membranes. Curr. Biol. 8:729-739.
31. Li, S., T. Okamoto, M. Chun, M. Sargiacomo, J.E. Casanova, S.H. Hansen, I. Nishimoto, and M.P. Lisanti. 1995. Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J. Biol. Chem. 270:15693-15701.
32. Li, S., J. Couet, and M.P. Lisanti. 1996a. Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J. Biol. Chem. 271:29182-29190.
33. Li, S., R. Seitz, and M.P. Lisanti. 1996b. 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.
34. Liljestrom, P., and H. Garoff. 1991. A new generation of animal cell expression vectors based on the semliki forest virus replicon. Biotechnology. 9:1356-1361.
35. 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.
36. 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.
37. Lisanti, M.P., Z. Tang, P.E. Scherer, E. Kubler, A.J. Koleske, and M. Sargiacomo. 1995. Caveolae, transmembrane signaling and cellular transformation. Mol. Membr. Biol. 12:121-124.
38. Liu, J., T.E. Hughes, and W.C. Sessa. 1997. The first 35 amino acids and fatty acylation sites determine the molecular targeting of endothelial nitric oxide synthase into the Golgi region of cells: a green fluorescent protein study. J. Cell Biol. 137:1525-1535.
39. Mastick, C.C., M.J. Brady, and A.R. Saltiel. 1995. Insulin stimulates the tyrosine phosphorylation of caveolin. J. Cell Biol. 129:1523-1531.
40. Mastick, C.C., and A.R. Saltiel. 1997. Insulin-stimulated tyrosine phosphorylation of caveolin is specific for the differentiated adipocyte phenotype in 3T3-L1 cells. J. Biol. Chem. 272:20706-20714.
41. Michel, J.B., O. Feron, K. Sase, P. Prabhakar, and T. Michel. 1997. Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. J. Biol. Chem. 272:25907-25912.
42. Monier, S., D.J. Dietzen, W.R. Hastings, D.M. Lublin, and T.V. Kurzchalia. 1996. Oligomerization of V1P21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol. FEBS Lett. 388:143-149.
43. Monie'r, 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.
44. Montesano, R., J. Roth, A. Robert, and L. Orci. 1982. Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature. 296:651-653.
45. 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.
46. Okamoto, T., A. Schlegel, P.E. Scherer, and M.P. Lisanti. 1998. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J. Biol. Chem. 273:5419-5422.
47. Olkkonen, V.M., P. Liljestrom, H. Garoff, K. Simons, and C.G. Dotti. 1993. Expression of heterologous proteins in cultured rat hippocampal neurons using the Semliki Forest virus vector. J. Neurosci. Res. 35:445-451.
48. Palade, G.E. 1953. Fine structure of blood capillaries. J. Appl. Physics. 24:1424.
49. Parton, R.G. 1996. Caveolae and caveolins. Curr. Opin. Cell Biol. 8:542-548.
50. Parton, R.G., and K. Simons. 1995. Digging into caveolae. Science. 269:1398-1399.
51. Parton, R.G., and M.R. Lindsay. 1999. Exploitation of Major Histocompatibility class I molecules and caveolae by simian virus 40. Immunol. Rev. In press.
52. Parton, R.G., B. Joggerst, and K. Simons. 1994. Regulated internalization of caveolae. J. Cell Biol. 127:1199-1215.
53. Parton, R.G., M. Way, N. Zorzi, and E. Stang. 1997. Caveolin-3 associates with developing T-tubules during muscle differentiation. J. Cell Biol. 136:137-154.
54. Rabouille, C., N. Hui, F. Hunte, R. Kieckbusch, E.G. Berger, G. Warren, and T. Nilsson. 1995. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J. Cell Sci. 108:1617-1627.
55. Rizzuto, R., M. Brini, P. Pizzo, M. Murgia, and T. Pozzan. 1995. Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. Curr. Biol. 5:635-642.
56. Rojo, M., R. Pepperkok, G. Emery, R. Kellner, E. Stang, R.G. Parton, and J. Gruenberg. 1997. Involvement of the transmembrane protein p23 in biosynthetic protein transport. J. Cell Biol. 139:1119-1135
57. Rothberg, K., J.E. Heuser, W.C. Donzell, Y.-S. Ying, J.R. Glenney, and R.G.W. Anderson. 1992. Caveolin, a protein component of caveolae membrane coats. Cell. 68:673-682.
58. Roy, S., R. Luetterforst, A. Harding, A. Apolloni, M. Etheridge, E. Stang, B. Rolls, J.F. Hancock, and R.G. Parton. 1999. Dominant negative caveolin selectively inhibits H-ras function by disrupting cholesterol-rich domains. Nat. Cell Biol. 1:98-105.
59. Sargiacomo, M., P.E. Scherer, Z. Tang, E. Kubler, K.S. Song, M.C. Sanders, and M.P. Lisanti. 1995. Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc. Natl. Acad. Sci. USA. 92:9407-9411.
60. Scheiffele, P., P. Verkade, A.M. Fra, H. Virta, K. Simons, and E. Ikonen. 1998. Caveolin-1 and -2 in the cxocytic pathway of MDCK cells. J. Cell Biol. 140: 795-806.
61. Scherer, P.E., T. Okamoto, M. Chun, I. Nishimoto, H.F. Lodish, and M.P. Lisanti. 1996. Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Proc. Natl. Acad. Sci. USA. 93:131-135.
62. Schnitzer, J.E., P. Oh, E. Pinney, and J. Allard. 1994. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J. Cell Biol. 127: 1217-1232.
63. Sessa, W.C., G. Garcia-Cardena, J. Liu, A. Keh, J.S. Pollock, J. Bradley, S. Thiru, I.M. Braverman, and K.M. Desai. 1995. The Golgi association of endothelial nitric oxide synthase is necessary for the efficient synthesis of nitric oxide. J. Biol. Chem. 270:17641-17644.
64. Severs, N.J. 1988. Caveolae: static inpocketings of the plasma membrane, dynamic vesicles or plain artifact? J. Cell Sci. 90:341-348.
65. Simionescu, M., and N. Simionescu. 1991. Endothelial transport of macromolecules: transcytosis and endocytosis. Cell Biol. Rev. 25:1-80.
66. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
67. Smart, E.J., Y.S. Ying, P.A. Conrad, and R.G. Anderson. 1994. Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 127:1185-1197.
68. Smart, E.J., Y. Ying, W.C. Donzell, and R.G. Anderson. 1996. A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J. Biol. Chem. 271:29427-29435.
69. Solimena, M., R. Dirkx, Jr., M. Radzynski, O. Mundigl, and P. De Camilli. 1994. A signal located within amino acids 1-27 of GAD65 is required for its targeting to the Golgi complex region. J. Cell Biol. 126:331-341.
70. Song, S.K., S. Li, T. Okamoto, L.A. Quilliam, M. Sargiacomo, and M.P. Lisanti. 1996. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J. Biol. Chem. 271:9690-9697.
71. Song, K.S., Z. Tang, S. Li, and M.P. Lisanti. 1997. Mutational analysis of the properties of caveolin-1. A novel role for the C-terminal domain in mediating homo-typic caveolin-caveolin interactions. J. Biol. Chem. 272:4398-4403.
72. Stang, E., J. Kartenbeck, and R.G. Parton. 1997. Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol. Biol. Cell. 8:47-57.
73. Tang, Z., P.E. Scherer, T. Okamoto, K. Song, C. Chu, D.S. Kohtz, I. Nishimoto, H.F. Lodish, and M.P. Lisanti. 1996. Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. J. Biol. Chem. 271:2255-2261.
74. Tang, Z., T. Okamoto, P. Boontrakulpoontawee, T. Katada, A.J. Otsuka, and M.P. Lisanti. 1997. Identification, sequence, and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegans. Implications for the molecular evolution of mammalian caveolin genes. J. Biol. Chem. 272:2437-2445.
75. Tran, D., J.-L. Carpentier, F. Sawano, P. Gorden, and L. Orci. 1987. Ligands internalized through coated or non-coated invaginations follow a common intracellular pathway. Proc. Natl. Acad. Sci. USA. 84:7957-7961.
76. Uittenbogaard, A., Y. Ying, and E.J. Smart. 1998. Characterization of a cytosolic heat-shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking. J. Biol. Chem. 273:6525-6532.
77. Ullrich, O., S. Reinsch, S. Urbé, M. Zerial, and R.G. Parton. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. 135:913-924.
78. Venema, V.J., H. Ju, R. Zou, and R.C. Venema. 1997. Interaction of neuronal nitric-oxide synthase with caveolin-3 in skeletal muscle. Identification of a novel caveolin scaffolding/inhibitory domain. J. Biol. Chem. 272:28187-28190.
79. Way, M., and R.G. Parton. 1995. M-caveolin, a muscle-specific caveolin-related protein. FEBS Lett. 376:108-112.
80. Yamada, E. 1955. The fine structure of the gall bladder epithelium of the mouse. J. Biophys. Biochem. Cytol. 1:445-458.