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PMID: 9472032 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Caveolin-1 and -2 in the exocytic pathway of MDCK cells.

The Journal of cell biology ·Vol. 140 ·No. 4 ·1998-02-23 ·Pages 795-806

Scheiffele P, Verkade P, Fra AM, Virta H, Simons K, Ikonen E

Abstract

We have studied the biosynthesis and transport of the endogenous caveolins in MDCK cells. We show that in addition to homooligomers of caveolin-1, heterooligomeric complexes of caveolin-1 and -2 are formed in the ER. The oligomers become larger, increasingly detergent insoluble, and phosphorylated on caveolin-2 during transport to the cell surface. In the TGN caveolin-1/-2 heterooligomers are sorted into basolateral vesicles, whereas larger caveolin-1 homooligomers are targeted to the apical side. Caveolin-1 is present on both the apical and basolateral plasma membrane, whereas caveolin-2 is enriched on the basolateral surface where caveolae are present. This suggests that caveolin-1 and -2 heterooligomers are involved in caveolar biogenesis in the basolateral plasma membrane. Anti-caveolin-1 antibodies inhibit the apical delivery of influenza virus hemagglutinin without affecting basolateral transport of vesicular stomatitis virus G protein. Thus, we suggest that caveolin-1 homooligomers play a role in apical transport.

MeSH Terms
Amino Acid Sequence Animals Antibodies/analysis,pharmacology Base Sequence Biological Transport Caveolin 1 Caveolins Cell Line/chemistry Cell Membrane/chemistry,ultrastructure Cloning, Molecular Cytosol/chemistry,ultrastructure DNA, Complementary/genetics Exocytosis/genetics,physiology Hemagglutinin Glycoproteins, Influenza Virus/drug effects,metabolism Membrane Proteins/chemistry,genetics,physiology Molecular Sequence Data Polymers Precipitin Tests Proteins/chemistry Sheep Solubility
Chemicals
Antibodies Caveolin 1 Caveolins DNA, Complementary Hemagglutinin Glycoproteins, Influenza Virus Membrane Proteins Polymers Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Scheiffele P
Cell Biology Programme, European Molecular Biology Laboratory, D-69012 Heidelberg, Germany.
Verkade P
Fra A M
Virta H
Simons K
Ikonen E
References (39)
39 references, click to expand
  1. Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein block its transport to the cell surface.
    EMBO J. 1986 May;5(5):931-41 PMID: 3013626
  2. Caveolin isoforms differ in their N-terminal protein sequence and subcellular distribution. Identification and epitope mapping of an isoform-specific monoclonal antibody probe.
    J Biol Chem. 1995 Jul 7;270(27):16395-401 PMID: 7608210
  3. Semi-intact cells permeable to macromolecules: use in reconstitution of protein transport from the endoplasmic reticulum to the Golgi complex.
    Cell. 1987 Aug 14;50(4):523-34 PMID: 3038335
  4. Distinct transport vesicles mediate the delivery of plasma membrane proteins to the apical and basolateral domains of MDCK cells.
    J Cell Biol. 1990 Sep;111(3):987-1000 PMID: 2202740
  5. Caveolin, a protein component of caveolae membrane coats.
    Cell. 1992 Feb 21;68(4):673-82 PMID: 1739974
  6. VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles.
    J Cell Biol. 1992 Sep;118(5):1003-14 PMID: 1512286
  7. 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 U S A. 1992 Nov 1;89(21):10517-21 PMID: 1279683
  8. Rapid affinity-purification and biotinylation of antibodies.
    Biotechniques. 1992 Oct;13(4):546-9 PMID: 1335734
  9. Regulation of apical transport in epithelial cells by a Gs class of heterotrimeric G protein.
    Nature. 1993 Apr 1;362(6419):456-8 PMID: 8385268
  10. Caveolae and sorting in the trans-Golgi network of epithelial cells.
    EMBO J. 1993 Apr;12(4):1597-605 PMID: 8385608
  11. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells.
    J Cell Biol. 1993 Aug;122(4):789-807 PMID: 8349730
  12. Prohormone processing in the trans-Golgi network: endoproteolytic cleavage of prosomatostatin and formation of nascent secretory vesicles in permeabilized cells.
    J Cell Biol. 1993 Sep;122(6):1169-84 PMID: 8104189
  13. VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells.
    EMBO J. 1994 Jan 1;13(1):42-53 PMID: 8306971
  14. Basolateral protein transport in streptolysin O-permeabilized MDCK cells.
    J Cell Biol. 1994 Jun;125(5):1025-35 PMID: 8195286
  15. Regulated internalization of caveolae.
    J Cell Biol. 1994 Dec;127(5):1199-215 PMID: 7962085
  16. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules.
    J Cell Biol. 1994 Dec;127(5):1217-32 PMID: 7525606
  17. Digging into caveolae.
    Science. 1995 Sep 8;269(5229):1398-9 PMID: 7660120
  18. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8655-9 PMID: 7567992
  19. Oligomeric structure of caveolin: implications for caveolae membrane organization.
    Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9407-11 PMID: 7568142
  20. VIP21/caveolin is a cholesterol-binding protein.
    Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10339-43 PMID: 7479780
  21. VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro.
    Mol Biol Cell. 1995 Jul;6(7):911-27 PMID: 7579702
  22. Characterization of proteins in detergent-resistant membrane complexes from Madin-Darby canine kidney epithelial cells.
    Biochemistry. 1995 Dec 12;34(49):16161-70 PMID: 8519773
  23. Expression and characterization of recombinant caveolin. Purification by polyhistidine tagging and cholesterol-dependent incorporation into defined lipid membranes.
    J Biol Chem. 1996 Jan 5;271(1):568-73 PMID: 8550621
  24. Identification, sequence, and expression of caveolin-2 defines a caveolin gene family.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):131-5 PMID: 8552590
  25. Phosphorylation of caveolin by src tyrosine kinases. The alpha-isoform of caveolin is selectively phosphorylated by v-Src in vivo.
    J Biol Chem. 1996 Feb 16;271(7):3863-8 PMID: 8632005
  26. Transport of vesicular stomatitis virus G protein to the cell surface is signal mediated in polarized and nonpolarized cells.
    J Cell Biol. 1996 May;133(3):543-58 PMID: 8636230
  27. Oligomerization of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol.
    FEBS Lett. 1996 Jun 17;388(2-3):143-9 PMID: 8690074
  28. Dissecting the molecular mechanisms of polarized membrane traffic: reconstitution of three transport steps in epithelial cells using streptolysin-O permeabilization.
    Cold Spring Harb Symp Quant Biol. 1995;60:753-62 PMID: 8824450
  29. Detergent-resistant membrane microdomains from Caco-2 cells do not contain caveolin.
    Am J Physiol. 1996 Sep;271(3 Pt 1):C887-94 PMID: 8843719
  30. Baculovirus-based expression of mammalian caveolin in Sf21 insect cells. A model system for the biochemical and morphological study of caveolae biogenesis.
    J Biol Chem. 1996 Nov 8;271(45):28647-54 PMID: 8910498
  31. 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. 1997 Feb 14;272(7):4398-403 PMID: 9020162
  32. Functional rafts in cell membranes.
    Nature. 1997 Jun 5;387(6633):569-72 PMID: 9177342
  33. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain.
    EMBO J. 1997 Sep 15;16(18):5501-8 PMID: 9312009
  34. Identification of components of trans-Golgi network-derived transport vesicles and detergent-insoluble complexes by nanoelectrospray tandem mass spectrometry.
    Electrophoresis. 1997 Dec;18(14):2591-600 PMID: 9527489
  35. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae.
    J Biol Chem. 1994 Dec 9;269(49):30745-8 PMID: 7982998
  36. Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae.
    J Biol Chem. 1995 Mar 24;270(12):6838-42 PMID: 7896831
  37. Different requirements for NSF, SNAP, and Rab proteins in apical and basolateral transport in MDCK cells.
    Cell. 1995 May 19;81(4):571-80 PMID: 7758111
  38. Insulin stimulates the tyrosine phosphorylation of caveolin.
    J Cell Biol. 1995 Jun;129(6):1523-31 PMID: 7540611
  39. The trans Golgi network: sorting at the exit site of the Golgi complex.
    Science. 1986 Oct 24;234(4775):438-43 PMID: 2945253
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.140.4.795
Published
1998-02-23
Pages
795-806
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2141752
Subset
IM
Grants
Telethon · E.0490 · Italy
Databases
GENBANK
AF039223
External Links
PubMed source DOI: 10.1083/jcb.140.4.795 PMC Full Text View journal details
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