Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1994 Jul 1;126(1):111–126. doi: 10.1083/jcb.126.1.111

Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease

PMCID: PMC2120102  PMID: 7517942

Abstract

Caveolae are 50-100-nm membrane microdomains that represent a subcompartment of the plasma membrane. Previous morphological studies have implicated caveolae in (a) the transcytosis of macromolecules (including LDL and modified LDLs) across capillary endothelial cells, (b) the uptake of small molecules via a process termed potocytosis involving GPI-linked receptor molecules and an unknown anion transport protein, (c) interactions with the actin-based cytoskeleton, and (d) the compartmentalization of certain signaling molecules, including G- protein coupled receptors. Caveolin, a 22-kD integral membrane protein, is an important structural component of caveolae that was first identified as a major v-Src substrate in Rous sarcoma virus transformed cells. This finding initially suggested a relationship between caveolin, transmembrane signaling, and cellular transformation. We have recently developed a procedure for isolating caveolin-rich membrane domains from cultured cells. To facilitate biochemical manipulations, we have applied this procedure to lung tissue--an endothelial and caveolin-rich source-allowing large scale preparation of these complexes. These membrane domains retain approximately 85% of caveolin and approximately 55% of a GPI-linked marker protein, while they exclude > or = 98% of integral plasma membrane protein markers and > or = 99.6% of other organelle-specific membrane markers tested. Characterization of these complexes by micro-sequencing and immuno- blotting reveals known receptors for modified forms of LDL (scavenger receptors: CD 36 and RAGE), multiple GPI-linked proteins, an anion transporter (plasma membrane porin), cytoskeletal elements, and cytoplasmic signaling molecules--including Src-like kinases, hetero- trimeric G-proteins, and three members of the Rap family of small GTPases (Rap 1--the Ras tumor suppressor protein, Rap 2, and TC21). At least a fraction of the actin in these complexes appeared monomeric (G- actin), suggesting that these domains could represent membrane bound sites for microfilament nucleation/assembly during signaling. Given that the majority of these proteins are known molecules, our current studies provide a systematic basis for evaluating these interactions in vivo.

Full Text

The Full Text of this article is available as a PDF (2.9 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abumrad N. A., el-Maghrabi M. R., Amri E. Z., Lopez E., Grimaldi P. A. Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J Biol Chem. 1993 Aug 25;268(24):17665–17668. [PubMed] [Google Scholar]
  2. Akiho H., Tokumitsu Y., Noda M., Nomura Y. Decrease in coupling of Gs in v-src-transformed NIH-3T3 fibroblasts: possible involvement of tyrosine phosphorylation of Gs by pp60v-src. Arch Biochem Biophys. 1993 Jul;304(1):235–241. doi: 10.1006/abbi.1993.1344. [DOI] [PubMed] [Google Scholar]
  3. Akino T. [Biochemical and clinical aspects of pulmonary surfactant proteins]. Nihon Kyobu Shikkan Gakkai Zasshi. 1992 Dec;30 (Suppl):5–14. [PubMed] [Google Scholar]
  4. Anderson R. G. Caveolae: where incoming and outgoing messengers meet. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):10909–10913. doi: 10.1073/pnas.90.23.10909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Anderson R. G., Kamen B. A., Rothberg K. G., Lacey S. W. Potocytosis: sequestration and transport of small molecules by caveolae. Science. 1992 Jan 24;255(5043):410–411. doi: 10.1126/science.1310359. [DOI] [PubMed] [Google Scholar]
  6. Anderson R. G. Plasmalemmal caveolae and GPI-anchored membrane proteins. Curr Opin Cell Biol. 1993 Aug;5(4):647–652. doi: 10.1016/0955-0674(93)90135-d. [DOI] [PubMed] [Google Scholar]
  7. Baldini G., Hohl T., Lin H. Y., Lodish H. F. Cloning of a Rab3 isotype predominantly expressed in adipocytes. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):5049–5052. doi: 10.1073/pnas.89.11.5049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bamezai A., Rock K. L. Effect of ras-activation on the expression of glycosyl-phosphatidylinositol-anchored proteins on the plasma membrane. Oncogene. 1991 Aug;6(8):1445–1451. [PubMed] [Google Scholar]
  9. Blachly-Dyson E., Zambronicz E. B., Yu W. H., Adams V., McCabe E. R., Adelman J., Colombini M., Forte M. Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependent anion channel. J Biol Chem. 1993 Jan 25;268(3):1835–1841. [PubMed] [Google Scholar]
  10. Bomsel M., Mostov K. Role of heterotrimeric G proteins in membrane traffic. Mol Biol Cell. 1992 Dec;3(12):1317–1328. doi: 10.1091/mbc.3.12.1317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bonilla E., Fischbeck K., Schotland D. L. Freeze-fracture studies of muscle caveolae in human muscular dystrophy. Am J Pathol. 1981 Aug;104(2):167–173. [PMC free article] [PubMed] [Google Scholar]
  12. Bourguignon L. Y., Jin H., Iida N., Brandt N. R., Zhang S. H. The involvement of ankyrin in the regulation of inositol 1,4,5-trisphosphate receptor-mediated internal Ca2+ release from Ca2+ storage vesicles in mouse T-lymphoma cells. J Biol Chem. 1993 Apr 5;268(10):7290–7297. [PubMed] [Google Scholar]
  13. Brada D., Dubach U. C. Isolation of a homogeneous glucosidase II from pig kidney microsomes. Eur J Biochem. 1984 May 15;141(1):149–156. doi: 10.1111/j.1432-1033.1984.tb08169.x. [DOI] [PubMed] [Google Scholar]
  14. Bretscher M. S., Whytock S. Membrane-associated vesicules in fibroblasts. J Ultrastruct Res. 1977 Nov;61(2):215–217. doi: 10.1016/s0022-5320(77)80088-9. [DOI] [PubMed] [Google Scholar]
  15. Brett J., Schmidt A. M., Yan S. D., Zou Y. S., Weidman E., Pinsky D., Nowygrod R., Neeper M., Przysiecki C., Shaw A. Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am J Pathol. 1993 Dec;143(6):1699–1712. [PMC free article] [PubMed] [Google Scholar]
  16. Brown D. A., Rose J. K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 1992 Feb 7;68(3):533–544. doi: 10.1016/0092-8674(92)90189-j. [DOI] [PubMed] [Google Scholar]
  17. Brown L. F., Berse B., Van de Water L., Papadopoulos-Sergiou A., Perruzzi C. A., Manseau E. J., Dvorak H. F., Senger D. R. Expression and distribution of osteopontin in human tissues: widespread association with luminal epithelial surfaces. Mol Biol Cell. 1992 Oct;3(10):1169–1180. doi: 10.1091/mbc.3.10.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Bucci C., Parton R. G., Mather I. H., Stunnenberg H., Simons K., Hoflack B., Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell. 1992 Sep 4;70(5):715–728. doi: 10.1016/0092-8674(92)90306-w. [DOI] [PubMed] [Google Scholar]
  19. Béranger F., Goud B., Tavitian A., de Gunzburg J. Association of the Ras-antagonistic Rap1/Krev-1 proteins with the Golgi complex. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1606–1610. doi: 10.1073/pnas.88.5.1606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Caldwell R. B., Slapnick S. M. Freeze-fracture and lanthanum studies of the retinal microvasculature in diabetic rats. Invest Ophthalmol Vis Sci. 1992 Apr;33(5):1610–1619. [PubMed] [Google Scholar]
  21. Cao L. G., Fishkind D. J., Wang Y. L. Localization and dynamics of nonfilamentous actin in cultured cells. J Cell Biol. 1993 Oct;123(1):173–181. doi: 10.1083/jcb.123.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Coulter S., Rodbell M. Heterotrimeric G proteins in synaptoneurosome membranes are crosslinked by p-phenylenedimaleimide, yielding structures comparable in size to crosslinked tubulin and F-actin. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5842–5846. doi: 10.1073/pnas.89.13.5842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Creutz C. E. The annexins and exocytosis. Science. 1992 Nov 6;258(5084):924–931. doi: 10.1126/science.1439804. [DOI] [PubMed] [Google Scholar]
  24. Drivas G. T., Shih A., Coutavas E., Rush M. G., D'Eustachio P. Characterization of four novel ras-like genes expressed in a human teratocarcinoma cell line. Mol Cell Biol. 1990 Apr;10(4):1793–1798. doi: 10.1128/mcb.10.4.1793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Dráberová L., Dráber P. Thy-1 glycoprotein and src-like protein-tyrosine kinase p53/p56lyn are associated in large detergent-resistant complexes in rat basophilic leukemia cells. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3611–3615. doi: 10.1073/pnas.90.8.3611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Dupree P., Parton R. G., Raposo G., Kurzchalia T. V., Simons K. Caveolae and sorting in the trans-Golgi network of epithelial cells. EMBO J. 1993 Apr;12(4):1597–1605. doi: 10.1002/j.1460-2075.1993.tb05804.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Esposito C., Gerlach H., Brett J., Stern D., Vlassara H. Endothelial receptor-mediated binding of glucose-modified albumin is associated with increased monolayer permeability and modulation of cell surface coagulant properties. J Exp Med. 1989 Oct 1;170(4):1387–1407. doi: 10.1084/jem.170.4.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Fan J. Y., Carpentier J. L., van Obberghen E., Grunfeld C., Gorden P., Orci L. Morphological changes of the 3T3-L1 fibroblast plasma membrane upon differentiation to the adipocyte form. J Cell Sci. 1983 May;61:219–230. doi: 10.1242/jcs.61.1.219. [DOI] [PubMed] [Google Scholar]
  29. Fernandez J., DeMott M., Atherton D., Mische S. M. Internal protein sequence analysis: enzymatic digestion for less than 10 micrograms of protein bound to polyvinylidene difluoride or nitrocellulose membranes. Anal Biochem. 1992 Mar;201(2):255–264. doi: 10.1016/0003-2697(92)90336-6. [DOI] [PubMed] [Google Scholar]
  30. Forbes M. S., Rennels M. L., Nelson E. Caveolar systems and sarcoplasmic reticulum in coronary smooth muscle cells of the mouse. J Ultrastruct Res. 1979 Jun;67(3):325–339. doi: 10.1016/s0022-5320(79)80032-5. [DOI] [PubMed] [Google Scholar]
  31. Fujimoto T. Calcium pump of the plasma membrane is localized in caveolae. J Cell Biol. 1993 Mar;120(5):1147–1157. doi: 10.1083/jcb.120.5.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Fujimoto T., Nakade S., Miyawaki A., Mikoshiba K., Ogawa K. Localization of inositol 1,4,5-trisphosphate receptor-like protein in plasmalemmal caveolae. J Cell Biol. 1992 Dec;119(6):1507–1513. doi: 10.1083/jcb.119.6.1507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ghitescu L., Fixman A., Simionescu M., Simionescu N. Specific binding sites for albumin restricted to plasmalemmal vesicles of continuous capillary endothelium: receptor-mediated transcytosis. J Cell Biol. 1986 Apr;102(4):1304–1311. doi: 10.1083/jcb.102.4.1304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Gimeno C. J., Ljungdahl P. O., Styles C. A., Fink G. R. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell. 1992 Mar 20;68(6):1077–1090. doi: 10.1016/0092-8674(92)90079-r. [DOI] [PubMed] [Google Scholar]
  35. Glenney J. R., Jr Tyrosine phosphorylation of a 22-kDa protein is correlated with transformation by Rous sarcoma virus. J Biol Chem. 1989 Dec 5;264(34):20163–20166. [PubMed] [Google Scholar]
  36. Glenney J. R., Jr, Zokas L. Novel tyrosine kinase substrates from Rous sarcoma virus-transformed cells are present in the membrane skeleton. J Cell Biol. 1989 Jun;108(6):2401–2408. doi: 10.1083/jcb.108.6.2401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Goldberg R. I., Smith R. M., Jarett L. Insulin and alpha 2-macroglobulin-methylamine undergo endocytosis by different mechanisms in rat adipocytes: I. Comparison of cell surface events. J Cell Physiol. 1987 Nov;133(2):203–212. doi: 10.1002/jcp.1041330202. [DOI] [PubMed] [Google Scholar]
  38. Gupta S. K., Gallego C., Johnson G. L., Heasley L. E. MAP kinase is constitutively activated in gip2 and src transformed rat 1a fibroblasts. J Biol Chem. 1992 Apr 25;267(12):7987–7990. [PubMed] [Google Scholar]
  39. Hagmann J., Fishman P. H. Detergent extraction of cholera toxin and gangliosides from cultured cells and isolated membranes. Biochim Biophys Acta. 1982 Apr 29;720(2):181–187. doi: 10.1016/0167-4889(82)90010-6. [DOI] [PubMed] [Google Scholar]
  40. Hare J. F., Holocher A. Solubility in non-ionic detergents distinguishes between slowly and rapidly degraded plasma membrane proteins. J Biol Chem. 1994 Feb 25;269(8):5981–5988. [PubMed] [Google Scholar]
  41. Hausdorff W. P., Pitcher J. A., Luttrell D. K., Linder M. E., Kurose H., Parsons S. J., Caron M. G., Lefkowitz R. J. Tyrosine phosphorylation of G protein alpha subunits by pp60c-src. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5720–5724. doi: 10.1073/pnas.89.13.5720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Hooper N. M., Turner A. J. Ectoenzymes of the kidney microvillar membrane. Differential solubilization by detergents can predict a glycosyl-phosphatidylinositol membrane anchor. Biochem J. 1988 Mar 15;250(3):865–869. doi: 10.1042/bj2500865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Huang M. M., Bolen J. B., Barnwell J. W., Shattil S. J., Brugge J. S. Membrane glycoprotein IV (CD36) is physically associated with the Fyn, Lyn, and Yes protein-tyrosine kinases in human platelets. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7844–7848. doi: 10.1073/pnas.88.17.7844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Huang X. Y., Morielli A. D., Peralta E. G. Tyrosine kinase-dependent suppression of a potassium channel by the G protein-coupled m1 muscarinic acetylcholine receptor. Cell. 1993 Dec 17;75(6):1145–1156. doi: 10.1016/0092-8674(93)90324-j. [DOI] [PubMed] [Google Scholar]
  45. Izumi T., Shibata Y., Yamamoto T. Striped structures on the cytoplasmic surface membranes of the endothelial vesicles of the rat aorta revealed by quick-freeze, deep-etching replicas. Anat Rec. 1988 Mar;220(3):225–232. doi: 10.1002/ar.1092200302. [DOI] [PubMed] [Google Scholar]
  46. Izumi T., Shibata Y., Yamamoto T. The cytoplasmic surface structures of uncoated vesicles in various tissues of rat as revealed by quick-freeze, deep-etching replicas. J Electron Microsc (Tokyo) 1989;38(1):47–53. [PubMed] [Google Scholar]
  47. Jahangeer S., Rodbell M. The disaggregation theory of signal transduction revisited: further evidence that G proteins are multimeric and disaggregate to monomers when activated. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8782–8786. doi: 10.1073/pnas.90.19.8782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Janmey P. A., Lamb J., Allen P. G., Matsudaira P. T. Phosphoinositide-binding peptides derived from the sequences of gelsolin and villin. J Biol Chem. 1992 Jun 15;267(17):11818–11823. [PubMed] [Google Scholar]
  49. Jelinek M. A., Hassell J. A. Reversion of middle T antigen-transformed Rat-2 cells by Krev-1: implications for the role of p21c-ras in polyomavirus-mediated transformation. Oncogene. 1992 Sep;7(9):1687–1698. [PubMed] [Google Scholar]
  50. Jürgens L., Ilsemann P., Kratzin H. D., Hesse D., Eckart K., Thinnes F. P., Hilschmann N. Studies on human porin. IV. The primary structures of "Porin 31HM" purified from human skeletal muscle membranes and of "Porin 31HL" derived from human B lymphocyte membranes are identical. Biol Chem Hoppe Seyler. 1991 Jul;372(7):455–463. doi: 10.1515/bchm3.1991.372.2.455. [DOI] [PubMed] [Google Scholar]
  51. Kamen B. A., Smith A. K., Anderson R. G. The folate receptor works in tandem with a probenecid-sensitive carrier in MA104 cells in vitro. J Clin Invest. 1991 Apr;87(4):1442–1449. doi: 10.1172/JCI115150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Kim S., Mizoguchi A., Kikuchi A., Takai Y. Tissue and subcellular distributions of the smg-21/rap1/Krev-1 proteins which are partly distinct from those of c-ras p21s. Mol Cell Biol. 1990 Jun;10(6):2645–2652. doi: 10.1128/mcb.10.6.2645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Kitayama H., Sugimoto Y., Matsuzaki T., Ikawa Y., Noda M. A ras-related gene with transformation suppressor activity. Cell. 1989 Jan 13;56(1):77–84. doi: 10.1016/0092-8674(89)90985-9. [DOI] [PubMed] [Google Scholar]
  54. Krieger M., Herz J. Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP). Annu Rev Biochem. 1994;63:601–637. doi: 10.1146/annurev.bi.63.070194.003125. [DOI] [PubMed] [Google Scholar]
  55. Kurzchalia T. V., Dupree P., Parton R. G., Kellner R., Virta H., Lehnert M., Simons K. VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J Cell Biol. 1992 Sep;118(5):1003–1014. doi: 10.1083/jcb.118.5.1003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Lisanti M. P., Tang Z. L., Sargiacomo M. Caveolin forms a hetero-oligomeric protein complex that interacts with an apical GPI-linked protein: implications for the biogenesis of caveolae. J Cell Biol. 1993 Nov;123(3):595–604. doi: 10.1083/jcb.123.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Lodish H. F., Kong N. Cyclosporin A inhibits an initial step in folding of transferrin within the endoplasmic reticulum. J Biol Chem. 1991 Aug 15;266(23):14835–14838. [PubMed] [Google Scholar]
  58. Lyons T. J. Glycation and oxidation: a role in the pathogenesis of atherosclerosis. Am J Cardiol. 1993 Feb 25;71(6):26B–31B. doi: 10.1016/0002-9149(93)90142-y. [DOI] [PubMed] [Google Scholar]
  59. Mescher M. F., Jose M. J., Balk S. P. Actin-containing matrix associated with the plasma membrane of murine tumour and lymphoid cells. Nature. 1981 Jan 15;289(5794):139–144. doi: 10.1038/289139a0. [DOI] [PubMed] [Google Scholar]
  60. Miyauchi A., Alvarez J., Greenfield E. M., Teti A., Grano M., Colucci S., Zambonin-Zallone A., Ross F. P., Teitelbaum S. L., Cheresh D. Binding of osteopontin to the osteoclast integrin alpha v beta 3. Osteoporos Int. 1993;3 (Suppl 1):132–135. doi: 10.1007/BF01621887. [DOI] [PubMed] [Google Scholar]
  61. Montesano R., Roth J., Robert A., Orci L. Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature. 1982 Apr 15;296(5858):651–653. doi: 10.1038/296651a0. [DOI] [PubMed] [Google Scholar]
  62. Moyers J. S., Bouton A. H., Parsons S. J. The sites of phosphorylation by protein kinase C and an intact SH2 domain are required for the enhanced response to beta-adrenergic agonists in cells overexpressing c-src. Mol Cell Biol. 1993 Apr;13(4):2391–2400. doi: 10.1128/mcb.13.4.2391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Neeper M., Schmidt A. M., Brett J., Yan S. D., Wang F., Pan Y. C., Elliston K., Stern D., Shaw A. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem. 1992 Jul 25;267(21):14998–15004. [PubMed] [Google Scholar]
  64. North A. J., Galazkiewicz B., Byers T. J., Glenney J. R., Jr, Small J. V. Complementary distributions of vinculin and dystrophin define two distinct sarcolemma domains in smooth muscle. J Cell Biol. 1993 Mar;120(5):1159–1167. doi: 10.1083/jcb.120.5.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Oquendo P., Hundt E., Lawler J., Seed B. CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell. 1989 Jul 14;58(1):95–101. doi: 10.1016/0092-8674(89)90406-6. [DOI] [PubMed] [Google Scholar]
  66. Payne G. S., Baker D., van Tuinen E., Schekman R. Protein transport to the vacuole and receptor-mediated endocytosis by clathrin heavy chain-deficient yeast. J Cell Biol. 1988 May;106(5):1453–1461. doi: 10.1083/jcb.106.5.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Puchelle E., Jacquot J., Fuchey C., Burlet H., Klossek J. M., Gilain L., Triglia J. M., Thinnes F. P., Hilschmann N. Studies on human porin. IX. Immunolocalization of porin and CFTR channels in human surface respiratory epithelium. Biol Chem Hoppe Seyler. 1993 May;374(5):297–304. doi: 10.1515/bchm3.1993.374.1-6.297. [DOI] [PubMed] [Google Scholar]
  68. Raposo G., Dunia I., Delavier-Klutchko C., Kaveri S., Strosberg A. D., Benedetti E. L. Internalization of beta-adrenergic receptor in A431 cells involves non-coated vesicles. Eur J Cell Biol. 1989 Dec;50(2):340–352. [PubMed] [Google Scholar]
  69. Raposo G., Dunia I., Marullo S., André C., Guillet J. G., Strosberg A. D., Benedetti E. L., Hoebeke J. Redistribution of muscarinic acetylcholine receptors on human fibroblasts induced by regulatory ligands. Biol Cell. 1987;60(2):117–123. doi: 10.1111/j.1768-322x.1987.tb00551.x. [DOI] [PubMed] [Google Scholar]
  70. Robinson P. J., Millrain M., Antoniou J., Simpson E., Mellor A. L. A glycophospholipid anchor is required for Qa-2-mediated T cell activation. Nature. 1989 Nov 2;342(6245):85–87. doi: 10.1038/342085a0. [DOI] [PubMed] [Google Scholar]
  71. Rothberg K. G., Heuser J. E., Donzell W. C., Ying Y. S., Glenney J. R., Anderson R. G. Caveolin, a protein component of caveolae membrane coats. Cell. 1992 Feb 21;68(4):673–682. doi: 10.1016/0092-8674(92)90143-z. [DOI] [PubMed] [Google Scholar]
  72. Rozakis-Adcock M., McGlade J., Mbamalu G., Pelicci G., Daly R., Li W., Batzer A., Thomas S., Brugge J., Pelicci P. G. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature. 1992 Dec 17;360(6405):689–692. doi: 10.1038/360689a0. [DOI] [PubMed] [Google Scholar]
  73. Ruggieri R., Bender A., Matsui Y., Powers S., Takai Y., Pringle J. R., Matsumoto K. RSR1, a ras-like gene homologous to Krev-1 (smg21A/rap1A): role in the development of cell polarity and interactions with the Ras pathway in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Feb;12(2):758–766. doi: 10.1128/mcb.12.2.758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Sargiacomo M., Sudol M., Tang Z., Lisanti M. P. 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. doi: 10.1083/jcb.122.4.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Schmidt A. M., Vianna M., Gerlach M., Brett J., Ryan J., Kao J., Esposito C., Hegarty H., Hurley W., Clauss M. Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J Biol Chem. 1992 Jul 25;267(21):14987–14997. [PubMed] [Google Scholar]
  76. Schoenenberger C. A., Zuk A., Kendall D., Matlin K. S. Multilayering and loss of apical polarity in MDCK cells transformed with viral K-ras. J Cell Biol. 1991 Mar;112(5):873–889. doi: 10.1083/jcb.112.5.873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Severs N. J. Caveolae: static inpocketings of the plasma membrane, dynamic vesicles or plain artifact? J Cell Sci. 1988 Jul;90(Pt 3):341–348. doi: 10.1242/jcs.90.3.341. [DOI] [PubMed] [Google Scholar]
  78. Simionescu N., Mora R., Vasile E., Lupu F., Filip D. A., Simionescu M. Prelesional modifications of the vessel wall in hyperlipidemic atherogenesis. Extracellular accumulation of modified and reassembled lipoproteins. Ann N Y Acad Sci. 1990;598:1–16. doi: 10.1111/j.1749-6632.1990.tb42271.x. [DOI] [PubMed] [Google Scholar]
  79. Simonson M. S., Herman W. H. Protein kinase C and protein tyrosine kinase activity contribute to mitogenic signaling by endothelin-1. Cross-talk between G protein-coupled receptors and pp60c-src. J Biol Chem. 1993 May 5;268(13):9347–9357. [PubMed] [Google Scholar]
  80. Smart E. J., Foster D. C., Ying Y. S., Kamen B. A., Anderson R. G. Protein kinase C activators inhibit receptor-mediated potocytosis by preventing internalization of caveolae. J Cell Biol. 1994 Feb;124(3):307–313. doi: 10.1083/jcb.124.3.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Snelting-Havinga I., Mommaas M., Van Hinsbergh V. W., Daha M. R., Daems W. T., Vermeer B. J. Immunoelectron microscopic visualization of the transcytosis of low density lipoproteins in perfused rat arteries. Eur J Cell Biol. 1989 Feb;48(1):27–36. [PubMed] [Google Scholar]
  82. Steele-Mortimer O., Clague M. J., Huber L. A., Chavrier P., Gruenberg J., Gorvel J. P. The N-terminal domain of a rab protein is involved in membrane-membrane recognition and/or fusion. EMBO J. 1994 Jan 1;13(1):34–41. doi: 10.1002/j.1460-2075.1994.tb06232.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Stefanová I., Corcoran M. L., Horak E. M., Wahl L. M., Bolen J. B., Horak I. D. Lipopolysaccharide induces activation of CD14-associated protein tyrosine kinase p53/56lyn. J Biol Chem. 1993 Oct 5;268(28):20725–20728. [PubMed] [Google Scholar]
  84. Stefanová I., Horejsí V., Ansotegui I. J., Knapp W., Stockinger H. GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science. 1991 Nov 15;254(5034):1016–1019. doi: 10.1126/science.1719635. [DOI] [PubMed] [Google Scholar]
  85. Streuli C. H., Patel B., Critchley D. R. The cholera toxin receptor ganglioside GM remains associated with triton X-100 cytoskeletons of BALB/c-3T3 cells. Exp Cell Res. 1981 Dec;136(2):247–254. doi: 10.1016/0014-4827(81)90002-1. [DOI] [PubMed] [Google Scholar]
  86. Strosberg A. D. Structure/function relationship of proteins belonging to the family of receptors coupled to GTP-binding proteins. Eur J Biochem. 1991 Feb 26;196(1):1–10. doi: 10.1111/j.1432-1033.1991.tb15778.x. [DOI] [PubMed] [Google Scholar]
  87. Thomas P. M., Samelson L. E. The glycophosphatidylinositol-anchored Thy-1 molecule interacts with the p60fyn protein tyrosine kinase in T cells. J Biol Chem. 1992 Jun 15;267(17):12317–12322. [PubMed] [Google Scholar]
  88. Vasile E., Antohe F. An ultrastructural study of beta-very low density lipoprotein uptake and transport by valvular endothelium of hyperlipidemic rabbits. J Submicrosc Cytol Pathol. 1991 Apr;23(2):279–287. [PubMed] [Google Scholar]
  89. Vasile E., Simionescu M., Simionescu N. Visualization of the binding, endocytosis, and transcytosis of low-density lipoprotein in the arterial endothelium in situ. J Cell Biol. 1983 Jun;96(6):1677–1689. doi: 10.1083/jcb.96.6.1677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Vidugiriene J., Menon A. K. Early lipid intermediates in glycosyl-phosphatidylinositol anchor assembly are synthesized in the ER and located in the cytoplasmic leaflet of the ER membrane bilayer. J Cell Biol. 1993 Jun;121(5):987–996. doi: 10.1083/jcb.121.5.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Wagner R. C., Kreiner P., Barrnett R. J., Bitensky M. W. Biochemical characterization and cytochemical localization of a catecholamine-sensitive adenylate cyclase in isolated capillary endothelium. Proc Natl Acad Sci U S A. 1972 Nov;69(11):3175–3179. doi: 10.1073/pnas.69.11.3175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Walker S. R., Williams M. C., Benson B. Immunocytochemical localization of the major surfactant apoproteins in type II cells, Clara cells, and alveolar macrophages of rat lung. J Histochem Cytochem. 1986 Sep;34(9):1137–1148. doi: 10.1177/34.9.2426341. [DOI] [PubMed] [Google Scholar]
  93. Williams S. K., Devenny J. J., Bitensky M. W. Micropinocytic ingestion of glycosylated albumin by isolated microvessels: possible role in pathogenesis of diabetic microangiopathy. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2393–2397. doi: 10.1073/pnas.78.4.2393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Ying Y. S., Anderson R. G., Rothberg K. G. Each caveola contains multiple glycosyl-phosphatidylinositol-anchored membrane proteins. Cold Spring Harb Symp Quant Biol. 1992;57:593–604. doi: 10.1101/sqb.1992.057.01.065. [DOI] [PubMed] [Google Scholar]
  95. Zurzolo C., van't Hof W., van Meer G., Rodriguez-Boulan E. VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO J. 1994 Jan 1;13(1):42–53. doi: 10.1002/j.1460-2075.1994.tb06233.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. van Corven E. J., Hordijk P. L., Medema R. H., Bos J. L., Moolenaar W. H. Pertussis toxin-sensitive activation of p21ras by G protein-coupled receptor agonists in fibroblasts. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1257–1261. doi: 10.1073/pnas.90.4.1257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. von Zastrow M., Kobilka B. K. Ligand-regulated internalization and recycling of human beta 2-adrenergic receptors between the plasma membrane and endosomes containing transferrin receptors. J Biol Chem. 1992 Feb 15;267(5):3530–3538. [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES