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. 1993 Aug 2;122(4):789–807. doi: 10.1083/jcb.122.4.789

Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells

PMCID: PMC2119592  PMID: 8349730

Abstract

GPI-linked protein molecules become Triton-insoluble during polarized sorting to the apical cell surface of epithelial cells. These insoluble complexes, enriched in cholesterol, glycolipids, and GPI-linked proteins, have been isolated by flotation on sucrose density gradients and are thought to contain the putative GPI-sorting machinery. As the cellular origin and molecular protein components of this complex remain unknown, we have begun to characterize these low-density insoluble complexes isolated from MDCK cells. We find that these complexes, which represent 0.4-0.8% of the plasma membrane, ultrastructurally resemble caveolae and are over 150-fold enriched in a model GPI-anchored protein and caveolin, a caveolar marker protein. However, they exclude many other plasma membrane associated molecules and organelle-specific marker enzymes, suggesting that they represent microdomains of the plasma membrane. In addition to caveolin, these insoluble complexes contain a subset of hydrophobic plasma membrane proteins and cytoplasmically-oriented signaling molecules, including: (a) GTP- binding proteins--both small and heterotrimeric; (b) annex II--an apical calcium-regulated phospholipid binding protein with a demonstrated role in exocytic fusion events; (c) c-Yes--an apically localized member of the Src family of non-receptor type protein- tyrosine kinases; and (d) an unidentified serine-kinase activity. As we demonstrate that caveolin is both a transmembrane molecule and a major phospho-acceptor component of these complexes, we propose that caveolin could function as a transmembrane adaptor molecule that couples luminal GPI-linked proteins with cytoplasmically oriented signaling molecules during GPI-membrane trafficking or GPI-mediated signal transduction events. In addition, our results have implications for understanding v- Src transformation and the actions of cholera and pertussis toxins on hetero-trimeric G proteins.

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Selected References

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  1. Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., Shibuya M., Fukami Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem. 1987 Apr 25;262(12):5592–5595. [PubMed] [Google Scholar]
  2. Ali S. M., Geisow M. J., Burgoyne R. D. A role for calpactin in calcium-dependent exocytosis in adrenal chromaffin cells. Nature. 1989 Jul 27;340(6231):313–315. doi: 10.1038/340313a0. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Anderson R. G., Pathak R. K. Vesicles and cisternae in the trans Golgi apparatus of human fibroblasts are acidic compartments. Cell. 1985 Mar;40(3):635–643. doi: 10.1016/0092-8674(85)90212-0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Boyle W. J., van der Geer P., Hunter T. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 1991;201:110–149. doi: 10.1016/0076-6879(91)01013-r. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Brown D. A., Crise B., Rose J. K. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science. 1989 Sep 29;245(4925):1499–1501. doi: 10.1126/science.2571189. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Brugge J. S., Erikson R. L. Identification of a transformation-specific antigen induced by an avian sarcoma virus. Nature. 1977 Sep 22;269(5626):346–348. doi: 10.1038/269346a0. [DOI] [PubMed] [Google Scholar]
  11. Campbell K. S., Hager E. J., Friedrich R. J., Cambier J. C. IgM antigen receptor complex contains phosphoprotein products of B29 and mb-1 genes. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3982–3986. doi: 10.1073/pnas.88.9.3982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chamberlain J. P. Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor, sodium salicylate. Anal Biochem. 1979 Sep 15;98(1):132–135. doi: 10.1016/0003-2697(79)90716-4. [DOI] [PubMed] [Google Scholar]
  13. Cross G. A. Glycolipid anchoring of plasma membrane proteins. Annu Rev Cell Biol. 1990;6:1–39. doi: 10.1146/annurev.cb.06.110190.000245. [DOI] [PubMed] [Google Scholar]
  14. Domínguez P., Velasco G., Barros F., Lazo P. S. Intestinal brush border membranes contain regulatory subunits of adenylyl cyclase. Proc Natl Acad Sci U S A. 1987 Oct;84(20):6965–6969. doi: 10.1073/pnas.84.20.6965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Drust D. S., Creutz C. E. Aggregation of chromaffin granules by calpactin at micromolar levels of calcium. Nature. 1988 Jan 7;331(6151):88–91. doi: 10.1038/331088a0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Emans N., Gorvel J. P., Walter C., Gerke V., Kellner R., Griffiths G., Gruenberg J. Annexin II is a major component of fusogenic endosomal vesicles. J Cell Biol. 1993 Mar;120(6):1357–1369. doi: 10.1083/jcb.120.6.1357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ercolani L., Stow J. L., Boyle J. F., Holtzman E. J., Lin H., Grove J. R., Ausiello D. A. Membrane localization of the pertussis toxin-sensitive G-protein subunits alpha i-2 and alpha i-3 and expression of a metallothionein-alpha i-2 fusion gene in LLC-PK1 cells. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4635–4639. doi: 10.1073/pnas.87.12.4635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Garcia M., Mirre C., Quaroni A., Reggio H., Le Bivic A. GPI-anchored proteins associate to form microdomains during their intracellular transport in Caco-2 cells. J Cell Sci. 1993 Apr;104(Pt 4):1281–1290. doi: 10.1242/jcs.104.4.1281. [DOI] [PubMed] [Google Scholar]
  22. Gerke V., Weber K. Identity of p36K phosphorylated upon Rous sarcoma virus transformation with a protein purified from brush borders; calcium-dependent binding to non-erythroid spectrin and F-actin. EMBO J. 1984 Jan;3(1):227–233. doi: 10.1002/j.1460-2075.1984.tb01789.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gilbert T., Le Bivic A., Quaroni A., Rodriguez-Boulan E. Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells. J Cell Biol. 1991 Apr;113(2):275–288. doi: 10.1083/jcb.113.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Glenney J. R., Jr Microinjection of antibodies to the calpactin I light chain in MDBK cells causes precipition of the cytoskeletal calpactin I complex without affecting the distribution of related proteins. Prog Clin Biol Res. 1990;349:135–146. [PubMed] [Google Scholar]
  25. Glenney J. R., Jr, Soppet D. 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):10517–10521. doi: 10.1073/pnas.89.21.10517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Glenney J. R., Jr The sequence of human caveolin reveals identity with VIP21, a component of transport vesicles. FEBS Lett. 1992 Dec 7;314(1):45–48. doi: 10.1016/0014-5793(92)81458-x. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Gottesman M. M., Roth C., Vlahakis G., Pastan I. Cholera toxin treatment stimulates tumorigenicity of Rous sarcoma virus-transformed cells. Mol Cell Biol. 1984 Dec;4(12):2639–2642. doi: 10.1128/mcb.4.12.2639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Grandori C., Sudol M., Hanafusa H. c-yes protein kinase is associated with a 38 kD protein in cerebellum. Oncogene. 1991 Jun;6(6):1063–1066. [PubMed] [Google Scholar]
  31. 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]
  32. Hannan L. A., Lisanti M. P., Rodriguez-Boulan E., Edidin M. Correctly sorted molecules of a GPI-anchored protein are clustered and immobile when they arrive at the apical surface of MDCK cells. J Cell Biol. 1993 Jan;120(2):353–358. doi: 10.1083/jcb.120.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hoessli D., Rungger-Brändle E. Association of specific cell-surface glycoproteins with a triton X-100-resistant complex of plasma membrane proteins isolated from T-lymphoma cells (P1798). Exp Cell Res. 1985 Jan;156(1):239–250. doi: 10.1016/0014-4827(85)90278-2. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. 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]
  36. 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]
  37. Le Bivic A., Quaroni A., Nichols B., Rodriguez-Boulan E. Biogenetic pathways of plasma membrane proteins in Caco-2, a human intestinal epithelial cell line. J Cell Biol. 1990 Oct;111(4):1351–1361. doi: 10.1083/jcb.111.4.1351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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. 1989 Nov;109(5):2145–2156. doi: 10.1083/jcb.109.5.2145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lisanti M. P., Caras I. W., Gilbert T., Hanzel D., Rodriguez-Boulan E. Vectorial apical delivery and slow endocytosis of a glycolipid-anchored fusion protein in transfected MDCK cells. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7419–7423. doi: 10.1073/pnas.87.19.7419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lisanti M. P., Caras I. W., Rodriguez-Boulan E. Fusion proteins containing a minimal GPI-attachment signal are apically expressed in transfected MDCK cells. J Cell Sci. 1991 Jul;99(Pt 3):637–640. doi: 10.1242/jcs.99.3.637. [DOI] [PubMed] [Google Scholar]
  41. Lisanti M. P., Field M. C., Caras I. W., Menon A. K., Rodriguez-Boulan E. Mannosamine, a novel inhibitor of glycosylphosphatidylinositol incorporation into proteins. EMBO J. 1991 Aug;10(8):1969–1977. doi: 10.1002/j.1460-2075.1991.tb07726.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lisanti M. P., Le Bivic A., Saltiel A. R., Rodriguez-Boulan E. Preferred apical distribution of glycosyl-phosphatidylinositol (GPI) anchored proteins: a highly conserved feature of the polarized epithelial cell phenotype. J Membr Biol. 1990 Feb;113(2):155–167. doi: 10.1007/BF01872889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lisanti M. P., Rodriguez-Boulan E. Glycophospholipid membrane anchoring provides clues to the mechanism of protein sorting in polarized epithelial cells. Trends Biochem Sci. 1990 Mar;15(3):113–118. doi: 10.1016/0968-0004(90)90195-h. [DOI] [PubMed] [Google Scholar]
  44. Lisanti M. P., Sargiacomo M., Graeve L., Saltiel A. R., Rodriguez-Boulan E. Polarized apical distribution of glycosyl-phosphatidylinositol-anchored proteins in a renal epithelial cell line. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9557–9561. doi: 10.1073/pnas.85.24.9557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Low M. G. Glycosyl-phosphatidylinositol: a versatile anchor for cell surface proteins. FASEB J. 1989 Mar;3(5):1600–1608. doi: 10.1096/fasebj.3.5.2522071. [DOI] [PubMed] [Google Scholar]
  46. Luo K., Hurley T. R., Sefton B. M. Transfer of proteins to membranes facilitates both cyanogen bromide cleavage and two-dimensional proteolytic mapping. Oncogene. 1990 Jun;5(6):921–923. [PubMed] [Google Scholar]
  47. Löw A., Faulhammer H. G., Sprinzl M. Affinity labeling of GTP-binding proteins in cellular extracts. FEBS Lett. 1992 May 25;303(1):64–68. doi: 10.1016/0014-5793(92)80478-y. [DOI] [PubMed] [Google Scholar]
  48. Melançon P. Vesicle traffic: G whizz. Curr Biol. 1993 Apr 1;3(4):230–233. doi: 10.1016/0960-9822(93)90341-k. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Nakata T., Sobue K., Hirokawa N. Conformational change and localization of calpactin I complex involved in exocytosis as revealed by quick-freeze, deep-etch electron microscopy and immunocytochemistry. J Cell Biol. 1990 Jan;110(1):13–25. doi: 10.1083/jcb.110.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Nigam S. K., Rodriguez-Boulan E., Silver R. B. Changes in intracellular calcium during the development of epithelial polarity and junctions. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6162–6166. doi: 10.1073/pnas.89.13.6162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Peter M. E., Hall C., Rühlmann A., Sancho J., Terhorst C. The T-cell receptor zeta chain contains a GTP/GDP binding site. EMBO J. 1992 Mar;11(3):933–941. doi: 10.1002/j.1460-2075.1992.tb05132.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Peters K. R., Carley W. W., Palade G. E. Endothelial plasmalemmal vesicles have a characteristic striped bipolar surface structure. J Cell Biol. 1985 Dec;101(6):2233–2238. doi: 10.1083/jcb.101.6.2233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Pimplikar S. W., Simons K. Regulation of apical transport in epithelial cells by a Gs class of heterotrimeric G protein. Nature. 1993 Apr 1;362(6419):456–458. doi: 10.1038/362456a0. [DOI] [PubMed] [Google Scholar]
  55. Radke K., Carter V. C., Moss P., Dehazya P., Schliwa M., Martin G. S. Membrane association of a 36,000-dalton substrate for tyrosine phosphorylation in chicken embryo fibroblasts transformed by avian sarcoma viruses. J Cell Biol. 1983 Nov;97(5 Pt 1):1601–1611. doi: 10.1083/jcb.97.5.1601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. 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]
  57. Rodriguez-Boulan E., Nelson W. J. Morphogenesis of the polarized epithelial cell phenotype. Science. 1989 Aug 18;245(4919):718–725. doi: 10.1126/science.2672330. [DOI] [PubMed] [Google Scholar]
  58. Rodriguez-Boulan E. Polarized assembly of enveloped viruses from cultured epithelial cells. Methods Enzymol. 1983;98:486–501. doi: 10.1016/0076-6879(83)98176-4. [DOI] [PubMed] [Google Scholar]
  59. Rodriguez-Boulan E., Powell S. K. Polarity of epithelial and neuronal cells. Annu Rev Cell Biol. 1992;8:395–427. doi: 10.1146/annurev.cb.08.110192.002143. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. Rothberg K. G., Ying Y. S., Kamen B. A., Anderson R. G. Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate. J Cell Biol. 1990 Dec;111(6 Pt 2):2931–2938. doi: 10.1083/jcb.111.6.2931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Sargiacomo M., Lisanti M., Graeve L., Le Bivic A., Rodriguez-Boulan E. Integral and peripheral protein composition of the apical and basolateral membrane domains in MDCK cells. J Membr Biol. 1989 Mar;107(3):277–286. doi: 10.1007/BF01871942. [DOI] [PubMed] [Google Scholar]
  63. Saukkonen K., Burnette W. N., Mar V. L., Masure H. R., Tuomanen E. I. Pertussis toxin has eukaryotic-like carbohydrate recognition domains. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):118–122. doi: 10.1073/pnas.89.1.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Schell M. J., Maurice M., Stieger B., Hubbard A. L. 5'nucleotidase is sorted to the apical domain of hepatocytes via an indirect route. J Cell Biol. 1992 Dec;119(5):1173–1182. doi: 10.1083/jcb.119.5.1173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. 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]
  66. Shenker A., Goldsmith P., Unson C. G., Spiegel A. M. The G protein coupled to the thromboxane A2 receptor in human platelets is a member of the novel Gq family. J Biol Chem. 1991 May 15;266(14):9309–9313. [PubMed] [Google Scholar]
  67. Shpetner H. S., Vallee R. B. Dynamin is a GTPase stimulated to high levels of activity by microtubules. Nature. 1992 Feb 20;355(6362):733–735. doi: 10.1038/355733a0. [DOI] [PubMed] [Google Scholar]
  68. Simionescu N., Siminoescu M., Palade G. E. Permeability of muscle capillaries to small heme-peptides. Evidence for the existence of patent transendothelial channels. J Cell Biol. 1975 Mar;64(3):586–607. doi: 10.1083/jcb.64.3.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Simons K., Wandinger-Ness A. Polarized sorting in epithelia. Cell. 1990 Jul 27;62(2):207–210. doi: 10.1016/0092-8674(90)90357-k. [DOI] [PubMed] [Google Scholar]
  70. 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]
  71. Stow J. L., de Almeida J. B., Narula N., Holtzman E. J., Ercolani L., Ausiello D. A. A heterotrimeric G protein, G alpha i-3, on Golgi membranes regulates the secretion of a heparan sulfate proteoglycan in LLC-PK1 epithelial cells. J Cell Biol. 1991 Sep;114(6):1113–1124. doi: 10.1083/jcb.114.6.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. 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]
  73. Su B., Waneck G. L., Flavell R. A., Bothwell A. L. The glycosyl phosphatidylinositol anchor is critical for Ly-6A/E-mediated T cell activation. J Cell Biol. 1991 Feb;112(3):377–384. doi: 10.1083/jcb.112.3.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Sudol M., Hanafusa H. Cellular proteins homologous to the viral yes gene product. Mol Cell Biol. 1986 Aug;6(8):2839–2846. doi: 10.1128/mcb.6.8.2839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. 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]
  76. Thompson J. A., Lau A. L., Cunningham D. D. Selective radiolabeling of cell surface proteins to a high specific activity. Biochemistry. 1987 Feb 10;26(3):743–750. doi: 10.1021/bi00377a014. [DOI] [PubMed] [Google Scholar]
  77. 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]
  78. Wandinger-Ness A., Bennett M. K., Antony C., Simons K. 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. doi: 10.1083/jcb.111.3.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Yu J., Fischman D. A., Steck T. L. Selective solubilization of proteins and phospholipids from red blood cell membranes by nonionic detergents. J Supramol Struct. 1973;1(3):233–248. doi: 10.1002/jss.400010308. [DOI] [PubMed] [Google Scholar]
  80. Zachary I., Sinnett-Smith J., Rozengurt E. Stimulation of tyrosine kinase activity in anti-phosphotyrosine immune complexes of Swiss 3T3 cell lysates occurs rapidly after addition of bombesin, vasopressin, and endothelin to intact cells. J Biol Chem. 1991 Dec 15;266(35):24126–24133. [PubMed] [Google Scholar]
  81. Zhao Y. H., Krueger J. G., Sudol M. Expression of cellular-yes protein in mammalian tissues. Oncogene. 1990 Nov;5(11):1629–1635. [PubMed] [Google Scholar]
  82. 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. 1993 Jun;121(5):1031–1039. doi: 10.1083/jcb.121.5.1031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. van den Berghe N., Nieuwkoop N. J., Vaandrager A. B., de Jonge H. R. Asymmetrical distribution of G-proteins among the apical and basolateral membranes of rat enterocytes. Biochem J. 1991 Sep 1;278(Pt 2):565–571. doi: 10.1042/bj2780565. [DOI] [PMC free article] [PubMed] [Google Scholar]

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