Involvement of a Triton-insoluble Floating Fraction inDictyostelium Cell-Cell Adhesion

We have isolated and characterized a Triton-insoluble floating fraction (TIFF) fromDictyostelium. Ten major proteins were consistently detected in TIFF, and six species were identified by mass spectrometry as actin, porin, comitin, regulatory myosin light chain, a novel member of the CD36 family, and the phospholipid-anchored cell adhesion molecule gp80. TIFF was enriched with many acylated proteins. Also, the sterol/phospholipid ratio of TIFF was 10-fold higher than that of the bulk plasma membrane. Immunoelectron microscopy showed that TIFF has vesicular morphology and confirmed the association of gp80 and comitin with TIFF membranes. Several TIFF properties were similar to those ofDictyostelium contact regions, which were isolated as a cytoskeleton-associated membrane fraction. Mass spectrometry demonstrated that TIFF and contact regions shared the same major proteins. During development, gp80 colocalized with F-actin, porin, and comitin at cell-cell contacts. These proteins were also recruited to gp80 caps induced by antibody cross-linking. Filipin staining revealed high sterol levels in both gp80-enriched cell-cell contacts and gp80 caps. Moreover, sterol sequestration by filipin and digitonin inhibited gp80-mediated cell-cell adhesion. This study reveals thatDictyostelium TIFF has structural properties previously attributed to vertebrate TIFF and establishes a role forDictyostelium TIFF in cell-cell adhesion during development. We have isolated and characterized a Triton-insoluble floating fraction (TIFF) fromDictyostelium. Ten major proteins were consistently detected in TIFF, and six species were identified by mass spectrometry as actin, porin, comitin, regulatory myosin light chain, a novel member of the CD36 family, and the phospholipid-anchored cell adhesion molecule gp80. TIFF was enriched with many acylated proteins. Also, the sterol/phospholipid ratio of TIFF was 10-fold higher than that of the bulk plasma membrane. Immunoelectron microscopy showed that TIFF has vesicular morphology and confirmed the association of gp80 and comitin with TIFF membranes. Several TIFF properties were similar to those ofDictyostelium contact regions, which were isolated as a cytoskeleton-associated membrane fraction. Mass spectrometry demonstrated that TIFF and contact regions shared the same major proteins. During development, gp80 colocalized with F-actin, porin, and comitin at cell-cell contacts. These proteins were also recruited to gp80 caps induced by antibody cross-linking. Filipin staining revealed high sterol levels in both gp80-enriched cell-cell contacts and gp80 caps. Moreover, sterol sequestration by filipin and digitonin inhibited gp80-mediated cell-cell adhesion. This study reveals thatDictyostelium TIFF has structural properties previously attributed to vertebrate TIFF and establishes a role forDictyostelium TIFF in cell-cell adhesion during development. Triton-insoluble floating fraction 3-[(3-cholamidopropyl)dimethylammonio]-1-propanesulfonic acid CHAPS-insoluble floating fraction matrix-assisted laser desorption ionization time-of-flight green fluorescent protein regulatory myosin light chain glycosylphosphatidylinositol polyacrylamide gel electrophoresis expressed sequence tag monoclonal antibody 4-morpholine ethanesulfonic acid Cell membranes are thought to exist primarily in a fluid, liquid crystalline phase. However, certain membranes display elevated acyl chain order and exist in a liquid-ordered phase. These membranes exhibit Triton X-100 insolubility and can be separated from other insoluble cellular material by floatation into density gradients after isopycnic centrifugation (1Brown D.A. London E. Annu. Rev. Cell Dev. Biol. 1998; 14: 111-136Crossref PubMed Scopus (2545) Google Scholar, 2Brown D.A. London E. J. Memb. Biol. 1998; 164: 103-114Crossref PubMed Scopus (833) Google Scholar, 3Hooper N.M. Mol. Membr. Biol. 1999; 16: 145-156Crossref PubMed Scopus (357) Google Scholar). We will refer to these membranes as a Triton X-100-insoluble floating fraction (TIFF).1 TIFF has distinctive structural properties and is involved in a variety of cellular functions. TIFF is typically isolated as membrane vesicles (4Brown D.A. Rose J.K. Cell. 1992; 68: 533-544Abstract Full Text PDF PubMed Scopus (2604) Google Scholar, 5Sargiacomo M. Sudol M. Tang Z. Lisanti M.P. J. Cell Biol. 1993; 122: 789-807Crossref PubMed Scopus (860) Google Scholar, 6Kubler E. Dohlman H.G. Lisanti M.P. J. Biol. Chem. 1996; 271: 32975-32980Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar). These membranes are enriched in lipids, such as cholesterol and those with saturated acyl chains, which are expected to pack closely within the liquid-ordered environment (7Simons K. Ikonen E. Nature. 1997; 387: 569-572Crossref PubMed Scopus (8047) Google Scholar). In addition, many cell membrane-associated structural and signaling proteins have been found in TIFF (8Anderson R.G. Annu. Rev. Biochem. 1998; 67: 199-225Crossref PubMed Scopus (1719) Google Scholar). TIFF proteins are often anchored to the membranes through a lipid moiety (7Simons K. Ikonen E. Nature. 1997; 387: 569-572Crossref PubMed Scopus (8047) Google Scholar). TIFF was originally characterized in vertebrate cells (4Brown D.A. Rose J.K. Cell. 1992; 68: 533-544Abstract Full Text PDF PubMed Scopus (2604) Google Scholar, 5Sargiacomo M. Sudol M. Tang Z. Lisanti M.P. J. Cell Biol. 1993; 122: 789-807Crossref PubMed Scopus (860) Google Scholar). However, TIFF analyses have been extended to yeast and Drosophila (6Kubler E. Dohlman H.G. Lisanti M.P. J. Biol. Chem. 1996; 271: 32975-32980Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar,9Rietveld A. Neutz S. Simons K. Eaton S. J. Biol. Chem. 1999; 274: 12049-12054Abstract Full Text Full Text PDF PubMed Scopus (242) Google Scholar, 10Bagnat M. Keranen S. Shevchenko A. Shevchenko A. Simons K. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 3254-3259Crossref PubMed Scopus (502) Google Scholar), and a CHAPS-insoluble floating fraction (CHIFF) has been reported in Dictyostelium discoideum (11Xiao Z. Devreotes P.N. Mol. Biol. Cell. 1997; 8: 855-869Crossref PubMed Scopus (37) Google Scholar). The physiological importance of TIFF has been shown by perturbation of TIFF protein activities by cholesterol sequestration and through the co-localization of TIFF components at sites of cellular activity. Processes that involve TIFF include cellular trafficking (7Simons K. Ikonen E. Nature. 1997; 387: 569-572Crossref PubMed Scopus (8047) Google Scholar), T-cell signaling (12Xavier R. Brennan T. Li Q. McCormack C. Seed B. Immunity. 1998; 8: 723-732Abstract Full Text Full Text PDF PubMed Scopus (837) Google Scholar, 13Webb Y Hermida-Matsumoto L. Resh M.D. J. Biol. Chem. 2000; 275: 261-270Abstract Full Text Full Text PDF PubMed Scopus (372) Google Scholar, 14Wulfing C. Davis M.M. Science. 1998; 282: 2266-2269Crossref PubMed Scopus (534) Google Scholar, 15Stulnig T.M. Berger M. Sigmund T. Raederstorff D. Stockinger H. Waldhausl W. J. Cell Biol. 1998; 143: 637-644Crossref PubMed Scopus (237) Google Scholar, 16Viola A. Schroeder S. Sakakibara Y. Lanzavecchia A. Science. 1999; 283: 680-682Crossref PubMed Scopus (840) Google Scholar), integrin signaling (17Green J.M. Zhelesnyak A. Chung J. Lindberg F.P. Sarfati M. Frazier W.A. Brown E.J. J. Cell Biol. 1999; 146: 673-682Crossref PubMed Scopus (154) Google Scholar, 18Krauss K. Altevogt P. J. Biol. Chem. 1999; 274: 36921-36927Abstract Full Text Full Text PDF PubMed Scopus (157) Google Scholar), and bacterial interactions with macrophages (19Gatfield J. Pieters J. Science. 2000; 288: 1647-1650Crossref PubMed Scopus (472) Google Scholar) and mast cells (20Shin J.-S. Gao Z. Abraham S.N. Science. 2000; 289: 785-788Crossref PubMed Scopus (272) Google Scholar). Dictyostelium is a favorable model organism for the study of plasma membrane structure and function. Dictyostelium is amenable to both biochemical and molecular genetic analyses of its cellular and developmental processes. During Dictyosteliumdevelopment, unicellular amoeboid cells aggregate through chemotaxis toward cAMP and embark on a multicellular developmental program (21Loomis W.F. Dictyostelium discoideum: A Developmental System. Academic Press, Inc., New York1975Google Scholar). Three components of the cAMP signaling pathway (the cAMP receptor cAR1, adenylate cyclase, and the cell surface phosphodiesterase) are found in CHIFF, suggesting that they are components of specialized microdomains on the plasma membrane (11Xiao Z. Devreotes P.N. Mol. Biol. Cell. 1997; 8: 855-869Crossref PubMed Scopus (37) Google Scholar). Multicellularity in Dictyostelium is maintained by several cell adhesion molecules, including DdCAD-1/gp24 (22Knecht D.A. Fuller D.L. Loomis W.F. Dev. Biol. 1987; 121: 277-283Crossref PubMed Scopus (70) Google Scholar, 23Brar S.K. Siu C.-H. J. Biol. Chem. 1993; 268: 24902-24909Abstract Full Text PDF PubMed Google Scholar, 24Wong E.F.S. Brar S.K. Sesaki H. Yang C. Siu C.-H. J. Biol. Chem. 1996; 271: 16399-16408Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar), gp150/LagC (25Geltosky J. A. Cell. Full Text PDF PubMed Scopus Google Scholar, P. Siu C.-H. J. Biol. Chem. 1992; Full Text PDF PubMed Google Scholar, J. L. D. Loomis W.F. Siu C.-H. Dev. Biol. 2000; PubMed Scopus Google Scholar), and gp80 K. Nature. 274: PubMed Scopus Google Scholar, C.-H. J. Biol. Chem. Full Text PDF PubMed Google Scholar). gp80 is expressed during the of A. J. M. J. PubMed Google Scholar, Siu C.-H. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, L. Brar S.K. Siu C.-H. J. Cell Sci. Google Scholar) and the contact sites A by a C.-H. A. J. Cell Biol. 1987; PubMed Scopus Google Scholar, Siu C.-H. J. Cell Biol. PubMed Scopus Google Scholar, J. Siu C.-H. Cell. Full Text PDF PubMed Scopus Google Scholar). gp80 is both for adhesion during C. Dev. PubMed Scopus Google Scholar, C.-H. Dev. PubMed Scopus (37) Google Scholar, E. E. J. S. Proc. Natl. Acad. Sci. U. S. A. 1998; PubMed Scopus Google Scholar) and for the of cells J. J. PubMed Scopus Google Scholar, Siu C.-H. Cell PubMed Scopus Google Scholar). is that interactions cell-cell adhesion Dictyostelium However, structural of gp80 adhesion are gp80 is enriched in Triton cytoskeleton-associated contact regions E.J. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). This fraction membranes with of cell-cell contacts and can be isolated after the cell of development. that gp80 is phospholipid-anchored H. C. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, J. J. 8: PubMed Scopus Google Scholar), that these Triton X-100-insoluble contact regions be a of TIFF and that gp80 adhesion be as membrane within the plasma membrane. In the have isolated Dictyostelium TIFF, characterized its identified its protein and its lipid We that TIFF membranes many and biochemical properties with the Triton X-100-insoluble contact a role for TIFF components during gp80-mediated adhesion is through and adhesion perturbation Dictyostelium including the and the C. Dev. PubMed Scopus Google Scholar), were in association with in liquid M. Cell Biol. 1987; PubMed Scopus Google Scholar). development, cells at the were and at in H. K. J. Cell Biol. 1996; PubMed Scopus Google Scholar) and at gp80 cells were with cAMP at a of were also in on A was by the comitin A. Biochem. Cell Biol. 1992; PubMed Scopus Google Scholar), by into the of the Dictyostelium from R. of at of comitin was the of the The of from H. the of was into the of comitin in the was and of was into cells by the 1987; PubMed Scopus Google Scholar). were and maintained in of TIFF was isolated from cell that were at of and at in Triton X-100 was to a of and the was at for at The insoluble material was at and the was with at with and at The was in and at a ratio with at the of a and with of The gradients were at for at a The TIFF material at was In TIFF was isolated in gradients from the and TIFF from the gradients was with and by centrifugation at for at membranes were isolated the C.-H. Loomis W.F. J. Mol. Biol. PubMed Scopus Google Scholar). Triton X-100-insoluble contact regions were isolated to E.J. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). were with Triton X-100 at and at The was and in and on the of a of of and of in for centrifugation at for at The material at the was and in a The material was in of and on of of The was at for at at were were the acid protein proteins were and by for in and and separated in a gel Nature. PubMed Scopus Google Scholar). were detected and the were the protein by mass gel were and with The were the of Shevchenko A. M. M. Chem. 1996; Scopus Google Scholar). The were to and with a of acid at in and The were and to mass were a mass in the with laser and and of and were for The were to the and the on the for were including for mass of for protein mass of from molecular by and a of were at of for TIFF TIFF membranes were with C.-H. J. Biol. Chem. Full Text PDF PubMed Google Scholar) antibody Inc., in with at were with to at in were at were at with in several the were in in for at were with by and in were with a and with and to a Triton X-100 of cell on were to by the with and the on for and Triton X-100 was to a of the Triton X-100 was and the were with for on by at for were and for were at for in were and in of acid and for with cAMP Cell were and proteins in were by were with and to at for were by as previously A. A. J. Biol. Chem. 1999; 274: Full Text Full Text PDF PubMed Scopus Google Scholar). were with and with The was with of as The were in for at are into species by and they were after on a were for on and and as previously H. Siu C.-H. Dev. Biol. 1996; PubMed Scopus Google Scholar, H. E.F.S. Siu C.-H. J. Cell Biol. 1997; PubMed Scopus Google Scholar). were with gp80 porin, by at was with at microscopy was a with a and was maintained within the of the to filipin cells were on and in in for at were with filipin in for at and for were in for with cAMP Cell were and on in were to cells for at The were with of of for were at for by The cells were at after the of the molecules, cells were with Cell was as previously J. Siu C.-H. PubMed Scopus Google Scholar). the of on cell were by aggregate high were on and for in liquid at cell were and in the of filipin and digitonin were in to of were to Cell were in for at with was by for a at Cell was by cells with a and were as and the of cell was to the of cells at which was TIFF was isolated cells after of in liquid of material in a density TIFF a at the The that TIFF a This of TIFF protein from staining of TIFF proteins revealed a The were with by molecular mass in was mass spectrometry and and were identified to be expressed sequence tag actin, porin, comitin, and regulatory myosin light chain These proteins the mass of the the mass of is shown similar and on similar sequence with and the expected the of was to a was of the to the sequence of the the the the was to for similar proteins. The showed that the of of the CD36 the and was The of actin, porin, and comitin were confirmed by proteins anchored to the plasma membrane a lipid moiety are to be with TIFF (7Simons K. Ikonen E. Nature. 1997; 387: 569-572Crossref PubMed Scopus (8047) Google Scholar), cells with acid and proteins were enriched in the TIFF fraction. cells were into the Triton the Triton X-100-insoluble fraction after floatation and of protein from fraction were separated by and after TIFF was enriched with many proteins. Several species gel to actin, and suggesting that these proteins species were membrane insolubility in Triton X-100 is a of liquid-ordered membrane structure (1Brown D.A. London E. Annu. Rev. Cell Dev. Biol. 1998; 14: 111-136Crossref PubMed Scopus (2545) Google Scholar, 2Brown D.A. London E. J. Memb. Biol. 1998; 164: 103-114Crossref PubMed Scopus (833) Google Scholar, 3Hooper N.M. Mol. Membr. Biol. 1999; 16: 145-156Crossref PubMed Scopus (357) Google Scholar), expected Dictyostelium TIFF to be enriched in to in plasma membranes and TIFF were and TIFF a higher sterol and a higher than the plasma membrane. The elevated in TIFF for its density The sterol/phospholipid ratio in TIFF was higher than that of plasma membranes. The sterol species in TIFF were identified to be and on The species was for of the in Loomis W. The of Dictyostelium Academic Press, Inc., New Google Scholar). TIFF and plasma membranes similar sterol of Dictyostelium plasma membranes and the plasma for TIFF, are in in a The the plasma for TIFF, are in the of Triton X-100 on the plasma membrane of the of gp80 was was the TIFF protein and a plasma membrane on were with Triton X-100 and to staining with microscopy revealed a of gp80 staining the cell suggesting the of gp80-enriched vesicular on the plasma membrane The morphology of TIFF was by vesicles with from to were These membranes often to similar to those for the Triton X-100-insoluble contact regions E.J. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). The and were of other comitin showed with several protein were be detected and showed that the protein was enriched in TIFF of gp80 and showed the association of both proteins with the TIFF membranes and gp80 a which was a 10-fold of antibody was the membranes. gp80 is the protein in TIFF and Triton-insoluble gp80 of cellular was to gp80 with other TIFF components as in the plasma membrane of was the of gp80 on cells by antibody to the of other TIFF proteins. were induced to gp80 and revealed the of both and with gp80 and was also found to with gp80 caps and porin, F-actin, and comitin were membrane-associated components that be induced to with gp80 antibody cross-linking. In addition, of gp80 induced cell of revealed high levels of in the gp80-enriched TIFF membranes and The gp80 and was by gp80 on which were and with Filipin staining revealed a high of with gp80 caps and In to gp80 co-localization of with gp80 at cell-cell contacts was and by antibody cells were also with filipin with microscopy revealed high sterol levels at cell-cell contacts cells These that are enriched in cell-cell contact regions as as The of TIFF proteins in cells was by of gp80 and was at cell-cell contact regions A and staining for gp80 and also revealed co-localization at cell-cell contact regions and In addition, with its association H. D. A. B. M. A. R. J. Biol. Chem. 1992; Full Text PDF PubMed Google Scholar). was also with gp80 at cell-cell contact regions and In to contact regions, The Triton X-100-insoluble contact regions were also enriched in gp80 E.J. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar), suggesting that membrane fraction be to the properties and of these membrane contact regions were isolated from cell at of In to TIFF, the contact regions with the and a high density after the contact regions to a density and a and after centrifugation through a This density was similar to that of The protein of the contact regions was also similar to that of TIFF were from the with and by mass The proteins with the mass were with by molecular mass in The contact proteins and were identified as comitin, porin, actin, and were also shared the TIFF and contact showed that the isolated contact regions were also enriched in TIFF and Triton X-100-insoluble contact regions many the are with the In cholesterol is for the structural of TIFF T. Simons K. Cell Biol. 1997; PubMed Scopus Google Scholar). the that TIFF and cell-cell contacts are enriched in filipin and of digitonin are to within Dictyostelium plasma membranes C. A. J. Cell Sci. Google Scholar). these on the structural of cell were with digitonin filipin to Triton X-100 TIFF was to than of The of sterol sequestration on gp80-mediated cell-cell adhesion were also The cell adhesion sites by are during the of S.K. Siu C.-H. J. Biol. Chem. 1993; 268: 24902-24909Abstract Full Text PDF PubMed Google Scholar, C. Brar S.K. L. Siu C.-H. 1997; PubMed Scopus Google Scholar), and they can be by The adhesion sites and adhesion cells C. Dev. PubMed Scopus Google Scholar, C.-H. Dev. PubMed Scopus (37) Google Scholar, E. E. J. S. Proc. Natl. Acad. Sci. U. S. A. 1998; PubMed Scopus Google Scholar). cell-cell adhesion was the cell J. Siu C.-H. PubMed Scopus Google Scholar). cell was digitonin filipin a on cell similar have cellular and of vertebrate TIFF proteins R.G. Cell. 1992; 68: Full Text PDF PubMed Scopus Google Scholar, P. E. J. J. Cell Biol. PubMed Scopus Google Scholar), was that a was to perturbation of the adhesion by gp80. a cell was to the of cell to high and of development, cells were to high and revealed cell at both The in the cell at was to cell to the surface with development. that were and the of cells was was by The of cell with the of high levels of suggesting that cell-cell adhesion was by gp80. Cell of through the adhesion molecules, were to high and revealed cell at developmental the to was to with of filipin and of cells with filipin digitonin for to high levels of cell at sequestration is a of these that have cellular K. Rev. Mol. Cell. Biol. 2000; PubMed Scopus Google Scholar). for other such as the of cells were with Triton This on the of cell to filipin and digitonin similar to those with the with the that the of gp80 is to sterol We have isolated and characterized TIFF In many is similar to other floating protein components have in vertebrate such as actin, porin, and (8Anderson R.G. Annu. Rev. Biochem. 1998; 67: 199-225Crossref PubMed Scopus (1719) Google Scholar). Dictyostelium TIFF is enriched in gp80 of and as found in vertebrate TIFF (1Brown D.A. London E. Annu. Rev. Cell Dev. Biol. 1998; 14: 111-136Crossref PubMed Scopus (2545) Google Scholar, K. Ikonen E. Nature. 1997; 387: 569-572Crossref PubMed Scopus (8047) Google Scholar). TIFF has the vesicular TIFF morphology (4Brown D.A. Rose J.K. Cell. 1992; 68: 533-544Abstract Full Text PDF PubMed Scopus (2604) Google Scholar, 5Sargiacomo M. Sudol M. Tang Z. Lisanti M.P. J. Cell Biol. 1993; 122: 789-807Crossref PubMed Scopus (860) Google Scholar, 6Kubler E. Dohlman H.G. Lisanti M.P. J. Biol. Chem. 1996; 271: 32975-32980Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar). levels of cholesterol and have been found in TIFF (4Brown D.A. Rose J.K. Cell. 1992; 68: 533-544Abstract Full Text PDF PubMed Scopus (2604) Google E. Dohlman H.G. Lisanti M.P. J. Biol. Chem. 1996; 271: 32975-32980Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar, A. Neutz S. Simons K. Eaton S. J. Biol. Chem. 1999; 274: 12049-12054Abstract Full Text Full Text PDF PubMed Scopus (242) Google Scholar). Dictyostelium cells primarily and the sterol ofDictyostelium TIFF is higher than that of plasma membranes. of Dictyostelium TIFF is its high sterol/phospholipid ratio in with vertebrate TIFF (4Brown D.A. Rose J.K. Cell. 1992; 68: 533-544Abstract Full Text PDF PubMed Scopus (2604) Google Scholar) and Drosophila TIFF A. Neutz S. Simons K. Eaton S. J. Biol. Chem. 1999; 274: 12049-12054Abstract Full Text Full Text PDF PubMed Scopus (242) Google Scholar). The ofDictyostelium are also (11Xiao Z. Devreotes P.N. Mol. Biol. Cell. 1997; 8: 855-869Crossref PubMed Scopus (37) Google Scholar). These high sterol levels be to the high of acid in Dictyostelium Loomis W. The of Dictyostelium Academic Press, Inc., New Google Scholar). The acyl to the liquid-ordered membrane structure expected for TIFF and CHIFF, they membrane at the Dictyostelium of These lipid of the bulk plasma membrane the floating have on the structure and of the in Dictyostelium membranes. TIFF and have a similar lipid these proteins. The cAMP receptor is the protein in CHIFF, was from TIFF, and the is for the cell adhesion molecule gp80 (11Xiao Z. Devreotes P.N. Mol. Biol. Cell. 1997; 8: 855-869Crossref PubMed Scopus (37) Google Scholar). gp80 and also display during cell gp80 in cell-cell contact regions H. Siu C.-H. Dev. Biol. 1996; PubMed Scopus Google Scholar), with other TIFF proteins and is the plasma membrane Z. Devreotes P.N. J. Cell Biol. 1997; PubMed Scopus Google Scholar). the Dictyostelium plasma membrane be as a of with specialized functions. of have been shown to within the plasma membranes of vertebrate cells A. K. S. R. J. 1999; PubMed Scopus Google Scholar, K. D. Cell Biol. 2000; PubMed Scopus Google Scholar). This of specialized membrane components cells to and to Several of that TIFF components membrane that are involved in gp80-mediated adhesion. gp80 with TIFF proteins and in membrane involved in cell-cell contact that TIFF components are to gp80. TIFF many properties with the Triton-insoluble contact regions E.J. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). sterol sequestration TIFF and TIFF properties the cell-cell by adhesion is adhesion to that are with the cell adhesion molecules, can with proteins that to the Cell. 1996; Full Text Full Text PDF PubMed Scopus Google Scholar, B. Cell Biol. 1997; PubMed Scopus Google Scholar, Cell Biol. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). In adhesion to the However, TIFF membranes a lipid for the of both and proteins. a membrane of liquid-ordered adhesion by both adhesion and interactions with the have that gp80-mediated contacts membrane which are enriched in and with the Moreover, found that the Triton-insoluble contact regions were cytoskeleton-associated of that sterol sequestration gp80-mediated adhesion by liquid-ordered membrane within gp80 adhesion We have TIFF components to membrane involved in cell-cell contact However, TIFF can also be from plasma membrane microdomains (7Simons K. Ikonen E. Nature. 1997; 387: 569-572Crossref PubMed Scopus (8047) Google Scholar, K. Rev. Mol. Cell. Biol. 2000; PubMed Scopus Google Scholar). is that gp80 adhesion from In microscopy have revealed gp80 on cells H. H. R. Cell PubMed Scopus Google Scholar). and to to vertebrate R. S. Nature. 1998; PubMed Scopus Google Scholar, A. P. Simons K. J. Cell Biol. 2000; PubMed Scopus Google Scholar). is that gp80 within on the cell surface to cell-cell be for adhesion of components within and interactions gp80 the to the of a cell adhesion A variety of molecular cell-cell adhesion. adhesion by adhesion molecules, such as is to the lipid vertebrate cell adhesion are including P. Cell Biol. PubMed Scopus Google Scholar), B. Full Text PDF PubMed Scopus Google Scholar), H. K. M. K. J. 1996; PubMed Scopus Google Scholar), P. Nature. 1987; PubMed Scopus Google Scholar), and of the T. J. 1996; 16: PubMed Google Scholar, S. H. M. K. Y. Y. S. J. Biol. Chem. 1999; 274: Full Text Full Text PDF PubMed Scopus Google Scholar). In several cell adhesion have been found in TIFF S. C. M. J. PubMed Scopus Google Scholar, M.P. 1998; PubMed Scopus (70) Google Scholar, J. E. B. J. Biol. Chem. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar). We have demonstrated a role for TIFF in gp80-mediated adhesion that involve lipid and be of to TIFF is involved in adhesion by other adhesion Moreover, adhesion from TIFF display and such signaling and regulatory TIFF interactions that gp80 to the are We M. and R. for and for the of and for We also and of the of the of of for with and

Fetched live from OpenAlex and de-inverted. Abstracts are not stored in this database: the inverted indexes are 8.6 GB of the frame’s 9.3 GB of text, and the host has 13 GB free.