FcεRI and Thy-1 domains have unique protein and lipid compositions

Journal of Lipid Research

Volumn 48, Issue 6, 2007, Pages 1325-1335

  Surviladze, Zurab ^a   Harrison, Kathleen A ^b   Murphy, Robert C ^b   Wilson, Bridget S ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Glycerophosphoinositol anchored proteins; Immunoglobulin E receptor; Lipid rafts; Lipidomics; Membrane microdomains

Indexed keywords

CHOLESTEROL; FATTY ACID DERIVATIVE; GLYCEROPHOSPHOETHANOLAMINE; GLYCEROPHOSPHORYLCHOLINE; IMMUNOGLOBULIN E RECEPTOR; IMMUNOGLOBULIN FC FRAGMENT; MEMBRANE PROTEIN; PHOSPHOLIPID; PHOSPHOSERINE; PROTEIN THY 1; SPHINGOMYELIN; UNCLASSIFIED DRUG; DRUG DERIVATIVE; GLYCEROPHOSPHORYLSERINE; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE LIPID; PHOSPHATIDYLETHANOLAMINE; THY 1 ANTIGEN;

ANIMAL CELL; ARTICLE; ELECTROSPRAY MASS SPECTROMETRY; LIPID COMPOSITION; NEGATIVE ION ELECTROSPRAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CONTENT; RAT; ANIMAL; CELL MEMBRANE; CHEMISTRY; COMET ASSAY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOMAGNETIC SEPARATION; METABOLISM; TUMOR CELL LINE;

ANIMALS; ANTIGENS, THY-1; CELL LINE, TUMOR; CELL MEMBRANE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMET ASSAY; GLYCERYLPHOSPHORYLCHOLINE; GLYCOSYLPHOSPHATIDYLINOSITOLS; IMMUNOMAGNETIC SEPARATION; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; PHOSPHATIDYLETHANOLAMINES; PHOSPHOSERINE; RECEPTORS, IGE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPHINGOMYELINS;

EID: 34548161721     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M600485-JLR200     Document Type: Article

References (56)

1. Melkonian, K. A., T. Chu, L. B. Tortorella, and D. A. Brown. 1995. Characterization of proteins in detergent-resistant membrane complexes from Madin-Darby canine kidney epithelial cells. Biochemistry. 34: 16161-16170.
2. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387: 569-572.
3. Bhatnager, R. S., and J. I. Gordon. 1997. Understanding covalent modifications of proteins by lipids: where cell biology and biophysics mingle. Trends Cell Biol. 7: 14-20.
4. Ilangumaran, S., S. Arni, G. van Echten-Deckert, B. Borisch, and D. C. Hoessli. 1999. Microdomain-dependent regulation of Lck and Fyn protein-tyrosine kinases in T lymphocyte plasma membranes. Mol. Biol. Cell. 10: 891-905.
5. Janes, P. W., S. C. Ley, and A. I. Magee. 1999. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147: 447-461.
6. Zhang, W., R. Treble, and L. E. Samelson. 1999. Essential role of LAT in T cell development. Immunity. 9: 239-246.
7. Moffett, S., D. A. Brown, and M. E. Linder. 2000. Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 275: 2191-2198.
8. Brown, D. A., and J. K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68: 533-544.
9. Horejsi, V., K. Drbal, M. Cebecauer, J. Cerny, T. Brdicka, P. Angelisova, and H. Stockinger. 1999. GPI-microdomains: a role in signalling via immunoreceptors. Immunol. Today. 20: 356-361.
10. Field, K. A., D. Holowka, and B. Baird. 1995. FcεRI-mediated recruitment of p53/56(lyn) to detergent-resistant membrane domains accompanies cellular signaling. Proc. Natl. Acad. Sci. USA. 92: 9201-9205.
11. Montixi, C., C. Langlet, A. M. Bernard, J. Thimonier, C. Dubois, M. A. Wurbel, J. P. Chauvin, M. Pierres, and H. T. He. 1998. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17: 5334-5348.
12. Cheng, P. C., A. Cherukuri, M. Dykstra, S. Malapati, T. Sproul, M. R. Chen, and S. K. Pierce. 2001. Floating the raft hypothesis: the roles of lipid rafts in B cell antigen receptor function. Semin. Immunol. 13: 107-114.
13. Guo, B. C., R. M. Kato, M. Garcia-Lloret, M. I. Wahl, and D. J. Rawlings. 2000. Engagement of the human pre-B cell receptor generates a lipid raft-dependent calcium signaling complex. Immunity. 13: 2243-2253.
14. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1: 31-40.
15. Edidin, M. 2003. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Mol. Struct. 32: 257-283.
16. Shogomori, H., and D. A. Brown. 2003. Use of detergents to study membrane rafts: the good, the bad, and the ugly. Biol. Chem. 384: 1259-1263.
17. Mayor, S., and F. R. Maxfield. 1995. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol. Biol. Cell. 6: 929-944.
18. Field, K. A., D. Holowka, and B. Baird. 1999. Structural aspects of the association of FceRI with detergent-resistant membranes. J. Biol. Chem. 274: 1753-1758.
19. Parolini, I., S. Topa, M. Sorice, A. Pace, P. Ceddia, F. Montesoro, A. Pavan, M. P. Linasanti, C. Peschle, and M. Sargiacomo. 1999. Phorbol ester-induced disruption of the CD4-Lck complex occurs within a detergent-resistant microdomain of the plasma membrane - involvement of the translocation of activated protein kinase C isoforms. J. Biol. Chem. 20: 14176-14187.
20. Surviladze, Z., L. Dráberová, L. Kubínová, and P. Dráber. 1998. Functional heterogeneity of Thy-1 membrane microdomains in rat basophilic leukemia cells. Eur. J. Immunol. 28: 1847-1858.
21. Madore, N., K. L. Smith, C. H. Graham, A. Jen, K. Brady, S. Hall, and R. Morris. 1999. Functionally different GPI proteins are organized in different domains on the neuronal surface. EMBO J. 18: 6917-6926.
22. Surviladze, Z., L. Dráberova, M. Kovářová, M. Bouceik, and P. Dráber. 2001. Differential sensitivity to acute cholesterol lowering of activation mediated via the high-affinity IgE receptor and Thy-1 glycoprotein. Eur. J. Immunol. 31: 1-10.
23. Macdonald, J. L., and L. J. Pike. 2005. A simplified method for the preparation of detergent-free lipid rafts. J. Lipid Res. 46: 11061-11067.
24. Lagerholm, B. C., G. E. Weinreb, K. Jacobson, and N. L. Thompson. 2005. Detecting microdomains in intact cell membranes. Annu. Rev. Phys. Chem. 56: 309-336.
25. Friedrichson, T., and T. Kurzhalia. 1998. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature. 394: 802-805.
26. Varma, R., and S. Mayor. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature. 394: 798-801.
27. Dietrich, C., B. Yang, T. Fujiwara, A. Kusumi, and K. Jacobson. 2002. Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys. J. 82: 274-284.
28. Bacia, K., I. V. Majoul, and P. Schwille. 2002. Probing the endocytic pathway in live cells using dual-color fluorescence cross-correlation analysis. Biophys. J. 83: 1184-1193.
29. Fujiwara, T., K. Ritchie, H. Murakoshi, K. Jacobson, and A. Kusumi. 2002. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157: 1071-1081.
30. Kenworthy, A. K., B. J. Nichols, C. L. Remmert, G. M. Hendrix, M. Kumar, J. Zimmerberg, and J. Lippincott-Schwartz. 2004. Dynamics of putative raft-associated proteins at the cell surface. J. Cell Biol. 165: 735-746.
31. Vereb, G., J. Szöllosi, J. Matko, P. Nagy, T. Farkas, L. Vigh, L. Matyus, T. A. Waldmann, and S. Damjanovich. 2003. Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model. Proc. Natl. Acad. Sci. USA. 100: 8053-8058.
32. Pike, L. J. 2006. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 47: 1597-1598.
33. Sanan, D. A., and R. G. W. Anderson. 1991. Simultaneous visualization of LDL receptor distribution and clathrin lattices on membranes torn from the upper surface of cultured cells. J. Histochem. Cytochem. 39: 1017-1024.
34. Wilson, B. S., S. L. Steinberg, K. Liederman, J. R. Pfeiffer, Z. Surviladze, J. Zhang, L. E. Samelson, L. H. Yang, P. B. Kotula, and J. M. Oliver. 2004. Markers for detergent-resistant lipid rafts occupy distinct and dynamic domains in native membranes. Mol. Biol. Cell. 15: 2580-2592.
35. Wilson, B. S., J. R. Pfeiffer, and J. M. Oliver. 2000. Observing FcεRI signalling from the inside of the mast cell membrane. J. Cell Biol. 149: 1131-1142.
36. Wilson, B. S., J. R. Pfeiffer, Z. Surviladze, E. A. Gaudet, and J. M. Oliver. 2001. High resolution mapping reveals distinct FcεRI and LAT domains in activated mast cells. J. Cell Biol. 154: 645-658.
37. Harder, T., P. Scheiffele, P. Verkade, and K. Simons. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141: 929-942.
38. Fridriksson, E. K., P. A. Shipkova, E. D. Sheets, D. Holowka, B. Baird, and F. W. McLafferty. 1999. Quantitative analysis of phospholipids in functionally important membrane domains from RBL-2H3 mast cells using tandem high-resolution mass spectrometry. Biochemistry. 38: 8056-8063.
39. Pike, L. J., X. L. Han, and R. W. Gross. 2005. Epidermal growth factor receptors are localized to lipid rafts that contain a balance of inner and outer leaflet lipids. A shotgun lipidomics study. J. Biol. Chem. 280: 26796-26804.
40. Clay, K. L. 1990. Quantitation of platelet-activating factor by gas chromatography-mass spectrometry. Methods Enzymol. 187: 134-142.
41. Hadley, J. S., A. Fradin, and R. C. Murphy. 1988. Electron capture negative ion chemical ionization analysis of arachidonic acid. Biomed. Environ. Mass Spectrom. 15: 175-178.
42. Pulfer, M., and R. C. Murphy. 2003. Electrospray mass spectrometry of phospholipids. Mass Spectrom. Rev. 22: 332-364.
43. Kayganich, K., and R. C. Murphy. 1992. Fast atom bombardment tandem mass spectrometric identification of diacyl, alkylacyl, and alk-1-enylacyl molecular-species of glycerophosphoethanolamine in human polymorphonuclear leukocytes. Anal. Chem. 64: 2965-2971.
44. Zemski Berry, K. A., and R. C. Murphy. 2005. Analysis of cell membrane aminophospholipids as isotope-tagged derivatives. J. Lipid Res. 46: 1038-1046.
45. Harder, T., and M. Kunh. 2000. Selective accumulation of raft-associated membrane protein LAT in T cell receptor signaling assemblies. J. Cell Biol. 151: 199-207.
46. Saucan, L., and G. E. Palade. 1994. Membrane and secretory proteins are transported from the Golgi complex to the sinusoidal plasmalemma of hepatocytes by distinct vesicular carriers. J. Cell Biol. 125: 733-741.
47. van Meer, G. 2005. Cellular lipidomics. EMBO J. 24: 3159-3165.
48. London, E. 2002. Insights into lipid raft structure and formation from experiments inmodelmembranes. Curr. Opin. Struct. Biol. 12: 480-486.
49. Schwartz, A., L. Jurgens, A. Licht, H. Schneider, A. H. Futerman, and I. Pecht. 2000. An IgE-dependent secretory response of mast cells can be induced by a glycosphingolipid-specific monoclonal antibody. Eur. J. Immunol. 30: 217-226.
50. Rivnay, B., and G. Fischer. 1986. Phospholipid distribution in the microenvironment of the immunoglobulin E-receptor from rat basophilic leukemia cell membrane. Biochemistry. 25: 5686-5693.
51. Simons, K., and E. Ikonen. 2000. Cell biology. How cells handle cholesterol. Science. 290: 1721-1726.
52. Brugger, B., C. Grahma, I. Leibrecht, E. Monbelli, A. Jen, F. Wieland, and R. Morris. 2004. The membrane domains occupied by glycosylphosphatidylinositol-anchored prion protein and Thy-1 differ in lipid composition. J. Biol. Chem. 279: 7530-7536.
53. Anderson, R. G. W., and K. Jacobson. 2002. Cell biology. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science. 296: 1821-1825.
54. Gillooly, D. J., and H. Stenmark. 2001. Cell biology. A lipid oils the endocytosis machine. Science. 291: 993-994.
55. Ivanova, P., B. A. Cerda, D. A. Horn, J. S. Cohen, F. W. McLafferty, and H. A. Brown. 2001. Electrospray ionization mass spectrometry analysis of changes in phospholipids in RBL-2H3 mastocytoma cells during degranulation. Proc. Natl. Acad. Sci. USA. 98: 7152-7157.
56. Forrester, J. S., S. B. Milne, P. T. Ivanova, and H. A. Brown. 2004. Computational lipidomics: a multiplexed analysis of dynamic changes in membrane lipid composition during signal transduction. Mol. Pharmacol. 66: 813-821.