Temporal proteomics profiling of lipid rafts in CCR6-activated T cells reveals the integration of actin cytoskeleton dynamics

Journal of Proteome Research

Volumn 9, Issue 1, 2010, Pages 283-297

  Lin, Shu Ling ^a   Chien, Chih Wei ^b   Han, Chia Li ^c   Chen, Eric S W ^a   Kao, Shao Hsuan ^a   Chen, Yu Ju ^c   Liao, Fang ^a  

^a INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c INSTITUTE OF CHEMISTRY   (Taiwan)

Author keywords

CCR6; G protein coupled receptors; Gel assisted digestion; iTRAQ; Lipid raft proteome; Mass spectrometry; T cells

Indexed keywords

ACTIN; CHEMOKINE; CHEMOKINE RECEPTOR CCR6; CHOLESTEROL; G PROTEIN COUPLED RECEPTOR; SMALL INTERFERING RNA; SPHINGOLIPID;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HUMAN CELL; INFECTION; INFLAMMATION; LEUKOCYTE MIGRATION; LIPID RAFT; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEOMICS; QUANTITATIVE ANALYSIS; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; WESTERN BLOTTING;

ACTINS; BLOTTING, WESTERN; CHEMOKINE CCL20; CHEMOTAXIS; CYTOSKELETON; HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; JURKAT CELLS; MEMBRANE MICRODOMAINS; MICROFILAMENT PROTEINS; PROTEOMICS; RECEPTORS, CCR6; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TANDEM MASS SPECTROMETRY;

EID: 73649084806     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr9006156     Document Type: Article

References (88)

1. Rollins, B. J. Chemokines. Blood 1997, 90 (3), 909-928.
2. Baggiolini, M. Chemokines in pathology and medicine. J. Intern. Med. 2001, 250 (2), 91-104.
3. Murphy, P. M.; Baggiolini, M.; Charo, I. F.; Hebert, C. A.; Horuk, R.; Matsushima, K.; Miller, L. H.; Oppenheim, J. J.; Power, C. A. International union of pharmacology. Pharmacol. Rev. 2000, 52 (1), 145-176.
4. Liao, F.; Alderson, R.; Su, J.; Ullrich, S. J.; Kreider, B. L.; Farber, J. M. STRL22 is a receptor for the CC chemokine MIP-3alpha. Biochem. Biophys. Res. Commun. 1997, 236 (1), 212-7.
5. Baba, M.; Imai, T.; Nishimura, M.; Kakizaki, M.; Takagi, S.; Hieshima, K.; Nimiyama, H.; Yoshie, O. Identification of CCR6, the specific receptor for a novel lymphocyte-directed CC chemokine LARC. J. Biol. Chem. 1997, 272, 14893-14898.
6. Power, C. A.; Church, D. J.; Meyer, A.; Alouani, S.; Proudfoot, A. E.; Clark-Lewis, I.; Sozzani, S.; Mantovani, A.; Wells, T. N. Cloning and characterization of a specific receptor for the novel CC chemokine MIP-3alpha from lung dendritic cells. J. Exp. Med. 1997, 186 (6), 825-835.
7. Greaves, D. R.; Wang, W.; Dairaghi, D. J.; Dieu, M. C.; Saint-Vis, B.; Franz-Bacon, K.; Rossi, D.; Caux, C.; McClanahan, T.; Gordon, S.; Zlotnik, A.; Schall, T. J. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3alpha and is highly expressed in human dendritic cells. J. Exp. Med. 1997, 186 (6), 837-844.
8. Dieu, M. C.; Vanbervliet, B.; Vicari, A.; Bridon, J. M.; Oldham, E.; Ait-Yahia, S.; Briere, F.; Zlotnik, A.; Lebecque, S.; Caux, C. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 1998, 188 (2), 373-386.
9. Liao, F.; Rabin, R. L.; Smith, C. S.; Sharma, G.; Nutman, T. B.; Farber, J. M. CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3 alpha. J. Immunol. 1999, 162 (1), 186-194.
10. Liao, F.; Lee, H.-H.; Farber, J. M. Cloning of STRL22, a new human gene encoding a G protein-coupled receptor related to chemokine receptors and located on chromosome 6q27. Genomics 1997, 40, 175-180.
11. Schutyser, E.; Struyf, S.; Van Damme, J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 2003, 14 (5), 409-426.
12. Williams, I. R. CCR6 and CCL20: partners in intestinal immunity and lymphorganogenesis. Ann. N.Y. Acad. Sci. 2006, 1072, 52-61.
13. Annunziato, F.; Cosmi, L.; Santarlasci, V.; Maggi, L.; Liotta, F.; Mazzinghi, B.; Parente, E.; Fili, L.; Ferri, S.; Frosali, F.; Giudici, F.; Romagnani, P.; Parronchi, P.; Tonelli, F.; Maggi, E.; Romagnani, S. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 2007, 204 (8), 1849-1861.
14. Singh, S. P.; Zhang, H. H.; Foley, J. F.; Hedrick, M. N.; Farber, J. M. Human T cells that are able to produce IL-17 express the chemokine receptor CCR6. J. Immunol. 2008, 180 (1), 214-221.
15. Acosta-Rodriguez, E. V.; Rivino, L.; Geginat, J.; Jarrossay, D.; Gattorno, M.; Lanzavecchia, A.; Sallusto, F.; Napolitani, G. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 2007, 8 (6), 639-646.
16. Liao, F.; Shirakawa, A. K.; Foley, J. F.; Rabin, R. L.; Farber, J. M. Human B cells become highly responsive to macrophage-inflammatory protein-3 alpha/CC chemokine ligand-20 after cellular activation without changes in CCR6 expression or ligand binding. J. Immunol. 2002, 168 (10), 4871-4880.
17. Ai, L. S.; Liao, F. Mutating the four extracellular cysteines in the chemokine receptor CCR6 reveals their differing roles in receptor trafficking, ligand binding, and signaling. Biochemistry 2002, 41 (26), 8332-8341.
18. Ai, L. S.; Lee, S. F.; Chen, S. S.; Liao, F. Molecular characterization of CCR6: involvement of multiple domains in ligand binding and receptor signaling. J. Biomed. Sci. 2004, 11 (6), 818-828.
19. Simons, K.; Ikonen, E. Functional rafts in cell membranes. Nature 1997, 387 (6633), 569-572.
20. Brown, D. A.; London, E. Structure and origin of ordered lipid domains in biological membranes. J. Membr. Biol. 1998, 164 (2), 103-114.
21. Lagerholm, B. C.; Weinreb, G. E.; Jacobson, K.; Thompson, N. L. Detecting microdomains in intact cell membranes. Annu. Rev. Phys. Chem. 2005, 56, 309-336.
22. Brown, D. A. Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 2006, 21, 430-439.
23. Kenworthy, A. K. Have we become overly reliant on lipid rafts? Talking Point on the involvement of lipid rafts in T-cell activation. EMBO Rep. 2008, 9 (6), 531-535.
24. Zech, T.; Ejsing, C. S.; Gaus, K.; de Wet, B.; Shevchenko, A.; Simons, K.; Harder, T. Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signalling. EMBO J. 2009, 28 (5), 466-476.
25. Simons, K.; Toomre, D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 2000, 1 (1), 31-39.
26. Nguyen, D. H.; Taub, D. CXCR4 function requires membrane cholesterol: implications for HIV infection. J. Immunol. 2002, 168 (8), 4121-4126.
27. Nguyen, D. H.; Taub, D. Cholesterol is essential for macrophage inflammatory protein 1 beta binding and conformational integrity of CC chemokine receptor 5. Blood 2002, 99 (12), 4298-4306.
28. Gomez-Mouton, C.; Lacalle, R. A.; Mira, E.; Jimenez-Baranda, S.; Barber, D. F.; Carrera, A. C.; Martinez, A. C.; Manes, S. Dynamic redistribution of raft domains as an organizing platform for signaling during cell chemotaxis. J. Cell Biol. 2004, 164 (5), 759-768.
29. Jiao, X.; Zhang, N.; Xu, X.; Oppenheim, J. J.; Jin, T. Ligand-induced partitioning of human CXCR1 chemokine receptors with lipid raft microenvironments facilitates G-protein-dependent signaling. Mol. Cell. Biol. 2005, 25 (13), 5752-5762.
30. von Haller, P. D.; Donohoe, S.; Goodlett, D. R.; Aebersold, R.; Watts, J. D. Mass spectrometric characterization of proteins extracted from Jurkat T cell detergent-resistant membrane domains. Proteomics 2001, 1 (8), 1010-1021.
31. Bini, L.; Pacini, S.; Liberatori, S.; Valensin, S.; Pellegrini, M.; Raggiaschi, R.; Pallini, V.; Baldari, C. T. Extensive temporally regulated reorganization of the lipid raft proteome following T-cell antigen receptor triggering. Biochem. J. 2003, 369 (Pt 2), 301-309.
32. Mielenz, D.; Vettermann, C.; Hampel, M.; Lang, C.; Avramidou, A.; Karas, M.; Jack, H. M. Lipid rafts associate with intracellular B cell receptors and exhibit a B cell stage-specific protein composition. J. Immunol. 2005, 174 (6), 3508-3517.
33. Kobayashi, M.; Katagiri, T.; Kosako, H.; Iida, N.; Hattori, S. Global analysis of dynamic changes in lipid raft proteins during T-cell activation. Electrophoresis 2007, 28 (12), 2035-2043.
34. MacLellan, D. L.; Steen, H.; Adam, R. M.; Garlick, M.; Zurakowski, D.; Gygi, S. P.; Freeman, M. R.; Solomon, K. R. A quantitative proteomic analysis of growth factor-induced compositional changes in lipid rafts of human smooth muscle cells. Proteomics 2005, 5 (18), 4733-4742.
35. Gupta, N.; Wollscheid, B.; Watts, J. D.; Scheer, B.; Aebersold, R.; DeFranco, A. L. Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat. Immunol. 2006, 7 (6), 625-633.
36. Guo, Y.; Singleton, P. A.; Rowshan, A.; Gucek, M.; Cole, R. N.; Graham, D. R.; Van Eyk, J. E.; Garcia, J. G. Quantitative proteomics analysis of human endothelial cell membrane rafts: evidence of MARCKS and MRP regulation in the sphingosine 1-phosphate-induced barrier enhancement. Mol. Cell. Proteomics 2007, 6 (4), 689-696.
37. Mannova, P.; Fang, R.; Wang, H.; Deng, B.; McIntosh, M. W.; Hanash, S. M.; Beretta, L. Modification of host lipid raft proteome upon hepatitis C virus replication. Mol. Cell. Proteomics 2006, 5 (12), 2319-2325.
38. Foster, L. J.; De Hoog, C. L.; Mann, M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (10), 5813-5818.
39. Han, C. L.; Chien, C. W.; Chen, W. C.; Chen, Y. R.; Wu, C. P.; Li, H.; Chen, Y. J. A multiplexed quantitative strategy for membrane proteomics: opportunities for mining therapeutic targets for autosomal dominant polycystic kidney disease. Mol. Cell. Proteomics 2008, 7 (10), 1983-1997.
40. Kersey, P. J.; Duarte, J.; Williams, A.; Karavidopoulou, Y.; Birney, E.; Apweiler, R. The International Protein Index: an integrated database for proteomics experiments. Proteomics 2004, 4 (7), 1985-1988.
41. Lin, W. T.; Hung, W. N.; Yian, Y. H.; Wu, K. P.; Han, C. L.; Chen, Y. R.; Chen, Y. J.; Sung, T. Y.; Hsu, W. L. Multi-Q: a fully automated tool for multiplexed protein quantitation. J. Proteome Res. 2006, 5 (9), 2328-2338.
42. Brown, D. A.; London, E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 1998, 14, 111-136.
43. DeSouza, L. V.; Taylor, A. M.; Li, W.; Minkoff, M. S.; Romaschin, A. D.; Colgan, T. J.; Siu, K. W. Multiple reaction monitoring of mTRAQ-labeled peptides enables absolute quantification of endogenous levels of a potential cancer marker in cancerous and normal endometrial tissues. J. Proteome Res. 2008, 7 (8), 3525-3534.
44. Suzuki, K.; Nishihata, J.; Arai, Y.; Honma, N.; Yamamoto, K.; Irimura, T.; Toyoshima, S. Molecular cloning of a novel actin-binding protein, p57, with a WD repeat and a leucine zipper motif. FEBS Lett. 1995, 364 (3), 283-288.
45. Foger, N.; Rangell, L.; Danilenko, D. M.; Chan, A. C. Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science 2006, 313 (5788), 839-842.
46. Shiow, L. R.; Roadcap, D. W.; Paris, K.; Watson, S. R.; Grigorova, I. L.; Lebet, T.; An, J.; Xu, Y.; Jenne, C. N.; Foger, N.; Sorensen, R. U.; Goodnow, C. C.; Bear, J. E.; Puck, J. M.; Cyster, J. G. The actin regulator coronin 1A is mutant in a thymic egress-deficient mouse strain and in a patient with severe combined immunodeficiency. Nat. Immunol. 2008, 9 (11), 1307-1315.
47. Mugnier, B.; Nal, B.; Verthuy, C.; Boyer, C.; Lam, D.; Chasson, L.; Nieoullon, V.; Chazal, G.; Guo, X. J.; He, H. T.; Rueff-Juy, D.; Alcover, A.; Ferrier, P. Coronin-1A links cytoskeleton dynamics to TCR alpha beta-induced cell signaling. PLoS One 2008, 3 (10), e3467.
48. Goldstein, D.; Djeu, J.; Latter, G.; Burbeck, S.; Leavitt, J. Abundant synthesis of the transformation-induced protein of neoplastic human fibroblasts, plastin, in normal lymphocytes. Cancer Res. 1985, 45 (11 Pt 2), 5643-5647.
49. Pearl, L. H.; Prodromou, C. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 2006, 75, 271-94.
50. Zhao, R.; Houry, W. A. Molecular interaction network of the Hsp90 chaperone system. Adv. Exp. Med. Biol. 2007, 594, 27-36.
51. Pai, K. S.; Mahajan, V. B.; Lau, A.; Cunningham, D. D. Thrombin receptor signaling to cytoskeleton requires Hsp90. J. Biol. Chem. 2001, 276 (35), 32642-32647.
52. Shinozaki, F.; Minami, M.; Chiba, T.; Suzuki, M.; Yoshimatsu, K.; Ichikawa, Y.; Terasawa, K.; Emori, Y.; Matsumoto, K.; Kurosaki, T.; Nakai, A.; Tanaka, K.; Minami, Y. Depletion of hsp90beta induces multiple defects in B cell receptor signaling. J. Biol. Chem. 2006, 281 (24), 16361-16369.
53. He, F.; Qiao, Z. H.; Cai, J.; Pierce, W.; He, D. C.; Song, Z. H. Involvement of the 90-kDa heat shock protein (Hsp-90) in CB2 cannabinoid receptor-mediated cell migration: a new role of Hsp-90 in migration signaling of a G protein-coupled receptor. Mol. Pharmacol. 2007, 72 (5), 1289-1300.
54. Sidera, K.; Samiotaki, M.; Yfanti, E.; Panayotou, G.; Patsavoudi, E. Involvement of cell surface HSP90 in cell migration reveals a novel role in the developing nervous system. J. Biol. Chem. 2004, 279 (44), 45379-45388.
55. Pratt, W. B. The role of the hsp90-based chaperone system in signal transduction by nuclear receptors and receptors signaling via MAP kinase. Annu. Rev. Pharmacol. Toxicol. 1997, 37, 297-326.
56. Gaestel, M. Molecular chaperones in signal transduction. Handb. Exp. Pharmacol. 2006, (172), 93-109.
57. Stebbins, C. E.; Russo, A. A.; Schneider, C.; Rosen, N.; Hartl, F. U.; Pavletich, N. P. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 1997, 89 (2), 239-250.
58. Uehara, Y. Natural product origins of Hsp90 inhibitors. Curr. Cancer Drug Targets 2003, 3 (5), 325-330.
59. Yu, H.; Wakim, B.; Li, M.; Halligan, B.; Tint, G. S.; Patel, S. B. Quantifying raft proteins in neonatal mouse brain by 'tube-gel' protein digestion label-free shotgun proteomics. Proteome Sci. 2007, 5, 17.
60. Pollard, T. D.; Borisy, G. G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003, 112 (4), 453-465.
61. Svitkina, T. M.; Borisy, G. G. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 1999, 145 (5), 1009-1026.
62. Manes, S.; Viola, A. Lipid rafts in lymphocyte activation and migration. Mol. Membr. Biol. 2006, 23 (1), 59-69.
63. Galkin, V. E.; Orlova, A.; Brieher, W.; Kueh, H. Y.; Mitchison, T. J.; Egelman, E. H. Coronin-1A stabilizes F-actin by bridging adjacent actin protomers and stapling opposite strands of the actin filament. J. Mol. Biol. 2008, 376 (3), 607-613.
64. Cai, L.; Marshall, T. W.; Uetrecht, A. C.; Schafer, D. A.; Bear, J. E. Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell 2007, 128 (5), 915-929.
65. Kato, A.; Kurita, S.; Hayashi, A.; Kaji, N.; Ohashi, K.; Mizuno, K. Critical roles of actin-interacting protein 1 in cytokinesis and chemotactic migration of mammalian cells. Biochem. J. 2008, 414 (2), 261-270.
66. Rot, A.; von Andrian, U. H. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 2004, 22, 891-928.
67. Thelen, M.; Stein, J. V. How chemokines invite leukocytes to dance. Nat. Immunol. 2008, 9 (9), 953-959.
68. Viola, A.; Gupta, N. Tether and trap: regulation of membrane-raft dynamics by actin-binding proteins. Nat. Rev. Immunol. 2007, 7 (11), 889-896.
69. Lin, C. S.; Aebersold, R. H.; Kent, S. B.; Varma, M.; Leavitt, J. Molecular cloning and characterization of plastin, a human leukocyte protein expressed in transformed human fibroblasts. Mol. Cell. Biol. 1988, 8 (11), 4659-4668.
70. Jones, S. L.; Brown, E. J. FcgammaRII-mediated adhesion and phagocytosis induce L-plastin phosphorylation in human neutrophils. J. Biol. Chem. 1996, 271 (24), 14623-14630.
71. Jones, S. L.; Wang, J.; Turck, C. W.; Brown, E. J. A role for the actin-bundling protein L-plastin in the regulation of leukocyte integrin function. Proc. Natl. Acad. Sci. U.S.A. 1998, 95 (16), 9331-9336.
72. Paclet, M. H.; Davis, C.; Kotsonis, P.; Godovac-Zimmermann, J.; Segal, A. W.; Dekker, L. V. N-Formyl peptide receptor subtypes in human neutrophils activate L-plastin phosphorylation through different signal transduction intermediates. Biochem. J. 2004, 377 (Pt 2), 469-477.
73. Park, S. J.; Suetsugu, S.; Takenawa, T. Interaction of HSP90 to N-WASP leads to activation and protection from proteasome-dependent degradation. EMBO J. 2005, 24 (8), 1557-1570.
74. Park, S. J.; Suetsugu, S.; Sagara, H.; Takenawa, T. HSP90 crosslinks branched actin filaments induced by N-WASP and the Arp2/3 complex. Genes Cells 2007, 12 (5), 611-622.
75. Scheufler, C.; Brinker, A.; Bourenkov, G.; Pegoraro, S.; Moroder, L.; Bartunik, H.; Hartl, F. U.; Moarefi, I. Structure of TPR domainpeptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 2000, 101 (2), 199-210.
76. Hyduk, S. J.; Chan, J. R.; Duffy, S. T.; Chen, M.; Peterson, M. D.; Waddell, T. K.; Digby, G. C.; Szaszi, K.; Kapus, A.; Cybulsky, M. I.; Phospholipase, C. calcium, and calmodulin are critical for alpha4beta1 integrin affinity up-regulation and monocyte arrest triggered by chemoattractants. Blood 2007, 109 (1), 176-184.
77. Moffett, S.; Brown, D. A.; Linder, M. E. Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 2000, 275 (3), 2191-8.
78. Oh, P.; Schnitzer, J. E. Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default. Mol. Biol. Cell 2001, 12 (3), 685-698.
79. Quinton, T. M.; Kim, S.; Jin, J.; Kunapuli, S. P. Lipid rafts are required in Galpha(i) signaling downstream of the P2Y12 receptor during ADP-mediated platelet activation. J. Thromb. Haemostasis 2005, 3 (5), 1036-1041.
80. Garin, J.; Diez, R.; Kieffer, S.; Dermine, J. F.; Duclos, S.; Gagnon, E.; Sadoul, R.; Rondeau, C.; Desjardins, M. The phagosome proteome: insight into phagosome functions. J. Cell Biol. 2001, 152 (1), 165-180.
81. Kabouridis, P. S.; Janzen, J.; Magee, A. L.; Ley, S. C. Cholesterol depletion disrupts lipid rafts and modulates the activity of multiple signaling pathways in T lymphocytes. Eur. J. Immunol. 2000, 30 (3), 954-963.
82. Saeki, K.; Miura, Y.; Aki, D.; Kurosaki, T.; Yoshimura, A. The B cell-specific major raft protein, Raftlin, is necessary for the integrity of lipid raft and BCR signal transduction. EMBO J. 2003, 22 (12), 3015-3026.
83. Nishio, M.; Fukumoto, S.; Furukawa, K.; Ichimura, A.; Miyazaki, H.; Kusunoki, S.; Urano, T. Overexpressed GM1 suppresses nerve growth factor (NGF) signals by modulating the intracellular localization of NGF receptors and membrane fluidity in PC12 cells. J. Biol. Chem. 2004, 279 (32), 33368-33378.
84. Assossou, O.; Besson, F.; Rouault, J. P.; Persat, F.; Brisson, C.; Duret, L.; Ferrandiz, J.; Mayencon, M.; Peyron, F.; Picot, S. Subcellular localization of 14-3-3 proteins in Toxoplasma gondii tachyzoites and evidence for a lipid raft-associated form. FEMS Microbiol. Lett. 2003, 224 (2), 161-168.
85. Stickney, J. T.; Bacon, W. C.; Rojas, M.; Ratner, N.; Ip, W. Activation of the tumor suppressor merlin modulates its interaction with lipid rafts. Cancer Res. 2004, 64 (8), 2717-2724.
86. Eleme, K.; Taner, S. B.; Onfelt, B.; Collinson, L. M.; McCann, F. E.; Chalupny, N. J.; Cosman, D.; Hopkins, C.; Magee, A. I.; Davis, D. M. Cell surface organization of stress-inducible proteins ULBP and MICA that stimulate human NK cells and T cells via NKG2D. J. Exp. Med. 2004, 199 (7), 1005-1010.
87. Drbal, K.; Moertelmaier, M.; Holzhauser, C.; Muhammad, A.; Fuertbauer, E.; Howorka, S.; Hinterberger, M.; Stockinger, H.; Schutz, G. J. Single-molecule microscopy reveals heterogeneous dynamics of lipid raft components upon TCR engagement. Int. Immunol. 2007, 19 (5), 675-684.
88. Triantafilou, M.; Miyake, K.; Golenbock, D. T.; Triantafilou, K. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci. 2002, 115 (Pt 12), 2603-11.