Protein sorting by lipid phase-like domains supports emergent signaling function in b lymphocyte plasma membranes

eLife

Volumn 6, Issue , 2017, Pages

  Stone, Matthew B ^a   Shelby, Sarah A ^a   Nńñez, Marcos F ^a   Wisser, Kathleen ^a   Veatch, Sarah L ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CALCIUM; CD45 ANTIGEN; CHOLESTEROL; CLATHRIN; IMMUNOGLOBULIN F(AB')2 FRAGMENT; LIPID; PHOSPHATASE; PHOSPHOTRANSFERASE; PROTEIN KINASE LYN; MEMBRANE LIPID;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; B LYMPHOCYTE; CALCIUM MOBILIZATION; CELL HETEROGENEITY; CELL MEMBRANE; CONTROLLED STUDY; FLUORESCENCE; GENE EXPRESSION; GENETIC TRANSFECTION; LYMPHOMA CELL; MEMBRANE VESICLE; MICROSCOPY; MOUSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SIMULATION; SUPER RESOLUTION FLUORESCENCE LOCALIZATION MICROSCOPY; WESTERN BLOTTING; ANIMAL; FLUORESCENCE MICROSCOPY; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; B-LYMPHOCYTES; CELL MEMBRANE; MEMBRANE LIPIDS; MICE; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 85017162878     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.19891     Document Type: Article

References (91)

1. Aimon S, Callan-Jones A, Berthaud A, Pinot M, Toombes GE, Bassereau P. 2014. Membrane shape modulates transmembrane protein distribution. Developmental Cell 28:212–218. doi: 10.1016/j.devcel.2013.12.012 PMID: 24480645
2. Anderson RG, Jacobson K. 2002. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296:1821–1825. doi: 10.1126/science.1068886 PMID: 12052946
3. Awasthi-Kalia M, Schnetkamp PP, Deans JP. 2001. Differential effects of filipin and methyl-beta-cyclodextrin on B cell receptor signaling. Biochemical and Biophysical Research Communications 287:77–82. doi: 10.1006/bbrc.2001.5536 PMID: 11549256
4. Balagopalan L, Kortum RL, Coussens NP, Barr VA, Samelson LE. 2015. The Linker for activation of T cells (LAT) signaling hub: from signaling complexes to microclusters. Journal of Biological Chemistry 290:26422–26429. doi: 10.1074/jbc.R115.665869 PMID: 26354432
5. Batista FD, Iber D, Neuberger MS. 2001. B cells acquire antigen from target cells after synapse formation. Nature 411:489–494. doi: 10.1038/35078099 PMID: 11373683
6. Baumgart T, Hammond AT, Sengupta P, Hess ST, Holowka DA, Baird BA, Webb WW. 2007. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. PNAS 104:3165–3170. doi: 10.1073/pnas.0611357104 PMID: 17360623
7. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313: 1642–1645. doi: 10.1126/science.1127344 PMID: 16902090
8. Cambier JC, Ransom JT. 1987. Molecular mechanisms of transmembrane signaling in B lymphocytes. Annual Review of Immunology 5:175–199. doi: 10.1146/annurev.iy.05.040187.001135 PMID: 2439102
9. Campbell MA, Sefton BM. 1990. Protein tyrosine phosphorylation is induced in murine B lymphocytes in response to stimulation with anti-immunoglobulin. The EMBO Journal 9:2125–2131. PMID: 2357961
10. Campbell ID, Humphries MJ. 2011. Integrin structure, activation, and interactions. Cold Spring Harbor Perspectives in Biology 3:a004994. doi: 10.1101/cshperspect.a004994 PMID: 21421922
11. Chau AH, Walter JM, Gerardin J, Tang C, Lim WA. 2012. Designing synthetic regulatory networks capable of self-organizing cell polarization. Cell 151:320–332. doi: 10.1016/j.cell.2012.08.040 PMID: 23039994
12. Cheng PC, Dykstra ML, Mitchell RN, Pierce SK. 1999. A role for lipid rafts in B cell antigen receptor signaling and antigen targeting. The Journal of Experimental Medicine 190:1549–1560. doi: 10.1084/jem.190.11.1549 PMID: 10587346
13. Choudhuri K, Wiseman D, Brown MH, Gould K, van der Merwe PA. 2005. T-cell receptor triggering is critically dependent on the dimensions of its peptide-MHC ligand. Nature 436:578–582. doi: 10.1038/nature03843 PMID: 16049493
14. Christian AE, Haynes MP, Phillips MC, Rothblat GH. 1997. Use of cyclodextrins for manipulating cellular cholesterol content. Journal of Lipid Research 38:2264–2272. PMID: 9392424
15. Churchman LS, Okten Z, Rock RS, Dawson JF, Spudich JA. 2005. Single molecule high-resolution colocalization of Cy3 and Cy5 attached to macromolecules measures intramolecular distances through time. PNAS 102:1419–1423. doi: 10.1073/pnas.0409487102 PMID: 15668396
16. Cordoba SP, Choudhuri K, Zhang H, Bridge M, Basat AB, Dustin ML, van der Merwe PA, der MPAvan. 2013. The large ectodomains of CD45 and CD148 regulate their segregation from and inhibition of ligated T-cell receptor. Blood 121:4295–4302. doi: 10.1182/blood-2012-07-442251 PMID: 23580664
17. Dal Porto JM, Gauld SB, Merrell KT, Mills D, Pugh-Bernard AE, Cambier J. 2004. B cell antigen receptor signaling 101. Molecular Immunology 41:599–613. doi: 10.1016/j.molimm.2004.04.008 PMID: 15219998
18. Davis SJ, van der Merwe PA. 2006. The kinetic-segregation model: TCR triggering and beyond. Nature Immunology 7:803–809. doi: 10.1038/ni1369 PMID: 16855606
19. DeMond AL, Mossman KD, Starr T, Dustin ML, Groves JT. 2008. T cell receptor microcluster transport through molecular mazes reveals mechanism of translocation. Biophysical Journal 94:3286–3292. doi: 10.1529/biophysj.107.119099 PMID: 18199675
20. Douglass AD, Vale RD. 2005. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121:937–950. doi: 10.1016/j.cell.2005.04.009 PMID: 15960980
21. Endesfelder U, Malkusch S, Flottmann B, Mondry J, Liguzinski P, Verveer PJ, Heilemann M. 2011. Chemically induced photoswitching of fluorescent probes–a general concept for super-resolution microscopy. Molecules 16:3106–3118. doi: 10.3390/molecules16043106 PMID: 21490558
22. Francis ML, Ryan J, Jobling MG, Holmes RK, Moss J, Mond JJ. 1992. Cyclic AMP-independent effects of cholera toxin on B cell activation. II. binding of ganglioside GM1 induces B cell activation. Journal of Immunology 148: 1999–2005.
23. Gosse JA, Wagenknecht-Wiesner A, Holowka D, Baird B. 2005. Transmembrane sequences are determinants of immunoreceptor signaling. Journal of Immunology 175:2123–2131. doi: 10.4049/jimmunol.175.4.2123
24. Goswami D, Gowrishankar K, Bilgrami S, Ghosh S, Raghupathy R, Chadda R, Vishwakarma R, Rao M, Mayor S. 2008. Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135:1085–1097. doi: 10.1016/j.cell.2008.11.032 PMID: 19070578
25. Gray E, Karslake J, Machta BB, Veatch SL. 2013. Liquid general anesthetics lower critical temperatures in plasma membrane vesicles. Biophysical Journal 105:2751–2759. doi: 10.1016/j.bpj.2013.11.005 PMID: 24359747
26. Grimm JB, English BP, Chen J, Slaughter JP, Zhang Z, Revyakin A, Patel R, Macklin JJ, Normanno D, Singer RH, Lionnet T, Lavis LD. 2015. A general method to improve fluorophores for live-cell and single-molecule microscopy. Nature Methods 12:244–250. doi: 10.1038/nmeth.3256 PMID: 25599551
27. Grimm JB, English BP, Choi H, Muthusamy AK, Mehl BP, Dong P, Brown TA, Lippincott-Schwartz J, Liu Z, Lionnet T, Lavis LD. 2016. Bright photoactivatable fluorophores for single-molecule imaging. Nature Methods 13:985–988. doi: 10.1038/nmeth.4034 PMID: 27776112
28. Guan XM, Kobilka TS, Kobilka BK. 1992. Enhancement of membrane insertion and function in a type IIIb membrane protein following introduction of a cleavable signal peptide. The Journal of Biological Chemistry 267:21995–21998. PMID: 1331042
29. Gupta N, DeFranco AL. 2007. Lipid rafts and B cell signaling. Seminars in Cell & Developmental Biology 18:616–626. doi: 10.1016/j.semcdb.2007.07.009 PMID: 17719248
30. Harder T, Simons K. 1999. Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation. European Journal of Immunology 29: 556–562. doi: 10.1002/(SICI)1521-4141(199902)29:02<556::AID-IMMU556>3.0.CO;2-2 PMID: 10064071
31. Haughton G, Arnold LW, Bishop GA, Mercolino TJ. 1986. The CH series of murine B cell lymphomas: neoplastic analogues of Ly-1+ normal B cells. Immunological Reviews 93:35–52. doi: 10.1111/j.1600-065X.1986.tb01501.x PMID: 3491037
32. Heerklotz H. 2002. Triton promotes domain formation in lipid raft mixtures. Biophysical Journal 83:2693–2701. doi: 10.1016/S0006-3495(02)75278-8 PMID: 12414701
33. Heilemann M, van de Linde S, Mukherjee A, Sauer M. 2009. Super-resolution imaging with small organic fluorophores. Angewandte Chemie International Edition 48:6903–6908. doi: 10.1002/anie.200902073 PMID: 19670280
34. Hess ST, Girirajan TP, Mason MD. 2006. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophysical Journal 91:4258–4272. doi: 10.1529/biophysj.106.091116 PMID: 16980368
35. Honerkamp-Smith AR, Cicuta P, Collins MD, Veatch SL, den Nijs M, Schick M, Keller SL. 2008. Line tensions, correlation lengths, and critical exponents in lipid membranes near critical points. Biophysical Journal 95:236–246. doi: 10.1529/biophysj.107.128421 PMID: 18424504
36. Horejsi V, Hrdinka M. 2014. Membrane microdomains in immunoreceptor signaling. FEBS Letters 588:2392–2397. doi: 10.1016/j.febslet.2014.05.047 PMID: 24911201
37. Huang F, Hartwich TM, Rivera-Molina FE, Lin Y, Duim WC, Long JJ, Uchil PD, Myers JR, Baird MA, Mothes W, Davidson MW, Toomre D, Bewersdorf J. 2013. Video-rate nanoscopy using sCMOS camera-specific single-molecule localization algorithms. Nature Methods 10:653–658. doi: 10.1038/nmeth.2488 PMID: 23708387
38. Hui E, Vale RD. 2014. In vitro membrane reconstitution of the T-cell receptor proximal signaling network. Nature Structural & Molecular Biology 21:133–142. doi: 10.1038/nsmb.2762 PMID: 24463463
39. Johnson SA, Pleiman CM, Pao L, Schneringer J, Hippen K, Cambier JC. 1995. Phosphorylated immunoreceptor signaling motifs (ITAMs) exhibit unique abilities to bind and activate Lyn and Syk tyrosine kinases. Journal of Immunology 155:4596–4603. PMID: 7594458
40. Kaizuka Y, Douglass AD, Varma R, Dustin ML, Vale RD. 2007. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. PNAS 104:20296–20301. doi: 10.1073/pnas.0710258105 PMID: 18077330
41. Kenworthy AK, Edidin M. 1998. Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 A using imaging fluorescence resonance energy transfer. The Journal of Cell Biology 142:69–84. doi: 10.1083/jcb.142.1.69 PMID: 9660864
42. Kenworthy AK. 2008. Have we become overly reliant on lipid rafts? talking Point on the involvement of lipid rafts in T-cell activation. EMBO Reports 9:531–535. doi: 10.1038/embor.2008.92 PMID: 18516088
43. Kurosaki T, Kurosaki M. 1997. Transphosphorylation of Bruton’s tyrosine kinase on tyrosine 551 is critical for B cell antigen receptor function. Journal of Biological Chemistry 272:15595–15598. doi: 10.1074/jbc.272.25.15595 PMID: 9188445
44. Kwik J, Boyle S, Fooksman D, Margolis L, Sheetz MP, Edidin M. 2003. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. PNAS 100:13964–13969. doi: 10.1073/pnas.2336102100 PMID: 14612561
45. Levental I, Lingwood D, Grzybek M, Coskun U, Simons K. 2010. Palmitoylation regulates raft affinity for the majority of integral raft proteins. PNAS 107:22050–22054. doi: 10.1073/pnas.1016184107 PMID: 21131568
46. Lingwood D, Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science 327:46–50. doi: 10.1126/science.1174621 PMID: 20044567
47. Machta BB, Papanikolaou S, Sethna JP, Veatch SL. 2011. Minimal model of plasma membrane heterogeneity requires coupling cortical actin to criticality. Biophysical Journal 100:1668–1677. doi: 10.1016/j.bpj.2011.02.029 PMID: 21463580
48. Machta BB, Veatch SL, Sethna JP. 2012. Critical Casimir forces in cellular membranes. Physical Review Letters 109:138101. doi: 10.1103/PhysRevLett.109.138101 PMID: 23030121
49. Machta BB, Gray E, Nouri M, McCarthy NL, Gray EM, Miller AL, Brooks NJ, Veatch SL. 2016. Conditions that stabilize membrane domains also antagonize n-Alcohol Anesthesia. Biophysical Journal 111:537–545. doi: 10.1016/j.bpj.2016.06.039 PMID: 27508437
50. Malhotra S, Kovats S, Zhang W, Coggeshall KM. 2009. Vav and Rac activation in B cell antigen receptor endocytosis involves Vav recruitment to the adapter protein LAB. Journal of Biological Chemistry 284:36202–36212. doi: 10.1074/jbc.M109.040089 PMID: 19858206
51. Metzger H. 1992. Transmembrane signaling: the joy of aggregation. Journal of Immunology 149:1477–1487. PMID: 1324276
52. Minguet S, Dopfer EP, Schamel WW. 2010. Low-valency, but not monovalent, antigens trigger the B-cell antigen receptor (BCR). International Immunology 22:205–212. doi: 10.1093/intimm/dxp129 PMID: 20145007
53. Munro S. 2003. Lipid rafts: elusive or illusive? Cell 115:377–388. doi: 10.1016/S0092-8674(03)00882-1 PMID: 14622593
54. Mutch CM, Sanyal R, Unruh TL, Grigoriou L, Zhu M, Zhang W, Deans JP. 2007. Activation-induced endocytosis of the raft-associated transmembrane adaptor protein LAB/NTAL in B lymphocytes: evidence for a role in internalization of the B cell receptor. International Immunology 19:19–30. doi: 10.1093/intimm/dxl118 PMID: 17090619
55. Olszowy MW, Leuchtmann PL, Veillette A, Shaw AS. 1995. Comparison of p56lck and p59fyn protein expression in thymocyte subsets, peripheral T cells, NK cells, and lymphoid cell lines. Journal of Immunology 155:4236–4240. PMID: 7594580
56. Ovesný M, Krˇízˇek P, Borkovec J, Svindrych Z, Hagen GM. 2014. ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging. Bioinformatics 30:2389–2390. doi: 10.1093/bioinformatics/btu202 PMID: 24771516
57. Packard TA, Cambier JC. 2013. B lymphocyte antigen receptor signaling: initiation, amplification, and regulation. F1000Prime Reports 5:40. doi: 10.12703/P5-40 PMID: 24167721
58. Pierce SK. 2002. Lipid rafts and B-cell activation. Nature Reviews Immunology 2:96–105. doi: 10.1038/nri726 PMID: 11910900
59. Pierce SK, Liu W. 2010. The tipping points in the initiation of B cell signalling: how small changes make big differences. Nature Reviews Immunology 10:767–777. doi: 10.1038/nri2853 PMID: 20935671
60. Pyenta PS, Holowka D, Baird B. 2001. Cross-correlation analysis of inner-leaflet-anchored green fluorescent protein co-redistributed with IgE receptors and outer leaflet lipid raft components. Biophysical Journal 80: 2120–2132. doi: 10.1016/S0006-3495(01)76185-1 PMID: 11325715
61. Rao M, Mayor S. 2005. Use of Forster’s resonance energy transfer microscopy to study lipid rafts. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1746:221–233. doi: 10.1016/j.bbamcr.2005.08.002
62. Schroeder R, London E, Brown D. 1994. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. PNAS 91:12130–12134. doi: 10.1073/pnas.91.25.12130 PMID: 7991596
63. Sengupta P, Holowka D, Baird B. 2007. Fluorescence resonance energy transfer between lipid probes detects nanoscopic heterogeneity in the plasma membrane of live cells. Biophysical journal 92:3564–3574. doi: 10.1529/biophysj.106.094730 PMID: 17325019
64. Sengupta P, Jovanovic-Talisman T, Skoko D, Renz M, Veatch SL, Lippincott-Schwartz J. 2011. Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nature methods 8:969–975. doi: 10.1038/nmeth.1704 PMID: 21926998
65. Sharma P, Varma R, Sarasij RC, Ira , Gousset K, Krishnamoorthy G, Rao M, Mayor S. 2004. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116:577–589. doi: 10.1016/S0092-8674(04)00167-9 PMID: 14980224
66. Shelby SA, Holowka D, Baird B, Veatch SL. 2013. Distinct stages of stimulated fceri receptor clustering and immobilization are identified through superresolution imaging. Biophysical Journal 105:2343–2354. doi: 10.1016/j.bpj.2013.09.049 PMID: 24268146
67. Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387:569–572. doi: 10.1038/42408 PMID: 9177342
68. Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nature Reviews. Molecular Cell Biology 1:31–39. doi: 10.1038/35036052 PMID: 11413487
69. Siraganian RP, McGivney A, Barsumian EL, Crews FT, Hirata F, Axelrod J. 1982. Variants of the rat basophilic leukemia cell line for the study of histamine release. Federation Proceedings 41:30–34. PMID: 6173265
70. Sochacki KA, Shtengel G, van Engelenburg SB, Hess HF, Taraska JW. 2014. Correlative super-resolution fluorescence and metal-replica transmission electron microscopy. Nature Methods 11:305–308. doi: 10.1038/nmeth.2816 PMID: 24464288
71. Sohn HW, Tolar P, Jin T, Pierce SK. 2006. Fluorescence resonance energy transfer in living cells reveals dynamic membrane changes in the initiation of B cell signaling. PNAS 103:8143–8148. doi: 10.1073/pnas.0509858103 PMID: 16690746
72. Sohn HW, Tolar P, Pierce SK. 2008b. Membrane heterogeneities in the formation of B cell receptor-Lyn kinase microclusters and the immune synapse. The Journal of Cell Biology 182:367–379. doi: 10.1083/jcb.200802007 PMID: 18644892
73. Sohn HW, Pierce SK, Tzeng S-J. 2008a. Live cell imaging reveals that the inhibitory FcgammaRIIB destabilizes B cell receptor membrane-lipid interactions and blocks immune synapse formation. Journal of Immunology 180: 793–799. doi: 10.4049/jimmunol.180.2.793
74. Sotirellis N, Johnson TM, Hibbs ML, Stanley IJ, Stanley E, Dunn AR, Cheng HC. 1995. Autophosphorylation induces autoactivation and a decrease in the Src homology 2 domain accessibility of the Lyn protein kinase. The Journal of Biological Chemistry 270:29773–29780. doi: 10.1074/jbc.270.50.29773 PMID: 8530369
75. Sounier R, Mas C, Steyaert J, Laeremans T, Manglik A, Huang W, Kobilka BK, Déméné H, Granier S. 2015. Propagation of conformational changes during m-opioid receptor activation. Nature 524:375–378. doi: 10.1038/nature14680 PMID: 26245377
76. Stone MB, Veatch SL. 2014. Far-red organic fluorophores contain a fluorescent impurity. ChemPhysChem 15: 2240–2246. doi: 10.1002/cphc.201402002 PMID: 24782148
77. Stone MB, Veatch SL. 2015. Steady-state cross-correlations for live two-colour super-resolution localization data sets. Nature Communications 6:7347. doi: 10.1038/ncomms8347 PMID: 26066572
78. Stone MB, Shelby SA, Veatch SL. 2017. Super-Resolution microscopy: shedding light on the cellular plasma membrane. Chemical Reviews. In press. doi: 10.1021/acs.chemrev.6b00716 PMID: 28211677
79. Su X, Ditlev JA, Hui E, Xing W, Banjade S, Okrut J, King DS, Taunton J, Rosen MK, Vale RD. 2016a. Phase separation of signaling molecules promotes T cell receptor signal transduction. Science 352:595–599. doi: 10.1126/science.aad9964 PMID: 27056844
80. Su X, Ditlev JA, Hui E, Xing W, Banjade S, Okrut J, King DS, Taunton J, Rosen MK, Vale RD. 2016b. Phase separation of signaling molecules promotes T cell receptor signal transduction. Science 352:595–599. doi: 10.1126/science.aad9964 PMID: 27056844
81. Varma R, Mayor S. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394:798–801. doi: 10.1038/29563 PMID: 9723621
82. Veatch SL, Keller SL. 2005. Seeing spots: Complex phase behavior in simple membranes. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1746:172–185. doi: 10.1016/j.bbamcr.2005.06.010
83. Veatch SL, Cicuta P, Sengupta P, Honerkamp-Smith A, Holowka D, Baird B. 2008. Critical fluctuations in plasma membrane vesicles. ACS Chemical Biology 3:287–293. doi: 10.1021/cb800012x PMID: 18484709
84. Veatch SL, Machta BB, Shelby SA, Chiang EN, Holowka DA, Baird BA. 2012. Correlation functions quantify super-resolution images and estimate apparent clustering due to over-counting. PLoS One 7:e31457. doi: 10.1371/journal.pone.0031457 PMID: 22384026
85. Wülfing C, Davis MM. 1998. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282:2266–2269. doi: 10.1126/science.282.5397.2266 PMID: 9856952
86. Yang J, Reth M. 2010a. Oligomeric organization of the B-cell antigen receptor on resting cells. Nature 467:465–469. doi: 10.1038/nature09357 PMID: 20818374
87. Yang J, Reth M. 2010b. The dissociation activation model of B cell antigen receptor triggering. FEBS Letters 584:4872–4877. doi: 10.1016/j.febslet.2010.09.045 PMID: 20920502
88. Young RM, Holowka D, Baird B. 2003. A lipid raft environment enhances Lyn kinase activity by protecting the active site tyrosine from dephosphorylation. Journal of Biological Chemistry 278:20746–20752. doi: 10.1074/jbc.M211402200 PMID: 12670955
89. Zacharias DA, Violin JD, Newton AC, Tsien RY. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296:913–916. doi: 10.1126/science.1068539 PMID: 11988576
90. Zhao J, Wu J, Veatch SL. 2013. Adhesion stabilizes robust lipid heterogeneity in supercritical membranes at physiological temperature. Biophysical Journal 104:825–834. doi: 10.1016/j.bpj.2012.12.047 PMID: 23442961
91. Zhu C, Das SL, Baumgart T. 2012. Nonlinear sorting, curvature generation, and crowding of endophilin N-BAR on tubular membranes. Biophysical Journal 102:1837–1845. doi: 10.1016/j.bpj.2012.03.039 PMID: 22768939