A Mechanistic Model of Early FcεRI Signaling: Lipid Rafts and the Question of Protection from Dephosphorylation

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Barua, Dipak ^a,b   Goldstein, Byron ^a  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

^b CENTER FOR NONLINEAR STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; IMMUNOGLOBULIN E RECEPTOR; LAT PROTEIN; PHOSPHATASE; PROTEIN KINASE LYN;

ANIMAL CELL; ANTIGEN ANTIBODY COMPLEX; ARTICLE; ENZYME ACTIVITY; HAPTEN CARRIER COMPLEX; LIPID RAFT; MAST CELL; MEMBRANE COMPONENT; MEMBRANE MODEL; MEMBRANE STRUCTURE; NONHUMAN; PROTEIN AGGREGATION; PROTEIN CROSS LINKING; PROTEIN DEPHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; CALCIUM; CELL MEMBRANE; COMPUTER SIMULATION; HAPTENS; IMMUNOGLOBULIN E; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEUKEMIA, BASOPHILIC, ACUTE; LIPOYLATION; MAST CELLS; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; MUTATION; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RATS; RECEPTORS, IGE; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TUMOR CELLS, CULTURED; TYROSINE;

RATTUS;

EID: 84871319035     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051669     Document Type: Article

References (68)

1. Simons K, Vaz WL, (2004) Model systems, lipid rafts, and cell membranes Annu Rev Biophys Biomol Struct. 33: 269-295.
2. Lingwood D, Simons K, (2010) Lipid rafts as a membrane-organizing principle Science. 327: 46-50.
3. Jacobson K, Mouritsen OG, Anderson RG, (2007) Lipid rafts: at a crossroad between cell biology and physics Nat Cell Biol. 9: 7-14.
4. Elson EL, Fried E, Dolbow JE, Genin GM, (2010) Phase separation in biological membranes: integration of theory and experiment Annu Rev Biophys. 39: 207-226.
5. Simons K, Toomre D, (2000) Lipid rafts and signal transduction Nat Rev Mol Cell Biol. 1: 31-39.
6. Harder T, (2004) Lipid raft domains and protein networks in T-cell receptor signal transduction Curr Opin Immunol. 16: 353-359.
7. Katagiri YU, Kiyokawa N, Fujimoto J, (2001) A role for lipid rafts in immune cell signaling Microbiol Immunol. 45: 1-8.
8. Resh MD, (1999) Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins Biochim Biophys Acta. 1451: 1-16.
9. Zhang W, Trible RP, Samelson LE, (1998) LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation Immunity. 9: 239-246.
10. Chatterjee S, Mayor S, (2001) The GPI-anchor and protein sorting Cell Mol Life Sci. 58: 1969-1987.
11. Rajendran L, Masilamani M, Solomon S, Tikkanen R, Stuermer CA, et al. (2003) Asymmetric localization of flotillins/reggies in preassembled platforms confers inherent polarity to hematopoietic cells Proc Natl Acad Sci U S A. 100: 8241-8246.
12. Karpen HE, Bukowski JT, Hughes T, Gratton JP, Sessa WC, et al. (2001) The sonic hedgehog receptor patched associates with caveolin-1 in cholesterol-rich microdomains of the plasma membrane J Biol Chem. 276: 19503-19511.
13. Kurzchalia TV, Parton RG, (1999) Membrane microdomains and caveolae Curr Opin Cell Biol. 11: 424-431.
14. Babiychuk EB, Monastyrskaya K, Burkhard FC, Wray S, Draeger A, (2002) Modulating signaling events in smooth muscle: cleavage of annexin 2 abolishes its binding to lipid rafts FASEB J. 16: 1177-1184.
15. Melkonian KA, Ostermeyer AG, Chen JZ, Roth MG, Brown DA, (1999) Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated J Biol Chem 274: 3910-3917.
16. Dykstra M, Cherukuri A, Sohn HW, Tzeng SJ, Pierce SK, (2003) Location is everything: lipid rafts and immune cell signaling Annu Rev Immunol. 21: 457-481.
17. Janes PW, Ley SC, Magee AI, Kabouridis PS, (2000) The role of lipid rafts in T cell antigen receptor (TCR) signalling Semin Immunol. 12: 23-34.
18. Pierce SK, (2002) Lipid rafts and B-cell activation Nat Rev Immunol. 2: 96-105.
19. Holowka D, Gosse JA, Hammond AT, Han X, Sengupta P, et al. (2005) Lipid segregation and IgE receptor signaling: a decade of progress Biochim Biophys Acta. 1746: 252-259.
20. Sengupta P, Baird B, Holowka D, (2007) Lipid rafts, fluid/fluid phase separation, and their relevance to plasma membrane structure and function Semin Cell Dev Biol. 18: 583-590.
21. Thomas JL, Holowka D, Baird B, Webb WW, (1994) Large-scale co-aggregation of fluorescent lipid probes with cell surface proteins J Cell Biol. 125: 795-802.
22. Field KA, Holowka D, Baird B, (1995) FcεRI-mediated recruitment of p53/56lyn to detergent-resistant membrane domains accompanies cellular signaling Proc Natl Acad Sci U S A. 92: 9201-9205.
23. Sheets ED, Holowka D, Baird B, (1999) Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FcεRI and their association with detergent-resistant membranes J Cell Biol. 145: 877-887.
24. Young RM, Holowka D, Baird B, (2003) A lipid raft environment enhances Lyn kinase activity by protecting the active site tyrosine from dephosphorylation J Biol Chem. 278: 20746-20752.
25. Young RM, Zheng X, Holowka D, Baird B, (2005) Reconstitution of regulated phosphorylation of FcεRI by a lipid raft-excluded protein-tyrosine phosphatase J Biol Chem. 280: 1230-1235.
26. 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 Biophys J. 80: 2120-2132.
27. Field KA, Holowka D, Baird B, (1997) Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains J Biol Chem. 272: 4276-4280.
28. Davey AM, Walvick RP, Liu Y, Heikal AA, Sheets ED, (2007) Membrane order and molecular dynamics associated with IgE receptor cross-linking in mast cells Biophys J. 92: 343-355.
29. Kovarova M, Tolar P, Arudchandran R, Draberova L, Rivera J, et al. (2001) Structure-function analysis of Lyn kinase association with lipid rafts and initiation of early signaling events after Fcε receptor I aggregation Mol Cell Biol. 21: 8318-8328.
30. Tanimura N, Nagafuku M, Minaki Y, Umeda Y, Hayashi F, et al. (2003) Dynamic changes in the mobility of LAT in aggregated lipid rafts upon T cell activation J Cell Biol. 160: 125-135.
31. Shogomori H, Hammond AT, Ostermeyer-Fay AG, Barr DJ, Feigenson GW, et al. (2005) Palmitoylation and intracellular domain interactions both contribute to raft targeting of linker for activation of T cells J Biol Chem. 280: 18931-18942.
32. Resh MD, (1994) Myristylation and palmitylation of Src family members: the fats of the matter Cell. 76: 411-413.
33. Wilson BS, Pfeiffer JR, Surviladze Z, Gaudet EA, Oliver JM, (2001) High resolution mapping of mast cell membranes reveals primary and secondary domains of FcεRI and LAT J Cell Biol. 154: 645-658.
34. Lillemeier BF, Mortelmaier MA, Forstner MB, Huppa JB, Groves JT, et al. (2010) TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation Nat Immunol. 11: 90-96.
35. Saitoh S, Arudchandran R, Manetz TS, Zhang W, Sommers CL, et al. (2000) LAT is essential for FcεRI-mediated mast cell activation Immunity. 12: 525-535.
36. Pribluda VS, Pribluda C, Metzger H, (1994) Transphosphorylation as the mechanism by which the high-affinity receptor for IgE is phosphorylated upon aggregation Proc Natl Acad Sci U S A. 91: 11246-11250.
37. Kihara H, Siraganian RP, (1994) Src homology 2 domains of Syk and Lyn bind to tyrosine-phosphorylated subunits of the high affinity IgE receptor J Biol Chem. 269: 22427-22432.
38. Gidwani A, Holowka D, Baird B, (2001) Fluorescence anisotropy measurements of lipid order in plasma membranes and lipid rafts from RBL-2H3 mast cells Biochemistry. 40: 12422-12429.
39. Ge M, Gidwani A, Brown HA, Holowka D, Baird B, et al. (2003) Ordered and disordered phases coexist in plasma membrane vesicles of RBL-2H3 mast cells. An ESR study Biophys J 85: 1278-1288.
40. Peirce M, Metzger H, (2000) Detergent-resistant microdomains offer no refuge for proteins phosphorylated by the IgE receptor J Biol Chem. 275: 34976-34982.
41. Faeder JR, Hlavacek WS, Reischl I, Blinov ML, Metzger H, et al. (2003) Investigation of early events in FcεRI-mediated signaling using a detailed mathematical model J Immunol. 170: 3769-3781.
42. Mao SY, Metzger H, (1997) Characterization of protein-tyrosine phosphatases that dephosphorylate the high affinity IgE receptor J Biol Chem. 272: 14067-14073.
43. Zhang W, Sloan-Lancaster J, Kitchen J, Trible RP, Samelson LE, (1998) LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation Cell. 92: 83-92.
44. Zhang J, Berenstein E, Siraganian RP, (2002) Phosphorylation of Tyr342 in the linker region of Syk is critical for FcεRI signaling in mast cells Mol Cell Biol. 22: 8144-8154.
45. Saitoh S, Odom S, Gomez G, Sommers CL, Young HA, et al. (2003) The four distal tyrosines are required for LAT-dependent signaling in FcεRI-mediated mast cell activation J Exp Med. 198: 831-843.
46. Holowka D, Baird B, (2001) FcεRI as a paradigm for a lipid raft-dependent receptor in hematopoietic cells Semin Immunol. 13: 99-105.
47. Arudchandran R, Brown MJ, Peirce MJ, Song JS, Zhang J, et al. (2000) The Src homology 2 domain of Vav is required for its compartmentation to the plasma membrane and activation of c-Jun NH(2)-terminal kinase 1 J Exp Med. 191: 47-60.
48. Wilson BS, Pfeiffer JR, Oliver JM, (2002) FcεRI signaling observed from the inside of the mast cell membrane Mol Immunol. 38: 1259-1268.
49. Das R, Hammond S, Holowka D, Baird B, (2008) Real-time cross-correlation image analysis of early events in IgE receptor signaling Biophys J. 94: 4996-5008.
50. Fischer EH, Charbonneau H, Tonks NK, (1991) Protein tyrosine phosphatases: a diverse family of intracellular and transmembrane enzymes Science. 253: 401-406.
51. Brown DA, (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals Physiology (Bethesda). 21: 430-439.
52. Rodgers W, Rose JK, (1996) Exclusion of CD45 inhibits activity of p56lck associated with glycolipid-enriched membrane domains J Cell Biol. 135: 1515-1523.
53. Goldstein B, Griego R, Wofsy C, (1984) Diffusion-limited forward rate constants in two dimensions. Application to the trapping of cell surface receptors by coated pits Biophys J 46: 573-586.
54. Pralle A, Keller P, Florin EL, Simons K, Horber JK, (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells J Cell Biol. 148: 997-1008.
55. Andrews NL, Pfeiffer JR, Martinez AM, Haaland DM, Davis RW, et al. (2009) Small, mobile FcεRI receptor aggregates are signaling competent Immunity. 31: 469-479.
56. Larson DR, Gosse JA, Holowka DA, Baird BA, Webb WW, (2005) Temporally resolved interactions between antigen-stimulated IgE receptors and Lyn kinase on living cells J Cell Biol. 171: 527-536.
57. Faeder JR, Blinov ML, Hlavacek WS, (2009) Rule-based modeling of biochemical systems with BioNetGen Methods Mol Biol. 500: 113-167.
58. Wofsy C, Torigoe C, Kent UM, Metzger H, Goldstein B, (1997) Exploiting the difference between intrinsic and extrinsic kinases: implications for regulation of signaling by immunoreceptors J Immunol. 159: 5984-5992.
59. Torigoe C, Goldstein B, Wofsy C, Metzger H, (1997) Shuttling of initiating kinase between discrete aggregates of the high affinity receptor for IgE regulates the cellular response Proc Natl Acad Sci U S A. 94: 1372-1377.
60. Wofsy C, Vonakis BM, Metzger H, Goldstein B, (1999) One lyn molecule is sufficient to initiate phosphorylation of aggregated high-affinity IgE receptors Proc Natl Acad Sci U S A. 96: 8615-8620.
61. Tolar P, Draberova L, Tolarova H, Draber P, (2004) Positive and negative regulation of Fcε receptor I-mediated signaling events by Lyn kinase C-terminal tyrosine phosphorylation Eur J Immunol. 34: 1136-1145.
62. Liu FT, Bohn JW, Ferry EL, Yamamoto H, Molinaro CA, et al. (1980) Monoclonal dinitrophenyl-specific murine IgE antibody: preparation, isolation, and characterization J Immunol. 124: 2728-2737.
63. Kusumi A, Koyama-Honda I, Suzuki K, (2004) Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts Traffic. 5: 213-230.
64. Fan J, Sammalkorpi M, Haataja M, (2010) Formation and regulation of lipid microdomains in cell membranes: theory, modeling, and speculation FEBS Lett. 584: 1678-1684.
65. Rosenbluth MJ, Lam WA, Fletcher DA, (2006) Force microscopy of nonadherent cells: a comparison of leukemia cell deformability Biophys J. 90: 2994-3003.
66. Sotirellis N, Johnson TM, Hibbs ML, Stanley IJ, Stanley E, et al. (1995) Autophosphorylation induces autoactivation and a decrease in the Src homology 2 domain accessibility of the Lyn protein kinase J Biol Chem. 270: 29773-29780.
67. Janes PW, Ley SC, Magee AI, (1999) Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor J Cell Biol. 147: 447-461.
68. Lillemeier BF, Pfeiffer JR, Surviladze Z, Wilson BS, Davis MM, (2006) Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton Proc Natl Acad Sci U S A. 103: 18992-18997.