A tale of two TRAPs: LAT and LAB in the regulation of lymphocyte development, activation, and autoimmunity

Immunologic Research

Volumn 49, Issue 1-3, 2011, Pages 97-108

  Fuller, Deirdre M ^a   Zhu, Minghua ^a   Ou Yang, Chih Wen ^a   Sullivan, Sarah A ^a   Zhang, Weiguo ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Autoimmunity; Lymphoproliferative disease; PLC ; T cell homeostasis; TRAP (transmembrane adaptor protein); Tyrosine phosphorylation

Indexed keywords

ADAPTOR PROTEIN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; INTERLEUKIN 10; INTERLEUKIN 4; L SELECTIN; LAB PROTEIN; LAT PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

AUTOIMMUNITY; B LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CYTOKINE PRODUCTION; HOMEOSTASIS; HYPERGAMMAGLOBULINEMIA; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LEUKEMIA CELL LINE; LYMPHOCYTE ACTIVATION; LYMPHOPROLIFERATIVE DISEASE; MAST CELL; NATURAL KILLER CELL; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; TH1 CELL; TH2 CELL; THYMOCYTE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOIMMUNITY; CELL DIFFERENTIATION; HUMANS; LYMPHOCYTE ACTIVATION; MEMBRANE PROTEINS; T-LYMPHOCYTES;

EID: 79952704606     PISSN: 0257277X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12026-010-8197-3     Document Type: Review

References (62)

1. Samelson LE. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu Rev Immunol. 2002;20:371-94. (Pubitemid 34293429)
2. Horejsi V, Zhang W, Schraven B. Transmembrane adaptor proteins: organizers of immunoreceptor signalling. Nat Rev Immunol. 2004;4:603-16. (Pubitemid 39025046)
3. Finco TS, Kadlecek T, Zhang W, Samelson LE, Weiss A. LAT is required for TCR-mediated activation of PLCgamma1 and the Ras pathway. Immunity. 1998;9:617-26. (Pubitemid 28557590)
4. Zhang W, et al. Essential role of LAT in T cell development. Immunity. 1999;10:323-32. (Pubitemid 29165287)
5. Saitoh S, et al. LAT is essential for Fc (epsilon) RI-mediated mast cell activation. Immunity. 2000;12:525-35.
6. Brdicka T, et al. Non-T cell activation linker (NTAL): a transmembrane adaptor protein involved in immunoreceptor signaling. J Exp Med. 2002;196:1617-26. (Pubitemid 36026473)
7. Janssen E, Zhu M, Zhang W, Koonpaew S, Zhang W. LAB: a new membrane-associated adaptor molecule in B cell activation. Nat Immunol. 2003;4:117-23. (Pubitemid 36193012)
8. Zhu M, et al. Negative regulation of lymphocyte activation by the adaptor protein LAX. J Immunol. 2005;174:5612-9. (Pubitemid 40593202)
9. Zhu M, et al. Negative regulation of T cell activation and autoimmunity by the transmembrane adaptor protein LAB. Immunity. 2006;25:757-68. (Pubitemid 46107283)
10. Koelsch U, Schraven B, Simeoni L. SIT and TRIM determine T cell fate in the thymus. J Immunol. 2008;181:5930-9.
11. Davidson D, Bakinowski M, Thomas ML, Horejsi V, Veillette A. Phosphorylation-dependent regulation of T-cell activation by PAG/Cbp, a lipid raft-associated transmembrane adaptor. Mol Cell Biol. 2003;23:2017-28. (Pubitemid 36278813)
12. Brdicka T, et al. Phosphoprotein associated with glycosphingolipid- enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J Exp Med. 2000;191:1591-604. (Pubitemid 30257355)
13. Smida M, Posevitz-Fejfar A, Horejsi V, Schraven B, Lindquist JA. A novel negative regulatory function of the phosphoprotein associated with glycosphingolipid-enriched microdomains: blocking Ras activation. Blood. 2007;110:596-615.
14. Hur EM, et al. LIME, a novel transmembrane adaptor protein, associates with p56lck and mediates T cell activation. J Exp Med. 2003;198:1463-73. (Pubitemid 37467161)
15. Zhang W, Sloan-Lancaster J, Kitchen J, Trible RP, Samelson LE. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell. 1998;92:83-92. (Pubitemid 28053300)
16. Su YW, Jumaa H. LAT links the pre-BCR to calcium signaling. Immunity. 2003;19:295-305. (Pubitemid 37011343)
17. Facchetti F, et al. Linker for activation of T cells (LAT), a novel immunohistochemical marker for T cells, NK cells, mast cells, and megakaryocytes: evaluation in normal and pathological conditions. Am J Pathol. 1999;154:1037-46. (Pubitemid 29169738)
18. Weber JR, et al. Molecular cloning of the cDNA encoding pp36, a tyrosine-phosphorylated adaptor protein selectively expressed by T cells and natural killer cells. J Exp Med. 1998;187:1157-61. (Pubitemid 28176417)
19. Zhang W, Irvin BJ, Trible RP, Abraham RT, Samelson LE. Functional analysis of LAT in TCR-mediated signaling pathways using a LAT-deficient Jurkat cell line. Int Immunol. 1999;11:943-50. (Pubitemid 29276606)
20. Liu SK, McGlade CJ. Gads is a novel SH2 and SH3 domain-containing adaptor protein that binds to tyrosine-phosphorylated Shc. Oncogene. 1998;17:3073-82. (Pubitemid 29020803)
21. Zhang W, Trible RP, Zhu M, Liu SK, McGlade CJ, Samelson LE. Association of Grb2, Gads, and phospholipase C-gamma 1 with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell antigen receptor-mediated signaling. J Biol Chem. 2000;275:23355-61. (Pubitemid 30646238)
22. Lin J, Weiss A. Identification of the minimal tyrosine residues required for linker for activation of T cell function. J Biol Chem. 2001;276:29588-95. (Pubitemid 37452058)
23. Zhu M, Janssen E, Zhang W. Minimal requirement of tyrosine residues of linker for activation of T cells in TCR signaling and thymocyte development. J Immunol. 2003;170:325-33. (Pubitemid 36026156)
24. Zhang W, Trible RP, Samelson LE. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity. 1998;9:239-46. (Pubitemid 28400037)
25. Zhu M, Shen S, Liu Y, Granillo O, Zhang W. Cutting edge: localization of linker for activation of T cells to lipid rafts is not essential in T cell activation and development. J Immunol. 2005;174:31-5. (Pubitemid 40007388)
26. Otahal P, et al. A new type of membrane raft-like microdomains and their possible involvement in TCR signaling. J Immunol. 2010;184:3689-96.
27. Hundt M, et al. Impaired activation and localization of LAT in anergic T cells as a consequence of a selective palmitoylation defect. Immunity. 2006;24:513-22. (Pubitemid 43728146)
28. Shen S, Zhu M, Lau J, Chuck M, Zhang W. The essential role of LAT in thymocyte development during transition from the double-positive to single-positive stage. J Immunol. 2009;182:5596-604.
29. Sommers CL, et al. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science. 2002;296:2040-3. (Pubitemid 34627529)
30. Aguado E, et al. Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science. 2002;296:2036-40. (Pubitemid 34627528)
31. Archambaud C, et al. STAT6 deletion converts the Th2 inflammatory pathology afflicting Lat (Y136F) mice into a lymphoproliferaltive disorder involving Th1 and CD8 effector T cells. J Immunol. 2009;182:2680-9.
32. Nunez-Cruz S, et al. LAT regulates gamma delta T cell homeostasis and differentiation. Nat Immunol. 2003;4:999-1008. (Pubitemid 37265921)
33. Sommers CL, et al. Mutation of the phospholipase C-gamma1-binding site of LAT affects both positive and negative thymocyte selection. J Exp Med. 2005;201:1125-34. (Pubitemid 40524680)
34. Wang Y, et al. Th2 lymphoproliferaltive disorder of LatY136F mutant mice unfolds independently of TCR-MHC engagement and is insensitive to the action of Foxp3+ regulatory T cells. J Immunol. 2008;180:1565-75.
35. Koonpaew S, Shen S, Flowers L, Zhang W. LAT-mediated signaling in CD4+CD25+ regulatory T cell development. J Exp Med. 2006;203:119-29. (Pubitemid 43139651)
36. Chuck MI, Zhu M, Shen S, Zhang W. The role of the LAT-PLC-gamma1 interaction in T regulatory cell function. J Immunol. 2010;184:2476-86.
37. Shen S, Chuck MI, Zhu M, Fuller DM, Ou Yang CW, Zhang W. The importance of LAT in the activation, homeostasis, and regulatory function of T cells. J Biol Chem. 2010.
38. Koonpaew S, Janssen E, Zhu M, Zhang W. The importance of three membrane-distal tyrosine's in the adaptor protein NTAL/LAB. J Biol Chem. 2004;279:11229-35. (Pubitemid 38401618)
39. Janssen E, Zhu M, Craven B, Zhang W. Linker for activation of B cells: a functional equivalent of a mutant linker for activation of T cells deficient in phospholipase C-gamma1 binding. J Immunol. 2004;172:6810-9. (Pubitemid 38669119)
40. Zhu M, Liu Y, Koonpaew S, Granillo O, Zhang W. Positive and negative regulation of FcepsilonRI-mediated signaling by the adaptor protein LAB/NTAL. J Exp Med. 2004;200:991-1000. (Pubitemid 39431124)
41. Wang Y, et al. Single and combined deletions of the NTAL/LAB and LAT adaptors minimally affect B-cell development and function. Mol Cell Biol. 2005;25:4455-65. (Pubitemid 40705752)
42. Stork B, et al. Grb2 and the non-T cell activation linker NTAL constitute a Ca (2+)-regulating signal circuit in B lymphocytes. Immunity. 2004;21:681-91.
43. Malhotra S, Kovats S, Zhang W, Coggeshall KM. Vav and Rac activation in B cell antigen receptor endocytosis involves Vav recruitment to the adapter protein LAB. J Biol Chem. 2009;284:36202-12.
44. Malhotra S, Kovats S, Zhang W, Coggeshall KM. B cell antigen receptor endocytosis and antigen presentation to T cells require Vav and dynamin. J Biol Chem. 2009;284:24088-97.
45. Denning TL, et al. Mouse TCRalphabeta + CD8alphaalpha intraepithelial lymphocytes express genes that down-regulate their antigen reactivity and suppress immune responses. J Immunol. 2007;178:4230-9. (Pubitemid 46492373)
46. Tessarz AS, Weiler S, Zanzinger K, Angelisova P, Horejsi V, Cerwenka A. Non-T cell activation linker (NTAL) negatively regulates TREM-1/DAP12-induced inflammatory cytokine production in myeloid cells. J Immunol. 2007;178:1991-9. (Pubitemid 46233395)
47. Hamerman JA, Jarjoura JR, Humphrey MB, Nakamura MC, Seaman WE, Lanier LL. Cutting edge: inhibition of TLR and FcR responses in macrophages by triggering receptor expressed on myeloid cells (TREM)-2 and DAP12. J Immunol. 2006;177:2051-5. (Pubitemid 44200961)
48. Whittaker GC, et al. The linker for activation of B cells (LAB)/non-T cell activation linker (NTAL) regulates triggering receptor expressed on myeloid cells (TREM)-2 signaling and macrophage inflammatory responses independently of the linker for activation of T cells. J Biol Chem. 2010;285:2976-85.
49. Tkaczyk C, et al. NTAL phosphorylation is a pivotal link between the signaling cascades leading to human mast cell degranulation following Kit activation and Fc epsilon RI aggregation. Blood. 2004;104:207-14. (Pubitemid 38879859)
50. Lebduska P, Korb J, Tumova M, Heneberg P, Draber P. Topography of signaling molecules as detected by electron microscopy on plasma membrane sheets isolated from non-adherent mast cells. J Immunol Methods. 2007;328:139-51. (Pubitemid 350007627)
51. Iwaki S, et al. Kit- and Fc epsilonRI-induced differential phosphorylation of the transmembrane adaptor molecule NTAL/LAB/LAT2 allows flexibility in its scaffolding function in mast cells. Cell Signal. 2008;20:195-205. (Pubitemid 350138381)
52. Dong S, et al. T cell receptor for antigen induces linker for activation of T cell-dependent activation of a negative signaling complex involving Dok-2, SHIP-1, and Grb-2. J Exp Med. 2006;203:2509-18. (Pubitemid 44664620)
53. Malbec O, et al. Linker for activation of T cells integrates positive and negative signaling in mast cells. J Immunol. 2004;173:5086-94. (Pubitemid 39387791)
54. Roget K, Malissen M, Malbec O, Malissen B, Daeron M. Non-T cell activation linker promotes mast cell survival by dampening the recruitment of SHIP1 by linker for activation of T cells. J Immunol. 2008;180:3689-98.
55. Yamasaki S, Ishikawa E, Kohno M, Saito T. The quantity and duration of FcRgamma signals determine mast cell degranulation and survival. Blood. 2004;103:3093-101. (Pubitemid 38451686)
56. Yamasaki S, et al. LAT and NTAL mediate immunoglobulin E-induced sustained extracellular signal-regulated kinase activation critical for mast cell survival. Mol Cell Biol. 2007;27:4406-15. (Pubitemid 46906564)
57. Galandrini R, Palmieri G, Piccoli M, Frati L, Santoni A. CD16-mediated p21ras activation is associated with Shc and p36 tyrosine phosphorylation and their binding with Grb2 in human natural killer cells. J Exp Med. 1996;183:179-86.
58. Valiante NM, Phillips JH, Lanier LL, Parham P. Killer cell inhibitory receptor recognition of human leukocyte antigen (HLA) class I blocks formation of a pp36/PLC-gamma signaling complex in human natural killer (NK) cells. J Exp Med. 1996;184:2243-50. (Pubitemid 27023724)
59. Chiesa S, et al. Multiplicity and plasticity of natural killer cell signaling pathways. Blood. 2006;107:2364-72. (Pubitemid 43345556)
60. Whittaker GC, et al. Analysis of the linker for activation of T cells and the linker for activation of B cells in natural killer cells reveals a novel signaling cassette, dual usage in ITAM signaling, and influence on development of the Ly49 repertoire. Blood. 2008;112:2869-77.
61. Matsuda S, et al. Negative feedback loop in T-cell activation through MAPK-catalyzed threonine phosphorylation of LAT. EMBO J. 2004;23:2577-85. (Pubitemid 38988229)
62. Fukata Y, Iwanaga T, Fukata M. Systematic screening for palmitoyl transferase activity of the DHHC protein family in mammalian cells. Methods. 2006;40:177-82. (Pubitemid 44442975)