Regulation of lymphocyte development and activation by the LAT family of adapter proteins

Immunological Reviews

Volumn 232, Issue 1, 2009, Pages 72-83

  Fuller, Deirdre M ^a   Zhang, Weiguo ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Adapter proteins; Autoimmunity; Protein kinases phosphatases; Signal transduction; Signaling proteins

Indexed keywords

ADAPTOR PROTEIN; LAB PROTEIN; LAT PROTEIN; LAX PROTEIN; UNCLASSIFIED DRUG;

B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL MATURATION; CELL SURVIVAL; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INNATE IMMUNITY; MAST CELL; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; FEEDBACK, PHYSIOLOGICAL; HUMANS; IMMUNITY, CELLULAR; LYMPHOCYTE ACTIVATION; MEMBRANE PROTEINS; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION;

EID: 70350376377     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2009.00828.x     Document Type: Review

References (98)

1. Freitas AA, Rocha B. Population biology of lymphocytes: the flight for survival. Annu Rev Immunol 2000 18 : 83 111.
2. Samelson LE. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu Rev Immunol 2002 20 : 371 394.
3. Cambier JC. Signal transduction by T- and B-cell antigen receptors: converging structures and concepts. Curr Opin Immunol 1992 4 : 257 264.
4. Reth M. Antigen receptor tail clue. Nature 1989 338 : 383 384.
5. Cambier JC. New nomenclature for the Reth motif (or ARH1/TAM/ARAM/YXXL). Immunol Today 1995 16 : 110.
6. Shaw A, Thomas ML. Coordinate interactions of protein tyrosine kinases and protein tyrosine phosphatases in T-cell receptor-mediated signalling. Curr Opin Cell Biol 1991 3 : 862 868.
7. Shores EW, et al. Role of the multiple T cell receptor (TCR)-zeta chain signaling motifs in selection of the T cell repertoire. J Exp Med 1997 185 : 893 900.
8. van Oers NS, et al. Regulation of TCR signal transduction in murine thymocytes by multiple TCR zeta-chain signaling motifs. J Immunol 1998 160 : 163 170.
9. Rolli V, et al. Amplification of B cell antigen receptor signaling by a Syk/ITAM positive feedback loop. Mol Cell 2002 10 : 1057 1069.
10. Horejsi V, Zhang W, Schraven B. Transmembrane adaptor proteins: organizers of immunoreceptor signalling. Nat Rev Immunol 2004 4 : 603 616.
11. Lindquist J.A., Simeoni L., Schraven B. Transmembrane adapters: attractants for cytoplasmic effectors. Immunol Rev 2003 191 : 165 182.
12. Kliche S, Lindquist JA, Schraven B. Transmembrane adapters: structure, biochemistry and biology. Semin Immunol 2004 16 : 367 377.
13. Zhang W, et al. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 1998 92 : 83 92.
14. Wange RL. LAT, the linker for activation of T cells: a bridge between T cell-specific and general signaling pathways. Sci STKE 2000 63 : RE1.
15. Zhu M, et al. Negative regulation of lymphocyte activation by the adaptor protein LAX. J Immunol 2005 174 : 5612 5619.
16. Zhu M, et al. Negative regulation of T cell activation and autoimmunity by the transmembrane adaptor protein LAB. Immunity 2006 25 : 757 768. (Pubitemid 46107283)
17. Koelsch U, Schraven B, Simeoni L. SIT and TRIM determine T cell fate in the thymus. J Immunol 2008 181 : 5930 5939.
18. Davidson D, et al. Phosphorylation-dependent regulation of T-cell activation by PAG/Cbp, a lipid raft-associated transmembrane adaptor. Mol Cell Biol 2003 23 : 2017 2028.
19. 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 1604.
20. Smida M, et al. A novel negative regulatory function of the phosphoprotein associated with glycosphingolipid-enriched microdomains: blocking Ras activation. Blood 2007 110 : 596 615.
21. Hur EM, et al. LIME, a novel transmembrane adaptor protein, associates with p56lck and mediates T cell activation. J Exp Med 2003 198 : 1463 1473.
22. June CH, et al. Increases in tyrosine phosphorylation are detectable before phospholipase C activation after T cell receptor stimulation. J Immunol 1990 144 : 1591 1599.
23. Gilliland LK, et al. Lymphocyte lineage-restricted tyrosine- phosphorylated proteins that bind PLC gamma 1 SH2 domains. J Biol Chem 1992 267 : 13610 13616.
24. Buday L, et al. A complex of Grb2 adaptor protein, Sos exchange factor, and a 36-kDa membrane-bound tyrosine phosphoprotein is implicated in ras activation in T cells. J Biol Chem 1994 269 : 9019 9023.
25. Sieh M, et al. GRB2 and phospholipase C-gamma 1 associate with a 36- to 38-kilodalton phosphotyrosine protein after T-cell receptor stimulation. Mol Cell Biol 1994 14 : 4435 4442.
26. Fukazawa T, et al. T cell activation-dependent association between the p85 subunit of the phosphatidylinositol 3-kinase and Grb2/phospholipase C-gamma 1-binding phosphotyrosyl protein pp36/38. J Biol Chem 1995 270 : 20177 20182.
27. Trub T, et al. The role of a lymphoid-restricted, Grb2-like SH3-SH2-SH3 protein in T cell receptor signaling. J Biol Chem 1997 272 : 894 902.
28. Su YW, Jumaa H. LAT links the pre-BCR to calcium signaling. Immunity 2003 19 : 295 305.
29. 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 1046.
30. 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 1161.
31. 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 : 239 246.
32. Zhu M, et al. 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 35.
33. 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 : 513 522.
34. Zhang W, et al. Functional analysis of LAT in TCR-mediated signaling pathways using a LAT-deficient Jurkat cell line. Int Immunol 1999 11 : 943 950.
35. Zhang W, et al. Essential role of LAT in T cell development. Immunity 1999 10 : 323 332.
36. Shen S, et al. The essential role of LAT in thymocyte development during transition from the double-positive to single-positive stage. J Immunol 2009 182 : 5596 5604.
37. 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 : 325 333.
38. Liu Y, Zhang W. Identification of a new transmembrane adaptor protein that constitutively binds Grb2 in B cells. J Leukoc Biol 2008 84 : 842 851.
39. Koretzky GA, Abtahian F, Silverman MA. SLP76 and SLP65: complex regulation of signalling in lymphocytes and beyond. Nat Rev Immunol 2006 6 : 67 78.
40. Zhang W, et al. Association of Grb2, Gads, and phospholipase C-gamma 1 with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell angigen receptor-mediated signaling. J Biol Chem 2000 275 : 23355 23361.
41. Sommers CL, et al. Knock-in mutation of the distal four tyrosines of linker for activation of T cells blocks murine T cell development. J Exp Med 2001 194 : 135 142.
42. Paz PE, et al. Mapping the Zap-70 phosphorylation sites on LAT (linker for activation of T cells) required for recruitment and activation of signalling proteins in T cells. Biochem J 2001 356 : 461 471.
43. 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 29595. (Pubitemid 37452058)
44. Sommers CL, et al. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science 2002 296 : 2040 2043.
45. Aguado E, et al. Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science 2002 296 : 2036 2040.
46. Genton C, et al. The Th2 lymphoproliferation developing in LatY136F mutant mice triggers polyclonal B cell activation and systemic autoimmunity. J Immunol 2006 177 : 2285 2293.
47. 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 1134.
48. Wang Y, et al. Th2 lymphoproliferative 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 1575.
49. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003 4 : 330 336.
50. Koonpaew S, et al. LAT-mediated signaling in CD4+CD25+ regulatory T cell development. J Exp Med 2006 203 : 119 129.
51. Archambaud C, et al. STAT6 deletion converts the Th2 inflammatory pathology afflicting Lat(Y136F) mice into a lymphoproliferative disorder involving Th1 and CD8 effector T cells. J Immunol 2009 182 : 2680 2689.
52. Nunez-Cruz S, et al. LAT regulates gammadelta T cell homeostasis and differentiation. Nat Immunol 2003 4 : 999 1008.
53. Leduc I, et al. T cell development in TCR beta enhancer-deleted mice: implications for alpha beta T cell lineage commitment and differentiation. J Immunol 2000 165 : 1364 1373.
54. Mombaerts P, et al. Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature 1992 360 : 225 231.
55. Yamasaki S, et al. Docking protein Gab2 is phosphorylated by ZAP-70 and negatively regulates T cell receptor signaling by recruitment of inhibitory molecules. J Biol Chem 2001 276 : 45175 45183.
56. Yamasaki S, et al. Gads/Grb2-mediated association with LAT is critical for the inhibitory function of Gab2 in T cells. Mol Cell Biol 2003 23 : 2515 2529.
57. 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 2518.
58. Kosugi A, et al. Involvement of SHP-1 tyrosine phosphatase in TCR-mediated signaling pathways in lipid rafts. Immunity 2001 14 : 669 680.
59. Matsuda S, et al. Negative feedback loop in T-cell activation through MAPK-catalyzed threonine phosphorylation of LAT. EMBO J 2004 23 : 2577 2585.
60. Saitoh S, et al. LAT is essential for Fc(epsilon)RI-mediated mast cell activation. Immunity 2000 12 : 525 535.
61. Saitoh S, et al. The four distal tyrosines are required for LAT-dependent signaling in FcepsilonRI-mediated mast cell activation. J Exp Med 2003 198 : 831 843.
62. Malbec O, et al. Linker for activation of T cells integrates positive and negative signaling in mast cells. J Immunol 2004 173 : 5086 5094.
63. Janssen E, et al. LAB: a new membrane-associated adaptor molecule in B cell activation. Nat Immunol 2003 4 : 117 123.
64. Brdicka T, et al. Non-T cell activation linker (NTAL): a transmembrane adaptor protein involved in immunoreceptor signaling. J Exp Med 2002 196 : 1617 1626.
65. Koonpaew S, et al. The importance of three membrane-distal tyrosines in the adaptor protein NTAL/LAB. J Biol Chem 2004 279 : 11229 11235.
66. Janssen E, et al. 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 6819.
67. Zhu M, et al. Positive and negative regulation of FcepsilonRI-mediated signaling by the adaptor protein LAB/NTAL. J Exp Med 2004 200 : 991 1000.
68. 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 4465.
69. 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 : 681 691.
70. Herzog S, Jumaa H. The N terminus of the non-T cell activation linker (NTAL) confers inhibitory effects on pre-B cell differentiation. J Immunol 2007 178 : 2336 2343.
71. 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 : 207 214.
72. Lebduska P, et al. Topography of signaling molecules as detected by electron microscopy on plasma membrane sheets isolated from non-adherent mast cells. J Immunol Methods 2007 328 : 139 151.
73. Draberova L, et al. Regulation of Ca2+ signaling in mast cells by tyrosine-phosphorylated and unphosphorylated non-T cell activation linker. J Immunol 2007 179 : 5169 5180.
74. Iwaki S, et al. Kit- and FceRI-induced differential phosphorylation of the transmembrane adaptor molecule NTAL/LAB/LAT2 allows flexibility in its scaffolding function in mast cells. Cell Signaling 2008 20 : 195 205.
75. Roget K, et al. 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 3698.
76. Yamasaki S, et al. The quantity and duration of FcRgamma signals determine mast cell degranulation and survival. Blood 2004 103 : 3093 3101.
77. Yamasaki S, et al. Selective impairment of FcepsilonRI-mediated allergic reaction in Gads-deficient mice. Int Immunol 2008 20 : 1289 1297.
78. 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 4415.
79. Tessarz AS, et al. Non-T cell activation linker (NTAL) negatively regulates TREM-1/DAP12-induced inflammatory cytokine production in myeloid cells. J Immunol 2007 178 : 1991 1999.
80. Hamerman JA, et al. 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 2055.
81. Galandrini R, et al. 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 : 179 186.
82. Valiante NM, et al. 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 2250.
83. Chiesa S, et al. Multiplicity and plasticity of natural killer cell signaling pathways. Blood 2006 107 : 2364 2372.
84. 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 2877.
85. Zhu M, et al. Molecular cloning of a novel gene encoding a membrane-associated adaptor protein (LAX) in lymphocyte signaling. J Biol Chem 2002 277 : 46151 46158.
86. Zhu M, et al. Negative regulation of Fc epsilonRI-mediated signaling and mast cell function by the adaptor protein LAX. J Biol Chem 2006 281 : 18408 18413.
87. Perchonock CE, et al. Negative regulation of interleukin-2 and p38 mitogen-activated protein kinase during T-cell activation by the adaptor ALX. Mol Cell Biol 2006 26 : 6005 6015.
88. Greene TA, et al. Cloning and characterization of ALX, an adaptor downstream of CD28. J Biol Chem 2003 278 : 45128 45134.
89. Shapiro MJ, et al. Negative regulation of TCR signaling by linker for activation of X cells via phosphotyrosine-dependent and -independent mechanisms. J Immunol 2008 181 : 7055 7061.
90. Simeoni L, et al. The transmembrane adapter protein SIT regulates thymic development and peripheral T-cell functions. Mol Cell Biol 2005 25 : 7557 7568.
91. Simeoni L, et al. Control of lymphocyte development and activation by negative regulatory transmembrane adapter proteins. Immunol Rev 2008 224 : 215 228.
92. Brown DA, London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 2000 275 : 17221 17224.
93. Zacharias DA, et al. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002 296 : 913 916.
94. Bartels DJ, et al. Erf2, a novel gene product that affects the localization and palmitoylation of Ras2 in Saccharomyces cerevisiae. Mol Cell Biol 1999 19 : 6775 6787.
95. Putilina T, Wong P, Gentleman S. The DHHC domain: a new highly conserved cysteine-rich motif. Mol Cell Biochem 1999 195 : 219 226.
96. Roth AF, et al. The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J Cell Biol 2002 159 : 23 28.
97. Fukata Y, Iwanaga T, Mukata F. Systematic screening for palmitoyl transferase activity of the DHHC protein family in mammalian cells. Methods 2006 40 : 177 182.
98. Zhang J, et al. Identification of CKAP4/p63 as a major substrate of the palmitoyl acyltransferase DHHC2, a putative tumor suppressor, using a novel proteomics method. Mol Cell Proteomics 2008 7 : 1378 1388.