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Association of Killer Cell Ig-like Receptor (KIR) with an Adaptor Protein Shc

  • Cho, Hyun-Il (Department of Microbiology, Yonsei University College of Medicine) ;
  • Chwae, Yong-Joon (Department of Microbiology, Yonsei University College of Medicine) ;
  • Park, Sang-Myun (Department of Microbiology, Yonsei University College of Medicine) ;
  • Kim, Jong-Sun (Department of Microbiology, Yonsei University College of Medicine)
  • Published : 2006.06.30
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Abstract

Background: Cytotoxic function of killer cells is inhibited by specific recognition of class I MHC molecules on target cells by inhibitory killer Ig-like receptors (KIR) expressed on NK cells and some cytotoxic T cells. The inhibitory effect of KIR is accomplished by recruitment of SH2-containing protein tyrosine phosphatase (SHP) to the phosphotyrosine residues in the cytoplasmic tail. Methods: By in vitro coprecipitation experiments and transfection analysis, we investigated the association of KIR with an adaptor protein Shc in Jurkat T cells. Results: The cytoplasmic tail of KIR appeared to associate with an adaptor protein Shc in Jurkat T celilysates. Similar in vitro experiments showed that phosphorylated KIR cytoplasmic tail bound SHP-1 and Shc in Jurkat T cell lysates. The association of KIR with Shc was further confirmed by transfection analysis in 293T cells. Interestingly, however, Shc appeared to be replaced by SHP-2 upon engagement of KIR in 293T cells. Conclusion: Our data indicate that KIR associate with an adaptor protein Shc in Jurkat T cells, and suggest that KIR might have an additional role which is mediated by this adaptor protein.

Keywords

References

  1. Moretta L, Moretta A: Killer Immunoglobulin-like receptors. Curr Opin Immunol 16;626-633, 2004 https://doi.org/10.1016/j.coi.2004.07.010
  2. Moretta A, Biassoni R, Bottino C, Pende D, Vitale M, Poggi A, Mingari MC, Moretta L: Major histocompatibility complex class-I specific receptors on human natural killer and T lymphocytes. Immunol Rev 155;105-117, 1997 https://doi.org/10.1111/j.1600-065X.1997.tb00943.x
  3. Lanier LL: NK cells: from no receptor to too many. Immunity 6;371-378, 1997 https://doi.org/10.1016/S1074-7613(00)80280-0
  4. Lanier LL, Phillips JH: Inhibitory MHC class I receptors on NK cells and T cells. Immunol Today 17;86-91, 1996 https://doi.org/10.1016/0167-5699(96)80585-8
  5. Vitale M, Sivori S, Pende D, Moretta L, Moretta A: Coexpression of two functionally independent p58 inhibitory receptors in human natural killer cell clones results in the inability to kill all normal allogeneic target cells. Proc Natl Acad Sci USA 92;3536-3540, 1995
  6. Cambiaggi A, Orengo AM, Meazza R, Sforzini S, Tazzari TZ, Lauria F, Raspadori D, Zambello R, Semenzato G, Moretta L, Ferrini S: The natural killer-related receptor for HLA-C expressed on T cells from CD3+ lymphoproliferative disease of granular lymphocytes displays either inhibitory or stimulatory function. Blood 87;2369-2375, 1996
  7. Mingari MC, Vitale C, Cambiaggi A, Schiavetti F, Melioli G, Ferrini S, Poggi A: Cytolytic T lymphocytes displaying natural killer (NK)-like activity: expression of NK-related fucnctional receptors for HLA class I molecules (p58 and CD94) and inhibitory effect on the TCR-mediated target cell lysis or lymphokine production. Int Immunol 7;697-703, 1995 https://doi.org/10.1093/intimm/7.4.697
  8. Phillips JH, Gumperz JE, Parham P, Lanier LL: Superantigen dependent, cell-mediated cytotoxicity inhibited by MHC class I receptors on T lymphocytes. Science 268;403-405, 1995 https://doi.org/10.1126/science.7716542
  9. Ugolini S, Arpin C, Anfossi N, Walzer T, Cambiaggi A, Forster R, Lipp M, Toes RE, Melief CJ, Marvel J, Vivier E: Involvement of inhibitory NKRs in the survival of a subset of memory-phenotype CD8+ T cells. Nat Immunol 2;430- 435, 2001 https://doi.org/10.1038/87740
  10. Young NT, Uhrberg M, Phillips JH, Lanier LL, Parham P: Differential expression of leukocyte receptor complex-encoded Ig-like receptors correlates with the transition from effector to memory CTL. J Immunol 166;3933-3941, 2001 https://doi.org/10.4049/jimmunol.166.6.3933
  11. Roger J, Chalifour A, Lemieux S, Duplay P: Cutting edge: Ly49A inhibits TCR/CD3-induced apoptosis and IL-2 secretion. J Immunol 167;6-10, 2001 https://doi.org/10.4049/jimmunol.167.1.6
  12. Chwae YJ, Chang MJ, Park SM, Yoon H, Park HJ, Kim SJ, Kim J: Molecular mechanism of the activation-induced cell death inhibition mediated by a p70 inhibitory killer cell Ig-like receptor in Jurkat T cells. J Immunol 169;3726-3735, 2002 https://doi.org/10.4049/jimmunol.169.7.3726
  13. Colonna M, Samaridis J: Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 268;405-408, 1995 https://doi.org/10.1126/science.7716543
  14. D'Andrea A, Chang C, Franz-Bacon K, McClanahan T, Phillips JH, Lanier LL: Molecular cloning of NKB1: a natural killer cell receptor for HLA-B allotypes. J Immunol 155; 2306-2310, 1995
  15. Wagtmann N, Biassoni R, Cantoni C, Verdani S, Manati MS, Vitale M, Cottino C, Moretta L, Moretta A, Long EO: Molecular clones of the p58 NK cell receptor reveal immunoglobulin- related molecules with diversity in both the extraand intracellular domains. Immunity 2;439-449, 1995 https://doi.org/10.1016/1074-7613(95)90025-X
  16. Selvakumar A, Steffens U, Dupont B: NK cell receptor gene of the KIR family with two Ig domains but highest homology to KIR receptors with three Ig domains. Tissue Antigens 48; 285-295, 1996 https://doi.org/10.1111/j.1399-0039.1996.tb02647.x
  17. Wagtmann N, Rajagopalan S, Winter CC, Peruzzi M, Long EO: Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and by functional transfer. Immunity 3;801-809, 1995 https://doi.org/10.1016/1074-7613(95)90069-1
  18. Fan QR, Garboczi DN, Winter CC, Wagtmann N, Long EO, Wiley DC: Direct binding of a soluble natural killer cell inhibitory receptor to a soluble human leukocyte antigen-Cw4 class I major histocompatibility complex molecule. Proc Natl Acad Sci USA 93;7178-7183, 1996
  19. Kim J, Chwae YJ, Kim MY, Choi IH, Park JH, Kim SJ: Molecular basis of HLA-C recognition by p58 natural killer cell inhibitory receptors. J Immunol 159;3875-3882, 1997
  20. Rojo S, Wagtmann N, Long EO: Binding of a soluble p70 killer cell inhibitory receptor to HLA-B*5101: requirement for all three p70 immunoglobulin domains. Eur J Immunol 27;568-571, 1997 https://doi.org/10.1002/eji.1830270231
  21. Binstadt BA, Brumbaugh KM, Dick CJ, Scharenberg AM, Williams BL, Colonna M, Lanier LL, Kinet JP, Abraham RT, Leibson PJ: Sequential involvement of Lck and SHP-1 with MHC-recognizing receptors on NK cells inhibits FcR-initiated tyrosine kinase activation. Immunity 5;629-638, 1996 https://doi.org/10.1016/S1074-7613(00)80276-9
  22. Burshtyn DN, Scharenberg AM, Wagtman N, Rajagopalan S, Berrada K, Yi T, Kinet JP, Long EO: Recruitment of tyrosine phosphatase HCP by the killer cell inhibitor receptor. Immunity 4;77-85, 1996 https://doi.org/10.1016/S1074-7613(00)80300-3
  23. Fry AM, Lanier LL, Weiss A: Phosphotyrosines in the killer cell inhibitory receptor motif of NKB1 are required for negative signaling and for association with protein phosphatase 1C. J Exp Med 184;295-300, 1996 https://doi.org/10.1084/jem.184.1.295
  24. Campbell KS, Dessing M, Lopez-Botet M, Cella M, Colonna M: Tyrosine phosphorylation of a human killer inhibitory receptor recruits protein tyrosine phosphatase 1C. J Exp Med 184;93-100, 1996 https://doi.org/10.1084/jem.184.1.93
  25. Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV: A 13-amino-acid motif in the cytoplasmic domain of FcgRIIB modulates B-cell receptor signaling. Nature 369;70-74, 1994
  26. Thomas ML: Of ITAMs and ITIMs: turning on and off the B cell antigen receptor. J Exp Med 181;1953-1956, 1995 https://doi.org/10.1084/jem.181.6.1953
  27. Ono M, Bolland S, Tempst P, Ravetch JV: Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor FcgRIIB. Nature 383;263-266, 1996 https://doi.org/10.1038/383263a0
  28. Daeron M, Latour S, Malbec O, Espinosa E, Pina P, Pasmans S, Fridman WH: The same tyrosine-based inhibition motif, in the intracytoplasmic domain of FcgRIIB, regulates negatively BCR-, TCR-, and FCR-dependent cell activation. Immunity 3;635-646, 1995 https://doi.org/10.1016/1074-7613(95)90134-5
  29. Reth M: Antigen receptor tail clue. Nature 338;383-384, 1989
  30. Cambier JC: New nomenclature for the Reth motif (or ARH1/ TAM/ARAM/YXXL). Immunol Today 16;110, 1995
  31. Olcese L, Lang P, Vely F, Cambiaggi A, Marguet D, Blery M, Hippen KL, Biassoni R, Moretta A, Moretta L, Cambier JC, Vivier E: Human and mouse killer-cell inhibitory receptors recruit PTP1C and PTP1D protein tyrosine phosphatases. J Immunol 156;4531-4534, 1996
  32. Marti F, Wilson C, Selvakumar A, Brent R, Dupont B, King PD: Lck-phosphorylated human killer cell-inhibitory receptors recruit and activate phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 95;11810-11815, 1998
  33. Raab M, Rudd CE: Hematopoietic cell phosphatase (HCP) regulates P56lck phosphorylation and ZAP-70 binding to T cell receptor zeta chain. Biochem Biophys Res Commun 222; 50-57, 1996
  34. 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 184; 2243-2250, 1996 https://doi.org/10.1084/jem.184.6.2243
  35. Binstadt BA, Billadeau DD, Jevremovic D, Williams BL, Fang N, Yi T, Koretzky GA, Abraham RT, Leibson PJ: Slp-76 is a direct substrate of SHP-1 recruited to killer cell inhibitory receptors. J Biochem Chem 273;27518-27523, 1998
  36. Pelicci G, Lanfrancone L, Grignani F, McGlade J, Cavallo F, Forni G, Nicoletti I, Grignani F, Pawson T, Pelicci PG: A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70;93- 104, 1992 https://doi.org/10.1016/0092-8674(92)90536-L
  37. Kavanaugh MW, Williams LT: An alternative to SH2 domains for binding tyrosine-phosphorylated proteins. Science 266; 1862-1865, 1994 https://doi.org/10.1126/science.7527937
  38. Simeoni L, Kliche S, Lindquist J, Schraven B: Adaptors and linkers in T and B cells. Curr Opin Immunol 16;304-313, 2004 https://doi.org/10.1016/j.coi.2004.03.001
  39. Bonfini L, Migliaccio E, Pelicci G, Lanfrancone L, Pelicci P: Not all Shc's roads lead to Ras. Trens Biochem Sci 21;257- 261, 1996 https://doi.org/10.1016/S0968-0004(96)10033-5
  40. Van der Geer P, Pawson T: The PTB domain: a new protein module implicated in signal transduction. Trends Biochem Sci 20;277-280, 1995 https://doi.org/10.1016/S0968-0004(00)89043-X
  41. Gu H, Maeda H, Moon JJ, Lord JD, Yoakim M, Nelson BH, Neel BG: New role for Shc in activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol Cell Biol 20;7109-7120, 2000 https://doi.org/10.1128/MCB.20.19.7109-7120.2000
  42. Cho HI, Park CG, Kim J: Reconstitution of killer cell inhibitory receptor-mediated signal transduction machinery in a cell-free model sysytem. Arch Biochem Biophys 368;221-231, 1999 https://doi.org/10.1006/abbi.1999.1334
  43. Cho HI, Park CG, Kim J: The cytoplasmic tail of killer inhibitory receptor (KIR) associates with TCR$\zeta$ in a phosphorylation dependent manner. Immunol Lett 68;339-345, 1999 https://doi.org/10.1016/S0165-2478(99)00057-7
  44. Lee SY, Park CG, Choi YI: T cell receptor-dependent cell death of T cell hybridomas mediated by the CD30 cytoplasmic domain in association with tumor necrosis factor receptor-associated factors. J Exp Med 183;669-674, 1996 https://doi.org/10.1084/jem.183.2.669
  45. Gunning P, Leavitt J, Muscat G, Ng SY, Kedes LA: Human beta-actin expression vector system directs high-level accumulation of antisense transcripts. Proc Natl Acad Sci USA 84; 4831-4835, 1987
  46. Blery M, Delon J, Trautmann A, Cambiaggi A, Olcese L, Biassoni R, Moretta L, Charvier P, Moretta A, Daeron M, Vivier E: Reconstituted killer cell inhibitory receptors for major histocompatibility complex class I molecules control mast cell activation induced via immunoreceptor tyrosine-based activation motifs. J Biol Chem 272;8989-8996, 1997 https://doi.org/10.1074/jbc.272.14.8989
  47. Bottino C, Vitale M, Pende D, Biassoni R, Moretta A: Receptors for HLA class I molecules in human NK cells. Semin Immunol 7;67-73, 1995 https://doi.org/10.1006/smim.1995.0010
  48. 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 92;83-92, 1998 https://doi.org/10.1016/S0092-8674(00)80901-0
  49. Lowenstein EJ, Daly RJ, Batzer AG, Li W, Margolis B, Lammers R, Ullrich A, Skolnik EY, Barsagi D, Schlessinger J: The SH2 and SH3 domain-containing protein Grb2 links receptor tyrosine kinases to ras signaling. Cell 70;431-442, 1992 https://doi.org/10.1016/0092-8674(92)90167-B
  50. Sarmay G, Koncz G, Gergely J: Human type II Fc $\gamma$ receptors inhibit B cell activation by interacting with the $p21^{ras}$dependent pathway. J Biol Chem 271;30499-30504, 1996 https://doi.org/10.1074/jbc.271.48.30499
  51. Ravichandran KS, Lee KK, Songyang Z, Cantley LC, Burn P, Burakoff SJ: Interaction of Shc with the zeta chain of the T cell receptor upon T cell activation. Science 262;902-905, 1993 https://doi.org/10.1126/science.8235613
  52. Rozakis-Adcock M, McGlade J, Mbamalu G, Pelicci G, Daly R, Li W, Batzer A, Thomas S, Brugge J, Pelicci PG, et al: Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360;689-692, 1992 https://doi.org/10.1038/360689a0
  53. Gotoh N, Tojo A, Shibuya M: A novel pathway from phosphorylation of tyrosine residues 239/240 of Shc, contributing to suppress apoptosis by IL-3. EMBO J 15;6197-6204, 1996
  54. Gotoh N, Toyoda M, Shibuya M: Tyrosine phosphorylation sites at amino acids 239 and 240 of Shc are involved in epidermal growth factor-induced mitogenic signaling that is distinct from Ras/mitogen-activated protein kinase activation. Mol Cell Biol 17;1824-1831, 1997 https://doi.org/10.1128/MCB.17.4.1824
  55. Lai KM, Oliver JP, Gish GD, Henkemeyer M, McGlade J, Pawson T: A Drosophila shc gene product is implicated in signaling by the DER receptor tyrosine kinase. Mol Cell Biol 15;4810-4818, 1995 https://doi.org/10.1128/MCB.15.9.4810
  56. Li K, Shao R, Hung MC: Collagen-homology domain 1 deletion mutant of Shc suppresses transformation mediated by neu through a MAPK-independent pathway. Oncogene 18; 2617-2626, 1999 https://doi.org/10.1038/sj.onc.1202605
  57. Mingari MC, Schiavetti F, Ponte M, Vitale C, Maggi E, Romanaugnani S, Demarest J, Pantaleo G, Fauci A, Moretta L: Human $CD8^+$ T lymphocyte subsets that express HLA class I-specific inhibitory receptors represent oligoclonally or monoclonally expanded cell populations. Proc Natl Acad Sci USA 93;12433-12438, 1996
  58. O'Shea JJ, McVicar DW, Bailey TL, Burns C, Smyth MJ: Activation of human peripheral blood T lymphocytes by pharmacological induction of protein tyrosine phosphorylation. Proc Natl Acad Sci USA 89;10306-10310, 1992