Murine natural killer immunoreceptors use distinct proximal signaling complexes to direct cell function

Blood

Volumn 121, Issue 16, 2013, Pages 3135-3146

  May, Rebecca M ^a,b   Okumura, Mariko ^a   Hsu, Chin Jung ^c   Bassiri, Hamid ^d   Yang, Enjun ^a   Rak, Gregory ^d   Mace, Emily M ^d   Philip, Naomi H ^a   Zhang, Weiguo ^e   Baumgart, Tobias ^c   Orange, Jordan S ^d   Nichols, Kim E ^d   Kambayashi, Taku ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; GAMMA INTERFERON; LAT PROTEIN; LAT1 PROTEIN; LAT2 PROTEIN; LY49D RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN SH2; PROTEIN SLP 76; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; AMINO ACID TRANSPORTER; CD98 ANTIGEN; FYB PROTEIN, MOUSE; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SLC7A7 PROTEIN, MOUSE; SLC7A8 PROTEIN, MOUSE; SLP 76 SIGNAL TRANSDUCING ADAPTOR PROTEINS; SLP-76 SIGNAL TRANSDUCING ADAPTOR PROTEINS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MATURATION; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DEGRANULATION; ENZYME PHOSPHORYLATION; FEMALE; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; MEMBRANE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR ENGRAFTMENT; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; NEOPLASM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID TRANSPORT SYSTEM Y+; ANIMALS; ANTIGENS, CD98 LIGHT CHAINS; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; INTERFERON-GAMMA; KILLER CELLS, NATURAL; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; NEOPLASMS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

MLCS; MLOWN;

EID: 84879172156     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-12-474361     Document Type: Article

References (42)

1. Yokoyama WM. Natural killer cell immune responses. Immunol Res. 2005;32(1-3): 317-325.
2. Di Santo JP. Natural killer cell developmental pathways: A question of balance. Annu Rev Immunol. 2006;24:257-286.
3. Lanier LL. NK cell recognition. Annu Rev Immunol. 2005;23:225-274.
4. Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol. 2008;9(5): 495-502.
5. Zou T, May RM, Koretzky GA. Understanding signal integration through targeted mutations of an adapter protein. FEBS Lett. 2010;584(24): 4901-4909.
6. Jordan MS, Koretzky GA. Coordination of receptor signaling in multiple hematopoietic cell lineages by the adaptor protein SLP-76. Cold Spring Harb Perspect Biol. 2010;2(4): A002501.
7. Kambayashi T, Okumura M, Baker RG, et al. Independent and cooperative roles of adaptor molecules in proximal signaling during FcepsilonRI-mediated mast cell activation. Mol Cell Biol. 2010;30(17): 4188-4196.
8. Peterson EJ, Clements JL, Ballas ZK, et al. NK cytokine secretion and cytotoxicity occur independently of the SLP-76 adaptor protein. Eur J Immunol. 1999;29(7):2223-2232.
9. Zhang W, Sommers CL, Burshtyn DN, et al. Essential role of LAT in T cell development. Immunity. 1999;10(3):323-332.
10. Chiesa S, Mingueneau M, Fuseri N, et al. Multiplicity and plasticity of natural killer cell signaling pathways. Blood. 2006;107(6): 2364-2372.
11. Hidano S, Sasanuma H, Ohshima K, et al. Distinct regulatory functions of SLP-76 and MIST in NK cell cytotoxicity and IFN-gamma production. Int Immunol. 2008;20(3):345-352.
12. Clements JL, Yang B, Ross-Barta SE, et al. Requirement for the leukocyte-specific adapter protein SLP-76 for normal T cell development. Science. 1998;281(5375):416-419.
13. Maltzman JS, Kovoor L, Clements JL, et al. Conditional deletion reveals a cell-autonomous requirement of SLP-76 for thymocyte selection. J Exp Med. 2005;202(7):893-900.
14. Volná P, Lebduska P, Dráberová L, et al. Negative regulation of mast cell signaling and function by the adaptor LAB/NTAL. J. Exp. Med. 2004;200(8):1001-1013.
15. Nuñez-Cruz S, Aguado E, Richelme S, et al. LAT regulates gammadelta T cell homeostasis and differentiation. Nat. Immunol. 2003;4(10): 999-1008.
16. Peterson EJ, Woods ML, Dmowski SA, et al. Coupling of the TCR to integrin activation by Slap-130/Fyb. Science. 2001;293(5538): 2263-2265.
17. Singer AL, Bunnell SC, Obstfeld AE, et al. Roles of the proline-rich domain in SLP-76 subcellular localization and T cell function. J Biol Chem. 2004;279(15):15481-15490.
18. Myung PS, Derimanov GS, Jordan MS, et al. Differential requirement for SLP-76 domains in T cell development and function. Immunity. 2001; 15(6):1011-1026.
19. Roth C, Rothlin C, Riou S, et al. Stromal-cell regulation of natural killer cell differentiation. J Mol Med (Berl). 2007;85(10):1047-1056.
20. Trotta R, Puorro KA, Paroli M, et al. Dependence of both spontaneous and antibody-dependent, granule exocytosismediated NK cell cytotoxicity on extracellular signal-regulated kinases. J Immunol. 1998; 161(12):6648-6656.
21. Guo H, Samarakoon A, Vanhaesebroeck B, et al. The p110 delta of PI3K plays a critical role in NK cell terminal maturation and cytokine/chemokine generation. J Exp Med. 2008;205(10):2419-2435.
22. Jiang K, Zhong B, Gilvary DL, et al. Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells. Nat Immunol. 2000;1(5):419-425.
23. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009; 457(7229):557-561.
24. Steelman LS, Chappell WH, Abrams SL, et al. Roles of the Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR pathways in controlling growth and sensitivity to therapy-implications for cancer and aging. Aging (Albany NY). 2011;3(3): 192-222.
25. Joncker NT, Fernandez NC, Treiner E, et al. NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: The rheostat model. J Immunol. 2009; 182(8):4572-4580.
26. Brodin P, Lakshmikanth T, Johansson S, et al. The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells. Blood. 2009; 113(11):2434-2441.
27. Kim S, Poursine-Laurent J, Truscott SM, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature. 2005;436(7051): 709-713.
28. Furukawa H, Iizuka K, Poursine-Laurent J, et al. A ligand for the murine NK activation receptor Ly-49D: Activation of tolerized NK cells from beta 2-microglobulin-deficient mice. J Immunol. 2002; 169(1):126-136.
29. Ito M, Hiramatsu H, Kobayashi K, et al. NOD/SCID/gamma(c)(null) mouse: An excellent recipient mouse model for engraftment of human cells. Blood. 2002;100(9): 3175-3182.
30. Fostel LV, Dluzniewska J, Shimizu Y, Burbach BJ, Peterson EJ. ADAP is dispensable for NK cell development and function. Int. Immunol. 2006; 18(8):1305-1314.
31. Mingueneau M, Roncagalli R, Grégoire C, et al. Loss of the LAT adaptor converts antigenresponsive T cells into pathogenic effectors that function independently of the T cell receptor. Immunity. 2009;31(2):197-208.
32. Zhu M, Koonpaew S, Liu Y, et al. Negative regulation of T cell activation and autoimmunity by the transmembrane adaptor protein LAB. Immunity. 2006;25(5):757-768.
33. Grégoire C, Simova S, Wang Y, et al. Deletion of the LIME adaptor protein minimally affects T and B cell development and function. Eur J Immunol. 2007;37(11):3259-3269.
34. Wu JN, Koretzky GA. The SLP-76 family of adapter proteins. Semin Immunol. 2004;16(6): 379-393.
35. Caraux A, Kim N, Bell SE, et al. Phospholipase C-gamma2 is essential for NK cell cytotoxicity and innate immunity to malignant and virally infected cells. Blood. 2006;107(3): 994-1002.
36. Regunathan J, Chen Y, Kutlesa S, et al. Differential and nonredundant roles of phospholipase Cgamma2 and phospholipase Cgamma1 in the terminal maturation of NK cells. J Immunol. 2006; 177(8):5365-5376.
37. Colucci F, Schweighoffer E, Tomasello E, et al. Natural cytotoxicity uncoupled from the Syk and ZAP-70 intracellular kinases. Nat Immunol. 2002; 3(3):288-294.
38. Lowin-Kropf B, Kunz B, Schneider P, et al. A role for the src family kinase Fyn in NK cell activation and the formation of the repertoire of Ly49 receptors. Eur J Immunol. 2002;32(3):773-782.
39. Whittaker GC, Burshtyn DN, Orr SJ, 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(7):2869-2877.
40. Tassi I, Le Friec G, Gilfillan S, et al. DAP10 associates with Ly49 receptors but contributes minimally to their expression and function in vivo. Eur J Immunol. 2009;39(4): 1129-1135.
41. Billadeau DD, Upshaw JL, Schoon RA, et al. NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat Immunol. 2003;4(6):557-564.
42. Arase N, Arase H, Park SY, et al. Association with FcRgamma is essential for activation signal through NKR-P1 (CD161) in natural killer (NK) cells and NK1.11 T cells. J Exp Med. 1997;186(12):1957-1963.