NKp46 clusters at the immune synapse and regulates NK cell polarization

Frontiers in Immunology

Volumn 6, Issue SEP, 2015, Pages

  Hadad, Uzi ^a,b   Thauland, Timothy J ^a   Martinez, Olivia M ^a   Butte, Manish J ^a   Porgador, Angel ^b   Krams, Sheri M ^a  

^a STANFORD UNIVERSITY   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Cellular activation; Cytoskeleton rearrangement; Cytotoxicity; Immune synapse; NKp46

Indexed keywords

NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1;

ARTICLE; CELL VIABILITY; CYTOTOXICITY; DIAGNOSTIC IMAGING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; LIVER CELL CARCINOMA; NEUROMUSCULAR SYNAPSE; NK T CELL LYMPHOMA; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

EID: 84946575485     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00495     Document Type: Article

References (79)

1. Herberman RB, Nunn ME, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. I. Distribution of reactivity and specificity. Int J Cancer (1975) 16:216-29. doi:10.1002/ijc.2910160204.
2. Kiessling R, Klein E, Wigzell H. "Natural" killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol (1975) 5:112-7. doi:10.1002/eji.1830050208.
3. Welsh RM Jr. Cytotoxic cells induced during lymphocytic choriomeningitis virus infection of mice. I. Characterization of natural killer cell induction. J Exp Med (1978) 148:163-81. doi:10.1084/jem.148.1.163.
4. Orange JS. Natural killer cell deficiency. J Allergy Clin Immunol (2013) 132:515-25. doi:10.1016/j.jaci.2013.07.020.
5. Bukowski JF, Woda BA, Welsh RM. Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J Virol (1984) 52:119-28.
6. Westermann J, Pabst R. Distribution of lymphocyte subsets and natural killer cells in the human body. Clin Investig (1992) 70:539-44. doi:10.1007/BF00184787.
7. Baume DM, Robertson MJ, Levine H, Manley TJ, Schow PW, Ritz J. Differential responses to interleukin 2 define functionally distinct subsets of human natural killer cells. Eur J Immunol (1992) 22:1-6. doi:10.1002/eji.1830220102.
8. Ljunggren H, Kärre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol Today (1990) 11:237-44. doi:10.1016/0167-5699(90)90097-S.
9. Moretta A, Vitale M, Bottino C, Orengo AM, Morelli L, Augugliaro R, et al. P58 molecules as putative receptors for major histocompatibility complex (MHC) class I molecules in human natural killer (NK) cells. Anti-p58 antibodies reconstitute lysis of MHC class I-protected cells in NK clones displaying different specificities. J Exp Med (1993) 178:597-604. doi:10.1084/jem.178.2.597.
10. Karlhofer FM, Ribaudo RK, Yokoyama WM. MHC class I alloantigen specificity of Ly-49 IL-2-activated natural killer cells. Nature (1992) 358:66-70. doi:10.1038/358066a0.
11. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science (1999) 285:727. doi:10.1126/science.285.5428.727.
12. Sivori S, Vitale M, Morelli L, Sanseverino L, Augugliaro R, Bottino C, et al. p46, a novel natural killer cell-specific surface molecule that mediates cell activation. J Exp Med (1997) 186:1129. doi:10.1084/jem.186.7.1129.
13. Vitale M, Bottino C, Sivori S, Sanseverino L, Castriconi R, Marcenaro E, et al. NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non-major histocompatibility complex-restricted tumor cell lysis. J Exp Med (1998) 187:2065. doi:10.1084/jem.187.12.2065.
14. Pende D, Parolini S, Pessino A, Sivori S, Augugliaro R, Morelli L, et al. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J Exp Med (1999) 190:1505. doi:10.1084/jem.190.10.1505.
15. Biassoni R, Pessino A, Bottino C, Pende D, Moretta L, Moretta A. The murine homologue of the human NKp46, a triggering receptor involved in the induction of natural cytotoxicity. Eur J Immunol (1999) 29:1014-20. doi:10.1002/(SICI)1521-4141(199903)29:03<1014::AID-IMMU1014>3.0.CO;2-O.
16. Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, et al. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol (2006) 7:517-23. doi:10.1038/ni1322.
17. Eckelhart E, Warsch W, Zebedin E, Simma O, Stoiber D, Kolbe T, et al. A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK-cell survival and development. Blood (2011) 117:1565-73. doi:10.1182/blood-2010-06-291633.
18. Narni-Mancinelli E, Jaeger BN, Bernat C, Fenis A, Kung S, De Gassart A, et al. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science (2012) 335:344. doi:10.1126/science.1215621.
19. Narni-Mancinelli E, Chaix J, Fenis A, Kerdiles YM, Yessaad N, Reynders A, et al. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc Natl Acad Sci U S A (2011) 108:18324-9. doi:10.1073/pnas.1112064108.
20. Walzer T, Bléry M, Chaix J, Fuseri N, Chasson L, Robbins SH, et al. Identification, activation, and selective in vivo ablation of mouse NK cells via NKp46. Proc Natl Acad Sci U S A (2007) 104:3384. doi:10.1073/pnas.0609692104.
21. Pessino A, Sivori S, Bottino C, Malaspina A, Morelli L, Moretta L, et al. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J Exp Med (1998) 188:953. doi:10.1084/jem.188.5.953.
22. Westgaard IH, Berg SF, Vaage JT, Wang LL, Yokoyama WM, Dissen E, et al. Rat NKp46 activates natural killer cell cytotoxicity and is associated with FcepsilonRIgamma and CD3zeta. J Leukoc Biol (2004) 76:1200-6. doi:10.1189/jlb.0903428.
23. Cantoni C, Ponassi M, Biassoni R, Conte R, Spallarossa A, Moretta A, et al. The three-dimensional structure of the human NK cell receptor NKp44, a triggering partner in natural cytotoxicity. Structure (2003) 11:725-34. doi:10.1016/S0969-2126(03)00095-9.
24. Foster CE, Colonna M, Sun PD. Crystal structure of the human natural killer (NK) cell activating receptor NKp46 reveals structural relationship to other leukocyte receptor complex immunoreceptors. J Biol Chem (2003) 278:46081-6. doi:10.1074/jbc. M308491200.
25. Arnon TI, Achdout H, Lieberman N, Gazit R, Gonen-Gross T, Katz G, et al. The mechanisms controlling the recognition of tumor-and virus-infected cells by NKp46. Blood (2004) 103:664. doi:10.1182/blood-2003-05-1716.
26. Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, et al. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature (2001) 409:1055-60. doi:10.1038/35059110.
27. Mendelson M, Tekoah Y, Zilka A, Gershoni-Yahalom O, Gazit R, Achdout H, et al. NKp46 O-glycan sequences that are involved in the interaction with hemagglutinin type 1 of influenza virus. J Virol (2010) 84:3789. doi:10.1128/JVI.01815-09.
28. Jarahian M, Watzl C, Fournier P, Arnold A, Djandji D, Zahedi S, et al. Activation of natural killer cells by Newcastle disease virus hemagglutinin-neuraminidase. J Virol (2009) 83:8108. doi:10.1128/JVI.00211-09.
29. Garg A, Barnes PF, Porgador A, Roy S, Wu S, Nanda JS, et al. Vimentin expressed on Mycobacterium tuberculosis-infected human monocytes is involved in binding to the NKp46 receptor. J Immunol (2006) 177:6192. doi:10.4049/jimmunol.177.9.6192.
30. Hershkovitz O, Jarahian M, Zilka A, Bar-Ilan A, Landau G, Jivov S, et al. Altered glycosylation of recombinant NKp30 hampers binding to heparan sulfate: a lesson for the use of recombinant immunoreceptors as an immunological tool. Glycobiology (2008) 18:28. doi:10.1093/glycob/cwm125.
31. Hecht ML, Rosental B, Horlacher T, Hershkovitz O, De Paz JL, Noti C, et al. Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences. J Proteome Res (2009) 8:712-20. doi:10.1021/pr800747c.
32. Porgador A, Brusilovsky M, Radinsky O, Yossef R, Campbell KS. Carbohydrate-mediated modulation of NK cell receptor function: structural and functional influences of heparan sulfate moieties expressed on NK cell surface. Front Oncol (2014) 4:185. doi:10.3389/fonc.2014.00185.
33. Koch J, Steinle A, Watzl C, Mandelboim O. Activating natural cytotoxicity receptors of natural killer cells in cancer and infection. Trends Immunol (2013) 34:182-91. doi:10.1016/j.it.2013.01.003.
34. Gur C, Porgador A, Elboim M, Gazit R, Mizrahi S, Stern-Ginossar N, et al. The activating receptor NKp46 is essential for the development of type 1 diabetes. Nat Immunol (2010) 11:121-8. doi:10.1038/ni.1834.
35. Gur C, Enk J, Kassem SA, Suissa Y, Magenheim J, Stolovich-Rain M, et al. Recognition and killing of human and murine pancreatic beta cells by the NK receptor NKp46. J Immunol (2011) 187:3096-103. doi:10.4049/jimmunol.1101269.
36. Elhaik-Goldman S, Kafka D, Yossef R, Hadad U, Elkabets M, Vallon-Eberhard A, et al. The natural cytotoxicity receptor 1 contribution to early clearance of Streptococcus pneumoniae and to natural killer-macrophage cross talk. PLoS One (2011) 6:e23472. doi:10.1371/journal.pone.0023472.
37. Gur C, Doron S, Kfir-Erenfeld S, Horwitz E, Abu-Tair L, Safadi R, et al. NKp46-mediated killing of human and mouse hepatic stellate cells attenuates liver fibrosis. Gut (2012) 61:885-93. doi:10.1136/gutjnl-2011-301400.
38. Golden-Mason L, Stone AE, Bambha KM, Cheng L, Rosen HR. Race-and gender-related variation in natural killer p46 expression associated with differential anti-hepatitis c virus immunity. Hepatology (2012) 56:1214-22. doi:10.1002/hep.25771.
39. Yossef R, Gur C, Shemesh A, Guttman O, Hadad U, Nedvetzki S, et al. Targeting natural killer cell reactivity by employing antibody to NKp46: implications for type 1 diabetes. PLoS One (2015) 10:e0118936. doi:10.1371/journal.pone.0118936.
40. Ghadially H, Ohana M, Elboim M, Gazit R, Gur C, Nagler A, et al. NK cell receptor NKp46 regulates graft-versus-host disease. Cell Rep (2014) 7:1809-14. doi:10.1016/j.celrep.2014.05.011.
41. Ghadially H, Horani A, Glasner A, Elboim M, Gazit R, Shoseyov D, et al. NKp46 regulates allergic responses. Eur J Immunol (2013) 43:3006-16. doi:10.1002/eji.201343388.
42. Davis DM, Chiu I, Fassett M, Cohen GB, Mandelboim O, Strominger JL. The human natural killer cell immune synapse. Proc Natl Acad Sci U S A (1999) 96:15062. doi:10.1073/pnas.96.26.15062.
43. Mace EM, Dongre P, Hsu H, Sinha P, James AM, Mann SS, et al. Cell biological steps and checkpoints in accessing NK cell cytotoxicity. Immunol Cell Biol (2014) 92:245-55. doi:10.1038/icb.2013.96.
44. Edelstein AD, Tsuchida MA, Amodaj N, Pinkard H, Vale RD, Stuurman N. Advanced methods of microscope control using μ Manager software. J Biol Methods (2014) 1:e11. doi:10.14440/jbm.2014.36.
45. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods (2012) 9:676-82. doi:10.1038/nmeth.2019.
46. Vyas YM, Maniar H, Dupont B. Visualization of signaling pathways and cortical cytoskeleton in cytolytic and noncytolytic natural killer cell immune synapses. Immunol Rev (2002) 189:161-78. doi:10.1034/j.1600-065X.2002.18914.x.
47. Bertrand F, Muller S, Roh KH, Laurent C, Dupre L, Valitutti S. An initial and rapid step of lytic granule secretion precedes microtubule organizing center polarization at the cytotoxic T lymphocyte/target cell synapse. Proc Natl Acad Sci U S A (2013) 110:6073-8. doi:10.1073/pnas.1218640110.
48. Orange JS, Ramesh N, Remold-O'Donnell E, Sasahara Y, Koopman L, Byrne M, et al. Wiskott-Aldrich syndrome protein is required for NK cell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc Natl Acad Sci U S A (2002) 99:11351-6. doi:10.1073/pnas.162376099.
49. Orange JS, Harris KE, Andzelm MM, Valter MM, Geha RS, Strominger JL. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc Natl Acad Sci U S A (2003) 100:14151. doi:10.1073/pnas.1835830100.
50. Brown AC, Dobbie IM, Alakoskela J, Davis I, Davis DM. Super-resolution imaging of remodeled synaptic actin reveals different synergies between NK cell receptors and integrins. Blood (2012) 120:3729-40. doi:10.1182/blood-2012-05-429977.
51. Rak GD, Mace EM, Banerjee PP, Svitkina T, Orange JS. Natural killer cell lytic granule secretion occurs through a pervasive actin network at the immune synapse. PLoS Biol (2011) 9:e1001151. doi:10.1371/journal.pbio.1001151.
52. Orange J, Stone K, Turvey S, Krzewski K. The Wiskott-Aldrich syndrome. Cell Mole Life Sci (2004) 61:2361-85. doi:10.1007/s00018-004-4086-z.
53. Huang W, Ochs HD, Dupont B, Vyas YM. The Wiskott-Aldrich syndrome protein regulates nuclear translocation of NFAT2 and NF-kappa B (RelA) independently of its role in filamentous actin polymerization and actin cytoskeletal rearrangement. J Immunol (2005) 174:2602-11. doi:10.4049/jimmunol.174.8.5134.
54. Mentlik AN, Sanborn KB, Holzbaur EL, Orange JS. Rapid lytic granule convergence to the MTOC in natural killer cells is dependent on dynein but not cytolytic commitment. Mol Biol Cell (2010) 21:2241-56. doi:10.1091/mbc. E09-11-0930.
55. Wulfing C, Purtic B, Klem J, Schatzle JD. Stepwise cytoskeletal polarization as a series of checkpoints in innate but not adaptive cytolytic killing. Proc Natl Acad Sci U S A (2003) 100:7767-72. doi:10.1073/pnas.1336920100.
56. Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM. Centrosome polarization delivers secretory granules to the immunological synapse. Nature (2006) 443:462-5. doi:10.1038/nature05071.
57. Vyas YM, Mehta KM, Morgan M, Maniar H, Butros L, Jung S, et al. Spatial organization of signal transduction molecules in the NK cell immune synapses during MHC class I-regulated noncytolytic and cytolytic interactions. J Immunol (2001) 167:4358. doi:10.4049/jimmunol.167.8.4358.
58. Carlin LM, Eleme K, McCann FE, Davis DM. Intercellular transfer and supramolecular organization of human leukocyte antigen C at inhibitory natural killer cell immune synapses. J Exp Med (2001) 194:1507-17. doi:10.1084/jem.194.10.1507.
59. Treanor B, Lanigan PM, Kumar S, Dunsby C, Munro I, Auksorius E, et al. Microclusters of inhibitory killer immunoglobulin-like receptor signaling at natural killer cell immunological synapses. J Cell Biol (2006) 174:153-61. doi:10.1083/jcb.200601108.
60. Endt J, McCann FE, Almeida CR, Urlaub D, Leung R, Pende D, et al. Inhibitory receptor signals suppress ligation-induced recruitment of NKG2D to GM1-rich membrane domains at the human NK cell immune synapse. J Immunol (2007) 178:5606. doi:10.4049/jimmunol.178.9.5606.
61. Guia S, Jaeger BN, Piatek S, Mailfert S, Trombik T, Fenis A, et al. Confinement of activating receptors at the plasma membrane controls natural killer cell tolerance. Sci Signal (2011) 4:ra21. doi:10.1126/scisignal.2001608.
62. Chen X, Trivedi PP, Ge B, Krzewski K, Strominger JL. Many NK cell receptors activate ERK2 and JNK1 to trigger microtubule organizing center and granule polarization and cytotoxicity. Proc Natl Acad Sci U S A (2007) 104:6329-34. doi:10.1073/pnas.0611655104.
63. Brown AC, Oddos S, Dobbie IM, Alakoskela J, Parton RM, Eissmann P, et al. Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol (2011) 9:e1001152. doi:10.1371/journal.pbio.1001152.
64. Bida AT, Upshaw NeffJL, Dick CJ, Schoon RA, Brickshawana A, Chini CC, et al. 2B4 utilizes ITAM-containing receptor complexes to initiate intracellular signaling and cytolysis. Mol Immunol (2011) 48:1149-59. doi:10.1016/j.molimm.2011.02.008.
65. Jaron-Mendelson M, Yossef R, Appel MY, Zilka A, Hadad U, Afergan F, et al. Dimerization of NKp46 receptor is essential for NKp46-mediated lysis: characterization of the dimerization site by epitope mapping. J Immunol (2012) 188:6165-74. doi:10.4049/jimmunol.1102496.
66. Bryceson YT, March ME, Ljunggren HG, Long EO. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood (2006) 107:159-66. doi:10.1182/blood-2005-04-1351.
67. Springer TA, Dustin ML. Integrin inside-out signaling and the immunological synapse. Curr Opin Cell Biol (2012) 24:107-15. doi:10.1016/j.ceb.2011.10.004.
68. Wai LE, Garcia JA, Martinez OM, Krams SM. Distinct roles for the NK cell-activating receptors in mediating interactions with dendritic cells and tumor cells. J Immunol (2011) 186:222. doi:10.4049/jimmunol.1002597.
69. Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, Münz C. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med (2002) 195:343. doi:10.1084/jem.20011149.
70. Spaggiari GM, Carosio R, Pende D, Marcenaro S, Rivera P, Zocchi MR, et al. NK cell-mediated lysis of autologous antigen-presenting cells is triggered by the engagement of the phosphatidylinositol 3-kinase upon ligation of the natural cytotoxicity receptors NKp30 and NKp46. Eur J Immunol (2001) 31:1656-65. doi:10.1002/1521-4141(200106)31:6<1656::AID-IMMU1656>3.0.CO;2-V.
71. Draghi M, Pashine A, Sanjanwala B, Gendzekhadze K, Cantoni C, Cosman D, et al. NKp46 and NKG2D recognition of infected dendritic cells is necessary for NK cell activation in the human response to influenza infection. J Immunol (2007) 178:2688. doi:10.4049/jimmunol.178.5.2688.
72. Magri G, Muntasell A, Romo N, Saez-Borderias A, Pende D, Geraghty DE, et al. NKp46 and DNAM-1 NK-cell receptors drive the response to human cytomegalovirus-infected myeloid dendritic cells overcoming viral immune evasion strategies. Blood (2011) 117:848-56. doi:10.1182/blood-2010-08-301374.
73. Borg C, Jalil A, Laderach D, Maruyama K, Wakasugi H, Charrier S, et al. NK cell activation by dendritic cells (DCs) requires the formation of a synapse leading to IL-12 polarization in DCs. Blood (2004) 104:3267-75. doi:10.1182/blood-2004-01-0380.
74. Nedvetzki S. Reciprocal regulation of natural killer cells and macrophages associated with distinct immune synapses. Blood (2007) 109:3776-85. doi:10.1182/blood-2006-10-052977.
75. Barreira da Silva R, Münz C. Natural killer cell activation by dendritic cells: balancing inhibitory and activating signals. Cell Mole Life Sci (2011) 68:1-14. doi:10.1007/s00018-011-0801-8.
76. Mace EM, Orange JS. Multiple distinct NK-cell synapses. Blood (2011) 118:6475-6. doi:10.1182/blood-2011-10-381392.
77. Bryceson YT, Ljunggren HG, Long EO. Minimal requirement for induction of natural cytotoxicity and intersection of activation signals by inhibitory receptors. Blood (2009) 114:2657-66. doi:10.1182/blood-2009-01-201632.
78. Horowitz A, Strauss-Albee DM, Leipold M, Kubo J, Nemat-Gorgani N, Dogan OC, et al. Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry. Sci Transl Med (2013) 5:208ra145. doi:10.1126/scitranslmed.3006702.
79. Rosental B, Brusilovsky M, Hadad U, Oz D, Appel MY, Afergan F, et al. Proliferating cell nucleur antigen is a novel inhibitory ligand for teh natural cytotoxicity receptor Nkp44. J. Immunol (2011) 187:5693-702. doi:10.4042/jimmunol.1102267.