Dimerization of NKp46 receptor is essential for NKp46-mediated lysis: Characterization of the dimerization site by epitope mapping

Journal of Immunology

Volumn 188, Issue 12, 2012, Pages 6165-6174

  Jaron Mendelson, Michal ^a   Yossef, Rami ^a   Appel, Michael Y ^a   Zilka, Alon ^a   Hadad, Uzi ^a   Afergan, Fabian ^a   Rosental, Benyamin ^a   Engel, Stanislav ^a   Nedvetzki, Shlomo ^b   Braiman, Alex ^a   Porgador, Angel ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b Bio LineRx   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; PEPTIDE 4; PEPTIDE 5; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOLYSIS; DEGRANULATION; DIMERIZATION; EPITOPE MAPPING; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; LIGAND BINDING; NATURAL KILLER CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SURFACE PROPERTY; TUMOR CELL DESTRUCTION;

AMINO ACID SEQUENCE; CELL LINE; EPITOPE MAPPING; FLOW CYTOMETRY; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; PEPTIDES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; SURFACE PLASMON RESONANCE; TRANSFECTION;

EID: 84862604056     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102496     Document Type: Article

References (55)

1. Arnon, T. I., G. Markel, and O. Mandelboim. 2006. Tumor and viral recognition by natural killer cells receptors. Semin. Cancer Biol. 16: 348-358. (Pubitemid 44311503)
2. López-Botet, M., M. Llano, F. Navarro, and T. Bellón. 2000. NK cell recognition of non-classical HLA class I molecules. Semin. Immunol. 12: 109-119. (Pubitemid 30199275)
3. Eissmann, P., and D. M. Davis. 2010. Inhibitory and regulatory immune synapses. Curr. Top. Microbiol. Immunol. 340: 63-79.
4. Cerwenka, A., and L. L. Lanier. 2001. Ligands for natural killer cell receptors: redundancy or specificity. Immunol. Rev. 181: 158-169. (Pubitemid 32703404)
5. Campbell, K. S., and M. Colonna. 2001. Human natural killer cell receptors and signal transduction. Int. Rev. Immunol. 20: 333-370. (Pubitemid 33146068)
6. Moretta, A., C. Bottino, M. Vitale, D. Pende, C. Cantoni, M. C. Mingari, R. Biassoni, and L. Moretta. 2001. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19: 197-223. (Pubitemid 32368034)
7. Moretta, L., C. Bottino, D. Pende, R. Castriconi, M. C. Mingari, and A. Moretta. 2006. Surface NK receptors and their ligands on tumor cells. Semin. Immunol. 18: 151-158. (Pubitemid 43817561)
8. Gazit, R., R. Gruda, M. Elboim, T. I. Arnon, G. Katz, H. Achdout, J. Hanna, U. Qimron, G. Landau, E. Greenbaum, et al. 2006. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat. Immunol. 7: 517-523.
9. Pogge von Strandmann, E., V. R. Simhadri, B. von Tresckow, S. Sasse, K. S. Reiners, H. P. Hansen, A. Rothe, B. Böll, V. L. Simhadri, P. Borchmann, et al. 2007. Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity 27: 965-974. (Pubitemid 350251218)
10. Brandt, C. S., M. Baratin, E. C. Yi, J. Kennedy, Z. Gao, B. Fox, B. Haldeman, C. D. Ostrander, T. Kaifu, C. Chabannon, et al. 2009. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J. Exp. Med. 206: 1495-1503.
11. Arnon, T. I., H. Achdout, O. Levi, G. Markel, N. Saleh, G. Katz, R. Gazit, T. Gonen-Gross, J. Hanna, E. Nahari, et al. 2005. Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat. Immunol. 6: 515-523. (Pubitemid 41716765)
12. Hecht, M. L., B. Rosental, T. Horlacher, O. Hershkovitz, J. L. De Paz, C. Noti, S. Schauer, A. Porgador, and P. H. Seeberger. 2009. Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences. J. Proteome Res. 8: 712-720.
13. Mandelboim, O., N. Lieberman, M. Lev, L. Paul, T. I. Arnon, Y. Bushkin, D. M. Davis, J. L. Strominger, J. W. Yewdell, and A. Porgador. 2001. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409: 1055-1060. (Pubitemid 32204059)
14. Ho, J. W., O. Hershkovitz, M. Peiris, A. Zilka, A. Bar-Ilan, B. Nal, K. Chu, M. Kudelko, Y. W. Kam, H. Achdout, et al. 2008. H5-type influenza virus hemagglutinin is functionally recognized by the natural killer-activating receptor NKp44. J. Virol. 82: 2028-2032. (Pubitemid 351206948)
15. Hershkovitz, O., B. Rosental, L. A. Rosenberg, M. E. Navarro-Sanchez, S. Jivov, A. Zilka, O. Gershoni-Yahalom, E. Brient-Litzler, H. Bedouelle, J. W. Ho, et al. 2009. NKp44 receptor mediates interaction of the envelope glycoproteins from the West Nile and dengue viruses with NK cells. J. Immunol. 183: 2610-2621.
16. Bloushtain, N., U. Qimron, A. Bar-Ilan, O. Hershkovitz, R. Gazit, E. Fima, M. Korc, I. Vlodavsky, N. V. Bovin, and A. Porgador. 2004. Membrane-associated heparan sulfate proteoglycans are involved in the recognition of cellular targets by NKp30 and NKp46. J. Immunol. 173: 2392-2401. (Pubitemid 39063095)
17. Hershkovitz, O., S. Jivov, N. Bloushtain, A. Zilka, G. Landau, A. Bar-Ilan, R. G. Lichtenstein, K. S. Campbell, T. H. van Kuppevelt, and A. Porgador. 2007. Characterization of the recognition of tumor cells by the natural cytotoxicity receptor, NKp44. Biochemistry 46: 7426-7436. (Pubitemid 46986369)
18. Ito, K., K. Higai, M. Sakurai, C. Shinoda, K. Yanai, Y. Azuma, and K. Matsumoto. 2011. Binding of natural cytotoxicity receptor NKp46 to sulfate-and α2,3-NeuAc-containing glycans and its mutagenesis. Biochem. Biophys. Res. Commun. 406: 377-382.
19. Garg, A., P. F. Barnes, A. Porgador, S. Roy, S. Wu, J. S. Nanda, D. E. Griffith, W. M. Girard, N. Rawal, S. Shetty, and R. Vankayalapati. 2006. Vimentin expressed on Mycobacterium tuberculosis-infected human monocytes is involved in binding to the NKp46 receptor. J. Immunol. 177: 6192-6198. (Pubitemid 44628837)
20. Geysen, H. M., S. J. Rodda, T. J. Mason, G. Tribbick, and P. G. Schoofs. 1987. Strategies for epitope analysis using peptide synthesis. J. Immunol. Methods 102: 259-274. (Pubitemid 17139413)
21. Joyce, M. G., P. Tran, M. A. Zhuravleva, J. Jaw, M. Colonna, and P. D. Sun. 2011. Crystal structure of human natural cytotoxicity receptor NKp30 and identification of its ligand binding site. Proc. Natl. Acad. Sci. USA 108: 6223-6228.
22. Loiarro, M., C. Sette, G. Gallo, A. Ciacci, N. Fantò, D. Mastroianni, P. Carminati, and V. Ruggiero. 2005. Peptide-mediated interference of TIR domain dimerization in MyD88 inhibits interleukin-1-dependent activation of NF-kappaB. J. Biol. Chem. 280: 15809-15814. (Pubitemid 40616701)
23. Kramer, J. M., W. Hanel, F. Shen, N. Isik, J. P. Malone, A. Maitra, W. Sigurdson, D. Swart, J. Tocker, T. Jin, and S. L. Gaffen. 2007. Cutting edge: identification of a pre-ligand assembly domain (PLAD) and ligand binding site in the IL-17 receptor. J. Immunol. 179: 6379-6383.
24. Cantoni, C., M. Ponassi, R. Biassoni, R. Conte, A. Spallarossa, A. Moretta, L. Moretta, M. Bolognesi, and D. Bordo. 2003. The three-dimensional structure of the human NK cell receptor NKp44, a triggering partner in natural cytotoxicity. Structure 11: 725-734. (Pubitemid 37281187)
25. Ponassi, M., C. Cantoni, R. Biassoni, R. Conte, A. Spallarossa, A. Pesce, A. Moretta, L. Moretta, M. Bolognesi, and D. Bordo. 2003. Structure of the human NK cell triggering receptor NKp46 ectodomain. Biochem. Biophys. Res. Commun. 309: 317-323. (Pubitemid 37025894)
26. Foster, C. E., M. Colonna, and P. D. Sun. 2003. Crystal structure of the human natural killer (NK) cell activating receptor NKp46 reveals structural relationship to other leukocyte receptor complex immunoreceptors. J. Biol. Chem. 278: 46081-46086. (Pubitemid 37432758)
27. Zilka, A., G. Landau, O. Hershkovitz, N. Bloushtain, A. Bar-Ilan, F. Benchetrit, E. Fima, T. H. van Kuppevelt, J. T. Gallagher, S. Elgavish, and A. Porgador. 2005. Characterization of the heparin/heparan sulfate binding site of the natural cytotoxicity receptor NKp46. Biochemistry 44: 14477-14485. (Pubitemid 41567456)
28. Arnon, T. I., H. Achdout, N. Lieberman, R. Gazit, T. Gonen-Gross, G. Katz, A. Bar-Ilan, N. Bloushtain, M. Lev, A. Joseph, et al. 2004. The mechanisms controlling the recognition of tumor- and virus-infected cells by NKp46. Blood 103: 664-672. (Pubitemid 38140102)
29. Miyazaki, J., K. Araki, E. Yamato, H. Ikegami, T. Asano, Y. Shibasaki, Y. Oka, and K. Yamamura. 1990. Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127: 126-132. (Pubitemid 20228111)
30. Esko, J. D. 1991. Genetic analysis of proteoglycan structure, function and metabolism. Curr. Opin. Cell Biol. 3: 805-816. (Pubitemid 121006137)
31. Zilka, A., M. Mendelson, B. Rosental, O. Hershkovitz, and A. Porgador. 2010. Generating NK cell receptor-Fc chimera proteins from 293T cells and considerations of appropriate glycosylation. Methods Mol. Biol. 612: 275-283.
32. Lecoeur, H., M. Février, S. Garcia, Y. Rivière, and M. L. Gougeon. 2001. A novel flow cytometric assay for quantitation and multiparametric characterization of cell-mediated cytotoxicity. J. Immunol. Methods 253: 177-187. (Pubitemid 32522525)
33. Hershkovitz, O., M. Jarahian, A. Zilka, A. Bar-Ilan, G. Landau, S. Jivov, Y. Tekoah, R. Glicklis, J. T. Gallagher, S. C. Hoffmann, et al. 2008. Altered glycosylation of recombinant NKp30 hampers binding to heparan sulfate: a lesson for the use of recombinant immunoreceptors as an immunological tool. Glycobiology 18: 28-41.
34. Schneidman-Duhovny, D., Y. Inbar, R. Nussinov, and H. J. Wolfson. 2005. PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res. 33(Web Server issue): W363-7.
35. Dina, D., N. Ruth, and J. W. Haim. 2002. Efficient unbound docking of rigid molecules. In Proceedings of the Second International Workshop on Algorithms in Bioinformatics. Springer-Verlag.
36. Mashiach, E., D. Schneidman-Duhovny, N. Andrusier, R. Nussinov, and H. J. Wolfson. 2008. FireDock: a web server for fast interaction refinement in molecular docking. Nucleic Acids Res. 36: W229-232.
37. Andrusier, N., R. Nussinov, and H. J. Wolfson. 2007. FireDock: fast interaction refinement in molecular docking. Proteins 69: 139-159. (Pubitemid 47339146)
38. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14: 33-8, 27-8.
39. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kalé, and K. Schulten. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26: 1781-1802. (Pubitemid 43078511)
40. MacKerell, A. D., D. Bashford, M. Bellott, R. L. Dunbrack, Jr., J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, et al. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102: 3586-3616. (Pubitemid 128576688)
41. Darnell, S. J., L. LeGault, and J. C. Mitchell. 2008. KFC Server: interactive forecasting of protein interaction hot spots. Nucleic Acids Res. 36(Web Server issue): W265-9.
42. Braiman, A., M. Barda-Saad, C. L. Sommers, and L. E. Samelson. 2006. Recruitment and activation of PLCgamma1 in T cells: a new insight into old domains. EMBO J. 25: 774-784. (Pubitemid 43292439)
43. Barda-Saad, M., A. Braiman, R. Titerence, S. C. Bunnell, V. A. Barr, and L. E. Samelson. 2005. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat. Immunol. 6: 80-89. (Pubitemid 40136699)
44. Zal, T., and N. R. Gascoigne. 2004. Using live FRET imaging to reveal early protein-protein interactions during T cell activation. Curr. Opin. Immunol. 16: 674-683.
45. Periasamy, A., and R. N. Day. 1999. Visualizing protein interactions in living cells using digitized GFP imaging and FRET microscopy. Methods Cell Biol. 58: 293-314.
46. Jares-Erijman, E. A., and T. M. Jovin. 2006. Imaging molecular interactions in living cells by FRET microscopy. Curr. Opin. Chem. Biol. 10: 409-416. (Pubitemid 44375073)
47. Springael, J. Y., E. Urizar, S. Costagliola, G. Vassart, and M. Parmentier. 2007. Allosteric properties of G protein-coupled receptor oligomers. Pharmacol. Ther. 115: 410-418. (Pubitemid 47362379)
48. Garrity, D., M. E. Call, J. Feng, and K. W. Wucherpfennig. 2005. The activating NKG2D receptor assembles in the membrane with two signaling dimers into a hexameric structure. Proc. Natl. Acad. Sci. USA 102: 7641-7646. (Pubitemid 40741024)
49. Gerber, D., N. Sal-Man, and Y. Shai. 2004. Two motifs within a transmembrane domain, one for homodimerization and the other for heterodimerization. J. Biol. Chem. 279: 21177-21182. (Pubitemid 38656521)
50. Tolar, P., H. W. Sohn, and S. K. Pierce. 2005. The initiation of antigen-induced B cell antigen receptor signaling viewed in living cells by fluorescence resonance energy transfer. Nat. Immunol. 6: 1168-1176. (Pubitemid 41541795)
51. Zal, T., M. A. Zal, and N. R. Gascoigne. 2002. Inhibition of T cell receptor-coreceptor interactions by antagonist ligands visualized by live FRET imaging of the T-hybridoma immunological synapse. Immunity 16: 521-534. (Pubitemid 34442577)
52. Moldovan, M. C., L. Sabbagh, G. Breton, R. P. Sékaly, and M. F. Krummel. 2006. Triggering of T cell activation via CD4 dimers. J. Immunol. 176: 5438-5445.
53. Treanor, B., P. M. Lanigan, S. Kumar, C. Dunsby, I. Munro, E. Auksorius, F. J. Culley, M. A. Purbhoo, D. Phillips, M. A. Neil, et al. 2006. Microclusters of inhibitory killer immunoglobulin-like receptor signaling at natural killer cell immunological synapses. J. Cell Biol. 174: 153-161.
54. Gur, C., A. Porgador, M. Elboim, R. Gazit, S. Mizrahi, N. Stern-Ginossar, H. Achdout, H. Ghadially, Y. Dor, T. Nir, et al. 2010. The activating receptor NKp46 is essential for the development of type 1 diabetes. Nat. Immunol. 11: 121-128.
55. Liu, S., J. Julian, and D. D. Carson. 1998. A peptide sequence of heparin/heparan sulfate (HP/HS)-interacting protein supports selective, high affinity binding of HP/HS and cell attachment. J. Biol. Chem. 273: 9718-9726. (Pubitemid 28183063)