Molecular recognition of paired receptors in the immune system

Frontiers in Microbiology

Volumn 3, Issue DEC, 2012, Pages

  Kuroki, Kimiko ^a   Furukawa, Atsushi ^a,b   Maenaka, Katsumi ^a,b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

C type lectin like receptor; Immunoglobulin like receptor; Infectious diseases; ITAM; ITIM; Paired receptor; Structural biology; Tumorigenesis

Indexed keywords

EID: 84875883066     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00429     Document Type: Review

References (88)

1. Adams, E. J., Juo, Z. S., Venook, R. T., Boulanger, M. J., Arase, H., Lanier, L. L., et al. (2007). Structural elucidation of the m157 mouse cytomegalovirus ligand for Ly49 natural killer cell receptors. Proc. Natl. Acad. Sci. U.S.A. 104, 10128-10133.
2. Adams, S., Van Der Laan, L. J., Vernon Wilson, E., Renardel De Lavalette, C., Dopp, E. A., Dijkstra, C. D., et al. (1998). Signal-regulatory protein is selectively expressed by myeloid and neuronal cells. J. Immunol. 161, 1853-1859
3. Ahrens, S., Zelenay, S., Sancho, D., Hanc, P., Kjaer, S., Feest, C., et al. (2012). F-actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR-1, a receptor for dead cells. Immunity 36, 635-645
4. Aldemir, H., Prod'homme, V., Dumaurier, M. J., Retiere, C., Poupon, G., Cazareth, J., et al. (2005). Cutting edge: lectin-like transcript 1 is a ligand for the CD161 receptor. J. Immunol. 175, 7791-7795
5. Allen, R. L., Raine, T., Haude, A., Trowsdale, J., and Wilson, M. J. (2001). Leukocyte receptor complexencoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J. Immunol. 167, 5543-5547
6. Alter, G., Heckerman, D., Schneidewind, A., Fadda, L., Kadie, C. M., Carlson, J. M., et al. (2011). HIV1 adaptation to NK-cell-mediated immune pressure. Nature 476, 96-100
7. Arase, H., and Lanier, L. L. (2004). Specific recognition of virus-infected cells by paired NK receptors. Rev. Med. Virol. 14, 83-93
8. Arase, H., Mocarski, E. S., Campbell, A. E., Hill, A. B., and Lanier, L. L. (2002). Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296, 1323-1326
9. Arase, N., Arase, H., Park, S. Y., Ohno, H., Ra, C., and Saito, T. (1997). Association with FcRgamma is essential for activation signal through NKRP1 (CD161) in natural killer (NK) cells and NK1.1+ T cells. J. Exp. Med. 186, 1957-1963
10. Atwal, J. K., Pinkston-Gosse, J., Syken, J., Stawicki, S., Wu, Y., Shatz, C., et al. (2008). PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 322, 967-970.
11. Barclay, A. N., and Brown, M. H. (2006). The SIRP family of receptors and immune regulation. Nat. Rev. Immunol. 6, 457-464
12. Barclay, A. N., and Hatherley, D. (2008). The counterbalance theory for evolution and function of paired receptors. Immunity 29, 675-678
13. Bates, E. E., Fournier, N., Garcia, E., Valladeau, J., Durand, I., Pin, J. J., et al. (1999). APCs express DCIR, a novel C-type lectin surface receptor containing an immunoreceptor tyrosine-based inhibitory motif. J. Immunol. 163, 1973-1983
14. Beck, S., and Barrell, B. G. (1988). Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature 331, 269-272
15. Borges, L., Hsu, M. L.,Fanger,N.,Kubin, M., and Cosman, D. (1997). A family of human lymphoid and myeloid Iglike receptors, some of which bind to MHC class I molecules. J. Immunol. 159, 5192-5196
16. Borrego, F., Ulbrecht, M., Weiss, E. H., Coligan, J. E., and Brooks, A. G. (1998). Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J. Exp. Med. 187, 813-818
17. Boyington, J. C., Motyka, S. A., Schuck, P., Brooks, A. G., and Sun, P. D. (2000). Crystal structure of an NK cell immunoglobulinlike receptor in complex with its class I MHC ligand. Nature 405, 537-543
18. Braud, V. M., Allan, D. S., O'callaghan, C. A., Soderstrom, K., D'andrea, A., Ogg, G. S., et al. (1998). HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391, 795-799
19. Brooke, G., Holbrook, J. D., Brown, M. H., and Barclay, A. N. (2004). Human lymphocytes interact directly with CD47 through a novel member of the signal regulatory protein (SIRP) family. J. Immunol. 173, 2562-2570
20. Brooks, A. G., Borrego, F., Posch, P. E., Patamawenu, A., Scorzelli, C. J., Ulbrecht, M., et al. (1999). Specific recognition of HLA-E, but not classical, HLA class I molecules by soluble CD94/NKG2A and NK cells. J. Immunol. 162, 305-313
21. Chapman, T. L., Heikeman, A. P., and Bjorkman, P. J. (1999). The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 11, 603-613
22. Colonna, M., Navarro, F., Bellon, T., Llano, M., Garcia, P., Samaridis, J., et al. (1997). A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med. 186, 1809-1818
23. Cooley,S.,Xiao,F.,Pitt,M.,Gleason,M., Mccullar, V., Bergemann, T. L., et al. (2007). A subpopulation of human peripheral blood NK cells that lacks inhibitory receptors for self-MHC is developmentally immature. Blood 110, 578-586
24. Cosman, D., Fanger, N., Borges, L., Kubin, M., Chin, W., Peterson, L., et al. (1997). A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7, 273-282
25. Fan, Q. R., Long, E. O., and Wiley, D. C. (2001). Crystal structure of the human natural killer cell inhibitory receptor KIR2DL1-HLA-Cw4 complex. Nat. Immunol. 2, 452-460
26. Fournier, B., Andargachew, R., Robin, A. Z., Laur, O., Voelker, D. R., Lee, W. Y., et al. (2012). Surfactant protein D (Sp-D) binds to membraneproximal domain (D3) of signal regulatory protein alpha (SIRPalpha), a site distant from binding domain of CD47, while also binding to analogousregiononsignalregulatoryprotein beta (SIRPbeta). J. Biol. Chem. 287, 19386-19398
27. Fournier,N.,Chalus,L.,Durand,I.,Garcia, E., Pin, J. J., Churakova, T., et al. (2000). FDF03, a novel inhibitory receptor of the immunoglobulin superfamily, is expressed by human dendritic and myeloid cells. J. Immunol. 165, 1197-1209
28. Fujikado, N., Saijo, S., Yonezawa, T., Shimamori, K., Ishii, A., Sugai, S., et al. (2008). Dcir deficiency causes development of autoimmune diseases in mice due to excess expansion of dendritic cells. Nat. Med. 14, 176-180
29. Gallez-Hawkins, G. M., Franck,A. E., Li, X., Thao, L., Oki, A., Gendzekhadze, K., et al. (2011). Expression of activating KIR2DS2 and KIR2DS4 genes after hematopoietic cell transplantation: relevance to cytomegalovirus infection. Biol. Blood Marrow Transplant. 17, 1662-1672
30. Gardai, S. J., Xiao, Y. Q., Dickinson, M., Nick, J. A., Voelker, D. R., Greene, K. E., et al. (2003). By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115, 13-23
31. Gringhuis, S. I., Den Dunnen, J., Litjens, M., Van Der Vlist, M., and Geijtenbeek, T. B. (2009). Carbohydratespecific signaling through the DCSIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat. Immunol. 10, 1081-1088
32. Gringhuis, S. I., den Dunnen, J., Litjens, M., van Het Hof, B., van Kooyk, Y., Geijtenbeek, T. B. (2007). C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinasedependent acetylation of transcription factor NF-κB. Immunity 26, 605
33. Hanke, T., Takizawa, H., Mcmahon, C. W.,Busch,D. H.,Pamer,E. G.,Miller, J. D., et al. (1999). Direct assessment of MHC class I binding by seven Ly49 inhibitory NK cell receptors. Immunity 11, 67-77
34. Hatherley, D., Graham, S. C., Turner, J., Harlos, K., Stuart, D. I., and Barclay, A. N. (2008). Paired receptor specificity explained by structures of signal regulatory proteins alone and complexed with CD47. Mol. Cell 31, 266-277
35. Held, W., Cado, D., and Raulet, D. H. (1996). Transgenic expression of the Ly49A natural killer cell receptor confers class I major histocompatibility complex (MHC)-specific inhibition and prevents bone marrow allograft rejection. J. Exp. Med. 184, 2037-2041
36. Hiby, S. E., Walker, J. J., O'shaughnessy, K. M., Redman, C. W., Carrington, M., Trowsdale, J., et al. (2004). Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200, 957-965
37. Hirayasu, K., Ohashi, J., Kashiwase, K., Hananantachai, H., Naka, I., Ogawa, A., et al. (2012). Significant association of KIR2DL3-HLA-C1 combination with cerebral malaria and implications for co-evolution of KIR and HLA. PLoS Pathog. 8:e1002565.
38. Hirayasu, K., Ohashi, J., Tanaka, H., Kashiwase, K., Ogawa, A., Takanashi, M., et al. (2008).Evidence for natural selection on leukocyte immunoglobulin-like receptors for HLA class I in Northeast Asians. Am. J. Hum. Genet. 82, 1075-1083
39. Hodges, A., Sharrocks, K., Edelmann, M., Baban, D., Moris, A., Schwartz, O., et al. (2007). Activation of the lectin DC-SIGN induces an immature dendritic cell phenotype triggering Rho-GTPase activity required for HIV-1 replication. Nat. Immunol. 8, 569
40. Iizuka,K.,Naidenko,O.V.,Plougastel,B. F.,Fremont,D. H.,and Yokoyama,W. M. (2003). Genetically linked C-type lectin-related ligands for the NKRP1 family of natural killer cell receptors. Nat. Immunol. 4, 801-807
41. Ishikawa, E., Ishikawa, T., Morita, Y. S., Toyonaga, K., Yamada, H., Takeuchi, O., et al. (2009). Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J. Exp. Med. 206, 2879-2888.
42. Kaiser, B. K., Pizarro, J. C., Kerns, J., and Strong, R. K. (2008). Structural basis for NKG2A/CD94 recognition of HLA-E. Proc. Natl. Acad. Sci. U.S.A. 105, 6696-6701
43. Kamishikiryo, J., Fukuhara, H., Okabe, Y., Kuroki, K., and Maenaka, K. (2011). Molecular basis for LLT1 protein recognition by human CD161 protein (NKRP1A/KLRB1). J. Biol. Chem. 286, 23823-23830
44. Kogure,A., Shiratori, I.,Wang, J., Lanier, L. L., and Arase, H. (2011). PANP is a novel O-glycosylated PILRalpha ligand expressed in neural tissues. Biochem. Biophys. Res. Commun. 405, 428-433
45. Lambert, A. A., Barabe, F., Gilbert, C., and Tremblay, M. J. (2011). DCIRmediated enhancement of HIV1 infection requires the ITIMassociated signal transduction pathway. Blood 117, 6589-6599
46. Lambert, A. A., Gilbert, C., Richard, M., Beaulieu, A. D., and Tremblay, M. J. (2008). The C-type lectin surface receptor DCIR acts as a new attachment factor for HIV-1 in dendritic cells and contributes to transand cis-infection pathways. Blood 112, 1299-1307
47. Lee, N., Llano, M., Carretero, M., Ishitani,A.,Navarro,F.,Lopez-Botet,M., et al. (1998). HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. U.S.A. 95, 5199-5204
48. Li, H., Peng, S. L., Cui, Y., Fu, Q. X., Zhou, Y., Wang, Q. L., et al. (2010). Kinetics of interaction of HLA-B2705 with natural killer cell immunoglobulin-like receptor 3DS1.ProteinPept.Lett. 17,547-554.
49. Ljunggren, H. G., and Karre, K. (1990). In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 11, 237-244
50. Maenaka, K., Juji, T., Stuart, D. I., and Jones, E. Y. (1999). Crystal structure of the human p58 killer cell inhibitory receptor (KIR2DL3) specific for HLA-Cw3-related MHC class I. Structure 7, 391-398
51. Matsumoto, M., Tanaka, T., Kaisho, T., Sanjo, H., Copeland, N. G., Gilbert, D. J., et al. (1999). A novel LPS-inducible C-type lectin is a transcriptional target of NF-IL6 in macrophages. J. Immunol. 163, 5039-5048
52. Nakamura, A., Kobayashi, E., and Takai, T. (2004). Exacerbated graft-versushost disease in Pirb-/mice. Nat. Immunol. 5, 623-629
53. Parham, P. (2005). MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 5, 201-214
54. Petrie, E. J., Clements, C. S., Lin, J., Sullivan, L. C., Johnson, D., Huyton, T., et al. (2008). CD94-NKG2A recognition of human leukocyte antigen (HLA)-E bound to an HLA class I leader sequence. J. Exp. Med. 205, 725-735
55. Pozo, D., Vales-Gomez, M., Mavaddat, N., Williamson, S. C., Chisholm, S. E., and Reyburn, H. (2006). CD161 (human NKR-P1A) signaling in NK cells involves the activation of acid sphingomyelinase. J. Immunol. 176, 2397-2406
56. Richard, M., Thibault, N., Veilleux, P., Gareau-Page, G., and Beaulieu, A. D. (2006). Granulocyte macrophagecolony stimulating factor reduces the affinity of SHP-2 for the ITIM of CLECSF6 in neutrophils: a new mechanism of action for SHP-2. Mol. Immunol. 43, 1716-1721
57. Richard, M., Veilleux, P., Rouleau, M., Paquin, R., and Beaulieu, A. D. (2002). The expression pattern of the ITIM-bearing lectin CLECSF6 in neutrophils suggests a key role in the control of inflammation. J. Leukoc. Biol. 71, 871-880
58. Rosen, D. B., Bettadapura, J., Alsharifi, M., Mathew, P. A., Warren, H. S., and Lanier, L. L. (2005). Cutting edge: lectin-like transcript-1 is a ligand for the inhibitory human NKR-P1A receptor. J. Immunol. 175, 7796-7799
59. Rosen, D. B., Cao, W., Avery, D. T., Tangye, S. G., Liu, Y. J., Houchins, J. P., et al. (2008). Functional consequences of interactions between human NKR-P1A and its ligand LLT1 expressed on activated dendritic cells and B cells. J. Immunol. 180, 6508-6517
60. Ryu, M., Chen, Y., Qi, J., Liu, J., Fan, Z., Nam, G., et al. (2011). LILRA3 binds both classical and non-classical HLA class I molecules but with reduced affinities compared to LILRB1/LILRB2: structural evidence. PLoS ONE 6:e19245.
61. Sancho, D., Joffre, O. P., Keller, A. M., Rogers, N. C., Martinez, D., Hernanz-Falcon, P., et al. (2009). Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 458, 899-903
62. Sancho, D., and Reis e Sousa, C. (2012). Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu. Rev. Immunol. 30, 491-529
63. Satoh, T., Arii, J., Suenaga, T., Wang, J., Kogure, A., Uehori, J., et al. (2008). PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 132, 935-944
64. Schleypen, J. S.,Von Geldern, M., Weiss, E. H., Kotzias, N., Rohrmann, K., Schendel, D. J., et al. (2003). Renal cell carcinoma-infiltrating natural killer cells express differential repertoires of activating and inhibitory receptors and are inhibited by specific HLA class I allotypes. Int. J. Cancer 106, 905-912
65. Schoenen, H., Bodendorfer, B., Hitchens, K., Manzanero, S., Werninghaus, K., Nimmerjahn, F., et al. (2010). Cutting edge: Mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J. Immunol. 184, 2756-2760
66. Shiroishi, M., Kuroki, K., Rasubala, L., Tsumoto, K., Kumagai, I., Kurimoto, E., et al. (2006). Structural basis for recognition of the nonclassical MHC molecule HLAG by the leukocyte Ig-like receptor B2 (LILRB2/LIR2/ILT4/CD85d). Proc. Natl. Acad. Sci. U.S.A. 103, 16412-16417
67. Shiroishi, M., Tsumoto, K., Amano, K., Shirakihara, Y., Colonna, M., Braud, V. M., et al. (2003). Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLAG. Proc. Natl. Acad. Sci. U.S.A. 100, 8856-8861
68. Sivori, S., Falco, M., Carlomagno, S., Romeo, E., Soldani, C., Bensussan, A., et al. (2010). A novel KIRassociated function: evidence that CpG DNA uptake and shuttling to early endosomes is mediated by KIR3DL2. Blood 116, 1637-1647
69. Smith, H. R., Heusel, J. W., Mehta, I. K., Kim, S., Dorner, B. G., Naidenko, O. V., et al. (2002). Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. U.S.A. 99, 8826-8831
70. Stewart, C. A., Laugier-Anfossi, F., Vely, F., Saulquin, X., Riedmuller, J., Tisserant, A., et al. (2005). Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. Proc. Natl. Acad. Sci. U.S.A. 102, 13224-13229
71. Sudmant, P. H., Kitzman, J. O., Antonacci, F., Alkan, C., Malig, M., Tsalenko, A., et al. (2010). Diversity of human copy number variation and multicopy genes. Science 330, 641-646
72. Sun, Y., Senger, K., Baginski, T. K., Mazloom, A., Chinn, Y., Pantua, H., et al. (2012). Evolutionarily conserved paired immunoglobulin-like receptor alpha (PILRalpha) domain mediates its interaction with diverse sialylated ligands. J. Biol. Chem. 287, 15837-15850
73. Tabata, S., Kuroki, K., Wang, J., Kajikawa, M., Shiratori, I., Kohda, D., et al. (2008). Biophysical characterization of O-glycosylated CD99 recognition by paired Ig-like type 2 receptors. J. Biol. Chem. 283, 8893-8901
74. Thananchai, H., Makadzange, T., Maenaka, K., Kuroki, K., Peng, Y., Conlon, C., et al. (2009). Reciprocal recognition of an HLA-Cw4restricted HIV-1 gp120 epitope by CD8+ T cells and NK cells. AIDS 23, 189-193
75. Tomasec, P., Braud, V. M., Rickards, C., Powell, M. B., Mcsharry, B. P., Gadola, S., et al. (2000). Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287, 1031
76. Ulbrecht, M., Martinozzi, S., Grzeschik, M., Hengel, H., Ellwart, J. W., Pla, M., et al. (2000). Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cellmediated lysis. J. Immunol. 164, 5019-5022
77. Valiante, N. M., Uhrberg, M., Shilling, H. G., Lienert-Weidenbach, K., Arnett, K. L., D'andrea, A., et al. (1997). Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7, 739-751
78. Vivian, J. P., Duncan, R. C., Berry, R., O'connor, G. M., Reid, H. H., Beddoe, T., et al. (2011). Killer cell immunoglobulin-like receptor 3DL1-mediated recognition of human leukocyte antigen B. Nature 479, 401-405
79. Wang, J., Shiratori, I., Satoh, T., Lanier, L. L., and Arase, H. (2008). An essential role of sialylated O-linked sugar chains in the recognition of mouse CD99 by paired Ig-like type 2 receptor (PILR). J. Immunol. 180, 1686-1693
80. Willcox,B.E.,Thomas,L. M.,andBjorkman, P. J. (2003). Crystal structure of HLA-A2 bound to LIR-1, a host and viral major histocompatibility complex receptor. Nat. Immunol. 4, 913-919
81. Wright, G. J., Cherwinski, H., Foster Cuevas, M., Brooke, G., Puklavec, M. J.,Bigler,M.,et al. (2003). Characterization of the CD200 receptor family in mice and humans and their interactions with CD200. J. Immunol. 171, 3034-3046
82. Yamasaki, S., Ishikawa, E., Sakuma, M., Hara, H., Ogata, K., and Saito, T. (2008). Mincle is an ITAMcoupled activating receptor that senses damaged cells. Nat. Immunol. 9, 1179-1188
83. Yamasaki, S., Matsumoto, M., Takeuchi, O., Matsuzawa, T., Ishikawa, E., Sakuma, M., et al. (2009). Ctype lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc. Natl. Acad. Sci. U.S.A. 106, 1897-1902
84. Yang, Z., and Bjorkman, P. J. (2008). Structure of UL18, a peptidebinding viral MHC mimic, bound to a host inhibitory receptor. Proc. Natl. Acad. Sci. U.S.A. 105, 10095-10100.
85. Yu, Y. Y., George, T., Dorfman, J. R., Roland, J., Kumar, V., and Bennett, M. (1996). The role of Ly49A and 5E6 (Ly49C) molecules in hybrid resistance mediated by murine natural killer cells against normal T cell blasts. Immunity 4, 67-76
86. Zelensky, A. N., and Gready, J. E. (2005). The C-type lectin-like domain superfamily. FEBS J. 272, 6179-6217
87. Zhang, J. G., Czabotar, P. E., Policheni, A. N., Caminschi, I., Wan, S. S., Kitsoulis, S., et al. (2012). The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity 36, 646-657
88. Zheng, J., Umikawa, M., Cui, C., Li, J., Chen, X., Zhang, C., et al. (2012). Inhibitory receptors bind ANGPTLs and support blood stem cells and leukaemia development. Nature 485, 656-660