ERAP1 regulates natural killer cell function by controlling the engagement of inhibitory receptors

Cancer Research

Volumn 75, Issue 5, 2015, Pages 824-834

  Cifaldi, Loredana ^a   Romania, Paolo ^a   Falco, Michela ^b   Lorenzi, Silvia ^a   Meazza, Raffaella ^c   Petrini, Stefania ^a   Andreani, Marco ^d   Pende, Daniela ^c   Locatelli, Franco ^a,e   Fruci, Doriana ^a  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^b G GASLINI INSTITUTE   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d IME Foundation   (Italy)

^e UNIVERSITY OF PAVIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPEPTIDASE; CD94 ANTIGEN; ENDOPLASMIC RETICULUM AMINOPEPTIDASE 1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL LECTIN LIKE RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2A; UNCLASSIFIED DRUG; ENZYME INHIBITOR; ERAP1 PROTEIN, HUMAN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL1; KIR2DL1 PROTEIN, HUMAN; KIR2DL3 PROTEIN, HUMAN; KIR3DL1 PROTEIN, HUMAN; LEUCINE; LEUCINETHIOL; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY C; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY D; NATURAL KILLER CELL RECEPTOR; SMALL INTERFERING RNA; THIOL DERIVATIVE;

ADAPTIVE IMMUNITY; ALLOIMMUNITY; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; BINDING AFFINITY; CANCER CELL LINE; CANCER IMMUNOTHERAPY; CELL STIMULATION; COCULTURE; CONTROLLED STUDY; DEGRANULATION; ENZYME INHIBITION; GENOTYPE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN CELL; INNATE IMMUNITY; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; T LYMPHOCYTE ACTIVATION; TUMOR CELL LINE; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; GENETICS; HEK293 CELL LINE; HELA CELL LINE; IMMUNOLOGY; MEDULLOBLASTOMA;

AMINOPEPTIDASES; CELL LINE, TUMOR; ENZYME INHIBITORS; HEK293 CELLS; HELA CELLS; HUMANS; KILLER CELLS, NATURAL; LEUCINE; MEDULLOBLASTOMA; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY D; RECEPTORS, KIR2DL1; RECEPTORS, KIR2DL3; RECEPTORS, KIR3DL1; RECEPTORS, NATURAL KILLER CELL; RNA, SMALL INTERFERING; SULFHYDRYL COMPOUNDS;

EID: 84928699284     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1643     Document Type: Article

References (50)

1. Lanier LL. NK cell recognition. Annu Rev Immunol 2005;23:225-74.
2. Raulet DH, Vance RE. Self-tolerance of natural killer cells. Nat Rev Immunol 2006;6:520-31.
3. Raulet DH, Vance RE, McMahon CW. Regulation of the natural killer cell receptor repertoire. Annu Rev Immunol 2001;19:291-330.
4. Lanier LL. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol 2008;8:259-68.
5. Orr MT, Murphy WJ, Lanier LL. 'Unlicensed' natural killer cells dominate the response to cytomegalovirus infection. Nat Immunol 2010;11:321-7.
6. Cerwenka A, Lanier LL. Natural killer cells, viruses, and cancer. Nat Rev Immunol 2001;1:41-9.
7. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001;413:165-71.
8. Colonna M, Samaridis J. Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 1995;268:405-8.
9. Moretta A, Bottino C, Vitale M, Pende D, Biassoni R, Mingari MC, et al. Receptors for HLA class-I molecules in human natural killer cells. Annu Rev Immunol 1996;14:619-48.
10. Braud VM, Allan DS, O'Callaghan CA, Soderstrom K, D'Andrea A, Ogg GS, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 1998;391:795-9.
11. 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.
12. Kim S, Sunwoo JB, Yang L, Choi T, Song YJ, French AR, et al. HLA alleles determine differences in human natural killer cell responsiveness and potency. Proc Natl Acad Sci U S A 2008;105:3053-8.
13. Anfossi N, Andre P, Guia S, Falk CS, Roetynck S, Stewart CA, et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity 2006;25:331-42.
14. Joncker NT, Fernandez NC, Treiner E, Vivier E, Raulet DH. NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J Immunol 2009;182:4572-80.
15. Hoglund P, Brodin P. Current perspectives of natural killer cell education by MHC class I molecules. Nat Rev 2010;10:724-34.
16. Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, Yang L, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 2005;436:709-13.
17. Vilches C, Parham P. KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Immunol 2002;20:217-51.
18. Colonna M, Borsellino G, Falco M, Ferrara GB, Strominger JL. HLA-C is the inhibitory ligand that determines dominant resistance to lysis by NK1- and NK2-specific natural killer cells. Proc Natl Acad SciUS A 1993;90:12000-4.
19. 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 1995;3:801-9.
20. Boyington JC, Motyka SA, Schuck P, Brooks AG, Sun PD. Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC ligand. Nature 2000;405:537-43.
21. Fan QR, Long EO, Wiley DC. Crystal structure of the human natural killer cell inhibitory receptor KIR2DL1-HLA-Cw4 complex. Nat Immunol 2001;2:452-60.
22. Hoare HL, Sullivan LC, Clements CS, Ely LK, Beddoe T, Henderson KN, et al. Subtle changes in peptide conformation profoundly affect recognition of the nonclassical MHC class I molecule HLA-E by the CD94-NKG2 natural killer cell receptors. J Mol Biol 2008;377:1297-303.
23. Stewart CA, Laugier-Anfossi F, Vely F, Saulquin X, Riedmuller J, Tisserant A, et al. Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. Proc Natl Acad Sci U S A 2005;102:13224-9.
24. Cheent KS, Jamil KM, Cassidy S, Liu M, Mbiribindi B, Mulder A, et al. Synergistic inhibition of natural killer cells by the nonsignaling molecule CD94. Proc Natl Acad Sci U S A 2013;110:16981-6.
25. Cassidy SA, Cheent KS, Khakoo SI. Effects of Peptide on NK cell-mediated MHC I recognition. Front Immunol 2014;5:133.
26. Serwold T, Gonzalez F, Kim J, Jacob R, Shastri N. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 2002;419:480-3.
27. Saric T, Chang SC, Hattori A, York IA, Markant S, Rock KL, et al. An IFNgammainduced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat Immunol 2002;3:1169-76.
28. York IA, Chang SC, Saric T, Keys JA, Favreau JM, Goldberg AL, et al. The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat Immunol 2002;3:1177-84.
29. Saveanu L, Carroll O, Lindo V, Del Val M, Lopez D, Lepelletier Y, et al. Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat Immunol 2005;6:689-97.
30. Cifaldi L, Lo Monaco E, Forloni M, Giorda E, Lorenzi S, Petrini S, et al. Natural killer cells efficiently reject lymphoma silenced for the endoplasmic reticulum aminopeptidase associated with antigen processing. Cancer Res 2011;71:1597-606.
31. Chersi A, Galati R, Accapezzato D, Francavilla V, Barnaba V, Butler RH, et al. Responses of peptide-specific T cells to stimulation with polystyrene beads carrying HLA class I molecules loaded with single peptides. J Immunol Methods 2004;291:79-91.
32. Pende D, Marcenaro S, Falco M, Martini S, BernardoME, Montagna D, et al. Anti-leukemia activity of alloreactive NK cells in KIR ligand-mismatched haploidentical HSCT for pediatric patients: evaluation of the functional role of activating KIR and redefinition of inhibitory KIR specificity. Blood 2009;113:3119-29.
33. Perussia B, Ramoni C, Anegon I, Cuturi MC, Faust J, Trinchieri G. Preferential proliferation of natural killer cells among peripheral blood mononuclear cells cocultured with B lymphoblastoid cell lines. Nat Immun Cell Growth Regul 1987;6:171-88.
34. Villanueva J, Lee S, Giannini EH, Graham TB, Passo MH, Filipovich A, et al. Natural killer cell dysfunction is a distinguishing feature of systemic onset juvenile rheumatoid arthritis and macrophage activation syndrome. Arthritis Res Ther 2005;7:R30-7.
35. Borhis G, Ahmed PS, Mbiribindi B, Naiyer MM, Davis DM, Purbhoo MA, et al. A peptide antagonist disrupts NK cell inhibitory synapse formation. J Immunol 2013;190:2924-30.
36. Fadda L, Borhis G, Ahmed P, Cheent K, Pageon SV, Cazaly A, et al. Peptide antagonismas amechanism forNK cell activation. Proc Natl Acad SciUS A 2010;107:10160-5.
37. Serwold T, Gaw S, Shastri N. ER aminopeptidases generate a unique pool of peptides for MHC class I molecules. Nat Immunol 2001;2:644-51.
38. Sidney J, Peters B, Frahm N, Brander C, Sette A. HLA class I supertypes: a revised and updated classification. BMC Immunol 2008;9:1.
39. Falk K, Rotzschke O, Grahovac B, Schendel D, Stevanovic S, Gnau V, et al. Allele-specific peptide ligand motifs of HLA-C molecules. Proc Natl Acad Sci U S A 1993;90:12005-9.
40. Chelvanayagam G. A roadmap for HLA-A, HLA-B, and HLA-C peptide binding specificities. Immunogenetics 1996;45:15-26.
41. Yan J, Parekh VV, Mendez-Fernandez Y, Olivares-Villagomez D, Dragovic S, Hill T, et al. In vivo role of ER-associated peptidase activity in tailoring peptides for presentation by MHC class Ia and class Ib molecules. J ExpMed 2006;203:647-59.
42. Cifaldi L, Romania P, Lorenzi S, Locatelli F, Fruci D. Role of endoplasmic reticulum aminopeptidases in health and disease: from infection to cancer. Int J Mol Sci 2012;13:8338-52.
43. Zervoudi E, Saridakis E, Birtley JR, Seregin SS, Reeves E, Kokkala P, et al. Rationally designed inhibitor targeting antigen-trimming aminopeptidases enhances antigen presentation and cytotoxic T-cell responses. Proc Natl Acad Sci U S A 2013;110:19890-5.
44. van Endert PM, Riganelli D, Greco G, Fleischhauer K, Sidney J, Sette A, et al. The peptide-binding motif for the human transporter associated with antigen processing. J Exp Med 1995;182:1883-95.
45. Testi M, Andreani M, Locatelli F, Arcese W, Troiano M, Battarra M, et al. Influence of the HLA characteristics of Italian patients on donor search outcome in unrelated hematopoietic stem cell transplantation. Tissue Antigens 2014;84:198-205.
46. Hammer GE, Gonzalez F, James E, Nolla H, Shastri N. In the absence of aminopeptidase ERAAP, MHC class I molecules present many unstable and highly immunogenic peptides. Nat Immunol 2007;8:101-8.
47. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002;295:2097-100.
48. Locatelli F, Pende D, Mingari MC, Bertaina A, Falco M, Moretta A, et al. Cellular and molecular basis of haploidentical hematopoietic stem cell transplantation in the successful treatment of highrisk leukemias: role of alloreactive NK cells. Front Immunol 2013;4:15.
49. Mentlik James A, Cohen AD, Campbell KS. Combination Immune Therapies to Enhance Anti-Tumor Responses by NK Cells. Front Immunol 2013;4:481.
50. Chen D, Frezza M, Schmitt S, Kanwar J, Dou QP. Bortezomib as the first proteasome inhibitor anticancer drug: current status and future perspectives. Curr Cancer Drug Targets 2011;11:239-53.