The diversity of the HLA-E-restricted peptide repertoire explains the immunological impact of the Arg107Gly mismatch

Immunogenetics

Volumn 68, Issue 1, 2016, Pages 29-41

  Celik, Alexander A ^a   Kraemer, Thomas ^a   Huyton, Trevor ^a   Blasczyk, Rainer ^a   Bade Döding, Christina ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Diverse HLA E peptide repertoire; HLA E*01:03; Non canonical peptides; Tumor immune escape

Indexed keywords

ARGININE; GLYCINE; HLA E ANTIGEN; CARRIER PROTEIN; HLA ANTIGEN CLASS 1; HLA-E ANTIGEN; ISOPROTEIN; PEPTIDE; SIGNAL PEPTIDE; TAPASIN;

ALLELE; ARTICLE; ASSAY; CELL SURFACE; CYTOTOXICITY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MASS SPECTROMETRY; NATURAL KILLER CELL; PRIORITY JOURNAL; SEQUENCE ANALYSIS; AMINO ACID SEQUENCE; CELL LINE; CYTOTOXICITY TEST; GENE; GENETICS; IMMUNOLOGY; LYMPHOCYTE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM;

AMINO ACID SEQUENCE; ARGININE; CELL LINE; CYTOTOXICITY TESTS, IMMUNOLOGIC; GENES, MHC CLASS I; GLYCINE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTES; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDES; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN ISOFORMS; PROTEIN SORTING SIGNALS;

EID: 84953369558     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-015-0880-z     Document Type: Article

References (65)

1. Bade-Doding C, Theodossis A, Gras S, Kjer-Nielsen L, Eiz-Vesper B, Seltsam A, Huyton T, Rossjohn J, McCluskey J, Blasczyk R (2011) The impact of human leukocyte antigen (HLA) micropolymorphism on ligand specificity within the HLA-B*41 allotypic family. Haematologica 96:110–118. doi:10.3324/haematol.2010.030924
2. Bade-Doeding C, Elsner HA, Eiz-Vesper B, Seltsam A, Holtkamp U, Blasczyk R (2004) A single amino-acid polymorphism in pocket A of HLA-A*6602 alters the auxiliary anchors compared with HLA-A*6601 ligands. Immunogenetics 56:83–88. doi:10.1007/s00251-004-0677-y
3. Bade-Doeding C, DeLuca DS, Seltsam A, Blasczyk R, Eiz-Vesper B (2007) Amino acid 95 causes strong alteration of peptide position Pomega in HLA-B*41 variants. Immunogenetics 59:253–259. doi:10.1007/s00251-007-0197-7
4. Badrinath S, Huyton T, Schumacher H, Blasczyk R, Bade-Doeding C (2012a) Position 45 influences the peptide binding motif of HLA-B*44:08. Immunogenetics 64:245–249. doi:10.1007/s00251-011-0583-z
5. Badrinath S, Saunders P, Huyton T, Aufderbeck S, Hiller O, Blasczyk R, Bade-Doeding C (2012b) Position 156 influences the peptide repertoire and tapasin dependency of human leukocyte antigen B*44 allotypes. Haematologica 97:98–106. doi:10.3324/haematol.2011.046037
6. Badrinath S, Huyton T, Kunze-Schumacher H, Elsner HA, Blasczyk R, Bade-Doeding C (2014) Differential impact of HLA-B*44 allelic mismatches at position 156 on peptide binding specificities and T-cell diversity. Stem Cell Res Ther 4:9. doi:10.4172/2157-7633.1000192
7. Bjorkman PJ, Parham P (1990) Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem 59:253–288. doi:10.1146/annurev.bi.59.070190.001345
8. Braud V, Jones EY, McMichael A (1997) The human major histocompatibility complex class Ib molecule HLA-E binds signal sequence-derived peptides with primary anchor residues at positions 2 and 9. Eur J Immunol 27:1164–1169. doi:10.1002/eji.1830270517
9. Braud VM, Allan DS, O’Callaghan CA, Soderstrom K, D’Andrea A, Ogg GS, Lazetic S, Young NT, Bell JI, Phillips JH, Lanier LL, McMichael AJ (1998) HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795–799. doi:10.1038/35869
10. Brooks AG, Posch PE, Scorzelli CJ, Borrego F, Coligan JE (1997) NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J Exp Med 185:795–800
11. Burrows SR, Rossjohn J, McCluskey J (2006) Have we cut ourselves too short in mapping CTL epitopes? Trends Immunol 27:11–16. doi:10.1016/j.it.2005.11.001
12. Cooley S, Trachtenberg E, Bergemann TL, Saeteurn K, Klein J, Le CT, Marsh SG, Guethlein LA, Parham P, Miller JS, Weisdorf DJ (2009) Donors with group B KIR haplotypes improve relapse-free survival after unrelated hematopoietic cell transplantation for acute myelogenous leukemia. Blood 113:726–732. doi:10.1182/blood-2008-07-171926
13. Danzer M, Polin H, Proll J, Haunschmid R, Hofer K, Stabentheiner S, Hackl C, Kasparu H, Konig J, Hauser H, Binder M, Weiss R, Gabriel C, Krieger O (2009) Clinical significance of HLA-E*0103 homozygosity on survival after allogeneic hematopoietic stem-cell transplantation. Transplantation 88:528–532. doi:10.1097/TP.0b013e3181b0e79e
14. Drexler HG, Matsuo Y (2000) Malignant hematopoietic cell lines: in vitro models for the study of natural killer cell leukemia-lymphoma. Leukemia 14:777–782
15. Elamin NE, Bade-Doeding C, Blasczyk R, Eiz-Vesper B (2010) Polymorphism between HLA-A*0301 and A*0302 located outside the pocket F alters the Pomega peptide motif. Tissue Antigens 76:487–490. doi:10.1111/j.1399-0039.2010.01547.x
16. Felicio LP, Porto IO, Mendes-Junior CT, Veiga-Castelli LC, Santos KE, Vianello-Brondani RP, Sabbagh A, Moreau P, Donadi EA, Castelli EC (2014) Worldwide HLA-E nucleotide and haplotype variability reveals a conserved gene for coding and 3′ untranslated regions. Tissue Antigens 83:82–93. doi:10.1111/tan.12283
17. Grimsley C, Ober C (1997) Population genetic studies of HLA-E: evidence for selection. Hum Immunol 52:33–40. doi:10.1016/S0198-8859(96)00241-8
18. Guzman-Fulgencio M, Berenguer J, Rallon N, Fernandez-Rodriguez A, Miralles P, Soriano V, Jimenez-Sousa MA, Cosin J, Medrano J, Garcia-Alvarez M, Lopez JC, Benito JM, Resino S (2013) HLA-E variants are associated with sustained virological response in HIV/hepatitis C virus-coinfected patients on hepatitis C virus therapy. AIDS 27:1231–1238. doi:10.1097/QAD.0b013e32835f5b9c
19. Hirosawa M, Hoshida M, Ishikawa M, Toya T (1993) MASCOT: multiple alignment system for protein sequences based on three-way dynamic programming. Comput Appl Biosci: CABIOS 9:161–167
20. Hoare HL, Sullivan LC, Pietra G, Clements CS, Lee EJ, Ely LK, Beddoe T, Falco M, Kjer-Nielsen L, Reid HH, McCluskey J, Moretta L, Rossjohn J, Brooks AG (2006) Structural basis for a major histocompatibility complex class Ib-restricted T cell response. Nat Immunol 7:256–264. doi:10.1038/ni1312
21. Hosseini E, Schwarer AP, Jalali A, Ghasemzadeh M (2013) The impact of HLA-E polymorphisms on relapse following allogeneic hematopoietic stem cell transplantation. Leuk Res 37:516–519. doi:10.1016/j.leukres.2013.01.011
22. Huyton T, Schumacher H, Blasczyk R, Bade-Doeding C (2012) Residue 81 confers a restricted C-terminal peptide binding motif in HLA-B*44:09. Immunogenetics 64:663–668. doi:10.1007/s00251-012-0625-1
23. Kaiser BK, Barahmand-Pour F, Paulsene W, Medley S, Geraghty DE, Strong RK (2005) Interactions between NKG2x immunoreceptors and HLA-E ligands display overlapping affinities and thermodynamics. J Immunol 174:2878–2884
24. Kraemer T, Blasczyk R, Bade-Doeding C (2014) HLA-E: a novel player for histocompatibility. J Immunol Res 2014:352160. doi:10.1155/2014/352160
25. Kraemer T, Celik AA, Huyton T, Kunze-Schumacher H, Blasczyk R, Bade-Döding C (2015) HLA-E: presentation of a broader peptide repertoire impacts the cellular immune response-implications on HSCT outcome. Stem Cells Int 2015:12. doi:10.1155/2015/346714
26. Kroger N, Zabelina T, Berger J, Duske H, Klyuchnikov E, Binder T, Stubig T, Hilde-brandt Y, Atanackovic D, Alchalby H, Ayuk F, Zander AR, Bacher U, Eiermann T (2011) Donor KIR haplotype B improves progression-free and overall survival after allogeneic hematopoietic stem cell transplantation for multiple myeloma. Leukemia 25:1657–1661. doi:10.1038/leu.2011.138
27. Kunze-Schumacher H, Blasczyk R, Bade-Doeding C (2014) Soluble HLA technology as a strategy to evaluate the impact of HLA mismatches. J Immunol Res 2014:246171. doi:10.1155/2014/246171
28. Lajoie J, Hargrove J, Zijenah LS, Humphrey JH, Ward BJ, Roger M (2006) Genetic variants in nonclassical major histocompatibility complex class I human leukocyte antigen (HLA)-E and HLA-G molecules are associated with susceptibility to heterosexual acquisition of HIV-1. J Infect Dis 193:298–301. doi:10.1086/498877
29. Lampen MH, Hassan C, Sluijter M, Geluk A, Dijkman K, Tjon JM, de Ru AH, van der Burg SH, van Veelen PA, van Hall T (2013) Alternative peptide repertoire of HLA-E reveals a binding motif that is strikingly similar to HLA-A2. Mol Immunol 53:126–131. doi:10.1016/j.molimm.2012.07.009
30. Lanier LL (2008) Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 9:495–502. doi:10.1038/ni1581
31. Lee N, Goodlett DR, Ishitani A, Marquardt H, Geraghty DE (1998a) HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J Immunol 160:4951–4960
32. Lee N, Llano M, Carretero M, Ishitani A, Navarro F, Lopez-Botet M, Geraghty DE (1998b) HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci U S A 95:5199–5204
33. Llano M, Lee N, Navarro F, Garcia P, Albar JP, Geraghty DE, Lopez-Botet M (1998) HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur J Immunol 28:2854–2863. doi:10.1002/(SICI)1521-4141(199809)28:09<2854::AID-IMMU2854>3.0.CO;2-W
34. Macdonald WA, Purcell AW, Mifsud NA, Ely LK, Williams DS, Chang L, Gorman JJ, Clements CS, Kjer-Nielsen L, Koelle DM, Burrows SR, Tait BD, Holdsworth R, Brooks AG, Lovrecz GO, Lu L, Rossjohn J, McCluskey J (2003) A naturally selected dimorphism within the HLA-B44 supertype alters class I structure, peptide repertoire, and T cell recognition. J Exp Med 198:679–691. doi:10.1084/jem.20030066
35. Mazzarino P, Pietra G, Vacca P, Falco M, Colau D, Coulie P, Moretta L, Mingari MC (2005) Identification of effector-memory CMV-specific T lymphocytes that kill CMV-infected target cells in an HLA-E-restricted fashion. Eur J Immunol 35:3240–3247. doi:10.1002/eji.200535343
36. McMahon CW, Raulet DH (2001) Expression and function of NK cell receptors in CD8+ T cells. Curr Opin Immunol 13:465–470
37. Michaelsson J, Teixeira de Matos C, Achour A, Lanier LL, Karre K, Soderstrom K (2002) A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J Exp Med 196:1403–1414
38. Mingari MC, Schiavetti F, Ponte M, Vitale C, Maggi E, Romagnani S, Demarest J, Pantaleo G, Fauci AS, Moretta L (1996) Human CD8+ T lymphocyte subsets that express HLA class I-specific inhibitory receptors represent oligoclonally or monoclonally expanded cell populations. Proc Natl Acad Sci U S A 93:12433–12438
39. Nattermann J, Nischalke HD, Hofmeister V, Ahlenstiel G, Zimmermann H, Leifeld L, Weiss EH, Sauerbruch T, Spengler U (2005a) The HLA-A2 restricted T cell epitope HCV core 35–44 stabilizes HLA-E expression and inhibits cytolysis mediated by natural killer cells. Am J Pathol 166:443–453. doi:10.1016/S0002-9440(10)62267-5
40. Nattermann J, Nischalke HD, Hofmeister V, Kupfer B, Ahlenstiel G, Feldmann G, Rockstroh J, Weiss EH, Sauerbruch T, Spengler U (2005b) HIV-1 infection leads to increased HLA-E expression resulting in impaired function of natural killer cells. Antivir Ther 10:95–107
41. Nattermann J, Feldmann G, Ahlenstiel G, Langhans B, Sauerbruch T, Spengler U (2006) Surface expression and cytolytic function of natural killer cell receptors is altered in chronic hepatitis C. Gut 55:869–877. doi:10.1136/gut.2005.076463
42. Oliveira CC, van Veelen PA, Querido B, de Ru A, Sluijter M, Laban S, Drijfhout JW, van der Burg SH, Offringa R, van Hall T (2010) The nonpolymorphic MHC Qa-1b mediates CD8+ T cell surveillance of antigen-processing defects. J Exp Med 207:207–221. doi:10.1084/jem.20091429
43. Parham P, Lomen CE, Lawlor DA, Ways JP, Holmes N, Coppin HL, Salter RD, Wan AM, Ennis PD (1988) Nature of polymorphism in HLA-A, -B, and -C molecules. Proc Natl Acad Sci U S A 85:4005–4009
44. Park B, Kim Y, Shin J, Lee S, Cho K, Fruh K, Lee S, Ahn K (2004) Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity 20:71–85
45. Petrie EJ, Clements CS, Lin J, Sullivan LC, Johnson D, Huyton T, Heroux A, Hoare HL, Beddoe T, Reid HH, Wilce MC, Brooks AG, Rossjohn J (2008) CD94-NKG2A recognition of human leukocyte antigen (HLA)-E bound to an HLA class I leader sequence. J Exp Med 205:725–735. doi:10.1084/jem.20072525
46. Pietra G, Romagnani C, Mazzarino P, Falco M, Millo E, Moretta A, Moretta L, Mingari MC (2003) HLA-E-restricted recognition of cytomegalovirus-derived peptides by human CD8+ cytolytic T lymphocytes. Proc Natl Acad Sci U S A 100:10896–10901. doi:10.1073/pnas.1834449100
47. Rammensee HG, Falk K, Rotzschke O (1993) Peptides naturally presented by MHC class I molecules. Annu Rev Immunol 11:213–244. doi:10.1146/annurev.iy.11.040193.001241
48. Ressing ME, Keating SE, van Leeuwen D, Koppers-Lalic D, Pappworth IY, Wiertz EJ, Rowe M (2005) Impaired transporter associated with antigen processing-dependent peptide transport during productive EBV infection. J Immunol 174:6829–6838
49. Robertson MJ, Cochran KJ, Cameron C, Le JM, Tantravahi R, Ritz J (1996) Characterization of a cell line, NKL, derived from an aggressive human natural killer cell leukemia. Exp Hematol 24:406–415
50. Robinson J, Halliwell JA, Hayhurst JD, Flicek P, Parham P, Marsh SG (2015) The IPD and IMGT/HLA database: allele variant databases. Nucleic Acids Res 43:D423–D431. doi:10.1093/nar/gku1161
51. Romagnani C, Pietra G, Falco M, Millo E, Mazzarino P, Biassoni R, Moretta A, Moretta L, Mingari MC (2002) Identification of HLA-E-specific alloreactive T lymphocytes: a cell subset that undergoes preferential expansion in mixed lymphocyte culture and displays a broad cytolytic activity against allogeneic cells. Proc Natl Acad Sci U S A 99:11328–11333. doi:10.1073/pnas.172369799
52. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F, Martelli MF, Velardi A (2002) Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295:2097–2100. doi:10.1126/science.1068440
53. Schulte D, Vogel M, Langhans B, Kramer B, Korner C, Nischalke HD, Steinberg V, Michalk M, Berg T, Rockstroh JK, Sauerbruch T, Spengler U, Nattermann J (2009) The HLA-E(R)/HLA-E(R) genotype affects the natural course of hepatitis C virus (HCV) infection and is associated with HLA-E-restricted recognition of an HCV-derived peptide by interferon-gamma-secreting human CD8(+) T cells. J Infect Dis 200:1397–1401. doi:10.1086/605889
54. Seliger B, Harders C, Lohmann S, Momburg F, Urlinger S, Tampe R, Huber C (1998) Down-regulation of the MHC class I antigen-processing machinery after oncogenic transformation of murine fibroblasts. Eur J Immunol 28:122–133. doi:10.1002/(SICI)1521-4141(199801)28:01<122::AID-IMMU122>3.0.CO;2-F
55. Seliger B, Maeurer MJ, Ferrone S (2000) Antigen-processing machinery breakdown and tumor growth. Immunol Today 21:455–464
56. Steinle A, Schendel DJ (1994) HLA class I alleles of LCL 721 and 174 × CEM. T2(T2). Tissue Antigens 44:268–270
57. Stevens J, Joly E, Trowsdale J, Butcher GW (2001) Peptide binding characteristics of the non-classical class Ib MHC molecule HLA-E assessed by a recombinant random peptide approach. BMC Immunol 2:5
58. Strong RK, Holmes MA, Li P, Braun L, Lee N, Geraghty DE (2003) HLA-E allelic variants. Correlating differential expression, peptide affinities, crystal structures, and thermal stabilities. J Biol Chem 278:5082–5090. doi:10.1074/jbc.M208268200
59. Tamouza R, Busson M, Rocha V, Fortier C, Haddad Y, Brun M, Boukouaci W, Bleux H, Socie G, Krishnamoorthy R, Toubert A, Gluckman E, Charron D (2006) Homozygous status for HLA-E*0103 confers protection from acute graft-versus-host disease and transplant-related mortality in HLA-matched sibling hematopoietic stem cell transplantation. Transplantation 82:1436–1440. doi:10.1097/01.tp.0000244598.92049.dd
60. Terrazzano G, Sica M, Gianfrani C, Mazzarella G, Maurano F, De Giulio B, de Saint-Mezard S, Zanzi D, Maiuri L, Londei M, Jabri B, Troncone R, Auricchio S, Zappacosta S, Carbone E (2007) Gliadin regulates the NK-dendritic cell cross-talk by HLA-E surface stabilization. J Immunol 179:372–381
61. Tomasec P, Braud VM, Rickards C, Powell MB, McSharry BP, Gadola S, Cerundolo V, Borysiewicz LK, McMichael AJ, Wilkinson GW (2000) Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031
62. Vambutas A, DeVoti J, Pinn W, Steinberg BM, Bonagura VR (2001) Interaction of human papillomavirus type 11 E7 protein with TAP-1 results in the reduction of ATP-dependent peptide transport. Clin Immunol 101:94–99. doi:10.1006/clim.2001.5094
63. Verneris MR (2013) Natural killer cells and regulatory T cells: how to manipulate a graft for optimal GVL. Hematology Am Soc Hematol Educ Program 2013:335–341. doi:10.1182/asheducation-2013.1.335
64. Wiertz EJ, Tortorella D, Bogyo M, Yu J, Mothes W, Jones TR, Rapoport TA, Ploegh HL (1996) Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384:432–438. doi:10.1038/384432a0
65. Wooden SL, Kalb SR, Cotter RJ, Soloski MJ (2005) Cutting edge: HLA-E binds a peptide derived from the ATP-binding cassette transporter multidrug resistance-associated protein 7 and inhibits NK cell-mediated lysis. J Immunol 175:1383–1387