HLA-E: A novel player for histocompatibility

Journal of Immunology Research

Volumn 2014, Issue , 2014, Pages

  Kraemer, Thomas ^a   Blasczyk, Rainer ^a   Bade Doeding, Christina ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HLA E ANTIGEN; SIGNAL PEPTIDE; HLA ANTIGEN CLASS 1; HLA-E ANTIGEN; PEPTIDE; PROTEIN BINDING;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; CD8+ T LYMPHOCYTE; EFFECTOR CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HISTOCOMPATIBILITY; HLA MATCHING; HUMAN; REVIEW; CHEMICAL STRUCTURE; CHEMISTRY; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; HISTOCOMPATIBILITY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNITY, INNATE; MODELS, MOLECULAR; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84911059564     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2014/352160     Document Type: Review

References (57)

1. Felício L. P., Porto I. O. P., Mendes-Junior C. T., Veiga-Castelli L. C., Santos K. E., Vianello-Brondani R. P., Sabbagh A., Moreau P., Donadi E. A., Castelli E. C., Worldwide HLA-E nucleotide and haplotype variability reveals a conserved gene for coding and 3′ untranslated regions. Tissue Antigens 2014 83 2 82 93 10.1111/tan.12283 2-s2.0-84892983707
2. Grimsley C., Ober C., Population genetic studies of HLA-E: evidence for selection. Human Immunology 1997 52 1 33 40 10.1016/S0198-8859(96)00241-8 2-s2.0-0031030340
3. Hughes A. L., Nei M., Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 1988 335 6186 167 170 10.1038/335167a0 2-s2.0-0023764283
4. Petrie E. J., Clements C. S., Lin J., Sullivan L. C., Johnson D., Huyton T., Heroux A., Hoare H. L., Beddoe T., Reid H. H., Wilce M. C. J., Brooks A. G., Rossjohn J., CD94-NKG2A recognition of human leukocyte antigen (HLA)-E bound to an HLA class I leader sequence. Journal of Experimental Medicine 2008 205 3 725 735 10.1084/jem.20072525 2-s2.0-41149126707
5. Bade-Doeding C., DeLuca D. S., Seltsam A., Blasczyk R., Eiz-Vesper B., Amino acid 95 causes strong alteration of peptide position P Ω in HLA-B41 variants. Immunogenetics 2007 59 4 253 259 10.1007/s00251-007-0197-7 2-s2.0-33847785568
6. Huyton T., Ladas N., Schumacher H., Blasczyk R., Bade-Doeding C., Pocketcheck: updating the HLA class I peptide specificity roadmap. Tissue Antigens 2012 80 3 239 248 10.1111/j.1399-0039.2012.01928.x 2-s2.0-84864794833
7. Huyton T., Schumacher H., Blasczyk R., Bade-Doeding C., Residue 81 confers a restricted C-terminal peptide binding motif in HLA-B44:09. Immunogenetics 2012 64 9 663 668 10.1007/s00251-012-0625-1 2-s2.0-84866731288
8. Bade-Döding C., Theodossis A., Gras S., Kjer-Nielsen L., Eiz-Vesper B., Seltsam A., Huyton T., Rossjohn J., McCluskey J., Blasczyk R., The impact of human leukocyte antigen (HLA) micropolymorphism on ligand specificity within the HLA-B41 allotypic family. Haematologica 2011 96 1 110 118 10.3324/haematol.2010.030924 2-s2.0-78650992438
9. Bjorkman P. J., Saper M. A., Samraoui B., Bennett W. S., Strominger J. L., Wiley D. C., The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 1987 329 6139 512 518 10.1038/329512a0 2-s2.0-0023187442
10. Strong R. K., Holmes M. A., Li P., Braun L., Lee N., Geraghty D. E., HLA-E allelic variants: correlating differential expression, peptide affinities, crystal structures, and thermal stabilities. Journal of Biological Chemistry 2003 278 7 5082 5090 10.1074/jbc.M208268200 2-s2.0-0038075329
11. Zeng X., Chen H., Gupta R., Paz-Altschul O., Bowcock A. M., Liao W., Deletion of the activating NKG2C receptor and a functional polymorphism in its ligand HLA-E in psoriasis susceptibility. Experimental Dermatology 2013 22 10 679 681 10.1111/exd.12233 2-s2.0-84884718080
12. Zhang J., Pan L., Chen L., Feng X., Zhou L., Zheng S., Non-classical MHC- Ι genes in chronic hepatitis B and hepatocellular carcinoma. Immunogenetics 2012 64 3 251 258 10.1007/s00251-011-0580-2 2-s2.0-84857366461
13. Braud V. M., Allan D. S. J., Wilson D., McMichael A. J., TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Current Biology 1998 8 1 1 10 2-s2.0-0031963752
14. Braud V., Jones E. Y., McMichael A., The human major histocompatibility complex class Ib molecule HLA-E binds signal sequence-derived peptides with primary anchor residues at positions 2 and 9. European Journal of Immunology 1997 27 5 1164 1169 10.1002/eji.1830270517 2-s2.0-0030988540
15. Merino A. M., Sabbaj S., Easlick J., Goepfert P., Kaslow R. A., Tang J., Dimorphic HLA-B signal peptides differentially influence HLA-E- and natural killer cell-mediated cytolysis of HIV-1-infected target cells. Clinical and Experimental Immunology 2013 174 3 414 423 10.1111/cei.12187 2-s2.0-84886312967
16. Stevens J., Joly E., Trowsdale J., Butcher G. W., Peptide binding characteristics of the non-classical class Ib MHC molecule HLA-E assessed by a recombinant random peptide approach. BMC Immunology 2001 2 1, article 5 2-s2.0-0001845725
17. Michaëlsson J., Teixeira de Matos C., Achour A., Lanier L. L., Kärre K., Söderström K., A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. Journal of Experimental Medicine 2002 196 11 1403 1414 10.1084/jem.20020797 2-s2.0-0037011156
18. Wooden S. L., Kalb S. R., Cotter R. J., Soloski M. J., 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. Journal of Immunology 2005 175 3 1383 1387 10.4049/jimmunol.175.3.1383 2-s2.0-22544439950
19. Nattermann J., Nischalke H. D., Hofmeister V., Kupfer B., Ahlenstiel G., Feldmann G., Rockstroh J., Weiss E. H., Sauerbruch T., Spengler U., HIV-1 infection leads to increased HLA-E expression resulting in impaired function of natural killer cells. Antiviral Therapy 2005 10 1 95 107 2-s2.0-18044365482
20. 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., Gliadin regulates the NK-dendritic cell cross-talk by HLA-E surface stabilization. Journal of Immunology 2007 179 1 372 381 10.4049/jimmunol.179.1.372 2-s2.0-34250807802
21. 35-44 stabilizes HLA-E expression and inhibits cytolysis mediated by natural killer cells. The American Journal of Pathology 2005 166 2 443 453 10.1016/S0002-9440(10)62267-5 2-s2.0-13244257273
22. Lampen M. H., Hassan C., Sluijter M., Geluk A., Dijkman K., Tjon J. M., de Ru A. H., van der Burg S. H., van Veelen P. A., van Hall T., Alternative peptide repertoire of HLA-E reveals a binding motif that is strikingly similar to HLA-A2. Molecular Immunology 2013 53 1-2 126 131 10.1016/j.molimm.2012.07.009 2-s2.0-84864936907
23. Posch P. E., Borrego F., Brooks A. G., Coligan J. E., HLA-E is the ligand for the natural killer cell CD94/NKG2 receptors. Journal of Biomedical Science 1998 5 5 321 331 10.1007/BF02253442 2-s2.0-0031717783
24. Braud V. M., Allan D. S. J., O'Callaghan C. A., Soderstrom K., D'Andrea A., Ogg G. S., Lazetic S., Young N. T., Bell J. I., Phillips J. H., Lanler L. L., McMichael A. J., HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 1998 391 6669 795 799 10.1038/35869 2-s2.0-0032546001
25. Kaiser B. K., Pizarro J. C., Kerns J., Strong R. K., Structural basis for NKG2A/CD94 recognition of HLA-E. Proceedings of the National Academy of Sciences of the United States of America 2008 105 18 6696 6701 10.1073/pnas.0802736105 2-s2.0-44349121055
26. Tomasec P., Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 2000 287 5455 1031 1033 10.1126/science.287.5455.1031 2-s2.0-0034635414
27. Heatley S. L., Pietra G., Lin J., Widjaja J. M. L., Harpur C. M., Lester S., Rossjohn J., Szer J., Schwarer A., Bradstock K., Bardy P. G., Mingari M. C., Moretta L., Sullivan L. C., Brooks A. G., Polymorphism in human cytomegalovirus UL40 impacts on recognition of human leukocyte antigen-E (HLA-E) by natural killer cells. Journal of Biological Chemistry 2013 288 12 8679 8690 10.1074/jbc.M112.409672 2-s2.0-84875438461
28. Pegram H. J., Andrews D. M., Smyth M. J., Darcy P. K., Kershaw M. H., Activating and inhibitory receptors of natural killer cells. Immunology and Cell Biology 2011 89 2 216 224 10.1038/icb.2010.78 2-s2.0-79951953456
29. Raulet D. H., Vance R. E., Self-tolerance of natural killer cells. Nature Reviews Immunology 2006 6 7 520 531 10.1038/nri1863 2-s2.0-33745567831
30. Valés-Gómez M., Reyburn H. T., Erskine R. A., López-Botet M., Strominger J. L., Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NIKG2-A and the activating receptor CD94/NKG2-C to HLA-E. The EMBO Journal 1999 18 15 4250 4260 10.1093/emboj/18.15.4250 2-s2.0-0345583696
31. Hoare H. L., Sullivan L. C., Clements C. S., Ely L. K., Beddoe T., Henderson K. N., Lin J., Reid H. H., Brooks A. G., Rossjohn J., Subtle changes in peptide conformation profoundly affect recognition of the non-classical MHC class I molecule HLA-E by the CD94-NKG2 natural killer cell receptors. Journal of Molecular Biology 2008 377 5 1297 1303 10.1016/j.jmb.2008.01.098 2-s2.0-40849101548
32. Pietra G., Romagnani C., Falco M., The analysis of the natural killer-like activity of human cytolytic T lymphocytes revealed HLA-E as a novel target for TCR alpha/beta-mediated recognition. European Journal of Immunology 2001 31 12 3687 3693 10.1002/1521-4141(200112)31:12<3687::AID-IMMU3687>3.0.CO;2-C
33. Garcia P., Llano M., de Heredia A. B., Willberg C. B., Caparrós E., Aparicio P., Braud V. M., López-Botet M., Human T cell receptor-mediated recognition of HLA-E. European Journal of Immunology 2002 32 4 936 944
34. + T cell subset in volunteers immunized with Salmonella enterica serovar Typhi strain Ty21a typhoid vaccine. Journal of Immunology 2004 173 9 5852 5862 10.4049/jimmunol.173.9.5852 2-s2.0-6344269539
35. Mazzarino P., Pietra G., Vacca P., Falco M., Colau D., Coulie P., Moretta L., Mingari M. C., Identification of effector-memory CMV-specific T lymphocytes that kill CMV-infected target cells in an HLA-E-restricted fashion. European Journal of Immunology 2005 35 11 3240 3247 10.1002/eji.200535343 2-s2.0-27944510988
36. + cytolytic T lymphocytes. Proceedings of the National Academy of Sciences of the United States of America 2003 100 19 10896 10901 10.1073/pnas.1834449100 2-s2.0-0141703232
37. Davis M. M., Boniface J. J., Reich Z., Ligand recognition by alpha beta T cell receptors. Annual Review of Immunology 1998 16 523 544
38. Hoare H. L., Sullivan L. C., Pietra G., Clements C. S., Lee E. J., Ely L. K., Beddoe T., Falco M., Kjer-Nielsen L., Reid H. H., McCluskey J., Moretta L., Rossjohn J., Brooks A. G., Structural basis for a major histocompatibility complex class Ib-restricted T cell response. Nature Immunology 2006 7 3 256 264 10.1038/ni1312 2-s2.0-33645944673
39. Sullivan L. C., Hoare H. L., McCluskey J., Rossjohn J., Brooks A. G., A structural perspective on MHC class Ib molecules in adaptive immunity. Trends in Immunology 2006 27 9 413 420 10.1016/j.it.2006.07.006 2-s2.0-33747040156
40. Nachmani D., Zimmermann A., Djian E. O., MicroRNA editing facilitates immune elimination of HCMV infected cells. PLoS Pathogens 2014 10 2 e1003963 10.1371/journal.ppat.1003963
41. Garrido F., Algarra I., MHC antigens and tumor escape from immune surveillance. Advances in Cancer Research 2001 83 117 158 10.1016/S0065-230X(01)83005-0 2-s2.0-0034788243
42. Ruiz-Cabello F., Cabrera T., Lopez-Nevot M.-A., Garrido F., Impaired surface antigen presentation in tumors: implications for T cell-based immunotherapy. Seminars in Cancer Biology 2002 12 1 15 24 2-s2.0-0036155882
43. Bossard C., Bézieau S., Matysiak-Budnik T., Volteau C., Laboisse C. L., Jotereau F., Mosnier J.-F., HLA-E/ β 2 microglobulin overexpression in colorectal cancer is associated with recruitment of inhibitory immune cells and tumor progression. International Journal of Cancer 2012 131 4 855 863 10.1002/ijc.26453 2-s2.0-84862578622
44. Levy E. M., Bianchini M., Von Euw E. M., Barrio M. M., Bravo A. I., Furman D., Domenichini E., Macagno C., Pinsky V., Zucchini C., Valvassori L., Mordoh J., Human leukocyte antigen-E protein is overexpressed in primary human colorectal cancer. International Journal of Oncology 2008 32 3 633 641 2-s2.0-40249101995
45. + T lymphocytes. Proceedings of the National Academy of Sciences of the United States of America 2011 108 26 10656 10661 10.1073/pnas.1100354108 2-s2.0-79960587042
46. + T lymphocytes in human cervical carcinoma. Cancer Research 2005 65 7 2921 2929 10.1158/0008-5472.CAN-04-2108 2-s2.0-16844368435
47. de Kruijf E. M., Sajet A., van Nes J. G. H., Natanov R., Putter H., Smit V. T. H. B. M., Liefers G. J., van den Elsen P. J., van de Velde C. J. H., Kuppen P. J. K., HLA-E and HLA-G expression in classical HLA class I-negative tumors is of prognostic value for clinical outcome of early breast cancer patients. Journal of Immunology 2010 185 12 7452 7459 10.4049/jimmunol.1002629 2-s2.0-78650666422
48. Wang E. C. Y., McSharry B., Retiere C., Tomasec P., Williams S., Borysiewicz L. K., Braud V. M., Wilkinson G. W. G., UL40-mediated NK evasion during productive infection with human cytomegalovirus. Proceedings of the National Academy of Sciences of the United States of America 2002 99 11 7570 7575 10.1073/pnas.112680099 2-s2.0-0037188543
49. Mocarski E. S. Jr., Immunomodulation by cytomegaloviruses: manipulative strategies beyond evasion. Trends in Microbiology 2002 10 7 332 339 10.1016/S0966-842X(02)02393-4 2-s2.0-0036646149
50. Halenius A., Hauka S., Dölken L., Stindt J., Reinhard H., Wiek C., Hanenberg H., Koszinowski U. H., Momburg F., Hengel H., Human cytomegalovirus disrupts the major histocompatibility complex class I peptide-loading complex and inhibits tapasin gene transcription. Journal of Virology 2011 85 7 3473 3485 10.1128/JVI.01923-10 2-s2.0-79952596162
51. Kraemer T., Schumacher H., Huyton T., Badrinath S., Moneer S., Blasczyk R., Bade-Doeding C., Loading complex and presentation of non-canonical peptides by HLA-E impacts NKG2-mediated cellular function. Tissue Antigens 2013 81 5 264 265
52. Fürst D., Bindja J., Arnold R., Herr W., Schwerdtfeger R., Müller C. H., Recker K., Schrezenmeier H., Mytilineos J., HLA-E polymorphisms in hematopoietic stem cell transplantation. Tissue Antigens 2012 79 4 287 290 10.1111/j.1399-0039.2011.01832.x 2-s2.0-84857785674
53. Danzer M., Polin H., Pröll J., Haunschmid R., Hofer K., Stabentheiner S., Hackl C., Kasparu H., König J., Hauser H., Binder M., Weiss R., Gabriel C., Krieger O., Clinical significance of HLA-E0103 homozygosity on survival after allogeneic hematopoietic stem-cell transplantation. Transplantation 2009 88 4 528 532 10.1097/TP.0b013e3181b0e79e 2-s2.0-70349153871
54. Ludajic K., Rosenmayr A., Faé I., Fischer G. F., Balavarca Y., Bickeböller H., Kalhs P., Greinix H. T., Association of HLA-E polymorphism with the outcome of hematopoietic stem-cell transplantation with unrelated donors. Transplantation 2009 88 10 1227 1228 10.1097/TP.0b013e3181bbb8fe 2-s2.0-73849094764
55. Allard M., Tonnerre P., Nedellec S., Oger R., Morice A., Guilloux Y., Houssaint E., Charreau B., Gervois N., HLA-E-restricted cross-recognition of allogeneic endothelial cells by CMV-associated CD8 T cells: a potential risk factor following transplantation. PLoS ONE 2012 7 11 e50951 10.1371/journal.pone.0050951 2-s2.0-84870626321
56. David G., Djaoud Z., Willem C., Legrand N., Rettman P., Gagne K., Cesbron A., Retière C., Large spectrum of HLA-C recognition by killer Ig-like receptor (KIR)2DL2 and KIR2DL3 and restricted C1 specificity of KIR2DS2: dominant impact of KIR2DL2/KIR2DS2 on KIR2D NK cell repertoire formation. Journal of Immunology 2013 191 9 4778 4788 10.4049/jimmunol.1301580 2-s2.0-84886045832
57. Sensi M., Pietra G., Molla A., Nicolini G., Vegetti C., Bersani I., Millo E., Weiss E., Moretta L., Mingari M. C., Anichini A., Peptides with dual binding specificity for HLA-A2 and HLA-E are encoded by alternatively spliced isoforms of the antioxidant enzyme peroxiredoxin 5. International Immunology 2009 21 3 257 268 10.1093/intimm/dxn141 2-s2.0-61349133041