The major histocompatibility complex class Ib molecule HLA-E at the interface between innate and adaptive immunity

Tissue Antigens

Volumn 72, Issue 5, 2008, Pages 415-424

  Sullivan, L C ^a   Clements, C S ^b   Rossjohn, J ^b   Brooks, A G ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

CD94 NKG2; HLA E; Major histocompatibility complex class I; T cell receptor

Indexed keywords

CD94 ANTIGEN; HLA B ANTIGEN; HLA E ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2A; T LYMPHOCYTE RECEPTOR;

ADAPTIVE IMMUNITY; AMINO ACID SUBSTITUTION; ANTIGEN PRESENTATION; BINDING AFFINITY; CD8+ T LYMPHOCYTE; COMPLEX FORMATION; DNA POLYMORPHISM; GENE FREQUENCY; GENOTYPE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; INNATE IMMUNITY; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

CD8-POSITIVE T-LYMPHOCYTES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; IMMUNITY, ACTIVE; IMMUNITY, INNATE; KILLER CELLS, NATURAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY D; POLYMORPHISM, GENETIC; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, NATURAL KILLER CELL;

EID: 54049123706     PISSN: 00012815     EISSN: 13990039     Source Type: Journal    
DOI: 10.1111/j.1399-0039.2008.01138.x     Document Type: Review

References (47)

1. Lee N, Goodlett DR, Ishitani A, Marquardt H, Geraghty DE. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J Immunol 1998 : 160 : 4951 60.
2. Lemberg MK, Bland FA, Weihofen A, Braud VM, Martoglio B. Intramembrane proteolysis of signal peptides: an essential step in the generation of HLA-E epitopes. J Immunol 2001 : 167 : 6441 6.
3. Bland FA, Lemberg MK, McMichael AJ, Martoglio B, Braud VM. Requirement of the proteasome for the trimming of signal peptide-derived epitopes presented by the nonclassical major histocompatibility complex class I molecule HLA-E. J Biol Chem 2003 : 278 : 33747 52.
4. Grimsley C, Kawasaki A, Gassner C et al. Definitive high resolution typing of HLA-E allelic polymorphisms: identifying potential errors in existing allele data. Tissue Antigens 2002 : 60 : 206 12.
5. Strong RK, Holmes MA, Li P, Braun L, Lee N, Geraghty DE. HLA-E allelic variants. Correlating differential expression, peptide affinities, crystal structures, and thermal stabilities. J Biol Chem 2003 : 278 : 5082 90.
6. Lafont BA, Buckler-White A, Plishka R, Buckler C, Martin MA. Pig-tailed macaques (Macaca nemestrina) possess six MHC-E families that are conserved among macaque species: implication for their binding to natural killer receptor variants. Immunogenetics 2004 : 56 : 142 54.
7. Stevens J, Joly E, Trowsdale J, Butcher GW. Peptide binding characteristics of the non-classical class Ib MHC molecule HLA-E assessed by a recombinant random peptide approach. BMC Immunol 2001 : 2 : 5.
8. Kurepa Z, Forman J. Peptide binding to the class Ib molecule, Qa-1b. J Immunol 1997 : 158 : 3244 51.
9. Yeager M, Hughes AL. Evolution of the mammalian MHC: natural selection, recombination, and convergent evolution. Immunol Rev 1999 : 167 : 45 58.
10. Joly E, Rouillon V. The orthology of HLA-E and H2-Qa1 is hidden by their concerted evolution with other MHC class I molecules. Biol Direct 2006 : 1 : 2.
11. O'Callaghan CA, Tormo J, Willcox BE et al. Structural features impose tight peptide binding specificity in the nonclassical MHC molecule HLA-E. Mol Cell 1998 : 1 : 531 41.
12. Braud VM, Allan DS, O'Callaghan CA et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 1998 : 391 : 795 9.
13. Brooks AG, Borrego F, Posch PE et al. Specific recognition of HLA-E, but not classical, HLA class I molecules by soluble CD94/NKG2A and NK cells. J Immunol 1999 : 162 : 305 13.
14. Gao GF, Willcox BE, Wyer JR et al. Classical and nonclassical class I major histocompatibility complex molecules exhibit subtle conformational differences that affect binding to CD8alphaalpha. J Biol Chem 2000 : 275 : 15232 8.
15. Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. 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 1998 : 187 : 813 8.
16. Lee N, Llano M, Carretero M et al. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci U S A 1998 : 95 : 5199 204.
17. Brooks AG, Posch PE, Scorzelli CJ, Borrego F, Coligan JE. NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J Exp Med 1997 : 185 : 795 800.
18. Carretero M, Cantoni C, Bellon T et al. The CD94 and NKG2-A C-type lectins covalently assemble to form a natural killer cell inhibitory receptor for HLA class I molecules. Eur J Immunol 1997 : 27 : 563 7.
19. Lazetic S, Chang C, Houchins JP, Lanier LL, Phillips JH. Human natural killer cell receptors involved in MHC class I recognition are disulfide-linked heterodimers of CD94 and NKG2 subunits. J Immunol 1996 : 157 : 4741 5.
20. Brostjan C, Bellon T, Sobanov Y, Lopez-Botet M, Hofer E. Differential expression of inhibitory and activating CD94/NKG2 receptors on NK cell clones. J Immunol Methods 2002 : 264 : 109 19.
21. Houchins JP, Lanier LL, Niemi EC, Phillips JH, Ryan JC. Natural killer cell cytolytic activity is inhibited by NKG2-A and activated by NKG2-C. J Immunol 1997 : 158 : 3603 9.
22. Lanier LL, Corliss B, Wu J, Phillips JH. Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity 1998 : 8 : 693 701.
23. Maenaka K, Juji T, Nakayama T et al. Killer cell immunoglobulin receptors and T cell receptors bind peptide-major histocompatibility complex class I with distinct thermodynamic and kinetic properties. J Biol Chem 1999 : 274 : 28329 34.
24. Kaiser BK, Barahmand-Pour F, Paulsene W, Medley S, Geraghty DE, Strong RK. Interactions between NKG2x immunoreceptors and HLA-E ligands display overlapping affinities and thermodynamics. J Immunol 2005 : 174 : 2878 84.
25. Sullivan LC, Clements CS, Beddoe T et al. The heterodimeric assembly of the CD94-NKG2 receptor family and implications for human leukocyte antigen-E recognition. Immunity 2007 : 27 : 900 11.
26. Vales-Gomez M, Reyburn HT, Erskine RA, Lopez-Botet M, Strominger JL. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J 1999 : 18 : 4250 60.
27. Wada H, Matsumoto N, Maenaka K, Suzuki K, Yamamoto K. The inhibitory NK cell receptor CD94/NKG2A and the activating receptor CD94/NKG2C bind the top of HLA-E through mostly shared but partly distinct sets of HLA-E residues. Eur J Immunol 2004 : 34 : 81 90.
28. Petrie EJ, Clements CS, Lin J et al. CD94-NKG2A recognition of human leukocyte antigen (HLA)-E bound to an HLA class I leader sequence. J Exp Med 2008 : 205 : 725 35.
29. King A, Boocock C, Sharkey AM et al. Evidence for the expression of HLAA-C class I mRNA and protein by human first trimester trophoblast. J Immunol 1996 : 156 : 2068 76.
30. Hoare HL, Sullivan LC, Clements CS et al. 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. J Mol Biol 2008 : 377 : 1297 303.
31. Miller JD, Weber DA, Ibegbu C, Pohl J, Altman JD, Jensen PE. Analysis of HLA-E peptide-binding specificity and contact residues in bound peptide required for recognition by CD94/NKG2. J Immunol 2003 : 171 : 1369 75.
32. Michaelsson J, Teixeira de Matos C, Achour A, Lanier LL, Karre K, Soderstrom K. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J Exp Med 2002 : 196 : 1403 14.
33. Tomasec P, Braud VM, Rickards C et al. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 2000 : 287 : 1031.
34. Nattermann J, Nischalke HD, Hofmeister V et al. The HLA-A2 restricted T cell epitope HCV Core35-44 stabilizes HLA-E expression and inhibits cytolysis mediated by natural killer cells. Am J Pathol 2005 : 166 : 443 53.
35. Nattermann J, Nischalke HD, Hofmeister V et al. HIV-1 infection leads to increased HLA-E expression resulting in impaired function of natural killer cells. Antivir Ther 2005 : 10 : 95 107.
36. Guma M, Budt M, Saez A et al. Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 2006 : 107 : 3624 31.
37. Kaiser BK, Pizarro JC, Kerns J, Strong RK. Structural basis for NKG2A/CD94 recognition of HLA-E. Proc Natl Acad Sci U S A 2008 : 105 : 6696 701.
38. Pietra G, Romagnani C, Falco M et al. 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. Eur J Immunol 2001 : 31 : 3687 93.
39. Pietra G, Romagnani C, Mazzarino P et al. HLA-E-restricted recognition of cytomegalovirus-derived peptides by human CD8+ cytolytic T lymphocytes. Proc Natl Acad Sci U S A 2003 : 100 : 10896 901.
40. Mazzarino P, Pietra G, Vacca P et al. Identification of effector-memory CMV-specific T lymphocytes that kill CMV-infected target cells in an HLA-E-restricted fashion. Eur J Immunol 2005 : 35 : 3240 7.
41. Hoare HL, Sullivan LC, Pietra G et al. Structural basis for a major histocompatibility complex class Ib-restricted T cell response. Nat Immunol 2006 : 7 : 256 64.
42. Salerno-Goncalves R, Fernandez-Vina M, Lewinsohn DM, Sztein MB. Identification of a human HLA-E-restricted CD8+ T cell subset in volunteers immunized with Salmonella enterica serovar Typhi strain Ty21a typhoid vaccine. J Immunol 2004 : 173 : 5852 62.
43. Heinzel AS, Grotzke JE, Lines RA et al. HLA-E-dependent presentation of Mtb-derived antigen to human CD8+ T cells. J Exp Med 2002 : 196 : 1473 81.
44. Tamouza R, Busson M, Rocha V et al. 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 2006 : 82 : 1436 40.
45. Tamouza R, Rocha V, Busson M et al. Association of HLA-E polymorphism with severe bacterial infection and early transplant-related mortality in matched unrelated bone marrow transplantation. Transplantation 2005 : 80 : 140 4.
46. Fishman JA, Rubin RH. Infection in organ-transplant recipients. N Engl J Med 1998 : 338 : 1741 51.
47. Romagnani C, Pietra G, Falco M et al. 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 2002 : 99 : 11328 33.