T cells engaging the conserved MHC class Ib molecule Qa-1b with TAP-independent peptides are semi-invariant lymphocytes

Frontiers in Immunology

Volumn 9, Issue JAN, 2018, Pages

  Doorduijn, Elien M ^a   Sluijter, Marjolein ^a   Querido, Bianca J ^a   Seidel, Ursula J E ^a   Oliveira, Claudia C ^a   van der Burg, Sjoerd H ^a   van Hall, Thorbald ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

CD8+ T cells; Non classical MHC; Peptide transporter TAP; Qa 1b; T cell receptor; Thymus

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; HLA B ANTIGEN; HLA E ANTIGEN; HLA QA1B ANTIGEN; INTERLEUKIN 2 RECEPTOR BETA; PEPTIDE TRANSPORTER TAP; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA BETA CHAIN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; T LYMPHOCYTE RECEPTOR V ALPHA CHAIN; T LYMPHOCYTE RECEPTOR V BETA CHAIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; MEMORY CELL; MOUSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; SPLEEN CELL; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; THYMUS; VACCINATION;

EID: 85041114213     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2018.00060     Document Type: Article

References (45)

1. Jensen PE, Sullivan BA, Reed-Loisel LM, Weber DA. Qa-1, a nonclassical class I histocompatibility molecule with roles in innate and adaptive immunity. Immunol Res (2004) 29:81-92. doi:10.1385/IR:29:1-3:081
2. Rodgers JR, Cook RG. MHC class Ib molecules bridge innate and acquired immunity. Nat Rev Immunol (2005) 5:459-71. doi:10.1038/nri1635
3. Aldrich CJ, DeCloux A, Woods AS, Cotter RJ, Soloski MJ, Forman J. Identification of a Tap-dependent leader peptide recognized by alloreactive T cells specific for a class Ib antigen. Cell (1994) 79:649-58. doi:10.1016/0092-8674(94)90550-9
4. DeCloux A, Woods AS, Cotter RJ, Soloski MJ, Forman J. Dominance of a single peptide bound to the class I(B) molecule, Qa-1b. J Immunol (1997) 158:2183-91
5. Kurepa Z, Hasemann CA, Forman J. Qa-1b binds conserved class I leader peptides derived from several mammalian species. J Exp Med (1998) 188:973-8. doi:10.1084/jem.188.5.973
6. van Hall T, Oliveira CC, Joosten SA, OttenhoffTH. The other Janus face of Qa-1 and HLA-E: diverse peptide repertoires in times of stress. Microbes Infect (2010) 12:910-8. doi:10.1016/j.micinf.2010.07.011
7. Zeng L, Sullivan LC, Vivian JP, Walpole NG, Harpur CM, Rossjohn J, et al. A structural basis for antigen presentation by the MHC class Ib molecule, Qa-1b. J Immunol (2012) 188:302-10. doi:10.4049/jimmunol.1102379
8. Davies A, Kalb S, Liang B, Aldrich CJ, Lemonnier FA, Jiang H, et al. A peptide from heat shock protein 60 is the dominant peptide bound to Qa-1 in the absence of the MHC class Ia leader sequence peptide Qdm. J Immunol (2003) 170:5027-33. doi:10.4049/jimmunol.170.10.5027
9. Chun T, Aldrich CJ, Baldeon ME, Kawczynski LV, Soloski MJ, Gaskins HR. Constitutive and regulated expression of the class IB molecule Qa-1 in pancreatic beta cells. Immunology (1998) 94:64-71. doi:10.1046/j.1365-2567.1998.00475.x
10. Tompkins SM, Kraft JR, Dao CT, Soloski MJ, Jensen PE. Transporters associated with antigen processing (TAP)-independent presentation of soluble insulin to alpha/beta T cells by the class Ib gene product, Qa-1(b). J Exp Med (1998) 188:961-71. doi:10.1084/jem.188.5.961
11. Lo WF, Woods AS, DeCloux A, Cotter RJ, Metcalf ES, Soloski MJ. Molecular mimicry mediated by MHC class Ib molecules after infection with Gram-negative pathogens. Nat Med (2000) 6:215-8. doi:10.1038/72329
12. Wooden SL, Kalb SR, Cotter RJ, Soloski MJ. 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 (2005) 175:1383-7. doi:10.4049/jimmunol.175.3.1383
13. Hansen SG, Wu HL, Burwitz BJ, Hughes CM, Hammond KB, Ventura AB, et al. Broadly targeted CD8(+) T cell responses restricted by major histocompatibility complex E. Science (2016) 351:714-20. doi:10.1126/science.aac9475
14. Heinzel AS, Grotzke JE, Lines RA, Lewinsohn DA, McNabb AL, Streblow DN, et al. HLA-E-dependent presentation of Mtb-derived antigen to human CD8+ T cells. J Exp Med (2002) 196:1473-81. doi:10.1084/jem.20020609
15. Nattermann J, Nischalke HD, Hofmeister V, Ahlenstiel G, Zimmermann H, Leifeld L, et al. 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 (2005) 166:443-53. doi:10.1016/S0002-9440(10)62267-5
16. 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. doi:10.4049/jimmunol.173.9.5852
17. Tomasec P, Braud VM, Rickards C, Powell MB, McSharry BP, Gadola S, et al. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science (2000) 287:1031. doi:10.1126/science.287.5455.1031
18. Bian Y, Shang S, Siddiqui S, Zhao J, Joosten SA, OttenhoffTHM, et al. MHC Ib molecule Qa-1 presents Mycobacterium tuberculosis peptide antigens to CD8+ T cells and contributes to protection against infection. PLoS Pathog (2017) 13:e1006384. doi:10.1371/journal.ppat.1006384
19. Caccamo N, Pietra G, Sullivan LC, Brooks AG, Prezzemolo T, La Manna MP, et al. Human CD8 T lymphocytes recognize Mycobacterium tuberculosis antigens presented by HLA-E during active tuberculosis and express type 2 cytokines. Eur J Immunol (2015) 45:1069-81. doi:10.1002/eji.201445193
20. Joosten SA, van Meijgaarden KE, van Weeren PC, Kazi F, Geluk A, Savage ND, et al. Mycobacterium tuberculosis peptides presented by HLA-E molecules are targets for human CD8 T-cells with cytotoxic as well as regulatory activity. PLoS Pathog (2010) 6:e1000782. doi:10.1371/journal.ppat.1000782
21. Hu D, Ikizawa K, Lu L, Sanchirico ME, Shinohara ML, Cantor H. Analysis of regulatory CD8 T cells in Qa-1-deficient mice. Nat Immunol (2004) 5:516-23. doi:10.1038/ni1063
22. Jiang H, Canfield SM, Gallagher MP, Jiang HH, Jiang Y, Zheng Z, et al. HLA-E-restricted regulatory CD8(+) T cells are involved in development and control of human autoimmune type 1 diabetes. J Clin Invest (2010) 120:3641-50. doi:10.1172/JCI43522
23. Kim HJ, Verbinnen B, Tang X, Lu L, Cantor H. Inhibition of follicular T-helper cells by CD8(+) regulatory T cells is essential for self tolerance. Nature (2010) 467:328-32. doi:10.1038/nature09370
24. Hoare HL, Sullivan LC, Pietra G, Clements CS, Lee EJ, Ely LK, et al. Structural basis for a major histocompatibility complex class Ib-restricted T cell response. Nat Immunol (2006) 7:256-64. doi:10.1038/ni1312
25. O'Callaghan CA, Tormo J, Willcox BE, Braud VM, Jakobsen BK, Stuart DI, et al. Structural features impose tight peptide binding specificity in the nonclassical MHC molecule HLA-E. Mol Cell (1998) 1:531-41. doi:10.1016/S1097-2765(00)80053-2
26. Nagarajan NA, Gonzalez F, Shastri N. Nonclassical MHC class Ib-restricted cytotoxic T cells monitor antigen processing in the endoplasmic reticulum. Nat Immunol (2012) 13:579-86. doi:10.1038/ni.2282
27. Oliveira CC, van Veelen PA, Querido B, de Ru A, Sluijter M, Laban S, et al. The nonpolymorphic MHC Qa-1b mediates CD8+ T cell surveillance of antigen-processing defects. J Exp Med (2010) 207:207-21. doi:10.1084/jem.20091429
28. Lampen MH, Hassan C, Sluijter M, Geluk A, Dijkman K, Tjon JM, et al. Alternative peptide repertoire of HLA-E reveals a binding motif that is strikingly similar to HLA-A2. Mol Immunol (2013) 53:126-31. doi:10.1016/j.molimm.2012.07.009
29. van Montfoort N, Camps MG, Khan S, Filippov DV, Weterings JJ, Griffith JM, et al. Antigen storage compartments in mature dendritic cells facilitate prolonged cytotoxic T lymphocyte cross-priming capacity. Proc Natl Acad Sci U S A (2009) 106:6730-5. doi:10.1073/pnas.0900969106
30. Zhumabekov T, Corbella P, Tolaini M, Kioussis D. Improved version of a human CD2 minigene based vector for T cell-specific expression in transgenic mice. J Immunol Methods (1995) 185:133-40. doi:10.1016/0022-1759(95)00124-S
31. Doorduijn EM, Sluijter M, Querido BJ, Oliveira CC, Achour A, Ossendorp F, et al. TAP-independent self-peptides enhance T cell recognition of immune-escaped tumors. J Clin Invest (2016) 126:784-94. doi:10.1172/JCI83671
32. Guan J, Yang SJ, Gonzalez F, Yin Y, Shastri N. Antigen processing in the endoplasmic reticulum is monitored by semi-invariant alphabeta TCRs specific for a conserved peptide-Qa-1b MHC class Ib ligand. J Immunol (2017) 198:2017-27. doi:10.4049/jimmunol.1600764
33. Van Kaer L, Ashton-Rickardt PG, Ploegh HL, Tonegawa S. TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells. Cell (1992) 71:1205-14. doi:10.1016/S0092-8674(05)80068-6
34. van Hall T, Laban S, Koppers-Lalic D, Koch J, Precup C, Asmawidjaja P, et al. The varicellovirus-encoded TAP inhibitor UL49.5 regulates the presentation of CTL epitopes by Qa-1b1. J Immunol (2007) 178:657-62. doi:10.4049/jimmunol.178.2.657
35. Koppers-Lalic D, Reits EA, Ressing ME, Lipinska AD, Abele R, Koch J, et al. Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the transporter associated with antigen processing. Proc Natl Acad Sci U S A (2005) 102:5144-9. doi:10.1073/pnas.0501463102
36. Kraft JR, Vance RE, Pohl J, Martin AM, Raulet DH, Jensen PE. Analysis of Qa-1(b) peptide binding specificity and the capacity of CD94/NKG2A to discriminate between Qa-1-peptide complexes. J Exp Med (2000) 192:613-24. doi:10.1084/jem.192.5.613
37. Stritesky GL, Jameson SC, Hogquist KA. Selection of self-reactive T cells in the thymus. Annu Rev Immunol (2012) 30:95-114. doi:10.1146/annurev-immunol-020711-075035
38. Bendelac A, Savage PB, Teyton L. The biology of NKT cells. Annu Rev Immunol (2007) 25:297-336. doi:10.1146/annurev.immunol.25.022106.141711
39. Birkinshaw RW, Kjer-Nielsen L, Eckle SB, McCluskey J, Rossjohn J. MAITs, MR1 and vitamin B metabolites. Curr Opin Immunol (2014) 26:7-13. doi:10.1016/j.coi.2013.09.007
40. Kain L, Costanzo A, Webb B, Holt M, Bendelac A, Savage PB, et al. Endogenous ligands of natural killer T cells are alpha-linked glycosylceramides. Mol Immunol (2015) 68:94-7. doi:10.1016/j.molimm.2015.06.009
41. de Jong A, Pena-Cruz V, Cheng TY, Clark RA, Van Rhijn I, Moody DB. CD1a-autoreactive T cells are a normal component of the human alphabeta T cell repertoire. Nat Immunol (2010) 11:1102-9. doi:10.1038/ni.1956
42. Maurice MM, Gould DS, Carroll J, Vugmeyster Y, Ploegh HL. Positive selection of an MHC class-I restricted TCR in the absence of classical MHC class I molecules. Proc Natl Acad Sci U S A (2001) 98:7437-42. doi:10.1073/pnas.141143298
43. Reed-Loisel LM, Sullivan BA, Laur O, Jensen PE. An MHC class Ib-restricted TCR that cross-reacts with an MHC class Ia molecule. J Immunol (2005) 174:7746-52. doi:10.4049/jimmunol.174.12.7746
44. Urdahl KB, Sun JC, Bevan MJ. Positive selection of MHC class Ib-restricted CD8+ T cells on hematopoietic cells. Nat Immunol (2002) 3:772-9. doi:10.1038/ni814
45. Engel I, Kronenberg M. Making memory at birth: understanding the differentiation of natural killer T cells. Curr Opin Immunol (2012) 24:184-90. doi:10.1016/j.coi.2012.01.012