Qa-1, a nonclassical class I histocompatibility molecule with roles in innate and adaptive immunity
Tóm tắt
Qa-1, a nonclassical class I histocompatibility molecule expressed in mice, predominantly assembles with a single nonameric peptide, Qdm, derived from the signal sequence of certain class Ia molecules. The Qa-1/Qdm complex is the primary ligand for CD94/NKG2A inhibitory receptors expressed on a major fraction of natural killer (NK) cells. cells become susceptible to killing by NK cells under conditions where surface expression of the Qa-1/Qdm inhibitory ligand is reduced. The CD94/NKG2 “missingself” recognition system serves as mechanism for removing cells that have abnormalities in the intracellular machinery required for assembly and expression of class I-peptides complexes, as a consequence of viral infection, for example. Despite its highly focused peptide-binding specificity, Qa-1 also has a capacity to act as an antigen-presentation molecule for CD8+ T cells. It appears that a small subpopulation of these T cells undergoes positive selection by interaction with Qa-1 in the thymus, and they maintain their specificity for Qa-1 after maturation. The role of these unusual T cells in adaptive immune responses remains to be defined.
Tài liệu tham khảo
Lalanne JL, Transy C, Guerin S, Darche S, Meulien P, Kourilsky P: Expression of class I genes in the major histocompatibility complex: identification of eight distinct mRNAs in DBA/2 mouse liver. Cell 1985;41:469–478.
Transy C, Nash SR, David-Watine B, Cochet M, Hunt SWD, Hood LE, Kourilsky P: A low polymorphic mouse H-2 class I gene from the Tla complex is expressed in a broad variety of cell types. J Exp Med 1987;166:341–361.
Wolf PR, Cook RG: The class I-b molecule Qa-1 forms heterodimers with H-2Ld and a novel 50-kD glycoprotein encoded centromeric to I-E beta PG-657-68. J Exp Med 1995;181:657–668.
Stanton TH, Boyse EA: A new serologically defined locus, Qa-1, in the Tla-region of the mouse. Immunogenetics 1976;3:525–531.
Stevens C, Flaherty L: Evidence foe antigen presentation by the class Ib molecule, Qa-1. Res Immunol 1996;147:286–290.
Connolly DJ, Cotterill LA, Hederer RA, Thorpe CJ, Travers PJ, McVey JH, et al.: A cDNA clone encoding the mouse Qa-1 a histocompatibility antigen and proposed structure of the putative peptide binding site. J Immunol 1993;151:6089–6098.
Hermel E, Hart AJ, Miller R, Aldrich CJ: CTL and sequence analyses of MHC class 1B antigens Qa1c (H2-T23r) and QaId (H2-T23f). Immunogenetics 1999;49:712–717.
Bouvier M, Wiley DC: Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules. Science 1994;265:398–402.
Kastner DL, Rich RR, Shen FW: Qa-1-associated antigens. I. Generation of H-2-nonrestricted cytotoxic T lymphocytes specific for determinants of the Qa-1 region. J Immunol 1979;123:1232–1238.
Forman J: H-2 unrestricted cytotoxic T cell activity against antigens controlled by genes in the QA/TLA region. J Immunol 1979;123:2451–2455.
Lindahl KF, Hausmann B, Flaherty L: Polymorphism of a Qa-1-associated antigen defined by cytotoxic T cells. I. Qed-1 a and Qed-1 d. Eur J Immunol 1982;12:159–166.
Aldrich CJ, Rodgers JR, Rich RR: Regulation of Qa-1 expression and determinant modification by an H-2D-linked gene, Qdm. Immunogenet 1988;28:334–344.
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;79:649–658.
DeCloux A, Woods AS, Cotter RJ, Soloski MJ, Forman J: Dominance of a single peptide bound to the class 1(B) molecule, Qa-1b. J Immunol 1997;158:2183–2191.
Cotterill LA, Stauss HJ, Millrain MM, Pappin DJ, Rahman D, Canas B, et al.: Qa-1 interaction and T cell recognition of the Qa-1 determinant modifier peptide. Eur J Immunol 1997;27:2123–2132.
Aldrich CJ, Waltrip R, Hermel E, Attaya M, Lindahl KF, Monaco JJ, Forman J: T cell recognition of QA-1b antigens on cells lacking a functional Tap-2 transporter. J Immunol 1992;149:3773–3777.
Lowen LC, Aldrich CJ, Forman J: Analysis of T cell receptors specific for recognition of class IB antigens. J Immunol 1993;151:6155–6165.
Vidovic D, Roglic M, McKune K, Guerder S, MacKay C, Dembic Z: Qa-1 restricted recognition of foreign antigen by a gamma delta T-cell hybridoma. Nature 1989;340:646–650.
Imani F, Soloski MJ: Heat shock proteins can regulate expression of the Tla region-encoded class Ib molecule Qa-1. Proc Natl Acad Sci USA 1991;88:10475–10479.
Bouwer HG, Lindahl KF, Baldridge JR, Wagner CR, Barry RA, Hinrichs DJ: An H2-T MHC class Ib molecule presents Listeria monocytogenes-derived antigen to immune CD8+ cytotoxic T cells. J Immunol 1994;152:5352–5360.
Bouwer HG, Seaman MS, Forman J, Hinrichs DJ: MHC class Ib-restricted cells contribute to antilisterial immunity: evidence for Qa-1b as a key restricting element for Listeria-specific CTLs. J Immunol 1997;159:2795–2801.
Bouwer HG, Bai A, Forman J, Gregory SH, Wing EJ, Barry RA, Hinrichs DJ: Listeria monocytogenes-infected hepatocytes are targets of major histocompatibility complex class Ib-restricted antilisterial cytotoxic T lymphocytes. Infect Immun 1998;66:2814–2817.
Seaman MS, Perarnau B, Lindahl KF, Lemonnier FA, Forman J: Response to Listeria monocytogenes in mice lacking MHC class Ia molecules. J Immunol 1999;162:5429–5436.
Bouwer HG, Barry RA, Hinrichs DJ: Lack of expansion of major histocompatibility complex class Ib-restricted effector cells following recovery from secondary infection with the intracellular pathogen Listeria monocytogenes. Infect Immun 2001;69:2286–2292.
Lo WF, Ong H, Metcalf ES, Soloski MJ: T cell responses to Gram-negative intracellular bacterial pathogens: a role for CD8+ T cells in immunity to Salmonella infection and the involvement of MHC class Ib molecules. J Immunol 1999;162:5398–5406.
Lo WF, Woods AS, DeCloux A, Cotter RJ, Metcalf ES, Soloski MJ: Molecular minicry mediated by MHC class Ib molecules after infection with gram-negative pathogens. Nat Med 2000;6:215–218.
Soloski MJ, Metcalf ES: The involvement of class Ib molecules in the host response to infection with Salmonella and its relevance to autoimmunity. Microbes Infect 2001;3:1249–1259.
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 1a leader sequence peptide Qdm. J Immunol 2003;170:5027–5033.
Chun T, Aldrich CJ, Baldeon ME, Kawczynski LV, Soloski MJ, Gaskins HR: Constitutive and regulated expression of the class 1B molecule Qa-1 in pancreatic beta cells. Immunology 1998;94:64–71.
Jiang H, Ware R, Stall A, Flaherty L, Chess L, Pernis B: Murine CD8+ T cells that specifically delete autologous CD4+ T cells expressing V beta 8 TCR: a role of the Qa-1 molecule. Immunity 1995;2:185–194.
Jiang H, Chess L: The specific regulation of immune responses by CD8+ T cells restricted by the MHC class 1b molecule, Qa-1. Annu Rev Immunol 2000;18:185–216.
Jiang H, Braunstein NS, Yu B, Winchester R, Chess L: CD8+ T cells control the TH phenotype of MBP-reactive CD4+ T cells in EAE mice. Proc Natl Acad Sci USA 2001;98:6301–6306.
Noble A, Zhao ZS, Cantor H: Suppression of immune responses by CD8 cells. II. Qa-1 on activated B cells stimulates CD8 cell suppression of T helper 2 responses. PG-566-71. J Immunol 1998;160:566–571.
D'Orazio TJ, Mayhew E, Niederkorn JY: Ocular immune privilege promoted by the presentation of peptide on tolerogenic B cells in the spleen. II. Evidence for presentation by Qa-1. J Immunol 2001;166:26–32.
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; 192:613–624.
Salcedo M, Bousso P, Ljunggren HG, Kourilsky P, Abastado JP: The Qa-1 b molecule binds to a large subpopulation of murine NK cells. Eur J Immunol 1998;28:4356–4361.
Salcedo M, Colucci F, Dyson PJ, Cotterill LA, Lemonnier FA, Kourilsky P, et al.: Role of Qa-1(b)-binding receptors in the specificity of developing NK cells. Eur J Immunol 2000;30:1094–1101.
Vance RE, Kraft JR, Altman JD, Jensen PE, Raulet DH: Mouse CD94/NKG2A is a natural killer cell receptor for the nonclassical major histocompatibility complex (MHC) class 1 molecule Qa-1(b). J Exp Med 1998;188:1841–1848.
Vance RE, Jamieson AM, Raulet DH: Recognition of the class Ib molecule Qa-1 (b) by putative activating receptors CD94/NKG2C and CD94/NKG2E on mouse natural killer cells. J Exp Med 1999;190:1801–1812.
Moser JM, Gibbs J, Jensen PE, Lukacher AE: CD94-NKG2A receptors regulate antiviral CD8(+) T cell responses. Nat Immunol 2002;3:189–195.
Miller JD, Peters M, Oran AE, Beresford GW, Harrington L, Boss JM, Altman JD: CD94/NKG2 expression does not inhibit cytotoxic function of lymphocytic choriomeningitis virus-specific CD8+ T cells. J Immunol 2002;169:693–701.
McMahon CW, Zajac AJ, Jamieson AM, Corral L, Hammer GE, Ahmed R, Raulet DH: Viral and bacterial infections induce expression of multiple NK cell receptors in responding CD8(+) T cells. J Immunol 2002;169:1444–1452.
Meyers JH, Ryu A, Monney L, Nguyen K, Greenfield EA, Freeman GJ, Kuchnoo VK: Cutting edge: CD94/NKG2 is expressed on Th1 but not Th2 cells and costimulates Th1 effector functions. J Immunol 2002;169:5382–5386.
Braud VM, Aldemir H, Breart B, Ferlin WG: Expression of CD94-NK G2A inhibitory receptor is restricted to a subset of CD8(+) T cells. Trends Immunol 2003;24:162–164.
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;391:795–799.
Lee N, Llano M, Carretero M, Ishitani A, Navarro F, Lopez-Botet M, Geraghty DE: HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci USA 1998;95:5199–5204
Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG: Recognition of human histocompatility 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;187:813–818.
Keck K: Ir-gene control of immunogenicity of insulin and A-chain loop as a carrier determinant. Nature 1975;254:78–79.
Thayer WP, Kraft JR, Tompkins SM, Moore JCt, Jensen PE: Assessment of the role of determinant selection in genetic control of the immune response to insulin in H-2b mice. J Immunol 1999;163:2549–2554.
Jensen PE: Reduction of disulfide bonds during antigen processing: evidence from a thiol-dependent insulin determinant. J Exp Med 1991;174:1121–1130.
Fink PJ, Bevan MJ: Positive selection of thymocytes. Adv Immunol 1995;59:99–133.
Fowlkes BJ SE: Positive selection of T cells. Curr Opin Immunol 1995;7:188–195.
Bendelac A: Positive selection of mouse NK1+T cells by CD1-expressing cortical thymocytes. J Exp Med 1995;182:2091–2096.
Coles MC, Raulet DH: NK 1.1+T cells in the liver arise in the thymus and are selected by interactions with class I molecules on CD4+CD8+ cells. J Immunol 2000;164:2412–2418.
Urdahl KB, Sun JC, Bevan MJ: Positive selection of MHC class Ib-restricted CD8(+) T cells on hematopoietic cells. Nat Immunol 2002;3:772–779.
Pacasova R, Martinozzi S, Boulouis HJ, Szpak Y, Ulbrecht M, Sigaux F, et al.: Cell surface detection of HLA-E gene products with a specific monoclonal antibody. J Reprod Immunol 1999;43:195–201.
Pietra G, Romagnani C, Falco M, Vitale M, Castriconi R, Pende D, 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;31:3687–3693.
Romagnani C, Pietra G, Falco M, Millo E, Mazzarino P, Biassoni R, 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 USA 2002;99:11328–11333.
Garcia P, Llano M, de Heredia AB, Willberg CB, Caparros E, Aparicio P, et al.: Human T cell receptor-mediated recognition of HLA-E. Eur J Immunol 2002;32:936–944.
Li J, Goldstein I, Glickman-Nir E, Jiang H, Chess L: Induction of TCR V beta-specific CD8+CTLs by TCR V beta-derived peptides bound to HLA-E. J Immunol 2001;167:3800–3808.
Heinzel AS, Grotzke JE, Lines RA, Lewinsohn OA, McNabb AL, Streblow DN, et al.: HLA-E-dependent presentation of Mtb-derived antigen to human CD8+T cells. J Exp Med 2002;196:1473–1481.
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;171:1369–1375.
Braud V, Jones EY, 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. Eur J Immunol 1997;27:1164–1169.
O'Callaghan CA, Tomo J, Willcos 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;1:531–541.
Karre K, Ljunggren HG, Piontek G, Kiessling R: Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 1986;319:675–678.
Ljunggren HG, Karre K: In search of the ‘missing self’ MHC molecules and NK cell recognition. Immunol Today 1990;11:237–244.
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;158:3603–3609.
Lanier LL, Corliss B, Wu J, Phillips JH: Association of DAP 12 with activating CD94/NKG2C NK cell receptors. Immunity 1998;8:693–701.
Lohwasser S, Kubota A, Salcedo M, Lian RH, Takei F: The non-classical MHC class I molecule Qa-1(b) inhibits classical MHC class I-restricted cytotoxicity of cytotoxic T lymphocytes. Int Immunol 2001;13:321–327.
Braud VM, Allan DS, Wilson D, McMichael AJ: TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr Biol 1998;8:1–10.
Le Drean E, Vely F, Olcese L, Cambiaggi A, Guia S, Krystal G, et al.: Inhibition of antigen-induced T cell response and antibody-induced NK cell cytotoxicity by NKG2A: association of NKG2A with SHP-1 and SHP-2 protein-tyrosine phosphatases. Eur J Immunol 1998;28:264–276.
Noppen C, Schaefer C, Zajac P, Schutz A, Kocher T, Kloth J, et al.: C-type lectin-like receptors in peptidespecific HLA class I-restricted cytotoxic T lymphocytes: differential expression and modulation of effector functions in clones sharing identical TCR structure and epitope specificity. Eur J Immunol 1998;28:1134–1142.
Speiser DE, Pittet MJ, Valmori D, Dunbar R, Rimoldi D, Lienard D, et al.: In vivo expression of natural killer cell inhibitory receptors by human melanoma-specific cytolytic T lymphocytes. J Exp Med 1999;190:775–782.
Mingari MC, Ponte M, Bertone S, Schiavetti F, Vitale C, Bellomo R, et al.: HLA class I-specific inhibitory receptors in human T lymphocytes: interleukin 15-induced expression of CD94/NKG2A in sure rantigen- or alloantigen-activated CD8+ T cells. Proc Natl Acad Sci USA 1998;95:1172–1177.
Gunturi A, Berg RE, Forman J: Preferential survival of CD8 T and NK cells expressing high levels of CD94. J Immunol 2003;170:1737–1745.
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;196:1403–1414.
Llano M, Lee N, Navarro F, Garcia P, Albar JP, Geraghty DE, Lopez-Botet M: HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur J Immunol 1998;28:2854–2863.
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/NKG2A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J 1999;18:4250–4260.
Brooks AG, Borrego F, Posch PE, Patamawenu A, Scorzelli CJ, Ulbrecht M, et al.: Specific recognition of HLA-E, but not classical, HLA class I molecules by soluble CD94/NKG2A and NK cells. J Immunol 1999;162:305–313.
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.
Ulbrecht M, Martinozzi S, Gzeschik M, Hengel H, Ellwart JW, Pla M, Weiss EH: Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J Immunol 2000;164:5019–5022.
Trowsdale J: Genetic and functional relationships between MHC and NK receptor genes. Immunity 2001;15:363–374.