Abstract
Prior to the binding of antigenic peptide, a complex of chaperone proteins associates with the Major Histocompatibility Complex (MHC) class I heavy chain/β2m heterodimer. Although each dornain of the MHC class I heavy chain contains amino acid resid uses that influence chaperone binding, there are several pieces of evidence that point to an interaction between the MHC clas 1α2/α3 domains and tapasin. In egard to the site on tapasin involved in the tapasin/MHC interface, we have found that a particular region of tapasin (containing amino acid residues 334–342) is necessary for the binding of tapasin to the MHC class I heavy chain. Our results also indicate that amino acids in this region of tapasin also affect the proportion of MHC class I open forms expressed at the cell surface and MHC class I egress from the endoplasmic reticulurn. Based on these results and those obtained by other laboratories, a model for MHC class I/tapasin interaction is proposed.
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References
Pamer E, Cresswell P: Mechanisms of MHC class I-restricted antigen processing. Annu Rev Immunol 1998;16:323–358.
Ortmann B, Copeman J, Lehner PJ, Sadasivan B, Herberg JA, Grandea AG, Riddell SR, Tampé R, Spies T, Trowsdale J, Cresswell P: Acritical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science 1997;277:1306–1309.
Sadasivan B, Lehner PJ, Ortmann B, Spies T, Cresswell P: Roles for clareticul in and a novel glycoprotein, tapasin, in the interaction of MHC class I mole cules with TAP. Immunity 1996;5:103–114.
Solheim JC, Harris MR, Kindle CS, Hansen TH: Prominence of β2-microglobulin, class I heavy chain conformation, and tapasin in the interactions of class I heavy chain with calreticulin and the transport erassociated with antigen processing. J Immunol 1997:158: 2236–2241.
Ortmann B, Androlewicz MJ, Cresswell P: MHC class I/β2-microglobulin complexes associate with TAP transporters before peptide binding. Nature 1994;368: 864–867.
Suh WK, Cohen-Doyle MF, Fruh K, Wang K, Peterson PA, Williams DB: Interaction of MHC class I molecules with the transporter associated with antigen processing. Science 1994;264:1322–1326.
Carreno BM, Solheim JC, Harris M, Stroynowski I, Connolly JM, Hansen TH: TAP associates with a unique class I conformation, where as calnex in associates with multiple class I forms in mouse and man. J Immunol 1995;155: 4726–4733.
Greenwood R, Shimizu Y, Sehon GS, DeMars R: Novel, allelespecific, post-translational reduction in HLA class I surface expression in a mutant human B cell line. J Immunol 1994;153:5525–5536.
Grandea III AG, Androlewicz MJ, Athwal RS, Geraghty DE, Spies T: Dependence of peptide binding by MHC class I molecules on their interaction with TAP. Science 1995;270:105–108.
Copeman J, Bangia N, Cross JC, Cresswell P: Elucidation of the genetic basis of the antigen presentation defects in the mutant cell line. 220 reveals polymorphism and alternative splicing of the tapasin gene. Eur J Immunol 1998;28:3783–3791.
Peh CA, Burrows SR, Bamden, M, Khanna R, Cresswell, P, Moss D, McCluskey J: HLA-B27 restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I-peptide loading. Immunity 1998;8: 531–542.
Barnden MJ, Purcell AW, Gorman JJ, McCluskey J: Tapasin-mediated retention and optimization of peptide ligands during the assembly of class I molecules. J Immunol 2000;165:322.
Purcell AW, Gorman, JJ, Garcia-Peydro M, Paradela A, Burrows SR, Talbo GH, Laham N, Peh CA, Reynolds EC, Lopez de Castro JA, McCluskey J: Quantitative and qualitative influences of tapasin on the class I peptide repertoire. J Immunol 2001;166:1016–1027.
Purcell AW: The peptide-loading complex and ligand selection during the assembly of HLA class I molecules. Mol Immunol 2000;37: 483–492.
Grandea AG III, Golovina TN, Hamilton SE, Sriram V, Spies T, Brutkiewicz RR, Harty JT, Eisenlohr LC, Van Kaer L: Impaired assembly yet normal trafficking of MHC class I molecules in tapasin mutant mice. Immunity 2000;13: 213–222.
Garbi N, Tan P, Diehl AD, Chambers BJ, Ljunggren HG, Momburg F, Hammerling GJ: Impaired immune responses and altered peptide repertoire in tapasin-deficient mice. Natl Immunol. 2000;1: 234–238.
Lehner PJ, Surman MJ, Cresswell P: Soluble tapasin restores MHC class 1 expression and function in the tapasin-negative cell line. 220. Immunity 1998;8:221–231.
Li S, Paulsson KM, Chen S, Sjögren HO, Wang P: Tapasin is required forefficient peptide binding to transporter associated with antigen processing. J Biol Chem 2000;275:1581–1586.
Tumquist HR, Thomas HJ, Prilliman KR, Lutz CT, Hildebrand WH, Solheim JC: HLA-B polymorphism affects interactions with multiple endoplasmic reticulum proteins. Eur J Immunol 2000;30: 3021–3028.
Turnquist HR, Schenk EL, McIlhaney MM, Hickman HD, Hildebrand WH, Solheim JC: Disparate binding of chaperone proteins by HLA-A subtypes. Immunogenetics, 2002;53:830–834.
Neisig A, Wubbolts R, Zang X, Melief C, Neefjes J: Allele-specific differences in the interaction of MHC class I molecules with transporters associated with antigen processing. J Immunol 1996;156: 3196–3206.
Prilliman KR, Jackson KW, Lindsey, M, Wang J, Crawford D, Hildebrand WH: HLA-B15 peptide ligandsare preferentially anchored at their C termini. J Immunol 1999;162:7277–7284.
Harris MR, Yu YYL, Kindle CS, Hansen TH, Solheim JC: Calreticulin and calnexin interact with different protein and glycan determinants during the assembly of MHC class J. J Immunol 1998;160: 5404–5409.
YU YYL, Tumquist HR, Myers NB, Balendiran GK, Hansen TH, Solheim JC: An extensive region of an MHC class I α2 domain loop influences interaction with the assembly complex. J Immunol 1999;163: 4427–4433.
Peace-Brewer AL, Tussey LG, Matsui M, Li G, Quinn DG, Frelinger JA: A point mutation in HLA-A*0201 results in failure to bind the TAP complex and to present virus-derived peptides to CTL. Immunity 1996;4:505–514.
Lewis JW, Neisig A, Neefjes J, Elliott T: Point mutations in the α2 domain of HLA-A2. 1 define a functionally relevant interaction with TAP. Curr Biol 1996;6:873–883.
Kulig K, Nandi D, Bacík I, Monaco JJ, Vukmanovic S: Physical and functional association of the major histocompatibility complex class I heavy chain α3 domain with the transporter associated with antigen processing. J Exp Med 1998;187: 865–874.
Suh W-K, Mitchell EK, Yang Y, Peterson PA, Waneck GL, Williams DB: MHC class I molecules form ternary complexes with calnexin and TAP and undergo peptide-regulated interaction with TAP via their extracellular domains. J Exp Med 1996;184: 337–348.
Suh WK, Derby MA, Cohen-Doyle MF, Schoenhals GJ, Früh K, Berzofsky JA, Williams DB: Interaction of murine MHC class I molecules with tapasin and TAP enhances peptide loading and involves the heavy chain α3 domain. J Immunol 1999;162: 1530–1540.
Turnquist HR, Vargas SE, McIlhaney MM, Li S, Wang P, Solheim JC: Calreticulin binds to the α1 domain of MHC class 1 independently of tapasin. Tissue Antigens, in press.
Harris MR, Lybarger L, Myers NB, Hilbert C, Solheim JC, Hansen TH, Yu: Interactions of HLA-B27 with the peptide loading complex as revealed by heavy chain mutations. Int Immunol 2001;13: 1275–1282.
Saper MA, Bjorkman PJ, Wiley DC: Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 Å resolution. J Mol Biol 1991;219:277–319.
Balendiran GK,* Solheim JC,* Young ACM,* Hansen TH, Nathenson SG, Sacchettini JC (*equal contributors): The three-dimensional structure of an H-2Ld-peptide complex explains the unique interaction of Ld with beta-2 microglobulin and peptide. Proc Natl Acad Sci USA 1997;94: 6880–6885.
Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC: The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 1987;329: 512–518.
Watts S, Wheeler C, Morse R, and Goodenow RS. 1989. Amino acid comparison of the class 1 antigens of mouse major histocompatibility complex. Immunogenetics 1989;30:90–92.
Turnquist HR, Vargas SE, Solheim JC: Loss of a glycine in the α2 domain affects MHC peptide binding but not chaperone binding. Biochem Biophys Res Commun 2001;289:825–831.
Turnquist HR, Solheim JC: Analysis of MHC class 1 interactions with endoplasmic reticulum proteins. Methods Mol Biol 2001;156: 165–173.
Turnquist, H. R., S. E. Vargas, M. M. McIlhaney, S. D. Sanderson, S. Li, P. Wang, B. Gubler, P. van Endert, and J. C. Solheim: A region of tapasin that affects Ld binding and assembly. J Immunol 2001; 167:4443–4449.
Myers NB, Harris MR, Connolly JM, Lybarger L, Yu YYL, Hansen TH: Kb, Kd, and Ld molecules share common tapasin dependencies as determined using a novel epitopetag. J Immunol 2000; 165:5656–5663.
Lie W-R, Myers NB, Gorka J, Rubocki RJ, Connolly JM, Hansen TH: Peptide ligand-induced conformation and surface expression of the Ld class I MHC molecule. Nature 1990;344:439–441.
Smith JD, Lie WR, Gorka J, Kindle CS, Myers NB, Hansen TH: Disparate interaction of peptide ligand with nascent versus mature class I major histocompatibility complex molecules: comparisons of peptide binding to alternative forms of Ld in cell lysates and at the cell surface. J Exp Med 1992;175: 191–202.
Lie WR, Myers NB, Connolly IM, Gorka J, Lee DR, Hansen TH: The specific binding of peptide ligand to Ld class I major histocompatibility complex molecules determines their antigenic structure. J Exp Med 1991;173:449–459.
Smith JD, Myers NB, Gorka J, Hansen TH: Model for the in vivo assembly of nascent Ld class I molecules and for the expression of unfolded Ld molecules at the cell surface. J Exp Med 1993;178: 2035–2046.
Smith JD, Solheim JC, Carreno BM, Hansen TH: Characterization of class I MHC folding intermediates and their disparate interactions with peptide and β2-microglobulin. Mol Immunol 1995;32:531–540.
Bangia N, Lehner PJ, Hughes EA, Surman M, Cresswell P: The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur J Immunol 1999;29:1858–1870.
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Turnquist, H.R., Vargas, S.E., Schenk, E.L. et al. The interface between tapasin and MHC class I. Immunol Res 25, 261–269 (2002). https://doi.org/10.1385/IR:25:3:261
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DOI: https://doi.org/10.1385/IR:25:3:261