Tapasin and other chaperones: models of the MHC class I loading complex (original) (raw)

Abstract

MHC (major histocompatibility complex) class I molecules bind intracellular virus-derived peptides in the endoplasmic reticulum (ER) and present them at the cell surface to cytotoxic T lymphocytes. Peptide-free class I molecules at the cell surface, however, could lead to aberrant T cell killing. Therefore, cells ensure that class I molecules bind high-affinity ligand peptides in the ER, and restrict the export of empty class I molecules to the Golgi apparatus. For both of these safeguard mechanisms, the MHC class I loading complex (which consists of the peptide transporter TAP, the chaperones tapasin and calreticulin, and the protein disulfide isomerase ERp57) plays a central role. This article reviews the actions of accessory proteins in the biogenesis of class I molecules, specifically the functions of the loading complex in high-affinity peptide binding and localization of class I molecules, and the known connections between these two regulatory mechanisms. It introduces new models for the mode of action of tapasin, the role of the class I loading complex in peptide editing, and the intracellular localization of class I molecules.

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References

Androlewicz, M., Anderson, K., and Cresswell, P. (1993). Evidence that transporters associated with antigen processing translocate a major histocompatibility complex class I-binding peptide into the endoplasmic reticulum in an ATP-dependent manner. Proc. Natl. Acad. Sci. USA90, 9130–9134.10.1073/pnas.90.19.9130Search in Google Scholar

Baas, E. J., van Santen, H. M., Kleijmeer, M. J., Geuze, H. J., Peters, P. J., and Ploegh, H. L. (1992). Peptide-induced stabilization and intracellular localization of empty HLA class I complexes. J. Exp. Med.176, 147–156.10.1084/jem.176.1.147Search in Google Scholar

Balow, J. P., Weissman, J. D., and Kearse, K. P. (1995). Unique expression of major histocompatibility complex class I proteins in the absence of glucose trimming and calnexin association. J. Biol. Chem.270, 29025–29029.10.1074/jbc.270.48.29025Search in Google Scholar

Bangia, N., Lehner, P. J., Hughes, E. A., Surman, M., and Cresswell, P. (1999). The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur. J. Immunol.29, 1858–1870.10.1002/(SICI)1521-4141(199906)29:06<1858::AID-IMMU1858>3.0.CO;2-CSearch in Google Scholar

Barnden, M. J., Purcell, A. W., Gorman, J. J., and McCluskey, J. (2000). Tapasin-mediated retention and optimization of peptide ligands during the assembly of class I molecules. J. Immunol.165, 322–330.10.4049/jimmunol.165.1.322Search in Google Scholar

Beissbarth, T., Sun, J., Kavathas, P. B., and Ortmann, B. (2000). Increased efficiency of folding and peptide loading of mutant MHC class I molecules. Eur. J. Immunol.30, 1203–1213.10.1002/(SICI)1521-4141(200004)30:4<1203::AID-IMMU1203>3.0.CO;2-LSearch in Google Scholar

Bouvier, M., Guo, H. C., Smith, K. J., and Wiley, D. C. (1998). Crystal structures of HLA-A*0201 complexed with antigenic peptides with either the amino- or carboxyl-terminal group substituted by a methyl group. Proteins33, 97–106.10.1002/(SICI)1097-0134(19981001)33:1<97::AID-PROT9>3.0.CO;2-ISearch in Google Scholar

Bouvier, M., and Wiley, D. C. (1994). Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules. Science265, 398–402.10.1126/science.8023162Search in Google Scholar

Bresnahan, P. A., Barber, L. D., and Brodsky, F. M. (1997). Localization of class I histocompatibility molecule assembly by subfractionation of the early secretory pathway. Hum. Immunol.53, 129–139.10.1016/S0198-8859(97)00001-3Search in Google Scholar

Brocke, P., Garbi, N., Momburg, F., and Hammerling, G. J. (2002). HLA-DM, HLA-DO and tapasin: functional similarities and differences. Curr. Opin. Immunol.14, 22–29.10.1016/S0952-7915(01)00294-1Search in Google Scholar

Busch, D. H., and Pamer, E. G. (1998). MHC class I/peptide stability: implications for immunodominance, in vitro proliferation, and diversity of responding CTL. J. Immunol.160, 4441–4448.10.4049/jimmunol.160.9.4441Search in Google Scholar

Cerundolo, V., Elliott, T., Elvin, J., Bastin, J., Rammensee, H.-G., and Townsend, A. (1991). The binding affinity and dissociation rates of peptides for class I histocompatibility complex molecules. Eur. J. Immunol.21, 2069–2075.10.1002/eji.1830210915Search in Google Scholar

Chen, M., Stafford, W. F., Diedrich, G., Khan, A., and Bouvier, M. (2002). A characterization of the lumenal region of human tapasin reveals the presence of two structural domains. Biochemistry41, 14539–14545.10.1021/bi020521uSearch in Google Scholar

Chen, Y., Sidney, J., Southwood, S., Cox, A. L., Sakaguchi, K., Henderson, R. A., Apella, E., Hunt, D. F., Sette, A., and Engelhard, V. H. (1994). Naturally processed peptides longer than nine amino acid residues bind to the class I MHC molecule HLA-A2.1 with high affinity and with different conformations. J. Immunol.152, 2874–2881.Search in Google Scholar

Chen, Z. W., Craiu, A., Shen, L., Kuroda, M. J., Iroku, U. C., Watkins, D. I., Voss, G., and Letvin, N. L. (2000). Simian immunodeficiency virus evades a dominant epitope-specific cytotoxic T lymphocyte response through a mutation resulting in the accelerated dissociation of viral peptide and MHC class I. J. Immunol.164, 6474–6479.10.4049/jimmunol.164.12.6474Search in Google Scholar

Collins, E. J., Garboczi, D. N., and Wiley, D. C. (1994). Three-dimensional structure of a peptide extending from one end of a class I MHC binding site. Nature371, 626–629.10.1038/371626a0Search in Google Scholar

Cresswell, P. (2000). Intracellular surveillance: controlling the assembly of MHC class I-peptide complexes. Traffic1, 301–305.10.1034/j.1600-0854.2000.010402.xSearch in Google Scholar

Croze, E. M., and Morre, D. J. (1981). Flow kinetics of mouse histocompatibility antigens. Proc. Natl. Acad. Sci. USA78, 1547–1551.10.1073/pnas.78.3.1547Search in Google Scholar

Dam, J., Guan, R., Natarajan, K., Dimasi, N., Chlewicki, L. K., Kranz, D. M., Schuck, P., Margulies, D. H., Mariuzza, R. A., Wang, J., and Tormo, J. (2003). Variable MHC class I engagement by Ly49 natural killer cell receptors demonstrated by the crystal structure of Ly49C bound to H-2K(b). Nat. Immunol.4, 1213–1222.10.1038/ni1006Search in Google Scholar

Danilczyk, U. G., Cohen-Doyle, M. F., and Williams, D. B. (2000). Functional relationship between calreticulin, calnexin, and the endoplasmic reticulum luminal domain of calnexin. J. Biol. Chem.275, 13089–13097.10.1074/jbc.275.17.13089Search in Google Scholar

Danilczyk, U. G., and Williams, D. B. (2001). The lectin chaperone calnexin utilizes polypeptide-based interactions to associate with many of its substrates in vivo. J. Biol. Chem.276, 25532–25540.10.1074/jbc.M100270200Search in Google Scholar

Dick, T. P., and Cresswell, P. (2002). Thiol oxidation and reduction in major histocompatibility complex class I-restricted antigen processing and presentation. Methods Enzymol.348, 49–54.10.1016/S0076-6879(02)48625-9Search in Google Scholar

Dick, T. P., Bangia, N., Peaper, D. R., and Cresswell, P. (2002). Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity16, 87–98.10.1016/S1074-7613(02)00263-7Search in Google Scholar

Diedrich, G., Bangia, N., Pan, M., and Cresswell, P. (2001). A role for calnexin in the assembly of the MHC class I loading complex in the endoplasmic reticulum. J. Immunol.166, 1703–1709.10.4049/jimmunol.166.3.1703Search in Google Scholar

Ellgaard, L., and Helenius, A. (2001). ER quality control: towards an understanding at the molecular level. Curr. Opin. Cell Biol.13, 431–437.10.1016/S0955-0674(00)00233-7Search in Google Scholar

Ellgaard, L., and Helenius, A. (2003). Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol.4, 181–191.10.1038/nrm1052Search in Google Scholar

Elliott, T. (1997). How does TAP associate with MHC class I molecules? Immunol. Today18, 375–379.Search in Google Scholar

Elliott, T., Cerundolo, V., Elvin, J., and Townsend, A. (1991). Peptide-induced conformational change of the class I heavy chain. Nature351, 402–406.10.1038/351402a0Search in Google Scholar

Fahnestock, M. L., Johnson, J. L., Feldman, R. M., Tsomides, T. J., Mayer, J., Narhi, L. O., and Bjorkman, P. J. (1994). Effects of peptide length and composition on binding to an empty class I MHC heterodimer. Biochemistry33, 8149–8158.10.1021/bi00192a020Search in Google Scholar

Farmery, M. R., Allen, S., Allen, A. J., and Bulleid, N. J. (2000). The role of ERp57 in disulfide bond formation during the assembly of major histocompatibility complex class I in a synchronized semipermeabilized cell translation system. J. Biol. Chem.275, 14933–14938.10.1074/jbc.275.20.14933Search in Google Scholar

Frickel, E. M., Riek, R., Jelesarov, I., Helenius, A., Wuthrich, K., and Ellgaard, L. (2002). TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc. Natl. Acad. Sci. USA99, 1954–1959.10.1073/pnas.042699099Search in Google Scholar

Gao, B., Adhikari, R., Howarth, M., Nakamura, K., Gold, M. C., Hill, A. B., Knee, R., Michalak, M., and Elliott, T. (2002). Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity16, 99–109.10.1016/S1074-7613(01)00260-6Search in Google Scholar

Gao, B., Williams, A., Sewell, A., and Elliott, T. (2004). Generation of a functional, soluble tapasin protein from an alternatively spliced mRNA. Genes Immun.5, 101–108.10.1038/sj.gene.6364043Search in Google Scholar PubMed

Gao, G. F., Tormo, J., Gerth, U. C., Wyer, J. R., McMichael, A. J., Stuart, D. I., Bell, J. I., Jones, E. Y., and Jakobsen, B. K. (1997). Crystal structure of the complex between human CD8(a) and HLA-A2. Nature387, 630–634.10.1038/42523Search in Google Scholar PubMed

Garbi, N., Tiwari, N., Momburg, F., and Hammerling, G. J. (2003). A major role for tapasin as a stabilizer of the TAP peptide transporter and consequences for MHC class I expression. Eur. J. Immunol.33, 264–273.10.1002/immu.200390029Search in Google Scholar PubMed

Grandea 3rd, A. G., and Van Kaer, L. (2001). Tapasin: an ER chaperone that controls MHC class I assembly with peptide. Trends Immunol.22, 194–199.Search in Google Scholar

Grandea 3rd, A. G., Androlewicz, M. J., Athwal, R. S., Geraghty, D. E., and Spies, T. (1995). Dependence of peptide binding by MHC class I molecules on their interaction with TAP. Science270, 105–108.Search in Google Scholar

Grandea 3rd, A. G., Lehner, P. J., Cresswell, P., and Spies, T. (1997). Regulation of MHC class I heterodimer stability and interaction with TAP by tapasin. Immunogenetics46, 477–483.Search in Google Scholar

Grandea 3rd, A. G., Golovina, T. N., Hamilton, S. E., Sriram, V., Spies, T., Brutkiewicz, R. R., Harty, J. T., Eisenlohr, L. C., and Van Kaer, L. (2000). Impaired assembly yet normal trafficking of MHC class I molecules in Tapasin mutant mice. Immunity13, 213–222.Search in Google Scholar

Hammond, C., Braakman, I., and Helenius, A. (1994). Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc. Natl. Acad. Sci. USA91, 913–917.10.1073/pnas.91.3.913Search in Google Scholar PubMed PubMed Central

Hammond, C., and Helenius, A. (1994a). Folding of VSV G protein: sequential interaction with BiP and calnexin. Science266, 456–458.10.1126/science.7939687Search in Google Scholar PubMed

Hammond, C., and Helenius, A. (1994b). Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol.126, 41–52.10.1083/jcb.126.1.41Search in Google Scholar PubMed PubMed Central

Harris, M. R., Lybarger, L., Myers, N. B., Hilbert, C., Solheim, J. C., Hansen, T. H., and Yu, Y. Y. (2001a). Interactions of HLA-B27 with the peptide loading complex as revealed by heavy chain mutations. Int. Immunol.13, 1275–1282.10.1093/intimm/13.10.1275Search in Google Scholar PubMed

Harris, M. R., Lybarger, L., Yu, Y. Y., Myers, N. B., and Hansen, T. H. (2001b). Association of ERp57 with mouse MHC class I molecules is tapasin dependent and mimics that of calreticulin and not calnexin. J. Immunol.166, 6686–6692.10.4049/jimmunol.166.11.6686Search in Google Scholar PubMed

Hayes, B. K., Esquivel, F., Bennink, J. R., Yewdell, J. W., and Varki, A. (1995). Structure of the N-linked oligosaccharides of MHC class I molecules from cells deficient in the antigenic peptide transporter. Implications for the site of peptide association. J. Immunol.155, 3780–3787.Search in Google Scholar

Hebert, A. M., Strohmaier, J., Whitman, M. C., Chen, T., Gubina, E., Hill, D. M., Lewis, M. S., and Kozlowski, S. (2001). Kinetics and thermodynamics of beta 2-microglobulin binding to the α3 domain of major histocompatibility complex class I heavy chain. Biochemistry40, 5233–5242.10.1021/bi002392sSearch in Google Scholar PubMed

Hill, A., Takiguchi, M., and Mc Michael, A. (1993). Different rates of HLA class I molecule assembly which are determined by amino acid sequence in the α2 domain. Immunogenetics37, 95–101.Search in Google Scholar

Hillig, R. C., Coulie, P. G., Stroobant, V., Saenger, W., Ziegler, A., and Hulsmeyer, M. (2001). High-resolution structure of HLA-A*0201 in complex with a tumour-specific antigenic peptide encoded by the MAGE-A4 gene. J. Mol. Biol.310, 1167–1176.10.1006/jmbi.2001.4816Search in Google Scholar PubMed

Horig, H., Young, A. C., Papadopoulos, N. J., DiLorenzo, T. P., and Nathenson, S. G. (1999). Binding of longer peptides to the H-2Kb heterodimer is restricted to peptides extended at their C terminus: refinement of the inherent MHC class I peptide binding criteria. J. Immunol.163, 4434–4441.10.4049/jimmunol.163.8.4434Search in Google Scholar

Hsu, V. W., Yuan, L. C., Nuchtern, J. G., Lippincott, S. J., Hämmerling, G. J., and Klausner, R. D. (1991). A recycling pathway between the endoplasmic reticulum and the Golgi apparatus for retention of unassembled MHC class I molecules. Nature352, 441–444.10.1038/352441a0Search in Google Scholar PubMed

Hughes, E. A., and Cresswell, P. (1998). The thiol oxidoreductase ERp57 is a component of the MHC class I peptide-loading complex. Curr. Biol.8, 709–712.10.1016/S0960-9822(98)70278-7Search in Google Scholar

Jackson, M. R., Cohen-Doyle, M. F., Peterson, P. A., and Williams, D. B. (1994). Regulation of MHC class I transport by the molecular chaperone, calnexin (p88, IP90). Science263, 384–387.10.1126/science.8278813Search in Google Scholar PubMed

Jones, E. Y., Tormo, J., Reid, S. W., and Stuart, D. I. (1998). Recognition surfaces of MHC class I. Immunol. Rev.163, 121–128.10.1111/j.1600-065X.1998.tb01191.xSearch in Google Scholar PubMed

Khan, A. R., Baker, B. M., Ghosh, P., Biddison, W. E., and Wiley, D. C. (2000). The structure and stability of an HLA-A*0201/octameric tax peptide complex with an empty conserved peptide-N-terminal binding site. J. Immunol.164, 6398–6405.10.4049/jimmunol.164.12.6398Search in Google Scholar PubMed

Kleijmeer, M., Kelly, A., Geuze, H., Slot, J., Townsend, A., and Trowsdale, J. (1992). Location of MHC-encoded transporters in the endoplasmic reticulum and _cis_-Golgi. Nature357, 342–344.10.1038/357342a0Search in Google Scholar PubMed

Kulig, K., Nandi, D., Bacik, I., Monaco, J. J., and Vukmanovic, S. (1998). 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.187, 865–874.10.1084/jem.187.6.865Search in Google Scholar PubMed PubMed Central

Latron, F., Pazmany, L., Morrison, J., Moots, R., Saper, M. A., McMichael, A., and Strominger, J. L. (1992). A critical role for conserved residues in the cleft of HLA-A2 in presentation of a nonapeptide to T cells. Science257, 964–967.10.1126/science.1380181Search in Google Scholar PubMed

Leach, M. R., Cohen-Doyle, M. F., Thomas, D. Y., and Williams, D. B. (2002). Localization of the lectin, ERp57 binding, and polypeptide binding sites of calnexin and calreticulin. J. Biol. Chem.277, 29686–29697.10.1074/jbc.M202405200Search in Google Scholar PubMed

Leach, M. R., and Williams, D. B. (2004). Lectin-deficient calnexin is capable of binding class I histocompatibility molecules in vivo and preventing their degradation. J. Biol. Chem.279, 9072–9079.10.1074/jbc.M310788200Search in Google Scholar PubMed

Lee, N., and Geraghty, D. E. (2003). HLA-F surface expression on B cell and monocyte cell lines is partially independent from tapasin and completely independent from TAP. J. Immunol.171, 5264–5271.10.4049/jimmunol.171.10.5264Search in Google Scholar PubMed

Lehner, P. J., Surman, M. J., and Cresswell, P. (1998). Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line.220. Immunity8, 221–231.10.1016/S1074-7613(00)80474-4Search in Google Scholar

Lewis, J. W., and Elliott, T. (1998). Evidence for successive peptide binding and quality control stages during MHC class I assembly. Curr. Biol.8, 717–720.10.1016/S0960-9822(98)70280-5Search in Google Scholar

Lewis, J. W., Neisig, A., Neefjes, J., and Elliott, T. (1996). Point mutations in the α2 domain of HLA-A2.1 define a functionally relevant interaction with TAP. Curr. Biol.6, 873–883.Search in Google Scholar

Lewis, J. W., Sewell, A., Price, D., and Elliott, T. (1998). HLA-A*0201 presents TAP-dependent peptide epitopes to cytotoxic T lymphocytes in the absence of tapasin. Eur. J. Immunol.28, 3214–3220.10.1002/(SICI)1521-4141(199810)28:10<3214::AID-IMMU3214>3.0.CO;2-CSearch in Google Scholar

Lindahl, K. F., Byers, D. E., Dabhi, V. M., Hovik, R., Jones, E. P., Smith, G. P., Wang, C. R., Xiao, H., and Yoshino, M. (1997). H2-M3, a full-service class Ib histocompatibility antigen. Annu. Rev. Immunol.15, 851–879.10.1146/annurev.immunol.15.1.851Search in Google Scholar

Lindquist, J. A., Hammerling, G. J., and Trowsdale, J. (2001). ER60/ERp57 forms disulfide-bonded intermediates with MHC class I heavy chain. FASEB J.15, 1448–1450.10.1096/fj.00-0720fjeSearch in Google Scholar

Machold, R. P., Andree, S., Van Kaer, L., Ljunggren, H. G., and Ploegh, H. L. (1995). Peptide influences the folding and intracellular transport of free major histocompatibility complex class I heavy chains. J. Exp. Med.181, 1111–1122.10.1084/jem.181.3.1111Search in Google Scholar

Madden, D. R. (1995). The three-dimensional structure of peptide-MHC complexes. Annu. Rev. Immunol.13, 587–622.10.1146/annurev.iy.13.040195.003103Search in Google Scholar

Madden, D. R., Gorga, J. C., Strominger, J. L., and Wiley, D. C. (1992). The three-dimensional structure of HLA-B27 at 2.1 Å resolution suggests a general mechanism for tight peptide binding to MHC. Cell70, 1035–1048.Search in Google Scholar

Mancino, L., Rizvi, S. M., Lapinski, P. E., and Raghavan, M. (2002). Calreticulin recognizes misfolded HLA-A2 heavy chains. Proc. Natl. Acad. Sci. USA99, 5931–5936.10.1073/pnas.092031799Search in Google Scholar

Marguet, D., Spiliotis, E. T., Pentcheva, T., Lebowitz, M., Schneck, J., and Edidin, M. (1999). Lateral diffusion of GFP-tagged H2Ld molecules and of GFP-TAP1 reports on the assembly and retention of these molecules in the endoplasmic reticulum. Immunity11, 231–240.10.1016/S1074-7613(00)80098-9Search in Google Scholar

Matlack, K. E., Mothes, W., and Rapoport, T. A. (1998). Protein translocation: tunnel vision. Cell92, 381–390.10.1016/S0092-8674(00)80930-7Search in Google Scholar

Matsumura, M., Fremont, D. H., Peterson, P. A., and Wilson, I. A. (1992). Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science257, 927–934.10.1126/science.1323878Search in Google Scholar

Mayer, W. E., and Klein, J. (2001). Is tapasin a modified MHC class I molecule? Immunogenetics53, 719–723.10.1007/s00251-001-0403-ySearch in Google Scholar

Meyer, T. H., van Endert, P. M., Uebel, S., Ehring, B., and Tampé , R. (1994). Functional expression and purification of the ABC transporter complex associated with antigen processing (TAP) in insect cells. FEBS Lett.351, 443–447.10.1016/0014-5793(94)00908-2Search in Google Scholar

Molinari, M., and Helenius, A. (1999). Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature402, 90–93.10.1038/47062Search in Google Scholar

Molinari, M., and Helenius, A. (2000). Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science288, 331–333.10.1126/science.288.5464.331Search in Google Scholar

Molinari, M., Eriksson, K. K., Calanca, V., Galli, C., Cresswell, P., Michalak, M., and Helenius, A. (2004). Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol. Cell13, 125–135.10.1016/S1097-2765(03)00494-5Search in Google Scholar

Momburg, F., and Tan, P. (2002). Tapasin-the keystone of the loading complex optimizing peptide binding by MHC class I molecules in the endoplasmic reticulum. Mol. Immunol.39, 217–233.10.1016/S0161-5890(02)00103-7Search in Google Scholar

Mossessova, E., Bickford, L. C., and Goldberg, J. (2003). SNARE selectivity of the COPII coat. Cell114, 483–495.10.1016/S0092-8674(03)00608-1Search in Google Scholar

Myers, N. B., Harris, M. R., Connolly, J. M., Lybarger, L., Yu, Y. Y., and Hansen, T. H. (2000). Kb, Kd, and Ld molecules share common tapasin dependencies as determined using a novel epitope tag. J. Immunol.165, 5656–5663.10.4049/jimmunol.165.10.5656Search in Google Scholar

Natarajan, K., Dimasi, N., Wang, J., Margulies, D. H., Mariuzza, R. A., and Tormo, J. (2002). MHC class I recognition by Ly49 natural killer cell receptors-Crystal structure of a lectin-like natural killer cell receptor bound to its MHC class I ligand. Mol. Immunol.38, 1023–1027.10.1016/S0161-5890(02)00031-7Search in Google Scholar

Neefjes, J., Momburg, F., and Hämmerling, G. (1993). Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science261, 769–771.10.1126/science.8342042Search in Google Scholar

Neisig, A., Wubbolts, R., Zang, X., Melief, C., and Neefjes, J. (1996). Allele-specific differences in the interaction of MHC class I molecules with transporters associated with antigen processing. J. Immunol.156, 3196–3206.10.4049/jimmunol.156.9.3196Search in Google Scholar

Nossner, E., and Parham, P. (1995). Species-specific differences in chaperone interaction of human and mouse major histocompatibility complex class I molecules. J. Exp. Med.181, 327–337.10.1084/jem.181.1.327Search in Google Scholar

Oliver, J. D., Roderick, H. L., Llewellyn, D. H., and High, S. (1999). ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol. Biol. Cell10, 2573–2582.10.1091/mbc.10.8.2573Search in Google Scholar

Ortmann, B., Androlewicz, M. J., and Cresswell, P. (1994). MHC class I/β2-microglobulin complexes associate with TAP transporters before peptide binding. Nature368, 864–867.10.1038/368864a0Search in Google Scholar

Ortmann, B., Copeman, J., Lehner, P. J., Sadasivan, B., Herberg, J. A., Grandea, A. G., Riddell, S. R., Tampe, R., Spies, T., Trowsdale, J., and Cresswell, P. (1997). A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science277, 1306–1309.10.1126/science.277.5330.1306Search in Google Scholar

Paquet, M. E., and Williams, D. B. (2002). Mutant MHC class I molecules define interactions between components of the peptide-loading complex. Int. Immunol.14, 347–358.10.1093/intimm/14.4.347Search in Google Scholar

Park, B., and Ahn, K. (2003). An essential function of Tapasin in quality control of HLA-G molecules. J. Biol. Chem.278, 14337–14345.10.1074/jbc.M212882200Search in Google Scholar

Park, B., Kim, Y., Shin, J., Lee, S., Cho, K., Fruh, K., and Ahn, K. (2004). Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity20, 71–85.10.1016/S1074-7613(03)00355-8Search in Google Scholar

Park, B., Lee, S., Kim, E., and Ahn, K. (2003). A single polymorphic residue within the peptide-binding cleft of MHC class I molecules determines spectrum of tapasin dependence. J. Immunol.170, 961–968.10.4049/jimmunol.170.2.961Search in Google Scholar PubMed

Parodi, A. J. (2000). Protein glucosylation and its role in protein folding. Annu. Rev. Biochem.69, 69–93.10.1146/annurev.biochem.69.1.69Search in Google Scholar PubMed

Patil, A. R., Thomas, C. J., and Surolia, A. (2000). Kinetics and the mechanism of interaction of the endoplasmic reticulum chaperone, calreticulin, with monoglucosylated (Glc1Man9GlcNAc2) substrate. J. Biol. Chem.275, 24348–24356.10.1074/jbc.M003102200Search in Google Scholar

Paulsson, K. M., Anderson, P. O., Chen, S., Sjogren, H. O., Ljunggren, H. G., Wang, P., and Li, S. (2001a). Assembly of tapasin-associated MHC class I in the absence of the transporter associated with antigen processing (TAP). Int. Immunol.13, 23–29.10.1093/intimm/13.1.23Search in Google Scholar

Paulsson, K. M., Wang, P., Anderson, P. O., Chen, S., Pettersson, R. F., and Li, S. (2001b). Distinct differences in association of MHC class I with endoplasmic reticulum proteins in wild-type, and β2-microglobulin- and TAP-deficient cell lines. Int. Immunol.13, 1063–1073.10.1093/intimm/13.8.1063Search in Google Scholar

Paulsson, K. M., Kleijmeer, M. J., Griffith, J., Jevon, M., Chen, S., Anderson, P. O., Sjogren, H. O., Li, S., and Wang, P. (2002). Association of tapasin and COPI provides a mechanism for the retrograde transport of major histocompatibility complex (MHC) class I molecules from the Golgi complex to the endoplasmic reticulum. J. Biol. Chem.277, 18266–18271.10.1074/jbc.M201388200Search in Google Scholar

Peace-Brewer, A. L., Tussey, L. G., Matsui, M., Li, G., Quinn, D. G., and Frelinger, J. A. (1996). A point mutation in HLAA*0201 results in failure to bind the TAP complex and to present virus-derived peptides to CTL. Immunity4, 505–514.10.1016/S1074-7613(00)80416-1Search in Google Scholar

Peh, C. A., Burrows, S. R., Barnden, M., Khanna, R., Cresswell, P., Moss, D. J., and McCluskey, J. (1998). HLA-B27-restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I peptide loading. Immunity8, 531–542.10.1016/S1074-7613(00)80558-0Search in Google Scholar

Petrone, P. M., and Garcia, A. E. (2004). MHC-peptide binding is assisted by bound water molecules. J. Mol. Biol.338, 419–435.10.1016/j.jmb.2004.02.039Search in Google Scholar PubMed

Prilliman, K. R., Jackson, K. W., Lindsey, M., Wang, J., Crawford, D., and Hildebrand, W. H. (1999). HLA-B15 peptide ligands are preferentially anchored at their C termini. J. Immunol.162, 7277–7284.10.4049/jimmunol.162.12.7277Search in Google Scholar

Purcell, A. W., Gorman, J. J., Garcia-Peydro, M., Paradela, A., Burrows, S. R., Talbo, G. H., Laham, N., Peh, C. A., Reynolds, E. C., Lopez De Castro, J. A., and McCluskey, J. (2001). Quantitative and qualitative influences of tapasin on the class I peptide repertoire. J. Immunol.166, 1016–1027.10.4049/jimmunol.166.2.1016Search in Google Scholar PubMed

Radcliffe, C. M., Diedrich, G., Harvey, D. J., Dwek, R. A., Cresswell, P., and Rudd, P. M. (2002). Identification of specific glycoforms of major histocompatibility complex class I heavy chains suggests that class I peptide loading is an adaptation of the quality control pathway involving calreticulin and ERp57. J. Biol. Chem.277, 46415–46423.10.1074/jbc.M202466200Search in Google Scholar PubMed

Raghuraman, G., Lapinski, P. E., and Raghavan, M. (2002). Tapasin interacts with the membrane-spanning domains of both TAP subunits and enhances the structural stability of TAP1 × TAP2 Complexes. J. Biol. Chem.277, 41786–41794.10.1074/jbc.M207128200Search in Google Scholar PubMed

Raposo, G., van Santen, H. M., Leijendekker, R., Geuze, H. J., and Ploegh, H. L. (1995). Misfolded major histocompatibility complex class I molecules accumulate in an expanded ER-Golgi intermediate compartment. J. Cell Biol.131, 1403–1419.10.1083/jcb.131.6.1403Search in Google Scholar

Reits, E. A., Vos, J. C., Gromme, M., and Neefjes, J. (2000). The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature404, 774–778.10.1038/35008103Search in Google Scholar

Rock, K. L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D., and Goldberg, A. L. (1994). Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell78, 761–771.10.1016/S0092-8674(94)90462-6Search in Google Scholar

Rock, K. L., York, I. A., and Goldberg, A. L. (2004). Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nat. Immunol.5, 670–677.10.1038/ni1089Search in Google Scholar

Russ, G., Esquivel, F., Yewdell, J. W., Cresswell, P., Spies, T., and Bennink, J. R. (1995). Assembly, intracellular localization, and nucleotide binding properties of the human peptide transporters TAP1 and TAP2 expressed by recombinant vaccinia viruses. J. Biol. Chem.270, 21312–21318.10.1074/jbc.270.36.21312Search in Google Scholar

Sadasivan, B., Lehner, P. J., Ortmann, B., Spies, T., and Cresswell, P. (1996). Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity5, 103–114.10.1016/S1074-7613(00)80487-2Search in Google Scholar

Sadasivan, B. K., Cariappa, A., Waneck, G. L., and Cresswell, P. (1995). Assembly, peptide loading, and transport of MHC class I molecules in a calnexin-negative cell line. Cold Spring Harb. Symp. Quant. Biol.60, 267–275.10.1101/SQB.1995.060.01.031Search in Google Scholar PubMed

Saric, T., Chang, S. C., Hattori, A., York, I. A., Markant, S., Rock, K. L., Tsujimoto, M., and Goldberg, A. L. (2002). An IFN-γ-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat. Immunol.3, 1169–1176.10.1038/ni859Search in Google Scholar PubMed

Schoenhals, G. J., Krishna, R. M., Grandea, A. G., 3rd, Spies, T., Peterson, P. A., Yang, Y., and Fruh, K. (1999). Retention of empty MHC class I molecules by tapasin is essential to reconstitute antigen presentation in invertebrate cells. EMBO J.18, 743–753.10.1093/emboj/18.3.743Search in Google Scholar PubMed PubMed Central

Serwold, T., Gonzalez, F., Kim, J., Jacob, R., and Shastri, N. (2002). ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature419, 480–483.10.1038/nature01074Search in Google Scholar PubMed

Sette, A., Vitiello, A., Reherman, B., Fowler, P., Nayersina, R., Kast, W. M., Melief, C. J., Oseroff, C., Yuan, L., Ruppert, J., and et al. (1994). The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J. Immunol.153, 5586–5592.10.4049/jimmunol.153.12.5586Search in Google Scholar

Sijts, A. J., and Pamer, E. G. (1997). Enhanced intracellular dissociation of major histocompatibility complex class I-associated peptides: a mechanism for optimizing the spectrum of cell surface-presented cytotoxic T lymphocyte epitopes. J. Exp. Med.185, 1403–1411.10.1084/jem.185.8.1403Search in Google Scholar

Smith, J. D., Solheim, J. C., Carreno, B. M., and Hansen, T. H. (1995). Characterization of class I MHC folding intermediates and their disparate interactions with peptide and β2-microglobulin. Mol. Immunol.32, 531–540.10.1016/0161-5890(95)00013-5Search in Google Scholar

Snyder, H. L., Yewdell, J. W., and Bennink, J. R. (1994). Trimming of antigenic peptides in an early secretory compartment. J. Exp. Med.180, 2389–2394.10.1084/jem.180.6.2389Search in Google Scholar

Spies, T., Cerundolo, V., Colonna, M., Cresswell, P., Townsend, A., and DeMars, R. (1992). Presentation of viral antigen by MHC class I molecules is dependent on a putative peptide transporter heterodimer. Nature355, 644–646.10.1038/355644a0Search in Google Scholar

Spiliotis, E. T., Manley, H., Osorio, M., Zuniga, M. C., and Edidin, M. (2000). Selective export of MHC class I molecules from the ER after their dissociation from TAP. Immunity13, 841–851.10.1016/S1074-7613(00)00081-9Search in Google Scholar

Springer, S., Döring, K., Skipper, J. C., Townsend, A. R., and Cerundolo, V. (1998). Fast association rates suggest a conformational change in the MHC class I molecule H-2Db upon peptide binding. Biochemistry37, 3001–3012.10.1021/bi9717441Search in Google Scholar

Springer, S., Spang, A., and Schekman, R. (1999). A primer on vesicle budding. Cell97, 145–148.10.1016/S0092-8674(00)80722-9Search in Google Scholar

Sugita, M., and Brenner, M. B. (1994). An unstable β2-microglobulin: major histocompatibility complex class I heavy chain intermediate dissociates from calnexin and then is stabilized by binding peptide. J. Exp. Med.180, 2163–2171.10.1084/jem.180.6.2163Search in Google Scholar PubMed PubMed Central

Suh, W., Cohen, D., Fruh, K., Wang, K., Peterson, P., and Williams, D. (1994). Interaction of MHC class I molecules with the transporter associated with antigen processing. Science264, 1322–1326.10.1126/science.8191286Search in Google Scholar PubMed

Suh, W. K., Mitchell, E. K., Yang, Y., Peterson, P. A., Waneck, G. L., and Williams, D. B. (1996). 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.184, 337–348.10.1084/jem.184.2.337Search in Google Scholar PubMed PubMed Central

Suh, W. K., Derby, M. A., Cohen-Doyle, M. F., Schoenhals, G. J., Fruh, K., Berzofsky, J. A., and Williams, D. B. (1999). Interaction of murine MHC class I molecules with tapasin and TAP enhances peptide loading and involves the heavy chain α3 domain. J. Immunol.162, 1530–1540.10.4049/jimmunol.162.3.1530Search in Google Scholar

Sun, J., Leahy, D. J., and Kavathas, P. B. (1995). Interaction between CD8 and major histocompatibility complex (MHC) class I mediated by multiple contact surfaces that include the α2 and α3 domains of MHC class I. J. Exp. Med.182, 1275–1280.10.1084/jem.182.5.1275Search in Google Scholar

Tan, P., Kropshofer, H., Mandelboim, O., Bulbuc, N., Hammerling, G. J., and Momburg, F. (2002). Recruitment of MHC class I molecules by tapasin into the transporter associated with antigen processing-associated complex is essential for optimal peptide loading. J. Immunol.168, 1950–1960.10.4049/jimmunol.168.4.1950Search in Google Scholar

Tanioka, T., Hattori, A., Masuda, S., Nomura, Y., Nakayama, H., Mizutani, S., and Tsujimoto, M. (2003). Human leukocyte-derived arginine aminopeptidase. The third member of the oxytocinase subfamily of aminopeptidases. J. Biol. Chem.278, 32275–32283.10.1074/jbc.M305076200Search in Google Scholar

Tector, M., Zhang, Q., and Salter, R. D. (1997). β2-Microglobulin and calnexin can independently promote folding and disulfide bond formation in class I histocompatibility proteins. Mol. Immunol.34, 401–408.10.1016/S0161-5890(97)00045-XSearch in Google Scholar

Teng, M. S., Stephens, R., Du Pasquier, L., Freeman, T., Lindquist, J. A., and Trowsdale, J. (2002). A human TAPBP (TAPASIN)-related gene, TAPBP-R. Eur. J. Immunol.32, 1059–1068.10.1002/1521-4141(200204)32:4<1059::AID-IMMU1059>3.0.CO;2-GSearch in Google Scholar

Tormo, J., Natarajan, K., Margulies, D. H., and Mariuzza, R. A. (1999). Crystal structure of a lectin-like natural killer cell receptor bound to its MHC class I ligand. Nature402, 623–631.10.1038/45170Search in Google Scholar

Townsend, A., Elliott, T., Cerundolo, V., Foster, L., Barber, B., and Tse, A. (1990). Assembly of MHC class I molecules analyzed in vitro. Cell62, 285–295.10.1016/0092-8674(90)90366-MSearch in Google Scholar

Trombetta, E. S., and Helenius, A. (1998). Lectins as chaperones in glycoprotein folding. Curr. Opin. Struct. Biol.8, 587–592.10.1016/S0959-440X(98)80148-6Search in Google Scholar

Trombetta, E. S., and Helenius, A. (2000). Conformational requirements for glycoprotein reglucosylation in the endoplasmic reticulum. J. Cell Biol.148, 1123–1129.10.1083/jcb.148.6.1123Search in Google Scholar

Turnquist, H. R., Petersen, J. L., Vargas, S. E., McIlhaney, M. M., Bedows, E., Mayer, W. E., Grandea 3rd, A. G., Van Kaer, L., and Solheim, J. C. (2004). The Ig-like domain of tapasin influences intermolecular interactions. J. Immunol.172, 2976–2984.10.4049/jimmunol.172.5.2976Search in Google Scholar

Turnquist, H. R., Vargas, S. E., McIlhaney, M. M., Li, S., Wang, P., and Solheim, J. C. (2002a). Calreticulin binds to the α1 domain of MHC class I independently of tapasin. Tissue Antigens59, 18–24.10.1034/j.1399-0039.2002.590104.xSearch in Google Scholar

Turnquist, H. R., Vargas, S. E., Schenk, E. L., McIlhaney, M. M., Reber, A. J., and Solheim, J. C. (2002b). The interface between tapasin and MHC class I: identification of amino acid residues in both proteins that influence their interaction. Immunol. Res.25, 261–269.10.1385/IR:25:3:261Search in Google Scholar

van der Burg, S. H., Visseren, M. J., Brandt, R. M., Kast, W. M., and Melief, C. J. (1996). Immunogenicity of peptides bound to MHC class I molecules depends on the MHC-peptide complex stability. J. Immunol.156, 3308–3314.10.4049/jimmunol.156.9.3308Search in Google Scholar

van Leeuwen, J. E., and Kearse, K. P. (1996). Deglucosylation of N-linked glycans is an important step in the dissociation of calreticulin-class I-TAP complexes. Proc. Natl. Acad. Sci. USA93, 13997–14001.10.1073/pnas.93.24.13997Search in Google Scholar

Vassilakos, A., Cohen-Doyle, M. F., Peterson, P. A., Jackson, M. R., and Williams, D. B. (1996). The molecular chaperone calnexin facilitates folding and assembly of class I histocompatibility molecules. EMBO J.15, 1495–1506.10.1002/j.1460-2075.1996.tb00493.xSearch in Google Scholar

Vilches, C. (2003). MHC class I peptide binding and tapasin. J. Immunol.171, 3.10.4049/jimmunol.171.1.3Search in Google Scholar

Walker, K. W., and Gilbert, H. F. (1997). Scanning and escape during protein-disulfide isomerase-assisted protein folding. J. Biol. Chem.272, 8845–8848.10.1074/jbc.272.14.8845Search in Google Scholar

Wearsch, P. A., Jakob, C. A., Vallin, A., Dwek, R. A., Rudd, P. M., and Cresswell, P. (2004). MHC class I molecules expressed with monoglucosylated N-linked glycans bind calreticulin independently of their assembly status. J. Biol. Chem.279, 25112–25121.10.1074/jbc.M401721200Search in Google Scholar

Wei, M. L., and Cresswell, P. (1992). HLA-A2 molecules in an antigen processing mutant cell contain signal sequence-derived peptides. Nature356, 443–446.10.1038/356443a0Search in Google Scholar

Williams, A., Peh, C. A., and Elliott, T. (2002a). The cell biology of MHC class I antigen presentation. Tissue Antigens59, 3–17.10.1034/j.1399-0039.2002.590103.xSearch in Google Scholar

Williams, A. P., Peh, C. A., Purcell, A. W., McCluskey, J., and Elliott, T. (2002b). Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity16, 509–520.10.1016/S1074-7613(02)00304-7Search in Google Scholar

Williams, D., Swiedler, S., and Hart, G. (1985). Intracellular transport of memebrane glycoproteins: two closely related histocompatibility antigens differ in their rates of transit to the cell surface. J. Cell Biol.101, 725–734.10.1083/jcb.101.3.725Search in Google Scholar

Wilson, I. A., and Bjorkman, P. J. (1998). Unusual MHC-like molecules: CD1, Fc receptor, the hemochromatosis gene product, and viral homologs. Curr. Opin. Immunol.10, 67–73.10.1016/S0952-7915(98)80034-4Search in Google Scholar

Yague, J., Alvarez, I., Rognan, D., Ramos, M., Vazquez, J., and de Castro, J. A. (2000). An N-acetylated natural ligand of human histocompatibility leukocyte antigen (HLA)-B39. Classical major histocompatibility complex class I proteins bind peptides with a blocked NH2 terminus in vivo. J. Exp. Med.191, 2083–2092.10.1084/jem.191.12.2083Search in Google Scholar PubMed PubMed Central

Yu, Y. Y., Myers, N. B., Hilbert, C. M., Harris, M. R., Balendiran, G. K., and Hansen, T. H. (1999a). Definition and transfer of a serological epitope specific for peptide-empty forms of MHC class I. Int. Immunol.11, 1897–1906.10.1093/intimm/11.12.1897Search in Google Scholar PubMed

Yu, Y. Y., Turnquist, H. R., Myers, N. B., Balendiran, G. K., Hansen, T. H., and Solheim, J. C. (1999b). An extensive region of an MHC class I α2 domain loop influences interaction with the assembly complex. J. Immunol.163, 4427–4433.10.4049/jimmunol.163.8.4427Search in Google Scholar

Zacharias, M., and Springer, S. (2004). Conformational flexibility of the MHC class I α1-α2 domain in peptide bound and free states: a molecular dynamics simulation study. Biophys. J., in press.10.1529/biophysj.104.044743Search in Google Scholar PubMed PubMed Central

Zapun, A., Darby, N. J., Tessier, D. C., Michalak, M., Bergeron, J. J., and Thomas, D. Y. (1998). Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J. Biol. Chem.273, 6009–6012.10.1074/jbc.273.11.6009Search in Google Scholar PubMed

Zarling, A. L., Luckey, C. J., Marto, J. A., White, F. M., Brame, C. J., Evans, A. M., Lehner, P. J., Cresswell, P., Shabanowitz, J., Hunt, D. F., and Engelhard, V. H. (2003). Tapasin is a facilitator, not an editor, of class I MHC Peptide binding. J. Immunol.171, 5287–5295.10.4049/jimmunol.171.10.5287Search in Google Scholar PubMed

Zernich, D., Purcell, A. W., Macdonald, W. A., Kjer-Nielsen, L., Ely, L. K., Laham, N., Crockford, T., Mifsud, N. A., Bharadwaj, M., Chang, L. et al. (2004). Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion. J. Exp. Med.200, 13–24.10.1084/jem.20031680Search in Google Scholar PubMed PubMed Central

Zhang, C., Anderson, A., and DeLisi, C. (1998). Structural principles that govern the peptide-binding motifs of class I MHC molecules. J. Mol. Biol.281, 929–947.10.1006/jmbi.1998.1982Search in Google Scholar PubMed

Published Online: 2005-06-01

Published in Print: 2004-09-01

© Walter de Gruyter