Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion

Journal of Experimental Medicine

Volumn 200, Issue 1, 2004, Pages 13-24

  Zernich, Danielle ^a   Purcell, Anthony W ^a   Macdonald, Whitney A ^a   Kjer Nielsen, Lars ^a   Ely, Lauren K ^b   Laham, Nihay ^a   Crockford, Tanya ^a   Mifsud, Nicole A ^a   Bharadwaj, Mandvi ^a   Chang, Linus ^a   Tait, Brian D ^c   Holdsworth, Rhonda ^c   Brooks, Andrew G ^a   Bottomley, Stephen P ^b   Beddoe, Travis ^b   Peh, Chen Au ^d   Rossjohn, Jamie ^b   McCluskey, James ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c AUSTRALIAN RED CROSS BLOOD SERVICE   (Australia)

^d ROYAL ADELAIDE HOSPITAL   (Australia)

Author keywords

Ag presentation; HLA; Immune evasion; Polymorphism; Tapasin

Indexed keywords

COMPLEMENTARY DNA; HLA ANTIGEN CLASS 1; HLA B44 ANTIGEN; TAPASIN;

ANTIGEN PRESENTATION; ARTICLE; CELL MEMBRANE TRANSPORT; FLOW CYTOMETRY; GENETIC POLYMORPHISM; HERPES SIMPLEX VIRUS; HLA SYSTEM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOPRECIPITATION; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; VIRUS INFECTION; WESTERN BLOTTING;

ANIMALS; ANTIGEN PRESENTATION; ANTIPORTERS; CELL LINE; CRYSTALLOGRAPHY, X-RAY; DISEASE SUSCEPTIBILITY; GENES, MHC CLASS I; HERPES SIMPLEX; HLA-B ANTIGENS; HUMANS; IMMUNOGLOBULINS; MEMBRANE TRANSPORT PROTEINS; MICE; MODELS, MOLECULAR; PEPTIDES; POLYMORPHISM, GENETIC; PROTEIN CONFORMATION; PROTEIN ISOFORMS; SIMPLEXVIRUS;

EID: 2942753075     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20031680     Document Type: Article

References (65)

1. Parham, P., and T. Ohta. 1996. Population biology of antigen presentation by MHC class I molecules. Science. 272:67-74.
2. Messaoudi, I., J.A. Patino, R. Dyall, J. LeMaoult, and J. Nikolich-Zugich. 2002. Direct link between MHC polymorphism, T cell avidity, and diversity in immune defense. Science. 298:1797-1800.
3. Potts, W.K., and P.R. Slev. 1995. Pathogen-based models favoring MHC genetic diversity. Immunol. Rev. 143:181-197.
4. Greenwood, R., Y. Shimizu, G.S. Sekhon, and R. DeMars. 1994. Novel allele-specific, post-translational reduction in HLA class I surface expression in a mutant human B cell line. J. Immunol. 153:5525-5536.
5. Neisig, A., R. Wubbolts, X. Zang, C. Melief, and J. Neefjes. 1996. Allele-specific differences in the interaction of MHC class I molecules with transporters associated with antigen processing. J. Immunol. 156:3196-3206.
6. Peh, C.A., S.R. Burrows, M. Barnden, R. Khanna, P. Cresswell, D.J. Moss, and J. McCluskey. 1998. HLA-B27-restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I peptide loading. Immunity. 8:531-542.
7. Knittler, M.R., K. Gulow, A. Seelig, and J.C. Howard. 1998. MHC class I molecules compete in the endoplasmic reticulum for access to transporter associated with antigen processing. J. Immunol. 161:5967-5977.
8. Turnquist, H.R., H.J. Thomas, K.R. Prilliman, C.T. Lutz, W.H. Hildebrand, and J.C. Solheim. 2000. HLA-B polymorphism affects interactions with multiple endoplasmic reticulum proteins. Eur. J. Immunol. 30:3021-3028.
9. Turnquist, H.R., E.L. Schenk, M.M. McIlhaney, H.D. Hickman, W.H. Hildebrand, and J.C. Solheim. 2002. Disparate binding of chaperone proteins by HLA-A subtypes. Immunogenetics. 53:830-834.
10. Hildebrand, W.H., H.R. Turnquist, K.R. Prilliman, H.D. Hickman, E.L. Schenk, M.M. McIlhaney, and J.C. Solheim. 2002. HLA class I polymorphism has a dual impact on ligand binding and chaperone interaction. Hum. Immunol. 63:248-255.
11. Park, B., S. Lee, E. Kim, and K. Ahn. 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.
12. Park, B., S. Lee, E. Kim, and K. Ahn. 2003. Correction: a single polymorphic residue within the peptide-binding cleft of MHC class I molecules determines spectrum of tapasin dependence. J. Immunol. 170:4869.
13. Cresswell, P., N. Bangia, T. Dick, and G. Diedrich. 1999. The nature of the MHC class I peptide loading complex. Immunol. Rev. 172:21-28.
14. Sadasivan, B., P.J. Lehner, B. Ortmann, T. Spies, and P. Cresswell. 1996. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity. 5:103-114.
15. Williams, A., C.A. Peh, and T. Elliott. 2002. The cell biology of MHC class I antigen presentation. Tissue Antigens. 59:3-17.
16. Lehner, P.J., M.J. Surman, and P. Cresswell. 1998. Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line .220. Immunity. 8:221-231.
17. Peh, C.A., N. Laham, S.R. Burrows, Y. Zhu, and J. McCluskey. 2000. Distinct functions of tapasin revealed by polymorphism in MHC class I peptide loading. J. Immunol. 164:292-299.
18. Williams, A.P., C.A. Peh, A.W. Purcell, J. McCluskey, and T. Elliott. 2002. Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity. 16:509-520.
19. Dick, T.P., N. Bangia, D.R. Peaper, and P. Cresswell. 2002. Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity. 16:87-98.
20. Park, B., and K. Ahn. 2003. An essential function of tapasin in quality control of HLA-G molecules. J. Biol. Chem. 278:14337-14345.
21. Ortmann, B., J. Copeman, P.J. Lehner, B. Sadasivan, J.A. Herberg, A.G. Grandea, S.R. Riddell, R. Tampe, T. Spies, J. Trowsdale, and P. Cresswell. 1997. A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science. 277:1306-1309.
22. Powis, S.J., L.L. Young, E. Joly, P.J. Barker, L. Richardson, R.P. Brandt, C.J. Melief, J.C. Howard, and G.W. Butcher. 1996. The rat cim effect: TAP allele-dependent changes in a class I MHC anchor motif and evidence against C-terminal trimming of peptides in the ER. Immunity. 4:159-165.
23. Purcell, A.W., J.J. Gorman, M. Garcia-Peydro, A. Paradela, S.R. Burrows, G.H. Talbo, N. Laham, C.A. Peh, E.C. Reynolds, J.A. Lopez De Castro, et al. 2001. Quantitative and qualitative influences of tapasin on the class I peptide repertoire. J. Immunol. 166:1016-1027.
24. Park, B., Y. Kim, J. Shin, S. Lee, K. Cho, K. Fruh, and K. Ahn. 2004. Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity. 20:71-85.
25. Raffoux, C., R.C. Williams, C. Gorodezky, E.D. Albert, E. Gyodi, M.G. Hammond, Z. Layrisse, M. Mariani, G. de la Rosa, J.M. Tiercy, et al. 1997. AHS#7: HLA-B12, B13, B21, B37, B40, B41, B81, B4005. In Genetic Diversity of HLA Functional and Medical Implication. D. Charron, editor. EDK Medical and Scientific International Publisher, Paris. 69-72.
26. Fleischhauer, K., N.A. Kernan, B. Dupont, and S.Y. Yang. 1991. The two major subtypes of HLA-B44 differ for a single amino acid in codon 156. Tissue Antigens. 37:133-137.
27. Vilches, C. 2003. MHC class I peptide binding and tapasin. J. Immunol. 171:3.
28. Copeman, J., N. Bangia, J.C. Cross, and P. Cresswell. 1998. 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. 28:3783-3791.
29. Zemmour, J., A.M. Little, D.J. Schendel, and P. Parham. 1992. The HLA-A,B "negative" mutant cell line C1R expresses a novel HLA-B35 allele, which also has a point mutation in the translation initiation codon. J. Immunol. 148:1941-1948.
30. Hill, A., P. Jugovic, I. York, G. Russ, J. Bennink, J. Yewdell, H. Ploegh, and D. Johnson. 1995. Herpes simplex virus turns off the TAP to evade host immunity. Nature. 375:411-415.
31. Stam, N.J., H. Spits, and H.L. Ploegh. 1986. Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J. Immunol. 137:2299-2306.
32. Carreno, B.M., J.C. Solheim, M. Harris, I. Stroynowski, J.M. Connolly, and T.H. Hansen. 1995. TAP associates with a unique class I conformation, whereas calnexin associates with multiple class I forms in mouse and man. J. Immunol. 155:4726-4733.
33. van Endert, P.M., R. Tampe, T.H. Meyer, R. Tisch, J.F. Bach, and H.O. McDevitt. 1994. A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity. 1:491-500.
34. Androlewicz, M.J., B. Ortmann, P.M. van Endert, T. Spies, and P. Cresswell. 1994. Characteristics of peptide and major histocompatibility complex class I/beta 2-microglobulin binding to the transporters associated with antigen processing (TAP1 and TAP2). Proc. Natl. Acad. Sci. USA. 91:12716-12720.
35. Macdonald, W.A., A.W. Purcell, N. Mifsud, L.K. Ely, D.S. Williams, L. Chang, J.J. Gorman, C.S. Clements, L. Kjer-Nielsen, D.M. Koelle, et al. 2003. A naturally selected dimorphism within the HLA-B44 supertype alters class I structure, peptide repertoire and T cell recognition. J. Exp. Med. 198:679-691.
36. Macdonald, W., D.S. Williams, C.S. Clements, J.J. Gorman, L. Kjer-Nielsen, A.G. Brooks, J. McCluskey, J. Rossjohn, and A.W. Purcell. 2002. Identification of a dominant self-ligand bound to three HLA B44 alleles and the preliminary crystallographic analysis of recombinant forms of each complex. FEBS Lett. 527:27-32.
37. Ottwinowski, Z. 1993. Oscillation data reduction program. In Data Collection and Processing. L. Sawyer, N. Issacs, and S. Bailey, editors. SEKC Daresbury Laboratory, U.K., Warrington, U.K. 56-62.
38. Brunger, A.T., P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, N.S. Pannu, et al. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
39. Nicholls, A., K.A. Sharp, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins. 11:281-296.
40. Fruh, K., A. Gruhler, R.M. Krishna, and G.J. Schoenhals. 1999. A comparison of viral immune escape strategies targeting the MHC class I assembly pathway. Immunol. Rev. 168:157-166.
41. Khanna, R., S.R. Burrows, A. Neisig, J. Neefjes, D.J. Moss, and S.L. Silins. 1997. Hierarchy of Epstein-Barr virus-specific cytotoxic T-cell responses in individuals carrying different subtypes of an HLA allele: implications for epitope-based antiviral vaccines. J. Virol. 71:7429-7435.
42. Neisig, A., C.J. Melief, and J. Neefjes. 1998. Reduced cell surface expression of HLA-C molecules correlates with restricted peptide binding and stable TAP interaction. J. Immunol. 160:171-179.
43. Ford, S., A.N. Antoniou, G.W. Butcher, and S.J. Powis. 2004. Competition for access to the rat MHC class I peptide loading complex reveals optimisation of peptide cargo in the absence of TAP association. J. Biol. Chem. 279:16077-16082. First published on February 4, 2004; 10.1074/jbc. M400456200.
44. Garcia-Peydro, M., M. Marti, and J. Lopez de Castro. 1999. High T cell epitope sharing between two HLA-B27 subtypes (B*2705 and B*2709) differentially associated to ankylosing spondylitis. J. Immunol. 163:2299-2305.
45. Ramos, M., A. Paradela, M. Vazquez, A. Marina, J. Vazquez, and J.A. Lopez de Castro. 2002. Differential association of HLA-B*2705 and B*2709 to ankylosing spondylitis correlates with limited peptide subsets but not with altered cell surface stability. J. Biol. Chem. 277:28749-28756.
46. Reits, E., A. Griekspoor, J. Neijssen, T. Groothuis, K. Jalink, P. van Veelen, H. Janssen, J. Calafat, J.W. Drijfhout, and J. Neefjes. 2003. Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity. 18:97-108.
47. Lybarger, L., X. Wang, M.R. Harris, H.W.t. Virgin, and T.H. Hansen. 2003. Virus subversion of the MHC class I peptide-loading complex. Immunity 18:121-130.
48. Fruh, K., K. Ahn, and P.A. Peterson. 1997. Inhibition of MHC class I antigen presentation by viral proteins. J. Mol. Med. 75:18-27.
49. Hughes, E.A., C. Hammond, and P. Cresswell. 1997. Misfolded major histocompatibility complex class I heavy chains are translocated into the cytoplasm and degraded by the proteasome. Proc. Natl. Acad. Sci. USA. 94:1896-1901.
50. Schoenhals, G.J., R.M. Krishna, A.G. Grandea III, T. Spies, P.A. Peterson, Y. Yang, and K. Fruh. 1999. Retention of empty MHC class I molecules by tapasin is essential to reconstitute antigen presentation in invertebrate cells. EMBO J. 18:743-753.
51. Barnden, M.J., A.W. Purcell, J.J. Gorman, and J. McCluskey. 2000. Tapasin-mediated retention and optimization of peptide ligands during the assembly of class I molecules. J. Immunol. 165:322-330.
52. Froloff, N., A. Windemuth, and B. Honig. 1997. On the calculation of binding free energies using continuum methods: application to MHC class I protein-peptide interactions. Protein Sci. 6:1293-1301.
53. Matthews, B.W. 1993. Structural and genetic analysis of protein stability. Annu. Rev. Biochem. 62:139-160.
54. Serrano, L., M. Bycroft, and A.R. Fersht. 1991. Aromatic-aromatic interactions and protein stability. Investigation by double-mutant cycles. J. Mol. Biol. 218:465-475.
55. Fruci, D., G. Niedermann, R.H. Butler, and P.M. van Endert. 2001. Efficient MHC class I-independent amino-terminal trimming of epitope precursor peptides in the endoplasmic reticulum. Immunity. 15:467-476.
56. Brouwenstijn, N., T. Serwold, and N. Shastri. 2001. MHC class I molecules can direct proteolytic cleavage of antigenic precursors in the endoplasmic reticulum. Immunity. 15:95-104.
57. Lorenzo, M.E., H.L. Ploegh, and R.S. Tirabassi. 2001. Viral immune evasion strategies and the underlying cell biology. Semin. Immunol. 13:1-9.
58. Burgert, H.G., Z. Ruzsics, S. Obermeier, A. Hilgendorf, M. Windheim, and A. Elsing. 2002. Subversion of host defense mechanisms by adenoviruses. Curr. Top. Microbiol. Immunol. 269:273-318.
59. Boname, J.M., B.D. De Lima, P.J. Lehner, and P.G. Stevenson. 2004. Viral degradation of the MHC class I peptide loading complex. Immunity. 20:305-317.
60. Reddehase, M.J. 2002. Antigens and immunoevasins: opponents in cytomegalovirus immune surveillance. Nat. Rev. Immunol. 2:831-844.
61. Benjamin, R.J., J.A. Madrigal, and P. Parham. 1991. Peptide binding to empty HLA-B27 molecules of viable human cells. Nature. 351:74-77.
62. Carreno, B.M., and T.H. Hansen. 1994. Exogenous peptide ligand influences the expression and half-life of free HLA class I heavy chains ubiquitously detected at the cell surface. Eur. J. Immunol. 24:1285-1292.
63. Purcell, A.W., A.J. Kelly, C.A. Peh, N.L. Dudek, and J. McCluskey. 2000. Endogenous and exogenous factors contributing to the surface expression of HLA B27 on mutant APC. Hum. Immunol. 61:120-130.
64. Kaufman, J., S. Milne, T.W. Gobel, B.A. Walker, J.P. Jacob, C. Auffray, R. Zoorob, and S. Beck. 1999. The chicken B locus is a minimal essential major histocompatibility complex. Nature. 401:923-925.
65. Beier, D.C., J.H. Cox, D.R. Vining, P. Cresswell, and V.H. Engelhard. 1994. Association of human class I MHC alleles with the adenovirus E3/19K protein. J. Immunol. 152:3862-3872.