Characterization of a proteasome and TAP-independent presentation of intracellular epitopes by HLA-B27 molecules

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30358-30367

  Magnacca, Adriana ^a   Persiconi, Irene ^a   Nurzia, Elisa ^a   Caristi, Silvana ^a   Meloni, Francesca ^a   Barnaba, Vincenzo ^a   Paladini, Fabiana ^a   Raimondo, Domenico ^a   Fiorillo, Maria Teresa ^a   Sorrentino, Rosa ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELLS; CELL SURFACES; CHIMERIC PROTEINS; PROTEASOMES;

ANTIGENS; CELL MEMBRANES; PROTEINS;

MOLECULES;

CARRIER PROTEIN; CHIMERIC PROTEIN; CYSTEINE; EPITOPE; GAMMA INTERFERON; HLA B27 ANTIGEN; PROTEASOME; TRANSPORTERS ASSOCIATED WITH ANTIGEN PRESENTATION; UNCLASSIFIED DRUG;

ANKYLOSING SPONDYLITIS; ANTIGEN PRESENTING CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE PRODUCTION; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STABILITY;

ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; EPITOPES; HELA CELLS; HLA-A2 ANTIGEN; HLA-B27 ANTIGEN; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING;

EID: 84865764371     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.384339     Document Type: Article

References (43)

1. Hülsmeyer, M., Fiorillo, M. T., Bettosini, F., Sorrentino, R., Saenger, W., Ziegler, A., and Uchanska-Ziegler, B. (2004) Dual, HLA-B27 subtype-dependent conformation of a self-peptide. J. Exp. Med. 199, 271-281
2. Fiorillo, M. T., Maragno, M., Butler, R., Dupuis, M. L., and Sorrentino, R. (2000) CD8(+) T-cell autoreactivity to an HLA-B27-restricted selfepitope correlates with ankylosing spondylitis. J. Clin. Invest. 106, 47-53
3. Nurzia, E., Panimolle F., Cauli, A., Mathieu, A., Magnacca, A., Paladini, F., Sorrentino, R., and Fiorillo, M. T. (2010) CD8+ T-cell mediated self-reactivity in HLA-B27 context as a consequence of dual peptide conformation. Clin. Immunol. 135, 476-482
4. Mathieu, A., Paladini, F., Vacca, A., Cauli, A., Fiorillo, M. T., and Sorrentino, R. (2009) The interplay between the geographic distribution of HLAB27 alleles and their role in infectious and autoimmune diseases: a unifying hypothesis. Autoimmun. Rev. 8, 420-425
5. Blanco-Gelaz, M. A., López-Vázquez, A., García-Fernández, S., Martínez- Borra, J., González, S., and López-Larrea, C. (2001) Genetic variability, molecular evolution, and geographic diversity of HLA-B27. Hum. Immunol. 62, 1042-1050
6. McNeil, A. J., Yap, P. L., Gore, S. M., Brettle, R. P., McColl, M., Wyld, R., Davidson, S., Weightman, R., Richardson, A. M., and Robertson, J. R. (1996) Association of HLA types A1-B8-DR3 and B27 with rapid and slow progression of HIV disease. Q. J. M. 89, 177-185
7. Neumann-Haefelin, C., McKiernan, S., Ward, S., Viazov, S., Spangenberg, H. C., Killinger, T., Baumert, T. F., Nazarova, N., Sheridan, I., Pybus, O., von Weizsäcker, F., Roggendorf, M., Kelleher, D., Klenerman, P., Blum, H. E., and Thimme, R. (2006) Dominant influence of an HLA-B27 restricted CD8+ Tcell response in mediatingHCVclearance and evolution. Hepatology 43, 563-572
8. Hendel, H., Caillat-Zucman, S., Lebuanec, H., Carrington, M., O'Brien, S., Andrieu, J. M., Schächter, F., Zagury, D., Rappaport, J., Winkler, C., Nelson, G. W., and Zagury, J. F. (1999) New class I and II HLA alleles strongly associated with opposite patterns of progression to AIDS. J. Immunol. 162, 6942-6946
9. Altfeld, M., Kalife, E. T., Qi, Y., Streeck, H., Lichterfeld, M., Johnston, M. N., Burgett, N., Swartz, M. E., Yang, A., Alter, G., Yu, X. G., Meier, A., Rockstroh, J. K., Allen, T. M., Jessen, H., Rosenberg, E. S., Carrington, M., and Walker, B. D. (2006) HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(+) T cell response against HIV-1. PLoS Med. 3, e403
10. Kosmrlj, A., Read, E. L., Qi, Y., Allen, T. M., Altfeld, M., Deeks, S. G., Pereyra, F., Carrington, M., Walker, B. D., and Chakraborty, A. K. (2010) Effects of thymic selection of the T-cell repertoire on HLA class I-associated control of HIV infection. Nature 465, 350-354
11. Elahi, S., Dinges, W. L., Lejarcegui, N., Laing, K. J., Collier, A. C., Koelle, D. M., McElrath, M. J., and Horton, H. (2011) Protective HIV-specific CD8+ T cells evade Treg cell suppression. Nat. Med. 17, 989-996
12. D'Amato, M., Fiorillo, M. T., Carcassi, C., Mathieu, A., Zuccarelli, A., Bitti, P. P., Tosi, R., and Sorrentino, R. (1995) Relevance of residue 116 of HLAB27 in determining susceptibility to ankylosing spondylitis. Eur. J. Immunol. 25, 3199-3201
13. Paladini, F., Taccari, E., Fiorillo, M. T., Cauli, A., Passiu, G., Mathieu, A., Punzi, L., Lapadula, G., Scarpa, R., and Sorrentino, R. (2005) Distribution of HLA-B27 subtypes in Sardinia and Continental Italy and their association with spondyloarthropathies. Arth. Rheum. 52, 3319-3321
14. García-Fernández, S., Gonzalez, S., Miña-Blanco, A., Martinez-Borra, J., Blanco-Gelaz, M., López-Vasquez, A., and López-Larrea, C. (2001) New insights regarding HLA-B27 diversity in the Asian population. Tissue Antigens 58, 259-262
15. Fiorillo, M. T., Rückert, C., Hülsmeyer, M., Sorrentino, R., Saenger, W., Ziegler, A., and Uchanska-Ziegler, B. (2005) Allele-dependent similarity between viral and self-peptide presentation by HLA-B27 subtypes. J. Biol. Chem. 280, 2962-2971
16. Taurog, J. D. (2009) Animal models of spondyloarthritis. Adv. Exp. Med. Biol. 649, 245-254
17. Evans, D. M., Spencer, C. C., Pointon, J. J., Su, Z., Harvey, D., Kochan, G., Oppermann, U., Dilthey, A., Pirinen, M., Stone, M. A., Appleton, L., Moutsianas, L., Leslie, S., Wordsworth, T., Kenna, T. J., Karaderi, T., Thomas, G. P., Ward, M. M., Weisman, M. H., Farrar, C., Bradbury, L. A., Danoy, P., Inman, R. D., Maksymowych, W., Gladman, D., Rahman, P., Spondyloarthritis Research Consortium of Canada (SPARCC), Morgan, A., Marzo- Ortega, H., Bowness, P., Gaffney, K., Gaston, J. S., Smith, M., Bruges- Armas, J., Couto, A. R., Sorrentino, R., Paladini, F., Ferreira, M. A., Xu, H., Liu, Y., Jiang, L., Lopez-Larrea, C., Díaz-Peña, R., López-Vázquez, A., Zayats, T., Band, G., Bellenguez, C., Blackburn, H., Blackwell, J. M., Bramon, E., Bumpstead, S. J., Casas, J. P., Corvin, A., Craddock, N., Deloukas, P., Dronov, S., Duncanson, A., Edkins, S., Freeman, C., Gillman, M., Gray, E., Gwilliam, R., Hammond, N., Hunt, S. E., Jankowski, J., Jayakumar, A., Langford, C., Liddle, J., Markus, H. S., Mathew, C. G., McCann, O. T., McCarthy, M. I., Palmer, C. N., Peltonen, L., Plomin, R., Potter, S. C., Rautanen, A., Ravindrarajah, R., Ricketts, M., Samani, N., Sawcer, S. J., Strange, A., Trembath, R. C., Viswanathan, A. C., Waller, M., Weston, P., Whittaker, P., Widaa, S., Wood, N. W., McVean, G., Reveille, J. D., Wordsworth, B. P., Brown, M. A., and Donnelly, P.; Australo-Anglo-American Spondyloarthritis Consortium (TASC); Wellcome Trust Case Control Consortium 2 (WTCCC2). (2011) Interaction between ERAP1 and HLAB27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility. Nat. Genet. 43, 761-767
18. Ben Dror, L., Barnea E., Beer, I., Mann M., and Admon, A. (2010) The HLA-B*2705 peptidome. Arthritis Rheum. 62, 420-429
19. Leonhardt, R. M., Fiegl, D., Rufer, E., Karger, A., Bettin, B., and Knittler, M. R. (2010) Post-endoplasmic reticulum rescue of unstable MHC class I requires proprotein convertase PC7. J. Immunol. 184, 2985-2998
20. Bettosini, F., Fiorillo, M. T., Magnacca, A., Leone, L., Torrisi, M. R., and Sorrentino, R. (2005) The C terminus of the nucleoprotein of influenza A virus delivers antigens transduced by Tat to the trans-Golgi network and promotes an efficient presentation through HLA class I. J. Virol. 79, 15537-15546
21. Urban, R. G., Chicz, R. M., Lane, W. S., Strominger, J. L., Rehm, A., Kenter, M. J., UytdeHaag, F. G., Ploegh, H., Uchanska-Ziegler, B., and Ziegler, A. (1994) A subset of HLA-B27 molecules contains peptides much longer than nonamers. Proc. Natl. Acad. Sci. U.S.A. 91, 1534-1538
22. Campbell, E. C., Antoniou, A. N., and Powis, S. J. (2012) The multifaceted nature of HLA class I dimer molecules. Immunology 136, 380-384
23. Bowness, P., Ridley, A., Shaw, J., Chan, A. T., Wong-Baeza, I., Fleming, M., Cummings, F., McMichael, A., and Kollnberger, S. (2011) Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J. Immunol. 186, 2672-2680
24. Fiorillo, M. T., Meadows, L., D'Amato, M., Shabanowitz, J., Hunt, D. F., Appella, E., and Sorrentino, R. (1997) Susceptibility to ankylosing spondylitis correlates with the C-terminal residue of peptides presented by various HLA-B27 subtypes. Eur. J. Immunol. 27, 368-373
25. Sesma, L., Montserrat, V., Lamas, J. R., Marina, L., Lamas, J. R., Marina, A., Vázquez, J., and López de Castro, J. A. (2002) The peptide repertoires of HLA-B27 subtypes differentially associated to spondyloarthropathy (B*2704 and B*2706) differ by specific changes at three anchor positions. J. Biol. Chem. 277, 16744-16749
26. Montserrat, V., Martí, M., and López de Castro J. A. (2003) Allospecific T cell epitope sharing reveals extensive conservation of the antigenic features of peptide ligands among HLA-B27 subtypes differentially associated with spondyloarthritis. J. Immunol. 170, 5778-5785
27. Rückert, C., Fiorillo, M. T., Loll, B., Moretti, R., Biesiadka, J., Saenger, W., Ziegler, A., Sorrentino, R., and Uchanska-Ziegler, B. (2006) Conformational dimorphism of self-peptides and molecular mimicry in a disease-associated HLA-B27 subtype. J. Biol. Chem. 281, 2306-2316
28. Tran, T. M., Satumtira, N., Dorris, M. L., May, E., Wang, A., Furuta, E., and Taurog, J. D. (2004) HLA-B27 in transgenic rats forms disulfide-linked heavy chain oligomers and multimers that bind to the chaperone BiP. J. Immunol. 172, 5110-5119
29. Nagahara, H., Vocero-Akbani, A. M., Snyder, E. L., Ho, A., Latham, D. G., Lissy, N. A., Becker-Hapak, M., Ezhevsky, S. A., and Dowdy, S. F. (1998) Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat. Med. 4, 1449-1452
30. Propato, A., Cutrona, G., Francavilla, V., Ulivi, M., Schiaffella, E., Landt, O., Dunbar, R., Cerundolo, V., Ferrarini, M., and Barnaba, V. (2001) Apoptotic cells overexpress vinculin and induce vinculin-specific cytotoxic T-cell cross-priming. Nat. Med. 7, 807-813
31. Tuncbag, N., Gursoy, A., and Keskin, O. (2009) Identification of computational hot spots in protein interfaces: combining solvent accessibility and inter-residue potentials improves the accuracy. Bioinformatics 25, 1513-1520
32. Wallace, A. C., Laskowski, R. A., and Thornton, J. M. (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8, 127-134
33. Santos, S. G., Antoniou, A. N., Sampaio, P., Powis, S. J., and Arosa, F. A. (2006) Lack of tyrosine 320 impairs spontaneous endocytosis and enhances release of HLA-B27 molecules. J. Immunol. 176, 2942-2949
34. Alvarez, I., Martí, M., Vázquez, J., Camafeita, E., Ogueta, S., and López de Castro, J. A. (2001) The Cys-67 residue of HLA-B27 influences cell surface stability, peptide specificity, and T-cell antigen presentation. J. Biol. Chem. 276, 48740-48747
35. London, N., Raveh, B., Cohen, E., Fathi, G., and Schueler-Furman, O. (2011) Rosetta FlexPepDock web server-high resolution modeling of peptide-protein interactions. Nucleic Acids Res. 39, W249-253
36. Kessler, J. H., Khan, S., Seifert, U., Le Gall, S., Chow, K. M., Paschen, A., Bres-Vloemans, S. A., de Ru, A., van Montfoort, N., Franken, K. L., Benckhuijsen, W. E., Brooks, J. M., van Hall, T., Ray, K., Mulder, A., Doxiadis, I. I., van Swieten, P. F., Overkleeft, H. S., Prat, A., Tomkinson, B., Neefjes, J., Kloetzel, P. M., Rodgers, D. W., Hersh, L. B., Drijfhout, J. W., van Veelen, P. A., Ossendorp, F., and Melief, C. J. (2011) Antigen processing by nardilysin and thimet oligopeptidase generates cytotoxic T cell epitopes. Nat. Immunol. 12, 45-53
37. Demaurex, N., Furuya, W., D'Souza, S., Bonifacino, J. S., and Grinstein, S. (1998) Mechanism of acidification of the trans-Golgi network (TGN). In situ measurements of pH using retrieval of TGN38 and furin from the cell surface. J. Biol. Chem. 273, 2044-2051
38. Nakamura, N., Tanaka, S., Teko, Y., Mitsui, K., and Kanazawa, H. (2005) Four Na+/H+ exchanger isoforms are distributed to Golgi and post-Golgi compartments and are involved in organelle pH regulation. J. Biol. Chem. 280, 1561-1572
39. Mear, J. P., Schreiber, K. L., Münz, C., Zhu, X., Stevanović, S., Rammensee, H. G., Rowland-Jones, S. L., and Colbert, R. A. (1999) Misfolding of HLAB27 as a result of its B pocket suggests a novel mechanism for its role in susceptibility to spondyloarthropathies. J. Immunol. 163, 6665-6670
40. Appel, H., Kuon, W., Kuhne, M., Hülsmeyer, M., Kollnberger, S., Kuhlmann, S., Weiss, E., Zeitz, M., Wucherpfennig, K., Bowness, P., and Sieper, J. (2004) The solvent-inaccessible Cys-67 residue of HLA-B27 contributes to T cell recognition of HLA-B27/peptide complexes. J. Immunol. 173, 6564-6573
41. Stewart-Jones, G. B., di Gleria, K., Kollnberger, S., McMichael A. J., Jones E. Y., and Bowness, P. (2005) Crystal structures and KIR3DL1 recognition of three immunodominant viral peptides complexed to HLA-B*2705. Eur. J. Immunol. 35, 341-351
42. Fiorillo, M. T., Greco, G., Maragno, M., Potolicchio, I., Monizio, A., Dupuis, M. L., and Sorrentino, R. (1998) The naturally occurring polymorphism Asp116-His116, differentiating the ankylosing spondylitis-associated HLA-B*2705 from the non-associated HLA-B*2709 subtype, influences peptide-specific CD8 T cell recognition. Eur. J. Immunol. 28, 2508-2516
43. Evnouchidou, I., Kamal, R. P., Seregin, S. S., Goto, Y., Tsujimoto, M., Hattori, A., Voulgari, P. V, Drosos, A. A., Amalfitano, A., York, I. A., and Stratikos, E. (2011) Cutting Edge: Coding single nucleotide polymorphisms of endoplasmic reticulum aminopeptidase 1 can affect antigenic peptide generation in vitro by influencing basic enzymatic properties of the enzyme. J. Immunol. 186, 1909-1913