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

Journal of Experimental Medicine

Volumn 191, Issue 12, 2000, Pages 2083-2092

  Yagüe, Jesús ^a   Alvarez, Iñaki ^a   Rognan, Didier ^b   Ramos, Manuel ^a   Vázquez, Jesús ^a   López De Castro, José A ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b Eidgenössiche TH ^*  (Switzerland)

Author keywords

Antigen processing; Biochemistry; Human; Molecular biology; Tolerance

Indexed keywords

AMINOPEPTIDASE; HLA B ANTIGEN; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ARTICLE; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SEQUENCE ANALYSIS;

ACETYLATION; AMINO ACID SEQUENCE; HLA-B ANTIGENS; HUMANS; LIGANDS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING;

EID: 0034686435     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.12.2083     Document Type: Article

References (50)

1. Bjorkman, P.J., M.A. Saper, B. Samraoui, W.S. Bennett, J.L. Strominger, and D.C. Wiley. 1987. Structure of the human class I histocompatibility antigen, HLA-A2. Nature. 329:506-512.
2. Bjorkman, P.J., M.A. Saper, B. Samraoui, W.S. Bennett, J.L. Strominger, and D.C. Wiley. 1987. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature. 329:512-518.
3. Garrett, T.P., M.A. Saper, P.J. Bjorkman, J.L. Strominger, and D.C. Wiley. 1989. Specificity pockets for the side chains of peptide antigens in HLA-Aw68. Nature. 342:692-696.
4. Saper, M.A., P.J. Bjorkman, and D.C. Wiley. 1991. Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. J. Mol. Biol. 219:277-319.
5. Madden, D.R. 1995. The three-dimensional structure of peptide-MHC complexes. Annu. Rev. Immunol. 13:587-622.
6. Rammensee, H.G., T. Friede, and S. Stevanoviic. 1995. MHC ligands and peptide motifs: first listing. Immunogenetics. 41:178-228.
7. Guo, H.C., T.S. Jardetzky, T.P. Garrett, W.S. Lane, J.L. Strominger, and D.C. Wiley. 1992. Different length peptides bind to HLA-Aw68 similarly at their ends but bulge out in the middle. Nature. 360:364-366.
8. Fremont, D.H., M. Matsumura, E.A. Stura, P.A. Peterson, and I.A. Wilson. 1992. Crystal structures of two viral peptides in complex with murine MHC class I H-2Kb. Science. 257:919-927.
9. Madden, D.R., D.N. Garboczi, and D.C. Wiley. 1993. The antigenic identity of peptide-MHC complexes: a comparison of the conformations of five viral peptides presented by HLA-A2 [published erratum at 76:410]. Cell. 75:693-708.
10. Bouvier, M., and D.C. Wiley. 1994. Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules. Science. 265:398-402.
11. Bouvier, M., H.C. Guo, K.J. Smith, and D.C. Wiley. 1998. Crystal structures of HLA-A*0201 complexed with antigenic peptides with either the amino-or carboxyl-terminal group substituted by a methyl group. Proteins. 33:97-106.
12. Collins, E.J., D.N. Garboczi, and D.C. Wiley. 1994. Three-dimensional structure of a peptide extending from one end of a class I MHC binding site. Nature. 371:626-629.
13. Madden, D.R., J.C. Gorga, J.L. Strominger, and D.C. Wiley. 1992. The three-dimensional structure of HLA-B27 at 2.1 A resolution suggests a general mechanism for tight peptide binding to MHC. Cell. 70:1035-1048.
14. Elliott, T., J. Elvin, V. Cerundolo, H. Allen, and A. Townsend. 1992. Structural requirements for the peptide-induced conformational change of free major histocompatibility complex class I heavy chains. Eur. J. Immunol. 22:2085-2091.
15. Matsumura, M., Y. Saito, M.R. Jackson, E.S. Song, and P.A. Peterson. 1992. In vitro peptide binding to soluble empty class I major histocompatibility complex molecules isolated from transfected Drosophila melanogaster cells. J. Biol. Chem. 267:23589-23595.
16. Shawar, S.M., R.G. Cook, J.R. Rodgers, and R.R. Rich. 1990. Specialized functions of MHC class I molecules. I. An N-formyl peptide receptor is required for construction of the class I antigen Mta. J. Exp. Med. 171:897-912.
17. Shawar, S.M., J.M. Vyas, J.R. Rodgers, R.G. Cook, and R.R. Rich. 1991. Specialized functions of major histocompatibility complex class I molecules. II. Hmt binds N-formylated peptides of mitochondrial and prokaryotic origin. J. Exp. Med. 174:941-944.
18. Wang, C.R., B.E. Loveland, and K.F. Lindahl. 1991. H-2M3 encodes the MHC class I molecule presenting the maternally transmitted antigen of the mouse. Cell. 66:335-345.
19. Wang, C.R., A.R. Castano, P.A. Peterson, C. Slaughter, K.F. Lindahl, and J. Deisenhofer. 1995. Nonclassical binding of formylated peptide in crystal structure of the MHC class Ib molecule H2-M3. Cell. 82:655-664.
20. Fischer-Lindahl, K., D.E. Byers, V.M. Dabhi, R. Hovik, E.P. Jones, G.P. Smith, C.R. Wang, H. Xiao, and M. Yoshino. 1997. H2-M3, a full-service class Ib histocompatibility antigen. Annu. Rev. Immunol. 15:851-879.
21. Jornvall, H. 1975. Acetylation of protein N-terminal amino groups structural observations on alpha-amino acetylated proteins. J. Theor. Biol. 55:1-12.
22. Persson, B., C. Flinta, G. von Heijne, and H. Jornvall. 1985. Structures of N-terminally acetylated proteins. Eur. J. Biochem. 152:523-527.
23. Yague, J., M. Ramos, J. Vazquez, A. Marina, J.P. Albar, and J.A. Lopez de Castro. 1999. The South Amerindian allotype HLA-B*3909 has the largest known similarity in peptide specificity and common natural ligands with HLA-B27. Tissue Antigens. 53:227-236.
24. Ljunggren, H.G., and K. Karre. 1985. Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J. Exp. Med. 162:1745-1759.
25. Townsend, A., C. Ohlen, J. Bastin, H.G. Ljunggren, L. Foster, and K. Karre. 1989. Association of class I major histocompatibility heavy and light chains induced by viral peptides. Nature. 340:443-448.
26. Lopez, D., R. Garcia Hoyo, F. Garcia, and J.A. Lopez de Castro. 1994. T cell allorecognition and endogenous HLA-B27-bound peptides in a cell line with defective HLA-B27-restricted antigen presentation. Eur. J. Immunol. 24:1194-1199.
27. Paradela, A., M. Garcia-Peydro, J. Vazquez, D. Rognan, and J.A. Lopez de Castro. 1998. The same natural ligand is involved in allorecognition of multiple HLA-B27 subtypes by a single T cell clone: role of peptide and the MHC molecule in alloreactivity. J. Immunol. 161:5481-5490.
28. Barnstable, C.J., W.F. Bodmer, G. Brown, G. Galfre, C. Milstein, A.F. Williams, and A. Ziegler. 1978. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens. New tools for genetic analysis. Cell. 14:9-20.
29. Marina, A., M.A. Garcia, J.P. Albar, J. Yague, J.A. Lopez de Castro, and J. Vazquez. 1999. High-sensitivity analysis and sequencing of peptides and proteins by quadrupole ion trap mass spectrometry. J. Mass Spectrom. 34:17-27.
30. Ellis, S.A., C. Taylor, and A. McMichael. 1982. Recognition of HLA-B27 and related antigens by a monoclonal antibody. Hum. Immunol. 5:49-59.
31. Villadangos, J.A., B. Galocha, F. Garcia, J.P. Albar, and J.A. Lopez de Castro. 1995. Modulation of peptide binding by HLA-B27 polymorphism in pockets A and B, and peptide specificity of B*2703. Eur. J. Immunol. 25:2370-2377.
32. Lahn, B.T., and D.C. Page. 1997. Functional coherence of the human Y chromosome. Science. 278:675-680.
33. You, L.R., C.M. Chen, T.S. Yeh, T.Y. Tsai, R.T. Mai, C.H. Lin, and Y.H. Lee. 1999. Hepatitis C virus core protein interacts with cellular putative RNA helicase. J. Virol. 73: 2841-2853.
34. Wachsmuth, E.D., I. Fritze, and G. Pfleiderer. 1966. An aminopeptidase occurring in pig kidney. I. An improved method of preparation. Physical and enzymic properties. Biochemistry. 5:169-174.
35. Wachsmuth, E.D., I. Fritze, and G. Pfleiderer. 1966. An aminopeptidase occurring in pig kidney. II. A study on the mechanism of the hydrolysis. Biochemistry. 5:175-182.
36. Huet, S., D.F. Nixon, J.B. Rothbard, A. Townsend, S.A. Ellis, and A.J. McMichael. 1990. Structural homologies between two HLA B27-restricted peptides suggest residues important for interaction with HLA B27. Int. Immunol. 2:311-316.
37. Skipper, J.C., R.C. Hendrickson, P.H. Gulden, V. Brichard, A. Van Pel, Y. Chen, J. Shabanowitz, T. Wolfel, C.L.J. Slingluff, T. Boon, et al. 1996. An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins. J. Exp. Med. 183:527-534.
38. Meadows, L., W. Wang, J.M. den Haan, E. Blokland, C. Reinhardus, J.W. Drijfhout, J. Shabanowitz, R. Pierce, A.I. Agulnik, C.E. Bishop, et al. 1997. The HLA-A*0201-restricted H-Y antigen contains a posttranslationally modified cysteine that significantly affects T cell recognition. Immunity. 6:273-281.
39. Haurum, J.S., I.B. Hoier, G. Arsequell, A. Neisig, G. Valencia, J. Zeuthen, J. Neefjes, and T. Elliott. 1999. Presentation of cytosolic glycosylated peptides by human class I major histocompatibility complex molecules in vivo. J. Exp. Med. 190: 145-150.
40. Andersen, M.H., J.E. Bonfill, A. Neisig, G. Arsequell, I. Sondergaard, J. Neefjes, J. Zeuthen, T. Elliott, and J.S. Haurum. 1999. Phosphorylated peptides can be transported by TAP molecules, presented by class I MHC molecules, and recognized by phosphopeptide-specific CTL. J. Immunol. 163: 3812-3818.
41. Lamas, J.R., A. Paradela, and J.A. Lopez de Castro. 1999. The peptide specificity of HLA-B27 subtypes differentially associated to ankylosing spondylitis is modulated at multiple anchor positions. Arthritis Rheum. 42:1975-1985.
42. Vyas, J.M., S.M. Shawar, J.R. Rodgers, R.G. Cook, and R.R. Rich. 1992. Biochemical specificity of H-2M3a. Stereospecificity and space-filling requirements at position 1 maintain N-formyl peptide binding. J. Immunol. 149:3605-3611.
43. Rock, K.L., and A. Goldberg. 1999. Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 17:739-779.
44. Mayer, A., N.R. Siegel, A.L. Schwartz, and A. Ciechanover. 1989. Degradation of proteins with acetylated amino termini by the ubiquitin system. Science. 244:1480-1483.
45. Gonen, H., C.E. Smith, N.R. Siegel, C. Kahana, W.C. Merrick, K. Chakraburtty, A.L. Schwartz, and A. Ciechanover. 1994. Protein synthesis elongation factor EF-1 alpha is essential for ubiquitin-dependent degradation of certain N alpha-acetylated proteins and may be substituted for by the bacterial elongation factor EF-Tu. Proc. Natl. Acad. Sci. USA. 91: 7648-7652.
46. Ciechanover, A. 1994. The ubiquitin-proteasome proteolytic pathway. Cell. 79:13-21.
47. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
48. Rickinson, A.B., and D.J. Moss. 1997. Human cytotoxic T lymphocyte responses to Epstein-Barr virus infection. Annu. Rev. Immunol. 15:405-431.
49. Roepstorff, P., and J. Fohlman. 1984. Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed. Mass Spectrom. 11:601.
50. Jardetzky, T.S., W.S. Lane, R.A. Robinson, D.R. Madden, and D.C. Wiley. 1991. Identification of self peptides bound to purified HLA-B27. Nature. 353:326-329.