A novel family of human leukocyte antigen class II receptors may have its origin in archaic human species

Journal of Biological Chemistry

Volumn 289, Issue 2, 2014, Pages 639-653

  Temme, Sebastian ^a,b   Zacharias, Martin ^c   Neumann, Jürgen ^a   Wohlfromm, Sebastian ^b   König, Angelika ^a   Temme, Nadine ^a,d   Springer, Sebastian ^e   Trowsdale, John ^f   Koch, Norbert ^a  

^a UNIVERSITY OF BONN   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d CENTER OF ADVANCED EUROPEAN STUDIES AND RESEARCH CAESAR   (Germany)

^e JACOBS UNIVERSITY BREMEN   (Germany)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOTYPES; CLASS II; CRITICAL SEQUENCE; HETERODIMERS; HUMAN LEUKOCYTE ANTIGEN; HUMAN SPECIES; INVARIANT CHAIN;

BIOCHEMISTRY;

BIOLOGY;

CARBOHYDRATE; GLYCINE; HETERODIMER; HLA ANTIGEN CLASS 2; HLA DP ANTIGEN; LYSINE; METHIONINE; PROLINE;

AFRICA SOUTH OF THE SAHARA; ALLELE; AMINO ACID SEQUENCE; ANTIGEN BINDING; ARTICLE; CRYSTAL STRUCTURE; GENE SEQUENCE; GENE STRUCTURE; HOMO NEANDERTHALENSIS; HUMAN; HUMAN CELL; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN POLYMORPHISM; X RAY CRYSTALLOGRAPHY;

ANTIGEN PRESENTATION; HLA CLASS II; INVARIANT CHAIN; MAJOR HISTOCOMPATIBILITY COMPLEX (MHC); PROTEIN ASSEMBLY; PROTEIN DOMAINS; PROTEIN EVOLUTION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; EVOLUTION, MOLECULAR; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-DP ALPHA-CHAINS; HLA-DP ANTIGENS; HLA-DP BETA-CHAINS; HLA-DR ALPHA-CHAINS; HLA-DR ANTIGENS; HLA-DR BETA-CHAINS; HUMANS; IMMUNOBLOTTING; MODELS, MOLECULAR; MUTATION; NEANDERTHALS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84891954729     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.515767     Document Type: Article

References (54)

1. Koch, N., McLellan, A. D., and Neumann, J. (2007) A revised model for invariant chain-mediated assembly of major histocompatibility complex class II assembly and isotype pairing. TiBS 32, 532-537
2. Bikoff, E. K., Germain, R. N., and Robertson, E. J. (1995) Allelic differences affecting invariant chain dependency of MHC class II subunit assembly. Immunity 2, 301-310
3. Lechler, R. I., Sant, A. J., Braunstein, N. S., Sekaly, R., Long, E., and Germain, R. N. (1990) Cell surface expression of hybrid murine/humanMHC class II-dimers. Key influence of residues in the amino-terminal portion of the-1 domain. J. Immunol. 144, 329-333
4. Anderson, M. S., and Miller, J. (1992) Invariant chain can function as a chaperone protein for class II major histocompatibility complex molecules. Proc. Natl. Acad. Sci. U.S.A. 89, 2282-2286
5. Layet, C., and Germain, R. N. (1991) Invariant chain promotes egress of poorly expressed, haplotype-mismatched class II major histocompatibility complex A-A-dimers from the endoplasmic reticulum/cis-Golgi compartment. Proc. Natl. Acad. Sci. U.S.A. 88, 2346-2350
6. Bikoff, E. K., Huang, L. Y., Episkopou, V., van Meerwijk, J., Germain, R. N., and Robertson, E. J. (1993) Defective major histocompatibility complex class II assembly, transport, peptide acquisition, and CD4-T cell selection in mice lacking invariant chain expression. J. Exp. Med. 177, 1699-1712
7. Neumann, J., and Koch, N. (2006) A novel domain on HLA-DR-chain regulates the chaperon role of invariant chain. J. Cell Sci. 119, 4207-4214
8. Koch, N., Zacharias, M., König, A., Temme, S., Neumann, J., and Springer, S. (2011) Stoichiometry of HLA Class II-invariant chain oligomers. PLoS ONE 6, e17257
9. Malissen, B., Shastri, N., Pierres, M., and Hood, L. (1986) Cotransfer of the Ed-and Ad-genes into L cells results in the surface expression of a functional mixed-isotype Ia molecule. Proc. Natl. Acad. Sci. U.S.A. 83, 3958-3962
10. Germain, R. N., and Quill, H. (1986) Unexpected expression of a unique mixed-isotype class II MHC molecule by transfected L-cells. Nature 320, 72-75
11. Lotteau, V., Teyton, L., Burroughs, D., and Charron, D. (1987) A novel HLA class II molecule (DR-DQ-) created by mismatched isotype pairing. Nature 329, 339-341
12. Spencer, J. S., and Kubo, R. T. (1989) Mixed isotype Class II antigen expression. J. Exp. Med. 169, 625-640
13. Ruberti, G., Sellins, K. S., Hill, C. M., Germain, R. N., Fathman, C. G., and Livingstone, A. (1992) Presentation of antigen by mixed isotype class II molecules in normal H-2d mice. J. Exp. Med. 175, 157-162
14. Silk, J. D., Schoendorf, D., Bartok, I., Chai, J. G., Gray, D., Simpson, E., and Dyson, J. (2005) Mixed-haplotype MHC class II molecules select functional CD4-T cells. Mol. Immunol. 42, 1129-1139
15. Stern, L. J., Brown, J. H., Jardetzky, T. S., Gorga, J. C., Urban, R. G., Strominger, J. L., and Wiley, D. C. (1994) Crystal structure of the human class IIMHCprotein Hla-DR1 complexes with an influenza virus peptide. Nature 368, 215-221
16. Ghosh, P., Amaya, M., Mellins E., and Wiley, D. C. (1995) The structure of an intermediate in class II MHC maturation. CLIP bound to HLA-DR3. Nature 378, 457-462
17. Braunstein, N. S., and Germain, R. N. (1987) Allele-specific control of Ii molecule surface expression and conformation. Implications for a general model of Ii structure-function relationship. Proc. Natl. Acad. Sci. U.S.A. 84, 2921-2925
18. Murthy, V. L., and Stern, L. J. (1997) The class II MHC protein HLA-DR1 in complex with an endogenous peptide. Implications for the structural basis of the specificity of peptide binding. Structure 5, 1385-1396
19. Grüneberg, U., Rich, T., Roucard, C., Marieke van Ham, S., Charron, D., and Trowsdale, J. (1997) Two widely used anti DR-monoclonal antibodies bind to an intracellular C-terminal epitope. Hum. Immunol. 53, 34-38
20. Koch, S., Schultz, A., and Koch, N. (1987) The production of recombinant HLA-DR-and invariant chain polypeptides by cDNA expression in E. coli. J. Immunol. Methods 103, 211-220
21. Adams, T. E., Bodmer, J. G., and Bodmer, W. F. (1983) Production and characterization of monoclonal antibodies recognizing the-chain subunits of human Ia alloantigens. Immunology 50, 613-624
22. Pesando, J. M., and Graf, L. (1986) Differential expression of HLA-DR,-DQ, and-DP antigens on malignant B cells. J. Immunol. 136, 4311-4318
23. Charron, D. J., Engelman, E. G., Benike, C. J., and McDevitt, H. O. (1980) Ia antigens on alloreactiveTcells in man detected by monoclonal antibodies. Evidence for synthesis of HLA-D/DR molecules of the responder type. J. Exp. Med. 152, 127s-136s
24. Temponi, M., Kekish, U., Hamby, C. V., Nielsen, H., Marboe, C. C., and Ferrone, S. (1993) Characterization of anti-HLA class II monoclonal antibody LGII-612.14. J. Immunol. Methods 161, 239-256
25. Lampson, L. A., and Levy, R. (1980) Two populations of Ia-like molecules on a human B cell line. J. Immunol. 125, 293-299
26. Wraight, C. J., van Endert, P., Möller, P., Lipp, J., Ling, N. R., MacLennan, I. C., Koch, N., and Moldenhauer, G. (1990) Human major histocompatibility complex class II invariant chain is expressed on the cell surface. J. Biol. Chem. 265, 5787-5792
27. Neumann, J., and Koch, N. (2005) Assembly of major histocompatibility complex class II subunits with invariant chain. FEBS Lett. 579, 6055-6059
28. Nagaraj, S., Neumann, J., Winzen, B., Frank, S., Ziske, C., Sievers, E., Koch, N., and Schmidt-Wolf, I. G. (2008) Pancreas carcinoma antigen fused to invariant chain elicits T cell response and tumor growth inhibition. Pancreas 37, 321-327
29. Neumann, J. (2005) Novel antibody tags from the rat lysosomal protein RT1.DM for immunodetection of recombinant proteins. J. Immunol. Methods 301, 66-76
30. Marks, M. S., Germain, R. N., and Bonifacino, J. S. (1995) Transient aggregation of major histocompatibility complex class II chains during assembly in normal spleen cells. J. Biol. Chem. 270, 10475-10481
31. Schaiff, W. T., Hruska, K. A., Jr., Bono, C., Shuman, S., and Schwartz, B. D. (1991) Invariant chain influences post-translational processing of HLA-DR molecules. J. Immunol. 147, 603-608
32. Sant, A. J., and Germain, R. N. (1989) Intracellular competition for component chains determines class II MHC cell surface phenotype. Cell 57, 797-805
33. Denzin, L. K., Hammond, C., and Cresswell, P. (1996) HLA-DM interactions with intermediates in HLA-DR maturation and a role for HLA-DM in stabilizing empty HLA-DR molecules. J. Exp. Med. 184, 2153-2165
34. Sanderson, F., Thomas, C., Neefjes, J., and Trowsdale, J. (1996) Association between HLA-DM and HLA-DR in vivo. Immunity 4, 87-96
35. Sato, A. K., Zarutskie, J. A., Rushe, M. M., Lomakin, A., Natarajan, S. K., Sadegh-Nasseri, S., Benedek, G. B., and Stern, L. J. (2000) Determinants of the peptide-induced conformational change in the human class II major histocompatibility complex protein HLA-DR1. J. Biol. Chem. 275, 2165-2173
36. Shackelford, D. A., and Strominger, J. L. (1983) Analysis of the oligosaccharides on the HLA-DR and DC1 B cell antigens. J. Immunol. 130, 274-282
37. Dai, S., Murphy, G. A., Crawford, F., Mack, D. G., Falta, M. T., Marrack, P., Kappler, J. W., and Fontenot, A. P. (2010) Crystal structure of HLA-DP2 and implications for chronic beryllium disease. Proc. Natl. Acad. Sci. U.S.A. 107, 7425-7430
38. Lancaster, A. K., Single, R. M., Solberg, O. D., Nelson, M. P., and Thomson, G. (2007) "PyPop update. A software pipeline for large-scale multilocus population genomics" Tissue Antigens 69, 192-197
39. Lancaster, A., Nelson, M. P., Single, R. M., Meyer, D., and Thomson, G. (2003) in Pacific Symposium on Biocomputing (Altman, R. B., Dunker, A. K., Hunter, L., Jung, T. A., and Klein, T. E., eds) Vol. 8, pp. 514-525, World Scientific, Singapore
40. Germain, R. N., and Rinker, A. G., Jr. (1993) Peptide binding inhibits protein aggregation of invariant-chain free class II dimers and promotes surface expression of occupied molecules. Nature 363, 725-728
41. Sant, A. J., Hendrix, L. R., Coligan, J. E., Maloy, W. L., and Germain, R. N. (1991) Defective intracellular transport as a common mechanism limiting expression of inappropriately paired class II major histocompatibility complex-/-chains. J. Exp. Med. 174, 799-808
42. Yaneva, R., Springer, S., and Zacharias, M. (2009) Flexibility of the MHC class II peptide binding cleft in the bound, partially filled, and empty states. A molecular dynamics simulation study. Biopolymers 91, 14-27
43. Sanderson, S., Frauwirth, K., and Shastri, N. (1995) Expression of endogenous peptide-major histocompatibility complex class II complexes derived from invariant chain-antigen fusion proteins. Proc. Natl. Acad. Sci. U.S.A. 92, 7217-7221
44. Koch, N., van Driel, I. R., and Gleeson, P. A. (2000) Highjacking a chaperone. Manipulation of the MHC class II presentation pathway. Immunol. Today 21, 546-550
45. Norcross, M. A., Raghupathy, R., Strominger, J., and Germain, R. N. (1986) Transfected human B lymphoblastoid cells express the mouse Ad-chain in association with DR-. J. Immunol. 137, 1714-1717
46. Karp, D. R., Teletski, C. L., Jaraquemada, D., Maloy, W. L., Coligan, J. E., and Long, E. O. (1990) Structural requirements for pairing of-and-chains in HLA-DR and HLA-DP molecules. J. Exp. Med. 171, 615-628
47. Buerstedde, J.-M., Pease, L. R., Nilson, A. E., Bell, M. P., Chase, C., Buerstedde, G., and McKean, D. J. (1988) Regulation of murine MHC class II molecule expression. J. Exp. Med. 168, 823-837
48. Gupta, S., Höpner, S., Rupp, B., Günther, S., Dickhaut, K., Agarwal, N., Cardoso, M. C., Kühne, R., Wiesmüller, K.-H., Jung, G., Falk K., and Rötzschke, O. (2008) Anchor side chains of short peptide fragments trigger ligand-exchange of class II MHC molecules. PLoS ONE 3, e1814
49. Natarajan, S. K., Stern, L. J., and Sadegh-Nasseri, S. (1999) Sodium dodecyl sulphate stability of HLA-DR1 complexes correlates with burial of hydrophobic residues in pocket 1. J. Immunol. 162, 3463-3470
50. Sidney, J., Steen, A., Moore, C., Ngo, S., Chung, J., Peters, B., and Sette, A. (2010) Five HLA-DP molecules frequently expressed in the worldwide human population share a common HLA supertypic binding specificity. J. Immunol. 184, 2492-2503
51. Arroyo, J., Alvarez, A. M., Nombela, C., and Sánchez-Pérez, M. (1995) The role of HLA-DP-residue 69 in the definition of antibody-binding epitope. Hum. Immunol. 43, 219-226
52. Díaz, G., Amicosante, M., Jaraquemada, D., Butler, R. H., Guillén, M. V., Sánchez, M., Nombela, C., and Arroyo, J. (2003) Functional analysis of HLA-DP polymorphism.Acrucial role of DP-residues 9, 11, 35, 55, 56, 69 and 84-87 in T cell allorecognition and peptide binding. Int. Immunol. 15, 565-576
53. Abi-Rached, L., Jobin, M. J., Kulkarni, S., McWhinnie, A., Dalva, K., Gragert, L., Babrzadeh, F., Gharizadeh, B., Luo, M., Plummer, F. A., Kimani, J., Carrington, M., Middleton, D., Rajalingam, R., Beksac, M., Marsh, S. G., Maiers, M., Guethlein, L. A., Tavoularis, S., Little, A. M., Green, R. E., Norman, P. J., and Parham, P. (2011) The shaping of modern immune systems by multiregional admixture with archaic humans. Science 334, 89-94
54. DeLano, W. L. (2002) The PyMOL Molecular Graphics System DeLano Scientific, San Carlos, CA