The β2-microglobulin-free heterodimerization of rhesus monkey MHC class I A with its normally spliced variant reduces the ubiquitin-dependent degradation of MHC class I A

Journal of Immunology

Volumn 188, Issue 5, 2012, Pages 2285-2296

  Dai, Zheng Xi ^a,b   Zhang, Gao Hong ^a   Zhang, Xi He ^a,b   Xia, Hou Jun ^a,b   Li, Shao You ^a,b   Zheng, Yong Tang ^a  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 MICROGLOBULIN; CYCLOHEXIMIDE; GLYCOPROTEIN; GLYCOSIDASE; HLA A ANTIGEN; NATURAL KILLER CELL RECEPTOR; T LYMPHOCYTE RECEPTOR; UBIQUITIN;

ANIMAL CELL; ARTICLE; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; DISULFIDE BOND; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; PROTEIN TRANSPORT; REGULATORY MECHANISM; RHESUS MONKEY; UBIQUITINATION;

ALTERNATIVE SPLICING; ANIMALS; BETA 2-MICROGLOBULIN; DISULFIDES; DOWN-REGULATION; GLYCOPROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; K562 CELLS; MACACA MULATTA; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE DELETION; TRANSFECTION; UBIQUITIN;

EID: 84863121827     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100665     Document Type: Article

References (54)

1. Antoniou, A. N., S. J. Powis, and T. Elliott. 2003. Assembly and export of MHC class I peptide ligands. Curr. Opin. Immunol. 15: 75-81. (Pubitemid 35454196)
2. Rock, K. L., and A. L. Goldberg. 1999. Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 17: 739-779. (Pubitemid 29241139)
3. Trinchieri, G. 1989. Biology of natural killer cells. Adv. Immunol. 47: 187-376. (Pubitemid 20010960)
4. López-Botet, M., and T. Bellón. 1999. Natural killer cell activation and inhibition by receptors for MHC class I. Curr. Opin. Immunol. 11: 301-307. (Pubitemid 29263958)
5. Bryceson, Y. T., and E. O. Long. 2008. Line of attack: NK cell specificity and integration of signals. Curr. Opin. Immunol. 20: 344-352.
6. Diedrich, G., N. Bangia, M. Pan, and P. Cresswell. 2001. A role for calnexin in the assembly of the MHC class I loading complex in the endoplasmic reticulum. J. Immunol. 166: 1703-1709. (Pubitemid 32114653)
7. Gao, B., R. Adhikari, M. Howarth, K. Nakamura, M. C. Gold, A. B. Hill, R. Knee, M. Michalak, and T. Elliott. 2002. Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 16: 99-109. (Pubitemid 34143220)
8. Pamer, E., and P. Cresswell. 1998. Mechanisms of MHC class I-restricted antigen processing. Annu. Rev. Immunol. 16: 323-358. (Pubitemid 28183368)
9. Schnabl, E., H. Stockinger, O. Majdic, H. Gaugitsch, I. J. Lindley, D. Maurer, A. Hajek-Rosenmayr, and W. Knapp. 1990. Activated human T lymphocytes express MHC class I heavy chains not associated with beta 2-microglobulin. J. Exp. Med. 171: 1431-1442. (Pubitemid 20167541)
10. Martayan, A., M. Fiscella, A. Setini, G. Ciccarelli, R. Gambari, G. Feriotto, A. Beretta, A. G. Siccardi, E. Appella, and P. Giacomini. 1997. Conformation and surface expression of free HLA-CW1 heavy chains in the absence of beta 2- microglobulin. Hum. Immunol. 53: 23-33. (Pubitemid 27175991)
11. Demaria, S., R. Schwab, and Y. Bushkin. 1992. The origin and fate of beta 2mfree MHC class I molecules induced on activated T cells. Cell. Immunol. 142: 103-113.
12. Goodridge, J. P., A. Burian, N. Lee, and D. E. Geraghty. 2010. HLA-F complex without peptide binds to MHC class I protein in the open conformer form. J. Immunol. 184: 6199-6208.
13. Santos, S. G., S. J. Powis, and F. A. Arosa. 2004. Misfolding of major histocompatibility complex class I molecules in activated T cells allows cisinteractions with receptors and signaling molecules and is associated with tyrosine phosphorylation. J. Biol. Chem. 279: 53062-53070. (Pubitemid 40051806)
14. Triantafilou, K., M. Triantafilou, K. M. Wilson, and N. Fernandez. 2000. Human major histocompatibility molecules have the intrinsic ability to form homotypic associations. Hum. Immunol. 61: 585-598. (Pubitemid 30346485)
15. Capps, G. G., B. E. Robinson, K. D. Lewis, and M. C. Zúñiga. 1993. In vivo dimeric association of class I MHC heavy chains. Possible relationship to class I MHC heavy chain-b 2-microglobulin dissociation. J. Immunol. 151: 159-169. (Pubitemid 23206981)
16. Arosa, F. A., S. G. Santos, and S. J. Powis. 2007. Open conformers: the hidden face of MHC-I molecules. Trends Immunol. 28: 115-123. (Pubitemid 46283689)
17. Boyson, J. E., R. Erskine, M. C. Whitman, M. Chiu, J. M. Lau, L. A. Koopman, M. M. Valter, P. Angelisova, V. Horejsi, and J. L. Strominger. 2002. Disulfide bond-mediated dimerization of HLA-G on the cell surface. Proc. Natl. Acad. Sci. USA 99: 16180-16185. (Pubitemid 35462769)
18. Shiroishi, M., K. Kuroki, T. Ose, L. Rasubala, I. Shiratori, H. Arase, K. Tsumoto, I. Kumagai, D. Kohda, and K. Maenaka. 2006. Efficient leukocyte Ig-like receptor signaling and crystal structure of disulfide-linked HLA-G dimer. J. Biol. Chem. 281: 10439-10447. (Pubitemid 43864583)
19. Allen, R. L., C. A. O'Callaghan, A. J. McMichael, and P. Bowness. 1999. Cutting edge: HLA-B27 can form a novel beta 2-microglobulin-free heavy chain homodimer structure. J. Immunol. 162: 5045-5048. (Pubitemid 29307101)
20. Kollnberger, S., and P. Bowness. 2009. The role of B27 heavy chain dimer immune receptor interactions in spondyloarthritis. Adv. Exp. Med. Biol. 649: 277-285.
21. Raine, T., and R. Allen. 2005. MHC-I recognition by receptors on myelomonocytic cells: new tricks for old dogs? Bioessays 27: 542-550. (Pubitemid 40780857)
22. Lynch, S., S. G. Santos, E. C. Campbell, A. M. Nimmo, C. Botting, A. Prescott, A. N. Antoniou, and S. J. Powis. 2009. Novel MHC class I structures on exosomes. J. Immunol. 183: 1884-1891.
23. Benoit, L. A., J. Shannon, J. W. Chamberlain, and R. G. Miller. 2005. Influence of xenogeneic beta2-microglobulin on functional recognition of H-2Kb by the NK cell inhibitory receptor Ly49C. J. Immunol. 175: 3542-3553. (Pubitemid 41292012)
24. Gonen-Gross, T., H. Achdout, T. I. Arnon, R. Gazit, N. Stern, V. Horejsí, D. Goldman-Wohl, S. Yagel, and O. Mandelboim. 2005. The CD85J/leukocyte inhibitory receptor-1 distinguishes between conformed and beta 2- microglobulin-free HLA-G molecules. J. Immunol. 175: 4866-4874. (Pubitemid 41456368)
25. Abu-hadid, M. M., H. Fuji, and A. K. Sood. 1994. Alternatively spliced MHC class I mRNAs show specific deletion of sequences encoding the extracellular polymorphic domains. Int. Immunol. 6: 323-337. (Pubitemid 24055111)
26. Tabaczewski, P., H. Shirwan, K. Lewis, and I. Stroynowski. 1994. Alternative splicing of class Ib major histocompatibility complex transcripts in vivo leads to the expression of soluble Qa-2 molecules in murine blood. Proc. Natl. Acad. Sci. USA 91: 1883-1887. (Pubitemid 24080310)
27. Norgaard, L., L. Fugger, H. O. Madsen, and A. Svejgaard. 1999. Identification of 4 different alternatively spliced HLA-A transcripts. Tissue Antigens 54: 370-378. (Pubitemid 29484278)
28. Malissen, M., B. Malissen, and B. R. Jordan. 1982. Exon/intron organization and complete nucleotide sequence of an HLA gene. Proc. Natl. Acad. Sci. USA 79: 893-897. (Pubitemid 12160328)
29. Krangel, M. S. 1986. Secretion of HLA-A and -B antigens via an alternative RNA splicing pathway. J. Exp. Med. 163: 1173-1190. (Pubitemid 16000416)
30. Wang, Z., F. M. Marincola, L. Rivoltini, G. Parmiani, and S. Ferrone. 1999. Selective histocompatibility leukocyte antigen (HLA)-A2 loss caused by aberrant pre-mRNA splicing in 624MEL28 melanoma cells. J. Exp. Med. 190: 205-215. (Pubitemid 29354914)
31. Paul, P., F. A. Cabestre, E. C. Ibrahim, S. Lefebvre, I. Khalil-Daher, G. Vazeux, R. M. Quiles, F. Bermond, J. Dausset, and E. D. Carosella. 2000. Identification of HLA-G7 as a new splice variant of the HLA-G mRNA and expression of soluble HLA-G5, -G6, and -G7 transcripts in human transfected cells. Hum. Immunol. 61: 1138-1149. (Pubitemid 32043892)
32. Ellis, S. A., K. A. Braem, and W. I. Morrison. 1992. Transmembrane and cytoplasmic domain sequences demonstrate at least two expressed bovine MHC class I loci. Immunogenetics 37: 49-56.
33. Ryan, A. F., R. L. Grendell, D. E. Geraghty, and T. G. Golos. 2002. A soluble isoform of the rhesus monkey nonclassical MHC class I molecule Mamu-AG is expressed in the placenta and the testis. J. Immunol. 169: 673-683. (Pubitemid 34753422)
34. Delgado-Cañedo, A., D. G. Santos, J. A. Chies, K. Kvitko, and N. B. Nardi. 2006. Optimization of an electroporation protocol using the K562 cell line as a model: role of cell cycle phase and cytoplasmic DNAses. Cytotechnology 51: 141-148. (Pubitemid 44875818)
35. Bartee, E., M. Mansouri, B. T. Hovey Nerenberg, K. Gouveia, and K. Früh. 2004. Downregulation of major histocompatibility complex class I by human ubiquitin ligases related to viral immune evasion proteins. J. Virol. 78: 1109-1120. (Pubitemid 38095821)
36. Boname, J. M., M. Thomas, H. R. Stagg, P. Xu, J. Peng, and P. J. Lehner. 2010. Efficient internalization of MHC I requires lysine-11 and lysine-63 mixed linkage polyubiquitin chains. Traffic 11: 210-220.
37. Lynch, K. W. 2004. Consequences of regulated pre-mRNA splicing in the immune system. Nat. Rev. Immunol. 4: 931-940. (Pubitemid 39620068)
38. Belicha-Villanueva, A., J. Blickwedehl, S. McEvoy, M. Golding, S. O. Gollnick, and N. Bangia. 2010. What is the role of alternate splicing in antigen presentation by major histocompatibility complex class I molecules? Immunol. Res. 46: 32-44.
39. Bresciani, A., G. Pirozz, M. Spera, M. Lombardi, L. Ambrosone, S. Migliaresi, S. Ferrone, and T. Manzo. 1998. Increased level of serum HLA class I antigens in patients with systemic lupus erythematosus. Correlation with disease activity. Tissue Antigens 52: 44-50. (Pubitemid 28327724)
40. Zavazava, N., H. Böttcher, and W. M. Ruchholtz. 1993. Soluble MHC class I antigens (sHLA) and anti-HLA antibodies in heart and kidney allograft recipients. Tissue Antigens 42: 20-26. (Pubitemid 23272643)
41. Puppo, F., M. Scudeletti, F. Indiveri, and S. Ferrone. 1995. Serum HLA class I antigens: markers and modulators of an immune response? Immunol. Today 16: 124-127.
42. King, D. W., E. Reed, and N. Suciu-Foca. 1989. Complexes of soluble HLA antigens and anti-HLA autoantibodies in human sera: possible role in maintenance of self-tolerance. Immunol. Res. 8: 249-262. (Pubitemid 19277873)
43. Ishitani, A., and D. E. Geraghty. 1992. Alternative splicing of HLA-G transcripts yields proteins with primary structures resembling both class I and class II antigens. Proc. Natl. Acad. Sci. USA 89: 3947-3951.
44. Riteau, B., N. Rouas-Freiss, C. Menier, P. Paul, J. Dausset, and E. D. Carosella. 2001. HLA-G2, -G3, and -G4 isoforms expressed as nonmature cell surface glycoproteins inhibit NK and antigen-specific CTL cytolysis. J. Immunol. 166: 5018-5026. (Pubitemid 32280714)
45. Rouas-Freiss, N., R. E. Marchal, M. Kirszenbaum, J. Dausset, and E. D. Carosella. 1997. The α1 domain of HLA-G1 and HLA-G2 inhibits cytotoxicity induced by natural killer cells: is HLA-G the public ligand for natural killer cell inhibitory receptors? Proc. Natl. Acad. Sci. USA 94: 5249-5254. (Pubitemid 27214769)
46. Morales, P. J., J. L. Pace, J. S. Platt, D. K. Langat, and J. S. Hunt. 2007. Synthesis of beta(2)-microglobulin-free, disulphide-linked HLA-G5 homodimers in human placental villous cytotrophoblast cells. Immunology 122: 179-188. (Pubitemid 47389946)
47. Kim, H. S., J. Garcia, M. Exley, K. W. Johnson, S. P. Balk, and R. S. Blumberg. 1999. Biochemical characterization of CD1d expression in the absence of beta2- microglobulin. J. Biol. Chem. 274: 9289-9295.
48. Duncan, L. M., S. Piper, R. B. Dodd, M. K. Saville, C. M. Sanderson, J. P. Luzio, and P. J. Lehner. 2006. Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J. 25: 1635-1645.
49. Boyson, J. E., C. Shufflebotham, L. F. Cadavid, J. A. Urvater, L. A. Knapp, A. L. Hughes, and D. I. Watkins. 1996. The MHC class I genes of the rhesus monkey. Different evolutionary histories of MHC class I and II genes in primates. J. Immunol. 156: 4656-4665. (Pubitemid 26174447)
50. Due, C., M. Simonsen, and L. Olsson. 1986. The major histocompatibility complex class I heavy chain as a structural subunit of the human cell membrane insulin receptor: implications for the range of biological functions of histocompatibility antigens. Proc. Natl. Acad. Sci. USA 83: 6007-6011. (Pubitemid 16000643)
51. Ramalingam, T. S., A. Chakrabarti, and M. Edidin. 1997. Interaction of class I human leukocyte antigen (HLA-I) molecules with insulin receptors and its effect on the insulin-signaling cascade. Mol. Biol. Cell 8: 2463-2474. (Pubitemid 27528214)
52. Doucey, M. A., L. Scarpellino, J. Zimmer, P. Guillaume, I. F. Luescher, C. Bron, and W. Held. 2004. Cis association of Ly49A with MHC class I restricts natural killer cell inhibition. Nat. Immunol. 5: 328-336. (Pubitemid 38332130)
53. Schreiber, A. B., J. Schlessinger, and M. Edidin. 1984. Interaction between major histocompatibility complex antigens and epidermal growth factor receptors on human cells. J. Cell Biol. 98: 725-731. (Pubitemid 14193307)
54. Apps, R., L. Gardner, A. M. Sharkey, N. Holmes, and A. Moffett. 2007. A homodimeric complex of HLA-G on normal trophoblast cells modulates antigen-presenting cells via LILRB1. Eur. J. Immunol. 37: 1924-1937. (Pubitemid 47065129)