HLA-E: Strong association with β2-microglobulin and surface expression in the absence of HLA class I signal sequence-derived peptides

Journal of Immunology

Volumn 181, Issue 8, 2008, Pages 5442-5450

  Lo Monaco, Elisa ^a   Sibilio, Leonardo ^a   Melucci, Elisa ^a   Tremante, Elisa ^a   Suchànek, Miloslav ^b   Horejsi, Vaclav ^c   Martayan, Aline ^a   Giacomini, Patrizio ^a  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b EXBIO Praha   (Czech Republic)

^c Institute of Molecular Genetics   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BETA 2 MICROGLOBULIN; BIOTIN; ENDOGLYCOSIDASE H; GLYCOSIDASE; HLA A ANTIGEN; HLA ANTIGEN CLASS 1; HLA B ANTIGEN; HLA C ANTIGEN; HLA E ANTIGEN; HLA F ANTIGEN; HLA G ANTIGEN; LIGAND; MEM E/02 ANTIBODY; MEM E/07 ANTIBODY; MEM E/08 ANTIBODY; MONOCLONAL ANTIBODY; SIGNAL PEPTIDE; TAPASIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; HLA ANTIGEN; HLA-E ANTIGEN; PEPTIDE;

ALLELE; ANTIBODY SCREENING; ANTIGEN EXPRESSION; ARTICLE; ASSAY; B LYMPHOCYTE; CONFORMATION; CONTROLLED STUDY; FLOW CYTOMETRY; HLA SYSTEM; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; ISOELECTRIC FOCUSING; LYMPHOID CELL; PRIORITY JOURNAL; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LYMPHOCYTE; PROTEIN FOLDING;

ALLELES; BETA 2-MICROGLOBULIN; CELL LINE; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; LIGANDS; LYMPHOCYTES; MEMBRANE TRANSPORT PROTEINS; PEPTIDES; PROTEIN FOLDING;

EID: 54049151957     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.8.5442     Document Type: Article

References (47)

1. Braud, V. M., E. Y. Jones, and A. McMichael. 1997. The human major histocompatibility complex class Ib molecule HLA-E binds signal sequence-derived peptides with primary anchor residues at positions 2 and 9. Eur. J. Immunol. 27: 1164-1169.
2. Braud, V. M., D. S. J. Allan, C. A. O'Callaghan, K. Söderström, A. D'Andrea, G. S. Ogg, S. Lazetic, N. T. Young, J. I. Bell, J. H. Phillips, et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391: 795-799. (Pubitemid 28099678)
3. Lee, N., D. R. Goodlett, A. Ishitani, H. Marquardt, and D. E. Geraghty. 1998. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J. Immunol. 160: 4951-4960. (Pubitemid 28215330)
4. Grimsley, C., A. Kawasaki, C. Gassner, N. Sageshima, Y. Nose, K. Hatake, D. E. Geraghty, and A. Ishitani. 2002. Definitive high resolution typing of HLA-E allelic polymorphisms: identifying potential errors in existing allele data. Tissue Antigens 60: 206-212. (Pubitemid 35398823)
5. 2m and allelic differences. Eur. J. Immunol. 29: 537-547.
6. Braud, V. M., D. S. J. Allan, D. Wilson, and A. J. McMichael. 1998. TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr. Biol. 8: 1-10. (Pubitemid 28056248)
7. Borrego, F., M. Ulbrecht, E. H. Weiss, J. E. Coligan, and A. G. Brooks. 1998. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J. Exp. Med. 187: 813-818. (Pubitemid 28115198)
8. Ulbrecht, M., S. Modrow, R. Srivastava, P. A. Peterson, and E. H. Weiss. 1998. Interaction of HLA-E with peptides and the peptide transporter in vitro: implications for its function in antigen presentation. J. Immunol. 160: 4375-4385. (Pubitemid 28217295)
9. Brooks, A. G., F. Borrego, P. E. Posch, A. Patamawenu, C. J. Scorzelli, M. Ulbrecht, E. H. Weiss, and J. E. Coligan. 1999. Specific recognition of HLA-E, but not classical, HLA class I molecules by soluble CD94/NKG2A and NK cells. J. Immunol. 162: 305-313.
10. O'Callaghan, C. A., J. Tormo, B. E. Willcox, V. M. Braud, B. K. Jakobsen, D. I. Stuart, A. J. McMichael, J. I. Bell, and E. Y. Jones. 1998. Structural features impose tight peptide binding specificity in the nonclassical MHC molecule HLA-E. Mol. Cell 1: 531-541.
11. Moretta, L., C. Romagnani, G. Pietra, A. Moretta, and M. C. Mingari. 2003. NK-CTLs, a novel HLA-E-restricted T-cell subset. Trends Immunol. 24: 136-143. (Pubitemid 36263098)
12. Kambayashi, T., J. Kraft-Leavy, J. Dauner, B. Sullivan, O. Laur, and P. Jensen. 2004. The nonclassical MHC class I molecule Qa-1 forms unstable peptide complexes. J. Immunol. 172: 1661-1669. (Pubitemid 38116814)
13. Stevens, J., E. Joly, J. Trowsdale, and G. W. Butcher. 2001. Peptide binding characteristics of the non-classical class Ib MHC molecule HLA-E assessed by a recombinant random peptide approach. BMC Immunol. 2: 5. (Pubitemid 38692905)
14. Ulbrecht, M., S. Martinozzi, M. Grzeschik, H. Hengel, J. W. Ellwart, M. Pla, and E. H. Weiss. 2000. The human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J. Immunol. 164: 5019-5022. (Pubitemid 30305172)
15. Tomasec, P., V. M. Braud, C. Rickards, M. B. Powell, B. P. McSharry, S. Gadola, V. Cerundolo, L. K. Borysiewicz, A. J. McMichael, and G. W. G. Wilkinson. 2000. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287: 1031-1033. (Pubitemid 30094357)
16. Michaelsson, J., C. Teixeira de Matos, A. Achour, L. L. Lanier, K. Kärre, and K. Soderstrom. 2005. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J. Exp. Med. 196: 1403-1414. (Pubitemid 35424935)
17. + CTLs by TCR Vβ-derived peptides bound to HLA-E. J. Immunol. 167: 3800-3808.
18. + T cells. J. Exp. Med. 196: 1473-1481.
19. Wooden, S., S. Kalb, R. Cotter, and M. Soloski. 2005. HLA-E binds a peptide derived from the ATP-binding cassette transporter multidrug resistance-associated protein 7 and inhibits NK cell-mediated lysis. J. Immunol. 175: 1383-1387. (Pubitemid 41023037)
20. + T cell subset in volunteers immunized with Salmonella enterica serovar Typhi strain Ty21a typhoid vaccine. J. Immunol. 173: 5852-5862.
21. Nattermann, J., H. D. Nischalke, V. Hofmeister, G. Ahlenstiel, H. Zimmermann, L. Leifeld, E. H. Weiss, T. Sauerbruch, and U. Spengler. 2005. The HLA-A2 restricted T cell epitope HCV core 35-44 stabilizes HLA-E expression and inhibits cytolysis mediated by natural killer cells. Am. J. Pathol. 166: 443-453. (Pubitemid 40189041)
22. Pietra, G., C. Romagnani, M. Falco, M. Vitale, R. Castriconi, D. Pende, E. Millo, S. Anfossi, R. Biassoni, L. Moretta, and M. C. Mingari. 2002. The analysis of the natural killer-like activity of human cytolytic T lymphocytes revealed HLA-E as a novel target for TCR α/β-mediated recognition. Eur. J. Immunol. 31: 3687-3693. (Pubitemid 34030982)
23. Lee, N., M. Llano, M. Carretero, A. Ishitani, F. Navarro, M. Lopez-Botet, and D. Geraghty. 1998. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 95: 5199-5204. (Pubitemid 28208575)
24. Llano, M., N. Lee, F. Navarro, P. García, J. P. Albar, D. E. Geraghty, and M. López-Botet. 1998. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur. J. Immunol. 28: 2854-2863.
25. 2-microglobulin but is TAP independent. J. Immunol. 160: 3217-3224.
26. Ulbrecht, M., V. Hofmeister, G. Yuksekdag, J. Ellwart, H. Hengel, F. Momburg, S. Martinozzi, M. Reboul, M. Pla, and E. Weiss. 2003. HCMV glycoprotein US6 mediated inhibition of TAP does not affect HLA-E dependent protection of K-562 cells from NK cell lysis. Hum. Immunol. 64: 231-237. (Pubitemid 36197351)
27. Pacasova, R., S. Martinozzi, H. Boulouis, Y. Szpak, M. Ulbrecht, F. Sigaux, E. Weiss, and M. Pla. 1999. Cell surface detection of HLA-E gene products with a specific monoclonal antibody. J. Reprod. Immunol. 43: 195-201.
28. Ishitani, A., N. Sageshima, N. Lee, N. Dorofeeva, K. Hatake, H. Marquardt, and D. Geraghty. 2003. Protein expression and peptide binding suggest unique and interacting functional roles for HLA-E, F, and G in maternal-placental immune recognition. J. Immunol. 171: 1376-1384. (Pubitemid 36900070)
29. Menier, C., B. Saez, V. Horejsi, S. Martinozzi, I. Krawice-Radanne, S. Bruel, C. Le Danff, M. Reboul, I. Hilgert, M. Rabreau, et al. 2003. Characterization of monoclonal antibodies recognizing HLA-G or HLA-E: new tools to analyze the expression of nonclassical HLA class I molecules. Hum. Immunol. 64: 315-326. (Pubitemid 36255272)
30. LeMaoult, J., M. Le Discorde, N. Rouas-Freiss, P. Moreau, C. Menier, J. McCluskey, and E. D. Carosella. 2003. Biology and functions of human leukocyte antigen-G in health and sickness. Tissue Antigens 62: 273-284. (Pubitemid 37204582)
31. Sibilio, L., A. Martayan, R. Fraioli, E. Lo Monaco, E. Melucci, M. Suchànek, and P. Giacomini. 2003. Biochemical characterization of monoclonal antibodies to HLA-E and HLA-G. Tissue Antigens 62: 356.
32. Coupel, S., A. Moreau, M. Hamidou, V. Horejsi, J. P. Soulillou, and B. Charreau. 2007. Expression and release of soluble HLA-E is an immunoregulatory feature of endothelial cell activation. Blood 109: 2806-2814. (Pubitemid 46482075)
33. Marin, R., F. Ruiz-Cabello, S. Pedrinaci, R. Mendez, P. Jimenez, D. E. Geraghty, and F. Garrido. 2003. Analysis of HLA-E expression in human tumors. Immunogenetics 54: 767-775. (Pubitemid 36384471)
34. Palmisano, G. L., E. Contardi, A. Morabito, V. Gargaglione, G. B. Ferrara, and M. P. Pistillo. 2005. HLA-E surface expression is independent of the availability of HLA class I signal sequence-derived peptides in human tumor cell lines. Hum. Immunol. 66: 1-12.
35. Derré, L., M. Corvaisier, B. Charreau, A. Moreau, E. Godefroy, A. Moreau- Aubry, F. Jotereau, and N. Gervois. 2006. Expression and release of HLA-E by melanoma cells and melanocytes: potential impact on the response of cytotoxic effector cells. J. Immunol. 177: 3100-3107. (Pubitemid 44277827)
36. Lee, N., A. R. Malacko, A. Ishitani, M. C. Chen, J. Bajorath, H. Marquardt, and D. E. Geraghty. 1995. The membrane-bound and soluble forms of HLA-G bind identical sets of endogenous peptides but differ with respect to TAP association. Immunity 3: 591-600.
37. 2-microglobulin. Hum. Immunol. 46: 69-81.
38. Sibilio, L., A. Martayan, A. Setini, R. Fraioli, D. Fruci, J. Shabanowitz, D. F. Hunt, and P. Giacomini. 2005. Impaired assembly results in the accumulation of multiple HLA-C heavy chain folding intermediates. J. Immunol. 175: 6651-6658. (Pubitemid 41598908)
39. Martayan, A., R. Fraioli, E. Giorda, A. Setini, G. Ciccarelli, L. Delfino, G. B. Ferrara, and P. Giacomini. 1999. Biosynthesis of HLA-C heavy chains in melanoma cells with multiple defects in the expression of HLA-A, -B, -C molecules. Br. J. Cancer 80: 639-649. (Pubitemid 29209824)
40. Steinle, A., and D. J. Schendel. 1994. HLA class I alleles of LCL 721 and 174 x CEM.T2 (T2). Tissue Antigens 44: 268-270. (Pubitemid 24310188)
41. Greenwood, R., Y. Shimizu, G. S. Sekhon, and R. DeMars. 1994. Novel allelespecific, post-translational reduction in HLA class I surface expression in a mutant human B cell line. J. Immunol. 153: 5525-5536. (Pubitemid 24377688)
42. Brodsky, F. M., P. Parham, C. J. Barnstable, M. J. Crumpton, and W. F. Bodmer. 1979. Monoclonal antibodies for analysis of the HLA system. Immunol. Rev. 47: 3-61.
43. 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 products. J. Immunol. 137: 2299-2306.
44. Wainwright, S. D., P. A. Biro, and C. H. Holmes. 2000. HLA-F is a predominantly empty, intracellular, TAP-associated MHC class Ib protein with a restricted expression pattern. J. Immunol. 164: 319-328.
45. Townsend, A., T. Elliott, V. Cerundolo, L. Foster, B. Barber, and A. Tse. 1990. Assembly of MHC class I molecules analyzed in vitro. Cell 62: 285-295. (Pubitemid 20233535)
46. 2m complex. Immunogenetics 53: 440-446.
47. Lee, N., and D. Geraghty. 2003. HLA-F surface expression on B cell and monocyte cell lines is partially independent from tapasin and completely independent from TAP. J. Immunol. 171: 5264-5271. (Pubitemid 37432811)