HLA-E expression on porcine cells: Protection from human NK cytotoxicity depends on peptide loading

American Journal of Transplantation

Volumn 5, Issue 9, 2005, Pages 2085-2093

  Forte, Pietro ^a   Baumann, Bettina C ^a   Weiss, Elisabeth H ^b   Seebach, Jörg D ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Endothelial cells; HLA antigens; Natural killer cells; Xenotransplantation

Indexed keywords

GAMMA INTERFERON; HLA A2 ANTIGEN; HLA B7 ANTIGEN; HLA E ANTIGEN;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL CLONE; CELL PROTECTION; CELL SURFACE; CELL TYPE; CONTROLLED STUDY; CYTOTOXICITY; ENDOTHELIUM CELL; GENETIC TRANSFECTION; LYMPHOBLASTOID CELL; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SWINE;

ANIMALS; BONE MARROW CELLS; CELL LINE; CELL MEMBRANE; CYTOTOXICITY TESTS, IMMUNOLOGIC; CYTOTOXICITY, IMMUNOLOGIC; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; INTERFERON TYPE II; KILLER CELLS, NATURAL; LYSINE; PEPTIDES; SWINE; TRANSFECTION; TRANSGENES; TRANSPLANTATION, HETEROLOGOUS;

EID: 27844548079     PISSN: 16006135     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2005.00987.x     Document Type: Article

References (48)

1. Yokoyama WM, Kim S, French AR. The dynamic life of natural killer cells. Annu Rev Immunol 2004; 22: 405-429.
2. McQueen KL, Parham P. Variable receptors controlling activation and inhibition of NK cells. Curr Opin Immunol 2002; 14: 615-621.
3. Moretta L, Moretta A. Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J 2004; 23: 255-259.
4. Natarajan K, Dimasi N, Wang J, Mariuzza RA, Margulies DH. Structure and function of natural killer cell receptors: multiple molecular solutions to self, nonself discrimination. Annu Rev Immunol 2002; 20: 853-885.
5. Ljunggren HG, Karre K. In search of the 'missing self: MHC molecules and NK cell recognition. Immunol Today 1990; 11: 237-244.
6. Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. 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 1998; 187: 813-818.
7. Lee N, Llano M, Carretero M et al. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci U S A 1998; 95: 5199-5204.
8. Marin R, Ruiz-Cabello F, Pedrinaci S et al. Analysis of HLA-E expression in human tumors. Immunogenetics 2003; 54: 767-775.
9. Wei XH, Orr HT. Differential expression of HLA-E, HLA-F, and HLA-G transcripts in human tissue. Hum Immunol 1990; 29: 131-142.
10. Strong RK, Holmes MA, Li P, Braun L, Lee N, Geraghty DE. HLA-E allelic variants. Correlating differential expression, peptide affinities, crystal structures, and thermal stabilities. J Biol Chem 2003; 278: 5082-5090.
11. Ulbrecht M, Couturier A, Martinozzi S et al. Cell surface expression of HLA-E: interaction with human beta2-microglobulin and allelic differences. Eur J Immunol 1999; 29: 537-547.
12. Michaelsson J, Teixeira dM, Achour A, Lanier LL, Karre K, Soderstrom K. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J Exp Med 2002; 196: 1403-1414.
13. Tomasec P, Braud VM, Rickards C et al. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 2000; 287: 1031.
14. Ulbrecht M, Martinozzi S, Grzeschik M et al. Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J Immunol 2000; 164: 5019-5022.
15. Miller JD, Weber DA, Ibegbu C, Pohl J, Altman JD, Jensen PE. Analysis of HLA-E peptide-binding specificity and contact residues in bound peptide required for recognition by CD94/NKG2. J Immunol 2003; 171: 1369-1375.
16. Maier S, Grzeschik M, Weiss EH, Ulbrecht M. Implications of HLA-E allele expression and different HLA-E ligand diversity for the regulation of NK cells. Hum Immunol 2000; 61: 1059-1065.
17. Vales-Gomez M, Reyburn HT, Erskine RA, Lopez-Botet M, Strominger JL. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J 1999; 18: 4250-4260.
18. Lopez-Botet M, Llano M, Navarro F, Bellon T. NK cell recognition of non-classical HLA class I molecules. Semin Immunol 2000; 12: 109-119.
19. Llano M, Lee N, Navarro F et al. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur J Immunol 1998; 28: 2854-2863.
20. Lin Y, Vandeputte M, Waer M. Natural killer cell-and macrophage-mediated rejection of concordant xenografts in the absence of T and B cell responses. J Immunol 1997; 158: 5658-5667.
21. Xia G, Ji P, Rutgeerts O, Waer M. Natural killer cell- and macrophage mediated discordant guinea pig->rat xenograft rejection in the absence of complement, xenoantibody and T cell immunity. Transplantation 2000; 70: 86-93.
22. Khalfoun B, Barrat D, Watier H et al. Development of an ex vivo model of pig kidney perfused with human lymphocytes. Analysis of xenogeneic cellular reactions. Surgery 2000; 128: 447-457.
23. Kirk AD, Heinle JS, Mault JR, Sanfilippo F. Ex vivo characterization of human anti-porcine hyperacute cardiac rejection. Transplantation 1993; 56: 785-793.
24. Quan D, Bravery C, Chavez G et al. Identification, detection, and in vitro characterization of cynomolgus monkey natural killer cells in delayed xenograft rejection of hDAF transgenic porcine renal xenografts. Transplant Proc 2000; 32: 936-937.
25. Itescu S, Kwiatkowski P, Artrip JH et al. Role of natural killer cells, macrophages, and accessory molecule interactions in the rejection of pig-to-primate xenografts beyond the hyperacute period. Hum Immunol 1998; 59: 275-286.
26. Xu H, Gundry SR, Hancock WW et al. Prolonged discordant xenograft survival and delayed xenograft rejection in a pig-to-baboon orthotopic cardiac xenograft model. J Thorac Cardiovasc Surg 1998; 115: 1342-1349.
27. Forte P, Matter-Reissmann UB, Strasser M, Schneider MK, Seebach JD. Porcine aortic endothelial cells transfected with HLA-G are partially protected from xenogeneic human NK cytotoxicity. Hum Immunol 2000; 61: 1066-1073.
28. Forte P, Pazmany L, Matter-Reissmann UB, Stussi G, Schneider MK, Seebach JD. HLA-G inhibits rolling adhesion of activated human nk cells on porcine endothelial cells. J Immunol 2001; 167: 6002-6008.
29. Seebach JD, Comrack C, Germana S, LeGuern C, Sachs DH, Der-Simonian H. HLA-Cw3 expression on porcine endothelial cells protects against xenogeneic cytotoxicity mediated by a subset of human NK cells. J Immunol 1997; 159: 3655-3661.
30. Sharland A, Patel A, Lee JH, Cestra AE, Saidman S, Waneck GL. Genetically modified HLA class I molecules able to inhibit human NK cells without provoking alloreactive CD8+ CTLs. J Immunol 2002; 168: 3266-3274.
31. Sharland A, Lee JH, Saidman S, Waneck GL. CD8-interaction mutant HLA-Cw3 molecules protect porcine cells from human natural killer cell-mediated antibody-dependent cellular cytotoxicity without stimulating cytotoxic T lymphocytes. Transplantation 2003; 76: 1615-1622.
32. Matsunami K, Miyagawa S, Nakai R, Yamada M, Shirakura R. Modulation of the leader peptide sequence of the HLA-E gene up-regulates its expression and down-regulates natural killer cell-mediated swine endothelial cell lysis. Transplantation 2002; 73: 1 582-1589.
33. Sasaki H, Xu XC, Mohanakumar T. HLA-E and HLA-G expression on porcine endothelial cells inhibit xenoreactive human NK cells through CD94/NKG2-dependent and -independent pathways. J Immunol 1999; 163: 6301-6305.
34. Seebach JD, Schneider MK, Comrack CA et al. Immortalized bone-marrow derived pig endothelial cells. Xenotransplantation 2001; 8: 48-61.
35. Huang CA, Fuchimoto Y, Gleit ZL et al. Posttransplantation lymphoproliferative disease in miniature swine after allogeneic hematopoietic cell transplantation: similarity to human PTLD and association with a porcine gammaherpesvirus. Blood 2001; 97: 1467-1473.
36. Lee N, Goodlett DR, Ishitani A, Marquardt H, Geraghty DE. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J Immunol 1998; 160: 4951-4960.
37. Ulbrecht M, Honka T, Person S, Johnson JP, Weiss EH. The HLA-E gene encodes two differentially regulated transcripts and a cell surface protein. J Immunol 1992; 149: 2945-2953.
38. Ladasky JJ, Shum BP, Canavez F, Seuanez HN, Parham P. Residue 3 of beta2-microglobulin affects binding of class I MHC molecules by the W6/32 antibody. Immunogenetics 1999; 49: 312-320.
39. Kwiatkowski P, Artrip JH, John R et al. Induction of swine major histocompatibility complex class I molecules on porcine endothelium by tumor necrosis factor-alpha reduces lysis by human natural killer cells. Transplantation 1999; 67: 211-218.
40. Crew MD, Cannon MJ, Phanavanh B, Garcia-Borges CN. An HLA-E single chain trimer inhibits human NK cell reactivity towards porcine cells. Mol Immunol 2005; 42: 1205-1214.
41. Shields MJ, Moffat LE, Ribaudo RK. Functional comparison of bovine, murine, and human beta2-microglobulin: interactions with murine MHC I molecules. Mol Immunol 1998; 35: 919-928.
42. Gustafson KS, Cinder GD. Interferon-gamma induction of the human leukocyte antigen-E gene is mediated through binding of a complex containing STAT1 alpha to a distinct interferon-gamma-responsive element. J Biol Chem 1996; 271: 20035-20046.
43. Ayalon O, Hughes EA, Cresswell P et al. Induction of transporter associated with antigen processing by Interferon gamma confers endothelial cell cytoprotection against natural killer-mediated lysis. Proc Natl Acad Sci U S A 1998; 95: 2435-2440.
44. Carreno BM, Hansen TH. Exogenous peptide ligand influences the expression and half-life of free HLA class I heavy chains ubiquitously detected at the cell surface. Eur J Immunol 1994; 24: 1285-1292.
45. Bland FA, Lemberg MK, McMichael AJ, Martoglio B, Braud VM. Requirement of the proteasome for the trimming of signal peptide-derived epitopes presented by the nonclassical major histocompatibility complex class I molecule HLA-E. J Biol Chem 2003; 278: 33747-33752.
46. Lemberg MK, Bland FA, Weihofen A, Braud VM, Martoglio B. Intramembrane proteolysis of signal peptides: an essential step in the generation of HLA-E epitopes. J Immunol 2001; 167: 6441-6446.
47. Ulbrecht M, Modrow S, Srivastava R, Peterson PA, Weiss EH. Interaction of HLA-E with peptides and the peptide transporter in vitro: implications for its function in antigen presentation. J Immunol 1998; 160: 4375-4385.
48. Yang YG. Application of xenogeneic stem cells for induction of transplantation tolerance: present state and future directions. Springer Semin Immunopathol 2004; 26: 187-200.