Synthetic HLA-G proteins for therapeutic use in transplantation

FASEB Journal

Volumn 27, Issue 9, 2013, Pages 3643-3651

  LeMaoult, Joel ^a,b   Daouya, Marina ^a,b   Wu, Juan ^c   Loustau, Maria ^a,b   Horuzsko, Anatolij ^c   Carosella, Edgardo D ^a,b  

^a DIF   (France)

^b UNIVERSITÉ PARIS DIDEROT   (France)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Engineered molecules; Immune regulation; Therapy; Tolerance

Indexed keywords

HLA G ANTIGEN; ILT 4 RECEPTOR; LILRB 1 RECEPTOR; LILRB 2 RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; MONOMER; POLYPEPTIDE; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; DIMERIZATION; DRUG RECEPTOR BINDING; GOOD MANUFACTURING PRACTICE; GRAFT SURVIVAL; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN SYNTHESIS; SKIN ALLOGRAFT; TRANSPLANTATION;

ENGINEERED MOLECULES; IMMUNE REGULATION; THERAPY; TOLERANCE;

ANIMALS; CELL LINE; CELL PROLIFERATION; FLOW CYTOMETRY; GRAFT SURVIVAL; HLA-G ANTIGENS; HUMANS; MICE; PEPTIDES; TRANSPLANTATION, HOMOLOGOUS;

EID: 84883364032     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-228247     Document Type: Article

References (49)

1. Kovats, S., Main, E. K., Librach, C., Stubblebine, M., Fisher, S. J., and DeMars, R. (1990) A class I antigen, HLA-G, expressed in human trophoblasts. Science 248, 220-223
2. Rouas-Freiss, N., Goncalves, R. M., Menier, C., Dausset, J., and Carosella, E. D. (1997) Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc. Natl. Acad. Sci. U. S. A. 94, 11520-11525
3. Mallet, V., Blaschitz, A., Crisa, L., Schmitt, C., Fournel, S., King, A., Loke, Y. W., Dohr, G., and Le Bouteiller, P. (1999) HLA-G in the human thymus: a subpopulation of medullary epithelial but not CD83(+) dendritic cells expresses HLA-G as a membranebound and soluble protein. Int. Immunol. 11, 889-898
4. Cirulli, V., Zalatan, J., McMaster, M., Prinsen, R., Salomon, D. R., Ricordi, C., Torbett, B. E., Meda, P., and Crisa, L. (2006) The class I HLA repertoire of pancreatic islets comprises the nonclassical class Ib antigen HLA-G. Diabetes 55, 1214-1222
5. Selmani, Z., Naji, A., Zidi, I., Favier, B., Gaiffe, E., Obert, L., Borg, C., Saas, P., Tiberghien, P., Rouas-Freiss, N., Carosella, E. D., and Deschaseaux, F. (2008) Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25highFOXP3+ regulatory T cells. Stem Cells 26, 212- 222
6. Verloes, A., Van de Velde, H., LeMaoult, J., Mateizel, I., Cauffman, G., Horn, P. A., Carosella, E. D., Devroey, P., De Waele, M., Rebmann, V., and Vercammen, M. (2011) HLA-G expression in human embryonic stem cells and preimplantation embryos. J. Immunol. 186, 2663-2671
7. Paul, P., Rouas-Freiss, N., Khalil-Daher, I., Moreau, P., Riteau, B., Le Gal, F. A., Avril, M. F., Dausset, J., Guillet, J. G., and Carosella, E. D. (1998) HLA-G expression in melanoma: a way for tumor cells to escape from immunosurveillance. Proc. Natl. Acad. Sci. U. S. A. 95, 4510-4515
8. Lila, N., Carpentier, A., Amrein, C., Khalil-Daher, I., Dausset, J., and Carosella, E. D. (2000) Implication of HLA-G molecule in heart-graft acceptance. Lancet 355, 2138
9. Aractingi, S., Briand, N., Le Danff, C., Viguier, M., Bachelez, H., Michel, L., Dubertret, L., and Carosella, E. D. (2001) HLA-G and NK receptor are expressed in psoriatic skin: a possible pathway for regulating infiltrating T cells? Am. J. Pathol. 159, 71-77
10. Lozano, J. M., Gonzalez, R., Kindelan, J. M., Rouas-Freiss, N., Caballos, R., Dausset, J., Carosella, E. D., and Pena, J. (2002) Monocytes and T lymphocytes in HIV-1-positive patients express HLA-G molecule. AIDS 16, 347-351
11. Carosella, E. D., Favier, B., Rouas-Freiss, N., Moreau, P., and Lemaoult, J. (2008) Beyond the increasing complexity of the immunomodulatory HLA-G molecule. Blood 111, 4862-4870
12. Rouas-Freiss, N., Marchal, R. E., Kirszenbaum, M., Dausset, J., and Carosella, E. D. (1997) The alpha1 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. U. S. A. 94, 5249-5254
13. Riteau, B., Rouas-Freiss, N., Menier, C., Paul, P., Dausset, J., and Carosella, E. D. (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
14. Rouas-Freiss, N., Khalil-Daher, I., Riteau, B., Menier, C., Paul, P., Dausset, J., and Carosella, E. D. (1999) The immunotolerance role of HLA-G. Seminars Cancer Biol. 9, 3-12
15. LeMaoult, J., Krawice-Radanne, I., Dausset, J., and Carosella, E. D. (2004) HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4+ T cells. Proc. Natl. Acad. Sci. U. S. A. 101, 7064-7069
16. Bahri, R., Hirsch, F., Josse, A., Rouas-Freiss, N., Bidere, N., Vasquez, A., Carosella, E. D., Charpentier, B., and Durrbach, A. (2006) Soluble HLA-G inhibits cell cycle progression in human alloreactive T lymphocytes. J. Immunol. 176, 1331-1339
17. Caumartin, J., Favier, B., Daouya, M., Guillard, C., Moreau, P., Carosella, E. D., and LeMaoult, J. (2007) Trogocytosis-based generation of suppressive NK cells. EMBO J. 26, 1423-1433
18. Ristich, V., Liang, S., Zhang, W., Wu, J., and Horuzsko, A. (2005) Tolerization of dendritic cells by HLA-G. Eur. J. Immunol. 35, 1133-1142
19. Liang, S., Ristich, V., Arase, H., Dausset, J., Carosella, E. D., and Horuzsko, A. (2008) Modulation of dendritic cell differentiation by HLA-G and ILT4 requires the IL-6-STAT3 signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 105, 8357-8362
20. Naji, A., Le Rond, S., Durrbach, A., Krawice-Radanne, I., Creput, C., Daouya, M., Caumartin, J., LeMaoult, J., Carosella, E. D., and Rouas-Freiss, N. (2007) CD3+CD4low and CD3+CD8low are induced by HLA-G: novel human peripheral blood suppressor T-cell subsets involved in transplant acceptance. Blood 110, 3936-3948
21. Gregori, S., Tomasoni, D., Pacciani, V., Scirpoli, M., Battaglia, M., Magnani, C. F., Hauben, E., and Roncarolo, M. G. (2010) Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood 116, 935-944
22. Agaugue, S., Carosella, E. D., and Rouas-Freiss, N. (2011) Role of HLA-G in tumor escape through expansion of myeloidderived suppressor cells and cytokinic balance in favor of Th2 versus Th1/Th17. Blood 117, 7021-7031
23. Carosella, E. D., Moreau, P., Lemaoult, J., and Rouas-Freiss, N. (2008) HLA-G: from biology to clinical benefits. Trends Immunol. 29, 125-132
24. Ibrahim, E. C., Aractingi, S., Allory, Y., Borrini, F., Dupuy, A., Duvillard, P., Carosella, E. D., Avril, M. F., and Paul, P. (2004) Analysis of HLA antigen expression in benign and malignant melanocytic lesions reveals that upregulation of HLA-G expression correlates with malignant transformation, high inflammatory infiltration and HLA-A1 genotype. Int. J. Cancer 108, 243-250
25. Ibrahim, E. C., Guerra, N., Lacombe, M. J., Angevin, E., Chouaib, S., Carosella, E. D., Caignard, A., and Paul, P. (2001) Tumor-specific up-regulation of the nonclassical class I HLA-G antigen expression in renal carcinoma. Cancer Res. 61, 6838- 6845
26. Urosevic, M., Kurrer, M. O., Kamarashev, J., Mueller, B., Weder, W., Burg, G., Stahel, R. A., Dummer, R., and Trojan, A. (2001) Human leukocyte antigen G up-regulation in lung cancer associates with high-grade histology, human leukocyte antigen class I loss and interleukin-10 production. Am. J. Pathol. 159, 817-824
27. Polakova, K., and Russ, G. (2000) Expression of the non-classical HLA-G antigen in tumor cell lines is extremely restricted. Neoplasma 47, 342-348
28. Davies, B., Hiby, S., Gardner, L., Loke, Y. W., and King, A. (2001) HLA-G expression by tumors. Am. J. Reprod. Immunol. 45, 103-107
29. Real, L. M., Cabrera, T., Collado, A., Jimenez, P., Garcia, A., Ruiz-Cabello, F., and Garrido, F. (1999) Expression of HLA G in human tumors is not a frequent event. Int. J. Cancer 81, 512-518
30. McMaster, M., Zhou, Y., Shorter, S., Kapasi, K., Geraghty, D., Lim, K. H., and Fisher, S. (1998) HLA-G isoforms produced by placental cytotrophoblasts and found in amniotic fluid are due to unusual glycosylation. J. Immunol. 160, 5922-5928
31. Lefebvre, S., Antoine, M., Uzan, S., McMaster, M., Dausset, J., Carosella, E. D., and Paul, P. (2002) Specific activation of the non-classical class I histocompatibility HLA-G antigen and expression of the ILT2 inhibitory receptor in human breast cancer. J. Pathol. 196, 266-274
32. Urosevic, M., Willers, J., Mueller, B., Kempf, W., Burg, G., and Dummer, R. (2002) HLA-G protein up-regulation in primary cutaneous lymphomas is associated with interleukin-10 expression in large cell T-cell lymphomas and indolent B-cell lymphomas. Blood 99, 609-617
33. Nuckel, H., Rebmann, V., Durig, J., Duhrsen, U., and Grosse-Wilde, H. (2005) HLA-G expression is associated with an unfavorable outcome and immunodeficiency in chronic lymphocytic leukemia. Blood 105, 1694-1698
34. Rebmann, V., Wagner, S., and Grosse-Wilde, H. (2007) HLA-G expression in malignant melanoma. Semin. Cancer Biol. 17, 422-429
35. Cooper, M. A., Fehniger, T. A., and Caligiuri, M. A. (2001) The biology of human natural killer-cell subsets. Trends Immunol. 22, 633-640
36. Rajagopalan, S., and Long, E. O. (1999) A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J. Exp. Med. 189, 1093-1100
37. Shiroishi, M., Kuroki, K., Ose, T., Rasubala, L., Shiratori, I., Arase, H., Tsumoto, K., Kumagai, I., Kohda, D., and Maenaka, K. (2006) Efficient leukocyte Ig-like receptor signaling and crystal structure of disulfide-linked HLA-G dimer. J. Biol. Chem. 281, 10439-10447
38. Colonna, M., Samaridis, J., Cella, M., Angman, L., Allen, R. L., O'Callaghan, C. A., Dunbar, R., Ogg, G. S., Cerundolo, V., and Rolink, A. (1998) Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J. Immunol. 160, 3096-3100
39. Gonen-Gross, T., Achdout, H., Arnon, T. I., Gazit, R., Stern, N., Horejsi, V., Goldman-Wohl, D., Yagel, S., and Mandelboim, O. (2005) The CD85J/leukocyte inhibitory receptor-1 distinguishes between conformed and β2-microglobulin-free HLA-G molecules. J. Immunol. 175, 4866-4874
40. Shiroishi, M., Kuroki, K., Rasubala, L., Tsumoto, K., Kumagai, I., Kurimoto, E., Kato, K., Kohda, D., and Maenaka, K. (2006) Structural basis for recognition of the nonclassical MHC molecule HLA-G by the leukocyte Ig-like receptor B2 (LILRB2/ LIR2/ILT4/CD85d). Proc. Natl. Acad. Sci. U. S. A. 103, 16412- 16417
41. HoWangYin, K. Y., Loustau, M., Wu, J., Alegre, E., Daouya, M., Caumartin, J., Sousa, S., Horuzsko, A., Carosella, E. D., and LeMaoult, J. (2012) Multimeric structures of HLA-G isoforms function through differential binding to LILRB receptors. Cell. Mol. Life Sci. 69, 4041-4049
42. Shiroishi, M., and Maenaka, K. (2009) Crystallization and preliminary X-ray analysis of the low-affinity complex between human leukocyte antigen-G (HLA-G) and leukocyte Ig-like receptor B2 (LILRB2). Protein Peptide Lett. 16, 447-449
43. Clements, C. S., Kjer-Nielsen, L., Kostenko, L., Hoare, H. L., Dunstone, M. A., Moses, E., Freed, K., Brooks, A. G., Rossjohn, J., and McCluskey, J. (2005) Crystal structure of HLA-G: a nonclassical MHC class I molecule expressed at the fetalmaternal interface. Proc. Natl. Acad. Sci. U. S. A. 102, 3360-3365
44. Boyson, J. E., Erskine, R., Whitman, M. C., Chiu, M., Lau, J. M., Koopman, L. A., Valter, M. M., Angelisova, P., Horejsi, V., and Strominger, J. L. (2002) Disulfide bond-mediated dimerization of HLA-G on the cell surface. Proc. Nat. Acad. Sci. U. S. A. 99, 16180-16185
45. Gonen-Gross, T., Achdout, H., Gazit, R., Hanna, J., Mizrahi, S., Markel, G., Goldman-Wohl, D., Yagel, S., Horejsi, V., Levy, O., Baniyash, M., and Mandelboim, O. (2003) Complexes of HLA-G protein on the cell surface are important for leukocyte Ig-like receptor-1 function. J. Immunol. 171, 1343-1351
46. Favier, B., HoWangYin, K. Y., Wu, J., Caumartin, J., Daouya, M., Horuzsko, A., Carosella, E. D., and LeMaoult, J. (2011) Tolerogenic function of dimeric forms of HLA-G recombinant proteins: a comparative study in vivo. PloS One 6, e21011
47. Robertson, M. J., Cochran, K. J., Cameron, C., Le, J. M., Tantravahi, R., and Ritz, J. (1996) Characterization of a cell line, NKL, derived from an aggressive human natural killer cell leukemia. Exp. Hematol. 24, 406-415
48. Liang, S., Baibakov, B., and Horuzsko, A. (2002) HLA-G inhibits the functions of murine dendritic cells via the PIR-B immune inhibitory receptor. Eur. J. Immunol. 32, 2418-2426
49. Lopes, C. T., Gallo, A. P., Palma, P. V., Cury, P. M., and Bueno, V. (2008) Skin allograft survival and analysis of renal parameters after FTY720 + tacrolimus treatment in mice. Transpl. Proc. 40, 856-860