HLA-G promotes myeloid-derived suppressor cell accumulation and suppressive activity during human pregnancy through engagement of the receptor ILT4

European Journal of Immunology

Volumn 47, Issue 2, 2017, Pages 374-384

  Köstlin, Natascha ^a   Ostermeir, Anna Lena ^a   Spring, Bärbel ^a   Schwarz, Julian ^a   Marmé, Alexander ^b   Walter, Christina B ^c   Poets, Christian F ^a   Gille, Christian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Am Lustnauer Tor   (Germany)

^c Department of Obstetrics and Gynecology ^*  (Germany)

Author keywords

HLA G; MDSC; Reproductive Immunology; T cells; Tolerance

Indexed keywords

CD33 ANTIGEN; HLA G ANTIGEN; IMMUNOGLOBULIN LIKE TRANSCRIPT 2; IMMUNOGLOBULIN LIKE TRANSCRIPT 4; INDOLEAMINE 2,3 DIOXYGENASE; RECEPTOR; STAT3 PROTEIN; UNCLASSIFIED DRUG; IMMUNOGLOBULIN RECEPTOR; LILRB2 PROTEIN, HUMAN; MEMBRANE PROTEIN; PROTEIN BINDING;

ARTICLE; BLOOD; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL INTERACTION; CONTROLLED STUDY; GRANULOCYTE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MYELOID-DERIVED SUPPRESSOR CELL; PHOSPHORYLATION; PLACENTA; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; UPREGULATION; ADOLESCENT; ADULT; CELL CULTURE; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MIDDLE AGED; MOTHER FETUS RELATIONSHIP; SIGNAL TRANSDUCTION; YOUNG ADULT;

ADOLESCENT; ADULT; CELLS, CULTURED; FEMALE; HLA-G ANTIGENS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, INNATE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MATERNAL-FETAL RELATIONS; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; MYELOID-DERIVED SUPPRESSOR CELLS; PREGNANCY; PROTEIN BINDING; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; YOUNG ADULT;

EID: 85006762273     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201646564     Document Type: Article

References (51)

1. Rai, R. and Regan, L., Recurrent miscarriage. Lancet 2006. 368: 601–611.
2. Warning, J. C., McCracken, S. A. and Morris, J. M., A balancing act: mechanisms by which the fetus avoids rejection by the maternal immune system. Reproduction 2011. 141: 715–724.
3. Gabrilovich, D. I. and Nagaraj, S., Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009. 9: 162–174.
4. Delano, M. J., Scumpia, P. O., Weinstein, J. S., Coco, D., Nagaraj, S., Kelly-Scumpia, K. M., O'Malley, K. A. et al., MyD88-dependent expansion of an immature GR-1(+)CD11b(+) population induces T cell suppression and Th2 polarization in sepsis. J. Exp. Med. 2007. 204: 1463–1474.
5. Mandruzzato, S., Solito, S., Falisi, E., Francescato, S., Chiarion-Sileni, V., Mocellin, S., Zanon, A. et al., IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J. Immunol. 2009. 182: 6562–6568.
6. Diaz-Montero, C. M., Salem, M. L., Nishimura, M. I., Garrett-Mayer, E., Cole, D. J. and Montero, A. J., Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer. Immunol. Immunother. 2009. 58: 49–59.
7. Goni, O., Alcaide, P. and Fresno, M., Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G (Gr1(+))CD11b(+)immature myeloid suppressor cells. Int. Immunol. 2002. 14: 1125–1134.
8. Makarenkova, V. P., Bansal, V., Matta, B. M., Perez, L. A. and Ochoa, J. B., CD11b+/Gr-1+ myeloid suppressor cells cause T cell dysfunction after traumatic stress. J. Immunol. 2006. 176: 2085–2094.
9. Zhu, B., Bando, Y., Xiao, S., Yang, K., Anderson, A. C., Kuchroo, V. K. and Khoury, S. J., CD11b+Ly-6C(hi) suppressive monocytes in experimental autoimmune encephalomyelitis. J. Immunol. 2007. 179: 5228–5237.
10. Youn, J. I., Nagaraj, S., Collazo, M. and Gabrilovich, D. I., Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 2008. 181: 5791–5802.
11. Luyckx, A., Schouppe, E., Rutgeerts, O., Lenaerts, C., Koks, C., Fevery, S., Devos, T. et al., Subset characterization of myeloid-derived suppressor cells arising during induction of BM chimerism in mice. Bone Marrow Transplant. 2011. 47: 985–992.
12. Zhang, W., Liang, S., Wu, J. and Horuzsko, A., Human inhibitory receptor immunoglobulin-like transcript 2 amplifies CD11b+Gr1+ myeloid-derived suppressor cells that promote long-term survival of allografts. Transplantation 2008. 86: 1125–1134.
13. Zoso, A., Mazza, E. M., Bicciato, S., Mandruzzato, S., Bronte, V., Serafini, P. and Inverardi, L., Human fibrocytic myeloid-derived suppressor cells express IDO and promote tolerance via Treg-cell expansion. Eur. J. Immunol. 2014. 44: 3307–3319.
14. Kostlin, N., Hofstadter, K., Ostermeir, A. L., Spring, B., Leiber, A., Haen, S., Abele, H. et al., Granulocytic myeloid-derived suppressor cells accumulate in human placenta and polarize toward a Th2 phenotype. J. Immunol. 2016. 196: 1132–1145.
15. Kostlin, N., Kugel, H., Spring, B., Leiber, A., Marme, A., Henes, M., Rieber, N. et al., Granulocytic myeloid-derived suppressor cells expand in human pregnancy and modulate T- cell responses. Eur. J. Immunol. 2014. 44: 2582–2591.
16. Mauti, L. A., Le Bitoux, M. A., Baumer, K., Stehle, J. C., Golshayan, D., Provero, P. and Stamenkovic, I., Myeloid-derived suppressor cells are implicated in regulating permissiveness for tumor metastasis during mouse gestation. J. Clin. Invest. 2011. 121: 2794–2807.
17. Rieber, N., Gille, C., Kostlin, N., Schafer, I., Spring, B., Ost, M., Spieles, H. et al., Neutrophilic myeloid-derived suppressor cells in cord blood modulate innate and adaptive immune responses. Clin. Exp. Immunol. 2013. 174: 45–52.
18. Zhao, H., Kalish, F., Schulz, S., Yang, Y., Wong, R. J. and Stevenson, D. K., Unique roles of infiltrating myeloid cells in the murine uterus during early to midpregnancy. J. Immunol. 2015. 194: 3713–3722.
19. Djurisic, S. and Hviid, T. V., HLA class Ib molecules and immune cells in pregnancy and preeclampsia. Front Immunol 2014. 5: 652.
20. Rouas-Freiss, N., Moreau, P., LeMaoult, J. and Carosella, E. D., The dual role of HLA-G in cancer. J Immunol Res 2014. 2014: 359748.
21. Hunt, J. S., Petroff, M. G., McIntire, R. H. and Ober, C., HLA-G and immune tolerance in pregnancy. FASEB J. 2005. 19: 681–693.
22. Alegre, E., Diaz-Lagares, A., Lemaoult, J., Lopez-Moratalla, N., Carosella, E. D. and Gonzalez, A., Maternal antigen presenting cells are a source of plasmatic HLA-G during pregnancy: longitudinal study during pregnancy. Hum. Immunol. 2007. 68: 661–667.
23. Yie, S. M., Taylor, R. N. and Librach, C., Low plasma HLA-G protein concentrations in early gestation indicate the development of preeclampsia later in pregnancy. Am. J. Obstet. Gynecol. 2005. 193: 204–208.
24. Peng, B., Zhang, L., Xing, A. Y., Hu, M. and Liu, S. Y., [The expression of human leukocyte antigen G and E on human first trimester placenta and its relationship with recurrent spontaneous abortion]. Sichuan Da Xue Xue Bao Yi Xue Ban 2008. 39: 976–979.
25. Riteau, B., Menier, C., Khalil-Daher, I., Sedlik, C., Dausset, J., Rouas-Freiss, N. and Carosella, E. D., HLA-G inhibits the allogeneic proliferative response. J. Reprod. Immunol. 1999. 43: 203–211.
26. Rouas-Freiss, N., Marchal, R. E., Kirszenbaum, M., Dausset, J. and Carosella, E. D., 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. 1997. 94: 5249–5254.
27. Le Gal, F. A., Riteau, B., Sedlik, C., Khalil-Daher, I., Menier, C., Dausset, J., Guillet, J. G. et al., HLA-G-mediated inhibition of antigen-specific cytotoxic T lymphocytes. Int. Immunol. 1999. 11: 1351–1356.
28. Agaugue, S., Carosella, E. D. and Rouas-Freiss, N., Role of HLA-G in tumor escape through expansion of myeloid-derived suppressor cells and cytokinic balance in favor of Th2 versus Th1/Th17. Blood 2011. 117: 7021–7031.
29. Loumagne, L., Baudhuin, J., Favier, B., Montespan, F., Carosella, E. D. and Rouas-Freiss, N., In vivo evidence that secretion of HLA-G by immunogenic tumor cells allows their evasion from immunosurveillance. Int. J. Cancer 2014. 135: 2107–2117.
30. Lechner, M. G., Liebertz, D. J. and Epstein, A. L., Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J. Immunol. 2010. 185: 2273–2284.
31. Cheng, P., Corzo, C. A., Luetteke, N., Yu, B., Nagaraj, S., Bui, M. M., Ortiz, M. et al., Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J. Exp. Med. 2008. 205: 2235–2249.
32. Vasquez-Dunddel, D., Pan, F., Zeng, Q., Gorbounov, M., Albesiano, E., Fu, J., Blosser, R. L. et al., STAT3 regulates arginase-I in myeloid-derived suppressor cells from cancer patients. J. Clin. Invest. 2013. 123: 1580–1589.
33. Wu, L., Du, H., Li, Y., Qu, P. and Yan, C., Signal transducer and activator of transcription 3 (Stat3C) promotes myeloid-derived suppressor cell expansion and immune suppression during lung tumorigenesis. Am. J. Pathol. 2011. 179: 2131–2141.
34. Lynge Nilsson, L., Djurisic, S. and Hviid, T. V., Controlling the immunological crosstalk during conception and pregnancy: HLA-G in reproduction. Front Immunol 2014. 5: 198.
35. Bankey, P. E., Banerjee, S., Zucchiatti, A., De, M., Sleem, R. W., Lin, C. F., Miller-Graziano, C. L. et al., Cytokine induced expression of programmed death ligands in human neutrophils. Immunol. Lett. 2010. 129: 100–107.
36. LeMaoult, J., Zafaranloo, K., Le Danff, C. and Carosella, E. D., HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells. FASEB J. 2005. 19: 662–664.
37. Hackmon, R., Hallak, M., Krup, M., Weitzman, D., Sheiner, E., Kaplan, B. and Weinstein, Y., HLA-G antigen and parturition: maternal serum, fetal serum and amniotic fluid levels during pregnancy. Fetal. Diagn. Ther. 2004. 19: 404–409.
38. Hunt, J. S., Jadhav, L., Chu, W., Geraghty, D. E. and Ober, C., Soluble HLA-G circulates in maternal blood during pregnancy. Am. J. Obstet. Gynecol. 2000. 183: 682–688.
39. Liang, S., Baibakov, B. and Horuzsko, A., HLA-G inhibits the functions of murine dendritic cells via the PIR-B immune inhibitory receptor. Eur. J. Immunol. 2002. 32: 2418–2426.
40. Dahl, M. and Hviid, T. V., Human leucocyte antigen class Ib molecules in pregnancy success and early pregnancy loss. Hum. Reprod. Update 2012. 18: 92–109.
41. Lechner, M. G., Megiel, C., Russell, S. M., Bingham, B., Arger, N., Woo, T. and Epstein, A. L., Functional characterization of human Cd33+ and Cd11b+ myeloid-derived suppressor cell subsets induced from peripheral blood mononuclear cells co-cultured with a diverse set of human tumor cell lines. J Transl Med 2011. 9: 90.
42. Rieber, N., Brand, A., Hector, A., Graepler-Mainka, U., Ost, M., Schafer, I., Wecker, I. et al., Flagellin induces myeloid-derived suppressor cells: implications for Pseudomonas aeruginosa infection in cystic fibrosis lung disease. J. Immunol. 2013. 190: 1276–1284.
43. Sippel, T. R., White, J., Nag, K., Tsvankin, V., Klaassen, M., Kleinschmidt-DeMasters, B. K. and Waziri, A., Neutrophil degranulation and immunosuppression in patients with GBM: restoration of cellular immune function by targeting arginase I. Clin. Cancer. Res. 2011. 17: 6992–7002.
44. Lee, C. L., Guo, Y., So, K. H., Vijayan, M., Guo, Y., Wong, V. H., Yao, Y. et al., Soluble human leukocyte antigen G5 polarizes differentiation of macrophages toward a decidual macrophage-like phenotype. Hum. Reprod. 2015. 30: 2263–2274.
45. Munn, D. H., Zhou, M., Attwood, J. T., Bondarev, I., Conway, S. J., Marshall, B., Brown, C. et al., Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998. 281: 1191–1193.
46. Santillan, M. K., Pelham, C. J., Ketsawatsomkron, P., Santillan, D. A., Davis, D. R., Devor, E. J., Gibson-Corley, K. N. et al., Pregnant mice lacking indoleamine 2,3-dioxygenase exhibit preeclampsia phenotypes. Physiol Rep 2015. 3.
47. Liang, S., Ristich, V., Arase, H., Dausset, J., Carosella, E. D. and Horuzsko, A., Modulation of dendritic cell differentiation by HLA-G and ILT4 requires the IL-6–STAT3 signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 2008. 105: 8357–8362.
48. Rebe, C., Vegran, F., Berger, H. and Ghiringhelli, F., STAT3 activation: A key factor in tumor immunoescape. JAKSTAT 2013. 2: e23010.
49. Pan, T., Zhong, L., Wu, S., Cao, Y., Yang, Q., Cai, Z., Cai, X. et al., 17beta-estradiol enhances the expansion and activation of myeloid-derived suppressor cells via STAT3 signaling in human pregnancy. Clin. Exp. Immunol. 2016. 185: 86–97.
50. Nefedova, Y., Huang, M., Kusmartsev, S., Bhattacharya, R., Cheng, P., Salup, R., Jove, R. et al., Hyperactivation of STAT3 is involved in abnormal differentiation of dendritic cells in cancer. J. Immunol. 2004. 172: 464–474.
51. Baudhuin, J., Migraine, J., Faivre, V., Loumagne, L., Lukaszewicz, A. C., Payen, D. and Favier, B., Exocytosis acts as a modulator of the ILT4-mediated inhibition of neutrophil functions. Proc. Natl. Acad. Sci. U. S. A. 2013. 110: 17957–17962.