Human endogenous retrovirus envelope proteins target dendritic cells to suppress T-cell activation

European Journal of Immunology

Volumn 45, Issue 6, 2015, Pages 1748-1759

  Hummel, Jonas ^a   Kämmerer, Ulrike ^b   Müller, Nora ^a   Avota, Elita ^a   Schneider Schaulies, Sibylle ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

DC T cell conjugates; DCs; HERV; Immune tolerance; Immunological synapse; T cell activation

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD83 ANTIGEN; HML2 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P70; SYNCYTIN 1 PROTEIN; SYNCYTIN 2 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; AMINO ACID TRANSPORTER; CYTOKINE; PLACENTA PROTEIN; SYNCYTIN;

ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CELL EXPANSION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; EFFECTOR CELL; ENDOGENOUS RETROVIRUS; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE PROLIFERATION; MIXED LYMPHOCYTE REACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE; CHO CELL LINE; CHORIOCARCINOMA; CRICETULUS; CYTOLOGY; FEMALE; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PHENOTYPE; PREGNANCY; T LYMPHOCYTE;

AMINO ACID TRANSPORT SYSTEM ASC; ANIMALS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE; CHO CELLS; CHORIOCARCINOMA; CRICETULUS; CYTOKINES; DENDRITIC CELLS; ENDOGENOUS RETROVIRUSES; FEMALE; GENE EXPRESSION; GENE PRODUCTS, ENV; HUMANS; LYMPHOCYTE ACTIVATION; PHENOTYPE; PREGNANCY; PREGNANCY PROTEINS; T-LYMPHOCYTES; VIRAL ENVELOPE PROTEINS;

EID: 84930417188     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201445366     Document Type: Article

References (47)

1. Bannert, N. and Kurth, R., Retroelements and the human genome: new perspectives on an old relation. Proc. Natl. Acad. Sci. USA 2004. 101(Suppl 2): 14572-14579.
2. Boller, K., Schonfeld, K., Lischer, S., Fischer, N., Hoffmann, A., Kurth, R. and Tonjes, R. R., Human endogenous retrovirus HERV-K113 is capable of producing intact viral particles. J. Gen. Virol. 2008. 89: 567-572.
3. Kassiotis, G., Endogenous retroviruses and the development of cancer. J. Immunol. 2014. 192: 1343-1349.
4. Harris, J. R., Placental endogenous retrovirus (ERV): structural, functional, and evolutionary significance. Bioessays 1998. 20: 307-316.
5. Kammerer, U., Germeyer, A., Stengel, S., Kapp, M. and Denner, J., Human endogenous retrovirus K (HERV-K) is expressed in villous and extravillous cytotrophoblast cells of the human placenta. J. Reprod. Immunol. 2011. 91: 1-8.
6. Blond, J. L., Beseme, F., Duret, L., Bouton, O., Bedin, F., Perron, H., Mandrand, B. et al., Molecular characterization and placental expression of HERV-W, a new human endogenous retrovirus family. J. Virol. 1999. 73: 1175-1185.
7. Blond, J. L., Lavillette, D., Cheynet, V., Bouton, O., Oriol, G., Chapel-Fernandes, S., Mandrand, B. et al., An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J. Virol. 2000. 74: 3321-3329.
8. Malassine, A., Blaise, S., Handschuh, K., Lalucque, H., Dupressoir, A., Evain-Brion, D. and Heidmann, T., Expression of the fusogenic HERV-FRD Env glycoprotein (syncytin 2) in human placenta is restricted to villous cytotrophoblastic cells. Placenta 2007. 28: 185-191.
9. Malassine, A., Frendo, J. L., Blaise, S., Handschuh, K., Gerbaud, P., Tsatsaris, V., Heidmann, T. et al., Human endogenous retrovirus-FRD envelope protein (syncytin 2) expression in normal and trisomy 21-affected placenta. Retrovirology 2008. 5: 6.
10. Mi, S., Lee, X., Li, X., Veldman, G. M., Finnerty, H., Racie, L., LaVallie, E. et al., Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 2000. 403: 785-789.
11. Vargas, A., Toufaily, C., LeBellego, F., Rassart, E., Lafond, J. and Barbeau, B., Reduced expression of both syncytin 1 and syncytin 2 correlates with severity of preeclampsia. Reprod. Sci. 2011. 18: 1085-1091.
12. Lee, X., Keith, J. C., Jr., Stumm, N., Moutsatsos, I., McCoy, J. M., Crum, C. P., Genest, D. et al., Downregulation of placental syncytin expression and abnormal protein localization in pre-eclampsia. Placenta 2001. 22: 808-812.
13. Kalter, S. S., Helmke, R. J., Heberling, R. L., Panigel, M., Fowler, A. K., Strickland, J. E. and Hellman, A., Brief communication: C-type particles in normal human placentas. J. Natl. Cancer Inst. 1973. 50: 1081-1084.
14. Larsson, E. and Andersson, G., Beneficial role of human endogenous retroviruses: facts and hypotheses. Scand. J. Immunol. 1998. 48: 329-338.
15. Rote, N. S., Chakrabarti, S. and Stetzer, B. P., The role of human endogenous retroviruses in trophoblast differentiation and placental development. Placenta 2004. 25: 673-683.
16. Blaise, S., deParseval, N., Benit, L. and Heidmann, T., Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc. Natl. Acad. Sci. USA 2003. 100: 13013-13018.
17. Mangeney, M., Renard, M., Schlecht-Louf, G., Bouallaga, I., Heidmann, O., Letzelter, C., Richaud, A. et al., Placental syncytins: genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins. Proc. Natl. Acad. Sci. USA 2007. 104: 20534-20539.
18. Denner, J., The transmembrane proteins contribute to immunodeficiencies induced by HIV-1 and other retroviruses. AIDS 2014. 28: 1081-1090.
19. Haraguchi, S., Good, R. A., Cianciolo, G. J., Engelman, R. W. and Day, N. K., Immunosuppressive retroviral peptides: immunopathological implications for immunosuppressive influences of retroviral infections. J. Leukoc. Biol. 1997. 61: 654-666.
20. Cianciolo, G. J., Copeland, T. D., Oroszlan, S. and Snyderman, R., Inhibition of lymphocyte proliferation by a synthetic peptide homologous to retroviral envelope proteins. Science 1985. 230: 453-455.
21. Weislow, O. S., Fisher, O. U., Jr., Twardzik, D. R., Hellman, A. and Fowler, A. K., Depression of mitogen-induced lymphocyte blastogenesis by baboon endogenous retrovirus-associated components. Proc. Soc. Exp. Biol. Med. 1981. 166: 522-527.
22. Denner, J., Wunderlich, V. and Bierwolf, D., Suppression of human lymphocyte mitogen response by proteins of the type-D retrovirus PMFV. Int. J. Cancer 1986. 37: 311-316.
23. Denner, J., Immunosuppression by retroviruses: implications for xenotransplantation. Ann. NY Acad. Sci. 1998. 862: 75-86.
24. deParseval, N., Lazar, V., Casella, J. F., Benit, L. and Heidmann, T., Survey of human genes of retroviral origin: identification and transcriptome of the genes with coding capacity for complete envelope proteins. J. Virol. 2003. 77: 10414-10422.
25. Morozov, V. A., Dao Thi, V. L. and Denner, J., The transmembrane protein of the human endogenous retrovirus-K (HERV-K) modulates cytokine release and gene expression. PLoS One 2013. 8: e70399.
26. Ruprecht, K., Mayer, J., Sauter, M., Roemer, K. and Mueller-Lantzsch, N., Endogenous retroviruses and cancer. Cell Mol. Life Sci. 2008. 65: 3366-3382.
27. Tolosa, J. M., Schjenken, J. E., Clifton, V. L., Vargas, A., Barbeau, B., Lowry, P., Maiti, K. et al., The endogenous retroviral envelope protein syncytin-1 inhibits LPS/PHA-stimulated cytokine responses in human blood and is sorted into placental exosomes. Placenta 2012. 33: 933-941.
28. Bartmann, C., Segerer, S. E., Rieger, L., Kapp, M., Sutterlin, M. and Kammerer, U., Quantification of the predominant immune cell populations in decidua throughout human pregnancy. Am. J. Reprod. Immunol. 2014. 71: 109-119.
29. Esnault, C., Priet, S., Ribet, D., Vernochet, C., Bruls, T., Lavialle, C., Weissenbach, J. et al., A placenta-specific receptor for the fusogenic, endogenous retrovirus-derived, human syncytin-2. Proc. Natl. Acad. Sci. USA 2008. 105: 17532-17537.
30. Hayward, M. D., Potgens, A. J., Drewlo, S., Kaufmann, P. and Rasko, J. E., Distribution of human endogenous retrovirus type W receptor in normal human villous placenta. Pathology 2007. 39: 406-412.
31. Grasso, E., Paparini, D., Hauk, V., Salamone, G., Leiros, C. P. and Ramhorst, R., Differential migration and activation profile of monocytes after trophoblast interaction. PLoS One 2014. 9: e97147.
32. Salamone, G., Fraccaroli, L., Gori, S., Grasso, E., Paparini, D., Geffner, J., Perez Leiros, C. et al., Trophoblast cells induce a tolerogenic profile in dendritic cells. Hum. Reprod. 2012. 27: 2598-2606.
33. Du, M. R., Guo, P. F., Piao, H. L., Wang, S. C., Sun, C., Jin, L. P., Tao, Y. et al., Embryonic trophoblasts induce decidual regulatory T cell differentiation and maternal-fetal tolerance through thymic stromal lymphopoietin instructing dendritic cells. J. Immunol. 2014. 192: 1502-1511.
34. Guo, P. F., Du, M. R., Wu, H. X., Lin, Y., Jin, L. P. and Li, D. J., Thymic stromal lymphopoietin from trophoblasts induces dendritic cell-mediated regulatory TH2 bias in the decidua during early gestation in humans. Blood 2010. 116: 2061-2069.
35. Bennett, W. A., Lagoo-Deenadayalan, S., Whitworth, N. S., Brackin, M. N., Hale, E. and Cowan, B. D., Expression and production of interleukin-10 by human trophoblast: relationship to pregnancy immunotolerance. Early Pregnancy 1997. 3: 190-198.
36. Komine-Aizawa, S., Majima, H., Yoshida-Noro, C. and Hayakawa, S., Stimuli through Toll-like receptor (TLR) 3 and 9 affect human chorionic gonadotropin (hCG) production in a choriocarcinoma cell line. J. Obstet. Gynaecol. Res. 2008. 34: 144-151.
37. Tangeras, L. H., Stodle, G. S., Olsen, G. D., Leknes, A. H., Gundersen, A. S., Skei, B., Vikdal, A. J. et al., Functional Toll-like receptors in primary first-trimester trophoblasts. J. Reprod. Immunol. 2014. 106: 89-99.
38. Holder, B. S., Tower, C. L., Forbes, K., Mulla, M. J., Aplin, J. D. and Abrahams, V. M., Immune cell activation by trophoblast-derived microvesicles is mediated by syncytin 1. Immunology 2012. 136: 184-191.
39. Rolland, A., Jouvin-Marche, E., Viret, C., Faure, M., Perron, H. and Marche, P. N., The envelope protein of a human endogenous retrovirus-W family activates innate immunity through CD14/TLR4 and promotes Th1-like responses. J. Immunol. 2006. 176: 7636-7644.
40. Plaks, V., Birnberg, T., Berkutzki, T., Sela, S., BenYashar, A., Kalchenko, V., Mor, G. et al., Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Invest. 2008. 118: 3954-3965.
41. Laskarin, G., Kammerer, U., Rukavina, D., Thomson, A. W., Fernandez, N. and Blois, S. M., Antigen-presenting cells and materno-fetal tolerance: an emerging role for dendritic cells. Am. J. Reprod. Immunol. 2007. 58: 255-267.
42. Ban, Y., Chang, Y., Dong, B., Kong, B. and Qu, X., Indoleamine 2, 3-dioxygenase levels at the normal and recurrent spontaneous abortion fetal-maternal interface. J. Int. Med. Res. 2013. 41: 1135-1149.
43. Segerer, S. E., Rieger, L., Kapp, M., Dombrowski, Y., Muller, N., Dietl, J. and Kammerer, U., MIC-1 (a multifunctional modulator of dendritic cell phenotype and function) is produced by decidual stromal cells and trophoblasts. Hum. Reprod. 2012. 27: 200-209.
44. Green, B. J., Lee, C. S. and Rasko, J. E., Biodistribution of the RD114/mammalian type D retrovirus receptor, RDR. J. Gene Med. 2004. 6: 249-259.
45. Fuchs, B. C. and Bode, B. P., Amino acid transporters ASCT2 and LAT1 in cancer: partners in crime? Semin. Cancer Biol. 2005. 15: 254-266.
46. Fuchs, B. C., Perez, J. C., Suetterlin, J. E., Chaudhry, S. B. and Bode, B. P., Inducible antisense RNA targeting amino acid transporter ATB0/ASCT2 elicits apoptosis in human hepatoma cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2004. 286: G467-G478.
47. Schneider-Schaulies, J. and Schneider-Schaulies, S., Receptor interactions, tropism, and mechanisms involved in morbillivirus-induced immunomodulation. Adv. Virus Res. 2008. 71: 173-205.