Disruption of maternal immune balance maintained by innate DC subsets results in spontaneous pregnancy loss in mice

Immunobiology

Volumn 217, Issue 10, 2012, Pages 951-961

  Negishi, Yasuyuki ^a   Wakabayashi, Ayako ^a   Shimizu, Masumi ^a   Ichikawa, Tomoko ^a   Kumagai, Yoshihiro ^a   Takeshita, Toshiyuki ^a   Takahashi, Hidemi ^a  

^a NIPPON MEDICAL SCHOOL   (Japan)

Author keywords

33D1; DC; DEC 205; Dendritic cell inhibitory receptor 2 (DCIR2); Paraaortic lymph nodes (PALNs); Pregnancy; Progesterone; Th1 Th2 balance

Indexed keywords

INTERLEUKIN 12; PROGESTERONE;

33D1 DENDRITIC CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CELL ACTIVITY; CELL DISRUPTION; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEC 205 DENDRITIC CELL; DENDRITIC CELL; FEMALE; HORMONE INHIBITION; INNATE IMMUNITY; INOCULATION; MOUSE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; SPONTANEOUS ABORTION; TH1 TH2 BALANCE; UPREGULATION;

ABORTION, SPONTANEOUS; ANIMALS; ANTIBODIES, MONOCLONAL; BONE MARROW CELLS; CYTOKINES; DENDRITIC CELLS; ESTRADIOL; FEMALE; INTERLEUKIN-12; KINETICS; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PREGNANCY; PROGESTERONE; SPLEEN; T-LYMPHOCYTE SUBSETS; UTERUS;

EID: 84865389590     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.01.011     Document Type: Article

References (35)

1. Bizargity P., Bonney E.A. Dendritic cells: a family portrait at mid-gestation. Immunology 2009, 126:565-578.
2. Blois S.M., Joachim R., Kandil J., Margni R., Tometten M., Klapp B.F., Arck P.C. Depletion of CD8+ cells abolishes the pregnancy protective effect of progesterone substitution with dydrogesterone in mice by altering the Th1/Th2 cytokine profile. J. Immunol. 2004, 172:5893-5899.
3. Blois S.M., Kammerer U., Alba Soto C., Tometten M.C., Shaikly V., Barrientos G., Jurd R., Rukavina D., Thomson A.W., Klapp B.F., et al. Dendritic cells: key to fetal tolerance?. Biol. Reprod. 2007, 77:590-598.
4. Bozzacco L., Trumpfheller C., Siegal F.P., Mehandru S., Markowitz M., Carrington M., Nussenzweig M.C., Piperno A.G., Steinman R.M. DEC-205 receptor on dendritic cells mediates presentation of HIV gag protein to CD8+ T cells in a spectrum of human MHC I haplotypes. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1289-1294.
5. Collins M.K., Tay C.S., Erlebacher A. Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. J. Clin. Invest. 2009, 119:2062-2073.
6. Doria A., Iaccarino L., Arienti S., Ghirardello A., Zampieri S., Rampudda M.E., Cutolo M., Tincani A., Todesco S. Th2 immune deviation induced by pregnancy: the two faces of autoimmune rheumatic diseases. Reprod. Toxicol. 2006, 22:234-241.
7. Doria A., Tincani A., Lockshin M. Challenges of lupus pregnancies. Rheumatology (Oxford) 2008, 47(Suppl. 3). iii9-12.
8. Dudziak D., Kamphorst A.O., Heidkamp G.F., Buchholz V.R., Trumpfheller C., Yamazaki S., Cheong C., Liu K., Lee H.W., Park C.G., et al. Differential antigen processing by dendritic cell subsets in vivo. Science 2007, 315:107-111.
9. Figdor C.G., van Kooyk Y., Adema G.J. C-type lectin receptors on dendritic cells and Langerhans cells. Nat. Rev. Immunol. 2002, 2:77-84.
10. Geijtenbeek T.B., Kwon D.S., Torensma R., van Vliet S.J., van Duijnhoven G.C., Middel J., Cornelissen I.L., Nottet H.S., KewalRamani V.N., Littman D.R., et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000, 100:587-597.
11. Kammerer U., Eggert A.O., Kapp M., McLellan A.D., Geijtenbeek T.B., Dietl J., van Kooyk Y., Kampgen E. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am. J. Pathol. 2003, 162:887-896.
12. Karsten C.M., Behrends J., Wagner A.K., Fuchs F., Figge J., Schmudde I., Hellberg L., Kruse A. DC within the pregnant mouse uterus influence growth and functional properties of uterine NK cells. Eur. J. Immunol. 2009, 39:2203-2214.
13. Kato M., McDonald K.J., Khan S., Ross I.L., Vuckovic S., Chen K., Munster D., MacDonald K.P., Hart D.N. Expression of human DEC-205 (CD205) multilectin receptor on leukocytes. Int. Immunol. 2006, 18:857-869.
14. Langenkamp A., Messi M., Lanzavecchia A., Sallusto F. Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 2000, 1:311-316.
15. Laskarin G., Kammerer U., Rukavina D., Thomson A.W., Fernandez N., Blois S.M. Antigen-presenting cells and materno-fetal tolerance: an emerging role for dendritic cells. Am. J. Reprod. Immunol. 2007, 58:255-267.
16. Liu K., Nussenzweig M.C. Origin and development of dendritic cells. Immunol. Rev. 2010, 234:45-54.
17. Lydon J.P., DeMayo F.J., Funk C.R., Mani S.K., Hughes A.R., Montgomery C.A., Shyamala G., Conneely O.M., O'Malley B.W. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 1995, 9:2266-2278.
18. Maldonado-Lopez R., De Smedt T., Michel P., Godfroid J., Pajak B., Heirman C., Thielemans K., Leo O., Urbain J., Moser M. CD8alpha+ and CD8alpha-subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 1999, 189:587-592.
19. Moriya K., Wakabayashi A., Shimizu M., Tamura H., Dan K., Takahashi H. Induction of tumor-specific acquired immunity against already established tumors by selective stimulation of innate DEC-205(+) dendritic cells. Cancer Immunol. Immunother. 2010, 59:1083-1095.
20. Nagler A., Ohana M., Alper R., Doviner V., Sherman Y., Rabbani E., Engelhardt D., Ilan Y. Induction of oral tolerance in bone marrow transplantation recipients suppresses graft-versus-host disease in a semiallogeneic mouse model. Bone Marrow Transplant. 2003, 32:363-369.
21. Nardo L.G., Sallam H.N. Progesterone supplementation to prevent recurrent miscarriage and to reduce implantation failure in assisted reproduction cycles. Reprod. Biomed. Online 2006, 13:47-57.
22. Paharkova-Vatchkova V., Maldonado R., Kovats S. Estrogen preferentially promotes the differentiation of CD11c+ CD11b(intermediate) dendritic cells from bone marrow precursors. J. Immunol. 2004, 172:1426-1436.
23. Piccinni M.P., Beloni L., Livi C., Maggi E., Scarselli G., Romagnani S. Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat. Med. 1998, 4:1020-1024.
24. Plaks V., Birnberg T., Berkutzki T., Sela S., BenYashar A., Kalchenko V., Mor G., Keshet E., Dekel N., Neeman M., Jung S. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Invest. 2008, 118:3954-3965.
25. Pollard J.W. Uterine DCs are essential for pregnancy. J. Clin. Invest. 2008, 118:3832-3835.
26. Reina M., Broccia M.L., Menegola E., Di Blasio A.M., Vigano P., Giavini E. Effects of interleukin-12 administration during the pre- and peri-implantation period on mouse embryofetal development. Am. J. Reprod. Immunol. 2004, 51:345-351.
27. Scholz C., Toth B., Santoso L., Kuhn C., Franz M., Mayr D., Jeschke U., Friese K., Schiessl B. Distribution and maturity of dendritic cells in diseases of insufficient placentation. Am. J. Reprod. Immunol. 2008, 60:238-245.
28. Segerer S.E., Muller N., van den Brandt J., Kapp M., Dietl J., Reichardt H.M., Rieger L., Kammerer U. Impact of female sex hormones on the maturation and function of human dendritic cells. Am. J. Reprod. Immunol. 2009, 62:165-173.
29. Shortman K., Liu Y.J. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2002, 2:151-161.
30. Steinman R.M. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 1991, 9:271-296.
31. Takahashi H. Species-specific CD1-restricted innate immunity for the development of HIV vaccine. Vaccine 2010, 28(Suppl. 2):B3-B7.
32. Takahashi H., Nakagawa Y., Leggatt G.R., Ishida Y., Saito T., Yokomuro K., Berzofsky J.A. Inactivation of human immunodeficiency virus (HIV)-1 envelope-specific CD8+ cytotoxic T lymphocytes by free antigenic peptide: a self-veto mechanism. J. Exp. Med. 1996, 183:879-889.
33. Trumpfheller C., Caskey M., Nchinda G., Longhi M.P., Mizenina O., Huang Y., Schlesinger S.J., Colonna M., Steinman R.M. The microbial mimic poly IC induces durable and protective CD4+ T cell immunity together with a dendritic cell targeted vaccine. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2574-2579.
34. Virgo B.B., Bellward G.D. Serum progesterone levels in the pregnant and postpartum laboratory mouse. Endocrinology 1974, 95:1486-1490.
35. Wan H., Versnel M.A., Leijten L.M., van Helden-Meeuwsen C.G., Fekkes D., Leenen P.J., Khan N.A., Benner R., Kiekens R.C. Chorionic gonadotropin induces dendritic cells to express a tolerogenic phenotype. J. Leukoc. Biol. 2008, 83:894-901.