Angiogenic DC-SIGN+ cells are present at the attachment sites of epitheliochorial placentae

Immunology and Cell Biology

Volumn 88, Issue 1, 2010, Pages 63-71

  Linton, Nicola F ^a   Wessels, Jocelyn M ^a   Cnossen, Sonya A ^a   Van Den Heuvel, Marianne J ^a   Croy, B Anne ^a,b   Tayade, Chandrakant ^a,b  

^a UNIVERSITY OF GUELPH   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

Angiogenesis; Cytokines; Dendritic cells; Fetal loss; Pregnancy; Toll like receptors

Indexed keywords

CYTOKINE; PLEXIN; SEMAPHORIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; CD209 ANTIGEN; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; DC-SPECIFIC ICAM-3 GRABBING NONINTEGRIN; LECTIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL ISOLATION; CONTROLLED STUDY; DENDRITIC CELL; ENDOMETRIUM BIOPSY; GESTATION PERIOD; LASER CAPTURE MICRODISSECTION; NONHUMAN; PLACENTA; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; TROPHOBLAST; ANIMAL; CYTOLOGY; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PREGNANCY; SWINE; VASCULARIZATION;

SUIDAE;

ANIMALS; CELL ADHESION; CELL ADHESION MOLECULES; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; LECTINS, C-TYPE; NEOVASCULARIZATION, PHYSIOLOGIC; PLACENTA; PREGNANCY; RECEPTORS, CELL SURFACE; SWINE; TOLL-LIKE RECEPTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 74249094755     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2009.62     Document Type: Article

References (45)

1. Aluvihare VR, Kallikourdis M, Betz AG. Tolerance, suppression and the fetal allograft. J Mol Med 2005; 83: 88-96.
2. Erlebacher A. Why isn't the fetus rejected? Curr Opin Immunol 2001; 13: 590-593.
3. Billington WD. The immunological problem of pregnancy: 50 years with the hope of progress. A tribute to Peter Medawar. J Reprod Immunol 2003; 60: 1-11.
4. Croy BA, van den Heuvel MJ, Borzychowski AM, Tayade C. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol Rev 2006; 214: 161-185.
5. Dimova T, Mihaylova A, Spassova P, Georgieva R. Establishment of the porcine epitheliochorial placenta is associated with endometrial T-cell recruitment. Am J Reprod Immunol 2007; 57: 250-261.
6. Mellor AL, Munn DH. Immunology at the maternal-fetal interface: lessons for T cell tolerance and suppression. Annu Rev Immunol 2000; 18: 367-391.
7. Gardner L, Moffett L. Dendritic cells in the human decidua. Biol Reprod 2003; 69: 1438-1446.
8. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol 2003; 21: 685-711.
9. Zarnani AH, Moazzeni SM, Shokri F, Salehnia M, Jeddi-Tehrani M. Kinetics of murine decidual dendritic cells. Reproduction 2007; 133: 275-283.
10. Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TB, Dietl J et al. 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.
11. Kammerer U, Kruse A, Barrientos G, Arck PC, Blois SM. Role of dendritic cells in the regulation of maternal immune responses to the fetus during mammalian gestation. Immunol Invest 2008; 37: 499-533.
12. Breburda EE, Dambaeva SV, Slukvin II, Golos TG. Selective distribution and pregnancy-specific expression of DC-SIGN at the maternal-fetal interface in the rhesus macaque: DC-SIGN is a putative marker of the recognition of pregnancy. Placenta 2006; 27: 11-21.
13. Conejo-Garcia JR, Benencia F, Courreges MC, Kang E, Mohamed-Hadley A, Buckanovich RJ et al. Tumor-infiltrating dendritic cell precursors recruited by a betadefensin contribute to vasculogenesis under the influence of Vegf-A. Nat Med 2004; 10: 950-958.
14. Plaks V, Birnberg T, Berkutzki T, Sela S, BenYashar A, Kalchenko V et al. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J Clin Invest 2008; 118: 3954-3965.
15. Krey G, Frank P, Shaikly V, Barrientos G, Cordo-Russo R, Ringel F et al. In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development in mice. J Mol Med 2008; 86: 999-1011.
16. Behrends J, Karsten CM, Wilke S, Robke A, Kruse A. Identification of ITGA4/ITGB7 and ITGAE/ITGB7 expressing subsets of decidual dendritic-like cells within distinct microdomains of the pregnant mouse uterus. Biol Reprod 2008; 79: 624-632.
17. Favier B, Alam A, Barron P, Bonnin J, Laboudie P, Fons P et al. Neuropilin-2 interacts with VEGFR-2 and VEGFR-3 and promotes human endothelial cell survival and migration. Blood 2006; 108: 1243-1250.
18. Pan Q, Chathery Y, Wu Y, Rathore N, Tong RK, Peale F et al. Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting. J Biol Chem 2007; 282: 24049-24056.
19. Sarris M, Andersen KG, Randow F, Mayr l, Betz AG. Neuropilin-1 expression on regulatory T cells enhances their interactions with dendritic cells during antigen recognition. Immunity 2008; 28: 402-413.
20. Takahashi T, Nakamura F, Jin Z, Kalb RG, Strittmatter SM. Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors. Nat Neurosci 1998; 1: 487-493.
21. Bussolino F, Valdembri D, Caccavari F, Serini G. Semaphoring vascular morphogenesis. Endothelium 2006; 13: 81-91.
22. Geretti E, Shimizu A, Klagsbrun M. Neuropilin structure governs VEGF and semaphorin binding and regulates angiogenesis. Angiogenesis 2008; 11: 31-39.
23. Guttmann-Raviv N, Shraga-Heled N, Varshavsky A, Guimaraes-Sternberg C, Kessler O, Neufeld G. Semaphorin-3A and semaphorin-3F work together to repel endothelial cells and to inhibit their survival by induction of apoptosis. J Biol Chem 2007; 282: 26294-26305.
24. Kessler O, Shraga-Heled N, Lange T, Gutmann-Raviv N, Sabo E, Baruch L et al. Semaphorin-3F is an inhibitor of tumor angiogenesis. Cancer Res 2004; 64: 1008-1015.
25. Huang YW, Dryman BA, Li W, Meng XJ. Porcine DC-SIGN: molecular cloning, gene structure, tissue distribution and binding characteristics. Dev Comp Immunol 2009; 33: 464-480.
26. Sun J, Pearce EJ. Suppression of early IL-4 production underlies the failure of CD4 T cells activated by TLR-stimulated dendritic cells to differentiate into Th2 cells. J Immunol 2007; 178: 1635-1644.
27. Krikun G, Lockwood CJ, Abrahams VM, Mor G, Paidas M, Guller S. Expression of Toll-like receptors in the human decidua. Histol Histopathol 2007; 22: 847-854.
28. Makhseed M, Raghupathy R, Azizieh F, Omu A, Al Shamali E, Ashkanani L. Th1 and Th2 cytokine profiles in recurrent aborters with successful pregnancy and with subsequent abortions. Hum Reprod 2001; 16: 2219-2226.
29. Raghupathy R. Pregnancy: success and failure within the Th1/Th2/Th3 paradigm. Semin Immunol 2001; 13: 219-227.
30. Borzychowski AM, Croy BA, Chan WL, Redman CW, Sargent IL. Changes in systemic type 1 and type 2 immunity in normal pregnancy and pre-eclampsia may be mediated by natural killer cells. Eur J Immunol 2005; 35: 3054-3063.
31. Curry AE, Vogel I, Drews C, Schendel D, Skogstrand K, Flanders WD et al. Midpregnancy maternal plasma levels of interleukin 2, 6, and 12, tumor necrosis factoralpha, interferon-gamma, and granulocyte-macrophage colony-stimulating factor and spontaneous preterm delivery. Acta Obstet Gynecol Scand 2007; 86: 1103-1110.
32. Sharma A, Satyam A, Sharma JB. Leptin, IL-10 and inflammatory markers (TNF-alpha, IL-6 and IL-8) in pre-eclamptic, normotensive pregnant and healthy non-pregnant women. Am J Reprod Immunol 2007; 58: 21-30.
33. Wegmann TG, Guilbert LJ. Immune signalling at the maternal-fetal interface and trophoblast differentiation. Dev Comp Immunol 1992; 16: 425-430.
34. Clark DA, Chaouat G, Mogil R, Wegmann TG. Prevention of spontaneous abortion in DBA/2-mated CBA/J mice by GM-CSF involves CD8+ T cell-dependent suppression of natural effector cell cytotoxicity against trophoblast target cells. Cell Immunol 1994; 154: 143-152.
35. Mimura K, Kono K, Takahashi A, Kawaguchi Y, Mizukami Y, Fujii H. Vascular endothelial growth factor inhibits inhibits the function of human mature dendritic cells mediated by VEGF receptor-2. Cancer Immunol Immunother 2007; 56: 761-770.
36. Scholz C, Toth B, Santoso L, Kuhn C, Franz M, Mayr D et al. Distribution and maturity of dendritic cells in diseases of insufficient placentation. Am J Repro Immunol 2008; 60: 238-245.
37. Li XF, Charnock-Jones DS, Zhang E, Hiby S, Malik S, Day K et al. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J Clin Endocrinol Metab 2001; 86: 1823-1834.
38. Abrahams VM, Mor G. Toll-like receptors and their role in the trophoblast. Placenta 2005; 26: 540-547.
39. Koga K, Mor G. Expression and function of toll-like receptors at the maternal-fetal interface. Reprod Sci 2008; 15: 231-242.
40. Lefevre F, Martinat-Botte F, Guillomot M, Zouari K, Charley B, La Bonnardiere C. Interferon-gamma gene and protein are spontaneously expressed by the porcine trophectoderm early in gestation. Eur J Immunol 1990; 20: 2485-2490.
41. Tayade C, Fang Y, Hilchie D, Croy BA. Lymphocyte contributions to altered endometrial angiogenesis during early and midgestation fetal loss. J Leukoc Biol 2007; 82: 877-886.
42. Dudley DJ, Chen C-L, Murray MD, Daynes RA, Araneo BA. Adaptive immune responses during murine pregnancy: pregnancy-induced regulation of lymphokine production by activated T lymphocytes. Am J Obstet Gynecol 1993; 168: 1155-1163.
43. Wegmann TG, Hin H, Guilbert L, Mosmann TR. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol Today 1993; 14: 353-356.
44. Chaouat G, Menu E, Clark DA, Dy M, Minkowski M, Wegmann TG. Control of fetal survival in CBA x DBA/2 mice by lymphokine therapy. J Reprod Fertil 1990; 89: 447-458.
45. Tayade C, Black GP, Fang Y, Croy BA. Differential gene expression in endometrium, endometrial lymphocytes, and trophoblasts during successful and abortive embryo implantation. J Immunol 2006; 176: 148-156.