Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice

Journal of Clinical Investigation

Volumn 119, Issue 7, 2009, Pages 2062-2073

  Collins, Mary K ^a   Tay, Chin Siean ^a   Erlebacher, Adrian ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FETAL ANTIGEN; LIPOPOLYSACCHARIDE; SECONDARY LYMPHOID TISSUE CHEMOKINE; CCR7 PROTEIN, MOUSE; CHEMOKINE RECEPTOR CCR7;

ALLOGRAFT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; DECIDUALIZATION; DENDRITIC CELL; FEMALE; GRAFT REJECTION; LYMPH VESSEL; LYMPHATIC DRAINAGE; MALE; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; CELL MOTION; DECIDUA; FETOMATERNAL TRANSFUSION; FETUS; IMMUNOLOGY; PHYSIOLOGY; PLACENTA; T LYMPHOCYTE; UTERUS;

ANIMALS; CELL MOVEMENT; CHEMOKINE CCL21; DECIDUA; DENDRITIC CELLS; FEMALE; FETUS; LIPOPOLYSACCHARIDES; MALE; MATERNAL-FETAL EXCHANGE; MICE; MICE, INBRED C57BL; PLACENTA; PREGNANCY; RECEPTORS, CCR7; T-LYMPHOCYTES; UTERUS;

EID: 67650804370     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI38714     Document Type: Article

References (46)

1. Trowsdale, J., and Betz, A.G. 2006. Mother's little helpers: mechanisms of maternal-fetal tolerance. Nat. Immunol. 7:241-246.
2. Moffett, A., and Loke, C. 2006. Immunology of placentation in eutherian mammals. Nat. Rev. Immunol. 6:584-594.
3. Erlebacher, A., Vencato, D., Price, K.A., Zhang, D., and Glimcher, L.H. 2007. Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J. Clin. Invest. 117:1399-1411.
4. Kruse, A., Martens, N., Fernekorn, U., Hallmann, R., and Butcher, E.C. 2002. Alterations in the expression of homing-associated molecules at the maternal/ fetal interface during the course of pregnancy. Biol. Reprod. 66:333-345.
5. Dey, S.K., et al. 2004. Molecular cues to implantation. Endocr. Rev. 25:341-373.
6. Plaks, V., et al. 2008. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Invest. 118:3954- 3965.
7. Krey, G., et al. 2008. In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development in mice. J. Mol. Med. 86:999-1011.
8. Blois, S.M., et al. 2004. Lineage, maturity, and phenotype of uterine murine dendritic cells throughout gestation indicate a protective role in maintaining pregnancy. Biol. Reprod. 70:1018-1023.
9. Zarnani, A.H., Moazzeni, S.M., Shokri, F., Salehnia, M., and Jeddi-Tehrani, M. 2007. Kinetics of murine decidual dendritic cells. Reproduction. 133:275-283.
10. Behrends, J., Karsten, C.M., Wilke, S., Robke, A., and Kruse, A. 2008. Identification of ITGA4/ ITGB7 and ITGAE/ITGB7 expressing subsets of decidual dendritic-like cells within distinct microdomains of the pregnant mouse uterus. Biol. Reprod. 79:624-632.
11. Gouon-Evans, V., and Pollard, J.W. 2001. Eotaxin is required for eosinophil homing into the stroma of the pubertal and cycling uterus. Endocrinology. 142:4515-4521.
12. Pollard, J.W., Lin, E.Y., and Zhu, L. 1998. Complexity in uterine macrophage responses to cytokines in mice. Biol. Reprod. 58:1469-1475.
13. Keenihan, S.N., and Robertson, S.A. 2004. Diversity in phenotype and steroid hormone dependence in dendritic cells and macrophages in the mouse uterus. Biol. Reprod. 70:1562-1572.
14. Johansson-Lindbom, B., et al. 2005. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202:1063-1073.
15. Sung, S.S., et al. 2006. A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J. Immunol. 176:2161-2172.
16. Jakubzick, C., et al. 2008. Blood monocyte subsets differentially give rise to CD103+ and CD103-pulmonary dendritic cell populations. J. Immunol. 180:3019-3027.
17. Sun, C.M., et al. 2007. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204:1775-1785.
18. Vermaelen, K.Y., Carro-Muino, I., Lambrecht, B.N., and Pauwels, R.A. 2001. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J. Exp. Med. 193:51-60.
19. Forster, R., Davalos-Misslitz, A.C., and Rot, A. 2008. CCR7 and its ligands: balancing immunity and tolerance. Nat. Rev. Immunol. 8:362-371.
20. Forster, R., et al. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell. 99:23-33.
21. Ohl, L., et al. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steadystate conditions. Immunity. 21:279-288.
22. Ehst, B.D., Ingulli, E., and Jenkins, M.K. 2003. Development of a novel transgenic mouse for the study of interactions between CD4 and CD8 T cells during graft rejection. Am. J. Transplant. 3:1355-1362.
23. Das, S.K., Lim, H., Paria, B.C., and Dey, S.K. 1999. Cyclin D3 in the mouse uterus is associated with the decidualization process during early pregnancy. J. Mol. Endocrinol. 22:91-101.
24. Red-Horse, K., et al. 2006. Cytotrophoblast induction of arterial apoptosis and lymphangiogenesis in an in vivo model of human placentation. J. Clin. Invest. 116:2643-2652.
25. Bany, B.M., and Cross, J.C. 2006. Post-implantation mouse conceptuses produce paracrine signals that regulate the uterine endometrium undergoing decidualization. Dev. Biol. 294:445-456.
26. Roake, J.A., et al. 1995. Dendritic cell loss from nonlymphoid tissues after systemic administration of lipopolysaccharide, tumor necrosis factor, and interleukin 1. J. Exp. Med. 181:2237-2247.
27. Brandon, J.M. 1995. Macrophage distribution in decidual tissue from early implantation to the periparturient period in mice as defined by the macrophage differentiation antigens F4/80, macrosialin and the type 3 complement receptor. J. Reprod. Fertil. 103:9-16.
28. Stewart, I.J., and Mitchell, B.S. 1991. The distribution of uterine macrophages in virgin and early pregnant mice. J. Anat. 179:183-196.
29. Pollard, J.W., Hunt, J.S., Wiktor-Jedrzejczak, W., and Stanley, E.R. 1991. A pregnancy defect in the osteopetrotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dev. Biol. 148:273-283.
30. Game, D.S., and Lechler, R.I. 2002. Pathways of allorecognition: implications for transplantation tolerance. Transpl. Immunol. 10:101-108.
31. Lafferty, K.J., Prowse, S.J., Simeonovic, C.J., and Warren, H.S. 1983. Immunobiology of tissue transplantation: a return to the passenger leukocyte concept. Annu. Rev. Immunol. 1:143-173.
32. Barker, C.F., and Billingham, R.E. 1968. The role of afferent lymphatics in the rejection of skin homografts. J. Exp. Med. 128:197-221.
33. Itano, A.A., et al. 2003. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity. 19:47-57.
34. Allenspach, E.J., Lemos, M.P., Porrett, P.M., Turka, L.A., and Laufer, T.M. 2008. Migratory and lymphoid-resident dendritic cells cooperate to efficiently prime naive CD4 T cells. Immunity. 29:795-806.
35. Farrar, J.D., and Carson, D.D. 1992. Differential temporal and spatial expression of mRNA encoding extracellular matrix components in decidua during the peri-implantation period. Biol. Reprod. 46:1095-1108.
36. Wewer, U.M., Damjanov, A., Weiss, J., Liotta, L.A., and Damjanov, I. 1986. Mouse endometrial stromal cells produce basement-membrane components. Differentiation. 32:49-58.
37. Brown, J.J., and Papaioannou, V.E. 1992. Distribution of hyaluronan in the mouse endometrium during the periimplantation period of pregnancy. Differentiation. 52:61-68.
38. Mummert, D.I., Takashima, A., Ellinger, L., and Mummert, M.E. 2003. Involvement of hyaluronan in epidermal Langerhans cell maturation and migration in vivo. J. Dermatol. Sci. 33:91-97.
39. Mummert, M.E., Mohamadzadeh, M., Mummert, D.I., Mizumoto, N., and Takashima, A. 2000. Development of a peptide inhibitor of hyaluronan-mediated leukocyte trafficking. J. Exp. Med. 192:769-779.
40. San Martin, S., Soto-Suazo, M., and Zorn, T.M. 2003. Distribution of versican and hyaluronan in the mouse uterus during decidualization. Braz. J. Med. Biol. Res. 36:1067-1071.
41. Weiss, J.M., et al. 1997. An essential role for CD44 variant isoforms in epidermal Langerhans cell and blood dendritic cell function. J. Cell Biol. 137:1137-1147.
42. Red-Horse, K. 2008. Lymphatic vessel dynamics in the uterine wall. Placenta. 29(Suppl. A):S55-S59.
43. Mitchell, M.H., Swanson, R.J., and Oehninger, S. 2002. In vivo effect of leukemia inhibitory factor (LIF) and an anti-LIF polyclonal antibody on murine embryo and fetal development following exposure at the time of transcervical blastocyst transfer. Biol. Reprod. 67:460-464.
44. Erlebacher, A., Zhang, D., Parlow, A.F., and Glimcher, L.H. 2004. Ovarian insufficiency and early pregnancy loss induced by activation of the innate immune system. J. Clin. Invest. 114:39-48.
45. Barnden, M.J., Allison, J., Heath, W.R., and Carbone, F.R. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76:34-40.
46. Nagy, A., Gertsenstein, M., Vintersten, K., and Behringer, R. 2003. Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, New York, USA. 764 pp.