Immunology of the maternal-fetal interface

Annual Review of Immunology

Volumn 31, Issue , 2013, Pages 387-411

  Erlebacher, Adrian ^a  

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

Author keywords

Decidua; Immune privilege; Leukocyte; Pregnancy

Indexed keywords

ANTIGEN SPECIFICITY; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CHORIOAMNIONITIS; CONGENITAL INFECTION; DECIDUA; DENDRITIC CELL; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGY; LEUKOCYTE; MACROPHAGE; MATERNAL CARE; METRITIS; MOTHER FETUS RELATIONSHIP; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PREECLAMPSIA; PREGNANCY; PREMATURE LABOR; PRENATAL GROWTH; PRIORITY JOURNAL; SPONTANEOUS ABORTION; T LYMPHOCYTE; UTERUS;

ANIMALS; CELL DIFFERENTIATION; DECIDUA; EMBRYO IMPLANTATION; FEMALE; HUMANS; KILLER CELLS, NATURAL; MATERNAL-FETAL EXCHANGE; PLACENTA; PREGNANCY;

EID: 84875532171     PISSN: 07320582     EISSN: 15453278     Source Type: Book Series    
DOI: 10.1146/annurev-immunol-032712-100003     Document Type: Article

References (150)

1. Salmon JE, de Groot PG. 2008. Pathogenic role of antiphospholipid antibodies. Lupus 17:405-111
2. Dekel N, Gnainsky Y, Granot I, Mor G. 2010. Inflammation and implantation. Am. J. Reprod. Immunol. 63:17-211
3. Mold JE, McCune JM. 2012. Immunological tolerance during fetal development: from mouse to man. Adv. Immunol. 115:73-1111
4. Nelson JL. 2012. The otherness of self:microchimerism in health and disease. Trends Immunol. 33:421-277
5. Munoz-Suano A, Hamilton AB, Betz AG. 2011. Gimme shelter: the immune system during pregnancy. Immunol. Rev. 241:20-388
6. Taglauer ES, Adams Waldorf KM, Petroff MG. 2010. The hidden maternal-fetal interface: events involving the lymphoid organs in maternal-fetal tolerance. Int. J. Dev. Biol. 54:421-300
7. Medawar PB. 1953. Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp. Soc. Exp. Biol. 7:320-388
8. Moffett A, Loke C. 2006. Immunology of placentation in eutherian mammals. Nat. Rev. Immunol. 6:584-944
9. Maltepe E, Bakardjiev AI, Fisher SJ. 2010. The placenta: transcriptional, epigenetic, and physiological integration during development. J. Clin. Investig. 120:1016-255
10. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, et al. 2004. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J. Clin. Investig. 114:744-544
11. Cartwright JE, Fraser R, Leslie K, Wallace AE, James JL. 2010. Remodelling at the maternal-fetal interface: relevance to human pregnancy disorders. Reproduction 140:803-133
12. Dey SK, Lim H, Das SK, Reese J, Paria BC, et al. 2004. Molecular cues to implantation. Endocr. Rev. 25:341-733
13. Gellersen B, Brosens IA, Brosens JJ. 2007. Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives. Semin. Reprod. Med. 25:445-533
14. Trundley A, Moffett A. 2004. Human uterine leukocytes and pregnancy. Tissue Antigens 63:1-122
15. Bulmer JN, Williams PJ, Lash GE. 2010. Immune cells in the placental bed. Int. J. Dev. Biol. 54:281-944
16. Tagliani E, Shi C, Nancy P, Tay CS, Pamer EG, Erlebacher A. 2011. Coordinate regulation of tissue macrophage and dendritic cell population dynamics by CSF-1. J. Exp. Med. 208:1901-166
17. Nancy P, Tagliani E, Tay CS, Asp P, Levy DE, Erlebacher A. 2012. Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface. Science 336:1317-211
18. Kruse A, Merchant MJ, Hallmann R, Butcher EC. 1999. Evidence of specialized leukocyte-vascular homing interactions at the maternal/fetal interface. Eur. J. Immunol. 29:1116-266
19. Zhang J, Chen Z, Smith GN, Croy BA. 2011. Natural killer cell-triggered vascular transformation: maternal care before birth? Cell. Mol. Immunol. 8:1-111
20. Chazara O, Xiong S, Moffett A. 2011. Maternal KIR and fetal HLA-C: a fine balance. J. Leukoc. Biol. 90:703-166
21. Manaster I, Mandelboim O. 2010. The unique properties of uterine NK cells. Am. J. Reprod. Immunol. 63:434-444
22. Wallace AE, Fraser R, Cartwright JE. 2012. Extravillous trophoblast and decidual natural killer cells: a remodelling partnership. Hum. Reprod. Update 18:458-711
23. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, et al. 2003. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 198:1201-122
24. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, et al. 2006. DecidualNKcells regulate key developmental processes at the human fetal-maternal interface. Nat. Med. 12:1065-744
25. Kitaya K, Yasuda J, Yagi I, Tada Y, Fushiki S, Honjo H. 2000. IL-15 expression at human endometrium and decidua. Biol. Reprod. 63:683-877
26. Keskin DB, Allan DS, Rybalov B, Andzelm MM, Stern JN, et al. 2007. TGFβ promotes conversion of CD16+ peripheral blood NK cells into CD16 NK cells with similarities to decidual NK cells. Proc. Natl. Acad. Sci. USA 104:3378-833
27. Manaster I, Mizrahi S, Goldman-Wohl D, Sela HY, Stern-Ginossar N, et al. 2008. Endometrial NK cells are special immature cells that await pregnancy. J. Immunol. 181:1869-766
28. Male V, Sharkey A, Masters L, Kennedy PR, Farrell LE, Moffett A. 2011. The effect of pregnancy on the uterine NK cell KIR repertoire. Eur. J. Immunol. 41:3017-277
29. Mallidi TV, Craig LE, Schloemann SR, Riley JK. 2009. Murine endometrial and decidual NK1.1+ natural killer cells display a B220+CD11c+ cell surface phenotype. Biol. Reprod. 81:310-188
30. Ashkar AA, Black GP, Wei Q, He H, Liang L, et al. 2003. Assessment of requirements for IL-15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy. J. Immunol. 171:2937-444
31. Ye W, Zheng LM, Young JD, Liu CC. 1996. The involvement of interleukin (IL)-15 in regulating the differentiation of granulated metrial gland cells in mouse pregnant uterus. J. Exp. Med. 184:2405-100
32. Verma S, Hiby SE, Loke YW, King A. 2000. Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol. Reprod. 62:959-688
33. Kiso Y, Pollard JW, Croy BA. 1992. A study of granulated metrial gland cell differentiation in pregnant, macrophage-deficient, osteopetrotic (op/op) mice. Experientia 48:973-755
34. Kopcow HD, Eriksson M, Mselle TF, Damrauer SM, Wira CR, et al. 2010. Human decidual NK cells from gravid uteri andNKcells from cycling endometrium are distinctNKcell subsets. Placenta 31:334-388
35. Kam EP, Gardner L, Loke YW, King A. 1999. The role of trophoblast in the physiological change in decidual spiral arteries. Hum. Reprod. 14:2131-388
36. Smith SD, Dunk CE, Aplin JD, Harris LK, Jones RL. 2009. Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy. Am. J. Pathol. 174:1959-711
37. Khong TY, De Wolf F, Robertson WB, Brosens I. 1986. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational-age infants. Br. J. Obstet. Gynaecol. 93:1049-599
38. Young BC, Levine RJ, Karumanchi SA. 2010. Pathogenesis of preeclampsia. Annu. Rev. Pathol. Mech. Dis. 5:173-922
39. Ashkar AA, Di Santo JP, Croy BA. 2000. Interferon γcontributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J. Exp. Med. 192:259-700
40. Apps R, Sharkey A, Gardner L, Male V, Kennedy P, et al. 2011. Ex vivo functional responses to HLA-G differ between blood and decidual NK cells. Mol. Hum. Reprod. 17:577-866
41. Parham P, Norman PJ, Abi-Rached L, Hilton HG, Guethlein LA. 2012. Review: immunogenetics of human placentation. Placenta 33(Suppl.):S71-800
42. Hiby SE, Walker JJ, O'Shaughnessy KM, Redman CW, Carrington M, et al. 2004. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200:957-655
43. Hiby SE, Apps R, Sharkey AM, Farrell LE, Gardner L, et al. 2010. Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Investig. 120:4102-100
44. Madeja Z, Yadi H, Apps R, Boulenouar S, Roper SJ, et al. 2011. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc. Natl. Acad. Sci. USA 108:4012-177
45. Leno-Duran E, Hatta K, Bianco J, Yamada AT, Ruiz-Ruiz C, et al. 2010. Fetal-placental hypoxia does not result from failure of spiral arterial modification in mice. Placenta 31:731-377
46. Burke SD, Barrette VF, Bianco J, Thorne JG, Yamada AT, et al. 2010. Spiral arterial remodeling is not essential for normal blood pressure regulation in pregnant mice. Hypertension 55:729-377
47. Zhang J, Adams MA, Croy BA. 2011. Alterations in maternal and fetal heart functions accompany failed spiral arterial remodeling in pregnant mice. Am. J. Obstet. Gynecol. 205:485.e1-166
48. Hazan AD, Smith SD, Jones RL, WhittleW, Lye SJ, Dunk CE. 2010. Vascular-leukocyte interactions: mechanisms of human decidual spiral artery remodeling in vitro. Am. J. Pathol. 177:1017-300
49. Hu Y, Dutz JP, MacCalman CD, Yong P, Tan R, von Dadelszen P. 2006. Decidual NK cells alter in vitro first trimester extravillous cytotrophoblast migration: a role for IFN-γ. J. Immunol. 177:8522-300
50. Chakraborty D, Rumi MA, Konno T, Soares MJ. 2011. Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions. Proc. Natl. Acad. Sci. USA 108:16295-3000
51. Fraser R, Whitley GS, Johnstone AP, Host AJ, Sebire NJ, et al. 2012. Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance. J. Pathol. 228:322-322
52. Cnossen JS, Morris RK, ter Riet G, Mol BW, van der Post JA, et al. 2008. Use of uterine artery Doppler ultrasonography to predict pre-eclampsia and intrauterine growth restriction: a systematic review and bivariable meta-analysis. CMAJ 178:701-111
53. Raulet DH. 2006. Missing self recognition and self tolerance of natural killer (NK) cells. Semin. Immunol. 18:145-500
54. Apps R, Gardner L, Moffett A. 2008. A critical look at HLA-G. Trends Immunol. 29:313-211
55. Robertson SA, Care AS, Skinner RJ. 2007. Interleukin 10 regulates inflammatory cytokine synthesis to protect against lipopolysaccharide-induced abortion and fetal growth restriction in mice. Biol. Reprod. 76:738-488
56. Murphy SP, Fast LD, Hanna NN, Sharma S. 2005. Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J. Immunol. 175:4084-900
57. Murphy SP, Hanna NN, Fast LD, Shaw SK, Berg G, et al. 2009. Evidence for participation of uterine natural killer cells in the mechanisms responsible for spontaneous preterm labor and delivery. Am. J. Obstet. Gynecol. 200:308.e1-99
58. Thaxton JE, Sharma S. 2010. Interleukin-10: amulti-faceted agent of pregnancy. Am. J. Reprod. Immunol. 63:482-911
59. QiuX, Zhu L, Pollard JW. 2009. Colony-stimulating factor-1-dependent macrophage functions regulate the maternal decidua immune responses against Listeria monocytogenes infections during early gestation in mice. Infect. Immun. 77:85-977
60. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG. 1993. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J. Immunol. 151:4562-733
61. BainesMG, Duclos AJ, AnteckaE, HaddadEK. 1997. Decidual infiltration and activation ofmacrophages leads to early embryo loss. Am. J. Reprod. Immunol. 37:471-777
62. Soilleux EJ, Morris LS, Lee B, Pohlmann S, Trowsdale J, et al. 2001. Placental expression of DC-SIGN may mediate intrauterine vertical transmission of HIV. J. Pathol. 195:586-922
63. Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TB, et al. 2003. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am. J. Pathol. 162:887-966
64. Soilleux EJ, Morris LS, Leslie G, Chehimi J, Luo Q, et al. 2002. Constitutive and induced expression of DC-SIGN on dendritic cell and macrophage subpopulations in situ and in vitro. J. Leukoc. Biol. 71:445-577
65. Ochoa MT, Loncaric A, Krutzik SR, Becker TC, Modlin RL. 2008. "Dermal dendritic cells" comprise two distinct populations: CD1+ dendritic cells and CD209+ macrophages. J. Investig. Dermatol. 128:2225-311
66. Rieger L, Honig A, Sutterlin M, Kapp M, Dietl J, et al. 2004. Antigen-presenting cells in human endometrium during the menstrual cycle compared to early pregnancy. J. Soc. Gynecol. Investig. 11:488-933
67. Gustafsson C, Mjosberg J, Matussek A, Geffers R, Matthiesen L, et al. 2008. Gene expression profiling of human decidual macrophages: evidence for immunosuppressive phenotype. PLoS ONE 3:e20788
68. Cupurdija K, Azzola D, Hainz U, Gratchev A, Heitger A, et al. 2004. Macrophages of human first trimester decidua express markers associated to alternative activation. Am. J. Reprod. Immunol. 51:117-222
69. Lidstrom C, Matthiesen L, BergG, Sharma S, Ernerudh J, Ekerfelt C. 2003. Cytokine secretion patterns of NK cells and macrophages in early human pregnancy decidua and blood: implications for suppressor macrophages in decidua. Am. J. Reprod. Immunol. 50:444-522
70. Heikkinen J, Mottonen M, Komi J, Alanen A, Lassila O. 2003. Phenotypic characterization of human decidual macrophages. Clin. Exp. Immunol. 131:498-5055
71. Nagamatsu T, Schust DJ. 2010. The contribution of macrophages to normal and pathological pregnancies. Am. J. Reprod. Immunol. 63:460-711
72. Renaud SJ, Graham CH. 2008. The role of macrophages in utero-placental interactions during normal and pathological pregnancy. Immunol. Investig. 37:535-644
73. Svensson J, Jenmalm MC, Matussek A, Geffers R, Berg G, Ernerudh J. 2011. Macrophages at the fetal-maternal interface express markers of alternative activation and are induced by M-CSF and IL-10. J. Immunol. 187:3671-822
74. Houser BL, Tilburgs T, Hill J, Nicotra ML, Strominger JL. 2011. Two unique human decidual macrophage populations. J. Immunol. 186:2633-422
75. Schonkeren D, van der HoornML, Khedoe P, Swings G, van Beelen E, et al. 2011. Differential distribution and phenotype of decidual macrophages in preeclamptic versus control pregnancies. Am. J. Pathol. 178:709-177
76. Reister F, Frank HG, Heyl W, Kosanke G, Huppertz B, et al. 1999. The distribution of macrophages in spiral arteries of the placental bed in pre-eclampsia differs from that in healthy patients. Placenta 20:229-333
77. Lockwood CJ, Matta P, Krikun G, Koopman LA, Masch R, et al. 2006. Regulation ofmonocyte chemoattractant protein-1 expression by tumor necrosis factor-α and interleukin-1β in first trimester human decidual cells: implications for preeclampsia. Am. J. Pathol. 168:445-522
78. Huang SJ, Chen CP, Schatz F, Rahman M, Abrahams VM, Lockwood CJ. 2008. Pre-eclampsia is associated with dendritic cell recruitment into the uterine decidua. J. Pathol. 214:328-366
79. Rieger L, Segerer S, Bernar T, KappM, Majic M, et al. 2009. Specific subsets of immune cells in human decidua differ between normal pregnancy and preeclampsia - A prospective observational study. Reprod. Biol. Endocrinol. 7:1322
80. Redline RW. 2001. Macrophages in the basal plate of pre-eclamptic placentae. Placenta 22:890-933
81. Kim JS, Romero R, Cushenberry E, Kim YM, Erez O, et al. 2007. Distribution of CD14+ and CD68+ macrophages in the placental bed and basal plate of women with preeclampsia and preterm labor. Placenta 28:571-766
82. Romero R, Espinoza J, Kusanovic JP, Gotsch F, Hassan S, et al. 2006. The preterm parturition syndrome. Br. J. Obstet. Gynaecol. 113(Suppl. 3):17-422
83. Hamilton S, Oomomian Y, Stephen G, Shynlova O, Tower CL, et al. 2012. Macrophages infiltrate the human and rat decidua during term and preterm labor: evidence that decidual inflammation precedes labor. Biol. Reprod. 86:399
84. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. 1991. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum. Reprod. 6:791-988
85. Pollard JW, Hunt JS, Wiktor-Jedrzejczak W, Stanley ER. 1991. A pregnancy defect in the osteopetrotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dev. Biol. 148:273-833
86. Stewart IJ, Mitchell BS. 1991. The distribution of uterine macrophages in virgin and early pregnant mice. J. Anat. 179:183-966
87. Brandon JM. 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. 103:9-166
88. CollinsMK, Tay CS, Erlebacher A. 2009. Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. J. Clin. Investig. 119:2062-733
89. Kauma SW, Aukerman SL, Eierman D, Turner T. 1991. Colony-stimulating factor-1 and c-fms expression in human endometrial tissues and placenta during the menstrual cycle and early pregnancy. J. Clin. Endocrinol. Metab. 73:746-511
90. Daiter E, Pampfer S, Yeung YG, Barad D, Stanley ER, Pollard JW. 1992. Expression of colonystimulating factor-1 in the human uterus and placenta. J. Clin. Endocrinol. Metab. 74:850-588
91. Jokhi PP, King A, Boocock C, Loke YW. 1995. Secretion of colony stimulating factor-1 by human first trimester placental and decidual cell populations and the effect of this cytokine on trophoblast thymidine uptake in vitro. Hum. Reprod. 10:2800-77
92. Engert S, Rieger L, Kapp M, Becker JC, Dietl J, KammererU. 2007. Profiling chemokines, cytokines and growth factors in human early pregnancy decidua by protein array. Am. J. Reprod. Immunol. 58:129-377
93. Cho CH, Koh YJ, Han J, Sung HK, Jong Lee H, et al. 2007. Angiogenic role of LYVE-1-positive macrophages in adipose tissue. Circ. Res. 100:e47-577
94. Ivanisevic M, Segerer S, Rieger L, Kapp M, Dietl J, et al. 2010. Antigen-presenting cells in pregnant and non-pregnant human myometrium. Am. J. Reprod. Immunol. 64:188-966
95. Tagliani E, Erlebacher A. 2011. Dendritic cell function at the maternal-fetal interface. Expert Rev. Clin. Immunol. 7:593-6022
96. Kammerer U, SchoppetM, McLellan AD, Kapp M, Huppertz HI, et al. 2000. Human decidua contains potent immunostimulatory CD83+ dendritic cells. Am. J. Pathol. 157:159-699
97. Kemp B, Schmitz S, Krusche CA, Rath W, von Rango U. 2011. Dendritic cells are equally distributed in intrauterine and tubal ectopic pregnancies. Fertil. Steril. 95:28-322
98. Ban YL, Kong BH, Qu X, Yang QF, Ma YY. 2008. BDCA-1+, BDCA-2+ and BDCA-3+ dendritic cells in early human pregnancy decidua. Clin. Exp. Immunol. 151:399-4066
99. Miyazaki S, Tsuda H, SakaiM, Hori S, Sasaki Y, et al. 2003. Predominance of Th2-promoting dendritic cells in early human pregnancy decidua. J. Leukoc. Biol. 74:514-222
100. Gardner L, Moffett A. 2003. Dendritic cells in the human decidua. Biol. Reprod. 69:1438-466
101. Red-Horse K, Rivera J, Schanz A, Zhou Y, Winn V, et al. 2006. Cytotrophoblast induction of arterial apoptosis and lymphangiogenesis in an in vivo model of human placentation. J. Clin. Investig. 116:2643-522
102. Volchek M, Girling JE, Lash GE, Cann L, Kumar B, et al. 2010. Lymphatics in the human endometrium disappear during decidualization. Hum. Reprod. 25:2455-644
103. Askelund K, Liddell HS, Zanderigo AM, Fernando NS, Khong TY, et al. 2004. CD83+ dendritic cells in the decidua of women with recurrent miscarriage and normal pregnancy. Placenta 25:140-455
104. Plaks V, Birnberg T, Berkutzki T, Sela S, Benyashar A, et al. 2008. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Investig. 118:3954-655
105. Krey G, Frank P, Shaikly V, Barrientos G, Cordo-Russo R, et al. 2008. In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development inmice. J. Mol. Med. 86:999-10111
106. Tilburgs T, van der Mast BJ, Nagtzaam NM, Roelen DL, Scherjon SA, Claas FH. 2009. Expression of NK cell receptors on decidual T cells in human pregnancy. J. Reprod. Immunol. 80:22-322
107. Vassiliadou N, Bulmer JN. 1996. Quantitative analysis of T lymphocyte subsets in pregnant and nonpregnant human endometrium. Biol. Reprod. 55:1017-222
108. Marlin R, Nugeyre MT, Duriez M, Cannou C, Le Breton A, et al. 2011. Decidual soluble factors participate in the control of HIV-1 infection at the maternofetal interface. Retrovirology 8:588
109. Mjosberg J, Berg G, Jenmalm MC, Ernerudh J. 2010. FOXP3+ regulatory T cells and T helper 1, T helper 2, and T helper 17 cells in human early pregnancy decidua. Biol. Reprod. 82:698-7055
110. Tilburgs T, Claas FH, Scherjon SA. 2010. Elsevier Trophoblast Research Award Lecture: Unique properties of decidual T cells and their role in immune regulation during human pregnancy. Placenta 31(Suppl.):S82-866
111. Tilburgs T, Roelen DL, van der Mast BJ, de Groot-Swings GM, Kleijburg C, et al. 2008. Evidence for a selective migration of fetus-specific CD4+CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J. Immunol. 180:5737-455
112. Tilburgs T, Roelen DL, van derMast BJ, van Schip JJ, Kleijburg C, et al. 2006. Differential distribution of CD4+CD25bright and CD8+CD28; T-cells in decidua andmaternal blood during human pregnancy. Placenta 27(Suppl. A):S47-533
113. Sasaki Y, Darmochwal-Kolarz D, Suzuki D, Sakai M, ItoM, et al. 2007. Proportion of peripheral blood and decidual CD4+ CD25bright regulatory T cells in pre-eclampsia. Clin. Exp. Immunol. 149:139-455
114. Saito S, Nakashima A, Shima T, Ito M. 2010. Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am. J. Reprod. Immunol. 63:601-100
115. Sasaki Y, Sakai M, Miyazaki S, Higuma S, Shiozaki A, Saito S. 2004. Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod. 10:347-533
116. Nakashima A, Ito M, Shima T, Bac ND, Hidaka T, Saito S. 2010. Accumulation of IL-17-positive cells in decidua of inevitable abortion cases. Am. J. Reprod. Immunol. 64:4-111
117. Piccinni MP, Beloni L, Livi C, Maggi E, Scarselli G, Romagnani S. 1998. Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat. Med. 4:1020-244
118. Kim CJ, Romero R, Kusanovic JP, YooW, Dong Z, et al. 2010. The frequency, clinical significance, and pathological features of chronic chorioamnionitis: a lesion associated with spontaneous preterm birth. Mod. Pathol. 23:1000-111
119. Edmondson N, Bocking A, Machin G, Rizek R, Watson C, Keating S. 2009. The prevalence of chronic deciduitis in cases of preterm labor without clinical chorioamnionitis. Pediatr. Dev. Pathol. 12:16-211
120. Redline RW. 2007. Villitis of unknown etiology: noninfectious chronic villitis in the placenta. Hum. Pathol. 38:1439-466
121. Tilburgs T, Scherjon SA, van der Mast BJ, Haasnoot GW, Versteeg-v.d. Voort Maarschalk M, et al. Fetal-maternal HLA-C mismatch is associated with decidual T cell activation and induction of functional T regulatory cells. J. Reprod. Immunol. 82:148-577
122. Unutmaz D, Pileri P, Abrignani S. 1994. Antigen-independent activation of naive and memory resting T cells by a cytokine combination. J. Exp. Med. 180:1159-644
123. Reinhardt RL, Bullard DC, Weaver CT, Jenkins MK. 2003. Preferential accumulation of antigenspecific effector CD4 T cells at an antigen injection site involves CD62E-dependent migration but not local proliferation. J. Exp. Med. 197:751-622
124. Masopust D, Vezys V, Usherwood EJ, Cauley LS, Olson S, et al. 2004. Activated primary and memory CD8Tcells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J. Immunol. 172:4875-822
125. Erlebacher A, Vencato D, Price KA, Zhang D, Glimcher LH. 2007. Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J. Clin. Investig. 117:1399-4111
126. Samstein RM, Josefowicz SZ, Arvey A, Treuting PM, Rudensky AY. 2012. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 150:29-388
127. Erlebacher A. 2010. Immune surveillance of the maternal/fetal interface: controversies and implications. Trends Endocrinol. Metab. 21:428-344
128. Schumacher A, Brachwitz N, Sohr S, Engeland K, Langwisch S, et al. 2009. Human chorionic gonadotropin attracts regulatory T cells into the fetal-maternal interface during early human pregnancy. J. Immunol. 182:5488-977
129. Kopcow HD, Rosetti F, Leung Y, Allan DS, Kutok JL, Strominger JL. 2008. T cell apoptosis at the maternal-fetal interface in early human pregnancy, involvement of galectin-1. Proc. Natl. Acad. Sci. USA 105:18472-777
130. Benirschke K, Kaufmann P, Baergen RN. 2006. Pathology of the Human Placenta. New York: Springerr
131. Robbins JR, Bakardjiev AI. 2012. Pathogens and the placental fortress. Curr. Opin. Microbiol. 15:36-433
132. Gandhi MK, Khanna R. 2004. Human cytomegalovirus: clinical aspects, immune regulation, and emerging treatments. Lancet Infect. Dis. 4:725-388
133. SnyderCM. 2011. Buffered memory: a hypothesis for themaintenance of functional, virus-specificCD8-T cells during cytomegalovirus infection. Immunol. Res. 51:195-2044
134. Pereira L, Maidji E, McDonagh S, Genbacev O, Fisher S. 2003. Human cytomegalovirus transmission from the uterus to the placenta correlates with the presence of pathogenic bacteria and maternal immunity. J. Virol. 77:13301-144
135. McDonagh S, Maidji E, Ma W, Chang HT, Fisher S, Pereira L. 2004. Viral and bacterial pathogens at the maternal-fetal interface. J. Infect. Dis. 190:826-344
136. Tamiolakis D, Venizelos I, Lambropoulou M, Kotini A, Barbagadaki S, et al. 2004. Human decidual cells activity in women with spontaneous abortions of probable CMV aetiology during the first trimester of gestation. An immunohistochemical study with CMV-associated antigen. Acta Medica (Hradec Kralove) 47:195-999
137. Pamer EG. 2004. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4:812-233
138. Robbins JR, Skrzypczynska KM, Zeldovich VB, Kapidzic M, Bakardjiev AI. 2010. Placental syncytiotrophoblast constitutes a major barrier to vertical transmission of Listeria monocytogenes. PLoS Pathog. 6:e10007322
139. Redline RW, Lu CY. 1988. Specific defects in the anti-listerial immune response in discrete regions of the murine uterus and placenta account for susceptibility to infection. J. Immunol. 140:3947-555
140. Bakardjiev AI, Theriot JA, Portnoy DA. 2006. Listeria monocytogenes traffics from maternal organs to the placenta and back. PLoS Pathog. 2:e666
141. Redline RW, Lu CY. 1987. Role of local immunosuppression in murine fetoplacental listeriosis. J. Clin. Investig. 79:1234-411
142. Zeldovich VB, Robbins JR, Kapidzic M, Lauer P, Bakardjiev AI. 2011. Invasive extravillous trophoblasts restrict intracellular growth and spread of Listeria monocytogenes. PLoS Pathog. 7:e10020055
143. Jokhi PP, Chumbley G, King A, Gardner L, Loke YW. 1993. Expression of the colony stimulating factor-1 receptor (c-fms product) by cells at the human uteroplacental interface. Lab. Investig. 68:308-200
144. Schatz F, Kayisli UA, Vatandaslar E, Ocak N, Guller S, et al. 2012. Toll-like receptor 4 expression in decidual cells and interstitial trophoblasts across human pregnancy. Am. J. Reprod. Immunol. 68:146-533
145. Koga K, Mor G. 2010. Toll-like receptors at the maternal-fetal interface in normal pregnancy and pregnancy disorders. Am. J. Reprod. Immunol. 63:587-6000
146. Thaxton JE, NeversTA, Sharma S. 2010. TLR-mediated preterm birth in response to pathogenic agents. Infect. Dis. Obstet. Gynecol. 2010:3784722
147. Sonnenberg GF, Fouser LA, Artis D. 2011. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 12:383-900
148. Ito M, Nakashima A, Hidaka T, Okabe M, Bac ND, et al. 2010. A role for IL-17 in induction of an inflammation at the fetomaternal interface in preterm labour. J. Reprod. Immunol. 84:75-855
149. Hamill N, Romero R, Gotsch F, Kusanovic JP, Edwin S, et al. 2008. Exodus-1 (CCL20): evidence for the participation of this chemokine in spontaneous labor at term, preterm labor, and intrauterine infection. J. Perinat. Med. 36:217-277
150. Bany BM, Cross JC. 2006. Post-implantation mouse conceptuses produce paracrine signals that regulate the uterine endometrium undergoing decidualization. Dev. Biol. 294:445-566