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Infection, Immune Homeostasis and Immune Privilege pp 53–91Cite as

The Role of Intrauterine Immune Privilege in Perinatal Infectious Diseases

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Part of the book series: Birkhäuser Advances in Infectious Diseases ((BAID))

Abstract

The pregnant uterus provides an immunologically “privileged” environment in which a genetically mismatched fetus typically thrives without deleterious allogeneic immune response. The mechanisms by which the fetus is protected from maternal immune attack are still incompletely understood but are undoubtedly multifactorial. Simple evasion of immune detection is no longer considered to be involved. There is now good evidence that the maternal immune system recognizes and responds to the presence of the fetus. However, maternal cellular and soluble immune responses, and those of the immunologically active, fetally derived trophoblast cells, generally support rather than harm the pregnancy. Gestational hormones and placenta-derived substances actively modulate maternal immunity and promote tolerance of the fetus. Still, the maternal immune system must continue to serve its protective role against pathogen invasion during pregnancy. Dramatic, pregnancy-related shifts in systemic and local immune responsiveness in the mother could compromise her ability to control infectious insults. To this point, clinical data indicate that pregnant women are more susceptible to specific types of viruses and parasites than their nonpregnant female counterparts. In this chapter, we will review the molecular mechanisms involved in creating the immunologically privileged intrauterine environment during pregnancy and discuss its costs to mother and fetus in terms of increased infectious disease risk.

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References

  • Al-husaini AM (2008) Role of placenta in the vertical transmission of human immunodeficiency virus. J Perinatol 29:331–336

    PubMed  Google Scholar 

  • Aluvihare VR, Kallikourdis M, Betz AG (2004) Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 5:266–271

    PubMed  CAS  Google Scholar 

  • Anderson J (1965) Immunological inertia in pregnancy. Nature 206:786–787

    PubMed  CAS  Google Scholar 

  • Anderson JM, Benirschke K (1964) Maternal tolerance of foetal tissue. Br Med J 1:1534–1535

    PubMed  CAS  Google Scholar 

  • Andrews WW, Hauth JC, Goldenberg RL (2000) Infection and preterm birth. Am J Perinatol 17:357–365

    PubMed  CAS  Google Scholar 

  • Aplin JD (1991) Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci 99:681–692

    PubMed  Google Scholar 

  • Aujla SJ, Dubin PJ, Kolls JK (2007) Th17 cells and mucosal host defense. Semin Immunol 19:377–382

    PubMed  CAS  Google Scholar 

  • Baban B, Chandler P, McCool D, Marshall B, Munn DH, Mellor AL (2004) Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J Reprod Immunol 61:67–77

    PubMed  CAS  Google Scholar 

  • Barel MT, Pizzato N, van Leeuwen D, Bouteiller PL, Wiertz EJ, Lenfant F (2003a) Amino acid composition of α1/α2 domains and cytoplasmic tail of MHC class I molecules determine their susceptibility to human cytomegalovirus US11-mediated down-regulation. Eur J Immunol 33:1707–1716

    PubMed  CAS  Google Scholar 

  • Barel MT, Ressing M, Pizzato N, van Leeuwen D, Le Bouteiller P, Lenfant F, Wiertz EJHJ (2003b) Human cytomegalovirus-encoded US2 differentially affects surface expression of MHC class I locus products and targets membrane-bound, but not soluble HLA-G1 for degradation. J Immunol 171:6757–6765

    PubMed  CAS  Google Scholar 

  • Barel MT, Pizzato N, Le Bouteiller P, Wiertz EJ, Lenfant F (2006) Subtle sequence variation among MHC class I locus products greatly influences sensitivity to HCMV US2- and US11-mediated degradation. Int Immunol 18:173–182

    PubMed  CAS  Google Scholar 

  • Baud O, Emilie D, Pelletier E, Lacaze-Masmonteil T, Zupan V, Fernandez H, Dehan M, Frydman R, Ville Y (1999) Amniotic fluid concentrations of interleukin-1beta, interleukin-6 and TNF-alpha in chorioamnionitis before 32 weeks of gestation: histological associations and neonatal outcome. Br J Obstet Gynaecol 106:72–77

    PubMed  CAS  Google Scholar 

  • Bianchi DW, Zickwolf GK, Weil GJ, Sylvester S, DeMaria MA (1996) Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proc Natl Acad Sci USA 93:705–708

    PubMed  CAS  Google Scholar 

  • Billington WD, Burrows FJ (1986) The rat placenta expresses paternal class I major histocompatibility antigens. J Reprod Immunol 9:155–160

    PubMed  CAS  Google Scholar 

  • Binstadt BA, Brumbaugh KM, Leibson PJ (1997) Signal transduction by human NK cell MHC-recognizing receptors. Immunol Rev 155:197–203

    PubMed  CAS  Google Scholar 

  • Blaschitz A, Hutter H, Dohr G (2001) HLA Class I protein expression in the human placenta. Early Pregnancy 5:67–69

    PubMed  CAS  Google Scholar 

  • Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, Cordo-Russo R, Toscano MA, Bianco GA, Kobelt P, Handjiski B, Tirado I, Markert UR, Klapp BF, Poirier F, Szekeres-Bartho J, Rabinovich GA, Arck PC (2007) A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 13:1450–1457

    PubMed  CAS  Google Scholar 

  • Brabin BJ (1983) An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61:1005–1016

    PubMed  CAS  Google Scholar 

  • Brocklehurst P, French R (1998) The association between maternal HIV infection and perinatal outcome: a systematic review of the literature and meta-analysis. Br J Obstet Gynaecol 105:836–848

    PubMed  CAS  Google Scholar 

  • Bulmer JN, Johnson PM (1984) Macrophage populations in the human placenta and amniochorion. Clin Exp Immunol 57:393–403

    PubMed  CAS  Google Scholar 

  • Bulmer JN, Johnson PM (1985) Antigen expression by trophoblast populations in the human placenta and their possible immunobiological relevance. Placenta 6:127–140

    PubMed  CAS  Google Scholar 

  • Butts CL, Shukair SA, Duncan KM, Bowers E, Horn C, Belyavskaya E, Tonelli L, Sternberg EM (2007) Progesterone inhibits mature rat dendritic cells in a receptor-mediated fashion. Int Immunol 19:287–296

    PubMed  CAS  Google Scholar 

  • Casares S, Richie TL (2009) Immune evasion by malaria parasites: a challenge for vaccine development. Curr Opin Immunol 21:321–330

    PubMed  CAS  Google Scholar 

  • Chapman TL, Heikema AP, Bjorkman PJ (1999) The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 11:603–613

    PubMed  CAS  Google Scholar 

  • Collins MK, Tay CS, Erlebacher A (2009) Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. J Clin Invest 119:2062–2073

    PubMed  CAS  Google Scholar 

  • Cooper MD, Alder MN (2006) The evolution of adaptive immune systems. Cell 124:815–822

    PubMed  CAS  Google Scholar 

  • Correale J, Arias M, Gilmore W (1998) Steroid hormone regulation of cytokine secretion by proteolipid protein-specific CD4+ T cell clones isolated from multiple sclerosis patients and normal control subjects. J Immunol 161:3365–3374

    PubMed  CAS  Google Scholar 

  • Cutolo M, Wilder R (2000) Different roles for androgens and estrogens in the susceptibility to autoimmune rheumatic diseases. Rheum Dis Clin North Am 26:825–839

    PubMed  CAS  Google Scholar 

  • Dai R, Phillips RA, Karpuzoglu E, Khan D, Ahmed SA (2009) Estrogen regulates transcription factors STAT-1 and NF-kappaB to promote inducible nitric oxide synthase and inflammatory responses. J Immunol 183:6998–7005

    PubMed  CAS  Google Scholar 

  • Darrasse-Jèze G, Klatzmann D, Charlotte F, Salomon BL, Cohen JL (2006) CD4 + CD25+ regulatory/suppressor T cells prevent allogeneic fetus rejection in mice. Immunol Lett 102:106–109

    PubMed  Google Scholar 

  • Debierre-Grockiego F, Campos MA, Azzouz N, Schmidt J, Bieker U, Resende MG, Mansur DS, Weingart R, Schmidt RR, Golenbock DT, Gazzinelli RT, Schwarz RT (2007) Activation of TLR2 and TLR4 by glycosylphosphatidylinositols derived from Toxoplasma gondii. J Immunol 179:1129–1137

    PubMed  CAS  Google Scholar 

  • Deshpande R, Khalili H, Pergolizzi RG, Michael SD, Chang MD (1997) Estradiol down-regulates LPS-induced cytokine production and NFkB activation in murine macrophages. Am J Reprod Immunol 38:46–54

    PubMed  CAS  Google Scholar 

  • Diouf I, Fievet N, Doucouré S, Ngom M, Andrieu M, Mathieu JF, Gaye A, Thiaw OT, Deloron P (2007) IL-12 producing monocytes and IFN-gamma and TNF-alpha producing T-lymphocytes are increased in placentas infected by plasmodium falciparum. J Reprod Immunol 74:152–162

    PubMed  CAS  Google Scholar 

  • Dodd JM, Flenady VJ, Cincotta R, Crowther CA (2008) Progesterone for the prevention of preterm birth: a systematic review. Obstet Gynecol 112:127–134

    PubMed  CAS  Google Scholar 

  • Donders GG, Van Calsteren K, Bellen G, Reybrouck R, Van den Bosch T, Riphagen I, Van Lierde S (2009) Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. BJOG 116:1315–1324

    PubMed  CAS  Google Scholar 

  • Dunn C, Chalupny NJ, Sutherland CL, Dosch S, Sivakumar PV, Johnson DC, Cosman D (2003) Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J Exp Med 197:1427–1439

    PubMed  CAS  Google Scholar 

  • 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 Invest 117:1399–1411

    PubMed  CAS  Google Scholar 

  • Estrada-Gutierrez G, Gomez-Lopez N, Zaga-Clavellina V, Giono-Cerezo S, Espejel-Nunez A, Gonzalez-Jimenez MA, Espino y Sosa S, Olson DM, Vadillo-Ortega F (2010) Interaction between pathogenic bacteria and intrauterine leukocytes triggers alternative molecular signaling cascades leading to labor in women. Infect Immun 78:4792–4799

    PubMed  CAS  Google Scholar 

  • Faust Z, Laskarin G, Rukavina D, Szekeres-Bartho J (1999) Progesterone-induced blocking factor inhibits degranulation of natural killer cells. Am J Reprod Immunol 42:71–75

    PubMed  CAS  Google Scholar 

  • Fielding CA, McLoughlin RM, Colmont CS, Kovaleva M, Harris DA, Rose-John S, Topley N, Jones SA (2005) Viral IL-6 blocks neutrophil infiltration during acute inflammation. J Immunol 175:4024–4029

    PubMed  CAS  Google Scholar 

  • Fievet N, Tami G, Maubert B, Moussa M, Shaw I, Cot M, Holder A, Chaouat G, Deloron P (2002) Cellular immune response to plasmodium falciparum after pregnancy is related to previous placental infection and parity. Malar J 1:16

    PubMed  Google Scholar 

  • Figueiró-Filho EA, Duarte G, El-Beitune P, Quintana SM, Maia TL (2004) Visceral leishmaniasis (kala-azar) and pregnancy. Infect Dis Obstet Gynecol 12:31–40

    PubMed  Google Scholar 

  • Fox HS, Bond BL, Parslow TG (1991) Estrogen regulates the IFN-gamma promoter. J Immunol 146:4362–4367

    PubMed  CAS  Google Scholar 

  • Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC, Horton HF, Fouser L, Carter L, Ling V, Bowman MR, Carreno BM, Collins M, Wood CR, Honjo T (2000) Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 192:1027–1034

    PubMed  CAS  Google Scholar 

  • Fried M, Duffy PE (1996) Adherence of plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272:1502–1504

    PubMed  CAS  Google Scholar 

  • Fried M, Muga RO, Misore AO, Duffy PE (1998) Malaria elicits type 1 cytokines in the human placenta: IFN-γ and TNF-α associated with pregnancy outcomes. J Immunol 160:2523–2530

    PubMed  CAS  Google Scholar 

  • Fujigaki S, Saito K, Takemura M, Maekawa N, Yamada Y, Wada H, Seishima M (2002) L-tryptophan-L-kynurenine pathway metabolism accelerated by Toxoplasma gondii infection is abolished in gamma interferon-gene-deficient mice: cross-regulation between inducible nitric oxide synthase and indoleamine-2,3-dioxygenase. Infect Immun 70:779–786

    PubMed  CAS  Google Scholar 

  • Fujii T, Ishitani A, Geraghty DE (1994) A soluble form of the HLA-G antigen is encoded by a messenger ribonucleic acid containing intron 4. J Immunol 153:5516–5524

    PubMed  CAS  Google Scholar 

  • Furman MH, Ploegh HL, Schust DJ (2000) Can viruses help us to understand and classify the MHC class I molecules at the maternal-fetal interface? Hum Immunol 61:1169–1176

    PubMed  CAS  Google Scholar 

  • Game DS, Lechler RI (2002) Pathways of allorecognition: implications for transplantation tolerance. Transpl Immunol 10:101–108

    PubMed  CAS  Google Scholar 

  • Gardner L, Moffett A (2003) Dendritic cells in the human decidua. Biol Reprod 69:1438–1446

    PubMed  CAS  Google Scholar 

  • Gerber S, Vial Y, Hohlfeld P, Witkin SS (2003) Detection of Ureaplasma urealyticum in second-trimester amniotic fluid by polymerase chain reaction correlates with subsequent preterm labor and delivery. J Infect Dis 187:518–521

    PubMed  Google Scholar 

  • Gewurz BE, Wang EW, Tortorella D, Schust DJ, Ploegh HL (2001) Human cytomegalovirus US2 endoplasmic reticulum-lumenal domain dictates association with major histocompatibility complex class I in a locus-specific manner. J Virol 75:5197–5204

    PubMed  CAS  Google Scholar 

  • Goldenberg RL, Hauth JC, Andrews WW (2000) Intrauterine infection and preterm delivery. N Engl J Med 342:1500–1507

    PubMed  CAS  Google Scholar 

  • González DA, Díaz BB, Rodríguez Pérez Mdel C, Hernández AG, Chico BN, de León AC (2010) Sex hormones and autoimmunity. Immunol Lett 133:6–13

    PubMed  Google Scholar 

  • Gregory MS, Duffner LA, Faunce DE, Kovacs EJ (2000) Estrogen mediates the sex difference in post-burn immunosuppression. J Endocrinol 164:129–138

    PubMed  CAS  Google Scholar 

  • Guleria I, Khosroshahi A, Ansari MJ, Habicht A, Azuma M, Yagita H, Noelle RJ, Coyle A, Mellor AL, Khoury SJ, Sayegh MH (2005) A critical role for the programmed death ligand 1 in fetomaternal tolerance. J Exp Med 202:231–237

    PubMed  CAS  Google Scholar 

  • Hanna J, Wald O, Goldman-Wohl D, Prus D, Markel G, Gazit R, Katz G, Haimov-Kochman R, Fujii N, Yagel S, Peled A, Mandelboim O (2003) CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood 102:1569–1577

    PubMed  CAS  Google Scholar 

  • Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V, Benharroch D, Porgador A, Keshet E, Yagel S, Mandelboim O (2006) Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 12:1065–1074

    PubMed  CAS  Google Scholar 

  • Hayakawa S, Nagai N, Kanaeda T, Karasaki-Suzuki M, Ishii M, Chishima F, Satoh K (1999) Interleukin-12 augments cytolytic activity of peripheral and decidual lymphocytes against choriocarcinoma cell lines and primary culture human placental trophoblasts. Am J Reprod Immunol 41:320–329

    PubMed  CAS  Google Scholar 

  • Hedley ML, Drake BL, Head JR, Tucker PW, Forman J (1989) Differential expression of the class I MHC genes in the embryo and placenta during midgestational development in the mouse. J Immunol 142:4046–4053

    PubMed  CAS  Google Scholar 

  • Heikkinen J, Möttönen M, Komi J, Alanen A, Lassila O (2003) Phenotypic characterization of human decidual macrophages. Clin Exp Immunol 131:498–505

    PubMed  CAS  Google Scholar 

  • Hiby SE, Regan L, Lo W, Farrell L, Carrington M, Moffett A (2008) Association of maternal killer-cell immunoglobulin-like receptors and parental HLA-C genotypes with recurrent miscarriage. Hum Reprod 23:972–976

    PubMed  CAS  Google Scholar 

  • Hiby SE, Apps R, Sharkey AM, Farrell LE, Gardner L, Mulder A, Claas FH, Walker JJ, Redman CW, Morgan L, Tower C, Regan L, Moore GE, Carrington M, Moffett A (2010) Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J Clin Invest 120:4102–4110

    PubMed  CAS  Google Scholar 

  • Hirose E (2003) Colonial allorecognition, hemolytic rejection, and viviparity in Botryllid ascidians. Zoolog Sci 20:387–394

    PubMed  Google Scholar 

  • Hirsch E, Filipovich Y, Mahendroo M (2006) Signaling via the type I IL-1 and TNF receptors is necessary for bacterially induced preterm labor in a murine model. Am J Obstet Gynecol 194:1334–1340

    PubMed  CAS  Google Scholar 

  • Hönig A, Rieger L, Kapp M, Sütterlin M, Dietl J, Kämmerer U (2004) Indoleamine 2,3-dioxygenase (IDO) expression in invasive extravillous trophoblast supports role of the enzyme for materno-fetal tolerance. J Reprod Immunol 61:79–86

    PubMed  Google Scholar 

  • Horowitz S, Mazor M, Romero R, Horowitz J, Glezerman M (1995) Infection of the amniotic cavity with Ureaplasma urealyticum in the midtrimester of pregnancy. J Reprod Med 40:375–379

    PubMed  CAS  Google Scholar 

  • Hunt JS, Vassmer D, Ferguson TA, Miller L (1997) Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus. J Immunol 158:4122–4128

    PubMed  CAS  Google Scholar 

  • Ilievski V, Lu SJ, Hirsch E (2007) Activation of toll-like receptors 2 or 3 and preterm delivery in the mouse. Reprod Sci 14:315–320

    PubMed  CAS  Google Scholar 

  • Ishihara O, Sulliban MH, Elder MG (1991) Differences of metabolism of prostaglandin E2 and F2 alpha by decidual stromal cells and macrophages in culture. Eicosanoids 4:203–207

    PubMed  CAS  Google Scholar 

  • Ishitani A, Geraghty DE (1992) Alternative splicing of HLA-G transcripts yields proteins with primary structures resembling both class I and class II antigens. Proc Natl Acad Sci USA 89:3947–3951

    PubMed  CAS  Google Scholar 

  • Ishitani A, Sageshima N, Lee N, Dorofeeva N, Hatake K, Marquardt H, Geraghty DE (2003) Protein expression and peptide binding suggest unique and interacting functional roles for HLA-E, F, and G in maternal-placental immune recognition. J Immunol 171:1376–1384

    PubMed  CAS  Google Scholar 

  • Jiang SP, Vacchio MS (1998) Multiple mechanisms of peripheral T cell tolerance to the fetal “allograft”. J Immunol 160:3086–3090

    PubMed  CAS  Google Scholar 

  • Jones LA, Anthony JP, Henriquez FL, Lyons RE, Nickdel MB, Carter KC, Alexander J, Roberts CW (2008) Toll-like receptor-4-mediated macrophage activation is differentially regulated by progesterone via the glucocorticoid and progesterone receptors. Immunology 125:59–69

    PubMed  CAS  Google Scholar 

  • Kanai T, Fujii T, Kozuma S, Miki A, Yamashita T, Hyodo H, Unno N, Yoshida S, Taketani Y (2003) A subclass of soluble HLA-G1 modulates the release of cytokines from mononuclear cells present in the decidua additively to membrane-bound HLA-G1. J Reprod Immunol 60:85–96

    PubMed  CAS  Google Scholar 

  • Kaufmann P, Black S, Huppertz B (2003) Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 69:1–7

    PubMed  CAS  Google Scholar 

  • Kenneson A, Cannon MJ (2007) Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection. Rev Med Virol 17:253–276

    PubMed  Google Scholar 

  • Khalil-Daher I, Riteau B, Menier C, Sedlik C, Paul P, Dausset J, Carosella ED, Rouas-Freiss N (1999) Role of HLA-G versus HLA-E on NK function: HLA-G is able to inhibit NK cytolysis by itself. J Reprod Immunol 43:175–182

    PubMed  CAS  Google Scholar 

  • King A (2000) Uterine leukocytes and decidualization. Hum Reprod Update 6:28–36

    PubMed  CAS  Google Scholar 

  • King A, Kaira P, Loke YW (1990) Human trophoblast cell resistance to decidual NK lysis is due to lack of NK target structure. Cell Immunol 127:230–237

    PubMed  CAS  Google Scholar 

  • King A, Wooding P, Gardner L, Loke YW (1993) Expression of perforin, granzyme A and TIA-1 by human uterine CD56+ NK cells implies they are activated and capable of effector functions. Hum Reprod 8:2061–2017

    PubMed  CAS  Google Scholar 

  • King A, Boocock C, Sharkey AM, Gardner L, Beretta A, Siccardi AG, Loke YW (1996) Evidence for the expression of HLAA-C class I mRNA and protein by human first trimester trophoblast. J Immunol 156:2068–2076

    PubMed  CAS  Google Scholar 

  • King A, Allan DS, Bowen M, Powis SJ, Joseph S, Verma S, Hiby SE, McMichael AJ, Loke YW, Braud VM (2000) HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur J Immunol 30:1623–1631

    PubMed  CAS  Google Scholar 

  • Knoferl MW, Diodato MD, Angele MK, Ayala A, Cioffi WG, Bland KI, Chaudry IH (2000) Do female sex steroids adversely or beneficially affect the depressed immune responses in males after trauma-hemorrhage? Arch Surg 135:425–433

    PubMed  CAS  Google Scholar 

  • Koga K, Mor G (2010) Toll-like receptors at the maternal–fetal interface in normal pregnancy and pregnancy disorders. Am J Reprod Immunol 63:587–600

    PubMed  CAS  Google Scholar 

  • Kollmann TR, Crabtree J, Rein-Weston A, Blimkie D, Thommai F, Wang XY, Lavoie PM, Furlong J, Fortuno ES, Hajjar AM, Hawkins NR, Self SG, Wilson CB (2009) Neonatal innate TLR-mediated responses are distinct from those of adults. J Immunol 183:7150–7160

    PubMed  CAS  Google Scholar 

  • 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 105:18472–18477

    PubMed  CAS  Google Scholar 

  • Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ, DeMars R (1990) A class I antigen, HLA-G, expressed in human trophoblasts. Science 248:220–223

    PubMed  CAS  Google Scholar 

  • Kozma N, Halasz M, Polgar B, Poehlmann TG, Markert UR, Palkovics T, Keszei M, Par G, Kiss K, Szeberenyi J, Grama L, Szekeres-Bartho J (2006) Progesterone-induced blocking factor activates STAT6 via binding to a novel IL-4 receptor. J Immunol 176:819–826

    PubMed  CAS  Google Scholar 

  • Krishnan L, Guilbert LJ, Russell AS, Wegmann TG, Mosmann TR, Belosevic M (1996) Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-gamma response and increased production of T helper 2 cytokines. J Immunol 156:644–652

    PubMed  CAS  Google Scholar 

  • Kudo Y, Boyd CA, Spyropoulou I, Redman CW, Takikawa O, Katsuki T, Hara T, Ohama K, Sargent IL (2004) Indoleamine 2,3-dioxygenase: distribution and function in the developing human placenta. J Reprod Immunol 61:87–98

    PubMed  CAS  Google Scholar 

  • Kusumi M, Yamashita T, Fujii T, Nagamatsu T, Kozuma S, Taketani Y (2006) Expression patterns of lectin-like natural killer receptors, inhibitory CD94/NKG2A, and activating CD94/NKG2C on decidual CD56bright natural killer cells differ from those on peripheral CD56dim natural killer cells. J Reprod Immunol 70:33–42

    PubMed  CAS  Google Scholar 

  • Laskin CA, Bombardier C, Hannah ME, Mandel FP, Ritchie K, Farewell V, Farine D, Spitzer K, Fielding L, Soloninka CA, Yeung M (1997) Prednisone and aspirin in women with autoantibodies and unexplained recurrent fetal loss. N Engl J Med 337:148–154

    PubMed  CAS  Google Scholar 

  • Le Gal FA, Riteau B, Sedlik C, Khalil-Daher I, Menier C, Dausset J, Guillet JG, Carosella ED, Rouas-Freiss N (1999) HLA-G-mediated inhibition of antigen-specific cytotoxic T lymphocytes. Int Immunol 11:1351–1356

    PubMed  Google Scholar 

  • Lee N, Llano M, Carretero M, Ishitani A, Navarro F, López-Botet M, Geraghty DE (1998) HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci USA 95:5199–5204

    PubMed  CAS  Google Scholar 

  • Lessin DL, Hunt JS, King CR, Wood GW (1988) Antigen expression by cells near the maternal-fetal interface. Am J Reprod Immunol Microbiol 16:1–7

    PubMed  CAS  Google Scholar 

  • Lettieri LVA, Rodis JF, Albini SM, Salafia CM (1993) Does “idiopathic” preterm labor resulting in preterm birth exist? Am J Obstet Gynecol 168:1480–1485

    PubMed  CAS  Google Scholar 

  • Leung AK, Sauve R, Davies HD (2003) Congenital cytomegalovirus infection. J Natl Med Assoc 95:213–218

    PubMed  Google Scholar 

  • Lightner A, Schust DJ, Chen YB, Barrier BF (2008) The fetal allograft revisited: does the study of an ancient invertebrate species shed light on the role of natural killer cells at the maternal-fetal interface? Clin Dev Immunol 2008:631920

    PubMed  Google Scholar 

  • 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 151:4562–4573

    PubMed  CAS  Google Scholar 

  • Lindsay S, Ansell J, Selman C, Cox V, Hamilton K, Walraven G (2000) Effect of pregnancy on exposure to malaria mosquitoes. Lancet 355:1972–1972

    PubMed  CAS  Google Scholar 

  • Liu Y-S, Wu L, Tong XH, Wu LM, He GP, Zhou GX, Luo LH, Luan HB (2011) Study on the relationship between Th17 cells and unexplained recurrent spontaneous abortion. Am J Reprod Immunol 65:503–511

    PubMed  CAS  Google Scholar 

  • MacKenzie CR, Heseler K, Müller A, Däubener W (2007) Role of indoleamine 2,3-dioxygenase in antimicrobial defence and immuno-regulation: tryptophan depletion versus production of toxic kynurenines. Curr Drug Metab 8:237–244

    PubMed  CAS  Google Scholar 

  • Makrigiannakis A, Zoumakis E, Kalantaridou S, Coutifaris C, Margioris AN, Coukos G, Rice KC, Gravanis A, Chrousos GP (2001) Corticotropin-releasing hormone promotes blastocyst implantation and early maternal tolerance. Nat Immunol 2:1018–1024

    PubMed  CAS  Google Scholar 

  • Manaseki S, Searle RF (1989) Natural killer (NK) cell activity of first trimester human decidua. Cell Immunol 121:166–173

    PubMed  CAS  Google Scholar 

  • Manaster I, Mizrahi S, Goldman-Wohl D, Sela HY, Stern-Ginossar N, Lankry D, Gruda R, Hurwitz A, Bdolah Y, Haimov-Kochman R, Yagel S, Mandelboim O (2008) Endometrial NK cells are special immature cells that await pregnancy. J Immunol 181:1869–1876

    PubMed  CAS  Google Scholar 

  • Mao G, Wang J, Kang Y, Tai P, Wen J, Zou Q, Li G, Ouyang H, Xia G, Wang B (2010) Progesterone increases systemic and local uterine proportions of CD4 + CD25+ Treg cells during midterm pregnancy in mice. Endocrinology 151:5477–5488

    PubMed  CAS  Google Scholar 

  • Martin JA, Hamilton BE, Sutton PD, Ventura SJ, Mathews TJ, Kirmeyer S, Osterman MJ (2010) Births: final data for 2007. Natl Vital Stat Rep 58:1–85

    PubMed  Google Scholar 

  • Matteelli A, Caligaris S, Castelli F, Carosi G (1997) The placenta and malaria. Ann Trop Med Parasitol 91:803–810

    PubMed  CAS  Google Scholar 

  • McCormick MC (1985) The contribution of low birth weight to infant mortality and childhood morbidity. N Engl J Med 312:82–90

    PubMed  CAS  Google Scholar 

  • McGilvray ID, Serghides L, Kapus A, Rotstein OD, Kain KC (2000) Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitized erythrocytes: a role for CD36 in malarial clearance. Blood 96:3231–3240

    PubMed  CAS  Google Scholar 

  • McIntire RH, Ganacias KG, Hunt JS (2008) Programming of human monocytes by the uteroplacental environment. Reprod Sci 15:437–447

    PubMed  CAS  Google Scholar 

  • Medawar PB (1961) Immunological tolerance. Science 133:303–306

    PubMed  CAS  Google Scholar 

  • Meinecke CK, Schottelius J, Oskam L, Fleischer B (1999) Congenital transmission of visceral leishmaniasis (Kala Azar) from an asymptomatic mother to her child. Pediatrics 104:e65

    PubMed  CAS  Google Scholar 

  • Menon R, Velez DR, Morgan N, Lombardi SJ, Fortunato SJ, Williams SM (2008) Genetic regulation of amniotic fluid TNF-alpha and soluble TNF receptor concentrations affected by race and preterm birth. Hum Genet 124:243–253

    PubMed  CAS  Google Scholar 

  • Menon R, Fortunato SJ, Edwards DR, Williams SM (2010) Association of genetic variants, ethnicity and preterm birth with amniotic fluid cytokine concentrations. Ann Hum Genet 74:165–183

    PubMed  CAS  Google Scholar 

  • Miller L, Hunt JS (1998) Regulation of TNF-α production in activated mouse macrophages by progesterone. J Immunol 160:5098–5104

    PubMed  CAS  Google Scholar 

  • Mockenhaupt F, Bedu-Addo G, von Gaertner C, Boyé R, Fricke K, Hannibal I, Karakaya F, Schaller M, Ulmen U, Acquah P, Dietz E, Eggelte T, Bienzle U (2006) Detection and clinical manifestation of placental malaria in southern Ghana. Malar J 5:119

    PubMed  Google Scholar 

  • Moore JM, Nahlen BL, Misore A, Lal AA, Udhayakumar V (1999) Immunity to placental malaria. I. Elevated production of interferon-gamma by placental blood mononuclear cells is associated with protection in an area with high transmission of malaria. J Infect Dis 179:1218–1225

    PubMed  CAS  Google Scholar 

  • Moormann AM, Sullivan AD, Rochford RA, Chensue SW, Bock PJ, Nyirenda T, Meshnick SR (1999) Malaria and pregnancy: placental cytokine expression and its relationship to intrauterine growth retardation. J Infect Dis 180:1987–1993

    PubMed  CAS  Google Scholar 

  • Muehlenbachs A, Fried M, McGready R, Harrington WE, Mutabingwa TK, Nosten F, Duffy PE (2010) A novel histological grading scheme for placental malaria applied in areas of high and low malaria transmission. J Infect Dis 202:1608–1616

    PubMed  Google Scholar 

  • Müller V, Szabó A, Viklicky O, Gaul I, Pörtl S, Philipp T, Heemann UW (1999) Sex hormones and gender-related differences: their influence on chronic renal allograft rejection. Kidney Int 55:2011–2020

    PubMed  Google Scholar 

  • Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, Brown C, Mellor AL (1998) Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281:1191–1193

    PubMed  CAS  Google Scholar 

  • Nagamatsu T, Schust DJ, Sugimoto J, Barrier BF (2009) Human decidual stromal cells suppress cytokine secretion by allogeneic CD4+ T cells via PD-1 ligand interactions. Hum Reprod 24:3160–3171

    PubMed  CAS  Google Scholar 

  • Nagata S, Golstein P (1995) The Fas death factor. Science 267:1449–1456

    PubMed  CAS  Google Scholar 

  • Nagata S, Suda T (1995) Fas and Fas ligand: lpr and gld mutations. Immunol Today 16:39–43

    PubMed  CAS  Google Scholar 

  • Nakae S, Iwakura Y, Suto H, Galli SJ (2007) Phenotypic differences between Th1 and Th17 cells and negative regulation of Th1 cell differentiation by IL-17. J Leukoc Biol 81:1258–1268

    PubMed  CAS  Google Scholar 

  • Nakashima A, Ito M, Yoneda S, Shiozaki A, Hidaka T, Saito S (2010) Circulating and decidual Th17 cell levels in healthy pregnancy. Am J Reprod Immunol 63:104–109

    PubMed  CAS  Google Scholar 

  • Nalbandian G, Kovats S (2005) Understanding sex biases in immunity. Immunol Res 31:91–106

    PubMed  CAS  Google Scholar 

  • Newman RD, Hailemariam A, Jimma D, Degifie A, Kebede D, Rietveld AEC, Nahlen BL, Barnwell JW, Steketee RW, Parise ME (2003) Burden of malaria during pregnancy in areas of stable and unstable transmission in ethiopia during a nonepidemic year. J Infect Dis 187:1765–1772

    PubMed  Google Scholar 

  • Nishimura H, Nose M, Hiai H, Minato N, Honjo T (1999) Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11:141–151

    PubMed  CAS  Google Scholar 

  • Nishimura H, Okazaki T, Tanaka Y, Nakatani K, Hara M, Matsumori A, Sasayama S, Mizoguchi A, Hiai H, Minato N, Honjo T (2001) Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 291:319–322

    PubMed  CAS  Google Scholar 

  • Nosten F, ter Kuile F, Maelankirri L, Decludt B, White NJ (1991) Malaria during pregnancy in an area of unstable endemicity. Trans R Soc Trop Med Hyg 85:424–429

    PubMed  CAS  Google Scholar 

  • Ober C, AldrichC RB, Robertson A, Walker MA, Willadsen S, Verp MS, Geraghty DE, Hunt JS (1998) HLA-G1 protein expression is not essential for fetal survival. Placenta 19:127–132

    PubMed  CAS  Google Scholar 

  • O'Brien RF (2005) Bacterial vaginosis: many questions – any answers? Curr Opin Pediatr 17:473–479

    PubMed  Google Scholar 

  • Ockenhouse CF, Schulman S, Shear HL (1984) Induction of crisis forms in the human malaria parasite plasmodium falciparum by gamma-interferon-activated, monocyte-derived macrophages. J Immunol 133:1601–1608

    PubMed  CAS  Google Scholar 

  • Onderdonk AB, Delaney ML, DuBois AM, Allred EN, Leviton A (2008) Detection of bacteria in placental tissues obtained from extremely low gestational age neonates. Am J Obstet Gynecol 198:110.e111–110.e117

    Google Scholar 

  • Ortiz-Alegría LB, Caballero-Ortega H, Cañedo-Solares I, Rico-Torres CP, Sahagún-Ruiz A, Medina-Escutia ME, Correa D (2010) Congenital toxoplasmosis: candidate host immune genes relevant for vertical transmission and pathogenesis. Genes Immun 11:363–373

    PubMed  Google Scholar 

  • Osorio Y, Bonilla DL, Peniche AG, Melby PC, Travi BL (2008) Pregnancy enhances the innate immune response in experimental cutaneous leishmaniasis through hormone-modulated nitric oxide production. J Leukoc Biol 83:1413–1422

    PubMed  CAS  Google Scholar 

  • Othoro C, Moore JM, Wannemuehler KA, Moses S, Lal A, Otieno J, Nahlen B, Slutsker L, Shi YP (2008) Elevated gamma interferon-producing NK cells, CD45RO memory-like T cells, and CD4 T cells are associated with protection against malaria infection in pregnancy. Infect Immun 76:1678–1685

    PubMed  CAS  Google Scholar 

  • Pararas MV, Skevaki CL, Kafetzis DA (2006) Preterm birth due to maternal infection: causative pathogens and modes of prevention. Eur J Clin Microbiol Infect Dis 25:562–569

    PubMed  CAS  Google Scholar 

  • Parhar RS, Yagel S, Lala PK (1989) PGE2-mediated immunosuppression by first trimester human decidual cells blocks activation of maternal leukocytes in the decidua with potential anti-trophoblast activity. Cell Immunol 120:61–74

    PubMed  CAS  Google Scholar 

  • Perillo NL, Pace KE, Seilhamer JJ, Baum LG (1995) Apoptosis of T cells mediated by galectin-1. Nature 378:736–739

    PubMed  CAS  Google Scholar 

  • Piccinni MP, Giudizi MG, Biagiotti R, Beloni L, Giannarini L, Sampognaro S, Parronchi P, Manetti R, Annunziato F, Livi C (1995) Progesterone favors the development of human T helper cells producing Th2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established Th1 cell clones. J Immunol 155:128–133

    PubMed  CAS  Google Scholar 

  • Piccinni M-P, 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 4:1020–1024

    PubMed  CAS  Google Scholar 

  • Pizzato N, Garmy-Susini B, Bouteiller PL, Lenfant F (2004) Differential down-modulation of HLA-G and HLA-A2 or -A3 cell surface expression following human cytomegalovirus infection. J Reprod Immunol 62:3–15

    PubMed  CAS  Google Scholar 

  • Plaks V, Birnberg T, Berkutzki T, Sela S, BenYashar A, Kalchenko V, Mor G, Keshet E, Dekel N, Neeman M, Jung S (2008) Uterine DCs are crucial for decidua formation during embryo implantation in mice. J Clin Invest 118:3954–3965

    PubMed  CAS  Google Scholar 

  • Potkul RK, Moawad AH, Ponto KL (1985) The association of subclinical infection with preterm labor: the role of C-reactive protein. Am J Obstet Gynecol 153:642–645

    PubMed  CAS  Google Scholar 

  • Raghupathy R (1997) Th 1-type immunity is incompatible with successful pregnancy. Immunol Today 18:478–482

    PubMed  CAS  Google Scholar 

  • Rajagopalan S, Long EO (1999) A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J Exp Med 189:1093–1100

    PubMed  CAS  Google Scholar 

  • Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, van der Meer A, Joosten I, Long EO (2005) Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol 4:e9

    Google Scholar 

  • Redline RW, Lu CY (1989) Localization of fetal major histocompatibility complex antigens and maternal leukocytes in murine placenta. Implications for maternal-fetal immunological relationship. Lab Invest 61:27–36

    PubMed  CAS  Google Scholar 

  • Repnik U, Tilburgs T, Roelen DL, van der Mast BJ, Kanhai HH, Scherjon S, Claas FH (2008) Comparison of macrophage phenotype between decidua basalis and decidua parietalis by flow cytometry. Placenta 29:405–412

    PubMed  CAS  Google Scholar 

  • Rogers AM, Boime I, Connolly J, Cook JR, Russell JH (1998) Maternal-fetal tolerance is maintained despite transgene-driven trophoblast expression of MHC class I, and defects in fas and its ligand. Eur J Immunol 28:3479–3487

    PubMed  CAS  Google Scholar 

  • Rogerson SJ, van den Broek NR, Chaluluka E, Qongwane C, Mhango CG, Molyneux ME (2000) Malaria and anemia in antenatal women in Blantyre, Malawi: a twelve-month survey. Am J Trop Med Hyg 62:335–340

    PubMed  CAS  Google Scholar 

  • Rölle A, Mousavi-Jazi M, Eriksson M, Odeberg J, Söderberg-Nauclér C, Cosman D, Kärre K, Cerboni C (2003) Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: up-regulation of UL16-binding protein (ULBP)1 and ULBP2 is counteracted by the viral UL16 protein. J Immunol 171:902–908

    PubMed  Google Scholar 

  • Romero R, Avila C, Santhanam U, Sehgal PB (1990) Amniotic fluid interleukin 6 in preterm labor. Association with infection. J Clin Invest 85:1392–1400

    PubMed  CAS  Google Scholar 

  • Sadowsky DW, Adams KM, Gravett MG, Witkin SS, Novy MJ (2006) Preterm labor is induced by intraamniotic infusions of interleukin-1beta and tumor necrosis factor-alpha but not by interleukin-6 or interleukin-8 in a nonhuman primate model. Am J Obstet Gynecol 195:1578–1589

    PubMed  CAS  Google Scholar 

  • Salem ML, Matsuzaki G, Kishihara K, Madkour GA, Nomoto K (2000) beta-estradiol suppresses T cell-mediated delayed-type hypersensitivity through suppression of antigen-presenting cell function and Th1 induction. Int Arch Allergy Immunol 121:161–169

    PubMed  CAS  Google Scholar 

  • 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 10:347–353

    PubMed  CAS  Google Scholar 

  • Scharton-Kersten TM, Yap G, Magram J, Sher A (1997) Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen toxoplasma gondii. J Exp Med 185:1261–1274

    PubMed  CAS  Google Scholar 

  • Schust DJ, Anderson DJ, Hill JA (1996) Progesterone-induced immunosuppression is not mediated through the progesterone receptor. Hum Reprod 11:980–985

    PubMed  CAS  Google Scholar 

  • Schust DJ, Tortorella D, Seebach J, Phan C, Ploegh HL (1998) Trophoblast class I major histocompatibility complex (MHC) products are resistant to rapid degradation imposed by the human cytomegalovirus (HCMV) gene products US2 and US11. J Exp Med 188:497–503

    PubMed  CAS  Google Scholar 

  • Seliger B, Ritz U, Soldano F (2006) Molecular mechanisms of HLA class I antigen abnormalities following viral infection and transformation. Int J Cancer 118:129–138

    PubMed  CAS  Google Scholar 

  • Serghides L, Patel SN, Ayi K, Kain KC (2006) Placental chondroitin sulfate A-binding malarial isolates evade innate phagocytic clearance. J Infect Dis 194:133–139

    PubMed  Google Scholar 

  • Sharkey AM, Gardner L, Hiby S, Farrell L, Apps R, Masters L, Goodridge J, Lathbury L, Stewart CA, Verma S, Moffett A (2008) Killer Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age. J Immunol 181:39–46

    PubMed  CAS  Google Scholar 

  • Shirahata T, Muroya N, Ohta C, Goto H, Nakane A (1992) Correlation between increased susceptibility to primary Toxoplasma gondii infection and depressed production of gamma interferon in pregnant mice. Microbiol Immunol 36:81–91

    PubMed  CAS  Google Scholar 

  • Shirahata T, Muroya N, Ohta C, Goto H, Nakane A (1993) Enhancement by recombinant human interleukin 2 of host resistance to Toxoplasma gondii infection in pregnant mice. Microbiol Immunol 37:583–590

    PubMed  CAS  Google Scholar 

  • Sibai BM, Caritis SN, Hauth JC, MacPherson C, VanDorsten JP, Klebanoff M, Landon M, Paul RH, Meis PJ, Miodovnik M, Dombrowski MP, Thurnau GR, Moawad AH, Roberts J (2000) Preterm delivery in women with pregestational diabetes mellitus or chronic hypertension relative to women with uncomplicated pregnancies. The National institute of Child health and Human Development Maternal- Fetal Medicine Units Network. Am J Obstet Gynecol 183:1520–1524

    PubMed  CAS  Google Scholar 

  • Silva NM, Rodrigues CV, Santoro MM, Reis LF, Alvarez-Leite JI, Gazzinelli RT (2002) Expression of indoleamine 2,3-dioxygenase, tryptophan degradation, and kynurenine formation during in vivo infection with Toxoplasma gondii: induction by endogenous gamma interferon and requirement of interferon regulatory factor 1. Infect Immun 70:859–868

    PubMed  CAS  Google Scholar 

  • Somerset DA, Zheng Y, Kilby MD, Sansom DM, Drayson MT (2004) Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory T-cell subset. Immunology 112:38–43

    PubMed  CAS  Google Scholar 

  • Steel JH, Malatos S, Kennea N, Edwards AD, Miles L, Duggan P, Reynolds PR, Feldman RG, Sullivan MH (2005) Bacteria and inflammatory cells in fetal membranes do not always cause preterm labor. Pediatr Res 57:404–411

    PubMed  Google Scholar 

  • Steketee RW, Wirima JJ, Slutsker L, Breman JG, Heymann DL (1996) Comparability of treatment groups and risk factors for parasitemia at the first antenatal clinic visit in a study of malaria treatment and prevention in pregnancy in rural Malawi. Am J Trop Med Hyg 55:17–23

    PubMed  CAS  Google Scholar 

  • Sturm A, Amino R, van de Sand C, Regen T, Retzlaff S, Rennenberg A, Krueger A, Pollok JM, Menard R, Heussler VT (2006) Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313:1287–1290

    PubMed  CAS  Google Scholar 

  • Su L, Sun Y, Ma F, Lü P, Huang H, Zhou J (2009) Progesterone inhibits Toll-like receptor 4-mediated innate immune response in macrophages by suppressing NF-kappaB activation and enhancing SOCS1 expression. Immunol Lett 125:151–155

    PubMed  CAS  Google Scholar 

  • Sunderland CA, Naiem M, Mason DY, Redman CW, Stirrat GM (1981) The expression of major histocompatibility antigens by human chorionic villi. J Reprod Immunol 3:323–331

    PubMed  CAS  Google Scholar 

  • Syggelou A, Iacovidou N, Kloudas S, Christoni Z, Papaevangelou V (2010) Congenital cytomegalovirus infection. Ann NY Acad Sci 1205:144–147

    PubMed  Google Scholar 

  • Tafuri A, Alferrink J, Möller P, Hämmerling GJ, Arnold B (1995) T cell awareness of paternal alloantigens during pregnancy. Science 270:630–633

    PubMed  CAS  Google Scholar 

  • Taglauer ES, Trikhacheva AS, Slusser JG, Petroff MG (2008) Expression and function of PDCD1 at the human maternal-fetal interface. Biol Reprod 79:562–569

    PubMed  CAS  Google Scholar 

  • Tai P, Wang J, Jin H, Song X, Yan J, Kang Y, Zhao L, An X, Du X, Chen X, Wang S, Xia G, Wang B (2008) Induction of regulatory T cells by physiological level estrogen. J Cell Physiol 214:456–464

    PubMed  CAS  Google Scholar 

  • Taylor MW, Feng GS (1991) Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J 5:2516–2522

    PubMed  CAS  Google Scholar 

  • Terauchi M, Koi H, Hayano C, Toyama-Sorimachi N, Karasuyama H, Yamanashi Y, Aso T, Shirakata M (2003) Placental extravillous cytotrophoblasts persistently express class I major histocompatibility complex molecules after human cytomegalovirus infection. J Virol 77:8187–8195

    PubMed  CAS  Google Scholar 

  • Thomas MR, Tutschek B, Frost A, Rodeck CH, Yazdani N, Craft I, Williamson R (1995) The time of appearance and disappearance of fetal DNA from the maternal circulation. Prenat Diagn 15:641–646

    PubMed  CAS  Google Scholar 

  • Tomasec P, Braud VM, Rickards C, Powell MB, McSharry BP, Gadola S, Cerundolo V, Borysiewicz LK, McMichael AJ, Wilkinson GWG (2000) Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031–1033

    PubMed  CAS  Google Scholar 

  • Torcia MG, Santarlasci V, Cosmi L, Clemente A, Maggi L, Mangano VD, Verra F, Bancone G, Nebie I, Sirima BS, Liotta F, Frosali F, Angeli R, Severini C, Sannella AR, Bonini P, Lucibello M, Maggi E, Garaci E, Coluzzi M, Cozzolino F, Annunziato F, Romagnani S, Modiano D (2008) Functional deficit of T regulatory cells in Fulani, an ethnic group with low susceptibility to Plasmodium falciparum malaria. Proc Natl Acad Sci USA 105:646–651

    PubMed  CAS  Google Scholar 

  • Tortorella D, Gewurz BE, Furman MH, Schust DJ, Ploegh HL (2000) Viral subversion of the immune system. Annu Rev Immunol 18:861

    PubMed  CAS  Google Scholar 

  • Toscano MA, Commodaro AG, Ilarregui JM, Bianco GA, Liberman A, Serra HM, Hirabayashi J, Rizzo LV, Rabinovich GA (2006) Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2- and T regulatory-mediated anti-inflammatory responses. J Immunol 176:6323–6332

    PubMed  CAS  Google Scholar 

  • Uckan D, Steele A, Cherry WBY, Chamizo W, Koutsonikolis A, Gilbert-Barness E, Good RA (1997) Trophoblasts express Fas ligand: a proposed mechanism for immune privilege in placenta and maternal invasion. Mol Hum Reprod 3:655–662

    PubMed  CAS  Google Scholar 

  • Uemura Y, Liu TY, Narita Y, Suzuki M, Matsushita S (2008) 17Beta-estradiol (E2) plus tumor necrosis factor-alpha induces a distorted maturation of human monocyte-derived dendritic cells and promotes their capacity to initiate T-helper 2 responses. Hum Immunol 69:149–157

    PubMed  CAS  Google Scholar 

  • Ulbrecht M, Martinozzi S, Grzeschik M, Hengel H, Ellwart JW, Pla M, Weiss EH (2000) Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J Immunol 164:5019–5022

    PubMed  CAS  Google Scholar 

  • Uneke CJ (2007) Impact of placental Plasmodium falciparum malaria on pregnancy and perinatal outcome in sub-Saharan Africa: I: introduction to placental malaria. Yale J Biol Med 80:39–50

    PubMed  Google Scholar 

  • Vacchio MS, Hodes RJ (2003) CD28 costimulation is required for in vivo induction of peripheral tolerance in CD8 T cells. J Exp Med 197:19–26

    PubMed  CAS  Google Scholar 

  • Vacchio MS, Hodes RJ (2005) Fetal expression of fas ligand is necessary and sufficient for induction of CD8 T cell tolerance to the fetal antigen H-Y during pregnancy. J Immunol 174:4657–4661

    PubMed  CAS  Google Scholar 

  • Vadillo-Ortega F, Sadowsky DW, Haluska GJ, Hernandez-Guerrero C, Guevara-Silva R, Gravett MG, Novy MJ (2002) Identification of matrix metalloproteinase-9 in amniotic fluid and amniochorion in spontaneous labor and after experimental intrauterine infection or interleukin-1[beta] infusion in pregnant rhesus monkeys. Am J Obstet Gynecol 186:128–138

    PubMed  CAS  Google Scholar 

  • Vanden Eijnden S, Goriely S, De Wit D, Willems F, Goldman M (2005) IL-23 up-regulates IL-10 and induces IL-17 synthesis by polyclonally activated naive T cells in human. Eur J Immunol 35:469–475

    PubMed  CAS  Google Scholar 

  • Vargas-Villavicencio JA, De León-Nava MA, Morales-Montor J (2009) Immunoendocrine mechanisms associated with resistance or susceptibility to parasitic diseases during pregnancy. Neuroimmunomodulation 16:114–121

    PubMed  CAS  Google Scholar 

  • Velez DR, Menon R, Thorsen P, Jiang L, Simhan H, Morgan N, Fortunato SJ, Williams SM (2007) Ethnic differences in interleukin 6 (IL-6) and IL6 receptor genes in spontaneous preterm birth and effects on amniotic fluid protein levels. Ann Hum Genet 71:586–600

    PubMed  CAS  Google Scholar 

  • Volchek M, Girling JE, Lash GE, Cann L, Kumar B, Robson SC, Bulmer JN, Rogers PA (2010) Lymphatics in the human endometrium disappear during decidualization. Hum Reprod 25:2455–2464

    PubMed  Google Scholar 

  • Wang WJ, Hao CF, Qu QL, Wang X, Qiu LH, Lin QD (2010) The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Hum Reprod 25:2591–2596

    PubMed  CAS  Google Scholar 

  • Witkin SS, Linhares IM, Bongiovanni AM, Herway C, Skupski D (2011) Unique alterations in infection-induced immune activation during pregnancy. BJOG 118:145–153

    PubMed  CAS  Google Scholar 

  • Yap GS, Sher A (1999) Effector cells of both nonhemopoietic and hemopoietic origin are required for interferon (IFN)-gamma-and tumor necrosis factor (TNF)-alpha-dependent host resistance to the intracellular pathogen, Toxoplasma gondii. J Exp Med 189:1083–1092

    PubMed  CAS  Google Scholar 

  • Yarovinsky F, Zhang D, Andersen JF, Bannenberg GL, Serhan CN, Hayden MS, Hieny S, Sutterwala FS, Flavell RA, Ghosh S, Sher A (2005) TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308:1626–1629

    PubMed  CAS  Google Scholar 

  • Zenclussen AC, Gerlof K, Zenclussen ML, Sollwedel A, Bertoja AZ, Ritter T, Kotsch K, Leber J, Volk HD (2005) Abnormal T-Cell reactivity against paternal antigens in spontaneous abortion: adoptive transfer of pregnancy-induced CD4 + CD25+ T regulatory cells prevents fetal rejection in a murine abortion model. Am J Pathol 166:811–822

    PubMed  Google Scholar 

  • Zhou M, Mellor AL (1998) Expanded cohorts of maternal CD8+ T-cells specific for paternal MHC class I accumulate during pregnancy. J Reprod Immunol 40:47–62

    PubMed  CAS  Google Scholar 

  • Zhou Y, McMaster M, Woo K, Janatpour M, Perry J, Karpanen T, Alitalo K, Damsky C, Fisher SJ (2002) Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am J Pathol 160:1405–1423

    PubMed  CAS  Google Scholar 

  • Zuckermann FA, Head J (1986) Expression of MHC antigens on murine trophoblast and their modulation by interferon. J Immunol 137:846–853

    PubMed  CAS  Google Scholar 

  • Zuckermann FA, Head J (1987) Murine trophoblast resists cell-mediated lysis. I. Resistance to allospecific cytotoxic T lymphocytes. J Immunol 139:2856–2864

    PubMed  CAS  Google Scholar 

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  1. Department of Obstetrics, Gynecology and Women’s Health, University of Missouri School of Medicine, 500 North Keene Street, Suite 203, Columbia, MO, 65201, USA

    Takeshi Nagamatsu & Danny J. Schust

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  1. Takeshi Nagamatsu
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Correspondence to Takeshi Nagamatsu .

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    Joan Stein-Streilein

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Nagamatsu, T., Schust, D.J. (2012). The Role of Intrauterine Immune Privilege in Perinatal Infectious Diseases. In: Stein-Streilein, J. (eds) Infection, Immune Homeostasis and Immune Privilege. Birkhäuser Advances in Infectious Diseases. Springer, Basel. https://doi.org/10.1007/978-3-0348-0445-5_3

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