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Immunology of Pregnancy and Systemic Consequences

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Book cover Sex and Gender Differences in Infection and Treatments for Infectious Diseases

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Abstract

The uterus is a site rich in immune cells and is subject to regulation by the sex hormones progesterone and estrogens. Immune modulation within the uterus is initiated during coitus and continues through to the delivery of the baby and for some time postpartum. Several mechanisms to protect the semiallogeneic fetus from maternal immune attack exist, with the carefully regulated recruitment and function of immune cells, as well as the mediators they produce, now recognized as crucial to the success of pregnancy. In the postpartum period, immune cells are also vital to aid the repair and remodeling process, as well as ensure defense against pathogens. Dysregulation of these maternal immune mechanisms can lead to the development of conditions such as preeclampsia, preterm birth, and spontaneous abortion. This chapter will evaluate the immune environment within the uterus and the systemic consequences from coitus to postpartum uterine involution. The effect of pregnancy-associated immune modulation on the symptoms of the autoimmune diseases such as arthritis and systemic lupus erythematosus (SLE) pregnancy-associated infections is also reviewed.

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References

  • Abrahams VM, Kim YM, Straszewski SL, Romero R, Mor G (2004) Macrophages and apoptotic cell clearance during pregnancy. Am J Reprod Immunol 51:275–282

    PubMed  Google Scholar 

  • Adams Waldorf KM, Nelson JL (2008) Autoimmune disease during pregnancy and the microchimerism legacy of pregnancy. Immunol Invest 37:631–644

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aghajanova L (2004) Leukemia inhibitory factor and human embryo implantation. Ann NY Acad Sci 1034:176–183

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Apps R, Murphy SP, Fernando R, Gardner L, Ahad T, Moffett A (2009) Human leucocyte antigen (HLA) expression of primary trophoblast cells and placental cell lines, determined using single antigen beads to characterize allotype specificities of anti-HLA antibodies. Immunology 127:26–39

    CAS  PubMed Central  PubMed  Google Scholar 

  • Balbin M, Fueyo A, Knauper V, Pendas AM, Lopez JM, Jimenez MG, Murphy G, Lopez-Otin C (1998) Collagenase 2 (MMP-8) expression in murine tissue-remodeling processes. Analysis of its potential role in postpartum involution of the uterus. J Biol Chem 273:23959–23968

    CAS  PubMed  Google Scholar 

  • Bao Y, Cao X (2014) The immune potential and immunopathology of cytokine-producing B cell subsets: a comprehensive review. J Autoimmun 55:10–23

    CAS  PubMed  Google Scholar 

  • Barrientos G, Fuchs D, Schrocksnadel K, Ruecke M, Garcia MG, Klapp BF, Raghupathy R, Miranda S, Arck PC, Blois SM (2009) Low levels of serum asymmetric antibodies as a marker of threatened pregnancy. J Reprod Immunol 79:201–210

    CAS  PubMed  Google Scholar 

  • Bellinge BS, Copeland CM, Thomas TD, Mazzucchelli RE, O’neil G, Cohen MJ (1986) The influence of patient insemination on the implantation rate in an in vitro fertilization and embryo transfer program. Fertil Steril 46:252–256

    CAS  PubMed  Google Scholar 

  • Belo L, Santos-Silva A, Rocha S, Caslake M, Cooney J, Pereira-Leite L, Quintanilha A, Rebelo I (2005) Fluctuations in C-reactive protein concentration and neutrophil activation during normal human pregnancy. Eur J Obstet Gynecol Reprod Biol 123:46–51

    CAS  PubMed  Google Scholar 

  • Billington WD (2003) The immunological problem of pregnancy: 50 years with the hope of progress. A tribute to Peter Medawar. J Reprod Immunol 60:1–11

    PubMed  Google Scholar 

  • Blaschitz A, Lenfant F, Mallet V, Hartmann M, Bensussan A, Geraghty DE, Le Bouteiller P, Dohr G (1997) Endothelial cells in chorionic fetal vessels of first trimester placenta express HLA-G. Eur J Immunol 27:3380–3388

    CAS  PubMed  Google Scholar 

  • Bollapragada S, Youssef R, Jordan F, Greer I, Norman J, Nelson S (2009) Term labor is associated with a core inflammatory response in human fetal membranes, myometrium, and cervix. Am J Obstet Gynecol 200(104):e1–e11

    PubMed  Google Scholar 

  • Bouman A, Heineman MJ, Faas MM (2005) Sex hormones and the immune response in humans. Hum Reprod Update 11:411–423

    CAS  PubMed  Google Scholar 

  • Bove R, Chitnis T (2014) The role of gender and sex hormones in determining the onset and outcome of multiple sclerosis. Mult Scler 20:520–526

    CAS  PubMed  Google Scholar 

  • Braundmeier AG, Nowak RA (2006) Cytokines regulate matrix metalloproteinases in human uterine endometrial fibroblast cells through a mechanism that does not involve increases in extracellular matrix metalloproteinase inducer. Am J Reprod Immunol 56:201–214

    CAS  PubMed  Google Scholar 

  • Bukowski REA (2011) Causes of death among stillbirths. JAMA 306:2459–2468

    CAS  Google Scholar 

  • Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D (1991) Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 6:791–798

    CAS  PubMed  Google Scholar 

  • Bulmer JN, Williams PJ, Lash GE (2010) Immune cells in the placental bed. Int J Dev Biol 54:281–294

    PubMed  Google Scholar 

  • Caballero-Campo P, Dominguez F, Coloma J, Meseguer M, Remohi J, Pellicer A, Simon C (2002) Hormonal and embryonic regulation of chemokines IL-8, MCP-1 and RANTES in the human endometrium during the window of implantation. Mol Hum Reprod 8:375–384

    CAS  PubMed  Google Scholar 

  • Care AS, Diener KR, Jasper MJ, Brown HM, Ingman WV, Robertson SA (2013) Macrophages regulate corpus luteum development during embryo implantation in mice. J Clin Invest 123:3472–3487

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cha J, Sun X, Dey SK (2012) Mechanisms of implantation: strategies for successful pregnancy. Nat Med 18:1754–1767

    CAS  PubMed  Google Scholar 

  • Challis JR, Lye SJ, Gibb W, Whittle W, Patel F, Alfaidy N (2001) Understanding preterm labor. Ann NY Acad Sci 943:225–234

    CAS  PubMed  Google Scholar 

  • Chantakru S, Wang WC, Van Den Heuvel M, Bashar S, Simpson A, Chen Q, Croy BA, Evans SS (2003) Coordinate regulation of lymphocyte-endothelial interactions by pregnancy-associated hormones. J Immunol 171:4011–4019

    CAS  PubMed Central  PubMed  Google Scholar 

  • Charnock-Jones DS, Sharkey AM, Fenwick P, Smith SK (1994) Leukaemia inhibitory factor mRNA concentration peaks in human endometrium at the time of implantation and the blastocyst contains mRNA for the receptor at this time. J Reprod Fertil 101:421–426

    CAS  PubMed  Google Scholar 

  • Chazara O, Xiong S, Moffett A (2011) Maternal KIR and fetal HLA-C: a fine balance. J Leukoc Biol 90:703–716

    CAS  PubMed  Google Scholar 

  • Chen T, Darrasse-Jeze G, Bergot AS, Courau T, Churlaud G, Valdivia K, Strominger JL, Ruocco MG, Chaouat G, Klatzmann D (2013) Self-specific memory regulatory T cells protect embryos at implantation in mice. J Immunol 191:2273–2281

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chevillard G, Derjuga A, Devost D, Zingg HH, Blank V (2007) Identification of interleukin-1beta regulated genes in uterine smooth muscle cells. Reproduction 134:811–822

    CAS  PubMed  Google Scholar 

  • Colasanti T, Maselli A, Conti F, Sanchez M, Alessandri C, Barbati C, Vacirca D, Tinari A, Chiarotti F, Giovannetti A, Franconi F, Valesini G, Malorni W, Pierdominici M, Ortona E (2012) Autoantibodies to estrogen receptor alpha interfere with T lymphocyte homeostasis and are associated with disease activity in systemic lupus erythematosus. Arthritis Rheum 64:778–787

    CAS  PubMed  Google Scholar 

  • Confavreux C, Hutchinson M, Hours MM, Cortinovis-Tourniaire P, Moreau T (1998) Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in multiple sclerosis group. N Engl J Med 339:285–291

    CAS  PubMed  Google Scholar 

  • Crispin JC, Liossis SN, Kis-Toth K, Lieberman LA, Kyttaris VC, Juang YT, Tsokos GC (2010) Pathogenesis of human systemic lupus erythematosus: recent advances. Trends Mol Med 16:47–57

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crouch SP, Crocker IP, Fletcher J (1995) The effect of pregnancy on polymorphonuclear leukocyte function. J Immunol 155:5436–5443

    CAS  PubMed  Google Scholar 

  • Cullinan EB, Abbondanzo SJ, Anderson PS, Pollard JW, Lessey BA, Stewart CL (1996) Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/paracrine function in regulating embryo implantation. Proc Natl Acad Sci USA 93:3115–3120

    CAS  PubMed Central  PubMed  Google Scholar 

  • De M, Wood GW (1990) Influence of oestrogen and progesterone on macrophage distribution in the mouse uterus. J Endocrinol 126:417–424

    CAS  PubMed  Google Scholar 

  • De M, Choudhuri R, Wood GW (1991) Determination of the number and distribution of macrophages, lymphocytes, and granulocytes in the mouse uterus from mating through implantation. J Leukoc Biol 50:252–262

    CAS  PubMed  Google Scholar 

  • Dimitriadis E, White CA, Jones RL, Salamonsen LA (2005) Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update 11:613–630

    CAS  PubMed  Google Scholar 

  • Disanto G, Ramagopalan SV (2013) On the sex ratio of multiple sclerosis. Mult Scler 19:3–4

    PubMed  Google Scholar 

  • Dominguez F, Remohi J, Pellicer A, Simon C (2002) Paracrine interactions during human implantation. Rev Endocr Metab Disord 3:97–105

    CAS  PubMed  Google Scholar 

  • Dominguez F, Galan A, Martin JJ, Remohi J, Pellicer A, Simon C (2003a) Hormonal and embryonic regulation of chemokine receptors CXCR1, CXCR4, CCR5 and CCR2B in the human endometrium and the human blastocyst. Mol Hum Reprod 9:189–198

    CAS  PubMed  Google Scholar 

  • Dominguez F, Pellicer A, Simon C (2003b) The chemokine connection: hormonal and embryonic regulation at the human maternal-embryonic interface – a review. Placenta 24(Suppl B):S48–S55

    CAS  PubMed  Google Scholar 

  • Dosiou C, Giudice LC (2005) Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr Rev 26:44–62

    CAS  PubMed  Google Scholar 

  • Druckmann R, Druckmann MA (2005) Progesterone and the immunology of pregnancy. J Steroid Biochem Mol Biol 97:389–396

    CAS  PubMed  Google Scholar 

  • Dunn CL, Kelly RW, Critchley HO (2003) Decidualization of the human endometrial stromal cell: an enigmatic transformation. Reprod Biomed Online 7:151–161

    PubMed  Google Scholar 

  • Eidinger D, Garrett TJ (1972) Studies of the regulatory effects of the sex hormones on antibody formation and stem cell differentiation. J Exp Med 136:1098–1116

    CAS  PubMed Central  PubMed  Google Scholar 

  • El-Etr M, Vukusic S, Gignoux L, Durand-Dubief F, Achiti I, Baulieu EE, Confavreux C (2005) Steroid hormones in multiple sclerosis. J Neurol Sci 233:49–54

    CAS  PubMed  Google Scholar 

  • El-Maallem H, Fletcher J (1980) Impaired neutrophil function and myeloperoxidase deficiency in pregnancy. Br J Haematol 44:375–381

    CAS  PubMed  Google Scholar 

  • Ferry BL, Starkey PM, Sargent IL, Watt GM, Jackson M, Redman CW (1990) Cell populations in the human early pregnancy decidua: natural killer activity and response to interleukin-2 of CD56-positive large granular lymphocytes. Immunology 70:446–452

    CAS  PubMed Central  PubMed  Google Scholar 

  • Foocharoen C, Nanagara R, Salang L, Suwannaroj S, Mahakkanukrauh A (2009) Pregnancy and disease outcome in patients with systemic lupus erythematosus (SLE): a study at Srinagarind Hospital. J Med Assoc Thai 92:167–174

    PubMed  Google Scholar 

  • Giltay EJ, Fonk JC, Von Blomberg BM, Drexhage HA, Schalkwijk C, Gooren LJ (2000) In vivo effects of sex steroids on lymphocyte responsiveness and immunoglobulin levels in humans. J Clin Endocrinol Metab 85:1648–1657

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Guerin LR, Prins JR, Robertson SA (2009) Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment? Hum Reprod Update 15:517–535

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guerin LR, Moldenhauer LM, Prins JR, Bromfield JJ, Hayball JD, Robertson SA (2011) Seminal fluid regulates accumulation of FOXP3+ regulatory T cells in the preimplantation mouse uterus through expanding the FOXP3+ cell pool and CCL19-mediated recruitment. Biol Reprod 85:397–408

    CAS  PubMed  Google Scholar 

  • Gutierrez G, Gentile T, Miranda S, Margni RA (2005) Asymmetric antibodies: a protective arm in pregnancy. Chem Immunol Allergy 89:158–168

    CAS  PubMed  Google Scholar 

  • Haines BP, Voyle RB, Rathjen PD (2000) Intracellular and extracellular leukemia inhibitory factor proteins have different cellular activities that are mediated by distinct protein motifs. Mol Biol Cell 11:1369–1383

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hammer A, Hutter H, Blaschitz A, Mahnert W, Hartmann M, Uchanska-Ziegler B, Ziegler A, Dohr G (1997) Amnion epithelial cells, in contrast to trophoblast cells, express all classical HLA class I molecules together with HLA-G. Am J Reprod Immunol 37:161–171

    CAS  PubMed  Google Scholar 

  • Hampl R, Kubatova J, Heracek J, Sobotka V, Starka L (2013) Hormones and endocrine disruptors in human seminal plasma. Endocr Regul 47:149–158

    CAS  PubMed  Google Scholar 

  • Handwerger S (1994) A critical role for interleukin-1 (IL-1) and the type 1 IL-1 receptor in blastocyst implantation. Endocrinology 134:519–520

    CAS  PubMed  Google Scholar 

  • Hannan NJ, Salamonsen LA (2007) Role of chemokines in the endometrium and in embryo implantation. Curr Opin Obstet Gynecol 19:266–272

    PubMed  Google Scholar 

  • Hannan NJ, Jones RL, Critchley HO, Kovacs GJ, Rogers PA, Affandi B, Salamonsen LA (2004) Coexpression of fractalkine and its receptor in normal human endometrium and in endometrium from users of progestin-only contraception supports a role for fractalkine in leukocyte recruitment and endometrial remodeling. J Clin Endocrinol Metab 89:6119–6129

    CAS  PubMed  Google Scholar 

  • Hirota Y, Osuga Y, Koga K, Yoshino O, Hirata T, Morimoto C, Harada M, Takemura Y, Nose E, Yano T, Tsutsumi O, Taketani Y (2006) The expression and possible roles of chemokine CXCL11 and its receptor CXCR3 in the human endometrium. J Immunol 177:8813–8821

    CAS  PubMed  Google Scholar 

  • Hua R, Pease JE, Sooranna SR, Viney JM, Nelson SM, Myatt L, Bennett PR, Johnson MR (2012) Stretch and inflammatory cytokines drive myometrial chemokine expression via NF-kappaB activation. Endocrinology 153:481–491

    CAS  PubMed  Google Scholar 

  • Hunt JS, Langat DL (2009) HLA-G: a human pregnancy-related immunomodulator. Curr Opin Pharmacol 9:462–469

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hunt JS, Petroff MG, Mcintire RH, Ober C (2005) HLA-G and immune tolerance in pregnancy. FASEB J 19:681–693

    CAS  PubMed  Google Scholar 

  • Hviid TV (2006) HLA-G in human reproduction: aspects of genetics, function and pregnancy complications. Hum Reprod Update 12:209–232

    CAS  PubMed  Google Scholar 

  • Inoue K, Inoue E, Imai Y (2013) Female sex hormones ameliorate arthritis in SKG mice. Biochem Biophys Res Commun 434:740–745

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Ito M, Nakashima A, Hidaka T, Okabe M, Bac ND, Ina S, Yoneda S, Shiozaki A, Sumi S, Tsuneyama K, Nikaido T, Saito S (2010) A role for IL-17 in induction of an inflammation at the fetomaternal interface in preterm labour. J Reprod Immunol 84:75–85

    CAS  PubMed  Google Scholar 

  • Johansson M, Bromfield JJ, Jasper MJ, Robertson SA (2004) Semen activates the female immune response during early pregnancy in mice. Immunology 112:290–300

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jones RL, Hannan NJ, Kaitu’u TJ, Zhang J, Salamonsen LA (2004) Identification of chemokines important for leukocyte recruitment to the human endometrium at the times of embryo implantation and menstruation. J Clin Endocrinol Metab 89:6155–6167

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kallikourdis M, Betz AG (2007) Periodic accumulation of regulatory T cells in the uterus: preparation for the implantation of a semi-allogeneic fetus? PLoS One 2:e382

    PubMed Central  PubMed  Google Scholar 

  • Kim S, Liva SM, Dalal MA, Verity MA, Voskuhl RR (1999) Estriol ameliorates autoimmune demyelinating disease: implications for multiple sclerosis. Neurology 52:1230–1238

    CAS  PubMed  Google Scholar 

  • Kimber SJ (2005) Leukaemia inhibitory factor in implantation and uterine biology. Reproduction 130:131–145

    CAS  PubMed  Google Scholar 

  • Kindzelskii AL, Ueki T, Michibata H, Chaiworapongsa T, Romero R, Petty HR (2004) 6-phosphogluconate dehydrogenase and glucose-6-phosphate dehydrogenase form a supramolecular complex in human neutrophils that undergoes retrograde trafficking during pregnancy. J Immunol 172:6373–6381

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • King A, Burrows TD, Hiby SE, Bowen JM, Joseph S, Verma S, Lim PB, Gardner L, Le Bouteiller P, Ziegler A, Uchanska-Ziegler B, Loke YW (2000b) Surface expression of HLA-C antigen by human extravillous trophoblast. Placenta 21:376–387

    CAS  PubMed  Google Scholar 

  • Kitaya K, Yasuda J, Yagi I, Tada Y, Fushiki S, Honjo H (2000) IL-15 expression at human endometrium and decidua. Biol Reprod 63:683–687

    CAS  PubMed  Google Scholar 

  • Kuang H, Peng H, Xu H, Zhang B, Peng J, Tan Y (2010) Hormonal regulation of uterine natural killer cells in mouse preimplantation uterus. J Mol Histol 41:1–7

    CAS  PubMed  Google Scholar 

  • Kuijper EA, Ket JC, Caanen MR, Lambalk CB (2013) Reproductive hormone concentrations in pregnancy and neonates: a systematic review. Reprod Biomed Online 27:33–63

    CAS  PubMed  Google Scholar 

  • Labeta MO, Margni RA, Leoni J, Binaghi RA (1986) Structure of asymmetric non-precipitating antibody: presence of a carbohydrate residue in only one Fab region of the molecule. Immunology 57:311–317

    CAS  PubMed Central  PubMed  Google Scholar 

  • Laird SM, Widdowson R, El-Sheikhi M, Hall AJ, Li TC (2011) Expression of CXCL12 and CXCR4 in human endometrium; effects of CXCL12 on MMP production by human endometrial cells. Hum Reprod 26:1144–1152

    CAS  PubMed  Google Scholar 

  • Lasarte S, Elsner D, Guia-Gonzalez M, Ramos-Medina R, Sanchez-Ramon S, Esponda P, Munoz-Fernandez MA, Relloso M (2013) Female sex hormones regulate the Th17 immune response to sperm and Candida albicans. Hum Reprod 28:3283–3291

    CAS  PubMed  Google Scholar 

  • Leber A, Teles A, Zenclussen AC (2010) Regulatory T cells and their role in pregnancy. Am J Reprod Immunol 63:445–459

    CAS  PubMed  Google Scholar 

  • Ledingham MA, Thomson AJ, Jordan F, Young A, Crawford M, Norman JE (2001) Cell adhesion molecule expression in the cervix and myometrium during pregnancy and parturition. Obstet Gynecol 97:235–242

    CAS  PubMed  Google Scholar 

  • Lee JH, Ulrich B, Cho J, Park J, Kim CH (2011) Progesterone promotes differentiation of human cord blood fetal T cells into T regulatory cells but suppresses their differentiation into Th17 cells. J Immunol 187:1778–1787

    CAS  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Linn S, Murtaugh B, Casey E (2012) Role of sex hormones in the development of osteoarthritis. PM R 4:S169–S173

    PubMed  Google Scholar 

  • Liu L, Wang Z (2013) Estrogen attenuates lipopolysaccharide-induced nitric oxide production in macrophages partially via the nongenomic pathway. Cell Immunol 286:53–58

    CAS  PubMed  Google Scholar 

  • Liu X, Wu H, Byrne M, Jeffrey J, Krane S, Jaenisch R (1995) A targeted mutation at the known collagenase cleavage site in mouse type I collagen impairs tissue remodeling. J Cell Biol 130:227–237

    CAS  PubMed  Google Scholar 

  • Liu F, Guo J, Tian T, Wang H, Dong F, Huang H, Dong M (2011) Placental trophoblasts shifted Th1/Th2 balance toward Th2 and inhibited Th17 immunity at fetomaternal interface. APMIS 119:597–604

    CAS  PubMed  Google Scholar 

  • Loras B, Vetele F, El Malki A, Rollet J, Soufir JC, Benahmed M (1999) Seminal transforming growth factor-beta in normal and infertile men. Hum Reprod 14:1534–1539

    CAS  PubMed  Google Scholar 

  • Loudon JA, Sooranna SR, Bennett PR, Johnson MR (2004) Mechanical stretch of human uterine smooth muscle cells increases IL-8 mRNA expression and peptide synthesis. Mol Hum Reprod 10:895–899

    CAS  PubMed  Google Scholar 

  • Loza MJ, Peters SP, Zangrilli JG, Perussia B (2002) Distinction between IL-13+ and IFN-gamma+ natural killer cells and regulation of their pool size by IL-4. Eur J Immunol 32:413–423

    CAS  PubMed  Google Scholar 

  • Luppi P, Haluszczak C, Betters D, Richard CA, Trucco M, Deloia JA (2002a) Monocytes are progressively activated in the circulation of pregnant women. J Leukoc Biol 72:874–884

    CAS  PubMed  Google Scholar 

  • Luppi P, Haluszczak C, Trucco M, Deloia JA (2002b) Normal pregnancy is associated with peripheral leukocyte activation. Am J Reprod Immunol 47:72–81

    CAS  PubMed  Google Scholar 

  • Ma WG, Song H, Das SK, Paria BC, Dey SK (2003) Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc Natl Acad Sci USA 100:2963–2968

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maeda Y, Ohtsuka H, Tomioka M, Oikawa M (2013) Effect of progesterone on Th1/Th2/Th17 and regulatory T cell-related genes in peripheral blood mononuclear cells during pregnancy in cows. Vet Res Commun 37:43–49

    PubMed  Google Scholar 

  • Maegawa M, Kamada M, Irahara M, Yamamoto S, Yoshikawa S, Kasai Y, Ohmoto Y, Gima H, Thaler CJ, Aono T (2002) A repertoire of cytokines in human seminal plasma. J Reprod Immunol 54:33–42

    CAS  PubMed  Google Scholar 

  • Manase K, Endo T, Chida M, Nagasawa K, Honnma H, Yamazaki K, Kitajima Y, Goto T, Kanaya M, Hayashi T, Mitaka T, Saito T (2006) Coordinated elevation of membrane type 1-matrix metalloproteinase and matrix metalloproteinase-2 expression in rat uterus during postpartum involution. Reprod Biol Endocrinol 4:32

    PubMed Central  PubMed  Google Scholar 

  • Manaster I, Mandelboim O (2010) The unique properties of uterine NK cells. Am J Reprod Immunol 63:434–444

    CAS  PubMed  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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Mariee N, Li TC, Laird SM (2012) Expression of leukaemia inhibitory factor and interleukin 15 in endometrium of women with recurrent implantation failure after IVF; correlation with the number of endometrial natural killer cells. Hum Reprod 27:1946–1954

    CAS  PubMed  Google Scholar 

  • Matthiesen L, Berg G, Ernerudh J, Skogh T (1995) Lymphocyte subsets and autoantibodies in pregnancies complicated by placental disorders. Am J Reprod Immunol 33:31–39

    CAS  PubMed  Google Scholar 

  • Medina KL, Kincade PW (1994) Pregnancy-related steroids are potential negative regulators of B lymphopoiesis. Proc Natl Acad Sci USA 91:5382–5386

    CAS  PubMed Central  PubMed  Google Scholar 

  • Menzies FM, Henriquez FL (2009) Immunomodulation by the female sex hormones. Open Infect Dis J 3:61–72

    CAS  Google Scholar 

  • Menzies FM, Henriquez FL, Alexander J, Roberts CW (2011a) Selective inhibition and augmentation of alternative macrophage activation by progesterone. Immunology 134:281–291

    CAS  PubMed Central  PubMed  Google Scholar 

  • Menzies FM, Higgins CA, Shepherd MC, Nibbs RJ, Nelson SM (2011b) Mast cells reside in myometrium and cervix, but are dispensable in mice for successful pregnancy and labor. Immunol Cell Biol 90:321–329

    PubMed  Google Scholar 

  • Menzies FM, Khan AH, Higgins CA, Nelson SM, Nibbs RJ (2012) The chemokine receptor CCR2 is not required for successful initiation of labor in mice. Biol Reprod 86:118

    PubMed  Google Scholar 

  • Minagawa M, Narita J, Tada T, Maruyama S, Shimizu T, Bannai M, Oya H, Hatakeyama K, Abo T (1999) Mechanisms underlying immunologic states during pregnancy: possible association of the sympathetic nervous system. Cell Immunol 196:1–13

    CAS  PubMed  Google Scholar 

  • Moffett-King A (2002) Natural killer cells and pregnancy. Nat Rev Immunol 2:656–663

    CAS  PubMed  Google Scholar 

  • Moldenhauer LM, Diener KR, Thring DM, Brown MP, Hayball JD, Robertson SA (2009) Cross-presentation of male seminal fluid antigens elicits T cell activation to initiate the female immune response to pregnancy. J Immunol 182:8080–8093

    CAS  PubMed  Google Scholar 

  • Mor G, Cardenas I, Abrahams V, Guller S (2011) Inflammation and pregnancy: the role of the immune system at the implantation site. Ann NY Acad Sci 1221:80–87

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mulayim N, Palter SF, Kayisli UA, Senturk L, Arici A (2003) Chemokine receptor expression in human endometrium. Biol Reprod 68:1491–1495

    CAS  PubMed  Google Scholar 

  • Mulic-Lutvica A, Bekuretsion M, Bakos O, Axelsson O (2001) Ultrasonic evaluation of the uterus and uterine cavity after normal, vaginal delivery. Ultrasound Obstet Gynecol 18:491–498

    CAS  PubMed  Google Scholar 

  • Muzzio D, Zenclussen AC, Jensen F (2013) The role of B cells in pregnancy: the good and the bad. Am J Reprod Immunol 69:408–412

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Nelson JL, Ostensen M (1997) Pregnancy and rheumatoid arthritis. Rheum Dis Clin North Am 23:195–212

    CAS  PubMed  Google Scholar 

  • Ng SC, Gilman-Sachs A, Thaker P, Beaman KD, Beer AE, Kwak-Kim J (2002) Expression of intracellular Th1 and Th2 cytokines in women with recurrent spontaneous abortion, implantation failures after IVF/ET or normal pregnancy. Am J Reprod Immunol 48:77–86

    PubMed  Google Scholar 

  • Norwitz ER, Schust DJ, Fisher SJ (2001) Implantation and the survival of early pregnancy. N Engl J Med 345:1400–1408

    CAS  PubMed  Google Scholar 

  • Oertelt-Prigione S (2012) The influence of sex and gender on the immune response. Autoimmun Rev 11:A479–A485

    CAS  PubMed  Google Scholar 

  • Oh MJ, Croy BA (2008) A map of relationships between uterine natural killer cells and progesterone receptor expressing cells during mouse pregnancy. Placenta 29:317–323

    CAS  PubMed  Google Scholar 

  • Osman I, Young A, Ledingham MA, Thomson AJ, Jordan F, Greer IA, Norman JE (2003) Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol Hum Reprod 9:41–45

    CAS  PubMed  Google Scholar 

  • Pennell LM, Galligan CL, Fish EN (2012) Sex affects immunity. J Autoimmun 38:J282–J291

    CAS  PubMed  Google Scholar 

  • Piccinni MP, Giudizi MG, Biagiotti R, Beloni L, Giannarini L, Sampognaro S, Parronchi P, Manetti R, Annunziato F, Livi C et al (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

    CAS  PubMed  Google Scholar 

  • 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 4:1020–1024

    CAS  PubMed  Google Scholar 

  • Poehlmann TG, Fitzgerald JS, Meissner A, Wengenmayer T, Schleussner E, Friedrich K, Markert UR (2005) Trophoblast invasion: tuning through LIF, signalling via Stat3. Placenta 26(Suppl A):S37–S41

    PubMed  Google Scholar 

  • Polanczyk MJ, Carson BD, Subramanian S, Afentoulis M, Vandenbark AA, Ziegler SF, Offner H (2004) Cutting edge: estrogen drives expansion of the CD4+CD25+ regulatory T cell compartment. J Immunol 173:2227–2230

    CAS  PubMed  Google Scholar 

  • Quinn KH, Lacoursiere DY, Cui L, Bui J, Parast MM (2011) The unique pathophysiology of early-onset severe preeclampsia: role of decidual T regulatory cells. J Reprod Immunol 91:76–82

    CAS  PubMed  Google Scholar 

  • Robb L, Dimitriadis E, Li R, Salamonsen LA (2002) Leukemia inhibitory factor and interleukin-11: cytokines with key roles in implantation. J Reprod Immunol 57:129–141

    CAS  PubMed  Google Scholar 

  • Robertson SA (2005) Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res 322:43–52

    PubMed  Google Scholar 

  • Robertson SA, O’Connell A, Ramsey A (2000) The effect of interleukin-6 deficiency on implantation, fetal development and parturition in mice. Proc Aust Soc Reprod Biol 31:97

    Google Scholar 

  • Robertson SA, Guerin LR, Bromfield JJ, Branson KM, Ahlstrom AC, Care AS (2009a) Seminal fluid drives expansion of the CD4+CD25+ T regulatory cell pool and induces tolerance to paternal alloantigens in mice. Biol Reprod 80:1036–1045

    CAS  PubMed Central  PubMed  Google Scholar 

  • Robertson SA, Guerin LR, Moldenhauer LM, Hayball JD (2009b) Activating T regulatory cells for tolerance in early pregnancy – the contribution of seminal fluid. J Reprod Immunol 83:109–116

    CAS  PubMed  Google Scholar 

  • Rossant J, Cross JC (2001) Placental development: lessons from mouse mutants. Nat Rev Genet 2:538–548

    CAS  PubMed  Google Scholar 

  • Rowe JH, Ertelt JM, Xin L, Way SS (2012) Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature 490:102–106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sadowska A (2005) Pregnancy in women with systemic lupus erythematosus (SLE). Przegl Lek 62:61–64

    PubMed  Google Scholar 

  • Saito S (2000) Cytokine network at the feto-maternal interface. J Reprod Immunol 47:87–103

    CAS  PubMed  Google Scholar 

  • Saito S, Nakashima A, Shima T, Ito M (2010) Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol 63:601–610

    CAS  PubMed  Google Scholar 

  • Salamonsen LA (2003) Tissue injury and repair in the female human reproductive tract. Reproduction 125:301–311

    CAS  PubMed  Google Scholar 

  • Salker MS, Nautiyal J, Steel JH, Webster Z, Sucurovic S, Nicou M, Singh Y, Lucas ES, Murakami K, Chan YW, James S, Abdallah Y, Christian M, Croy BA, Mulac-Jericevic B, Quenby S, Brosens JJ (2012) Disordered IL-33/ST2 activation in decidualizing stromal cells prolongs uterine receptivity in women with recurrent pregnancy loss. PLoS One 7:e52252

    CAS  PubMed Central  PubMed  Google Scholar 

  • Santner-Nanan B, Peek MJ, Khanam R, Richarts L, Zhu E, Fazekas De St Groth B, Nanan R (2009) Systemic increase in the ratio between Foxp3+ and IL-17-producing CD4+ T cells in healthy pregnancy but not in preeclampsia. J Immunol 183:7023–7030

    CAS  PubMed  Google Scholar 

  • Scaife PJ, Bulmer JN, Robson SC, Innes BA, Searle RF (2006) Effector activity of decidual CD8+ T lymphocytes in early human pregnancy. Biol Reprod 75:562–567

    CAS  PubMed  Google Scholar 

  • Sharkey DJ, Macpherson AM, Tremellen KP, Mottershead DG, Gilchrist RB, Robertson SA (2012a) TGF-beta mediates proinflammatory seminal fluid signaling in human cervical epithelial cells. J Immunol 189:1024–1035

    CAS  PubMed  Google Scholar 

  • Sharkey DJ, Tremellen KP, Jasper MJ, Gemzell-Danielsson K, Robertson SA (2012b) Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J Immunol 188:2445–2454

    CAS  PubMed  Google Scholar 

  • Shobu T, Sageshima N, Tokui H, Omura M, Saito K, Nagatsuka Y, Nakanishi M, Hayashi Y, Hatake K, Ishitani A (2006) The surface expression of HLA-F on decidual trophoblasts increases from mid to term gestation. J Reprod Immunol 72:18–32

    CAS  PubMed  Google Scholar 

  • Shynlova O, Tsui P, Dorogin A, Lye SJ (2008) Monocyte chemoattractant protein-1 (CCL-2) integrates mechanical and endocrine signals that mediate term and preterm labor. J Immunol 181:1470–1479

    CAS  PubMed  Google Scholar 

  • Shynlova O, Lee YH, Srikhajon K, Lye S (2012) Physiologic uterine inflammation and labor onset: integration of endocrine and mechanical signals. Reprod Sci 20:154–167

    PubMed  Google Scholar 

  • Simon C, Pellicer A, Polan ML (1995) Interleukin-1 system crosstalk between embryo and endometrium in implantation. Hum Reprod 10(Suppl 2):43–54

    CAS  PubMed  Google Scholar 

  • Simon C, Mercader A, Gimeno MJ, Pellicer A (1997) The interleukin-1 system and human implantation. Am J Reprod Immunol 37:64–72

    CAS  PubMed  Google Scholar 

  • Skurupiy VA, Obedinskaya KS, Nadeev AP (2010) Structural manifestations of mechanisms of myometrium involution after repeated pregnancies in mice. Bull Exp Biol Med 149:554–558

    CAS  PubMed  Google Scholar 

  • Smith R (2007) Parturition. N Engl J Med 356:271–283

    CAS  PubMed  Google Scholar 

  • Smith GC, Crossley JA, Aitken DA, Pell JP, Cameron AD, Connor JM, Dobbie R (2004) First-trimester placentation and the risk of antepartum stillbirth. JAMA 292:2249–2254

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ (1992) Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359:76–79

    CAS  PubMed  Google Scholar 

  • Suman P, Malhotra SS, Gupta SK (2013) LIF-STAT signaling and trophoblast biology. JAKSTAT 2:e25155

    PubMed Central  PubMed  Google Scholar 

  • Szekeres-Bartho J, Wegmann TG (1996) A progesterone-dependent immunomodulatory protein alters the Th1/Th2 balance. J Reprod Immunol 31:81–95

    CAS  PubMed  Google Scholar 

  • Szekeres-Bartho J, Par G, Dombay G, Smart YC, Volgyi Z (1997) The antiabortive effect of progesterone-induced blocking factor in mice is manifested by modulating NK activity. Cell Immunol 177:194–199

    CAS  PubMed  Google Scholar 

  • Tabibzadeh S, Kong QF, Babaknia A, May LT (1995) Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window. Hum Reprod 10:2793–2799

    CAS  PubMed  Google Scholar 

  • Tang AW, Alfirevic Z, Quenby S (2011) Natural killer cells and pregnancy outcomes in women with recurrent miscarriage and infertility: a systematic review. Hum Reprod 26:1971–1980

    CAS  PubMed  Google Scholar 

  • Teles A, Zenclussen AC, Schumacher A (2013) Regulatory T cells are baby’s best friends. Am J Reprod Immunol 69:331–339

    CAS  PubMed  Google Scholar 

  • Thomson AJ, Telfer JF, Young A, Campbell S, Stewart CJ, Cameron IT, Greer IA, Norman JE (1999) Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Hum Reprod 14:229–236

    CAS  PubMed  Google Scholar 

  • Thuere C, Zenclussen ML, Schumacher A, Langwisch S, Schulte-Wrede U, Teles A, Paeschke S, Volk HD, Zenclussen AC (2007) Kinetics of regulatory T cells during murine pregnancy. Am J Reprod Immunol 58:514–523

    CAS  PubMed  Google Scholar 

  • Tilburgs T, Strominger JL (2013) CD8+ effector T cells at the fetal-maternal interface, balancing fetal tolerance and antiviral immunity. Am J Reprod Immunol 69:395–407

    CAS  PubMed  Google Scholar 

  • Tilburgs T, Roelen DL, Van Der Mast BJ, Van Schip JJ, Kleijburg C, De Groot-Swings GM, Kanhai HH, Claas FH, Scherjon SA (2006) Differential distribution of CD4(+)CD25(bright) and CD8(+)CD28(−) T-cells in decidua and maternal blood during human pregnancy. Placenta 27(Suppl A):S47–S53

    PubMed  Google Scholar 

  • Tilburgs T, Roelen DL, Van Der Mast BJ, De Groot-Swings GM, Kleijburg C, Scherjon SA, Claas FH (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 180:5737–5745

    CAS  PubMed  Google Scholar 

  • Tilburgs T, Schonkeren D, Eikmans M, Nagtzaam NM, Datema G, Swings GM, Prins F, Van Lith JM, Van Der Mast BJ, Roelen DL, Scherjon SA, Claas FH (2010) Human decidual tissue contains differentiated CD8+ effector-memory T cells with unique properties. J Immunol 185:4470–4477

    CAS  PubMed  Google Scholar 

  • Timmons BC, Fairhurst AM, Mahendroo MS (2009) Temporal changes in myeloid cells in the cervix during pregnancy and parturition. J Immunol 182:2700–2707

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tremellen KP, Seamark RF, Robertson SA (1998) Seminal transforming growth factor beta1 stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus. Biol Reprod 58:1217–1225

    CAS  PubMed  Google Scholar 

  • Tremellen KP, Valbuena D, Landeras J, Ballesteros A, Martinez J, Mendoza S, Norman RJ, Robertson SA, Simon C (2000) The effect of intercourse on pregnancy rates during assisted human reproduction. Hum Reprod 15:2653–2658

    CAS  PubMed  Google Scholar 

  • Vacca P, Vitale C, Montaldo E, Conte R, Cantoni C, Fulcheri E, Darretta V, Moretta L, Mingari MC (2011) CD34+ hematopoietic precursors are present in human decidua and differentiate into natural killer cells upon interaction with stromal cells. Proc Natl Acad Sci USA 108:2402–2407

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vacca P, Mingari MC, Moretta L (2013) Natural killer cells in human pregnancy. J Reprod Immunol 97:14–19

    CAS  PubMed  Google Scholar 

  • Wang WJ, Hao CF, Yi L, Yin GJ, Bao SH, Qiu LH, Lin QD (2010) Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J Reprod Immunol 84:164–170

    CAS  PubMed  Google Scholar 

  • Wegmann TG, Lin H, Guilbert L, Mosmann TR (1993) Bidirectional cytokine interactions in the maternal-fetal relationship – is successful pregnancy a Th2 phenomenon. Immunol Today 14:353–356

    CAS  PubMed  Google Scholar 

  • Wilcox AJ, Weinberg CR, O’connor JF, Baird DD, Schlatterer JP, Canfield RE, Armstrong EG, Nisula BC (1988) Incidence of early loss of pregnancy. N Engl J Med 319:189–194

    CAS  PubMed  Google Scholar 

  • Wilcox AJ, Baird DD, Weinberg CR (1999) Time of implantation of the conceptus and loss of pregnancy. N Engl J Med 340:1796–1799

    CAS  PubMed  Google Scholar 

  • Winkler M, Kemp B, Fischer DC, Ruck P, Rath W (2003) Expression of adhesion molecules in the lower uterine segment during term and preterm parturition. Microsc Res Tech 60:430–444

    CAS  PubMed  Google Scholar 

  • Woessner JF Jr (1996) Regulation of matrilysin in the rat uterus. Biochem Cell Biol 74:777–784

    CAS  PubMed  Google Scholar 

  • Yan Yuen S, Krizova A, Ouimet JM, Pope JE (2008) Pregnancy outcome in systemic lupus erythematosus (SLE) is improving: results from a case control study and literature review. Open Rheumatol J 2:89–98

    PubMed Central  PubMed  Google Scholar 

  • Yang Y, Chu W, Geraghty DE, Hunt JS (1996) Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-gamma. J Immunol 156:4224–4231

    CAS  PubMed  Google Scholar 

  • Yeaman GR, Guyre PM, Fanger MW, Collins JE, White HD, Rathbun W, Orndorff KA, Gonzalez J, Stern JE, Wira CR (1997) Unique CD8+ T cell-rich lymphoid aggregates in human uterine endometrium. J Leukoc Biol 61:427–435

    CAS  PubMed  Google Scholar 

  • Yeaman GR, Collins JE, Fanger MW, Wira CR, Lydyard PM (2001) CD8+ T cells in human uterine endometrial lymphoid aggregates: evidence for accumulation of cells by trafficking. Immunology 102:434–440

    CAS  PubMed Central  PubMed  Google Scholar 

  • Young A, Thomson AJ, Ledingham M, Jordan F, Greer IA, Norman JE (2002) Immunolocalization of proinflammatory cytokines in myometrium, cervix, and fetal membranes during human parturition at term. Biol Reprod 66:445–449

    CAS  PubMed  Google Scholar 

  • Zenclussen AC, Gentile T, Kortebani G, Mazzolli A, Margni R (2001) Asymmetric antibodies and pregnancy. Am J Reprod Immunol 45:289–294

    CAS  PubMed  Google Scholar 

  • Zenclussen ML, Thuere C, Ahmad N, Wafula PO, Fest S, Teles A, Leber A, Casalis PA, Bechmann I, Priller J, Volk HD, Zenclussen AC (2010) The persistence of paternal antigens in the maternal body is involved in regulatory T-cell expansion and fetal-maternal tolerance in murine pregnancy. Am J Reprod Immunol 63:200–208

    CAS  PubMed  Google Scholar 

  • Zhang J, Lathbury LJ, Salamonsen LA (2000) Expression of the chemokine eotaxin and its receptor, CCR3, in human endometrium. Biol Reprod 62:404–411

    CAS  PubMed  Google Scholar 

  • Zinaman MJ, Clegg ED, Brown CC, O’connor J, Selevan SG (1996) Estimates of human fertility and pregnancy loss. Fertil Steril 65:503–509

    CAS  PubMed  Google Scholar 

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  1. Institute of Biomedical and Environmental Health Research, University of the West of Scotland, Paisley, Scotland

    Fiona M. Menzies & Fiona L. Henriquez

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  1. Fiona M. Menzies
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  1. Department of Molecular Microbiology & Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA

    Sabra L. Klein

  2. Professor of Parasitology, Strathclyde Institute of Pharmacy & Biomedical Sciences, University of Strathclyde, Glasgow, United Kingdom

    Craig W. Roberts

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Menzies, F.M., Henriquez, F.L. (2015). Immunology of Pregnancy and Systemic Consequences. In: Klein, S., Roberts, C. (eds) Sex and Gender Differences in Infection and Treatments for Infectious Diseases. Springer, Cham. https://doi.org/10.1007/978-3-319-16438-0_3

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