From mice to women: The conundrum of immunity to infection during pregnancy

Journal of Reproductive Immunology

Volumn 97, Issue 1, 2013, Pages 62-73

  Krishnan, Lakshmi ^a,b   Nguyen, Tina ^a,b   McComb, Scott ^a,b  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Abortion; Immune response; Infection; Inflammation; Mouse; Pre term labor; Pregnancy

Indexed keywords

CD15 ANTIGEN; GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; TUMOR NECROSIS FACTOR ALPHA;

ADVERSE OUTCOME; ARTICLE; BACTERIAL INFECTION; BLASTOCYST; BRUCELLA ABORTUS; CHLAMYDIA; CHLAMYDOPHILA; CHLAMYDOPHILA ABORTUS; COXIELLA BURNETII; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; CYTOMEGALOVIRUS; DECIDUALIZATION; FEMALE; FUSOBACTERIUM NUCLEATUM; GESTATIONAL AGE; HUMAN; IMMUNITY; IMMUNOREACTIVITY; IMMUNOREGULATION; INFECTION RESISTANCE; INFLUENZA; LEISHMANIA MAJOR; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE; MALARIA; MATERNAL DISEASE; NATURAL KILLER CELL; NEUTROPHIL; NIDATION; NONHUMAN; PARASITOSIS; PATHOGENESIS; PERIODONTITIS; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PREGNANCY; PREGNANCY OUTCOME; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REPRODUCTION; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SCHISTOSOMA MANSONI; SPONTANEOUS ABORTION; T LYMPHOCYTE; TH1 CELL; TH2 CELL; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRYPANOSOMA CRUZI; VIRUS INFECTION;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FETOMATERNAL TRANSFUSION; HUMANS; IMMUNE EVASION; MICE; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PREMATURE BIRTH; TRANSPLANTATION TOLERANCE;

EID: 84874546874     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2012.10.015     Document Type: Article

References (117)

1. Abou-Bacar A., Pfaff A.W., Letscher-Bru V., Filisetti D., Rajapakse R., Antoni E., Villard O., Klein J.P., Candolfi E. Role of gamma interferon and T cells in congenital Toxoplasma transmission. Parasite Immunol. 2004, 26:315-318.
2. Abram M., Schluter D., Vuckovic D., Wraber B., Doric M., Deckert M. Murine model of pregnancy-associated Listeria monocytogenes infection. FEMS Immunol. Med. Microbiol. 2003, 35:177-182.
3. Aliberti J., Valenzuela J.G., Carruthers V.B., Hieny S., Andersen J., Charest H., Reis e Sousa, Fairlamb A., Ribeiro J.M., Sher A. Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nat. Immunol. 2003, 4:485-490.
4. + T-regulatory cells: toward therapy for human diseases. Immunol. Rev. 2008, 223:391-421.
5. Aluvihare V.R., Kallikourdis M., Betz A.G. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 2004, 5:266-271.
6. Arce R.M., Barros S.P., Wacker B., Peters B., Moss K., Offenbacher S. Increased TLR4 expression in murine placentas after oral infection with periodontal pathogens. Placenta 2009, 30:156-162.
7. Baban B., Chandler P., McCool D., Marshall B., Munn D.H., Mellor A.L. Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J. Reprod. Immunol. 2004, 61:67-77.
8. Baban B., Chandler P.R., Sharma M.D., Pihkala J., Koni P.A., Munn D.H., Mellor A.L. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J. Immunol. 2009, 183:2475-2483.
9. Benshushan A., Tsafrir A., Arbel R., Rahav G., Ariel I., Rojansky N. Listeria infection during pregnancy: a 10 year experience. Israel Med. Assoc. J. 2002, 4:776-780.
10. Blois S.M., Klapp B.F., Barrientos G. Decidualization and angiogenesis in early pregnancy: unravelling the functions of DC and NK cells. J. Reprod. Immunol. 2011, 88:86-92.
11. + NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J. Immunol. 2001, 166:6477-6482.
12. Cardenas I., Means R.E., Aldo P., Koga K., Lang S.M., Booth C., Manzur A., Oyarzun E., Romero R., Mor G. Viral infection of the placenta leads to fetal inflammation and sensitization to bacterial products predisposing to preterm labor. J. Immunol. 2010, 185:1248-1257.
13. Cardoni R.L., Antunez M.I. Outcome of Trypanosoma cruzi infection in pregnant BALB/c mice. Ann. Trop. Med. Parasitol. 2004, 98:883-887.
14. Caro M.R., Buendia A.J., del R.L., Ortega N., Gallego M.C., Cuello F., Navarro J.A., Sanchez J., Salinas J. Chlamydophila abortus infection in the mouse: a useful model of the ovine disease. Vet. Microbiol. 2009, 135:103-111.
15. Cetin I., Pileri P., Villa A., Calabrese S., Ottolenghi L., Abati S. Pathogenic mechanisms linking periodontal diseases with adverse pregnancy outcomes. Reprod. Sci. 2012, 19:633-641.
16. Chaouat G. Innately moving away from the Th1/Th2 paradigm in pregnancy. Clin. Exp. Immunol. 2003, 131:393-395.
17. Chaouat G., Menu E., Clark D.A., Dy M., Minkowski M., Wegmann T.G. Control of fetal survival in CBA×DBA/2 mice by lymphokine therapy. J. Reprod. Fertil. 1990, 89:447-458.
18. Chattopadhyay A., Robinson N., Sandhu J.K., Finlay B.B., Sad S., Krishnan L. Salmonella enterica serovar Typhimurium-induced placental inflammation and not bacterial burden correlates with pathology and fatal maternal disease. Infect. Immun. 2010, 78:2292-2301.
19. + regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 2009, 326:986-991.
20. Combe C.L., Curiel T.J., Moretto M.M., Khan I.A. NK cells help to induce CD8(+)-T-cell immunity against Toxoplasma gondii in the absence of CD4(+) T cells. Infect. Immun. 2005, 73:4913-4921.
21. Coutinho L.B., Gomes A.O., Araujo E.C., Barenco P.V., Santos J.L., Caixeta D.R., Silva D.A., Cunha-Junior J.P., Ferro E.A., Silva N.M. The impaired pregnancy outcome in murine congenital toxoplasmosis is associated with a pro-inflammatory immune response, but not correlated with decidual inducible nitric oxide synthase expression. Int. J. Parasitol. 2012, 42:341-352.
22. Croy B.A., Chen Z., Hofmann A.P., Lord E.M., Sedlacek A.L., Gerber S.A. Imaging of vascular development in early mouse decidua and its association with leukocytes and trophoblasts. Biol. Reprod. 2012.
23. Croy B.A., He H., Esadeg S., Wei Q., McCartney D., Zhang J., Borzychowski A., Ashkar A.A., Black G.P., Evans S.S., Chantakru S., van den H.M., Paffaro V.A., Yamada A.T. Uterine natural killer cells: insights into their cellular and molecular biology from mouse modelling. Reproduction 2003, 126:149-160.
24. D'Addio F., Riella L.V., Mfarrej B.G., Chabtini L., Adams L.T., Yeung M., Yagita H., Azuma M., Sayegh M.H., Guleria I. The link between the PDL1 costimulatory pathway and Th17 in fetomaternal tolerance. J. Immunol. 2011, 187:4530-4541.
25. Dauby N., Goetghebuer T., Kollmann T.R., Levy J., Marchant A. Uninfected but not unaffected: chronic maternal infections during pregnancy, fetal immunity, and susceptibility to postnatal infections. Lancet Infect. Dis. 2012, 12:330-340.
26. Debierre-Grockiego F., Campos M.A., Azzouz N., Schmidt J., Bieker U., Resende M.G., Mansur D.S., Weingart R., Schmidt R.R., Golenbock D.T., Gazzinelli R.T., Schwarz R.T. Activation of TLR2 and TLR4 by glycosylphosphatidylinositols derived from Toxoplasma gondii. J. Immunol. 2007, 179:1129-1137.
27. Diaz-Lujan C., Triquell M.F., Schijman A., Paglini P., Fretes R.E. Differential susceptibility of isolated human trophoblasts to infection by Trypanosoma cruzi. Placenta 2012, 33:264-270.
28. Elovitz M.A., Brown A.G., Breen K., Anton L., Maubert M., Burd I. Intrauterine inflammation, insufficient to induce parturition, still evokes fetal and neonatal brain injury. Int. J. Dev. Neurosci. 2011, 29:663-671.
29. Erlebacher A. Immune surveillance of the maternal/fetal interface: controversies and implications. Trends Endocrinol. Metab. 2010, 21:428-434.
30. Feasey N.A., Dougan G., Kingsley R.A., Heyderman R.S., Gordon M.A. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 2012, 379:2489-2499.
31. Friebe A., Arck P. Causes for spontaneous abortion: what the bugs 'gut' to do with it?. Int. J. Biochem. Cell Biol. 2008, 40:2348-2352.
32. Fried M., Domingo G.J., Gowda C.D., Mutabingwa T.K., Duffy P.E. Plasmodium falciparum: chondroitin sulfate A is the major receptor for adhesion of parasitized erythrocytes in the placenta. Exp. Parasitol. 2006, 113:36-42.
33. Friedman J.F., Mital P., Kanzaria H.K., Olds G.R., Kurtis J.D. Schistosomiasis and pregnancy. Trends Parasitol. 2007, 23:159-164.
34. Gauthier S., Tetu A., Himaya E., Morand M., Chandad F., Rallu F., Bujold E. The origin of Fusobacterium nucleatum involved in intra-amniotic infection and preterm birth. J. Matern. Fetal Neonatal Med. 2011, 24:1329-1332.
35. + T cells and accompanied by overproduction of IL-12, IFNgamma and TNFalpha. J. Immunol. 1996, 157:798-805.
36. Gonzalez I.T., Barrientos G., Freitag N., Otto T., Thijssen V.L., Moschansky P., von K.P., Klapp B.F., Winterhager E., Bauersachs S., Blois S.M. Uterine NK cells are critical in shaping DC immunogenic functions compatible with pregnancy progression. PLoS. ONE 2012, 7:e46755.
37. + cell pool and CCL19-mediated recruitment. Biol. Reprod. 2011, 85:397-408.
38. Guimond M.J., Luross J.A., Wang B., Terhorst C., Danial S., Croy B.A. Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 mice. Biol. Reprod. 1997, 56:169-179.
39. Guleria I., Khosroshahi A., Ansari M.J., Habicht A., Azuma M., Yagita H., Noelle R.J., Coyle A., Mellor A.L., Khoury S.J., Sayegh M.H. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J. Exp. Med. 2005, 202:231-237.
40. Guleria I., Pollard J.W. The trophoblast is a component of the innate immune system during pregnancy. Nat. Med. 2000, 6:589-593.
41. Guleria I., Pollard J.W. Aberrant macrophage and neutrophil population dynamics and impaired Th1 response to Listeria monocytogenes in colony-stimulating factor 1-deficient mice. Infect. Immun. 2001, 69:1795-1807.
42. Gyang A., Saunders M. Salmonella Mississippi: a rare cause of second trimester miscarriage. Arch. Gynecol. Obstet. 2008, 277:437-438.
43. Hamrick T.S., Horton J.R., Spears P.A., Havell E.A., Smoak I.W., Orndorff P.E. Influence of pregnancy on the pathogenesis of listeriosis in mice inoculated intragastrically. Infect. Immun. 2003, 71:5202-5209.
44. Han Y.W., Redline R.W., Li M., Yin L., Hill G.B., McCormick T.S. Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect. Immun. 2004, 72:2272-2279.
45. Harger J.H., Ernest J.M., Thurnau G.R., Moawad A., Momirova V., Landon M.B., Paul R., Miodovnik M., Dombrowski M., Sibai B., Van D.P. Risk factors and outcome of varicella-zoster virus pneumonia in pregnant women. J. Infect. Dis. 2002, 185:422-427.
46. Hayslett J.P. Maternal and fetal complications in pregnant women with systemic lupus erythematosus. Am. J. Kidney Dis. 1991, 17:123-126.
47. Hedriana H.L., Mitchell J.L., Williams S.B. Salmonella typhi chorioamnionitis in a human immunodeficiency virus-infected pregnant woman. A case report. J. Reprod. Med. 1995, 40:157-159.
48. Houser B.L., Tilburgs T., Hill J., Nicotra M.L., Strominger J.L. Two unique human decidual macrophage populations. J. Immunol. 2011, 186:2633-2642.
49. Hviid L., Marinho C.R., Staalsoe T., Penha-Goncalves C. Of mice and women: rodent models of placental malaria. Trends Parasitol. 2010, 26:412-419.
50. Ilievski V., Hirsch E. Synergy between viral and bacterial Toll-like receptors leads to amplification of inflammatory responses and preterm labor in the mouse. Biol. Reprod. 2010, 83:767-773.
51. Ito S., Ishii K.J., Shirota H., Klinman D.M. CpG oligodeoxynucleotides improve the survival of pregnant and fetal mice following Listeria monocytogenes infection. Infect. Immun. 2004, 72:3543-3548.
52. Jamieson D.J., Honein M.A., Rasmussen S.A., Williams J.L., Swerdlow D.L., Biggerstaff M.S., Lindstrom S., Louie J.K., Christ C.M., Bohm S.R., Fonseca V.P., Ritger K.A., Kuhles D.J., Eggers P., Bruce H., Davidson H.A., Lutterloh E., Harris M.L., Burke C., Cocoros N., Finelli L., MacFarlane K.F., Shu B., Olsen S.J. H1N1 2009 influenza virus infection during pregnancy in the USA. Lancet 2009, 374:451-458.
53. Jamieson D.J., Theiler R.N., Rasmussen S.A. Emerging infections and pregnancy. Emerg. Infect. Dis. 2006, 12:1638-1643.
54. Kim S., Lee D.S., Watanabe K., Furuoka H., Suzuki H., Watarai M. Interferon-gamma promotes abortion due to Brucella infection in pregnant mice. BMC Microbiol. 2005, 5:22.
55. Klipple G.L., Cecere F.A. Rheumatoid arthritis and pregnancy. Rheum. Dis. Clin. North Am. 1989, 15:213-239.
56. Krey G., Frank P., Shaikly V., Barrientos G., Cordo-Russo R., Ringel F., Moschansky P., Chernukhin I.V., Metodiev M., Fernandez N., Klapp B.F., Arck P.C., Blois S.M. In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development in mice. J. Mol. Med. (Berl.) 2008, 86:999-1011.
57. Krishnan L., Guilbert L.J., Russell A.S., Wegmann T.G., Mosmann T.R., Belosevic M. Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFNgamma response and increased production of T helper 2 cytokines. J. Immunol. 1996, 156:644-652.
58. Krishnan L., Guilbert L.J., Wegmann T.G., Belosevic M., Mosmann T.R. T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions, Correlation with increased IFNgamma and TNF and reduced IL-10 production by placental cells. J. Immunol. 1996, 156:653-662.
59. + T-cell acquired immune response against Listeria monocytogenes despite preferential placental colonization. Am. J. Reprod. Immunol. 2010, 63:54-65.
60. Le Monnier A., Autret N., Join-Lambert O.F., Jaubert F., Charbit A., Berche P., Kayal S. ActA is required for crossing of the fetoplacental barrier by Listeria monocytogenes. Infect. Immun. 2007, 75:950-957.
61. Le Monnier A., Join-Lambert O.F., Jaubert F., Berche P., Kayal S. Invasion of the placenta during murine listeriosis. Infect. Immun. 2006, 74:663-672.
62. Lecuit M., Nelson D.M., Smith S.D., Khun H., Huerre M., Vacher-Lavenu M.C., Gordon J.I., Cossart P. Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6152-6157.
63. Lee S.K., Kim J.Y., Lee M., Gilman-Sachs A., Kwak-Kim J. Th17 and regulatory T cells in women with recurrent pregnancy loss. Am. J. Reprod. Immunol. 2012, 67:311-318.
64. Lim H.J., Wang H. Uterine disorders and pregnancy complications: insights from mouse models. J. Clin. Invest. 2010, 120:1004-1015.
65. Lin D., Smith M.A., Champagne C., Elter J., Beck J., Offenbacher S. Porphyromonas gingivalis infection during pregnancy increases maternal tumor necrosis factor alpha, suppresses maternal interleukin-10, and enhances fetal growth restriction and resorption in mice. Infect. Immun. 2003, 71:5156-5162.
66. Lin H., Mosmann T.R., Guilbert L., Tuntipopipat S., Wegmann T.G. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J. Immunol. 1993, 151:4562-4573.
67. Liu H., Redline R.W., Han Y.W. Fusobacterium nucleatum induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response. J. Immunol. 2007, 179:2501-2508.
68. Luft B.J., Remington J.S. Effect of pregnancy on resistance to Listeria monocytogenes and Toxoplasma gondii infections in mice. Infect. Immun. 1982, 38:1164-1171.
69. + T Cell response during infection with virulent Salmonella typhimurium. J. Immunol. 2006, 177:1516-1525.
70. Marcelin G., Aldridge J.R., Duan S., Ghoneim H.E., Rehg J., Marjuki H., Boon A.C., McCullers J.A., Webby R.J. Fatal outcome of pandemic H1N1 2009 influenza virus infection is associated with immunopathology and impaired lung repair, not enhanced viral burden, in pregnant mice. J. Virol. 2011, 85:11208-11219.
71. Marinho C.R., Neres R., Epiphanio S., Goncalves L.A., Catarino M.B., Penha-Goncalves C. Recrudescent Plasmodium berghei from pregnant mice displays enhanced binding to the placenta and induces protection in multigravida. PLoS ONE 2009, 4:e5630.
72. McDonagh S., Maidji E., Ma W., Chang H.T., Fisher S., Pereira L. Viral and bacterial pathogens at the maternal-fetal interface. J. Infect. Dis. 2004, 190:826-834.
73. Megnekou R., Hviid L., Staalsoe T. Variant-specific immunity to Plasmodium berghei in pregnant mice. Infect. Immun. 2009, 77:1827-1834.
74. Menzies F.M., Henriquez F.L., Roberts C.W. Immunological control of congenital toxoplasmosis in the murine model. Immunol. Lett. 2008, 115:83-89.
75. Miller C.M., Boulter N.R., Ikin R.J., Smith N.C. The immunobiology of the innate response to Toxoplasma gondii. Int. J. Parasitol. 2009, 39:23-39.
76. Moffett-King A., Entrican G., Ellis S., Hutchinson J., Bainbridge D. Natural killer cells and reproduction. Trends Immunol. 2002, 23:332-333.
77. Montoya J.G., Remington J.S. Management of Toxoplasma gondii infection during pregnancy. Clin. Infect. Dis. 2008, 47:554-566.
78. Mor G. Inflammation and pregnancy: the role of Toll-like receptors in trophoblast-immune interaction. Ann. N. Y. Acad. Sci. 2008, 1127:121-128.
79. Mun H.S., Aosai F., Yano A. Role of Toxoplasma gondii HSP70 and Toxoplasma gondii HSP30/bag1 in antibody formation and prophylactic immunity in mice experimentally infected with Toxoplasma gondii. Microbiol. Immunol. 1999, 43:471-479.
80. Murphy S.P., Tayade C., Ashkar A.A., Hatta K., Zhang J., Croy B.A. Interferon gamma in successful pregnancies. Biol. Reprod. 2009, 80:848-859.
81. Nagamatsu T., Schust D.J. The contribution of macrophages to normal and pathological pregnancies. Am. J. Reprod. Immunol. 2010, 63:460-471.
82. Nancy P., Tagliani E., Tay C.S., Asp P., Levy D.E., Erlebacher A. Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface. Science 2012, 336:1317-1321.
83. Neres R., Marinho C.R., Goncalves L.A., Catarino M.B., Penha-Goncalves C. Pregnancy outcome and placenta pathology in Plasmodium berghei ANKA infected mice reproduce the pathogenesis of severe malaria in pregnant women. PLoS ONE 2008, 3:e1608.
84. Ozer O., Cebesoy F.B., Sari I., Davutoglu V. A case of Salmonella typhi endocarditis in pregnancy. Am. J. Med. Sci. 2009, 337:210-211.
85. Pappas G., Roussos N., Falagas M.E. Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int. J. Parasitol. 2009, 39:1385-1394.
86. Pazos M., Sperling R.S., Moran T.M., Kraus T.A. The influence of pregnancy on systemic immunity. Immunol. Res. 2012.
87. Pazos M.A., Kraus T.A., Munoz-Fontela C., Moran T.M. Estrogen mediates innate and adaptive immune alterations to influenza infection in pregnant mice. PLoS ONE 2012, 7:e40502.
88. Pejcic-Karapetrovic B., Gurnani K., Russell M.S., Finlay B.B., Sad S., Krishnan L. Pregnancy impairs the innate immune resistance to Salmonella typhimurium leading to rapid fatal infection. J. Immunol. 2007, 179:6088-6096.
89. Poovassery J.S., Sarr D., Smith G., Nagy T., Moore J.M. Malaria-induced murine pregnancy failure: distinct roles for IFNgamma and TNF. J. Immunol. 2009, 183:5342-5349.
90. Redline R.W. Placental inflammation. Semin. Neonatol. 2004, 9:265-274.
91. Robbins J.R., Bakardjiev A.I. Pathogens and the placental fortress. Curr. Opin. Microbiol. 2012, 15:36-43.
92. Roberts C.W., Alexander J. Studies on a murine model of congenital toxoplasmosis: vertical disease transmission only occurs in BALB/c mice infected for the first time during pregnancy. Parasitology 1992, 104(Pt 1):19-23.
93. Rossant J., Cross J.C. Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2001, 2:538-548.
94. Rowe J.H., Ertelt J.M., Aguilera M.N., Farrar M.A., Way S.S. Foxp3(+) regulatory T cell expansion required for sustaining pregnancy compromises host defense against prenatal bacterial pathogens. Cell Host Microbe 2011, 10:54-64.
95. Saito S., Nakashima A., Shima T., Ito M. Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am. J. Reprod. Immunol. 2010, 63:601-610.
96. Samstein R.M., Josefowicz S.Z., Arvey A., Treuting P.M., Rudensky A.Y. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 2012, 150:29-38.
97. Santos R.L., Zhang S., Tsolis R.M., Kingsley R.A., Adams L.G., Baumler A.J. Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect. 2001, 3:1335-1344.
98. Schloesser R.L., Schaefer V., Groll A.H. Fatal transplacental infection with non-typhoidal Salmonella. Scand. J. Infect. Dis. 2004, 36:773-774.
99. Scialli A.R., Rarick T.L. Salmonella sepsis and second-trimester pregnancy loss. Obstet. Gynecol. 1992, 79:820-821.
100. Seveau S., Pizarro-Cerda J., Cossart P. Molecular mechanisms exploited by Listeria monocytogenes during host cell invasion. Microbes Infect. 2007, 9:1167-1175.
101. Shiono Y., Mun H.S., He N., Nakazaki Y., Fang H., Furuya M., Aosai F., Yano A. Maternal-fetal transmission of Toxoplasma gondii in interferon-gamma deficient pregnant mice. Parasitol. Int. 2007, 56:141-148.
102. Shirahata T., Muroya N., Ohta C., Goto H., Nakane A. Correlation between increased susceptibility to primary Toxoplasma gondii infection and depressed production of gamma interferon in pregnant mice. Microbiol. Immunol. 1992, 36:81-91.
103. Shirahata T., Muroya N., Ohta C., Goto H., Nakane A. Enhancement by recombinant human interleukin 2 of host resistance to Toxoplasma gondii infection in pregnant mice. Microbiol. Immunol. 1993, 37:583-590.
104. + T lymphocytes are the major cell population involved in the early gamma interferon response and resistance to acute primary Toxoplasma gondii infection in mice. Microbiol. Immunol. 1994, 38:789-796.
105. Sica A., Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J. Clin. Invest. 2012, 122:787-795.
106. Stein A., Lepidi H., Mege J.L., Marrie T.J., Raoult D. Repeated pregnancies in BALB/c mice infected with Coxiella burnetii cause disseminated infection, resulting in stillbirth and endocarditis. J. Infect. Dis. 2000, 181:188-194.
107. Stephens R., Culleton R.L., Lamb T.J. The contribution of Plasmodium chabaudi to our understanding of malaria. Trends Parasitol. 2012, 28:73-82.
108. Stern D.A., Riedler J., Nowak D., Braun-Fahrlander C., Swoboda I., Balic N., Chen K.W., Vrtala S., Gronlund H., van H.M., Valenta R., Spitzauer S., von M.E., Vercelli D. Exposure to a farming environment has allergen-specific protective effects on Th2-dependent isotype switching in response to common inhalants. J. Allergy Clin. Immunol. 2007, 119:351-358.
109. Su Z., Stevenson M.M. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect. Immun. 2000, 68:4399-4406.
110. Valdez Y., Ferreira R.B., Finlay B.B. Molecular mechanisms of Salmonella virulence and host resistance. Curr. Top. Microbiol. Immunol. 2009, 337:93-127.
111. van der Klooster J.M., Roelofs H.J. Management of Salmonella infections during pregnancy and puerperium. Neth. J. Med. 1997, 51:83-86.
112. Warning J.C., McCracken S.A., Morris J.M. A balancing act: mechanisms by which the fetus avoids rejection by the maternal immune system. Reproduction 2011, 141:715-724.
113. Wegmann T.G., Lin H., Guilbert L., Mosmann T.R. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a Th2 phenomenon? [see comments]. Immunol. Today 1993, 14:353-356.
114. Witkin S.S., Linhares I.M., Bongiovanni A.M., Herway C., Skupski D. Unique alterations in infection-induced immune activation during pregnancy. BJOG 2011, 118:145-153.
115. Wong S.F., Chow K.M., de S.M. Severe acute respiratory syndrome and pregnancy. BJOG 2003, 110:641-642.
116. Zeldovich V.B., Robbins J.R., Kapidzic M., Lauer P., Bakardjiev A.I. Invasive extravillous trophoblasts restrict intracellular growth and spread of Listeria monocytogenes. PLoS Pathog. 2011, 7:e1002005.
117. Zenclussen A.C., Gerlof K., Zenclussen M.L., Ritschel S., Zambon B.A., Fest S., Hontsu S., Ueha S., Matsushima K., Leber J., Volk H.D. Regulatory T cells induce a privileged tolerant microenvironment at the fetal-maternal interface. Eur. J. Immunol. 2006, 36:82-94.