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Published in: Seminars in Immunopathology 6/2017

01-11-2017 | Review

Transfer of maternal immunity and programming of the newborn immune system

Authors: Madeleine F. Jennewein, Bahaa Abu-Raya, Yiwei Jiang, Galit Alter, Arnaud Marchant

Published in: Seminars in Immunopathology | Issue 6/2017

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Abstract

As placental mammals, the pregnant women and the fetus have intense and prolonged interactions during gestation. There is increasing evidence that multiple molecular as well as cellular components originating in pregnant women are transferred to the fetus. The transfer of maternal antibodies has long been recognized as a central component of newborn immunity against pathogens. More recent studies indicate that inflammatory mediators, micronutrients, microbial products and maternal cells are transferred in utero and influence the fetal immune system. Together, these multiple signals are likely to form a complex network of interactions that program the neonatal immune system and tune its homeostatic regulation. Maternal disorders, in particular infectious diseases, modify these signals and may thereby alter immunity in early life. Understanding maternal programming of the newborn immune system could provide a basis for interventions promoting child health.
Literature
2.
go back to reference Ghazal P, Dickinson P, Smith CL (2013) Early life response to infection. Curr Opin Infect Dis 26(3):213–218CrossRefPubMed Ghazal P, Dickinson P, Smith CL (2013) Early life response to infection. Curr Opin Infect Dis 26(3):213–218CrossRefPubMed
3.
go back to reference Marchant A, Sadarangani M, Garand M, Dauby N, Verhasselt V, Pereira L et al (2017) Maternal immunisation: collaborating with mother nature. Lancet Infect Dis 17(7):e197–e208CrossRefPubMed Marchant A, Sadarangani M, Garand M, Dauby N, Verhasselt V, Pereira L et al (2017) Maternal immunisation: collaborating with mother nature. Lancet Infect Dis 17(7):e197–e208CrossRefPubMed
4.
go back to reference Abu-Raya B, Edwards KM, Scheifele DW, Halperin SA (2017) Pertussis and influenza immunisation during pregnancy: a landscape review. Lancet Infect Dis 17(7):e209–e222CrossRefPubMed Abu-Raya B, Edwards KM, Scheifele DW, Halperin SA (2017) Pertussis and influenza immunisation during pregnancy: a landscape review. Lancet Infect Dis 17(7):e209–e222CrossRefPubMed
5.
go back to reference Heath PT, Culley FJ, Jones CE, Kampmann B, Le Doare K, Nunes MC et al (2017) Group B streptococcus and respiratory syncytial virus immunisation during pregnancy: a landscape analysis. Lancet Infect Dis 17(7):e223–e234CrossRefPubMed Heath PT, Culley FJ, Jones CE, Kampmann B, Le Doare K, Nunes MC et al (2017) Group B streptococcus and respiratory syncytial virus immunisation during pregnancy: a landscape analysis. Lancet Infect Dis 17(7):e223–e234CrossRefPubMed
6.
go back to reference DeSesso JM, Williams AL, Ahuja A, Bowman CJ, Hurtt ME (2012) The placenta, transfer of immunoglobulins, and safety assessment of biopharmaceuticals in pregnancy. Crit Rev Toxicol 42(3):185–210CrossRefPubMed DeSesso JM, Williams AL, Ahuja A, Bowman CJ, Hurtt ME (2012) The placenta, transfer of immunoglobulins, and safety assessment of biopharmaceuticals in pregnancy. Crit Rev Toxicol 42(3):185–210CrossRefPubMed
7.
go back to reference Silverstein AM (1996) Paul Ehrlich: the founding of pediatric immunology. Cell Immunol 174(1):1–6CrossRefPubMed Silverstein AM (1996) Paul Ehrlich: the founding of pediatric immunology. Cell Immunol 174(1):1–6CrossRefPubMed
8.
go back to reference Bundhoo A, Paveglio S, Rafti E, Dhongade A, Blumberg RS, Matson AP (2015 Jun) Evidence that FcRn mediates the transplacental passage of maternal IgE in the form of IgG anti-IgE/IgE immune complexes. Clin Exp Allergy J Br Soc Allergy Clin Immunol 45(6):1085–1098CrossRef Bundhoo A, Paveglio S, Rafti E, Dhongade A, Blumberg RS, Matson AP (2015 Jun) Evidence that FcRn mediates the transplacental passage of maternal IgE in the form of IgG anti-IgE/IgE immune complexes. Clin Exp Allergy J Br Soc Allergy Clin Immunol 45(6):1085–1098CrossRef
9.
go back to reference Palmeira P, Quinello C, Silveira-Lessa AL, Zago CA, Carneiro-Sampaio M (2012) IgG placental transfer in healthy and pathological pregnancies. Clin Dev Immunol 2012:985646CrossRefPubMed Palmeira P, Quinello C, Silveira-Lessa AL, Zago CA, Carneiro-Sampaio M (2012) IgG placental transfer in healthy and pathological pregnancies. Clin Dev Immunol 2012:985646CrossRefPubMed
10.
go back to reference van den Berg JP, Westerbeek E (2011) A. M, van der Klis FRM, Berbers G a. M, van Elburg RM. Transplacental transport of IgG antibodies to preterm infants: a review of the literature. Early Hum Dev 87(2):67–72CrossRefPubMed van den Berg JP, Westerbeek E (2011) A. M, van der Klis FRM, Berbers G a. M, van Elburg RM. Transplacental transport of IgG antibodies to preterm infants: a review of the literature. Early Hum Dev 87(2):67–72CrossRefPubMed
11.
go back to reference Roopenian DC, Akilesh S (2007) FcRn: the neonatal fc receptor comes of age. Nat Rev Immunol 7(9):715–725CrossRefPubMed Roopenian DC, Akilesh S (2007) FcRn: the neonatal fc receptor comes of age. Nat Rev Immunol 7(9):715–725CrossRefPubMed
12.
go back to reference Einarsdottir HK, Stapleton NM, Scherjon S, Andersen JT, Rispens T, van der Schoot CE et al (2014) On the perplexingly low rate of transport of IgG2 across the human placenta. PLoS One 9(9):e108319CrossRefPubMedPubMedCentral Einarsdottir HK, Stapleton NM, Scherjon S, Andersen JT, Rispens T, van der Schoot CE et al (2014) On the perplexingly low rate of transport of IgG2 across the human placenta. PLoS One 9(9):e108319CrossRefPubMedPubMedCentral
13.
go back to reference van den Berg JP, Westerbeek EAM, Berbers GAM, van Gageldonk PGM, van der Klis FRM, van Elburg RM (2010) Transplacental transport of IgG antibodies specific for pertussis, diphtheria, tetanus, haemophilus influenzae type b, and Neisseria meningitidis serogroup C is lower in preterm compared with term infants. Pediatr Infect Dis J 29(9):801–805CrossRefPubMed van den Berg JP, Westerbeek EAM, Berbers GAM, van Gageldonk PGM, van der Klis FRM, van Elburg RM (2010) Transplacental transport of IgG antibodies specific for pertussis, diphtheria, tetanus, haemophilus influenzae type b, and Neisseria meningitidis serogroup C is lower in preterm compared with term infants. Pediatr Infect Dis J 29(9):801–805CrossRefPubMed
14.
go back to reference Jennewein MF, Alter G (2017) The Immunoregulatory roles of antibody glycosylation. Trends Immunol 38(5):358–372CrossRefPubMed Jennewein MF, Alter G (2017) The Immunoregulatory roles of antibody glycosylation. Trends Immunol 38(5):358–372CrossRefPubMed
15.
go back to reference Bondt A, Rombouts Y, Selman MHJ, Hensbergen PJ, Reiding KR, Hazes JMW et al (2014) Immunoglobulin G (IgG) fab glycosylation analysis using a new mass spectrometric high-throughput profiling method reveals pregnancy-associated changes. Mol Cell Proteomics MCP 13(11):3029–3039CrossRefPubMed Bondt A, Rombouts Y, Selman MHJ, Hensbergen PJ, Reiding KR, Hazes JMW et al (2014) Immunoglobulin G (IgG) fab glycosylation analysis using a new mass spectrometric high-throughput profiling method reveals pregnancy-associated changes. Mol Cell Proteomics MCP 13(11):3029–3039CrossRefPubMed
16.
go back to reference Jansen BC, Bondt A, Reiding KR, Scherjon SA, Vidarsson G, Wuhrer M (2016) MALDI-TOF-MS reveals differential N-linked plasma- and IgG-glycosylation profiles between mothers and their newborns. Sci Rep 6:34001CrossRefPubMedPubMedCentral Jansen BC, Bondt A, Reiding KR, Scherjon SA, Vidarsson G, Wuhrer M (2016) MALDI-TOF-MS reveals differential N-linked plasma- and IgG-glycosylation profiles between mothers and their newborns. Sci Rep 6:34001CrossRefPubMedPubMedCentral
17.
go back to reference Einarsdottir HK, Selman MHJ, Kapur R, Scherjon S, Koeleman CAM, Deelder AM et al (2013) Comparison of the fc glycosylation of fetal and maternal immunoglobulin G. Glycoconj J 30(2):147–157CrossRefPubMed Einarsdottir HK, Selman MHJ, Kapur R, Scherjon S, Koeleman CAM, Deelder AM et al (2013) Comparison of the fc glycosylation of fetal and maternal immunoglobulin G. Glycoconj J 30(2):147–157CrossRefPubMed
18.
19.
go back to reference Dashivets T, Thomann M, Rueger P, Knaupp A, Buchner J, Schlothauer T (2015) Multi-angle effector function analysis of human monoclonal IgG Glycovariants. PLoS One 10(12):e0143520CrossRefPubMedPubMedCentral Dashivets T, Thomann M, Rueger P, Knaupp A, Buchner J, Schlothauer T (2015) Multi-angle effector function analysis of human monoclonal IgG Glycovariants. PLoS One 10(12):e0143520CrossRefPubMedPubMedCentral
20.
go back to reference Freiberger T, Ravcuková B, Grodecká L, Kurecová B, Jarkovský J, Bartonková D et al (2010) No association of FCRN promoter VNTR polymorphism with the rate of maternal-fetal IgG transfer. J Reprod Immunol 85(2):193–197CrossRefPubMed Freiberger T, Ravcuková B, Grodecká L, Kurecová B, Jarkovský J, Bartonková D et al (2010) No association of FCRN promoter VNTR polymorphism with the rate of maternal-fetal IgG transfer. J Reprod Immunol 85(2):193–197CrossRefPubMed
21.
go back to reference Shields RL, Namenuk AK, Hong K, Meng YG, Rae J, Briggs J et al (2001) High resolution mapping of the binding site on human IgG1 for fc gamma RI, fc gamma RII, fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the fc gamma R. J Biol Chem 276(9):6591–6604CrossRefPubMed Shields RL, Namenuk AK, Hong K, Meng YG, Rae J, Briggs J et al (2001) High resolution mapping of the binding site on human IgG1 for fc gamma RI, fc gamma RII, fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the fc gamma R. J Biol Chem 276(9):6591–6604CrossRefPubMed
22.
go back to reference Takizawa T, Anderson CL, Robinson JM (2005) A novel Fc gamma R-defined, IgG-containing organelle in placental endothelium. J Immunol 175(4):2331–2339CrossRefPubMed Takizawa T, Anderson CL, Robinson JM (2005) A novel Fc gamma R-defined, IgG-containing organelle in placental endothelium. J Immunol 175(4):2331–2339CrossRefPubMed
23.
go back to reference Mishima T, Kurasawa G, Ishikawa G, Mori M, Kawahigashi Y, Ishikawa T et al (2007) Endothelial expression of fc gamma receptor IIb in the full-term human placenta. Placenta 28(2–3):170–174CrossRefPubMed Mishima T, Kurasawa G, Ishikawa G, Mori M, Kawahigashi Y, Ishikawa T et al (2007) Endothelial expression of fc gamma receptor IIb in the full-term human placenta. Placenta 28(2–3):170–174CrossRefPubMed
24.
go back to reference Van Den Herik-Oudijk IE, Westerdaal NA, Henriquez NV, Capel PJ, Van De Winkel JG (1994) Functional analysis of human Fc gamma RII (CD32) isoforms expressed in B lymphocytes. J Immunol 152(2):574–585 Van Den Herik-Oudijk IE, Westerdaal NA, Henriquez NV, Capel PJ, Van De Winkel JG (1994) Functional analysis of human Fc gamma RII (CD32) isoforms expressed in B lymphocytes. J Immunol 152(2):574–585
25.
go back to reference Ishikawa T, Takizawa T, Iwaki J, Mishima T, Ui-Tei K, Takeshita T et al (2015) Fc gamma receptor IIb participates in maternal IgG trafficking of human placental endothelial cells. Int J Mol Med 35(5):1273–1289CrossRefPubMedPubMedCentral Ishikawa T, Takizawa T, Iwaki J, Mishima T, Ui-Tei K, Takeshita T et al (2015) Fc gamma receptor IIb participates in maternal IgG trafficking of human placental endothelial cells. Int J Mol Med 35(5):1273–1289CrossRefPubMedPubMedCentral
26.
go back to reference Bruhns P, Iannascoli B, England P, Mancardi DA, Fernandez N, Jorieux S et al (2009) Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood 113(16):3716–3725CrossRefPubMed Bruhns P, Iannascoli B, England P, Mancardi DA, Fernandez N, Jorieux S et al (2009) Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood 113(16):3716–3725CrossRefPubMed
27.
go back to reference Mohanty S, Kim J, Ganesan LP, Phillips GS, Hua K, Jarjoura D et al (2010) IgG is transported across the mouse yolk sac independently of FcgammaRIIb. J Reprod Immunol 84(2):133–144CrossRefPubMed Mohanty S, Kim J, Ganesan LP, Phillips GS, Hua K, Jarjoura D et al (2010) IgG is transported across the mouse yolk sac independently of FcgammaRIIb. J Reprod Immunol 84(2):133–144CrossRefPubMed
28.
go back to reference Abu Raya B, Srugo I, Kessel A, Peterman M, Bader D, Peri R et al (2014) The induction of breast milk pertussis specific antibodies following gestational tetanus-diphtheria-acellular pertussis vaccination. Vaccine 32(43):5632–5637CrossRefPubMed Abu Raya B, Srugo I, Kessel A, Peterman M, Bader D, Peri R et al (2014) The induction of breast milk pertussis specific antibodies following gestational tetanus-diphtheria-acellular pertussis vaccination. Vaccine 32(43):5632–5637CrossRefPubMed
29.
go back to reference De Schutter S, Maertens K, Baerts L, De Meester I, Van Damme P, Leuridan E (2015) Quantification of vaccine-induced antipertussis toxin secretory IgA antibodies in breast milk: comparison of different vaccination strategies in women. Pediatr Infect Dis J 34(6):e149–e152CrossRefPubMed De Schutter S, Maertens K, Baerts L, De Meester I, Van Damme P, Leuridan E (2015) Quantification of vaccine-induced antipertussis toxin secretory IgA antibodies in breast milk: comparison of different vaccination strategies in women. Pediatr Infect Dis J 34(6):e149–e152CrossRefPubMed
30.
go back to reference Burton GJ, Hempstock J, Jauniaux E (2001) Nutrition of the human fetus during the first trimester--a review. Placenta 22(Suppl A):S70–S77CrossRefPubMed Burton GJ, Hempstock J, Jauniaux E (2001) Nutrition of the human fetus during the first trimester--a review. Placenta 22(Suppl A):S70–S77CrossRefPubMed
32.
go back to reference Pabst O, Cerovic V, Hornef M (2016) Secretory IgA in the coordination of establishment and maintenance of the microbiota. Trends Immunol 37(5):287–296CrossRefPubMed Pabst O, Cerovic V, Hornef M (2016) Secretory IgA in the coordination of establishment and maintenance of the microbiota. Trends Immunol 37(5):287–296CrossRefPubMed
33.
go back to reference Magri G, Comerma L, Pybus M, Sintes J, Lligé D, Segura-Garzón D et al (2017) Human Secretory IgM Emerges from Plasma Cells Clonally Related to Gut Memory B Cells and Targets Highly Diverse Commensals. Immunity 47(1):118–34.e8CrossRefPubMedPubMedCentral Magri G, Comerma L, Pybus M, Sintes J, Lligé D, Segura-Garzón D et al (2017) Human Secretory IgM Emerges from Plasma Cells Clonally Related to Gut Memory B Cells and Targets Highly Diverse Commensals. Immunity 47(1):118–34.e8CrossRefPubMedPubMedCentral
34.
go back to reference Abu-Raya B, Smolen KK, Willems F, Kollmann TR, Marchant A (2016) Transfer of maternal antimicrobial immunity to HIV-exposed uninfected newborns. Front Immunol 7:338PubMedPubMedCentral Abu-Raya B, Smolen KK, Willems F, Kollmann TR, Marchant A (2016) Transfer of maternal antimicrobial immunity to HIV-exposed uninfected newborns. Front Immunol 7:338PubMedPubMedCentral
35.
go back to reference Chau TNB, Hieu NT, Anders KL, Wolbers M, Lien LB, Hieu LTM et al (2009) Dengue virus infections and maternal antibody decay in a prospective birth cohort study of Vietnamese infants. J Infect Dis 200(12):1893–1900CrossRefPubMedPubMedCentral Chau TNB, Hieu NT, Anders KL, Wolbers M, Lien LB, Hieu LTM et al (2009) Dengue virus infections and maternal antibody decay in a prospective birth cohort study of Vietnamese infants. J Infect Dis 200(12):1893–1900CrossRefPubMedPubMedCentral
36.
go back to reference Okoko BJ, Wesumperuma LH, Ota MO, Pinder M, Banya W, Gomez SF et al (2001) The influence of placental malaria infection and maternal hypergammaglobulinemia on transplacental transfer of antibodies and IgG subclasses in a rural west African population. J Infect Dis 184(5):627–632CrossRefPubMed Okoko BJ, Wesumperuma LH, Ota MO, Pinder M, Banya W, Gomez SF et al (2001) The influence of placental malaria infection and maternal hypergammaglobulinemia on transplacental transfer of antibodies and IgG subclasses in a rural west African population. J Infect Dis 184(5):627–632CrossRefPubMed
37.
go back to reference Klase ZA, Khakhina S, Schneider ADB, Callahan MV, Glasspool-Malone J, Malone R (2016) Zika fetal Neuropathogenesis: etiology of a viral syndrome. PLoS Negl Trop Dis 10(8):e0004877CrossRefPubMedPubMedCentral Klase ZA, Khakhina S, Schneider ADB, Callahan MV, Glasspool-Malone J, Malone R (2016) Zika fetal Neuropathogenesis: etiology of a viral syndrome. PLoS Negl Trop Dis 10(8):e0004877CrossRefPubMedPubMedCentral
38.
go back to reference Sonneveld ME, Natunen S, Sainio S, Koeleman CAM, Holst S, Dekkers G et al (2016) Glycosylation pattern of anti-platelet IgG is stable during pregnancy and predicts clinical outcome in alloimmune thrombocytopenia. Br J Haematol 174(2):310–320CrossRefPubMed Sonneveld ME, Natunen S, Sainio S, Koeleman CAM, Holst S, Dekkers G et al (2016) Glycosylation pattern of anti-platelet IgG is stable during pregnancy and predicts clinical outcome in alloimmune thrombocytopenia. Br J Haematol 174(2):310–320CrossRefPubMed
39.
go back to reference Sonneveld ME, Koelewijn J, de Haas M, Admiraal J, Plomp R, Koeleman CAM et al (2017) Antigen specificity determines anti-red blood cell IgG-fc alloantibody glycosylation and thereby severity of haemolytic disease of the fetus and newborn. Br J Haematol 176(4):651–660CrossRefPubMed Sonneveld ME, Koelewijn J, de Haas M, Admiraal J, Plomp R, Koeleman CAM et al (2017) Antigen specificity determines anti-red blood cell IgG-fc alloantibody glycosylation and thereby severity of haemolytic disease of the fetus and newborn. Br J Haematol 176(4):651–660CrossRefPubMed
40.
go back to reference Zinkernagel RM (2001) Maternal antibodies, childhood infections, and autoimmune diseases. N Engl J Med 345(18):1331–1335CrossRefPubMed Zinkernagel RM (2001) Maternal antibodies, childhood infections, and autoimmune diseases. N Engl J Med 345(18):1331–1335CrossRefPubMed
41.
go back to reference Siegrist CA (2003) Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypotheses and definition of main determinants. Vaccine 21(24):3406–3412CrossRefPubMed Siegrist CA (2003) Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypotheses and definition of main determinants. Vaccine 21(24):3406–3412CrossRefPubMed
42.
go back to reference Niewiesk S (2014) Maternal antibodies: clinical significance, mechanism of interference with immune responses, and possible vaccination strategies. Front Immunol 5:446CrossRefPubMedPubMedCentral Niewiesk S (2014) Maternal antibodies: clinical significance, mechanism of interference with immune responses, and possible vaccination strategies. Front Immunol 5:446CrossRefPubMedPubMedCentral
43.
go back to reference Gans HA, Arvin AM, Galinus J, Logan L, DeHovitz R, Maldonado Y (1998) Deficiency of the humoral immune response to measles vaccine in infants immunized at age 6 months. JAMA 280(6):527–532CrossRefPubMed Gans HA, Arvin AM, Galinus J, Logan L, DeHovitz R, Maldonado Y (1998) Deficiency of the humoral immune response to measles vaccine in infants immunized at age 6 months. JAMA 280(6):527–532CrossRefPubMed
44.
go back to reference Nair N, Gans H, Lew-Yasukawa L, Long-Wagar AC, Arvin A, Griffin DE (2007) Age-dependent differences in IgG isotype and avidity induced by measles vaccine received during the first year of life. J Infect Dis 196(9):1339–1345CrossRefPubMed Nair N, Gans H, Lew-Yasukawa L, Long-Wagar AC, Arvin A, Griffin DE (2007) Age-dependent differences in IgG isotype and avidity induced by measles vaccine received during the first year of life. J Infect Dis 196(9):1339–1345CrossRefPubMed
45.
go back to reference Maertens K, Hoang TTH, Nguyen TD, Caboré RN, Duong TH, Huygen K et al (2016) The effect of maternal pertussis immunization on infant vaccine responses to a booster pertussis-containing vaccine in Vietnam. Clin Infect Dis Off Publ Infect Dis Soc Am 63(suppl 4):S197–S204CrossRef Maertens K, Hoang TTH, Nguyen TD, Caboré RN, Duong TH, Huygen K et al (2016) The effect of maternal pertussis immunization on infant vaccine responses to a booster pertussis-containing vaccine in Vietnam. Clin Infect Dis Off Publ Infect Dis Soc Am 63(suppl 4):S197–S204CrossRef
46.
go back to reference Kim D, Huey D, Oglesbee M, Niewiesk S (2011) Insights into the regulatory mechanism controlling the inhibition of vaccine-induced seroconversion by maternal antibodies. Blood 117(23):6143–6151CrossRefPubMedPubMedCentral Kim D, Huey D, Oglesbee M, Niewiesk S (2011) Insights into the regulatory mechanism controlling the inhibition of vaccine-induced seroconversion by maternal antibodies. Blood 117(23):6143–6151CrossRefPubMedPubMedCentral
47.
go back to reference Feunou PF, Mielcarek N, Locht C (2016) Reciprocal interference of maternal and infant immunization in protection against pertussis. Vaccine 34(8):1062–1069CrossRefPubMed Feunou PF, Mielcarek N, Locht C (2016) Reciprocal interference of maternal and infant immunization in protection against pertussis. Vaccine 34(8):1062–1069CrossRefPubMed
48.
go back to reference Maertens K, Caboré RN, Huygen K, Vermeiren S, Hens N, Van Damme P et al (2016) Pertussis vaccination during pregnancy in Belgium: follow-up of infants until 1 month after the fourth infant pertussis vaccination at 15 months of age. Vaccine 34(31):3613–3619CrossRefPubMed Maertens K, Caboré RN, Huygen K, Vermeiren S, Hens N, Van Damme P et al (2016) Pertussis vaccination during pregnancy in Belgium: follow-up of infants until 1 month after the fourth infant pertussis vaccination at 15 months of age. Vaccine 34(31):3613–3619CrossRefPubMed
49.
go back to reference Winter K, Cherry JD, Harriman K (2017) Effectiveness of prenatal tetanus, diphtheria, and acellular pertussis vaccination on pertussis severity in infants. Clin Infect Dis 64(1):9–14CrossRefPubMed Winter K, Cherry JD, Harriman K (2017) Effectiveness of prenatal tetanus, diphtheria, and acellular pertussis vaccination on pertussis severity in infants. Clin Infect Dis 64(1):9–14CrossRefPubMed
50.
go back to reference Ross KM, Miller G, Culhane J, Grobman W, Simhan HN, Wadhwa PD et al (2016) Patterns of peripheral cytokine expression during pregnancy in two cohorts and associations with inflammatory markers in cord blood. Am J Reprod Immunol 76(5):406–414CrossRefPubMed Ross KM, Miller G, Culhane J, Grobman W, Simhan HN, Wadhwa PD et al (2016) Patterns of peripheral cytokine expression during pregnancy in two cohorts and associations with inflammatory markers in cord blood. Am J Reprod Immunol 76(5):406–414CrossRefPubMed
51.
go back to reference Burns C, Hall ST, Smith R, Blackwell C (2015) Cytokine levels in late pregnancy: are female infants better protected against inflammation? Front Immunol 6:318CrossRefPubMedPubMedCentral Burns C, Hall ST, Smith R, Blackwell C (2015) Cytokine levels in late pregnancy: are female infants better protected against inflammation? Front Immunol 6:318CrossRefPubMedPubMedCentral
52.
go back to reference Duncombe G, Veldhuizen RAW, Gratton RJ, Han VKM, Richardson BS (2010) IL-6 and TNFalpha across the umbilical circulation in term pregnancies: relationship with labour events. Early Hum Dev 86(2):113–117CrossRefPubMed Duncombe G, Veldhuizen RAW, Gratton RJ, Han VKM, Richardson BS (2010) IL-6 and TNFalpha across the umbilical circulation in term pregnancies: relationship with labour events. Early Hum Dev 86(2):113–117CrossRefPubMed
53.
go back to reference Beloosesky R, Maravi N, Weiner Z, Khatib N, Awad N, Boles J et al (2010) Maternal lipopolysaccharide-induced inflammation during pregnancy programs impaired offspring innate immune responses. Am J Obstet Gynecol 203(2):185.e1–185.e4CrossRef Beloosesky R, Maravi N, Weiner Z, Khatib N, Awad N, Boles J et al (2010) Maternal lipopolysaccharide-induced inflammation during pregnancy programs impaired offspring innate immune responses. Am J Obstet Gynecol 203(2):185.e1–185.e4CrossRef
54.
go back to reference Aaltonen R, Heikkinen T, Hakala K, Laine K, Alanen A (2005) Transfer of proinflammatory cytokines across term placenta. Obstet Gynecol 106(4):802–807CrossRefPubMed Aaltonen R, Heikkinen T, Hakala K, Laine K, Alanen A (2005) Transfer of proinflammatory cytokines across term placenta. Obstet Gynecol 106(4):802–807CrossRefPubMed
55.
go back to reference Zaretsky MV, Alexander JM, Byrd W, Bawdon RE (2004) Transfer of inflammatory cytokines across the placenta. Obstet Gynecol 103(3):546–550CrossRefPubMed Zaretsky MV, Alexander JM, Byrd W, Bawdon RE (2004) Transfer of inflammatory cytokines across the placenta. Obstet Gynecol 103(3):546–550CrossRefPubMed
56.
go back to reference Dauby N, Goetghebuer T, Kollmann TR, Levy J, Marchant A (2012) Uninfected but not unaffected: chronic maternal infections during pregnancy, fetal immunity, and susceptibility to postnatal infections. Lancet Infect Dis 12(4):330–340CrossRefPubMed Dauby N, Goetghebuer T, Kollmann TR, Levy J, Marchant A (2012) Uninfected but not unaffected: chronic maternal infections during pregnancy, fetal immunity, and susceptibility to postnatal infections. Lancet Infect Dis 12(4):330–340CrossRefPubMed
57.
go back to reference Bunders MJ, van Hamme JL, Jansen MH, Boer K, Kootstra NA, Kuijpers TW (2014) Fetal exposure to HIV-1 alters chemokine receptor expression by CD4+T cells and increases susceptibility to HIV-1. Sci Rep 4:6690CrossRefPubMedPubMedCentral Bunders MJ, van Hamme JL, Jansen MH, Boer K, Kootstra NA, Kuijpers TW (2014) Fetal exposure to HIV-1 alters chemokine receptor expression by CD4+T cells and increases susceptibility to HIV-1. Sci Rep 4:6690CrossRefPubMedPubMedCentral
58.
go back to reference Ruck C, Reikie BA, Marchant A, Kollmann TR, Kakkar F (2016) Linking susceptibility to infectious diseases to immune system abnormalities among HIV-exposed uninfected infants. Front Immunol 7:310CrossRefPubMedPubMedCentral Ruck C, Reikie BA, Marchant A, Kollmann TR, Kakkar F (2016) Linking susceptibility to infectious diseases to immune system abnormalities among HIV-exposed uninfected infants. Front Immunol 7:310CrossRefPubMedPubMedCentral
59.
60.
go back to reference Netea MG, Joosten LAB, Latz E, Mills KHG, Natoli G, Stunnenberg HG et al (2016) Trained immunity: A program of innate immune memory in health and disease. Science 352(6284):aaf1098CrossRefPubMedPubMedCentral Netea MG, Joosten LAB, Latz E, Mills KHG, Natoli G, Stunnenberg HG et al (2016) Trained immunity: A program of innate immune memory in health and disease. Science 352(6284):aaf1098CrossRefPubMedPubMedCentral
61.
go back to reference Levy O, Wynn JL (2014) A prime time for trained immunity: innate immune memory in newborns and infants. Neonatology 105(2):136–141CrossRefPubMed Levy O, Wynn JL (2014) A prime time for trained immunity: innate immune memory in newborns and infants. Neonatology 105(2):136–141CrossRefPubMed
62.
go back to reference Marques AH, O’Connor TG, Roth C, Susser E, Bjørke-Monsen A-L (2013) The influence of maternal prenatal and early childhood nutrition and maternal prenatal stress on offspring immune system development and neurodevelopmental disorders. Front Neurosci 7:120CrossRefPubMedPubMedCentral Marques AH, O’Connor TG, Roth C, Susser E, Bjørke-Monsen A-L (2013) The influence of maternal prenatal and early childhood nutrition and maternal prenatal stress on offspring immune system development and neurodevelopmental disorders. Front Neurosci 7:120CrossRefPubMedPubMedCentral
63.
go back to reference von Mutius E, Martinez FD (2016) Inconclusive results of randomized trials of prenatal vitamin D for asthma prevention in offspring: curbing the enthusiasm. JAMA 315(4):347–348CrossRef von Mutius E, Martinez FD (2016) Inconclusive results of randomized trials of prenatal vitamin D for asthma prevention in offspring: curbing the enthusiasm. JAMA 315(4):347–348CrossRef
64.
go back to reference Dunstan JA, Mori TA, Barden A, Beilin LJ, Taylor AL, Holt PG et al (2003) Maternal fish oil supplementation in pregnancy reduces interleukin-13 levels in cord blood of infants at high risk of atopy. Clin Exp Allergy J Br Soc Allergy Clin Immunol 33(4):442–448CrossRef Dunstan JA, Mori TA, Barden A, Beilin LJ, Taylor AL, Holt PG et al (2003) Maternal fish oil supplementation in pregnancy reduces interleukin-13 levels in cord blood of infants at high risk of atopy. Clin Exp Allergy J Br Soc Allergy Clin Immunol 33(4):442–448CrossRef
65.
go back to reference Prescott SL, Barden AE, Mori TA, Dunstan JA (2007) Maternal fish oil supplementation in pregnancy modifies neonatal leukotriene production by cord-blood-derived neutrophils. Clin Sci Lond Engl 1979 113(10):409–416 Prescott SL, Barden AE, Mori TA, Dunstan JA (2007) Maternal fish oil supplementation in pregnancy modifies neonatal leukotriene production by cord-blood-derived neutrophils. Clin Sci Lond Engl 1979 113(10):409–416
66.
go back to reference von Mutius E (2012) Maternal farm exposure/ingestion of unpasteurized cow’s milk and allergic disease. Curr Opin Gastroenterol 28(6):570–576CrossRef von Mutius E (2012) Maternal farm exposure/ingestion of unpasteurized cow’s milk and allergic disease. Curr Opin Gastroenterol 28(6):570–576CrossRef
67.
go back to reference Loss G, Depner M, Ulfman LH, van Neerven RJJ, Hose AJ, Genuneit J et al (2015) Consumption of unprocessed cow’s milk protects infants from common respiratory infections. J Allergy Clin Immunol 135(1):56–62CrossRefPubMed Loss G, Depner M, Ulfman LH, van Neerven RJJ, Hose AJ, Genuneit J et al (2015) Consumption of unprocessed cow’s milk protects infants from common respiratory infections. J Allergy Clin Immunol 135(1):56–62CrossRefPubMed
68.
go back to reference Schaub B, Liu J, Höppler S, Schleich I, Huehn J, Olek S et al (2009) Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells. J Allergy Clin Immunol 123(4):774–82.e5CrossRefPubMed Schaub B, Liu J, Höppler S, Schleich I, Huehn J, Olek S et al (2009) Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells. J Allergy Clin Immunol 123(4):774–82.e5CrossRefPubMed
69.
go back to reference Kinder JM, Stelzer IA, Arck PC, Way SS (2017) Immunological implications of pregnancy-induced microchimerism. Nat Rev Immunol 17(8):483–494 Kinder JM, Stelzer IA, Arck PC, Way SS (2017) Immunological implications of pregnancy-induced microchimerism. Nat Rev Immunol 17(8):483–494
70.
go back to reference Mold JE, Michaëlsson J, Burt TD, Muench MO, Beckerman KP, Busch MP et al (2008) Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322(5907):1562–1565CrossRefPubMedPubMedCentral Mold JE, Michaëlsson J, Burt TD, Muench MO, Beckerman KP, Busch MP et al (2008) Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322(5907):1562–1565CrossRefPubMedPubMedCentral
71.
go back to reference Kinder JM, Jiang TT, Ertelt JM, Xin L, Strong BS, Shaaban AF et al (2015) Cross-generational reproductive fitness enforced by microchimeric maternal cells. Cell 162(3):505–515CrossRefPubMedPubMedCentral Kinder JM, Jiang TT, Ertelt JM, Xin L, Strong BS, Shaaban AF et al (2015) Cross-generational reproductive fitness enforced by microchimeric maternal cells. Cell 162(3):505–515CrossRefPubMedPubMedCentral
72.
go back to reference Mold JE, Venkatasubrahmanyam S, Burt TD, Michaëlsson J, Rivera JM, Galkina SA et al (2010) Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science 330(6011):1695–1699CrossRefPubMedPubMedCentral Mold JE, Venkatasubrahmanyam S, Burt TD, Michaëlsson J, Rivera JM, Galkina SA et al (2010) Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science 330(6011):1695–1699CrossRefPubMedPubMedCentral
73.
go back to reference McGovern N, Shin A, Low G, Low D, Duan K, Yao LJ et al (2017) Human fetal dendritic cells promote prenatal T-cell immune suppression through arginase-2. Nature 546(7660):662–666CrossRefPubMed McGovern N, Shin A, Low G, Low D, Duan K, Yao LJ et al (2017) Human fetal dendritic cells promote prenatal T-cell immune suppression through arginase-2. Nature 546(7660):662–666CrossRefPubMed
74.
go back to reference Malhotra I, Ouma J, Wamachi A, Kioko J, Mungai P, Omollo A et al (1997) In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults. J Clin Invest 99(7):1759–1766CrossRefPubMedPubMedCentral Malhotra I, Ouma J, Wamachi A, Kioko J, Mungai P, Omollo A et al (1997) In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults. J Clin Invest 99(7):1759–1766CrossRefPubMedPubMedCentral
75.
go back to reference Guadalupe I, Mitre E, Benitez S, Chico ME, Nutman TB, Cooper PJ (2009) Evidence for in utero sensitization to Ascaris Lumbricoides in newborns of mothers with ascariasis. J Infect Dis 199(12):1846–1850CrossRefPubMedPubMedCentral Guadalupe I, Mitre E, Benitez S, Chico ME, Nutman TB, Cooper PJ (2009) Evidence for in utero sensitization to Ascaris Lumbricoides in newborns of mothers with ascariasis. J Infect Dis 199(12):1846–1850CrossRefPubMedPubMedCentral
76.
go back to reference Broen K, Brustoski K, Engelmann I, Luty AJF (2007) Placental plasmodium falciparum infection: causes and consequences of in utero sensitization to parasite antigens. Mol Biochem Parasitol 151(1):1–8CrossRefPubMed Broen K, Brustoski K, Engelmann I, Luty AJF (2007) Placental plasmodium falciparum infection: causes and consequences of in utero sensitization to parasite antigens. Mol Biochem Parasitol 151(1):1–8CrossRefPubMed
77.
go back to reference Tena-Tomás C, Bouyou-Akotet MK, Kendjo E, Kombila M, Kremsner PG, Kun JFJ (2007) Prenatal immune responses to plasmodium falciparum erythrocyte membrane protein 1 DBL-alpha domain in Gabon. Parasitol Res 101(4):1045–1050CrossRefPubMed Tena-Tomás C, Bouyou-Akotet MK, Kendjo E, Kombila M, Kremsner PG, Kun JFJ (2007) Prenatal immune responses to plasmodium falciparum erythrocyte membrane protein 1 DBL-alpha domain in Gabon. Parasitol Res 101(4):1045–1050CrossRefPubMed
78.
go back to reference Zhang X, Mozeleski B, Lemoine S, Dériaud E, Lim A, Zhivaki D et al (2014) CD4 T cells with effector memory phenotype and function develop in the sterile environment of the fetus. Sci Transl Med 6(238):238ra72CrossRefPubMed Zhang X, Mozeleski B, Lemoine S, Dériaud E, Lim A, Zhivaki D et al (2014) CD4 T cells with effector memory phenotype and function develop in the sterile environment of the fetus. Sci Transl Med 6(238):238ra72CrossRefPubMed
79.
go back to reference May K, Grube M, Malhotra I, Long CA, Singh S, Mandaliya K et al (2009) Antibody-dependent transplacental transfer of malaria blood-stage antigen using a human ex vivo placental perfusion model. PLoS One 4(11):e7986CrossRefPubMedPubMedCentral May K, Grube M, Malhotra I, Long CA, Singh S, Mandaliya K et al (2009) Antibody-dependent transplacental transfer of malaria blood-stage antigen using a human ex vivo placental perfusion model. PLoS One 4(11):e7986CrossRefPubMedPubMedCentral
80.
go back to reference Bal MS, Mandal NN, Das MK, Kar SK, Sarangi SS, Beuria MK (2010) Transplacental transfer of filarial antigens from Wuchereria bancrofti-infected mothers to their offspring. Parasitology 137(4):669–673CrossRefPubMed Bal MS, Mandal NN, Das MK, Kar SK, Sarangi SS, Beuria MK (2010) Transplacental transfer of filarial antigens from Wuchereria bancrofti-infected mothers to their offspring. Parasitology 137(4):669–673CrossRefPubMed
81.
go back to reference Gill TJ, Repetti CF, Metlay LA, Rabin BS, Taylor FH, Thompson DS et al (1983) Transplacental immunization of the human fetus to tetanus by immunization of the mother. J Clin Invest 72(3):987–996CrossRefPubMedPubMedCentral Gill TJ, Repetti CF, Metlay LA, Rabin BS, Taylor FH, Thompson DS et al (1983) Transplacental immunization of the human fetus to tetanus by immunization of the mother. J Clin Invest 72(3):987–996CrossRefPubMedPubMedCentral
82.
go back to reference Vanderbeeken Y, Sarfati M, Bose R, Delespesse G (1985) In utero immunization of the fetus to tetanus by maternal vaccination during pregnancy. Am J Reprod Immunol Microbiol AJRIM 8(2):39–42CrossRefPubMed Vanderbeeken Y, Sarfati M, Bose R, Delespesse G (1985) In utero immunization of the fetus to tetanus by maternal vaccination during pregnancy. Am J Reprod Immunol Microbiol AJRIM 8(2):39–42CrossRefPubMed
83.
go back to reference Englund JA, Mbawuike IN, Hammill H, Holleman MC, Baxter BD, Glezen WP (1993) Maternal immunization with influenza or tetanus toxoid vaccine for passive antibody protection in young infants. J Infect Dis 168(3):647–656CrossRefPubMed Englund JA, Mbawuike IN, Hammill H, Holleman MC, Baxter BD, Glezen WP (1993) Maternal immunization with influenza or tetanus toxoid vaccine for passive antibody protection in young infants. J Infect Dis 168(3):647–656CrossRefPubMed
84.
go back to reference Rastogi D, Wang C, Mao X, Lendor C, Rothman PB, Miller RL (2007) Antigen-specific immune responses to influenza vaccine in utero. J Clin Invest 117(6):1637–1646CrossRefPubMedPubMedCentral Rastogi D, Wang C, Mao X, Lendor C, Rothman PB, Miller RL (2007) Antigen-specific immune responses to influenza vaccine in utero. J Clin Invest 117(6):1637–1646CrossRefPubMedPubMedCentral
85.
go back to reference Holloway JA, Warner JO, Vance GH, Diaper ND, Warner JA, Jones CA (2000) Detection of house-dust-mite allergen in amniotic fluid and umbilical-cord blood. Lancet 356(9245):1900–1902CrossRefPubMed Holloway JA, Warner JO, Vance GH, Diaper ND, Warner JA, Jones CA (2000) Detection of house-dust-mite allergen in amniotic fluid and umbilical-cord blood. Lancet 356(9245):1900–1902CrossRefPubMed
86.
go back to reference Devereux G, Barker RN, Seaton A (2002) Antenatal determinants of neonatal immune responses to allergens. Clin Exp Allergy J Br Soc Allergy Clin Immunol 32(1):43–50CrossRef Devereux G, Barker RN, Seaton A (2002) Antenatal determinants of neonatal immune responses to allergens. Clin Exp Allergy J Br Soc Allergy Clin Immunol 32(1):43–50CrossRef
87.
go back to reference Holt PG (2008) Prenatal versus postnatal priming of allergen specific immunologic memory: the debate continues. J Allergy Clin Immunol 122(4):717–718CrossRefPubMed Holt PG (2008) Prenatal versus postnatal priming of allergen specific immunologic memory: the debate continues. J Allergy Clin Immunol 122(4):717–718CrossRefPubMed
88.
go back to reference Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG (2015) The infant microbiome development: mom matters. Trends Mol Med 21(2):109–117CrossRefPubMed Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG (2015) The infant microbiome development: mom matters. Trends Mol Med 21(2):109–117CrossRefPubMed
89.
go back to reference Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK et al (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150(3):470–480CrossRefPubMedPubMedCentral Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK et al (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150(3):470–480CrossRefPubMedPubMedCentral
91.
go back to reference Gomez-Arango LF, Barrett HL, McIntyre HD, Callaway LK, Morrison M, Nitert MD (2017) Contributions of the maternal oral and gut microbiome to placental microbial colonization in overweight and obese pregnant women. Sci Rep 7(1):2860CrossRefPubMedPubMedCentral Gomez-Arango LF, Barrett HL, McIntyre HD, Callaway LK, Morrison M, Nitert MD (2017) Contributions of the maternal oral and gut microbiome to placental microbial colonization in overweight and obese pregnant women. Sci Rep 7(1):2860CrossRefPubMedPubMedCentral
92.
go back to reference Gomez de Agüero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H et al (2016) The maternal microbiota drives early postnatal innate immune development. Science 351(6279):1296–1302CrossRefPubMed Gomez de Agüero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H et al (2016) The maternal microbiota drives early postnatal innate immune development. Science 351(6279):1296–1302CrossRefPubMed
93.
go back to reference Prescott SL, Wickens K, Westcott L, Jung W, Currie H, Black PN et al (2008) Supplementation with lactobacillus rhamnosus or Bifidobacterium lactis probiotics in pregnancy increases cord blood interferon-gamma and breast milk transforming growth factor-beta and immunoglobin a detection. Clin Exp Allergy J 38(10):1606–1614CrossRef Prescott SL, Wickens K, Westcott L, Jung W, Currie H, Black PN et al (2008) Supplementation with lactobacillus rhamnosus or Bifidobacterium lactis probiotics in pregnancy increases cord blood interferon-gamma and breast milk transforming growth factor-beta and immunoglobin a detection. Clin Exp Allergy J 38(10):1606–1614CrossRef
94.
go back to reference Shadid R, Haarman M, Knol J, Theis W, Beermann C, Rjosk-Dendorfer D et al (2007) Effects of galactooligosaccharide and long-chain fructooligosaccharide supplementation during pregnancy on maternal and neonatal microbiota and immunity--a randomized, double-blind, placebo-controlled study. Am J Clin Nutr 86(5):1426–1437PubMed Shadid R, Haarman M, Knol J, Theis W, Beermann C, Rjosk-Dendorfer D et al (2007) Effects of galactooligosaccharide and long-chain fructooligosaccharide supplementation during pregnancy on maternal and neonatal microbiota and immunity--a randomized, double-blind, placebo-controlled study. Am J Clin Nutr 86(5):1426–1437PubMed
Metadata
Title
Transfer of maternal immunity and programming of the newborn immune system
Authors
Madeleine F. Jennewein
Bahaa Abu-Raya
Yiwei Jiang
Galit Alter
Arnaud Marchant
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 6/2017
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-017-0653-x

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