The impact of maternal obesity during pregnancy on offspring immunity

Molecular and Cellular Endocrinology

Volumn 418, Issue , 2015, Pages 134-142

  Wilson, Randall M ^a   Messaoudi, Ilhem ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epigenetics; Immune system; Inflammation; Neonatal; Obesity; Placenta; Pregnancy

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; STAT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CYTOKINE PRODUCTION; EPIGENETICS; GESTATIONAL AGE; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOLOGY; IMMUNOREGULATION; LIPID STORAGE; MACROPHAGE; MATERNAL OBESITY; NONHUMAN; OVERNUTRITION; PLACENTA; POSTNATAL DEVELOPMENT; PREGNANCY; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REGULATORY MECHANISM; UTERUS BLOOD FLOW; ANIMAL; BLOOD; COMPLICATION; FEMALE; GENETIC EPIGENESIS; IMMUNOLOGY; NEWBORN; OBESITY; PREGNANCY COMPLICATION; PRENATAL EXPOSURE;

ANIMALS; EPIGENESIS, GENETIC; FEMALE; HUMANS; INFANT, NEWBORN; OBESITY; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84949624473     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.07.028     Document Type: Article

References (114)

1. Aagaard-Tillery K.M., Grove K., Bishop J., et al. Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J. Mol. Endocrinol. 2008, 41:91-102.
2. Aaltonen R., Heikkinen T., Hakala K., Laine K., Alanen A. Transfer of proinflammatory cytokines across term placenta. Obstet. Gynecol. 2005, 106:802-807.
3. Adkins B., Leclerc C., Marshall-Clarke S. Neonatal adaptive immunity comes of age. Nat. Rev. Immunol. 2004, 4:553-564.
4. Aye I.L., Lager S., Ramirez V.I., et al. Increasing maternal body mass index is associated with systemic inflammation in the mother and the activation of distinct placental inflammatory pathways. Biol. Reprod. 2014, 90:129.
5. Bai L., Feuerer M., Beckhove P., Umansky V., Schirrmacher V. Generation of dendritic cells from human bone marrow mononuclear cells: advantages for clinical application in comparison to peripheral blood monocyte derived cells. Int. J. Oncol. 2002, 20:247-253.
6. Barker D.J. The fetal and infant origins of adult disease. BMJ 1990, 301:1111.
7. Barker D.J. In utero programming of cardiovascular disease. Theriogenology 2000, 53:555-574.
8. Barker D.J., Hales C.N., Fall C.H., Osmond C., Phipps K., Clark P.M. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993, 36:62-67.
9. Barker D.J., Eriksson J.G., Forsen T., Osmond C. Fetal origins of adult disease: strength of effects and biological basis. Int. J. Epidemiol. 2002, 31:1235-1239.
10. Basu S., Haghiac M., Surace P., et al. Pregravid obesity associates with increased maternal endotoxemia and metabolic inflammation. Obesity 2011, 19:476-482.
11. Brandtzaeg P. The mucosal immune system and its integration with the mammary glands. J. Pediatr. 2010, 156:S8-S15.
12. Bremer A.A., Stanhope K.L., Graham J.L., et al. Fructose-fed rhesus monkeys: a nonhuman primate model of insulin resistance, metabolic syndrome, and type 2 diabetes. Clin. Transl. Sci. 2011, 4:243-252.
13. Buro-Auriemma L.J., Salit J., Hackett N.R., et al. Cigarette smoking induces small airway epithelial epigenetic changes with corresponding modulation of gene expression. Hum. Mol. Genet. 2013, 22:4726-4738.
14. Buss C., Entringer S., Davis E.P., et al. Impaired executive function mediates the association between maternal pre-pregnancy body mass index and child ADHD symptoms. PloS One 2012, 7:e37758.
15. Calder P.C., Ahluwalia N., Brouns F., et al. Dietary factors and low-grade inflammation in relation to overweight and obesity. Br. J. Nutr. 2011, 106(Suppl. 3):S5-S78.
16. Calkins K., Devaskar S.U. Fetal origins of adult disease. Curr. Probl. Pediatr. Adolesc. Health Care 2011, 41:158-176.
17. Catalano P.M., Ehrenberg H.M. The short- and long-term implications of maternal obesity on the mother and her offspring. BJOG Int. J. Obstet. Gynaecol. 2006, 113:1126-1133.
18. Centers for Disease C, Prevention Vital signs: state-specific obesity prevalence among adults - United States, 2009. MMWR Morb. Mortal. Wkly. Rep. 2010, 59:951-955.
19. Cetin I., Parisi F., Berti C., Mando C., Desoye G. Placental fatty acid transport in maternal obesity. J. Dev. Orig. Health Dis. 2012, 3:409-414.
20. Challier J.C., Basu S., Bintein T., et al. Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta. Placenta 2008, 29:274-281.
21. Choi S.W., Friso S. Epigenetics: a new bridge between nutrition and health. Adv. Nutr. 2010, 1:8-16.
22. Clements W.K., Kim A.D., Ong K.G., Moore J.C., Lawson N.D., Traver D. A somitic Wnt16/Notch pathway specifies haematopoietic stem cells. Nature 2011, 474:220-224.
23. Cupedo T. Human lymph node development: an inflammatory interaction. Immunol. Lett. 2011, 138:4-6.
24. Dabelea D., Pettitt D.J. Intrauterine diabetic environment confers risks for type 2 diabetes mellitus and obesity in the offspring, in addition to genetic susceptibility. J. Pediatr. Endocrinol. Metab. JPEM 2001, 14:1085-1091.
25. Davies N.P., Buggins A.G., Snijders R.J., Jenkins E., Layton D.M., Nicolaides K.H. Blood leucocyte count in the human fetus. Arch. Dis. Child. 1992, 67:399-403.
26. de Boo H.A., Harding J.E. The developmental origins of adult disease (Barker) hypothesis. Aust. N. Z. J. Obstet. Gynaecol. 2006, 46:4-14.
27. De Kleer I., Willems F., Lambrecht B., Goriely S. Ontogeny of myeloid cells. Front. Immunol. 2014, 5:423.
28. Donath M.Y., Shoelson S.E. Type 2 diabetes as an inflammatory disease. Nat. Rev. Immunol. 2011, 11:98-107.
29. Dover G.J. The Barker hypothesis: how pediatricans will diagnose and prevent common adult-onset diseases. Trans. Am. Clin. Climatol. Assoc. 2009, 120:199-207.
30. Dowling D.J., Levy O. Ontogeny of early life immunity. Trends Immunol. 2014, 35:299-310.
31. Farley D., Tejero M.E., Comuzzie A.G., et al. Feto-placental adaptations to maternal obesity in the baboon. Placenta 2009, 30:752-760.
32. Feinberg A.P., Irizarry R.A., Fradin D., et al. Personalized epigenomic signatures that are stable over time and covary with body mass index. Sci. Transl. Med. 2010, 2. 49ra67.
33. Flegal K.M., Carroll M.D., Kit B.K., Ogden C.L. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA J Am. Med. Assoc. 2012, 307:491-497.
34. Forno E., Young O.M., Kumar R., Simhan H., Celedon J.C. Maternal obesity in pregnancy, gestational weight gain, and risk of childhood asthma. Pediatrics 2014, 134:e535-e546.
35. Forsen T., Eriksson J.G., Tuomilehto J., Teramo K., Osmond C., Barker D.J. Mother's weight in pregnancy and coronary heart disease in a cohort of Finnish men: follow up study. BMJ 1997, 315:837-840.
36. Frias A.E., Morgan T.K., Evans A.E., et al. Maternal high-fat diet disturbs uteroplacental hemodynamics and increases the frequency of stillbirth in a nonhuman primate model of excess nutrition. Endocrinology 2011, 152:2456-2464.
37. Frostegard J. Immunity, atherosclerosis and cardiovascular disease. BMC Med. 2013, 11:117.
38. Fujisaka S., Usui I., Bukhari A., et al. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 2009, 58:2574-2582.
39. Gaillard R., Durmus B., Hofman A., Mackenbach J.P., Steegers E.A., Jaddoe V.W. Risk factors and outcomes of maternal obesity and excessive weight gain during pregnancy. Obesity 2013, 21:1046-1055.
40. Gaillard R., Steegers E.A., Duijts L., et al. Childhood cardiometabolic outcomes of maternal obesity during pregnancy: the generation R Study. Hypertension 2014, 63:683-691.
41. Galley J.D., Bailey M., Kamp Dush C., Schoppe-Sullivan S., Christian L.M. Maternal obesity is associated with alterations in the gut microbiome in toddlers. PloS One 2014, 9:e113026.
42. Ginhoux F., Jung S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 2014, 14:392-404.
43. Go A.S., Mozaffarian D., Roger V.L., et al. Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 2013, 127:e6-e245.
44. Godfrey K.M., Sheppard A., Gluckman P.D., et al. Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes 2011, 60:1528-1534.
45. Greer E.L., Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat. Rev. Genet. 2012, 13:343-357.
46. Gregor M.F., Hotamisligil G.S. Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 2011, 29:415-445.
47. Grover S.A., Kaouache M., Rempel P., et al. Years of life lost and healthy life-years lost from diabetes and cardiovascular disease in overweight and obese people: a modelling study. Lancet Diabetes Endocrinol. 2015, 3:114-122.
48. Hales C.N., Barker D.J. The thrifty phenotype hypothesis. Br. Med. Bull. 2001, 60:5-20.
49. Hansson G.K., Hermansson A. The immune system in atherosclerosis. Nat. Immunol. 2011, 12:204-212.
50. Hansson G.K., Libby P. The immune response in atherosclerosis: a double-edged sword. Nat. Rev. Immunol. 2006, 6:508-519.
51. Hansson G.K., Libby P., Schonbeck U., Yan Z.Q. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circulation Res. 2002, 91:281-291.
52. Harpsoe M.C., Basit S., Bager P., et al. Maternal obesity, gestational weight gain, and risk of asthma and atopic disease in offspring: a study within the Danish National Birth Cohort. J. Allergy Clin. Immunol. 2013, 131:1033-1040.
53. Hayward A.R. The human fetus and newborn: development of the immune response. Birth Defects Orig. Artic. Ser. 1983, 19:289-294.
54. Hein W.R., Griebel P.J. A road less travelled: large animal models in immunological research. Nat. Rev. Immunol. 2003, 3:79-84.
55. Herbstman J.B., Wang S., Perera F.P., et al. Predictors and consequences of global DNA methylation in cord blood and at three years. PloS One 2013, 8:e72824.
56. Holgate S.T. Pathogenesis of asthma. Clin. Exp. Allergy J. Br. Soc. Allergy Clin. Immunol. 2008, 38:872-897.
57. Holliday R. DNA methylation and epigenetic inheritance. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 1990, 326:329-338.
58. Holt P.G., Jones C.A. The development of the immune system during pregnancy and early life. Allergy 2000, 55:688-697.
59. Homer R.J., Elias J.A. Airway remodeling in asthma: therapeutic implications of mechanisms. Physiology 2005, 20:28-35.
60. Johnson C.L., Versalovic J. The human microbiome and its potential importance to pediatrics. Pediatrics 2012, 129:950-960.
61. Kanda H., Tateya S., Tamori Y., et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J. Clin. Invest. 2006, 116:1494-1505.
62. Kips J.C. Cytokines in asthma. Eur. Respir. J. Suppl. 2001, 34:24s-33s.
63. Kollmann T.R., Levy O., Montgomery R.R., Goriely S. Innate immune function by Toll-like receptors: distinct responses in newborns and the elderly. Immunity 2012, 37:771-783.
64. Kon O.M., Kay A.B. T cells and chronic asthma. Int. Arch. Allergy Immunol. 1999, 118:133-135.
65. Kondilis-Mangum H.D., Wade P.A. Epigenetics and the adaptive immune response. Mol. Asp. Med. 2013, 34:813-825.
66. Kumar R., Story R.E., Pongracic J.A., et al. Maternal pre-pregnancy obesity and recurrent wheezing in early childhood. Pediatr. Allergy Immunol. Pulmonol. 2010, 23:183-190.
67. Lavebratt C., Almgren M., Ekstrom T.J. Epigenetic regulation in obesity. Int. J. Obes. 2012, 36:757-765.
68. Lawlor D.A., Smith G.D., O'Callaghan M., et al. Epidemiologic evidence for the fetal overnutrition hypothesis: findings from the mater-university study of pregnancy and its outcomes. Am. J. Epidemiol. 2007, 165:418-424.
69. Leddy M.A., Power M.L., Schulkin J. The impact of maternal obesity on maternal and fetal health. Rev. Obstet. Gynecol. 2008, 1:170-178.
70. Leibowitz K.L., Moore R.H., Ahima R.S., et al. Maternal obesity associated with inflammation in their children. World J. Pediatr. 2012, 8:76-79.
71. Leung T.Y., Leung T.N., Sahota D.S., et al. Trends in maternal obesity and associated risks of adverse pregnancy outcomes in a population of Chinese women. BJOG Int. J. Obstet. Gynaecol. 2008, 115:1529-1537.
72. Levy O. Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat. Rev. Immunol. 2007, 7:379-390.
73. Liu X., Chen Q., Tsai H.J., et al. Maternal preconception body mass index and offspring cord blood DNA methylation: exploration of early life origins of disease. Environ. Mol. Mutagen. 2014, 55:223-230.
74. Lloyd C.M., Hessel E.M. Functions of T cells in asthma: more than just T(H)2 cells. Nat. Rev. Immunol. 2010, 10:838-848.
75. McMahon D.M., Liu J., Zhang H., Torres M.E., Best R.G. Maternal obesity, folate intake, and neural tube defects in offspring. Birth Defects Res. Part A Clin. Mol. Teratol. 2013, 97:115-122.
76. Messal N., Mamessier E., Sylvain A., et al. Differential role for CD277 as a co-regulator of the immune signal in T and NK cells. Eur. J. Immunol. 2011, 41:3443-3454.
77. Mor G., Cardenas I. The immune system in pregnancy: a unique complexity. Am. J. Reprod. Immunol. 2010, 63:425-433.
78. Morgan A.R., Thompson J.M., Murphy R., et al. Obesity and diabetes genes are associated with being born small for gestational age: results from the Auckland Birthweight Collaborative study. BMC Med. Genet. 2010, 11:125.
79. Murphy K., Travers P., Walport M., Janeway C. Janeway's Immunobiology 2012, Garland Science, New York. eighth ed.
80. Myles I.A., Fontecilla N.M., Janelsins B.M., Vithayathil P.J., Segre J.A., Datta S.K. Parental dietary fat intake alters offspring microbiome and immunity. J. Immunol. 2013, 191:3200-3209.
81. Naito M., Takahashi K., Nishikawa S. Development, differentiation, and maturation of macrophages in the fetal mouse liver. J. Leukoc. Biol. 1990, 48:27-37.
82. Nishimura S., Manabe I., Nagasaki M., et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 2009, 15:914-920.
83. O'Reilly J.R., Reynolds R.M. The risk of maternal obesity to the long-term health of the offspring. Clin. Endocrinol. 2013, 78:9-16.
84. Odaka Y., Nakano M., Tanaka T., et al. The influence of a high-fat dietary environment in the fetal period on postnatal metabolic and immune function. Obesity 2010, 18:1688-1694.
85. Packer L., Sies H. Oxidative Stress and Inflammatory Mechanisms in Obesity, Diabetes, and the Metabolic Syndrome 2008, CRC Press, Boca Raton.
86. Parkin J., Cohen B. An overview of the immune system. Lancet 2001, 357:1777-1789.
87. Reynolds R.M., Allan K.M., Raja E.A., et al. Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. BMJ 2013, 347:f4539.
88. Roifman I.D.C.M. Immunity of the newborn. UpToDate 2015, UpToDate, Waltham, MA. D.S. Basow (Ed.).
89. Rose C.M., van den Driesche S., Meehan R.R., Drake A.J. Epigenetic reprogramming: preparing the epigenome for the next generation. Biochem. Soc. Trans. 2013, 41:809-814.
90. Saben J., Lindsey F., Zhong Y., et al. Maternal obesity is associated with a lipotoxic placental environment. Placenta 2014, 35:171-177.
91. Sacks G.P., Seyani L., Lavery S., Trew G. Maternal C-reactive protein levels are raised at 4 weeks gestation. Hum. Reprod. 2004, 19:1025-1030.
92. Salam M.T., Byun H.M., Lurmann F., et al. Genetic and epigenetic variations in inducible nitric oxide synthase promoter, particulate pollution, and exhaled nitric oxide levels in children. J. Allergy Clin. Immunol. 2012, 129. 232-9 e1-7.
93. Sautois B., Fillet G., Beguin Y. Comparative cytokine production by in vitro stimulated mononucleated cells from cord blood and adult blood. Exp. Hematol. 1997, 25:103-108.
94. Schmatz M., Madan J., Marino T., Davis J. Maternal obesity: the interplay between inflammation, mother and fetus. J. Perinatol. Off. J. Calif. Perinat. Assoc. 2010, 30:441-446.
95. Scott-Pillai R., Spence D., Cardwell C.R., Hunter A., Holmes V.A. The impact of body mass index on maternal and neonatal outcomes: a retrospective study in a UK obstetric population, 2004-2011. BJOG Int. J. Obstet. Gynaecol. 2013, 120:932-939.
96. Segula D. Complications of obesity in adults: a short review of the literature. Malawi Med. J. J. Med. Assoc. Malawi 2014, 26:20-24.
97. Shu C.J., Benoist C., Mathis D. The immune system's involvement in obesity-driven type 2 diabetes. Semin. Immunol. 2012, 24:436-442.
98. Silver M.J., Kessler N.J., Hennig B.J., et al. Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment. Genome Biol. 2015, 16:118.
99. Stephensen C.B., Rasooly R., Jiang X., et al. Vitamin A enhances in vitro Th2 development via retinoid X receptor pathway. J. Immunol. 2002, 168:4495-4503.
100. Stewart F.M., Freeman D.J., Ramsay J.E., Greer I.A., Caslake M., Ferrell W.R. Longitudinal assessment of maternal endothelial function and markers of inflammation and placental function throughout pregnancy in lean and obese mothers. J. Clin. Endocrinol. Metab. 2007, 92:969-975.
101. Swanson L.D., Bewtra C. Increase in normal placental weights related to increase in maternal body mass index. J. Matern. Fetal Neonatal Med. Off. J. Eur. Assoc. Perinat. Med. Fed. Asia Ocean Perinat. Soc. Int. Soc. Perinat. Obstet. 2008, 21:111-113.
102. Tavian M., Biasch K., Sinka L., Vallet J., Peault B. Embryonic origin of human hematopoiesis. Int. J. Dev. Biol. 2010, 54:1061-1065.
103. Vaag A.A., Grunnet L.G., Arora G.P., Brons C. The thrifty phenotype hypothesis revisited. Diabetologia 2012, 55:2085-2088.
104. Wang Y., van Boxel-Dezaire A.H., Cheon H., Yang J., Stark G.R. STAT3 activation in response to IL-6 is prolonged by the binding of IL-6 receptor to EGF receptor. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:16975-16980.
105. Wellen K.E., Hotamisligil G.S. Inflammation, stress, and diabetes. J. Clin. Invest. 2005, 115:1111-1119.
106. Wilson R.M., Marshall N.E., Jeske D.R., Purnell J.Q., Thornburg K., Messaoudi I. Maternal obesity alters immune cell frequencies and responses in umbilical cord blood samples. Pediatr. Allergy Immunol. Off. Publ. Eur. Soc. Pediatr. Allergy Immunol. 2015, 26:344-351.
107. Winer S., Chan Y., Paltser G., et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat. Med. 2009, 15:921-929.
108. Wink D.A., Hines H.B., Cheng R.Y., et al. Nitric oxide and redox mechanisms in the immune response. J. Leukoc. Biol. 2011, 89:873-891.
109. Wong A.H., Gottesman, Petronis A. Phenotypic differences in genetically identical organisms: the epigenetic perspective. Hum. Mol. Genet. 2005, 14(Spec No 1):R11-R18.
110. Ygberg S., Nilsson A. The developing immune system - from foetus to toddler. Acta Paediatr. 2012, 101:120-127.
111. Zaretsky M.V., Alexander J.M., Byrd W., Bawdon R.E. Transfer of inflammatory cytokines across the placenta. Obstet. Gynecol. 2004, 103:546-550.
112. Zauberman A., Zipori D., Krupsky M., Ben-Levy R. Stress activated protein kinase p38 is involved in IL-6 induced transcriptional activation of STAT3. Oncogene 1999, 18:3886-3893.
113. Zhu J., Yamane H., Paul W.E. Differentiation of effector CD4 T cell populations (*). Annu. Rev. Immunol. 2010, 28:445-489.
114. Zhu M.J., Du M., Nathanielsz P.W., Ford S.P. Maternal obesity up-regulates inflammatory signaling pathways and enhances cytokine expression in the mid-gestation sheep placenta. Placenta 2010, 31:387-391.