Inflammation, obesity, and neuromodulation in pregnancy and fetal development

Advances in Neuroimmune Biology

Volumn 1, Issue 2, 2011, Pages 193-203

  Thornton, C A ^a   Jones, R H ^a   Doekhie, A ^a   Bryant, A H ^a   Beynon, A L ^a   Davies, J S ^a  

^a SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

fetus; inflammation; neurodevelopment; obesity; Pregnancy

Indexed keywords

CYTOKINE; INDOLEAMINE 2,3 DIOXYGENASE;

ARTICLE; CARDIOVASCULAR SYSTEM; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM FUNCTION; CYTOKINE RELEASE; DENDRITIC CELL; ENERGY BALANCE; ENVIRONMENTAL IMPACT; FAT INTAKE; FETUS CELL; FETUS DEVELOPMENT; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; LIVER DEVELOPMENT; MACROPHAGE; MATERNAL OBESITY; METABOLIC REGULATION; NEUROMODULATION; NONHUMAN; OBESITY; PANCREAS; PERIPHERAL NERVOUS SYSTEM; PREGNANCY DISORDER; PREGNANCY OUTCOME; PREGNANT WOMAN; PRIORITY JOURNAL; PROGENY; TISSUE STRUCTURE;

EID: 84860174150     PISSN: 1878948X     EISSN: 18789498     Source Type: Journal    
DOI: 10.3233/NIB-2011-015     Document Type: Article

References (115)

1. Sargent IL, Borzychowski AM, Redman CW. NK cells and human pregnancy-an inflammatory view. Trends Immunol. 2006; 27(9): 399-404. (Pubitemid 44216188)
2. Thornton CA. Immunology of pregnancy. Proc Nutr Soc. 2010; 69(3): 357-365.
3. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol. 1993; 151(9): 4562-4573. (Pubitemid 23318510)
4. Piccinni MP, Scaletti C, Maggi E, Romagnani S. Role of hormone-controlled Th1-and Th2-type cytokines in successful pregnancy. J Neuroimmunol. 2000; 109(1): 30-33.
5. Wegmann TG, Lin H, Guilbert L, Mosmann TR. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol Today. 1993; 14(7): 353-356. (Pubitemid 23198169)
6. Ashkar AA, Di Santo JP, Croy BA. Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J Exp Med. 2000; 192(2): 259-270.
7. Borzychowski AM, Croy BA, Chan WL, Redman CW, Sargent IL. Changes in systemic type 1 and type 2 immunity in normal pregnancy and pre-eclampsia may be mediated by natural killer cells. Eur J Immunol. 2005; 35(10): 3054-3063. (Pubitemid 41555101)
8. Jones CA, Finlay-Jones JJ, Hart PH. Type-1 and type-2 cytokines in human late-gestation decidual tissue. Biol Reprod. 1997; 57(2): 303-311. (Pubitemid 27343688)
9. Shevach EM. From Vanilla to 28 Flavors: Multiple Varieties of T regulatory cells. Immunity. 2006; 25(2): 195-201. (Pubitemid 44224153)
10. Seddiki N, Santner-Nanan B, Martinson J, Zaunders J, Sas-son S, Landay A, et al. Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J Exp Med. 2006; 203(7): 1693-1700. (Pubitemid 44036275)
11. Fontenot JD, Rudensky AY. A well adapted regulatory contrivance: Regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol. 2005; 6(4): 331-337. (Pubitemid 41716769)
12. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol. 2004; 5(3): 266-271. (Pubitemid 38332123)
13. Darasse-Jèze G, Klatzmann D, Charlotte F, Salomon BL, Cohen JL. CD4+ CD25+ regulatory/suppressor T cells prevent allogeneic fetus rejection in mice. Immunology Letters. 2006; 102(1): 106-109. (Pubitemid 41606047)
14. Heikkinen J, Mottonen M, Alanen A, Lassila O. Phenotypic characterization of regulatory T cells in the human decidua. Clin Exp Immunol. 2004; 136(2): 373-378. (Pubitemid 38543459)
15. Mjosberg J, Svensson J, Johansson E, Hellstrom L, Casas R, Jenmalm MC, et al. Systemic reduction of functionally suppressive CD4dim CD25high Foxp3+ Tregs in human second trimester pregnancy is induced by progesterone and 17beta-estradiol. J Immunol. 2009; 183(1): 759-769.
16. Sasaki Y, Sakai M, Miyazaki S, Higuma S, Shiozaki A, Saito S. Decidual and peripheral blood CD4+ CD25+ regulatory T cellsin early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod. 2004; 10(5): 347-353. (Pubitemid 38714366)
17. Lin Y, Liang Z, Chen Y, Zeng Y. TLR3-involved modulation of pregnancy tolerance in double-stranded RNA-stimulated NOD/SCID mice. J Immunol. 2006; 176(7): 4147-4154. (Pubitemid 44264394)
18. Tai P, Wang J, Jin H, Song X, Yan J, Kang Y, et al. Induction of regulatory T cells by physiological level estrogen. J Cell Physiol. 2008; 214(2): 456-464. (Pubitemid 350309002)
19. Nakashima A, Ito M, Yoneda S, Shiozaki A, Hidaka T, Saito S. Circulating and decidual Th17 cell levels in healthy pregnancy. Am J Reprod Immunol. 2010; 63(2): 104-109.
20. Toldi G, Rigó J, Stenczer B, Vásárhelyi B, Molvarec A. Increased prevalence of IL-17-producing peripheral blood lymphocytes in pre-eclampsia. Am J Reprod Immunol. 2011; 66(3): 223-229.
21. Wang W-J, Hao C-F, Yi L, Yin G-J, Bao S-H, Qiu L-H, et al. Increased prevalence of T helper 17 (Th17) cells in peripheral blood and deciduainunexplained recurrent spontaneous abortion patients. J Reprod Immunol. 2010; 84(2): 164-170.
22. Wang W-J, Hao C-F, Qu Q-L, Wang X, Qiu L-H, Lin Q-D. The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Hum Reprod. 2010; 25(10): 2591-2596.
23. Shigeru S, Akitoshi N, Subaru M-H, Shiozaki A. The balance between cytotoxic NK cells and regulatory NK cells in human pregnancy. J Reprod Immunol. 2008; 77(1): 14-22.
24. Williams PJ, Searle RF, Robson SC, Innes BA, Bulmer JN. Decidual leucocyte populations in early to late gestation normal human pregnancy. J Reprod Immunol. 2009; 82(1): 24-31.
25. Heikkinen J, Mottonen M, Komi J, Alanen A, Las-sila O. Phenotypic characterization of human decidual macrophages. Clin Exp Immunol. 2003; 131(3): 498-505. (Pubitemid 36324142)
26. Repnik U, Tilburgs T, Roelen DL, van der Mast BJ, Kanhai HH, Scherjon S, et al. Comparison of macrophage pheno-type between decidua basalis and decidua parietalis by flow cytometry. Placenta. 2008; 29(5): 405-412.
27. Gustafsson C, Mjösberg J, Matussek A, Geffers R, Matthiesen L, Berg Gr, et al. Gene expression profiling of human decidual macrophages: Evidence for immunosup-pressive phenotype. PLoS One. 2008; 3(4): e2078.
28. Denison FC, Kelly RW, Calder AA, Riley SC. Cytokine secretion by human fetal membranes, decidua and placenta at term. Hum Reprod. 1998; 13(12): 3560-3565. (Pubitemid 29002658)
29. Gordon S. Alternative activation of macrophages. Nat Rev Immunol. 2003; 3(1): 23-35. (Pubitemid 37328697)
30. Ban YL, Kong BH, Qu X, Yang QF, Ma YY. BDCA-1+, BDCA-2+ and BDCA-3+ dendritic cells in early human pregnancy decidua. Clin Exp Immunol. 2008; 151(3): 399-406. (Pubitemid 351160726)
31. Gardner L, Moffett A. Dendritic cells in the human decidua. Biol Reprod. 2003; 69(4): 1438-1446. (Pubitemid 37173883)
32. Kammerer U, Schoppet M, McLellan AD, Kapp M, Hup-pertz HI, Kampgen E, et al. Human decidua contains potent immunostimulatory CD83(+) dendritic cells. Am J Pathol. 2000; 157(1): 159-169. (Pubitemid 30641733)
33. Miwa N, Hayakawa S, Miyazaki S, Myojo S, Sasaki Y, Sakai M, et al. IDO expression on decidual and peripheral blood dendritic cells and monocytes/macrophages after treatment with CTLA-4 or interferon-gamma increase in normal pregnancy but decrease in spontaneous abortion. Mol Hum Reprod. 2005; 11(12): 865-870.
34. Miyazaki S, Tsuda H, Sakai M, Hori S, Sasaki Y, Futatani T, et al. Predominance of Th2-promoting dendritic cells in early human pregnancy decidua. JLeukoc Biol. 2003; 74(4): 514-522. (Pubitemid 38040378)
35. Collins MK, Tay CS, Erlebacher A. Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. J Clin Invest. 2009; 119(7): 2062-2073.
36. Chakraborty R, Pulendran B. Restraining order for dendritic cells: all quiet on the fetal front. J Clin Invest. 2009; 119(7): 1854-1857.
37. Curti A, Trabanelli S, Salvestrini V, Baccarani M, Lemoli RM. The role of indoleamine 2, 3-dioxygenase in the induction of immune tolerance: Focus on hematology. Blood. 2009; 113(11): 2394-2401.
38. Terness P, Kallikourdis M, Betz AG, Rabinovich GA, Saito S, Clark DA. Tolerance signaling molecules and pregnancy: IDO, galectins, and the renaissance of regulatory T cells. Am J Reprod Immunol. 2007; 58(3): 238-254. (Pubitemid 47249063)
39. von Bubnoff D, Hanau D, Wenzel J, Takikawa O, Hall B, Koch S, et al. Indoleamine 2, 3-dioxygenase-expressing antigen-presenting cells and peripheral T-cell tolerance: Another piece to the atopic puzzle? J Allergy Clin Immunol. 2003; 112(5): 854-860. (Pubitemid 37412051)
40. Mellor AL, Sivakumar J, Chandler P, Smith K, Molina H, Mao D, et al. Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat Immunol. 2001; 2(1): 64-68. (Pubitemid 33704955)
41. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science. 1998; 281(5380): 1191-1193. (Pubitemid 28406294)
42. Bonney EA, Matzinger P. Much IDO about pregnancy. Nat Med. 1998; 4(10): 1128-1129. (Pubitemid 28468824)
43. Vacca P, Cantoni C, Vitale M, Prato C, Canegallo F, Fenoglio D, et al. Crosstalk between decidual NK and CD14+ myelomonocytic cells results in induction of Tregs and immunosuppression. PNAS. 2010; 107(26): 11918-11923.
44. Kvirkvelia N, Vojnovic I, Warner TD, Athie-Morales V, Free P, Rayment N, et al. Placentally derived prostaglandin E2 acts via the EP4 receptor to inhibit IL-2-dependent proliferation of CTLL-2 T cells. Clin Exp Immunol. 2002; 127(2): 263-269. (Pubitemid 34233931)
45. Jones RL, Stoikos C, Findlay JK, Salamonsen LA. TGF-I2; superfamily expression and actions in the endometrium and placenta. Reproduction. 2006; 132(2): 217-232. (Pubitemid 44269704)
46. Croy BA, Chantakru S, Esadeg S, Ashkar AA, Wei Q. Decidual natural killer cells: Key regulators of placental development (a review). J Reprod Immunol. 2002; 57(1-2): 151-168. (Pubitemid 35245746)
47. Patni S, Wynen LP, Seager AL, Morgan G, White JO, Thornton CA. Expression and activity of Toll-like receptors 1-9 in the human term placenta and changes associated with labor at term. Biol Reprod. 2009; 80(2): 243-248.
48. Germain SJ, Sacks GP, Sooranna SR, Sargent IL, Redman CW. Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syn-cytiotrophoblast microparticles. J Immunol. 2007; 178(9): 5949-5956. (Pubitemid 46674392)
49. Horne AW, Stock SJ, King AE. Innate immunity and disorders of the female reproductive tract. Reproduction. 2008; 135(6): 739-749. (Pubitemid 351837387)
50. Miller EM. Changes in serum immunity during pregnancy. Am J Hum Biol. 2009; 21(3): 401-403.
51. Power LL, Popplewell EJ, Holloway JA, Diaper ND, Warner JO, Jones CA. Immunoregulatory molecules during pregnancy andat birth. JReprod Immunol. 2002; 56(1-2): 19-28. (Pubitemid 34754353)
52. Zhao J, Lei Z, Liu Y, Li B, Zhang L, Fang H, et al. Human pregnancy up-regulates Tim-3 in innate immune cells for systemic immunity. J Immunol. 2009; 182(10): 6618-6624.
53. Redman CW, Sargent IL. Circulating microparticles in normal pregnancy and pre-eclampsia. Placenta. 2008; 29(Suppl A): S73-S77.
54. Huda SS, Brodie LE, Sattar N. Obesity in pregnancy: prevalence and metabolic consequences. Semin Fetal Neonatal Med. 2010; 15(2): 70-76.
55. Ramsay JE, Ferrell WR, Crawford L, Wallace AM, Greer IA, Sattar N. Maternal obesity is associated with dysregulation of metabolic, vascular, and inflammatory pathways. J Clin Endocrinol Metab. 2002; 87(9): 4231-4237.
56. Stewart FM, Freeman DJ, Ramsay JE, Greer IA, Caslake M, Ferrell WR. Longitudinal assessment of maternal endothelial function and markers of inflammation and pla-cental function throughout pregnancy in lean and obese mothers. J Clin Endocrinol Metab. 2007; 92(3): 969-975. (Pubitemid 46465671)
57. Denison FC, Roberts KA, Barr SM, Norman JE. Obesity, pregnancy, inflammation and vascular function. Reproduction. 2010; 140(3): 373-385.
58. Frias AE, Morgan TK, Evans AE, Rasanen J, Oh KY, Thornburg KL, 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(6): 2456-2464.
59. Basu S, Haghiac M, Surace P, Challier J-C, Guerre-Millo M, Singh K, et al. Pregravid obesity associates with increased maternal endotoxemia and metabolic inflammation. Obesity. 2011; 19(3): 476-82.
60. Catalano PM, Presley L, Minium J, Hauguel-de Mouzon S. Fetuses of obese mothers develop insulin resistance inutero. Diabetes Care. 2009; 32(6): 1076-1080.
61. Radaelli T, Uvena-Celebrezze J, Minium J, Huston-Presley L, Catalano P, Hauguel-de Mouzon S. Maternal interleukin-6: marker of fetal growth and adiposity. J Soc Gynecol Investig. 2006; 13(1): 53-57. (Pubitemid 43003567)
62. Samuelsson A-M, Ohrn I, Dahlgren J, Eriksson E, Angelin B, Folkow Br, et al. Prenatal exposure to interleukin-6 results in hypertension and increased hypotha-lamic-pituitary-adrenal axis activity in adult rats. Endocrinology. 2004; 145(11): 4897-4911. (Pubitemid 39551106)
63. Nilsson C, Larsson BM, Jennische E, Eriksson E, Bjorntorp P, York DA, et al. Maternal endotoxemia results in obesity and insulin resistance in adult male offspring. Endocrinology. 2001; 142(6): 2622-2630. (Pubitemid 32473119)
64. Challier JC, Basu S, Bintein T, Minium J, Hotmire K, Cata-lano PM, et al. Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta. Placenta. 2008; 29(3): 274-281.
65. Farley D, Tejero ME, Comuzzie AG, Higgins PB, Cox L, Werner SL, et al. Feto-placental adaptations to maternal obesity in the baboon. Placenta. 2009; 30(9): 752-760.
66. Thornton CA, Macfarlane TV, Holt PG. The hygiene hypothesis revisited: Role of materno-fetal interactions. Curr Allergy Asthma Rep. 2010; 10(6): 444-452.
67. Roberts KA, Riley SC, Reynolds RM, Barr S, Evans M, Statham A, et al. Placental structure and inflammation in pregnancies associated with obesity. Placenta. 2011; 32(3): 247-254.
68. Farley DM, Choi J, Dudley DJ, Li C, Jenkins SL, Myatt L, et al. Placental amino acid transport and placental leptin resistance in pregnancies complicated by maternal obesity. Placenta. 2010; 31(8): 718-724.
69. Zhu MJ, Du M, Nathanielsz PW, Ford SP. Maternal obesity up-regulates inflammatory signaling pathways and enhances cytokine expression in the mid-gestation sheep placenta. Placenta. 2010; 31(5): 387-391.
70. Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol. 2005; 115(5): 911-919.
71. Date Y, Kojima M, Hosoda H, Sawaguchi A, Mondal MS, Suganuma T, et al. Ghrelin, a novel growth hormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans. Endocrinology. 2000; 141(11): 4255-4261.
72. Davies JS, Kotokorpi P, Eccles SR, Barnes SK, Tokarczuk PF, Allen SK, et al. Ghrelin induces abdominal obesity via GHS-R-dependent lipid retention. Mol Endocrinol. 2009; 23(6): 914-924.
73. Lappas M, Yee K, Permezel M, Rice GE. Release and regulation of leptin, resistin and adiponectin from human placenta, fetal membranes, and maternal adipose tissue and skeletal muscle from normal and gestational diabetes mellitus-complicated pregnancies. J Endocrinol. 2005; 186(3): 457-465. (Pubitemid 41404064)
74. Morgan SA, Bringolf JB, Seidel ER. Visfatin expression is elevated in normal human pregnancy. Peptides. 2008; 29(8): 1382-1389.
75. Gualillo O, Caminos J, Blanco M, Garcia-Caballero T, Kojima M, Kangawa K, et al. Ghrelin, a novel placental-derived hormone. Endocrinology. 2001; 142(2): 788-794. (Pubitemid 32222428)
76. Kusanovic JP, Romero R, Mazaki-Tovi S, Chaiworapongsa T, Mittal P, Gotsch F, et al. Resistin in amniotic fluid and its association with intra-amniotic infection and inflammation. J Matern Fetal Neonatal Med. 2008; 21(12): 902-916.
77. Mueckler M, Caruso C, Baldwin SA, Panico M, Blench I, Morris HR, et al. Sequence and structure of a human glucose transporter. Science. 1985; 229(4717): 941-945. (Pubitemid 16248486)
78. Pan W, Cornelissen G, Halberg F, Kastin AJ. Selected contribution: Circadian rhythm of tumor necrosis factor-alpha uptake into mouse spinal cord. J Appl Physiol. 2002; 92(3): 1357-1362. (Pubitemid 34671000)
79. Hsuchou H, Kastin AJ, Wu X, Tu H, Pan W. Corticotropin-releasing hormone receptor-1 in cerebral microvessels changes during development and influences urocortin transport across the blood-brain barrier. Endocrinology. 2010; 151(3): 1221-1227.
80. Dziegielewska KM, Hinds LA, Mølǵard K, Reynolds ML, Saunders NR. Blood-brain, blood-cerebrospinal fluid and cerebrospinal fluid-brain barriers in a marsupial (Macropus eugenii) during development. J Physiol. 1988; 403(1): 367-388.
81. Moos T, Møllǵard K. Cerebrovascular permeability to azo dyes and plasma proteins in rodents of different ages. Neu-ropathol Appl Neurobiol. 1993; 19(2): 120-127. (Pubitemid 23136220)
82. Banks WA. Gut-brain communications: Not the same at all ages. Endocrinology. 2010; 151(3): 852-854.
83. Ek M, Arias C, Sawchenko P, Ericsson-Dahlstrand A. Distribution of the EP3 prostaglandin E2 receptor subtype in the rat brain: Relationship to sites of interleukin-1-induced cellular responsiveness. J Comp Neurol. 2000; 428(1): 5-20.
84. Theander-Carrillo C, Wiedmer P, Cettour-Rose P, Nogueiras R, Perez-Tilve D, Pfluger P, et al. Ghrelin action in the brain controls adipocyte metabolism. J Clin Invest. 2006; 116(7): 1983-1993. (Pubitemid 44033322)
85. Scherer T, O'Hare J, Diggs-Andrews K, Schweiger M, Cheng B, Lindtner C, et al. Brain insulin controls adipose tissue lipolysis and lipogenesis. Cell Metabolism. 2011; 13(2): 183-194.
86. Dixit VD, Schaffer EM, Pyle RS, Collins GD, Sakthivel SK, Palaniappan R, et al. Ghrelin inhibits leptin-and activation-induced proinflammatory cytokine expression by human monocytes and T cells. J Clin Invest. 2004; 114(1): 57-66. (Pubitemid 39071644)
87. Date Y, Shimbara T, Koda S, Toshinai K, Ida T, Murakami N, et al. Peripheral ghrelin transmits orexigenic signals through the noradrenergic pathway from the hindbrain to the hypothalamus. Cell Metabolism. 2006; 4(4): 323-331. (Pubitemid 44430917)
88. Moraes JC, Coope A, Morari J, Cintra DE, Roman EA, Pauli JR, et al. High-fat diet induces apoptosis of hypothalamic neurons. PLoS One. 2009; 4(4): e5045.
89. Lindqvist A, Mohapel P, Bouter B, Frielingsdorf H, Pizzo D, Brundin P, et al. High-fat diet impairs hippocampal neu-rogenesis in male rats. Eur J Neurol. 2006; 13(12): 1385-1388. (Pubitemid 44736653)
90. Adams MM, Shi L, Linville MC, Forbes ME, Long AB, Bennett C, et al. Caloric restriction and age affect synaptic proteins in hippocampal CA3 and spatial learning ability. Exp Neurol. 2008; 211(1): 141-149.
91. Fontán-Lozano A, Sáez-Cassanelli JL, Inda MC, de los Santos-Arteaga M, Sierra-Dominguez SA, López-Lluch G, et al. Caloric restriction increases learning consolidation and facilitates synaptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor. J Neurosci. 2007; 27(38): 10185-10195. (Pubitemid 47450454)
92. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, et al. Increasing adult hippocampal neuro-genesis is sufficient to improve pattern separation. Nature. 2011; 472(7344): 466-470.
93. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell. 2008; 132(4): 645-660. (Pubitemid 351253687)
94. Rolls A, Shechter R, London A, Ziv Y, Ronen A, Levy R, et al. Toll-like receptors modulate adult hippocampal neu-rogenesis. Nat Cell Biol. 2007; 9(9): 1081-1088. (Pubitemid 47338146)
95. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science. 2003; 302(5651): 1760-1765. (Pubitemid 37505739)
96. Barker DJ. The developmental origins of chronic adult disease. Acta Paediatr Suppl. 2004; 93(446): 26-33. (Pubitemid 39664526)
97. Samuelsson A-M, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EHJM, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance. Hypertension. 2008; 51(2): 383-392. (Pubitemid 351159954)
98. Freeman DJ. Effects of maternal obesity on fetal growth and body composition: Implications for programming and future health. Semin Fetal Neonatal Med. 2010; 15(2): 113-118.
99. Drake AJ, Reynolds RM. Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction. 2010; 140(3): 387-398.
100. Bodnar LM, Ness RB, Harger GF, Roberts JM. Inflammation and triglycerides partially mediate the effect of prepreg-nancy body mass index on the risk of preeclampsia. Am J Epidemiol. 2005; 162(12): 1198-1206. (Pubitemid 41785914)
101. Wolf M, Kettyle E, Sandler L, Ecker JL, Roberts J, Thadhani R. Obesity and preeclampsia: The potential role of inflammation. Obstet Gynecol. 2001; 98(5 Pt 1): 757-762. (Pubitemid 33042541)
102. Hakansson S, Kallen K. High maternal body mass index increases the risk of neonatal early onset group B strepto-coccal disease. Acta Paediatr. 2008; 97(10): 1386-1389.
103. Ha°berg SE, Stigum H, London SJ, Nystad W, Nafstad P. Maternal obesityinpregnancy and respiratory healthinearly childhood. Paediatr Perinat Epidemiol. 2009; 23(4): 352-362.
104. Tulic MK, Hodder M, Forsberg A, McCarthy S, Richman T, D'Vaz N, et al. Differences in innate immune function between allergic and nonallergic children: New insights into immune ontogeny. J Allergy Clin Immunol. 2011; 127(2): 470-478.
105. Sandovici I, Smith NH, Nitert MD, Ackers-Johnson M, Uribe-Lewis S, Ito Y, et al. Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. PNAS. 2011; 108(13): 5449-5454.
106. McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: Prediction, plasticity, and programming. Physiol Rev. 2005; 85(2): 571-633. (Pubitemid 40404637)
107. Tamashiro KL, Terrillion CE, Hyun J, Koenig JI, Moran TH. Prenatal stress or high-fat diet increases susceptibility to diet-induced obesity inrat offspring. Diabetes. 2009 May; 58(5): 1116-1125.
108. Beck B. Neuropeptide Y in normal eating and in genetic and dietary-induced obesity. Philos Trans R Soc Lond B Biol Sci. 2006; 361(1417): 1159-1185. (Pubitemid 44874227)
109. Kozak R, Mercer JG, Burlet A, Moar KM, Burlet C, Beck B. Hypothalamic neuropeptide Y content and mRNA expression in weanling rats subjected to dietary manipulations during fetal and neonatal life. Regul Pept. 1998; 75-76:397-402. (Pubitemid 28477553)
110. Chang GQ, Gaysinskaya V, Karatayev O, Leibowitz SF. Maternal high-fat diet and fetal programming: Increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci. 2008; 28(46): 12107-12119.
111. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature. 2011; 467(7318): 963-966.
112. Bilbo SD, Tsang V. Enduring consequencesofmaternal obesity for brain inflammation and behavior of offspring. Faseb J. 2010; 24(6): 2104-2115.
113. Nakahara K, Nakagawa M, Baba Y, Sato M, Toshinai K, Date Y, et al. Maternal ghrelin plays an important role in rat fetal development during pregnancy. Endocrinology. 2006; 147(3): 1333-1342. (Pubitemid 43244367)
114. Diano S, Farr SA, Benoit SC, McNay EC, daSilva I, Horvath B, et al. Ghrelin controls hippocampal spine synapse density and memory performance. Nat Neurosci. 2006; 9(3): 381-388. (Pubitemid 43290968)
115. Giraudo SQ, Della-Fera MA, Proctor L, Wickwire K, Ambati S, Baile CA. Maternal high fat feeding and gesta-tional dietary restriction: Effects on offspring body weight, food intake and hypothalamic gene expression over three generations in mice. Pharmacol Biochem Behavior. 2010; 97(1): 121-129.