The effect of maternal Inflammation on foetal programming of metabolic disease

Acta Physiologica

Volumn 214, Issue 4, 2015, Pages 440-449

  Ingvorsen, C ^a,b   Brix, S ^a   Ozanne, S E ^c   Hellgren, L I ^a,b  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b Center for Fetal Programming   (Denmark)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Foetal programming; Inflammation; Metabolic disease; Obesity; Pregnancy

Indexed keywords

CYTOKINE; LIPOPOLYSACCHARIDE;

FETUS CIRCULATION; FETUS DEVELOPMENT; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFLAMMATION; MATERNAL OBESITY; METABOLIC DISORDER; NONHUMAN; OBESITY; PHENOTYPE; PLACENTAL TRANSFER; PREGNANCY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; TH2 CELL; ANIMAL; COMPLICATION; FEMALE; METABOLIC DISEASES; PREGNANCY COMPLICATION; PRENATAL EXPOSURE;

ANIMALS; FEMALE; FETAL DEVELOPMENT; HUMANS; INFLAMMATION; METABOLIC DISEASES; OBESITY; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84949109744     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12533     Document Type: Review

References (86)

1. Andersen, S.L. 2003. Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27, 3-18.
2. Ashdown, H., Dumont, Y., Ng, M., Poole, S., Boksa, P. & Luheshi, G.N. 2006. The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia. Mol Psychiatry 11, 47-55.
3. Basu, S., Leahy, P., Challier, J.C., Minium, J., Catalano, P. & Hauguel-de Mouzon, S. 2011. Molecular phenotype of monocytes at the maternal-fetal interface. Am J Obstet Gynecol 205, 265 e1-8.
4. Belo, L., Santos-Silva, A., Rocha, S., Caslake, M., Cooney, J., Pereira-Leite, L., Quintanilha, A. & Rebelo, I. 2005. Fluctuations in C-reactive protein concentration and neutrophil activation during normal human pregnancy. Eur J Obstet Gynecol Reprod Biol 123, 46-51.
5. Beloosesky, R., Maravi, N., Weiner, Z., Khatib, N., Awad, N., Boles, J., Ross, M.G. & Itskovitz-Eldor, J. 2010. Maternal lipopolysaccharide-induced inflammation during pregnancy programs impaired offspring innate immune responses. Am J Obstet Gynecol203, 185 e1-4.
6. Berardis, S. & Sokal, E. 2014. Pediatric non-alcoholic fatty liver disease: an increasing public health issue. Eur J Pediatr 173, 131-139.
7. Bruce, K.D., Cagampang, F.R., Argenton, M., Zhang, J.L., Ethirajan, P.L., Burdge, G.C., Bateman, A.C., Clough, G.F., Poston, L., Hanson, M.A., McConnell, J.M. & Byrne, C.D. 2009. Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology 50, 1796-1808.
8. Brumbaugh, D.E. & Friedman, J.E. 2014. Developmental origins of nonalcoholic fatty liver disease. Pediatr Res 75, 140-147.
9. Cani, P.D., Amar, J., Iglesias, M.A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A.M., Fava, F., Tuohy, K.M., Chabo, C. et al. 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761-1772.
10. Catalano, P.M., Farrell, K., Thomas, A., Huston-Presley, L., Mencin, P., de Mouzon, S.H. & Amini, S.B. 2009. Perinatal risk factors for childhood obesity and metabolic dysregulation. Am J Clin Nutr 90, 1303-1313.
11. Challier, J.C., Basu, S., Bintein, T., Minium, J., Hotmire, K., Catalano, P.M. & Hauguel-de Mouzon, S. 2008. Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta. Placenta 29, 274-281.
12. Chawla, A., Nguyen, K.D. & Goh, Y.P. 2011. Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol 11, 738-749.
13. Cnattingius, S., Villamor, E., Lagerros, Y.T., Wikstrom, A.K. & Granath, F. 2012. High birth weight and obesity-a vicious circle across generations. Int J Obes 36, 1320-1324.
14. Confavreux, C., Hutchinson, M., Hours, M.M., Cortinovis-Tourniaire, P. & Moreau, T. 1998. Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in Multiple Sclerosis Group. N Engl J Med 339, 285-291.
15. Dahlgren, J. 2006. Pregnancy and insulin resistance. Metab Syndr Relat Disord 4, 149-152.
16. Dahlgren, J., Nilsson, C., Jennische, E., Ho, H.P., Eriksson, E., Niklasson, A., Bjorntorp, P., Wikland, K.A. & Holmang, A. 2001. Prenatal cytokine exposure results in obesity and gender-specific programming. Am J Physiol Endocrinol Metab 281, E326-E334.
17. Datti, F., Datti, M. & Antunes, E. 2008. Prenatal exposure to endotoxin in rats attenuates the allergic airways eosinophil infiltration in the adult offspring: role of inducible nitric oxide synthase activation. Pulm Pharmacol Ther 21, 349-404.
18. De Souza, C.T., Araujo, E.P., Bordin, S., Ashimine, R., Zollner, R.L., Boschero, A.C., Saad, M.J. & Velloso, L.A. 2005. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 146, 4192-4199.
19. Donath, M.Y. & Shoelson, S.E. 2011. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11, 98-107.
20. Du, M., Yan, X., Tong, J.F., Zhao, J. & Zhu, M.J. 2010. Maternal obesity, inflammation, and fetal skeletal muscle development. Biol Reprod 82, 4-12.
21. Dunna, S.F. & Finlay, A.Y. 1989. Psoriasis: improvement during and worsening after pregnancy. Br J Dermatol 120, 584.
22. Duval, C., Thissen, U., Keshtkar, S., Accart, B., Stienstra, R., Boekschoten, M.V., Roskams, T., Kersten, S. & Muller, M. 2010. Adipose tissue dysfunction signals progression of hepatic steatosis towards nonalcoholic steatohepatitis in C57BL/6 mice. Diabetes 59, 3181-3191.
23. Elahi, M.M., Cagampang, F.R., Mukhtar, D., Anthony, F.W., Ohri, S.K. & Hanson, M.A. 2009. Long-term maternal high-fat feeding from weaning through pregnancy and lactation predisposes offspring to hypertension, raised plasma lipids and fatty liver in mice. Br J Nutr 102, 514-519.
24. Fan, L., Lindsley, S.R., Comstock, S.M., Takahashi, D.L., Evans, A.E., He, G.W., Thornburg, K.L. & Grove, K.L. 2013. Maternal high-fat diet impacts endothelial function in nonhuman primate offspring. Int J Obes (Lond) 37, 254-262.
25. Farah, N., Hogan, A.E., O'Connor, N., Kennelly, M.M., O'Shea, D. & Turner, M.J. 2012. Correlation between maternal inflammatory markers and fetomaternal adiposity. Cytokine 60, 96-99.
26. Farley, D., Tejero, M.E., Comuzzie, A.G., Higgins, P.B., Cox, L., Werner, S.L., Jenkins, S.L., Li, C., Choi, J., Dick, E.J. Jr et al. 2009. Feto-placental adaptations to maternal obesity in the baboon. Placenta 30, 752-760.
27. Friis, C.M., Roland, M.C.P., Godang, K., Ueland, T., Tanbo, T., Bollerslev, J. & Henriksen, T. 2013. Adiposity-related inflammation: effects of pregnancy. Obesity 21, E124-E130.
28. Gaccioli, F., Lager, S., Powell, T.L. & Jansson, T. 2013. Placental transport in response to altered maternal nutrition. J Dev Orig Health Dis 4, 101-115.
29. Girard, S., Tremblay, L., Lepage, M. & Sebire, G. 2010. IL-1 receptor antagonist protects against placental and neurodevelopmental defects induced by maternal inflammation. J Immunol 184, 3997-4005.
30. Han, J., Xu, J., Epstein, P.N. & Liu, Y.Q. 2005. Long-term effect of maternal obesity on pancreatic beta cells of offspring: reduced beta cell adaptation to high glucose and high-fat diet challenges in adult female mouse offspring. Diabetologia 48, 1810-1818.
31. Hauguel-de Mouzon, S. & Guerre-Millo, M. 2006. The placenta cytokine network and inflammatory signals. Placenta 27, 794-798.
32. Hodyl, N.A., Krivanek, K.M., Clifton, V.L. & Hodgson, D.M. 2008. Innate immune dysfunction in the neonatal rat following prenatal endotoxin exposure. J Neuroimmunol 204, 126-130.
33. Hong, E.G., Ko, H.J., Cho, Y.R., Kim, H.J., Ma, Z., Yu, T.Y., Friedline, R.H., Kurt-Jones, E., Finberg, R., Fischer, M.A. et al. 2009. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 58, 2525-2535.
34. Ingvorsen, C., Thysen, A.H., Fernandez-Twinn, D., Nordby, P., Nielsen, K.F., Ozanne, S.E., Brix, S. & Hellgren, L.I. 2014. Effects of pregnancy on obesity-induced inflammation in a mouse model of fetal programming. Int J Obes (Lond) 38, 1282-1289.
35. Kanneganti, T.D. & Dixit, V.D. 2012. Immunological complications of obesity. Nat Immunol 13, 707-712.
36. Kirwan, J.P., Hauguel-De Mouzon, S., Lepercq, J., Challier, J.-C., Huston-Presley, L., Friedman, J.E., Kalhan, S.C. & Catalano, P.M. 2002a. TNF-α Is a predictor of insulin resistance in human pregnancy. Diabetes 51, 2207-2213.
37. Kirwan, J.P., Hauguel-De Mouzon, S., Lepercq, J., Challier, J.C., Huston-Presley, L., Friedman, J.E., Kalhan, S.C. & Catalano, P.M. 2002b. TNF-alpha is a predictor of insulin resistance in human pregnancy. Diabetes 51, 2207-2213.
38. Lager, S., Jansson, N., Olsson, A.L., Wennergren, M., Jansson, T. & Powell, T.L. 2011. Effect of IL-6 and TNF-alpha on fatty acid uptake in cultured human primary trophoblast cells. Placenta 32, 121-127.
39. Lanthier, N., Molendi-Coste, O., Horsmans, Y., van Rooijen, N., Cani, P.D. & Leclercq, I.A. 2010. Kupffer cell activation is a causal factor for hepatic insulin resistance. Am J Physiol Gastrointest Liver Physiol 298, G107-G116.
40. Lasala, N. & Zhou, H. 2007. Effects of maternal exposure to LPS on the inflammatory response in the offspring. J Neuroimmunol 189, 95-101.
41. Latouche, C., Heywood, S.E., Henry, S.L., Ziemann, M., Lazarus, R., El-Osta, A., Armitage, J.A. & Kingwell, B.A. 2014. Maternal overnutrition programs changes in the expression of skeletal muscle genes that are associated with insulin resistance and defects of oxidative phosphorylation in adult male rat offspring. J Nutr 144, 237-244.
42. Lawlor, D.A., Smith, G.D., O'Callaghan, M., Alati, R., Mamun, A.A., Williams, G.M. & Najman, J.M. 2007. Epidemiologic evidence for the fetal overnutrition hypothesis: findings from the mater-university study of pregnancy and its outcomes. Am J Epidemiol 165, 418-424.
43. Leibowitz, K.L., Moore, R.H., Ahima, R.S., Stunkard, A.J., Stallings, V.A., Berkowitz, R.I., Chittams, J.L., Faith, M.S. & Stettler, N. 2012. Maternal obesity associated with inflammation in their children. World J Pediatr 8, 76-79.
44. Lieb, W., Pencina, M.J., Lanier, K.J., Tofler, G.H., Levy, D., Fox, C.S., Wang, T.J., D'Agostino, R.B. Sr & Vasan, R.S. 2009. Association of parental obesity with concentrations of select systemic biomarkers in nonobese offspring: the Framingham Heart Study. Diabetes 58, 134-137.
45. Lumeng, C.N. 2013. Innate immune activation in obesity. Mol Aspects Med 34, 12-29.
46. Luppi, P. 2003. How immune mechanisms are affected by pregnancy. Vaccine 21, 3352-3357.
47. Maloney, S., Smith, A., Furst, D.E., Myerson, D., Rupert, K., Evans, P.C. & Nelson, J.L. 1999. Microchimerism of maternal origin persists into adult life. J Clin Investig 104, 41-47.
48. Marleau, A.M., Greenwood, J.D., Wei, Q., Singh, B. & Croy, B.A. 2003. Chimerism of murine fetal bone marrow by maternal cells occurs in late gestation and persists into adulthood. Lab Invest 83, 673-681.
49. Marzi, M., Vigano, A., Trabattoni, D., Villa, M.L., Salvaggio, A., Clerici, E. & Clerici, M. 1996. Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin Exp Immunol 106, 127-133.
50. McCurdy, C.E., Bishop, J.M., Williams, S.M., Grayson, B.E., Smith, M.S., Friedman, J.E. & Grove, K.L. 2009. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest 119, 323-335.
51. Modi, N., Murgasova, D., Ruager-Martin, R., Thomas, E.L., Hyde, M.J., Gale, C., Santhakumaran, S., Dore, C.J., Alavi, A. & Bell, J.D. 2011. The influence of maternal body mass index on infant adiposity and hepatic lipid content. Pediatr Res 70, 287-291.
52. Mold, J.E., Michaëlsson, J., Burt, T.D., Muench, M.O., Beckerman, K.P., Busch, M.P., Lee, T.-H., Nixon, D.F. & McCune, J.M. 2008. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322, 1562-1565.
53. Mor, G. & Cardenas, I. 2010. The immune system in pregnancy: a unique complexity. Am J Reprod Immunol 63, 425-433.
54. Mouralidarane, A., Soeda, J., Visconti-Pugmire, C., Samuelsson, A.-M., Pombo, J., Maragkoudaki, X., Butt, A., Saraswati, R., Novelli, M., Fusai, G., Poston, L., Taylor, P.D. & Oben, J.A. 2013. Maternal obesity programs offspring nonalcoholic fatty liver disease by innate immune dysfunction in mice. Hepatology 58, 128-138.
55. Murrin, C., Kelly, G., Tremblay, R. & Kelleher, C. 2012. Body mass index and height over three generations: evidence from the Lifeways cross-generational cohort study. BMC Public Health 12, 81.
56. Nelson, J.L., Gillespie, K.M., Lambert, N.C., Stevens, A.M., Loubiere, L.S., Rutledge, J.C., Leisenring, W.M., Erickson, T.D., Yan, Z., Mullarkey, M.E., Boespflug, N.D., Bingley, P.J. & Gale, E.A.M. 2007. Maternal microchimerism in peripheral blood in type 1 diabetes and pancreatic islet β cell microchimerism. Proc Natl Acad Sci U S A 104, 1637-1642.
57. Nilsson, C., Larsson, B.M., Jennische, E., Eriksson, E., Bjorntorp, P., York, D.A. & Holmang, A. 2001. Maternal endotoxemia results in obesity and insulin resistance in adult male offspring. Endocrinology 142, 2622-2630.
58. Oben, J.A., Mouralidarane, A., Samuelsson, A.M., Matthews, P.J., Morgan, M.L., McKee, C., Soeda, J., Fernandez-Twinn, D.S., Martin-Gronert, M.S., Ozanne, S.E., Sigala, B., Novelli, M., Poston, L. & Taylor, P.D. 2010. Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. J Hepatol 52, 913-920.
59. Odegaard, J.I. & Chawla, A. 2013. Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis. Science 339, 172-177.
60. Oskvig, D.B., Elkahloun, A.G., Johnson, K.R., Phillips, T.M. & Herkenham, M. 2012. Maternal immune activation by LPS selectively alters specific gene expression profiles of interneuron migration and oxidative stress in the fetus without triggering a fetal immune response. Brain Behav Immun 26, 623-634.
61. Ostensen, M. & Villiger, P.M. 2002. Immunology of pregnancy-pregnancy as a remission inducing agent in rheumatoid arthritis. Transpl Immunol 9, 155-160.
62. Pazos, M., Sperling, R.S., Moran, T.M. & Kraus, T.A. 2012. The influence of pregnancy on systemic immunity. Immunol Res 54, 254-261.
63. Plata, M.D., Williams, L., Seki, Y., Hartil, K., Kaur, H., Lin, C.L., Fiallo, A., Glenn, A.S., Katz, E.B., Fuloria, M., Charron, M.J. & Vuguin, P.M. 2014. Critical periods of increased fetal vulnerability to a maternal high fat diet. Reprod Biol Endocrinol 12, 1-11.
64. Poston, L. 2012. Maternal obesity, gestational weight gain and diet as determinants of offspring long term health. Best Pract Res Clin Endocrinol Metab 26, 627-639.
65. Ramsay, J.E., Ferrell, W.R., Crawford, L., Wallace, A.M., Greer, I.A. & Sattar, N. 2002. Maternal obesity is associated with dysregulation of metabolic, vascular, and inflammatory pathways. J Clin Endocrinol Metab 87, 4231-4237.
66. Raychaudhuri, S.P., Navare, T., Gross, J. & Raychaudhuri, S.K. 2003. Clinical course of psoriasis during pregnancy. Int J Dermatol 42, 518-520.
67. Robbins, J.R. & Bakardjiev, A.I. 2012. Pathogens and the placental fortress. Curr Opin Microbiol 15, 36-43.
68. Robinson, D.P. & Klein, S.L. 2012. Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm Behav 62, 263-271.
69. Saito, S. 2000. Cytokine network at the feto-maternal interface. J Reprod Immunol 47, 87-103.
70. Samuelsson, A.-M., Matthews, P.A., Argenton, M., Christie, M.R., McConnell, J.M., Jansen, E.H.J.M., Piersma, A.H., Ozanne, S.E., Twinn, D.F., Remacle, C., Rowlerson, A., Poston, L. & Taylor, P.D. 2008a. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 51, 383-392.
71. Samuelsson, A.M., Matthews, P.A., Argenton, M., Christie, M.R., McConnell, J.M., Jansen, E., Piersma, A.H., Ozanne, S.E., Twinn, D.F., Remacle, C., Rowlerson, A., Poston, L. & Taylor, P.D. 2008b. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance - a novel murine model of developmental programming. Hypertension 51, 383-392.
72. Schumacher, A., Brachwitz, N., Sohr, S., Engeland, K., Langwisch, S., Dolaptchieva, M., Alexander, T., Taran, A., Malfertheiner, S.F., Costa, S.D. et al. 2009. Human chorionic gonadotropin attracts regulatory T cells into the fetal-maternal interface during early human pregnancy. J Immunol 182, 5488-5497.
73. Segovia, S.A., Vickers, M.H., Gray, C. & Reynolds, C.M. 2014. Maternal obesity, inflammation, and developmental programming. BioMed Res Int 2014, 14.
74. Sen, S., Iyer, C., Klebenov, D., Histed, A., Aviles, J.A. & Meydani, S.N. 2013. Obesity impairs cell-mediated immunity during the second trimester of pregnancy. Am J Obstet Gynecol 208, 139.e1-139.e8.
75. Shankar, K., Harrell, A., Liu, X.L., Gilchrist, J.M., Ronis, M.J.J. & Badger, T.M. 2008. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 294, R528-R538.
76. Si-Tayeb, K., Lemaigre, F.P. & Duncan, S.A. 2010. Organogenesis and development of the liver. Dev Cell 18, 175-189.
77. Tsampalas, M., Gridelet, V., Berndt, S., Foidart, J.M., Geenen, V. & d'Hauterive, S.P. 2010. Human chorionic gonadotropin: a hormone with immunological and angiogenic properties. J Reprod Immunol 85, 93-98.
78. Unal, E.R., Cierny, J.T., Roedner, C., Newman, R. & Goetzl, L. 2011. Maternal inflammation in spontaneous term labor. Am J Obstet Gynecol 204, 223 e1-5.
79. Varma, V., Yao-Borengasser, A., Rasouli, N., Nolen, G.T., Phanavanh, B., Starks, T., Gurley, C., Simpson, P., McGehee, R.E. Jr, Kern, P.A. & Peterson, C.A. 2009. Muscle inflammatory response and insulin resistance: synergistic interaction between macrophages and fatty acids leads to impaired insulin action. Am J Physiol Endocrinol Metab 296, E1300-E1310.
80. Wei, Y.L., Li, X.H. & Zhou, J.Z. 2007. Prenatal exposure to lipopolysaccharide results in increases in blood pressure and body weight in rats. Acta Pharmacol Sin 28, 651-656.
81. Wienecke, J., Hebel, K., Hegel, K.J., Pierau, M., Brune, T., Reinhold, D., Pethe, A. & Brunner-Weinzierl, M.C. 2012. Pro-inflammatory effector Th cells transmigrate through anti-inflammatory environments into the murine fetus. Placenta 33, 39-46.
82. Williams, C.L., Teeling, J.L., Perry, V.H. & Fleming, T.P. 2011. Mouse maternal systemic inflammation at the zygote stage causes blunted cytokine responsiveness in lipopolysaccharide-challenged adult offspring. BMC Biol 9, 49.
83. Wu, D., Molofsky, A.B., Liang, H.E., Ricardo-Gonzalez, R.R., Jouihan, H.A., Bando, J.K., Chawla, A. & Locksley, R.M. 2011. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332, 243-247.
84. Xu, D.X., Wang, H., Zhao, L., Ning, H., Chen, Y.H. & Zhang, C. 2007. Effects of low-dose lipopolysaccharide (LPS) pretreatment on LPS-induced intra-uterine fetal death and preterm labor. Toxicology 234, 167-175.
85. Yan, Z., Aydelotte, T., Gadi, V.K., Guthrie, K.A. & Nelson, J.L. 2011. Acquisition of the rheumatoid arthritis HLA shared epitope through microchimerism. Arthritis Rheum 63, 640-644.
86. Zaretsky, M.V., Alexander, J.M., Byrd, W. & Bawdon, R.E. 2004. Transfer of inflammatory cytokines across the placenta. Obstet Gynecol 103, 546-550.