Shared Effects of Genetic and Intrauterine and Perinatal Environment on the Development of Metabolic Syndrome

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Vuguin, Patricia M ^a   Hartil, Kirsten ^b   Kruse, Michael ^b   Kaur, Harpreet ^a   Lin, Chia Lei Vivian ^b   Fiallo, Ariana ^b   Glenn, Alan Scott ^b   Patel, Avanee ^b   Williams, Lyda ^b   Seki, Yoshinori ^b   Katz, Ellen B ^b   Charron, Maureen J ^b,c  

^a CHILDREN S HOSPITAL AT MONTEFIORE   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c Department of Obstetrics and Gynecology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; COLONY STIMULATING FACTOR 1; GAMMA INTERFERON; GLUCOSE; GLUCOSE TRANSPORTER 4; MONOCYTE CHEMOTACTIC PROTEIN 1; PLASMINOGEN ACTIVATOR INHIBITOR 1; RANTES; CYTOKINE; GLUCOSE BLOOD LEVEL; PROTEASE NEXIN I; SERPINE2 PROTEIN, MOUSE; SLC2A4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE MEASUREMENT; CONTROLLED STUDY; CROWN RUMP LENGTH; DISEASE PREDISPOSITION; FEMALE; FETUS; FETUS WEIGHT; GENE EXPRESSION; GENETICS; GENOTYPE; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; GLYCOLYSIS; HETEROZYGOSITY; INFLAMMATION; INSULIN TOLERANCE TEST; LACTATION; LIPID DIET; MALE; METABOLIC SYNDROME X; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PATHOGENESIS; PERINATAL PERIOD; PREGNANCY; PROGENY; PROTEIN BLOOD LEVEL; SYSTOLIC BLOOD PRESSURE; UTERUS; ANALYSIS OF VARIANCE; ANIMAL; BLOOD; BLOOD PRESSURE; BODY COMPOSITION; CROSS BREEDING; GENE EXPRESSION REGULATION; HETEROZYGOTE; INSULIN RESISTANCE; LIVER; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRENATAL EXPOSURE; REAL TIME POLYMERASE CHAIN REACTION;

ADIPONECTIN; ADIPOSITY; ANALYSIS OF VARIANCE; ANIMALS; BLOOD GLUCOSE; BLOOD PRESSURE; BODY COMPOSITION; CROSSES, GENETIC; CYTOKINES; DIET, HIGH-FAT; FEMALE; FETAL WEIGHT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; GLUCOSE TRANSPORTER TYPE 4; HETEROZYGOTE; INSULIN RESISTANCE; LIVER; MALE; METABOLIC SYNDROME X; MICE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REAL-TIME POLYMERASE CHAIN REACTION; SERPIN E2;

EID: 84877853822     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063021     Document Type: Article

References (76)

1. Wang K, Li WD, Zhang CK, Wang Z, Glessner JT, et al. (2011) A genome-wide association study on obesity and obesity-related traits. PLoS One 6: e18939.
2. Wheeler E, Barroso I, (2011) Genome-wide association studies and type 2 diabetes. Brief Funct Genomics 10: 52-60.
3. Naukkarinen J, Rissanen A, Kaprio J, Pietilainen KH, (2011) Causes and consequences of obesity: the contribution of recent twin studies. Int J Obes (Lond) 36: 1017-24.
4. Poulsen P, Vaag A, (2006) The intrauterine environment as reflected by birth size and twin and zygosity status influences insulin action and intracellular glucose metabolism in an age- or time-dependent manner. Diabetes 55: 1819-1825.
5. Poston L, (2011) Intergenerational transmission of insulin resistance and type 2 diabetes. Prog Biophys Mol Biol 106: 315-322.
6. Dabelea D, Knowler WC, Pettitt DJ, (2000) Effect of diabetes in pregnancy on offspring: follow-up research in the Pima Indians. J Matern Fetal Med 9: 83-88.
7. Vuguin P, (2002) Animal models for assessing the consequences of intrauterine growth restriction on subsequent glucose metabolism of the offspring: a review. J Matern Fetal Neonatal Med 11: 254-257.
8. Vuguin PM, (2007) Animal models for small for gestational age and fetal programming of adult disease. Horm Res 68: 113-123.
9. Hales CN, Barker DJ, (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35: 595-601.
10. Martin-Gronert MS, Ozanne SE, (2012) Mechanisms underlying the developmental origins of disease. Rev Endocr Metab Disord 13: 85-92.
11. Cordain L, Eaton SB, Sebastian A, Mann N, Lindeberg S, et al. (2005) Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 81: 341-354.
12. Wolff CB, Wolff HK, (1995) Maternal eating patterns and birth weight of Mexican American infants. Nutr Health 10: 121-134.
13. Knudsen VK, Orozova-Bekkevold IM, Mikkelsen TB, Wolff S, Olsen SF, (2008) Major dietary patterns in pregnancy and fetal growth. Eur J Clin Nutr 62: 463-470.
14. Ainge H, Thompson C, Ozanne SE, Rooney KB, (2010) A systematic review on animal models of maternal high fat feeding and offspring glycaemic control. Int J Obes (Lond) 35: 325-35.
15. McCurdy CE, Bishop JM, Williams SM, Grayson BE, Smith MS, et al. (2009) Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest 119: 323-335.
16. Hartil K, Vuguin PM, Kruse M, Schmuel E, Fiallo A, et al. (2009) Maternal Substrate Utilization Programs the Development of the Metabolic Syndrome in Male Mice Exposed to High Fat in Utero. Pediatr Res 66: 368-373.
17. Stenbit AE, Tsao TS, Li J, Burcelin R, Geenen DL, et al. (1994) GLUT4 heterozygous knockout mice develop muscle insulin resistance and diabetes. Nat Med 3: 1096-1101.
18. Santalucia T, Camps M, Castello A, Munoz P, Nuel A, et al. (1992) Developmental regulation of GLUT-1 (erythroid/Hep G2) and GLUT-4 (muscle/fat) glucose transporter expression in rat heart, skeletal muscle, and brown adipose tissue. Endocrinology 130: 837-846.
19. Studelska DR, Campbell C, Pang S, Rodnick KJ, James DE, (1992) Developmental expression of insulin-regulatable glucose transporter GLUT-4. Am J Physiol 263: E102-106.
20. Katz EB, Stenbit AE, Hatton K, DePinho R, Charron MJ, (1995) Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature 377: 151-155.
21. Lambert JF, Benoit BO, Colvin GA, Carlson J, Delville Y, et al. (2000) Quick sex determination of mouse fetuses. J Neurosci Methods 95: 127-132.
22. Lo S, Russell JC, Taylor AW, (1970) Determination of glycogen in small tissue samples. J Appl Physiol 28: 234-236.
23. Carr TP, Andresen CJ, Rudel LL, (1993) Enzymatic determination of triglyceride, free cholesterol, and total cholesterol in tissue lipid extracts. Clin Biochem 26: 39-42.
24. Ranalletta M, Du XQ, Seki Y, Glenn AS, Kruse M, et al. (2007) Hepatic response to restoration of GLUT4 in skeletal muscle of GLUT4 null mice. Am J Physiol Endocrinol Metab 293: E1178-1187.
25. Vuguin PM, Kedees MH, Cui L, Guz Y, Gelling RW, et al. (2006) Ablation of the glucagon receptor gene increases fetal lethality and produces alterations in islet development and maturation. Endocrinology 147: 3995-4006.
26. Ouhilal S, Vuguin P, Cui L, Du XQ, Gelling RW, et al. (2012) Hypoglycemia, hyperglucagonemia, and fetoplacental defects in glucagon receptor knockout mice: a role for glucagon action in pregnancy maintenance. Am J Physiol Endocrinol Metab 302: E522-531.
27. Strakovsky RS, Zhang X, Zhou D, Pan YX, (2011) Gestational high fat diet programs hepatic phosphoenolpyruvate carboxykinase gene expression and histone modification in neonatal offspring rats. J Physiol 589: 2707-2717.
28. Akamine R, Yamamoto T, Watanabe M, Yamazaki N, Kataoka M, et al. (2007) Usefulness of the 5' region of the cDNA encoding acidic ribosomal phosphoprotein P0 conserved among rats, mice, and humans as a standard probe for gene expression analysis in different tissues and animal species. J Biochem Biophys Methods 70: 481-486.
29. Drake AJ, Tang JI, Nyirenda MJ, (2007) Mechanisms underlying the role of glucocorticoids in the early life programming of adult disease. Clin Sci (Lond) 113: 219-232.
30. Bayol SA, Farrington SJ, Stickland NC, (2007) A maternal 'junk food' diet in pregnancy and lactation promotes an exacerbated taste for 'junk food' and a greater propensity for obesity in rat offspring. Br J Nutr 98: 843-851.
31. Howie GJ, Sloboda DM, Kamal T, Vickers MH, (2009) Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol 587: 905-915.
32. Jackson CM, Alexander BT, Roach L, Haggerty D, Marbury DC, et al. (2012) Exposure to maternal overnutrition and a high-fat diet during early postnatal development increases susceptibility to renal and metabolic injury later in life. Am J Physiol Renal Physiol 302: F774-783.
33. Ferezou-Viala J, Roy AF, Serougne C, Gripois D, Parquet M, et al. (2007) Long-term consequences of maternal high-fat feeding on hypothalamic leptin sensitivity and diet-induced obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 293: R1056-1062.
34. Masuyama H, Hiramatsu Y, (2012) Effects of a High-Fat Diet Exposure in Utero on the Metabolic Syndrome-Like Phenomenon in Mouse Offspring through Epigenetic Changes in Adipocytokine Gene Expression. Endocrinology 153: 2823-2830.
35. Goodell LS, Wakefield DB, Ferris AM, (2009) Rapid weight gain during the first year of life predicts obesity in 2-3 year olds from a low-income, minority population. J Community Health 34: 370-375.
36. Eriksson JG, Forsen TJ, Osmond C, Barker DJ, (2003) Pathways of infant and childhood growth that lead to type 2 diabetes. Diabetes Care 26: 3006-3010.
37. Neitzke U, Harder T, Plagemann A, (2011) Intrauterine growth restriction and developmental programming of the metabolic syndrome: a critical appraisal. Microcirculation 18: 304-311.
38. Okamoto Y, Kihara S, Funahashi T, Matsuzawa Y, Libby P, (2006) Adiponectin: a key adipocytokine in metabolic syndrome. Clin Sci (Lond) 110: 267-278.
39. Jankun J, Al-Senaidy A, Skrzypczak-Jankun E, (2012) Can inactivators of plasminogen activator inhibitor alleviate the burden of obesity and diabetes? (Review). Int J Mol Med 29: 3-11.
40. Li J, Houseknecht KL, Stenbit AE, Katz EB, Charron MJ, (2000) Reduced glucose uptake precedes insulin signaling defects in adipocytes from heterozygous GLUT4 knockout mice. FASEB J 14: 1117-1125.
41. Vuguin P, Raab E, Liu B, Barzilai N, Simmons R, (2004) Hepatic insulin resistance precedes the development of diabetes in a model of intrauterine growth retardation. Diabetes 53: 2617-2622.
42. Mueller BR, Bale TL, (2008) Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28: 9055-9065.
43. Sun Y, Liu S, Ferguson S, Wang L, Klepcyk P, et al. (2002) Phosphoenolpyruvate carboxykinase overexpression selectively attenuates insulin signaling and hepatic insulin sensitivity in transgenic mice. J Biol Chem 277: 23301-23307.
44. Thorn SR, Regnault TR, Brown LD, Rozance PJ, Keng J, et al. (2009) Intrauterine growth restriction increases fetal hepatic gluconeogenic capacity and reduces messenger ribonucleic acid translation initiation and nutrient sensing in fetal liver and skeletal muscle. Endocrinology 150: 3021-3030.
45. Burgess SC, He T, Yan Z, Lindner J, Sherry AD, et al. (2007) Cytosolic phosphoenolpyruvate carboxykinase does not solely control the rate of hepatic gluconeogenesis in the intact mouse liver. Cell Metab 5: 313-320.
46. Ramnanan CJ, Edgerton DS, Rivera N, Irimia-Dominguez J, Farmer B, et al. (2010) Molecular characterization of insulin-mediated suppression of hepatic glucose production in vivo. Diabetes 59: 1302-1311.
47. Ranjit S, Boutet E, Gandhi P, Prot M, Tamori Y, et al. (2011) Regulation of fat specific protein 27 by isoproterenol and TNF-alpha to control lipolysis in murine adipocytes. J Lipid Res 52: 221-236.
48. Brown MS, Goldstein JL, (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89: 331-340.
49. Pihlajamaki J, Gylling H, Miettinen TA, Laakso M, (2004) Insulin resistance is associated with increased cholesterol synthesis and decreased cholesterol absorption in normoglycemic men. J Lipid Res 45: 507-512.
50. Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, et al. (2004) Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res 45: 1169-1196.
51. Zhao L, Chen Y, Tang R, Li Q, Gong J, et al. (2011) Inflammatory stress exacerbates hepatic cholesterol accumulation via increasing cholesterol uptake and de novo synthesis. J Gastroenterol Hepatol 26: 875-883.
52. Haggarty P (2002) Placental regulation of fatty acid delivery and its effect on fetal growth-a review. Placenta 23 Suppl A: S28-38.
53. Herrera E, Amusquivar E, (2000) Lipid metabolism in the fetus and the newborn. Diabetes Metab Res Rev 16: 202-210.
54. Herrera E, Amusquivar E, Lopez-Soldado I, Ortega H, (2006) Maternal lipid metabolism and placental lipid transfer. Horm Res 65Suppl 3: 59-64.
55. Rebholz SL, Burke KT, Yang Q, Tso P, Woollett LA, (2011) Dietary fat impacts fetal growth and metabolism: uptake of chylomicron remnant core lipids by the placenta. Am J Physiol Endocrinol Metab 301: E416-425.
56. Meshkani R, Adeli K, (2009) Hepatic insulin resistance, metabolic syndrome and cardiovascular disease. Clin Biochem 42: 1331-1346.
57. Burke-Gaffney A, Callister ME, Nakamura H, (2005) Thioredoxin: friend or foe in human disease? Trends Pharmacol Sci 26: 398-404.
58. Katsuoka F, Motohashi H, Ishii T, Aburatani H, Engel JD, et al. (2005) Genetic evidence that small maf proteins are essential for the activation of antioxidant response element-dependent genes. Mol Cell Biol 25: 8044-8051.
59. Emanuelli B, Eberle D, Suzuki R, Kahn CR, (2008) Overexpression of the dual-specificity phosphatase MKP-4/DUSP-9 protects against stress-induced insulin resistance. Proc Natl Acad Sci U S A 105: 3545-3550.
60. Fitzpatrick E, Dew TK, Quaglia A, Sherwood RA, Mitry RR, et al. (2012) Analysis of adipokine concentrations in paediatric non-alcoholic fatty liver disease. Pediatr Obes 7: 471-479.
61. Nemet D, Wang P, Funahashi T, Matsuzawa Y, Tanaka S, et al. (2003) Adipocytokines, body composition, and fitness in children. Pediatr Res 53: 148-152.
62. Bruce KD, Cagampang FR, Argenton M, Zhang J, Ethirajan PL, et al. (2009) Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology 50: 1796-1808.
63. Yoon BH, Romero R, Yang SH, Jun JK, Kim IO, et al. (1996) Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol 174: 1433-1440.
64. Bagchi A, Viscardi RM, Taciak V, Ensor JE, McCrea KA, et al. (1994) Increased activity of interleukin-6 but not tumor necrosis factor-alpha in lung lavage of premature infants is associated with the development of bronchopulmonary dysplasia. Pediatr Res 36: 244-252.
65. Catalano PM, Hauguel-De Mouzon S, (2011) Is it time to revisit the Pedersen hypothesis in the face of the obesity epidemic? Am J Obstet Gynecol 204: 479-487.
66. Amarilyo G, Oren A, Mimouni FB, Ochshorn Y, Deutsch V, et al. (2011) Increased cord serum inflammatory markers in small-for-gestational-age neonates. J Perinatol 31: 30-32.
67. Neta GI, von Ehrenstein OS, Goldman LR, Lum K, Sundaram R, et al. (2010) Umbilical cord serum cytokine levels and risks of small-for-gestational-age and preterm birth. Am J Epidemiol 171: 859-867.
68. Wright RJ, Visness CM, Calatroni A, Grayson MH, Gold DR, et al. (2010) Prenatal maternal stress and cord blood innate and adaptive cytokine responses in an inner-city cohort. Am J Respir Crit Care Med 182: 25-33.
69. Raghupathy R, Al-Azemi M, Azizieh F, (2012) Intrauterine growth restriction: cytokine profiles of trophoblast antigen-stimulated maternal lymphocytes. Clin Dev Immunol 2012: 734865.
70. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, et al. (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116: 1494-1505.
71. Wu H, Ghosh S, Perrard XD, Feng L, Garcia GE, et al. (2007) T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 115: 1029-1038.
72. Cai G, Cole SA, Butte NF, Smith CW, Mehta NR, et al. (2008) A genetic contribution to circulating cytokines and obesity in children. Cytokine 44: 242-247.
73. Bussolati B, Ahmed A, Pemberton H, Landis RC, Di Carlo F, et al. (2004) Bifunctional role for VEGF-induced heme oxygenase-1 in vivo: induction of angiogenesis and inhibition of leukocytic infiltration. Blood 103: 761-766.
74. Etienne-Manneville S, Chaverot N, Strosberg AD, Couraud PO, (1999) ICAM-1-coupled signaling pathways in astrocytes converge to cyclic AMP response element-binding protein phosphorylation and TNF-alpha secretion. J Immunol 163: 668-674.
75. Lee SA, Belyaeva OV, Kedishvili NY, (2008) Effect of lipid peroxidation products on the activity of human retinol dehydrogenase 12 (RDH12) and retinoid metabolism. Biochim Biophys Acta 1782: 421-425.
76. Symonds ME, Mostyn A, Pearce S, Budge H, Stephenson T, (2003) Endocrine and nutritional regulation of fetal adipose tissue development. J Endocrinol 179: 293-299.