Maternal obesity and the developmental programming of hypertension: A role for leptin

Acta Physiologica

Volumn 210, Issue 3, 2014, Pages 508-523

  Taylor, P D ^a   Samuelsson, A M ^a   Poston, L ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Developmental programming; Hypertension; Leptin; Obesity; Pregnancy

Indexed keywords

INSULIN; LEPTIN;

ADRENERGIC SYSTEM; BLOOD PRESSURE REGULATION; BODY MASS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; GESTATION PERIOD; GESTATIONAL WEIGHT GAIN; HEART FUNCTION; HUMAN; HYPERTENSION; MATERNAL OBESITY; NERVE CELL DIFFERENTIATION; NONHUMAN; OVERNUTRITION; PATHOPHYSIOLOGY; PREGNANCY; PRIORITY JOURNAL; REVIEW; WEIGHT GAIN;

DEVELOPMENTAL PROGRAMMING; HYPERTENSION; LEPTIN; OBESITY; PREGNANCY;

ANIMALS; FEMALE; HUMANS; HYPERTENSION; LEPTIN; MOTHERS; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84893503597     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12223     Document Type: Review

References (151)

1. Ahima, R.S., Prabakaran, D. & Flier, J.S. 1998. Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest 101, 1020-1027.
2. Ailhaud, G., Massiera, F., Weill, P., Legrand, P., Alessandri, J.M. & Guesnet, P. 2006. Temporal changes in dietary fats: role of n-6 polyunsaturated fatty acids in excessive adipose tissue development and relationship to obesity. Prog Lipid Res 45, 203-236.
3. Ailhaud, G., Guesnet, P. & Cunnane, S.C. 2008. An emerging risk factor for obesity: does disequilibrium of polyunsaturated fatty acid metabolism contribute to excessive adipose tissue development? Br J Nutr 100, 461-470.
4. Akcakus, M., Koklu, E., Baykan, A., Yikilmaz, A., Coskun, A., Gunes, T., Kurtoglu, S. & Narin, N. 2007. Macrosomic newborns of diabetic mothers are associated with increased aortic intima-media thickness and lipid concentrations. Horm Res 67, 277-283.
5. Akyol, A., Langley-Evans, S.C. & McMullen, S. 2009. Obesity induced by cafeteria feeding and pregnancy outcome in the rat. Br J Nutr 102, 1601-1610.
6. Almeida, J.R. & Mandarim-de-Lacerda, C.A. 2005. Overweight is gender-dependent in prenatal protein-calorie restricted adult rats acting on the blood pressure and the adverse cardiac remodeling. Life Sci 77, 1307-1318.
7. Anatskaya, O.V., Sidorenko, N.V., Beyer, T.V. & Vinogradov, A.E. 2009. Neonatal cardiomyocyte ploidy reveals critical windows of heart development. Int J Cardiol 141, 81-91.
8. Armitage, J.A., Lakasing, L., Taylor, P.D., Balachandran, A.A., Jensen, R.I., Dekou, V., Ashton, N., Nyengaard, J.R. & Poston, L. 2005a. Developmental programming of aortic and renal structure in offspring of rats fed fat-rich diets in pregnancy. J Physiol 565, 171-184.
9. Armitage, J.A., Taylor, P.D. & Poston, L. 2005b. Experimental models of developmental programming; Consequences of exposure to an energy rich diet during development. J Physiol 565, 171-184.
10. Armitage, J.A., Ishibashi, A., Balachandran, A.A., Jensen, R.I., Poston, L. & Taylor, P.D. 2007. Programmed aortic dysfunction and reduced Na+, K+-ATPase activity present in first generation offspring of lard-fed rats does not persist to the second generation. Exp Physiol 92, 583-589.
11. Attig, L., Solomon, G., Ferezou, J., Abdennebi-Najar, L., Taouis, M., Gertler, A. & Djiane, J. 2008. Early postnatal leptin blockage leads to a long-term leptin resistance and susceptibility to diet-induced obesity in rats. Int J Obes (Lond) 32, 1153-1160.
12. Bacharova, L., Krivosikova, Z., Wsolova, L. & Gajdos, M. 2012. Alterations in the QRS complex in the offspring of patients with metabolic syndrome and diabetes mellitus: early evidence of cardiovascular pathology. J Electrocardiol 45, 244-251.
13. Bae, S., Xiao, Y., Li, G., Casiano, C.A. & Zhang, L. 2003. Effect of maternal chronic hypoxic exposure during gestation on apoptosis in fetal rat heart. Am J Physiol Heart Circ Physiol 285, H983-H990.
14. Battista, M., Calvo, E., Chorvatova, A., Comte, B., Corbeil, J. & Brochu, M. 2005. Intra-uterine growth restriction and the programming of left ventricular remodelling in female rats. J Physiol 565(Pt 1), 197-205.
15. Bautista, C.J., Boeck, L., Larrea, F., Nathanielsz, P.W. & Zambrano, E. 2008. Effects of a maternal low protein isocaloric diet on milk leptin and progeny serum leptin concentration and appetitive behavior in the first 21 days of neonatal life in the rat. Pediatr Res 63, 358-363.
16. Bayol, S.A., Simbi, B.H. & Stickland, N.C. 2005. A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 567, 951-961.
17. Boney, C.M., Verma, A., Tucker, R. & Vohr, B.R. 2005. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 115, e290-e296.
18. Bouret, S.G. 2010. Neurodevelopmental actions of leptin. Brain Res 1350, 2-9.
19. Bouret, S.G., Draper, S.J. & Simerly, R.B. 2004a. Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J Neurosci 24, 2797-2805.
20. Bouret, S.G., Draper, S.J. & Simerly, R.B. 2004b. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304, 108-110.
21. Bouret, S.G., Gorski, J.N., Patterson, C.M., Chen, S., Levin, B.E. & Simerly, R.B. 2008. Hypothalamic neural projections are permanently disrupted in diet-induced obese rats. Cell Metab 7, 179-185.
22. Carlyle, M., Jones, O.B., Kuo, J.J. & Hall, J.E. 2002. Chronic cardiovascular and renal actions of leptin: role of adrenergic activity. Hypertension 39, 496-501.
23. Casabiell, X., Pineiro, V., Tome, M.A., Peino, R., Dieguez, C. & Casanueva, F.F. 1997. Presence of leptin in colostrum and/or breast milk from lactating mothers: a potential role in the regulation of neonatal food intake. J Clin Endocrinol Metab 82, 4270-4273.
24. Catalano, P.M., Presley, L., Minium, J. & Hauguel-de Mouzon, S. 2009. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care 32, 1076-1080.
25. Catta-Preta, M., Oliveira, D.A., Mandarim-de-Lacerda, C.A. & Aguila, M.B. 2006. Adult cardiorenal benefits from postnatal fish oil supplement in rat offspring of low-protein pregnancies. Life Sci 80, 219-229.
26. Cetin, I., Morpurgo, P.S., Radaelli, T., Taricco, E., Cortelazzi, D., Bellotti, M., Pardi, G. & Beck-Peccoz, P. 2000. Fetal plasma leptin concentrations: relationship with different intrauterine growth patterns from 19 weeks to term. Pediatr Res 48, 646-651.
27. Chan, L.L., Sebert, S.P., Hyatt, M.A., Stephenson, T., Budge, H., Symonds, M.E. & Gardner, D.S. 2009. Effect of maternal nutrient restriction from early to midgestation on cardiac function and metabolism after adolescent-onset obesity. Am J Physiol Regul Integr Comp Physiol 296, R1455-R1463.
28. Chang, G.Q., Gaysinskaya, V., Karatayev, O. & Leibowitz, S.F. 2008. Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci 28, 12107-12119.
29. Cheema, K.K., Dent, M.R., Saini, H.K., Aroutiounova, N. & Tappia, P.S. 2005. Prenatal exposure to maternal undernutrition induces adult cardiac dysfunction. Br J Nutr 93, 471-477.
30. Chen, H., Simar, D., Lambert, K., Mercier, J. & Morris, M.J. 2008. Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism. Endocrinology 149, 5348-5356.
31. Cottrell, E.C., Cripps, R.L., Duncan, J.S., Barrett, P., Mercer, J.G., Herwig, A. & Ozanne, S.E. 2009. Developmental changes in hypothalamic leptin receptor: relationship with the postnatal leptin surge and energy balance neuropeptides in the postnatal rat. Am J Physiol Regul Integr Comp Physiol 296, R631-R639.
32. Cripps, R.L., Martin-Gronert, M.S. & Ozanne, S.E. 2005. Fetal and perinatal programming of appetite. Clin Sci (Lond) 109, 1-11.
33. Davis, L., Roullet, J.B., Thornburg, K.L., Shokry, M., Hohimer, A.R. & Giraud, G.D. 2003. Augmentation of coronary conductance in adult sheep made anaemic during fetal life. J Physiol 547, 53-59.
34. Delahaye, F., Breton, C., Risold, P.Y., Enache, M., Dutriez-Casteloot, I., Laborie, C., Lesage, J. & Vieau, D. 2008. Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology 149, 470-475.
35. Denison, F.C., Norrie, G., Graham, B., Lynch, J., Harper, N. & Reynolds, R.M. 2009. Increased maternal BMI is associated with an increased risk of minor complications during pregnancy with consequent cost implications. BJOG 116, 1467-1472.
36. Devaskar, S.U., Ollesch, C., Rajakumar, R.A. & Rajakumar, P.A. 1997. Developmental changes in ob gene expression and circulating leptin peptide concentrations. Biochem Biophys Res Commun 238, 44-47.
37. Dodd, J.M., Grivell, R.M., Crowther, C.A. & Robinson, J.S. 2010. Antenatal interventions for overweight or obese pregnant women: a systematic review of randomised trials. BJOG 117, 1316-1326.
38. Drake, A.J. & Reynolds, R.M. 2010. Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction 140, 387-398.
39. Dunbar, J.C. & Lu, H. 1999. Leptin-induced increase in sympathetic nervous and cardiovascular tone is mediated by proopiomelanocortin (POMC) products. Brain Res Bull 50, 215-221.
40. Elmes, M.J., Gardner, D.S. & Langley-Evans, S.C. 2007. Fetal exposure to a maternal low-protein diet is associated with altered left ventricular pressure response to ischaemia-reperfusion injury. Br J Nutr 98, 93-100.
41. Elmes, M.J., McMullen, S., Gardner, D.S. & Langley-Evans, S.C. 2008. Prenatal diet determines susceptibility to cardiac ischaemia-reperfusion injury following treatment with diethylmaleic acid and N-acetylcysteine. Life Sci 82, 149-155.
42. Elmquist, J.K. & Flier, J.S. 2004. Neuroscience. The fat-brain axis enters a new dimension. Science 304, 63-64.
43. Ferezou-Viala, J., Roy, A.F., Serougne, C., Gripois, D., Parquet, M., Bailleux, V., Gertler, A., Delplanque, B., Djiane, J., Riottot, M. & Taouis, M. 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-R1062.
44. Fernandez-Twinn, D.S., Ekizoglou, S., Wayman, A., Petry, C.J. & Ozanne, S.E. 2006. Maternal low protein diet programs cardiac beta-adrenergic response and signalling in 3 month old male offspring. Am J Physiol Regul Integr Comp Physiol 291, 429-436.
45. Fernandez-Twinn, D.S., Blackmore, H.L., Siggens, L., Giussani, D.A., Cross, C.M., Foo, R. & Ozanne, S.E. 2012. The programming of cardiac hypertrophy in the offspring by maternal obesity is associated with hyperinsulinemia, AKT, ERK, and mTOR activation. Endocrinology 153, 5961-5971.
46. Filler, G., Yasin, A., Kesarwani, P., Garg, A.X., Lindsay, R. & Sharma, A.P. 2011. Big mother or small baby: which predicts hypertension? J Clin Hypertens (Greenwich) 13, 35-41.
47. Fraser, A., Tilling, K., Macdonald-Wallis, C., Hughes, R., Sattar, N., Nelson, S.M. & Lawlor, D.A. 2011. Associations of gestational weight gain with maternal body mass index, waist circumference, and blood pressure measured 16 y after pregnancy: the Avon Longitudinal Study of Parents and Children (ALSPAC). Am J Clin Nutr 93, 1285-1292.
48. Gademan, M.G., van Eijsden, M., Roseboom, T.J., van der Post, J.A., Stronks, K. & Vrijkotte, T.G. 2013. Maternal prepregnancy body mass index and their children's blood pressure and resting cardiac autonomic balance at age 5 to 6 years. Hypertension 62, 641-647.
49. Gardner, B., Wardle, J., Poston, L. & Croker, H. 2011. Changing diet and physical activity to reduce gestational weight gain: a meta-analysis. Obes Rev 12, e602-e620.
50. Giraud, G.D., Louey, S., Jonker, S., Schultz, J. & Thornburg, K.L. 2006. Cortisol stimulates cell cycle activity in the cardiomyocyte of the sheep fetus. Endocrinology 147, 3643-3649.
51. Glavas, M.M., Kirigiti, M.A., Xiao, X.Q., Enriori, P.J., Fisher, S.K., Evans, A.E., Grayson, B.E., Cowley, M.A., Smith, M.S. & Grove, K.L. 2010. Early overnutrition results in early-onset arcuate leptin resistance and increased sensitivity to high-fat diet. Endocrinology 151, 1598-1610.
52. Grayson, B.E., Allen, S.E., Billes, S.K., Williams, S.M., Smith, M.S. & Grove, K.L. 2006. Prenatal development of hypothalamic neuropeptide systems in the nonhuman primate. Neuroscience 143, 975-986.
53. Greenfield, J.R., Miller, J.W., Keogh, J.M., Henning, E., Satterwhite, J.H., Cameron, G.S., Astruc, B., Mayer, J.P., Brage, S., See, T.C., Lomas, D.J., O'Rahilly, S. & Farooqi, I.S. 2009. Modulation of blood pressure by central melanocortinergic pathways. N Engl J Med 360, 44-52.
54. Grove, K.L. & Smith, M.S. 2003. Ontogeny of the hypothalamic neuropeptide Y system. Physiol Behav 79, 47-63.
55. Grove, K.L., Grayson, B.E., Glavas, M.M., Xiao, X.Q. & Smith, M.S. 2005. Development of metabolic systems. Physiol Behav 86, 646-660.
56. Hales, C.N. & Barker, D.J. 2001. The thrifty phenotype hypothesis. Br Med Bull 60, 5-20.
57. Han, H.C., Austin, K.J., Nathanielsz, P.W., Ford, S.P., Nijland, M.J. & Hansen, T.R. 2004. Maternal nutrient restriction alters gene expression in the ovine fetal heart. J Physiol 558, 111-121.
58. Harlan, S.M., Morgan, D.A., Agassandian, K., Guo, D.F., Cassell, M.D., Sigmund, C.D., Mark, A.L. & Rahmouni, K. 2011. Ablation of the leptin receptor in the hypothalamic arcuate nucleus abrogates leptin-induced sympathetic activation. Circ Res 108, 808-812.
59. Haynes, W.G., Morgan, D.A., Walsh, S.A., Mark, A.L. & Sivitz, W.I. 1997. Receptor-mediated regional sympathetic nerve activation by leptin. J Clin Invest 100, 270-278.
60. Heerwagen, M.J., Stewart, M.S., de la Houssaye, B.A., Janssen, R.C. & Friedman, J.E. 2013. Transgenic increase in N-3/n-6 fatty acid ratio reduces maternal obesity-associated inflammation and limits adverse developmental programming in mice. PLoS ONE 8, e67791.
61. Hein, S., Arnon, E., Kostin, S., Schonburg, M., Elsasser, A., Polyakova, V., Bauer, E.P., Klovekorn, W.P. & Schaper, J. 2003. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation 107, 984-991.
62. Heslehurst, N., Simpson, H., Ells, L.J., Rankin, J., Wilkinson, J., Lang, R., Brown, T.J. & Summerbell, C.D. 2008. The impact of maternal BMI status on pregnancy outcomes with immediate short-term obstetric resource implications: a meta-analysis. Obes Rev 9, 635-683.
63. Heslehurst, N., Rankin, J., Wilkinson, J.R. & Summerbell, C.D. 2010. A nationally representative study of maternal obesity in England, UK: trends in incidence and demographic inequalities in 619 323 births, 1989-2007. Int J Obes (Lond) 34, 420-428.
64. Hochner, H., Friedlander, Y., Calderon-Margalit, R., Meiner, V., Sagy, Y., Avgil-Tsadok, M., Burger, A., Savitsky, B., Siscovick, D.S. & Manor, O. 2012. Associations of maternal prepregnancy body mass index and gestational weight gain with adult offspring cardiometabolic risk factors: the Jerusalem Perinatal Family Follow-up Study. Circulation 125, 1381-1389.
65. Holemans, K., Caluwaerts, S., Poston, L. & Van Assche, F.A. 2004. Diet-induced obesity in the rat: a model for gestational diabetes mellitus. Am J Obstet Gynecol 190, 858-865.
66. Jonker, S.S., Faber, J.J., Anderson, D.F., Thornburg, K.L., Louey, S. & Giraud, G.D. 2007. Sequential growth of fetal sheep cardiac myocytes in response to simultaneous arterial and venous hypertension. Am J Physiol Regul Integr Comp Physiol 292, R913-R919.
67. Khan, I.Y., Taylor, P.D., Dekou, V., Seed, P.T., Lakasing, L., Graham, D., Dominiczak, A.F., Hanson, M.A. & Poston, L. 2003. Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension 41, 168-175.
68. Khan, I.Y., Dekou, V., Douglas, G., Jensen, R., Hanson, M.A., Poston, L. & Taylor, P.D. 2005. A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol 288, R127-R133.
69. Kim, W.K., Lee, C.Y., Kang, M.S., Kim, M.H., Ryu, Y.H., Bae, K.H., Shin, S.J., Lee, S.C. & Ko, Y. 2008. Effects of leptin on lipid metabolism and gene expression of differentiation-associated growth factors and transcription factors during differentiation and maturation of 3T3-L1 preadipocytes. Endocr J 55, 827-837.
70. Kirk, S.L., Samuelsson, A.M., Argenton, M., Dhonye, H., Kalamatianos, T., Poston, L., Taylor, P.D. & Coen, C.W. 2009. Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLoS ONE 4, e5870.
71. Koutcherov, Y., Mai, J.K., Ashwell, K.W. & Paxinos, G. 2002. Organization of human hypothalamus in fetal development. J Comp Neurol 446, 301-324.
72. Kral, J.G., Biron, S., Simard, S., Hould, F.S., Lebel, S., Marceau, S. & Marceau, P. 2006. Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years. Pediatrics 118, e1644-e1649.
73. Krishnaveni, G.V., Veena, S.R., Hill, J.C., Kehoe, S., Karat, S.C. & Fall, C.H. 2010. Intrauterine exposure to maternal diabetes is associated with higher adiposity and insulin resistance and clustering of cardiovascular risk markers in Indian children. Diabetes Care 33, 402-404.
74. Langley-Evans, S.C. 2013. Fetal programming of CVD and renal disease: animal models and mechanistic considerations. Proc Nutr Soc 72, 317-325.
75. Laura, H.C., Menezes, A.B., Noal, R.B., Hallal, P.C. & Araujo, C.L. 2010. Maternal anthropometric characteristics in pregnancy and blood pressure among adolescents: 1993 live birth cohort, Pelotas, southern Brazil. BMC Public Health 10, 434.
76. Lawlor, D.A., Relton, C., Sattar, N. & Nelson, S.M. 2012. Maternal adiposity-a determinant of perinatal and offspring outcomes? Nat Rev Endocrinol 8, 679-688.
77. Lee, M.J. & Fried, S.K. 2009a. Integration of hormonal and nutrient signals that regulate leptin synthesis and secretion. Am J Physiol Endocrinol Metab 296, E1230-E1238.
78. Lee, M.J. & Fried, S.K. 2009b. Integration of hormonal and nutrient signals that regulate leptin synthesis and secretion. Am J Physiol Endocrinol Metab 292, E858-E864.
79. Lee, M.J., Wang, Y., Ricci, M.R., Sullivan, S., Russell, C.D. & Fried, S.K. 2007. Acute and chronic regulation of leptin synthesis, storage, and secretion by insulin and dexamethasone in human adipose tissue. Am J Physiol Endocrinol Metab 292, E858-E864.
80. Li, L., Fink, G.D., Watts, S.W., Northcott, C.A., Galligan, J.J., Pagano, P.J. & Chen, A.F. 2003. Endothelin-1 increases vascular superoxide via endothelin(A)-NADPH oxidase pathway in low-renin hypertension. Circulation 107, 1053-1058.
81. Louey, S., Jonker, S.S., Giraud, G.D. & Thornburg, K.L. 2007. Placental insufficiency decreases cell cycle activity and terminal maturation in fetal sheep cardiomyocytes. J Physiol 580, 639-648.
82. Mamun, A.A., O'Callaghan, M., Callaway, L., Williams, G., Najman, J. & Lawlor, D.A. 2009. Associations of gestational weight gain with offspring body mass index and blood pressure at 21 years of age: evidence from a birth cohort study. Circulation 119, 1720-1727.
83. Marco, L.J., McCloskey, K., Vuillermin, P.J., Burgner, D., Said, J. & Ponsonby, A.L. 2012. Cardiovascular disease risk in the offspring of diabetic women: the impact of the intrauterine environment. Exp Diabetes Res 2012, 565160.
84. Mark, A.L., Correia, M., Morgan, D.A., Shaffer, R.A. & Haynes, W.G. 1999. State-of-the-art-lecture: obesity-induced hypertension: new concepts from the emerging biology of obesity. Hypertension 33, 537-541.
85. Marsh, A.J., Fontes, M.A., Killinger, S., Pawlak, D.B., Polson, J.W. & Dampney, R.A. 2003. Cardiovascular responses evoked by leptin acting on neurons in the ventromedial and dorsomedial hypothalamus. Hypertension 42, 488-493.
86. Matsuda, J., Yokota, I., Iida, M., Murakami, T., Naito, E., Ito, M., Shima, K. & Kuroda, Y. 1997. Serum leptin concentration in cord blood: relationship to birth weight and gender. J Clin Endocrinol Metab 82, 1642-1644.
87. McMillen, I.C. & Robinson, J.S. 2005. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85, 571-633.
88. Mingrone, G., Manco, M., Mora, M.E., Guidone, C., Iaconelli, A., Gniuli, D., Leccesi, L., Chiellini, C. & Ghirlanda, G. 2008. Influence of maternal obesity on insulin sensitivity and secretion in offspring. Diabetes Care 31, 1872-1876.
89. Morash, B., Wilkinson, D., Murphy, P., Ur, E. & Wilkinson, M. 2001. Developmental regulation of leptin gene expression in rat brain and pituitary. Mol Cell Endocrinol 185, 151-159.
90. Morgan, D.A., Thedens, D.R., Weiss, R. & Rahmouni, K. 2008. Mechanisms mediating renal sympathetic activation to leptin in obesity. Am J Physiol Regul Integr Comp Physiol 295, R1730-R1736.
91. Morris, M.J. & Chen, H. 2009. Established maternal obesity in the rat reprograms hypothalamic appetite regulators and leptin signaling at birth. Int J Obes (Lond) 33, 115-122.
92. Muhlhausler, B.S., Adam, C.L., Marrocco, E.M., Findlay, P.A., Roberts, C.T., McFarlane, J.R., Kauter, K.G. & McMillen, I.C. 2005. Impact of glucose infusion on the structural and functional characteristics of adipose tissue and on hypothalamic gene expression for appetite regulatory neuropeptides in the sheep fetus during late gestation. J Physiol 565, 185-195.
93. Nathanielsz, P.W., Poston, L. & Taylor, P.D. 2007a. In utero exposure to maternal obesity and diabetes: animal models that identify and characterize implications for future health. Obstet Gynecol Clin North Am 34, 201-212, vii-viii.
94. Nathanielsz, P.W., Poston, L. & Taylor, P.D. 2007b. In utero exposure to maternal obesity and diabetes: animal models that identify and characterize implications for future health. Clin Perinatol 34, 515-526, v.
95. Nelson, S.M., Matthews, P. & Poston, L. 2010. Maternal metabolism and obesity: modifiable determinants of pregnancy outcome. Hum Reprod Update 16, 255-275.
96. Nivoit, P., Morens, C., Van Assche, F.A., Jansen, E., Poston, L., Remacle, C. & Reusens, B. 2009. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia 52, 1133-1142.
97. Norman, J.E. & Reynolds, R. 2011. The consequences of obesity and excess weight gain in pregnancy. Proc Nutr Soc 70, 450-456.
98. Ojala, T., Aaltonen, J., Siira, S., Jalonen, J., Ekholm, E., Ekblad, U. & Laitinen, K. 2009. Fetal cardiac sympathetic activation is linked with maternal body mass index. Early Hum Dev 85, 557-560.
99. Ojeda, N.B., Grigore, D. & Alexander, B.T. 2008. Developmental programming of hypertension. insight from animal models of nutritional manipulation. Hypertension 52, 44-50.
100. Oken, E., Rifas-Shiman, S.L., Field, A.E., Frazier, A.L. & Gillman, M.W. 2008. Maternal gestational weight gain and offspring weight in adolescence. Obstet Gynecol 112, 999-1006.
101. Oliver, P., Pico, C., De Matteis, R., Cinti, S. & Palou, A. 2002. Perinatal expression of leptin in rat stomach. Dev Dyn 223, 148-154.
102. O'Reilly, J.R. & Reynolds, R.M. 2013. The risk of maternal obesity to the long-term health of the offspring. Clin Endocrinol (Oxf) 78, 9-16.
103. Ozata, M., Ozdemir, I.C. & Licinio, J. 1999. Human leptin deficiency caused by a missense mutation: multiple endocrine defects, decreased sympathetic tone, and immune system dysfunction indicate new targets for leptin action, greater central than peripheral resistance to the effects of leptin, and spontaneous correction of leptin-mediated defects. J Clin Endocrinol Metab 84, 3686-3695.
104. Plagemann, A. 2006. Perinatal nutrition and hormone-dependent programming of food intake. Horm Res 65(Suppl 3), 83-89.
105. Porrello, E.R., Bell, J.R., Schertzer, J.D., Curl, C.L., McMullen, J.R., Mellor, K.M., Ritchie, R.H., Lynch, G.S., Harrap, S.B., Thomas, W.G. & Delbridge, L.M. 2009. Heritable pathologic cardiac hypertrophy in adulthood is preceded by neonatal cardiac growth restriction. Am J Physiol Regul Integr Comp Physiol 296, R672-R680.
106. Poston, L. 2011. Influence of maternal nutritional status on vascular function in the offspring. Microcirculation 18, 256-262.
107. 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.
108. Poston, L., Harthoorn, L.F. & Van Der Beek, E.M. 2011. Obesity in pregnancy: implications for the mother and lifelong health of the child. A consensus statement. Pediatr Res 69, 175-180.
109. Rahmouni, K. 2010. Sympathetic tone in the young: the mother weighs in. Hypertension 55, 21-22.
110. Rahmouni, K., Haynes, W.G., Morgan, D.A. & Mark, A.L. 2003. Role of melanocortin-4 receptors in mediating renal sympathoactivation to leptin and insulin. J Neurosci 23, 5998-6004.
111. Rahmouni, K., Correia, M.L., Haynes, W.G. & Mark, A.L. 2005. Obesity-associated hypertension: new insights into mechanisms. Hypertension 45, 9-14.
112. Rajani, C.K., Samuelsson, A.M., Clark, J., Shattock, M., Poston, L. & Taylor, P.D. 2009. Developmental programming of myocardial dysfunction arising from maternal obesity in a murine model. J Dev Orig Health Dis 1, S247.
113. Rajapurohitam, V., Gan, X.T., Kirshenbaum, L.A. & Karmazyn, M. 2003. The obesity-associated peptide leptin induces hypertrophy in neonatal rat ventricular myocytes. Circ Res 93, 277-279.
114. Rayner, D.V., Dalgliesh, G.D., Duncan, J.S., Hardie, L.J., Hoggard, N. & Trayhurn, P. 1997. Postnatal development of the ob gene system: elevated leptin levels in suckling fa/fa rats. Am J Physiol 273, R446-R450.
115. Reynolds, R.M., Allan, K.M., Raja, E.A., Bhattacharya, S., McNeill, G., Hannaford, P.C., Sarwar, N., Lee, A.J. & Norman, J.E. 2013. Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. BMJ 347, f4539.
116. Roigas, J., Roigas, C., Heydeck, D. & Papies, B. 1996. Prenatal hypoxia alters the postnatal development of beta-adrenoceptors in the rat myocardium. Biol Neonate 69, 383-388.
117. Roseboom, T.J., van der Meulen, J.H., Ravelli, A.C., Osmond, C., Barker, D.J. & Bleker, O.P. 2001. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol 185, 93-98.
118. Samuelsson, A.M., Matthews, P.A., Argenton, M., Christie, M.R., McConnell, J.M., Jansen, E.H., Piersma, A.H., Ozanne, S.E., Twinn, D.F., Remacle, C., Rowlerson, A., Poston, L. & Taylor, P.D. 2008. 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.
119. Samuelsson, A.M., Morris, A., Igosheva, N., Kirk, S.L., Pombo, J.M., Coen, C.W., Poston, L. & Taylor, P.D. 2010. Evidence for sympathetic origins of hypertension in juvenile offspring of obese rats. Hypertension 55, 76-82.
120. Samuelsson, A.M., Mullier, A., Stepien, A., Patel, K., Pombo, J., Coen, C.W., Poston, L. & Taylor, P.D. 2013a. Central role for melanocortin system in energy balance and blood pressure regulation in offspring of obese dams. IUPS, Abstract.
121. Samuelsson, A.M., Clark, J., Rudyk, O., Shattock, M.J., Baea, S.E., South, T., Pombo, J., Redington, K., Uppal, E., Coen, C.W., Poston, L. & Taylor, P.D. 2013b. Experimental Hyperleptinemia in neonatal rats leads to selective leptin responsiveness, hypertension and altered myocardial function. Hypertension 62, 627-633.
122. Schubring, C., Siebler, T., Kratzsch, J., Englaro, P., Blum, W.F., Triep, K. & Kiess, W. 1999. Leptin serum concentrations in healthy neonates within the first week of life: relation to insulin and growth hormone levels, skinfold thickness, body mass index and weight. Clin Endocrinol (Oxf) 51, 199-204.
123. Shek, E.W., Brands, M.W. & Hall, J.E. 1998. Chronic leptin infusion increases arterial pressure. Hypertension 31, 409-414.
124. Smith, J., Cianflone, K., Biron, S., Hould, F.S., Lebel, S., Marceau, S., Lescelleur, O., Biertho, L., Simard, S., Kral, J.G. & Marceau, P. 2009. Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity. J Clin Endocrinol Metab 94, 4275-4283.
125. Sohn, J.W., Harris, L.E., Berglund, E.D., Liu, T., Vong, L., Lowell, B.B., Balthasar, N., Williams, K.W. & Elmquist, J.K. 2013. Melanocortin 4 receptors reciprocally regulate sympathetic and parasympathetic preganglionic neurons. Cell 152, 612-619.
126. Srinivasan, M., Katewa, S.D., Palaniyappan, A., Pandya, J.D. & Patel, M.S. 2006. Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood. Am J Physiol Endocrinol Metab 291, E792-E799.
127. Stocker, C.J. & Cawthorne, M.A. 2008. The influence of leptin on early life programming of obesity. Trends Biotechnol 26, 545-551.
128. Tajmir, P., Ceddia, R.B., Li, R.K., Coe, I.R. & Sweeney, G. 2004. Leptin increases cardiomyocyte hyperplasia via extracellular signal-regulated kinase- and phosphatidylinositol 3-kinase-dependent signaling pathways. Endocrinology 145, 1550-1555.
129. Tam, W.H., Ma, R.C., Yip, G.W., Yang, X., Li, A.M., Ko, G.T., Lao, T.T. & Chan, J.C. 2012. The association between in utero hyperinsulinemia and adolescent arterial stiffness. Diabetes Res Clin Pract 95, 169-175.
130. Tappia, P.S., Sandhu, H., Abbi, T. & Aroutiounova, N. 2009. Alterations in the expression of myocardial calcium cycling genes in rats fed a low protein diet in utero. Mol Cell Biochem 324, 93-99.
131. Taylor, P.D. & Poston, L. 2007. Developmental programming of obesity in mammals. Exp Physiol 92, 287-298.
132. Taylor, P.D., Khan, I.Y., Lakasing, L., Dekou, V., O'Brien-Coker, I., Mallet, A.I., Hanson, M.A. & Poston, L. 2003. Uterine artery function in pregnant rats fed a diet supplemented with animal lard. Exp Physiol 88, 389-398.
133. Taylor, P.D., Khan, I.Y., Hanson, M.A. & Poston, L. 2004. Impaired EDHF-mediated vasodilatation in adult offspring of rats exposed to a fat-rich diet in pregnancy. J Physiol 558, 943-951.
134. Taylor, P.D., McConnell, J., Khan, I.Y., Holemans, K., Lawrence, K.M., Asare-Anane, H., Persaud, S.J., Jones, P.M., Petrie, L., Hanson, M.A. & Poston, L. 2005. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol 288, R134-R139.
135. Thornburg, K.L. & Louey, S. 2005. Fetal roots of cardiac disease. Heart 91, 867-868.
136. Toste, F.P., de Moura, E.G., Lisboa, P.C., Fagundes, A.T., de Oliveira, E. & Passos, M.C. 2006. Neonatal leptin treatment programmes leptin hypothalamic resistance and intermediary metabolic parameters in adult rats. Br J Nutr 95, 830-837.
137. Trevenzoli, I.H., Valle, M.M., Machado, F.B., Garcia, R.M., Passos, M.C., Lisboa, P.C. & Moura, E.G. 2007. Neonatal hyperleptinaemia programmes adrenal medullary function in adult rats: effects on cardiovascular parameters. J Physiol 580, 629-637.
138. Vickers, M.H., Gluckman, P.D., Coveny, A.H., Hofman, P.L., Cutfield, W.S., Gertler, A., Breier, B.H. & Harris, M. 2005. Neonatal leptin treatment reverses developmental programming. Endocrinology 146, 4211-4216.
139. Vickers, M.H., Gluckman, P.D., Coveny, A.H., Hofman, P.L., Cutfield, W.S., Gertler, A., Breier, B.H. & Harris, M. 2008. The effect of neonatal leptin treatment on postnatal weight gain in male rats is dependent on maternal nutritional status during pregnancy. Endocrinology 149, 1906-1913.
140. Vohr, B.R. & Boney, C.M. 2008. Gestational diabetes: the forerunner for the development of maternal and childhood obesity and metabolic syndrome? J Matern Fetal Neonatal Med 21, 149-157.
141. Wang, J., Ma, H., Tong, C., Zhang, H., Lawlis, G.B., Li, Y., Zang, M., Ren, J., Nijland, M.J., Ford, S.P., Nathanielsz, P.W. & Li, J. 2010. Overnutrition and maternal obesity in sheep pregnancy alter the JNK-IRS-1 signaling cascades and cardiac function in the fetal heart. FASEB J 24, 2066-2076.
142. Ward, K.R., Bardgett, J.F., Wolfgang, L. & Stocker, S.D. 2011. Sympathetic response to insulin is mediated by melanocortin 3/4 receptors in the hypothalamic paraventricular nucleus. Hypertension 57, 435-441.
143. Wen, X., Triche, E.W., Hogan, J.W., Shenassa, E.D. & Buka, S.L. 2011. Prenatal factors for childhood blood pressure mediated by intrauterine and/or childhood growth? Pediatrics 127, e713-e721.
144. West, N.A., Crume, T.L., Maligie, M.A. & Dabelea, D. 2011. Cardiovascular risk factors in children exposed to maternal diabetes in utero. Diabetologia 54, 504-507.
145. West, N.A., Kechris, K. & Dabelea, D. 2013. Exposure to maternal diabetes in utero and DNA methylation patterns in the offspring. Immunometabolism 1, 1-9.
146. Wright, C.S., Rifas-Shiman, S.L., Rich-Edwards, J.W., Taveras, E.M., Gillman, M.W. & Oken, E. 2009. Intrauterine exposure to gestational diabetes, child adiposity, and blood pressure. Am J Hypertens 22, 215-220.
147. Xu, Y., Williams, S.J., O'Brien, D. & Davidge, S.T. 2006. Hypoxia or nutrient restriction during pregnancy in rats leads to progressive cardiac remodeling and impairs postischemic recovery in adult male offspring. FASEB J 20, 1251-1253.
148. Xue, Q. & Zhang, L. 2009. Prenatal hypoxia causes a sex-dependent increase in heart susceptibility to ischemia and reperfusion injury in adult male offspring: role of PKC{epsilon}. J Pharmacol Exp Ther 330, 624-632.
149. Ye, Z.Y. & Li, D.P. 2011. Activation of the melanocortin-4 receptor causes enhanced excitation in presympathetic paraventricular neurons in obese Zucker rats. Regul Pept 166, 112-120.
150. Yli, B.M., Kallen, K., Stray-Pedersen, B. & Amer-Wahlin, I. 2008. Intrapartum fetal ECG and diabetes. J Matern Fetal Neonatal Med 21, 231-238.
151. Yura, S., Itoh, H., Sagawa, N., Yamamoto, H., Masuzaki, H., Nakao, K., Kawamura, M., Takemura, M., Kakui, K., Ogawa, Y. & Fujii, S. 2005. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab 1, 371-378.