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Physiol. Rev. 85: 571-633, 2005; doi:10.1152/physrev.00053.2003
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Developmental Origins of the Metabolic Syndrome: Prediction, Plasticity, and Programming

I. Caroline Mcmillen and Jeffrey S. Robinson

Discipline of Physiology, School of Molecular and Biomedical Sciences, and Department Obstetrics and Gynaecology, University of Adelaide, Adelaide, Australia

The "fetal" or "early" origins of adult disease hypothesis was originally put forward by David Barker and colleagues and stated that environmental factors, particularly nutrition, act in early life to program the risks for adverse health outcomes in adult life. This hypothesis has been supported by a worldwide series of epidemiological studies that have provided evidence for the association between the perturbation of the early nutritional environment and the major risk factors (hypertension, insulin resistance, and obesity) for cardiovascular disease, diabetes, and the metabolic syndrome in adult life. It is also clear from experimental studies that a range of molecular, cellular, metabolic, neuroendocrine, and physiological adaptations to changes in the early nutritional environment result in a permanent alteration of the developmental pattern of cellular proliferation and differentiation in key tissue and organ systems that result in pathological consequences in adult life. This review focuses on those experimental studies that have investigated the critical windows during which perturbations of the intrauterine environment have major effects, the nature of the epigenetic, structural, and functional adaptive responses which result in a permanent programming of cardiovascular and metabolic function, and the role of the interaction between the pre- and postnatal environment in determining final health outcomes.




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 ReproductionHome page
M G Gnanalingham, P Williams, V Wilson, J Bispham, M A Hyatt, A Pellicano, H Budge, T Stephenson, and M E Symonds
Nutritional manipulation between early to mid-gestation: effects on uncoupling protein-2, glucocorticoid sensitivity, IGF-I receptor and cell proliferation but not apoptosis in the ovine placenta
Reproduction, October 1, 2007; 134(4): 615 - 623.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
J. S. Dyer, C. R. Rosenfeld, J. Rice, M. Rice, and D. S. Hardin
Insulin Resistance in Hispanic Large-for-Gestational-Age Neonates at Birth
J. Clin. Endocrinol. Metab., October 1, 2007; 92(10): 3836 - 3843.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
M. A. Hyatt, H. Budge, D. Walker, T. Stephenson, and M. E. Symonds
Ontogeny and Nutritional Programming of the Hepatic Growth Hormone-Insulin-Like Growth Factor-Prolactin Axis in the Sheep
Endocrinology, October 1, 2007; 148(10): 4754 - 4760.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
N. B. Ojeda, D. Grigore, E. B. Robertson, and B. T. Alexander
Estrogen Protects Against Increased Blood Pressure in Postpubertal Female Growth Restricted Offspring
Hypertension, October 1, 2007; 50(4): 679 - 685.
[Abstract] [Full Text] [PDF]

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 Am J EpidemiolHome page
M. Gamborg, L. Byberg, F. Rasmussen, P. K. Andersen, J. L. Baker, C. Bengtsson, D. Canoy, W. Droyvold, J. G. Eriksson, T. Forsen, et al.
Birth Weight and Systolic Blood Pressure in Adolescence and Adulthood: Meta-Regression Analysis of Sex- and Age-specific Results from 20 Nordic Studies
Am. J. Epidemiol., September 15, 2007; 166(6): 634 - 645.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
M. Ceelen, M. M. van Weissenbruch, J. C. Roos, J. P. W. Vermeiden, F. E. van Leeuwen, and H. A. Delemarre-van de Waal
Body Composition in Children and Adolescents Born after in Vitro Fertilization or Spontaneous Conception
J. Clin. Endocrinol. Metab., September 1, 2007; 92(9): 3417 - 3423.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
J. Ferezou-Viala, A.-F. Roy, C. Serougne, D. Gripois, M. Parquet, V. Bailleux, A. Gertler, B. Delplanque, J. Djiane, M. Riottot, et al.
Long-term consequences of maternal high-fat feeding on hypothalamic leptin sensitivity and diet-induced obesity in the offspring
Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2007; 293(3): R1056 - R1062.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
D. C. Dolinoy, D. Huang, and R. L. Jirtle
Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development
PNAS, August 7, 2007; 104(32): 13056 - 13061.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
O. Khorram, N. Khorram, M. Momeni, G. Han, J. Halem, M. Desai, and M. G. Ross
Maternal undernutrition inhibits angiogenesis in the offspring: a potential mechanism of programmed hypertension
Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2007; 293(2): R745 - R753.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
G. N. Luheshi and C. Rummel
Is programming of weight regulation immune to neonatal inflammation?
Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2007; 293(2): R578 - R580.
[Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
P. D. Gluckman, K. A. Lillycrop, M. H. Vickers, A. B. Pleasants, E. S. Phillips, A. S. Beedle, G. C. Burdge, and M. A. Hanson
Metabolic plasticity during mammalian development is directionally dependent on early nutritional status
PNAS, July 31, 2007; 104(31): 12796 - 12800.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
N. Igosheva, P. D. Taylor, L. Poston, and V. Glover
Prenatal stress in the rat results in increased blood pressure responsiveness to stress and enhanced arterial reactivity to neuropeptide Y in adulthood
J. Physiol., July 15, 2007; 582(2): 665 - 674.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
J. L. Morrison, K. J. Botting, J. L. Dyer, S. J. Williams, K. L. Thornburg, and I. C. McMillen
Restriction of placental function alters heart development in the sheep fetus
Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2007; 293(1): R306 - R313.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
L. A. Cox and P. W. Nathanielsz
Importance of genetic differences in developmental programming: gene by environment interactions in models of maternal dietary restriction
J. Physiol., June 1, 2007; 581(2): 421 - 422.
[Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
A. Erhuma, A. M. Salter, D. V. Sculley, S. C. Langley-Evans, and A. J. Bennett
Prenatal exposure to a low-protein diet programs disordered regulation of lipid metabolism in the aging rat
Am J Physiol Endocrinol Metab, June 1, 2007; 292(6): E1702 - E1714.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
N. M. Thompson, A. M. Norman, S. S. Donkin, R. R. Shankar, M. H. Vickers, J. L. Miles, and B. H. Breier
Prenatal and Postnatal Pathways to Obesity: Different Underlying Mechanisms, Different Metabolic Outcomes
Endocrinology, May 1, 2007; 148(5): 2345 - 2354.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
L. Sedova, O. Seda, L. Kazdova, B. Chylikova, P. Hamet, J. Tremblay, V. Kren, and D. Krenova
Sucrose feeding during pregnancy and lactation elicits distinct metabolic response in offspring of an inbred genetic model of metabolic syndrome
Am J Physiol Endocrinol Metab, May 1, 2007; 292(5): E1318 - E1324.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
S. M. MacLaughlin, S. K. Walker, D. O. Kleemann, J. P. Sibbons, D. N. Tosh, S. Gentili, C. L. Coulter, and I. C. McMillen
Impact of Periconceptional Undernutrition on Adrenal Growth and Adrenal Insulin-Like Growth Factor and Steroidogenic Enzyme Expression in the Sheep Fetus during Early Pregnancy
Endocrinology, April 1, 2007; 148(4): 1911 - 1920.
[Abstract] [Full Text] [PDF]

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 J. Nutr.Home page
E. Lebenthal and D. M. Bier
Novel Concepts in the Developmental Origins of Adult Health and Disease
J. Nutr., April 1, 2007; 137(4): 1073 - 1075.
[Full Text] [PDF]

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 J. Physiol.Home page
M. G. Frasch, T. Muller, C. Wicher, C. Weiss, M. Lohle, K. Schwab, H. Schubert, P. W. Nathanielsz, O. W. Witte, and M. Schwab
Fetal body weight and the development of the control of the cardiovascular system in fetal sheep
J. Physiol., March 15, 2007; 579(3): 893 - 907.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
A. M. Nuyt and M. Szyf
Developmental Programming Through Epigenetic Changes
Circ. Res., March 2, 2007; 100(4): 452 - 455.
[Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
G. Cambonie, B. Comte, C. Yzydorczyk, T. Ntimbane, N. Germain, N. L. O. Le, P. Pladys, C. Gauthier, I. Lahaie, D. Abran, et al.
Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet
Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2007; 292(3): R1236 - R1245.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
B. N. Van Vliet and L. L. Chafe
Maternal Endothelial Nitric Oxide Synthase Genotype Influences Offspring Blood Pressure and Activity in Mice
Hypertension, March 1, 2007; 49(3): 556 - 562.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
N. B. Ojeda, D. Grigore, L. L. Yanes, R. Iliescu, E. B. Robertson, H. Zhang, and B. T. Alexander
Testosterone contributes to marked elevations in mean arterial pressure in adult male intrauterine growth restricted offspring
Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2007; 292(2): R758 - R763.
[Abstract] [Full Text] [PDF]

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 Reproductive SciencesHome page
O. Khorram, M. Momeni, M. Desai, and M. G. Ross
Nutrient Restriction In Utero Induces Remodeling of the Vascular Extracellular Matrix in Rat Offspring
Reproductive Sciences, January 1, 2007; 14(1): 73 - 80.
[Abstract] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
H. Dickinson, D. W. Walker, E. M. Wintour, and K. Moritz
Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse
Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2007; 292(1): R453 - R461.
[Abstract] [Full Text] [PDF]

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 PediatricsHome page
E. Landmann, F. Geller, J. Schilling, S. Rudloff, E. Foeller-Gaudier, and L. Gortner
Absence of the Wild-type Allele (192 Base Pairs) of a Polymorphism in the Promoter Region of the IGF-I Gene but Not a Polymorphism in the Insulin Gene Variable Number of Tandem Repeat Locus Is Associated With Accelerated Weight Gain in Infancy
Pediatrics, December 1, 2006; 118(6): 2374 - 2379.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
G. Iniguez, K. Ong, R. Bazaes, A. Avila, T. Salazar, D. Dunger, and V. Mericq
Longitudinal Changes in Insulin-Like Growth Factor-I, Insulin Sensitivity, and Secretion from Birth to Age Three Years in Small-for-Gestational-Age Children
J. Clin. Endocrinol. Metab., November 1, 2006; 91(11): 4645 - 4649.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
F. Rahnama, F. Shafiei, P. D. Gluckman, M. D. Mitchell, and P. E. Lobie
Epigenetic Regulation of Human Trophoblastic Cell Migration and Invasion
Endocrinology, November 1, 2006; 147(11): 5275 - 5283.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
C. Thone-Reineke, P. Kalk, M. Dorn, S. Klaus, K. Simon, T. Pfab, M. Godes, P. Persson, T. Unger, and B. Hocher
High-protein nutrition during pregnancy and lactation programs blood pressure, food efficiency, and body weight of the offspring in a sex-dependent manner
Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2006; 291(4): R1025 - R1030.
[Abstract] [Full Text] [PDF]


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