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Journal of Pregnancy
Volume 2012, Article ID 134758, 10 pages
http://dx.doi.org/10.1155/2012/134758
Review Article

In Utero Programming of Later Adiposity: The Role of Fetal Growth Restriction

1Department of Obstetrics and Gynaecology, Children's Health Research Institute and Lawson Research Institute, University of Western Ontario, 1151 Richmond Street, London, ON, Canada N6A 5C1
2Dental Science Building, Room 2027, University of Western Ontario, 1151 Richmond Street, London, ON, Canada N6A 5C1

Received 6 April 2012; Accepted 17 October 2012

Academic Editor: Janna Morrison

Copyright © 2012 Ousseynou Sarr et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. World Health Organization, “Obesity and overweight,” Fact Sheet, no. 311, 2011.
  2. S. E. Kahn, R. L. Hull, and K. M. Utzschneider, “Mechanisms linking obesity to insulin resistance and type 2 diabetes,” Nature, vol. 444, no. 7121, pp. 840–846, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. Prospective Studies Collaboration, “Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies,” The Lancet, vol. 373, no. 9669, pp. 1083–1096, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Withrow and D. A. Alter, “The economic burden of obesity worldwide: a systematic review of the direct costs of obesity,” Obesity Reviews, vol. 12, no. 2, pp. 131–141, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Gluckman and M. Hanson, Fat, Fate, and Disease: Why We Are Losing the War against Obesity and Chronic Disease, Oxford University Press, Oxford, UK, 2012.
  6. A. Lucas, “Programming by early nutrition in man,” Ciba Foundation Symposium, vol. 156, pp. 38–50, 1991. View at Google Scholar · View at Scopus
  7. R. A. McCance and E. M. Widdowson, “The determinants of growth and form,” Proceedings of the Royal Society of London B, vol. 185, no. 1078, pp. 1–17, 1974. View at Google Scholar · View at Scopus
  8. M. E. J. Wadsworth, H. A. Cripps, R. E. Midwinter, and J. R. T. Colley, “Blood pressure in a national birth cohort at the age of 36 related to social and familial factors, smoking, and body mass,” British Medical Journal, vol. 291, no. 6508, pp. 1534–1538, 1985. View at Google Scholar · View at Scopus
  9. D. J. P. Barker and C. Osmond, “Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales,” The Lancet, vol. 1, no. 8489, pp. 1077–1081, 1986. View at Google Scholar · View at Scopus
  10. C. N. Hales and D. J. P. Barker, “Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis,” Diabetologia, vol. 35, no. 7, pp. 595–601, 1992. View at Publisher · View at Google Scholar · View at Scopus
  11. D. J. P. Barker, “Fetal growth and adult disease,” British Journal of Obstetrics and Gynaecology, vol. 99, no. 4, pp. 275–276, 1992. View at Google Scholar · View at Scopus
  12. A. C. J. Ravelli, J. H. P. van Der Meulen, C. Osmond, D. J. P. Barker, and O. P. Bleker, “Obesity at the age of 50 y in men and women exposed to famine prenatally,” American Journal of Clinical Nutrition, vol. 70, no. 5, pp. 811–816, 1999. View at Google Scholar · View at Scopus
  13. S. P. Ford, B. W. Hess, M. M. Schwope et al., “Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring,” Journal of Animal Science, vol. 85, no. 5, pp. 1285–1294, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. A. R. Pinheiro, I. D. M. Salvucci, M. B. Aguila, and C. A. Mandarim-De-Lacerda, “Protein restriction during gestation and/or lactation causes adverse transgenerational effects on biometry and glucose metabolism in F1 and F2 progenies of rats,” Clinical Science, vol. 114, no. 5, pp. 381–392, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Bouanane, N. B. Benkalfat, F. Z. Baba Ahmed et al., “Time course of changes in serum oxidant/antioxidant status in overfed obese rats and their offspring,” Clinical Science, vol. 116, no. 8, pp. 669–680, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. R. J. Martin, G. J. Hausman, and D. B. Hausman, “Regulation of adipose cell development in utero,” Proceedings of the Society for Experimental Biology and Medicine, vol. 219, no. 3, pp. 200–210, 1998. View at Google Scholar · View at Scopus
  17. J. S. J. Brooks and P. M. Perosio, “Adipose tissue,” in Histology for Pathologists, S. Mills, Ed., 3rd edition, 2007. View at Google Scholar
  18. V. Large, O. Peroni, D. Letexier, H. Ray, and M. Beylot, “Metabolism of lipids in human white adipocyte,” Diabetes and Metabolism, vol. 30, no. 4, pp. 294–309, 2004. View at Google Scholar · View at Scopus
  19. J. Himms-Hagen, “Brown adipose tissue thermogenesis: interdisciplinary studies,” The FASEB Journal, vol. 4, no. 11, pp. 2890–2898, 1990. View at Google Scholar · View at Scopus
  20. A. L. Albright and J. S. Stern, “Adipose tissue,” in Encyclopedia of Sports Medicine and Science, T. D. Fahey, Ed., Internet Society for Sport Science, 1998, http://sportsci.org/. View at Google Scholar
  21. N. Billon, M. C. Monteiro, and C. Dani, “Developmental origin of adipocytes: new insights into a pending question,” Biology of the Cell, vol. 100, no. 10, pp. 563–575, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Ailhaud, P. Grimaldi, and R. Négrel, “Cellular and molecular aspects of adipose tissue development,” Annual Review of Nutrition, vol. 12, pp. 207–233, 1992. View at Google Scholar · View at Scopus
  23. O. A. MacDougald and M. D. Lane, “Transcriptional regulation of gene expression during adipocyte differentiation,” Annual Review of Biochemistry, vol. 64, pp. 345–373, 1995. View at Google Scholar · View at Scopus
  24. F. M. Gregoire, “Adipocyte differentiation: from fibroblast to endocrine cell,” Experimental Biology and Medicine, vol. 226, no. 11, pp. 997–1002, 2001. View at Google Scholar · View at Scopus
  25. P. Wang, E. Mariman, J. Keijer et al., “Profiling of the secreted proteins during 3T3-L1 adipocyte differentiation leads to the identification of novel adipokines,” Cellular and Molecular Life Sciences, vol. 61, no. 18, pp. 2405–2417, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. M. J. Cartwright, T. Tchkonia, and J. L. Kirkland, “Aging in adipocytes: potential impact of inherent, depot-specific mechanisms,” Experimental Gerontology, vol. 42, no. 6, pp. 463–471, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Koppen and E. Kalkhoven, “Brown vs white adipocytes: the PPARγ coregulator story,” FEBS Letters, vol. 584, no. 15, pp. 3250–3259, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Desai and M. G. Ross, “Fetal programming of adipose tissue: effects of intrauterine growth restriction and maternal obesity/high-fat diet,” Seminars in Reproductive Medicine, vol. 29, no. 3, pp. 237–245, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Klein, S. W. Coppack, V. Mohamed-Ali, and M. Landt, “Adipose tissue leptin production and plasma leptin kinetics in humans,” Diabetes, vol. 45, no. 7, pp. 984–987, 1996. View at Google Scholar · View at Scopus
  30. M. S. Mirza, “Obesity, visceral fat, and NAFLD: querying the role of adipokines in the progression of nonalcoholic fatty liver disease,” ISRN Gastroenterology, vol. 2011, Article ID 592404, 11 pages, 2011. View at Publisher · View at Google Scholar
  31. A. Cook and C. Cowan, Adipose, Stembook, 2009.
  32. N. M. Long, D. C. Rule, M. J. Zhu, P. W. Nathanielsz, and S. P. Ford, “Maternal obesity upregulates fatty acid and glucose transporters and increases expression of enzymes mediating fatty acid biosynthesis in fetal adipose tissue depots,” Journal of Animal Science, vol. 90, no. 7, pp. 2201–2210, 2012. View at Google Scholar
  33. M. E. Symonds, A. Mostyn, S. Pearce, H. Budge, and T. Stephenson, “Endocrine and nutritional regulation of fetal adipose tissue development,” Journal of Endocrinology, vol. 179, no. 3, pp. 293–299, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. M. E. Symonds, M. Pope, D. Sharkey, and H. Budge, “Adipose tissue and fetal programming,” Diabetologia, vol. 55, no. 6, pp. 1597–1606, 2012. View at Google Scholar
  35. S. Cinti, “The adipose organ,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 73, no. 1, pp. 9–15, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. B. A. Afzelius, “Brown adipose tissue: its gross anatomy, histology and cytology,” in Brown Adipose Tissue, O. Lindberg, Ed., pp. 1–31, Elsevier, New York, NY, USA, 1970. View at Google Scholar
  37. C. H. Saely, K. Geiger, and H. Drexel, “Brown versus white adipose tissue: a mini-review,” Gerontology, vol. 58, no. 1, pp. 15–23, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Cinti, “Transdifferentiation properties of adipocytes in the adipose organ,” American Journal of Physiology, vol. 297, no. 5, pp. E977–E986, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Napolitano and D. Fawcett, “The fine structure of brown adipose tissue in the newborn mouse and rat,” The Journal of Biophysical and Biochemical Cytology, vol. 4, no. 6, pp. 685–692, 1958. View at Google Scholar · View at Scopus
  40. D. Hull, “The structure and function of brown adipose tissue,” British Medical Bulletin, vol. 22, no. 1, pp. 92–96, 1966. View at Google Scholar · View at Scopus
  41. M. Borensztein, S. Viengchareun, D. Montarras et al., “Double Myod and Igf2 inactivation promotes brown adipose tissue development by increasing Prdm16 expression,” The FASEB Journal, vol. 26, no. 11, pp. 4584–4591, 2012. View at Publisher · View at Google Scholar
  42. S. Gesta, Y. H. Tseng, and C. R. Kahn, “Developmental origin of fat: tracking obesity to its source,” Cell, vol. 131, no. 2, pp. 242–256, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Seale, S. Kajimura, and B. M. Spiegelman, “Transcriptional control of brown adipocyte development and physiological function-of mice and men,” Genes and Development, vol. 23, no. 7, pp. 788–797, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Atit, S. K. Sgaier, O. A. Mohamed et al., “β-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse,” Developmental Biology, vol. 296, no. 1, pp. 164–176, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. R. J. Merklin, “Growth and distribution of human fetal brown fat,” The Anatomical Record, vol. 178, no. 3, pp. 637–645, 1974. View at Google Scholar · View at Scopus
  46. M. E. Lean and W. P. James, “Brown adipose tissue in man,” in Brown Adipose, P. Trayhurn and D. G. Nicholls, Eds., pp. 339–365, Edward Arnold, London, UK, 1986. View at Google Scholar
  47. J. Nedergaard, T. Bengtsson, and B. Cannon, “Unexpected evidence for active brown adipose tissue in adult humans,” American Journal of Physiology, vol. 293, no. 2, pp. E444–E452, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. A. M. Cypess, S. Lehman, G. Williams et al., “Identification and importance of brown adipose tissue in adult humans,” The New England Journal of Medicine, vol. 360, no. 15, pp. 1509–1517, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. M. E. Symonds, S. Sebert, and H. Budge, “The obesity epidemic: from the environment to epigenetics-not simply a response to dietary manipulation in a thermoneutral environment,” Frontiers in Genetics, vol. 2, article 24, 2011. View at Google Scholar
  50. B. Bjørndal, L. Burri, V. Staalesen, J. Skorve, and R. K. Berge, “Different adipose depots: their role in the development of metabolic syndrome and mitochondrial response to hypolipidemic agents,” Journal of Obesity, vol. 2011, Article ID 490650, 15 pages, 2011. View at Publisher · View at Google Scholar
  51. L. P. Kozak, R. A. Koza, R. Anunciado-Koza, T. Mendoza, and S. Newman, “Inherent plasticity of brown adipogenesis in white fat of mice allows for recovery from effects of post-natal malnutrition,” PLoS One, vol. 7, no. 2, Article ID e30392, 2012. View at Google Scholar
  52. R. T. Gemmell, A. W. Bell, and G. Alexander, “Morphology of adipose cells in lambs at birth and during subsequent transition of brown to white adipose tissue in cold and in warm conditons,” The American Journal of Anatomy, vol. 133, no. 2, pp. 143–164, 1972. View at Google Scholar · View at Scopus
  53. G. Alexander and A. W. Bell, “Quantity and calculated oxygen consumption during summit metabolism of brown adipose tissue in newborn lambs,” Biology of the Neonate, vol. 26, no. 3-4, pp. 214–220, 1975. View at Google Scholar · View at Scopus
  54. C. M. Poissonnet, A. R. Burdi, and F. L. Bookstein, “Growth and development of human adipose tissue during early gestation,” Early Human Development, vol. 8, no. 1, pp. 1–11, 1983. View at Google Scholar · View at Scopus
  55. C. M. Poissonnet, A. R. Burdi, and S. M. Garn, “The chronology of adipose tissue appearance and distribution in the human fetus,” Early Human Development, vol. 10, no. 1-2, pp. 1–11, 1984. View at Google Scholar · View at Scopus
  56. G. J. Hausman and G. B. Thomas, “Enzyme histochemical differentiation of white adipose tissue in the rat,” The American Journal of Anatomy, vol. 169, no. 3, pp. 315–326, 1984. View at Google Scholar · View at Scopus
  57. P. K. Atanassova, “Electron microscopic study of the differentiation of rat white subcutaneous adipocytes in situ,” Folia Medica, vol. 44, no. 4, pp. 45–49, 2002. View at Google Scholar · View at Scopus
  58. F. Desnoyers, “Morphological study of rat perirenal adipose tissue in the formative stage,” Annales de Biologie Animale, Biochimie, Biophysique, vol. 17, no. 5, pp. 787–798, 1977. View at Google Scholar · View at Scopus
  59. G. J. Hausman and R. L. Richardson, “Cellular and vascular development in immature rat adipose tissue,” Journal of Lipid Research, vol. 24, no. 5, pp. 522–532, 1983. View at Google Scholar · View at Scopus
  60. J. O. Nnodim and J. D. Lever, “The pre- and postnatal development and ageing of interscapular brown adipose tissue in the rat,” Anatomy and Embryology, vol. 173, no. 2, pp. 215–223, 1985. View at Google Scholar · View at Scopus
  61. R. E. Sheader and F. J. Zeman, “The enzyme histochemistry of developing brown fat in the fetal rat,” Histochemestry and Cell Biology, vol. 21, no. 2, pp. 147–159, 1970. View at Publisher · View at Google Scholar · View at Scopus
  62. R. J. Merklin, “Growth and distribution of human fetal brown fat,” The Anatomical Record, vol. 178, no. 3, pp. 637–645, 1974. View at Google Scholar · View at Scopus
  63. G. J. Hausman and R. L. Richardson, “Cellular and vascular development in immature rat adipose tissue,” Journal of Lipid Research, vol. 24, no. 5, pp. 522–532, 1983. View at Google Scholar · View at Scopus
  64. L. Casteilla, V. Planat-Benard, P. Laharrague, and B. Cousin, “Adipose-derived stromal cells: their identity and uses in clinical trials, an update,” World Journal of Stem Cells, vol. 3, no. 4, pp. 25–33, 2011. View at Google Scholar
  65. K. L. Spalding, E. Arner, P. O. Westermark et al., “Dynamics of fat cell turnover in humans,” Nature, vol. 453, no. 7196, pp. 783–787, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Hauner, G. Entenmann, M. Wabitsch et al., “Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium,” The Journal of Clinical Investigation, vol. 84, no. 5, pp. 1663–1670, 1989. View at Google Scholar · View at Scopus
  67. M. Maumus, C. Sengenès, P. Decaunes et al., “Evidence of in situ proliferation of adult adipose tissue-derived progenitor cells: influence of fat mass microenvironment and growth,” The Journal of Clinical Endocrinology and Metabolism, vol. 93, no. 10, pp. 4098–4106, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. T. J. Schulz, T. L. Huang, T. T. Tran et al., “Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 1, pp. 143–148, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Alisi, N. Panera, C. Agostoni, and V. Nobili, “Intrauterine growth retardation and nonalcoholic Fatty liver disease in children,” International Journal of Endocrinology, vol. 2011, Article ID 269853, 8 pages, 2011. View at Publisher · View at Google Scholar
  70. P. D. Gluckman, M. A. Hanson, and C. Pinal, “The developmental origins of adult disease,” Maternal and Child Nutrition, vol. 1, no. 3, pp. 130–141, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. M. G. Ross and M. H. Beall, “Adult sequelae of intrauterine growth restriction,” Seminars in Perinatology, vol. 32, no. 3, pp. 213–218, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. S. C. Langley-Evans, “Fetal programming of cardiovascular function through exposure to maternal undernutrition,” Proceedings of the Nutrition Society, vol. 60, no. 4, pp. 505–513, 2001. View at Google Scholar · View at Scopus
  73. E. Zambrano, C. J. Bautista, M. Deás et al., “A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat,” The Journal of Physiology, vol. 571, part 1, pp. 221–230, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. F. Bieswal, M. T. Ahn, B. Reusens et al., “The importance of catch-up growth after early malnutrition for the programming of obesity in male rat,” Obesity, vol. 14, no. 8, pp. 1330–1343, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. V. V. Bol, A. I. Delattre, B. Reusens, M. Raes, and C. Remacle, “Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice,” American Journal of Physiology, vol. 297, no. 2, pp. R291–R299, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. G. M. Sutton, A. V. Centanni, and A. A. Butler, “Protein malnutrition during pregnancy in C57BL/6J mice results in offspring with altered circadian physiology before obesity,” Endocrinology, vol. 151, no. 4, pp. 1570–1580, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. R. M. Anguita, D. M. Sigulem, and A. L. Sawaya, “Intrauterine food restriction is associated with obesity in young rats,” The Journal of Nutrition, vol. 123, no. 8, pp. 1421–1428, 1993. View at Google Scholar · View at Scopus
  78. C. Rehfeldt, B. Stabenow, R. Pfuhl et al., “Effects of limited and excess protein intakes of pregnant gilts on carcass quality and cellular properties of skeletal muscle and subcutaneous adipose tissue in fattening pigs,” Journal of Animal Science, vol. 90, no. 1, pp. 184–196, 2012. View at Google Scholar
  79. K. R. Poore and A. L. Fowden, “The effects of birth weight and postnatal growth patterns on fat depth and plasma leptin concentrations in juvenile and adult pigs,” The Journal of Physiology, vol. 558, part 1, pp. 295–304, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. R. Bauer, B. Walter, P. Brust, F. Füchtner, and U. Zwiener, “Impact of asymmetric intrauterine growth restriction on organ function in newborn piglets,” European Journal of Obstetrics Gynecology and Reproductive Biology, vol. 110, supplement 1, pp. S40–S49, 2003. View at Publisher · View at Google Scholar · View at Scopus
  81. M. J. De Blasio, K. L. Gatford, J. S. Robinson, and J. A. Owens, “Placental restriction of fetal growth reduces size at birth and alters postnatal growth, feeding activity, and adiposity in the young lamb,” American Journal of Physiology, vol. 292, no. 2, pp. R875–R886, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. L. A. Joss-Moore, Y. Wang, M. S. Campbell et al., “Uteroplacental insufficiency increases visceral adiposity and visceral adipose PPARγ2 expression in male rat offspring prior to the onset of obesity,” Early Human Development, vol. 86, no. 3, pp. 179–185, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. M. J. De Blasio, K. L. Gatford, J. S. Robinson, and J. A. Owens, “Placental restriction of fetal growth reduces size at birth and alters postnatal growth, feeding activity, and adiposity in the young lamb,” American Journal of Physiology, vol. 292, no. 2, pp. R875–R886, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Carey Satterfield, K. A. Dunlap, D. H. Keisler, W. Bazer, and G. Wu, “Arginine nutrition and fetal brown adipose tissue development in nutrient-restricted sheep,” Amino Acids, in press. View at Publisher · View at Google Scholar
  85. A. J. Watkins, E. S. Lucas, A. Wilkins, F. R. Cagampang, and T. P. Fleming, “Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age,” PloS One, vol. 6, no. 12, Article ID e28745, 2011. View at Google Scholar
  86. R. M. Anguita, D. M. Sigulem, and A. L. Sawaya, “Intrauterine food restriction is associated with obesity in young rats,” The Journal of Nutrition, vol. 123, no. 8, pp. 1421–1428, 1993. View at Google Scholar · View at Scopus
  87. G. P. Ravelli, Z. A. Stein, and M. W. Susser, “Obesity in young men after famine exposure in utero and early infancy,” The New England Journal of Medicine, vol. 295, no. 7, pp. 349–353, 1976. View at Google Scholar · View at Scopus
  88. R. Valdez, M. A. Athens, G. H. Thompson, B. S. Bradshaw, and M. P. Stern, “Birthweight and adult health outcomes in a biethnic population in the USA,” Diabetologia, vol. 37, no. 6, pp. 624–631, 1994. View at Google Scholar · View at Scopus
  89. B. Muhlhausler and S. R. Smith, “Early-life origins of metabolic dysfunction: role of the adipocyte,” Trends in Endocrinology and Metabolism, vol. 20, no. 2, pp. 51–57, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Desai, H. Guang, M. Ferelli, N. Kallichanda, and R. H. Lane, “Programmed upregulation of adipogenic transcription factors in intrauterine growth-restricted offspring,” Reproductive Sciences, vol. 15, no. 8, pp. 785–796, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. O. Sarr, I. Louveau, C. Kalbe, C. C. Metges, C. Rehfeldt, and F. Gondret, “Prenatal exposure to maternal low or high protein diets induces modest changes in the adipose tissue proteome of newborn piglets,” Journal of Animal Science, vol. 88, no. 5, pp. 1626–1641, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. J. A. Duffield, T. Vuocolo, R. Tellam, B. S. Yuen, B. S. Muhlhausler, and I. C. McMillen, “Placental restriction of fetal growth decreases IGF1 and leptin mRNA expression in the perirenal adipose tissue of late gestation fetal sheep,” American Journal of Physiology, vol. 294, no. 5, pp. R1413–R1419, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. L. Heilbronn, S. R. Smith, and E. Ravussin, “Failure of fat cell proliferation, mitochondrial function and fat oxidation results in ectopic fat storage, insulin resistance and type II diabetes mellitus,” International Journal of Obesity, vol. 28, supplement 4, pp. S12–S21, 2004. View at Publisher · View at Google Scholar · View at Scopus
  94. H. Guan, E. Arany, J. P. van Beek et al., “Adipose tissue gene expression profiling reveals distinct molecular pathways that define visceral adiposity in offspring of maternal protein-restricted rats,” American Journal of Physiology, vol. 288, no. 4, pp. E663–E673, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. P. Guilloteau, R. Zabielski, H. M. Hammon, and C. C. Metges, “Adverse effects of nutritional programming during prenatal and early postnatal life, some aspects of regulation and potential prevention and treatments,” Journal of Physiology and Pharmacology, vol. 60, supplement 3, pp. 17–35, 2009. View at Google Scholar · View at Scopus
  96. R. S. Ahima and J. S. Flier, “Adipose tissue as an endocrine organ,” Trends in Endocrinology and Metabolism, vol. 11, no. 8, pp. 327–332, 2000. View at Publisher · View at Google Scholar · View at Scopus
  97. J. Auwerx and B. Staels, “Leptin,” The Lancet, vol. 351, no. 9104, pp. 737–742, 1998. View at Publisher · View at Google Scholar · View at Scopus
  98. D. Jaquet, A. Gaboriau, P. Czernichow, and C. Levy-Marchal, “Insulin resistance early in adulthood in subjects born with intrauterine growth retardation,” Journal of Clinical Endocrinology and Metabolism, vol. 85, no. 4, pp. 1401–1406, 2000. View at Publisher · View at Google Scholar · View at Scopus
  99. I. Cetin, P. S. Morpurgo, T. Radaelli et al., “Fetal plasma leptin concentrations: relationship with different intrauterine growth patterns from 19 weeks to term,” Pediatric Research, vol. 48, no. 5, pp. 646–651, 2000. View at Google Scholar · View at Scopus
  100. M. Arslan, G. Yazici, A. Erdem, M. Erdem, E. O. Arslan, and O. Himmetoglu, “Endothelin 1 and leptin in the pathophysiology of intrauterine growth restriction,” International Journal of Gynecology and Obstetrics, vol. 84, no. 2, pp. 120–126, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. C. Martínez-Cordero, N. Amador-Licona, J. M. Guízar-Mendoza, J. Hernández-Méndez, and G. Ruelas-Orozco, “Body fat at birth and cord blood levels of insulin, adiponectin, leptin, and insulin-like growth factor-I in small-for-gestational-age infants,” Archives of Medical Research, vol. 37, no. 4, pp. 490–494, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. B. S. Yuen, P. C. Owens, B. S. Muhlhausler et al., “Leptin alters the structural and functional characteristics of adipose tissue before birth,” The FASEB Journal, vol. 17, no. 9, pp. 1102–1104, 2003. View at Google Scholar · View at Scopus
  103. I. C. McMillen and J. S. Robinson, “Developmental origins of the metabolic syndrome: prediction, plasticity, and programming,” Physiological Reviews, vol. 85, no. 2, pp. 571–633, 2005. View at Publisher · View at Google Scholar · View at Scopus
  104. M. H. Vickers, P. D. Gluckman, A. H. Coveny et al., “Neonatal leptin treatment reverses developmental programming,” Endocrinology, vol. 146, no. 10, pp. 4211–4216, 2005. View at Publisher · View at Google Scholar · View at Scopus
  105. L. Attig, J. Djiane, A. Gertler et al., “Study of hypothalamic leptin receptor expression in low-birth-weight piglets and effects of leptin supplementation on neonatal growth and development,” American Journal of Physiology, vol. 295, no. 5, pp. E1117–E1125, 2008. View at Publisher · View at Google Scholar · View at Scopus
  106. A. P. García, M. Palou, J. Sánchez, T. Priego, A. Palou, and C. Picó, “Moderate caloric restriction during gestation in rats alters adipose tissue sympathetic innervation and later adiposity in offspring,” PLoS One, vol. 6, no. 2, Article ID e17313, 2011. View at Publisher · View at Google Scholar · View at Scopus
  107. J. Djiane and L. Attig, “Role of leptin during perinatal metabolic programming and obesity,” Journal of Physiology and Pharmacology, vol. 59, supplement 1, pp. 55–63, 2008. View at Google Scholar · View at Scopus
  108. C. J. Stocker, J. R. S. Arch, and M. A. Cawthorne, “Fetal origins of insulin resistance and obesity,” The Proceedings of the Nutrition Society, vol. 64, no. 2, pp. 143–151, 2005. View at Publisher · View at Google Scholar · View at Scopus
  109. D. I. W. Phillips, “Birth weight and the future development of diabetes a review of the evidence,” Diabetes Care, vol. 21, no. 21, supplement 2, pp. B150–B155, 1998. View at Google Scholar · View at Scopus
  110. M. G. Gnanalingham, A. Mostyn, M. E. Symonds, and T. Stephenson, “Ontogeny and nutritional programming of adiposity in sheep: potential role of glucocorticoid action and uncoupling protein-2,” American Journal of Physiology, vol. 289, no. 5, pp. R1407–R1415, 2005. View at Publisher · View at Google Scholar · View at Scopus
  111. J. R. Seckl, “Glucocorticoids, feto-placental 11β-hydroxysteroid dehydrogenase type 2, and the early life origins of adult disease,” Steroids, vol. 62, no. 1, pp. 89–94, 1997. View at Publisher · View at Google Scholar · View at Scopus
  112. C. R. W. Edwards, P. M. Stewart, D. Burt et al., “Localisation of 11β-hydroxysteroid dehydrogenase—tissue specific protector of the mineralocorticoid receptor,” The Lancet, vol. 2, no. 8618, pp. 986–989, 1988. View at Google Scholar · View at Scopus
  113. A. Bird, “Perceptions of epigenetics,” Nature, vol. 447, no. 7143, pp. 396–398, 2007. View at Publisher · View at Google Scholar · View at Scopus
  114. C. Ling and L. Groop, “Epigenetics: a molecular link between environmental factors and type 2 diabetes,” Diabetes, vol. 58, no. 12, pp. 2718–2725, 2009. View at Publisher · View at Google Scholar · View at Scopus
  115. Y. Seki, L. Williams, P. M. Vuguin, and M. J. Charron, “Minireview: epigenetic programming of diabetes and obesity: animal models,” Endocrinology, vol. 153, no. 3, pp. 1031–1038, 2012. View at Google Scholar
  116. E. W. Tobi, L. H. Lumey, R. P. Talens et al., “DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific,” Human Molecular Genetics, vol. 18, no. 21, pp. 4046–4053, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. C. Church, S. Lee, E. A. L. Bagg et al., “A mouse model for the metabolic effects of the human fat mass and obesity associated FTO gene,” PLoS Genetics, vol. 5, no. 8, Article ID e1000599, 2009. View at Publisher · View at Google Scholar · View at Scopus
  118. S. P. Sébert, M. A. Hyatt, L. L. Y. Chan et al., “Influence of prenatal nutrition and obesity on tissue specific fat mass and obesity-associated (FTO) gene expression,” Reproduction, vol. 139, no. 1, pp. 265–274, 2010. View at Publisher · View at Google Scholar · View at Scopus
  119. L. L. Y. Chan, S. P. Sébert, M. A. Hyatt et al., “Effect of maternal nutrient restriction from early to midgestation on cardiac function and metabolism after adolescent-onset obesity,” American Journal of Physiology, vol. 296, no. 5, pp. R1455–R1463, 2009. View at Publisher · View at Google Scholar · View at Scopus
  120. J. Fischer, L. Koch, C. Emmerling et al., “Inactivation of the Fto gene protects from obesity,” Nature, vol. 458, no. 7240, pp. 894–898, 2009. View at Publisher · View at Google Scholar · View at Scopus