In utero programming of later adiposity: The role of fetal growth restriction

Journal of Pregnancy

Volumn 2012, Issue , 2012, Pages

  Sarr, Ousseynou ^a   Yang, Kaiping ^a   Regnault, Timothy R H ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER;

ADIPOSE TISSUE; FEMALE; GENETIC EPIGENESIS; GENETICS; HUMAN; INTRAUTERINE GROWTH RETARDATION; METABOLISM; OBESITY; PREGNANCY; PRENATAL DEVELOPMENT; PRENATAL EXPOSURE; REVIEW;

ADIPOSE TISSUE; ADIPOSITY; BIOLOGICAL MARKERS; EPIGENESIS, GENETIC; FEMALE; FETAL GROWTH RETARDATION; HUMANS; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84871828168     PISSN: 20902727     EISSN: 20902735     Source Type: Journal    
DOI: 10.1155/2012/134758     Document Type: Review

References (120)

1. World Health Organization, Obesity and overweight. Fact Sheet, no. 311, 2011
2. Kahn S. E., Hull R. L., Utzschneider K. M., Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006 444 7121 840 846 2-s2.0-33845881411 10.1038/nature05482 (Pubitemid 46024990)
3. Prospective Studies Collaboration, Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies. The Lancet 2009 373 9669 1083 1096 2-s2.0-62849107573 10.1016/S0140-6736(09) 60318-4
4. Withrow D., Alter D. A., The economic burden of obesity worldwide: a systematic review of the direct costs of obesity. Obesity Reviews 2011 12 2 131 141 2-s2.0-78851468865 10.1111/j.1467-789X.2009.00712.x
5. Gluckman P., Hanson M., Fat, Fate, and Disease: Why We Are Losing the War against Obesity and Chronic Disease 2012 Oxford, UK Oxford University Press
6. Lucas A., Programming by early nutrition in man. Ciba Foundation Symposium 1991 156 38 50 2-s2.0-0026091454
7. McCance R. A., Widdowson E. M., The determinants of growth and form. Proceedings of the Royal Society of London B 1974 185 1078 1 17 2-s2.0-0015991274
8. Wadsworth M. E. J., Cripps H. A., Midwinter R. E., Colley J. R. T., 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 1985 291 6508 1534 1538 2-s2.0-0022395463 (Pubitemid 16183916)
9. Barker D. J. P., Osmond C., Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. The Lancet 1986 1 8489 1077 1081 2-s2.0-0022621648 (Pubitemid 16106274)
10. Hales C. N., Barker D. J. P., Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 1992 35 7 595 601 2-s2.0-0026772772 10.1007/BF00400248
11. Barker D. J. P., Fetal growth and adult disease. British Journal of Obstetrics and Gynaecology 1992 99 4 275 276 2-s2.0-0026579314
12. Ravelli A. C. J., van Der Meulen J. H. P., Osmond C., Barker D. J. P., Bleker O. P., Obesity at the age of 50 y in men and women exposed to famine prenatally. American Journal of Clinical Nutrition 1999 70 5 811 816 2-s2.0-0032716565 (Pubitemid 29512905)
13. Ford S. P., Hess B. W., Schwope M. M., Nijland M. J., Gilbert J. S., Vonnahme K. A., Means W. J., Han H., Nathanielsz P. W., 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 2007 85 5 1285 1294 2-s2.0-34247884283 10.2527/jas.2005-624 (Pubitemid 46693428)
14. Pinheiro A. R., Salvucci I. D. M., Aguila M. B., Mandarim-De-Lacerda C. A., 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 2008 114 5 381 392 2-s2.0-39549121310 10.1042/CS20070302 (Pubitemid 351397387)
15. Bouanane S., Benkalfat N. B., Baba Ahmed F. Z., Merzouk H., Mokhtari N. S., Merzouk S. A., Gresti J., Tessier C., Narce M., Time course of changes in serum oxidant/antioxidant status in overfed obese rats and their offspring. Clinical Science 2009 116 8 669 680 2-s2.0-66949170327 10.1042/CS20080413
16. Martin R. J., Hausman G. J., Hausman D. B., Regulation of adipose cell development in utero. Proceedings of the Society for Experimental Biology and Medicine 1998 219 3 200 210 2-s2.0-0031754812
17. Brooks J. S. J., Perosio P. M., Mills S., Adipose tissue. Histology for Pathologists 2007 3rd
18. Large V., Peroni O., Letexier D., Ray H., Beylot M., Metabolism of lipids in human white adipocyte. Diabetes and Metabolism 2004 30 4 294 309 2-s2.0-4644356398 (Pubitemid 39280228)
19. Himms-Hagen J., Brown adipose tissue thermogenesis: interdisciplinary studies. The FASEB Journal 1990 4 11 2890 2898 2-s2.0-0025260137 (Pubitemid 120012535)
20. Albright A. L., Stern J. S., Fahey T. D., Adipose tissue. Encyclopedia of Sports Medicine and Science 1998 Internet Society for Sport Science. http://sportsci.org/
21. Billon N., Monteiro M. C., Dani C., Developmental origin of adipocytes: new insights into a pending question. Biology of the Cell 2008 100 10 563 575 2-s2.0-53349160483 10.1042/BC20080011
22. Ailhaud G., Grimaldi P., Négrel R., Cellular and molecular aspects of adipose tissue development. Annual Review of Nutrition 1992 12 207 233 2-s2.0-0026635508
23. MacDougald O. A., Lane M. D., Transcriptional regulation of gene expression during adipocyte differentiation. Annual Review of Biochemistry 1995 64 345 373 2-s2.0-0029062839
24. Gregoire F. M., Adipocyte differentiation: from fibroblast to endocrine cell. Experimental Biology and Medicine 2001 226 11 997 1002 2-s2.0-0035758094
25. Wang P., Mariman E., Keijer J., Bouwman F., Noben J. P., Robben J., Renes J., Profiling of the secreted proteins during 3T3-L1 adipocyte differentiation leads to the identification of novel adipokines. Cellular and Molecular Life Sciences 2004 61 18 2405 2417 2-s2.0-6044259083 10.1007/s00018-004-4256-z (Pubitemid 39382030)
26. Cartwright M. J., Tchkonia T., Kirkland J. L., Aging in adipocytes: potential impact of inherent, depot-specific mechanisms. Experimental Gerontology 2007 42 6 463 471 2-s2.0-34248550944 10.1016/j.exger.2007.03.003 (Pubitemid 46756096)
27. Koppen A., Kalkhoven E., Brown vs white adipocytes: the PPAR γ coregulator story. FEBS Letters 2010 584 15 3250 3259 2-s2.0-77955266460 10.1016/j.febslet.2010.06.035
28. Desai M., Ross M. G., Fetal programming of adipose tissue: effects of intrauterine growth restriction and maternal obesity/high-fat diet. Seminars in Reproductive Medicine 2011 29 3 237 245 2-s2.0-79959785542 10.1055/s-0031- 1275517
29. Klein S., Coppack S. W., Mohamed-Ali V., Landt M., Adipose tissue leptin production and plasma leptin kinetics in humans. Diabetes 1996 45 7 984 987 2-s2.0-0029974877 (Pubitemid 26225518)
30. Mirza M. S., Obesity, visceral fat, and NAFLD: querying the role of adipokines in the progression of nonalcoholic fatty liver disease. ISRN Gastroenterology 2011 2011 11 592404 10.5402/2011/592404
31. Cook A., Cowan C., Adipose 2009 Stembook
32. Long N. M., Rule D. C., Zhu M. J., Nathanielsz P. W., Ford S. P., 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 2012 90 7 2201 2210
33. Symonds M. E., Mostyn A., Pearce S., Budge H., Stephenson T., Endocrine and nutritional regulation of fetal adipose tissue development. Journal of Endocrinology 2003 179 3 293 299 2-s2.0-0346656883 10.1677/joe.0.1790293 (Pubitemid 38072082)
34. Symonds M. E., Pope M., Sharkey D., Budge H., Adipose tissue and fetal programming. Diabetologia 2012 55 6 1597 1606
35. Cinti S., The adipose organ. Prostaglandins Leukotrienes and Essential Fatty Acids 2005 73 1 9 15 2-s2.0-20444501459 10.1016/j.plefa.2005.04.010 (Pubitemid 40826923)
36. Afzelius B. A., Lindberg O., Brown adipose tissue: its gross anatomy, histology and cytology. Brown Adipose Tissue 1970 New York, NY, USA Elsevier 1 31
37. Saely C. H., Geiger K., Drexel H., Brown versus white adipose tissue: a mini-review. Gerontology 2012 58 1 15 23 2-s2.0-78649688847 10.1159/000321319
38. Cinti S., Transdifferentiation properties of adipocytes in the adipose organ. American Journal of Physiology 2009 297 5 E977 E986 2-s2.0-70350443275 10.1152/ajpendo.00183.2009
39. Napolitano L., Fawcett D., The fine structure of brown adipose tissue in the newborn mouse and rat. The Journal of Biophysical and Biochemical Cytology 1958 4 6 685 692 2-s2.0-0011964603
40. Hull D., The structure and function of brown adipose tissue. British Medical Bulletin 1966 22 1 92 96 2-s2.0-0013865726
41. Borensztein M., Viengchareun S., Montarras D., Journot L., Binart N., Lombès M., Dandolo L., Double Myod and Igf2 inactivation promotes brown adipose tissue development by increasing Prdm16 expression. The FASEB Journal 2012 26 11 4584 4591 10.1096/fj.12-208496
42. Gesta S., Tseng Y. H., Kahn C. R., Developmental origin of fat: tracking obesity to its source. Cell 2007 131 2 242 256 2-s2.0-35348874911 10.1016/j.cell.2007.10.004 (Pubitemid 47576146)
43. Seale P., Kajimura S., Spiegelman B. M., Transcriptional control of brown adipocyte development and physiological function-of mice and men. Genes and Development 2009 23 7 788 797 2-s2.0-64349121056 10.1101/gad.1779209
44. Atit R., Sgaier S. K., Mohamed O. A., Taketo M. M., Dufort D., Joyner A. L., Niswander L., Conlon R. A., β -catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Developmental Biology 2006 296 1 164 176 2-s2.0-33745966038 10.1016/j.ydbio.2006.04.449 (Pubitemid 44061762)
45. Merklin R. J., Growth and distribution of human fetal brown fat. The Anatomical Record 1974 178 3 637 645 2-s2.0-0016042975
46. Lean M. E., James W. P., Trayhurn P., Nicholls D. G., Brown adipose tissue in man. Brown Adipose 1986 London, UK Edward Arnold 339 365
47. Nedergaard J., Bengtsson T., Cannon B., Unexpected evidence for active brown adipose tissue in adult humans. American Journal of Physiology 2007 293 2 E444 E452 2-s2.0-34547631960 10.1152/ajpendo.00691.2006 (Pubitemid 47205086)
48. Cypess A. M., Lehman S., Williams G., Tal I., Rodman D., Goldfine A. B., Kuo F. C., Palmer E. L., Tseng Y. H., Doria A., Kolodny G. M., Kahn C. R., Identification and importance of brown adipose tissue in adult humans. The New England Journal of Medicine 2009 360 15 1509 1517 2-s2.0-64349105205 10.1056/NEJMoa0810780
49. Symonds M. E., Sebert S., Budge H., The obesity epidemic: from the environment to epigenetics-not simply a response to dietary manipulation in a thermoneutral environment. Frontiers in Genetics 2011 2, article 24
50. Bjørndal B., Burri L., Staalesen V., Skorve J., Berge R. K., Different adipose depots: their role in the development of metabolic syndrome and mitochondrial response to hypolipidemic agents. Journal of Obesity 2011 2011 15 490650 10.1155/2011/490650
51. Kozak L. P., Koza R. A., Anunciado-Koza R., Mendoza T., Newman S., Inherent plasticity of brown adipogenesis in white fat of mice allows for recovery from effects of post-natal malnutrition. PLoS One 2012 7 2 e30392
52. Gemmell R. T., Bell A. W., Alexander G., 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 1972 133 2 143 164 2-s2.0-0015292861
53. Alexander G., Bell A. W., Quantity and calculated oxygen consumption during summit metabolism of brown adipose tissue in newborn lambs. Biology of the Neonate 1975 26 3-4 214 220 2-s2.0-0016820751
54. Poissonnet C. M., Burdi A. R., Bookstein F. L., Growth and development of human adipose tissue during early gestation. Early Human Development 1983 8 1 1 11 2-s2.0-0020527898 (Pubitemid 13110477)
55. Poissonnet C. M., Burdi A. R., Garn S. M., The chronology of adipose tissue appearance and distribution in the human fetus. Early Human Development 1984 10 1-2 1 11 2-s2.0-0021136715 (Pubitemid 14002132)
56. Hausman G. J., Thomas G. B., Enzyme histochemical differentiation of white adipose tissue in the rat. The American Journal of Anatomy 1984 169 3 315 326 2-s2.0-0021354436 (Pubitemid 14160758)
57. Atanassova P. K., Electron microscopic study of the differentiation of rat white subcutaneous adipocytes in situ. Folia Medica 2002 44 4 45 49 2-s2.0-0037637434
58. Desnoyers F., Morphological study of rat perirenal adipose tissue in the formative stage. Annales de Biologie Animale, Biochimie, Biophysique 1977 17 5 787 798 2-s2.0-0017761587 (Pubitemid 8221468)
59. Hausman G. J., Richardson R. L., Cellular and vascular development in immature rat adipose tissue. Journal of Lipid Research 1983 24 5 522 532 2-s2.0-0020955532 (Pubitemid 13059188)
60. Nnodim J. O., Lever J. D., The pre- and postnatal development and ageing of interscapular brown adipose tissue in the rat. Anatomy and Embryology 1985 173 2 215 223 2-s2.0-0022380743 (Pubitemid 16182628)
61. Sheader R. E., Zeman F. J., The enzyme histochemistry of developing brown fat in the fetal rat. Histochemestry and Cell Biology 1970 21 2 147 159 2-s2.0-0014703044 10.1007/BF00306182
62. Merklin R. J., Growth and distribution of human fetal brown fat. The Anatomical Record 1974 178 3 637 645 2-s2.0-0016042975
63. Hausman G. J., Richardson R. L., Cellular and vascular development in immature rat adipose tissue. Journal of Lipid Research 1983 24 5 522 532 2-s2.0-0020955532 (Pubitemid 13059188)
64. Casteilla L., Planat-Benard V., Laharrague P., Cousin B., Adipose-derived stromal cells: their identity and uses in clinical trials, an update. World Journal of Stem Cells 2011 3 4 25 33
65. Spalding K. L., Arner E., Westermark P. O., Bernard S., Buchholz B. A., Bergmann O., Blomqvist L., Hoffstedt J., Näslund E., Britton T., Concha H., Hassan M., Rydén M., Frisén J., Arner P., Dynamics of fat cell turnover in humans. Nature 2008 453 7196 783 787 2-s2.0-44849132591 10.1038/nature06902 (Pubitemid 351793777)
66. Hauner H., Entenmann G., Wabitsch M., Gaillard D., Ailhaud G., Negrel R., Pfeiffer E. F., Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. The Journal of Clinical Investigation 1989 84 5 1663 1670 2-s2.0-0024440502 (Pubitemid 19272257)
67. Maumus M., Sengenès C., Decaunes P., Zakaroff-Girard A., Bourlier V., Lafontan M., Galitzky J., Bouloumie A., 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 2008 93 10 4098 4106 2-s2.0-53749087651 10.1210/jc.2008-0044
68. Schulz T. J., Huang T. L., Tran T. T., Zhang H., Townsend K. L., Shadrach J. L., Cerletti M., McDougall L. E., Giorgadze N., Tchkonia T., Schrier D., Falb D., Kirkland J. L., Wagers A. J., Tseng Y. H., 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 2011 108 1 143 148 2-s2.0-78651094465 10.1073/pnas.1010929108
69. Alisi A., Panera N., Agostoni C., Nobili V., Intrauterine growth retardation and nonalcoholic Fatty liver disease in children. International Journal of Endocrinology 2011 2011 8 269853 10.1155/2011/269853
70. Gluckman P. D., Hanson M. A., Pinal C., The developmental origins of adult disease. Maternal and Child Nutrition 2005 1 3 130 141 2-s2.0-28244472326 10.1111/j.1740-8709.2005.00020.x (Pubitemid 41702541)
71. Ross M. G., Beall M. H., Adult sequelae of intrauterine growth restriction. Seminars in Perinatology 2008 32 3 213 218 2-s2.0-43049179429 10.1053/j.semperi.2007.11.005 (Pubitemid 351636319)
72. Langley-Evans S. C., Fetal programming of cardiovascular function through exposure to maternal undernutrition. Proceedings of the Nutrition Society 2001 60 4 505 513 2-s2.0-0035663647 (Pubitemid 34016764)
73. Zambrano E., Bautista C. J., Deás M., Martínez-Samayoa P. M., González-Zamorano M., Ledesma H., Morales J., Larrea F., Nathanielsz P. W., 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 2006 571, part 1 221 230 2-s2.0-33645282282 10.1113/jphysiol.2005.100313
74. Bieswal F., Ahn M. T., Reusens B., Holvoet P., Raes M., Rees W. D., Remacle C., The importance of catch-up growth after early malnutrition for the programming of obesity in male rat. Obesity 2006 14 8 1330 1343 2-s2.0-33750597519 10.1038/oby.2006.151 (Pubitemid 46219658)
75. Bol V. V., Delattre A. I., Reusens B., Raes M., Remacle C., 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 2009 297 2 R291 R299 2-s2.0-68049086900 10.1152/ajpregu.90497.2008
76. Sutton G. M., Centanni A. V., Butler A. A., Protein malnutrition during pregnancy in C57BL/6J mice results in offspring with altered circadian physiology before obesity. Endocrinology 2010 151 4 1570 1580 2-s2.0-77950250922 10.1210/en.2009-1133
77. Anguita R. M., Sigulem D. M., Sawaya A. L., Intrauterine food restriction is associated with obesity in young rats. The Journal of Nutrition 1993 123 8 1421 1428 2-s2.0-0027326022 (Pubitemid 23235718)
78. Rehfeldt C., Stabenow B., Pfuhl R., Block J., Nürnberg G., Otten W., Metges C. C., Kalbe C., 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 2012 90 1 184 196
79. Poore K. R., Fowden A. L., 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 2004 558, part 1 295 304 2-s2.0-4043109047 10.1113/jphysiol.2004.061390 (Pubitemid 39077409)
80. Bauer R., Walter B., Brust P., Füchtner F., Zwiener U., Impact of asymmetric intrauterine growth restriction on organ function in newborn piglets. European Journal of Obstetrics Gynecology and Reproductive Biology 2003 110 supplement 1 S40 S49 2-s2.0-0042836801 10.1016/S0301-2115(03)00171-4 (Pubitemid 37072139)
81. De Blasio M. J., Gatford K. L., Robinson J. S., Owens J. A., 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 2007 292 2 R875 R886 2-s2.0-33846781645 10.1152/ajpregu.00430.2006 (Pubitemid 46207743)
82. Joss-Moore L. A., Wang Y., Campbell M. S., Moore B., Yu X., Callaway C. W., McKnight R. A., Desai M., Moyer-Mileur L. J., Lane R. H., Uteroplacental insufficiency increases visceral adiposity and visceral adipose PPAR γ 2 expression in male rat offspring prior to the onset of obesity. Early Human Development 2010 86 3 179 185 2-s2.0-77950342029 10.1016/j.earlhumdev.2010.02. 006
83. De Blasio M. J., Gatford K. L., Robinson J. S., Owens J. A., 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 2007 292 2 R875 R886 2-s2.0-33846781645 10.1152/ajpregu.00430.2006 (Pubitemid 46207743)
84. Carey Satterfield M., Dunlap K. A., Keisler D. H., Bazer W., Wu G., Arginine nutrition and fetal brown adipose tissue development in nutrient-restricted sheep. Amino Acids, in press 10.1007/s00726-011-1168-8
85. Watkins A. J., Lucas E. S., Wilkins A., Cagampang F. R., Fleming T. P., Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age. PloS One 2011 6 12 e28745
86. Anguita R. M., Sigulem D. M., Sawaya A. L., Intrauterine food restriction is associated with obesity in young rats. The Journal of Nutrition 1993 123 8 1421 1428 2-s2.0-0027326022 (Pubitemid 23235718)
87. Ravelli G. P., Stein Z. A., Susser M. W., Obesity in young men after famine exposure in utero and early infancy. The New England Journal of Medicine 1976 295 7 349 353 2-s2.0-0017305263
88. Valdez R., Athens M. A., Thompson G. H., Bradshaw B. S., Stern M. P., Birthweight and adult health outcomes in a biethnic population in the USA. Diabetologia 1994 37 6 624 631 2-s2.0-0028337093 (Pubitemid 24162436)
89. Muhlhausler B., Smith S. R., Early-life origins of metabolic dysfunction: role of the adipocyte. Trends in Endocrinology and Metabolism 2009 20 2 51 57 2-s2.0-63749129833 10.1016/j.tem.2008.10.006
90. Desai M., Guang H., Ferelli M., Kallichanda N., Lane R. H., Programmed upregulation of adipogenic transcription factors in intrauterine growth-restricted offspring. Reproductive Sciences 2008 15 8 785 796 2-s2.0-54349128127 10.1177/1933719108318597
91. Sarr O., Louveau I., Kalbe C., Metges C. C., Rehfeldt C., Gondret F., Prenatal exposure to maternal low or high protein diets induces modest changes in the adipose tissue proteome of newborn piglets. Journal of Animal Science 2010 88 5 1626 1641 2-s2.0-77951103164 10.2527/jas.2009-2542
92. Duffield J. A., Vuocolo T., Tellam R., Yuen B. S., Muhlhausler B. S., McMillen I. C., 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 2008 294 5 R1413 R1419 2-s2.0-45549108351 10.1152/ajpregu.00787.2007
93. Heilbronn L., Smith S. R., Ravussin E., 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 2004 28 supplement 4 S12 S21 2-s2.0-12444296524 10.1038/sj.ijo. 0802853 (Pubitemid 40143844)
94. Guan H., Arany E., van Beek J. P., Chamson-Reig A., Thyssen S., Hill D. J., Yang K., Adipose tissue gene expression profiling reveals distinct molecular pathways that define visceral adiposity in offspring of maternal protein-restricted rats. American Journal of Physiology 2005 288 4 E663 E673 2-s2.0-15444372088 10.1152/ajpendo.00461.2004 (Pubitemid 40397200)
95. Guilloteau P., Zabielski R., Hammon H. M., Metges C. C., 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 2009 60 supplement 3 17 35 2-s2.0-74549181276
96. Ahima R. S., Flier J. S., Adipose tissue as an endocrine organ. Trends in Endocrinology and Metabolism 2000 11 8 327 332 2-s2.0-0033789518 10.1016/S1043-2760(00)00301-5
97. Auwerx J., Staels B., Leptin. The Lancet 1998 351 9104 737 742 2-s2.0-0032492453 10.1016/S0140-6736(97)06348-4 (Pubitemid 28106955)
98. Jaquet D., Gaboriau A., Czernichow P., Levy-Marchal C., Insulin resistance early in adulthood in subjects born with intrauterine growth retardation. Journal of Clinical Endocrinology and Metabolism 2000 85 4 1401 1406 2-s2.0-0034456325 10.1210/jc.85.4.1401 (Pubitemid 32289480)
99. Cetin I., Morpurgo P. S., Radaelli T., Taricco E., Cortelazzi D., Bellotti M., Pardi G., Beck-Peccoz P., Fetal plasma leptin concentrations: relationship with different intrauterine growth patterns from 19 weeks to term. Pediatric Research 2000 48 5 646 651 2-s2.0-0033762191
100. Arslan M., Yazici G., Erdem A., Erdem M., Arslan E. O., Himmetoglu O., Endothelin 1 and leptin in the pathophysiology of intrauterine growth restriction. International Journal of Gynecology and Obstetrics 2004 84 2 120 126 2-s2.0-1142285561 10.1016/S0020-7292(03)00332-1 (Pubitemid 38210004)
101. Martínez-Cordero C., Amador-Licona N., Guízar-Mendoza J. M., Hernández-Méndez J., Ruelas-Orozco G., 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 2006 37 4 490 494 2-s2.0-33646061633 10.1016/j.arcmed.2005.11.004
102. Yuen B. S., Owens P. C., Muhlhausler B. S., Roberts C. T., Symonds M. E., Keisler D. H., McFarlane J. R., Kauter K. G., Evens Y., McMillen I. C., Leptin alters the structural and functional characteristics of adipose tissue before birth. The FASEB Journal 2003 17 9 1102 1104 2-s2.0-0038042210
103. McMillen I. C., Robinson J. S., Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiological Reviews 2005 85 2 571 633 2-s2.0-15544369982 10.1152/physrev.00053.2003 (Pubitemid 40404637)
104. Vickers M. H., Gluckman P. D., Coveny A. H., Hofman P. L., Cutfield W. S., Gertler A., Breier B. H., Harris M., Neonatal leptin treatment reverses developmental programming. Endocrinology 2005 146 10 4211 4216 2-s2.0-24944471310 10.1210/en.2005-0581 (Pubitemid 41324016)
105. Attig L., Djiane J., Gertler A., Rampin O., Larcher T., Boukthir S., Anton P. M., Madec J. Y., Gourdou I., Abdennebi-Najar L., 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 2008 295 5 E1117 E1125 2-s2.0-57049121154 10.1152/ajpendo.90542.2008
106. García A. P., Palou M., Sánchez J., Priego T., Palou A., Picó C., Moderate caloric restriction during gestation in rats alters adipose tissue sympathetic innervation and later adiposity in offspring. PLoS One 2011 6 2 2-s2.0-79951965635 10.1371/journal.pone.0017313 e17313
107. Djiane J., Attig L., Role of leptin during perinatal metabolic programming and obesity. Journal of Physiology and Pharmacology 2008 59 supplement 1 55 63 2-s2.0-51349169455
108. Stocker C. J., Arch J. R. S., Cawthorne M. A., Fetal origins of insulin resistance and obesity. The Proceedings of the Nutrition Society 2005 64 2 143 151 2-s2.0-20444453990 10.1079/PNS2005417 (Pubitemid 40813536)
109. Phillips D. I. W., Birth weight and the future development of diabetes a review of the evidence. Diabetes Care 1998 21 21, supplement 2 B150 B155 2-s2.0-0031848802 (Pubitemid 28357048)
110. Gnanalingham M. G., Mostyn A., Symonds M. E., Stephenson T., Ontogeny and nutritional programming of adiposity in sheep: potential role of glucocorticoid action and uncoupling protein-2. American Journal of Physiology 2005 289 5 R1407 R1415 2-s2.0-27144511493 10.1152/ajpregu.00375.2005 (Pubitemid 41507407)
111. Seckl J. R., Glucocorticoids, feto-placental 11 β -hydroxysteroid dehydrogenase type 2, and the early life origins of adult disease. Steroids 1997 62 1 89 94 2-s2.0-0031030590 10.1016/S0039-128X(96)00165-1 (Pubitemid 27066990)
112. Edwards C. R. W., Stewart P. M., Burt D., McIntyre M. A., De Kloet E. R., Brett L., Sutanto W. S., Monder C., Localisation of 11 β -hydroxysteroid dehydrogenase-tissue specific protector of the mineralocorticoid receptor. The Lancet 1988 2 8618 986 989 2-s2.0-0023761690
113. Bird A., Perceptions of epigenetics. Nature 2007 447 7143 396 398 2-s2.0-34249337761 10.1038/nature05913 (Pubitemid 46816744)
114. Ling C., Groop L., Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 2009 58 12 2718 2725 2-s2.0-73249133400 10.2337/db09-1003
115. Seki Y., Williams L., Vuguin P. M., Charron M. J., Minireview: epigenetic programming of diabetes and obesity: animal models. Endocrinology 2012 153 3 1031 1038
116. Tobi E. W., Lumey L. H., Talens R. P., Kremer D., Putter H., Stein A. D., Slagboom P. E., Heijmans B. T., DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Human Molecular Genetics 2009 18 21 4046 4053 2-s2.0-70349999407 10.1093/hmg/ddp353
117. Church C., Lee S., Bagg E. A. L., McTaggart J. S., Deacon R., Gerken T., Lee A., Moir L., Mecinović J., Quwailid M. M., Schofield C. J., Ashcroft F. M., Cox R. D., A mouse model for the metabolic effects of the human fat mass and obesity associated FTO gene. PLoS Genetics 2009 5 8 2-s2.0-70149100469 10.1371/journal.pgen.1000599 e1000599
118. Sébert S. P., Hyatt M. A., Chan L. L. Y., Yiallourides M., Fainberg H. P., Patel N., Sharkey D., Stephenson T., Rhind S. M., Bell R. C., Budge H., Gardner D. S., Symonds M. E., Influence of prenatal nutrition and obesity on tissue specific fat mass and obesity-associated (FTO) gene expression. Reproduction 2010 139 1 265 274 2-s2.0-75149169815 10.1530/REP-09-0173
119. Chan L. L. Y., Sébert S. P., Hyatt M. A., Stephenson T., Budge H., Symonds M. E., Gardner D. S., Effect of maternal nutrient restriction from early to midgestation on cardiac function and metabolism after adolescent-onset obesity. American Journal of Physiology 2009 296 5 R1455 R1463 2-s2.0-66149096170 10.1152/ajpregu.91019.2008
120. Fischer J., Koch L., Emmerling C., Vierkotten J., Peters T., Brüning J. C., Rüther U., Inactivation of the Fto gene protects from obesity. Nature 2009 458 7240 894 898 2-s2.0-67349211789 10.1038/nature07848