Animal models of epigenetic inheritance

Seminars in Reproductive Medicine

Volumn 27, Issue 5, 2009, Pages 369-379

  Bocock, Philip N ^a   Aagaard Tillery, Kjersti M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Chromatin; Developmental origins of disease; DNA methylation; Histone modification; Nutrition

Indexed keywords

GENOMIC DNA; HISTONE;

CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; EPIGENETICS; HYPOTHESIS; INHERITANCE; INTRAUTERINE GROWTH RETARDATION; NONHUMAN; PHENOTYPE; PREGNANCY; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ADULT; ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FETAL NUTRITION DISORDERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; GENOMIC IMPRINTING; HISTONES; HUMANS; INFANT NUTRITION DISORDERS; INFANT, NEWBORN; INHERITANCE PATTERNS; MODELS, ANIMAL; MODELS, GENETIC; PHENOTYPE; PREGNANCY;

EID: 69449107164     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0029-1237425     Document Type: Review

References (120)

1. Estivill X, Armengol L. Copy number variants and common disorders: filling the gaps and exploring complexity in genome-wide association studies. PLoS Genet 2007;3(10): 1787-1799 (Pubitemid 350072046)
2. Eichler EE, Nickerson DA, Altshuler D, et al; Human Genome Structural Variation Working Group. Completing the map of human genetic variation. Nature 2007;447(7141): 161-165
3. Vissers LE, Veltman JA, van Kessel AG, Brunner HG. Identification of disease genes by whole genome CGH arrays. Hum Mol Genet 2005;14 Spec No. 2:R215-223
4. Pennisi E. Breakthrough of the year. Human genetic variation. Science 2007;318(5858):1842-1843
5. Rickman L, Fiegler H, Carter NP, Bobrow M. Prenatal diagnosis by array-CGH. Eur J Med Genet 2005;48(3):232-240
6. Sebat J. Major changes in our DNA lead to major changes in our thinking. Nat Genet 2007;39(7, suppl):S3-S5 (Pubitemid 47014478)
7. Egan CM, Sridhar S, Wigler M, Hall IM. Recurrent DNA copy number variation in the laboratory mouse. Nat Genet 2007;39(11):1384-1389 (Pubitemid 350034999)
8. Verschure PJ, Visser AE, Rots MG. Step out of the groove: epigenetic gene control systems and engineered transcription factors. Adv Genet 2006;56:163-204
9. Jiang YH, Bressler J, Beaudet AL. Epigenetics and human disease. Annu Rev Genomics Hum Genet 2004;5:479-510
10. Rodenhiser D, Mann M. Epigenetics and human disease: translating basic biology into clinical applications. CMAJ 2006;174(3):341-348 (Pubitemid 43235307)
11. Waddington CH. Towards a theoretical biology. Nature 1968;218(5141):525- 527
12. Riggs A, Martienssen R, Russo V. Introduction. In: Epigenetic Mechanisms of Gene Regulation. Plainview, NY: Cold Spring Harbor Laboratory Press; 1996:1-4
13. Holliday R. The inheritance of epigenetic defects. Science 1987;238(4824):163-170
14. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 1999;23(3):314-318 (Pubitemid 29526429)
15. Wolffe AP, Matzke MA. Epigenetics: regulation through repression. Science 1999;286(5439):481-486
16. Egger G, Liang G, Aparicio A, Jones PA. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004;429(6990):457-463 (Pubitemid 38715140)
17. Birney E, Stamatoyannopoulos JA, Dutta A, et al; ENCODE Project Consortium NISC Comparative Sequencing Program Baylor College of Medicine Human Genome Sequencing Center Washington University Genome Sequencing Center Broad Institute Children's Hospital Oakland Research Institute. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007;447(7146):799-816
18. Turner BM. Cellular memory and the histone code. Cell 2002;111(3):285-291
19. Nightingale KP, O'Neill LP, Turner BM. Histone modifications: signalling receptors and potential elements of a heritable epigenetic code. Curr Opin Genet Dev 2006;16(2): 125-136
20. Turner BM. Histone acetylation and an epigenetic code. Bioessays 2000;22(9):836-845
21. Clayton AL, Hazzalin CA, Mahadevan LC. Enhanced histone acetylation and transcription: a dynamic perspective. Mol Cell 2006;23(3):289-296 (Pubitemid 44128853)
22. Mellor J. Dynamic nucleosomes and gene transcription. Trends Genet 2006;22(6):320-329
23. Shi Y. Histone lysine demethylases: emerging roles in development, physiology and disease. Nat Rev Genet 2007; 8(11):829-833 (Pubitemid 47609092)
24. Shi Y, Whetstine JR. Dynamic regulation of histone lysine methylation by demethylases. Mol Cell 2007;25(1): 1-14 (Pubitemid 46049067)
25. Barski A, Cuddapah S, Cui K, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007;129(4):823-837 (Pubitemid 46802390)
26. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007;130(1): 77-88 (Pubitemid 47031323)
27. Shi Y, Lan F, Matson C, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004;119(7):941-953 (Pubitemid 40037608)
28. Tsankova N, Renthal W, Kumar A, Nestler EJ. Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci 2007; 8(5):355-367
29. Karagiannis TC, El-Osta A. Will broad-spectrum histone deacetylase inhibitors be superseded by more specific compounds? Leukemia 2007;21(1):61-65
30. Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 2006;6(1):38-51 (Pubitemid 43054973)
31. Mann BS, Johnson JR, Cohen MH, Justice R, Pazdur R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 2007;12(10):1247-1252 (Pubitemid 350106355)
32. Ferrante RJ, Kubilus JK, Lee J, et al. Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington's disease mice. J Neurosci 2003;23(28):9418-9427 (Pubitemid 37323042)
33. Avila AM, Burnett BG, Taye AA, et al. Trichostatin A increases SMN expression and survival in a mouse model of spinal muscular atrophy. J Clin Invest 2007;117(3): 659-671
34. Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH. Recovery of learning and memory is associated with chromatin remodelling. Nature 2007;447(7141):178-182 (Pubitemid 46763080)
35. Kim TH, Abdullaev ZK, Smith AD, et al. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 2007;128(6):1231-1245
36. Ruthenburg AJ, Li H, Patel DJ, Allis CD. Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 2007;8(12):983-994 (Pubitemid 350174643)
37. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. Demethylation of the zygotic paternal genome. Nature 2000;403(6769):501-502
38. Oswald J, Engemann S, Lane N, et al. Active demethylation of the paternal genome in the mouse zygote. Curr Biol 2000;10(8):475-478 (Pubitemid 30247337)
39. Ehrlich M, Gama-Sosa MA, Huang LH, et al. Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res 1982; 10(8):2709-2721
40. Bestor TH. Activation of mammalian DNA methyltransferase by cleavage of a Zn binding regulatory domain. EMBO J 1992;11(7):2611-2617
41. Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 1992;69(6):915-926
42. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999;99(3): 247-257 (Pubitemid 29519904)
43. Lyko F, Ramsahoye BH, Kashevsky H, et al. Mammalian (cytosine-5) methyltransferases cause genomic DNA methylation and lethality in Drosophila. Nat Genet 1999;23(3): 363-366 (Pubitemid 29526439)
44. Bestor T, Laudano A, Mattaliano R, Ingram V. Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J Mol Biol 1988;203(4):971-983 (Pubitemid 18269490)
45. Chen T, Ueda Y, Dodge JE, Wang Z, Li E. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol Cell Biol 2003;23(16):5594-5605 (Pubitemid 36951325)
46. Rhee I, Bachman KE, Park BH, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 2002;416(6880):552-556 (Pubitemid 34288859)
47. Takai D, Jones PA. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci U S A 2002;99(6):3740-3745 (Pubitemid 34252176)
48. Jones PA. The DNA methylation paradox. Trends Genet 1999;15(1):34-37
49. Holliday R, Pugh JE. DNA modification mechanisms and gene activity during development. Science 1975;187(4173): 226-232
50. Riggs AD. X inactivation, differentiation, and DNA methylation. Cytogenet Cell Genet 1975;14(1):9-25
51. McGrath J, Solter D. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 1984; 37(1):179-183 (Pubitemid 14079849)
52. Surani MA, Barton SC, Norris ML. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 1984;308(5959):548-550
53. Gluckman PD, Hanson MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab 2004; 15(4):183-187
54. Dolinoy DC, Weidman JR, Jirtle RL. Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod Toxicol 2007;23(3):297-307
55. Santos F, Dean W. Epigenetic reprogramming during early development in mammals. Reproduction 2004;127(6):643-651 (Pubitemid 38878420)
56. Weidman JR, Maloney KA, Jirtle RL. Comparative phylogenetic analysis reveals multiple non-imprinted isoforms of opossum Dlk1. Mamm Genome 2006;17(2):157-167
57. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005;308(5727):1466- 1469
58. Ho SM, Tang WY, Belmonte de Frausto J, Prins GS. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res 2006;66(11):5624-5632
59. Dolinoy DC, Weidman JR, Waterland RA, Jirtle RL. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect 2006;114(4):567-572
60. Fernandez-Twinn DS, Ozanne SE. Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome. Physiol Behav 2006;88(3):234-243
61. Gluckman PD, Hanson MA. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res 2004;56(3):311-317
62. Lucas A. Programming by early nutrition in man. Ciba Found Symp 1991;156:38-50; discussion 50-35
63. McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 2005;85(2):571-633
64. Waterland RA, Garza C. Early postnatal nutrition determines adult pancreatic glucose-responsive insulin secretion and islet gene expression in rats. J Nutr 2002;132(3):357-364 (Pubitemid 34208733)
65. Cheung P, Allis CD, Sassone-Corsi P. Signaling to chromatin through histone modifications. Cell 2000;103(2): 263-271
66. Pham TD, MacLennan NK, Chiu CT, Laksana GS, Hsu JL, Lane RH. Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol 2003; 285(5):R962-R970
67. Ke X, Lei Q, James SJ, et al. Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats. Physiol Genomics 2006;25(1):16-28
68. Rakyan VK, Chong S, Champ ME, et al. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci U S A 2003;100(5):2538-2543 (Pubitemid 36297534)
69. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 2003;23(15):5293-5300
70. Wolff GL, Kodell RL, Moore SR, Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 1998;12(11):949-957
71. Waterland RA, Dolinoy DC, Lin JR, Smith CA, Shi X, Tahiliani KG. Maternal methyl supplements increase offspring DNA methylation at Axin Fused. Genesis 2006;44(9): 401-406 (Pubitemid 44454044)
72. Fernandez-Twinn DS, Ozanne SE, Ekizoglou S, et al. The maternal endocrine environment in the low-protein model of intra-uterine growth restriction. Br J Nutr 2003;90(4): 815-822 (Pubitemid 37270765)
73. Krechowec SO, Vickers M, Gertler A, Breier BH. Prenatal influences on leptin sensitivity and susceptibility to diet-induced obesity. J Endocrinol 2006;189(2):355-363 (Pubitemid 43757793)
74. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 2005;135(6):1382-1386
75. Ogata ES, Bussey ME, Finley S. Altered gas exchange, limited glucose and branched chain amino acids, and hypoinsulinism retard fetal growth in the rat. Metabolism 1986;35(10):970-977 (Pubitemid 17184368)
76. Ogata ES, Bussey ME, LaBarbera A, Finley S. Altered growth, hypoglycemia, hypoalaninemia, and ketonemia in the young rat: postnatal consequences of intrauterine growth retardation. Pediatr Res 1985;19(1):32-37 (Pubitemid 15187468)
77. Economides DL, Nicolaides KH, Campbell S. Metabolic and endocrine findings in appropriate and small for gestational age fetuses. J Perinat Med 1991;19(1-2):97-105
78. Economides DL, Nicolaides KH, Gahl WA, Bernardini I, Evans MI. Plasma amino acids in appropriate- and smallfor- gestational-age fetuses. Am J Obstet Gynecol 1989; 161(5):1219-1227 (Pubitemid 20007686)
79. Nicolaides KH, Economides DL, Soothill PW. Blood gases, pH, and lactate in appropriate- and small-for-gestational-age fetuses. Am J Obstet Gynecol 1989;161(4):996-1001 (Pubitemid 19266218)
80. Economides DL, Nicolaides KH, Gahl WA, Bernardini I, Bottoms S, Evans M. Cordocentesis in the diagnosis of intrauterine starvation. Am J Obstet Gynecol 1989;161(4): 1004-1008
81. Economides DL, Nicolaides KH. Blood glucose and oxygen tension levels in small-for-gestational-age fetuses. Am J Obstet Gynecol 1989;160(2):385-389
82. Simmons RA, Templeton LJ, Gertz SJ. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 2001;50(10):2279- 2286 (Pubitemid 33641912)
83. Tsirka AE, Gruetzmacher EM, Kelley DE, Ritov VH, Devaskar SU, Lane RH. Myocardial gene expression of glucose transporter 1 and glucose transporter 4 in response to uteroplacental insufficiency in the rat. J Endocrinol 2001; 169(2):373-380 (Pubitemid 32447616)
84. Vileisis RA, D'Ercole AJ. Tissue and serum concentrations of somatomedin-C/insulin-like growth factor I in fetal rats made growth retarded by uterine artery ligation. Pediatr Res 1986;20(2):126-130
85. Fu Q, McKnight RA, Yu X, Wang L, Callaway CW, Lane RH. Uteroplacental insufficiency induces site-specific changes in histone H3 covalent modifications and affects DNA-histone H3 positioning in day 0 IUGR rat liver. Physiol Genomics 2004;20(1):108-116 (Pubitemid 40388510)
86. Fu Q, McKnight RA, Yu X, Callaway CW, Lane RH. Growth retardation alters the epigenetic characteristics of hepatic dual specificity phosphatase 5. FASEB J 2006;20(12): 2127-2129
87. Strauss RS, Pollack HA. Epidemic increase in childhood overweight, 1986-1998. JAMA 2001;286(22):2845-2848
88. Slyper AH. The pediatric obesity epidemic: causes and controversies. J Clin Endocrinol Metab 2004;89(6):2540-2547
89. Speiser PW, Rudolf MC, Anhalt H et al Obesity Consensus Working Group. Childhood obesity. J Clin Endocrinol Metab 2005;90(3):1871-1887 (Pubitemid 40464063)
90. Newman WP III, Freedman DS, Voors AW, et al. Relation of serum lipoprotein levels and systolic blood pressure to early atherosclerosis. The Bogalusa Heart Study. N Engl J Med 1986;314(3):138-144
91. Brown SA, Rogers LK, Dunn JK, Gotto AM Jr, Patsch W. Development of cholesterol homeostatic memory in the rat is influenced by maternal diets. Metabolism 1990;39(5): 468-473 (Pubitemid 20156312)
92. Guo F, Jen KL. High-fat feeding during pregnancy and lactation affects offspring metabolism in rats. Physiol Behav 1995;57(4):681-686
93. Khan IY, Taylor PD, Dekou V, et al. Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension 2003;41(1):168-175 (Pubitemid 36056810)
94. Khan IY, Dekou V, Douglas G, et al. A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol 2005;288(1):R127-R133 (Pubitemid 40023922)
95. Buckley AJ, Keserü B, Briody J, Thompson M, Ozanne SE, Thompson CH. Altered body composition and metabolism in the male offspring of high fat-fed rats. Metabolism 2005;54(4):500-507 (Pubitemid 40410452)
96. Khan I, Dekou V, Hanson M, Poston L, Taylor P. Predictive adaptive responses to maternal high-fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation 2004;110(9):1097-1102 (Pubitemid 39319008)
97. Aagaard-Tillery KM, Grove K, Bishop J, et al. Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 2008;41(2):91-102
98. Nijland MJ, Ford SP, Nathanielsz PW. Prenatal origins of adult disease. Curr Opin Obstet Gynecol 2008;20(2):132-138
99. Jacobs R, Owens JA, Falconer J, Webster ME, Robinson JS. Changes to metabolite concentration in fetal sheep subjected to prolonged hypobaric hypoxia. J Dev Physiol 1988;10(2):113-121 (Pubitemid 18120327)
100. Fletcher AJ, Goodfellow MR, Forhead AJ, et al. Low doses of dexamethasone suppress pituitary-adrenal function but augment the glycemic response to acute hypoxemia in fetal sheep during late gestation. Pediatr Res 2000;47(5):684-691
101. Fletchert AJ, Edwards CM, Gardner DS, Fowden AL, Giussani DA. Neuropeptide Y in the sheep fetus: effects of acute hypoxemia and dexamethasone during late gestation. Endocrinology 2000;141(11):3976-3982
102. Gardner DS, Fletcher AJ, Fowden AL, Giussani DA. Plasma adrenocorticotropin and cortisol concentrations during acute hypoxemia after a reversible period of adverse intrauterine conditions in the ovine fetus during late gestation. Endocrinology 2001;142(2):589-598
103. Gardner DS, Fletcher AJ, Bloomfield MR, Fowden AL, Giussani DA. Effects of prevailing hypoxaemia, acidaemia or hypoglycaemia upon the cardiovascular, endocrine and metabolic responses to acute hypoxaemia in the ovine fetus. J Physiol 2002;540(Pt 1):351-366
104. Gardner DS, Giussani DA, Fowden AL. Hindlimb glucose and lactate metabolism during umbilical cord compression and acute hypoxemia in the late-gestation ovine fetus. Am J Physiol Regul Integr Comp Physiol 2003;284(4):R954-R964
105. Giussani DA, Phillips PS, Anstee S, Barker DJ. Effects of altitude versus economic status on birth weight and body shape at birth. Pediatr Res 2001;49(4):490-494 (Pubitemid 32274961)
106. Llanos AJ, Riquelme RA, Sanhueza EM, et al. Regional brain blood flow and cerebral hemispheric oxygen consumption during acute hypoxaemia in the llama fetus. J Physiol 2002; 538(Pt 3):975-983
107. Min SW, Ko H, Kim CS. Power spectral analysis of heart rate variability during acute hypoxia in fetal lambs. Acta Obstet Gynecol Scand 2002;81(11):1001-1005 (Pubitemid 35335061)
108. Barbera A, Giraud GD, Reller MD, Maylie J, Morton MJ, Thornburg KL. Right ventricular systolic pressure load alters myocyte maturation in fetal sheep. Am J Physiol Regul Integr Comp Physiol 2000;279(4):R1157-R1164 (Pubitemid 30953746)
109. Cleal JK, Poore KR, Boullin JP, et al. Mismatched pre- and postnatal nutrition leads to cardiovascular dysfunction and altered renal function in adulthood. Proc Natl Acad Sci U S A 2007;104(22):9529-9533
110. Davis L, Thornburg KL, Giraud GD. The effects of anaemia as a programming agent in the fetal heart. J Physiol 2005;565(Pt 1):35-41 (Pubitemid 40723689)
111. Houdijk EC, Engelbregt MJ, Popp-Snijders C, Delemarre- Vd Waal HA. Endocrine regulation and extended follow-up of longitudinal growth in intrauterine growth-retarded rats. J Endocrinol 2000;166(3):599-608
112. Sanders M, Fazzi G, Janssen G, Blanco C, De Mey J. Prenatal stress changes rat arterial adrenergic reactivity in a regionally selective manner. Eur J Pharmacol 2004;488(1-3): 147-155 (Pubitemid 38388534)
113. Sanders MW, Fazzi GE, Janssen GM, de Leeuw PW, Blanco CE, De Mey JG. Reduced uteroplacental blood flow alters renal arterial reactivity and glomerular properties in the rat offspring. Hypertension 2004;43(6):1283-1289
114. Vickers MH, Ikenasio BA, Breier BH. IGF-I treatment reduces hyperphagia, obesity, and hypertension in metabolic disorders induced by fetal programming. Endocrinology 2001;142(9):3964-3973
115. Vickers MH, Reddy S, Ikenasio BA, Breier BH. Dysregulation of the adipoinsular axis - a mechanism for the pathogenesis of hyperleptinemia and adipogenic diabetes induced by fetal programming. J Endocrinol 2001;170(2): 323-332 (Pubitemid 32771434)
116. Siebel AL, Mibus A, De Blasio MJ, et al. Improved lactational nutrition and postnatal growth ameliorates impairment of glucose tolerance by uteroplacental insufficiency in male rat offspring. Endocrinology 2008;149(6):3067-3076 (Pubitemid 351724507)
117. Louey S, Jonker SS, Giraud GD, Thornburg KL. Placental insufficiency decreases cell cycle activity and terminal maturation in fetal sheep cardiomyocytes. J Physiol 2007; 580(Pt. 2):639-648 (Pubitemid 46564188)
118. Broberg CS, Giraud GD, Schultz JM, Thornburg KL, Hohimer AR, Davis LE. Fetal anemia leads to augmented contractile response to hypoxic stress in adulthood. Am J Physiol Regul Integr Comp Physiol 2003;285(3):R649-R655
119. Woods LL, Ingelfinger JR, Nyengaard JR, Rasch R. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res 2001;49(4):460-467 (Pubitemid 32274957)
120. White MM, Zhang L. Effects of chronic hypoxia on maternal vasodilation and vascular reactivity in guinea pig and ovine pregnancy. High Alt Med Biol 2003;4(2):157-169 (Pubitemid 36950041)