Multigenerational programming in the glucocorticoid programmed rat is associated with generation-specific and parent of origin effects

Epigenetics

Volumn 6, Issue 11, 2011, Pages 1334-1343

  Drake, Amanda J ^a   Liu, Lincoln ^a   Kerrigan, David ^a   Meehan, Richard R ^b,c   Seckl, Jonathan R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b WESTERN GENERAL HOSPITAL   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Epigenetics; Glucocorticoids; Methylation; Multigenerational; Programming

Indexed keywords

DEXAMETHASONE; DNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRTH WEIGHT; CONTROLLED STUDY; DNA METHYLATION; DRUG EFFECT; EPIGENETICS; FEMALE; FERTILIZATION; FETUS WEIGHT; MALE; MULTIGENERATIONAL PROGRAMMING; NONHUMAN; NUCLEAR REPROGRAMMING; PLACENTA WEIGHT; PROGENY; RAT; SPERM;

ANIMALIA; RATTUS;

EID: 81055136660     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.11.17942     Document Type: Article

References (58)

1. Barker DJP. In utero programming of chronic disease. Clin Sci 1998; 95:115-28.
2. Thayer ZM, Kuzawa CW. Biological memories of past environments. Epigenetic pathways to health disparities. Epigenetics 2011; 6:1-6.
3. Drake AJ, Liu L. Intergenerational transmission of programmed effects: public health consequences. Trends Endocrinol Metab 2010; 21:206-13.
4. Kaati G, Bygren LO, Edvinson S. Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur J Hum Genet 2002; 10:682-8.
5. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DIW, Roseboom TJ. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 2008; 115:1243-9.
6. Kuzawa CW, Sweet E. Epigenetics and the embodiment of race: Developmental origins of US racial disparities in cardiovascular health. Am J Hum Biol 2009; 21:2-15.
7. Drake AJ, Walker BR. The intergenerational effects of fetal programming: non genomic mechanisms for the inheritance of low birth weight and cardiovascular risk. J Endocrinol 2004; 180:1-16.
8. Jablonka E, Lamb MJ. Evolution in four dimensions: Genetic, epigenetic, behavioural and symbolic variation in the history of life. MIT press, Cambridge, Massachusetts 2005.
9. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005; 308:1466-9.
10. Jimenez-Chillaron JC, Isganaitis E, Charalambous M, Gesta S, Pentinat-Pelegrin T, Faucette RR, et al. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 2009; 58:460-8.
11. Drake AJ, Walker BR, Seckl JR. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol 2005; 288:34-8.
12. Stouder C, Paoloni-Giacobino A. Specific transgenerational imprinting effects of the endocrine disruptor methoxychlor on male gametes. Reproduction 2011; 141:207-16.
13. Gluckman PD, Hanson MA, Buklijas T, Low FM, Beedle AS. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat Rev Endocrinol 2009; 5:401-8.
14. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33:245-54.
15. Davis TL, Yang GJ, McCarrey JR, Bartolomei MS. The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet 2000; 9:2885-94.
16. Ueda T, Abe K, Miura A, Yuzuriha M, Zubair M, Noguchi M, et al. The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells 2000; 5:649-59.
17. Georgiades P, Watkins M, Burton GJ, Ferguson-Smith A. Roles for genomic imprinting and the zygotic genome in placental development. Proc Natl Acad Sci USA 2001; 98:4522-7.
18. Constancia M, Angiolini E, Sandovici I, Smith P, Smith R, Kelsey G, et al. Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proc Natl Acad Sci USA 2005; 102:19219-24.
19. Lim AL, Ferguson-Smith AC. Genomic imprinting effects in a compromised in utero environment: Implications for a healthy pregnancy. Semin Cell Dev Biol 2010; 21:201-8.
20. Edwards CR, Benediktsson R, Lindsay RS, Seckl JR. Dysfunction of placental glucocorticoid barrier: a link between the fetal environment and adult hypertension? Lancet 1993; 341:355-7.
21. Nyirenda MJ, Lindsay RS, Kenyon CJ, Burchell A, Seckl JR. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest 1998; 101:2174-81.
22. Reinisch JM, Simon NG, Karow WG, Gandelman R. Prenatal exposure to prednisone in humans and animals retards intrauterine growth. Science 1978; 202:436-8.
23. Campbell AL, Murphy BE. The maternal-fetal cortisol gradient during pregnancy and at delivery. J Clin Endo Metab 1977; 45:435-40.
24. Seckl JR. Glucocorticoids, feto-placental 11 beta-hydroxysteroid dehydrogenase type 2, and the early life origins of adult disease. Steroids 1997; 62:89-94.
25. Venihaki M, Carrigan A, Dikkes P, Majzoub JA. Circadian rise in maternal glucocorticoid prevents pulmonary dysplasia in fetal mice with adrenal insufficiency. Proc Natl Acad Sci USA 2000; 97:7336-41.
26. Mairesse J, Lesage J, Breton C, Breant B, Hahn T, Darnaudery M, et al. Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol 2007; 292:1526-33.
27. Benediktsson R, Lindsay RS, Noble J, Seckl JR, Edwards CR. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet 1993; 341:339-41.
28. Welberg LA, Seckl JR, Holmes MC. Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. Eur J Neurosci 2000; 12:1047-54.
29. Welberg LA, Seckl JR. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 2001; 13:113-28.
30. Kim MS, Kondo T, Takada I, Youn MY, Yamamoto Y, Takahashi S, et al. DNA demethylation in hormone-induced transcriptional derepression. Nature 2009; 461:1007-12.
31. Thomassin H, Flavin M, Espinas ML, Grange T. Glucocorticoid-induced DNA demethylation and gene memory during development. EMBO J 2001; 20:1974-83.
32. Moore T, Constancia M, Zubair M, Bailleul B, Feil R, Sasaki K, et al. Multiple imprinted sense and antisense transcripts, differential methylation and tandem repeats in a putative imprinting control region upstream of mouse Igf2. Proc Natl Acad Sci USA 1997; 94:12509-14.
33. Murrell A, Heeson S, Bowden L, Constancia M, Dean W, Kelsey G, et al. An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO Rep 2001; 2:1101-6.
34. Forne T, Oswald J, Dean W, Saam JR, Bailleul B, Dandolo L, et al. Loss of the maternal H19 gene induces changes in Igf2 methylation in both cis and trans. Proc Natl Acad Sci USA 1997; 94:10243-8.
35. DeChiara TM, Efstratiadis A, Robertson EJ. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 1990; 345:78-80.
36. Andrews S, Wood M, Tunster S, Barton S, Surani MA, John R. Cdkn1c (p57Kip2) is the major regulator of embryonic growth within its imprinted domain on mouse distal chromosome 7. BMC Dev Biol 2007; 7:53.
37. Caspary T, Cleary MA, Perlman EJ, Zhang P, Elledge SJ, Tilghman SM. Oppositely imprinted genes p57Kip2 and Igf2 interact in a mouse model for Beckwith-Wiedemann syndrome. Genes Dev 1999; 13:3115-24.
38. Grandjean V, Smith J, Schofield PN, Ferguson-Smith AC. Increased IGF-II protein affects p57kip2 expression in vivo and in vitro: Implications for Beckwith-Wiedemann syndrome. Proc Natl Acad Sci USA 2000; 97:5279-84.
39. Charalambous M, Smith FM, Bennett WR, Crew TE, Mackenzie F, Ward A. Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc Natl Acad Sci USA 2003; 100:8292-7.
40. Wang L, Balas B, Christ-Roberts CY, Kim RY, Ramos FJ, Kikani CK, et al. Peripheral disruption of the Grb10 gene enhances insulin signaling and sensitivity in vivo. Mol Cell Biol 2007; 27:6497-505.
41. Tunster SJ, Tycko B, John RM. The imprinted Phlda2 gene regulates extraembryonic energy stores. Mol Cell Biol 2010; 30:295-306.
42. Haig D. The kinship theory of genomic imprinting. Annu Rev Ecol Syst 2000; 31:9-32.
43. Lopes S, Lewis A, Hajkova P, Dean W, Oswald J, Forne T, et al. Epigenetic modifications in an imprinting cluster are controlled by a hierarchy of DMRs suggesting long-range chromatin interactions. Hum Mol Genet 2003; 12:295-305.
44. Tabano S, Colapietro P, Cetin I, Grati FR, Zanutto S, Mando C, et al. Epigenetic modulation of the IGF2/H19 imprinted domain in human embryonic and extra-embryonic compartments and its possible role in fetal growth restriction. Epigenetics 2010; 5:313-24.
45. Einstein F, Thompson RF, Bhagat TD, Fazzari MJ, Verma A, Barzilai N, et al. Cytosine methylation dysregulation in neonates following intrauterine growth restriction. PLoS One 2010; 5:8887.
46. Murrell A, Ito Y, Verde G, Huddleston J, Woodfine K, Silengo MC, et al. Distinct methylation changes at the IGF2-H19 locus in congenital growth disorders and cancer. PLoS One 2008; 3:1849.
47. Coan PM, Vaughan OR, Sekita Y, Finn SL, Burton GJ, Constancia M, et al. Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J Physiol 2010; 588:527-38.
48. Lewis A, Mitsuya K, Umlauf D, Smith P, Dean W, Walter J, et al. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat Genet 2004; 36:1291-5
49. Kriaucionis S, Heintz N. The nuclear DNA base 5-Hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009; 324:929-30.
50. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 1999; 23:314-8.
51. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV, et al. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci USA 2003; 100:2538-43.
52. Guerrero-Bosagna C, Settles M, Lucker B, Skinner MK. Epigenetic transgenerational actions of Vinclozolin on promoter regions of the sperm epigenome. PLoS One 2011; 5:13100.
53. Daxinger L, Whitelaw E. Transgenerational epigenetic inheritance: More questions than answers. Genome Res 2010; 20:1623-8.
54. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. Distinctive chromatin in human sperm packages genes for embryo development. Nature 2009; 460:473-8.
55. Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I, Cuzin F. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 2006; 441:469-74.
56. Lalancette C, Miller DJ, Li Y, Krawetz SA. Paternal contributions: New functional insights for spermatozoal RNA. J Cell Biochem 2008; 104:1570-9.
57. Gluckman PD, Hanson MA. Living with the past: Evolution, development and patterns of disease. Science 2004; 305:1733-6.
58. Drake AJ, Raubenheimer PJ, Kerrigan D, McInnes KJ, Seckl JR, Walker BR. Prenatal dexamethasone programs expression of genes in liver and adipose tissue and increased hepatic lipid accumulation but not obesity on a high-fat diet. Endocrinology 2010; 151: 1581-7