Progressive, transgenerational changes in offspring phenotype and epigenotype following nutritional transition

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Burdge, Graham C ^a   Hoile, Samuel P ^a   Uller, Tobias ^b   Thomas, Nicola A ^a   Gluckman, Peter D ^c   Hanson, Mark A ^a   Lillycrop, Karen A ^d  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; CARNITINE PALMITOYLTRANSFERASE I; DINUCLEOTIDE; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3A2; GENOMIC DNA; GLUCOSE; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CONTROLLED STUDY; CPG ISLAND; DEVELOPMENTAL GENETICS; DIETARY INTAKE; DNA METHYLATION; ENERGY METABOLISM; EPIGENETICS; FEMALE; FOOD INTAKE; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC MARKER; GESTATIONAL AGE; GLUCOSE BLOOD LEVEL; LACTATION; NONHUMAN; NUTRIGENOMICS; NUTRITIONAL ASSESSMENT; PHENOTYPE; PROGENY; PROMOTER REGION; RAT; WEIGHT GAIN;

ANIMALS; BASE SEQUENCE; BODY WEIGHT; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EMBRYO, MAMMALIAN; ENERGY METABOLISM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; GLUCONEOGENESIS; HEREDITY; HSP90 HEAT-SHOCK PROTEINS; KETONES; LACTATION; LIVER; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PHENOTYPE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PREGNANCY; PROMOTER REGIONS, GENETIC; RATS; RATS, WISTAR; RNA, MESSENGER;

EID: 82355183890     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028282     Document Type: Article

References (40)

1. Kimura M, (1984) The Neutral Theory of Molecular Evolution. Cambridge Cambridge University Press.
2. West-Eberhard MJ, (2005) Phenotypic accommodation: adaptive innovation due to developmental plasticity. J Exp Zool B Mol Dev Evol 304: 610-618.
3. Badyaev AV, (2008) Maternal effects as generators of evolutionary change: a reassessment. Ann N Y Acad Sci 1133: 151-161.
4. Badyaev AV, Oh KP, (2008) Environmental induction and phenotypic retention of adaptive maternal effects. BMC Evol Biol 8: 3.
5. Badyaev AV, Uller T, (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R Soc Lond B Biol Sci 364: 1169-1177.
6. Badyaev AV, (2009) Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philos Trans R Soc Lond B Biol Sci 364: 1125-1141.
7. Uller T, (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23: 432-438.
8. Uller T, Badyaev AV, (2009) Evolution of "determinants" in sex-determination: a novel hypothesis for the origin of environmental contingencies in avian sex-bias. Semin Cell Dev Biol 20: 304-312.
9. Badyaev AV, (2005) Role of stress in evolution: From individual adaptability to evolutionary adaptation. In Variation. A central concept in biology. Edited by Hallgrímsson B, Hall BK. MA: Elsevier Academic Press 277-302.
10. Bonduriansky R, Day T, (2009) Nongenetic inheritance and its evolutionary implications. Annual Review of Ecology, Evolution, and Systematics 40: 103-125.
11. Jablonka E, Oborny B, Molnar I, Kisdi E, Hofbauer J, et al. (1995) The adaptive advantage of phenotypic memory in changing environments. Philos Trans R Soc Lond B Biol Sci 350: 133-141.
12. Maestripieri D, Mateo JM, (2009) Maternal effects in mammals. Chicago University of Chicago Press.
13. Gluckman PD, Hanson MA, Cooper C, Thornburg KL, (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359: 61-73.
14. Gluckman PD, Hanson MA, Beedle AS, (2007) Non-genomic transgenerational inheritance of disease risk. Bioessays 29: 145-154.
15. Burdge GC, Lillycrop KA, (2010) Nutrition, epigenetics, and developmental plasticity: implications for understanding human disease. Annu Rev Nutr 30: 315-339.
16. Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, et al. (2007) Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 97: 1064-1073.
17. Ruden DM, Xiao L, Garfinkel MD, Lu X, (2005) Hsp90 and environmental impacts on epigenetic states: a model for the trans-generational effects of diethylstibesterol on uterine development and cancer. Hum Mol Genet 14 Spec No1: R149-R155.
18. Rutherford SL, (2003) Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet 4: 263-274.
19. Rutherford SL, Lindquist S, (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
20. Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, et al. (2007) Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr 97: 435-439.
21. Goldberg AD, Allis CD, Bernstein E, (2007) Epigenetics: a landscape takes shape. Cell 128: 635-638.
22. Skinner MK, (2008) What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol 25: 2-6.
23. Drake AJ, Walker BR, Seckl JR, (2005) Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol 288: R34-R38.
24. Crews D, (2008) Epigenetics and its implications for behavioral neuroendocrinology. Front Neuroendocrinol 29: 344-357.
25. Guerrero-Bosagna CM, Skinner MK, (2009) Epigenetic transgenerational effects of endocrine disruptors on male reproduction. Semin Reprod Med 27: 403-408.
26. Herrera E, (2000) Metabolic adaptations in pregnancy and their implications for the availability of substrates to the fetus. Eur J Clin Nutr 54 (Suppl 1): S47-S51.
27. Chen T, Ueda Y, Xie S, Li E, (2002) A novel Dnmt3a isoform produced from an alternative promoter localizes to euchromatin and its expression correlates with active de novo methylation. J Biol Chem 277: 38746-38754.
28. Lane N, Dean W, Erhardt S, Hajkova P, Surani A,et al. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 2003 35: 88-93.
29. Benyshek DC, Johnston CS, Martin JF, (2006) Glucose metabolism is altered in the adequately-nourished grand-offspring (F-3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 49: 1117-1119.
30. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, et al. (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439: 871-874.
31. Rountree MR, Bachman KE, Baylin SB, (2000) DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 25: 269-277.
32. Ruden DM, Garfinkel MD, Sollars VE, Lu X, (2003) Waddington's widget: Hsp90 and the inheritance of acquired characters. Semin Cell Dev Biol 14: 301-310.
33. West-Eberhard MJ, (2003) Developmental Plasticity and Evolution. New York OUP USA.
34. Jablonka E, Raz G, (2009) Transgenerational Epigenetic Inheritance: Prevalence, Mechanisms, and Implications for the Study of Heredity and Evolution. The Quarterly Review of Biology 84: 131-176.
35. Pimm SL, (2009) Climate disruption and biodiversity. Curr Biol 19: R595-R601.
36. Burdge GC, Lillycrop KA, Jackson AA, Gluckman PD, Hanson MA, (2008) The nature of the growth pattern and of the metabolic response to fasting in the rat are dependent upon the dietary protein and folic acid intakes of their pregnant dams and post-weaning fat consumption. Br J Nutr 99: 540-549.
37. Burdge GC, Lillycrop KA, Phillips ES, Slater-Jefferies JL, Jackson AA, et al. (2009) Folic Acid Supplementation during the Juvenile-Pubertal Period in Rats Modifies the Phenotype and Epigenotype Induced by Prenatal Nutrition. J Nutr 139: 1054-1060.
38. Beale EG, Chrapkiewicz NB, Scoble HA, Metz RJ, Quick DP, et al. (1985) Rat hepatic cytosolic phosphoenolpyruvate carboxykinase (GTP). Structures of the protein, messenger RNA, and gene. J Biol Chem 260: 10748-10760.
39. Yang J, Reshef L, Cassuto H, Aleman G, Hanson RW, (2009) Aspects of the control of phosphoenolpyruvate carboxykinase gene transcription. J Biol Chem 284: 27031-27035.
40. Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, et al. (2008) Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPARalpha promoter of the offspring. British Journal of Nutrition 100: 278-282.