Developmental programming and transgenerational transmission of obesity

Annals of Nutrition and Metabolism

Volumn 64, Issue SUPPL.1, 2014, Pages 26-34

  Vickers, M H ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Developmental programming; Epigenetic inheritance; Germline; Maternal nutrition; Methylation; Obesity; Transgenerational transmission

Indexed keywords

TRANSCRIPTOME;

AGING; BEHAVIOR CHANGE; DEVELOPMENTAL PROGRAMMING; DISEASE TRANSMISSION; DNA DAMAGE; DNA METHYLATION; ENERGY METABOLISM; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; EPIGENETICS; FEMALE GENITAL SYSTEM; FETUS GROWTH; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENETIC ASSOCIATION; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HEREDITY; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; MALNUTRITION; MATERNAL NUTRITION; MATERNAL OBESITY; METABOLIC DISORDER; NONHUMAN; OBESITY; PHENOTYPE; PREGNANCY; PRIORITY JOURNAL; REVIEW; ARTICLE; FOLATE METABOLISM; LIFESTYLE; NUTRITION; PHYSICAL ACTIVITY; PROGENY; ANIMAL; COHORT ANALYSIS; DIET; DISEASE MODEL; FEMALE; FETUS DEVELOPMENT; GENETIC EPIGENESIS; GENETICS; MALE; MOUSE; PHYSIOLOGY; RAT;

ANIMALIA;

ANIMALS; COHORT STUDIES; DIET; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; FEMALE; FETAL DEVELOPMENT; HUMANS; LIFE STYLE; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MICE; OBESITY; PHENOTYPE; PREGNANCY; RATS;

EID: 84905055327     PISSN: 02506807     EISSN: 14219697     Source Type: Journal    
DOI: 10.1159/000360506     Document Type: Review

References (58)

1. Benyshek DC: The 'early life' origins of obesity-related health disorders: new discoveries regarding the intergenerational transmission of developmentally programmed traits in the global cardiometabolic health crisis. Am J Phys Anthropol 2013; 152(suppl 57):79-93.
2. Aiken CE, Ozanne SE: Transgenerational developmental programming. Hum Reprod Update 2014; 20: 63-75.
3. Skinner MK: What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol 2008; 25: 2-6.
4. Jirtle RL, Skinner MK: Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007; 8: 253-262. (Pubitemid 46439287)
5. Barker DJ: The origins of the developmental origins theory. J Intern Med 2007; 261: 412-417. (Pubitemid 46587729)
6. Painter RC, Osmond C, Gluckman P, et al: Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 2008; 115: 1243-1249.
7. Veenendaal MV, Painter RC, de Rooij SR, et al: Transgenerational effects of prenatal exposure to the 1944-45 Dutch famine. BJOG 2013; 120: 548-553.
8. Lumey LH: Decreased birthweights in infants after maternal in utero exposure to the Dutch famine of 1944-1945. Paediatr Perinat Epidemiol 1992; 6: 240-253.
9. Pembrey ME, Bygren LO, Kaati G, et al: Sexspecific, male-line transgenerational responses in humans. Eur J Hum Genet 2006; 14: 159-166. (Pubitemid 43135858)
10. Stein AD, Lumey LH: The relationship between maternal and offspring birth weights after maternal prenatal famine exposure: the Dutch Famine Birth Cohort Study. Hum Biol 2000; 72: 641-654.
11. Morgan DK, Whitelaw E: The case for transgenerational epigenetic inheritance in humans. Mamm Genome 2008; 19: 394-397.
12. Ozanne SE: Metabolic programming in animals. Br Med Bull 2001; 60: 143-152. (Pubitemid 34123509)
13. Benyshek DC, Johnston CS, Martin JF: Postnatal diet determines insulin resistance in fetally malnourished, low birthweight rats (F1) but diet does not modify the insulin resistance of their offspring (F2). Life Sci 2004; 74: 3033-3041. (Pubitemid 38402299)
14. Martin JF, Johnston CS, Han CT, et al: Nutritional origins of insulin resistance: a rat model for diabetes-prone human populations. J Nutr 2000; 130: 741-744. (Pubitemid 30173655)
15. Pinheiro AR, Salvucci ID, Aquila MB, et al: Protein restriction during gestation and/or lactation causes adverse transgenerational effects on biometry and glucose metabolism in F1 and F2 progenies of rats. Clin Sci (Lond) 2008; 114: 381-392. (Pubitemid 351397387)
16. Benyshek DC, Johnston CS, Martin JF, et al: Insulin sensitivity is normalized in the third generation (F3) offspring of developmentally programmed insulin resistant (F2) rats fed an energy-restricted diet. Nutr Metab (Lond) 2008; 5: 26.
17. Benyshek DC, Johnston CS, Martin JF: Glucose metabolism is altered in the adequatelynourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 2006; 49: 1117-1119.
18. 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:R34-R38. (Pubitemid 40023908)
19. Drake AJ, Seckl JR: Transmission of programming effects across generations. Pediatr Endocrinol Rev 2011; 9: 566-578.
20. Lagisz M, Blair H, Kenyon P, et al: Transgenerational effects of caloric restriction on appetite: a meta-analysis. Obes Rev 2014; 15: 294-309.
21. Jimenez-Chillaron JC, Isganaitis E, Charalambous M, et al: Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 2009; 58: 460-468.
22. Ding GL, Wang FF, Shu J, et al: Transgenerational glucose intolerance with Igf2/H19 epigenetic alterations in mouse islet induced by intrauterine hyperglycemia. Diabetes 2012; 61: 1133-1142.
23. Anderson CM, Lopez F, Sandeen A, et al: Placental insufficiency: programming of leptin secretion, blood pressure, and postnatal growth in two generations of Sprague-Dawley rats. Biol Res Nurs 2009; 10: 284-291.
24. Zambrano E: The transgenerational mechanisms in developmental programming of metabolic diseases (in Spanish). Rev Invest Clin 2009; 61: 41-52.
25. Crudo A, Petropoulos S, Moisiadis VG, et al: Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects. Endocrinology 2012; 153: 3269-3283.
26. Bertram C, Khan O, Ohri S, et al: Transgenerational effects of prenatal nutrient restriction on cardiovascular and hypothalamicpituitary-adrenal function. J Physiol 2008; 586: 2217-2229. (Pubitemid 351524573)
27. Beach RS, Gershwin ME, Hurley LS: Persistent immunological consequences of gestation zinc deprivation. Am J Clin Nutr 1983; 38: 579-590. (Pubitemid 13010204)
28. Beach RS, Gershwin ME, Hurley LS: Gestational zinc deprivation in mice: persistence of immunodeficiency for three generations. Science 1982; 218: 469-471. (Pubitemid 12000899)
29. Nascimento FA, Ceciliano TC, Aquila MB, et al: Maternal vitamin D deficiency delays glomerular maturity in F1 and F2 offspring. PLoS One 2012; 7:e41740.
30. Pentinat T, Ramon-Krauel M, Cebria J, et al: Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition. Endocrinology 2010; 151: 5617-5623.
31. Fullston T, Ohlsson Teague EM, Palmer NO, et al: Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J 2013; 27: 4226-4243.
32. Dunn GA, Bale TL: Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 2009; 150: 4999-5009.
33. Dunn GA, Bale TL: Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 2011; 152: 2228-2236.
34. Braunschweig M, Jagannathan V, Gutzwiller A, et al: Investigations on transgenerational epigenetic response down the male line in F2 pigs. PLoS One 2012; 7:e30583.
35. Buchwald U, Teupser D, Kuehnel F, et al: Prenatal stress programs lipid metabolism enhancing cardiovascular risk in the female F1, F2, and F3 generation in the primate model common marmoset (Callithrix jacchus). J Med Primatol 2012; 41: 231-240.
36. Long NM, Smith DT, Ford SP, et al: Elevated glucocorticoids during ovine pregnancy increase appetite and produce glucose dysregulation and adiposity in their granddaughters in response to ad libitum feeding at 1 year of age. Am J Obstet Gynecol 2013; 209: 353.e1-e9.
37. Roseboom TJ, Watson ED: The next generation of disease risk: are the effects of prenatal nutrition transmitted across generations? Evidence from animal and human studies. Placenta 2012; 33(suppl 2):e40-e44.
38. Danchin É, Charmantier A, Champagne FA, et al: Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat Rev Genet 2011; 12: 475-486.
39. Skinner MK, Mohan M, Hague MM, et al: Epigenetic transgenerational inheritance of somatic transcriptomes and epigenetic control regions. Genome Biol 2012; 13:R91.
40. Burdge GC, Hoile SP, Uller T, et al: Progressive, transgenerational changes in offspring phenotype and epigenotype following nutritional transition. PLoS One 2011; 6:e28282.
41. Champagne FA: Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 2008; 29: 386-397.
42. Champagne FA, Meaney MJ: Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav Neurosci 2007; 121: 1353-1363.
43. Connor KL, Vickers MH, Beltrand J, et al: Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J Physiol 2012; 590: 2167-2180.
44. Skinner MK, Hague CG, Nilsson E, et al: Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line. PLoS One 2013; 8:e66318.
45. Salian S, Doshi T, Vanage G: Impairment in protein expression profile of testicular steroid receptor coregulators in male rat offspring perinatally exposed to Bisphenol A. Life Sci 2009; 85: 11-18.
46. Palanza PL, Howdeshell KL, Parmigiani S, et al: Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ Health Perspect 2002; 110(suppl 3):415-422. (Pubitemid 34669809)
47. Skinner MK, Manikkam M, Tracey R, et al: Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity. BMC Med 2013; 11: 228.
48. Zhang HY, Xue WY, Li YY, et al: Perinatal exposure to 4-nonylphenol affects adipogenesis in first and second generation rats offspring. Toxicol Lett 2014;225(2):325-332.
49. Padmanabhan N, Jia D, Geary-Joo C, et al: Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development. Cell 2013; 155: 81-93.
50. Burdge GC, Lillycrop KA: Folic acid supplementation in pregnancy: are there devils in the detail? Br J Nutr 2012; 108: 1924-1930.
51. Hollingsworth JW, Maruoka S, Boon K, et al: In utero supplementation with methyl donors enhances allergic airway disease in mice. J Clin Invest 2008; 118: 3462-3469.
52. Aiken CE, Tarry-Adkins JL, Ozanne SE: Suboptimal nutrition in utero causes DNA damage and accelerated aging of the female reproductive tract. FASEB J 2013; 27: 3959-3965.
53. Howie GJ, Sloboda DM, Kamal T, et al: Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol 2009; 587: 905-915.
54. Catalano PM: Obesity and pregnancy-the propagation of a viscous cycle? J Clin Endocrinol Metab 2003; 88: 3505-3506. (Pubitemid 37034485)
55. Waterland RA, Travisano M, Tahiliani KG, et al: Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond) 2008; 32: 1373-1379.
56. Aiken CE, Ozanne SE: Sex differences in developmental programming models. Reproduction 2013; 145:R1-R13.
57. Drake AJ, Liu L, Kerrigan D, et al: Multigenerational programming in the glucocorticoid programmed rat is associated with generation-specific and parent of origin effects. Epigenetics 2011; 6: 1334-1343.
58. Radford EJ, Isganaitis E, Jimenez-Chillaron J, et al: An unbiased assessment of the role of imprinted genes in an intergenerational model of developmental programming. PLoS Genet 2012; 8:e1002605.