The plasticity of development: How knowledge of epigenetics may advance understanding of eating disorders

International Journal of Eating Disorders

Volumn 47, Issue 7, 2014, Pages 696-704

  Strober, Michael ^a,b   Peris, Tara ^a   Steiger, Howard ^c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Douglas Institute Eating Disorders Program   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

development; environment; epigenetics; genes

Indexed keywords

DNA;

BIRTH WEIGHT; CHILD REARING; DESCRIPTIVE RESEARCH; DIET; EATING DISORDER; EPIGENETICS; GENETIC VARIABILITY; GERM LINE; HUMAN; INHERITANCE; LIFE HISTORY; MATERNAL STRESS; NATURAL DISASTER; NONHUMAN; PHENOTYPE; PLASTICITY; REVIEW; ANIMAL; ANXIETY DISORDER; COMPLICATION; DISEASE MODEL; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; FEMALE; GENETIC EPIGENESIS; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; GERM CELL; MALE; MATERNAL NUTRITION; MENTAL STRESS; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; ANXIETY DISORDERS; BIRTH WEIGHT; DISEASE MODELS, ANIMAL; DNA METHYLATION; EATING DISORDERS; ENVIRONMENTAL EXPOSURE; EPIGENESIS, GENETIC; FEMALE; GENE-ENVIRONMENT INTERACTION; GERM CELLS; HUMANS; MALE; MATERNAL EXPOSURE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PATERNAL EXPOSURE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STRESS, PSYCHOLOGICAL;

EID: 84916876786     PISSN: 02763478     EISSN: 1098108X     Source Type: Journal    
DOI: 10.1002/eat.22322     Document Type: Review

References (78)

1. Waddington CH,. The epiphenotype. Endeavor 1942; 1: 18-20.
2. Lickliter R,. The dynamics of development and evolution: Insights from behavioral embryology. Dev Psychobiol 2007; 49: 749-757.
3. Gottlieb G,. Individual Development and Evolution: The Genesis of Novel Behavior. Mahwah, NJ: Ehrlbaum, 2002.
4. Gottlieb G,. Probabilistic epigenesis. Dev Sci 2007; 10: 1-11.
5. Vinci T, Robert JS,. Aristotle and modern genetics. J Hist Ideas 2005; 66: 201-221.
6. Gudsnuk MA, Champagne, FA,. Epigenetic effects of early developmental experiences. Clin Perinatol 2011; 38: 703-711.
7. Zhang T-Y, Meaney MJ,. Epigenetics and environmental regulation of the genome and its function. Ann Rev Psychol 2010; 61: 419-466.
8. Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD, Hanson MA,. Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr Res 2007; 61: 5-10.
9. Gluckman PD, Hanson MA, Beedle AS,. Early life events and their consequences for later disease: A life history and evolutionary perspective. Am J Hum Biol 2007; 19: 1-19.
10. Barker DJP,. The developmental origins of adult disease. J Am College Nutr 2004; 23: 588-595.
11. Bohacek J, Mansuy IM,. Epigenetic inheritance of disease and disease risk. Neuropsychopharm 2013; 38: 220-236.
12. Campbell IC, Mill J, Uher R, Schmidt U,. Eating disorders, gene-environment interactions and epigenetics. Neurosci Biobehav Rev 2011; 35: 784-793.
13. Pjetri E, Schmidt U, Kas M, Campbell I,. Epigenetics and eating disorders. Curr Opin Clin Nutri Metabol Care 2012; 15: 330-335.
14. Frieling H, Gozner A, Römer KD, Lenz B, Bönsch D, Wilhelm J, et al. Global DNA hypomethylation and DNA hypermethylation of the alpha synuclein promoter in females with anorexia nervosa. Mol Psychiatry 2007; 12: 229-230.
15. Frieling H, Bleich S, Otten J, Römer KD, Kornhuber J, de Zwaan M, Georg Jacoby GE, et al. Epigenetic downregulation of atrial natriuretic peptide but not vasopressin mRNA expression in females with eating disorders is related to impulsivity. Neuropsychopharm 2008; 33: 2605-2609.
16. Ehrlich S, Weiss D, Burghardt R, Infante-Duarte C, Brockhaus S, Muschler MA, et al. Promoter specific DNA methylation gene expression of POMC in acutely underweight and recovered patients with anorexia nervosa. J Psychiatr Res 2010; 44: 827-833.
17. Frieling H, Römer KD, Scholz S, Mittelbach F, Wilhelm J, De Zwaan M, et al. Epigenetic dysregulation of dopaminergic genes in eating disorders. Int J Eat Disord 2010; 43: 577-583.
18. Steiger H, Labonté B, Groleau P, Turecki G, Israel M,. Methylation of the glucocorticoid receptor gene promoter in bulimic women: Associations with borderline personality disorder, suicidality, and exposure to childhood abuse. Int J Eat Disord 2013; 46: 246-255.
19. Groleau P, Joober R, Israel M, Zeramdini N, DeGuzman R, Steiger H,. Methylation of the dopamine D2 receptor (DRD2) gene promoter in women with a bulimia-spectrum disorder: Associations with borderline personality disorder and exposure to childhood abuse. Psychiatr Res 2014; 48: 121-127.
20. Thaler L, Gauvan L, Joober R, Groleau P, de Guzman R, Ambalavanan A, Israel M, Wilson S, Steiger H,. Methylation of BDNF in women with bulimic eating syndromes: Associations with childhood abuse and borderline personality disorder. Prog Neuropsychopharm Bio Psychiatry, Epub ahead of print.
21. Strober M, Johnson C,. The need for complex ideas in anorexia nervosa: Why biology, environment, and psyche all matter, why therapists make mistakes, and why clinical benchmarks are needed for managing weight correction. Int J Eat Disord 2012; 45: 155-178.
22. Gluckman P, Hanson M,. Mismatch: Why Our World No Longer Fits Our Bodies. Oxford: Oxford University Press, 2006.
23. Strober M, Freeman R, Lampert C, Diamond J,. The association of anxiety disorders and obsessive compulsive personality disorder with anorexia nervosa: Evidence from a family study with discussion of nosological and neurodevelopmental implications. Int J Eat Disord 2007; 40 (SUPPL.): 46-51.
24. Monk C, Spicer J, Champagne FA,. Linking prenatal maternal adversity to developmental outcomes. Dev Psychopathology 2012; 24: 1361-1376.
25. Sandman CA, Davis EP, Buss C, Glynn L,. Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus. Neuroendocrinology 2012; 95: 8-21.
26. Weinstock M,. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 2005; 19: 296-308.
27. Weinstock M,. Long-term behavioral consequences of prenatal stress. Neurosci Biobehav Rev 2008; 32: 1073-1086.
28. McGowan PO, Meaney MJ, Szyf M,. Diet and the epigenetic (re)programming of phenotypic differences in behavior. Brain Res 2008; 1237: 12-24.
29. Field T, Diego M, Hernandez-Reif M,. Prenatal depression effects on the fetus and newborn: A review. Infant Behav Dev 2006; 29: 445-455.
30. Buss C, Davis EP, Muftuler LT, Head K, Sandman CA,. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology 2010; 35: 141-153.
31. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM,. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008; 3: 97-106.
32. Davidson RJ,. Anterior cerebral asymmetry and the nature of emotion. Brain Cog 1992; 20: 125-151.
33. Schwabe L,. Stress and the engagement of multiple memory systems: Integration of animal and human studies. Hippocampus 2013; 23: 1035-1043.
34. Worthman CM, Kuzawa J,. Life history and the early origins of health differentials. Am J Hum Biol 2005; 17: 95-112.
35. Milagro FI, Campiõn J, Cordero P, Goyenechea E, Gõmez-Uriz AM, Abete I, et al. A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. FASEB J 2011; 25: 1378-1389.
36. Campiõn J, Milagro FI, Goyenechea E, Martínez JA,. TNF-alpha promoter methylation as a predictive biomarker for weight-loss response. Obesity 2009; 17: 1293-1297.
37. Bouchard L, Rabasa-Lhoret R, Faraj M, Lavoie ME, Mill J, Pérusse L, et al. Differential epigenomic and transcriptomic responses in subcutaneous adipose tissue between low and high responders to caloric restriction. Am J Clin Nutr 2010; 91: 309-320.
38. Kuzawa CW,. Fetal origins of developmental plasticity: Are fetal cues reliable predictors of future nutritional environments? Am J Hum Biol 2005; 17: 5-21.
39. Ramakrishnan U, Martorell R, Schroeder DG, Flores R,. Role of intergenerational effects on linear growth. J Nutr 1999; 129S: 544-549.
40. Fairburn CG, Welch SL, Doll HA, Davies BA, O'Connor ME,. Risk factors for bulimia nervosa. A community-based case-control study. Arch Gen Psychiatry 1997; 54: 509-517.
41. Painter RC, Roseboom TJ, Bleker OP,. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol 2005; 20: 345-352.
42. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci 2008; 105: 17046-17049.
43. Agis-Balboa RC, Arcos-Diaz D, Wittnam J, Govindarajan N, Blom K, Burkhardt S, Haladyniak U, et al. A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. EMBO J 2011; 30: 4071-4083.
44. Pidsley R, Mill J,. Epigenetic studies of psychosis: Current findings, methodological approaches, and implications for postmortem research. Biol Psychiatry 2011; 69: 146-156.
45. Pidsley R, Dempster EL, Mill J,. Brain weight in males is correlated with DNA methylation at IGF2. Mol Psychiatry 2010; 15: 880-881.
46. Braun JM, Kalkbrenner AE, Calafat AM, Yolton K, Ye X, Dietrich KN, et al. Impact of early-life bisphenol A exposure on behavior and executive function in children. Pediatrics 2011; 128: 873-882.
47. Kundakovic M, Gudsnuk K, Franks B, Madrid J, Miller RL, Perera FP, et al. Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci U S A 2013; 110: 9956-9961.
48. King S, Dancause K, Turcotte-Tremblay AM, Veru F, Laplante DP,. Using natural disasters to study the effects of prenatal maternal stress on child health and development. Birth Defects Res C Embryo Today 2012; 96: 273-288.
49. St-Hilaire A, Thaler L, Steiger H, Magill T, Liu A, Laplante D, et al. Prenatal maternal stress and bulimia-spectrum symptoms in offspring during early adolescence: A prospective study. Presented at the International Conference for Eating Disorders, New York, March 27-29, 2014.
50. Cnattingius S, Hultman CM, Dahl M, Sparen P,. Very preterm birth, birth trauma, and the risk of anorexia nervosa among girls. Arch Gen Psychiatry 1999; 56: 634-638.
51. Favaro A, Tenconi E, Santonastaso P,. Perinatal factors and the risk of developing anorexia nervosa and bulimia nervosa. Arch Gen Psychiatry 2006; 6: 82-88.
52. Levine S, Alpert M, Lewis GW,. Infantile experience and the maturation of the pituitary adrenal axis. Science 1957; 126: 1347.
53. Denenberg VH,. Critical periods, stimulus input, and emotional reactivity: A theory of infantile stimulation. Psychol Rev 1964; 71: 335-351.
54. Kosten TA, Kim JJ, Lee HJ,. Early life manipulations alter learning and memory in rats. Neurosci Biobehav Rev 2012; 36: 1985-2006.
55. Curley JP, Jensen CL, Mashoodh R, Champagne FA,. Social influences on neurobiology and behavior: Epigenetic effects during development. Psychoneuroendocrinology 2011; 36: 352-71.
56. Champagne FA,. Early environment, glucocorticoid receptors, and behavioral genetics. Behav Neurosci 2013; 127: 628-636.
57. Szyf M, Weaver I, Meaney M,. Maternal care, the epigenome, and phenotypic differences in behavior. Reprod Toxicol 2007; 24: 9-19.
58. Champagne FA,. Epigenetic influence of social experiences across the lifespan. Dev Psychobiol 2011; 52: 299-311.
59. Champagne FA,. Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 2008; 29: 386-397.
60. Curley JP, Davidson S, Bateson P, Champagne FA,. Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice. Front Behav Neurosci 2009; 3: 25.
61. Weaver IC, Meaney MJ, Szyf M,. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci U S A 2006; 103: 3480-34855.
62. Alter M, Gilani AI, Champagne FA, Curley JP, Turner JB, Hen R,. Paternal transmission of complex phenotypes in inbred mice. Bioll Psychiatry 2009; 66: 1061-1066.
63. Franklin TB, Russig H, Weiss IC, Graff J, Linder N, Michalon A, et al. Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 2010; 68: 408-415.
64. Franklin TB, Linder N, Russig H, Thöny B, Mansuy IM,. Influence of early stress on social abilities and serotonergic functions across generations in mice. PLoS One 2011; 6: e21842
65. Lambrot R, Xu C, Saint-Phar S, Chountalos G, Cohen T, Paquet M, et al. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun 2013; 4: 2889.
66. Mashoodh R, Franks B, Curley JP, Champagne FA,. Paternal social enrichment effects on maternal behavior and offspring growth. Proc Natl Acad Sci U S A 2012; 109 (SUPPL. 2): 17232-17238.
67. Keller EF,. The Century of the Gene. Cambridge, MA: Harvard University Press, 2000.
68. Tozzi F, Thornton LM, Klump KL, Fichter MM, Halmi KA, Kaplan AS, et al. Symptom fluctuation in eating disorders: Correlates of diagnostic crossover. Am J Psychiatry 2005; 162: 732-740.
69. Dellava JE, Kendler KS, Neale MC,. Generalized anxiety disorder and anorexia nervosa: evidence of shared genetic variation. Depress Anxiety 2011; 28: 728-733.
70. Thornton LM, Dellava JE, Root TL, Lichtenstein P, Bulik CM,. Anorexia nervosa and generalized anxiety disorder: Further explorations of the relation between anxiety and body mass index. J Anxiety Disord 2011; 25: 727-730.
71. Raney TJ, Thornton LM, Berrettini W, Brandt H, Crawford S, Fichter MM, et al. Influence of overanxious disorder of childhood on the expression of anorexia nervosa. Int J Eat Disord 2008; 41: 326-332.
72. Dellava JE, Thornton LM, Hamer RM, Strober M, Plotnicov K, Klump KL, Brandt H, et al. Childhood anxiety associated with low BMI in women with anorexia nervosa. Behav Res Ther 2010; 48: 60-67.
73. Falloon IR,. Family interventions for mental disorders: Efficacy and effectiveness. World Psychiatry 2003; 2: 20-28.
74. Miklowitz DJ, Schneck CD, Singh MK, Taylor DO, George EL, Cosgrove VE, Howe ME, et al. Early intervention for symptomatic youth at risk for bipolar disorder: A randomized trial of family-focused therapy. J Am Acad Child Adolesc Psychiatry 2013; 52: 121-131.
75. Peris TS, Piacentini J,. Optimizing treatment for complex cases of childhood obsessive compulsive disorder: A preliminary trial. J Clin Child Adolesc Psychol 2013; 42: 1-8.
76. Guifang J, Fu Y, Zhao X, Dai Q, Zheng G, Yang Y, et al. N6-Methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol 2011; 7: 885-887.
77. Barbarich-Marsteller NC, Underwood MD, Foltin RW, Myers MM, Walsh BT, Barrett JS, et al. Identifying novel phenotypes of vulnerability and resistance to activity-based anorexia in adolescent female rats. Int J Eat Disord 2013; 46: 737-746.
78. Gutierrez E,. A rat in the labyrinth of anorexia nervosa: Contributions of the activity-based anorexia rodent model to the understanding of anorexia nervosa. Int J Eat Disord 2013; 46: 289-301.