Perinatal overnutrition and the programming of food preferences: Pathways and mechanisms

Journal of Developmental Origins of Health and Disease

Volumn 3, Issue 5, 2012, Pages 299-308

  Ong, Z Y ^a,b   Gugusheff, J R ^b   Muhlhausler, B S ^a,b  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Dopamine; Opioid; Programming; Reward

Indexed keywords

DOPAMINE RECEPTOR; INSULIN; LEPTIN; OPIATE RECEPTOR;

ADULT; ANIMAL; FEEDING BEHAVIOR; FEMALE; FETUS DEVELOPMENT; HUMAN; LIMBIC SYSTEM; MATERNAL NUTRITION; METABOLISM; OBESITY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; RAT;

ADULT; ANIMALS; FEMALE; FETAL DEVELOPMENT; FOOD HABITS; HUMANS; INSULIN; LEPTIN; LIMBIC SYSTEM; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RECEPTORS, DOPAMINE; RECEPTORS, OPIOID;

EID: 84888332084     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S204017441200030X     Document Type: Review

References (86)

1. WHO. World Health Organisation fact sheet: obesity and overweight, 2011. Retrieved 15 October 2011 from http:// www.who.int/mediacentre/factsheets/fs311/ en/index.html
2. Thiele S, Mensink GB, Beitz R. Determinants of diet quality. Public Health Nutr. 2004; 7, 29-37. (Pubitemid 38294525)
3. Vicennati V, Pasqui F, Cavazza C, et al. Cortisol, energy intake, and food frequency in overweight/obese women. Nutrition. 2011; 27, 677-680.
4. Drewnowski A, Krahn DD, Demitrack MA, et al. Taste responses and preferences for sweet high-fat foods: evidence for opioid involvement. Physiol Behav. 1992; 51, 371-379.
5. Drewnowski A, Brunzell JD, Sande K, et al. Sweet tooth reconsidered: taste responsiveness in human obesity. Physiol Behav. 1985; 35, 617-622. (Pubitemid 16237717)
6. Pasquet P, Frelut ML, Simmen B, et al. Taste perception in massively obese and in non-obese adolescents. Int J Pediatr Obes. 2007; 2, 242-248. (Pubitemid 350153998)
7. Bayol S, Simbi B, Bertrand J, et al. Offspring from mothers fed a 'junk food'diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females. J Physiol. 2008; 586, 3219-3230. (Pubitemid 351984701)
8. Brion M-JA, Ness AR, Rogers I, et al. Maternal macronutrient and energy intakes in pregnancy and offspring intake at 10 y: exploring parental comparisons and prenatal effects. Am J Clin Nutr. 2010; 91, 748-756.
9. Johnson PM, Kenny PJ. Dopamine D2 receptors in addictionlike reward dysfunction and compulsive eating in obese rats. Nat Neurosci. 2010; 13, 635-641.
10. South T, Huang XF. High-fat diet exposure increases dopamine D2 receptor and decreases dopamine transporter receptor binding density in the nucleus accumbens and caudate putamen of mice. Neurochem Res. 2008; 33, 598-605. (Pubitemid 351230463)
11. Wang GJ, Volkow ND, Logan J, et al. Brain dopamine and obesity. The Lancet. 2001; 357, 354-357. (Pubitemid 32128542)
12. Volkow ND, Wang GJ, Fowler JS, et al. Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Lond B Biol Sci. 2008; 363, 3191-3200.
13. Volkow ND, Wise RA. How can drug addiction help us understand obesity? Nat Neurosci. 2005; 8, 555-560. (Pubitemid 40594193)
14. Nestler EJ. Is there a common molecular pathway for addiction? Nat Neurosci. 2005; 8, 1445-1449. (Pubitemid 41573654)
15. Gainetdinov RR, Jones SR, Fumagalli F, et al. Re-evaluation of the role of the dopamine transporter in dopamine system homeostasis. Brain Res Rev. 1998; 26, 148-153. (Pubitemid 28318071)
16. Boney CM, Verma A, Tucker R, et al. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005; 115, e290-e296. (Pubitemid 43373011)
17. Ravelli GP, Stein ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med. 1976; 295, 349-353.
18. Yura S, Itoh H, Sagawa N, et al. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab. 2005; 1, 371-378. (Pubitemid 43960627)
19. Bayol SA, Farrington SJ, Stickland NC. A maternal "junk food" diet in pregnancy and lactation promotes an exacerbated taste for "junk food" and a greater propensity for obesity in rat offspring. Br J Nutr. 2007; 98, 843-851. (Pubitemid 47487954)
20. Ehrenberg HM, Mercer BM, Catalano PM. The influence of obesity and diabetes on the prevalence of macrosomia. Am J Obstet Gynecol. 2004; 191, 964-968. (Pubitemid 39298142)
21. Sobngwi E, Boudou P, Mauvais-Jarvis F, et al. Effect of a diabetic environment in utero on predisposition to type 2 diabetes. The Lancet. 2003; 361, 1861-1865. (Pubitemid 36645181)
22. Li M, Sloboda DM, Vickers MH. Maternal obesity and developmental programming of metabolic disorders in offspring: evidence from animal models. Exp Diabetes Res. 2011; 2011, Article ID 592408, 9pp, doi:10.1155/2011/592408.
23. Chang G-Q, Gaysinskaya V, Karatayev O, et al. Maternal highfat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci. 2008; 28, 12107-12119.
24. Chen H, Simar D, Morris MJ. Hypothalamic neuroendocrine circuitry is programmed by maternal obesity: interaction with postnatal nutritional environment. PLoS ONE. 2009; 4, e6259.
25. Kirk SL, Samuelsson A-M, Argenton M, et al. Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLoS ONE. 2009; 4, e5870.
26. Page KC, Malik RE, Ripple JA, et al. Maternal and postweaning diet interaction alters hypothalamic gene expression and modulates response to a high-fat diet in male offspring. Am J Physiol Regul Intergr Comp Physiol. 2009; 297, R1049-R1057.
27. Ong Z, Muhlhausler B. Maternal "junk-food" feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. The FASEB Journal. 2011; 25, 2167-2179.
28. Vucetic Z, Kimmel J, Totoki K, et al. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology. 2010; 151, 4756-4764.
29. Wardle J, Guthrie C, Sanderson S, et al. Food and activity preferences in children of lean and obese parents. Int J Obes Relat Metab Disord. 2001; 25, 971-977. (Pubitemid 32566050)
30. Teegarden SL, Scott AN, Bale TL. Early life exposure to a high fat diet promotes long-term changes in dietary preferences and central reward signaling. Neuroscience. 2009; 162, 924-932.
31. Antonopoulos J, Dori I, Dinopoulos A, et al. Postnatal development of the dopaminergic system of the striatum in the rat. Neuroscience. 2002; 110, 245-256. (Pubitemid 34214943)
32. Smidt MP, Burbach JPH. How to make a mesodiencephalic dopaminergic neuron. Nat Rev Neurosci. 2007; 8, 21-32. (Pubitemid 46011996)
33. Van den Heuvel DMA, Pasterkamp RJ. Getting connected in the dopamine system. Prog Neurobiol. 2008; 85, 75-93.
34. Tepper JM, Sharpe NA, Koós TZ, et al. Postnatal development of the rat neostriatum: electrophysiological, light- and electronmicroscopic studies. Dev Neurosci. 1998; 20, 125-145. (Pubitemid 28349869)
35. Schambra UB, Duncan GE, Breese GR, et al. Ontogeny of D1a and D2 dopamine receptor subtypes in rat brain using in situ hybridization and receptor binding. Neuroscience. 1994; 62, 65-85.
36. Tarazi FI, Baldessarini RJ. Comparative postnatal development of dopamine D1, D2 and D4 receptors in rat forebrain. Int J Dev Neurosci. 2000; 18, 29-37. (Pubitemid 30116706)
37. Herlenius E, Lagercrantz H. Neurotransmitters and neuromodulators during early human development. Early Hum Dev. 2001; 65, 21-37. (Pubitemid 32743368)
38. Brana C, Charron G, Aubert I, et al. Ontogeny of the striatal neurons expressing neuropeptide genes in the human fetus and neonate. J Comp Neurol. 1995; 360, 488-505.
39. Brana C, Aubert I, Charron G, et al. Ontogeny of the striatal neurons expressing the D2 dopamine receptor in humans: an in situ hybridization and receptor-binding study. Mol Brain Res. 1997; 48, 389-400. (Pubitemid 27394926)
40. Meng SZ, Ozawa Y, Itoh M, et al. Developmental and agerelated changes of dopamine transporter, and dopamine D1 and D2 receptors in human basal ganglia. Brain Res. 1999; 843, 136-144. (Pubitemid 29488704)
41. McDowell J, Kitchen I. Development of opioid systems: peptides, receptors and pharmacology. Brain Res Rev. 1987; 12, 397-421. (Pubitemid 17152528)
42. Spain J, Roth B, Coscia C. Differential ontogeny of multiple opioid receptors (mu, delta, and kappa). J Neurosci. 1985; 5, 584-588. (Pubitemid 15100447)
43. Kornblum HI, Hurlbut DE, Leslie FM. Postnatal development of multiple opioid receptors in rat brain. Dev Brain Res. 1987; 37, 21-41. (Pubitemid 18000138)
44. Magnan J, Tiberi M. Evidence for the presence of [mu]-and [kappa]-but not of [delta]-opioid sites in the human fetal brain. Dev Brain Res. 1989; 45, 275-281. (Pubitemid 19045215)
45. Naef L, Moquin L, Dal Bo G, et al. Maternal high-fat intake alters presynaptic regulation of dopamine in the nucleus accumbens and increases motivation for fat rewards in the offspring. Neuroscience. 2011; 176, 225-236.
46. Beauchamp GK, Mennella JA. Early flavor learning and its impact on later feeding behavior. J Pediatr Gastroenterol Nutr. 2009; 48(Suppl 1), S25-S30.
47. Erlanson-Albertsson C. How palatable food disrupts appetite regulation. Basic Clin Pharmacol Toxicol. 2005; 97, 61-73. (Pubitemid 41021104)
48. Ahima RS, Flier JS. Leptin. Annu Rev Physiol. 2000; 62, 413-437. (Pubitemid 30618269)
49. Woods SC, Seeley RJ, Porte D, et al. Signals that regulate food intake and energy homeostasis. Science. 1998; 280, 1378-1383. (Pubitemid 28264819)
50. Figlewicz DP, Evans SB, Murphy J, et al. Expression of receptors for insulin and leptin in the ventral tegmental area/ substantia nigra (VTA/SN) of the rat. Brain Res. 2003; 964, 107-115. (Pubitemid 36165075)
51. Hommel JD, Trinko R, Sears RM, et al. Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron. 2006; 51, 801-810. (Pubitemid 44374908)
52. Figlewicz DP, Bennett J, Evans SB, et al. Intraventricular insulin and leptin reverse place preference conditioned with high-fat diet in rats. Behav Neurosci. 2004; 118, 479-487. (Pubitemid 38685315)
53. Proulx K, Richard D, Walker C-D. Leptin regulates appetiterelated neuropeptides in the hypothalamus of developing rats without affecting food intake. Endocrinology. 2002; 143, 4683-4692. (Pubitemid 35397610)
54. Ahima RS, Prabakaran D, Flier JS. Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest. 1998; 101, 1020-1027. (Pubitemid 28125280)
55. Bouret SG, Draper SJ, Simerly RB. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science. 2004; 304, 108-110. (Pubitemid 38451467)
56. Roseberry AG, Painter T, Mark GP, et al. Decreased vesicular somatodendritic dopamine stores in leptin-deficient mice. J Neurosci. 2007; 27, 7021-7027. (Pubitemid 47015890)
57. Sánchez J, Priego T, Palou M, et al. Oral supplementation with physiological doses of leptin during lactation in rats improves insulin sensitivity and affects food preferences later in life. Endocrinology. 2008; 149, 733-740. (Pubitemid 351159328)
58. Zheng H, Corkern M, Stoyanova I, et al. Appetite-inducing accumbens manipulation activates hypothalamic orexin neurons and inhibits POMC neurons. Am J Physiol Regul Intergr Comp Physiol. 2003; 284, R1436-R1444. (Pubitemid 36617482)
59. Vittoz NM, Berridge CW. Hypocretin/orexin selectively increases dopamine efflux within the prefrontal cortex: involvement of the ventral aegmental area. Neuropsychopharmacology. 2005; 31, 384-395. (Pubitemid 43113402)
60. Korotkova TM, Sergeeva OA, Eriksson KS, et al. Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexins/hypocretins. J Neurosci. 2003; 23, 7-11. (Pubitemid 36050397)
61. Zheng H, Patterson LM, Berthoud H-R. Orexin signaling in the ventral tegmental area is required for high-fat appetite induced by opioid stimulation of the nucleus accumbens. J Neurosci. 2007; 27, 11075-11082. (Pubitemid 47574162)
62. Kelley AE, Baldo BA, Pratt WE. A proposed hypothalamic-thalamic-striatal axis for the integration of energy balance, arousal, and food reward. J Comp Neurol. 2005; 493, 72-85. (Pubitemid 41636189)
63. Beck B, Kozak R, Moar KM, et al. Hypothalamic orexigenic peptides are overexpressed in young Long-Evans rats after early life exposure to fat-rich diets. Biochem Biophys Res Commun. 2006; 342, 452-458. (Pubitemid 43289013)
64. Recio-Pinto E, Rechler MM, Ishii DN. Effects of insulin, insulin-like growth factor-II, and nerve growth factor on neurite formation and survival in cultured sympathetic and sensory neurons. J Neurosci. 1986; 6, 1211-1219. (Pubitemid 16078010)
65. Baron-Van Evercooren A, Olichon-Berthe C, Kowalski A, et al. Expression of IGF-I and insulin receptor genes in the rat central nervous system: a developmental, regional, and cellular analysis. J Neurosci Res. 1991; 28, 244-253.
66. Harder T, Plagemann A, Rohde W, et al. Syndrome X-like alterations in adult female rats due to neonatal insulin treatment. Metabolism. 1998; 47, 855-862. (Pubitemid 28313195)
67. Plagemann A, Harder T, Janert U, et al. Malformations of hypothalamic nuclei in hyperinsulinemic offspring of rats with gestational diabetes. Dev Neurosci. 1999; 21, 58-67. (Pubitemid 29121751)
68. Patterson TA, Brot MD, Zavosh A, et al. Food deprivation decreases mRNA and activity of the rat dopamine transporter. Neuroendocrinology. 1998; 68, 11-20. (Pubitemid 28310604)
69. Owens WA, Sevak RJ, Galici R, et al. Deficits in dopamine clearance and locomotion in hypoinsulinemic rats unmask novel modulation of dopamine transporters by amphetamine. J Neurochem. 2005; 94, 1402-1410. (Pubitemid 41232595)
70. Sevak RJ, Koek W, Owens WA, et al. Feeding conditions differentially affect the neurochemical and behavioral effects of dopaminergic drugs in male rats. Eur J Pharmacol. 2008; 592, 109-115.
71. Zhen J, Reith ME, Carr KD. Chronic food restriction and dopamine transporter function in rat striatum. Brain Res. 2006; 1082, 98-101.
72. Speed N, Saunders C, Davis AR, et al. Impaired striatal Akt signaling disrupts dopamine homeostasis and increases feeding. PLoS ONE. 2011; 6, e25169.
73. Figlewicz DP, Bennett JL, Naleid AM, et al. Intraventricular insulin and leptin decrease sucrose self-administration in rats. Physiol Behav. 2006; 89, 611-616. (Pubitemid 44634584)
74. Vathy I, Slamberova R, Rimanoczy A, et al. Autoradiographic evidence that prenatal morphine exposure sex-dependently alters [mu]-opioid receptor densities in brain regions that are involved in the control of drug abuse and other motivated behaviors. Prog Neuropsychopharmacol Biol Psychiatry. 2003; 27, 381-393. (Pubitemid 36403729)
75. Tempel A, Habas JE, Paredes W, et al. Morphine-induced downregulation of [mu]-opioid receptors in neonatal rat brain. Dev Brain Res. 1988; 41, 129-133.
76. Kirby ML, Aronstam RS. Levorphanol-sensitive [3 H]naloxone binding in developing brainstem following prenatal morphine exposure. Neurosci Lett. 1983; 35, 191-195. (Pubitemid 13120726)
77. Handelmann GE, Quirion R. Neonatal exposure to morphine increases [mu] opiate binding in the adult forebrain. Eur J Pharmacol. 1983; 94, 357-358.
78. Vathy I, Slamberová R, Rimanóczy A, et al. Autoradiographic evidence that prenatal morphine exposure sex-dependently alters [mu]-opioid receptor densities in brain regions that are involved in the control of drug abuse and other motivated behaviors. Prog Neuropsychopharmacol Biol Psychiatry. 2003; 27, 381-393. (Pubitemid 36403729)
79. Burford NT, Tolbert LM, Sadee W. Specific G protein activation and m-opioid receptor internalization caused by morphine, DAMGO and endomorphin I. Eur J Pharmacol. 1998; 342, 123-126. (Pubitemid 28131354)
80. Keith DE, Murray SR, Zaki PA, et al. Morphine activates opioid receptors without causing their rapid internalization. J Biol Chem. 1996; 271, 19021-19024. (Pubitemid 26271556)
81. Chang GQ, Karatayev O, Barson JR, et al. Increased enkephalin in brain of rats prone to overconsuming a fat-rich diet. Physiol Behav. 2010; 101, 360-369.
82. Chandorkar GA, Ampasavate C, Stobaugh JF, et al. Peptide transport and metabolism across the placenta. Adv Drug Delivery Rev. 1999; 38, 59-67. (Pubitemid 29216953)
83. Kastin AJ, Kostrzewa RM, Schally AV, et al. Neonatal administration of met-enkephalin facilitates maze performance of adult rats. Pharmacol Biochem and Behav. 1980; 13, 883-886.
84. Stickrod G, Kimble DP, Smotherman WP. Met-enkephalin effects on associations formed in utero. Peptides. 1982; 3, 881-883. (Pubitemid 13184716)
85. Vucetic Z, Carlin J, Totoki K, et al. Epigenetic dysregulation of the dopamine system in diet-induced obesity. J Neurochem. 2012; 120, 891-898.
86. Vucetic Z, Kimmel J, Reyes TM. Chronic high-fat diet drives postnatal epigenetic regulation of mu-opioid receptor in the brain. Neuropsychopharmacology 36 2011, 1199-1206.