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

Published online by Cambridge University Press:  14 May 2012

Z. Y. Ong ,
J. R. Gugusheff  and
B. S. Muhlhausler
Z. Y. Ong
Affiliation:
Sansom Institute for Health Research, School of Pharmacy and Medical Sciences, University of South Australia, Adelaide, South Australia, Australia FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Adelaide, South Australia, Australia
J. R. Gugusheff
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Adelaide, South Australia, Australia
B. S. Muhlhausler*
Affiliation:
Sansom Institute for Health Research, School of Pharmacy and Medical Sciences, University of South Australia, Adelaide, South Australia, Australia FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Adelaide, South Australia, Australia
*
*Address for correspondence: Dr B. S. Muhlhausler, FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Adelaide 5064, South Australia, Australia. Email beverly.muhlhausler@adelaide.edu.au
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Abstract

One of the major contributing factors to the continuous rise in obesity rates is the increase in caloric intake, which is driven to a large extent by the ease of access and availability of palatable high-fat, high-sugar ‘junk foods’. It is also clear that some individuals are more likely to overindulge in these foods than others; however, the factors that determine an individual's susceptibility towards the overconsumption of palatable foods are not well understood. There is growing evidence that an increased preference for these foods may have its origins early in life. Recent work from our group and others has reported that in utero and early life exposure to these palatable foods in rodents increased the offspring's preference towards foods high in fat and sugar. One of the potential mechanisms underlying the programming of food preferences is the altered development of the mesolimbic reward system, a system that plays an important role in driving palatable food intake in adults. The aim of this review is to explore the current knowledge of the programming of food preferences, a relatively new and emerging area in the DOHAD field, with a particular focus on maternal overnutrition, the development of the mesolimbic reward system and the biological mechanisms which may account for the early origins of an increased preference for palatable foods.

Keywords

dopamineopioidprogrammingreward
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 3 , Issue 5 , October 2012 , pp. 299 - 308
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012

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References

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 Google Scholar
2. Thiele, S, Mensink, GB, Beitz, R. Determinants of diet quality. Public Health Nutr. 2004; 7, 29–37.CrossRefGoogle ScholarPubMed
3. Vicennati, V, Pasqui, F, Cavazza, C, et al. . Cortisol, energy intake, and food frequency in overweight/obese women. Nutrition. 2011; 27, 677–680.Google Scholar
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.CrossRefGoogle ScholarPubMed
5. Drewnowski, A, Brunzell, JD, Sande, K, et al. . Sweet tooth reconsidered: taste responsiveness in human obesity. Physiol Behav. 1985; 35, 617–622.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
9. Johnson, PM, Kenny, PJ. Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci. 2010; 13, 635–641.CrossRefGoogle ScholarPubMed
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.Google Scholar
11. Wang, GJ, Volkow, ND, Logan, J, et al. . Brain dopamine and obesity. The Lancet. 2001; 357, 354–357.Google Scholar
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.CrossRefGoogle ScholarPubMed
13. Volkow, ND, Wise, RA. How can drug addiction help us understand obesity? Nat Neurosci. 2005; 8, 555–560.CrossRefGoogle ScholarPubMed
14. Nestler, EJ. Is there a common molecular pathway for addiction? Nat Neurosci. 2005; 8, 1445–1449.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
23. Chang, G-Q, Gaysinskaya, V, Karatayev, O, et al. . Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci. 2008; 28, 12107–12119.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
32. Smidt, MP, Burbach, JPH. How to make a mesodiencephalic dopaminergic neuron. Nat Rev Neurosci. 2007; 8, 21–32.Google Scholar
33. Van den Heuvel, DMA, Pasterkamp, RJ. Getting connected in the dopamine system. Prog Neurobiol. 2008; 85, 75–93.CrossRefGoogle ScholarPubMed
34. Tepper, JM, Sharpe, NA, Koós, TZ, et al. . Postnatal development of the rat neostriatum: electrophysiological, light- and electron-microscopic studies. Dev Neurosci. 1998; 20, 125–145.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
37. Herlenius, E, Lagercrantz, H. Neurotransmitters and neuromodulators during early human development. Early Hum Dev. 2001; 65, 21–37.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
40. Meng, SZ, Ozawa, Y, Itoh, M, et al. . Developmental and age-related changes of dopamine transporter, and dopamine D1 and D2 receptors in human basal ganglia. Brain Res. 1999; 843, 136–144.Google Scholar
41. McDowell, J, Kitchen, I. Development of opioid systems: peptides, receptors and pharmacology. Brain Res Rev. 1987; 12, 397–421.Google Scholar
42. Spain, J, Roth, B, Coscia, C. Differential ontogeny of multiple opioid receptors (mu, delta, and kappa). J Neurosci. 1985; 5, 584–588.Google Scholar
43. Kornblum, HI, Hurlbut, DE, Leslie, FM. Postnatal development of multiple opioid receptors in rat brain. Dev Brain Res. 1987; 37, 21–41.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
47. Erlanson-Albertsson, C. How palatable food disrupts appetite regulation. Basic Clin Pharmacol Toxicol. 2005; 97, 61–73.Google Scholar
48. Ahima, RS, Flier, JS. Leptin. Annu Rev Physiol. 2000; 62, 413–437.Google Scholar
49. Woods, SC, Seeley, RJ, Porte, D, et al. . Signals that regulate food intake and energy homeostasis. Science. 1998; 280, 1378–1383.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
51. Hommel, JD, Trinko, R, Sears, RM, et al. . Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron. 2006; 51, 801–810.Google Scholar
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.Google Scholar
53. Proulx, K, Richard, D, Walker, C-D. Leptin regulates appetite-related neuropeptides in the hypothalamus of developing rats without affecting food intake. Endocrinology. 2002; 143, 4683–4692.CrossRefGoogle ScholarPubMed
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.Google Scholar
55. Bouret, SG, Draper, SJ, Simerly, RB. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science. 2004; 304, 108–110.CrossRefGoogle ScholarPubMed
56. Roseberry, AG, Painter, T, Mark, GP, et al. . Decreased vesicular somatodendritic dopamine stores in leptin-deficient mice. J Neurosci. 2007; 27, 7021–7027.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
71. Zhen, J, Reith, ME, Carr, KD. Chronic food restriction and dopamine transporter function in rat striatum. Brain Res. 2006; 1082, 98–101.Google Scholar
72. Speed, N, Saunders, C, Davis, AR, et al. . Impaired striatal Akt signaling disrupts dopamine homeostasis and increases feeding. PLoS ONE. 2011; 6, e25169.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
76. Kirby, ML, Aronstam, RS. Levorphanol-sensitive [3 H]naloxone binding in developing brainstem following prenatal morphine exposure. Neurosci Lett. 1983; 35, 191–195.Google Scholar
77. Handelmann, GE, Quirion, R. Neonatal exposure to morphine increases [mu] opiate binding in the adult forebrain. Eur J Pharmacol. 1983; 94, 357–358.Google Scholar
78. Vathy, I, Slamberová, R, Rimanóczy, Á, 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.Google Scholar
79. Burford, NT, Tolbert, LM, Sadee, W. Specific G protein activation and μ-opioid receptor internalization caused by morphine, DAMGO and endomorphin I. Eur J Pharmacol. 1998; 342, 123–126.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
82. Chandorkar, GA, Ampasavate, C, Stobaugh, JF, et al. . Peptide transport and metabolism across the placenta. Adv Drug Delivery Rev. 1999; 38, 59–67.Google Scholar
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.Google Scholar
84. Stickrod, G, Kimble, DP, Smotherman, WP. Met-enkephalin effects on associations formed in utero. Peptides. 1982; 3, 881–883.Google Scholar
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.Google Scholar
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.Google Scholar