A maternal "junk-food" diet reduces sensitivity to the opioid antagonist naloxone in offspring postweaning

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 1275-1284

  Gugusheff, Jessica R ^a   Ong, Zhi Yi ^a,b   Muhlhausler, Beverly S ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Fetal programming; High fat diet; Reward

Indexed keywords

MESSENGER RNA; MU OPIATE RECEPTOR; NALOXONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CONTROLLED STUDY; DRUG SENSITIVITY; ENVIRONMENTAL EXPOSURE; FAT INTAKE; FEMALE; FOOD; JUNK FOOD; MALE; MATERNAL NUTRITION; NONHUMAN; NUTRITION; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT; VENTRAL TEGMENTUM; WEANING;

ANIMALS; ANIMALS, NEWBORN; DIETARY FATS; EATING; FEMALE; MALE; NALOXONE; NARCOTIC ANTAGONISTS; RATS; RATS, WISTAR; RECEPTORS, OPIOID, MU;

EID: 84874593614     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-217653     Document Type: Article

References (40)

1. Bayol, S. A., Farrington, S. J., and Stickland, N. C. (2007) 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. Brit. J. Nut. 98, 843-851 (Pubitemid 47487954)
2. Ong, Z. Y., and Muhlhausler, B. S. (2011) Maternal "junk-food" feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. FASEB J. 25, 2167-2179
3. Vucetic, Z., Kimmel, J., Totoki, K., Hollenbeck, E., and Reyes, T. M. (2010) Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151, 4756-4764
4. Naef, L., Srivastava, L., Gratton, A., Hendrickson, H., Owens, S., and Walker, C.-D. (2008) Maternal high fat diet during the perinatal period alters mesocorticolimbic dopamine in the adult rat offspring: reduction in the behavioral responses to repeated amphetamine administration. Psychopharmacology (Berl.) 197, 83-94
5. Teegarden, S. L., Scott, A. N., and Bale, T. L. (2009) Early life exposure to a high fat diet promotes long-term changes in dietary preferences and central reward signaling. Neuroscience 162, 924-932
6. Kelley, A. E., Bakshi, V. P., Haber, S. N., Steininger, T. L., Will, M. J., and Zhang, M. (2002) Opioid modulation of taste hedonics within the ventral striatum. Physiol. Behav. 76, 365-377 (Pubitemid 34765590)
7. Van Ree, J. M., Niesink, R. J. M., Van Wolfswinkel, L., Ramsey, N. F., Kornet, M. M. W., Van Furth, W. R., Vanderschuren, L. J. M. J., Gerrits, M. A. F. M., and Van den Berg, C. L. (2000) Endogenous opioids and reward. Eur. J. Pharmacol. 405, 89-101
8. Zhang, M., Gosnell, B. A., and Kelley, A. E. (1998) Intake of high-fat food is selectively enhanced by muopioid receptor stimulation within the nucleus accumbens. J. Pharmacol. Exp. Ther. 285, 908-914 (Pubitemid 28237478)
9. Giraudo, S. Q., Grace, M. K., Welch, C. C., Billington, C. J., and Levine, A. S. (1993) Naloxone's anorectic effect is dependent upon the relative palatability of food. Pharmacol. Biochem. Behav. 46, 917-921
10. Bergevin, A., Girardot, D., Bourque, M.-J., and Trudeau, L.-E. (2002) Presynaptic μ-opioid receptors regulate a late step of the secretory process in rat ventral tegmental area GABAergic neurons. Neuropharmacology 42, 1065-1078 (Pubitemid 34786559)
11. Sampey, B. P., Vanhoose, A. M., Winfield, H. M., Freemerman, A. J., Muehlbauer, M. J., Fueger, P. T., Newgard, C. B., and Makowski, L. (2011) Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity 19, 1109-1117
12. Kelley, A., Will, M., Steininger, T., Zhang, M., and Haber, S. (2003) Restricted daily consumption of a highly palatable food (chocolate Ensure®) alters striatal enkephalin gene expression. Eur. J. Neurosci. 18, 2592-2598 (Pubitemid 37455408)
13. Colantuoni, C., Rada, P., McCarthy, J., Patten, C., Avena, N. M., Chadeayne, A., and Hoebel, B. G. (2002) Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obesity 10, 478-488 (Pubitemid 135686640)
14. Chandorkar, G. A., Ampasavate, C., Stobaugh, J. F., and Audus, K. L. (1999) Peptide transport and metabolism across the placenta. Adv. Drug. Delivery Rev. 38, 59-67 (Pubitemid 29216953)
15. Lindemalm, S., Nydert, P., Svensson, J.-O., Stahle, L., and Sarman, I. (2009) Transfer of buprenorphine into breast milk and calculation of infant drug dose. J. Hum. Lact. 25, 199-205
16. Robieux, I., Koren, G., Vandenbergh, H., and Schneiderman, J. (1990) Morphine excretion in breast milk and resultant exposure of a nursing infant. Clin. Toxicol. 28, 365-370
17. Marks-Kaufman, R., and Kanarek, R. B. (1981) Modifications of nutrient selection induced by naloxone in rats. Psychopharmacology (Berl.) 74, 321-324 (Pubitemid 11003749)
18. Repke, J. T., and Villar, J. (1991) Pregnancy-induced hypertension and low birth weight: the role of calcium. Am. J. Clin. Nutr. 54, 237S-241S
19. Takaya, J., Yamato, F., and Kaneko, K. (2006) Possible relationship between low birth weight and magnesium status: from the standpoint of "fetal origin" hypothesis. Magnes. Res. 19, 63-69 (Pubitemid 43945612)
20. Bellinger, L., Lilley, C., and Langley-Evans, S. C. (2004) Prenatal exposure to a maternal low-protein diet programmes a preference for high-fat foods in the young adult rat. Brit. J. Nut. 92, 513-520 (Pubitemid 40277073)
21. Zambrano, E., Bautista, C., Deas, M., Martínez Samayoa, P., González Zamorano, M., Ledesma, H., Morales, J., Larrea, F., and Nathanielsz, P. (2006) A low maternal protein diet during pregnancy and lactation has sex and window of exposure specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J. Physiol. 571, 221-230
22. Bardo, M. T., Bhatnagar, R. K., and Gebhart, G. F. (1981) Opiate receptor ontogeny and morphine-induced effects: influence of chronic footshock stress in preweanling rats. Dev. Brain Res. 1, 487-495 (Pubitemid 11063483)
23. Zhu, Y., Hsu, M.-S., and Pintar, J. E. (1998) Developmental expression of the μ, κ, and δ opioid receptor mRNAs in mouse. J. Neurosci. 18, 2538-2549 (Pubitemid 28141801)
24. Bardo, M. T., Bhatnagar, R. K., and Gebhart, G. F. (1983) Age-related differences in the effect of chronic administration of naloxone on opiate binding in rat brain. Neuropharmacology 22, 453-461 (Pubitemid 13080548)
25. Brands, B., Thornhill, J. A., Hirst, M., and Gowdey, C. W. (1979) Suppression of food intake and body weight gain by naloxone in rats. Life Sci. 24, 1773-1778 (Pubitemid 9242164)
26. Cooper, S. J. (1980) Naloxone: Effects on food and water consumption in the non-deprived and deprived rat. Psychopharmacology (Berl.) 71, 1-6 (Pubitemid 11226277)
27. Berkowitz, B. A., Ngai, S. H., Hempstead, J., and Spector, S. (1975) Disposition of naloxone: use of a new radioimmunoassay. J. Pharmacol. Exp. Ther. 195, 499-504
28. Sakaguchi, T., Takahashi, M., and Bray, G. (1988) Diurnal changes in sympathetic activity. Relation to food intake and to insulin injected into the ventromedial or suprachiasmatic nucleus. J. Clin. Invest. 82, 282
29. Glass, M. J., Grace, M., Cleary, J. P., Billington, C. J., and Levine, A. S. (1996) Potency of naloxone's anorectic effect in rats is dependent on diet preference. Am. J. Physiol. Regul. Intergr. Comp. Physiol. 271, R217-R221
30. Marks-Kaufman, R., Plager, A., and Kanarek, R. B. (1985) Central and peripheral contributions of endogenous opioid systems to nutrient selection in rats. Psychopharmacology (Berl.) 85, 414-418 (Pubitemid 15075590)
31. Childers, S. R., Creese, I., Snowman, A. M., and Snyder, S. H. (1979) Opiate receptor binding affected differentially by opiates and opioid peptides. Eur. J. Pharmacol. 55, 11-18 (Pubitemid 9211603)
32. Goldstein, A., and Naidu, A. (1989) Multiple opioid receptors: ligand selectivity profiles and binding site signatures. Mol. Pharmacol. 36, 265-272 (Pubitemid 19218794)
33. Bakshi, V. P., and Kelley, A. E. (1993) Feeding induced by opioid stimulation of the ventral striatum: role of opiate receptor subtypes. J. Pharmacol. Exp. Ther. 265, 1253-1260 (Pubitemid 23321027)
34. Spanagel, R., Herz, A., and Shippenberg, T. S. (1992) Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc. Nat. Acad. Sci. 89, 2046-2050
35. Klitenick, M., DeWitte, P., and Kalivas, P. (1992) Regulation of somatodendritic dopamine release in the ventral tegmental area by opioids and GABA: an in vivo microdialysis study. J. Neurosci. 12, 2623-2632
36. Naef, L., Moquin, L., Dal Bo, G., Giros, B., Gratton, A., and Walker, C. D. (2011) Maternal high-fat intake alters presynaptic regulation of dopamine in the nucleus accumbens and increases motivation for fat rewards in the offspring. Neuroscience 176, 225-236
37. Acosta-Martinez, M., and Etgen, A. M. (2002) Estrogen modulation of mu-opioid receptor-stimulated [35S]-GTP-gamma-S binding in female rat brain visualized by in vitro autoradiography. Neuroendocrinology 76, 235-242 (Pubitemid 36151493)
38. Le Saux, M., and Di Paolo, T. (2005) Chronic estrogenic drug treatment increases preproenkephalin mRNA levels in the rat striatum and nucleus accumbens. Psychoneuroendocrinology 30, 251-260 (Pubitemid 39423359)
39. Roca, P., Rodriguez, A. M., Oliver, P., Bonet, M. L., Quevedo, S., Picó, C., and Palou, A. (1999) Brown adipose tissue response to cafeteria diet-feeding involves induction of the UCP2 gene and is impaired in female rats as compared to males. Pflügers Archiv. Eur. J. Physiol. 438, 628-634 (Pubitemid 29454977)
40. Bayol, S., Simbi, B., Bertrand, J., and Stickland, N. (2008) Offspring from mothers fed a "junk food" diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females. J. Physiol. 586, 3219-3230 (Pubitemid 351984701)