Role of prenatal undernutrition in the expression of serotonin, dopamine and leptin receptors in adult mice: Implications of food intake

Manuel‑Apolinar,Leticia; Rocha,Luisa; Damasio,Leticia; Tesoro‑Cruz,Emiliano; Zarate,Arturo

doi:10.3892/mmr.2013.1853

Role of prenatal undernutrition in the expression of serotonin, dopamine and leptin receptors in adult mice: Implications of food intake

Authors:
- Leticia Manuel‑Apolinar
- Luisa Rocha
- Leticia Damasio
- Emiliano Tesoro‑Cruz
- Arturo Zarate
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Affiliations: Endocrine Research Unit, National Medical Center, Mexican Social Security Institute, Mexico City, Mexico, Department of Pharmacobiology, Center for Research and Advanced Studies, Mexico City, Mexico, Department of Research and Animal Facility, INCMN, Mexico City, Mexico
Published online on: December 10, 2013 https://doi.org/10.3892/mmr.2013.1853
Pages: 407-412
Copyright: © Manuel‑Apolinar et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].

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Abstract

Perturbations in the levels of serotonin expression have a significant impact on behavior and have been implicated in the pathogenesis of several neuropsychiatric disorders including anxiety, mood and appetite. Fetal programming is a risk factor for the development of metabolic diseases during adulthood. Moreover, previous studies have shown that serotonin (5‑HT), dopamine and leptin are important in energy balance. In the present study, the impact of maternal malnutrition‑induced prenatal undernutrition (UN) was investigated in mice and the expression of 5‑HT1A, dopamine (D)1, D2 and Ob‑Rb receptors was analyzed in the hypothalamus during adulthood. The UN group showed a low birth weight compared with the control group. With regard to receptor expression, 5‑HT1A in the UN group was increased in the hypothalamus and D1 was reduced, whereas D2 showed an increase from postnatal day (P)14 in the arcuate nucleus. Ob‑Rb receptor expression was increased in the hypothalamus at P14 and P90. These observations indicated that maternal caloric restriction programs a postnatal body weight gain in offspring with an increased food intake in early postnatal life which continues into adulthood. In addition, UN in mice was found to be affected by Ob‑Rb, 5‑HT1A and D1/2 receptor expression, indicating that these observations may be associated with hyperphagia and obesity.

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1	Barker DJP, Hales CN, Fall CHD, Osmond C, Phipps K and Clark PMS: Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 36:62–67. 1993. View Article : Google Scholar : PubMed/NCBI
2	Fontaine KR, Redden DT, Wang C, Westfall AO and Allison DB: Years of life lost due to obesity. JAMA. 289:187–193. 2003. View Article : Google Scholar : PubMed/NCBI
3	Poston L: Developmental programming and diabetes. The human experience and insight from animal models. Best Pract Res Clin Endocrinol Metab. 24:541–552. 2010. View Article : Google Scholar : PubMed/NCBI
4	Desai M, Gayle D, Babu J and Ross GM: Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. Am J Physiol Regul Integr Comp Physiol. 288:R91–R96. 2005. View Article : Google Scholar : PubMed/NCBI
5	Hokken-Koelega AC, De Ridder MA, Lemmen RJ, Den Hartong H, De Muinck Keizer-Schrama SM and Drop SL: Children born small for gestation age: do they catch up? Pediatr Res. 38:267–271. 1995. View Article : Google Scholar
6	Jones AP, Simson EL and Friedman MI: Gestational undernutrition and the development of obesity in rats. J Nutr. 114:1484–1492. 1984.PubMed/NCBI
7	Vickers MH, Breier BH, Cutfield WS, Hofman PL and Gluckman PD: Fetal origin of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab. 279:E83–E87. 2000.PubMed/NCBI
8	Begum G, Stevens A, Smith EB, Connor K, Challis JR, Bloomfield F and White A: Epigenetic changes in fetal hypothalamic energy regulating pathways are associated with maternal undernutrition and twinning. FASEB J. 26:1694–1703. 2012. View Article : Google Scholar : PubMed/NCBI
9	Tamashiro K and Moran T: Perinatal environment and its influences on metabolic programming of offspring. Physiol Behav. 100:560–566. 2010. View Article : Google Scholar : PubMed/NCBI
10	Berger MA, Barros VG, Sarchi MI, Tarazi FI and Antonelli MC: Long-term effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. Neurochem Res. 27:1525–1533. 2002. View Article : Google Scholar : PubMed/NCBI
11	Pôrto LC, Sardinha FL, Telles MM, Guimarães RB, Albuquerque KT, Andrade IS, Oyama LM, Nascimento CM, Santos OF and Ribeiro EB: Impairment of the serotonergic control of feeding in adult female rats exposed to intrauterine malnutrition. Br J Nutr. 101:1255–1261. 2009.PubMed/NCBI
12	Manuel-Apolinar L, Zarate A, Rocha L and Hernández M: Fetal malnutrition affects hypothalamic leptin receptor expression after birth in male mice. Arch Med Res. 41:240–245. 2010. View Article : Google Scholar : PubMed/NCBI
13	Bauer A, Zilles K, Matusch A, Holzmann C, Riess O and von Hörsten S: Regional and subtype selective changes of neurotransmitter receptor density in a rat transgenic for the Huntington’s disease mutation. J Neurochem. 94:639–650. 2005.PubMed/NCBI
14	Luna-Munguía H, Manuel-Apolinar L, Rocha L and Meneses A: 5-HT1A receptors expression during memory formation. Psychopharmacol. 181:309–318. 2005.PubMed/NCBI
15	Díaz-Romero M, Arias-Montaño JA, Eguibar JR and Flores G: Enhanced binding of dopamine D1 receptors in caudate putamen subregions in High-Yawning Sprague-Dawley rats. Synapse. 56:69–73. 2005.PubMed/NCBI
16	Harder T, Rodekamp E, Schellong K, Dudenhausen JW and Plagemann A: Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. Am J Epidemiol. 165:849–857. 2007. View Article : Google Scholar : PubMed/NCBI
17	Stevens A, Begum G and White A: Epigenetic changes in the hypothalamic pro-opiomelanocortin gene: a mechanism linking maternal undernutrition to obesity in the offspring? Eur J Pharmacol. 660:194–201. 2011. View Article : Google Scholar : PubMed/NCBI
18	Hales CN and Barker DJP: The thrifty phenotype hypothesis. Br Med Bull. 60:5–20. 2001. View Article : Google Scholar
19	Ozanne SE, Lewis R, Jennings BJ and Hales CN: Early programming of weight gain in mice prevents the induction of obesity by a highly palatable diet. Clin Sci (Lond). 106:141–145. 2004. View Article : Google Scholar : PubMed/NCBI
20	Jousse C, Parry L, Lambert-Langlais S, Maurin AC, Averous J, Bruhat A, Carraro V, et al: Perinatal undernutrition affects the methylation and expression of the leptin gene in adults: implication for the understanding of metabolic syndrome. FASEB J. 25:3271–3278. 2011. View Article : Google Scholar : PubMed/NCBI
21	Kwak SH, Park BL, Kim H, German MS, Go MJ, Jung HS, et al: Association of variations in TPH1 and HTR2B with gestational weight gain and measures of obesity. Obesity (Silver Spring). 20:233–238. 2012. View Article : Google Scholar : PubMed/NCBI
22	Lage R, Vázquez MJ, Varela L, Saha AK, Vidal-Puig A, Nogueiras R, Diéguez C and López M: Ghrelin effects on neuropeptides in the rat hypothalamus depend on fatty acid metabolism actions on BSX but not on gender. FASEB J. 24:2670–2679. 2010. View Article : Google Scholar : PubMed/NCBI
23	Bina KG and Cincotta AH: Dopaminergic agonists normalize elevated hypothalamic neuropeptide Y and corticotropin-releasing hormone, body weight gain, and hyperglycemia in ob/ob mice. Neuroendocrinol. 71:68–78. 2000. View Article : Google Scholar
24	Schwartz MW, Woods SC, Porte D Jr, Seeley RJ and Baskin DG: Central nervous system control of food intake. Nature. 404:661–671. 2000.PubMed/NCBI
25	Davis JD and Smith GP: Learning to sham feed: behavioral adjustments to loss of physiological postingestional stimuli. Am J Physiol. 259:R1228–R1235. 1990.PubMed/NCBI
26	Smith GP: The controls of eating: a shift from nutritional homeostasis to behavioral neuroscience. Nutrition. 16:814–820. 2000. View Article : Google Scholar : PubMed/NCBI
27	Schellekens H, Clarke G, Jeffery IB, Dinan TG and Cryan JF: Dynamic 5-HT2C receptor editing in a mouse model of obesity. PLos One. 7:e322662012. View Article : Google Scholar : PubMed/NCBI
28	Dryden S, Burns SJ, Frankish HM and Williams G: Increased hypothalamic neuropeptide Y concentration or hyperphagia in streptozotocin-diabetic rats are not mediated by glucocorticoids. Eur J Pharmacol. 340:221–225. 1997. View Article : Google Scholar : PubMed/NCBI
29	Dryden S, Pickavance L, Frankish HM and Williams G: Increased neuropeptide Y secretion in the hypothalamic paraventricular nucleus of obese (fa/fa) Zucker rats. Brain Res. 690:185–188. 1995. View Article : Google Scholar : PubMed/NCBI
30	Pfaffly J, Michaelides M, Wang GJ, Pessin JE, Volkow ND and Thanos PK: Leptin increases striatal dopamine D2 receptor binding in leptin-deficient obese (ob/ob) mice. Synapse. 64:503–510. 2010. View Article : Google Scholar : PubMed/NCBI
31	Sullivan EL, Smith MS and Grove KL: Perinatal exposure to high-fat diet programs energy balance, metabolism and behavior in adulthood. Neuroendocrinology. 93:1–8. 2011. View Article : Google Scholar : PubMed/NCBI
32	Sullivan EL, Grayson B, Takahashi D, Robertson N, Maier A, Bethea CL, Smit MS, Coleman K and Grove KL: Chronic consumption of a high-fat diet during pregnancy causes perturbations in in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring. J Neurosci. 30:3826–3830. 2010. View Article : Google Scholar