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Late effects of early weaning on food preference and the dopaminergic and endocannabinoid systems in male and female rats

Published online by Cambridge University Press:  02 March 2021

Patricia Novaes Soares ,
Rosiane Aparecida Miranda ,
Iala Milene Bertasso ,
Carla Bruna Pietrobon ,
Vanessa Silva Tavares Rodrigues ,
Elaine de Oliveira ,
Alex Christian Manhães ,
Egberto Gaspar de Moura Open the ORCID record for Egberto Gaspar de Moura [Opens in a new window]  and
Patricia Cristina Lisboa Open the ORCID record for Patricia Cristina Lisboa [Opens in a new window]
Patricia Novaes Soares
Affiliation:
Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
Rosiane Aparecida Miranda
Affiliation:
Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
Iala Milene Bertasso
Affiliation:
Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
Carla Bruna Pietrobon
Affiliation:
Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
Vanessa Silva Tavares Rodrigues
Affiliation:
Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
Elaine de Oliveira
Affiliation:
Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
Alex Christian Manhães
Affiliation:
Laboratory of Neurophysiology, Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
Egberto Gaspar de Moura
Affiliation:
Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
Patricia Cristina Lisboa*
Affiliation:
Laboratory of Endocrine Physiology, Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil
*
Address for correspondence: Dr. Patricia Cristina Lisboa, B.Sc., Ph.D., Departamento de Ciências Fisiológicas, Instituto de Biologia, Universidade do Estado do Rio de Janeiro, Av. 28 de Setembro, 87, 5o andar, Vila Isabel, Rio de Janeiro 20551-031, Brazil. Email: [email protected]
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Abstract

Early weaning (EW) is associated with obesity later in life. Here, using an EW model in rats, we investigated changes in feeding behavior and the dopaminergic and endocannabinoid systems (ECS) in the adult offspring. Lactating Wistar rats were divided into two groups: EW, dams were wrapped with a bandage to interrupt suckling during the last 3 days of breastfeeding; CONT; dams fed the pups throughout the period without hindrances. EW animals were compared with CONT animals of the same sex. At PN175, male and female offspring of both groups could freely self-select between high-fat and high-sugar diets (food challenge test). EW males preferred the high-fat diet at 30 min and more of the high-sugar diet after 12 h compared to CONT males. EW females did not show differences in their preference for the palatable diets compared to CONT females. Total intake of standard diet from PN30-PN180 was higher in both male and female EW animals, indicating hyperphagia. At PN180, EW males showed lower type 2 dopamine receptor (D2r) in the nucleus accumbens (NAc) and dorsal striatum, while EW females had lower tyrosine hydroxylase in the ventral tegmental area and NAc, D1r in the NAc, and D2r in the prefrontal cortex. In the lateral hypothalamus, EW males had lower fatty acid amide hydrolase (FAAH) and monoacylglycerol lipase, whereas EW females showed lower N-arachidonoyl-phosphatidylethanolamine phospholipase-D and increased FAAH. Early weaning altered both the dopaminergic and ECS parameters at adulthood, contributing to the eating behavior changes of the progeny in a sex-dependent manner.

Keywords

Lactationearly weaningprogrammingdopaminergic statusendocannabinoid status
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 13 , Issue 1 , February 2022 , pp. 90 - 100
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Copyright
© The Author(s), 2021. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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Footnotes

Patricia Novaes Soares and Rosiane Aparecida Miranda contributed equally to this work.

References

Barker, DJ. The developmental origins of adult disease. Eur J Epidemiol 2003; 18(8), 733–736.CrossRefGoogle ScholarPubMed
Sellayah, D, Cagampang, FR. The divergent effect of maternal protein restriction during pregnancy and postweaning high-fat diet feeding on blood pressure and adiposity in adult mouse offspring. Nutrients 2018; 10(12), 1832–1841.CrossRefGoogle ScholarPubMed
Franzago, M, Fraticelli, F, Stuppia, L, Vitacolonna, E. Nutrigenetics, epigenetics and gestational diabetes: consequences in mother and child. Epigenetics 2019; 14(3), 215–235.CrossRefGoogle ScholarPubMed
Agosti, M, Tandoi, F, Morlacchi, L, Bossi, A. Nutritional and metabolic programming during the first thousand days of life. Pediatr Med Chir 2017; 39(2), 157.CrossRefGoogle ScholarPubMed
Organization WH. Report of the Expert Consultation on the Optimal Duration of Exclusive Breastfeeding, 2001. WHO, Geneva.Google Scholar
Harder, T, Bergmann, R, Kallischnigg, G, Plagemann, A. Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol 2005;162(5), 397–403.CrossRefGoogle ScholarPubMed
de Albuquerque Maia, L, Lisboa, PC, de Oliveira, E, et al. Two models of early weaning decreases bone structure by different changes in hormonal regulation of bone metabolism in neonate rat. Horm Metab Res 2013; 45(5), 332–337.Google ScholarPubMed
Devlin, MJ, Bouxsein, ML. Influence of pre- and peri-natal nutrition on skeletal acquisition and maintenance. Bone 2012; 50(2), 444–451.CrossRefGoogle ScholarPubMed
Kikusui, T, Kanbara, N, Ozaki, M, et al. Early weaning increases anxiety via brain-derived neurotrophic factor signaling in the mouse prefrontal cortex. Sci Rep 2019; 9(1), 3991.CrossRefGoogle ScholarPubMed
Lima Nda, S, de Moura, EG, Passos, MC, et al. Early weaning causes undernutrition for a short period and programmes some metabolic syndrome components and leptin resistance in adult rat offspring. Br J Nutr 2011; 105(9), 1405–1413.CrossRefGoogle Scholar
Lima, NS, Moura, EG, Franco, JG, et al. Developmental plasticity of endocrine disorders in obesity model primed by early weaning in dams. Horm Metab Res 2013; 45(1), 22–30.Google ScholarPubMed
Lima Nda, S, Franco, JG, Peixoto-Silva, N, et al. Ilex paraguariensis (yerba mate) improves endocrine and metabolic disorders in obese rats primed by early weaning. Eur J Nutr 2014; 53(1), 73–82.CrossRefGoogle ScholarPubMed
Franco, JG, Lisboa, PC, Lima, NS, et al. Resveratrol attenuates oxidative stress and prevents steatosis and hypertension in obese rats programmed by early weaning. J Nutr Biochem 2013; 24(6), 960–966.CrossRefGoogle ScholarPubMed
Pietrobon, CB, Bertasso, IM, Silva, BS, et al. Body adiposity and endocrine profile of female Wistar rats of distinct ages that were early weaned. Horm Metab Res 2020; 52(1), 58–66.Google ScholarPubMed
Souza, LL, de Moura, EG, Lisboa, PC. Does early weaning shape future endocrine and metabolic disorders? Lessons from animal models. J Dev Orig Health Dis 2020; 11(5), 441–451.CrossRefGoogle ScholarPubMed
Williams, EP, Mesidor, M, Winters, K, Dubbert, PM, Wyatt, SB. Overweight and obesity: prevalence, consequences, and causes of a growing public health problem. Curr Obes Rep 2015; 4(3), 363–370.CrossRefGoogle ScholarPubMed
Quarta, C, Mazza, R, Obici, S, Pasquali, R, Pagotto, U. Energy balance regulation by endocannabinoids at central and peripheral levels. Trends Mol Med 2011; 17(9), 518–526.CrossRefGoogle ScholarPubMed
Watkins, BA, Kim, J. The endocannabinoid system: directing eating behavior and macronutrient metabolism. Front Psychol 2014; 5, 1506.Google ScholarPubMed
Alsio, J, Olszewski, PK, Norback, AH, et al. Dopamine D1 receptor gene expression decreases in the nucleus accumbens upon long-term exposure to palatable food and differs depending on diet-induced obesity phenotype in rats. Neuroscience 2010; 171(3), 779–787.CrossRefGoogle ScholarPubMed
Volkow, ND, Wise, RA, Baler, R. The dopamine motive system: implications for drug and food addiction. Nat Rev Neurosci 2017; 18(12), 741–752.CrossRefGoogle ScholarPubMed
Frieling, H, Albrecht, H, Jedtberg, S, et al. Elevated cannabinoid 1 receptor mRNA is linked to eating disorder related behavior and attitudes in females with eating disorders. Psychoneuroendocrinology 2009; 34(4), 620–624.CrossRefGoogle ScholarPubMed
Monteleone, P, Matias, I, Martiadis, V, et al. Blood levels of the endocannabinoid anandamide are increased in anorexia nervosa and in binge-eating disorder, but not in bulimia nervosa. Neuropsychopharmacology 2005; 30(6), 1216–1221.CrossRefGoogle ScholarPubMed
Mazier, W, Saucisse, N, Gatta-Cherifi, B, Cota, D. The endocannabinoid system: pivotal orchestrator of obesity and metabolic disease. Trends Endocrinol Metab 2015; 26(10), 524–537.CrossRefGoogle ScholarPubMed
Kessler, RM, Hutson, PH, Herman, BK, Potenza, MN. The neurobiological basis of binge-eating disorder. Neurosci Biobehav Rev 2016; 63, 223–238.CrossRefGoogle ScholarPubMed
Hu, SS, Mackie, K. Distribution of the endocannabinoid system in the central nervous system. Handb Exp Pharmacol 2015; 231, 59–93.CrossRefGoogle ScholarPubMed
Cota, D, Marsicano, G, Tschop, M, et al. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J Clin Invest 2003; 112(3), 423–431.CrossRefGoogle ScholarPubMed
Bazwinsky-Wutschke, I, Zipprich, A, Dehghani, F. Endocannabinoid system in hepatic glucose metabolism, fatty liver disease, and cirrhosis. Int J Mol Sci 2019; 20(10), 2516–2541.CrossRefGoogle Scholar
Di Marzo, V, De Petrocellis, L, Bisogno, T. Endocannabinoids Part I: molecular basis of endocannabinoid formation, action and inactivation and development of selective inhibitors. Expert Opin Ther Targets 2001; 5(2), 241–265.Google ScholarPubMed
Di Marzo, V. Endocannabinoids: synthesis and degradation. Rev Physiol Biochem Pharmacol 2008; 160, 1–24.CrossRefGoogle Scholar
Sanchez-Fuentes, A, Marichal-Cancino, BA, Mendez-Diaz, M, et al. mGluR1/5 activation in the lateral hypothalamus increases food intake via the endocannabinoid system. Neurosci Lett 2016; 631, 104–108.CrossRefGoogle ScholarPubMed
Bermudez-Silva, FJ, Cardinal, P, Cota, D. The role of the endocannabinoid system in the neuroendocrine regulation of energy balance. J Psychopharmacol 2012; 26(1), 114–124.CrossRefGoogle ScholarPubMed
Jo, YH, Chen, YJ, Chua, SC Jr., Talmage, DA, Role, LW. Integration of endocannabinoid and leptin signaling in an appetite-related neural circuit. Neuron 2005; 48(6), 1055–1066.CrossRefGoogle Scholar
van Eenige, R, van der Stelt, M, Rensen, PCN, Kooijman, S. Regulation of adipose tissue metabolism by the endocannabinoid system. Trends Endocrinol Metab 2018; 29(5), 326–337.CrossRefGoogle ScholarPubMed
Siegmund, SV, Schwabe, RF. Endocannabinoids and liver disease. II. Endocannabinoids in the pathogenesis and treatment of liver fibrosis. Am J Physiol Gastrointest Liver Physiol 2008; 294(2), G357–G362.CrossRefGoogle ScholarPubMed
de Macedo, IC, de Freitas, JS, da Silva Torres, IL. The influence of palatable diets in reward system activation: a mini review. Adv Pharmacol Sci 2016; 2016, 7238679.Google ScholarPubMed
Bassareo, V, Di Chiara, G. Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience 1999; 89(3), 637–641.CrossRefGoogle ScholarPubMed
Hoebel, BG, Hernandez, L, Schwartz, DH, Mark, GP, Hunter, GA. Microdialysis studies of brain norepinephrine, serotonin, and dopamine release during ingestive behavior. Theoretical and clinical implications. Ann N Y Acad Sci 1989; 575, 171–191; discussion 192–173.CrossRefGoogle ScholarPubMed
Hanlon, EC, Baldo, BA, Sadeghian, K, Kelley, AE. Increases in food intake or food-seeking behavior induced by GABAergic, opioid, or dopaminergic stimulation of the nucleus accumbens: is it hunger? Psychopharmacology (Berl) 2004; 172(3), 241–247.CrossRefGoogle ScholarPubMed
Liang, SL, Pan, JT. Potent inhibitory effect of selective D2 and D3 agonists on dopamine-responsive dorsomedial arcuate neurons in brain slices of estrogen-primed rats. Life Sci 2001; 69(22), 2653–2662.CrossRefGoogle ScholarPubMed
Bloomfield, MA, Ashok, AH, Volkow, ND, Howes, OD. The effects of Delta(9)-tetrahydrocannabinol on the dopamine system. Nature 2016; 539(7629), 369–377.CrossRefGoogle ScholarPubMed
Quinn, R. Comparing rat’s to human’s age: how old is my rat in people years? Nutrition 2005; 21(6), 775–777.CrossRefGoogle ScholarPubMed
Pinheiro, CR, Moura, EG, Manhaes, AC, et al. Concurrent maternal and pup postnatal tobacco smoke exposure in Wistar rats changes food preference and dopaminergic reward system parameters in the adult male offspring. Neuroscience 2015; 301, 178–192.CrossRefGoogle ScholarPubMed
Pinheiro, CR, Moura, EG, Manhaes, AC, et al. Maternal nicotine exposure during lactation alters food preference, anxiety-like behavior and the brain dopaminergic reward system in the adult rat offspring. Physiol Behav 2015; 149, 131–141.CrossRefGoogle ScholarPubMed
Avena, NM, Long, KA, Hoebel, BG. Sugar-dependent rats show enhanced responding for sugar after abstinence: evidence of a sugar deprivation effect. Physiol Behav 2005; 84(3), 359–362.CrossRefGoogle ScholarPubMed
Hermanussen, M, Garcia, AP, Sunder, M, et al. Obesity, voracity, and short stature: the impact of glutamate on the regulation of appetite. Eur J Clin Nutr 2006; 60(1), 25–31.CrossRefGoogle ScholarPubMed
Avena, NM. Examining the addictive-like properties of binge eating using an animal model of sugar dependence. Exp Clin Psychopharmacol 2007; 15(5), 481–491.CrossRefGoogle ScholarPubMed
Avena, NM, Rada, P, Hoebel, BG. Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 2008; 32(1), 20–39.CrossRefGoogle ScholarPubMed
Paxinos, G, Watson, CR, Emson, PC. AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. J Neurosci Methods 1980; 3(2), 129–149.CrossRefGoogle ScholarPubMed
Palou, M, Priego, T, Sanchez, J, Palou, A, Pico, C. Sexual dimorphism in the lasting effects of moderate caloric restriction during gestation on energy homeostasis in rats is related with fetal programming of insulin and leptin resistance. Nutr Metab (Lond) 2010; 7, 69.CrossRefGoogle Scholar
Corwin, RL, Wojnicki, FH, Zimmer, DJ, et al. Binge-type eating disrupts dopaminergic and GABAergic signaling in the prefrontal cortex and ventral tegmental area. Obesity (Silver Spring) 2016; 24(10), 2118–2125.CrossRefGoogle ScholarPubMed
Baik, JH. Dopamine signaling in food addiction: role of dopamine D2 receptors. BMB Rep 2013; 46(11), 519–526.CrossRefGoogle ScholarPubMed
Jaber, M, Robinson, SW, Missale, C, Caron, MG. Dopamine receptors and brain function. Neuropharmacology 1996; 35(11), 1503–1519.CrossRefGoogle ScholarPubMed
Moore, CF, Leonard, MZ, Micovic, NM, et al. Reward sensitivity deficits in a rat model of compulsive eating behavior. Neuropsychopharmacology 2020; 45(4), 589–596.CrossRefGoogle Scholar
Geiger, BM, Haburcak, M, Avena, NM, et al. Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience 2009; 159(4), 1193–1199.CrossRefGoogle ScholarPubMed
Selleck, RA, Zhang, W, Samberg, HD, Padival, M, Rosenkranz, JA. Limited prefrontal cortical regulation over the basolateral amygdala in adolescent rats. Sci Rep 2018; 8(1), 17171.CrossRefGoogle ScholarPubMed
Iwasaki, Y, Maejima, Y, Suyama, S, et al. Peripheral oxytocin activates vagal afferent neurons to suppress feeding in normal and leptin-resistant mice: a route for ameliorating hyperphagia and obesity. Am J Physiol Regul Integr Comp Physiol 2015; 308(5), R360–R369.CrossRefGoogle ScholarPubMed
Di Marzo, V, Ligresti, A, Cristino, L. The endocannabinoid system as a link between homoeostatic and hedonic pathways involved in energy balance regulation. Int J Obes (Lond) 2009; 33(Suppl 2), S18–S24.CrossRefGoogle ScholarPubMed
Rodriguez de Fonseca, F. The endocannabinoid system and food intake control. Rev Med Univ Navarra 2004; 48(2), 18–23.Google ScholarPubMed
Pagano, C, Pilon, C, Calcagno, A, et al. The endogenous cannabinoid system stimulates glucose uptake in human fat cells via phosphatidylinositol 3-kinase and calcium-dependent mechanisms. J Clin Endocrinol Metab 2007; 92(12), 4810–4819.CrossRefGoogle ScholarPubMed
Silvestri, C, Ligresti, A, Di Marzo, V. Peripheral effects of the endocannabinoid system in energy homeostasis: adipose tissue, liver and skeletal muscle. Rev Endocr Metab Disord 2011; 12(3), 153–162.CrossRefGoogle ScholarPubMed
Kuipers, EN, Kantae, V, Maarse, BCE, et al. High fat diet increases circulating endocannabinoids accompanied by increased synthesis enzymes in adipose tissue. Front Physiol 2018; 9, 1913.CrossRefGoogle ScholarPubMed
Osei-Hyiaman, D, DePetrillo, M, Pacher, P, et al. Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J Clin Invest 2005; 115(5), 1298–1305.CrossRefGoogle ScholarPubMed
Julien, B, Grenard, P, Teixeira-Clerc, F, et al. Antifibrogenic role of the cannabinoid receptor CB2 in the liver. Gastroenterology 2005; 128(3), 742–755.CrossRefGoogle ScholarPubMed
Louvet, A, Teixeira-Clerc, F, Chobert, MN, et al. Cannabinoid CB2 receptors protect against alcoholic liver disease by regulating Kupffer cell polarization in mice. Hepatology 2011; 54(4), 1217–1226.CrossRefGoogle ScholarPubMed
Bertasso, IM, Pietrobon, CB, da Silva, BS, et al. Hepatic lipid metabolism in adult rats using early weaning models: sex-related differences. J Dev Orig Health Dis 2020; 11(5), 499–508.CrossRefGoogle ScholarPubMed
Dearden, L, Bouret, SG, Ozanne, SE. Sex and gender differences in developmental programming of metabolism. Mol Metab 2018; 15, 8–19.CrossRefGoogle ScholarPubMed
McEwen, BS, Milner, TA. Understanding the broad influence of sex hormones and sex differences in the brain. J Neurosci Res 2017; 95(1–2), 24–39.CrossRefGoogle ScholarPubMed
McCarthy, MM. Estradiol and the developing brain. Physiol Rev 2008; 88(1), 91–124.CrossRefGoogle ScholarPubMed
McCarthy, MM. The two faces of estradiol: effects on the developing brain. Neuroscientist 2009; 15(6), 599–610.CrossRefGoogle ScholarPubMed
Arnold, AP, Gorski, RA. Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci 1984; 7, 413–442.CrossRefGoogle Scholar
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