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Cross-fostering reduces obesity induced by early exposure to monosodium glutamate in male rats

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Abstract

Maternal obesity programmes a range of metabolic disturbances for the offspring later in life. Moreover, environmental changes during the suckling period can influence offspring development. Because both periods significantly affect long-term metabolism, we aimed to study whether cross-fostering during the lactation period was sufficient to rescue a programmed obese phenotype in offspring induced by maternal obesity following monosodium l-glutamate (MSG) treatment. Obesity was induced in female Wistar rats by administering subcutaneous MSG (4 mg/g body weight) for the first 5 days of postnatal life. Control and obese female rats were mated in adulthood. The resultant pups were divided into control second generation (F2) (CTLF2), MSG-treated second generation (F2) (MSGF2), which suckled from their CTL and MSG biological dams, respectively, or CTLF2-CR, control offspring suckled by MSG dams and MSGF2-CR, MSG offspring suckled by CTL dams. At 120 days of age, fat tissue accumulation, lipid profile, hypothalamic leptin signalling, glucose tolerance, glucose-induced, and adrenergic inhibition of insulin secretion in isolated pancreatic islets were analysed. Maternal MSG-induced obesity led to an obese phenotype in male offspring, characterized by hyperinsulinaemia, hyperglycaemia, hyperleptinaemia, dyslipidaemia, and impaired leptin signalling, suggesting central leptin resistance, glucose intolerance, impaired glucose-stimulated, and adrenergic inhibition of insulin secretion. Cross-fostering normalized body weight, food intake, leptin signalling, lipid profiles, and insulinaemia, but not glucose homeostasis or insulin secretion from isolated pancreatic islets. Our findings suggest that alterations during the lactation period can mitigate the development of obesity and prevent the programming of adult diseases.

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References

  1. M. Li, D.M. Sloboda, M.H. Vickers, Maternal obesity and developmental programming of metabolic disorders in offspring: evidence from animal models. Exp. Diabetes Res. 2011, 592408 (2011). doi:10.1155/2011/592408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. D.J. Barker, The origins of the developmental origins theory. J. Intern. Med. 261(5), 412–417 (2007). doi:10.1111/j.1365-2796.2007.01809.x

    Article  CAS  PubMed  Google Scholar 

  3. E.A. Markakis, Development of the neuroendocrine hypothalamus. Front. Neuroendocr. 23(3), 257–291 (2002)

    Article  CAS  Google Scholar 

  4. A. Plagemann, K. Roepke, T. Harder, M. Brunn, A. Harder, M. Wittrock-Staar, T. Ziska, K. Schellong, E. Rodekamp, K. Melchior, J.W. Dudenhausen, Epigenetic malprogramming of the insulin receptor promoter due to developmental overfeeding. J. Perinat. Med. 38(4), 393–400 (2010). doi:10.1515/JPM.2010.051

    Article  CAS  PubMed  Google Scholar 

  5. E. Isganaitis, M. Woo, H. Ma, M. Chen, W. Kong, A. Lytras, V. Sales, J. Decoste-Lopez, K.J. Lee, C. Leatherwood, D. Lee, C. Fitzpatrick, W. Gall, S. Watkins, M.E. Patti, Developmental programming by maternal insulin resistance: hyperinsulinemia, glucose intolerance, and dysregulated lipid metabolism in male offspring of insulin-resistant mice. Diabetes 63(2), 688–700 (2014). doi:10.2337/db13-0558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. F. Lifshitz, Obesity in children. J. Clin. Res. Pediatri. Endocrinol. 1(2), 53–60 (2008). doi:10.4008/jcrpe.v1i2.35

    Article  Google Scholar 

  7. R.J. Qasem, E. Yablonski, J. Li, H.M. Tang, L. Pontiggia, A.P. D’Mello, Elucidation of thrifty features in adult rats exposed to protein restriction during gestation and lactation. Physiol Behav 105(5), 1182–1193 (2012). doi:10.1016/j.physbeh.2011.12.010

    Article  CAS  PubMed  Google Scholar 

  8. S.G. Bouret, S.J. Draper, R.B. Simerly, Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304(5667), 108–110 (2004). doi:10.1126/science.1095004

    Article  CAS  PubMed  Google Scholar 

  9. C. de OliveiraCravo, C.V. Teixeira, M.C. Passos, S.C. Dutra, E.G. de Moura, C. Ramos, Leptin treatment during the neonatal period is associated with higher food intake and adult body weight in rats. Horm. Metab. Res. 34(7), 400–405 (2002). doi:10.1055/s-2002-33473

    Article  Google Scholar 

  10. F.P. Toste, E.G. de Moura, P.C. Lisboa, A.T. Fagundes, E. de Oliveira, M.C. Passos, Neonatal leptin treatment programmes leptin hypothalamic resistance and intermediary metabolic parameters in adult rats. Br. J. Nutr. 95(4), 830–837 (2006)

    Article  CAS  PubMed  Google Scholar 

  11. X. Casabiell, V. Pineiro, M.A. Tome, R. Peino, C. Dieguez, F.F. Casanueva, Presence of leptin in colostrum and/or breast milk from lactating mothers: a potential role in the regulation of neonatal food intake. J. Clin. Endocrinal. Metab. 82(12), 4270–4273 (1997). doi:10.1210/jcem.82.12.4590

    Article  CAS  Google Scholar 

  12. H. Shimizu, Y. Shimomura, R. Hayashi, K. Ohtani, N. Sato, T. Futawatari, M. Mori, Serum leptin concentration is associated with total body fat mass, but not abdominal fat distribution. Int. J. Obes. Relat. Metab. Disord. 21(7), 536–541 (1997)

    Article  CAS  PubMed  Google Scholar 

  13. H. Munzberg, L. Huo, E.A. Nillni, A.N. Hollenberg, C. Bjorbaek, Role of signal transducer and activator of transcription 3 in regulation of hypothalamic proopiomelanocortin gene expression by leptin. Endocrinology 144(5), 2121–2131 (2003). doi:10.1210/en.2002-221037

    Article  CAS  PubMed  Google Scholar 

  14. C. Bjorbaek, J.K. Elmquist, J.D. Frantz, S.E. Shoelson, J.S. Flier, Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol. Cell 1(4), 619–625 (1998)

    Article  CAS  PubMed  Google Scholar 

  15. J.G. Franco, C.P. Dias-Rocha, T.P. Fernandes, L. Albuquerque Maia, P.C. Lisboa, E.G. Moura, C.C. Pazos-Moura, I.H. Trevenzoli, Resveratrol treatment rescues hyperleptinemia and improves hypothalamic leptin signaling programmed by maternal high-fat diet in rats. Eur. J. Nutr. (2015). doi:10.1007/s00394-015-0880-7

    PubMed Central  Google Scholar 

  16. M. Mazariegos, M.R. Zea, Breastfeeding and non-communicable diseases later in life. Arch. Latinoam. Nutr. 65(3), 143–151 (2015)

    PubMed  Google Scholar 

  17. K.F. Michaelsen, A. Larnkjaer, C. Molgaard, Amount and quality of dietary proteins during the first two years of life in relation to NCD risk in adulthood. Nutr. Metab. Cardiovasc. Dis. 22(10), 781–786 (2012). doi:10.1016/j.numecd.2012.03.014

    Article  CAS  PubMed  Google Scholar 

  18. B.A. Rolls, M.I. Gurr, P.M. van Duijvenvoorde, B.J. Rolls, E.A. Rowe, Lactation in lean and obese rats: effect of cafeteria feeding and of dietary obesity on milk composition. Physiol. Behav. 38(2), 185–190 (1986)

    Article  CAS  PubMed  Google Scholar 

  19. J.L. Saben, E.S. Bales, M.R. Jackman, D. Orlicky, P.S. MacLean, J.L. McManaman, Maternal obesity reduces milk lipid production in lactating mice by inhibiting acetyl-CoA carboxylase and impairing fatty acid synthesis. PLoS One 9(5), e98066 (2014). doi:10.1371/journal.pone.0098066

    Article  PubMed  PubMed Central  Google Scholar 

  20. J.T. Smith, B.J. Waddell, Leptin distribution and metabolism in the pregnant rat: transplacental leptin passage increases in late gestation but is reduced by excess glucocorticoids. Endocrinology 144(7), 3024–3030 (2003). doi:10.1210/en.2003-0145

    Article  CAS  PubMed  Google Scholar 

  21. B. Sun, R.H. Purcell, C.E. Terrillion, J. Yan, T.H. Moran, K.L. Tamashiro, Maternal high-fat diet during gestation or suckling differentially affects offspring leptin sensitivity and obesity. Diabetes 61(11), 2833–2841 (2012). doi:10.2337/db11-0957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. A.E. Hirata, I.S. Andrade, P. Vaskevicius, M.S. Dolnikoff, Monosodium glutamate (MSG)-obese rats develop glucose intolerance and insulin resistance to peripheral glucose uptake. Braz. J. Med. Biol. Res. 30(5), 671–674 (1997)

    Article  CAS  PubMed  Google Scholar 

  23. R.A. Miranda, A.R. Agostinho, I.H. Trevenzoli, L.F. Barella, C.C. Franco, A.B. Trombini, A. Malta, C. Gravena, R. Torrezan, P.C. Mathias, J.C. de Oliveira, Insulin oversecretion in MSG-obese rats is related to alterations in cholinergic muscarinic receptor subtypes in pancreatic islets. Cell. Physiol. Biochem. 33(4), 1075–1086 (2014). doi:10.1159/000358677

    Article  CAS  PubMed  Google Scholar 

  24. K.E. de Campos, Y.K. Sinzato, W. de Pimenta, M.V. Rudge, D.C. Damasceno, Effect of maternal obesity on diabetes development in adult rat offspring. Life Sci. 81((19–20)), 1473–1478 (2007). doi:10.1016/j.lfs.2007.09.016

    Article  PubMed  Google Scholar 

  25. L.L. Bernardis, B.D. Patterson, Correlation between ‘Lee index’ and carcass fat content in weanling and adult female rats with hypothalamic lesions. J. Endocrinol. 40(4), 527–528 (1968)

    Article  CAS  PubMed  Google Scholar 

  26. J.S. Wattez, F. Delahaye, L.F. Barella, A. Dickes-Coopman, V. Montel, C. Breton, P. Mathias, B. Foligne, J. Lesage, D. Vieau, Short- and long-term effects of maternal perinatal undernutrition are lowered by cross-fostering during lactation in the male rat. J. Dev. Orig. Health Dis. 5(2), 109–120 (2014). doi:10.1017/S2040174413000548

    Article  CAS  PubMed  Google Scholar 

  27. F.M. Howells, L. Bindewald, V.A. Russell, Cross-fostering does not alter the neurochemistry or behavior of spontaneously hypertensive rats. Behav. Brain Funct. 5, 24 (2009). doi:10.1186/1744-9081-5-24

    Article  PubMed  PubMed Central  Google Scholar 

  28. R.W. van Vugt, F. Meyer, J.A. van Hulten, J. Vernooij, A.R. Cools, M.M. Verheij, G.J. Martens, Maternal care affects the phenotype of a rat model for schizophrenia. Front. Behav. Neurosci. 8, 268 (2014). doi:10.3389/fnbeh.2014.00268

    PubMed  PubMed Central  Google Scholar 

  29. E.J. DePeters, R.C. Hovey, Methods for collecting milk from mice. J. Mammary Gland Biol. Neoplasia 14(4), 397–400 (2009). doi:10.1007/s10911-009-9158-0

    Article  PubMed  PubMed Central  Google Scholar 

  30. N. Boumahrou, S. Andrei, G. Miranda, C. Henry, J.J. Panthier, P. Martin, S. Bellier, The major protein fraction of mouse milk revisited using proven proteomic tools. J. Physiol. Pharmacol. 60(Suppl 3), 113–118 (2009)

    PubMed  Google Scholar 

  31. S. Grassiolli, C. Gravena, P.C. FreitasMathias, Muscarinic M2 receptor is active on pancreatic islets from hypothalamic obese rat. Eur. J. Pharmacol. 556(1–3), 223–228 (2007). doi:10.1016/j.ejphar.2006.11.022

    Article  CAS  PubMed  Google Scholar 

  32. P. Trinder, Determination of blood glucose using an oxidase-peroxidase system with a non-carcinogenic chromogen. J. Clin. Pathol. 22(2), 158–161 (1969)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. W.T. Friedewald, R.I. Levy, D.S. Fredrickson, Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem. 18(6), 499–502 (1972)

    CAS  PubMed  Google Scholar 

  34. A.M. Scott, I. Atwater, E. Rojas, A method for the simultaneous measurement of insulin release and B cell membrane potential in single mouse islets of Langerhans. Diabetologia 21(5), 470–475 (1981)

    Article  CAS  PubMed  Google Scholar 

  35. C. Gravena, P.C. Mathias, S.J. Ashcroft, Acute effects of fatty acids on insulin secretion from rat and human islets of Langerhans. J. Endocrinol. 173(1), 73–80 (2002)

    Article  CAS  PubMed  Google Scholar 

  36. J.C. de Oliveira, P.C. Lisboa, E.G. de Moura, L.F. Barella, R.A. Miranda, A. Malta, C.C. Franco, T.A. Ribeiro, R. Torrezan, C. Gravena, P.C. Mathias, Poor pubertal protein nutrition disturbs glucose-induced insulin secretion process in pancreatic islets and programs rats in adulthood to increase fat accumulation. J. Endocrinol. 216(2), 195–206 (2013). doi:10.1530/JOE-12-0408

    Article  PubMed  Google Scholar 

  37. U.K. Laemmli, Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259), 680–685 (1970)

    Article  CAS  PubMed  Google Scholar 

  38. M.C. Vogt, L. Paeger, S. Hess, S.M. Steculorum, M. Awazawa, B. Hampel, S. Neupert, H.T. Nicholls, J. Mauer, A.C. Hausen, R. Predel, P. Kloppenburg, T.L. Horvath, J.C. Bruning, Neonatal insulin action impairs hypothalamic neurocircuit formation in response to maternal high-fat feeding. Cell 156(3), 495–509 (2014). doi:10.1016/j.cell.2014.01.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. P.A. Trotta, E.G. Moura, J.G. Franco, N.S. Lima, E. Oliveira, A. Cordeiro, L.L. Souza, K.J. Oliveira, P.C. Lisboa, C.C. PazosMoura, M.C. Passos, Blocking leptin action one week after weaning reverts most of the programming caused by neonatal hyperleptinemia in the adult rat. Horm. Metab. Res. 43(3), 171–177 (2011). doi:10.1055/s-0031-1271694

    Article  CAS  PubMed  Google Scholar 

  40. L. Attig, G. Solomon, J. Ferezou, L. Abdennebi-Najar, M. Taouis, A. Gertler, J. Djiane, Early postnatal leptin blockage leads to a long-term leptin resistance and susceptibility to diet-induced obesity in rats. Int. J. Obes. 32(7), 1153–1160 (2008). doi:10.1038/ijo.2008.39

    Article  CAS  Google Scholar 

  41. L.F. Silva, B.E. Etchebarne, M.S. Nielsen, J.S. Liesman, M. Kiupel, M.J. VandeHaar, Intramammary infusion of leptin decreases proliferation of mammary epithelial cells in prepubertal heifers. J. Dairy Sci. 91(8), 3034–3044 (2008). doi:10.3168/jds.2007-0761

    Article  CAS  PubMed  Google Scholar 

  42. J.F. Rodriguez-Sierra, R. Sridaran, C.A. Blake, Monosodium glutamate disruption of behavioral and endocrine function in the female rat. Neuroendocrinology 31(3), 228–235 (1980)

    Article  CAS  PubMed  Google Scholar 

  43. M. Iqbal, V.G. Moisiadis, A. Kostaki, S.G. Matthews, Transgenerational effects of prenatal synthetic glucocorticoids on hypothalamic-pituitary-adrenal function. Endocrinology 153(7), 3295–3307 (2012). doi:10.1210/en.2012-1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. C.C. Vega, L.A. Reyes-Castro, C.J. Bautista, F. Larrea, P.W. Nathanielsz, E. Zambrano, Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int. J. Obes. 39(4), 712–719 (2015). doi:10.1038/ijo.2013.150

    Article  CAS  Google Scholar 

  45. F. Ornellas, V. Souza-Mello, C.A. Mandarim-de-Lacerda, M.B. Aguila, Programming of obesity and comorbidities in the progeny: lessons from a model of diet-induced obese parents. PLoS One 10(4), e0124737 (2015). doi:10.1371/journal.pone.0124737

    Article  PubMed  PubMed Central  Google Scholar 

  46. D.S. Vido, M.B. Nejm, N.R. Silva, S.M. Silva, S.L. Cravo, J. Luz, Maternal obesity and late effects on offspring metabolism. Arq. Bras. Endocrinol. Metabol. 58(3), 301–307 (2014)

    Article  PubMed  Google Scholar 

  47. B.E. Levin, A.A. Dunn-Meynell, W.A. Banks, Obesity-prone rats have normal blood-brain barrier transport but defective central leptin signaling before obesity onset. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286(1), R143–R150 (2004). doi:10.1152/ajpregu.00393.2003

    Article  CAS  PubMed  Google Scholar 

  48. R.S. Ahima, D. Prabakaran, J.S. Flier, Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J. Clin. Investig. 101(5), 1020–1027 (1998). doi:10.1172/JCI1176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. M.J. Morris, H. Chen, Established maternal obesity in the rat reprograms hypothalamic appetite regulators and leptin signaling at birth. Int. J. Obes. 33(1), 115–122 (2009). doi:10.1038/ijo.2008.213

    Article  CAS  Google Scholar 

  50. J.G. Franco, T.P. Fernandes, C.P. Rocha, C. Calvino, C.C. Pazos-Moura, P.C. Lisboa, E.G. Moura, I.H. Trevenzoli, Maternal high-fat diet induces obesity and adrenal and thyroid dysfunction in male rat offspring at weaning. J. Physiol. 590(Pt 21), 5503–5518 (2012). doi:10.1113/jphysiol.2012.240655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. S.E. Mitchell, R. Nogueiras, A. Morris, S. Tovar, C. Grant, M. Cruickshank, D.V. Rayner, C. Dieguez, L.M. Williams, Leptin receptor gene expression and number in the brain are regulated by leptin level and nutritional status. J. Physiol. 587(Pt 14), 3573–3585 (2009). doi:10.1113/jphysiol.2009.173328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. S. Lee, K.A. Lee, G.Y. Choi, M. Desai, S.H. Lee, M.G. Pang, I. Jo, Y.J. Kim, Feed restriction during pregnancy/lactation induces programmed changes in lipid, adiponectin and leptin levels with gender differences in rat offspring. J Matern. Fetal. Neonatal. Med. 26(9), 908–914 (2013). doi:10.3109/14767058.2013.766686

    Article  CAS  PubMed  Google Scholar 

  53. P.A. Matthews, A.M. Samuelsson, P. Seed, J. Pombo, J.A. Oben, L. Poston, P.D. Taylor, Fostering in mice induces cardiovascular and metabolic dysfunction in adulthood. J. Physiol. 589(Pt 16), 3969–3981 (2011). doi:10.1113/jphysiol.2011.212324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. J.P. Despres, Lipoprotein metabolism in visceral obesity. Int. J. Obes. 15(Suppl 2), 45–52 (1991)

    CAS  PubMed  Google Scholar 

  55. G.S. Tannenbaum, W. Gurd, M. Lapointe, Leptin is a potent stimulator of spontaneous pulsatile growth hormone (GH) secretion and the GH response to GH-releasing hormone. Endocrinology 139(9), 3871–3875 (1998). doi:10.1210/endo.139.9.6206

    CAS  PubMed  Google Scholar 

  56. A. Perez-Perez, J. Maymo, Y. Gambino, J.L. Duenas, R. Goberna, C. Varone, V. Sanchez-Margalet, Leptin stimulates protein synthesis-activating translation machinery in human trophoblastic cells. Biol. Reprod. 81(5), 826–832 (2009). doi:10.1095/biolreprod.109.076513

    Article  CAS  PubMed  Google Scholar 

  57. S. Rajia, H. Chen, M.J. Morris, Maternal overnutrition impacts offspring adiposity and brain appetite markers-modulation by postweaning diet. J. Neuroendocrinol. 22(8), 905–914 (2010). doi:10.1111/j.1365-2826.2010.02005.x

    CAS  PubMed  Google Scholar 

  58. A.E. Andreazzi, S. Grassiolli, P.B. Marangon, A.G. Martins, J.C. de Oliveira, R. Torrezan, C. Gravena, R.M.G. Garcia, P.C. Mathias, Impaired sympathoadrenal axis function contributes to enhanced insulin secretion in prediabetic obese rats. Exp. Diabetes Res. 2011, 947917 (2011). doi:10.1155/2011/947917

    Article  PubMed  PubMed Central  Google Scholar 

  59. A.C. Marçal, S. Grassiolli, D.N. da Rocha, M.A. Puzzi, C. Gravena, D.X. Scomparin, P.C. de Freitas Mathias, The dual effect of isoproterenol on insulin release is suppressed in pancreatic islets from hypothalamic obese rats. Endocrine 29(3), 445–449 (2006)

    Article  PubMed  Google Scholar 

  60. O. Ballard, A.L. Morrow, Human milk composition: nutrients and bioactive factors. Pediatr. Clin. N. Am. 60(1), 49–74 (2013). doi:10.1016/j.pcl.2012.10.002

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Brazilian Federal Foundation, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

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Authors and Affiliations

  1. Department of Biotechnology, Cell Biology and Genetics, State University of Maringá/UEM, Block H67, room 19, Colombo Avenue 5790, Maringá, PR, Brazil

    Rosiane Aparecida Miranda, Claudinéia Conationi da Silva Franco, Laize Peron Tófolo, Tatiane Aparecida Ribeiro, Audrei Pavanello, Paulo Cezar de Freitas Mathias & Elaine Vieira

  2. Carlos Chagas Filho Biophysics Institute, Federal University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    Rosiane Aparecida Miranda

  3. Health Sciences Institute, Federal University of Mato Grosso, Sinop, MT, Brazil

    Júlio Cezar de Oliveira

  4. Molecular Signaling Section, Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, USA

    Luiz Felipe Barella

  5. Department of Physiological Sciences Roberto Alcântara Gomes Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    Ellen Paula Santos da Conceição, Patrícia Cristina Lisboa & Egberto Gaspar de Moura

  6. Department of Physiological Sciences, State University of Maringá, Maringá, PR, Brazil

    Rosana Torrezan

  7. School of Medicine (Optometr), Deakin University, Waurn Ponds, Geelong, VIC, 3216, Australia

    James Armitage

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Miranda, R.A., da Silva Franco, C.C., de Oliveira, J.C. et al. Cross-fostering reduces obesity induced by early exposure to monosodium glutamate in male rats. Endocrine 55, 101–112 (2017). https://doi.org/10.1007/s12020-016-0965-y

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