Perinatal protein restriction reduces the inhibitory action of serotonin on food intake

European Journal of Neuroscience

Volumn 27, Issue 6, 2008, Pages 1400-1408

  Lopes De Souza, Sandra ^a,b   Orozco Solis, Ricardo ^a,c   Grit, Isabelle ^a,c   Manhães De Castro, Raul ^d   Bolaños Jiménez, Francisco ^a,c,e  

^a Universite de Nantes   (France)

^b DEPARTAMENTO DE MICOLOGIA   (Brazil)

^c UNIVERSITÉ DE NANTES   (France)

^d FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^e CRNH AUVERGNE   (France)

Author keywords

Food intake; Metabolic programming; Perinatal malnutrition; Rat; Serotonin

Indexed keywords

2 (6 CHLORO 5 FLUORO 1 INDOLYL) 1 METHYLETHYLAMINE; 5 PROPOXY 3 (1,2,5,6 TETRAHYDRO 4 PYRIDYL)PYRROLO[3,2 B]PYRIDINE; FENFLURAMINE; SEROTONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DRUG MECHANISM; FEEDING BEHAVIOR; FEMALE; FOOD INTAKE; HYPERPHAGIA; IMMUNOREACTIVITY; LACTATION; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN RESTRICTION; THALAMUS MIDLINE NUCLEUS;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; DIET, PROTEIN-RESTRICTED; EATING; FEMALE; HYPERPHAGIA; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SEROTONIN AGONISTS;

EID: 40949136196     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06105.x     Document Type: Article

References (63)

1. Allen, R.G., Pintar, J.E., Stack, J. Kendall, J.W. (1984) Biosynthesis and processing of proopiomelanocortin-derived peptides during fetal pituitary development. Dev. Biol., 102, 43 50.
2. Almeida, S.S., Tonkiss, J. Galler, J.R. (1996) Malnutrition and reactivity to drugs acting in the central nervous system. Neurosci. Biobehav. Rev., 20, 389 402.
3. Bellinger, L. Langley-Evans, S.C. (2005) Fetal programming of appetite by exposure to a maternal low-protein diet in the rat. Clin. Sci., 109, 413 420.
4. Bellinger, L., Lilley, C. 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. Br. J. Nutr., 92, 513 520.
5. Bellinger, L., Sculley, D.V. Langley-Evans, S.C. (2006) Exposure to undernutrition in fetal life determines fat distribution, locomotor activity and food intake in ageing rats. Int. J. Obes. (Lond.), 30, 729 738.
6. Bieswal, F., Hay, S.M., McKinnon, C., Reusens, B., Cuignet, M., Rees, W.D. Remacle, C. (2004) Prenatal protein restriction does not affect the proliferation and differentiation of rat preadipocytes. J. Nutr., 134, 1493 1499.
7. Blundell, J.E. (1984) Serotonin and appetite. Neuropharmacology, 23, 1537 1551.
8. Blundell, J.E. (1986) Serotonin manipulations and the structure of feeding behaviour. Appetite, 7, S39 S56.
9. Brozek, J. (1990) Effects of generalized malnutrition on personality. Nutrition, 6, 389 395.
10. Brunton, L., Lazo, J. Parker, K. (2005) Goodman and Gilman's the Pharmacological Basis of Therapeutics. McGraw-Hill Professional, New York.
11. Caccia, S., Confalonieri, S., Bergami, A., Fracasso, C., Anelli, M. Garattini, S. (1997) Neuropharmacological effects of low and high doses of repeated oral dexfenfluramine in rats: a comparison with fluoxetine. Pharmacol. Biochem. Behav., 157, 851 856.
12. Chen, J.C., Tonkiss, J., Galler, J.R. Volicer, L. (1992) Prenatal protein malnutrition in rats enhances serotonin release from hippocampus. J. Nutr., 122, 2138 2143.
13. Clausing, P., Newport, G.D. Bowyer, J.F. (1998) Fenfluramine and norfenfluramine levels in brain microdialysate, brain tissue and plasma of rats administered doses of d-fenfluramine known to deplete 5-hydroxytryptamine levels in brain. J. Pharmacol. Exp. Ther., 284, 618 624.
14. 2C receptor agonist and d-fenfluramine on feeding patterns in the rat. Psychopharmacology (Berl.), 152, 256 267.
15. 2C receptor interactions in the modulation of feeding behaviour in the mouse. Psychopharmacology (Berl.), 185, 45 57.
16. Desai, M., Gayle, D., Babu, J. Ross, M.G. (2005) Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R91 R96.
17. Eriksson, J.G., Forsen, T.J., Osmond, C. Barker, D.J. (2003) Pathways of infant and childhood growth that lead to type 2 diabetes. Diabetes Care, 26, 3006 3010.
18. Fracasso, C., Guiso, G., Confalonieri, S., Bergami, A., Garattini, S. Caccia, S. (1995) Depletion and time-course of recovery of brain serotonin after repeated subcutaneous dexfenfluramine in the mouse. A comparison with the rat. Neuropharmacology, 34, 1653 1659.
19. Gluckman, P.D. Hanson, M.A. (2004) Living with the past: evolution, development, and patterns of disease. Science, 305, 1733 1736.
20. Grignaschi, G. Samanin, R. (1992) Role of 5-HT receptors in the effect of d-fenfluramine on feeding patterns in the rat. Eur. J. Pharmacol., 212, 287 289.
21. Grove, K.L. Smith, M.S. (2003) Ontogeny of the hypothalamic neuropeptide Y system. Physiol, Behav., 79, 47 63.
22. Hales, C.N. Barker, D.J. (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia, 35, 595 601.
23. Hales, C.N. Barker, D.J. (2001) The thrifty phenotype hypothesis. Br. Med. Bull., 60, 5 20.
24. 1B receptor agonist CP-94,253 reduces food intake and preserves the behavioural satiety sequence. Physiol. Behav., 60, 933 939.
25. 2C) receptor-mediated weight control in rats. Psychopharmacology (Berl.), 178, 241 249.
26. Heisler, L.K., Cowley, M.A., Tecott, L.H., Fan, W., Low, M.J., Smart, J.L., Rubinstein, M., Tatro, J.B., Marcus, J.N., Holstege, H., Lee, C.E., Cone, R.D. Elmquist, J.K. (2002) Activation of central melanocortin pathways by fenfluramine. Science, 297, 609 611.
27. Heisler, L.K., Jobst, E.E., Sutton, G.M., Zhou, L., Borok, E., Thornton-Jones, Z., Liu, H.Y., Zigman, J.M., Balthasar, N., Kishi, T., Lee, C.E., Aschkenasi, C.J., Zhang, C.Y., Yu, J., Boss, O., Mountjoy, K.G., Clifton, P.G., Lowell, B.B., Friedman, J.M., Horvath, T., Butler, A.A., Elmquist, J.K. Cowley, M.A. (2006) Serotonin reciprocally regulates melanocortin neurons to modulate food intake. Neuron, 51, 239 249.
28. Hernandez, J., Manjarrez, G.G. Chagoya, G. (1989) Newborn humans and rats malnourished in utero: free plasma L-tryptophan, neutral amino acids and brain serotonin synthesis. Brain Res., 488, 1 13.
29. Ikenasio-Thorpe, B.A., Breier, B.H., Vickers, M.H. Fraser, M. (2007) Prenatal influences on susceptibility to diet-induced obesity are mediated by altered neuroendocrine gene expression. J. Endocrinol., 193, 31 37.
30. Kagotani, Y., Hashimoto, T., Tsuruo, Y., Kawano, H., Daikoku, S. Chihara, K. (1989) Development of the neuronal system containing neuropeptide Y in the rat hypothalamus. Int. J. Dev. Neurosci., 7, 359 374.
31. Knight, B.S., Pennell, C.E., Shah, R. Lye, S.J. (2007) Strain differences in the impact of dietary restriction on fetal growth and pregnancy in mice. Reprod. Sci., 14, 81 90.
32. Langley-Evans, S.C. (2001) Fetal programming of cardiovascular function through exposure to maternal undernutrition. Proc. Nutr. Soc., 60, 505 513.
33. Law, C.M., Barker, D.J., Osmond, C., Fall, C.H. Simmonds, S.J. (1992) Early growth and abdominal fatness in adult life. J. Epidemiol. Commun. Health, 46, 184 186.
34. 1B agonist CP-94,253. Psychopharmacology (Berl.), 164, 49 60.
35. Leibowitz, S.F., Weiss, G.F. Shor-Posner, G. (1988) Hypothalamic serotonin: pharmacological, biochemical, and behavioral analyses of its feeding-suppressive action. Clin. Neuropharmacol., 11, S51 S71.
36. Leibowitz, S.F., Weiss, G.F. Suh, J.S. (1990) Medial hypothalamic nuclei mediate serotonin's inhibitory effect on feeding behavior. Pharmacol. Biochem. Behav., 37, 735 742.
37. Levine, R.R., Walsh, C.T. Schwartz-Bloom, R.D. (2000) Pharmacology Drug Action and Reactions. Pathernon Publishing, New York.
38. Livak, K.J. Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402 408.
39. Manjarrez, G.G., Chagoya, G.G. Hernandez, J. (1994) Early nutritional changes modify the kinetics and phosphorylation capacity of tryptophan-5- hydroxylase. Int. J. Dev. Neurosci., 12, 695 702.
40. Manjarrez, G., Manuel, A.L., Mercado, C.R. Hernandez, R.J. (2003) Serotonergic receptors in the brain of in utero undernourished rats. Int. J. Dev. Neurosci., 21, 283 289.
41. Mennini, T., Garattini, S. Caccia, S. (1985) Anorectic effect of fenfluramine isomers and metabolites: relationship between brain levels and in vitro potencies on serotonergic mechanisms. Psychopharmacology, 85, 111 114.
42. Mokler, D.J., Galler, J.R. Morgane, P.J. (2003) Modulation of 5-HT release in the hippocampus of 30-day-old rats exposed in utero to protein malnutrition. Brain Res. Dev. Brain Res., 142, 203 208.
43. Morgane, P.J., Mokler, D.J. Galler, J.R. (2002) Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci. Biobehav. Rev., 26, 471 483.
44. Morton, G.J., Cummings, D.E., Baskin, D.G., Barsh, G.S. Schwartz, M.W. (2006) Central nervous system control of food intake and body weight. Nature, 443, 289 295.
45. Plagemann, A., Rittel, F., Waas, T., Harder, T. Rohde, W. (1999) Cholecystokinin-8S levels in discrete hypothalamic nuclei of weanling rats exposed to maternal protein malnutrition. Regul. Pept., 85, 109 113.
46. Plagemann, A., Harder, T., Rake, A., Melchior, K., Rohde, W. Dorner, G. (2000a) Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J. Nutr., 130, 2582 2589.
47. Plagemann, A., Waas, T., Harder, T., Rittel, F., Ziska, T. Rohde, W. (2000b) Hypothalamic neuropeptide Y levels in weaning offspring of low-protein malnourished mother rats. Neuropeptides, 34, 1 6.
48. Ravelli, G.P., Stein, Z.A. Susser, M.W. (1976) Obesity in young men after famine exposure in utero and early infancy. N. Engl. J. Med., 295, 349 353.
49. Resnick, O. Morgane, P.J. (1984) Ontogeny of the levels of serotonin in various parts of the brain in severely protein malnourished rats. Brain Res., 303, 163 170.
50. Rose, S., Hindmarsh, J.G., Collins, P. Jenner, P. (1997) The effect of fenfluramine dosage regimen and reduced food intake on levels of 5-HT in rat brain. J. Neural Transm., 104, 1339 1351.
51. Sardinha, F.L., Telles, M.M., Albuquerque, K.T., Oyama, L.M., Guimarães, P.A., Santos, O.F. Ribeiro, E.B. (2006) Gender difference in the effect of intrauterine malnutrition on the central anorexigenic action of insulin in adult rats. Nutrition, 22, 1152 1161.
52. Shor-Posner, G., Grinker, J.A., Marinescu, C., Brown, O. Leibowitz, S.F. (1986) Hypothalamic serotonin in the control of meal patterns and macronutrient selection. Brain Res. Bull., 17, 663 671.
53. Simansky, K.J. (1996) Serotonergic control of the organization of feeding and satiety. Behav. Brain Res., 73, 37 42.
54. Terroni, P.L., Anthony, F.W., Hanson, M.A. Cagampang, F.R. (2005) Expression of agouti-related peptide, neuropeptide Y, pro-opiomelanocortin and the leptin receptor isoforms in fetal mouse brain from pregnant dams on a protein-restricted diet. Brain Res. Mol. Brain Res., 140, 111 115.
55. 2C receptors. Brain Res., 1067, 170 176.
56. Vickers, M.H., Breier, B.H., Cutfield, W.S., Hofman, P.L. Gluckman, P.D. (2000) Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am. J. Physiol. Endocrinol. Metab., 279, E83 E87.
57. Weiss, G.F., Rogacki, N., Fueg, A., Buchen, D. Leibowitz, S.F. (1990) Impact of hypothalamic d-norfenfluramine and peripheral d-fenfluramine injection on macronutrient intake in the rat. Brain Res. Bull., 25, 849 859.
58. Weiss, G.F., Rogacki, N., Fueg, A., Buchen, D., Suh, J.S., Wong, D.T. Leibowitz, S.F. (1991) Effect of hypothalamic and peripheral fluoxetine injection on natural patterns of macronutrient intake in the rat. Psychopharmacology (Berl.), 105, 467 476.
59. Welling, P.G. De la Iglesia, F.A. (1993) Drug Toxicokinetics. M. Dekker, New York.
60. Wiggins, R.C., Fuller, G. Enna, S.J. (1984) Undernutrition and the development of brain neurotransmitter systems. Life Sci., 35, 2085 2094.
61. Woodhams, P.L., Allen, Y.S., McGovern, J., Allen, J.M., Bloom, S.R., Balazs, R. Polak, J.M. (1985) Immunohistochemical analysis of the early ontogeny of the neuropeptide Y system in rat brain. Neuroscience, 15, 173 202.
62. Wynne, K., Stanley, S., McGowan, B. Bloom, S. (2005) Appetite control. J. Endocrinol., 184, 291 318.
63. Yura, S., Itoh, H., Sagawa, N., Yamamoto, H., Masuzaki, H., Nakao, K., Kawamura, M., Takemura, M., Kakui, K., Ogawa, Y. Fujii, S. (2005) Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab., 1, 371 378.