Brain responses to high-protein diets

Advances in Nutrition

Volumn 3, Issue 3, 2012, Pages 322-329

  Journel, Marion ^a,b   Chaumontet, Catherine ^b   Darcel, Nicolas ^a   Fromentin, Gilles ^b   Tomé, Daniel ^a  

^a AGROPARISTECH   (France)

^b CENTRE MAURICE HALBWACHS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLECYSTOKININ; GLUCAGON LIKE PEPTIDE 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PEPTIDE HORMONE; PEPTIDE YY; TARGET OF RAPAMYCIN KINASE;

ANIMAL; ARCUATE NUCLEUS; DIET; DRUG EFFECT; EATING; ENERGY METABOLISM; FEEDING BEHAVIOR; GASTROINTESTINAL TRACT; GENETICS; HOMEOSTASIS; HUMAN; HYPOTHALAMUS; METABOLISM; PHYSIOLOGY; PROTEIN INTAKE; REVIEW; SATIETY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ARCUATE NUCLEUS; CHOLECYSTOKININ; DIET; DIETARY PROTEINS; EATING; ENERGY METABOLISM; FEEDING BEHAVIOR; GASTROINTESTINAL TRACT; GLUCAGON-LIKE PEPTIDE 1; HOMEOSTASIS; HUMANS; HYPOTHALAMUS; PEPTIDE HORMONES; PEPTIDE YY; SATIATION; TOR SERINE-THREONINE KINASES;

EID: 84866775766     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.112.002071     Document Type: Review

References (71)

1. Fromentin G, Darcel N, Chaumontet C, Marsset-Baglieri A, Nadkarni N, Tome D. Peripheral and central mechanisms involved in the control of food intake by dietary amino acids and proteins. NRR. 2012; in press.
2. Koda S, Date Y, Murakami N, Shimbara T, Hanada T, Toshinai K, Niijima A, Furuya M, Inomata N, Osuye K, et al. The role of the vagal nerve in peripheral PYY3-36-induced feeding reduction in rats. Endocrinology. 2005;146:2369-75.
3. Veldhorst M, Smeets A, Soenen S, Hochstenbach-Waelen A, Hursel R, Diepvens K, Lejeune M, Luscombe-Marsh N, Westerterp-Plantenga M. Protein-induced satiety:effects and mechanisms of different proteins. Physiol Behav. 2008;94:300-7.
4. Moran TH, Dailey MJ. Intestinal feedback signaling and satiety. Physiol Behav. 2011;105:77-81.
5. Feurte S, Nicolaidis S, Even PC, Tome D, Mahe S, Fromentin G. Rapid fall in plasma threonine followed by increased intermeal interval in response to first ingestion of a threonine-devoid diet in rats. Appetite. 1999;33:329-41.
6. Hao S, Sharp JW, Ross-Inta CM, McDaniel BJ, Anthony TG, Wek RC, Cavener DR, McGrath BC, Rudell JB, Koehnle TJ, et al. Uncharged tRNA and sensing of amino acid deficiency in mammalian piriform cortex. Science. 2005;307:1776-8.
7. Whitedouble Dagger BD, Porter MH, Martin RJ. Protein selection, food intake, and body composition in response to the amount of dietary protein. Physiol Behav. 2000;69:383-9.
8. Sorensen A, Mayntz D, Raubenheimer D, Simpson SJ. Protein-leverage in mice:the geometry of macronutrient balancing and consequences for fat deposition. Obesity (Silver Spring). 2008;16:566-71.
9. Harper AE, Peters JC. Protein intake, brain amino acid and serotonin concentrations and protein self-selection. J Nutr. 1989;119:677-89.
10. Du F, Higginbotham DA, White BD. Food intake, energy balance and serum leptin concentrations in rats fed low-protein diets. J Nutr. 2000;130:514-21.
11. Bensaïd A, Tome D, L'Heureux-Bourdon D, Even P, Gietzen D, Morens C, Gaudichon C, Larue-Achagiotis C, Fromentin G. A high-protein diet enhances satiety without conditioned taste aversion in the rat. Physiol Behav. 2003;78:311-20.
12. Morrison CD, Xi X, White CL, Ye J, Martin RJ. Amino acids inhibit Agrp gene expression via an mTOR-dependent mechanism. Am J Physiol Endocrinol Metab. 2007;293:E165-71.
13. Griffioen-Roose S, Mars M, Siebelink E, Finlayson G, Tome D, de Graaf C. Protein status elicits compensatory changes in food intake and food preferences. Am J Clin Nutr. 2012;95:32-8.
14. L'Heureux-Bouron D, Tome D, Bensaid A, Morens C, Gaudichon C, Fromentin G. A very high 70%-protein diet does not induce conditioned taste aversion in rats. J Nutr. 2004;134:1512-5.
15. Bensaid A, Tome D, Gietzen D, Even P, Morens C, Gausseres N, Fromentin G. Protein is more potent than carbohydrate for reducing appetite in rats. Physiol Behav. 2002;75:577-82.
16. Pichon L, Potier M, Tome D, Mikogami T, Laplaize B, Martin-Rouas C, Fromentin G. High-protein diets containing different milk protein fractions differently influence energy intake and adiposity in the rat. Br J Nutr. 2008;99:739-48.
17. Jean C, Rome S, Mathe V, Huneau JF, Aattouri N, Fromentin G, Achagiotis CL, Tome D. Metabolic evidence for adaptation to a high protein diet in rats. J Nutr. 2001;131:91-8.
18. Kinzig KP, Hargrave SL, Hyun J, Moran TH. Energy balance and hypothalamic effects of a high-protein/low-carbohydrate diet. Physiol Behav. 2007;92:454-60.
19. Ropelle ER, Pauli JR, Fernandes MFA, Rocco SA, Marin RM, Morari J, Souza KK, Dias MM, Gomes-Marcondes MC, Gontijo JAR, et al. A central role for neuronal AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) in high-protein diet-induced weight loss. Diabetes. 2008;57:594-605.
20. Skov AR, Toubro S, Ronn B, Holm L, Astrup A. Randomized trial on protein vs carbohydrate in ad libitum fat reduced diet for the treatment of obesity. Int J Obes Relat Metab Disord. 1999;23:528-36.
21. Josse AR, Atkinson SA, Tarnopolsky MA, Phillips SM. Increased consumption of dairy foods and protein during diet-and exercise-induced weight loss promotes fat mass loss and lean mass gain in overweight and obese premenopausal women. J Nutr. 2011;141:1626-34.
22. Acheson KJ, Blondel-Lubrano A, Oguey-Araymon S, Beaumont M, Emady-Azar S, Ammon-Zufferey C, Monnard I, Pinaud S, Nielsen-Moennoz C, Bovetto L. Protein choices targeting thermogenesis and metabolism. Am J Clin Nutr. 2011;93:525-34.
23. Westerterp-Plantenga MS, Lejeune MP, Nijs I, van Ooijen M, Kovacs EM. High protein intake sustains weight maintenance after body weight loss in humans. Int J Obes Relat Metab Disord. 2004;28:57-64.
24. Porrini M, Crovetti R, Testolin G, Silva S. Evaluation of satiety sensations and food intake after different preloads. Appetite. 1995;25:17-30.
25. Johnstone AM, Stubbs RJ, Harbron CG. Effect of overfeeding macronutrients on day-to-day food intake in man. Eur J Clin Nutr. 1996; 50:418-30.
26. Poppitt SD, McCormack D, Buffenstein R. Short-term effects of macronutrient preloads on appetite and energy intake in lean women. Physiol Behav. 1998;64:279-85.
27. Stubbs RJ, O'Reilly LM, Johnstone AM, Harrison CL, Clark H, Franklin MF, Reid CA, Mazlan N. Description and evaluation of an experimental model to examine changes in selection between high-protein, high-carbohydrate and high-fat foods in humans. Eur J Clin Nutr. 1999;53:13-21.
28. Potier M, Fromentin G, Lesdema A, Benamouzig R, Tome D, Marsset-Baglieri A. The satiety effect of disguised liquid preloads administered acutely and differing only in their nutrient content tended to be weaker for lipids but did not differ between proteins and carbohydrates in human subjects. Br J Nutr. 2010;104:1406-14.
29. Westerterp-Plantenga MS, Rolland V, Wilson SA, Westerterp KR. Satiety related to 24 h diet-induced thermogenesis during high protein/carbohydrate vs high fat diets measured in a respiration chamber. Eur J Clin Nutr. 1999;53:495-502.
30. Porrini M, Santangelo A, Crovetti R, Riso P, Testolin G, Blundell JE. Weight, protein, fat, and timing of preloads affect food intake. Physiol Behav. 1997;62:563-70.
31. Weigle DS, Breen PA, Matthys CC, Callahan HS, Meeuws KE, Burden VR, Purnell JQ. A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr. 2005;82:41-8.
32. Batterham RL, Heffron H, Kapoor S, Chivers JE, Chandarana K, Herzog H, Le Roux CW, Thomas EL, Bell JD, Withers DJ. Critical role for peptide YY in protein-mediated satiation and body-weight regulation. Cell Metab. 2006;4:223-33.
33. Anderson GH, Tecimer SN, Shah D, Zafar TA. Protein source, quantity, and time of consumption determine the effect of proteins on shortterm food intake in young men. J Nutr. 2004;134:3011-5.
34. Veldhorst MA, Nieuwenhuizen AG, Hochstenbach-Waelen A, van Vught AJ, Westerterp KR, Engelen MP, Brummer RJ, Deutz NE, Westerterp-Plantenga MS. Dose-dependent satiating effect of whey relative to casein or soy. Physiol Behav. 2009;96:675-82.
35. Lejeune MP, Westerterp KR, Adam TC, Luscombe-Marsh ND,Westerterp-Plantenga MS. Ghrelin and glucagon-like peptide 1 concentrations, 24-h satiety, and energy and substrate metabolism during a high-protein diet and measured in a respiration chamber. Am J Clin Nutr. 2006; 83:89-94.
36. Hochstenbach-Waelen A, Veldhorst MA, Nieuwenhuizen AG, Westerterp-Plantenga MS, Westerterp KR. Comparison of 2 diets with either 25% or 10% of energy as casein on energy expenditure, substrate balance, and appetite profile. Am J Clin Nutr. 2009;89:831-8.
37. Tomé D, Schwarz J, Darcel N, Fromentin G. Protein, amino acids, vagus nerve signaling, and the brain. Am J Clin Nutr. 2009;90:838S-43S.
38. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS. The receptors for mammalian sweet and umami taste. Cell. 2003;115:255-66.
39. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS. An amino-acid taste receptor. Nature. 2002;416:199-202.
40. Chaudhari N, Landin AM, Roper SD. A metabotropic glutamate receptor variant functions as a taste receptor. Nat Neurosci. 2000;3:113-9.
41. Blackshaw LA, Page AJ, Young RL. Metabotropic glutamate receptors as novel therapeutic targets on visceral sensory pathways. Front Neurosci. 2011;5:40.
42. Rasoamanana R, Darcel N, Fromentin G, Tome D. Nutrient sensing and signalling by the gut. Proc Nutr Soc. 2012;1-10.
43. Niijima A. Reflex effects of oral, gastrointestinal and hepatoportal glutamate sensors on vagal nerve activity. J Nutr. 2000;130(4S Suppl): 971S-3S.
44. Leech CA, Habener JF. Regulation of glucagon-like peptide-1 receptor and calcium-sensing receptor signaling by L-histidine. Endocrinology. 2003;144:4851-8.
45. Hira T, Nakajima S, Eto Y, Hara H. Calcium-sensing receptor mediates phenylalanine-induced cholecystokinin secretion in enteroendocrine STC-1 cells. FEBS J. 2008;275:4620-6.
46. Nakajima S, Hira T, Eto Y, Asano K, Hara H. Soybean beta 51-63 peptide stimulates cholecystokinin secretion via a calcium-sensing receptor in enteroendocrine STC-1 cells. Regul Pept. 2010;159:148-55.
47. Cordier-Bussat M, Bernard C, Haouche S, Roche C, Abello J, Chayvialle JA, Cuber JC. Peptones stimulate cholecystokinin secretion and gene transcription in the intestinal cell line STC-1. Endocrinology. 1997; 138:1137-44.
48. Cordier-Bussat M, Bernard C, Levenez F, Klages N, Laser-Ritz B, Philippe J, Chayvialle JA, Cuber JC. Peptones stimulate both the secretion of the incretin hormone glucagon-like peptide 1 and the transcription of the proglucagon gene. Diabetes. 1998;47:1038-45.
49. Choi S, Lee M, Shiu AL, Yo SJ, Hallden G, Aponte GW. GPR93 activation by protein hydrolysate induces CCK transcription and secretion in STC-1 cells. Am J Physiol Gastrointest Liver Physiol. 2007;292:G1366-75.
50. Darcel NP, Liou AP, Tome D, Raybould HE. Activation of vagal afferents in the rat duodenum by protein digests requires PepT1. J Nutr. 2005;135:1491-5.
51. Liou AP, Chavez DI, Espero E, Hao S, Wank SA, Raybould HE. Protein hydrolysate-induced cholecystokinin secretion from enteroendocrine cells is indirectly mediated by the intestinal oligopeptide transporter PepT1. Am J Physiol Gastrointest Liver Physiol. 2011;300: G895-902.
52. Matsumura K, Miki T, Jhomori T, Gonoi T, Seino S. Possible role of PEPT1 in gastrointestinal hormone secretion. Biochem Biophys Res Commun. 2005;336:1028-32.
53. Faipoux R, Tome D, Gougis S, Darcel N, Fromentin G. Proteins activate satiety-related neuronal pathways in the brainstem and hypothalamus of rats. J Nutr. 2008;138:1172-8.
54. Schwarz J, Burguet J, Rampin O, Fromentin G, Andrey P, Tome D, Maurin Y, Darcel N. Three-dimensional macronutrient-associated Fos expression patterns in the mouse brainstem. PLoS ONE. 2010;5:e8974.
55. Nefti W. Les modifications de la sensibilité du nerf vague aux neuropeptides gastro-intestinaux induites par des situations nutritionnelles chez la souris:bases cellulaires et conséquences sur le comportement alimentaire. Thesis. Paris:Agroparistech, 2009. 138 p.
56. Tsujino N, Yamanaka A, Ichiki K, Muraki Y, Kilduff TS, Yagami K, Takahashi S, Goto K, Sakurai T. Cholecystokinin activates orexin/-hypocretin neurons through the cholecystokinin A receptor. J Neurosci. 2005;25:7459-69.
57. Minokoshi Y, Alquier T, Furukawa N, Kim YB, Lee A, Xue B, Mu J, Foufelle F, Ferre P, Birnbaum MJ, et al. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature. 2004;428:569-74.
58. Cota D, Proulx K, Blake S, Kathi A, Kozma SC, Thomas G, Woods SC, Seeley RJ. Hypothalamic mTOR signaling regulates food intake. Science. 2006;312:927-30.
59. McArthur LH, Kelly WF, Gietzen DW, Rogers QR. The role of palatability in the food intake response of rats fed high-protein diets. Appetite. 1993;20:181-96.
60. Semon BA, Leung PM, Rogers QR, Gietzen DW. Effect of type of protein on food intake of rats fed high protein diets. Physiol Behav. 1987; 41:451-8.
61. Pérez C, Ackroff K, Sclafani A. Carbohydrate-and protein-conditioned flavor preferences:effects of nutrient preloads. Physiol Behav. 1996;59: 467-74.
62. Holsen LM, Zarcone JR, Thompson TI, Brooks WM, Anderson MF, Ahluwalia JS, Nollen NL, Savage CR. Neural mechanisms underlying food motivation in children and adolescents. Neuroimage. 2005;27: 669-76.
63. Goldstone AP, Prechtl de Hernandez CG, Beaver JD, Muhammed K, Croese C, Bell G, Durighel G, Hughes E, Waldman AD, Frost G, et al. Fasting biases brain reward systems towards high-calorie foods. Eur J Neurosci. 2009;30:1625-35.
64. Zeeni N, Nadkarni N, Bell JD, Even PC, Fromentin G, Tome D, Darcel N. Peripherally injected cholecystokinin-induced neuronal activation is modified by dietary composition in mice. Neuroimage. 2010;50:1560-5.
65. Potier M. Caractérisation de l'effet satiétogène des protéines et mécanismes impliqués:application aux protéines laitières. Thesis. Paris: Agroparistech, 2009.
66. Min DK, Tuor UI, Koopmans HS, Chelikani PK. Changes in differential functional magnetic resonance signals in the rodent brain elicited by mixed-nutrient or protein-enriched meals. Gastroenterology. 2011; 141:1832-41.
67. Leidy HJ, Lepping RJ, Savage CR, Harris CT. Neural responses to visual food stimuli after a normal vs. higher protein breakfast in breakfastskipping teens:a pilot fMRI study. Obesity (Silver Spring) 2011;19: 2019-25.
68. Choi S, Disilvio B, Fernstrom MH, Fernstrom JD. Meal ingestion, amino acids and brain neurotransmitters:effects of dietary protein source on serotonin and catecholamine synthesis rates. Physiol Behav. 2009;98:156-62.
69. Choi S, DiSilvio B, Fernstrom MH, Fernstrom JD. The chronic ingestion of diets containing different proteins produces marked variations in brain tryptophan levels and serotonin synthesis in the rat. Neurochem Res. 2011;36:559-65.
70. Akana SF. Feeding and stress interact through the serotonin 2C receptor in developing mice. Physiol Behav. 2008;94:569-79.
71. Fernstrom JD, Fernstrom MH. Tyrosine, phenylalanine, and catecholamine synthesis and function in the brain. J Nutr. 2007;137:1539S-47S.