Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods

American Journal of Clinical Nutrition

Volumn 104, Issue 1, 2016, Pages 5-14

  Byrne, Claire S ^a   Chambers, Edward S ^a   Alhabeeb, Habeeb ^a   Chhina, Navpreet ^a   Morrison, Douglas J ^b   Preston, Tom ^b   Tedford, Catriona ^c   Fitzpatrick, Julie ^a   Irani, Cherag ^a   Busza, Albert ^a   Garcia Perez, Isabel ^d   Fountana, Sofia ^d   Holmes, Elaine ^d   Goldstone, Anthony P ^a   Frost, Gary S ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b SCOTTISH UNIVERSITIES ENVIRONMENTAL RESEARCH CENTRE   (United Kingdom)

^c UNIVERSITY OF THE WEST OF SCOTLAND   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Appetite; fMRI; Propionate; Reward; Striatum

Indexed keywords

COLONIC PROPIONATE; ESTER DERIVATIVE; GASTROINTESTINAL HORMONE; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; HYDROGEN; INSULIN; INULIN; INULIN PROPIONATE ESTER; PEPTIDE YY; PLACEBO; PROPIONIC ACID; UNCLASSIFIED DRUG; GLUCOSE BLOOD LEVEL; PROPIONIC ACID DERIVATIVE;

ADULT; AGED; AMYGDALA; ANTERIOR INSULA; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; BRAIN REGION; CALORIC INTAKE; CAUDATE NUCLEUS; CONTROLLED STUDY; CORPUS STRIATUM; CROSSOVER PROCEDURE; FEEDING BEHAVIOR; FEMALE; FOOD; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HORMONE RELEASE; HUMAN; INSULIN BLOOD LEVEL; MALE; NORMAL HUMAN; NUCLEUS ACCUMBENS; ORBITAL CORTEX; RANDOMIZED CONTROLLED TRIAL; REACTION TIME; REWARD; SINGLE BLIND PROCEDURE; VISUAL ANALOG SCALE; ANTICIPATION; APPETITE; ASSOCIATION; BLOOD; COLON; FOOD INTAKE; GLUCOSE BLOOD LEVEL; MEAL; METABOLISM; MIDDLE AGED; NERVE TRACT; SATIETY RESPONSE;

ADULT; ANTICIPATION, PSYCHOLOGICAL; APPETITE; APPETITE REGULATION; BLOOD GLUCOSE; COLON; CORPUS STRIATUM; CROSS-OVER STUDIES; CUES; ENERGY INTAKE; GASTROINTESTINAL HORMONES; GLUCAGON-LIKE PEPTIDE 1; HUMANS; INSULIN; INULIN; MALE; MEALS; MIDDLE AGED; NEURAL PATHWAYS; PEPTIDE YY; PROPIONATES; REWARD; SATIETY RESPONSE;

EID: 84977084263     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.115.126706     Document Type: Article

References (48)

1. Murphy KG, Bloom SR. Gut hormones and the regulation of energy homeostasis. Nature 2006;444:854-9.
2. Dagher A. Functional brain imaging of appetite. Trends Endocrinol Metab 2012;23:250-60.
3. Goldstone AP, Prechtl de Hernandez CG, Beaver JD, Muhammed K, Croese C, Bell G, Durighel G, Hughes E, Waldman AD, Frost G. Fasting biases brain reward systems towards high-calorie foods. Eur J Neurosci 2009;30:1625-35.
4. De Silva A, Salem V, Long CJ, Makwana A, Newbould RD, Rabiner EA, Ghatei MA, Bloom SR, Matthews PM, Beaver JD. The gut hormones PYY 3-36 and GLP-1 7-36 amide reduce food intake and modulate brain activity in appetite centers in humans. Cell Metab 2011;14:700-6.
5. Shen L, Keenan MJ, Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, Zhou J. Dietary resistant starch increases hypothalamic POMC expression in rats. Obesity (Silver Spring) 2009;17:40-5.
6. So P-W, Yu W-S, Kuo Y-T, Wasserfall C, Goldstone AP, Bell JD, Frost G. Impact of resistant starch on body fat patterning and central appetite regulation. PLoS One 2007;2:e1309.
7. Frost G, Sleeth ML, Sahuri-Arisoylu M, Lizarbe B, Cerdan S, Brody L, Anastasovska J, Ghourab S, Hankir M, Zhang S. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun 2014;5:3611.
8. Cani PD, Neyrinck AM, Maton N, Delzenne NM. Oligofructose promotes satiety in rats fed a high-fat diet: involvement of glucagon-like peptide-1. Obes Res 2005;13:1000-7.
9. Delmée E, Cani PD, Gual G, Knauf C, Burcelin R, Maton N, Delzenne NM. Relation between colonic proglucagon expression and metabolic response to oligofructose in high fat diet-fed mice. Life Sci 2006;79:1007-13.
10. Arora T, Loo RL, Anastasovska J, Gibson GR, Tuohy KM, Sharma RK, Swann JR, Deaville ER, Sleeth ML, Thomas EL. Differential effects of two fermentable carbohydrates on central appetite regulation and body composition. PLoS One 2012;7:e43263.
11. Cummings JH, Pomare E, Branch W, Naylor C, Macfarlane G. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 1987;28:1221-7.
12. Chambers ES, Viardot A, Psichas A, Morrison DJ, Murphy KG, Zac-Varghese SE, MacDougall K, Preston T, Tedford C, Finlayson GS. Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut 2015;64:1744-54.
13. Psichas A, Sleeth M, Murphy K, Brooks L, Bewick G, Hanyaloglu A, Ghatei M, Bloom S, Frost G. The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents. Int J Obes (Lond) 2015;39:424-9.
14. van Bloemendaal L, IJzerman RG, Ten Kulve JS, Barkhof F, Konrad RJ, Drent ML, Veltman DJ, Diamant M. GLP-1 receptor activation modulates appetite-and reward-related brain areas in humans. Diabetes 2014;63:4186-96.
15. Berthoud H-R. Metabolic and hedonic drives in the neural control of appetite: who is the boss? Curr Opin Neurobiol 2011;21:888-96.
16. Volkow ND, Wang G-J, Tomasi D, Baler RD. The addictive dimensionality of obesity. Biol Psychiatry 2013;73:811-8.
17. Goldstone AP, Prechtl CG, Scholtz S, Miras AD, Chhina N, Durighel G, Deliran SS, Beckmann C, Ghatei MA, Ashby DR. Ghrelin mimics fasting to enhance human hedonic, orbitofrontal cortex, and hippocampal responses to food. Am J Clin Nutr 2014;99:1319-30.
18. Scholtz S, Miras AD, Chhina N, Prechtl CG, Sleeth ML, Daud NM, Ismail NA, Durighel G, Ahmed AR, Olbers T. Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding. Gut 2014;63:891-902.
19. Goldstone AP, Miras AD, Scholtz S, Jackson S, Neff KJ, Pénicaud L, Geoghegan J, Chhina N, Durighel G, Bell JD. Link between increased satiety gut hormones and reduced food reward following gastric bypass surgery for obesity. J Clin Endocrinol Metab 2016;101: 599-609.
20. Beck AT, Steer RA, Ball R, Ranieri WF. Comparison of Beck Depression Inventories-IA and-II in psychiatric outpatients. J Pers Assess 1996;67:588-97.
21. Killgore WD, Yurgelun-Todd DA. Affect modulates appetite-related brain activity to images of food. Int J Eat Disord 2006;39:357-63.
22. Levitt MD. Production and excretion of hydrogen gas in man. N Engl J Med 1969;281:122-7.
23. Woodend DM, Anderson GH. Effect of sucrose and safflower oil preloads on short term appetite and food intake of young men. Appetite 2001;37:185-95.
24. Adrian TE, Ferri G, Bacarese-Hamilton A, Fuessl H, Polak J, Bloom S. Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology 1985;89:1070-7.
25. Kreymann B, Ghatei M, Williams G, Bloom S. Glucagon-like peptide-1 7-36: a physiological incretin in man. Lancet 1987;2:1300-4.
26. Moreau NM, Goupry S, Antignac J, Monteau F, Le Bizec B, Champ M, Martin L, Dumon H. Simultaneous measurement of plasma concentrations and 13 C-enrichment of short-chain fatty acids, lactic acid and ketone bodies by gas chromatography coupled to mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2003;784:395-403.
27. Finlayson G, King N, Blundell J. The role of implicit wanting in relation to explicit liking and wanting for food: implications for appetite control. Appetite 2008;50:120-7.
28. Fletcher PC, Napolitano A, Skeggs A, Miller SR, Delafont B, Cambridge VC, de Wit S, Nathan PJ, Brooke A, O'Rahilly S. Distinct modulatory effects of satiety and sibutramine on brain responses to food images in humans: a double dissociation across hypothalamus, amygdala, and ventral striatum. J Neurosci 2010;30:14346-55.
29. Stice E, Burger K, Yokum S. Caloric deprivation increases responsivity of attention and reward brain regions to intake, anticipated intake, and images of palatable foods. Neuroimage 2013;67:322-30.
30. Lawrence NS, Hinton EC, Parkinson JA, Lawrence AD. Nucleus accumbens response to food cues predicts subsequent snack consumption in women and increased body mass index in those with reduced self-control. Neuroimage 2012;63:415-22.
31. Thomas JM, Higgs S, Dourish CT, Hansen PC, Harmer CJ, McCabe C. Satiation attenuates BOLD activity in brain regions involved in reward and increases activity in dorsolateral prefrontal cortex: an fMRI study in healthy volunteers. Am J Clin Nutr 2015;101:697-704.
32. Gautier JF, Parigi A, Chen K, Salbe AD, Bandy D, Pratley RE, Ravussin E, Reiman EM, Tataranni PA. Effect of satiation on brain activity in obese and lean women. Obes Res 2001;9:676-84.
33. Murdaugh DL, Cox JE, Cook EW, Weller RE. fMRI reactivity to high-calorie food pictures predicts short-and long-term outcome in a weight-loss program. Neuroimage 2012;59:2709-21.
34. Burger KS, Stice E. Variability in reward responsivity and obesity: evidence from brain imaging studies. Curr Drug Abuse Rev 2011;4:182.
35. Stice E, Burger KS, Yokum S. Reward region responsivity predicts future weight gain and moderating effects of the TaqIA allele. J Neurosci 2015;35:10316-24.
36. Stice E, Spoor S, Bohon C, Small D. Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 2008;322:449-52.
37. Liou AP, Paziuk M, Luevano J-M, Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Trans Med 2013;5:178ra41.
38. Carmichael FJ, Israel Y, Crawford M, Minhas K, Saldivia V, Sandrin S, Campisi P, Orrego H. Central nervous system effects of acetate: contribution to the central effects of ethanol. J Pharmacol Exp Ther 1991;259:403-8.
39. Pedersen C, Lefevre S, Peters V, Patterson M, Ghatei MA, Morgan LM, Frost GS. Gut hormone release and appetite regulation in healthy non-obese participants following oligofructose intake. A dose-escalation study. Appetite 2013;66:44-53.
40. Peters SG, Pomare E, Fisher C. Portal and peripheral blood short chain fatty acid concentrations after caecal lactulose instillation at surgery. Gut 1992;33:1249-52.
41. den Besten G, Lange K, Havinga R, van Dijk TH, Gerding A, van Eunen K, Müller M, Groen AK, Hooiveld GJ, Bakker BM. Gut-derived short-chain fatty acids are vividly assimilated into host carbohydrates and lipids. Am J Physiol Gastrointest Liver Physiol 2013;305:G900-10.
42. van der Beek CM, Bloemen JG, van den Broek MA, Lenaerts K, Venema K, Buurman WA, Dejong CH. Hepatic uptake of rectally administered butyrate prevents an increase in systemic butyrate concentrations in humans. J Nutr 2015;145:2019-24.
43. Anastasovska J, Arora T, Canon GJS, Parkinson JR, Touhy K, Gibson GR, Nadkarni NA, So PW, Goldstone AP, Thomas EL. Fermentable carbohydrate alters hypothalamic neuronal activity and protects against the obesogenic environment. Obesity (Silver Spring) 2012;20:1016-23.
44. Anil MH, Forbes J. Feeding in sheep during intraportal infusions of short-chain fatty acids and the effect of liver denervation. J Physiol 1980;298:407-14.
45. Anil MH, Forbes J. The roles of hepatic nerves in the reduction of food intake as a consequence of intraportal sodium propionate administration in sheep. Q. Q J Exp Physiol 1988;73:539-46.
46. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, Bäckhed F, Mithieux G. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 2014;156:84-96.
47. Lal S, Kirkup AJ, Brunsden AM, Thompson DG, Grundy D. Vagal afferent responses to fatty acids of different chain length in the rat. Am J Physiol Gastrointest Liver Physiol 2001;281:G907-15.
48. Kentish SJ, Page AJ. The role of gastrointestinal vagal afferent fibres in obesity. J Physiol 2015;593:775-86.