Intermittent access to liquid sucrose differentially modulates energy intake and related central pathways in control or high-fat fed mice

Physiology and Behavior

Volumn 140, Issue , 2015, Pages 44-53

  Soto, Marion ^a   Chaumontet, Catherine ^a   Even, Patrick C ^a   Nadkarni, Nachiket ^a   Piedcoq, Julien ^a   Darcel, Nicolas ^a   Tomé, Daniel ^a   Fromentin, Gilles ^a  

^a CENTRE MAURICE HALBWACHS   (France)

Author keywords

Binge like drinking; Energy balance; Intermittent access; Mice; Reward gene expression; Scheduled feeding; Sucrose solution

Indexed keywords

CANNABINOID RECEPTOR; CHOLECYSTOKININ; CHOLESTEROL; DOPAMINE RECEPTOR; DRINKING WATER; ENDOCANNABINOID; HIGH DENSITY LIPOPROTEIN; INSULIN; LEPTIN; NEUROPEPTIDE; OPIATE RECEPTOR; PROOPIOMELANCORTIN; SUCROSE; UNCLASSIFIED DRUG; GHRELIN; PEPTIDE YY; SWEETENING AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CALORIC INTAKE; CHOLECYSTOKININ BLOOD LEVEL; CHOLESTEROL BLOOD LEVEL; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRINKING BEHAVIOR; FAT MASS; FEEDING BEHAVIOR; FOOD INTAKE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HYPERPHAGIA; HYPOTHALAMUS; INSULIN BLOOD LEVEL; LIPID DIET; LIPOPROTEIN BLOOD LEVEL; LIQUID; MALE; METABOLITE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PROTEIN BLOOD LEVEL; SUBCUTANEOUS FAT; UPREGULATION; WEIGHT GAIN; ANATOMY AND HISTOLOGY; ANIMAL; BLOOD; BODY COMPOSITION; BRAIN; C57BL MOUSE; DRUG EFFECTS; EATING; FOOD DEPRIVATION; GENE EXPRESSION REGULATION; METABOLISM; TIME;

ANIMALS; BODY COMPOSITION; BODY WEIGHT; BRAIN; CHOLECYSTOKININ; DIET, HIGH-FAT; DRINKING BEHAVIOR; EATING; ENERGY INTAKE; FEEDING BEHAVIOR; FOOD DEPRIVATION; GENE EXPRESSION REGULATION; GHRELIN; LEPTIN; MALE; MICE; MICE, INBRED C57BL; PEPTIDE YY; SUCROSE; SWEETENING AGENTS; TIME FACTORS;

EID: 84916918783     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2014.12.008     Document Type: Article

References (76)

1. Vartanian L.R., Schwartz M.B., Brownell K.D. Effects of soft drink consumption on nutrition and health: a systematic review and meta-analysis. Am. J. Public Health 2007, 97(4):667-675.
2. Malik V.S., Pan A., Willett W.C., Hu F.B. Sugar-sweetened beverages and weight gain in children and adults: a systematic review and meta-analysis. Am. J. Clin. Nutr. 2013, 98(4):1084-1102.
3. Schulze M.B., Manson J.E., Ludwig D.S., Colditz G.A., Stampfer M.J., Willett W.C., Hu F.B. Sugar-sweetened beverages, weight gain, and incidence of type 2 diabetes in young and middle-aged women. JAMA 2004, 292(8):927-934.
4. de Ruyter J.C., Olthof M.R., Seidell J.C., Katan M.B. A trial of sugar-free or sugar-sweetened beverages and body weight in children. N. Engl. J. Med. 2012, 367(15):1397-1406.
5. Hu F.B. Resolved: there is sufficient scientific evidence that decreasing sugar-sweetened beverage consumption will reduce the prevalence of obesity and obesity-related diseases. Obes. Rev. 2013, 14(8):606-619.
6. Te Morenga L., Mallard S., Mann J. Dietary sugars and body weight: systematic review and meta-analyses of randomised controlled trials and cohort studies. BMJ 2013, 346:e7492.
7. Kaiser K.A., Shikany J.M., Keating K.D., Allison D.B. Will reducing sugar-sweetened beverage consumption reduce obesity? Evidence supporting conjecture is strong, but evidence when testing effect is weak. Obes. Rev. 2013, 14(8):620-633.
8. Mattes R.D., Shikany J.M., Kaiser K.A., Allison D.B. Nutritively sweetened beverage consumption and body weight: a systematic review and meta-analysis of randomized experiments. Obes. Rev. 2011, 12(5):346-365.
9. Drewnowski A., Bellisle F. Liquid calories, sugar, and body weight. Am. J. Clin. Nutr. 2007, 85(3):651-661.
10. Cao D., Lu H., Lewis T.L., Li L. Intake of sucrose-sweetened water induces insulin resistance and exacerbates memory deficits and amyloidosis in a transgenic mouse model of Alzheimer disease. J. Biol. Chem. 2007, 282(50):36275-36282.
11. Chou Y.C., Wang S.Y., Chen G.C., Lin Y.S., Chao P.M. The functional assessment of Alpinia pricei on metabolic syndrome induced by sucrose-containing drinking water in mice. Phytother. Res. 2009, 23(4):558-563.
12. Lindqvist A., de la Cour C.D., Stegmark A., Hakanson R., Erlanson-Albertsson C. Overeating of palatable food is associated with blunted leptin and ghrelin responses. Regul. Pept. 2005, 130(3):123-132.
13. Glendinning J.I., Breinager L., Kyrillou E., Lacuna K., Rocha R., Sclafani A. Differential effects of sucrose and fructose on dietary obesity in four mouse strains. Physiol. Behav. 2010, 101(3):331-343.
14. Ackroff K., Bonacchi K., Magee M., Yiin Y.M., Graves J.V., Sclafani A. Obesity by choice revisited: effects of food availability, flavor variety and nutrient composition on energy intake. Physiol. Behav. 2007, 92(3):468-478.
15. Lindqvist A., Baelemans A., Erlanson-Albertsson C. Effects of sucrose, glucose and fructose on peripheral and central appetite signals. Regul. Pept. 2008, 150(1-3):26-32.
16. Kanarek R.B., Orthen-Gambill N. Differential effects of sucrose, fructose and glucose on carbohydrate-induced obesity in rats. J. Nutr. 1982, 112(8):1546-1554.
17. Kawasaki T., Kashiwabara A., Sakai T., Igarashi K., Ogata N., Watanabe H., Ichiyanagi K., Yamanouchi T. Long-term sucrose-drinking causes increased body weight and glucose intolerance in normal male rats. Br. J. Nutr. 2005, 93(05):613.
18. Bocarsly M.E., Powell E.S., Avena N.M., Hoebel B.G. High-fructose corn syrup causes characteristics of obesity in rats: increased body weight, body fat and triglyceride levels. Pharmacol. Biochem. Behav. 2010, 97(1):101-106.
19. Jurgens H., Haass W., Castaneda T.R., Schurmann A., Koebnick C., Dombrowski F., Otto B., Nawrocki A.R., Scherer P.E., Spranger J., et al. Consuming fructose-sweetened beverages increases body adiposity in mice. Obes. Res. 2005, 13(7):1146-1156.
20. Avena N.M., Rada P., Hoebel B.G. Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci. Biobehav. Rev. 2008, 32(1):20-39.
21. Bello N.T., Lucas L.R., Hajnal A. Repeated sucrose access influences dopamine D2 receptor density in the striatum. Neuroreport 2002, 13(12):1575-1578.
22. Bello N.T., Sweigart K.L., Lakoski J.M., Norgren R., Hajnal A. Restricted feeding with scheduled sucrose access results in an upregulation of the rat dopamine transporter. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 284(5):R1260-R1268.
23. Colantuoni C., Schwenker J., McCarthy J., Rada P., Ladenheim B., Cadet J.L., Schwartz G.J., Moran T.H., Hoebel B.G. Excessive sugar intake alters binding to dopamine and mu-opioid receptors in the brain. Neuroreport 2001, 12(16):3549-3552.
24. Wojnicki F.H., Stine J.G., Corwin R.L. Liquid sucrose bingeing in rats depends on the access schedule, concentration and delivery system. Physiol. Behav. 2007, 92(4):566-574.
25. Boggiano M.M., Artiga A.I., Pritchett C.E., Chandler-Laney P.C., Smith M.L., Eldridge A.J. High intake of palatable food predicts binge-eating independent of susceptibility to obesity: an animal model of lean vs obese binge-eating and obesity with and without binge-eating. Int. J. Obes. 2007, 31(9):1357-1367.
26. Corwin R.L. Binge-type eating induced by limited access in rats does not require energy restriction on the previous day. Appetite 2004, 42(2):139-142.
27. Colantuoni C., Rada P., McCarthy J., Patten C., Avena N.M., Chadeayne A., Hoebel B.G. Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obes. Res. 2002, 10(6):478-488.
28. Berner L.A., Avena N.M., Hoebel B.G. Bingeing, self-restriction, and increased body weight in rats with limited access to a sweet-fat diet. Obesity 2008, 16(9):1998-2002.
29. Babbs R.K., Wojnicki F.H., Corwin R.L. Assessing binge eating. An analysis of data previously collected in bingeing rats. Appetite 2012, 59(2):478-482.
30. Woods S.C. Gastrointestinal satiety signals I. An overview of gastrointestinal signals that influence food intake. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 286(1):G7-G13.
31. Li J., Ma W., Wang S. Slower gastric emptying in high-fat diet induced obese rats is associated with attenuated plasma ghrelin and elevated plasma leptin and cholecystokinin concentrations. Regul. Pept. 2011, 171(1-3):53-57.
32. Xu J., McNearney T.A., Chen J.D. Impaired postprandial releases/syntheses of ghrelin and PYY(3-36) and blunted responses to exogenous ghrelin and PYY(3-36) in a rodent model of diet-induced obesity. J. Gastroenterol. Hepatol. 2011, 26(4):700-705.
33. Covasa M., Ritter R.C. Rats maintained on high-fat diets exhibit reduced satiety in response to CCK and bombesin. Peptides 1998, 19(8):1407-1415.
34. Feillet C.A. Food for thoughts: feeding time and hormonal secretion. J. Neuroendocrinol. 2010, 22(6):620-628.
35. Dourmashkin J.T., Chang G.Q., Gayles E.C., Hill J.O., Fried S.K., Julien C., Leibowitz S.F. Different forms of obesity as a function of diet composition. Int. J. Obes. 2005, 29(11):1368-1378.
36. Mercer J.G., Archer Z.A. Putting the diet back into diet-induced obesity: diet-induced hypothalamic gene expression. Eur. J. Pharmacol. 2008, 585(1):31-37.
37. Avena N.M., Rada P., Hoebel B.G. Sugar and fat bingeing have notable differences in addictive-like behavior. J. Nutr. 2009, 139(3):623-628.
38. Pritchett C.E., Hajnal A. Obesogenic diets may differentially alter dopamine control of sucrose and fructose intake in rats. Physiol. Behav. 2011, 104(1):111-116.
39. Naleid A.M., Grace M.K., Chimukangara M., Billington C.J., Levine A.S. Paraventricular opioids alter intake of high-fat but not high-sucrose diet depending on diet preference in a binge model of feeding. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293(1):R99-R105.
40. Rada P., Avena N.M., Hoebel B.G. Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 2005, 134(3):737-744.
41. Millar L., Rowland B., Nichols M., Swinburn B., Bennett C., Skouteris H., Allender S. Relationship between raised BMI and sugar sweetened beverage and high fat food consumption among children. Obesity 2014, 22(5):E96-E103.
42. Apolzan J.W., Harris R.B. Differential effects of chow and purified diet on the consumption of sucrose solution and lard and the development of obesity. Physiol. Behav. 2012, 105(2):325-331.
43. la Fleur S.E., Luijendijk M.C., van der Zwaal E.M., Brans M.A., Adan R.A. The snacking rat as model of human obesity: effects of a free-choice high-fat high-sugar diet on meal patterns. Int. J. Obes. 2014, 38(5):643-649.
44. Corwin R.L. The face of uncertainty eats. Curr. Drug Abuse Rev. 2011, 4(3):174-181.
45. Rasoamanana R., Chaumontet C., Nadkarni N., Tome D., Fromentin G., Darcel N. Dietary fibers solubilized in water or an oil emulsion induce satiation through CCK-mediated vagal signaling in mice. J. Nutr. 2012, 142(11):2033-2039.
46. Hayes M.R., Savastano D.M., Covasa M. Cholecystokinin-induced satiety is mediated through interdependent cooperation of CCK-A and 5-HT3 receptors. Physiol. Behav. 2004, 82(4):663-669.
47. Rasoamanana R., Even P.C., Darcel N., Tome D., Fromentin G. Dietary fibers reduce food intake by satiation without conditioned taste aversion in mice. Physiol. Behav. 2013, 110-111:13-19.
48. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, San Diego, CA.
49. Azzout-Marniche D., Chaumontet C., Nadkarni N.A., Piedcoq J., Fromentin G., Tome D., Even P.C. Food intake and energy expenditure are increased in high-fat-sensitive but not in high-carbohydrate-sensitive obesity-prone rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2014, 307(3):R299-R309.
50. Sellayah D., Sek K., Anthony F.W., Hanson M.A., Cagampang F.R. Sensitivity of housekeeping genes in the hypothalamus to mismatch in diets between pre- and postnatal periods in mice. Neurosci. Lett. 2008, 447(1):54-57.
51. Bachmanov A.A., Tordoff M.G., Beauchamp G.K. Sweetener preference of C57BL/6ByJ and 129P3/J mice. Chem. Senses 2001, 26(7):905-913.
52. Pothion S., Bizot J.C., Trovero F., Belzung C. Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav. Brain Res. 2004, 155(1):135-146.
53. Sclafani A. Sucrose motivation in sweet "sensitive" (C57BL/6J) and "subsensitive" (129P3/J) mice measured by progressive ratio licking. Physiol. Behav. 2006, 87(4):734-744.
54. Figlewicz D.P., Jay J.L., Acheson M.A., Magrisso I.J., West C.H., Zavosh A., Benoit S.C., Davis J.F. Moderate high fat diet increases sucrose self-administration in young rats. Appetite 2013, 61(1):19-29.
55. Lucas F., Sclafani A. Hyperphagia in rats produced by a mixture of fat and sugar. Physiol. Behav. 1990, 47(1):51-55.
56. DiMeglio D.P., Mattes R.D. Liquid versus solid carbohydrate: effects on food intake and body weight. Int. J. Obes. Relat. Metab. Disord. 2000, 24(6):794-800.
57. Bake T., Duncan J.S., Morgan D.G., Mercer J.G. Arcuate nucleus homeostatic systems are not altered immediately prior to the scheduled consumption of large, binge-type meals of palatable solid or liquid diet in rats and mice. J. Neuroendocrinol. 2013, 25(4):357-371.
58. Light H.R., Tsanzi E., Gigliotti J., Morgan K., Tou J.C. The type of caloric sweetener added to water influences weight gain, fat mass, and reproduction in growing Sprague-Dawley female rats. Exp. Biol. Med. (Maywood) 2009, 234(6):651-661.
59. Wojnicki F.H., Babbs R.K., Corwin R.L. Environments predicting intermittent shortening access reduce operant performance but not home cage binge size in rats. Physiol. Behav. 2013, 116-117:35-43.
60. Dissard R., Klein J., Caubet C., Breuil B., Siwy J., Hoffman J., Sicard L., Ducasse L., Rascalou S., Payre B., et al. Long term metabolic syndrome induced by a high fat high fructose diet leads to minimal renal injury in C57BL/6 mice. PLoS One 2013, 8(10):e76703.
61. Benoit B., Plaisancie P., Awada M., Geloen A., Estienne M., Capel F., Malpuech-Brugere C., Debard C., Pesenti S., Morio B., et al. High-fat diet action on adiposity, inflammation, and insulin sensitivity depends on the control low-fat diet. Nutr. Res. 2013, 33(11):952-960.
62. Kalsbeek A., Scheer F.A., Perreau-Lenz S., La Fleur S.E., Yi C.X., Fliers E., Buijs R.M. Circadian disruption and SCN control of energy metabolism. FEBS Lett. 2011, 585(10):1412-1426.
63. Escobar C., Martinez-Merlos M.T., Angeles-Castellanos M., del Carmen Minana M., Buijs R.M. Unpredictable feeding schedules unmask a system for daily resetting of behavioural and metabolic food entrainment. Eur. J. Neurosci. 2007, 26(10):2804-2814.
64. Savastano D.M., Covasa M. Adaptation to a high-fat diet leads to hyperphagia and diminished sensitivity to cholecystokinin in rats. J. Nutr. 2005, 135(8):1953-1959.
65. Nefti W., Chaumontet C., Fromentin G., Tome D., Darcel N. A high-fat diet attenuates the central response to within-meal satiation signals and modifies the receptor expression of vagal afferents in mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296(6):R1681-R1686.
66. Poggioli R., Vergoni A.V., Bertolini A. ACTH-(1-24) and alpha-MSH antagonize feeding behavior stimulated by kappa opiate agonists. Peptides 1986, 7(5):843-848.
67. Dutia R., Meece K., Dighe S., Kim A.J., Wardlaw S.L. Beta-endorphin antagonizes the effects of alpha-MSH on food intake and body weight. Endocrinology 2012, 153(9):4246-4255.
68. Millington G.W. Proopiomelanocortin (POMC): the cutaneous roles of its melanocortin products and receptors. Clin. Exp. Dermatol. 2006, 31(3):407-412.
69. Silva R.M., Hadjimarkou M.M., Rossi G.C., Pasternak G.W., Bodnar R.J. Beta-endorphin-induced feeding: pharmacological characterization using selective opioid antagonists and antisense probes in rats. J. Pharmacol. Exp. Ther. 2001, 297(2):590-596.
70. Tung Y.C., Piper S.J., Yeung D., O'Rahilly S., Coll A.P. A comparative study of the central effects of specific proopiomelancortin (POMC)-derived melanocortin peptides on food intake and body weight in pomc null mice. Endocrinology 2006, 147(12):5940-5947.
71. la Fleur S.E., van Rozen A.J., Luijendijk M.C., Groeneweg F., Adan R.A. A free-choice high-fat high-sugar diet induces changes in arcuate neuropeptide expression that support hyperphagia. Int. J. Obes. 2010, 34(3):537-546.
72. Olszewski P.K., Levine A.S. Central opioids and consumption of sweet tastants: when reward outweighs homeostasis. Physiol. Behav. 2007, 91(5):506-512.
73. Hajnal A., Smith G.P., Norgren R. Oral sucrose stimulation increases accumbens dopamine in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286(1):R31-R37.
74. Mahler S.V., Smith K.S., Berridge K.C. Endocannabinoid hedonic hotspot for sensory pleasure: anandamide in nucleus accumbens shell enhances 'liking' of a sweet reward. Neuropsychopharmacology 2007, 32(11):2267-2278.
75. Koob G.F., Volkow N.D. Neurocircuitry of addiction. Neuropsychopharmacology 2010, 35(1):217-238.
76. Avena N.M. The study of food addiction using animal models of binge eating. Appetite 2010, 55(3):734-737.