Roux-en-Y gastric bypass in rats increases sucrose taste-related motivated behavior independent of pharmacological GLP-1-receptor modulation

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 302, Issue 6, 2012, Pages 751-767

  Mathes, C M ^a   Bueter, M ^b   Smith, K R ^a   Lutz, T A ^c   le Roux, C W ^b   Spector, A C ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b HAMMERSMITH HOSPITAL   (United Kingdom)

^c VETSUISSE FACULTY UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Anorexigenic peptides; Bariatric surgery; Gustatory; Sugar; Type 2 diabetes mellitus

Indexed keywords

EXENDIN 3; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; HORMONE RECEPTOR BLOCKING AGENT; SUCROSE; UNCLASSIFIED DRUG; WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; APPETITE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; GLASS BOTTLE; INCREASED APPETITE; KNOCKOUT MOUSE; LEAN BODY WEIGHT; LICKING; MALE; MOTIVATION; MOUSE; NONHUMAN; OBESITY; POSTOPERATIVE PERIOD; PREOPERATIVE EVALUATION; PRIORITY JOURNAL; RAT; ROUX Y ANASTOMOSIS; SHAM PROCEDURE; STOMACH BYPASS; SUGAR INTAKE; TASTE ACUITY;

ANIMALS; APPETITE; BEHAVIOR, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRINKING; EATING; GASTRIC BYPASS; INJECTIONS, INTRAPERITONEAL; MALE; MODELS, ANIMAL; PEPTIDE FRAGMENTS; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCAGON; SUCROSE; TIME FACTORS; VENOMS;

EID: 84863393484     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00214.2011     Document Type: Article

References (75)

1. Aja S, Schwartz GJ, Kuhar MJ, Moran TH. Intracerebroventricular CART peptide reduces ingestive behavior and alters licking microstructure. Am J Physiol Regul Integr Comp Physiol 280: R1613-R1619, 2001.
2. Barnett AH, Burger J, Johns D, Brodows R, Kendall DM, Roberts A, Trautmann ME. Tolerability and efficacy of exenatide and titrated insulin glargine in adult patients with type 2 diabetes previously uncontrolled with metformin or a sulfonylurea: a multinational, randomized, open-label, twoperiod, crossover noninferiority trial. Clin Ther 29: 2333-2348, 2007.
3. Barrera JG, D'Alessio DA, Drucker DJ, Woods SC, Seeley RJ. Differences in the central anorectic effects of glucagon-like peptide-1 and exendin-4 in rats. Diabetes 58: 2820-2827, 2009.
4. Bavaresco M, Simara P, Lima TP, Salgado W Jr, Ceneviva R, Dos Santos JE, Nonino-Borges CB. Nutritional course of patients submitted to bariatric surgery. Obes Surg 20: 716-21, 2010.
5. Bojanowska E, Nowak A. Interactions between leptin and exendin-4, a glucagon-like peptide-1 agonist, in the regulation of food intake in the rat. J Physiol Pharmacol 58: 349-360, 2007.
6. Borg CM, le Roux CW, Ghatei MA, Bloom SR, Patel AG, Aylwin SJ. Progressive rise in gut hormone levels after Roux-en-Y gastric bypass suggests gut adaptation and explains altered satiety. Br J Surg 93: 210-215, 2006.
7. Brolin RL, Robertson LB, Kenler HA, Cody RP. Weight loss and dietary intake after vertical banded gastroplasty and roux-en-y gastric bypass. Ann Surg 220: 782-790, 1994.
8. Brosvic GM, Slotnick BM. Absolute and intensity-difference taste thresholds in the rat: evaluation of an automated multi-channel gustometer. Physiol Behav 38: 711-717, 1986.
9. Brown EK, Settle EA, Van Rij AM. Food intake patterns of gastric bypass patients. J Am Diet Assoc 80: 437-443, 1982.
10. Bueter M, Ashrafian H, Frankel AH, Tam FW, Unwin RJ, le Roux CW. Sodium and water handling after gastric bypass surgery in a rat model. Surg Obes Relat Dis 7: 68-73, 2011.
11. Bueter M, Lowenstein C, Ashrafian H, Hillebrand J, Bloom SR, Olbers T, Lutz T, Le Roux CW. Vagal sparing surgical technique but not stoma size affects body weight loss in rodent model of gastric bypass. Obes Surg 20: 616-622, 2010.
12. Bueter M, Lowenstein C, Olbers T, Wang M, Cluny NL, Bloom SR, Sharkey KA, Lutz TA, Le Roux CW. Gastric bypass increases energy expenditure in rats. Gastroenterology 138: 1845-1853, 2010.
13. Bueter M, Miras AD, Chichger H, Fenske W, Ghatei MA, Bloom SR, Unwin RJ, Lutz TA, Spector AC, le Roux CW. Alterations of sucrose preference after Roux-en-Y gastric bypass. Physiol Behav 104: 709-721, 2011.
14. Burge JC, Schaumburg JZ, Choban PS, DiSilvestro RA, Flancbaum L. Changes in patients' taste acuity after Roux-en-Y gastric bypass for clinically severe obesity. J Am Diet Assoc 95: 666-670, 1995.
15. Corbit JD, Luschei ES. Invariance of the rat's rate of drinking. J Comp Physiol Psychol 60: 119-125, 1969.
16. Coughlin K, Bell RM, Bivins BA, Wrobel S, Griffen WO. Preoperative and postoperative assessment of nutrient intakes in patients who have undergone gastric bypass surgery. Arch Surg 118: 813-816, 1983.
17. Davis JD, Smith GP. Analysis of the microstructure of the rhythmic tongue movements of rats ingesting maltose and sucrose solutions. Behav Neurosci 106: 217-228, 1992.
18. Drewnowski A, Brunzell JD, Sande K, Iverius PH, Greenwood MR. Sweet tooth reconsidered: taste responsiveness in human obesity. Physiol Behav 35: 617-622, 1985.
19. Fowler SC, Mortell C. Low doses of haloperidol interfere with rat tongue extensions during licking: a quantitative analysis. Behav Neurosci 106: 386-395, 1992.
20. Gramling SE, Fowler SC. Some effects of pimozide and of shifts in sucrose concentration on lick rate, duration, and interlick interval. Pharmacol Biochem Behav 25: 219-222, 1986.
21. Hajnal A, Kovacs P, Ahmed T, Meirelles K, Lynch CJ, Cooney RN. Gastric bypass surgery alters behavioral and neural taste functions for sweet taste in obese rats. Am J Physiol Gastrointest Liver Physiol 299: G967-G979, 2010.
22. Halmi KA, Mason E, Falk JR, Stunkard A. Appetitive behavior after gastric bypass for obesity. Int J Obes 5: 457-464, 1981.
23. Hernandez-Mesa N, Mamedov Z, Bures J. Operant control of the pattern of licking in rats. Exp Brain Res 58: 117-124, 1985.
24. Kararil TT. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos 16: 351-380, 1995.
25. Kashyap SR, Bhatt DL, Schauer PR, STAMPEDE investigators. Bariatric surgery vs. advanced practice medical management in the treatment of type 2 diabetes mellitus: rationale and design of the Surgical Therapy And Medications Potentially Eradicate Diabetes Efficiently trial (STAMPEDE). Diabetes Obes Metab 12: 452-454, 2010.
26. Kenler HA, Brolin RE, Cody RP. Changes in eating behavior after horizontal gastroplasty and Roux-en-Y gastric bypass. Am J Clin Nutr 52: 87-92, 1990.
27. Kinzig KP, D'Alessio DA, Seeley RJ. The diverse roles of specific GLP-1 receptors in the control of food intake and the response to visceral illness. J Neurosci 22: 10470-10476, 2002.
28. Klein DA, Schebendach JE, Gershkovich M, Smith GP, Walsh BT. Modified sham feeding of sweet solutions in women with anorexia nervosa. Physiol Behav 101: 132-140, 2010.
29. Kruseman M, Leimgruber A, Zumbach F, Golay A. Dietary, weight, and psychological changes among patients with obesity, 8 years after gastric bypass. J Am Diet Assoc 110: 527-534, 2010.
30. le Roux CW, Aylwin SJ, Batterham RL, Borg CM, Coyle F, Prasad V, Shurey S, Ghatei MA, Patel AG, Bloom SR. Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg 243: 108-114, 2006.
31. le Roux CW, Borg C, Wallis K, Vincent RP, Bueter M, Goodlad R, Ghatei MA, Patel A, Bloom SR, Aylwin SJ. Gut hypertrophy after gastric bypass is associated with increased glucagon-like peptide 2 and intestinal crypt cell proliferation. Ann Surg 252: 50-56, 2010.
32. le Roux CW, Bueter M, Theis N, Werling M, Ashradian H, Lowenstein C, Athanasiou T, Bloom SR, Spector AC, Olbers T, Lutz TA. Gastric bypass reduces fat intake and preference. Am J Physiol Regul Integr Comp Physiol 301: R1057-R1066, 2011.
33. le Roux CW, Welbourn R, Werling M, Osborne A, Kokkinos A, Laurenius A, Lonroth H, Fandriks L, Ghatei MA, Bloom SR, Olbers T. Gut hormones as mediators of appetite and weight loss after roux-en-y gastric bypass. Ann Surg 246: 780-785, 2007.
34. Lydall ES, Gilmour G, Dwyer DM. Analysis of licking microstructure provides no evidence for a reduction in reward value following acute or sub-chronic phencyclidine administration. Psychopharmacology (Berl) 209: 153-162, 2010.
35. Mack CM, Moore CX, Jodka CM, Bhavsar S, Wilson JK, Hoyt JA, Roan JL, Vu C, Laugero KD, Parkes DG, Young AA. Antiobesity action of peripheral exenatide (exendin-4) in rodents: effects on food intake, body weight, metabolic status and side-effect measures. Int J Obes 30: 1332-1340, 2006.
36. Mamedov Z, Bures J. Sensory feedback modulates the central pacemaker of licking in rats. Neurosci Lett 45: 1-6, 1984.
37. Nowak A, Bojanowska E. Effects of peripheral or central GLP-1 receptor blockade on leptin-induced suppression of appetite. J Physiol Pharmacol 59: 501-510, 2008.
38. O'Brien PE. Bariatric surgery: mechanisms, indications and outcomes. J Gastroenterol Hepatol 25: 1358-1365, 2010.
39. Ochner CN, Gibson C, Carnell S, Dambkowski C, Geliebter A. The neurohormonal regulation of energy intake in relation to bariatric surgery for obesity. Physiol Behav 100: 549-559, 2010.
40. O'Connor EA, Carlin AM. Lack of correlation between variation in small-volume gastric pouch size and weight loss after laparoscopic rouxen-y gastric bypass. Surg Obes Relat Dis 4: 399-403, 2008.
41. Pouranaras DJ, le Roux CW. Obesity, gut hormones, and bariatric surgery. World J Surg 33: 1983-1988, 2009.
42. Roberts K, Duffy A, Kaufman J, Burrell M, Dziura J, Bell R. Size matters: gastric pouch size correlates with weight loss after laparoscopic roux-en-y gastric bypass. Surg Endosc 21: 1397-1402, 2007.
43. Ruttimann EB, Arnold M, Geary N, Langhans W. GLP-1 antagonism with exendin (9 -39) fails to increase spontaneous meal size in rats. Physiol Behav 100: 291-296, 2010.
44. Scruggs DM, Cowan GS, Klesges L, Defibaugh N, Walker R, Kuyper B, Hiler ML. Weight loss and caloric intake after regular and extended gastric bypass. Obes Surg 3: 233-238, 1993.
45. Seeley RJ, Blake K, Rushing PA, Benoit S, Eng J, Woods SC, D'Alessio D. The role of CNS glucagon-like peptide-1 (7-36) amide receptors in mediating the visceral illness effects of lithium chloride. J Neurosci 20: 1616-1621, 2000.
46. Shin AC, Zheng H, Pistell PJ, Berthoud HR. Roux-en-Y gastric bypass surgery changes food reward in rats. Int J Obes (Lond) 35: 642-651, 2010.
47. Shin Y, Martin B, Golden E, Doston C, Maudsley S, Kim W, Jang H, Mattson M, Drucker D, Egan J, Munger S. Modulation of taste sensitivity by GLP-1 signaling. J Neurochem 106: 455-463, 2008.
48. Sjostrom L, Lindroos AK, Peltonen M, Torgerson J, Bouchard C, Carlsson B, Dahlgren S, Larsson B, Narbro K, Sjostrom CD, Sullivan M, Wedel H, Swedish Obese Subjects Study Scientific Group. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med 351: 2683-2693, 2004.
49. Sjöström L, Narbro K, Sjöström CD, Karason K, Larsson B, Wedel H, Lystig T, Sullivan M, Bouchard C, Carlsson B, Bengtsson C, Dahlgren S, Gummesson A, Jacobson P, Karlsson J, Lindroos AK, Lönroth H, Näslund I, Olbers T, Stenlöf K, Torgerson J, Agren G, Carlsson LM; Swedish Obese Subjects Study. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med 357: 741-752, 2007.
50. Smith JC. The history of the "Davis Rig". Appetite 36: 93-98, 2001.
51. Spector AC. Psychophysical evaluation of taste function in nonhuman animals. In: Handbook of Olfaction and Gustation, edited by Doty RL. New York: Dekker, 2003, p. 861-879.
52. Spector AC, Grill HJ, Norgren R. Concentration-dependent licking of sucrose and sodium chloride in rats with parabrachial gustatory lesions. Physiol Behav 53: 277-283, 1993.
53. Spector AC, Redman R, Garcea M. The consequences of gustatory nerve transaction on taste-guided licking of sucrose and maltose in the rat. Behav Neurosci 100: 1096-1109, 1996.
54. Spector AC, Scalera G, Grill HJ, Norgren R. Gustatory detection thresholds after parabrachial nuclei lesions in rats. Behav Neurosci 109: 939-954, 1995.
55. Spector AC, Travers SP, Norgren R. Taste receptors on the anterior tongue and nasoincisor ducts of rats contribute synergistically to behavioral responses to sucrose. Behav Neurosci 107: 694-702, 1993.
56. Stanford JA, Vorontsova E, Surgener SP, Gerhardt GA, Fowler SC. Aged Fischer 344 rats exhibit altered orolingual motor function: relationships with nigrostriatal neurochemical measures. Neurobiol Aging 24: 259-266, 2003.
57. Stylopolous N, Hoppin AG, Kaplan LM. Roux-en-Y gastric bypass enhances energy expenditure and extends lifespan in diet-induced obese rats. Obesity (Silver Spring) 17: 1839-1847, 2009.
58. Sugerman HJ, Starkey JV, Birkenhauser R. A randomized prospective trial of gastric bypass versus vertical banded gastroplasty for morbid obesity and their effects on sweets versus non-sweets eaters. Ann Surg 205: 613-622, 1987.
59. Tadross JA, le Roux CW. The mechanisms of weight loss after bariatric surgery. Int J Obes 33: S28-S32, 2009.
60. Thaw AK, Smith JC. Conditioned suppression as a method of detecting taste thresholds in the rat. Chem Senses 17: 211-223, 1992.
61. Thiele TE, Van Dijk G, Campfield LA, Smith FJ, Burn P, Woods SC, Bernstein IL, Seeley RJ. Central infusions of GLP-1, but not leptin, produces conditioned taste aversion in rats. Am J Physiol Regul Integr Comp Physiol 272: R726-R730, 1997.
62. Tichansky DS, Glatt AR, Madan AK, Harper J, Tokita K, Boughter JD. Decrease in sweet taste in rats after gastric bypass surgery. Surg Endosc 25: 1176-1181, 2011.
63. Topart P, Becouarn G, Ritz P. Pouch size after gastric bypass does not correlate with weight loss outcome. Obes Surg 21: 1350-1354, 2011.
64. Travers JB, Dinardo LA, Karimnamazi H. Motor and premotor mechanics of licking. Neurosci Biobehav Rev 21: 631-647, 1997.
65. Treesukosol Y, Blonde GD, Spector AC. T1R2 and T1R3 subunits are individually unnecessary for normal affective licking responses to Polycose: implications for saccharide taste receptors in mice. Am J Physiol Regul Integr Comp Physiol 296: R855-R865, 2009.
66. Trostler N, Mann A, Zilberbush N, Avinoach E, Charuzi II. Weight loss and food intake 18 months following vertical banded gastroplasty or gastric bypass for severe obesity. Obes Surg 5: 39-51, 1995.
67. Vincent RP, Le Roux CW. Changes in gut hormones after bariatric surgery. Clin Endocrinol (Oxf) 69: 173-179, 2008.
68. Washington MC, Raboin SJ, Thompson W, Larsen CJ, Sayegh AI. Exenatide reduces food intake and activates the enteric nervous system of the gastrointestinal tract and the dorsal vagal complex of the hindbrain in the rat by a GLP-1 receptor. Brain Res 1344: 124-133, 2010.
69. Weijnen JAWM. The recording of licking behavior. In: Drinking Behavior, edited by Weijnen JAWM and Mendelson J. New York: Plenum, 1977, p. 93-114.
70. Weijnen JAWM. Licking behavior in the rat: measurement and situational control of licking frequency. Neurosci Biobehav Rev 22: 751-760, 1998.
71. Weisenfeld ZB, Halpern B, Tapper DN. Licking behavior: evidence of hypoglossal oscillator. Science 196: 1122-1124, 1977.
72. Williams DL, Baskin DG, Schwartz MW. Leptin regulation of the anorexic response to glucagon-like peptide-1 receptor stimulation. Diabetes 55: 3387-3393, 2006.
73. Williams DL, Baskin DG, Schwartz MW. Evidence that intestinal glucagon-like peptide-1 plays a physiological role in satiety. Endocrinology 150: 1680-1687, 2009.
74. Williams DL, Hyvarinen N, Lilly N, Kay K, Dossat A, Parise E, Torregrossa AM. Maintenance on a high-fat diet impairs the anorexic response to glucagon-like-peptide-1 receptor activation. Physiol Behav 103: 557-564, 2011.
75. Yoon NM, Cavaghan MK, Brunelle RL, Roach P. Exenatide added to insulin therapy: a retrospective review of clinical practice over two years in an academic endocrinology outpatient setting. Clin Ther 31: 1511-1523, 2009.