High-fat diets induce a rapid loss of the insulin anorectic response in the amygdala

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 5, 2009, Pages

  Boghossian, Stéphane ^a   Lemmon, Karalee ^a   Park, MieJung ^a   York, David A ^a  

^a UTAH STATE UNIVERSITY   (United States)

Author keywords

Central insulin sensitivity; Food intake; Limbic system; Rat

Indexed keywords

INSULIN; INSULIN RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOREXIA; ARCUATE NUCLEUS; ARTICLE; BRAIN MAPPING; BRAIN REGION; CONTROLLED STUDY; FOOD INTAKE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANCE; INSULIN RESPONSE; INSULIN TOLERANCE TEST; LIPID DIET; MALE; NERVE CELL NETWORK; NONHUMAN; OBESITY; ONCOGENE C FOS; PRIORITY JOURNAL; RAT; REFEEDING; REGULATORY MECHANISM; SPRAGUE DAWLEY RAT; THALAMUS MIDLINE NUCLEUS;

AMYGDALA; ANIMALS; ANOREXIA; BLOOD GLUCOSE; DIET, FAT-RESTRICTED; DIETARY FATS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EATING; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; MALE; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 70449644663     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00252.2009     Document Type: Article

References (58)

1. Al-Amin ZM, Thomson M, Al-Qattan KK, Peltonen-Shalaby R, Ali M. Anti-diabetic and hypolipidaemic properties of ginger (Zingiber officinale) in streptozotocin-induced diabetic rats. Br J Nutr 96: 660-666, 2006. (Pubitemid 46470189)
2. Arase K, Fisler JS, Shargill NS, York DA, Bray GA. Intracerebroventricular infusions of 3-OHB and insulin in a rat model of dietary obesity. Am J Physiol Regul Integr Comp Physiol 255: R974-R981, 1988.
3. Balthasar N. Genetic dissection of neuronal pathways controlling energy homeostasis. Obesity 14 Suppl 5: 222S-227S, 2006.
4. Balthasar N, Dalgaard LT, Lee CE, Yu J, Funahashi H, Williams T, Ferreira M, Tang V, McGovern RA, Kenny CD, Christiansen LM, Edelstein E, Choi B, Boss O, Aschkenasi C, Zhang CY, Mountjoy K, Kishi T, Elmquist JK, Lowell BB. Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123: 493-505, 2005. (Pubitemid 41546678)
5. Barnard RJ, Roberts CK, Varon SM, Berger JJ. Diet-induced insulin resistance precedes other aspects of the metabolic syndrome. J Appl Physiol 84: 1311-1315, 1998. (Pubitemid 28158697)
6. Baskin DG, Figlewicz DP, Woods SC, Porte D Jr, Dorsa DM. Insulin in the brain. Annu Rev Physiol 49: 335-347, 1987.
7. Benoit SC, Clegg DJ, Seeley RJ, Woods SC. Insulin and leptin as adiposity signals. Recent Prog Horm Res 59: 267-285, 2004.
8. Berthoud HR. An overview of neural pathways and networks involved in the control of food intake and selection. In: Neural and Metabolic Control of Macronutrient Intake, edited by Berthoud H-R and Seeley RJ. Boca Raton, FL: CRC, 2000, p. 361-387.
9. Berthoud HR. Multiple neural systems controlling food intake and body weight. Neurosci Biobehav Rev 26: 393-428, 2002. (Pubitemid 36158660)
10. Bloomgarden ZT. Insulin resistance concepts. Diabetes Care 30: 1320-1326, 2007.
11. Bray GA. Afferent signals regulating food intake. Proc Nutr Soc 59: 373-384, 2000.
12. Bruning JC, Gautam D, Burks DJ, Gillette J, Schubert M, Orban PC, Klein R, Krone W, Muller-Wieland D, Kahn CR. Role of brain insulin receptor in control of body weight and reproduction. Science 289: 2122-2125, 2000.
13. Clegg DJ, Benoit SC, Air EL, Jackman A, Tso P, D'Alessio D, Woods SC, Seeley RJ. Increased dietary fat attenuates the anorexic effects of intracerebroventricular injections of MTII. Endocrinology 144: 2941-2946, 2003.
14. Clegg DJ, Benoit SC, Reed JA, Woods SC, Dunn-Meynell A, Levin BE. Reduced anorexic effects of insulin in obesity-prone rats fed a moderate-fat diet. Am J Physiol Regul Integr Comp Physiol 288: R981-R986, 2005.
15. Figlewicz DP, Bennett JL, Aliakbari S, Zavosh A, Sipols AJ. Insulin acts at different CNS sites to decrease acute sucrose intake and sucrose self-administration in rats. Am J Physiol Regul Integr Comp Physiol 295: R388-R394, 2008.
16. Figlewicz DP, Bennett JL, Naleid AM, Davis C, Grimm JW. Intraventricular insulin and leptin decrease sucrose self-administration in rats. Physiol Behav 89: 611-616, 2006. (Pubitemid 44634584)
17. Figlewicz DP, Naleid AM, Sipols AJ. Modulation of food reward by adiposity signals. Physiol Behav 91: 473-478, 2007.
18. Glass MJ, Billington CJ, Levine AS. Naltrexone administered to central nucleus of amygdala or PVN: neural dissociation of diet and energy. Am J Physiol Regul Integr Comp Physiol 279: R86-R92, 2000.
19. Glass MJ, Billington CJ, Levine AS. Opioids and food intake: distributed functional neural pathways? Neuropeptides 33: 360-368, 1999.
20. Goodyear LJ, Kahn BB. Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 49: 235-261, 1998. (Pubitemid 28197452)
21. Havrankova J, Schmechel D, Roth J, Brownstein M. Identification of insulin in rat brain. Proc Natl Acad Sci USA 75: 5737-5741, 1978.
22. Hill JO, Lin D, Yakubu F, Peters JC. Development of dietary obesity in rats: influence of amount and composition of dietary fat. Int J Obes Relat Metab Disord 16: 321-333, 1992.
23. Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest 106: 473-481, 2000.
24. Kaiyala KJ, Prigeon RL, Kahn SE, Woods SC, Schwartz MW. Obesity induced by a high-fat diet is associated with reduced brain insulin transport in dogs. Diabetes 49: 1525-1533, 2000.
25. Kalra SP, Dube MG, Pu S, Xu B, Horvath TL, Kalra PS. Interacting appetite-regulating pathways in the hypothalamic regulation of body weight. Endocr Rev 20: 68-100, 1999. (Pubitemid 29092036)
26. Kelley AE. Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27: 765-776, 2004.
27. Kim EM, Quinn JG, Levine AS, O'Hare E. A bi-directional mu-opioidopioid connection between the nucleus of the accumbens shell and the central nucleus of the amygdala in the rat. Brain Res 1029: 135-139, 2004. (Pubitemid 39467744)
28. Kim JY, Nolte LA, Hansen PA, Han DH, Ferguson K, Thompson PA, Holloszy JO. High-fat diet-induced muscle insulin resistance: relationship to visceral fat mass. Am J Physiol Regul Integr Comp Physiol 279: R2057-R2065, 2000.
29. King BM, Rossiter KN, Stines SG, Zaharan GM, Cook JT, Humphries MD, York DA. Amygdaloid-lesion hyperphagia: impaired response to caloric challenges and altered macronutrient selection. Am J Physiol Regul Integr Comp Physiol 275: R485-R493, 1998. (Pubitemid 128734463)
30. Koch L, Wunderlich FT, Seibler J, Konner AC, Hampel B, Irlenbusch S, Brabant G, Kahn CR, Schwenk F, Bruning JC. Central insulin action regulates peripheral glucose and fat metabolism in mice. J Clin Invest 118: 2132-2147, 2008. (Pubitemid 351872332)
31. Kraegen EW, Clark PW, Jenkins AB, Daley EA, Chisholm DJ, Storlien LH. Development of muscle insulin resistance after liver insulin resistance in high-fat-fed rats. Diabetes 40: 1397-1403, 1991.
32. Leibowitz SF. Macronutrients and brain peptides: What they do and how they respond. In: Neural and Metabolic Control of Macronutrient Intake, edited by Berthoud H-R Seeley RJ. Boca Raton, FL: CRC Press, 2000, p. 389-406.
33. Levin BE, Dunn-Meynell AA, Banks WA. Obesity-prone rats have normal blood-brain barrier transport but defective central leptin signaling before obesity onset. Am J Physiol Regul Integr Comp Physiol 286: R143-R150, 2004.
34. Lin L, Park M, York DA. Enterostatin inhibition of dietary fat intake is modulated through the melanocortin system. Peptides 28: 643-649, 2007. (Pubitemid 46204988)
35. Lin L, York DA. Amygdala enterostatin induces c-Fos expression in regions of hypothalamus that innervate the PVN. Brain Res 1020: 147-153, 2004. (Pubitemid 39092980)
36. Lin L, York DA. Enterostatin actions in the amygdala and PVN to suppress feeding in the rat. Peptides 18: 1341-1347, 1997. (Pubitemid 27519744)
37. Manin M, Balage M, Larue-Achagiotis C, Grizard J. Chronic intracerebroventricular infusion of insulin failed to alter brain insulin-binding sites, food intake, and body weight. J Neurochem 51: 1689-1695, 1988. (Pubitemid 19010953)
38. Naleid AM, Grace MK, Chimukangara M, Billington CJ, Levine AS. 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 293: R99-R105, 2007.
39. Nishijo H, Ono T, Uwano T, Kondoh T, Torii K. Hypothalamic and amygdalar neuronal responses to various tastant solutions during ingestive behavior in rats. J Nutr 130: 954S-959S, 2000.
40. Niswender KD, Morrison CD, Clegg DJ, Olson R, Baskin DG, Myers MG Jr, Seeley RJ, Schwartz MW. Insulin activation of phosphatidylinositol 3-kinase in the hypothalamic arcuate nucleus: a key mediator of insulin-induced anorexia. Diabetes 52: 227-231, 2003.
41. Ono H, Pocai A, Wang Y, Sakoda H, Asano T, Backer JM, Schwartz GJ, Rossetti L. Activation of hypothalamic S6 kinase mediates diet-induced hepatic insulin resistance in rats. J Clin Invest 118: 2959-2968, 2008.
42. Ono T, Steffens AB, Sasaki K. Influence of peripheral and intracerebroventricular glucose and insulin infusions on peripheral and cerebrospinal fluid glucose and insulin levels. Physiol Behav 30: 301-306, 1983. (Pubitemid 13140047)
43. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH, Hotamisligil GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461, 2004. (Pubitemid 39372439)
44. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. Sydney, Australia: Academic, 1982.
45. Pincock S. Paul Zimmet: fighting the "diabesity" pandemic. Lancet 368: 1643, 2006.
46. Posey KA, Clegg DJ, Printz RL, Byun J, Morton GJ, Vivekanandan- Giri A, Pennathur S, Baskin DG, Heinecke JW, Woods SC, Schwartz MW, Niswender KD. Hypothalamic proinflammatory lipid accumulation, inflammation, and insulin resistance in rats fed a high-fat diet. Am J Physiol Endocrinol Metab 296: E1003-E1012, 2009.
47. Primeaux SD, Wilson SP, Bray GA, York DA, Wilson MA. Overexpression of neuropeptide Y in the central nucleus of the amygdala decreases ethanol self-administration in "anxious" rats. Alcohol Clin Exp Res 30: 791-801, 2006.
48. Primeaux SD, York DA, Bray GA. Neuropeptide Y administration into the amygdala alters high fat food intake. Peptides 27: 1644-1651, 2006.
49. Qatanani M, Lazar MA. Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev 21: 1443-1455, 2007.
50. Ropelle ER, Pauli JR, Prada PO, de Souza CT, Picardi PK, Faria MC, Cintra DE, Fernandes MF, Flores MB, Velloso LA, Saad MJ, Carvalheira JB. Reversal of diet-induced insulin resistance with a single bout of exercise in the rat: the role of PTP1B and IRS-1 serine phosphorylation. J Physiol 577: 997-1007, 2006.
51. Samuel VT, Liu ZX, Qu X, Elder BD, Bilz S, Befroy D, Romanelli AJ, Shulman GI. Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J Biol Chem 279: 32345-32353, 2004.
52. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 404: 661-671, 2000. (Pubitemid 30205071)
53. St. Andre J, Reilly S. Effects of central and basolateral amygdala lesions on conditioned taste aversion and latent inhibition. Behav Neurosci 121: 90-99, 2007. (Pubitemid 46328627)
54. Werther GA, Hogg A, Oldfield BJ, McKinley MJ, Figdor R, Allen AM, Mendelsohn FA. Localization and characterization of insulin receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry. Endocrinology 121: 1562-1570, 1987. (Pubitemid 17155909)
55. Will MJ, Franzblau EB, Kelley AE. The amygdala is critical for opioid-mediated binge eating of fat. Neuroreport 15: 1857-1860, 2004.
56. Yamamoto T. Brain regions responsible for the expression of conditioned taste aversion in rats. Chem Senses 32: 105-109, 2007. (Pubitemid 46017880)
57. Yamano Y, Yoshioka M, Toda Y, Oshida Y, Chaki S, Hamamoto K, Morishima I. Regulation of CRF, POMC and MC4R gene expression after electrical foot shock stress in the rat amygdala and hypothalamus. J Vet Med Sci 66: 1323-1327, 2004. (Pubitemid 41365446)
58. Zierath JR. Exercise training-induced changes in insulin signaling in skeletal muscle. J Appl Physiol 93: 773-781, 2002. (Pubitemid 34810245)