Fructose-induced leptin resistance: Discovery of an unsuspected form of the phenomenon and its significance. Focus on "Fructose-induced leptin resistance exacerbates weight gain in response to subsequent high-fat feeding," by Shapiro et al.

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 295, Issue 5, 2008, Pages

  Vasselli, Joseph R ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b ST LUKE S ROOSEVELT HOSPITAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRUCTOSE; LEPTIN;

APPETITE; BODY FAT; BODY MASS; BODY WEIGHT; CEREBROSPINAL FLUID; DISEASE EXACERBATION; DNA POLYMORPHISM; EDITORIAL; FOOD INTAKE; HORMONE RESISTANCE; HUMAN; LEPTIN RESISTANCE; LIPID DIET; NONHUMAN; OBESITY; PRIORITY JOURNAL; WEIGHT GAIN;

ANIMALS; BLOTTING, WESTERN; DIETARY FATS; DRUG SYNERGISM; FRUCTOSE; LEPTIN; MALE; RATS; RATS, SPRAGUE-DAWLEY; SWEETENING AGENTS; TRIGLYCERIDES; WEIGHT GAIN;

EID: 57349098608     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90674.2008     Document Type: Editorial

References (74)

1. Ackroff K, Sclafani A. Sucrose-induced hyperphagia and obesity in rats fed a macronutrient self-selection diet. Physiol Behav 44: 181-187, 1988.
2. Akhavan T, Anderson GH. Effects of glucose-to-fructose ratios in solutions on subjective satiety, food intake, and satiety hormones in young men. Am J Clin Nutr 86: 1354-1363, 2007.
3. Arch JR. Central regulation of energy balance: inputs, outputs and leptin resistance. Proc Nutr Soc 64: 39-46, 2005.
4. Arch JRS, Stock MJ, Trayhurn P. Leptin resistance in obese humans: does it exist and what does it mean? Int J Obes 22: 1159-1163, 1998.
5. Banks WA. The many lives of leptin. Peptides 25: 331-338, 2004.
6. Banks WA, Coon AB, Robinson SM, Moinuddin A, Shultz JM, Nakaoke R, Morley JE. Triglycerides induce leptin resistance at the blood-brain barrier. Diabetes 53: 1253-1260, 2004.
7. Banks WA, DiPalma CR, Farrell CL. Impaired transport of leptin across the blood-brain barrier in obesity. Peptides 20: 1341-1345, 1999.
8. Basciano H, Federico L, Adeli K. Fructose, insulin resistance, and metabolic dyslipidemia (NOT AN ABSTRACT). Nutr Metab (Lond) 2: 5-29, 2005.
9. Bjørbæk C, Elmquist JK, Frantz JD, Shoelson SE, Flier JS. Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol Cell 1: 619-625, 1998.
10. Bowen H, Mitchell TD, Harris RB. Method of leptin dosing, strain, and group housing influence leptin sensitivity in high-fat-fed weanling mice. Am J Physiol Regul Integr Comp Physiol 284: R87-R100, 2003.
11. Bray GA, Nielsen SJ, Popkin BM. Consumption of high-fructose corn syrup in beverages may play a role in the epidemic of obesity. Am J Clin Nutr 79: 537-543, 2004.
12. Burguera B, Couce ME, Curran GL, Jensen MD, Lloyd R, Cleary MP, Poduslo JF. Obesity is associated with a decreased leptin transport across the blood-brain barrier in rats. Diabetes 49: 1219-1223, 2000.
13. Campfield LA, Smith FJ, Guisez Y, Devos R, Burn P. Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 269: 546-549, 1995.
14. Caro JF, Kolaczynski JW, Nyce MR, Ohannesian JP, Opentanova I, Goldman WH, Lynn RB, Zhang PL, Sinha MK, Considine RV. Decreased cerebrospinal-fluid/serum leptin ratio in obesity: a possible mechanism for leptin resistance. Lancet 348: 159-161, 1996.
15. Chagnon YC, Wilmore JH, Borecki IB, Gagnon J, Pérusse L, Gagnon M, Collier GR, Leon AS, Skinner JS, Rao DC, Bouchard C. Associations between the leptin receptor gene and adiposity in middle-aged Caucasian males from the HERITAGE family study. J Clin Endocrinol Metab 85: 29-34, 2000.
16. Chessler SD, Fujimoto WY, Shofer JB, Boyko EJ, Weigle DS. Increased plasma leptin levels are associated with fat accumulation in Japanese Americans. Diabetes 47: 239-243, 1998.
17. 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.
18. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL Caro JF. Serum immunoreactive-leptin concentrations in normal weight and obese animals. N Engl J Med 334: 292-295, 1996.
19. D'Angelo G, Elmarakby AA, Pollock DM, Stepp DW. Fructose feeding increases insulin resistance but not blood pressure in Sprague-Dawley rats. Hypertension 46: 806-811, 2005.
20. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol Endocrinol Metab 291: E1141-E1143, 2006.
21. de Krom M, van der Schouw YT, Hendriks J, Ophoff RA, van Gils CH, Stolk RP, Grobbee DE, Adan R. Common genetic variations in CCK, leptin, and leptin receptor genes are associated with specific human eating patterns. Diabetes 56: 276-280, 2007.
22. De Souza CT, Araujo EP, Bordin S, Ashimine R, Zollner RL, Boschero AC, Saad MJ, Velloso LA. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 146: 4192-4199, 2005.
23. El-Haschimi K, Pierroz DD, Hileman SM, Bjørbæk C, Flier JS. Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J Clin Invest 105: 1827-1832, 2000.
24. Frederich RC, Hamann A, Anderson S, Löllmann B, Lowell BB, Flier JS. Leptin levels reflect body lipid content in mice: Evidence for diet-induced resistance to leptin action. Nat Med 1: 1311-1314, 1995.
25. Halaas JL, Boozer C, Blair-West J, Fidahusein N, Denton DA, Friedman JM. Physiological response to long-term peripheral and central leptin infusion in lean and obese mice. Proc Natl Acad Sci USA 94: 8878-8883, 1997.
26. Hampton AG Jr, Hunt WB Jr, Mulholland HB. Insulin resistance. JAMA 161: 788-793, 1956.
27. Havel PJ. Dietary fructose: implications for dysregulation of energy homeostasis and lipid/carbohydrate metabolism. Nutr Rev 63: 133-157, 2005.
28. Heymsfield SB, Greenberg AS, Fujioka K, Dixon RM, Kushner R, Hunt T, Lubina JA, Patane J, Self B, Hunt P, McCamish M. Recombinant leptin for weight loss in obese and lean adults: a randomized, controlled, dose-escalation trial. JAMA 282: 1568-1575, 1999.
29. Howard JK, Flier JS. Attenuation of leptin and insulin signaling by SOCS proteins. Trends Endocrinol Metab 17: 365-371, 2006.
30. Huang XF, Xin X, McLennan P, Storlien L. Role of fat amount and type in ameliorating diet-induced obesity: insights at the level of hypothalamic arcuate nucleus leptin receptor, neuropeptide Y and pro-opiomelanocortin mRNA expression. Diabetes Obes Metab 6: 35-44, 2004.
31. Hukshorn CJ, Saris WH, Westerterp-Plantenga MS, Farid AR, Smith FJ, Campfield LA. Weekly subcutaneous pegylated recombinant native human leptin (PEG-OB) administration in obese men. J Clin Endocrinol Metab 85: 4003-4009, 2000.
32. Irani BG, Dunn-Meynell AA, Levin BE. Altered hypothalamic leptin, insulin, and melanocortin binding associated with moderate-fat diet and predisposition to obesity. Endocrinology 148: 310-316, 2007.
33. Johnson RJ, Segal MS, Sautin Y, Nakagawa T, Feig DI, Kang DH, Gersch MS, Benner S, Sánchez-Lozada LG. Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. Am J Clin Nutr 86: 899-906, 2007.
34. Jürgens H, Haass W, Castañeda TR, Schürmann A, Koebnick C, Dombrowski F, Otto B, Nawrocki AR, Scherer PE, Spranger J, Ristow M, Joost HG, Havel PJ, Tschöp MH. Consuming fructose-sweetened beverages increases adiposity in mice. Obes Res 13: 1146-1156, 2005.
35. Kanarek RB, Aprille JR, Hirsch E, Gualtiere L, Brown CA. Sucrose-induced obesity: effect of diet on obesity and brown adipose tissue. Am J Physiol Regul Integr Comp Physiol 253: R158-R166, 1987.
36. Kennedy A, Gettys TW, Watson P, Wallace P, Ganaway E, Pan Q, Garvey WT. The metabolic significance of leptin in humans: gender-based differences in relationship to adiposity, insulin sensitivity, and energy expenditure. J Clin Endocrinol Metab 82: 1293-1300, 1997.
37. Lin L, Martin R, Schaffhauser AO, York DA. Acute changes in the response to peripheral leptin with alteration in diet composition. Am J Physiol Regul Integr Comp Physiol 280: R504-R509, 2001.
38. Lin S, Storlien LH, Huang XF. Leptin receptor, NPY, POMC mRNA expression in the diet-induced obese mouse brain. Brain Res 875: 89-95, 2000.
39. Lin S, Thomas TC, Storlien LH, Huang XF. Development of high fat diet-induced obesity and leptin resistance in C57Bl/6J mice. Int J Obes 24: 639-646, 2000.
40. Liu ZJ, Bian J, Liu J, Endoh A. Obesity reduced the gene expressions of leptin receptors in hypothalamus and liver. Horm Metab Res 39: 489-494, 2007.
41. Liuzzi A, Savia G, Tagliaferri M, Lucantoni R, Berselli ME, Petroni ML, De Medici C, Viberti GC. Serum leptin concentration in moderate and severe obesity: relationship with clinical anthropometric and metabolic factors. Int J Obes Relat Metab Disord 23: 1066-1073, 1999.
42. Madiehe AM, Schaffhauser AO, Braymer DH, Bray GA, York DA. Differential expression of leptin receptor in high- and low-fat-fed Osborne-Mendel and S5B/P1 rats. Obes Res 8: 467-474, 2000.
43. Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y, Fei H, Kim S, Lallone R, Ranganathan S, Kern PA, Friedman JM. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1: 1155-1161, 1995.
44. Mantzoros CS, Flier JS. Leptin as a therapeutic agent-trials and tribulations. J Clin Endocrinol Metab 85: 4000-4002, 2000.
45. Morrison CD. Leptin resistance and the response to positive energy balance. Physiol Behav 94: 660-663, 2008.
46. Nakagawa T, Hu H, Zharikov S, Tuttle KR, Short RA, Glushakova O, Ouyang X, Feig DI, Block ER, Herrera-Acosta J, Patel JM, Johnson RJ. A causal role for uric acid in fructose-induced metabolic syndrome. Am J Physiol Renal Physiol 290: F625-F631, 2006.
47. Oldendorf WH. Brain uptake of radiolabeled amino acids, amines, and hexoses after arterial injection. Am J Physiol 221: 1629-1639, 1971.
48. Olsen NS, Nuetzel JA. Resistance to small doses of insulin in various clinical conditions. J Clin Invest 29: 862-866, 1950.
49. Pacini G, Finegood DT, Bergman RN. A minimal-model-based glucose clamp yielding insulin sensitivity independent of glycemia. Diabetes 31: 432-441, 1982.
50. Park CR, Johnson LH, Wright JH Jr, Batsel H. Effect of insulin on transport of several hexoses and pentoses into cells of muscle and brain. Am J Physiol 191: 13-18, 1957.
51. Parks EJ, Parks EJ. Changes in fat synthesis influenced by dietary macronutrient content. Proc Nutr Soc 61: 281-286, 2002.
52. Robertson SA, Leinninger GM, Myers MG Jr. Molecular and neural mediators of leptin actin. Physiol Behav 94: 637-642, 2008.
53. Rodin J. Comparative effects of fructose, aspartame, glucose, and water preloads on calorie and macronutrient intake. Am J Clin Nutr 51: 428-435, 1990.
54. Rodin J, Reed D, Jamner J. Metabolic effects of fructose and glucose: implications for food intake. Am J Clin Nutr 47: 683-689, 1988.
55. Roglans N, Vilà L, Farré M, Alegret M, Sánchez RM, Vázquez-Carrera M, Laguna JC. Impairment of hepatic Stat-3 activation and reduction of PPAR-α activity in fructose-fed rats. Hepatology 45: 778-788, 2007.
56. Rosenbaum M, Leibel RL. The role of leptin in human physiology. N Engl J Med 341: 913-915, 1999.
57. Rosenbaum M, Sy M, Pavlovich K, Leibel RL, Hirsch J. Leptin reverses weight loss-induced changes in regional neural activity responses to visual food stimuli. J Clin Invest 118: 2583-2591, 2008.
58. Scarpace PJ, Matheny M, Zhang Y, Shek EW, Prima V, Zolotukhin S, Tümer N. Leptin-induced leptin resistance reveals separate roles for the anorexic and thermogenic responses in weight maintenance. Endocrinology 143: 3026-3035, 2002.
59. Scarpace PJ, Zhang Y. Elevated leptin: consequence or cause of obesity? Front Biosci 12: 3531-3544, 2007.
60. Shapiro A, Mu W, Roncal C, Cheng KY, Johnson RJ, Scarpace PJ. Fructose-induced leptin resistance exacerbates weight gain in response to subsequent high fat feeding. Am J Physiol Regul Integr Comp Physiol (August 13, 2008). doi:10.1152/ajpregu.00195.2008.
61. Schwartz M, Peskind E, Raskind M, Boyko BJ, Porte D Jr. Cerebrospinal fluid leptin levels: relationship to plasma levels and to adiposity in humans. Nat Med 2: 589-593, 1996.
62. Soenen S, Westerterp-Plantenga MS. No differences in satiety or energy intake after high-fructose corn syrup, sucrose, or milk preloads. Am J Clin Nutr 86: 1586-1594, 2007.
63. Stanhope KL, Griffen SC, Bair BR, Swarbrick MM, Keim NL, Havel PJ. Twenty-four-hour endocrine and metabolic profiles following consumption of high-fructose syrup, sucrose, fructose, and glucose-sweetened beverages with meals. Am J Clin Nutr 87: 1194-1203, 2008.
64. Steinberg GR, Parolin ML, Heigenhauser GJF, Pyck DJ. Leptin increases FA oxidation in lean but not obese human skeletal muscle: evidence of peripheral leptin resistance. Am J Physiol Endocrinol Metab 283: E187-E192, 2002.
65. Teff KL, Elliott SS, Tschöp M, Kieffer TJ, Rader D, Heiman M, Townsend RR, Keim NL, D'Alessio D, Havel PJ. Dietary fructose reduces circulating insulin and leptin, attenuates postprandial suppression of ghrelin, and increases triglycerides in women. J Clin Endocrinol Metab 89: 2963-2972, 2004.
66. Uotani S, Bjørbæk C, Tornøe J, Flier JS. Functional properties of leptin receptor isoforms: internalization and degradation of leptin and ligand-induced receptor downregulation. Diabetes 48: 279-286, 1999.
67. Urayama A, Banks WA. Starvation and triglycerides reverse the obesity-induced impairment of insulin transport at the blood-brain barrier. Endocrinology 149: 3592-3597, 2008.
68. Van Heek M, Compton DS, France CF, Tedesco RP, Fawzi AB, Graziano MP, Sybertz EJ, Strader CD, Davis HR Jr. Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J Clin Invest 99: 385-390, 1997.
69. Van Rossum CT, Hoebee B, Van Baak MA, Mars M, Saris WH, Seidell JC. Genetic variation in the leptin receptor gene, leptin, and weight gain in young Dutch adults. Obes Res 11: 377-386, 2003.
70. Vasselli JR. Behavioral and biological determinants of leptin resistance. Appetite 37: 115-117, 2001.
71. Wang J, Obici S, Morgan K, Barzilai N, Feng Z, Rossetti L. Over-feeding rapidly induces leptin and insulin resistance. Diabetes 50: 2786-2791, 2001.
72. Widdowson PS, Upton R, Buckingham R, Arch J, Williams G. Inhibition of food response to intracerebroventricular injection of leptin is attenuated in rats with diet-induced obesity. Diabetes 46: 1782-1785, 1997.
73. Wu-Peng XS, Chua SC Jr, Okada N, Liu SM, Nicolson M, Leibel RL. Phenotype of the obese Koletsky (f) rat due To Tyr763Stop mutation in the extracellular domain of the leptin receptor (LepR): evidence for deficient plasma-to-CSF transport of leptin in both the Zucker and Koletsky obese rat. Diabetes 46: 513-518, 1997.
74. Zabolotny JM, Bence-Hanulec KK, Stricker-Krongrad A, Haj F, Wang Y, Minokoshi Y, Kim YB, Elmquist JK, Tartaglia LA, Kahn BB, Neel BG. PTP1B regulates leptin signal transduction in vivo. Dev Cell 2: 489-495, 2002.