Cooperative interaction between leptin and amylin signaling in the ventral tegmental area for the control of food intake

American Journal of Physiology - Endocrinology and Metabolism

Volumn 308, Issue 12, 2015, Pages E1116-E1122

  Mietlicki Baase, Elizabeth G ^a   Olivos, Diana R ^a   Jeffrey, Brianne A ^a   Hayes, Matthew R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Islet amyloid polypeptide; Mesolimbic; Obesity; Reward

Indexed keywords

AMYLIN; AMYLIN RECEPTOR; CALCITONIN[8-32][30 ASPARAGINE 32 TYROSINAMIDE]; LEPTIN; RECOMBINANT AMYLIN; RECOMBINANT LEPTIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; BODY WEIGHT; CONTROLLED STUDY; ENERGY BALANCE; FEEDING; FOOD INTAKE; HYPOPHAGIA; MALE; MEDIATOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; VENTRAL TEGMENTUM; WEIGHT GAIN; WEIGHT REDUCTION; ANIMAL; DRUG EFFECTS; ENERGY METABOLISM; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; APPETITE REGULATION; BODY WEIGHT; ENERGY METABOLISM; ISLET AMYLOID POLYPEPTIDE; LEPTIN; MALE; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; VENTRAL TEGMENTAL AREA; WEIGHT LOSS;

EID: 84931081506     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00087.2015     Document Type: Article

References (60)

1. Banks WA, DiPalma CR, Farrell CL. Impaired transport of leptin across the blood-brain barrier in obesity. Peptides 20: 1341–1345, 1999.
2. Banks WA, Kastin AJ. Differential permeability of the blood-brain barrier to two pancreatic peptides: insulin and amylin. Peptides 19: 883–889, 1998.
3. Banks WA, Kastin AJ, Huang W, Jaspan JB, Maness LM. Leptin enters the brain by a saturable system independent of insulin. Peptides 17: 305–311, 1996.
4. Banks WA, Kastin AJ, Maness LM, Huang W, Jaspan JB. Permeability of the blood-brain barrier to amylin. Life Sci 57: 1993–2001, 1995.
5. Bell-Anderson KS, Bryson JM. Leptin as a potential treatment for obesity: progress to date. Treat Endocrinol 3: 11–18, 2004.
6. Bello NT, Kemm MH, Ofeldt EM, Moran TH. Dose combinations of exendin-4 and salmon calcitonin produce additive and synergistic reductions in food intake in nonhuman primates. Am J Physiol Regul Integr Comp Physiol 299: R945–R952, 2010.
7. Boyle CN, Rossier MM, Lutz TA. Influence of high-fat feeding, diet-induced obesity, and hyperamylinemia on the sensitivity to acute amylin. Physiol Behav 104: 20–28, 2011.
8. Bray GA. Medical treatment of obesity: the past, the present and the future. Best Pract Res Clin Gastroenterol 28: 665–684, 2014.
9. Chan JL, Roth JD, Weyer C. It takes two to tango: combined amylin/ leptin agonism as a potential approach to obesity drug development. J Investig Med 57: 777–783, 2009.
10. Clapper JR, Athanacio J, Wittmer C, Griffin PS, D’Souza L, Parkes DG, Roth JD. Effects of amylin and bupropion/naltrexone on food intake and body weight are interactive in rodent models. Eur J Pharmacol 698: 292–298, 2013.
11. Dee A, Kearns K, O’Neill C, Sharp L, Staines A, O’Dwyer V, Fitzgerald S, Perry IJ. The direct and indirect costs of both overweight and obesity: a systematic review. BMC Res Notes 7: 242, 2014.
12. Dunican KC, Adams NM, Desilets AR. The role of pramlintide for weight loss. Ann Pharmacother 44: 538–545, 2010.
13. Eiden S, Daniel C, Steinbrueck A, Schmidt I, Simon E. Salmon calcitonin - a potent inhibitor of food intake in states of impaired leptin signalling in laboratory rodents. J Physiol 541: 1041–1048, 2002.
14. Fulton S, Pissios P, Manchon RP, Stiles L, Frank L, Pothos EN, Maratos-Flier E, Flier JS. Leptin regulation of the mesoaccumbens dopamine pathway. Neuron 51: 811–822, 2006.
15. Grabler V, Lutz TA. Chronic infusion of the amylin antagonist AC 187 increases feeding in Zucker fa/fa rats but not in lean controls. Physiol Behav 81: 481–488, 2004.
16. Grill HJ. Leptin and the systems neuroscience of meal size control. Front Neuroendocrinol 31: 61–78, 2010.
17. Hommel JD, Trinko R, Sears RM, Georgescu D, Liu ZW, Gao XB, Thurmon JJ, Marinelli M, DiLeone RJ. Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51: 801–810, 2006.
18. Kanoski SE, Zhao S, Guarnieri DJ, DiLeone RJ, Yan J, De Jonghe BC, Bence KK, Hayes MR, Grill HJ. Endogenous leptin receptor signaling in the medial nucleus tractus solitarius affects meal size and potentiates intestinal satiation signals. Am J Physiol Endocrinol Metab 303: E496–E503, 2012.
19. Karl JP, Roberts SB. Energy density, energy intake, and body weight regulation in adults. Adv Nutr 5: 835–850, 2014.
20. Le Foll C, Johnson MD, Dunn-Meynell A, Boyle CN, Lutz TA, Levin BE. Amylin-induced central IL-6 production enhances ventromedial hy-pothalamic leptin signaling. Diabetes 64: 1621–1631, 2015.
21. Leshan RL, Opland DM, Louis GW, Leinninger GM, Patterson CM, Rhodes CJ, Munzberg H, Myers MG. Ventral tegmental area leptin receptor neurons specifically project to and regulate cocaine- and amphetamine-regulated transcript neurons of the extended central amygdala. J Neurosci 30: 5713–5723, 2010.
22. Lutz TA. The interaction of amylin with other hormones in the control of eating. Diabetes Obes Metab 15: 99–111, 2013.
23. Lutz TA. Roles of amylin in satiation, adiposity and brain development. Forum Nutr 63: 64–74, 2010.
24. Lutz TA, Del Prete E, Scharrer E. Subdiaphragmatic vagotomy does not influence the anorectic effect of amylin. Peptides 16: 457–462, 1995.
25. Lutz TA, Geary N, Szabady MM, Del Prete E, Scharrer E. Amylin decreases meal size in rats. Physiol Behav 58: 1197–1202, 1995.
26. Lutz TA, Mollet A, Rushing PA, Riediger T, Scharrer E. The anorectic effect of a chronic peripheral infusion of amylin is abolished in area postrema/nucleus of the solitary tract (AP/NTS) lesioned rats. Int J Obes Relat Metab Disord 25: 1005–1011, 2001.
27. Lutz TA, Senn M, Althaus J, Del Prete E, Ehrensperger F, Scharrer E. Lesion of the area postrema/nucleus of the solitary tract (AP/NTS) attenuates the anorectic effects of amylin and calcitonin gene-related peptide (CGRP) in rats. Peptides 19: 309–317, 1998.
28. Matheny M, Shapiro A, Tumer N, Scarpace PJ. Region-specific diet-induced and leptin-induced cellular leptin resistance includes the ventral tegmental area in rats. Neuropharmacology 60: 480–487, 2011.
29. Meye FJ, Adan RA. Feelings about food: the ventral tegmental area in food reward and emotional eating. Trends Pharmacol Sci 35: 31–40, 2014.
30. Mietlicki-Baase EG, Hayes MR. Amylin activates distributed CNS nuclei to control energy balance. Physiol Behav 136: 39–46, 2014.
31. Mietlicki-Baase EG, Ortinski PI, Rupprecht LE, Olivos DR, Alhadeff AL, Pierce RC, Hayes MR. The food intake-suppressive effects of glucagon-like peptide-1 receptor signaling in the ventral tegmental area are mediated by AMPA/kainate receptors. Am J Physiol Endocrinol Metab 305: E1367–E1374, 2013.
32. Mietlicki-Baase EG, Reiner DJ, Cone JJ, Olivos DR, McGrath LE, Zimmer DJ, Roitman MF, Hayes MR. Amylin modulates the mesolim-bic dopamine system to control energy balance. Neuropsychopharmacol-ogy 40: 372–385, 2015.
33. Mietlicki-Baase EG, Rupprecht LE, Olivos DR, Zimmer DJ, Alter MD, Pierce RC, Schmidt HD, Hayes MR. Amylin receptor signaling in the ventral tegmental area is physiologically relevant for the control of food intake. Neuropsychopharmacology 38: 1685–1697, 2013.
34. Mollet A, Gilg S, Riediger T, Lutz TA. Infusion of the amylin antagonist AC 187 into the area postrema increases food intake in rats. Physiol Behav 81: 149–155, 2004.
35. Mollet A, Meier S, Grabler V, Gilg S, Scharrer E, Lutz TA. Endogenous amylin contributes to the anorectic effects of cholecystokinin and bombesin. Peptides 24: 91–98, 2003.
36. Moon HS, Chamberland JP, Diakopoulos KN, Fiorenza CG, Ziemke F, Schneider B, Mantzoros CS. Leptin and amylin act in an additive manner to activate overlapping signaling pathways in peripheral tissues: in vitro and ex vivo studies in humans. Diabetes Care 34: 132–138, 2011.
37. Moon HS, Chamberland JP, Mantzoros CS. Amylin and leptin activate overlapping signalling pathways in an additive manner in mouse GT1-7 hypothalamic, C2C12 muscle and AML12 liver cell lines. Diabetologia 55: 215–225, 2012.
38. Moon HS, Dincer F, Mantzoros CS. Amylin-induced downregulation of hippocampal neurogenesis is attenuated by leptin in a STAT3/AMPK/ ERK-dependent manner in mice. Diabetologia 56: 627–634, 2013.
39. Munzberg H, Flier JS, Bjorbaek C. Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology 145: 4880–4889, 2004.
40. Narayanan NS, Guarnieri DJ, DiLeone RJ. Metabolic hormones, do-pamine circuits, and feeding. Front Neuroendocrinol 31: 104–112, 2010.
41. Nguyen N, Champion JK, Ponce J, Quebbemann B, Patterson E, Pham B, Raum W, Buchwald JN, Segato G, Favretti F. A review of unmet needs in obesity management. Obes Surg 22: 956–966, 2012.
42. Osto M, Wielinga PY, Alder B, Walser N, Lutz TA. Modulation of the satiating effect of amylin by central ghrelin, leptin and insulin. Physiol Behav 91: 566–572, 2007.
43. Pérez Rodrigo C. Current mapping of obesity. Nutr Hosp 28, Suppl 5: 21–31, 2013.
44. Popkin BM, Slining MM. New dynamics in global obesity facing low-and middle-income countries. Obes Rev 14, Suppl 2: 11–20, 2013.
45. Potes CS, Boyle CN, Wookey PJ, Riediger T, Lutz TA. Involvement of the extracellular signal-regulated kinase 1/2 signaling pathway in amylin’s eating inhibitory effect. Am J Physiol Regul Integr Comp Physiol 302: R340–R351, 2012.
46. Ravussin E, Smith SR, Mitchell JA, Shringarpure R, Shan K, Maier H, Koda JE, Weyer C. Enhanced weight loss with pramlintide/metrelep-tin: an integrated neurohormonal approach to obesity pharmacotherapy. Obesity (Silver Spring) 17: 1736–1743, 2009.
47. Roth JD. Amylin and the regulation of appetite and adiposity: recent advances in receptor signaling, neurobiology and pharmacology. Curr Opin Endocrinol Diabetes Obes 20: 8–13, 2013.
48. Roth JD, Roland BL, Cole RL, Trevaskis JL, Weyer C, Koda JE, Anderson CM, Parkes DG, Baron AD. Leptin responsiveness restored by amylin agonism in diet-induced obesity: evidence from nonclinical and clinical studies. Proc Natl Acad Sci USA 105: 7257–7262, 2008.
49. Roth JD, Trevaskis JL, Turek VF, Parkes DG. “Weighing in” on synergy: preclinical research on neurohormonal anti-obesity combinations. Brain Res 1350: 86–94, 2010.
50. Rushing PA, Hagan MM, Seeley RJ, Lutz TA, Woods SC. Amylin: a novel action in the brain to reduce body weight. Endocrinology 141: 850–853, 2000.
51. Sadry SA, Drucker DJ. Emerging combinatorial hormone therapies for the treatment of obesity and T2DM. Nat Rev Endocrinol 9: 425–433, 2013.
52. Singh-Franco D, Perez A, Harrington C. The effect of pramlintide acetate on glycemic control and weight in patients with type 2 diabetes mellitus and in obese patients without diabetes: a systematic review and meta-analysis. Diabetes Obes Metab 13: 169–180, 2011.
53. Smith SR, Blundell JE, Burns C, Ellero C, Schroeder BE, Kesty NC, Chen KS, Halseth AE, Lush CW, Weyer C. Pramlintide treatment reduces 24-h caloric intake and meal sizes and improves control of eating in obese subjects: a 6-wk translational research study. Am J Physiol Endocrinol Metab 293: E620–E627, 2007.
54. Tam CS, Lecoultre V, Ravussin E. Novel strategy for the use of leptin for obesity therapy. Expert Opin Biol Ther 11: 1677–1685, 2011.
55. Thompson JL, Borgland SL. Presynaptic leptin action suppresses excitatory synaptic transmission onto ventral tegmental area dopamine neurons. Biol Psychiatry 73: 860–868, 2013.
56. Trevaskis JL, Coffey T, Cole R, Lei C, Wittmer C, Walsh B, Weyer C, Koda J, Baron AD, Parkes DG, Roth JD. Amylin-mediated restoration of leptin responsiveness in diet-induced obesity: magnitude and mechanisms. Endocrinology 149: 5679–5687, 2008.
57. Trevaskis JL, Lei C, Koda JE, Weyer C, Parkes DG, Roth JD. Interaction of leptin and amylin in the long-term maintenance of weight loss in diet-induced obese rats. Obesity (Silver Spring) 18: 21–26, 2010.
58. Trinko R, Gan G, Gao XB, Sears RM, Guarnieri DJ, DiLeone RJ. Erk1/2 mediates leptin receptor signaling in the ventral tegmental area. PLoS One 6: e27180, 2011.
59. Turek VF, Trevaskis JL, Levin BE, Dunn-Meynell AA, Irani B, Gu G, Wittmer C, Griffin PS, Vu C, Parkes DG, Roth JD. Mechanisms of amylin/leptin synergy in rodent models. Endocrinology 151: 143–152, 2010.
60. Vucetic Z, Reyes TM. Central dopaminergic circuitry controlling food intake and reward: implications for the regulation of obesity. Wiley Interdiscip Rev Syst Biol Med 2: 577–593, 2010.