Leptin resistance and desensitization of hypophagia during prolonged inflammatory challenge

American Journal of Physiology - Endocrinology and Metabolism

Volumn 300, Issue 5, 2011, Pages

  Borges, Beatriz C ^a   Rorato, Rodrigo ^a   Avraham, Yosefa ^b   da Silva, Lilian E C M ^a   Castro, Margaret ^a   Vorobiav, Lia ^b   Berry, Elliot ^b   Antunes Rodrigues, Jose ^a   Elias, Lucila L K ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b HEBREW UNIVERSITY   (Israel)

Author keywords

2 arachidonoyl glycerol; Adenosine 5' monophosphate activated protein kinase; Leptin signaling; Lipopolysaccharide tolerance; Phosphorylated signal transducer and activator of transcription 3

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ADENYLATE KINASE; BACTERIUM LIPOPOLYSACCHARIDE; ENDOTOXIN; LEPTIN; MELANOCORTIN 4 RECEPTOR; MESSENGER RNA; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DESENSITIZATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FOOD INTAKE; GENE EXPRESSION; HYPOPHAGIA; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LONG TERM EXPOSURE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ARACHIDONIC ACIDS; BODY WEIGHT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIET; DIETARY FATS; EATING; ENDOTOXINS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GLYCERIDES; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTERLEUKIN-10; LEPTIN; LIPOPOLYSACCHARIDES; MALE; PHOSPHORYLATION; RATS; RATS, WISTAR; RECEPTOR, MELANOCORTIN, TYPE 4; RECEPTORS, INTERLEUKIN-10; RECEPTORS, LEPTIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 79955562972     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00558.2010     Document Type: Article

References (56)

1. Avraham Y, Ben-Shushan D, Breuer A, Zolotarev O, Okon A, Fink N, Katz V, Berry EM. Very low doses of delta 8-THC increase food consumption and alter neurotransmitter levels following weight loss. Pharmacol Biochem Behav 77: 675-684, 2004.
2. Avraham Y, Menachem AB, Okun A, Zlotarav O, Abel N, Mechoulam R, Berry EM. Effects of the endocannabinoid noladin ether on body weight, food consumption, locomotor activity, and cognitive index in mice. Brain Res Bull 65: 117-123, 2005.
3. Bates SH, Stearns WH, Dundon TA, Schubert M, Tso AW, Wang Y, Banks AS, Lavery HJ, Haq AK, Maratos-Flier E, Neel BG, Schwartz MW, Myers MG Jr. STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature 421: 856-859, 2003.
4. Bellocchio L, Cervino C, Pasquali R, Pagotto U. The endocannabinoid system and energy metabolism. J Neuroendocrinol 20: 850-857, 2008.
5. Benamar K, Yondorf M, Meissler JJ, Geller EB, Tallarida RJ, Eisenstein TK, Adler MW. A novel role of cannabinoids: implication in the fever induced by bacterial lipopolysaccharide. J Pharmacol Exp Ther 320: 1127-1133, 2007.
6. Benoit S, Schwartz M, Baskin D, Woods SC, Seeley RJ. CNS melanocortin system involvement in the regulation of food intake. Horm Behav 37: 299-305, 2000.
7. Berlato C, Cassatella MA, Kinjyo I, Gatto L, Yoshimura A, Bazzoni F. Involvement of suppressor of cytokine signaling-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation. J Immunol 168: 6404-6411, 2002.
8. Berry EM, Mechoulam R. Tetrahydrocannabinol and endocannabinoids in feeding and appetite. Pharmacol Ther 95: 185-190, 2002.
9. Borges BC, Antunes-Rodrigues J, Castro M, Bittencourt JC, Elias CF, Elias LL. Expression of hypothalamic neuropeptides and the desensitization of pituitary-adrenal axis and hypophagia in the endotoxin tolerance. Horm Behav 52: 508-519, 2007.
10. Buettner C, Pocai A, Muse ED, Etgen AM, Myers MG Jr, Rossetti L. Critical role of STAT3 in leptin's metabolic actions. Cell Metab 4: 49-60, 2006.
11. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmée E, Cousin B, Sulpice T, Chamontin B, Ferrières J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56: 1761-1772, 2007.
12. Caruso C, Durand D, Schiöth HB, Rey R, Seilicovich A, Lasaga M. Activation of melanocortin 4 receptors reduces the inflammatory response and prevents apoptosis induced by lipopolysaccharide and interferongamma in astrocytes. Endocrinology 148: 4918-4926, 2007.
13. Cavaillon JM, Adrie C, Fitting C, Adib-Conquy M. Endotoxin tolerance: is there a clinical relevance? J Endotoxin Res 9: 101-107, 2003.
14. Cone DR. Anatomy and regulation of the central melanocortin system. Nat Neurosci 8: 571-578, 2005.
15. Dagon Y, Avraham Y, Magen I, Gertler A, Ben-Hur T, Berry EM. Nutritional status, cognition, and survival: a new role for leptin and AMP kinase. J Biol Chem 280: 42142-42148, 2005.
16. Di Marzo V, Bisogno T, De Petrocellis L, Melck D, Orlando P, Wagner JA, Kunos G. Biosynthesis and inactivation of the endocannabinoid 2-arachidonoylglycerol in circulating and tumoral macrophages. Eur J Biochem 264: 258-267, 1999.
17. Di Marzo V, Goparaju SK, Wang L, Liu J, Bátkai S, Járai Z, Fezza F, Miura GI, Palmiter RD, Sugiura T, Kunos G. Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410: 822-825, 2001.
18. Elias CF, Aschkenasi C, Lee C, Kelly J, Ahima RS, Bjorbaek C, Flier JS, Saper CB, Elmquist JK. Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron 23: 775-786, 1999.
19. Facchinetti F, Del Giudice E, Furegato S, Passarotto M, Leon A. Cannabinoids ablate release of TNFalpha in rat microglial cells stimulated with lypopolysaccharide. Glia 41: 161-168, 2003.
20. Faggioni R, Fuller J, Moser A, Feingold KR, Grunfeld C. LPS-induced anorexia in leptin-deficient (ob/ob) and leptin receptor-deficient (db/db) mice. Am J Physiol Regul Integr Comp Physiol 273: R181-R186, 1997.
21. Feng GS. Shp2 as a therapeutic target for leptin resistance and obesity. Expert Opin Ther Targets 10: 135-142, 2006.
22. Fraga D, Zanoni CI, Rae GA, Parada CA, Souza GE. Endogenous cannabinoids induce fever through the activation of CB1 receptors. Br J Pharmacol 157: 1494-1501, 2009.
23. Freudenberg MA, Galanos C. Induction of tolerance to lipopolysaccharide (LPS)-D-galactosamine lethality by pretreatment with LPS is mediated by macrophages. Infect Immun 56: 1352-1357, 1988.
24. Frühbeck G. Intracellular signaling pathways activated by leptin. Biochem J 393: 7-20, 2006.
25. Gautron L, Mingam R, Moranis A, Combe C, Laye S. Influence of feeding status on neuronal activity in the hypothalamus during lipopolysaccharide- induced anorexia in rats. Neuroscience 134: 933-946, 2005.
26. Gayle D, Ilyin SE, Plata-Salamán CR. Feeding status and bacterial LPS-induced cytokine and neuropeptide gene expression in hypothalamus. Am J Physiol Regul Integr Comp Physiol 277: R1188-R1195, 1999.
27. Giri S, Nath N, Smith B, Viollet B, Singh AK, Singh I. 5-aminoimidazole- 4-carboxamide-1-beta-4-ribofuranoside inhibits proinflammatory response in glial cells: a possible role of AMP-activated protein kinase. J Neurosc 24: 479-487, 2004.
28. Hanus L, Avraham Y, Ben-Shushan D, Zolotarev O, Berry EM, Mechoulam R. Short-term fasting and prolonged semistarvation have opposite effects on 2-AG levels in mouse brain. Brain Res 983: 144-151, 2003.
29. Hardie DG, Scott JW, Pan DA, Hudson ER. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 546: 113-120, 2003.
30. Hofbauer KG, Lecourt AC, Peter JC. Antibodies as pharmacologic tools for studies on the regulation of energy balance. Nutrition 24: 791-797, 2008.
31. Johnson RW. Immune and endocrine regulation of food intake in sick animals. Domest Anim Endocrinol 15: 309-319, 1998.
32. Kaszubska W, Falls HD, Schaefer VG, Haasch D, Frost L, Hessler P, Kroeger PE, White DW, Jirousek MR, Trevillyan JM. Protein tyrosine phosphatase 1B negatively regulates leptin signaling in a hypothalamic cell line. Mol Cell Endocrinol 195: 109-118, 2002.
33. Kola B, Farkas I, Christ-Crain M, Wittmann G, Lolli F, Amin F, Harvey-White J, Liposits Z, Kunos G, Grossman AB, Fekete C, Korbonits M. The orexigenic effect of ghrelin is mediated through central activation of the endogenous cannabinoid system. PLoS One 3: e1797, 2008.
34. Koren S, Fantus IG. Inhibition of the protein tyrosine phosphatase PTP1B: potential therapy for obesity, insulin resistance and type-2 diabetes mellitus. Best Pract Res Clin Endocrinol Metab 21: 621-640, 2007.
35. Kristensen P, Judge ME, Thim L, Ribel U, Christjansen KN, Wulff BS, Clausen JT, Jensen PB, Madsen OD, Vrang N, Larsen PJ, Hastrup S. Hypothalamic CART is a new anorectic peptide regulated by leptin. Nature 393: 72-76, 1998.
36. Lugarini F, Hrupka BJ, Schwartz GJ, Plata-Salaman CR, Langhans W. Acute and chronic administration of immunomodulators induces anorexia in Zucker rats. Physiol Behav 84: 165-173, 2005.
37. Mastronardi CA, Srivastava V, Yu WH, Les Dees W, McCann SM. Lipopolysaccharide-induced leptin synthesis and release are differentially controlled by alpha-melanocyte-stimulating hormone. Neuroimmunomodulation 12: 182-188, 2005.
38. Milanski M, Degasperi G, Coope A, Morari J, Denis R, Cintra DE, Tsukumo DM, Anhe G, Amaral ME, Takahashi HK, Curi R, Oliveira HC, Carvalheira JB, Bordin S, Saad MJ, Velloso LA. Saturated fatty acids produce an inflammatory response predominantly through the activation of TLR4 signaling in hypothalamus: implications for the pathogenesis of obesity. J Neurosci 29: 359-370, 2009.
39. Minokoshi Y, Alquier T, Furukawa N, Kim YB, Lee A, Xue B, Mu J, Foufelle F, Ferré P, Birnbaum MJ, Stuck BJ, Kahn BB. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428: 569-574, 2004.
40. Mitch WE. Cachexia in chronic kidney disease: a link to defective central nervous system control of appetite. J Clin Invest 115: 1476-1478, 2005.
41. Münzberg H, Flier JS, Bjørbaek C. Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology 145: 4880-4889, 2004.
42. Münzberg H. Leptin-signaling pathways and leptin resistance. Forum Nutr 63: 123-132, 2010.
43. Ogimoto K, Harris MK Jr, Wisse BE. MyD88 is a key mediator of anorexia, but not weight loss, induced by lipopolysaccharide and interleukin-1 beta. Endocrinology 147: 4445-4453, 2006.
44. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 1998.
45. Qin H, Roberts KL, Niyongere SA, Cong Y, Elson CO, Benveniste EN. Molecular mechanism tk;2of lipopolysaccharide-induced SOCS-3 gene expression in macrophages and microglia. J Immunol 179: 5966-5976, 2007.
46. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123: 1939-1951, 1993.
47. Roche M, Kelly JP, O'Driscoll M, Finn DP. Augmentation of endogenous cannabinoid tone modulates lipopolysaccharide-induced alterations in circulating cytokine levels in rats. Immunology 125: 263-671, 2008.
48. Rorato R, Castro M, Borges BC, Benedetti M, Germano CM, Antunes-Rodrigues J, Elias LL. Adrenalectomy enhances endotoxemia-induced hypophagia: higher activation of corticotrophin-releasing-factor and proopiomelanocortin hypothalamic neurons. Horm Behav 54: 134-142, 2008.
49. Sachot C, Poole S, Luheshi GN. Circulating leptin mediates lipopolysaccharide- induced anorexia and fever in rats. J Physiol 15: 263-272, 2004.
50. Sag D, Carling D, Stout RD, Suttles J. Adenosine 5=-monophosphateactivated protein kinase promotes macrophage polarization to an antiinflammatory functional phenotype. J Immunol 181: 8633-8641, 2008.
51. Sinha PS, Schiöth HB, Tatro JB. Activation of central melanocortin-4 receptor suppresses lipopolysaccharide-induced fever in rats. Am J Physiol Regul Integr Comp Physiol 284: R1595-R1603, 2003.
52. Thaler JP, Choi SJ, Schwartz MW, Wisse BE. Hypothalamic inflammation and energy homeostasis: resolving the paradox. Front Neuroendocrinol 31: 79-84, 2010.
53. Tups A. Physiological models of leptin resistance. J Neuroendocrinol 21: 961-971, 2009.
54. Yamawaki Y, Kimura H, Hosoi T, Ozawa K. MyD88 plays a key role in LPS-induced Stat3 activation in the hypothalamus. Am J Physiol Regul Integr Comp Physiol 298: R403-R410, 2010.
55. Zhang EE, Chapeau E, Hagihara K, Feng GS. Neuronal Shp2 tyrosine phosphatase controls energy balance and metabolism. Proc Natl Acad Sci USA 101: 16064-16069, 2004.
56. Ziegler-Heitbrock HW. Molecular mechanism in tolerance to lipopolysaccharide. J Inflamm 45: 13-26, 1995.