Improved Leptin Sensitivity as a Potential Candidate Responsible for the Spontaneous Food Restriction of the Lou/C Rat

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Veyrat Durebex, Christelle ^a   Poher, Anne Laure ^a   Caillon, Aurélie ^a   Somm, Emmanuel ^b   Vallet, Philippe ^b   Charnay, Yves ^b   Rohner Jeanrenaud, Françoise ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; LEPTIN; MEGALIN; MESSENGER RNA; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN; PROTIRELIN; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CHOROID PLEXUS; CONTROLLED STUDY; DIET RESTRICTION; DOWN REGULATION; FEEDING BEHAVIOR; HORMONE ACTION; HORMONE SENSITIVITY; HYPERTRIGLYCERIDEMIA; HYPOPHAGIA; HYPOTHALAMUS; LOU C RAT; MALE; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RAT; RAT STRAIN; SIGNAL TRANSDUCTION; SPECIES COMPARISON; WISTAR RAT;

ANIMALS; EATING; HYPOTHALAMUS; LEPTIN; MALE; OBESITY; RATS; RATS, WISTAR; RECEPTORS, LEPTIN; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84883613615     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073452     Document Type: Article

References (45)

1. Levin BE, Dunn-Meynell AA, Banks WA, (2004) 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. PubMed: 12958061.
2. Veyrat-Durebex C, Alliot J, (1997) Changes in pattern of macronutrient intake during aging in male and female rats. Physiol Behav 62: 1273-1278. doi:10.1016/S0031-9384(97)00304-1. PubMed: 9383113.
3. Veyrat-Durebex C, Boghossian S, Alliot J, (1998) Age-related changes in adaptive mechanisms of macronutrient self-selection: evidence for a sexual dimorphism. Mech Ageing Dev 103: 223-234. doi:10.1016/S0047-6374(98)00013-X. PubMed: 9723900.
4. Veyrat-Durebex C, Montet X, Vinciguerra M, Gjinovci A, Meda P, et al. (2009) The Lou/C rat: a model of spontaneous food restriction associated with improved insulin sensitivity and decreased lipid storage in adipose tissue. Am J Physiol Endocrinol Metab 296: E1120-E1132. doi:10.1152/ajpendo.90592.2008. PubMed: 19208855.
5. Veyrat-Durebex C, Poher AL, Caillon A, Montet X, Rohner-Jeanrenaud F, (2011) Alterations in lipid metabolism and thermogenesis with emergence of brown adipocytes in white adipose tissue in diet-induced obesity-resistant Lou/C rats. Am J Physiol Endocrinol Metab 300: E1146-E1157. doi:10.1152/ajpendo.00575.2010. PubMed: 21406614.
6. Héliès JM, Diane A, Langlois A, Larue-Achagiotis C, Fromentin G, et al. (2005) Comparison of fat storage between Fischer 344 and obesity-resistant Lou/C rats fed different diets. Obes Res 13: 3-10. doi:10.1038/oby.2005.70. PubMed: 15761158.
7. Alliot J, Boghossian S, Jourdan D, Veyrat-Durebex C, Pickering G, et al. (2002) The LOU/c/jall rat as an animal model of healthy aging? J Gerontol A Biol Sci Med Sci 57: B312-B320. doi:10.1093/gerona/57.8.B312. PubMed: 12145357.
8. Taleux N, De Potter I, Deransart C, Lacraz G, Favier R, et al. (2008) Lack of starvation-induced activation of AMP-activated protein kinase in the hypothalamus of the Lou/C rats resistant to obesity. Int J Obes 32: 639-647. doi:10.1038/sj.ijo.0803759. PubMed: 18059408.
9. Moyse E, Bédard K, Segura S, Mahaut S, Tardivel C, et al. (2012) Effects of aging and caloric restriction on brainstem satiety center signals in rats. Mech Ageing Dev 133: 83-91. doi:10.1016/j.mad.2012.01.004. PubMed: 22285292.
10. Levin BE, (1999) Arcuate NPY neurons and energy homeostasis in diet-induced obese and resistant rats. Am J Physiol 276: R382-R387. PubMed: 9950915.
11. Levin BE, Dunn-Meynell AA, (2002) Reduced central leptin sensitivity in rats with diet-induced obesity. Am J Physiol Regul Integr Comp Physiol 283: R941-R948. PubMed: 12228064.
12. Banks WA, (2003) Is obesity a disease of the blood-brain barrier? Physiological, pathological, and evolutionary considerations. Curr Pharm Des 9: 801-809. doi:10.2174/1381612033455350. PubMed: 12678879.
13. Münzberg H, Myers MG Jr., (2005) Molecular and anatomical determinants of central leptin resistance. Nat Neurosci 8: 566-570. doi:10.1038/nn1454. PubMed: 15856064.
14. Banks WA, Coon AB, Robinson SM, Moinuddin A, Shultz JM, et al. (2004) Triglycerides induce leptin resistance at the blood-brain barrier. Diabetes 53: 1253-1260. doi:10.2337/diabetes.53.5.1253. PubMed: 15111494.
15. Caro JF, Kolaczynski JW, Nyce MR, Ohannesian JP, Opentanova I, et al. (1996) Decreased cerebrospinal-fluid/serum leptin ratio in obesity: a possible mechanism for leptin resistance. Lancet 348: 159-161. doi:10.1016/S0140-6736(96)03173-X. PubMed: 8684156.
16. Banks WA, DiPalma CR, Farrell CL, (1999) Impaired transport of leptin across the blood-brain barrier in obesity. Peptides 20: 1341-1345. doi:10.1016/S0196-9781(99)00139-4. PubMed: 10612449.
17. Schwartz MW, Peskind E, Raskind M, Boyko EJ, Porte D Jr., (1996) Cerebrospinal fluid leptin levels: relationship to plasma levels and to adiposity in humans. Nat Med 2: 589-593. doi:10.1038/nm0596-589. PubMed: 8616722.
18. Hosoi T, Sasaki M, Miyahara T, Hashimoto C, Matsuo S, et al. (2008) Endoplasmic reticulum stress induces leptin resistance. Mol Pharmacol 74: 1610-1619. doi:10.1124/mol.108.050070. PubMed: 18755873.
19. Thaler JP, Yi CX, Schur EA, Guyenet SJ, Hwang BH, et al. (2012) Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest 122: 153-162. doi:10.1172/JCI59660. PubMed: 22201683.
20. Schwartz MW, Woods SC, Porte D Jr., Seeley RJ, Baskin DG, (2000) Central nervous system control of food intake. Nature 404: 661-671. PubMed: 10766253.
21. Liao GY, An JJ, Gharami K, Waterhouse EG, Vanevski F, et al. (2012) Dendritically targeted Bdnf mRNA is essential for energy balance and response to leptin. Nat Med 18: 564-571. doi:10.1038/nm.2687. PubMed: 22426422.
22. Nillni EA, Vaslet C, Harris M, Hollenberg A, Bjørbak C, et al. (2000) Leptin regulates prothyrotropin-releasing hormone biosynthesis. Evidence for direct and indirect pathways. J Biol Chem 275: 36124-36133. doi:10.1074/jbc.M003549200. PubMed: 10967095.
23. Vettor R, Zarjevski N, Cusin I, Rohner-Jeanrenaud F, Jeanrenaud B, (1994) Induction and reversibility of an obesity syndrome by intracerebroventricular neuropeptide Y administration to normal rats. Diabetologia 37: 1202-1208. doi:10.1007/BF00399793. PubMed: 7895949.
24. Brown LM, Clegg DJ, Benoit SC, Woods SC, (2006) Intraventricular insulin and leptin reduce food intake and body weight in C57BL/6J mice. Physiol Behav 89: 687-691. doi:10.1016/j.physbeh.2006.08.008. PubMed: 16979194.
25. Williams DL, Baskin DG, Schwartz MW, (2006) Leptin regulation of the anorexic response to glucagon-like peptide-1 receptor stimulation. Diabetes 55: 3387-3393. doi:10.2337/db06-0558. PubMed: 17130484.
26. Herbert V, Lau KS, Gottlieb CW, Bleicher SJ, (1965) Coated charcoal immunoassay of insulin. J Clin Endocrinol Metab 25: 1375-1384. doi:10.1210/jcem-25-10-1375. PubMed: 5320561.
27. Moran TH, Aja S, Ladenheim EE, (2006) Leptin modulation of peripheral controls of meal size. Physiol Behav 89: 511-516. doi:10.1016/j.physbeh.2006.04.020. PubMed: 16735044.
28. Baggio LL, Huang Q, Brown TJ, Drucker DJ, (2004) Oxyntomodulin and glucagon-like peptide-1 differentially regulate murine food intake and energy expenditure. Gastroenterology 127: 546-558. doi:10.1053/j.gastro.2004.04.063. PubMed: 15300587.
29. Merchenthaler I, Lane M, Shughrue P, (1999) Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol 403: 261-280. doi:10.1002/(SICI)1096-9861(19990111)403:2. PubMed: 9886047.
30. Mitchell SE, Nogueiras R, Rance K, Rayner DV, Wood S, et al. (2006) Circulating hormones and hypothalamic energy balance: regulatory gene expression in the Lou/C and Wistar rats. J Endocrinol 190: 571-579. doi:10.1677/joe.1.06576. PubMed: 17003258.
31. Dietrich MO, Spuch C, Antequera D, Rodal I, de Yébenes JG, et al. (2008) Megalin mediates the transport of leptin across the blood-CSF barrier. Neurobiol Aging 29: 902-912. doi:10.1016/j.neurobiolaging.2007.01.008. PubMed: 17324488.
32. Hama H, Saito A, Takeda T, Tanuma A, Xie Y, et al. (2004) Evidence indicating that renal tubular metabolism of leptin is mediated by megalin but not by the leptin receptors. Endocrinology 145: 3935-3940. doi:10.1210/en.2004-0074. PubMed: 15131016.
33. Bjørbaek C, Elmquist JK, Frantz JD, Shoelson SE, Flier JS, (1998) Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol Cell 1: 619-625. doi:10.1016/S1097-2765(00)80062-3. PubMed: 9660946.
34. Ahima RS, Saper CB, Flier JS, Elmquist JK, (2000) Leptin regulation of neuroendocrine systems. Front Neuroendocrinol 21: 263-307. doi:10.1006/frne.2000.0197. PubMed: 10882542.
35. Leinninger GM, Opland DM, Jo YH, Faouzi M, Christensen L, et al. (2011) Leptin action via neurotensin neurons controls orexin, the mesolimbic dopamine system and energy balance. Cell Metab 14: 313-323. doi:10.1016/j.cmet.2011.06.016. PubMed: 21907138.
36. Lebrun B, Bariohay B, Moyse E, Jean A, (2006) Brain-derived neurotrophic factor (BDNF) and food intake regulation: a minireview. Auton Neurosci Basic Clin 126-127: 30-38. doi:10.1016/j.autneu.2006.02.027. PubMed: 16632412.
37. Kappeler L, Zizzari P, Grouselle D, Epelbaum J, Bluet-Pajot MT, (2004) Plasma and hypothalamic peptide-hormone levels regulating somatotroph function and energy balance in fed and fasted states: a comparative study in four strains of rats. J Neuroendocrinol 16: 980-988. doi:10.1111/j.1365-2826.2004.01259.x. PubMed: 15667453.
38. Lebrun B, Bariohay B, Moyse E, Jean A, (2006) Brain-derived neurotrophic factor (BDNF) and food intake regulation: a minireview. Auton Neurosci 126-127: 30-38. doi:10.1016/j.autneu.2006.02.027. PubMed: 16632412.
39. Pelleymounter MA, Cullen MJ, Wellman CL, (1995) Characteristics of BDNF-induced weight loss. Exp Neurol 131: 229-238. doi:10.1016/0014-4886(95)90045-4. PubMed: 7534721.
40. Fox EA, Byerly MS, (2004) A mechanism underlying mature-onset obesity: evidence from the hyperphagic phenotype of brain-derived neurotrophic factor mutants. Am J Physiol Regul Integr Comp Physiol 286: R994-1004. doi:10.1152/ajpregu.00727.2003. PubMed: 15142855.
41. Xu B, Goulding EH, Zang K, Cepoi D, Cone RD, et al. (2003) Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor. Nat Neurosci 6: 736-742. doi:10.1038/nn1073. PubMed: 12796784.
42. Levin BE, (2007) Neurotrophism and energy homeostasis: perfect together. Am J Physiol Regul Integr Comp Physiol 293: R988-R991. doi:10.1152/ajpregu.00434.2007. PubMed: 17596322.
43. Klaman LD, Boss O, Peroni OD, Kim JK, Martino JL, et al. (2000) Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice. Mol Cell Biol 20: 5479-5489. doi:10.1128/MCB.20.15.5479-5489.2000. PubMed: 10891488.
44. Howard JK, Cave BJ, Oksanen LJ, Tzameli I, Bjørbaek C, et al. (2004) Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3. Nat Med 10: 734-738. doi:10.1038/nm1072. PubMed: 15220914.
45. Ramadori G, Fujikawa T, Anderson J, Berglund ED, Frazao R, et al. (2011) SIRT1 deacetylase in SF1 neurons protects against metabolic imbalance. Cell Metab 14: 301-312. doi:10.1016/j.cmet.2011.06.014. PubMed: 21907137.