About this Journal Submit a Manuscript Table of Contents
Neural Plasticity
Volume 2013 (2013), Article ID 438072, 8 pages
http://dx.doi.org/10.1155/2013/438072
Review Article

Environment, Leptin Sensitivity, and Hypothalamic Plasticity

1CNR Neuroscience Institute, Via Moruzzi 1, 56124 Pisa, Italy
2Department of Neuroscience, Psychology, Drug Research and Child Health NEUROFARBA, University of Florence, Via San Salvi 12, 50135 Florence, Italy
3Dulbecco Telethon Institute at Endocrinology Unit, University Hospital of Pisa, Via Paradisa 2, 56124 Pisa, Italy
4CNR Institute of Food Sciences, Via Roma 64, 83100 Avellino, Italy

Received 5 April 2013; Accepted 25 June 2013

Academic Editor: Alessandro Sale

Copyright © 2013 Marco Mainardi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. W. Schwartz, S. C. Woods, D. Porte Jr., R. J. Seeley, and D. G. Baskin, “Central nervous system control of food intake,” Nature, vol. 404, no. 6778, pp. 661–671, 2000. View at Scopus
  2. E. E. Jobst, P. J. Enriori, and M. A. Cowley, “The electrophysiology of feeding circuits,” Trends in Endocrinology and Metabolism, vol. 15, no. 10, pp. 488–499, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. M. S. Dicken, R. E. Tooker, and S. T. Hentges, “Regulation of gaba and glutamate release from proopiomelanocortin neuron terminals in intact hypothalamic networks,” The Journal of Neuroscience, vol. 32, no. 12, pp. 4042–4048, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. M. G. Myers Jr., H. Münzberg, G. M. Leinninger, and R. L. Leshan, “The geometry of leptin action in the brain: more complicated than a simple ARC,” Cell Metabolism, vol. 9, no. 2, pp. 117–123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Plum, B. F. Belgardt, and J. C. Brüning, “Central insulin action in energy and glucose homeostasis,” The Journal of Clinical Investigation, vol. 116, no. 7, pp. 1761–1766, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. J.-H. Wang, F. Wang, M.-J. Yang et al., “Leptin regulated calcium channels of neuropeptide Y and proopiomelanocortin neurons by activation of different signal pathways,” Neuroscience, vol. 156, no. 1, pp. 89–98, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Qiu, Y. Fang, O. K. Rønnekleiv, and M. J. Kelly, “Leptin excites proopiomelanocortin neurons via activation of TRPC channels,” The Journal of Neuroscience, vol. 30, no. 4, pp. 1560–1565, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. H. T. Bergen, T. M. Mizuno, J. Taylor, and C. V. Mobbs, “Hyperphagia and weight gain after gold-thioglucose: relation to hypothalamic neuropeptide Y and proopiomelanocortin,” Endocrinology, vol. 139, no. 11, pp. 4483–4488, 1998. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Yaswen, N. Diehl, M. B. Brennan, and U. Hochgeschwender, “Obesity in the mouse model of pro-opiomelanocortin deficiency responds to peripheral melanocortin,” Nature Medicine, vol. 5, no. 9, pp. 1066–1070, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Gropp, M. Shanabrough, E. Borok et al., “Agouti-related peptide-expressing neurons are mandatory for feeding,” Nature Neuroscience, vol. 8, no. 10, pp. 1289–1291, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Mesaros, S. B. Koralov, E. Rother et al., “Activation of Stat3 signaling in AgRP neurons promotes locomotor activity,” Cell Metabolism, vol. 7, no. 3, pp. 236–248, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Aponte, D. Atasoy, and S. M. Sternson, “AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training,” Nature Neuroscience, vol. 14, no. 3, pp. 351–355, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Zhan, J. Zhou, Q. Feng, et al., “Acute and long-term suppression of feeding behavior by POMC neurons in the brainstem and hypothalamus, respectively,” The Journal of Neuroscience, vol. 33, no. 8, pp. 3624–3632, 2013.
  14. F. Zhang, V. Gradinaru, A. R. Adamantidis et al., “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nature Protocols, vol. 5, no. 3, pp. 439–456, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. V. K. Yadav, F. Oury, N. Suda et al., “A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure,” Cell, vol. 138, no. 5, pp. 976–989, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. J. M. Friedman and J. L. Halaas, “Leptin and the regulation of body weight in mammals,” Nature, vol. 395, no. 6704, pp. 763–770, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Lindström, “The physiology of obese-hyperglycemic mice [ob/ob mice],” The Scientific World Journal, vol. 7, pp. 666–685, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. F. F. Chehab, “A broader role for leptin,” Nature Medicine, vol. 2, no. 7, pp. 723–724, 1996. View at Scopus
  19. J. L. Halaas, K. S. Gajiwala, M. Maffei et al., “Weight-reducing effects of the plasma protein encoded by the obese gene,” Science, vol. 269, no. 5223, pp. 543–546, 1995. View at Scopus
  20. M. A. Pelleymounter, M. J. Cullen, M. B. Baker et al., “Effects of the obese gene product on body weight regulation in ob/ob mice,” Science, vol. 269, no. 5223, pp. 540–543, 1995. View at Scopus
  21. J. Salvador, J. Gomez-Ambrosi, and G. Fühbeck, “Perspectives in the therapeutic use of leptin,” Expert Opinion on Pharmacotherapy, vol. 2, no. 10, pp. 1615–1622, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. I. Sadaf Farooqi and S. O'Rahilly, “Leptin: a pivotal regulator of human energy homeostasis,” American Journal of Clinical Nutrition, vol. 89, no. 3, pp. 980S–984S, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Zhang, R. Proenca, M. Maffei, M. Barone, L. Leopold, and J. M. Friedman, “Positional cloning of the mouse obese gene and its human homologue,” Nature, vol. 372, no. 6505, pp. 425–432, 1994. View at Publisher · View at Google Scholar · View at Scopus
  24. D. L. Coleman, “A historical perspective on leptin,” Nature Medicine, vol. 16, no. 10, pp. 1097–1099, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. M.-D. Li, “Leptin and beyond: an odyssey to the central control of body weight,” Yale Journal of Biology and Medicine, vol. 84, no. 1, pp. 1–7, 2011. View at Scopus
  26. G.-H. Lee, R. Proenca, J. M. Montez et al., “Abnormal splicing of the leptin receptor in diabetic mice,” Nature, vol. 379, no. 6566, pp. 632–635, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Ravussin, R. E. Pratley, M. Maffei et al., “Relatively low plasma leptin concentrations precede weight gain in Pima Indians,” Nature Medicine, vol. 3, no. 2, pp. 238–240, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Maffei, H. Fei, G.-H. Lee et al., “Increased expression in adipocytes of ob RNA in mice with lesions of the hypothalamus and with mutations at the db locus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 15, pp. 6957–6960, 1995. View at Publisher · View at Google Scholar · View at Scopus
  29. L. A. Tartaglia, M. Dembski, X. Weng et al., “Identification and expression cloning of a leptin receptor, OB-R,” Cell, vol. 83, no. 7, pp. 1263–1271, 1995. View at Publisher · View at Google Scholar · View at Scopus
  30. M. E. Trujillo, M.-J. Lee, S. Sullivan et al., “Tumor necrosis factor α and glucocorticoid synergistically increase leptin production in human adipose tissue: role for p38 mitogen-activated protein kinase,” Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 4, pp. 1484–1490, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. S. K. Fried, M. R. Ricci, C. D. Russell, and B. Laferrère, “Regulation of leptin production in humans,” The Journal of Nutrition, vol. 130, no. 12, pp. 3127S–3131S, 2000.
  32. M. Mapfei, J. Halaas, E. Ravussin et al., “Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects,” Nature Medicine, vol. 1, no. 11, pp. 1155–1161, 1995. View at Scopus
  33. A. Parduca, J. Perez, and L. M. Garcia-Segura, “Estradiol induces plasticity of GABAergic synapses in the hypothalamus,” Neuroscience, vol. 53, no. 2, pp. 395–401, 1993. View at Publisher · View at Google Scholar · View at Scopus
  34. E. Csakvari, Z. Hoyk, A. Gyenes, D. Garcia-Ovejero, L. M. Garcia-Segura, and Á. Párducz, “Fluctuation of synapse density in the arcuate nucleus during the estrous cycle,” Neuroscience, vol. 144, no. 4, pp. 1288–1292, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. L. M. Zeltser, R. J. Seeley, and M. H. Tschop, “Synaptic plasticity in neuronal circuits regulating energy balance,” Nature Neuroscience, vol. 15, no. 10, pp. 1336–1342, 2012.
  36. S. G. Bouret, S. J. Draper, and R. B. Simerly, “Trophic action of leptin on hypothalamic neurons that regulate feeding,” Science, vol. 304, no. 5667, pp. 108–110, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. N. Berardi, T. Pizzorusso, and L. Maffei, “Critical periods during sensory development,” Current Opinion in Neurobiology, vol. 10, no. 1, pp. 138–145, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Pinto, A. G. Roseberry, H. Liu et al., “Rapid rewiring of arcuate nucleus feeding circuits by leptin,” Science, vol. 304, no. 5667, pp. 110–115, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. C. M. Novak, P. R. Burghardt, and J. A. Levine, “The use of a running wheel to measure activity in rodents: relationship to energy balance, general activity, and reward,” Neuroscience and Biobehavioral Reviews, vol. 36, no. 3, pp. 1001–1014, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. R. A. Hammond, “Social influence and obesity,” Current Opinion in Endocrinology, Diabetes and Obesity, vol. 17, no. 5, pp. 467–471, 2010.
  41. D. E. G. McNay, N. Briançon, M. V. Kokoeva, E. Maratos-Flier, and J. S. Flier, “Remodeling of the arcuate nucleus energy-balance circuit is inhibited in obese mice,” The Journal of Clinical Investigation, vol. 122, no. 1, pp. 142–152, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. C. M. Patterson, S. G. Bouret, A. A. Dunn-Meynell, and B. E. Levin, “Three weeks of postweaning exercise in DIO rats produces prolonged increases in central leptin sensitivity and signaling,” American Journal of Physiology, vol. 296, no. 3, pp. R537–R548, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. S. K. Panchal and L. Brown, “Rodent models for metabolic syndrome research,” Journal of Biomedicine and Biotechnology, vol. 2011, Article ID 351982, 14 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. E. M. Mercken, B. A. Carboneau, S. M. Krzysik-Walker, and R. de Cabo, “Of mice and men: the benefits of caloric restriction, exercise, and mimetics,” Ageing Research Reviews, vol. 11, no. 3, pp. 390–398, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Martin, M. P. Mattson, and S. Maudsley, “Caloric restriction and intermittent fasting: two potential diets for successful brain aging,” Ageing Research Reviews, vol. 5, no. 3, pp. 332–353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Coppola, Z.-W. Liu, Z. B. Andrews et al., “A central thermogenic-like mechanism in feeding regulation: an interplay between arcuate nucleus T3 and UCP2,” Cell Metabolism, vol. 5, no. 1, pp. 21–33, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Mainardi, G. Scabia, T. Vottari et al., “A sensitive period for environmental regulation of eating behavior and leptin sensitivity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 38, pp. 16673–16678, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Sale, N. Berardi, and L. Maffei, “Enrich the environment to empower the brain,” Trends in Neurosciences, vol. 32, no. 4, pp. 233–239, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. H. van Praag, G. Kempermann, and F. H. Gage, “Neural consequences of environmental enrichment,” Nature Reviews Neuroscience, vol. 1, no. 3, pp. 191–198, 2000. View at Scopus
  50. G. Di Cristo, B. Chattopadhyaya, S. J. Kuhlman et al., “Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity,” Nature Neuroscience, vol. 10, no. 12, pp. 1569–1577, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Benani, C. Hryhorczuk, A. Gouazé, et al., “Food intake adaptation to dietary fat involves PSA-dependent rewiring of the arcuate melanocortin system in mice,” The Journal of Neuroscience, vol. 32, no. 35, pp. 11970–11979, 2012.
  52. G. Lluri, G. D. Langlois, P. D. Soloway, and D. M. Jaworski, “Tissue inhibitor of metalloproteinase-2 (TIMP-2) regulates myogenesis and β1 integrin expression in vitro,” Experimental Cell Research, vol. 314, no. 1, pp. 11–24, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Gray, G. S. H. Yeo, J. J. Cox et al., “Hyperphagia, severe obesity, impaired cognitive function, and hyperactivity associated with functional loss of one copy of the brain-derived neurotrophic factor (BDNF) gene,” Diabetes, vol. 55, no. 12, pp. 3366–3371, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. B. Xu, E. H. Goulding, K. Zang et al., “Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor,” Nature Neuroscience, vol. 6, no. 7, pp. 736–742, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. C. A. Altar and P. S. Distefano, “Neurotrophin trafficking by anterograde transport,” Trends in Neurosciences, vol. 21, no. 10, pp. 433–437, 1998. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Barco, S. Patterson, J. M. Alarcon et al., “Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture,” Neuron, vol. 48, no. 1, pp. 123–137, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Cordeira and M. Rios, “Weighing in the role of BDNF in the central control of eating behavior,” Molecular Neurobiology, vol. 44, no. 3, pp. 441–448, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. L. Minichiello, A. M. Calella, D. L. Medina, T. Bonhoeffer, R. Klein, and M. Korte, “Mechanism of TrkB-mediated hippocampal long-term potentiation,” Neuron, vol. 36, no. 1, pp. 121–137, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. J.-S. Mu, W.-P. Li, Z.-B. Yao, and X.-F. Zhou, “Deprivation of endogenous brain-derived neurotrophic factor results in impairment of spatial learning and memory in adult rats,” Brain Research, vol. 835, no. 2, pp. 259–265, 1999. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Bartoletti, L. Cancedda, S. W. Reid et al., “Heterozygous knock-out mice for brain-derived neurotrophic factor show a pathway-specific impairment of long-term potentiation but normal critical period for monocular deprivation,” The Journal of Neuroscience, vol. 22, no. 23, pp. 10072–10077, 2002. View at Scopus
  61. L. Cancedda, E. Putignano, A. Sale, A. Viegi, N. Berardi, and L. Maffei, “Acceleration of visual system development by environmental enrichment,” The Journal of Neuroscience, vol. 24, no. 20, pp. 4840–4848, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Sale, J. F. Maya Vetencourt, P. Medini et al., “Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition,” Nature Neuroscience, vol. 10, no. 6, pp. 679–681, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. L. Cao, X. Liu, E.-J. D. Lin et al., “Environmental and genetic activation of a brain-adipocyte BDNF/leptin axis causes cancer remission and inhibition,” Cell, vol. 142, no. 1, pp. 52–64, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Stanley, S. Pinto, J. Segal et al., “Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 15, pp. 7024–7029, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. L. Cao, E. Y. Choi, X. Liu et al., “White to brown fat phenotypic switch induced by genetic and environmental activation of a hypothalamic-adipocyte axis,” Cell Metabolism, vol. 14, no. 3, pp. 324–338, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. M. A. Cowley, J. L. Smart, M. Rubinstein et al., “Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus,” Nature, vol. 411, no. 6836, pp. 480–484, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Mainardi, S. Landi, L. Gianfranceschi et al., “Environmental enrichment potentiates thalamocortical transmission and plasticity in the adult rat visual cortex,” Journal of Neuroscience Research, vol. 88, no. 14, pp. 3048–3059, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. M. V. Kokoeva, H. Yin, and J. S. Flier, “Neurogenesis in the hypothalamus of adult mice: potential role in energy balance,” Science, vol. 310, no. 5748, pp. 679–683, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Brown, C. M. Cooper-Kuhn, G. Kempermann et al., “Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis,” European Journal of Neuroscience, vol. 17, no. 10, pp. 2042–2046, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. Z. B. Yu, S. P. Han, X. G. Cao, and X. R. Guo, “Intelligence in relation to obesity: a systematic review and meta-analysis,” Obesity Reviews, vol. 11, no. 9, pp. 656–670, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. J. G. Mercer, N. Hoggard, L. M. Williams, C. B. Lawrence, L. T. Hannah, and P. Trayhurn, “Localization of leptin receptor mRNA and the long form splice variant (Ob-Rb) in mouse hypothalamus and adjacent brain regions by in situ hybridization,” FEBS Letters, vol. 387, no. 2-3, pp. 113–116, 1996. View at Scopus
  72. C. A. Grillo, G. G. Piroli, A. N. Evans et al., “Obesity/hyperleptinemic phenotype adversely affects hippocampal plasticity: effects of dietary restriction,” Physiology and Behavior, vol. 104, no. 2, pp. 235–241, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. Morikawa, E. Ueyama, and E. Senba, “Fasting-induced activation of mitogen-activated protein kinases (ERK/p38) in the mouse hypothalamus,” Journal of Neuroendocrinology, vol. 16, no. 2, pp. 105–112, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Davis and S. Laroche, “Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: a review,” Genes, Brain and Behavior, vol. 5, supplement 2, pp. 61–72, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. G. Di Cristo, N. Berardi, L. Cancedda et al., “Requirement of ERK activation for visual cortical plasticity,” Science, vol. 292, no. 5525, pp. 2337–2340, 2001. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Spolidoro, L. Baroncelli, E. Putignano, J. F. Maya-Vetencourt, A. Viegi, and L. Maffei, “Food restriction enhances visual cortex plasticity in adulthood,” Nature Communications, vol. 2, no. 1, article 320, 2011. View at Publisher · View at Google Scholar · View at Scopus
  77. K. P. Kinzig, S. L. Hargrave, and E. E. Tao, “Central and peripheral effects of chronic food restriction and weight restoration in the rat,” American Journal of Physiology, vol. 296, no. 2, pp. E282–E290, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. A. V. Witte, M. Fobker, R. Gellner, S. Knecht, and A. Flöel, “Caloric restriction improves memory in elderly humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 4, pp. 1255–1260, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. G. J. Paz-Filho, T. Babikian, R. Asarnow et al., “Leptin replacement improves cognitive development,” PLoS ONE, vol. 3, no. 8, Article ID e3098, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. X.-L. Li, S. Aou, Y. Oomura, N. Hori, K. Fukunaga, and T. Hori, “Impairment of long-term potentiation and spatial memory in leptin receptor-deficient rodents,” Neuroscience, vol. 113, no. 3, pp. 607–615, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. J. C. Garza, M. Guo, W. Zhang, and X.-Y. Lu, “Leptin increases adult hippocampal neurogenesis in vivo and in vitro,” The Journal of Biological Chemistry, vol. 283, no. 26, pp. 18238–18247, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Caleo and L. Maffei, “Neurotrophins and plasticity in the visual cortex,” Neuroscientist, vol. 8, no. 1, pp. 52–61, 2002. View at Scopus
  83. K. K. Cowansage, J. E. Ledoux, and M.-H. Monfils, “Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity,” Current Molecular Pharmacology, vol. 3, no. 1, pp. 12–29, 2010. View at Scopus