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Science 304 (5667): 110-115

Copyright © 2004 by the American Association for the Advancement of Science

Rapid Rewiring of Arcuate Nucleus Feeding Circuits by Leptin

Shirly Pinto,1* Aaron G. Roseberry,1* Hongyan Liu,1* Sabrina Diano,3 Marya Shanabrough,3 Xiaoli Cai,1,2 Jeffrey M. Friedman,1,2{dagger} Tamas L. Horvath3,4{dagger}

Abstract: The fat-derived hormone leptin regulates energy balance in part by modulating the activity of neuropeptide Y and proopiomelanocortin neurons in the hypothalamic arcuate nucleus. To study the intrinsic activity of these neurons and their responses to leptin, we generated mice that express distinct green fluorescent proteins in these two neuronal types. Leptin-deficient (ob/ob) mice differed from wild-type mice in the numbers of excitatory and inhibitory synapses and postsynaptic currents onto neuropeptide Y and proopiomelanocortin neurons. When leptin was delivered systemically to ob/ob mice, the synaptic density rapidly normalized, an effect detectable within 6 hours, several hours before leptin's effect on food intake. These data suggest that leptin-mediated plasticity in the ob/ob hypothalamus may underlie some of the hormone's behavioral effects.

1 Laboratory of Molecular Genetics, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.
2 Howard Hughes Medical Institute, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.
3 Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale University School of Medicine, New Haven, CT 06520, USA.
4 Department of Neurobiology, Yale University School of Medicine, New Haven, CT 06520, USA.

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* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: friedj{at}mail.rockefeller.edu (J.M.F.); tamas.horvath{at}yale.edu (T.L.H.)

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J. Biol. Chem. 281, 12950-12958
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Tamoxifen-Induced Anorexia Is Associated With Fatty Acid Synthase Inhibition in the Ventromedial Nucleus of the Hypothalamus and Accumulation of Malonyl-CoA..
M. Lopez, C. J. Lelliott, S. Tovar, W. Kimber, R. Gallego, S. Virtue, M. Blount, M. J. Vazquez, N. Finer, T. J. Powles, et al. (2006)
Diabetes 55, 1327-1336
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Altered sleep regulation in leptin-deficient mice.
A. D. Laposky, J. Shelton, J. Bass, C. Dugovic, N. Perrino, and F. W. Turek (2006)
Am J Physiol Regulatory Integrative Comp Physiol 290, R894-R903
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Cybernetic principles in the systematic concept of hypothalamic feeding control.
O. Fricke, G. Lehmkuhl, and D. W Pfaff (2006)
Eur. J. Endocrinol. 154, 167-173
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Ventromedial Arcuate Nucleus Communicates Peripheral Metabolic Information to the Suprachiasmatic Nucleus.
C.-X. Yi, J. van der Vliet, J. Dai, G. Yin, L. Ru, and R. M. Buijs (2006)
Endocrinology 147, 283-294
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Peptide YY3-36 Inhibits Both Anorexigenic Proopiomelanocortin and Orexigenic Neuropeptide Y Neurons: Implications for Hypothalamic Regulation of Energy Homeostasis.
C. Acuna-Goycolea and A. N. van den Pol (2005)
J. Neurosci. 25, 10510-10519
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Neurogenesis in the Hypothalamus of Adult Mice: Potential Role in Energy Balance.
M. V. Kokoeva, H. Yin, and J. S. Flier (2005)
Science 310, 679-683
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NPY/AgRP Neurons Are Essential for Feeding in Adult Mice but Can Be Ablated in Neonates.
S. Luquet, F. A. Perez, T. S. Hnasko, and R. D. Palmiter (2005)
Science 310, 683-685
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Hitting the Target: Leptin and Perinatal Nutrition in the Predisposition to Obesity.
M. G. Myers Jr., M. E. Patti, and R. L. Leshan (2005)
Endocrinology 146, 4209-4210
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Deoxyribonucleic Acid Microarray Analysis of Gene Expression Pattern in the Arcuate Nucleus/Ventromedial Nucleus of Hypothalamus during Lactation.
X. Q. Xiao, K. L. Grove, S. Y. Lau, S. McWeeney, and M. S. Smith (2005)
Endocrinology 146, 4391-4398
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Embracing Complexity, Inching Closer to Reality.
E. E. Schadt, A. Sachs, and S. Friend (2005)
Sci. STKE 2005, pe40
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Anorexia and Cachexia in Renal Failure--Is Leptin the Culprit?: Role of Leptin and Melanocortin Signaling in Uremia-Associated Cachexia. J Clin Invest 115: 1659-1665, 2005.
C. W, Y. PX, L. BM, C. RD, M. DL, M. RH, I. H, O. MH, W. K, B.-J. K, et al. (2005)
J. Am. Soc. Nephrol. 16, 2245-2250
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Nutritional Epigenomics of Metabolic Syndrome: New Perspective Against the Epidemic.
C. Gallou-Kabani and C. Junien (2005)
Diabetes 54, 1899-1906
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Plasma leptin and ghrelin in the neonatal rat: interaction of dexamethasone and hypoxia.
E. D Bruder, L. Jacobson, and H. Raff (2005)
J. Endocrinol. 185, 477-484
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Effect of Leptin Replacement on Brain Structure in Genetically Leptin-Deficient Adults.
J. A. Matochik, E. D. London, B. O. Yildiz, M. Ozata, S. Caglayan, A. M. DePaoli, M.-L. Wong, and J. Licinio (2005)
J. Clin. Endocrinol. Metab. 90, 2851-2854
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Use of Laser-Capture Microdissection for the Identification of Marker Genes for the Ventromedial Hypothalamic Nucleus.
J. P. Segal, N. R. Stallings, C. E. Lee, L. Zhao, N. Socci, A. Viale, T. M. Harris, M. B. Soares, G. Childs, J. K. Elmquist, et al. (2005)
J. Neurosci. 25, 4181-4188
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Deletion of the RII{beta}-Subunit of Protein Kinase A Decreases Body Weight and Increases Energy Expenditure in the Obese, Leptin-Deficient ob/ob Mouse.
K. J. Newhall, D. E. Cummings, M. A. Nolan, and G. S. McKnight (2005)
Mol. Endocrinol. 19, 982-991
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