Hunger states switch a flip-flop memory circuit via a synaptic AMPK-dependent positive feedback loop

Cell

Volumn 146, Issue 6, 2011, Pages 992-1003

  Yang, Yunlei ^a   Atasoy, Deniz ^a   Su, Helen H ^a   Sternson, Scott M ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; GHRELIN; LEPTIN; PROOPIOMELANOCORTIN;

ARTICLE; CELL TYPE; ELECTROPHYSIOLOGY; FOOD DEPRIVATION; HORMONE RELEASE; HUNGER; HYSTERESIS; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PHOTOSTIMULATION; POSITIVE FEEDBACK; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SYNAPTIC POTENTIAL;

EID: 80052922112     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.07.039     Document Type: Article

References (49)

1. K.A. Anderson, T.J. Ribar, F. Lin, P.K. Noeldner, M.F. Green, M.J. Muehlbauer, L.A. Witters, B.E. Kemp, and A.R. Means Hypothalamic CaMKK2 contributes to the regulation of energy balance Cell Metab. 7 2008 377 388 (Pubitemid 351598022)
2. Z.B. Andrews, Z.W. Liu, N. Walllingford, D.M. Erion, E. Borok, J.M. Friedman, M.H. Tschöp, M. Shanabrough, G. Cline, and G.I. Shulman UCP2 mediates ghrelin's action on NPY/AgRP neurons by lowering free radicals Nature 454 2008 846 851
3. Y. Aponte, D. Atasoy, and S.M. Sternson AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training Nat. Neurosci. 14 2011 351 355
4. S.M. Appleyard, M. Hayward, J.I. Young, A.A. Butler, R.D. Cone, M. Rubinstein, and M.J. Low A role for the endogenous opioid beta-endorphin in energy homeostasis Endocrinology 144 2003 1753 1760 (Pubitemid 36543312)
5. D. Atasoy, Y. Aponte, H.H. Su, and S.M. Sternson A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping J. Neurosci. 28 2008 7025 7030
6. U.S. Bhalla, and R. Iyengar Emergent properties of networks of biological signaling pathways Science 283 1999 381 387
7. A. Boelen, J. Kwakkel, X.G. Vos, W.M. Wiersinga, and E. Fliers Differential effects of leptin and refeeding on the fasting-induced decrease of pituitary type 2 deiodinase and thyroid hormone receptor beta2 mRNA expression in mice J. Endocrinol. 190 2006 537 544 (Pubitemid 44307819)
8. E.S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth Millisecond-timescale, genetically targeted optical control of neural activity Nat. Neurosci. 8 2005 1263 1268 (Pubitemid 43348147)
9. W.B. Cannon Organization for physiological homeostasis Physiol. Rev. 9 1929 399 431
10. J.M. Corton, J.G. Gillespie, S.A. Hawley, and D.G. Hardie 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur. J. Biochem. 229 1995 558 565
11. M.A. Cowley, J.L. Smart, M. Rubinstein, M.G. Cerdán, S. Diano, T.L. Horvath, R.D. Cone, and M.J. Low Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus Nature 411 2001 480 484 (Pubitemid 32494394)
12. M.A. Cowley, R.G. Smith, S. Diano, M. Tschöp, N. Pronchuk, K.L. Grove, C.J. Strasburger, M. Bidlingmaier, M. Esterman, and M.L. Heiman The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis Neuron 37 2003 649 661 (Pubitemid 36262986)
13. J. DeFalco, M. Tomishima, H. Liu, C. Zhao, X. Cai, J.D. Marth, L. Enquist, and J.M. Friedman Virus-assisted mapping of neural inputs to a feeding center in the hypothalamus Science 291 2001 2608 2613 (Pubitemid 32249686)
14. L.E. Dobrunz, and C.F. Stevens Heterogeneity of release probability, facilitation, and depletion at central synapses Neuron 18 1997 995 1008 (Pubitemid 27274617)
15. N.J. Emptage, C.A. Reid, and A. Fine Calcium stores in hippocampal synaptic boutons mediate short-term plasticity, store-operated Ca2+ entry, and spontaneous transmitter release Neuron 29 2001 197 208 (Pubitemid 32108732)
16. K. Endo, and H. Yawo mu-Opioid receptor inhibits N-type Ca2+ channels in the calyx presynaptic terminal of the embryonic chick ciliary ganglion J. Physiol. 524 2000 769 781 (Pubitemid 30303624)
17. A.M. Evans, K.J. Mustard, C.N. Wyatt, C. Peers, M. Dipp, P. Kumar, N.P. Kinnear, and D.G. Hardie Does AMP-activated protein kinase couple inhibition of mitochondrial oxidative phosphorylation by hypoxia to calcium signaling in O2-sensing cells? J. Biol. Chem. 280 2005 41504 41511 (Pubitemid 41832211)
18. P. Fatt, and B. Katz Spontaneous subthreshold activity at motor nerve endings J. Physiol. 117 1952 109 128
19. J.E. Ferrell Jr. Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability Curr. Opin. Cell Biol. 14 2002 140 148 (Pubitemid 34219501)
20. G.R. Gordon, and J.S. Bains Can homeostatic circuits learn and remember? J. Physiol. 576 2006 341 347 (Pubitemid 44490130)
21. L. Grandison, and A. Guidotti Stimulation of food intake by muscimol and beta endorphin Neuropharmacology 16 1977 533 536 (Pubitemid 8138715)
22. T.M. Hahn, J.F. Breininger, D.G. Baskin, and M.W. Schwartz Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons Nat. Neurosci. 1 1998 271 272 (Pubitemid 128652670)
23. S.A. Hawley, D.A. Pan, K.J. Mustard, L. Ross, J. Bain, A.M. Edelman, B.G. Frenguelli, and D.G. Hardie Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase Cell Metab. 2 2005 9 19 (Pubitemid 43239821)
24. S.A. Holm A simple sequentially rejective multiple test procedure Scand. J. Stat. 6 1979 65 70
25. B. Holst, A. Cygankiewicz, T.H. Jensen, M. Ankersen, and T.W. Schwartz High constitutive signaling of the ghrelin receptor - identification of a potent inverse agonist Mol. Endocrinol. 17 2003 2201 2210 (Pubitemid 37352532)
26. P. Horowitz, and W. Hill The Art of Electronics Second Edition 1989 Cambridge University Press Cambridge, UK
27. A.D. Howard, S.D. Feighner, D.F. Cully, J.P. Arena, P.A. Liberator, C.I. Rosenblum, M. Hamelin, D.L. Hreniuk, O.C. Palyha, and J. Anderson A receptor in pituitary and hypothalamus that functions in growth hormone release Science 273 1996 974 977 (Pubitemid 26275178)
28. R.L. Hurley, K.A. Anderson, J.M. Franzone, B.E. Kemp, A.R. Means, and L.A. Witters The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases J. Biol. Chem. 280 2005 29060 29066 (Pubitemid 41161355)
29. D.E. Koshland Jr., A. Goldbeter, and J.B. Stock Amplification and adaptation in regulatory and sensory systems Science 217 1982 220 225 (Pubitemid 12091224)
30. C. Li, P. Chen, and M.S. Smith Identification of neuronal input to the arcuate nucleus (ARH) activated during lactation: implications in the activation of neuropeptide Y neurons Brain Res. 824 1999 267 276 (Pubitemid 29225533)
31. M. López, R. Lage, A.K. Saha, D. Pérez-Tilve, M.J. Vázquez, L. Varela, S. Sangiao-Alvarellos, S. Tovar, K. Raghay, and S. Rodríguez-Cuenca Hypothalamic fatty acid metabolism mediates the orexigenic action of ghrelin Cell Metab. 7 2008 389 399 (Pubitemid 351618114)
32. S. Luquet, C.T. Phillips, and R.D. Palmiter NPY/AgRP neurons are not essential for feeding responses to glucoprivation Peptides 28 2007 214 225 (Pubitemid 46176250)
33. T. Martiáñez, S. Francs, and J.M. López Generation of digital responses in stress sensors J. Biol. Chem. 284 2009 23902 23911
34. Y. Minokoshi, T. Alquier, N. Furukawa, Y.B. Kim, A. Lee, B. Xue, J. Mu, F. Foufelle, P. Ferré, and M.J. Birnbaum AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus Nature 428 2004 569 574 (Pubitemid 38480541)
35. M. Nakazato, N. Murakami, Y. Date, M. Kojima, H. Matsuo, K. Kangawa, and S. Matsukura A role for ghrelin in the central regulation of feeding Nature 409 2001 194 198 (Pubitemid 32144284)
36. S. Pinto, A.G. Roseberry, H. Liu, S. Diano, M. Shanabrough, X. Cai, J.M. Friedman, and T.L. Horvath Rapid rewiring of arcuate nucleus feeding circuits by leptin Science 304 2004 110 115 (Pubitemid 38451468)
37. R.M. Silva, M.M. Hadjimarkou, G.C. Rossi, G.W. Pasternak, and R.J. Bodnar Beta-endorphin-induced feeding: pharmacological characterization using selective opioid antagonists and antisense probes in rats J. Pharmacol. Exp. Ther. 297 2001 590 596 (Pubitemid 32377989)
38. R.G. Smith Development of growth hormone secretagogues Endocr. Rev. 26 2005 346 360 (Pubitemid 40686648)
39. S.M. Sternson, G.M. Shepherd, and J.M. Friedman Topographic mapping of VMH - > arcuate nucleus microcircuits and their reorganization by fasting Nat. Neurosci. 8 2005 1356 1363 (Pubitemid 41630424)
40. K.A. Takahashi, and R.D. Cone Fasting induces a large, leptin-dependent increase in the intrinsic action potential frequency of orexigenic arcuate nucleus neuropeptide Y/Agouti-related protein neurons Endocrinology 146 2005 1043 1047 (Pubitemid 40289293)
41. K. Tanaka, and G.J. Augustine A positive feedback signal transduction loop determines timing of cerebellar long-term depression Neuron 59 2008 608 620
42. M. Tschöp, D.L. Smiley, and M.L. Heiman Ghrelin induces adiposity in rodents Nature 407 2000 908 913
43. A. Woods, K. Dickerson, R. Heath, S.P. Hong, M. Momcilovic, S.R. Johnstone, M. Carlson, and D. Carling Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells Cell Metab. 2 2005 21 33 (Pubitemid 43239822)
44. J.M. Zigman, J.E. Jones, C.E. Lee, C.B. Saper, and J.K. Elmquist Expression of ghrelin receptor mRNA in the rat and the mouse brain J. Comp. Neurol. 494 2006 528 548 (Pubitemid 41791000)
45. Balthasar, N., Coppari, R., McMinn, J., Liu, S.M., Lee, C.E., Tang, V., Kenny, C.D., McGovern, R.A., Chua, S.C., Jr., Elmquist, J.K., and Lowell, B.B. (2004). Leptin receptor signaling in POMC neurons is required for normal body weight homeostasis. Neuron 42, 983-991. (Pubitemid 38798236)
46. Kaelin, C.B., Xu, A.W., Lu, X.Y., and Barsh, G.S. (2004). Transcriptional regulation of agouti-related protein (Agrp) in transgenic mice. Endocrinology 145, 5798-5806. (Pubitemid 39564621)
47. 2+i via AMPK in hypothalamic arcuate nucleus NPY neurons. Biochem. Biophys. Res. Commun. 366, 388-392. (Pubitemid 50010409)
48. Pinto, S., Roseberry, A.G., Liu, H., Diano, S., Shanabrough, M., Cai, X., Friedman, J.M., and Horvath, T.L. (2004). Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304, 110-115. (Pubitemid 38451468)
49. Tian, L., Hires, S.A., Mao, T., Huber, D., Chiappe, M.E., Chalasani, S.H., Petreanu, L., Akerboom, J., McKinney, S.A., Schreiter, E.R., et al. (2009). Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875-881.