Nutrient Sensor in the Brain Directs the Action of the Brain-Gut Axis in Drosophila

Neuron

Volumn 87, Issue 1, 2015, Pages 139-151

  Dus, Monica ^a,c   Lai, Jason Sih Yu ^a   Gunapala, Keith M ^a   Min, Soohong ^a   Tayler, Timothy D ^b   Hergarden, Anne C ^b   Geraud, Eliot ^a   Joseph, Christina M ^a   Suh, Greg S B ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CELL RECEPTOR; DIURETIC HORMONE 44; DIURETIC HORMONE 44 RECEPTOR 1; HEXOKINASE; NUTRITIVE SWEETENER; SUGAR; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; DIURETIC HORMONE 44 RECEPTOR 1, DROSOPHILA; DIURETIC HORMONE 44 RECEPTOR 2, DROSOPHILA; DROME-DH(44) PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; FRUCTOSE; GLUCOSE; INSECT HORMONE; TREHALOSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOSENSOR; BRAIN CELL; BRAIN REGION; CELL ACTIVATION; CONTROLLED STUDY; DROSOPHILA; HEMOLYMPH; INTESTINE MOTILITY; MALE; NEUROSECRETORY CELL; NONHUMAN; NUTRIENT SENSOR; PARS INTERCEREBRALIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REINFORCEMENT; ANIMAL; BRAIN; DRUG EFFECTS; FEEDING BEHAVIOR; METABOLISM; NERVE CELL; NEUROSECRETION; PHYSIOLOGY; SENSORY FEEDBACK;

ANIMALS; BRAIN; DROSOPHILA; DROSOPHILA PROTEINS; FEEDBACK, SENSORY; FEEDING BEHAVIOR; FRUCTOSE; GLUCOSE; INSECT HORMONES; NEURONS; NEUROSECRETION; NUTRITIVE SWEETENERS; RECEPTORS, CELL SURFACE; TREHALOSE;

EID: 84937514728     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.05.032     Document Type: Article

References (57)

1. Ai M., Min S., Grosjean Y., Leblanc C., Bell R., Benton R., Suh G.S. Acid sensing by the Drosophila olfactory system. Nature 2010, 468:691-695.
2. Anand B.K., Chhina G.S., Sharma K.N., Dua S., Singh B. Activity of Single Neurons in the Hypothalamic Feeding Centers: Effect of Glucose. Am. J. Physiol. 1964, 207:1146-1154.
3. Audsley N., Goldsworthy G.J., Coast G.M. Circulating levels of Locusta diuretic hormone: the effects of feeding. Peptides 1997, 18:59-65.
4. Birch L.L., McPhee L., Steinberg L., Sullivan S. Conditioned flavor preferences in young children. Physiol. Behav. 1990, 47:501-505.
5. Brunstrom J.M., Mitchell G.L. Flavor-nutrient learning in restrained and unrestrained eaters. Physiol. Behav. 2007, 90:133-141.
6. Burke C.J., Waddell S. Remembering nutrient quality of sugar in Drosophila. Curr. Biol. 2011, 21:746-750.
7. Chiang A.S., Lin C.Y., Chuang C.C., Chang H.M., Hsieh C.H., Yeh C.W., Shih C.T., Wu J.J., Wang G.T., Chen Y.C., et al. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr. Biol. 2011, 21:1-11.
8. Claret M., Smith M.A., Batterham R.L., Selman C., Choudhury A.I., Fryer L.G., Clements M., Al-Qassab H., Heffron H., Xu A.W., et al. AMPK is essential for energy homeostasis regulation and glucose sensing by POMC and AgRP neurons. J. Clin. Invest. 2007, 117:2325-2336.
9. de Araujo I.E., Oliveira-Maia A.J., Sotnikova T.D., Gainetdinov R.R., Caron M.G., Nicolelis M.A., Simon S.A. Food reward in the absence of taste receptor signaling. Neuron 2008, 57:930-941.
10. de Araujo I.E., Lin T., Veldhuizen M.G., Small D.M. Metabolic regulation of brain response to food cues. Curr. Biol. 2013, 23:878-883.
11. de Velasco B., Erclik T., Shy D., Sclafani J., Lipshitz H., McInnes R., Hartenstein V. Specification and development of the pars intercerebralis and pars lateralis, neuroendocrine command centers in the Drosophila brain. Dev. Biol. 2007, 302:309-323.
12. Domingos A.I., Sordillo A., Dietrich M.O., Liu Z.W., Tellez L.A., Vaynshteyn J., Ferreira J.G., Ekstrand M.I., Horvath T.L., de Araujo I.E., Friedman J.M. Hypothalamic melanin concentrating hormone neurons communicate the nutrient value of sugar. eLife 2013, 2:e01462.
13. Dunn-Meynell A.A., Sanders N.M., Compton D., Becker T.C., Eiki J., Zhang B.B., Levin B.E. Relationship among brain and blood glucose levels and spontaneous and glucoprivic feeding. J. Neurosci. 2009, 29:7015-7022.
14. Dus M., Min S., Keene A.C., Lee G.Y., Suh G.S. Taste-independent detection of the caloric content of sugar in Drosophila. Proc. Natl. Acad. Sci. USA 2011, 108:11644-11649.
15. Dus M., Ai M., Suh G.S. Taste-independent nutrient selection is mediated by a brain-specific Na+ /solute co-transporter in Drosophila. Nat. Neurosci. 2013, 16:526-528.
16. Fujita M., Tanimura T. Drosophila evaluates and learns the nutritional value of sugars. Curr. Biol. 2011, 21:751-755.
17. Gelbart, W.M., and Emmert, D.B. (2013). FlyBase high throughput expression pattern data. ModENCODE. http://flybase.org/reports/FBrf0212041.html.
18. George S.A., Khan S., Briggs H., Abelson J.L. CRH-stimulated cortisol release and food intake in healthy, non-obese adults. Psychoneuroendocrinology 2010, 35:607-612.
19. Gordon M.D., Manzo A., Scott K. Fly neurobiology: development and function of the brain. Meeting on the Neurobiology of Drosophila. EMBO Rep. 2008, 9:239-242.
20. Hector C.E., Bretz C.A., Zhao Y., Johnson E.C. Functional differences between two CRF-related diuretic hormone receptors in Drosophila. J. Exp. Biol. 2009, 212:3142-3147.
21. Iaboni A., Holman G.M., Nachman R.J., Orchard I., Coast G.M. Immunocytochemical localisation and biological activity of diuretic peptides in the housefly, Musca domestica. Cell Tissue Res. 1998, 294:549-560.
22. Johnson E.C., Bohn L.M., Barak L.S., Birse R.T., Nässel D.R., Caron M.G., Taghert P.H. Identification of Drosophila neuropeptide receptors by G protein-coupled receptors-beta-arrestin2 interactions. J. Biol. Chem. 2003, 278:52172-52178.
23. Kang L., Routh V.H., Kuzhikandathil E.V., Gaspers L.D., Levin B.E. Physiological and molecular characteristics of rat hypothalamic ventromedial nucleus glucosensing neurons. Diabetes 2004, 53:549-559.
24. Kong D., Vong L., Parton L.E., Ye C., Tong Q., Hu X., Choi B., Brüning J.C., Lowell B.B. Glucose stimulation of hypothalamic MCH neurons involves K(ATP) channels, is modulated by UCP2, and regulates peripheral glucose homeostasis. Cell Metab. 2010, 12:545-552.
25. Lenzen S., Freytag S., Panten U. Inhibition of glucokinase by alloxan through interaction with SH groups in the sugar-binding site of the enzyme. Mol. Pharmacol. 1988, 34:395-400.
26. Levin B.E. Neuronal glucose sensing: still a physiological orphan?. Cell Metab. 2007, 6:252-254.
27. Lovejoy D.A., Jahan S. Phylogeny of the corticotropin-releasing factor family of peptides in the metazoa. Gen. Comp. Endocrinol. 2006, 146:1-8.
28. Manzo A., Silies M., Gohl D.M., Scott K. Motor neurons controlling fluid ingestion in Drosophila. Proc. Natl. Acad. Sci. USA 2012, 109:6307-6312.
29. Mather P., Nicolaidis S., Booth D.A. Compensatory and conditioned feeding responses to scheduled glucose infusions in the rat. Nature 1978, 273:461-463.
30. Mayer J. Glucostatic mechanism of regulation of food intake. N. Engl. J. Med. 1953, 249:13-16.
31. McCrimmon R.J., Song Z., Cheng H., McNay E.C., Weikart-Yeckel C., Fan X., Routh V.H., Sherwin R.S. Corticotrophin-releasing factor receptors within the ventromedial hypothalamus regulate hypoglycemia-induced hormonal counterregulation. J. Clin. Invest. 2006, 116:1723-1730.
32. Minokoshi Y., Alquier T., Furukawa N., Kim Y.B., Lee A., Xue B., Mu J., Foufelle F., Ferré P., Birnbaum M.J., et al. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 2004, 428:569-574.
33. Miselis R.R., Epstein A.N. Feeding induced by intracerebroventricular 2-deoxy-D-glucose in the rat. Am. J. Physiol. 1975, 229:1438-1447.
34. Miyamoto T., Slone J., Song X., Amrein H. A fructose receptor functions as a nutrient sensor in the Drosophila brain. Cell 2012, 151:1113-1125.
35. Musso P.Y., Tchenio P., Preat T. Delayed dopamine signaling of energy level builds appetitive long-term memory in Drosophila. Cell Rep. 2015, 10:1023-1031.
36. Nitabach M.N., Blau J., Holmes T.C. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 2002, 109:485-495.
37. Nitabach M.N., Sheeba V., Vera D.A., Blau J., Holmes T.C. Membrane electrical excitability is necessary for the free-running larval Drosophila circadian clock. J. Neurobiol. 2005, 62:1-13.
38. Oliveira-Maia A.J., Roberts C.D., Walker Q.D., Luo B., Kuhn C., Simon S.A., Nicolelis M.A. Intravascular food reward. PLoS ONE 2011, 6:e24992.
39. Oomura Y., Kimura K., Ooyama H., Maeno T., Iki M., Kuniyoshi M. Reciprocal activities of the ventromedial and lateral hypothalamic areas of cats. Science 1964, 143:484-485.
40. Parisky K.M., Agosto J., Pulver S.R., Shang Y., Kuklin E., Hodge J.J., Kang K., Liu X., Garrity P.A., Rosbash M., Griffith L.C. PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 2008, 60:672-682.
41. Parton L.E., Ye C.P., Coppari R., Enriori P.J., Choi B., Zhang C.Y., Xu C., Vianna C.R., Balthasar N., Lee C.E., et al. Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity. Nature 2007, 449:228-232.
42. Ren X., Ferreira J.G., Zhou L., Shammah-Lagnado S.J., Yeckel C.W., de Araujo I.E. Nutrient selection in the absence of taste receptor signaling. J. Neurosci. 2010, 30:8012-8023.
43. Richard D., Lin Q., Timofeeva E. The corticotropin-releasing factor family of peptides and CRF receptors: their roles in the regulation of energy balance. Eur. J. Pharmacol. 2002, 440:189-197.
44. Routh V.H. Glucose sensing neurons in the ventromedial hypothalamus. Sensors (Basel) 2010, 10:9002-9025.
45. Sclafani A., Ackroff K. Role of gut nutrient sensing in stimulating appetite and conditioning food preferences. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 302:R1119-R1133.
46. Stafford J.W., Lynd K.M., Jung A.Y., Gordon M.D. Integration of taste and calorie sensing in Drosophila. J. Neurosci. 2012, 32:14767-14774.
47. Tache Y., Perdue M.H. Role of peripheral CRF signalling pathways in stress-related alterations of gut motility and mucosal function. Neurogastroenterol. Motil. 2004, 16(Suppl. 1):137-142.
48. Talsma A.D., Christov C.P., Terriente-Felix A., Linneweber G.A., Perea D., Wayland M., Shafer O.T., Miguel-Aliaga I. Remote control of renal physiology by the intestinal neuropeptide pigment-dispersing factor in Drosophila. Proc. Natl. Acad. Sci. USA 2012, 109:12177-12182.
49. Thorner M.O., Holl R.W., Leong D.A. The somatotrope: an endocrine cell with functional calcium transients. J. Exp. Biol. 1988, 139:169-179.
50. Tordoff M.G., Friedman M.I. Hepatic portal glucose infusions decrease food intake and increase food preference. Am. J. Physiol. 1986, 251:R192-R196.
51. Wang J., Ma X., Yang J.S., Zheng X., Zugates C.T., Lee C.H., Lee T. Transmembrane/juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 2004, 43:663-672.
52. Waterhouse A.M., Procter J.B., Martin D.M., Clamp M., Barton G.J. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25:1189-1191.
53. Yarmolinsky D.A., Zuker C.S., Ryba N.J. Common sense about taste: from mammals to insects. Cell 2009, 139:234-244.
54. Yeomans M.R., Leitch M., Gould N.J., Mobini S. Differential hedonic, sensory and behavioral changes associated with flavor-nutrient and flavor-flavor learning. Physiol. Behav. 2008, 93:798-806.
55. Zhang Y.Q., Rodesch C.K., Broadie K. Living synaptic vesicle marker: synaptotagmin-GFP. Genesis 2002, 34:142-145.
56. Zitnan D., Sehnal F., Bryant P.J. Neurons producing specific neuropeptides in the central nervous system of normal and pupariation-delayed Drosophila. Dev. Biol. 1993, 156:117-135.
57. Zukerman S., Ackroff K., Sclafani A. Post-oral appetite stimulation by sugars and nonmetabolizable sugar analogs. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 305:R840-R853.