An integrated serotonin and octopamine neuronal circuit directs the release of an endocrine signal to control C. Elegans body fat

Cell Metabolism

Volumn 18, Issue 5, 2013, Pages 672-684

  Noble, Tallie ^a   Stieglitz, Jonathan ^a   Srinivasan, Supriya ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; OCTOPAMINE; SEROTONIN; TRIACYLGLYCEROL LIPASE;

ADIPOCYTE; ADRENERGIC ACTIVITY; ARTICLE; BODY FAT; CAENORHABDITIS ELEGANS; FAT CONTENT; FOOD INTAKE; LIPID HYDROLYSIS; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEROTONINERGIC NERVE CELL; SIGNAL TRANSDUCTION; WEIGHT REDUCTION;

CAENORHABDITIS ELEGANS; INVERTEBRATA;

ADIPOSE TISSUE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHLORIDE CHANNELS; ENDOCRINE SYSTEM; LIPOLYSIS; MODELS, BIOLOGICAL; NEURONS; OCTOPAMINE; OLFACTORY NERVE; SEROTONIN; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84887449305     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.09.007     Document Type: Article

References (55)

1. M.J. Alkema, M. Hunter-Ensor, N. Ringstad, and H.R. Horvitz Tyramine Functions independently of octopamine in the Caenorhabditis elegans nervous system Neuron 46 2005 247 260
2. H.E. Arda, S. Taubert, L.T. MacNeil, C.C. Conine, B. Tsuda, M. Van Gilst, R. Sequerra, L. Doucette-Stamm, K.R. Yamamoto, and A.J.M. Walhout Functional modularity of nuclear hormone receptors in a Caenorhabditis elegans metabolic gene regulatory network Mol. Syst. Biol. 6 2010 367
3. K. Ashrafi, F.Y. Chang, J.L. Watts, A.G. Fraser, R.S. Kamath, J. Ahringer, and G. Ruvkun Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes Nature 421 2003 268 272
4. C.I. Bargmann Chemosensation in C. Elegans WormBook 2006 1 29
5. S. Brenner The genetics of Caenorhabditis elegans Genetics 77 1974 71 94
6. P. Chakrabarti, T. English, S. Karki, L. Qiang, R. Tao, J. Kim, Z. Luo, S.R. Farmer, and K.V. Kandror SIRT1 controls lipolysis in adipocytes via FOXO1-mediated expression of ATGL J. Lipid Res. 52 2011 1693 1701
7. E.W. Chan, Y. He, C.S. Chui, A.Y. Wong, W.C. Lau, and I.C. Wong Efficacy and safety of lorcaserin in obese adults: a meta-analysis of 1-year randomized controlled trials (RCTs) and narrative review on short-term RCTs Obes. Rev. 14 2013 383 392
8. A.J. Chang, N. Chronis, D.S. Karow, M.A. Marletta, and C.I. Bargmann A distributed chemosensory circuit for oxygen preference in C. Elegans PLoS Biol. 4 2006 e274
9. D.L. Chase, and M.R. Koelle Biogenic amine neurotransmitters in C. Elegans WormBook 2007 1 15
10. B.H. Cheung, M. Cohen, C. Rogers, O. Albayram, and M. de Bono Experience-dependent modulation of C. Elegans behavior by ambient oxygen Curr. Biol. 15 2005 905 917
11. G.E. Cuellar, A.M. Ruiz, M.C. Monsalve, and A. Berber Six-month treatment of obesity with sibutramine 15 mg; a double-blind, placebo-controlled monocenter clinical trial in a Hispanic population Obes. Res. 8 2000 71 82
12. K.A. Cunningham, Z. Hua, S. Srinivasan, J. Liu, B.H. Lee, R.H. Edwards, and K. Ashrafi AMP-activated kinase links serotonergic signaling to glutamate release for regulation of feeding behavior in C. Elegans Cell Metab. 16 2012 113 121
13. G. Fanghänel, L. Cortinas, L. Sánchez-Reyes, and A. Berber A clinical trial of the use of sibutramine for the treatment of patients suffering essential obesity Int. J. Obes. Relat. Metab. Disord. 24 2000 144 150
14. P. Germain, P. Chambon, G. Eichele, R.M. Evans, M.A. Lazar, M. Leid, A.R. De Lera, R. Lotan, D.J. Mangelsdorf, and H. Gronemeyer International Union of Pharmacology. LXIII. Retinoid X receptors Pharmacol. Rev. 58 2006 760 772
15. M.D. Gershon 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract Curr. Opin. Endocrinol. Diabetes Obes. 20 2013 14 21
16. J.M. Gray, D.S. Karow, H. Lu, A.J. Chang, J.S. Chang, R.E. Ellis, M.A. Marletta, and C.I. Bargmann Oxygen sensation and social feeding mediated by a C. Elegans guanylate cyclase homologue Nature 430 2004 317 322
17. J.M. Gray, J.J. Hill, and C.I. Bargmann A circuit for navigation in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 102 2005 3184 3191
18. E.R. Greer, C.L. Pérez, M.R. Van Gilst, B.H. Lee, and K. Ashrafi Neural and molecular dissection of a C. Elegans sensory circuit that regulates fat and feeding Cell Metab. 8 2008 118 131
19. H.I. Ha, M. Hendricks, Y. Shen, C.V. Gabel, C. Fang-Yen, Y. Qin, D. Colón-Ramos, K. Shen, A.D. Samuel, and Y. Zhang Functional organization of a neural network for aversive olfactory learning in Caenorhabditis elegans Neuron 68 2010 1173 1186
20. G.P. Harris, V.M. Hapiak, R.T. Wragg, S.B. Miller, L.J. Hughes, R.J. Hobson, R. Steven, B. Bamber, and R.W. Komuniecki Three distinct amine receptors operating at different levels within the locomotory circuit are each essential for the serotonergic modulation of chemosensation in Caenorhabditis elegans J. Neurosci. 29 2009 1446 1456
21. K.T. Jones, E.R. Greer, D. Pearce, and K. Ashrafi Rictor/TORC2 regulates Caenorhabditis elegans fat storage, body size, and development through sgk-1 PLoS Biol. 7 2009 e60
22. E.E. Kershaw, M. Schupp, H.P. Guan, N.P. Gardner, M.A. Lazar, and J.S. Flier PPARgamma regulates adipose triglyceride lipase in adipocytes in vitro and in vivo Am. J. Physiol. Endocrinol. Metab. 293 2007 E1736 E1745
23. D. Kong, Q. Tong, C. Ye, S. Koda, P.M. Fuller, M.J. Krashes, L. Vong, R.S. Ray, D.P. Olson, and B.B. Lowell GABAergic RIP-Cre neurons in the arcuate nucleus selectively regulate energy expenditure Cell 151 2012 645 657
24. J. Liu, T. Li, D. Yang, R. Ma, T.H. Moran, and W.W. Smith Synphilin-1 alters metabolic homeostasis in a novel Drosophila obesity model Int J Obes (Lond) 36 2012 1529 1536
25. M. Lu, D.A. Sarruf, S. Talukdar, S. Sharma, P. Li, G. Bandyopadhyay, S. Nalbandian, W. Fan, J.R. Gayen, and S.K. Mahata Brain PPAR-γ promotes obesity and is required for the insulin-sensitizing effect of thiazolidinediones Nat. Med. 17 2011 618 622
26. S.M. Maguire, C.M. Clark, J. Nunnari, J.K. Pirri, and M.J. Alkema The C. Elegans touch response facilitates escape from predacious fungi Curr. Biol. 21 2011 1326 1330
27. H.Y. Mak Lipid droplets as fat storage organelles in Caenorhabditis elegans: Thematic Review Series: Lipid Droplet Synthesis and Metabolism: from Yeast to Man J. Lipid Res. 53 2012 28 33
28. D.J. Mangelsdorf, and R.M. Evans The RXR heterodimers and orphan receptors Cell 83 1995 841 850
29. H. Mills, R. Wragg, V. Hapiak, M. Castelletto, J. Zahratka, G. Harris, P. Summers, A. Korchnak, W. Law, B. Bamber, and R. Komuniecki Monoamines and neuropeptides interact to inhibit aversive behaviour in Caenorhabditis elegans EMBO J. 31 2012 667 678
30. C.A. Mok, M.P. Healey, T. Shekhar, M.R. Leroux, E. Héon, and M. Zhen Mutations in a guanylate cyclase GCY-35/GCY-36 modify Bardet-Biedl syndrome-associated phenotypes in Caenorhabditis elegans PLoS Genet. 7 2011 e1002335
31. S.D. Narasimhan, K. Yen, A. Bansal, E.S. Kwon, S. Padmanabhan, and H.A. Tissenbaum PDP-1 links the TGF-β and IIS pathways to regulate longevity, development, and metabolism PLoS Genet. 7 2011 e1001377
32. K. Nonogaki New insights into sympathetic regulation of glucose and fat metabolism Diabetologia 43 2000 533 549
33. K. Nonogaki, L. Abdallah, E.H. Goulding, S.J. Bonasera, and L.H. Tecott Hyperactivity and reduced energy cost of physical activity in serotonin 5-HT(2C) receptor mutant mice Diabetes 52 2003 315 320
34. E.J. O'Rourke, P. Kuballa, R. Xavier, and G. Ruvkun ω-6 Polyunsaturated fatty acids extend life span through the activation of autophagy Genes Dev. 27 2013 429 440
35. C.L. Perez, and M.R. Van Gilst A 13C isotope labeling strategy reveals the influence of insulin signaling on lipogenesis in C. Elegans Cell Metab. 8 2008 266 274
36. R. Ranganathan, S.C. Cannon, and H.R. Horvitz MOD-1 is a serotonin-gated chloride channel that modulates locomotory behaviour in C. Elegans Nature 408 2000 470 475
37. N. Ringstad, N. Abe, and H.R. Horvitz Ligand-gated chloride channels are receptors for biogenic amines in C. Elegans Science 325 2009 96 100
38. T. Roeder Tyramine and octopamine: ruling behavior and metabolism Annu. Rev. Entomol. 50 2005 447 477
39. A. Sagasti, O. Hobert, E.R. Troemel, G. Ruvkun, and C.I. Bargmann Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4 Genes Dev. 13 1999 1794 1806
40. B.M. Song, and L. Avery Serotonin activates overall feeding by activating two separate neural pathways in Caenorhabditis elegans J. Neurosci. 32 2012 1920 1931
41. S. Srinivasan, L. Sadegh, I.C. Elle, A.G. Christensen, N.J. Faergeman, and K. Ashrafi Serotonin regulates C. Elegans fat and feeding through independent molecular mechanisms Cell Metab. 7 2008 533 544
42. T.A. Starich, J. Xu, I.M. Skerrett, B.J. Nicholson, and J.E. Shaw Interactions between innexins UNC-7 and UNC-9 mediate electrical synapse specificity in the Caenorhabditis elegans locomotory nervous system Neural Dev. 4 2009 16
43. J.Y. Sze, M. Victor, C. Loer, Y. Shi, and G. Ruvkun Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant Nature 403 2000 560 564
44. P.S. Talbot, S. Bradley, C.P. Clarke, K.O. Babalola, A.W. Philipp, G. Brown, A.W. McMahon, and J.C. Matthews Brain serotonin transporter occupancy by oral sibutramine dosed to steady state: a PET study using (11)C-DASB in healthy humans Neuropsychopharmacology 35 2010 741 751
45. E.R. Troemel, B.E. Kimmel, and C.I. Bargmann Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. Elegans Cell 91 1997 161 169
46. A.K. Walker, R.L. Jacobs, J.L. Watts, V. Rottiers, K. Jiang, D.M. Finnegan, T. Shioda, M. Hansen, F. Yang, and L.J. Niebergall A conserved SREBP-1/phosphatidylcholine feedback circuit regulates lipogenesis in metazoans Cell 147 2011 840 852
47. J.G. White, E. Southgate, J.N. Thomson, and S. Brenner The structure of the nervous system of the nematode Caenorhabditis elegans Philos. Trans. R. Soc. Lond. B Biol. Sci. 314 1986 1 340
48. S.D. Wise Clinical studies with fluoxetine in obesity Am. J. Clin. Nutr. 55 Suppl 1992 181S 184S
49. D. Wong, K. Sullivan, and G. Heap The pharmaceutical market for obesity therapies Nat. Rev. Drug Discov. 11 2012 669 670
50. V.K. Yadav, J.-H. Ryu, N. Suda, K.F. Tanaka, J.A. Gingrich, G. Schütz, F.H. Glorieux, C.Y. Chiang, J.D. Zajac, and K.L. Insogna Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum Cell 135 2008 825 837
51. V.K. Yadav, F. Oury, N. Suda, Z.W. Liu, X.B. Gao, C. Confavreux, K.C. Klemenhagen, K.F. Tanaka, J.A. Gingrich, and X.E. Guo A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure Cell 138 2009 976 989
52. K. Yen, T.T. Le, A. Bansal, S.D. Narasimhan, J.X. Cheng, and H.A. Tissenbaum A comparative study of fat storage quantitation in nematode Caenorhabditis elegans using label and label-free methods PLoS ONE 5 2010 5
53. Y. Zhang, H. Lu, and C.I. Bargmann Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans Nature 438 2005 179 184
54. X. Zheng, S. Chung, T. Tanabe, and J.Y. Sze Cell-type specific regulation of serotonergic identity by the C. Elegans LIM-homeodomain factor LIM-4 Dev. Biol. 286 2005 618 628
55. R. Zimmermann, J.G. Strauss, G. Haemmerle, G. Schoiswohl, R. Birner-Gruenberger, M. Riederer, A. Lass, G. Neuberger, F. Eisenhaber, A. Hermetter, and R. Zechner Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase Science 306 2004 1383 1386