In Silico Molecular Comparisons of C. elegans and Mammalian Pharmacology Identify Distinct Targets That Regulate Feeding

PLoS Biology

Volumn 11, Issue 11, 2013, Pages

  Lemieux, George A ^a   Keiser, Michael J ^b,c   Sassano, Maria F ^d   Laggner, Christian ^c   Mayer, Fahima ^c   Bainton, Roland J ^c   Werb, Zena ^a   Roth, Bryan L ^d   Shoichet, Brian K ^c   Ashrafi, Kaveh ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SeaChange Pharmaceuticals Inc   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B16; D20 (DRUG); F15; H6; HORMONE RECEPTOR BLOCKING AGENT; METABOTROPIC RECEPTOR ANTAGONIST; PROTEIN TYROSINE KINASE INHIBITOR; TACHYKININ RECEPTOR ANTAGONIST; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CAENORHABDITIS ELEGANS; COMPARATIVE STUDY; COMPUTER MODEL; DRUG SCREENING; DRUG TARGETING; EPISTASIS; FEEDING; FEEDING BEHAVIOR; IN VITRO STUDY; IN VIVO STUDY; INFORMATION SCIENCE; MAMMAL; NONHUMAN;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; COMPUTER SIMULATION; DRUG EVALUATION, PRECLINICAL; FEEDING BEHAVIOR; HUMANS; PERISTALSIS; PHARYNX; PHENOTYPE; QUINOLINES; RECEPTORS, G-PROTEIN-COUPLED; SMALL MOLECULE LIBRARIES;

EID: 84889010695     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001712     Document Type: Article

References (64)

1. Keiser MJ, Irwin JJ, Shoichet BK, (2010) The chemical basis of pharmacology. Biochemistry 49: 10267-10276.
2. Ahlquist RP, (1948) A study of the adrenotropic receptors. Am J Physiol 153: 586-600.
3. Black JW, Duncan WA, Durant CJ, Ganellin CR, Parsons EM, (1972) Definition and antagonism of histamine H 2-receptors. Nature 236: 385-390.
4. Gilbert PE, Martin WR, (1976) The effects of morphine and nalorphine-like drugs in the nondependent, morphine-dependent and cyclazocine-dependent chronic spinal dog. J Pharmacol Exp Ther 198: 66-82.
5. Richardson BP, Engel G, Donatsch P, Stadler PA, (1985) Identification of serotonin M-receptor subtypes and their specific blockade by a new class of drugs. Nature 316: 126-131.
6. Elphick GF, Querbes W, Jordan JA, Gee GV, Eash S, et al. (2004) The human polyomavirus, JCV, uses serotonin receptors to infect cells. Science 306: 1380-1383.
7. Huang H-S, Allen JA, Mabb AM, King IF, Miriyala J, et al. (2012) Topoisomerase inhibitors unsilence the dormant allele of Ube3a in neurons. Nature 481: 185-189.
8. Sachlos E, Risueno RM, Laronde S, Shapovalova Z, Lee JH, et al. (2012) Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell 149: 1284-1297.
9. Williams KW, Elmquist JK, (2012) From neuroanatomy to behavior: central integration of peripheral signals regulating feeding behavior. Nat Neurosci 15: 1350-1355.
10. Kwok TC, Ricker N, Fraser R, Chan AW, Burns A, et al. (2006) A small-molecule screen in C. elegans yields a new calcium channel antagonist. Nature 441: 91-95.
11. Lemieux GA, Liu J, Mayer N, Bainton RJ, Ashrafi K, et al. (2011) A whole-organism screen identifies new regulators of fat storage. Nat Chem Biol 7: 206-213.
12. Luciani GM, Magomedova L, Puckrin R, Urbanus ML, Wallace IM, et al. (2011) Dafadine inhibits DAF-9 to promote dauer formation and longevity of Caenorhabditis elegans. Nat Chem Biol 7: 891-893.
13. Min J, Kyung Kim Y, Cipriani PG, Kang M, Khersonsky SM, et al. (2007) Forward chemical genetic approach identifies new role for GAPDH in insulin signaling. Nat Chem Biol 3: 55-59.
14. Moy TI, Conery AL, Larkins-Ford J, Wu G, Mazitschek R, et al. (2009) High-throughput screen for novel antimicrobials using a whole animal infection model. ACS Chem Biol 4: 527-533.
15. Avery L, You YJ, (2012) C. elegans feeding. WormBook pp. 1-23.
16. Avery L, (1993) The genetics of feeding in Caenorhabditis elegans. Genetics 133: 897-917.
17. Avery L, Horvitz HR, (1990) Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. Journal of Experimental Zoology 253: 263-270.
18. You Y-j, Kim J, Cobb M, Avery L, (2006) Starvation activates MAP kinase through the muscarinic acetylcholine pathway in Caenorhabditis elegans pharynx. Cell Metabolism 3: 237-245.
19. Shtonda BB, Avery L, (2006) Dietary choice behavior in Caenorhabditis elegans. J Exp Biol 209: 89-102.
20. You Y-j, Kim J, Raizen DM, Avery L, (2008) Insulin, cGMP, and TGF-β signals regulate food intake and quiescence in C. elegans: a model for satiety. Cell Metabolism 7: 249-257.
21. Song BM, Avery L, (2012) Serotonin activates overall feeding by activating two separate neural pathways in Caenorhabditis elegans. J Neurosci 32: 1920-1931.
22. Rogers CM, Franks CJ, Walker RJ, Burke JF, Holden-Dye L, (2001) Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides. J Neurobiol 49: 235-244.
23. Greer ER, Perez CL, Van Gilst MR, Lee BH, Ashrafi K, (2008) Neural and molecular dissection of a C. elegans sensory circuit that regulates fat and feeding. Cell Metab 8: 118-131.
24. Li Z, Li Y, Yi Y, Huang W, Yang S, et al. (2012) Dissecting a central flip-flop circuit that integrates contradictory sensory cues in C. elegans feeding regulation. Nat Commun 3: 776.
25. Lee RY, Sawin ER, Chalfie M, Horvitz HR, Avery L, (1999) EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in caenorhabditis elegans. J Neurosci 19: 159-167.
26. Cunningham KA, Hua Z, Srinivasan S, Liu J, Lee BH, et al. (2012) AMP-activated kinase links serotonergic signaling to glutamate release for regulation of feeding behavior in C. elegans. Cell Metab 16: 113-121.
27. Srinivasan S, Sadegh L, Elle IC, Christensen AG, Faergeman NJ, et al. (2008) Serotonin regulates C. elegans fat and feeding through independent molecular mechanisms. Cell Metab 7: 533-544.
28. Chen W, Zhang C, Song L, Sommerfeld M, Hu Q, (2009) A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae. J Microbiol Methods 77: 41-47.
29. Flynn EJ, (2009) Ontogeny and nutritional control of adipogenesis in zebrafish (Danio rerio). J Lipid Res 50: 1641-1652.
30. Greenspan P, Mayer EP, Fowler SD, (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100: 965-973.
31. Jones KS, Alimov AP, Rilo HL, Jandacek RJ, Woollett LA, et al. (2008) A high throughput live transparent animal bioassay to identify non-toxic small molecules or genes that regulate vertebrate fat metabolism for obesity drug development. Nutr Metab (Lond) 5: 23.
32. Siloto RM, Truksa M, He X, McKeon T, Weselake RJ, (2009) Simple methods to detect triacylglycerol biosynthesis in a yeast-based recombinant system. Lipids 44(10): 963-973.
33. Brooks KK, Liang B, Watts JL, (2009) The influence of bacterial diet on fat storage in C. elegans. PLoS ONE 4: e7545 doi:10.1371/journal.pone.0007545.
34. O'Rourke EJ, Soukas AA, Carr CE, Ruvkun G, (2009) C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell Metab 10: 430-435.
35. Yen K, Le TT, Bansal A, Narasimhan SD, Cheng JX, et al. (2010) A comparative study of fat storage quantitation in nematode Caenorhabditis elegans using label and label-free methods. PLoS ONE 5 (9) ():: pii: e12810 doi:10.1371/journal.pone.0012810.
36. Zhang SO, Trimble R, Guo F, Mak HY, (2010) Lipid droplets as ubiquitous fat storage organelles in C. elegans. BMC Cell Biol 11: 96.
37. Keiser MJ, Setola V, Irwin JJ, Laggner C, Abbas AI, et al. (2009) Predicting new molecular targets for known drugs relating protein pharmacology by ligand chemistry. Nature 462: 175-181.
38. Laggner C, Kokel D, Setola V, Tolia A, Lin H, et al. (2012) Chemical informatics and target identification in a zebrafish phenotypic screen. Nat Chem Biol 8: 144-146.
39. Keiser MJ, Roth BL, Armbruster BN, Ernsberger P, Irwin JJ, et al. (2007) Relating protein pharmacology by ligand chemistry. Nat Biotechnol 25: 197-206.
40. Lin H, Sassano MF, Roth BL, Shoichet BK, (2013) A pharmacological organization of G protein-coupled receptors. Nat Methods 10: 140-146.
41. Lounkine E, Keiser MJ, Whitebread S, Mikhailov D, Hamon J, et al. (2012) Large-scale prediction and testing of drug activity on side-effect targets. Nature 486: 361-367.
42. Schessl C, Rawat VP, Cusan M, Deshpande A, Kohl TM, et al. (2005) The AML1-ETO fusion gene and the FLT3 length mutation collaborate in inducing acute leukemia in mice. J Clin Invest 115: 2159-2168.
43. Fire A, (1999) RNA-triggered gene silencing. Trends Genet 15: 358-363.
44. Choi SJ, Moon MJ, Lee SD, Choi S-U, Han S-Y, et al. (2010) Indirubin derivatives as potent FLT3 inhibitors with anti-proliferative activity of acute myeloid leukemic cells. Bioorganic & Medicinal Chemistry Letters 20: 2033-2037.
45. Gaetani S, Fu J, Cassano T, Dipasquale P, Romano A, et al. (2010) The fat-induced satiety factor oleoylethanolamide suppresses feeding through central release of oxytocin. J Neurosci 30: 8096-8101.
46. Zhang G, Bai H, Zhang H, Dean C, Wu Q, et al. (2011) Neuropeptide exocytosis involving synaptotagmin-4 and oxytocin in hypothalamic programming of body weight and energy balance. Neuron 69: 523-535.
47. Atasoy D, Betley JN, Su HH, Sternson SM, (2012) Deconstruction of a neural circuit for hunger. Nature 488: 172-177.
48. Williams PD, Clineschmidt BV, Erb JM, Freidinger RM, Guidotti MT, et al. (1995) 1-(1-[4-[(N-acetyl-4-piperidinyl)oxy]-2-methoxybenzoyl]piperidin-4- yl)-4H-3,1-benzoxazin-2(1H)-one (L-371,257): a new, orally bioavailable, non-peptide oxytocin antagonist. J Med Chem 38: 4634-4636.
49. Garrison JL, Macosko EZ, Bernstein S, Pokala N, Albrecht DR, et al. (2012) Oxytocin/vasopressin-related peptides have an ancient role in reproductive behavior. Science 338: 540-543.
50. Beets I, Janssen T, Meelkop E, Temmerman L, Suetens N, et al. (2012) Vasopressin/oxytocin-related signaling regulates gustatory associative learning in C. elegans. Science 338: 543-545.
51. Dillon J, Hopper NA, Holden-Dye L, O'Connor V, (2006) Molecular characterization of the metabotropic glutamate receptor family in Caenorhabditis elegans. Biochem Soc Trans 34: 942-948.
52. Kang C, Avery L, (2009) Systemic regulation of starvation response in Caenorhabditis elegans. Genes Dev 23: 12-17.
53. Suzuki G, Tsukamoto N, Fushiki H, Kawagishi A, Nakamura M, et al. (2007) In vitro pharmacological characterization of novel isoxazolopyridone derivatives as allosteric metabotropic glutamate receptor 7 antagonists. J Pharmacol Exp Ther 323: 147-156.
54. Cong F, Cheung AK, Huang SM, (2012) Chemical genetics-based target identification in drug discovery. Annu Rev Pharmacol Toxicol 52: 57-78.
55. Olszewski PK, Klockars A, Schioth HB, Levine AS, (2010) Oxytocin as feeding inhibitor: maintaining homeostasis in consummatory behavior. Pharmacol Biochem Behav 97: 47-54.
56. Tachibana T, Khan MS, Matsuda K, Ueda H, Cline MA, (2010) Central administration of substance P inhibits feeding behavior in chicks. Horm Behav 57: 203-208.
57. Sasaki K, Oomura Y, Suzuki K, Muto T, Hanai K, et al. (1991) Effects of fibroblast growth factors and platelet-derived growth factor on food intake in rats. Brain Res Bull 27: 327-332.
58. Hert J, Irwin JJ, Laggner C, Keiser MJ, Shoichet BK, (2009) Quantifying biogenic bias in screening libraries. Nat Chem Biol 5: 479-483.
59. Rogers D, Hahn M, (2010) Extended-connectivity fingerprints. J Chem Inf Model 50: 742-754.
60. Roth BL, Baner K, Westkaemper R, Siebert D, Rice KC, et al. (2002) Salvinorin A: a potent naturally occurring nonnitrogenous κ opioid selective agonist. Proc Natl Acad Sci U S A 99: 11934-11939.
61. Shi Q, Savage JE, Hufeisen SJ, Rauser L, Grajkowska E, et al. (2003) l-homocysteine sulfinic acid and other acidic homocysteine derivatives are potent and selective metabotropic glutamate receptor agonists. Journal of Pharmacology and Experimental Therapeutics 305: 131-142.
62. Jensen NH, Rodriguiz RM, Caron MG, Wetsel WC, Rothman RB, et al. (2008) N-desalkylquetiapine, a potent norepinephrine reuptake inhibitor and partial 5-HT1A agonist, as a putative mediator of quetiapine's antidepressant activity. Neuropsychopharmacology 33: 2303-2312.
63. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
64. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, et al. (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421: 268-272.