Dopamine signaling regulates fat content through β-oxidation in Caenorhabditis elegans

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  De Barros, Alexandre Guimarães Almeida ^a   Bridi, Jessika Cristina ^a   De Souza, Bruno Rezende ^a   De Júnior, Célio Castro ^a   De Lima Torres, Karen Cecília ^a   Malard, Leandro ^a   Jorio, Ado ^a   De Miranda, Débora Marques ^a   Ashrafi, Kaveh ^b   Romano Silva, Marco Aurélio ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR; CAENORHABDITIS ELEGANS PROTEIN; DOPAMINE RECEPTOR STIMULATING AGENT; FAT; SEROTONIN; SEROTONIN AGONIST;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DOPAMINERGIC TRANSMISSION; ENERGY METABOLISM; FAT CONTENT; FATTY ACID OXIDATION; LIPID ANALYSIS; LIPID STORAGE; METABOLIC REGULATION; NONHUMAN; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENETICS; HOMEOSTASIS; LIPID METABOLISM; METABOLISM; MUTATION; OXIDATION REDUCTION REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TIME;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DOPAMINE; DOPAMINE AGENTS; ENERGY METABOLISM; FATS; GENE EXPRESSION; HOMEOSTASIS; LIPID METABOLISM; MICROSCOPY, FLUORESCENCE; MUTATION; OXIDATION-REDUCTION; RECEPTORS, DOPAMINE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SEROTONIN; SEROTONIN RECEPTOR AGONISTS; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84899805654     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085874     Document Type: Article

References (63)

1. Flegal KM, Carroll MD, Ogden CL, Curtin LR (2010) Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303: 235-241. 2009.2014 [pii];10.1001/jama.2009.2014 [doi].
2. Gallant P, Malutan T, McLean H, Verellen L, Caveney S, et al. (2003) Functionally distinct dopamine and octopamine transporters in the CNS of the cabbage looper moth. Eur J Biochem 270: 664-674. 3417 [pii].
3. Berthoud HR, Morrison C (2008) The brain, appetite, and obesity. Annu Rev Psychol 59: 55-92. 10.1146/annurev.psych.59.103006.093551 [doi].
4. Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW (2006) Central nervous system control of food intake and body weight. Nature 443: 289-295. nature05026 [pii];10.1038/nature05026 [doi].
5. Szczypka MS, Rainey MA, Kim DS, Alaynick WA, Marck BT, et al. (1999) Feeding behavior in dopamine-deficient mice. Proc Natl Acad Sci U S A 96: 12138-12143. (Pubitemid 29502871)
6. Zhou QY, Palmiter RD (1995) Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell 83: 1197-1209. 0092-8674(95)90145-0 [pii].
7. DiLeone RJ (2009) The influence of leptin on the dopamine system and implications for ingestive behavior. Int J Obes (Lond) 33 Suppl 2: S25-S29. ijo200968 [pii];10.1038/ijo.2009.68 [doi].
8. Palmiter RD (2007) Is dopamine a physiologically relevant mediator of feeding behavior? Trends Neurosci 30: 375-381. S0166-2236(07)00133-6 [pii];10.1016/j.tins.2007.06.004 [doi].
9. Fulton S, Pissios P, Manchon RP, Stiles L, Frank L, et al. (2006) Leptin regulation of the mesoaccumbens dopamine pathway. Neuron 51: 811-822. S0896-6273(06)00686-6 [pii];10.1016/j.neuron.2006.09.006 [doi].
10. Szczypka MS, Rainey MA, Palmiter RD (2000) Dopamine is required for hyperphagia in Lep(ob/ob) mice. Nat Genet 25: 102-104. 10.1038/75484 [doi]. (Pubitemid 30257046)
11. Wang GJ, Volkow ND, Logan J, Pappas NR, Wong CT, et al. (2001) Brain dopamine and obesity. Lancet 357: 354-357. S0140673600036436 [pii].
12. Stice E, Spoor S, Bohon C, Small DM (2008) Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 322: 449-452. 322/5900/449 [pii];10.1126/science.1161550 [doi].
13. 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. 10.1038/nature01279 [doi];nature01279 [pii].
14. Mullaney BC, Ashrafi K (2009) C. elegans fat storage and metabolic regulation. Biochim Biophys Acta 1791: 474-478. S1388-1981(08)00241-2 [pii];10.1016/j.bbalip.2008.12.013 [doi].
15. 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. S1550-4131(08)00144-7 [pii];10.1016/j.cmet.2008.04.012 [doi].
16. Cohen M, Reale V, Olofsson B, Knights A, Evans P, et al. (2009) Coordinated regulation of foraging and metabolism in C. elegans by RFamide neuropeptide signaling. Cell Metab 9: 375-385. S1550-4131(09)00041-2 [pii];10.1016/j.cmet.2009.02.003 [doi].
17. Sawin ER, Ranganathan R, Horvitz HR (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26: 619-631. S0896-6273(00)81199-X [pii].
18. Sulston J, Dew M, Brenner S (1975) Dopaminergic neurons in the nematode Caenorhabditis elegans. J Comp Neurol 163: 215-226. 10.1002/cne.901630207 [doi].
19. Nass R, Blakely RD (2003) The Caenorhabditis elegans dopaminergic system: opportunities for insights into dopamine transport and neurodegeneration. Annu Rev Pharmacol Toxicol 43: 521-544. 10.1146/annurev.pharmtox.43.100901.135934 [doi];100901.135934 [pii].
20. Chase DL, Pepper JS, Koelle MR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7: 1096-1103. 10.1038/nn1316 [doi];nn1316 [pii].
21. Hills T, Brockie PJ, Maricq AV (2004) Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J Neurosci 24: 1217-1225. 10.1523/JNEUROSCI.1569-03.2004 [doi];24/5/1217 [pii].
22. Ezcurra M, Tanizawa Y, Swoboda P, Schafer WR (2011) Food sensitizes C. elegans avoidance behaviours through acute dopamine signalling. EMBO J 30: 1110-1122. emboj201122 [pii];10.1038/emboj.2011.22 [doi].
23. Kimura KD, Fujita K, Katsura I (2010) Enhancement of odor avoidance regulated by dopamine signaling in Caenorhabditis elegans. J Neurosci 30: 16365-16375. 30/48/16365 [pii];10.1523/JNEUROSCI.6023-09.2010 [doi].
24. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
25. Barros AG, Liu J, Lemieux GA, Mullaney BC, Ashrafi K (2012) Analyses of C. elegans fat metabolic pathways. Methods Cell Biol 107: 383-407. B978-0-12-394620-1.00013-8 [pii];10.1016/B978-0-12-394620-1.00013-8 [doi].
26. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2: RESEARCH0002.
27. Potma EO, Xie XS (2008) Coherent Anti-Stokes Raman Scattering (CARS) Microscopy: Instrumentation and Applications. In: Barry R.Masters, Peter T.C.So, editors. Handbook of Biomedical Nonlinear Optical Microscopy. New York: Oxford University Press. pp. 164-186.
28. Wang MC, Min W, Freudiger CW, Ruvkun G, Xie XS (2011) RNAi screening for fat regulatory genes with SRS microscopy. Nat Methods 8: 135-138. nmeth.1556 [pii];10.1038/nmeth.1556 [doi].
29. Hellerer T, Axang C, Brackmann C, Hillertz P, Pilon M, et al. (2007) Monitoring of lipid storage in Caenorhabditis elegans using coherent anti-Stokes Raman scattering (CARS) microscopy. Proc Natl Acad Sci U S A 104: 14658-14663. 0703594104 [pii];10.1073/pnas.0703594104 [doi].
30. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
31. Van Gilst MR, Hadjivassiliou H, Jolly A, Yamamoto KR (2005) Nuclear hormone receptor NHR-49 controls fat consumption and fatty acid composition in C. elegans. PLoS Biol 3: e53. 10.1371/journal.pbio.0030053 [doi].
32. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108. (Pubitemid 351818697)
33. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
34. Allen AT, Maher KN, Wani KA, Betts KE, Chase DL (2011) Coexpressed D1-and D2-like dopamine receptors antagonistically modulate acetylcholine release in Caenorhabditis elegans. Genetics 188: 579-590. genetics.111.128512 [pii];10.1534/genetics.111.128512 [doi].
35. 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. S1550-4131(08)00144-7 [pii];10.1016/j.cmet.2008.04.012 [doi].
36. Jones KT, Greer ER, Pearce D, Ashrafi K (2009) Rictor/TORC2 regulates Caenorhabditis elegans fat storage, body size, and development through sgk-1. PLoS Biol 7: e60. 08-PLBI-RA-3327 [pii];10.1371/journal.pbio.1000060 [doi].
37. 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. S1550-4131(09)00301-5 [pii];10.1016/j.cmet.2009.10.002 [doi].
38. Brooks KK, Liang B, Watts JL (2009) The influence of bacterial diet on fat storage in C. elegans. PLoS One 4: e7545. 10.1371/journal.pone.0007545 [doi].
39. Ashrafi K (2007) Obesity and the regulation of fat metabolism. WormBook 1-20. 10.1895/wormbook.1.130.1 [doi].
40. Zhang SO, Box AC, Xu N, Le MJ, Yu J, et al. (2010) Genetic and dietary regulation of lipid droplet expansion in Caenorhabditis elegans. Proc Natl Acad Sci U S A 107: 4640-4645. 0912308107 [pii];10.1073/pnas.0912308107 [doi].
41. Hare EE, Loer CM (2004) Function and evolution of the serotonin-synthetic bas-1 gene and other aromatic amino acid decarboxylase genes in Caenorhabditis. BMC Evol Biol 4: 24. 10.1186/1471-2148-4-24 [doi];1471-2148-4-24 [pii].
42. McDonald PW, Hardie SL, Jessen TN, Carvelli L, Matthies DS, et al. (2007) Vigorous motor activity in Caenorhabditis elegans requires efficient clearance of dopamine mediated by synaptic localization of the dopamine transporter DAT-1. J Neurosci 27: 14216-14227. 27/51/14216 [pii];10.1523/JNEUROSCI. 2992-07.2007 [doi].
43. Sanyal S, Wintle RF, Kindt KS, Nuttley WM, Arvan R, et al. (2004) Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans. EMBO J 23: 473-482. 10.1038/sj.emboj.7600057 [doi];7600057 [pii].
44. Suo S, Culotti JG, Van Tol HH (2009) Dopamine counteracts octopamine signalling in a neural circuit mediating food response in C. elegans. EMBO J 28: 2437-2448. emboj2009194 [pii];10.1038/emboj.2009.194 [doi].
45. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560-564. 10.1038/35000609 [doi]. (Pubitemid 30082203)
46. Cumming P (2011) Absolute abundances and affinity states of dopamine receptors in mammalian brain: A review. Synapse 65: 892-909. 10.1002/syn.20916 [doi].
47. Suo S, Sasagawa N, Ishiura S (2003) Cloning and characterization of a Caenorhabditis elegans D2-like dopamine receptor. J Neurochem 86: 869-878. 1896 [pii].
48. Sugiura M, Fuke S, Suo S, Sasagawa N, Van Tol HH, et al. (2005) Characterization of a novel D2-like dopamine receptor with a truncated splice variant and a D1-like dopamine receptor unique to invertebrates from Caenorhabditis elegans. J Neurochem 94: 1146-1157. JNC3268 [pii];10.1111/j.1471- 4159.2005.03268.x [doi].
49. Ringstad N, Abe N, Horvitz HR (2009) Ligand-gated chloride channels are receptors for biogenic amines in C. elegans. Science 325: 96-100. 325/5936/96 [pii];10.1126/science.1169243 [doi].
50. Avery L (1993) The genetics of feeding in Caenorhabditis elegans. Genetics 133: 897-917.
51. You YJ, Kim J, Raizen DM, Avery L (2008) Insulin, cGMP, and TGF-beta signals regulate food intake and quiescence in C. elegans: a model for satiety. Cell Metab 7: 249-257. S1550-4131(08)00006-5 [pii];10.1016/j.cmet.2008.01.005 [doi].
52. Weinshenker D, Garriga G, Thomas JH (1995) Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J Neurosci 15: 6975-6985.
53. Schafer WR, Kenyon CJ (1995) A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375: 73-78. 10.1038/375073a0 [doi].
54. Dempsey CM, Mackenzie SM, Gargus A, Blanco G, Sze JY (2005) Serotonin (5HT), fluoxetine, imipramine and dopamine target distinct 5HT receptor signaling to modulate Caenorhabditis elegans egg-laying behavior. Genetics 169: 1425-1436. genetics.104.032540 [pii];10.1534/genetics.104.032540 [doi].
55. Wanders RJ, Waterham HR (2006) Biochemistry of mammalian peroxisomes revisited. Annu Rev Biochem 75: 295-332. 10.1146/annurev.biochem.74.082803. 133329 [doi]. (Pubitemid 44118035)
56. 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. S1550-4131(08)00176-9 [pii];10.1016/j.cmet.2008. 06.005 [doi].
57. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277: 942-946. (Pubitemid 27366677)
58. Palmiter RD (2007) Is dopamine a physiologically relevant mediator of feeding behavior? Trends Neurosci 30: 375-381. S0166-2236(07)00133-6 [pii];10.1016/j.tins.2007.06.004 [doi].
59. Johnson PM, Kenny PJ (2010) Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13: 635-641. nn.2519 [pii];10.1038/nn.2519 [doi].
60. Nasrallah HA (2008) Atypical antipsychotic-induced metabolic side effects: insights from receptor-binding profiles. Mol Psychiatry 13: 27-35. 4002066 [pii];10.1038/sj.mp.4002066 [doi].
61. Lieberman JA, Stroup TS, McEvoy JP, Swartz MS, Rosenheck RA, et al. (2005) Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. N Engl J Med 353: 1209-1223. NEJMoa051688 [pii];10.1056/ NEJMoa051688 [doi].
62. Kok P, Roelfsema F, Frolich M, van PJ, Stokkel MP, et al. (2006) Activation of dopamine D2 receptors simultaneously ameliorates various metabolic features of obese women. Am J Physiol Endocrinol Metab 291: E1038-E1043. 00567.2005 [pii];10.1152/ajpendo.00567.2005 [doi].
63. Tseng YH, Cypess AM, Kahn CR (2010) Cellular bioenergetics as a target for obesity therapy. Nat Rev Drug Discov 9: 465-482. nrd3138 [pii];10.1038/nrd3138 [doi].