Fingerprinting of psychoactive drugs in zebrafish anxiety-like behaviors

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Maximino, Caio ^a   Da Silva, Annanda Waneza Batista ^b   Arauj́o, Juliana ^b   Lima, Monica Gomes ^a   Miranda, Vanessa ^b   Puty, Bruna ^b   Benzecry, Rancés ^b   Picanco̧ Diniz, Domingos Luiz Wanderley ^c   Gouveia Jr , Amauri ^b   Oliveira, Karen Renata Matos ^b   Herculano, Anderson Manoel ^b  

^a UNIVERSIDADE DO ESTADO DO PARÁ   (Brazil)

^b FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^c UNIVERSIDADE FEDERAL DO OESTE DO PARÁ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,6,7 TETRAHYDRO 1' METHYL 5 [[2' METHYL 4' (5 METHYL 1,2,4 OXADIAZOL 3 YL) 4 BIPHENYLYL]CARBONYL]SPIRO[FURO[2,3 F]INDOLE 3,4' PIPERIDINE]; 4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ALCOHOL; AMFEBUTAMONE; AMFEPRAMONE; ANXIOLYTIC AGENT; BENZODIAZEPINE DERIVATIVE; BUSPIRONE; CAFFEINE; CHLORDIAZEPOXIDE; CLONAZEPAM; DIAZEPAM; DIZOCILPINE; FLUOXETINE; HYPERICUM PERFORATUM EXTRACT; MOCLOBEMIDE; N METHYL DEXTRO ASPARTIC ACID; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; N(G) NITROARGININE; PSYCHOTROPIC AGENT; SEROTONIN; VERAPAMIL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; DARKNESS; DRUG DOSE COMPARISON; DRUG SCREENING; FEAR; ILLUMINATION; LOCOMOTION; NONHUMAN; PHENOTYPE; PLACE PREFERENCE; PREDICTION; PROTEIN METABOLISM; RISK ASSESSMENT; SWIMMING; ZEBRA FISH; ANIMAL; CATALEPSY; DRUG EFFECTS; DRUG THERAPY; METABOLISM;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BUSPIRONE; CAFFEINE; DIAZEPAM; DRUG EVALUATION, PRECLINICAL; FREEZING REACTION, CATALEPTIC; SEROTONIN; SWIMMING; ZEBRAFISH;

EID: 84905102303     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103943     Document Type: Article

References (65)

1. Baldwin DS, Waldman S, Allgulander C (2011) Evidence-based pharmacological treatment of generalized anxiety disorder. Int J Neuropsychopharmacol 14: 697-710. doi:10.1017/S1461145710001434.
2. Griebel G, Holmes A (2013) 50 years of hurdles and hope in anxiolytic drug discovery. Nat Rev Drug Discov 12: 667-687. doi:10.1038/nrd4075.
3. Tecott LH, Nestler EJ (2004) Neurobehavioral assessment in the information age. Nat Neurosci 7: 462-466. doi:10.1038/nn1225. (Pubitemid 38544576)
4. Crabbe JC, Morris RGM (2004) Festina lente: Late-night thoughts on high-throughput screening of mouse behavior. Nat Neurosci 7: 1175-1179. doi:10.1038/nn1343. (Pubitemid 39426233)
5. Brennand KJ, Simone A, Tran N, Gage FH (2012) Modeling psychiatric disorders at the cellular and network levels. Mol Psychiatry 17: 1239-1253. Available: http://dx.doi.org/10.1038/mp.2012.20.
6. Kokel D, Peterson RT (2008) Chemobehavioural phenomics and behaviour-based psychiatric drug discovery in the zebrafish. Briefings Funct Genomics Proteomics 7: 483-490.
7. Gottesman II, Gould TD (2003) The endophenotype concept in psychiatry: Etymology and strategic intentions. Am J Psychiatry 160: 636-645. (Pubitemid 41079594)
8. Van der Staay FJ (2006) Animal models of behavioral dysfunctions: Basic concepts and classifications, and an evaluation strategy. Brain Res Rev 52: 131-159. Available: http://www.ncbi.nlm.nih.gov/pubmed/16529820.
9. Arguello PA, Gogos JA (2006) Modeling madness in mice: One piece at a time. Neuron 52: 179-196. doi:10.1016/j.neuron.2006.09.023. (Pubitemid 44466363)
10. Gould TD, Gottesman II (2006) Psychiatric endophenotypes and the development of valid animal models. Genes, Brain Behav 5: 113-119. doi:10.1111/j.1601-183X.2005.00186.x. (Pubitemid 43344963)
11. Stewart AM, Kalueff A V (2014) Developing better and more valid animal models of brain disorders. Behav Brain Res In press.
12. Kalueff AV, Ren-Patterson RF, LaPorte JL, Murphy DL (2008) Domain interplay concept in animal models of neuropsychiatric disorders: A new strategy for high-throughput neurophenotyping research. Behav Brain Res 188: 243-249. doi:10.1016/j.bbr.2007.11.011.
13. Kari G, Rodeck U, Dicker AP (2007) Zebrafish: An emerging model system for human disease and drug discovery. Clin Pharmacol Ther 82: 70-80. doi:10.1038/sj.clpt.6100223. (Pubitemid 46944200)
14. Ahmad F, Noldus LPJJ, Tegelenbosch RAJ, Richardson MK (2012) Zebrafish embryos and larvae in behavioural assays. Behaviour 149: 1241-1281. doi:10.1163/1568539X-00003020.
15. Cachat J, Stewart A, Utterback E, Hart P, Gaikwad S, et al. (2011) Three-dimensional neurophenotyping of adult zebrafish behavior. PLoS One 6: e17597. doi:10.1371/journal.pone.0017597.
16. Zon LI, Peterson RT (2005) In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 4: 35-44. doi:10.1038/nrd1606. (Pubitemid 40109588)
17. Kalueff AV, Gebhardt M, Stewart AM, Cachat JM, Brimmer M, et al. (2013) Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond. Zebrafish 10: 70-86. doi:10.1089/zeb.2012.0861.
18. Stewart AM, Kalueff AV (2012) The developing utility of zebrafish models for cognitive enhancers research. Curr Neuropharmacol In press.
19. Nguyen M, Poudel MK, Stewart AM, Kalueff AV (2013) Skin too thin? The developing utility of zebrafish skin (neuro)pharmacology for CNS drug discovery research. Brain Res Bull 98: 145-154. doi:10.1016/j.brainresbull.2013.08.004.
20. Cachat J, Canavello P, Elegante M, Bartels B, Hart P, et al. (2010) Modeling withdrawal syndrome in zebrafish. Behav Brain Res 208: 371-376.
21. Shimada Y, Hirano M, Nishimura Y, Tanaka T (2012) A high-throughput fluorescence-based assay system for appetite-regulating gene and drug screening. PLoS One 7: e52549. doi:10.1371/journal.pone.0052549.
22. Hill AJ, Teraoka H, Heideman W, Peterson RE (2005) Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 86: 6-19. doi:10.1093/toxsci/k. (Pubitemid 41511344)
23. Gerlai R (2010) High-throughput behavioral screens: The first step towards finding genes involved in vertebrate brain function using zebrafish. Molecules 15: 2609-2622. doi:10.3390/molecules15042609.
24. Key B, Devine CA (2003) Zebrafish as an experimental model: Strategies for developmental and molecular neurobiology studies. Methods Cell Sci 25: 1-6. doi:10.1023/B:MICS.0000006849.98007.03. (Pubitemid 38094406)
25. Redfern WS, Waldron G, Winter MJ, Butler P, Holbrook M, et al. (2008) Zebrafish assays as early safety pharmacology screens: Paradigm shift or red herring? J Pharmacol Toxicol Methods 58: 110-117. doi:10.1016/j.vascn.2008.05. 006.
26. Ahmad F, Noldus LPJJ, Tegelenbosch RAJ, Richardson MK (2012) Zebrafish embryos and larvae in behavioural assays. Behaviour 149: 1241-1281. doi:10.1163/1568539X-00003020.
27. Maximino C, Herculano AM (2010) A review of monoaminergic neuropsychopharmacology in zebrafish. Zebrafish 7: 359-378. doi:10.1089/zeb. 2010.0669.
28. Norton W, Bally-Cuif L (2010) Adult zebrafish as amodel organism for behavioural genetics. BMC Neurosci 11: 90. Available: http://www.pubmedcentral. nih.gov/articlerender.fcgi?artid=2919542&tool=pmcentrez&rendertype= abstract.
29. Schilling TF (2002) Morphology of larval and adult zebrafish. In: Nüsslein-Volhard C, Dahm R, editors. Zebrafish: A Practical Approach. Oxford: Oxford University Press. 59-94.
30. Levin ED, Bencan Z, Cerutti DT (2007) Anxiolytic effects of nicotine in zebrafish. Physiol Behav 90: 54-58. doi:10.1016/j.physbeh.2006.08.026. (Pubitemid 44918005)
31. Egan RJ, Bergner CL, Hart PC, Cachat JM, Canavello PR, et al. (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 205: 38-44. doi:10.1016/j.bbr.2009.06.022.
32. Stewart A, Wu N, Cachat J, Hart P, Gaikwad S, et al. (2011) Pharmacological modulation of anxiety-like phenotypes in adult zebrafish behavioral models. Prog Neuropsychopharmacol Biol Psychiatry 35: 1421-1431. doi:10.1016/j.pnpbp.2010.11.035.
33. Blaser RE, Goldsteinholm K (2012) Depth preference in zebrafish, Danio rerio: Control by surface and substrate cues. Anim Behav 83: 953-959. doi:10.1016/j.anbehav.2012.01.014.
34. Maximino C, Silva AWB da, Gouveia A Jr, Herculano AM (2011) Pharmacological analysis of zebrafish (Danio rerio) scototaxis. Prog Neuropsychopharmacol Biol Psychiatry 35: 624-631. doi:10.1016/j.pnpbp.2011.01. 006.
35. Araujo J, Maximino C, Brito TM de, Silva AWB da, Batista E de JO, et al. (2012) Behavioral and pharmacological aspects of anxiety in the light/dark preference test. In: Kalueff A V, Stewart AM, editors. Zebrafish Protocols for Neurobehavioral Research. New York: Humana Press. doi:10.1007/978-1-61779-597-8- 14.
36. Stewart A, Maximino C, de Brito TM, Herculano AM, Gouveia A Jr, et al. (2011) Neurophenotyping of adult zebrafish using the light/dark box paradigm. In: Kalueff A V, Cachat JM, editors. Zebrafish Neurobehavioral Protocols. New York: Humana Press. 157-167. doi:10.1007/978-1-60761-953-6-13.
37. Maximino C, Brito TM, Colmanetti R, Pontes AAA, Castro HM de, et al. (2010) Parametric analyses of anxiety in zebrafish scototaxis. Behav Brain Res 210: 1-7. doi:10.1016/j.bbr.2010.01.031.
38. Maximino C (2011) Parâmetros da escototaxia como modelo comportamental de ansiedade no paulistinha (Danio rerio, Cyprinidae, Pisces) Universidade Federal do Pará. doi:10.6084/m9.figshare.928644.
39. Serra EL, Medalha CC, Mattioli R (1999) Natural preference of zebrafish (Danio rerio) for a dark environment. Brazilian J Med Biol Res 32: 1551-1553.
40. Maximino C, Brito TM De, Dias CA de M, Gouveia A Jr, Morato S (2010) Scototaxis as anxiety-like behavior in fish. Nat Protoc 5: 209-216. doi:10.1038/nprot.2009.225.
41. Rihel J, Prober DA, Arvanites A, Lam K, Zimmerman S, et al. (2010) Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science (80-) 347: 348-351. doi:10.1126/science.1183090.
42. Kokel D, Bryan J, Laggner C, White R, Cheung CYJ, et al. (2010) Rapid behavior-based identification of neuroactive small molecules in the zebrafish. Nat Chem Biol 6: 231-237. doi:10.1038/nchembio.307.
43. Stewart AM, Cachat J, Green J, Gaikwad S, Kyzar E, et al. (2013) Constructing the habituome for phenotype-driven zebrafish research. Behav Brain Res 236: 110-117. doi:10.1016/j.bbr.2012.08.026.
44. Linker A, Stewart A, Gaikwad S, Cachat JM, Elegante MF, et al. (2011) Assessing the Maximum Predictive Validity for neuropharmacological anxiety screening assays using zebrafish. In: Kalueff A V, Cachat JM, editors. Zebrafish Neurobehavioral Protocols. New York: Humana Press. 181-190.
45. Herculano AM, Maximino C (2014) Serotonergic modulation of zebrafish behavior: Towards a paradox. Prog Neuropsychopharmacol Biol Psychiatry In press. doi:10.1016/j.pnpbp.2014.03.008.
46. Papke RL, Ono F, Stokes C, Urban JM, Boyd RT (2012) The nicotinic acetylcholine receptors of zebrafish and an evaluation of pharmacological tools used for their study. Biochem Pharmacol 84: 352-365. Available: http://dx.doi.org/10.1016/j.bcp.2012.04.022.
47. Sackerman J, Donegan JJ, Cunningham CS, Nguyen NN, Lawless K, et al. (2010) Zebrafish behavior in novel environments: Effects of acute exposure to anxiolytic compounds and choice of Danio rerio line. Int J Comp Psychol 23: 43-61.
48. Norton WHJ, Stumpenhorst K, Faus-Kessler T, Folchert A, Rohner N, et al. (2011) Modulation of fgfr1a signaling in zebrafish reveals a genetic basis for the aggression-boldness syndrome. J Neurosci 31: 13796-13807. doi:10.1523/JNEUROSCI.2892-11.2011.
49. Peitsaro N, Kaslin J, Anichtchik O V, Panula P (2003) Modulation of the histaminergic system and behaviour by a-fluoromethylhistidine in zebrafish. J Neurochem 86: 432-441. doi:10.1046/j.1471-4159.2003.01850.x. (Pubitemid 36842442)
50. Cofiel LP V, Mattioli R (2009) L-histidine enhances learning in stressed zebrafish. Brazilian J Med Biol Res 42: 128-134.
51. Bencan Z, Sledge D, Levin ED (2009) Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety. Pharmacol Biochem Behav 94: 75-80. doi:10.1016/j.pbb.2009.07.009.
52. Richendrfer H, Pelkowski SD, Colwill RM, Creton R (2011) On the edge: Pharmacological evidence for anxiety-related behavior in zebrafish larvae. Behav Brain Res. doi:10.1016/j.bbr.2011.11.041.
53. Steenbergen PJ, Richardson MK, Champagne DL (2011) Patterns of avoidance behaviours in the light/dark preference test in young juvenile zebrafish: A pharmacological study. Behav Brain Res 222: 15-25. doi:10.1016/j.bbr.2011.03. 025.
54. Lau BYB, Mathur P, Gould GG, Guo S (2011) Identification of a brain center whose activity discriminates a choice behavior in zebrafish. Proc Natl Acad Sci U S A 108: 2581-2586. doi:10.1073/pnas.1018275108.
55. Stewart AM, Kalueff AV (2014) The behavioral effects of acute D9-tetrahydrocannabinol and heroin (diacetylmorphine) exposure in adult zebrafish. Brain Res 1543: 109-119. Available: http://dx.doi.org/10.1016/j. brainres.2013.11.002.
56. Connors KA, Valenti TW, Lawless K, Sackerman J, Onaivi ES, et al. (2013) Similar anxiolytic effects of agonists targeting serotonin 5-HT1A or cannabinoid CB1 receptors on zebrafish behavior in novel environments. Aquat Toxicol.
57. Investigation O (2014) Acute administration of THC impairs spatial but not associative memory function in zebrafish. Psychopharmacology (Berl) In press. doi:10.1007/s00213-014-3522-5.
58. Maximino C, Puty B, Benzecry R, Araújo J, Lima MG, et al. (2013) Role of serotonin in zebrafish (Danio rerio) anxiety: Relationship with serotonin levels and effect of buspirone, WAY 100635, SB 224289, fluoxetine and parachlorophenylalanine in two behavioral models. Neuropharmacology 71: 83-97. doi:10.1016/j.neuropharm.2013.03.006.
59. Herculano AM, Maximino C (2014) Serotonergic modulation of zebrafish behavior: Towards a paradox. Prog Neuropsychopharmacol Biol Psychiatry In press. doi:10.1016/j.pnpbp.2014.03.008.
60. Stewart AM, Cachat J, Gaikwad S, Robinson K, Gebhardt M, et al. (2013) Perspectives on experimental models of serotonin syndrome in zebrafish. Neurochem Int 62: 893-902. doi:10.1016/j.neuint.2013.02.018.
61. Wong K, Elegante M, Bartels B, Elkhayat S, Tien D, et al. (2010) Analyzing habituation responses to novelty in zebrafish (Danio rerio). Behav Brain Res 208: 450-457. doi:10.1016/j.bbr.2009.12.023.
62. Maximino C, Lima MG, Oliveira KRM, Picanço-diniz DLW, Herculano AM (2011) Adenosine A1, but not A2, receptor blockade increases anxiety and arousal in zebrafish. Basic Clin Pharmacol Toxicol 109: 203-207. doi:10.1111/j.1742-7843.2011.00710.x.
63. Maximino C, Benzecry R, Matos KRO, Batista E de JO, Herculano AM, et al. (2012) A comparison of the light/dark and novel tank tests in zebrafish. Behaviour 149: 1099-1123. doi:10.1163/1568539X-00003029.
64. Canadian Council on Animal Care (2005) CCAC guidelines on: The care and use of fish in research, teaching and testing. Available: http://www.ccac.ca/en/ CCAC-Programs/Guidelines-Policies/GDLINES/Fish/Fish-Guidelines-English.pdf.
65. Lawrence C (2007) The husbandry of zebrafish (Danio rerio) : A review. Aquaculture 269: 1-20. doi:10.1016/j.aquaculture.2007.04.077.