Leveraging Large-scale Behavioral Profiling in Zebrafish to Explore Neuroactive Polypharmacology

ACS Chemical Biology

Volumn 11, Issue 4, 2016, Pages 842-849

  McCarroll, Matthew N ^a   Gendelev, Leo ^a   Keiser, Michael J ^a   Kokel, David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; DRUG SCREENING; IN VITRO STUDY; NEUROPHARMACOLOGY; NONHUMAN; PHENOTYPE; POLYPHARMACOLOGY; PRIORITY JOURNAL; REVIEW; ZEBRA FISH; ANIMAL; DRUG EFFECTS; PHYSIOLOGY; POLYPHARMACY;

ANIMALS; BEHAVIOR, ANIMAL; POLYPHARMACY; ZEBRAFISH;

EID: 84966264849     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00800     Document Type: Review

References (72)

1. Anighoro, A., Bajorath, J., and Rastelli, G. (2014) Polypharmacology: Challenges and Opportunities in Drug Discovery J. Med. Chem. 57, 7874-7887 10.1021/jm5006463
2. Roth, B. L., Sheffler, D. J., and Kroeze, W. K. (2004) Magic shotguns versus magic bullets: selectively non-selective drugs for mood disorders and schizophrenia Nat. Rev. Drug Discovery 3, 353-359 10.1038/nrd1346
3. Besnard, J., Ruda, G. F., Setola, V., Abecassis, K., Rodriguiz, R. M., Huang, X.-P., Norval, S., Sassano, M. F., Shin, A. I., Webster, L. A., Simeons, F. R. C., Stojanovski, L., Prat, A., Seidah, N. G., Constam, D. B., Bickerton, G. R., Read, K. D., Wetsel, W. C., Gilbert, I. H., Roth, B. L., and Hopkins, A. L. (2012) Automated design of ligands to polypharmacological profiles Nature 492, 215-220 10.1038/nature11691
4. Schizophrenia Working Group of the Psychiatric Genomics Consortium (2014) Biological insights from 108 schizophrenia-associated genetic loci Nature 511, 421-427 10.1038/nature13595
5. Kendler, K. S., Aggen, S. H., and Neale, M. C. (2013) EVidence for multiple genetic factors underlying dsm-iv criteria for major depression JAMA Psychiatry 70, 599-607 10.1001/jamapsychiatry.2013.751
6. Craddock, N. and Sklar, P. (2013) Genetics of bipolar disorder Lancet 381, 1654-1662 10.1016/S0140-6736(13)60855-7
7. Roth, B. L., Sheffler, D., and Potkin, S. G. (2003) Atypical antipsychotic drug actions: unitary or multiple mechanisms for "atypicality"? Clin. Neurosci. Res. 3, 108-117 10.1016/S1566-2772(03)00021-5
8. Griebel, G. and Holmes, A. (2013) 50 years of hurdles and hope in anxiolytic drug discovery Nat. Rev. Drug Discovery 12, 667-687 10.1038/nrd4075
9. Roth, B. L., Lopez, E., Patel, S., and Kroeze, W. K. (2000) The Multiplicity of Serotonin Receptors: Uselessly Diverse Molecules or an Embarrassment of Riches? Neuroscientist 6, 252-262 10.1177/107385840000600408
10. Singh, D. K., Ku, C.-J., Wichaidit, C., Steininger, R. J., Wu, L. F., and Altschuler, S. J. (2010) Patterns of basal signaling heterogeneity can distinguish cellular populations with different drug sensitivities Mol. Syst. Biol. 6, 369 10.1038/msb.2010.22
11. Kokel, D. and Peterson, R. T. (2011) Chapter 22-Using the Zebrafish Photomotor Response for Psychotropic Drug Screening, in Methods in Cell Biology (Detrich, H. W., Westerfield, M., and Zon, L. I., Ed.), pp 517-524, Academic Press.
12. Rihel, J. and Schier, A. F. (2012) Behavioral screening for neuroactive drugs in zebrafish Dev. Neurobiol. 72, 373-385 10.1002/dneu.20910
13. Gleeson, M. P., Hersey, A., Montanari, D., and Overington, J. (2011) Probing the links between in vitro potency, ADMET and physicochemical parameters Nat. Rev. Drug Discovery 10, 197-208 10.1038/nrd3367
14. Szymański, P., Markowicz, M., and Mikiciuk-Olasik, E. (2012) Adaptation of High-Throughput Screening in Drug Discovery-Toxicological Screening Tests Int. J. Mol. Sci. 13, 427-452 10.3390/ijms13010427
15. Kokel, D., Cheung, C. Y. J., Mills, R., Coutinho-Budd, J., Huang, L., Setola, V., Sprague, J., Jin, S., Jin, Y. N., Huang, X.-P., Bruni, G., Woolf, C. J., Roth, B. L., Hamblin, M. R., Zylka, M. J., Milan, D. J., and Peterson, R. T. (2013) Photochemical activation of TRPA1 channels in neurons and animals Nat. Chem. Biol. 9, 257-263 10.1038/nchembio.1183
16. Peterson, R. T., Link, B. A., Dowling, J. E., and Schreiber, S. L. (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development Proc. Natl. Acad. Sci. U. S. A. 97, 12965-12969 10.1073/pnas.97.24.12965
17. Rennekamp, A. J. and Peterson, R. T. (2015) 15 years of zebrafish chemical screening Curr. Opin. Chem. Biol. 24, 58-70 10.1016/j.cbpa.2014.10.025
18. Agetsuma, M., Aizawa, H., Aoki, T., Nakayama, R., Takahoko, M., Goto, M., Sassa, T., Amo, R., Shiraki, T., Kawakami, K., Hosoya, T., Higashijima, S., and Okamoto, H. (2010) The habenula is crucial for experience-dependent modification of fear responses in zebrafish Nat. Neurosci. 13, 1354-1356 10.1038/nn.2654
19. Nowicki, M., Tran, S., Muraleetharan, A., Markovic, S., and Gerlai, R. (2014) Serotonin antagonists induce anxiolytic and anxiogenic-like behavior in zebrafish in a receptor-subtype dependent manner Pharmacol., Biochem. Behav. 126, 170-180 10.1016/j.pbb.2014.09.022
20. Maximino, C., da Silva, A. W. B., Araújo, J., Lima, M. G., Miranda, V., Puty, B., Benzecry, R., Picanço-Diniz, D. L. W., Gouveia, A., Jr, Oliveira, K. R. M., and Herculano, A. M. (2014) Fingerprinting of Psychoactive Drugs in Zebrafish Anxiety-Like Behaviors PLoS One 9, e103943 10.1371/journal.pone.0103943
21. Maximino, C., Marques de Brito, T., Dias, C. A. G., de, M., Gouveia, A., and Morato, S. (2010) Scototaxis as anxiety-like behavior in fish Nat. Protoc. 5, 209-216 10.1038/nprot.2009.225
22. Pradhan, A. and Olsson, P.-E. (2015) Zebrafish sexual behavior: role of sex steroid hormones and prostaglandins Behav. Brain Funct. 11, 23 10.1186/s12993-015-0068-6
23. Gumm, J. M., Snekser, J. L., and Iovine, M. K. (2009) Fin-mutant female zebrafish (Danio rerio) exhibit differences in association preferences for male fin length Behav. Processes 80, 35-38 10.1016/j.beproc.2008.09.004
24. De Marco, R. J., Groneberg, A. H., Yeh, C.-M., Treviño, M., and Ryu, S. (2014) The behavior of larval zebrafish reveals stressor-mediated anorexia during early vertebrate development Front. Behav. Neurosci. 8, 367 10.3389/fnbeh.2014.00367
25. Jordi, J., Guggiana-Nilo, D., Soucy, E., Song, E. Y., Wee, C. L., and Engert, F. (2015) A high-throughput assay for quantifying appetite and digestive dynamics Am. J. Physiol.-Regul. Integr. Comp. Physiol. 309, R345-R357 10.1152/ajpregu.00225.2015
26. Curtright, A., Rosser, M., Goh, S., Keown, B., Wagner, E., Sharifi, J., Raible, D. W., and Dhaka, A. (2015) Modeling nociception in zebrafish: a way forward for unbiased analgesic discovery PLoS One 10, e0116766 10.1371/journal.pone.0116766
27. Malafoglia, V., Bryant, B., Raffaeli, W., Giordano, A., and Bellipanni, G. (2013) The zebrafish as a model for nociception studies J. Cell. Physiol. 228, 1956-1966 10.1002/jcp.24379
28. Malafoglia, V., Colasanti, M., Raffaeli, W., Balciunas, D., Giordano, A., and Bellipanni, G. (2014) Extreme thermal noxious stimuli induce pain responses in zebrafish larvae J. Cell. Physiol. 229, 300-308 10.1002/jcp.24447
29. Del Bene, F., Wyart, C., Robles, E., Tran, A., Looger, L., Scott, E. K., Isacoff, E. Y., and Baier, H. (2010) Filtering of Visual Information in the Tectum by an Identified Neural Circuit Science 330, 669-673 10.1126/science.1192949
30. Lacoste, A. M. B., Schoppik, D., Robson, D. N., Haesemeyer, M., Portugues, R., Li, J. M., Randlett, O., Wee, C. L., Engert, F., and Schier, A. F. (2015) A Convergent and Essential Interneuron Pathway for Mauthner-Cell-Mediated Escapes Curr. Biol. 25, 1526-1534 10.1016/j.cub.2015.04.025
31. Rihel, J., Prober, D. A., Arvanites, A., Lam, K., Zimmerman, S., Jang, S., Haggarty, S. J., Kokel, D., Rubin, L. L., Peterson, R. T., and Schier, A. F. (2010) Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation Science 327, 348-351 10.1126/science.1183090
32. Gandhi, A. V., Mosser, E. A., Oikonomou, G., and Prober, D. A. (2015) Melatonin Is Required for the Circadian Regulation of Sleep Neuron 85, 1193-1199 10.1016/j.neuron.2015.02.016
33. Singh, C., Oikonomou, G., and Prober, D. A. (2015) Norepinephrine is required to promote wakefulness and for hypocretin-induced arousal in zebrafish eLife 4, e07000 10.7554/eLife.07000
34. Kalueff, A. V., Gebhardt, M., Stewart, A. M., Cachat, J. M., Brimmer, M., Chawla, J. S., Craddock, C., Kyzar, E. J., Roth, A., Landsman, S., Gaikwad, S., Robinson, K., Baatrup, E., Tierney, K., Shamchuk, A., Norton, W., Miller, N., Nicolson, T., Braubach, O., Gilman, C. P., Pittman, J., Rosemberg, D. B., Gerlai, R., Echevarria, D., Lamb, E., Neuhauss, S. C. F., Weng, W., Bally-Cuif, L., and Schneider, H. (2013) Towards a Comprehensive Catalog of Zebrafish Behavior 1.0 and Beyond Zebrafish 10, 70-86 10.1089/zeb.2012.0861
35. Panula, P., Chen, Y.-C., Priyadarshini, M., Kudo, H., Semenova, S., Sundvik, M., and Sallinen, V. (2010) The comparative neuroanatomy and neurochemistry of zebrafish CNS systems of relevance to human neuropsychiatric diseases Neurobiol. Dis. 40, 46-57 10.1016/j.nbd.2010.05.010
36. Mathur, P. and Guo, S. (2010) Use of zebrafish as a model to understand mechanisms of addiction and complex neurobehavioral phenotypes Neurobiol. Dis. 40, 66-72 10.1016/j.nbd.2010.05.016
37. Burgess, H. A. and Granato, M. (2007) Sensorimotor Gating in Larval Zebrafish J. Neurosci. 27, 4984-4994 10.1523/JNEUROSCI.0615-07.2007
38. Wolman, M. A., Jain, R. A., Marsden, K. C., Bell, H., Skinner, J., Hayer, K. E., Hogenesch, J. B., and Granato, M. (2015) A Genome-wide Screen Identifies PAPP-AA-Mediated IGFR Signaling as a Novel Regulator of Habituation Learning Neuron 85, 1200-1211 10.1016/j.neuron.2015.02.025
39. Kokel, D. and Peterson, R. T. (2008) Chemobehavioural phenomics and behaviour-based psychiatric drug discovery in the zebrafish Briefings Funct. Genomics Proteomics 7, 483-490 10.1093/bfgp/eln040
40. Baraban, S. C., Dinday, M. T., and Hortopan, G. A. (2013) Drug screening in Scn1a zebrafish mutant identifies clemizole as a potential Dravet syndrome treatment Nat. Commun. 4 2410 10.1038/ncomms3410
41. Neelkantan, N., Mikhaylova, A., Stewart, A. M., Arnold, R., Gjeloshi, V., Kondaveeti, D., Poudel, M. K., and Kalueff, A. V. (2013) Perspectives on Zebrafish Models of Hallucinogenic Drugs and Related Psychotropic Compounds ACS Chem. Neurosci. 4, 1137-1150 10.1021/cn400090q
42. Cachat, J., Kyzar, E. J., Collins, C., Gaikwad, S., Green, J., Roth, A., El-Ounsi, M., Davis, A., Pham, M., Landsman, S., Stewart, A. M., and Kalueff, A. V. (2013) Unique and potent effects of acute ibogaine on zebrafish: The developing utility of novel aquatic models for hallucinogenic drug research Behav. Brain Res. 236, 258-269 10.1016/j.bbr.2012.08.041
43. Cachat, J., Stewart, A., Utterback, E., Hart, P., Gaikwad, S., Wong, K., Kyzar, E., Wu, N., and Kalueff, A. V. (2011) Three-dimensional neurophenotyping of adult zebrafish behavior PLoS One 6, e17597 10.1371/journal.pone.0017597
44. Grossman, L., Utterback, E., Stewart, A., Gaikwad, S., Chung, K. M., Suciu, C., Wong, K., Elegante, M., Elkhayat, S., Tan, J., Gilder, T., Wu, N., DiLeo, J., Cachat, J., and Kalueff, A. V. (2010) Characterization of behavioral and endocrine effects of LSD on zebrafish Behav. Brain Res. 214, 277-284 10.1016/j.bbr.2010.05.039
45. Tran, S., Muraleetharan, A., Fulcher, N., Chatterjee, D., and Gerlai, R. (2015) MK-801 increases locomotor activity in a context-dependent manner in zebrafish Behav. Brain Res. 296, 26-29 10.1016/j.bbr.2015.08.029
46. Tran, S., Nowicki, M., Muraleetharan, A., Chatterjee, D., and Gerlai, R. (2015) Differential effects of acute administration of SCH-23390, a D1 receptor antagonist, and of ethanol on swimming activity, anxiety-related responses, and neurochemistry of zebrafish Psychopharmacology (Berl.) 232, 3709-3718 10.1007/s00213-015-4030-y
47. Guo, N., Lin, J., Peng, X., Chen, H., Zhang, Y., Liu, X., and Li, Q. (2015) Influences of acute ethanol exposure on locomotor activities of zebrafish larvae under different illumination Alcohol 49, 727 10.1016/j.alcohol.2015.08.003
48. Gebauer, D. L., Pagnussat, N., Piato, Â. L., Schaefer, I. C., Bonan, C. D., and Lara, D. R. (2011) Effects of anxiolytics in zebrafish: Similarities and differences between benzodiazepines, buspirone and ethanol Pharmacol., Biochem. Behav. 99, 480-486 10.1016/j.pbb.2011.04.021
49. Kyzar, E. J., Collins, C., Gaikwad, S., Green, J., Roth, A., Monnig, L., El-Ounsi, M., Davis, A., Freeman, A., Capezio, N., Stewart, A. M., and Kalueff, A. V. (2012) Effects of hallucinogenic agents mescaline and phencyclidine on zebrafish behavior and physiology Prog. Neuro-Psychopharmacol. Biol. Psychiatry 37, 194-202 10.1016/j.pnpbp.2012.01.003
50. Stewart, A., Wong, K., Cachat, J., Gaikwad, S., Kyzar, E., Wu, N., Hart, P., Piet, V., Utterback, E., Elegante, M., Tien, D., and Kalueff, A. V. (2011) Zebrafish models to study drug abuse-related phenotypes Rev. Neurosci. 22, 95-105 10.1515/rns.2011.011
51. Kyzar, E., Stewart, A. M., Landsman, S., Collins, C., Gebhardt, M., Robinson, K., and Kalueff, A. V. (2013) Behavioral effects of bidirectional modulators of brain monoamines reserpine and d-amphetamine in zebrafish Brain Res. 1527, 108-116 10.1016/j.brainres.2013.06.033
52. Renier, C., Faraco, J. H., Bourgin, P., Motley, T., Bonaventure, P., Rosa, F., and Mignot, E. (2007) Genomic and functional conservation of sedative-hypnotic targets in the zebrafish Pharmacogenet. Genomics 17, 237-253 10.1097/FPC.0b013e3280119d62
53. Chen, F., Chen, S., Liu, S., Zhang, C., and Peng, G. (2015) Effects of lorazepam and WAY-200070 in larval zebrafish light/dark choice test Neuropharmacology 95, 226-233 10.1016/j.neuropharm.2015.03.022
54. Kokel, D., Dunn, T. W., Ahrens, M. B., Alshut, R., Cheung, C. Y. J., Saint-Amant, L., Bruni, G., Mateus, R., van Ham, T. J., Shiraki, T., Fukada, Y., Kojima, D., Yeh, J.-R. J., Mikut, R., von Lintig, J., Engert, F., and Peterson, R. T. (2013) Identification of Nonvisual Photomotor Response Cells in the Vertebrate Hindbrain J. Neurosci. 33, 3834-3843 10.1523/JNEUROSCI.3689-12.2013
55. Kokel, D., Bryan, J., Laggner, C., White, R., Cheung, C. Y. J., Mateus, R., Healey, D., Kim, S., Werdich, A. A., Haggarty, S. J., MacRae, C. A., Shoichet, B., and Peterson, R. T. (2010) Rapid behavior-based identification of neuroactive small molecules in the zebrafish Nat. Chem. Biol. 6, 231-237 10.1038/nchembio.307
56. Ahrens, M. B., Li, J. M., Orger, M. B., Robson, D. N., Schier, A. F., Engert, F., and Portugues, R. (2012) Brain-wide neuronal dynamics during motor adaptation in zebrafish Nature 485, 471-477 10.1038/nature11057
57. Yokogawa, T., Hannan, M. C., and Burgess, H. A. (2012) The Dorsal Raphe Modulates Sensory Responsiveness during Arousal in Zebrafish J. Neurosci. 32, 15205-15215 10.1523/JNEUROSCI.1019-12.2012
58. Wyart, C., Del Bene, F., Warp, E., Scott, E. K., Trauner, D., Baier, H., and Isacoff, E. Y. (2009) Optogenetic dissection of a behavioural module in the vertebrate spinal cord Nature 461, 407-410 10.1038/nature08323
59. Keiser, M. J., Roth, B. L., Armbruster, B. N., Ernsberger, P., Irwin, J. J., and Shoichet, B. K. (2007) Relating protein pharmacology by ligand chemistry Nat. Biotechnol. 25, 197-206 10.1038/nbt1284
60. Keiser, M. J., Setola, V., Irwin, J. J., Laggner, C., Abbas, A. I., Hufeisen, S. J., Jensen, N. H., Kuijer, M. B., Matos, R. C., Tran, T. B., Whaley, R., Glennon, R. A., Hert, J., Thomas, K. L. H., Edwards, D. D., Shoichet, B. K., and Roth, B. L. (2009) Predicting new molecular targets for known drugs Nature 462, 175-181 10.1038/nature08506
61. Lemieux, G. A., Keiser, M. J., Sassano, M. F., Laggner, C., Mayer, F., Bainton, R. J., Werb, Z., Roth, B. L., Shoichet, B. K., and Ashrafi, K. (2013) In Silico Molecular Comparisons of C. elegans and Mammalian Pharmacology Identify Distinct Targets That Regulate Feeding PLoS Biol. 11, e1001712 10.1371/journal.pbio.1001712
62. Laggner, C., Kokel, D., Setola, V., Tolia, A., Lin, H., Irwin, J. J., Keiser, M. J., Cheung, C. Y. J., Jr, Minor, D. L., Roth, B. L., Peterson, R. T., and Shoichet, B. K. (2012) Chemical informatics and target identification in a zebrafish phenotypic screen Nat. Chem. Biol. 8, 144-146 10.1038/nchembio.732
63. Kokel, D., Rennekamp, A. J., Shah, A. H., Liebel, U., and Peterson, R. T. (2012) Behavioral barcoding in the cloud: embracing data-intensive digital phenotyping in neuropharmacology Trends Biotechnol. 30, 421-425 10.1016/j.tibtech.2012.05.001
64. Lounkine, E., Keiser, M. J., Whitebread, S., Mikhailov, D., Hamon, J., Jenkins, J. L., Lavan, P., Weber, E., Doak, A. K., Côté, S., Shoichet, B. K., and Urban, L. (2012) Large-scale prediction and testing of drug activity on side-effect targets Nature 486, 361-367 10.1038/nature11159
65. Ciceri, P., Müller, S., O'Mahony, A., Fedorov, O., Filippakopoulos, P., Hunt, J. P., Lasater, E. A., Pallares, G., Picaud, S., Wells, C., Martin, S., Wodicka, L. M., Shah, N. P., Treiber, D. K., and Knapp, S. (2014) Dual kinase-bromodomain inhibitors for rationally designed polypharmacology Nat. Chem. Biol. 10, 305-312 10.1038/nchembio.1471
66. Carrieri, A., Pérez-Nueno, V. I., Lentini, G., and Ritchie, D. W. (2013) Recent trends and future prospects in computational GPCR drug discovery: from virtual screening to polypharmacology Curr. Top. Med. Chem. 13, 1069-1097 10.2174/15680266113139990028
67. Zhao, S. and Iyengar, R. (2012) Systems Pharmacology: Network Analysis to Identify Multiscale Mechanisms of Drug Action Annu. Rev. Pharmacol. Toxicol. 52, 505-521 10.1146/annurev-pharmtox-010611-134520
68. Eliceiri, B. P., Gonzalez, A. M., and Baird, A. (2011) Zebrafish Model of the Blood-Brain Barrier: Morphological and Permeability Studies Methods Mol. Biol. 686, 371-378 10.1007/978-1-60761-938-3-18
69. Jeong, J.-Y., Kwon, H.-B., Ahn, J.-C., Kang, D., Kwon, S.-H., Park, J. A., and Kim, K.-W. (2008) Functional and developmental analysis of the blood-brain barrier in zebrafish Brain Res. Bull. 75, 619-628 10.1016/j.brainresbull.2007.10.043
70. Xie, J., Farage, E., Sugimoto, M., and Anand-Apte, B. (2010) A novel transgenic zebrafish model for blood-brain and blood-retinal barrier development BMC Dev. Biol. 10, 76 10.1186/1471-213X-10-76
71. Zhang, J., Piontek, J., Wolburg, H., Piehl, C., Liss, M., Otten, C., Christ, A., Willnow, T. E., Blasig, I. E., and Abdelilah-Seyfried, S. (2010) Establishment of a neuroepithelial barrier by Claudin5a is essential for zebrafish brain ventricular lumen expansion Proc. Natl. Acad. Sci. U. S. A. 107, 1425-1430 10.1073/pnas.0911996107
72. Vardy, E., Sassano, M. F., Rennekamp, A. J., Kroeze, W. K., Mosier, P. D., Westkaemper, R. B., Stevens, C. W., Katritch, V., Stevens, R. C., Peterson, R. T., and Roth, B. L. (2015) Single Amino Acid Variation Underlies Species-Specific Sensitivity to Amphibian Skin-Derived Opioid-like Peptides Chem. Biol. 22, 764-775 10.1016/j.chembiol.2015.05.012