Aquatic toxicology of fluoxetine: Understanding the knowns and the unknowns

Aquatic Toxicology

Volumn 156, Issue , 2014, Pages 269-273

  Stewart, Adam Michael ^a,b   Grossman, Leah ^a,c,d   Nguyen, Michael ^a,e   Maximino, Caio ^b,f   Rosemberg, Denis Broock ^b,g   Echevarria, David J ^b,h   Kalueff, Allan V ^a,b,i  

^a ZENEREI Institute   (United States)

^b International Zebrafish Neuroscience Research Consortium (ZNRC)   (United States)

^c ST GEORGE S UNIVERSITY SCHOOL OF MEDICINE   (Grenada)

^d Department of Biomedical Engineering University of Virginia ^*  (United States)

^e University of Virginia   (United States)

^f UNIVERSIDADE DO ESTADO DO PARÁ   (Brazil)

^g FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^h UNIVERSITY OF SOUTHERN MISSISSIPPI   (United States)

ⁱ GUANGDONG OCEAN UNIVERSITY   (China)

Author keywords

Antidepressants; Aquatic model; Ecotoxicology; Fluoxetine; Neuroscience; Zebrafish

Indexed keywords

FLUOXETINE; SEROTONIN AGONIST; SEROTONIN UPTAKE INHIBITOR; SEROTONIN; WATER POLLUTANT;

AQUATIC ENVIRONMENT; CHEMICAL ANALYSIS; ECOTOXICOLOGY; ENVIRONMENTAL EXPOSURE; IN VIVO STUDY; LETTER; NEUROTOXICITY; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; SEROTONIN UPTAKE; TRANQUILIZING ACTIVITY; TRANSLATIONAL RESEARCH; ZEBRA FISH; ANIMAL; ANIMAL BEHAVIOR; ANIMAL MODEL; AQUATIC SPECIES; DRUG EFFECTS; METABOLISM; STANDARDS; TOXICITY; WATER POLLUTANT;

DANIO RERIO;

ANIMALS; AQUATIC ORGANISMS; BEHAVIOR, ANIMAL; ECOTOXICOLOGY; FLUOXETINE; MODELS, ANIMAL; SEROTONIN; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

EID: 84908338194     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2014.08.014     Document Type: Letter

References (86)

1. Abreu M.S., Koakoski G., Ferreira D., Oliveira T.A., Rosa J.G., Gusso D., Giacomini A.C., Piato A.L., Barcellos L.J. Diazepam and fluoxetine decrease the stress response in zebrafish. PloS One 2014, 9:e103232.
2. Alderman S.L., Bernier N.J. Ontogeny of the corticotropin-releasing factor system in zebrafish. Gen. Comp. Endocrinol. 2009, 164:61-69.
3. Bailey K.R., Rustay N.R., Crawley J.N. Behavioral phenotyping of transgenic and knockout mice: practical concerns and potential pitfalls. ILAR J./Natl. Res. Council, Instit. Lab. Animal Resources 2006, 47:124-131.
4. Bertorini T.E. Myoglobinuria, malignant hyperthermia, neuroleptic malignant syndrome and serotonin syndrome. Neurol. Clin. 1997, 15:649-671.
5. Blaser R.E., Rosemberg D.B. Measures of anxiety in zebrafish (Danio rerio): dissociation of black/white preference and novel tank test. PloS One 2012, 7:e36931.
6. Brooks B.W. Fish on Prozac (and Zoloft): ten years later. Aquat. Toxicol. 2014, 151:61-67.
7. Bruni G., Lakhani P., Kokel D. Discovering novel neuroactive drugs through high-throughput behavior-based chemical screening in the zebrafish. Front. Pharmacol. 2014, 5:153.
8. Cachat J., Stewart A., Grossman L., Gaikwad S., Kadri F., Chung K.M., Wu N., Wong K., Roy S., Suciu C., Goodspeed J., Elegante M., Bartels B., Elkhayat S., Tien D., Tan J., Denmark A., Gilder T., Kyzar E., Dileo J., Frank K., Chang K., Utterback E., Hart P., Kalueff A.V. Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. Nat. Protocols 2010, 5:1786-1799.
9. Cachat J., Stewart A., Grossman L., Gaikwad S., Kadri F., Min Chung K., Wu N., Wong K., Roy S., Suciu C., Goodspeed J., Elegante M., Bartels B., Elkhayat S., Tien D., Tan J., Denmark A., Gilder T., Kyzar E., DiLeo J., Frank K., Chang K., Utterback E., Hart P., Kalueff A.V. Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. Nat. Prot. 2010, 5:1786-1799.
10. Cachat J., Stewart A., Utterback E., Hart P., Gaikwad S., Wong K., Kyzar E., Wu N., Kalueff A.V. Three-dimensional neurophenotyping of adult zebrafish behavior. PloS One 2011, 6:e17597.
11. Chatterjee D., Shams S., Gerlai R. Chronic and acute alcohol administration induced neurochemical changes in the brain: comparison of distinct zebrafish populations. Amino Acids 2014, 46:921-930.
12. Clements S., Schreck C.B. Chronic administration of fluoxetine alters locomotor behavior, but does not potentiate the locomotor stimulating effects of CRH in juvenile Chinook salmon (Oncorhynchus tshawytscha). Comp. Biochem. Physiol. Part A, Mol. Integrat. Physiol. 2007, 147:43-49.
13. Collier A.D., Khan K.M., Caramillo E.M., Mohn R.S., Echevarria D.J. Zebrafish and conditioned place preference: a translational model of drug reward. Progr. Neuro-Psychopharmacol. Biol. Psychiatry 2014.
14. Crabbe J.C., Wahlsten D., Dudek B.C. Genetics of mouse behavior: interactions with laboratory environment. Science 1999, 284:1670-1672.
15. Crawley J.N. Behavioral phenotyping of rodents. Comp. Med. 2003, 53:140-146.
16. Crawley J.N. Behavioral phenotyping strategies for mutant mice. Neuron 2008, 57:809-818.
17. Dzieweczynski T.L., Hebert O.L. Fluoxetine alters behavioral consistency of aggression and courtship in male Siamese fighting fish, Betta splendens. Physiol. Behav. 2012, 107:92-97.
18. Echevarria D.J., Jouandot D.J., Toms C.N. Assessing attention in the zebrafish: are we there yet?. Progr. Neuro-Psychopharmacol. Biol. Psychiatry 2011, 35:1416-1420.
19. Echevarria D.J., Toms C.N., Jouandot D.J. Alcohol-induced behavior change in zebrafish models. Rev. Neurosci. 2011, 22:85-93.
20. Egan R.J., Bergner C.L., Hart P.C., Cachat J.M., Canavello P.R., Elegante M.F., Elkhayat S.I., Bartels B.K., Tien A.K., Tien D.H., Mohnot S., Beeson E., Glasgow E., Amri H., Zukowska Z., Kalueff A.V. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav. Brain Res. 2009, 205:38-44.
21. Fabbri C., Porcelli S., Serretti A. From pharmacogenetics to pharmacogenomics: the way toward the personalization of antidepressant treatment. Canad. J. Psychiatry. Revue canadienne de psychiatrie 2014, 59:62-75.
22. Fent K., Weston A.A., Caminada D. Ecotoxicology of human pharmaceuticals. Aquat. Toxicol. 2006, 76:122-159.
23. Fernandes D., Schnell S., Porte C. Can pharmaceuticals interfere with the synthesis of active androgens in male fish? An in vitro study. Marine Pollut. Bull. 2011, 62:2250-2253.
24. Griffiths B.B., Schoonheim P.J., Ziv L., Voelker L., Baier H., Gahtan E. A zebrafish model of glucocorticoid resistance shows serotonergic modulation of the stress response. Front. Behav. Neurosci. 2012, 6:68.
25. 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., Kalueff A.V. Characterization of behavioral and endocrine effects of LSD on zebrafish. Behav. Brain Res. 2010, 214:277-284.
26. Haberzettl R., Bert B., Fink H., Fox M.A. Animal models of the serotonin syndrome: a systematic review. Behav. Brain Res. 2013, 256:328-345.
27. Herculano A.M., Maximino C. Serotonergic modulation of zebrafish behavior: towards a paradox. Progr. Neuro-psychopharmacol. Biol. Psychiatry 2014.
28. Kalueff A.V., Echevarria D.J., Stewart A.M. Gaining translational momentum: more zebrafish models for neuroscience research. Progr. neuro-Psychopharmacol. Biol. Psychiatry 2014.
29. 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., Weng W., Bally-Cuif L., Schneider H. Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond. Zebrafish 2013, 10:70-86.
30. Kalueff A.V., LaPorte J.L., Murphy D.L. Perspectives on genetic animal models of serotonin toxicity. Neurochem. Int. 2008, 52:649-658.
31. Kalueff A.V., Olivier J.D., Nonkes L.J., Homberg J.R. Conserved role for the serotonin transporter gene in rat and mouse neurobehavioral endophenotypes. Neurosci. Biobehav. Rev. 2010, 34:373-386.
32. Kalueff A.V., Stewart A.M., Gerlai R. Zebrafish as an emerging model for studying complex brain disorders. Trends Pharmacol. Sci. 2014, 35:63-75.
33. Kalueff A.V., Wheaton M., Murphy D.L. What's wrong with my mouse model?. Advances and strategies in animal modeling of anxiety and depression. Behav. Brain Res. 2007, 179:1-18.
34. Kohlert J.G., Mangan B.P., Kodra C., Drako L., Long E., Simpson H. Decreased aggressive and locomotor behaviors in Betta splendens after exposure to fluoxetine. Psychol. Rep. 2012, 110:51-62.
35. Kokel D., Bryan J., Laggner C., White R., Cheung C.Y., Mateus R., Healey D., Kim S., Werdich A.A., Haggarty S.J., Macrae C.A., Shoichet B., Peterson R.T. Rapid behavior-based identification of neuroactive small molecules in the zebrafish. Nat. Chem. Biol. 2010, 6:231-237.
36. Kokel D., Peterson R.T. Chemobehavioural phenomics and behaviour-based psychiatric drug discovery in the zebrafish. Briefings Funct. Genom. Proteomics 2008, 7:483-490.
37. Kokel D., Peterson R.T. Using the zebrafish photomotor response for psychotropic drug screening. Methods Cell Biol. 2011, 105:517-524.
38. Kokel D., Rennekamp A.J., Shah A.H., Liebel U., Peterson R.T. Behavioral barcoding in the cloud: embracing data-intensive digital phenotyping in neuropharmacology. Trends Biotechnol. 2012, 30:421-425.
39. Laggner C., Kokel D., Setola V., Tolia A., Lin H., Irwin J.J., Keiser M.J., Cheung C.Y., Minor D.L., Roth B.L., Peterson R.T., Shoichet B.K. Chemical informatics and target identification in a zebrafish phenotypic screen. Nat. Chem. Biol. 2012, 8:144-146.
40. Lajeunesse A., Gagnon C., Gagne F., Louis S., Cejka P., Sauve S. Distribution of antidepressants and their metabolites in brook trout exposed to municipal wastewaters before and after ozone treatment-evidence of biological effects. Chemosphere 2011, 83:564-571.
41. Mahabir S., Chatterjee D., Gerlai R. Strain dependent neurochemical changes induced by embryonic alcohol exposure in zebrafish. Neurotoxicol. Teratol. 2014, 41:1-7.
42. Maximino C., da Silva A.W., Araujo J., Lima M.G., Miranda V., Puty B., Benzecry R., Picanco-Diniz D.L., Gouveia A., Oliveira K.R., Herculano A.M. Fingerprinting of psychoactive drugs in zebrafish anxiety-like behaviors. PloS One 2014, 9:e103943.
43. Maximino C., da Silva A.W., Gouveia A., Herculano A.M. Pharmacological analysis of zebrafish (Danio rerio) scototaxis. Progr. Neuro-psychopharmacol. Biol. Psychiatry 2011, 35:624-631.
44. Maximino C., de Brito T.M., Colmanetti R., Pontes A.A., de Castro H.M., de Lacerda R.I., Morato S., Gouveia A. Parametric analyses of anxiety in zebrafish scototaxis. Behav. Brain Res. 2010, 210:1-7.
45. Maximino C., Herculano A.M. A review of monoaminergic neuropsychopharmacology in zebrafish. Zebrafish 2010, 7:359-378.
46. Maximino C., Lima M.G., Costa C.C., Guedes I.M., Herculano A.M. Fluoxetine and WAY 100,635 dissociate increases in scototaxis and analgesia induced by conspecific alarm substance in zebrafish (Danio rerio Hamilton 1822). Pharmacol., Biochem. Behav. 2014.
47. Maximino C., Puty B., Benzecry R., Araujo J., Lima M.G., de Jesus Oliveira Batista E., Renata de Matos Oliveira K., Crespo-Lopez M.E., Herculano A.M. Role of serotonin in zebrafish (Danio rerio) anxiety: relationship with serotonin levels and effect of buspirone, WAY 100635, SB 224289, fluoxetine and para-chlorophenylalanine (pCPA) in two behavioral models. Neuropharmacology 2013, 71:83-97.
48. Maximino C., Puty B., Matos Oliveira K.R., Herculano A.M. Behavioral and neurochemical changes in the zebrafish leopard strain. Genes, Brain Behav. 2013, 12:576-582.
49. Mennigen J.A., Lado W.E., Zamora J.M., Duarte-Guterman P., Langlois V.S., Metcalfe C.D., Chang J.P., Moon T.W., Trudeau V.L. Waterborne fluoxetine disrupts the reproductive axis in sexually mature male goldfish Carassius auratus. Aquat. Toxicol. 2010, 100:354-364.
50. Mennigen J.A., Sassine J., Trudeau V.L., Moon T.W. Waterborne fluoxetine disrupts feeding and energy metabolism in the goldfish Carassius auratus. Aquat. Toxicol. 2010, 100:128-137.
51. Mennigen J.A., Stroud P., Zamora J.M., Moon T.W., Trudeau V.L. Pharmaceuticals as neuroendocrine disruptors: lessons learned from fish on Prozac. J. Toxicol. Environ. Health Part B, Crit. Rev. 2011, 14:387-412.
52. Morando M.B., Medeiros L.R., McDonald M.D. Fluoxetine treatment affects nitrogen waste excretion and osmoregulation in a marine teleost fish. Aquat. Toxicol. 2009, 95:164-171.
53. Murphy D.L., Lesch K.P. Targeting the murine serotonin transporter: insights into human neurobiology. Nat. Rev. Neurosci. 2008, 9:85-96.
54. Neelkantan N., Mikhaylova A., Stewart A.M., Arnold R., Gjeloshi V., Kondaveeti D., Poudel M.K., Kalueff A.V. Perspectives on zebrafish models of hallucinogenic drugs and related psychotropic compounds. ACS Chem. Neurosci. 2013, 4:1137-1150.
55. Nguyen M., Stewart A.M., Kalueff A.V. Aquatic blues: modeling depression and antidepressant action in zebrafish. Progr. Neuro-psychopharmacol. Biol. Psychiatry 2014.
56. Pan Y., Chatterjee D., Gerlai R. Strain dependent gene expression and neurochemical levels in the brain of zebrafish: focus on a few alcohol related targets. Physiol. Behav. 2012, 107:773-780.
57. Pittman J.T., Ichikawa K.M. iPhone(R) applications as versatile video tracking tools to analyze behavior in zebrafish (Danio rerio). Pharmacol., Biochem. Behav. 2013, 106:137-142.
58. Pittman J.T., Lott C.S. Startle response memory and hippocampal changes in adult zebrafish pharmacologically-induced to exhibit anxiety/depression-like behaviors. Physiol. Behav. 2014, 123:174-179.
59. Ramirez A.J., Brain R.A., Usenko S., Mottaleb M.A., O'Donnell J.G., Stahl L.L., Wathen J.B., Snyder B.D., Pitt J.L., Perez-Hurtado P., Dobbins L.L., Brooks B.W., Chambliss C.K. Occurrence of pharmaceuticals and personal care products in fish: results of a national pilot study in the United States. Environ. Toxicol. Chem./SETAC 2009, 28:2587-2597.
60. Richendrfer H., Pelkowski S.D., Colwill R.M., Creton R. On the edge: pharmacological evidence for anxiety-related behavior in zebrafish larvae. Behav. Brain Res. 2012, 228:99-106.
61. Rihel J., Prober D.A., Arvanites A., Lam K., Zimmerman S., Jang S., Haggarty S.J., Kokel D., Rubin L.L., Peterson R.T., Schier A.F. Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 2010, 327:348-351.
62. Rosemberg D.B., Rico E.P., Mussulini B.H., Piato A.L., Calcagnotto M.E., Bonan C.D., Dias R.D., Blaser R.E., Souza D.O., de Oliveira D.L. Differences in spatio-temporal behavior of zebrafish in the open tank paradigm after a short-period confinement into dark and bright environments. PloS One 2011, 6:e19397.
63. Sackerman J., Donegan J.J., Cunningham C.S., Nguyen N.N., Lawless K., Long A., Benno R.H., Gould G.G. Zebrafish behavior in novel environments: effects of acute exposure to anxiolytic compounds and choice of Danio rerio line. Int. J. Comp. Psychol./ISCP; sponsored by the International Society for Comparative Psychology and the University of Calabria 2010, 23:43-61.
64. Schultz M.M., Furlong E.T., Kolpin D.W., Werner S.L., Schoenfuss H.L., Barber L.B., Blazer V.S., Norris D.O., Vajda A.M. Antidepressant pharmaceuticals in two U.S. effluent-impacted streams: occurrence and fate in water and sediment, and selective uptake in fish neural tissue. Environ. Sci. Technol. 2010, 44:1918-1925.
65. Schultz M.M., Painter M.M., Bartell S.E., Logue A., Furlong E.T., Werner S.L., Schoenfuss H.L. Selective uptake and biological consequences of environmentally relevant antidepressant pharmaceutical exposures on male fathead minnows. Aquat. Toxicol. 2011, 104:38-47.
66. Silva L.J., Pereira A.M., Meisel L.M., Lino C.M., Pena A. A one-year follow-up analysis of antidepressants in Portuguese wastewaters: occurrence and fate, seasonal influence, and risk assessment. Sci. Total Environ. 2014, 490:279-287.
67. Stewart A., Riehl R., Wong K., Green J., Cosgrove J., Vollmer K., Kyzar E., Hart P., Allain A., Cachat J., Gaikwad S., Hook M., Rhymes K., Newman A., Utterback E., Chang K., Kalueff A.V. Behavioral effects of MDMA ('ecstasy') on adult zebrafish. Behav. Pharmacol. 2011, 22:275-280.
68. Stewart A., Wu N., Cachat J., Hart P., Gaikwad S., Wong K., Utterback E., Gilder T., Kyzar E., Newman A., Carlos D., Chang K., Hook M., Rhymes C., Caffery M., Greenberg M., Zadina J., Kalueff A.V. Pharmacological modulation of anxiety-like phenotypes in adult zebrafish behavioral models. Progr. Neuro-Psychopharmacol. Biol. Psychiatry 2011, 35:1421-1431.
69. Stewart A.M., Braubach O., Spitsbergen J., Gerlai R., Kalueff A.V. Zebrafish models for translational neuroscience research: from tank to bedside. Trends Neurosci. 2014, 37:264-278.
70. Stewart A.M., Cachat J., Gaikwad S., Robinson K.S., Gebhardt M., Kalueff A.V. Perspectives on experimental models of serotonin syndrome in zebrafish. Neurochem. Int. 2013, 62:893-902.
71. Stewart A.M., Kalueff A.V. Developing better and more valid animal models of brain disorders. Behav. Brain Res. 2013.
72. Stewart A.M., Kalueff A.V. Anxiolytic drug discovery: what are the novel approaches and how can we improve them?. Expert Opin. Drug Discov. 2014, 9:15-26.
73. Stewart A.M., Ullmann J., Brennan C.H., Parker M.O., Norton W.H., Gerlai R., Kalueff A.V. Molecular psychiatry of zebrafish. Mol. Psychiatry. 2015.
74. Sumpter J.P., Donnachie R.L., Johnson A.C. The apparently very variable potency of the anti-depressant fluoxetine. Aquat. Toxicol. 2014, 151:57-60.
75. Sumpter J.P., Margiotta-Casaluci L. Are some invertebrates exquisitely sensitive to the human pharmaceutical fluoxetine?. Aquat. Toxicol. 2014, 146:259-260.
76. Toms C.N., Echevarria D.J. Back to basics: searching for a comprehensive framework for exploring individual differences in zebrafish (danio rerio) behavior. Zebrafish 2014, 11:325-340.
77. Tran S., Gerlai R. Individual differences in activity levels in zebrafish (Danio rerio). Behav. Brain Res. 2013, 257:224-229.
78. Wahlsten D., Metten P., Phillips T.J., Boehm S.L., Burkhart-Kasch S., Dorow J., Doerksen S., Downing C., Fogarty J., Rodd-Henricks K., Hen R., McKinnon C.S., Merrill C.M., Nolte C., Schalomon M., Schlumbohm J.P., Sibert J.R., Wenger C.D., Dudek B.C., Crabbe J.C. Different data from different labs: lessons from studies of gene-environment interaction. J. Neurobiol. 2003, 54:283-311.
79. Weinberger J., Klaper R. Environmental concentrations of the selective serotonin reuptake inhibitor fluoxetine impact specific behaviors involved in reproduction, feeding and predator avoidance in the fish Pimephales promelas (fathead minnow). Aquat. Toxicol. 2014, 151:77-83.
80. Winder V.L., Pennington P.L., Hurd M.W., Wirth E.F. Fluoxetine effects on sheepshead minnow (Cyprinodon variegatus) locomotor activity. J. Environ. Sci. Health Part. B, Pesticides, Food Contam. Agric. Wastes 2012, 47:51-58.
81. Wong K., Elegante M., Bartels B., Elkhayat S., Tien D., Roy S., Goodspeed J., Suciu C., Tan J., Grimes C., Chung A., Rosenberg M., Gaikwad S., Denmark A., Jackson A., Kadri F., Chung K.M., Stewart A., Gilder T., Beeson E., Zapolsky I., Wu N., Cachat J., Kalueff A.V. Analyzing habituation responses to novelty in zebrafish (Danio rerio). Behav. Brain Res. 2010, 208:450-457.
82. Wong R.Y., Oxendine S.E., Godwin J. Behavioral and neurogenomic transcriptome changes in wild-derived zebrafish with fluoxetine treatment. BMC Genom. 2013, 14:348.
83. Wurbel H. Behavioral phenotyping enhanced--beyond (environmental) standardization. Genes Brain Behav. 2002, 1:3-8.
84. Zakhary S.M., Ayubcha D., Ansari F., Kamran K., Karim M., Leheste J.R., Horowitz J.M., Torres G. A behavioral and molecular analysis of ketamine in zebrafish. Synapse 2011, 65:160-167.
85. Ziv L., Muto A., Schoonheim P.J., Meijsing S.H., Strasser D., Ingraham H.A., Schaaf M.J., Yamamoto K.R., Baier H. An affective disorder in zebrafish with mutation of the glucocorticoid receptor. Mol. Psychiatry 2012.
86. Ziv L., Muto A., Schoonheim P.J., Meijsing S.H., Strasser D., Ingraham H.A., Schaaf M.J., Yamamoto K.R., Baier H. An affective disorder in zebrafish with mutation of the glucocorticoid receptor. Mol. Psychiatry 2013, 18:681-691.