Behavioral changes induced by long-term proline exposure are reversed by antipsychotics in zebrafish

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 36, Issue 2, 2012, Pages 258-263

  Savio, Luiz Eduardo Baggio ^a   Vuaden, Fernanda Cenci ^a   Piato, Angelo L ^b   Bonan, Carla Denise ^b,c   Wyse, Angela T S ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^c Instituto Nacional de Ciencia e Tecnologia Translacional em Medicina INCT TM   (Brazil)

Author keywords

Anxiety; Hyperprolinemia; Locomotor activity; Social interaction; Zebrafish

Indexed keywords

HALOPERIDOL; NEUROLEPTIC AGENT; PROLINE; SULPIRIDE;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; FEMALE; HYPERPROLACTINEMIA; LOCOMOTION; LONG TERM EXPOSURE; MALE; NONHUMAN; SCHIZOPHRENIA; SOCIAL INTERACTION; ZEBRA FISH;

AMINO ACID METABOLISM, INBORN ERRORS; ANIMALS; ANTIPSYCHOTIC AGENTS; ANXIETY; DISEASE MODELS, ANIMAL; DRUG INTERACTIONS; FEMALE; HALOPERIDOL; LOCOMOTION; MALE; PROLINE; PROLINE OXIDASE; SOCIAL BEHAVIOR; SULPIRIDE; TIME FACTORS; ZEBRAFISH;

EID: 84855406133     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2011.10.002     Document Type: Article

References (61)

1. Barbazuk W.B., Korf I., Kadavi C., Heyen J., Tate S., Wun E., et al. The syntenic relationship of the zebrafish and human genomes. Genome Res 2000, 10:1351-1358.
2. Bavaresco C.S., Streck E.L., Netto C.A., Wyse A.T.S. Chronic hyperprolinemia provokes a memory deficit in the Morris water maze task. Metab Brain Dis 2005, 20:73-80.
3. Bertoglio L.J., Carobrez A.P. Anxiolytic-like effects of NMDA/glycine-B receptor ligands are abolished during the elevated plus-maze trial 2 in rats. Psychopharmacology (Berl) 2003, 170:335-342.
4. Blank M., Guerim L.D., Cordeiro R.F., Vianna M.R. A one-trial inhibitory avoidance task to zebrafish: rapid acquisition of an NMDA-dependent long-term memory. Neurobiol Learn Mem 2009, 92:529-534.
5. 1A agonist activities: improvement of social interaction deficits induced by phencyclidine in rats. Neuropharmacology 2004, 46:1121-1129.
6. Champagne D.L., Hoefnagels C.C., de Kloet R.E., Richardson M.K. Translating rodent behavioral repertoire to zebrafish (Danio rerio): relevance for stress research. Behav Brain Res 2010, 214:332-342.
7. Cohen S.M., Nadler J.V. Sodium-dependent proline and glutamate uptake by hippocampal synaptosomes during postnatal development. Brain Res Dev Brain Res 1997, 100:230-233.
8. Delwing D., Chiarani F., Wannmacher C.M., Wajner M., Wyse A.T.S. Effect of hyperprolinemia on acetylcholinesterase and butyrylcholinesterase activities in rat. Amino Acids 2005, 28:305-308.
9. Delwing D., Bavaresco C.S., Monteiro S.C., Matté C., Netto C.A., Wyse A.T.S. Alpha-tocopherol and ascorbic acid prevent memory deficits provoked by chronic hyperprolinemia in rats. Behav Brain Res 2006, 168:185-189.
10. Delwing D., Sanna R.J., Wofchuk S., Wyse A.T.S. Proline promotes decrease in glutamate uptake in slices of cerebral cortex and hippocampus of rats. Life Sci 2007, 81:1645-1650.
11. Di Rosa G., Pustorino G., Spano M., Campion D., Calabrò M., Aguennouz M., et al. Type I hyperprolinemia and proline dehydrogenase (PRODH) mutations in four Italian children with epilepsy and mental retardation. Psychiatr Genet 2008, 18:40-42.
12. 1A receptor agonists and NMDA receptor antagonists in the social interaction test and the elevated plus maze. Eur J Pharmacol 1989, 169:1-10.
13. Egan R.J., Bergner C.L., Hart P.C., Cachat J.M., Canavello P.R., Elegante M.F., et al. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 2009, 205:38-44.
14. Flynn M.P., Martin M.C., Moore P.T., Stafford J.A., Fleming G.A., Phang J.M. Type II hyperprolinaemia in a pedigree of Irish travellers (nomads). Arch Dis Child 1989, 64:1699-1707.
15. Fontaine E., Lentink D., Kranenbarg S., Muller U.K., van Leeuwen J.L., Barr A.H., et al. Automated visual tracking for studying the ontogeny of zebrafish swimming. J Exp Biol 2008, 211:1305-1316.
16. Fremeau R.T.J., Caron M.G., Blakely R.D. Molecular cloning and expression of a high affinity l-proline transporter expressed in putative glutamatergic pathways of rat brain. Neuron 1992, 8:915-926.
17. Ganser L.R., Dallman J.E. Glycinergic synapse development, plasticity, and homeostasis in zebrafish. Front Mol Neurosci 2009, 2:30.
18. Gerlai R., Lahav M., Guo S., Rosenthal A. Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects. Pharmacol Biochem Behav 2000, 67:773-782.
19. Geyer M.A., Krebs-Thomson K., Braff D.L., Swerdlow N.R. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology (Berl) 2001, 156:117-154.
20. Giacomini N.J., Rose B., Kobayashi K., Guo S. Antipsychotics produce locomotor impairment in larval zebrafish. Neurotoxicol Teratol 2006, 28:245-250.
21. Guo S. Linking genes to brain, behavior and neurological diseases: what can we learn from zebrafish?. Genes Brain Behav 2004, 3:63-74.
22. 1A receptors in HEK293 cells. Eur J Pharmacol 2008, 581:37-46.
23. Jacquet H., Demily C., Houy E., Hecketsweiler B., Bou J., Raux G., et al. Hyperprolinemia is a risk factor for schizoaffective disorder. Mol Psychiatry 2005, 10:479-485.
24. 3 receptor antagonist sulpiride on amphetamine-induced changes in striatal extracellular dopamine. Eur J Pharmacol 2001, 418:201-206.
25. Jentsch J.D., Roth R.H. The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1999, 20:201-225.
26. Jones D.N.C., Gartlon J.E., Minassian A., Perry W., Geyer M. Developing new drugs for schizophrenia: from animals to the clinic. Animal and translational models for CNS drug discovery. Psychiatric Disorders 2008, volume 1:199-261. Elsevier, New York. R.A. McArthur, F. Borsini (Eds.).
27. Kabashi E., Champagne N., Brustein E., Drapeau P. In the swim of things: recent insights to neurogenetic disorders from zebrafish. Trends Genet 2010, 26:373-381.
28. Kari G., Rodeck U., Dicker A.P. Zebrafish: an emerging model system for human disease and drug discovery. Clin Pharmacol Ther 2007, 82:70-80.
29. Kessler A., Costabeber E., Dutra-Filho C.S., Wyse A.T.S., Wajner M., Wannmacher C.M.D. Proline reduces creatine kinase activity in the brain cortex of rats. Neurochem Res 2003, 28:1175-1180.
30. Lavergne F., Jay T.M. A new strategy for antidepressant prescription. Front Neurosci 2010, 19:192.
31. Lele Z., Krone P.H. The zebrafish as a model system in developmental, toxicological and transgenic research. Biotech Adv 1996, 14:57-72.
32. Levin E.D., Bencan Z., Cerutti D.T. Anxiolytic effects of nicotine in zebrafish. Physiol Behav 2007, 90:54-58.
33. Linck V.M., Herrmann A.P., Goerck G.C., Iwu M.M., Okunji C.O., Leal M.B., et al. The putative antipsychotic alstonine reverses social interaction withdrawal in mice. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32:1449-1452.
34. Mitsubuchi H., Nakamura K., Matsumoto S., Endo F. Inborn errors of proline metabolism. J Nutr 2008, 138:2016-2020.
35. Moghaddam B. Stress activation of glutamate neurotransmission in the prefrontal cortex: implications for dopamine-associated psychiatric disorders. Biol Psychiatry 2002, 51:775-787.
36. Moghaddam B., Adams B.W. Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 1998, 281:1349-1352.
37. Moreira J.C.F., Wannmacher C.M.D., Costa S.M., Wajner M. Effect of proline administration on rat behavior in aversive and nonaversive tasks. Pharmacol Biochem Behav 1989, 32:885-890.
38. Nadler J.V. Sodium-dependent proline uptake in the rat hippocampal formation: association with ipsilateral-commissural projections of CA3 pyramidal cells. J Neurochem 1987, 49:1155-1160.
39. Nadler J.V., Bray S.D., Evenson D.A. Autoradiographic localization of proline uptake in excitatory hippocampal pathways. Hippocampus 1992, 2:269-278.
40. Norton W., Bally-Cuif L. Adult zebrafish as a model organism for behavioural genetics. BMC Neurosci 2010, 11:90.
41. Oresic M., Tang J., Seppanen-Laakso T., Mattila I., Saarni S.E., Saarni S.I., et al. Metabolome in schizophrenia and other psychotic disorders: a general population-based study. Genome Med 2011, 3:19.
42. Parng C., Seng W.L., Semino C., McGrath P. Zebrafish: a preclinical model for drug screening. Assay Drug Dev Technol 2002, 1:41-48.
43. Paterlini M., Zakharenko S.S., Lai W.S., Qin J., Zhang H., Mukai J., et al. Transcriptional and behavioral interaction between 22q11.2 orthologs modulates schizophrenia-related phenotypes in mice. Nat Neurosci 2005, 8:1586-1594.
44. Pather S., Gerlai R. Shuttle box learning in zebrafish (Danio rerio). Behav Brain Res 2009, 196:323-327.
45. Phang J.M., Hu C.A., Valle D. Disorders of proline and hydroxyproline metabolism. The metabolic and molecular bases of inherited disease 2001, 1821-1838. McGraw-Hill, New York. 8th ed. C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle (Eds.).
46. Piato A.L., Capiotti K.M., Tamborski A.R., Oses J.P., Barcellos L.J., Bogo M.R., et al. Unpredictable chronic stress model in zebrafish (Danio rerio): behavioral and physiological responses. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:561-567.
47. +-ATPase activity in the synaptic plasma membrane from cerebral cortex of rats. Metab Brain Dis 1999, 26:1321-1326.
48. Pontes Z.L., Oliveira L.S., Franzon R., Wajner M., Wannmacher C.M.D., Wyse A.T.S. Inhibition of Na+, K+-ATPase activity from rat hippocampus by proline. Neurochem Res 2001, 26:1321-1326.
49. Renick S.E., Kleven D.T., Chan J., Stenius K., Milner T.A., Pickel V.M., et al. The mammalian brain high-affinity l-proline transporter is enriched preferentially in synaptic vesicles in a subpopulation of excitatory nerve terminals in rat forebrain. J Neurosci 1999, 19:21-33.
50. Rosemberg D.B., Rico E.P., Mussulini B.H., Piato A.L., Calcagnotto M.E., Bonan C.D., et al. 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.
51. Seibt K.J., Oliveira R.L., Zimmermann F.F., Capiotti K.M., Bogo M.R., Ghisleni G., et al. Antipsychotic drugs prevent the motor hyperactivity induced by psychotomimetic MK-801 in zebrafish (Danio rerio). Behav Brain Res 2010, 214:417-422.
52. Seibt K.J., Piato A.L., Oliveira R.L., Capiotti K.M., Vianna M.R., Bonan C.D. Antipsychotic drugs reverse MK-801-induced cognitive and social interaction deficits in zebrafish (Danio rerio). Behav Brain Res 2011, 224:135-139.
53. Skolnick P., Popik P., Trullas R. Glutamate-based antidepressants: 20years on. Trends Pharmacol Sci 2009, 30:563-569.
54. Stewart A., Wong K., Cachat J., Gaikwad S., Kyzar E., Wu N., et al. Zebrafish models to study drug abuse-related phenotypes. Rev Neurosci 2011, 22:95-105.
55. 3 receptors. Eur J Pharmacol 2011, 666:43-52.
56. Van Harreveld A., Fifkova E. Involvement of glutamate in memory formation. Brain Res 1974, 81:455-467.
57. 1 receptor actions on prefrontal neurons engaged in working memory. Nat Neurosci 2007, 10:376-384.
58. Vorstman J.A., Turetsky B.I., Sijmens-Morcus M.E., de Sain M.G., Dorland B., Sprong M., et al. Proline affects brain function in 22q11DS children with the low activity COMT 158 allele. Neuropsychopharmacology 2009, 34:739-746.
59. Westerfield M. The zebrafish book 2007, University of Oregon Press, Eugene. 5th ed.
60. Wyse A.T.S., Netto C.A. Behavioral and neurochemical effects of proline. Metab Brain Dis 2011, 26:159-172.
61. Zon L.I., Peterson R.T. In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 2005, 4:35-44.