Dopaminergic signaling regulates zebrafish larvae's response to electricity.
dopamine
electric response
locomotion
microfluidic
zebrafish
Journal
Biotechnology journal
ISSN: 1860-7314
Titre abrégé: Biotechnol J
Pays: Germany
ID NLM: 101265833
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
revised:
27
02
2022
received:
14
10
2021
accepted:
19
03
2022
pubmed:
26
3
2022
medline:
7
6
2022
entrez:
25
3
2022
Statut:
ppublish
Résumé
Electrical stimulation of brain or muscle activities has gained attention for studying the molecular and cellular mechanisms involved in electric-induced responses. We recently showed zebrafish's response to electricity. Here, we hypothesized that this response is affected by the dopaminergic signaling pathways. The effects of multiple dopamine agonists and antagonists on the electric response of 6 days-postfertilization zebrafish larvae were investigated using a microfluidic device with enhanced control of experimentation and throughput. All dopamine antagonists decreased locomotor activities, while dopamine agonists did not induce similar behaviors. The D2-selective dopamine agonist quinpirole enhanced the movement. Exposure to nonselective and D1-selective dopamine agonists apomorphine and SKF-81297 caused no significant change in the electric response. Exposing larvae that were pretreated with nonselective and D2-selective dopamine antagonists butaclamol and haloperidol to apomorphine and quinpirole, respectively, restored the electric locomotion. These results reveal a correlation between electric response and dopamine signaling pathway. Furthermore, they demonstrate that electric-induced zebrafish larvae locomotion can be conditioned by modulating dopamine receptor functions. Our electrofluidic assay has profound application potential for fundamental electric-induced response research and brain disorder studies especially those related to the dopamine imbalance and as a chemical screening method when investigating biological pathways and behaviors.
Identifiants
pubmed: 35332995
doi: 10.1002/biot.202100561
doi:
Substances chimiques
Dopamine Agonists
0
Dopamine Antagonists
0
Quinpirole
20OP60125T
Apomorphine
N21FAR7B4S
Dopamine
VTD58H1Z2X
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2100561Informations de copyright
© 2022 Wiley-VCH GmbH.
Références
Sui, Y., Tian, Y., Ko, W. K. D., Wang, Z., Jia, F., Horn, A., De Ridder, D., Choi, K. S., Bari, A. A., Wang, S., Hamani, C., Baker, K. B., Machado, A. G., Aziz, T. Z., Fonoff, E. T., Kühn, A. A., Bergman, H., Sanger, T., Liu, H., … Li, L. (2021). Deep brain stimulation initiative: Toward innovative technology, new disease indications, and approaches to current and future clinical challenges in neuromodulation therapy. Frontiers in Neurology, 11, 1-21.
Lozano, A. M., Lipsman, N., Bergman, H., Brown, P., Chabardes, S., Chang, J. W., Matthews, K., McIntyre, C. C., Schlaepfer, T. E., Schulder, M., Temel, Y., Volkmann, J., & Krauss, J. K. (2019). Deep brain stimulation: Current challenges and future directions. Nature Reviews Neurology, 15, 148-160.
Nussbaum, E. L., Houghton, P., Anthony, J., Rennie, S., Shay, B. L., & Hoens, A. M. (2017). Neuromuscular electrical stimulation for treatment of muscle impairment: critical review and recommendations for clinical practice. Physiother. Canada, 69, 1-76.
Ungerstedt, U. (1976). 6-hydroxydopamine-induced degeneration of the nigrostriatal dopamine pathway: The turning syndrome. Pharmacology & therapeutics. Part B, 2, 37-40.
Oberlander, C., Euvrard, C., Dumont, C., & Boissier, J. R. (1979). Circling behaviour induced by dopamine releasers and/or uptake inhibitors during degeneration of the nigrostriatal pathway. European Journal of Pharmacology, 60, 163-170.
Erickstad, M., Hale, L. A., Chalasani, S. H., & Groisman, A. (2015). A microfluidic system for studying the behavior of zebrafish larvae under acute hypoxia. Lab on A Chip, 15, 857-866.
Boehmier, W., Obrecht-Pflumio, S., Canfield, V., Thisse, C. C., Thisse, B., Levenson, R., Boehmler, W., Obrecht-Pflumio, S., Canfield, V., Thisse, C. C., Thisse, B., & Levenson, R. (2004). Dev. Dyn. an Off. Publ. Am. Assoc. Anat., 230, 481-493.
Maximino, C., & Herculano, A. M. (2010). A review of monoaminergic neuropsychopharmacology in zebrafish. Zebrafish, 7, 359-378.
Irons, T. D. D., Kelly, P. E., Hunterb, D. L., MacPhail, R. C. C., Padilla, S., Hunter, D. L., MacPhail, R. C. C., & Padilla, S. (2013). Acute administration of dopaminergic drugs has differential effects on locomotion in larval zebrafish. Pharmacology Biochemistry and Behavior, 103, 792-813.
Souza, B. R., Romano-Silva, M. A., & Tropepe, V. (2011). Dopamine D2 receptor activity modulates akt signaling and alters GABAergic neuron development and motor behavior in zebrafish larvae. Journal of Neuroscience, 31, 5512-5525.
Seibt, K. J., Piato, A. L., da Luz Oliveira, R., Capiotti, K. M., Vianna, M. R., & Bonan, C. D. (2011). Antipsychotic drugs reverse MK-801-induced cognitive and social interaction deficits in zebrafish (Danio rerio). Behavioural Brain Research, 224, 135-139.
Savio, L. E. B., Vuaden, F. C., Piato, A. L., Bonan, C. D., & Wyse, A. T. S. (2012). Behavioral changes induced by long-term proline exposure are reversed by antipsychotics in zebrafish. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 36, 258-263.
Kokel, D., & Peterson, R. T. (2008). Chemobehavioural phenomics and behaviour-based psychiatric drug discovery in the zebrafish. Briefings in Functional Genomics Proteomics, 7, 483-490.
Giacomini, N. J., Rose, B., Kobayashi, K., & Guo, S. (2006). Antipsychotics produce locomotor impairment in larval zebrafish. Neurotoxicology and Teratology, 28, 245-250.
Farrell, T. C., Cario, C. L., Milanese, C., Vogt, A., Jeong, J. - H., & Burton, E. A. (2011). Evaluation of spontaneous propulsive movement as a screening tool to detect rescue of Parkinsonism phenotypes in zebrafish models. Neurobiology of Disease, 44, 9-18.
Boehmler, W., Carr, T., Thisse, C., Thisse, B., Canfield, V. A., & Levenson, R. (2007). D4 Dopamine receptor genes of zebrafish and effects of the antipsychotic clozapine on larval swimming behaviour. Genes, Brain, and Behavior, 6, 155-166.
Burgess, H. A., & Granato, M. (2007). Modulation of locomotor activity in larval zebrafish during light adaptation. Journal of Experimental Biology, 210, 2526-2539.
Lin, X., Li, V. W. T., Chen, S., Chan, C. Y., Cheng, S. H., & Shi, P. (2016). Autonomous system for cross-organ investigation of ethanol-induced acute response in behaving larval zebrafish. Biomicrofluidics, 10, 024123-1.
Rudin-Bitterli, T. S., Tills, O., Spicer, J. I., Culverhouse, P. F., Wielhouwer, E. M., Richardson, M. K., Rundle, S. D., & Tanguay, R. L. (2014). Combining motion analysis and microfluidics a-novel approach for detecting whole-animal responses to test substances. Plos One, 9, e113235.
Peimani, A. R., Zoidl, G., & Rezai, P. (2018). A microfluidic device to study electrotaxis and dopaminergic system of zebrafish larvae. Biomicrofluidics, 12, 1-15.
Nady, A., Peimani, A. R., Zoidl, G., & Rezai, P. (2017). A microfluidic device for partial immobilization, chemical exposure and behavioural screening of zebrafish larvae. Lab on A Chip, 17, 4048-4058.
Candelier, R., Sriti Murmu, M., Alejo Romano, S., Jouary, A., Debrégeas, G., & Sumbre, G. (2015). A microfluidic device to study neuronal and motor responses to acute chemical stimuli in zebrafish. Science Reports, 5, 1-10.
Khalili, A., Peimani, A. R., Safarian, N., Youssef, K., Zoidl, G., & Rezai, P. (2019). Phenotypic chemical and mutant screening of zebrafish larvae using an on-demand response to electric stimulation. Integrative Biology, 11, 373-383.
Khalili, A., van Wijngaarden, E., Youssef, K., Zoidl, G., & Rezai, P. (2022). Designing microfluidic devices for behavioral screening of multiple zebrafish larvae. Biotechnology Journal, 17, 2100076.
Yokogawa, T., Iadarola, M., & Burgess, H. (2014). In Proceedings of Measuring Behavior (pp. 1-2). Wageningen, The Netherlands.
Redd, M. J., Kelly, G., Dunn, G., Way, M., & Martin, P. (2006). Imaging macrophage chemotaxis in vivo: Studies of microtubule function in zebrafish wound inflammation. Cell Motility and the Cytoskeleton, 63, 415-422.
Peimani, A. R., Zoidl, G., & Rezai, P. (2017). A microfluidic device for quantitative investigation of zebrafish larvae's rheotaxis. Biomedical Microdevices, 19, 1-6.
Tabor, K. M., Bergeron, S. A., Horstick, E. J., Jordan, D. C., Aho, V., Porkka-Heiskanen, T., Haspel, G., & Burgess, H. A. (2014). Direct activation of the Mauthner cell by electric field pulses drives ultrarapid escape responses. Journal of Neurophysiology, 112, 834-844.
Steenbergen, P. J. (2018). Response of zebrafish larvae to mild electrical stimuli: A 96-well setup for behavioural screening. Journal of Neuroscience Methods, 301, 52-61.
Bartolini, T., Mwaffo, V., Butail, S., & Porfiri, M. (2015). Effect of acute ethanol administration on zebrafish tail-beat motion. Alcohol, 49, 721-725.
Morgan, R. P., Ulanowicz, R. E., Rasin, V. J., Noe, L. A., & Gray, G. B. (1976). Effects of shear on eggs and larvae of striped bass, morone saxatilis, and white perch, m. americana. Transactions of the American Fisheries Society, 105, 149-154.
Ulanowicz, R. E. (1976). The mechanical effects of water flow on fish eggs and larvae. Fish. energy Prod. a Symp, 1, 77-87.
Ek, F., Malo, M., Åberg Andersson, M., Wedding, C., Kronborg, J., Svensson, P., Waters, S., Petersson, P., & Olsson, R. (2016). Behavioral analysis of dopaminergic activation in zebrafish and rats reveals similar phenotypes. ACS Chemical Neuroscience, 7, 633-646.
Peimani, A. R., Zoidl, G., & Rezai, P. (2018). A microfluidic device to study electrotaxis and dopaminergic system of zebrafish larvae. Biomicrofluidics, 12, 014113-1.
Outeiro, T. F., & Ferreira, J. J. (2018). Zebrafish as an animal model for drug discovery in Parkinson's disease and other movement disorders: A systematic review. Frontiers in Neurology, 9, 1-23.
Jauhar, S., Veronese, M., Rogdaki, M., Bloom, M., Natesan, S., Turkheimer, F., Kapur, S., & Howes, O. D. (2017). Regulation of dopaminergic function: an [18F]-DOPA PET apomorphine challenge study in humans. Translational Psychiatry, 1-7.
Nyberg, S., Chou, Y., & Halldin, C. (2002). Saturation of striatal D2 dopamine receptors by clozapine. The International Journal of Neuropsychopharmacology, 5, 11-16.
Voith, K., & Herr, F. (1975). The behavioral pharmacology of butaclamol hydrochloride (AY-23,028), a new potent neuroleptic drug. Psychopharmacologia, 42, 11-20.
Bergman, J., Madras, B. K., & Spealman, R. D. (1991). Behavioral effects of D1 and D2 dopamine receptor antagonists in squirrel monkeys. Journal of Pharmacology and Experimental Therapeutics, 258, 910-917.
Beninger, R. J., Mazurski, E. J., & Hoffman, D. C. (1991). Receptor subtype-specific dopaminergic agents and unconditioned behavior. Polish Journal of Pharmacology and Pharmacy, 43, 507-528.
Morato, G. S., Lemos, T., & Takahashi, R. N. (1989). Acute exposure to maneb alters some behavioral functions in the mouse. Neurotoxicology and Teratology, 11, 421-425.
Choi, W. Y., Morvan, C., Balsam, P. D., & Horvitz, J. C. (2009). Dopamine D1 and D2 antagonist effects on response likelihood and duration. Behavioral Neuroscience, 123, 1279-1287.
King, D. J., Lucas, M. B., & Lucas, R. A. (1995). Antipsychotic drug-induced dysphoria. British Journal of Psychiatry, 167, 480-482.
Spulber, S., Kilian, P., Ibrahim, W. N. W., Onishchenko, N., Ulhaq, M., Norrgren, L., Negri, S., Di Tuccio, M., & Ceccatelli, S. (2014). PFOS induces behavioral alterations, including spontaneous hyperactivity that is corrected by dexamfetamine in zebrafish larvae. Plos One, 9, e94227.
Dracheva, S., Xu, M., Kelley, K. A., Haroutunian, V., Holstein, G. R., Haun, S., Silverstein, J. H., & Sealfon, S. C. (1999). Paradoxical locomotor behavior of dopamine d1 receptor transgenic mice. Experimental Neurology, 157, 169-179.
Xu, M., Moratalla, R., Gold, L. H., Hiroi, N., Koob, G. F., & Graybiel, A. M. (1994). 79, 729-742.
White, N. M., Packard, M. G., & Hiroi, N. (1991). Place conditioning with dopamine D1 and D2 agonists injected peripherally or into nucleus accumbens. Psychopharmacology (Berl), 103, 271-276.
Shieh, G. J., & Walters, D. E. (1996). Stimulating dopamine D1 receptors increases the locomotor activity of developing rats. European Journal of Pharmacology, 311, 103-107.
Scott, L., Forssberg, H., Aperia, A., & Diaz-heijtz, R. (2005). 58, 779-783.
Chausmer, A. L., & Katz, J. L. (2002). Comparison of interactions of D1-like agonists, SKF 81297, SKF 82958 and A-77636, with cocaine: Locomotor activity and drug discrimination studies in rodents. Psychopharmacology (Berl), 159, 145-153.
Sobrian, S. K., Jones, B. L., Varghese, S., & Holson, R. R. (2003). Behavioral response profiles following drug challenge with dopamine receptor subtype agonists and antagonists in developing rat. Neurotoxicology and Teratology, 25, 311-328.
Millan, M. J., Maiofiss, L., Cussac, D., Audinot, V., Boutin, J. - A., & Newman-Tancredi, A. (2002). Differential actions of antiparkinson agents at multiple classes of monoaminergic receptor. I. A multivariate analysis of the binding profiles of 14 drugs at 21 native and cloned human receptor subtypes. Journal of Pharmacology and Experimental Therapeutics, 303, 791-804.
Hyttel, J. (1983). SCH 23390: The first selective dopamine D-1 antagonist. European Journal of Pharmacology, 91, 153-154.
Bymaster, F. P., Calligaro, D. O., Falcone, J. F., Marsh, R. D., Moore, N. A., Tye, N. C., Seeman, P., & Wong, D. T. (1996). Radioreceptor binding profile of the atypical antipsychotic olanzapine. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol, 14, 87-96.