Skip to main content
Log in

Developing Peripheral Biochemical Biomarkers of Brain Disorders: Insights from Zebrafish Models

  • REVIEW
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

High prevalence of human brain disorders necessitates development of the reliable peripheral biomarkers as diagnostic and disease-monitoring tools. In addition to clinical studies, animal models markedly advance studying of non-brain abnormalities associated with brain pathogenesis. The zebrafish (Danio rerio) is becoming increasingly popular as an animal model organism in translational neuroscience. These fish share some practical advantages over mammalian models together with high genetic homology and evolutionarily conserved biochemical and neurobehavioral phenotypes, thus enabling large-scale modeling of human brain diseases. Here, we review mounting evidence on peripheral biomarkers of brain disorders in zebrafish models, focusing on altered biochemistry (lipids, carbohydrates, proteins, and other non-signal molecules, as well as metabolic reactions and activity of enzymes). Collectively, these data strongly support the utility of zebrafish (from a systems biology standpoint) to study peripheral manifestations of brain disorders, as well as highlight potential applications of biochemical biomarkers in zebrafish models to biomarker-based drug discovery and development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Abbreviations

ATP:

adenosine triphosphate

CNS:

central nervous system

EEG:

electroencephalography

GABA:

γ-aminobutyric acid

NPC:

Niemann–Pick type C

PLP:

pyridoxal 5′-phosphate

PLPBP:

PLP-binding protein

PNPO:

pyridoxamine 5′-phosphate oxidase

References

  1. Feigin, V. L., Nichols, E., Alam, T., Bannick, M. S., Beghi, E., Blake, N., and Ellenbogen, R. G. (2019) Global, regional, and national burden of neurological disorders, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016, Lancet Neurol., 18, 459-480, https://doi.org/10.1016/S1474-4422(18)30499-X.

    Article  Google Scholar 

  2. Vigo, D., Thornicroft, G., and Atun, R. (2016) Estimating the true global burden of mental illness, Lancet Psychiatry, 3, 171-178, https://doi.org/10.1016/S2215-0366(15)00505-2.

    Article  PubMed  Google Scholar 

  3. Hayashi-Takagi, A., Vawter, M. P., and Iwamoto, K. (2014) Peripheral biomarkers revisited: integrative profiling of peripheral samples for psychiatric research, Biol. Psychiatry, 75, 920-928, https://doi.org/10.1016/j.biopsych.2013.09.035.

    Article  CAS  PubMed  Google Scholar 

  4. Htike, T. T., Mishra, S., Kumar, S., Padmanabhan, P., and Gulyás, B. (2019) Peripheral biomarkers for early detection of Alzheimer’s and Parkinson’s diseases, Mol. Neurobiol., 56, 2256-2277, https://doi.org/10.1007/s12035-018-1151-4.

    Article  CAS  PubMed  Google Scholar 

  5. Tomasik, J., Han, S. Y. S., Barton-Owen, G., Mirea, D. M., Martin-Key, N. A., Rustogi, N., Lago, S. G., Olmert, T., Cooper, J. D., and Ozcan, S. (2021) A machine learning algorithm to differentiate bipolar disorder from major depressive disorder using an online mental health questionnaire and blood biomarker data, Translat. Psychiatry, 11, 41, https://doi.org/10.1038/s41398-020-01181-x.

    Article  Google Scholar 

  6. Chmielewska, N., Szyndler, J., Makowska, K., Wojtyna, D., Maciejak, P., and Płaźnik, A. (2018) Looking for novel, brain-derived, peripheral biomarkers of neurological disorders, Neurol. Neurochirurg. Polska, 52, 318-325, https://doi.org/10.1016/j.pjnns.2018.02.002.

    Article  Google Scholar 

  7. Lopresti, A. L., Maker, G. L., Hood, S. D., and Drummond, P. D. (2014) A review of peripheral biomarkers in major depression: the potential of inflammatory and oxidative stress biomarkers, Progr. Neuro Psychopharmacol. Biol. Psychiatry, 48, 102-111, https://doi.org/10.1016/j.pnpbp.2013.09.017.

    Article  Google Scholar 

  8. Porter, F. D., Scherrer, D. E., Lanier, M. H., Langmade, S. J., Molugu, V., Gale, S. E., and Fu, R. (2010) Cholesterol oxidation products are sensitive and specific blood-based biomarkers for Niemann-Pick C1 disease, Sci. Translat. Med., 2, 56ra81, https://doi.org/10.1126/scitranslmed.3001417.

    Article  CAS  Google Scholar 

  9. Birmpili, D., Charmarke Askar, I., Bigaut, K., and Bagnard, D. (2022) The translatability of multiple sclerosis animal models for biomarkers discovery and their clinical use, Int. J. Mol. Sci., 23, 11532, https://doi.org/10.3390/ijms231911532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. McGonigle, P. (2014) Animal models of CNS disorders, Biochem. Pharmacol., 87, 140-149, https://doi.org/10.1016/j.bcp.2013.06.016.

    Article  CAS  PubMed  Google Scholar 

  11. Murtazina, A. R., Bondarenko, N. S., Pronina, T. S., Chandran, K. I., Bogdanov, V. V., Dilmukhametova, L. K., and Ugrumov, M. V. (2021) A comparative analysis of CSF and the blood levels of monoamines as neurohormones in rats during ontogenesis, Acta Naturae, 13, 89-97, https://doi.org/10.32607/actanaturae.11516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Carboni, L. (2013) Peripheral biomarkers in animal models of major depressive disorder, Dis. Markers, 35, 33-41, https://doi.org/10.1155/2013/284543.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ugrumov, M. (2020) Development of early diagnosis of Parkinson’s disease: illusion or reality? CNS Neurosci. Ther., 26, 997-1009, https://doi.org/10.1111/cns.13429.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sabbagh, J. J., Kinney, J. W., and Cummings, J. L. (2013) Animal systems in the development of treatments for Alzheimer’s disease: challenges, methods, and implications, Neurobiol. Aging, 34, 169-183, https://doi.org/10.1016/j.neurobiolaging.2012.02.027.

    Article  PubMed  Google Scholar 

  15. Ugrumov, M. (2023) Preclinical diagnosis of Parkinson’s disease: upgraded and new approaches, Parkinsonism Rel. Disord., 113, https://doi.org/10.1016/j.parkreldis.2023.105547.

    Article  Google Scholar 

  16. Costa, F. V., Zabegalov, K. N., Kolesnikova, T. O., de Abreu, M. S., Kotova, M. M., Petersen, E. V., and Kalueff, A. V. (2023) Experimental models of human cortical malformations: from mammals to 'acortical' zebrafish, Neurosci. Biobehav. Rev., 155, 105429, https://doi.org/10.1016/j.neubiorev.2023.105429.

    Article  PubMed  Google Scholar 

  17. De Abreu, M. S., Demin, K. A., Kotova, M. M., Mirzaei, F., Shariff, S., Kantawala, B., Zakharchenko, K. V., Kolesnikova, T. O., Dilbaryan, K., and Grigoryan, A. (2023) Developing novel experimental models of m-TORopathic epilepsy and related neuropathologies: translational insights from zebrafish, Int. J. Mol. Sci., 24, 1530, https://doi.org/10.3390/ijms24021530.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Krotova, N. A., Lakstygal, A. M., Taranov, A. S., Ilyin, N. P., Bytov, M. V., Volgin, A. D., Amstislavskaya, T. G., Demin, K. A., and Kaluev, A. V. (2019) Zebrafish as a new prospective model in translational neurobiology, Russ. J. Physiol., 105, 1417-1435.

    Google Scholar 

  19. Maslov, G. O., Zabegalov, K. N., Demin, K. A., Kolesnikova, T. O., Kositsyn, Y. M., de Abreu, M. S., Petersen, E. V., and Kalueff, A. V. (2023) Towards experimental models of delirium utilizing zebrafish, Behav. Brain Res., 453, 114607, https://doi.org/10.1016/j.bbr.2023.114607.

    Article  PubMed  Google Scholar 

  20. Zabegalov, K. N., Costa, F., Viktorova, Y. A., Maslov, G. O., Kolesnikova, T. O., Gerasimova, E. V., Grinevich, V. P., Budygin, E. A., and Kalueff, A. V. (2023) Behavioral profile of adult zebrafish acutely exposed to a selective dopamine uptake inhibitor, GBR 12909, J. Psychopharmacol., 37, 601-609, https://doi.org/10.1177/02698811231166463.

    Article  CAS  PubMed  Google Scholar 

  21. Wendler, A., and Wehling, M. (2010) The translatability of animal models for clinical development: biomarkers and disease models, Curr. Opin. Pharmacol., 10, 601-606, https://doi.org/10.1016/j.coph.2010.05.009.

    Article  CAS  PubMed  Google Scholar 

  22. Manger, P., Cort, J., Ebrahim, N., Goodman, A., Henning, J., Karolia, M., and Strkalj, G. (2008) Is 21st century neuroscience too focussed on the rat/mouse model of brain function and dysfunction? Front. Neuroanat., 2, 5, https://doi.org/10.3389/neuro.05.005.2008.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Burne, T., Scott, E., van Swinderen, B., Hilliard, M., Reinhard, J., Claudianos, C., and McGrath, J. (2011) Big ideas for small brains: what can psychiatry learn from worms, flies, bees and fish? Mol. Psychiatry, 16, 7-16, https://doi.org/10.1038/mp.2010.35.

    Article  CAS  PubMed  Google Scholar 

  24. Kalueff, A., Wheaton, M., and Murphy, D. (2007) What's wrong with my mouse model?: Advances and strategies in animal modeling of anxiety and depression, Behav. Brain Res., 179, 1-18, https://doi.org/10.1016/j.bbr.2007.01.023.

    Article  CAS  PubMed  Google Scholar 

  25. Kalueff, A. V., Echevarria, D. J., and Stewart, A. M. (2014) Gaining translational momentum: more zebrafish models for neuroscience research, Prog. Neuropsychopharmacol. Biol. Psychiatry, 55, 1-6, https://doi.org/10.1016/j.pnpbp.2014.01.022.

    Article  PubMed  Google Scholar 

  26. Stewart, A. M., Braubach, O., Spitsbergen, J., Gerlai, R., and Kalueff, A. V. (2014) Zebrafish models for translational neuroscience research: from tank to bedside, Trends Neurosci., 37, 264-278, https://doi.org/10.1016/j.tins.2014.02.011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Gerlai, R. (2020) Evolutionary conservation, translational relevance and cognitive function: the future of zebrafish in behavioral neuroscience, Neurosci. Biobehav. Rev., 116, 426-435, https://doi.org/10.1016/j.neubiorev.2020.07.009.

    Article  PubMed  Google Scholar 

  28. Fontana, B. D., Mezzomo, N. J., Kalueff, A. V., and Rosemberg, D. B. (2018) The developing utility of zebrafish models of neurological and neuropsychiatric disorders: a critical review, Exp. Neurol., 299, 157-171, https://doi.org/10.1016/j.expneurol.2017.10.004.

    Article  PubMed  Google Scholar 

  29. Meshalkina, D. A., Kysil, E. V., Warnick, J. E., Demin, K. A., and Kalueff, A. V. (2017) Adult zebrafish in CNS disease modeling: a tank that’s half-full, not half-empty, and still filling, Lab. Animal, 46, 378-387, https://doi.org/10.1038/laban.1345.

    Article  PubMed  Google Scholar 

  30. Kalueff, A. V., Stewart, A. M., and Gerlai, R. (2014) Zebrafish as an emerging model for studying complex brain disorders, Trends Pharmacol. Sci., 35, 63-75, https://doi.org/10.1016/j.tips.2013.12.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Woods, I. G., Kelly, P. D., Chu, F., Ngo-Hazelett, P., Yan, Y. L., Huang, H., and Talbot, W. S. (2000) A comparative map of the zebrafish genome, Genome Res., 10, 1903-1914, https://doi.org/10.1101/gr.164600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Howe, K., Clark, M. D., Torroja, C. F., Torrance, J., Berthelot, C., Muffato, M., and Matthews, L. (2013) The zebrafish reference genome sequence and its relationship to the human genome, Nature, 496, 498-503, https://doi.org/10.1038/nature12111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Varshney, G. K., Sood, R., and Burgess, S. M. (2015) Understanding and editing the zebrafish genome, Adv. Genet., 92, 1-52, https://doi.org/10.1016/bs.adgen.2015.09.002.

    Article  CAS  PubMed  Google Scholar 

  34. Lessman, C. A. (2011) The developing zebrafish (Danio rerio): A vertebrate model for high-throughput screening of chemical libraries, Birth Defects Res. Part C Embryo Today Rev., 93, 268-280, https://doi.org/10.1002/bdrc.20212.

    Article  CAS  Google Scholar 

  35. Postlethwait, J. H. (2007) The zebrafish genome in context: Ohnologs gone missing, J. Exp. Zool. B Mol. Dev. Evol., 308, 563-577, https://doi.org/10.1002/jez.b.21137.

    Article  CAS  PubMed  Google Scholar 

  36. Bayés, À., Collins, M. O., Reig-Viader, R., Gou, G., Goulding, D., Izquierdo, A., Choudhary, J. S., Emes, R. D., and Grant, S. G. (2017) Evolution of complexity in the zebrafish synapse proteome, Nat. Commun., 8, 14613, https://doi.org/10.1038/ncomms14613.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Butler, A. B. (2000) Topography and topology of the teleost telencephalon: A paradox resolved, Neurosci. Lett., 293, 95-98, https://doi.org/10.1016/S0304-3940(00)01497-X.

    Article  CAS  PubMed  Google Scholar 

  38. Du, Y., Guo, Q., Shan, M., Wu, Y., Huang, S., Zhao, H., Hong, H., Yang, M., Yang, X., and Ren, L. (2016) Spatial and temporal distribution of dopaminergic neurons during development in zebrafish, Front. Neuroanat., 10, 115, https://doi.org/10.3389/fnana.2016.00115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Glasauer, S. M., and Neuhauss, S. C. (2014) Whole-genome duplication in teleost fishes and its evolutionary consequences, Mol. Genet. Genomics, 289, 1045-1060, https://doi.org/10.1007/s00438-014-0889-2.

    Article  CAS  PubMed  Google Scholar 

  40. Sison, M., Cawker, J., Buske, C., and Gerlai, R. (2006) Fishing for genes influencing vertebrate behavior: Zebrafish making headway, Lab Animal, 35, 33-39, https://doi.org/10.1038/laban0506-33.

    Article  PubMed  Google Scholar 

  41. Zambusi, A., and Ninkovic, J. (2020) Regeneration of the central nervous system-principles from brain regeneration in adult zebrafish, World J. Stem Cells, 12, 8, https://doi.org/10.4252/wjsc.v12.i1.8.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Facciol, A., and Gerlai, R. (2020) Zebrafish shoaling, its behavioral and neurobiological mechanisms, and its alteration by embryonic alcohol exposure: a review, Front. Behav. Neurosci., 14, 572175, https://doi.org/10.3389/fnbeh.2020.572175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Edson, A. J., Hushagen, H. A., Frøyset, A. K., Elda, I., Khan, E. A., Di Stefano, A., and Fladmark, K. E. (2019) Dysregulation in the brain protein profile of zebrafish lacking the Parkinson’s disease-related protein DJ-1, Mol. Neurobiol., 56, 8306-8322, https://doi.org/10.1007/s12035-019-01667-w.

    Article  CAS  PubMed  Google Scholar 

  44. Wang, Y., Liu, W., Yang, J., Wang, F., Sima, Y., Zhong, Z. M., and Liu, C. F. (2017) Parkinson’s disease-like motor and non-motor symptoms in rotenone-treated zebrafish, Neurotoxicology, 58, 103-109, https://doi.org/10.1016/j.neuro.2016.11.006.

    Article  CAS  PubMed  Google Scholar 

  45. Baraban, S. C., Taylor, M., Castro, P., and Baier, H. (2005) Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression, Neuroscience, 131, 759-768, https://doi.org/10.1016/j.neuroscience.2004.11.031.

    Article  CAS  PubMed  Google Scholar 

  46. Wong, K., Stewart, A., Gilder, T., Wu, N., Frank, K., Gaikwad, S., and Chang, K. (2010) Modeling seizure-related behavioral and endocrine phenotypes in adult zebrafish, Brain Res., 1348, 209-215, https://doi.org/10.1016/j.brainres.2010.06.012.

    Article  CAS  PubMed  Google Scholar 

  47. Gan, D., Wu, S., Chen, B., and Zhang, J. (2020) Application of the zebrafish traumatic brain injury model in assessing cerebral inflammation, Zebrafish, 17, 73-82, https://doi.org/10.1089/zeb.2019.1793.

    Article  CAS  PubMed  Google Scholar 

  48. Ilyin, N. P., Galstyan, D. S., Demin, K. A., and Kalueff, A. V. (2023) Behavioral, genomic and neurochemical deficits evoked by neurotrauma in adult zebrafish (Danio rerio), Russ. J. Physiol., 109, 1-19.

    Google Scholar 

  49. Leclercq, K., Afrikanova, T., Langlois, M., De Prins, A., Buenafe, O. E., Rospo, C. C., and Smolders, I. (2015) Cross-species pharmacological characterization of the allylglycine seizure model in mice and larval zebrafish, Epilepsy Behav., 45, 53-63, https://doi.org/10.1016/j.yebeh.2015.03.019.

    Article  PubMed  Google Scholar 

  50. Piato, Â. L., Capiotti, K. M., Tamborski, A. R., Oses, J. P., Barcellos, L. J., Bogo, M. R., and Bonan, C. D. (2011) Unpredictable chronic stress model in zebrafish (Danio rerio): behavioral and physiological responses, Progr. Neuro Psychopharmacol. Biol. Psychiatry, 35, 561-567, https://doi.org/10.1016/j.pnpbp.2010.12.018.

    Article  CAS  Google Scholar 

  51. Shams, S., Chatterjee, D., and Gerlai, R. (2015) Chronic social isolation affects thigmotaxis and whole-brain serotonin levels in adult zebrafish, Behav. Brain Res., 292, 283-287, https://doi.org/10.1016/j.bbr.2015.05.061.

    Article  CAS  PubMed  Google Scholar 

  52. Mushtaq, M. Y., Marçal, R. M., Champagne, D. L., Van Der Kooy, F., Verpoorte, R., and Choi, Y. H. (2014) Effect of acute stresses on zebra fish (Danio rerio) metabolome measured by NMR-based metabolomics, Planta Medica, 80, 1227-1233, https://doi.org/10.1055/s-0034-1382878.

    Article  CAS  PubMed  Google Scholar 

  53. Magdeldin, S., Blaser, R. E., Yamamoto, T., and Yates Iii, J. R. (2015) Behavioral and proteomic analysis of stress response in zebrafish (Danio rerio), J. Proteome Res., 14, 943-952, https://doi.org/10.1021/pr500998e.

    Article  CAS  PubMed  Google Scholar 

  54. Geary, B., Magee, K., Cash, P., Husi, H., Young, I. S., Whitfield, P. D., and Doherty, M. K. (2019) Acute stress alters the rates of degradation of cardiac muscle proteins, J. Proteomics, 191, 124-130, https://doi.org/10.1016/j.jprot.2018.03.015.

    Article  CAS  PubMed  Google Scholar 

  55. Lin, Y., Cai, X., Wang, G., Ouyang, G., and Cao, H. (2018) Model construction of Niemann-Pick type C disease in zebrafish, Biol. Chem., 399, 903-910, https://doi.org/10.1515/hsz-2018-0118.

    Article  CAS  PubMed  Google Scholar 

  56. Louwette, S., Régal, L., Wittevrongel, C., Thys, C., Vandeweeghde, G., Decuyper, E., and Jaeken, J. (2013) NPC1 defect results in abnormal platelet formation and function: studies in Niemann–Pick disease type C1 patients and zebrafish, Human Mol. Genet., 22, 61-73, https://doi.org/10.1093/hmg/dds401.

    Article  CAS  Google Scholar 

  57. Majewski, L., Adamek-Urbanska, D., Wasilewska, I., and Kuznicki, J. (2021) npc2-deficient zebrafish reproduce neurological and inflammatory symptoms of Niemann-Pick type C disease, Front. Cell. Neurosci., 15, 131, https://doi.org/10.3389/fncel.2021.647860.

    Article  CAS  Google Scholar 

  58. Tseng, W. C., Johnson Escauriza, A. J., Tsai-Morris, C. H., Feldman, B., Dale, R. K., Wassif, C. A., and Porter, F. D. (2021) The role of Niemann–Pick type C2 in zebrafish embryonic development, Development, 148, dev194258, https://doi.org/10.1242/dev.194258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Tseng, W. C., Loeb, H. E., Pei, W., Tsai-Morris, C. H., Xu, L., Cluzeau, C. V., and Pavan, W. J. (2018) Modeling Niemann-Pick disease type C1 in zebrafish: a robust platform for in vivo screening of candidate therapeutic compounds, Dis. Model. Mech., 11, dmm034165, https://doi.org/10.1242/dmm.034165.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Liang, X., Cao, S., Xie, P., Hu, X., Lin, Y., and Liang, J. (2021) Three-dimensional imaging of whole-body zebrafish revealed lipid disorders associated with Niemann–Pick disease type C1, Anal. Chem., 93, 8178-8187, https://doi.org/10.1021/acs.analchem.1c00196.

    Article  CAS  PubMed  Google Scholar 

  61. Banerji, R., Huynh, C., Figueroa, F., Dinday, M. T., Baraban, S. C., and Patel, M. (2021) Enhancing glucose metabolism via gluconeogenesis is therapeutic in a zebrafish model of Dravet syndrome, Brain Commun., 3, fcab004, https://doi.org/10.1093/braincomms/fcab004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Grone, B. P., Marchese, M., Hamling, K. R., Kumar, M. G., Krasniak, C. S., Sicca, F., and Baraban, S. C. (2016) Epilepsy, behavioral abnormalities, and physiological comorbidities in syntaxin-binding protein 1 (STXBP1) mutant zebrafish, PLoS One, 11, e0151148, https://doi.org/10.1371/journal.pone.0151148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Kumar, M. G., Rowley, S., Fulton, R., Dinday, M. T., Baraban, S. C., and Patel, M. (2016) Altered glycolysis and mitochondrial respiration in a zebrafish model of Dravet syndrome, ENeuro, 3, ENEURO.0008-16.2016, https://doi.org/10.1523/ENEURO.0008-16.2016.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Ibhazehiebo, K., Gavrilovici, C., de la Hoz, C. L., Ma, S. C., Rehak, R., Kaushik, G., and Kim, D. Y. (2018) A novel metabolism-based phenotypic drug discovery platform in zebrafish uncovers HDACs 1 and 3 as a potential combined anti-seizure drug target, Brain, 141, 744-761, https://doi.org/10.1093/brain/awx364.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Ciapaite, J., Albersen, M., Savelberg, S. M., Bosma, M., Tessadori, F., Gerrits, J., and Zwartkruis, F. J. (2020) Pyridox(am)ine 5′-phosphate oxidase (PNPO) deficiency in zebrafish results in fatal seizures and metabolic aberrations, Biochim. Biophys. Acta, 1866, 165607, https://doi.org/10.1016/j.bbadis.2019.165607.

    Article  CAS  Google Scholar 

  66. Johnstone, D. L., Al-Shekaili, H. H., Tarailo-Graovac, M., Wolf, N. I., Ivy, A. S., Demarest, S., and Kernohan, K. D. (2019) PLPHP deficiency: clinical, genetic, biochemical, and mechanistic insights, Brain, 142, 542-559, https://doi.org/10.1093/brain/awy346.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Pena, I. A., Roussel, Y., Daniel, K., Mongeon, K., Johnstone, D., Weinschutz Mendes, H., and Chakraborty, P. (2017) Pyridoxine-dependent epilepsy in zebrafish caused by Aldh7a1 deficiency, Genetics, 207, 1501-1518, https://doi.org/10.1534/genetics.117.300137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Zabinyakov, N., Bullivant, G., Cao, F., Fernandez Ojeda, M., Jia, Z. P., Wen, X. Y., and Mercimek-Andrews, S. (2017) Characterization of the first knock-out aldh7a1 zebrafish model for pyridoxine-dependent epilepsy using CRISPR-Cas9 technology, PLoS One, 12, e0186645, https://doi.org/10.1371/journal.pone.0186645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Minenkova, A., Jansen, E. E., Cameron, J., Barto, R., Hurd, T., MacNeil, L., and Mercimek-Andrews, S. (2021) Is impaired energy production a novel insight into the pathogenesis of pyridoxine-dependent epilepsy due to biallelic variants in ALDH7A1? PLoS One, 16, e0257073, https://doi.org/10.1371/journal.pone.0257073.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Pinho, B. R., Reis, S. D., Guedes-Dias, P., Leitão-Rocha, A., Quintas, C., Valentão, P., and Oliveira, J. M. (2016) Pharmacological modulation of HDAC1 and HDAC6 in vivo in a zebrafish model: therapeutic implications for Parkinson’s disease, Pharmacol. Res., 103, 328-339, https://doi.org/10.1016/j.phrs.2015.11.024.

    Article  CAS  PubMed  Google Scholar 

  71. Wang, X. H., Souders Ii, C. L., Zhao, Y. H., and Martyniuk, C. J. (2018) Paraquat affects mitochondrial bioenergetics, dopamine system expression, and locomotor activity in zebrafish (Danio rerio), Chemosphere, 191, 106-117, https://doi.org/10.1016/j.chemosphere.2017.10.032.

    Article  CAS  PubMed  Google Scholar 

  72. Díaz-Casado, M. E., Lima, E., García, J. A., Doerrier, C., Aranda, P., Sayed, R. K., and Acuña-Castroviejo, D. (2016) Melatonin rescues zebrafish embryos from the parkinsonian phenotype restoring the parkin/PINK 1/DJ-1/MUL 1 network, J. Pineal Res., 61, 96-107, https://doi.org/10.1111/jpi.12332.

    Article  CAS  PubMed  Google Scholar 

  73. Cansız, D., Ünal, İ., Üstündağ, Ü. V., Alturfan, A. A., Altinoz, M. A., Elmacı, İ., and Emekli-Alturfan, E. (2021) Caprylic acid ameliorates rotenone induced inflammation and oxidative stress in the gut-brain axis in Zebrafish, Mol. Biol. Rep., 48, 5259-5273, https://doi.org/10.1007/s11033-021-06532-5.

    Article  CAS  PubMed  Google Scholar 

  74. Ünal, İ., Üstündağ, Ü. V., Ateş, P. S., Eğilmezer, G., Alturfan, A. A., Yiğitbaşı, T., and Emekli-Alturfan, E. (2019) Rotenone impairs oxidant/antioxidant balance both in brain and intestines in zebrafish, Int. J. Neurosci., 129, 363-368, https://doi.org/10.1080/00207454.2018.1538141.

    Article  CAS  PubMed  Google Scholar 

  75. Nellore, J., and Nandita, P. (2015) Paraquat exposure induces behavioral deficits in larval zebrafish during the window of dopamine neurogenesis, Toxicol. Rep., 2, 950-956, https://doi.org/10.1016/j.toxrep.2015.06.007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. McEwen, B. S. (2004) Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders, Ann. NY Acad. Sci., 1032, 1-7, https://doi.org/10.1196/annals.1314.001.

    Article  PubMed  Google Scholar 

  77. Melchior, M., Caspi, A., Milne, B. J., Danese, A., Poulton, R., and Moffitt, T. E. (2007) Work stress precipitates depression and anxiety in young, working women and men, Psychol. Med., 37, 1119, https://doi.org/10.1017/S0033291707000414.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Slavich, G. M., and Irwin, M. R. (2014) From stress to inflammation and major depressive disorder: a social signal transduction theory of depression, Psychol. Bull., 140, 774, https://doi.org/10.1037/a0035302.

    Article  PubMed  PubMed Central  Google Scholar 

  79. De Abreu, M. S., Koakoski, G., Ferreira, D., Oliveira, T. A., da Rosa, J. G. S., Gusso, D., and Barcellos, L. J. G. (2014) Diazepam and fluoxetine decrease the stress response in zebrafish, PLoS One, 9, e103232, https://doi.org/10.1371/journal.pone.0103232.

    Article  CAS  PubMed Central  Google Scholar 

  80. Gaikwad, S., Stewart, A., Hart, P., Wong, K., Piet, V., Cachat, J., and Kalueff, A. V. (2011) Acute stress disrupts performance of zebrafish in the cued and spatial memory tests: the utility of fish models to study stress–memory interplay, Behav. Processes, 87, 224-230, https://doi.org/10.1016/j.beproc.2011.04.004.

    Article  PubMed  Google Scholar 

  81. Giacomini, A. C. V., Abreu, M. S., Giacomini, L. V., Siebel, A. M., Zimerman, F. F., Rambo, C. L., and Barcellos, L. J. (2016) Fluoxetine and diazepam acutely modulate stress induced-behavior, Behav. Brain Res., 296, 301-310, https://doi.org/10.1016/j.bbr.2015.09.027.

    Article  CAS  PubMed  Google Scholar 

  82. Mocelin, R., Herrmann, A. P., Marcon, M., Rambo, C. L., Rohden, A., Bevilaqua, F., and Barcellos, L. J. (2015) N-acetylcysteine prevents stress-induced anxiety behavior in zebrafish, Pharmacol. Biochem. Behav., 139, 121-126, https://doi.org/10.1016/j.pbb.2015.08.006.

    Article  CAS  PubMed  Google Scholar 

  83. Demin, K. A., Lakstygal, A. M., Chernysh, M. V., Krotova, N. A., Taranov, A. S., Ilyin, N. P., and Mor, M. S. (2020) The zebrafish tail immobilization (ZTI) test as a new tool to assess stress-related behavior and a potential screen for drugs affecting despair-like states, J. Neurosci. Methods, 337, 108637, https://doi.org/10.1016/j.jneumeth.2020.108637.

    Article  CAS  PubMed  Google Scholar 

  84. Fulcher, N., Tran, S., Shams, S., Chatterjee, D., and Gerlai, R. (2017) Neurochemical and behavioral responses to unpredictable chronic mild stress following developmental isolation: the zebrafish as a model for major depression, Zebrafish, 14, 23-34, https://doi.org/10.1089/zeb.2016.1295.

    Article  CAS  PubMed  Google Scholar 

  85. Marcon, M., Herrmann, A. P., Mocelin, R., Rambo, C. L., Koakoski, G., Abreu, M. S., and Zanatta, L. (2016) Prevention of unpredictable chronic stress-related phenomena in zebrafish exposed to bromazepam, fluoxetine and nortriptyline, Psychopharmacology, 233, 3815-3824, https://doi.org/10.1007/s00213-016-4408-5.

    Article  CAS  PubMed  Google Scholar 

  86. Mocelin, R., Marcon, M., D’ambros, S., Mattos, J., Sachett, A., Siebel, A. M., and Piato, A. (2019) N-Acetylcysteine reverses anxiety and oxidative damage induced by unpredictable chronic stress in zebrafish, Mol. Neurobiol., 56, 1188-1195, https://doi.org/10.1007/s12035-018-1165-y.

    Article  CAS  PubMed  Google Scholar 

  87. Rambo, C. L., Mocelin, R., Marcon, M., Villanova, D., Koakoski, G., de Abreu, M. S., and Bonan, C. D. (2017) Gender differences in aggression and cortisol levels in zebrafish subjected to unpredictable chronic stress, Physiol. Behav., 171, 50-54, https://doi.org/10.1016/j.physbeh.2016.12.032.

    Article  CAS  PubMed  Google Scholar 

  88. Song, C., Liu, B. P., Zhang, Y. P., Peng, Z., Wang, J., Collier, A. D., and Rex, C. S. (2018) Modeling consequences of prolonged strong unpredictable stress in zebrafish: Complex effects on behavior and physiology, Progr. Neuro Psychopharmacol. Biol. Psychiatry, 81, 384-394, https://doi.org/10.1016/j.pnpbp.2017.08.021.

    Article  Google Scholar 

  89. Demin, K. A., Lakstygal, A. M., Krotova, N. A., Masharsky, A., Tagawa, N., Chernysh, M. V., and Derzhavina, K. A. (2020) Understanding complex dynamics of behavioral, neurochemical and transcriptomic changes induced by prolonged chronic unpredictable stress in zebrafish, Sci. Rep., 10, 1-20, https://doi.org/10.1038/s41598-020-75855-3.

    Article  CAS  Google Scholar 

  90. Canavello, P. R., Cachat, J. M., Beeson, E. C., Laffoon, A. L., Grimes, C., Haymore, W. A., and Elkhayat, S. I. (2011) Measuring endocrine (cortisol) responses of zebrafish to stress, in Zebrafish Neurobehavioral Protocols, Springer, pp. 135-142, https://doi.org/10.1007/978-1-60761-953-6_11.

  91. Egan, R. J., Bergner, C. L., Hart, P. C., Cachat, J. M., Canavello, P. R., Elegante, M. F., and Tien, D. H. (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish, Behav. Brain Res., 205, 38-44, https://doi.org/10.1016/j.bbr.2009.06.022.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Ramsay, J. M., Feist, G. W., Varga, Z. M., Westerfield, M., Kent, M. L., and Schreck, C. B. (2009) Whole-body cortisol response of zebrafish to acute net handling stress, Aquaculture, 297, 157-162, https://doi.org/10.1016/j.aquaculture.2009.08.035.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Cohen, B. E., Edmondson, D., and Kronish, I. M. (2015) State of the art review: depression, stress, anxiety, and cardiovascular disease, Am. J. Hypertens., 28, 1295-1302, https://doi.org/10.1093/ajh/hpv047.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Golbidi, S., Frisbee, J. C., and Laher, I. (2015) Chronic stress impacts the cardiovascular system: animal models and clinical outcomes, Am. J. Physiol. Heart Circ. Physiol., 308, H1476-H1498, https://doi.org/10.1152/ajpheart.00859.2014.

    Article  CAS  PubMed  Google Scholar 

  95. Geary, B. (2016) Determining the Rates of Protein Synthesis in the Zebrafish Heart in Response to Chronic Unpredictable Stress, Doctoral Thesis.

  96. Cologna, S. M., and Rosenhouse-Dantsker, A. (2019) Insights into the molecular mechanisms of cholesterol binding to the NPC1 and NPC2 proteins, Adv. Exp. Med. Biol., 1135, 139-160, https://doi.org/10.1007/978-3-030-14265-0_8.

    Article  CAS  PubMed  Google Scholar 

  97. Vanier, M. T. (2010) Niemann-Pick disease type C, Orphanet J. Rare Dis., 5, 1-18, https://doi.org/10.1186/1750-1172-5-16.

    Article  Google Scholar 

  98. Vanier, M. T., and Millat, G. (2004) Structure and function of the NPC2 protein, Biochim. Biophys. Acta, 1685, 14-21, https://doi.org/10.1016/j.bbalip.2004.08.007.

    Article  CAS  PubMed  Google Scholar 

  99. Patterson, M. C., Hendriksz, C. J., Walterfang, M., Sedel, F., Vanier, M. T., Wijburg, F., and NP-C Guidelines Working Group (2012) Recommendations for the diagnosis and management of Niemann–Pick disease type C: an update, Mol. Genet. Metab., 106, 330-344, https://doi.org/10.1016/j.ymgme.2012.03.012.

    Article  CAS  PubMed  Google Scholar 

  100. Patterson, M. C., Mengel, E., Wijburg, F. A., Muller, A., Schwierin, B., Drevon, H., and Pineda, M. (2013) Disease and patient characteristics in NP-C patients: findings from an international disease registry, Orphanet J. Rare Dis., 8, 1-10, https://doi.org/10.1186/1750-1172-8-12.

    Article  Google Scholar 

  101. Gawel, K., Langlois, M., Martins, T., van der Ent, W., Tiraboschi, E., Jacmin, M., and Esguerra, C. V. (2020) Seizing the moment: Zebrafish epilepsy models, Neurosci. Biobehav. Rev., 116, 1-20, https://doi.org/10.1016/j.neubiorev.2020.06.010.

    Article  CAS  PubMed  Google Scholar 

  102. Mills, P. B., Footitt, E. J., Mills, K. A., Tuschl, K., Aylett, S., Varadkar, S., and Baxter, P. (2010) Genotypic and phenotypic spectrum of pyridoxine-dependent epilepsy (ALDH7A1 deficiency), Brain, 133, 2148-2159, https://doi.org/10.1093/brain/awq143.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Pearl, P. L., Hyland, K., Chiles, J., McGavin, C. L., Yu, Y., and Taylor, D. (2012) Partial pyridoxine responsiveness in PNPO deficiency, JIMD Rep., 9, 139-142, https://doi.org/10.1007/8904_2012_194.

    Article  PubMed  PubMed Central  Google Scholar 

  104. Mills, P. B., Struys, E., Jakobs, C., Plecko, B., Baxter, P., Baumgartner, M., and Uhlenberg, B. (2006) Mutations in antiquitin in individuals with pyridoxine-dependent seizures, Nat. Med., 12, 307-309, https://doi.org/10.1038/nm1366.

    Article  CAS  PubMed  Google Scholar 

  105. Khayat, M., Korman, S. H., Frankel, P., Weintraub, Z., Hershckowitz, S., Sheffer, V. F., and Falik-Zaccai, T. C. (2008) PNPO deficiency: an under diagnosed inborn error of pyridoxine metabolism, Mol. Genet. Metab., 94, 431-434, https://doi.org/10.1016/j.ymgme.2008.04.008.

    Article  CAS  PubMed  Google Scholar 

  106. Chen, P. Y., Tu, H. C., Schirch, V., Safo, M. K., and Fu, T. F. (2019) Pyridoxamine supplementation effectively reverses the abnormal phenotypes of zebrafish larvae with PNPO deficiency, Front. Pharmacol., 10, 1086, https://doi.org/10.3389/fphar.2019.01086.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Tremiño, L., Forcada-Nadal, A., and Rubio, V. (2018) Insight into vitamin B6-dependent epilepsy due to PLPBP (previously PROSC) missense mutations, Hum. Mutat., 39, 1002-1013, https://doi.org/10.1002/humu.23540.

    Article  CAS  PubMed  Google Scholar 

  108. Patel, M. (2018) A metabolic paradigm for epilepsy, Epilepsy Curr., 18, 318-322, https://doi.org/10.5698/1535-7597.18.5.318.

    Article  PubMed  PubMed Central  Google Scholar 

  109. Pearson-Smith, J. N., and Patel, M. (2017) Metabolic dysfunction and oxidative stress in epilepsy, Int. J. Mol. Sci., 18, 2365, https://doi.org/10.3390/ijms18112365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Ibhazehiebo, K., Rho, J. M., and Kurrasch, D. M. (2020) Metabolism-based drug discovery in zebrafish: An emerging strategy to uncover new anti-seizure therapies, Neuropharmacology, 167, 107988, https://doi.org/10.1016/j.neuropharm.2020.107988.

    Article  CAS  PubMed  Google Scholar 

  111. Dias, V., Junn, E., and Mouradian, M. M. (2013) The role of oxidative stress in Parkinson’s disease, J. Parkinson's Dis., 3, 461-491, https://doi.org/10.3233/JPD-130230.

    Article  CAS  Google Scholar 

  112. Park, J. S., Davis, R. L., and Sue, C. M. (2018) Mitochondrial dysfunction in Parkinson’s disease: new mechanistic insights and therapeutic perspectives, Curr. Neurol. Neurosci. Rep., 18, 1-11, https://doi.org/10.1007/s11910-018-0829-3.

    Article  CAS  Google Scholar 

  113. Bretaud, S., Lee, S., and Guo, S. (2004) Sensitivity of zebrafish to environmental toxins implicated in Parkinson’s disease, Neurotoxicol. Teratol., 26, 857-864, https://doi.org/10.1016/j.ntt.2004.06.014.

    Article  CAS  PubMed  Google Scholar 

  114. Inden, M., Kitamura, Y., Abe, M., Tamaki, A., Takata, K., and Taniguchi, T. (2011) Parkinsonian rotenone mouse model: reevaluation of long-term administration of rotenone in C57BL/6 mice, Biol. Pharmaceut. Bull., 34, 92-96, https://doi.org/10.1248/bpb.34.92.

    Article  CAS  Google Scholar 

  115. Langston, J., Forno, L., Tetrud, J., Reeves, A., Kaplan, J., and Karluk, D. (1999) Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine exposure, Ann. Neurol., 46, 598-605, https://doi.org/10.1002/1531-8249(199910)46:4<598::AID-ANA7>3.0.CO;2-F.

    Article  CAS  PubMed  Google Scholar 

  116. Vaz, R. L., Outeiro, T. F., and Ferreira, J. J. (2018) Zebrafish as an animal model for drug discovery in Parkinson’s disease and other movement disorders: a systematic review, Front. Neurol., 9, 347, https://doi.org/10.3389/fneur.2018.00347.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Trempe, J. F., and Fon, E. A. (2013) Structure and function of Parkin, PINK1, and DJ-1, the three musketeers of neuroprotection, Front. Neurol., 4, 38, https://doi.org/10.3389/fneur.2013.00038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Melo, K. M., Oliveira, R., Grisolia, C. K., Domingues, I., Pieczarka, J. C., de Souza Filho, J., and Nagamachi, C. Y. (2015) Short-term exposure to low doses of rotenone induces developmental, biochemical, behavioral, and histological changes in fish, Environ. Sci. Pollut. Res., 22, 13926-13938, https://doi.org/10.1007/s11356-015-4596-2.

    Article  CAS  Google Scholar 

  119. Fasano, A., Visanji, N. P., Liu, L. W., Lang, A. E., and Pfeiffer, R. F. (2015) Gastrointestinal dysfunction in Parkinson’s disease, Lancet Neurol., 14, 625-639, https://doi.org/10.1016/S1474-4422(15)00007-1.

    Article  CAS  PubMed  Google Scholar 

  120. Harsanyiova, J., Buday, T., and Kralova Trancikova, A. (2020) Parkinson’s disease and the gut: future perspectives for early diagnosis, Front. Neurosci., 14, 626, https://doi.org/10.3389/fnins.2020.00626.

    Article  PubMed  PubMed Central  Google Scholar 

  121. Kurrasch, D. (2018) A Phase II Pilot Clinical Trial Testing the Safety and Efficacy of Vorinostat in Pediatric Patients with Medically Intractable Epilepsy, Alberta Health Services.

  122. 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, https://doi.org/10.1016/j.nbd.2010.05.010.

    Article  CAS  PubMed  Google Scholar 

  123. Alberico, S. L., Cassell, M. D., and Narayanan, N. S. (2015) The vulnerable ventral tegmental area in Parkinson’s disease, Basal Ganglia, 5, 51-55, https://doi.org/10.1016/j.baga.2015.06.001.

    Article  PubMed  PubMed Central  Google Scholar 

  124. Trist, B. G., Hare, D. J., and Double, K. L. (2019) Oxidative stress in the aging substantia nigra and the etiology of Parkinson’s disease, Aging Cell, 18, e13031, https://doi.org/10.1111/acel.13031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Bretaud, S., Allen, C., Ingham, P. W., and Bandmann, O. (2007) P53-dependent neuronal cell death in a DJ-1-deficient zebrafish model of Parkinson’s disease, J. Neurochem., 100, 1626-1635, https://doi.org/10.1111/j.1471-4159.2006.04291.x.

    Article  CAS  PubMed  Google Scholar 

  126. Flinn, L., Mortiboys, H., Volkmann, K., Köster, R. W., Ingham, P. W., and Bandmann, O. (2009) Complex I deficiency and dopaminergic neuronal cell loss in parkin-deficient zebrafish (Danio rerio), Brain, 132, 1613-1623, https://doi.org/10.1093/brain/awp108.

    Article  PubMed  Google Scholar 

  127. Rink, E., and Wullimann, M. F. (2001) The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum), Brain Res., 889, 316-330, https://doi.org/10.1016/S0006-8993(00)03174-7.

    Article  CAS  PubMed  Google Scholar 

  128. Schweitzer, J., Löhr, H., Filippi, A., and Driever, W. (2012) Dopaminergic and noradrenergic circuit development in zebrafish, Dev. Neurobiol., 72, 256-268, https://doi.org/10.1002/dneu.20911.

    Article  CAS  PubMed  Google Scholar 

  129. Alsop, D., and Vijayan, M. (2009) The zebrafish stress axis: molecular fallout from the teleost-specific genome duplication event, Gen. Compar. Endocrinol., 161, 62-66, https://doi.org/10.1016/j.ygcen.2008.09.011.

    Article  CAS  Google Scholar 

  130. Taylor, J. S., Van de Peer, Y., Braasch, I., and Meyer, A. (2001) Comparative genomics provides evidence for an ancient genome duplication event in fish, Philos. Trans. R. Soc. London Ser B Biol. Sci., 356, 1661-1679, https://doi.org/10.1098/rstb.2001.0975.

    Article  CAS  Google Scholar 

  131. Audira, G., Siregar, P., Chen, J. R., Lai, Y. H., Huang, J. C., and Hsiao, C. D. (2020) Systematical exploration of the common solvent toxicity at whole organism level by behavioral phenomics in adult zebrafish, Environ. Pollut., 266, 115239, https://doi.org/10.1016/j.envpol.2020.115239.

    Article  CAS  PubMed  Google Scholar 

  132. Vaz, R., Hofmeister, W., and Lindstrand, A. (2019) Zebrafish models of neurodevelopmental disorders: limitations and benefits of current tools and techniques, Int. J. Mol. Sci., 20, 1296, https://doi.org/10.3390/ijms20061296.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Blaser, R., and Gerlai, R. (2006) Behavioral phenotyping in zebrafish: comparison of three behavioral quantification methods, Behav. Res. Methods, 38, 456-469, https://doi.org/10.3758/BF03192800.

    Article  PubMed  Google Scholar 

  134. Echevarria, D. J., Hammack, C. M., Pratt, D. W., and Hosemann, J. D. (2008) A novel behavioral test battery to assess global drug effects using the zebrafish, Int. J. Compar. Psychol., 21, 19-34, https://doi.org/10.46867/IJCP.2008.21.01.02.

    Article  Google Scholar 

  135. Stewart, A. M., Gaikwad, S., Kyzar, E., and Kalueff, A. V. (2012) Understanding spatio-temporal strategies of adult zebrafish exploration in the open field test, Brain Res., 1451, 44-52, https://doi.org/10.1016/j.brainres.2012.02.064.

    Article  CAS  PubMed  Google Scholar 

  136. Costa, F. V., Kolesnikova, T. O., Galstyan, D. S., Ilyin, N. P., de Abreu, M. S., Petersen, E. V., Demin, K. A., Yenkoyan, K. B., and Kalueff, A. V. (2023) Current state of modeling human psychiatric disorders using zebrafish, Int. J. Mol. Sci., 24, 3187, https://doi.org/10.3390/ijms24043187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The work was financially supported by the St. Petersburg State University budgetary funds (Project ID 94030626). A.V.K. and T.O.K. are supported by the Sirius University of Science and Technology budgetary funds (Project ID NRB-RND-2116).

Author information

Authors and Affiliations

Authors

Contributions

A.V.K. conceived and supervised the study; N.P.I., T.O.K., and S.L.Kh. analyzed the data and discussed findings with input from all authors; N.P.I. and K.A.D. wrote the manuscript; E.V.P. and A.V.K. edited the manuscript.

Corresponding authors

Correspondence to Tatyana O. Kolesnikova, Konstantin A. Demin or Allan V. Kalueff.

Ethics declarations

This work does not contain any studies involving human and animal subjects. The authors of this work declare that they have no conflicts of interest.

Additional information

Publisher’s Note. Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ilyin, N.P., Petersen, E.V., Kolesnikova, T.O. et al. Developing Peripheral Biochemical Biomarkers of Brain Disorders: Insights from Zebrafish Models. Biochemistry Moscow 89, 377–391 (2024). https://doi.org/10.1134/S0006297924020160

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297924020160

Keywords

Navigation