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.
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
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.
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.
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.
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.
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.
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.
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.
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.
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.
McGonigle, P. (2014) Animal models of CNS disorders, Biochem. Pharmacol., 87, 140-149, https://doi.org/10.1016/j.bcp.2013.06.016.
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.
Carboni, L. (2013) Peripheral biomarkers in animal models of major depressive disorder, Dis. Markers, 35, 33-41, https://doi.org/10.1155/2013/284543.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Geary, B. (2016) Determining the Rates of Protein Synthesis in the Zebrafish Heart in Response to Chronic Unpredictable Stress, Doctoral Thesis.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Patel, M. (2018) A metabolic paradigm for epilepsy, Epilepsy Curr., 18, 318-322, https://doi.org/10.5698/1535-7597.18.5.318.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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
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
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
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297924020160