Zebrafish Embryo as an Emerging Model Organism in Neurodevelopmental Toxicity Research
Year 2021,
Volume: 80 Issue: 2, 179 - 187, 17.12.2021
Sukriye Caliskan
Ebru Emekli Alturfan
Abstract
Zebrafish is a model organism that has become increasingly popular in recent years due to some of the advantages it has when compared to traditional model organisms. Its genetic similarity with humans has contributed significantly to the elucidation of the molecular mechanisms underlying diseases. Moreover, external fertilization and rapid embryonic development of zebrafish embryos have made it attractive in many research areas. The genome of humans and zebrafish are found to be highly conserved having 76-82 % of the disease genes in humans that are also present in zebrafish. Zebrafish have been used in different studies in several concepts of neurogenesis. Unlike mammals, the external development of a zebrafish embryo makes it accessible for experimental manipulation in central nervous system research. It was observed that neurotoxic agents induced similar responses to other vertebral models in zebrafish embryos, whose brain development and blood-brain barrier were similar to those of other vertebrates. This review provides brief information about the availability of zebrafish embryos in neurodevelopmental toxicity research while giving brief information on embryogenesis and neurogenesis in zebrafish. Evaluation of neurotoxicity and the specific effects of various neurotoxins on motor and dopaminergic neurons, neuronal proliferation, mobility, and neurodevelopment are also explained.
Supporting Institution
Marmara University Scientific Research Projects Commission
Project Number
Grant number: TYL-2021-10205
References
- 1. Ünal İ, Emekli-Alturfan E. Fishing for Parkinson’s Disease: A review of the literature. J Clin Neurosci 2019; 62: 1-6. google scholar
- 2. Renier C, Faraco JH, Bourgin P, Motley T, Bonaventure P, Rosa F. Genomic and functional conservation of sedative-hypnotic targets in the zebrafish. Pharmacogenet Genomics
2007; 17: 237-53. google scholar
- 3. Rihel J, Prober DA, Arvanites A, Lam K, Zimmerman S, Jang S. Ze-brafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 2010; 327: 348-
51. google scholar
- 4. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, etal. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496:
498-503. google scholar
- 5. Kozol RA, Abrams AJ, James DM, Buglo E, Yan Q, Dallman JE. Func-tion over form: modeling groups of inherited neurological condi-tions in zebrafish. Front Mol Neurosci 2016; 7:
9-55. google scholar
- 6. Engeszer RE, Patterson LB, Rao AA, Parichy DM. Zebrafish in the wild: A review of natural history and new notes from the field. Ze-brafish 2007; 4: 21-40. google scholar
- 7. Bally-Cuif L, Vernier P. Organization and Physiology of the Zebraf-ish Nervous System. Fish Physiol 2010; 29: 25-80. google scholar
- 8. Schmidt R, Strahle U, Scholpp S. Neurogenesis in zebrafish - from embryo to adult. Neural Dev 2013; 8: 3. google scholar
- 9. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 2009; 10: 507-18. google scholar
- 10. Brustein E, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Drapeau P. Steps during the development of the zebrafish loco-motor network. J Physiol Paris 2003; 97: 77-86.
google scholar
- 11. Gould E, Gross CG. Neurogenesis in adult mammals: some prog-ress and problems. J Neurosci 2002; 22(3): 619-23. google scholar
- 12. Gould E. How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 2007; 8: 481-88. google scholar
- 13. Zupanc GKH, Hinsch K, Gage FH. Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult ze-brafish brain. J Comp Neurol 2005; 488:
290-319. google scholar
- 14. Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M. Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol
2006; 295: 263-77. google scholar
- 15. Hinsch K, Zupanc GKH. Generation and long-term persistence of new neurons in the adult zebrafish brain: a quantitative analysis. Neuroscience 2007; 146: 679-96. google
scholar
- 16. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995: 203(3): 253-310. google scholar
- 17. Sasai Y, De Robertis EM. Ectodermal patterning in vertebrate em-bryos. Dev Biol 1997; 182: 5-20. google scholar
- 18. Spemann H, Mangold H. Induction of embryonic primordia by im-plantation of organizers from a different species. 1923. Int J Dev Biol 2001; 45: 13-38. google scholar
- 19. Zebrafish developmental timeline (Reprinted from “Zebrafish De-velopmental Timeline”, by BioRender.com (2021). Retrieved from https://app.biorender.com/biorender-
templates) google scholar
- 20. Doniach T, Musci TJ. Induction of anteroposterior neural pattern in Xenopus: evidence for a quantitative mechanism. Mech Dev 1995; 53: 403-13. google scholar
- 21. Lumsden A, Krumlauf R. Patterning the vertebrate neuraxis. Sci-ence 1996; 274: 1109-15. google scholar
- 22. Weinstein DC, Hemmati-Brivanlou A. Neural induction. Annu Rev Cell Dev Biol 1999; 15: 411-33. google scholar
- 23. Okuda Y, Ogura E, Kondoh H, Kamachi Y. B1 SOX coordinate cell specification with patterning and morphogenesis in the early ze-brafish embryo. PloS Genet 2010; 6(5):
e1000936. google scholar
- 24. Kim CH, Oda T, Itoh M, Jiang D, Artinger KB, Chandrasekharappa SC, et al. Repressor activity of Headless/Tcf3 is essential for verte-brate head formation. Nature 2000; 407:
913-16. google scholar
- 25. Rhinn M, Lun K, Luz M, Werner M, Brand M. Positioning of the mid-brain-hindbrain boundary organizer through global posterioriza-tion of the neuroectoderm mediated by
Wnt8 signaling. Develop-ment 2005; 132: 1261-72. google scholar
- 26. Houart C, Westerfield M, Wilson SW. A small population of anteri-or cells patterns the forebrain during zebrafish gastrulation. Natur 1998; 391: 788-92. google scholar
- 27. Üstündağ ÜV, Emekli-Alturfan E. Wnt pathway: A mechanism worth considering in endocrine disrupting chemical action. Toxi-col Ind Health 2020; 36(1): 41-53. google scholar
- 28. Üstündağ ÜV, Ünal İ, Ateş PS, Alturfan AA, Yiğitbaşı T, Emekli-Altur-fan E. Bisphenol A and di(2-ethylhexyl) phthalate exert divergent effects on apoptosis and the Wnt/0-
catenin pathway in zebrafish embryos: A possible mechanism of endocrine disrupting chemical action. Toxicol Ind Health 2017; 33(12): 901-10. google scholar
- 29. Bielen H, Houart C. BMP signaling protects telencephalic fate by repressing eye identity and its Cxcr4-dependent morphogenesis. Dev Cell 2012; 23: 812-22. google scholar
- 30. Stern CD. Neural induction: 10 years on since the “default model” Curr Opin Cell Biol 2006; 18: 692-7. google scholar
- 31. Penzel R, Oschwald R, Chen Y, Tacke L, Grunz H. Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. Int J Dev Biol
1997; 41: 667-77. google scholar
- 32. Dee CT, Hirst CS, Shih Y-H, Tripathi VB, Patient RK, Scotting PJ. Sox3 regulates both neural fate and differentiation in the zebrafish ec-toderm. Dev Biol 2008; 320: 289301. google
scholar
- 33. Kaslin J, Ganz J, Geffarth M, Grandel H, Hans S, Brand M. Stem cells in the adult zebrafish cerebellum: initiation and maintenance of a novel stem cell niche. J Neurosci 2009;
29: 6142-53. google scholar
- 34. Bani-Yaghoub M, Tremblay RG, Lei JX, Zhang D, Zurakowski B, Sandhu JK, et al. Role of Sox2 in the development of the mouse neocortex. Dev Biol 2006; 295: 52-66. google
scholar
- 35. Allende ML, Weinberg ES. The expression pattern of two zebrafish achaete-scute homolog (ash) genes is altered in the embryonic brain of the cyclops mutant. Dev Biol 1994;
166: 509-30. google scholar
- 36. Scholpp S, Delogu A, Gilthorpe J, Peukert D, Schindler S, Lumsden A. Her6 regulates the neurogenetic gradient and neuronal identity in the thalamus. Proc Natl Acad Sci U S A
2009; 106: 19895-900. google scholar
- 37. Tallafuss A, Adolf B, Bally-Cuif L. Selective control of neuronal clus-ter size at the forebrain/midbrain boundary by signaling from the prechordal plate. Dev Dyn 2003; 227:
524-35. google scholar
- 38. Geling A, Itoh M, Tallafuss A, Chapouton P, Tannhauser B, Kuwa-da JY, Chitnis AB, Bally-Cuif L. bHLH transcription factor Her5 links patterning to regional inhibition of
neurogenesis at the mid-brain-hindbrain boundary. Development 2003; 130: 1591-604. google scholar
- 39. Ninkovic J, Tallafuss A, Leucht C, Topczewski J, Tannhauser B, Solni-ca-Krezel L, Bally-Cuif L. Inhibition of neurogenesis at the zebrafish midbrain-hindbrain boundary by the
combined and dose-depen-dent activity of a new hairy/E(spl) gene pair. Development 2005; 132(1): 75-88. google scholar
- 40. Lyons DA, Guy AT, Clarke JDW. Monitoring neural progenitor fate through multiple rounds of division in an intact vertebrate brain. Development 2003; 130: 3427-36. google
scholar
- 41. Wysowski DK, Swartz L. Adverse drug event surveillance and drug withdrawals in the United States, 1969-2002: the importance of re-porting suspected reactions. Arch Intern
Med 2005; 165(12): 13639. google scholar
- 42. Kulkarni HS, Keskar VS, Bavdekar SB, Gabhale Y. Bilateral optic neu-ritis due to isoniazid (INH). Indian Pediatr 2010; 47(6): 533-5. google scholar
- 43. Edson RS, Terrell CL. The aminoglycosides. Mayo Clin Proc 1999; 74(5): 519-28. google scholar
- 44. Moser VC. Functional assays for neurotoxicity testing. Toxicol Pathol 2011; 39(1): 36-45. google scholar
- 45. Kulig B, Alleva E, Bignami G, Cohn J, Cory-Slechta D, Landa V, et al. Animal behavioral methods in neurotoxicity assessment: SGOM-SEC joint report. Environ Health Perspect
1996; 104(Suppl 2): 193204. google scholar
- 46. Kung MP, Kostyniak PJ, Olson JR, Sansone FM, Nickerson PA, Malone MA, et al. Cell specific enzyme markers as indicators of neurotoxicity: effects of acute exposure to
methylmercury. Neuro-toxicology 1989; 10(1): 41-52. google scholar
- 47. Kuwada JY, Bernhardt RR, Nguyen N. Development of spinal neu-rons and tracts in the zebrafish embryo. J Comp Neurol 1990; 302(3): 617-28. google scholar
- 48. Moens CB, Fritz A. Techniques in neural development. Methods Cell Biol 1999; 59: 253-72. google scholar
- 49. Brustein E, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Drapeau P. Steps during the development of the zebrafish loco-motor network. J Physiol Paris 2003; 97(1): 77-86.
google scholar
- 50. Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an over-view: structure, regulation, and clinical implications. Neurobiol Dis 2004; 16(1): 1-13. google scholar
- 51. Engelhardt B. Development of the blood-brain barrier. Cell Tissue Res 2003; 314(1): 119-29. google scholar
- 52. Cserr HF, Bundgaard M. Blood-brain interfaces in vertebrates: a comparative approach. Am J Physiol 1984; 246(3): R277-88. google scholar
- 53. Eliceiri BP, Gonzalez AM, Baird A. Zebrafish model of the blood-brain barrier: morphological and permeability studies. Methods Mol Biol 2011; 686: 371-8. google scholar
- 54. Kimmel CB, Miller CT, Kruze G, Ullmann B, BreMiller RA, Larison KD, Snyder HC. The shaping of pharyngeal cartilages during early de-velopment of the zebrafish. Dev Biol 1998;
203(2): 245-63. google scholar
- 55. Eisen JS, Pike SH. The spt-1 mutation alters segmental arrange-ment and axonal development of identified neurons in the spinal cord of the embryonic zebrafish. Neuron
1991; 6(5): 767-76. google scholar
- 56. Schier AF, Neuhauss SC, Harvey M, Malicki J, Solnica-Krezel L, Stain-ier DY, et al. Mutations affecting the development of the embryon-ic zebrafish brain. Development 1996;
123: 165-78. google scholar
- 57. Biller A, Bartsch AJ, Homola G, Solymosi L, Bendszus M. The effect of ethanol on human brain metabolites longitudinally character-ized by proton MR spectroscopy. J Cereb
Blood Flow Metab 2009; 29(5): 891-902. google scholar
- 58. Parng C, Roy NM, Ton C, Lin Y, McGrath P. Neurotoxicity assessment using zebrafish. J Pharmacol Toxicol Methods 2007; 55(1): 103-12. google scholar
- 59. Elkon H, Melamed E, Offen D. Oxidative stress, induced by 6-hy-droxydopamine, reduces proteasome activities in PC12 cells. J Mol Neurosci 2004; 24: 387-400. google scholar
- 60. Ünal İ, Çalışkan-Ak E, Üstündağ ÜV, Ateş PS, Alturfan AA, Altinoz MA,et al. Neuroprotective effects of mitoquinone and oleandrin on Parkinson’s disease model in zebrafish. Int J
Neurosci 2020; 130(6): 574-82. google scholar
- 61. Ünal İ, Üstündağ ÜV, Ateş PS, Eğilmezer G, Alturfan AA, Yiğitbaşı T, et al. Rotenone impairs oxidant/antioxidant balance both in brain and intestines in zebrafish. Int J Neurosci
2019; 129(4): 363-68. google scholar
- 62. McKinley ET, Baranowski TC, Blavo DO, Cato C, Doan TN, Rubinstein AL. Neuroprotection of MPTP-induced toxicity in zebrafish dopa-minergic neurons. Brain Research.
Molecular Brain Research 2005; 141(2): 128-37. google scholar
- 63. Cansız D, Ustundag UV, Unal I, Alturfan AA, Emekli-Alturfan E. Mor-phine attenuates neurotoxic effects of MPTP in zebrafish embryos by regulating oxidant/antioxidant balance
and acetylcholinester-ase activity. Drug Chem Toxicol 2021; 2: 1-9. google scholar
- 64. Üstündağ FD, Ünal İ, Cansız D, Üstündağ ÜV, Subaşat HK, Alturfan AA, et al. 3-Pyridinylboronic acid normalizes the effects of 1-Meth-yl-4-phenyl-1,2,3,6-tetrahydropyridine
exposure in zebrafish em-bryos. Drug Chem Toxicol 2020; 21: 1-8. google scholar
- 65. Lam CS, Korzh V, Strahle U. Zebrafish embryos are susceptible to the dopaminergic neurotoxin MPTP. The European Journal of Neu-roscience 2005; 21(6): 1758-62. google
scholar
- 66. Granato M, Nüsslein-Volhard C. Fishing for genes controlling de-velopment. Curr Opin Genet Dev 1996; 6(4): 461-8. google scholar
- 67. Drapeau P, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Brust-ein E. Development of the locomotor network in zebrafish. Prog Neurobiol 2002; 68(2): 85-111. google
scholar
- 68. Best JD, Alderton WK. Zebrafish: An in vivo model for the study of neurological diseases. Neuropsychiatr Dis Treat 2008; 4(3): 567-76. google scholar
- 69. Winter MJ, Redfern WS, Hayfield AJ, Owen SF, Valentin JP, Hutchin-son TH. Validation of a larval zebrafish locomotor assay for assess-ing the seizure liability of early-stage
development drugs. J Phar-macol Toxicol Methods 2008; 57(3): 176-87. google scholar
- 70. Rice D, Barone S Jr. Critical periods of vulnerability for the develop-ing nervous system: evidence from humans and animal models. Environ Health Perspect 2000; 108(3): 511-
33. google scholar
- 71. Ton C, Lin Y, Willett C. Zebrafish as a model for developmental neurotoxicity testing. Birth Defects Res A Clin Mol Teratol 2006; 76: 553-67. google scholar
- 72. Legradi JB, Di Paolo C, Kraak MHS, van der Geest HG, Schymanski EL, Williams AJ, et al. An ecotoxicological view on neurotoxicity as-sessment. Environ Sci Eur 2018; 30(1): 46.
google scholar
- 73. Panlilio JM, Aluru N, Hahn ME. Developmental Neurotoxicity of the Harmful Algal Bloom Toxin Domoic Acid: Cellular and Molecular Mechanisms Underlying Altered Behavior in
the Zebrafish Model. Environ Health Perspect. 2020; 128(11): 117002. google scholar
- 74. Costa LG, Giordano G, Aschner M. Domoic Acid. Aminoff MJ, Daroff RB, editors. Encyclopedia of the Neurological Sciences. 2nd ed. Massachusetts: Academic Press; 2014. p.
1016-17. google scholar
- 75. Qiu Y, Chen X, Yan X, Wang J, Yu G, Ma W, et al. Gut microbiota per-turbations and neurodevelopmental impacts in offspring rats con-currently exposure to inorganic arsenic
and fluoride. Environ Int. 2020; 140: 105763. google scholar
- 76. Fan CY, Cowden J, Simmons SO, Padilla S, Ramabhadran R. Gene expression changes in developing zebrafish as potential markers for rapid developmental neurotoxicity
screening. Neurotoxicol. Teratol 2010; 32: 91-8. google scholar
- 77. Yang L, Kemadjou JR, Zinsmeister C, Bauer M, Legradi J, Müller F, et al. Transcriptional profiling reveals barcode-like toxicogenomic responses in the zebrafish embryo.
Genome Biol 2007; 8(10): R227. google scholar
- 78. Ho NY, Yang L, Legradi J, Armant O, Takamiya M, Rastegar S, et al. Gene responses in the central nervous system of zebrafish em-bryos exposed to the neurotoxicant methyl
mercury. Environ. Sci. Technol 2013; 47: 3316-3325. google scholar
- 79. Xia L, Zheng L, Zhou JL. Effects of ibuprofen, diclofenac and parac-etamol on hatch and motor behavior in developing zebrafish (Da-nio rerio). Chemosphere 2017; 182: 416-25.
google scholar
- 80. Jeong JY, Einhorn Z, Mercurio S, Lee S, Lau B, Mione M, Wilson SW, Guo S. Neurogenin1 is a determinant of zebrafish basal forebrain dopaminergic neurons and is regulated by
the conserved zinc fin-ger protein Tof/Fezl. Proc Natl Acad Sci U S A. 2006; 28; 103(13): 5143-8. google scholar
- 81. Li R, Zhang L, Shi Q, Guo Y, Zhang W, Zhou B. A protective role of autophagy in TDCIPP-induced developmental neurotoxicity in ze-brafish larvae. Aquat Toxicol 2018; 199: 46-54.
google scholar
- 82. Shi Q, Wang M, Shi F, Yang L, Guo Y, Feng C, et al. Developmental neurotoxicity of triphenyl phosphate in zebrafish larvae. Aquat Toxicol 2018; 203: 80-7. google scholar
- 83. Lee S, Chun HS, Lee J, Park HJ, Kim KT, Kim CH, et al. Plausibility of the zebrafish embryos/larvae as an alternative animal model for autism: A comparison study of
transcriptome changes. PloS one 2018; 13(9): e0203543. google scholar
- 84. Chen J, Lei L, Tian L, et al. Developmental and behavioral alter-ations in zebrafish embryonically exposed to valproic acid (VPA): An aquatic model for autism. Neurotoxicol Teratol 2018; 66: 8-16. google scholar
Year 2021,
Volume: 80 Issue: 2, 179 - 187, 17.12.2021
Sukriye Caliskan
Ebru Emekli Alturfan
Project Number
Grant number: TYL-2021-10205
References
- 1. Ünal İ, Emekli-Alturfan E. Fishing for Parkinson’s Disease: A review of the literature. J Clin Neurosci 2019; 62: 1-6. google scholar
- 2. Renier C, Faraco JH, Bourgin P, Motley T, Bonaventure P, Rosa F. Genomic and functional conservation of sedative-hypnotic targets in the zebrafish. Pharmacogenet Genomics
2007; 17: 237-53. google scholar
- 3. Rihel J, Prober DA, Arvanites A, Lam K, Zimmerman S, Jang S. Ze-brafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 2010; 327: 348-
51. google scholar
- 4. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, etal. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496:
498-503. google scholar
- 5. Kozol RA, Abrams AJ, James DM, Buglo E, Yan Q, Dallman JE. Func-tion over form: modeling groups of inherited neurological condi-tions in zebrafish. Front Mol Neurosci 2016; 7:
9-55. google scholar
- 6. Engeszer RE, Patterson LB, Rao AA, Parichy DM. Zebrafish in the wild: A review of natural history and new notes from the field. Ze-brafish 2007; 4: 21-40. google scholar
- 7. Bally-Cuif L, Vernier P. Organization and Physiology of the Zebraf-ish Nervous System. Fish Physiol 2010; 29: 25-80. google scholar
- 8. Schmidt R, Strahle U, Scholpp S. Neurogenesis in zebrafish - from embryo to adult. Neural Dev 2013; 8: 3. google scholar
- 9. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 2009; 10: 507-18. google scholar
- 10. Brustein E, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Drapeau P. Steps during the development of the zebrafish loco-motor network. J Physiol Paris 2003; 97: 77-86.
google scholar
- 11. Gould E, Gross CG. Neurogenesis in adult mammals: some prog-ress and problems. J Neurosci 2002; 22(3): 619-23. google scholar
- 12. Gould E. How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 2007; 8: 481-88. google scholar
- 13. Zupanc GKH, Hinsch K, Gage FH. Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult ze-brafish brain. J Comp Neurol 2005; 488:
290-319. google scholar
- 14. Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M. Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol
2006; 295: 263-77. google scholar
- 15. Hinsch K, Zupanc GKH. Generation and long-term persistence of new neurons in the adult zebrafish brain: a quantitative analysis. Neuroscience 2007; 146: 679-96. google
scholar
- 16. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995: 203(3): 253-310. google scholar
- 17. Sasai Y, De Robertis EM. Ectodermal patterning in vertebrate em-bryos. Dev Biol 1997; 182: 5-20. google scholar
- 18. Spemann H, Mangold H. Induction of embryonic primordia by im-plantation of organizers from a different species. 1923. Int J Dev Biol 2001; 45: 13-38. google scholar
- 19. Zebrafish developmental timeline (Reprinted from “Zebrafish De-velopmental Timeline”, by BioRender.com (2021). Retrieved from https://app.biorender.com/biorender-
templates) google scholar
- 20. Doniach T, Musci TJ. Induction of anteroposterior neural pattern in Xenopus: evidence for a quantitative mechanism. Mech Dev 1995; 53: 403-13. google scholar
- 21. Lumsden A, Krumlauf R. Patterning the vertebrate neuraxis. Sci-ence 1996; 274: 1109-15. google scholar
- 22. Weinstein DC, Hemmati-Brivanlou A. Neural induction. Annu Rev Cell Dev Biol 1999; 15: 411-33. google scholar
- 23. Okuda Y, Ogura E, Kondoh H, Kamachi Y. B1 SOX coordinate cell specification with patterning and morphogenesis in the early ze-brafish embryo. PloS Genet 2010; 6(5):
e1000936. google scholar
- 24. Kim CH, Oda T, Itoh M, Jiang D, Artinger KB, Chandrasekharappa SC, et al. Repressor activity of Headless/Tcf3 is essential for verte-brate head formation. Nature 2000; 407:
913-16. google scholar
- 25. Rhinn M, Lun K, Luz M, Werner M, Brand M. Positioning of the mid-brain-hindbrain boundary organizer through global posterioriza-tion of the neuroectoderm mediated by
Wnt8 signaling. Develop-ment 2005; 132: 1261-72. google scholar
- 26. Houart C, Westerfield M, Wilson SW. A small population of anteri-or cells patterns the forebrain during zebrafish gastrulation. Natur 1998; 391: 788-92. google scholar
- 27. Üstündağ ÜV, Emekli-Alturfan E. Wnt pathway: A mechanism worth considering in endocrine disrupting chemical action. Toxi-col Ind Health 2020; 36(1): 41-53. google scholar
- 28. Üstündağ ÜV, Ünal İ, Ateş PS, Alturfan AA, Yiğitbaşı T, Emekli-Altur-fan E. Bisphenol A and di(2-ethylhexyl) phthalate exert divergent effects on apoptosis and the Wnt/0-
catenin pathway in zebrafish embryos: A possible mechanism of endocrine disrupting chemical action. Toxicol Ind Health 2017; 33(12): 901-10. google scholar
- 29. Bielen H, Houart C. BMP signaling protects telencephalic fate by repressing eye identity and its Cxcr4-dependent morphogenesis. Dev Cell 2012; 23: 812-22. google scholar
- 30. Stern CD. Neural induction: 10 years on since the “default model” Curr Opin Cell Biol 2006; 18: 692-7. google scholar
- 31. Penzel R, Oschwald R, Chen Y, Tacke L, Grunz H. Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. Int J Dev Biol
1997; 41: 667-77. google scholar
- 32. Dee CT, Hirst CS, Shih Y-H, Tripathi VB, Patient RK, Scotting PJ. Sox3 regulates both neural fate and differentiation in the zebrafish ec-toderm. Dev Biol 2008; 320: 289301. google
scholar
- 33. Kaslin J, Ganz J, Geffarth M, Grandel H, Hans S, Brand M. Stem cells in the adult zebrafish cerebellum: initiation and maintenance of a novel stem cell niche. J Neurosci 2009;
29: 6142-53. google scholar
- 34. Bani-Yaghoub M, Tremblay RG, Lei JX, Zhang D, Zurakowski B, Sandhu JK, et al. Role of Sox2 in the development of the mouse neocortex. Dev Biol 2006; 295: 52-66. google
scholar
- 35. Allende ML, Weinberg ES. The expression pattern of two zebrafish achaete-scute homolog (ash) genes is altered in the embryonic brain of the cyclops mutant. Dev Biol 1994;
166: 509-30. google scholar
- 36. Scholpp S, Delogu A, Gilthorpe J, Peukert D, Schindler S, Lumsden A. Her6 regulates the neurogenetic gradient and neuronal identity in the thalamus. Proc Natl Acad Sci U S A
2009; 106: 19895-900. google scholar
- 37. Tallafuss A, Adolf B, Bally-Cuif L. Selective control of neuronal clus-ter size at the forebrain/midbrain boundary by signaling from the prechordal plate. Dev Dyn 2003; 227:
524-35. google scholar
- 38. Geling A, Itoh M, Tallafuss A, Chapouton P, Tannhauser B, Kuwa-da JY, Chitnis AB, Bally-Cuif L. bHLH transcription factor Her5 links patterning to regional inhibition of
neurogenesis at the mid-brain-hindbrain boundary. Development 2003; 130: 1591-604. google scholar
- 39. Ninkovic J, Tallafuss A, Leucht C, Topczewski J, Tannhauser B, Solni-ca-Krezel L, Bally-Cuif L. Inhibition of neurogenesis at the zebrafish midbrain-hindbrain boundary by the
combined and dose-depen-dent activity of a new hairy/E(spl) gene pair. Development 2005; 132(1): 75-88. google scholar
- 40. Lyons DA, Guy AT, Clarke JDW. Monitoring neural progenitor fate through multiple rounds of division in an intact vertebrate brain. Development 2003; 130: 3427-36. google
scholar
- 41. Wysowski DK, Swartz L. Adverse drug event surveillance and drug withdrawals in the United States, 1969-2002: the importance of re-porting suspected reactions. Arch Intern
Med 2005; 165(12): 13639. google scholar
- 42. Kulkarni HS, Keskar VS, Bavdekar SB, Gabhale Y. Bilateral optic neu-ritis due to isoniazid (INH). Indian Pediatr 2010; 47(6): 533-5. google scholar
- 43. Edson RS, Terrell CL. The aminoglycosides. Mayo Clin Proc 1999; 74(5): 519-28. google scholar
- 44. Moser VC. Functional assays for neurotoxicity testing. Toxicol Pathol 2011; 39(1): 36-45. google scholar
- 45. Kulig B, Alleva E, Bignami G, Cohn J, Cory-Slechta D, Landa V, et al. Animal behavioral methods in neurotoxicity assessment: SGOM-SEC joint report. Environ Health Perspect
1996; 104(Suppl 2): 193204. google scholar
- 46. Kung MP, Kostyniak PJ, Olson JR, Sansone FM, Nickerson PA, Malone MA, et al. Cell specific enzyme markers as indicators of neurotoxicity: effects of acute exposure to
methylmercury. Neuro-toxicology 1989; 10(1): 41-52. google scholar
- 47. Kuwada JY, Bernhardt RR, Nguyen N. Development of spinal neu-rons and tracts in the zebrafish embryo. J Comp Neurol 1990; 302(3): 617-28. google scholar
- 48. Moens CB, Fritz A. Techniques in neural development. Methods Cell Biol 1999; 59: 253-72. google scholar
- 49. Brustein E, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Drapeau P. Steps during the development of the zebrafish loco-motor network. J Physiol Paris 2003; 97(1): 77-86.
google scholar
- 50. Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an over-view: structure, regulation, and clinical implications. Neurobiol Dis 2004; 16(1): 1-13. google scholar
- 51. Engelhardt B. Development of the blood-brain barrier. Cell Tissue Res 2003; 314(1): 119-29. google scholar
- 52. Cserr HF, Bundgaard M. Blood-brain interfaces in vertebrates: a comparative approach. Am J Physiol 1984; 246(3): R277-88. google scholar
- 53. Eliceiri BP, Gonzalez AM, Baird A. Zebrafish model of the blood-brain barrier: morphological and permeability studies. Methods Mol Biol 2011; 686: 371-8. google scholar
- 54. Kimmel CB, Miller CT, Kruze G, Ullmann B, BreMiller RA, Larison KD, Snyder HC. The shaping of pharyngeal cartilages during early de-velopment of the zebrafish. Dev Biol 1998;
203(2): 245-63. google scholar
- 55. Eisen JS, Pike SH. The spt-1 mutation alters segmental arrange-ment and axonal development of identified neurons in the spinal cord of the embryonic zebrafish. Neuron
1991; 6(5): 767-76. google scholar
- 56. Schier AF, Neuhauss SC, Harvey M, Malicki J, Solnica-Krezel L, Stain-ier DY, et al. Mutations affecting the development of the embryon-ic zebrafish brain. Development 1996;
123: 165-78. google scholar
- 57. Biller A, Bartsch AJ, Homola G, Solymosi L, Bendszus M. The effect of ethanol on human brain metabolites longitudinally character-ized by proton MR spectroscopy. J Cereb
Blood Flow Metab 2009; 29(5): 891-902. google scholar
- 58. Parng C, Roy NM, Ton C, Lin Y, McGrath P. Neurotoxicity assessment using zebrafish. J Pharmacol Toxicol Methods 2007; 55(1): 103-12. google scholar
- 59. Elkon H, Melamed E, Offen D. Oxidative stress, induced by 6-hy-droxydopamine, reduces proteasome activities in PC12 cells. J Mol Neurosci 2004; 24: 387-400. google scholar
- 60. Ünal İ, Çalışkan-Ak E, Üstündağ ÜV, Ateş PS, Alturfan AA, Altinoz MA,et al. Neuroprotective effects of mitoquinone and oleandrin on Parkinson’s disease model in zebrafish. Int J
Neurosci 2020; 130(6): 574-82. google scholar
- 61. Ünal İ, Üstündağ ÜV, Ateş PS, Eğilmezer G, Alturfan AA, Yiğitbaşı T, et al. Rotenone impairs oxidant/antioxidant balance both in brain and intestines in zebrafish. Int J Neurosci
2019; 129(4): 363-68. google scholar
- 62. McKinley ET, Baranowski TC, Blavo DO, Cato C, Doan TN, Rubinstein AL. Neuroprotection of MPTP-induced toxicity in zebrafish dopa-minergic neurons. Brain Research.
Molecular Brain Research 2005; 141(2): 128-37. google scholar
- 63. Cansız D, Ustundag UV, Unal I, Alturfan AA, Emekli-Alturfan E. Mor-phine attenuates neurotoxic effects of MPTP in zebrafish embryos by regulating oxidant/antioxidant balance
and acetylcholinester-ase activity. Drug Chem Toxicol 2021; 2: 1-9. google scholar
- 64. Üstündağ FD, Ünal İ, Cansız D, Üstündağ ÜV, Subaşat HK, Alturfan AA, et al. 3-Pyridinylboronic acid normalizes the effects of 1-Meth-yl-4-phenyl-1,2,3,6-tetrahydropyridine
exposure in zebrafish em-bryos. Drug Chem Toxicol 2020; 21: 1-8. google scholar
- 65. Lam CS, Korzh V, Strahle U. Zebrafish embryos are susceptible to the dopaminergic neurotoxin MPTP. The European Journal of Neu-roscience 2005; 21(6): 1758-62. google
scholar
- 66. Granato M, Nüsslein-Volhard C. Fishing for genes controlling de-velopment. Curr Opin Genet Dev 1996; 6(4): 461-8. google scholar
- 67. Drapeau P, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Brust-ein E. Development of the locomotor network in zebrafish. Prog Neurobiol 2002; 68(2): 85-111. google
scholar
- 68. Best JD, Alderton WK. Zebrafish: An in vivo model for the study of neurological diseases. Neuropsychiatr Dis Treat 2008; 4(3): 567-76. google scholar
- 69. Winter MJ, Redfern WS, Hayfield AJ, Owen SF, Valentin JP, Hutchin-son TH. Validation of a larval zebrafish locomotor assay for assess-ing the seizure liability of early-stage
development drugs. J Phar-macol Toxicol Methods 2008; 57(3): 176-87. google scholar
- 70. Rice D, Barone S Jr. Critical periods of vulnerability for the develop-ing nervous system: evidence from humans and animal models. Environ Health Perspect 2000; 108(3): 511-
33. google scholar
- 71. Ton C, Lin Y, Willett C. Zebrafish as a model for developmental neurotoxicity testing. Birth Defects Res A Clin Mol Teratol 2006; 76: 553-67. google scholar
- 72. Legradi JB, Di Paolo C, Kraak MHS, van der Geest HG, Schymanski EL, Williams AJ, et al. An ecotoxicological view on neurotoxicity as-sessment. Environ Sci Eur 2018; 30(1): 46.
google scholar
- 73. Panlilio JM, Aluru N, Hahn ME. Developmental Neurotoxicity of the Harmful Algal Bloom Toxin Domoic Acid: Cellular and Molecular Mechanisms Underlying Altered Behavior in
the Zebrafish Model. Environ Health Perspect. 2020; 128(11): 117002. google scholar
- 74. Costa LG, Giordano G, Aschner M. Domoic Acid. Aminoff MJ, Daroff RB, editors. Encyclopedia of the Neurological Sciences. 2nd ed. Massachusetts: Academic Press; 2014. p.
1016-17. google scholar
- 75. Qiu Y, Chen X, Yan X, Wang J, Yu G, Ma W, et al. Gut microbiota per-turbations and neurodevelopmental impacts in offspring rats con-currently exposure to inorganic arsenic
and fluoride. Environ Int. 2020; 140: 105763. google scholar
- 76. Fan CY, Cowden J, Simmons SO, Padilla S, Ramabhadran R. Gene expression changes in developing zebrafish as potential markers for rapid developmental neurotoxicity
screening. Neurotoxicol. Teratol 2010; 32: 91-8. google scholar
- 77. Yang L, Kemadjou JR, Zinsmeister C, Bauer M, Legradi J, Müller F, et al. Transcriptional profiling reveals barcode-like toxicogenomic responses in the zebrafish embryo.
Genome Biol 2007; 8(10): R227. google scholar
- 78. Ho NY, Yang L, Legradi J, Armant O, Takamiya M, Rastegar S, et al. Gene responses in the central nervous system of zebrafish em-bryos exposed to the neurotoxicant methyl
mercury. Environ. Sci. Technol 2013; 47: 3316-3325. google scholar
- 79. Xia L, Zheng L, Zhou JL. Effects of ibuprofen, diclofenac and parac-etamol on hatch and motor behavior in developing zebrafish (Da-nio rerio). Chemosphere 2017; 182: 416-25.
google scholar
- 80. Jeong JY, Einhorn Z, Mercurio S, Lee S, Lau B, Mione M, Wilson SW, Guo S. Neurogenin1 is a determinant of zebrafish basal forebrain dopaminergic neurons and is regulated by
the conserved zinc fin-ger protein Tof/Fezl. Proc Natl Acad Sci U S A. 2006; 28; 103(13): 5143-8. google scholar
- 81. Li R, Zhang L, Shi Q, Guo Y, Zhang W, Zhou B. A protective role of autophagy in TDCIPP-induced developmental neurotoxicity in ze-brafish larvae. Aquat Toxicol 2018; 199: 46-54.
google scholar
- 82. Shi Q, Wang M, Shi F, Yang L, Guo Y, Feng C, et al. Developmental neurotoxicity of triphenyl phosphate in zebrafish larvae. Aquat Toxicol 2018; 203: 80-7. google scholar
- 83. Lee S, Chun HS, Lee J, Park HJ, Kim KT, Kim CH, et al. Plausibility of the zebrafish embryos/larvae as an alternative animal model for autism: A comparison study of
transcriptome changes. PloS one 2018; 13(9): e0203543. google scholar
- 84. Chen J, Lei L, Tian L, et al. Developmental and behavioral alter-ations in zebrafish embryonically exposed to valproic acid (VPA): An aquatic model for autism. Neurotoxicol Teratol 2018; 66: 8-16. google scholar