Issue
Zebrafish; an emerging model organism for studying toxicity and biocompatibility of dental materials
Corresponding Author(s) : Ebru Emekli-Alturfan
Cellular and Molecular Biology,
Vol. 66 No. 8: Issue 8
Abstract
Zebrafish (danio rerio) is a small, tropical freshwater teleost fish that belongs to the Cyprinidae family and lives in natural waters and rice fields in South Asia, North India, and Pakistan. Zebrafish has become a popular vertebrate model organism for biomedical research due to its numerous advantages such as their small size, short life cycle, accessibility in large numbers and inexpensive maintenance. In addition, fertilization happens externally in zebrafish and allows zebrafish to be manipulated directly. As another important advantage, the embryos are transparent thus the stages of development can be easily identified. Zebrafish can have multiple co-orthologs for human genes. In the 1930s, the zebrafish was first used as a model for developmental and embryological studies and in 1981, was introduced as a genetic model by Streisinger by force of developed genetic techniques in zebrafish such as cloning, mutagenesis and transgenesis. In the 1990s, various genetic manipulations were introduced. These improvements have contributed to the popularity of zebrafish. After that zebrafish was used in various research areas including genetics, biomedicine, neurobiology, toxicology, pharmacology as well as in human disease models. Zebrafish is also becoming a popular model organism in dental research. It is preferred in dental material toxicity studies and in research related to the genetic and molecular factors in tooth formation and craniofacial development. This review provides information on the use of zebrafish in dental research, focusing on tooth formation and dentition (pharyngeal dentition) of zebrafish and the dental research performed using zebrafish.
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- Bolis C, Piccolella M, Dalla Valle A, Rankin JC. Fish as model in pharmacological and biological research. Pharmacological research 2001; 44(4):265-280.
- Williams CH and Hong CC. Multi-step usage of in vivo models during rational drug design and discovery. International Journal of Molecular Sciences, 2011; 12(4): 2262-2274.
- Filazi A and í–zhancı L. Genetically Modified Animals in Pharmacology and Toxicology Research: Review.Turkiye Klinikleri Journal of Laboratory Animals. 2017; 1(1): p. 28-40.
- Saleem S and Kannan RR. Zebrafish: an emerging real-time model system to study Alzheimer's disease and neurospecific drug discovery. Cell Death Discov 2018; 4: 45.
- Van der heyden C and Huysseune A. Dynamics of tooth formation and replacement in the zebrafish (Danio rerio)(Teleostei, Cyprinidae. Developmental dynamics: an official publication of the American Association of Anatomists, 2000; 219(4): 486-496.
- Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995;203(3):253-310.
- Detrich HW, Westerfield M, Zon LI. Overview of the Zebrafish system. Methods Cell Biol. 1999; 59: 3–10.
- Lieschke GJ and Currie PD. Animal models of human disease: zebrafish swim into view. Nature Reviews Genetics, 2007; 8(5): 353.
- Gerlai R. Zebra fish: an uncharted behavior genetic model. Behavior Genetics 2003; 33(5): 461-468.
- Langheinrich U. Zebrafish: a new model on the pharmaceutical catwalk. Bioessays 2003; 25(9): 904-912.
- Sieber S, Grossen P, Bussmann J, et al. Zebrafish as a preclinical in vivo screening model for nanomedicines. Adv Drug Del Rev 2019; 151-152:152-168.
- Beis D and Stainier DY. In vivo cell biology: following the zebrafish trend. Trends in cell Biology 2006; 16(2): 105-112.
- Wautier K and Huysseune A. Tooth succession in the zebrafish (Danio rerio). Archives of oral biology 2001;46(11): 1051-1058.
- Kari G, Rodeck U, Dicker AP. Zebrafish: an emerging model system for human disease and drug discovery. Clinical Pharmacology & Therapeutics 2007; 82(1):70-80.
- Ali S, Champagne DL, Spaink HP, Richardson MK. Zebrafish embryos and larvae: a new generation of disease models and drug screens. Birth Defects Research Part C: Embryo Today: Reviews. 2011; 93(2):115-133.
- Ustündağ íœV, í‡alıskan-Ak E, Ateş PS. et al. White LED Light Exposure Inhibits the Development and Xanthophore Pigmentation of Zebrafish Embryo. Sci Rep 2019; 9(1): 10810.
- íœnal ć° and Emekli-Alturfan E. Fishing for Parkinson's Disease: A review of the literature. J Clin Neurosci 2019; 62:1-62019.
- íœnal ć°, íœstündağ íœV, Ateş PS, et al. Rotenone impairs oxidant/antioxidant balance both in brain and intestines in zebrafish. Int J Neurosci 2019;129(4):363-368.
- Ateş PS, íœnal ć°, íœstündağ íœV, et al. Methylparaben induces malformations and alterations on apoptosis, oxidant-antioxidant status, ccnd1 and myca expressions in zebrafish embryos. J Biochem Mol Toxicol 2018; 32(3):e22036
- Eryılmaz O, Ateş PS, íœnal ć°, et al. Evaluation of the interaction between proliferation, oxidant-antioxidant status, Wnt pathway, and apoptosis in zebrafish embryos exposed to silver nanoparticles used in textile industry. J Biochem Mol Toxicol. 2018;32(1):10.1002/jbt.22015.
- íœstündağ íœV, íœnal ć°, Ateş PS, Alturfan AA, Yiğitbaşı T, Emekli-Alturfan E. Bisphenol A and di(2-ethylhexyl) phthalate exert divergent effects on apoptosis and the Wnt/β-catenin pathway in zebrafish embryos: A possible mechanism of endocrine disrupting chemical action. Toxicol Ind Health 2017;33(12):901-910.
- Huysseune A and JY Sire. Development and fine structure of pharyngeal replacement teeth in juvenile zebrafish (Danio rerio)(Teleostei, Cyprinidae). Cell Tissue Res 2000; 302(2): 205-219.
- Huysseune A and JY Sire. Early development of the zebrafish (Danio rerio) pharyngeal dentition (Teleostei, Cyprinidae). Anat Embryol 1998; 198(4): 289-305.
- Cubbage CC and Mabee PM. Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). J Morphol 1996; 229(2): 121-160.
- Schilling TF, Piotrowski T, Grandel H, et al. Jaw and branchial arch mutants in zebrafish I: branchial arches. Development 1996;123:329-344.
- Wautier K, Huysseune A. Tooth succession in the zebrafish (Danio rerio). Arch Oral Biol 2001; 46(11):1051-1058.
- Wiweger MI, Zhao Z, van Merkesteyn RJ, Roehl HH, Hogendoorn PC. HSPG-deficient zebrafish uncovers dental aspect of multiple osteochondromas. PLoS One 2012;7(1):e29734.
- Stock DW. Zebrafish dentition in comparative context. J Exp Zool B Mol Dev Evol 2007; 308(5):523-549.
- Smith KK. Heterochrony revisited: the evolution of developmental sequences, Biol J Linn Soc 2001; 73(2): 169–186.
- Evans HE, Deubler EE. Pharyngeal tooth replacement in Semotilus atromaculatus and Clinostomus elongatus, two species of cyprinid fishes. Copeia 1955(1):31-41.
- Nakajima T. The development and replacement pattern of the pharyngeal dentition in the Japanese cyprinid fish, Gnathopogon coerulescens. Copeia 1979; 22-28.
- Klein OD, OberoiS, Huysseune A, Hovorakova M, Peterka M, Peterkova R. Developmental disorders of the dentition: an update, Am J Med Genet C. 2013; 163(4): 318-332.
- Verstraeten B, van Hengel J, Sanders E, Van Roy F, Huysseune A. 2013. N-cadherin is required for cytodifferentiation during zebrafish odontogenesis. Journal of dental research. 92(4):365-370.
- Wise, S.B. and D.W. Stock, bmp2b and bmp4 are dispensable for zebrafish tooth development. Developmental Dynamics, 2010. 239(10): p. 2534-2546.
- Jackman WR, Yoo JJ, Stock DW. Hedgehog signaling is required at multiple stages of zebrafish tooth development. BMC Dev Biol 2010; 10(1):119.
- Verstraeten B, Sanders E, Van Hengel J, Huysseune A. Expression pattern of E"cadherin during development of the first tooth in zebrafish (Danio rerio). J Appl Ichthyol 2010; 26(2):202-204.
- Machado RG, Eames BF. Using zebrafish to test the genetic basis of human craniofacial diseases. Dent Res 2017; 96(11):1192-1199.
- Neues F, Arnold W, Fischer J, Beckmann F, Gaengler P, Epple M. 2006. The skeleton and pharyngeal teeth of zebrafish (Danio rerio) as a model of biomineralization in vertebrates. Materialwiss Werkst 2006; 37(6):426-431.
- Smith TL. Use of zebrafish to test candidate genes and mutations associated with structural birth defects, primarily in cleft lip and palate. 2014; University of Iowa https://doi.org/10.17077/etd.tmmb4ya6
- Neuhauss S, Solnica-Krezel L, Schier AF, Zwartkruis F, Stemple DL, Malicki J, Abdelilah S, Stainier D, Driever W. Mutations affecting craniofacial development in zebrafish. Development 1996; 123(1):357-367.
- Schilling TF, Piotrowski T, Grandel H, Brand M, Heisenberg C-P, Jiang Y-J, Beuchle D, Hammerschmidt M, Kane DA, Mullins MC. Jaw and branchial arch mutants in zebrafish I: branchial arches. Development 1996; 123(1):329-344.
- Piotrowski T, Schilling TF, Brand M, Jiang Y-J, Heisenberg C-P, Beuchle D, Grandel H, Van Eeden F, Furutani-Seiki M, Granato M. Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. Development 1996; 123(1):345-356.
- Cox SG, Kim H, Garnett AT, Medeiros DM, An W, Crump JG. An essential role of variant histone H3. 3 for ectomesenchyme potential of the cranial neural crest. PLoS Gen 2012; 8(9):e1002938.
- Ignatius MS, Eroglu AU, Malireddy S, Gallagher G, Nambiar RM, Henion PD. Distinct functional and temporal requirements for zebrafish Hdac1 during neural crest-derived craniofacial and peripheral neuron development. PLoS One 2013; 8(5):e63218.
- Bartlett J, Dwyer S, Beniash E, Skobe Z, Payne-Ferreira T. Fluorosis: a new model and new insights. J Dent Res 2005; 84(9):832-836.
- Zhang Y, Zhang Y, Zheng X, Xu R, He H, Duan X. Grading and quantification of dental fluorosis in zebrafish larva. Arch Oral Biol 2016; 70:16-23.
- Samuel RR, Annadurai G, Rajeshkumar S. Characterization and toxicology evaluation of zirconium oxide nanoparticles on the embryonic development of zebrafish, Danio rerio. Drug Chem Toxicol 2019; 42(1):104-111.
- Zhao L, Si J, Wei Y, Li S, Jiang Y, Zhou R, Liu B, Zhang H. Toxicity of porcelain-fused-to-metal substrate to zebrafish (Danio rerio) embryos and larvae. Life Sci 2018; 203:66-71.
- Makkar H, Verma SK, Panda PK, Jha E, Das B, Mukherjee K, Suar M. In vivo molecular toxicity profile of dental bioceramics in embryonic Zebrafish (Danio rerio). Chem Res Toxicol 2018; 31(9):914-923.
- Kramer AG, Vuthiganon J, Lassiter CS. Bis-GMA affects craniofacial development in zebrafish embryos (Danio rerio). Environ Toxicol Pharmacol 2016; 43:159-165.
- Altayıb B, Eğilmezer G, íœnal ć°, íœstündağ íœV, Gözneli R. 2019. Effects of Methacrylate Exposure on Developing Zebrafish Embryos. Eur J Res Dent 2019; 3(1):25-28.
- Widziolek M, Prajsnar TK, Tazzyman S, Stafford GP, Potempa J, Murdoch C. Zebrafish as a new model to study effects of periodontal pathogens on cardiovascular diseases. Sci Rep 2016; 6:36023.
References
Bolis C, Piccolella M, Dalla Valle A, Rankin JC. Fish as model in pharmacological and biological research. Pharmacological research 2001; 44(4):265-280.
Williams CH and Hong CC. Multi-step usage of in vivo models during rational drug design and discovery. International Journal of Molecular Sciences, 2011; 12(4): 2262-2274.
Filazi A and í–zhancı L. Genetically Modified Animals in Pharmacology and Toxicology Research: Review.Turkiye Klinikleri Journal of Laboratory Animals. 2017; 1(1): p. 28-40.
Saleem S and Kannan RR. Zebrafish: an emerging real-time model system to study Alzheimer's disease and neurospecific drug discovery. Cell Death Discov 2018; 4: 45.
Van der heyden C and Huysseune A. Dynamics of tooth formation and replacement in the zebrafish (Danio rerio)(Teleostei, Cyprinidae. Developmental dynamics: an official publication of the American Association of Anatomists, 2000; 219(4): 486-496.
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995;203(3):253-310.
Detrich HW, Westerfield M, Zon LI. Overview of the Zebrafish system. Methods Cell Biol. 1999; 59: 3–10.
Lieschke GJ and Currie PD. Animal models of human disease: zebrafish swim into view. Nature Reviews Genetics, 2007; 8(5): 353.
Gerlai R. Zebra fish: an uncharted behavior genetic model. Behavior Genetics 2003; 33(5): 461-468.
Langheinrich U. Zebrafish: a new model on the pharmaceutical catwalk. Bioessays 2003; 25(9): 904-912.
Sieber S, Grossen P, Bussmann J, et al. Zebrafish as a preclinical in vivo screening model for nanomedicines. Adv Drug Del Rev 2019; 151-152:152-168.
Beis D and Stainier DY. In vivo cell biology: following the zebrafish trend. Trends in cell Biology 2006; 16(2): 105-112.
Wautier K and Huysseune A. Tooth succession in the zebrafish (Danio rerio). Archives of oral biology 2001;46(11): 1051-1058.
Kari G, Rodeck U, Dicker AP. Zebrafish: an emerging model system for human disease and drug discovery. Clinical Pharmacology & Therapeutics 2007; 82(1):70-80.
Ali S, Champagne DL, Spaink HP, Richardson MK. Zebrafish embryos and larvae: a new generation of disease models and drug screens. Birth Defects Research Part C: Embryo Today: Reviews. 2011; 93(2):115-133.
Ustündağ íœV, í‡alıskan-Ak E, Ateş PS. et al. White LED Light Exposure Inhibits the Development and Xanthophore Pigmentation of Zebrafish Embryo. Sci Rep 2019; 9(1): 10810.
íœnal ć° and Emekli-Alturfan E. Fishing for Parkinson's Disease: A review of the literature. J Clin Neurosci 2019; 62:1-62019.
íœnal ć°, íœstündağ íœV, Ateş PS, et al. Rotenone impairs oxidant/antioxidant balance both in brain and intestines in zebrafish. Int J Neurosci 2019;129(4):363-368.
Ateş PS, íœnal ć°, íœstündağ íœV, et al. Methylparaben induces malformations and alterations on apoptosis, oxidant-antioxidant status, ccnd1 and myca expressions in zebrafish embryos. J Biochem Mol Toxicol 2018; 32(3):e22036
Eryılmaz O, Ateş PS, íœnal ć°, et al. Evaluation of the interaction between proliferation, oxidant-antioxidant status, Wnt pathway, and apoptosis in zebrafish embryos exposed to silver nanoparticles used in textile industry. J Biochem Mol Toxicol. 2018;32(1):10.1002/jbt.22015.
íœstündağ íœV, íœnal ć°, Ateş PS, Alturfan AA, Yiğitbaşı T, Emekli-Alturfan E. Bisphenol A and di(2-ethylhexyl) phthalate exert divergent effects on apoptosis and the Wnt/β-catenin pathway in zebrafish embryos: A possible mechanism of endocrine disrupting chemical action. Toxicol Ind Health 2017;33(12):901-910.
Huysseune A and JY Sire. Development and fine structure of pharyngeal replacement teeth in juvenile zebrafish (Danio rerio)(Teleostei, Cyprinidae). Cell Tissue Res 2000; 302(2): 205-219.
Huysseune A and JY Sire. Early development of the zebrafish (Danio rerio) pharyngeal dentition (Teleostei, Cyprinidae). Anat Embryol 1998; 198(4): 289-305.
Cubbage CC and Mabee PM. Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). J Morphol 1996; 229(2): 121-160.
Schilling TF, Piotrowski T, Grandel H, et al. Jaw and branchial arch mutants in zebrafish I: branchial arches. Development 1996;123:329-344.
Wautier K, Huysseune A. Tooth succession in the zebrafish (Danio rerio). Arch Oral Biol 2001; 46(11):1051-1058.
Wiweger MI, Zhao Z, van Merkesteyn RJ, Roehl HH, Hogendoorn PC. HSPG-deficient zebrafish uncovers dental aspect of multiple osteochondromas. PLoS One 2012;7(1):e29734.
Stock DW. Zebrafish dentition in comparative context. J Exp Zool B Mol Dev Evol 2007; 308(5):523-549.
Smith KK. Heterochrony revisited: the evolution of developmental sequences, Biol J Linn Soc 2001; 73(2): 169–186.
Evans HE, Deubler EE. Pharyngeal tooth replacement in Semotilus atromaculatus and Clinostomus elongatus, two species of cyprinid fishes. Copeia 1955(1):31-41.
Nakajima T. The development and replacement pattern of the pharyngeal dentition in the Japanese cyprinid fish, Gnathopogon coerulescens. Copeia 1979; 22-28.
Klein OD, OberoiS, Huysseune A, Hovorakova M, Peterka M, Peterkova R. Developmental disorders of the dentition: an update, Am J Med Genet C. 2013; 163(4): 318-332.
Verstraeten B, van Hengel J, Sanders E, Van Roy F, Huysseune A. 2013. N-cadherin is required for cytodifferentiation during zebrafish odontogenesis. Journal of dental research. 92(4):365-370.
Wise, S.B. and D.W. Stock, bmp2b and bmp4 are dispensable for zebrafish tooth development. Developmental Dynamics, 2010. 239(10): p. 2534-2546.
Jackman WR, Yoo JJ, Stock DW. Hedgehog signaling is required at multiple stages of zebrafish tooth development. BMC Dev Biol 2010; 10(1):119.
Verstraeten B, Sanders E, Van Hengel J, Huysseune A. Expression pattern of E"cadherin during development of the first tooth in zebrafish (Danio rerio). J Appl Ichthyol 2010; 26(2):202-204.
Machado RG, Eames BF. Using zebrafish to test the genetic basis of human craniofacial diseases. Dent Res 2017; 96(11):1192-1199.
Neues F, Arnold W, Fischer J, Beckmann F, Gaengler P, Epple M. 2006. The skeleton and pharyngeal teeth of zebrafish (Danio rerio) as a model of biomineralization in vertebrates. Materialwiss Werkst 2006; 37(6):426-431.
Smith TL. Use of zebrafish to test candidate genes and mutations associated with structural birth defects, primarily in cleft lip and palate. 2014; University of Iowa https://doi.org/10.17077/etd.tmmb4ya6
Neuhauss S, Solnica-Krezel L, Schier AF, Zwartkruis F, Stemple DL, Malicki J, Abdelilah S, Stainier D, Driever W. Mutations affecting craniofacial development in zebrafish. Development 1996; 123(1):357-367.
Schilling TF, Piotrowski T, Grandel H, Brand M, Heisenberg C-P, Jiang Y-J, Beuchle D, Hammerschmidt M, Kane DA, Mullins MC. Jaw and branchial arch mutants in zebrafish I: branchial arches. Development 1996; 123(1):329-344.
Piotrowski T, Schilling TF, Brand M, Jiang Y-J, Heisenberg C-P, Beuchle D, Grandel H, Van Eeden F, Furutani-Seiki M, Granato M. Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. Development 1996; 123(1):345-356.
Cox SG, Kim H, Garnett AT, Medeiros DM, An W, Crump JG. An essential role of variant histone H3. 3 for ectomesenchyme potential of the cranial neural crest. PLoS Gen 2012; 8(9):e1002938.
Ignatius MS, Eroglu AU, Malireddy S, Gallagher G, Nambiar RM, Henion PD. Distinct functional and temporal requirements for zebrafish Hdac1 during neural crest-derived craniofacial and peripheral neuron development. PLoS One 2013; 8(5):e63218.
Bartlett J, Dwyer S, Beniash E, Skobe Z, Payne-Ferreira T. Fluorosis: a new model and new insights. J Dent Res 2005; 84(9):832-836.
Zhang Y, Zhang Y, Zheng X, Xu R, He H, Duan X. Grading and quantification of dental fluorosis in zebrafish larva. Arch Oral Biol 2016; 70:16-23.
Samuel RR, Annadurai G, Rajeshkumar S. Characterization and toxicology evaluation of zirconium oxide nanoparticles on the embryonic development of zebrafish, Danio rerio. Drug Chem Toxicol 2019; 42(1):104-111.
Zhao L, Si J, Wei Y, Li S, Jiang Y, Zhou R, Liu B, Zhang H. Toxicity of porcelain-fused-to-metal substrate to zebrafish (Danio rerio) embryos and larvae. Life Sci 2018; 203:66-71.
Makkar H, Verma SK, Panda PK, Jha E, Das B, Mukherjee K, Suar M. In vivo molecular toxicity profile of dental bioceramics in embryonic Zebrafish (Danio rerio). Chem Res Toxicol 2018; 31(9):914-923.
Kramer AG, Vuthiganon J, Lassiter CS. Bis-GMA affects craniofacial development in zebrafish embryos (Danio rerio). Environ Toxicol Pharmacol 2016; 43:159-165.
Altayıb B, Eğilmezer G, íœnal ć°, íœstündağ íœV, Gözneli R. 2019. Effects of Methacrylate Exposure on Developing Zebrafish Embryos. Eur J Res Dent 2019; 3(1):25-28.
Widziolek M, Prajsnar TK, Tazzyman S, Stafford GP, Potempa J, Murdoch C. Zebrafish as a new model to study effects of periodontal pathogens on cardiovascular diseases. Sci Rep 2016; 6:36023.