wnt10a is required for zebrafish median fin fold maintenance and adult unpaired fin metamorphosis.

fin metamorphosis median fin fold tooth development wnt10a zebrafish

Journal

Developmental dynamics : an official publication of the American Association of Anatomists
ISSN: 1097-0177
Titre abrégé: Dev Dyn
Pays: United States
ID NLM: 9201927

Informations de publication

Date de publication:
23 Oct 2023
Historique:
revised: 03 10 2023
received: 24 08 2023
accepted: 08 10 2023
medline: 23 10 2023
pubmed: 23 10 2023
entrez: 23 10 2023
Statut: aheadofprint

Résumé

Mutations of human WNT10A are associated with odonto-ectodermal dysplasia syndromes. Here, we present analyses of wnt10a loss-of-function mutants in the zebrafish. wnt10a mutant zebrafish embryos display impaired tooth development and a collapsing median fin fold (MFF). Rescue experiments show that wnt10a is essential for MFF maintenance both during embryogenesis and later metamorphosis. The MFF collapse could not be attributed to increased cell death or altered proliferation rates of MFF cell types. Rather, wnt10a mutants show reduced expression levels of dlx2a in distal-most MFF cells, followed by compromised expression of col1a1a and other extracellular matrix proteins encoding genes. Transmission electron microscopy analysis shows that although dermal MFF compartments of wnt10a mutants initially are of normal morphology, with regular collagenous actinotrichia, positioning of actinotrichia within the cleft of distal MFF cells becomes compromised, coinciding with actinotrichia shrinkage and MFF collapse. MFF collapse of wnt10a mutant zebrafish is likely caused by the loss of distal properties in the developing MFF, strikingly similar to the proposed molecular pathomechanisms underlying the teeth defects caused by the loss of Wnt10 in fish and mammals. In addition, it points to thus fur unknown mechanisms controlling the linear growth and stability of actinotrichia and their collagen fibrils.

Sections du résumé

BACKGROUND BACKGROUND
Mutations of human WNT10A are associated with odonto-ectodermal dysplasia syndromes. Here, we present analyses of wnt10a loss-of-function mutants in the zebrafish.
RESULTS RESULTS
wnt10a mutant zebrafish embryos display impaired tooth development and a collapsing median fin fold (MFF). Rescue experiments show that wnt10a is essential for MFF maintenance both during embryogenesis and later metamorphosis. The MFF collapse could not be attributed to increased cell death or altered proliferation rates of MFF cell types. Rather, wnt10a mutants show reduced expression levels of dlx2a in distal-most MFF cells, followed by compromised expression of col1a1a and other extracellular matrix proteins encoding genes. Transmission electron microscopy analysis shows that although dermal MFF compartments of wnt10a mutants initially are of normal morphology, with regular collagenous actinotrichia, positioning of actinotrichia within the cleft of distal MFF cells becomes compromised, coinciding with actinotrichia shrinkage and MFF collapse.
CONCLUSIONS CONCLUSIONS
MFF collapse of wnt10a mutant zebrafish is likely caused by the loss of distal properties in the developing MFF, strikingly similar to the proposed molecular pathomechanisms underlying the teeth defects caused by the loss of Wnt10 in fish and mammals. In addition, it points to thus fur unknown mechanisms controlling the linear growth and stability of actinotrichia and their collagen fibrils.

Identifiants

pubmed: 37870737
doi: 10.1002/dvdy.672
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM063904
Pays : United States

Informations de copyright

© 2023 The Authors. Developmental Dynamics published by Wiley Periodicals LLC on behalf of American Association for Anatomy.

Références

MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell. 2009;17(1):9-26. doi:10.1016/j.devcel.2009.06.016
Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004;20:781-810. doi:10.1146/annurev.cellbio.20.010403.113126
Dassule HR, McMahon AP. Analysis of epithelial-mesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev Biol. 1998;202(2):215-227. doi:10.1006/dbio.1998.8992
Yamashiro T, Zheng L, Shitaku Y, et al. Wnt10a regulates dentin sialophosphoprotein mRNA expression and possibly links odontoblast differentiation and tooth morphogenesis. Differentiation. 2007;75(5):452-462. doi:10.1111/j.1432-0436.2006.00150.x
Reddy S, Andl T, Bagasra A, et al. Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis. Mech Dev. 2001;107(1-2):69-82. doi:10.1016/s0925-4773(01)00452-x
Narita T, Sasaoka S, Udagawa K, et al. Wnt10a is involved in AER formation during chick limb development. Dev Dyn. 2005;233(2):282-287. doi:10.1002/dvdy.20321
Adaimy L, Chouery E, Megarbane H, et al. Mutation in WNT10A is associated with an autosomal recessive ectodermal dysplasia: the odonto-onycho-dermal dysplasia. Am J Hum Genet. 2007;81(4):821-828. doi:10.1086/520064
Schöpf E, Schulz HJ, Passarge E. Syndrome of cystic eyelids, palmo-plantar keratosis, hypodontia and hypotrichosis as a possible autosomal recessive trait. Birth Defects Orig Artic Ser. 1971;7(8):219-221.
Bohring A, Stamm T, Spaich C, et al. WNT10A mutations are a frequent cause of a broad spectrum of ectodermal dysplasias with sex-biased manifestation pattern in heterozygotes. Am J Hum Genet. 2009;85(1):97-105. doi:10.1016/j.ajhg.2009.06.001
Yuan Q, Zhao M, Tandon B, et al. Role of WNT10A in failure of tooth development in humans and zebrafish. Mol Genet Genomic Med. 2017;5(6):730-741. doi:10.1002/mgg3.332
Stoick-Cooper CL, Weidinger G, Riehle KJ, et al. Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development. 2007;134(3):479-489. doi:10.1242/dev.001123
Aman AJ, Fulbright AN, Parichy DM. Wnt/beta-catenin regulates an ancient signaling network during zebrafish scale development. Elife. 2018;7:e37001. doi:10.7554/eLife.37001
Nagendran M, Arora P, Gori P, et al. Canonical Wnt signalling regulates epithelial patterning by modulating levels of laminins in zebrafish appendages. Development. 2015;142(2):320-330. doi:10.1242/dev.118703
Nagayoshi S, Hayashi E, Abe G, et al. Insertional mutagenesis by the Tol2 transposon-mediated enhancer trap approach generated mutations in two developmental genes: tcf7 and synembryn-like. Development. 2008;135(1):159-169. doi:10.1242/dev.009050
Miyamoto K, Kawakami K, Tamura K, Abe G. Developmental independence of median fins from the larval fin fold revises their evolutionary origin. Sci Rep. 2022;12(1):7521. doi:10.1038/s41598-022-11180-1
Tzung KW, Lalonde RL, Prummel KD, et al. A median fin derived from the lateral plate mesoderm and the origin of paired fins. Nature. 2023;618(7965):543-549. doi:10.1038/s41586-023-06100-w
Parichy DM, Elizondo MR, Mills MG, Gordon TN, Engeszer RE. Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Dev Dyn. 2009;238(12):2975-3015. doi:10.1002/dvdy.22113
Spoorendonk KM, Peterson-Maduro J, Renn J, et al. Retinoic acid and Cyp26b1 are critical regulators of osteogenesis in the axial skeleton. Development. 2008;135(22):3765-3774. doi:10.1242/dev.024034
Iwasaki M, Kuroda J, Kawakami K, Wada H. Epidermal regulation of bone morphogenesis through the development and regeneration of osteoblasts in the zebrafish scale. Dev Biol. 2018;437(2):105-119. doi:10.1016/j.ydbio.2018.03.005
Sire JY, Allizard F, Babiar O, Bourguignon J, Quilhac A. Scale development in zebrafish (Danio rerio). J Anat. 1997;190:545-561. doi:10.1046/j.1469-7580.1997.19040545.x
Plaisancie J, Bailleul-Forestier I, Gaston V, et al. Mutations in WNT10A are frequently involved in oligodontia associated with minor signs of ectodermal dysplasia. Am J Med Genet A. 2013;161A(4):671-678. doi:10.1002/ajmg.a.35747
Yang J, Wang SK, Choi M, et al. Taurodontism, variations in tooth number, and misshapened crowns in Wnt10a null mice and human kindreds. Mol Genet Genomic Med. 2015;3(1):40-58. doi:10.1002/mgg3.111
Yu M, Liu Y, Liu H, et al. Distinct impacts of bi-allelic WNT10A mutations on the permanent and primary dentitions in odonto-onycho-dermal dysplasia. Am J Med Genet A. 2019;179(1):57-64. doi:10.1002/ajmg.a.60682
Huysseune A, Van der Heyden C, Sire JY. Early development of the zebrafish (Danio rerio) pharyngeal dentition (Teleostei, Cyprinidae). Anat Embryol. 1998;198(4):289-305. doi:10.1007/s004290050185
Van der Heyden C, Huysseune A. Dynamics of tooth formation and replacement in the zebrafish (Danio rerio) (Teleostei, Cyprinidae). Dev Dyn. 2000;219(4):486-496. doi:10.1002/1097-0177(2000)9999:9999
Verstraeten B, Sanders E, van Hengel J, Huysseune A. Zebrafish teeth as a model for repetitive epithelial morphogenesis: dynamics of E-cadherin expression. BMC Dev Biol. 2010;10:58. doi:10.1186/1471-213X-10-58
Huysseune A, Sire JY. Evolution of patterns and processes in teeth and tooth-related tissues in non-mammalian vertebrates. Eur J Oral Sci. 1998;106(Suppl 1):S437-S481. doi:10.1111/j.1600-0722.1998.tb02211.x
Jernvall J, Thesleff I. Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev. 2000;92(1):19-29. doi:10.1016/s0925-4773(99)00322-6
Thesleff I. Epithelial-mesenchymal signalling regulating tooth morphogenesis. J Cell Sci. 2003;116:1647-1648. doi:10.1242/jcs.00410
Miletich I, Sharpe PT. Normal and abnormal dental development. Hum Mol Genet 2003;12(Spec No 1):R69-R73. 10.1093/hmg/ddg085
Jackman WR, Draper BW, Stock DW. Fgf signaling is required for zebrafish tooth development. Dev Biol. 2004;274(1):139-157. doi:10.1016/j.ydbio.2004.07.003
Chen J, Lan Y, Baek JA, Gao Y, Jiang R. Wnt/beta-catenin signaling plays an essential role in activation of odontogenic mesenchyme during early tooth development. Dev Biol. 2009;334(1):174-185. doi:10.1016/j.ydbio.2009.07.015
Shimizu N, Kawakami K, Ishitani T. Visualization and exploration of Tcf/Lef function using a highly responsive Wnt/beta-catenin signaling-reporter transgenic zebrafish. Dev Biol. 2012;370(1):71-85. doi:10.1016/j.ydbio.2012.07.016
Tucker AS, Headon DJ, Schneider P, et al. Edar/Eda interactions regulate enamel knot formation in tooth morphogenesis. Development. 2000;127(21):4691-4700. doi:10.1242/dev.127.21.4691
Aigler SR, Jandzik D, Hatta K, Uesugi K, Stock DW. Selection and constraint underlie irreversibility of tooth loss in cypriniform fishes. Proc Natl Acad Sci U S A. 2014;111(21):7707-7712. doi:10.1073/pnas.1321171111
Mandler M, Neubuser A. FGF signaling is necessary for the specification of the odontogenic mesenchyme. Dev Biol. 2001;240(2):548-559. doi:10.1006/dbio.2001.0490
Kratochwil K, Galceran J, Tontsch S, Roth W, Grosschedl R. FGF4, a direct target of LEF1 and Wnt signaling, can rescue the arrest of tooth organogenesis in Lef1(−/−) mice. Genes Dev. 2002;16(24):3173-3185. doi:10.1101/gad.1035602
Thomas BL, Tucker AS, Qui M, et al. Role of Dlx-1 and Dlx-2 genes in patterning of the murine dentition. Development. 1997;124(23):4811-4818. doi:10.1242/dev.124.23.4811
Panganiban G, Rubenstein JL. Developmental functions of the Distal-less/Dlx homeobox genes. Development. 2002;129(19):4371-4386.
Jackman WR, Stock DW. Transgenic analysis of Dlx regulation in fish tooth development reveals evolutionary retention of enhancer function despite organ loss. Proc Natl Acad Sci U S A. 2006;103(51):19390-19395. doi:10.1073/pnas.0609575103
Liu F, Chu EY, Watt B, et al. Wnt/beta-catenin signaling directs multiple stages of tooth morphogenesis. Dev Biol. 2008;313(1):210-224. doi:10.1016/j.ydbio.2007.10.016
Glinka A, Wu W, Delius H, Monaghan AP, Blumenstock C, Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature. 1998;391(6665):357-362. doi:10.1038/34848
van de Water S, van de Wetering M, Joore J, et al. Ectopic Wnt signal determines the eyeless phenotype of zebrafish masterblind mutant. Development. 2001;128(20):3877-3888.
Grandel H, Draper BW, Schulte-Merker S. Dackel acts in the ectoderm of the zebrafish pectoral fin bud to maintain AER signaling. Development. 2000;127(19):4169-4178.
Geraudie J, Ferretti P. Correlation between RA-induced apoptosis and patterning defects in regenerating fins and limbs. Int J Dev Biol. 1997;41(3):529-532.
Todt WL, Fallon JF. Development of the apical ectodermal ridge in the chick wing bud. J Embryol Exp Morphol. 1984;80:21-41.
Dane PJ, Tucker JB. Modulation of epidermal cell shaping and extracellular matrix during caudal fin morphogenesis in the zebra fish Brachydanio rerio. J Embryol Exp Morphol. 1985;87:145-161.
Wood A, Thorogood P. An ultrastructural and morphometric analysis of an in vivo contact guidance system. Development. 1987;101:363-381.
Carney TJ, Feitosa NM, Sonntag C, et al. Genetic analysis of fin development in zebrafish identifies furin and hemicentin1 as potential novel fraser syndrome disease genes. PLoS Genet. 2010;6(4):e1000907. doi:10.1371/journal.pgen.1000907
Zhang J, Wagh P, Guay D, et al. Loss of fish actinotrichia proteins and the fin-to-limb transition. Nature. 2010;466(7303):234-237. doi:10.1038/nature09137
Duran I, Mari-Beffa M, Santamaria JA, Becerra J, Santos-Ruiz L. Actinotrichia collagens and their role in fin formation. Dev Biol. 2011;354(1):160-172. doi:10.1016/j.ydbio.2011.03.014
Lalonde RL, Akimenko MA. Effects of fin fold mesenchyme ablation on fin development in zebrafish. PLoS One. 2018;13(2):e0192500. doi:10.1371/journal.pone.0192500
Webb AE, Sanderford J, Frank D, Talbot WS, Driever W, Kimelman D. Laminin alpha5 is essential for the formation of the zebrafish fins. Dev Biol. 2007;311(2):369-382. doi:10.1016/j.ydbio.2007.08.034
Wood A, Thorogood P. An analysis of in vivo cell migration during teleost fin morphogenesis. J Cell Sci. 1984;66:205-222.
Westcot SE, Hatzold J, Urban MD, et al. Protein-trap insertional mutagenesis uncovers new genes involved in zebrafish skin development, including a neuregulin 2a-based ErbB signaling pathway required during median fin fold morphogenesis. PLoS One. 2015;10(6):e0130688. doi:10.1371/journal.pone.0130688
Nakagawa H, Kuroda J, Aramaki T, Kondo S. Mechanical role of actinotrichia in shaping the caudal fin of zebrafish. Dev Biol. 2022;481:52-63. doi:10.1016/j.ydbio.2021.09.003
Wehner D, Cizelsky W, Vasudevaro MD, et al. Wnt/beta-catenin signaling defines organizing centers that orchestrate growth and differentiation of the regenerating zebrafish caudal fin. Cell Rep. 2014;6(3):467-481. doi:10.1016/j.celrep.2013.12.036
Feng C, Xu Z, Li Z, Zhang D, Liu Q, Lu L. Down-regulation of Wnt10a by RNA interference inhibits proliferation and promotes apoptosis in mouse embryonic palatal mesenchymal cells through Wnt/beta-catenin signaling pathway. J Physiol Biochem. 2013;69(4):855-863. doi:10.1007/s13105-013-0262-7
Xu M, Horrell J, Snitow M, et al. WNT10A mutation causes ectodermal dysplasia by impairing progenitor cell proliferation and KLF4-mediated differentiation. Nat Commun. 2017;8:15397. doi:10.1038/ncomms15397
Shalini S, Dorstyn L, Dawar S, Kumar S. Old, new and emerging functions of caspases. Cell Death Differ. 2015;22(4):526-539. doi:10.1038/cdd.2014.216
Rufini A, Tucci P, Celardo I, Melino G. Senescence and aging: the critical roles of p53. Oncogene. 2013;32(43):5129-5143. doi:10.1038/onc.2012.640
Choo BG, Kondrichin I, Parinov S, et al. Zebrafish transgenic enhancer TRAP line database (ZETRAP). BMC Dev Biol. 2006;6:5. doi:10.1186/1471-213X-6-5
Feitosa NM, Zhang J, Carney TJ, et al. Hemicentin 2 and fibulin 1 are required for epidermal-dermal junction formation and fin mesenchymal cell migration during zebrafish development. Dev Biol. 2012;369(2):235-248. doi:10.1016/j.ydbio.2012.06.023
Cohen SM, Bronner G, Kuttner F, Jurgens G, Jackle H. Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature. 1989;338(6214):432-434. doi:10.1038/338432a0
Gautier P, Naranjo-Golborne C, Taylor MS, Jackson IJ, Smyth I. Expression of the fras1/frem gene family during zebrafish development and fin morphogenesis. Dev Dyn. 2008;237(11):3295-3304. doi:10.1002/dvdy.21729
Asharani PV, Keupp K, Semler O, et al. Attenuated BMP1 function compromises osteogenesis, leading to bone fragility in humans and zebrafish. Am J Hum Genet. 2012;90(4):661-674. doi:10.1016/j.ajhg.2012.02.026
Zhang JL, Richetti S, Ramezani T, et al. Vertebrate extracellular matrix protein hemicentin-1 interacts physically and genetically with basement membrane protein nidogen-2. Matrix Biol. 2022;112:132-154. doi:10.1016/j.matbio.2022.08.009
Silver FH. A molecular model for linear and lateral growth of type I collagen fibrils. Coll Relat Res. 1982;2(3):219-229. doi:10.1016/s0174-173x(82)80016-2
Birk DE, Nurminskaya MV, Zycband EI. Collagen fibrillogenesis in situ: fibril segments undergo post-depositional modifications resulting in linear and lateral growth during matrix development. Dev Dyn. 1995;202(3):229-243. doi:10.1002/aja.1002020303
Moorehead C, Prudnikova K, Marcolongo M. The regulatory effects of proteoglycans on collagen fibrillogenesis and morphology investigated using biomimetic proteoglycans. J Struct Biol. 2019;206(2):204-215. doi:10.1016/j.jsb.2019.03.005
Canty EG, Lu Y, Meadows RS, Shaw MK, Holmes DF, Kadler KE. Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon. J Cell Biol. 2004;165(4):553-563. doi:10.1083/jcb.200312071
Canty EG, Starborg T, Lu Y, et al. Actin filaments are required for fibripositor-mediated collagen fibril alignment in tendon. J Biol Chem. 2006;281(50):38592-38598. doi:10.1074/jbc.M607581200
Theodore LN, Hagedorn EJ, Cortes M, et al. Distinct roles for matrix metalloproteinases 2 and 9 in embryonic hematopoietic stem cell emergence, migration, and niche colonization. Stem Cell Rep. 2017;8(5):1226-1241. doi:10.1016/j.stemcr.2017.03.016
McGraw HF, Drerup CM, Culbertson MD, Linbo T, Raible DW, Nechiporuk AV. Lef1 is required for progenitor cell identity in the zebrafish lateral line primordium. Development. 2011;138(18):3921-3930. doi:10.1242/dev.062554
van den Boogaart JG, Muller M, Osse JW. Structure and function of the median finfold in larval teleosts. J Exp Biol. 2012;215:2359-2368. doi:10.1242/jeb.065615
Zhang J, Zhang W, Shi J, Dai J, Shen SG. Dlx2 overexpression enhanced accumulation of type II collagen and aggrecan by inhibiting MMP13 expression in mice chondrocytes. Biochem Biophys Res Commun. 2018;503(2):528-535. doi:10.1016/j.bbrc.2018.05.066
Leigh NR, Schupp MO, Li K, et al. Mmp17b is essential for proper neural crest cell migration in vivo. PLoS One. 2013;8(10):e76484. doi:10.1371/journal.pone.0076484
Norton WH, Ledin J, Grandel H, Neumann CJ. HSPG synthesis by zebrafish Ext2 and Extl3 is required for Fgf10 signalling during limb development. Development. 2005;132(22):4963-4973. doi:10.1242/dev.02084
Mari-Beffa M, Murciano C. Dermoskeleton morphogenesis in zebrafish fins. Dev Dyn. 2010;239(11):2779-2794. doi:10.1002/dvdy.22444
Freitas R, Zhang G, Cohn MJ. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature. 2006;442(7106):1033-1037. doi:10.1038/nature04984
Grandel H, Schulte-Merker S. The development of the paired fins in the zebrafish (Danio rerio). Mech Dev. 1998;79(1-2):99-120. doi:10.1016/s0925-4773(98)00176-2
Ahn DG, Kourakis MJ, Rohde LA, Silver LM, Ho RK. T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature. 2002;417(6890):754-758. doi:10.1038/nature00814
Lee RT, Knapik EW, Thiery JP, Carney TJ. An exclusively mesodermal origin of fin mesenchyme demonstrates that zebrafish trunk neural crest does not generate ectomesenchyme. Development. 2013;140(14):2923-2932. doi:10.1242/dev.093534
Sharpe PT. Fish scale development: hair today, teeth and scales yesterday? Curr Biol. 2001;11(18):R751-R752. doi:10.1016/s0960-9822(01)00438-9
Harris MP, Rohner N, Schwarz H, Perathoner S, Konstantinidis P, Nusslein-Volhard C. Zebrafish eda and edar mutants reveal conserved and ancestral roles of ectodysplasin signaling in vertebrates. PLoS Genet. 2008;4(10):e1000206. doi:10.1371/journal.pgen.1000206
Lecuit T, Cohen SM. Proximal-distal axis formation in the Drosophila leg. Nature. 1997;388(6638):139-145. doi:10.1038/40563
Abe G, Ide H, Tamura K. Function of FGF signaling in the developmental process of the median fin fold in zebrafish. Dev Biol. 2007;304(1):355-366. doi:10.1016/j.ydbio.2006.12.040
Poss KD, Shen J, Nechiporuk A, et al. Roles for Fgf signaling during zebrafish fin regeneration. Dev Biol. 2000;222(2):347-358. doi:10.1006/dbio.2000.9722
Heude E, Shaikho S, Ekker M. The dlx5a/dlx6a genes play essential roles in the early development of zebrafish median fin and pectoral structures. PLoS One. 2014;9(5):e98505. doi:10.1371/journal.pone.0098505
MacNeil RL, Berry JE, Strayhorn CL, Shigeyama Y, Somerman MJ. Expression of type I and XII collagen during development of the periodontal ligament in the mouse. Arch Oral Biol. 1998;43(10):779-787. doi:10.1016/s0003-9969(98)00054-5
Sahlberg C, Reponen P, Tryggvason K, Thesleff I. Timp-1, -2 and -3 show coexpression with gelatinases A and B during mouse tooth morphogenesis. Eur J Oral Sci. 1999;107(2):121-130. doi:10.1046/j.0909-8836.1999.eos107208.x
van Eeden FJ, Granato M, Schach U, et al. Genetic analysis of fin formation in the zebrafish, Danio rerio. Development. 1996;123:255-262.
Bouzaffour M, Dufourcq P, Lecaudey V, Haas P, Vriz S. Fgf and Sdf-1 pathways interact during zebrafish fin regeneration. PloS One. 2009;4(6):e5824. doi:10.1371/journal.pone.0005824
Kwan KM, Fujimoto E, Grabher C, et al. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn. 2007;236(11):3088-3099. doi:10.1002/dvdy.21343
Parng C, Anderson N, Ton C, McGrath P. Zebrafish apoptosis assays for drug discovery. Methods Cell Biol. 2004;76:75-85. doi:10.1016/s0091-679x(04)76005-7
Kimmel CB, DeLaurier A, Ullmann B, Dowd J, McFadden M. Modes of developmental outgrowth and shaping of a craniofacial bone in zebrafish. PLoS One. 2010;5(3):e9475. doi:10.1371/journal.pone.0009475
Walker MB, Kimmel CB. A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech Histochem. 2007;82(1):23-28. doi:10.1080/10520290701333558
Hammerschmidt M, Pelegri F, Mullins MC, et al. dino and mercedes, two genes regulating dorsal development in the zebrafish embryo. Development. 1996;123:95-102.
Zakrzewska A, Cui C, Stockhammer OW, Benard EL, Spaink HP, Meijer AH. Macrophage-specific gene functions in Spi1-directed innate immunity. Blood. 2010;116(3):e1-e11.
Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676-682. doi:10.1038/nmeth.2019

Auteurs

Erica L Benard (EL)

Developmental Biology Unit, Institute of Zoology, University of Cologne, Cologne, Germany.

Ismail Küçükaylak (I)

Developmental Biology Unit, Institute of Zoology, University of Cologne, Cologne, Germany.

Julia Hatzold (J)

Developmental Biology Unit, Institute of Zoology, University of Cologne, Cologne, Germany.

Kilian U W Berendes (KUW)

Developmental Biology Unit, Institute of Zoology, University of Cologne, Cologne, Germany.

Thomas J Carney (TJ)

Discovery Research Division, Institute of Molecular and Cell Biology (IMCB), A*STAR (Agency for Science, Technology and Research), Singapore, Republic of Singapore.
Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Republic of Singapore.

Filippo Beleggia (F)

Department I of Internal Medicine, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Department of Translational Genomics, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Mildred Scheel School of Oncology Aachen Bonn Cologne Düsseldorf (MSSO ABCD), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Matthias Hammerschmidt (M)

Developmental Biology Unit, Institute of Zoology, University of Cologne, Cologne, Germany.
Center for Molecular Medicine Cologne, University of Cologne, Cologne, Germany.

Classifications MeSH