Zebrafish models for ectopic mineralization disorders: Practical issues from morpholino design to post-injection observations

Frontiers in Genetics

Volumn 4, Issue MAY, 2013, Pages

  Hosen, Mohammad Jakir ^a,b   Vanakker, Olivier M ^a   Willaert, Andy ^a   Huysseune, Ann ^c   Coucke, Paul ^a   Paepe, Anne De ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b SHAHJALAL UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Bangladesh)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Embryos; Mineralization; Morpholino; Osteogenic pathways; Zebrafish

Indexed keywords

EID: 84882948485     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00074     Document Type: Review

References (127)

1. Akhtar, T., Li, J., Olden, T., and Wallace, K. N. (2009). Use of phospholipase A2 for antigen retrieval in zebrafish whole-mount immunohistochemistry. Zebrafish 6, 223-227.
2. Antkiewicz, D. S., Burns, C. G., Carney, S. A., Peterson, R. E., and Heideman, W. (2005). Heart malformation is an early response to TCDD in embryonic zebrafish. Toxicol. Sci. 84, 368-377.
3. Baker, K., Warren, K. S., Yellen, G., and Fishman, M. C. (1997). Defective "pacemaker"current in a zebrafish mutant with a slow heart rate. Proc. Natl. Acad. Sci. U.S.A. 94, 4554-4559.
4. Bedell, V. M., Westcot, S. E., and Ekker, S. C. (2011). Lessons from morpholino-based screening in zebrafish. Brief. Funct. Genomics 10, 181-188.
5. Bensimon-Brito, A., Cardeira, J., Cancela, M. L., Huysseune, A., and Witten, P. E. (2012). Distinct patterns of notochord mineralization in zebrafish coincide with the localization of osteocalcin isoform 1 during early vertebral centra formation. BMC Dev. Biol. 12:28. doi:10.1186/1471-213X-12-28
6. Bhartiya, D., Maini, J., Sharma, M., Joshi, P., Laddha, S. V., Jalali, S., et al. (2010). FishMap Zv update-a genomic regulatory map of zebrafish. Zebrafish 7, 179-180.
7. Bill, B. R., Petzold, A. M., Clark, K. J., Schimmenti, L. A., and Ekker, S. C. (2009). A primer for morpholino use in zebrafish. Zebrafish 6, 69-77.
8. Bouzaffour, M., Dufourcq, P., Lecaudey, V., Hass, P., and Vriz, S. (2009). Fgf and Sdf-1 pathways interact during zebrafish fin regeneration. PLoS ONE 4:e5824. doi:10.1371/journal.pone.0005824
9. Bruno, I. G., Jin, W., and Cote, G. J. (2004). Correction of aberrant FGFR1 alternative RNA splicing through targeting of intronic regulatory elements. Hum. Mol. Genet. 13, 2409-2420.
10. Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Kubista, M., Mueller, R., et al. (2009). Clin. Chem. 55, 511-522.
11. Cermak, T., Doyle, E. L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., et al. (2011). Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, 7879.
12. Chazotte, B. (2010). Labeling mitochondria with Mito Tracker dyes. Cold Spring Harb. Protoc. 8, 990-992.
13. Chen, J. N., Haffter, P., Odenthal, J., Vogelsang, E., Brand, M., van Eeden, F. J., et al. (1996). Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development 123, 293-302.
14. Cheng, K. C., Xin, X., Clark, D. P., and Riviere, P. L. (2011). Whole-animal imaging, gene function, and the zebrafish phenome project. Curr. Opin. Gene. Dev. 21, 620-629.
15. Clark, K. J., Voytas, D. F., and Ekker, S. C. (2011). A TALE of two nucleases: gene targeting for the masses? Zebrafish 8, 147-149.
16. Cline, A., Gao, N., Flanagan-Steet, H., Sharma, V., Rosa, S., Sonon, R., et al. (2012). A zebrafish model of PMM2-CDG reveals altered neurogenesis and a substrate-accumulation mechanism for N-linked glycosylation deficiency. Mol. Biol. Cell 23, 4175-4187.
17. Concordet, J. P., Lewis, K. E., Moore, J. W., Goodrich, L. V., Johnson, R. L., Scott, M. P., et al. (1996). Spatial regulation of a zebrafish patched homologue reflects the role of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122, 2835-2846.
18. Cooper, M. K., Porter, J. A., Young, K. E., and Beachy, P. A. (1998). Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 280, 1603-1607.
19. Côté, N., El Husseini, D., Pépin, A., Guauque-Olarte, S., Ducharme, V., Bouchard-Cannon, P., et al. (2012). ATO acts as a survival signal and prevents the mineralization of aortic valve. J. Mol. Cell. Cardiol. 52, 1191-1202.
20. Craven, S. E., French, D., Ye, W., de Sauvage, F., and Rosenthal, A. (2005). Loss of Hspa9b in zebrafish recapitulates the ineffective hematopoiesis of the myelodysplastic syndrome. Blood 105, 3528-3534.
21. De Rienzo, G., Gutzman, J. H., and Sive, H. (2012). Efficient shRNA-mediated inhibition of gene expression in zebrafish. Zebrafish 9, 97-107.
22. Denslow, N. D., Chow, M. C., Kroll, K. J., and Green, L. (1999). Vitellogenin as a biomarker of exposure for estrogen or estrogen mimics. Ecotoxicology 8, 485-488.
23. Deo, R. C., and MacRae, C. A. (2011). The zebrafish: scalable in vivo modeling for systems biology. Willy Interdiscip. Rev. Syst. Biol. Med. 3, 335-346.
24. Doyon, Y., McCammon, J. M., Miller, J. C., Faraji, F., Ngo, C., Katibah, G. E., et al. (2008). Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat. Biotechnol. 26, 702-708.
25. Draper, B. W., Morcos, P. A., and Kimmel, C. B. (2001). Inhibition of zebrafish fgf8 Pre-mRNA splicing with morpholino oligos: a quantifiable method for gene knockdown. Genesis 30, 154-156.
26. Du, S. J., Frenkel, V., Kindschi, G., and Zohar, Y. (2001). Visualizing normal and defective bone development in zebrafish embryos using the fluorescent chromophore calcein. Dev. Biol. 238, 239-246.
27. Ducy, P., Amling, M., Takeda, S., Priemel, M., Schilling, A. F., Beil, F. T., et al. (2000). Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 100, 197-207.
28. Eisen, J. S., and Smith, J. C. (2008). Controlling morpholino experiments: don't stop making antisense. Development 135, 1735-1743.
29. Ekker, S. C., and Larson, J. D. (2001). Morphant technology in model developmental systems. Genesis 30, 89-93.
30. Fadok, V. A., Savill, J. S., Haslett, C., Bratton, D. L., Doherty, D. E., Campbell, P. A., et al. (1992). Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J. Immunol. 149, 29-35.
31. Forouhar, A. S., Hove, J. R., Calvert, C., Flores, J., Jadvar, H., and Gharib, M. (2004). Electrocardiographic characterization of embryonic zebrafish. Conf. Proc. IEEE Eng. Med. Biol. Soc. 5, 3615-3617.
32. Garcia-Fernandez, M. I., Gheduzzi, D., Boraldi, F., Paolinelli, C. D., Sanchez, P., Valdivielso, P., et al. (2008). Parameters of oxidative stress are present in the circulation of PXE patient. Biochem. Biophys. Acta 1782, 474-481.
33. Gavaia, P. J., Simes, D. C., Ortiz-Delgado, J. B., Viegas, C. S., Pinto, J. P., Kelsh, R. N., et al. (2006). Osteocalcin and matrix Gla protein in zebrafish and sengal sole: comparative gene and protein expression during larval development through adulthood. Gene Expr. Patterns 6, 637-652.
34. Gavrieli, Y., Sherman, Y., and Ben-Sasson, S. A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
35. Haffter, P., Granato, M., Brand, M., Mllins, M. C., Maischein, H. M., Brand, M., et al. (1996). The identification of genes with unique and essential functions in the development of the zebrafish. Development 123, 1-36.
36. Hermann, A. C., Millard, P. J., Blake, S. L., and Kim, C. H. (2004). Development of respiratory burst assay using zebrafish kidneys and embryos. J. Immunol. Methods 292, 119-129.
37. Hong, Y. J., Choi, Y. W., Myung, K. B., and Choi, H. Y. (2011). The immunohistochemical patterns of calcicication-related molecules in epidermis and dermis of the zebrafish. Ann. Dermatol. 23, 299-303.
38. Hosen, M. J., Lamoen, A., De Paepe, A., and Vanakker, O. (2012). Histopathology of pseudoxanthoma elasticum and related disorders: histological hallmarks and diagnostic clues. Scientifica 2012, 1-15.
39. Hughes, I., Blasiole, B., Huss, D., Warchol, M. E., Rath, N. P., Hurle, B., et al. (2004). Otopetrin1 is required for otolith formation in the zebrafish Danio rerio. Dev. Biol. 276, 391-402.
40. Huitema, L. F., Renn, J., Logister, I., Gray, J. K., Waltz, S. E., Flik, G., et al. (2012). Macrophage-stimulating protein and calcium homeostasis in zebrafish. FASEB J. 26, 4092-4101.
41. Hutchinson, S. A., and Eisen, J. S. (2006). Islet1 and Islet2 have equivalent abilities to promote motoneuron formation and to specify motoneuron subtype identity. Development 133, 2137-2147.
42. Hyatt, T. M., and Ekker, S. C. (1999). Vectors and techniques for ectopic gene expression in zebrafish. Methods Cell Biol. 59, 117-126.
43. Islam, M. E., Kikuta, H., Inoue, F., Kanai, M., Kawakami, A., Parvin, M. S., et al. (2006). Three enhancer regions regulate gbx2 gene expression in the isthmic region during zebrafish development. Mech. Dev. 123, 907-924.
44. Jao, L. E., Maddison, L., Chen, W., and Burgess, S. M. (2008). Using retroviruses as a mutagenesis tool to explore the zebrafish genome. Brief. Funct. Genomics Proteomics 7, 427-443.
45. Jenny, M. J., Aluru, N., and Hahn, M. E. (2012). Effects of short-term exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin on microRNA expresson in zebrafish. Toxicol. Appl. Pharmacol. 264, 262-273.
46. Jowett, T., and Lettice, L. (1994). Whole-mount in-situ hybridizations on zebrafish embryos using a mixture of digoxigenin-labeled and fluorescein-labeled probes. Trends Genet. 10, 73-74.
47. Kawasaki, K., Buchanan, A. V., and Weiss, K. M. (2009). Biomineralization in humans: making the hard choices in life. Annu. Rev. Genet. 43, 119-142.
48. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
49. Lanham, K. A., Prasch, A. L., Weina, K. M., Peterson, R. E., and Heideman, W. (2011). A dominant negative zebrafish Ahr2 partially protects developing zebrafish from dioxin toxicity. PLoS ONE 6:e28020. doi:10.1371/journal.pone.0028020
50. Lawrence, C., and Mason, T. (2012). Zebrafish housing systems: a review of basic operating principles and considerations for design and functionality. ILAR J. 53, 179-191.
51. Lawson, N. D., and Wolfe, S. A. (2011). Forward and reverse genetic approaches for the analysis of vertebrate development in the zebrafish. Dev. Cell 21, 48-64.
52. Lecoeur, H., de Oliveira-Pinto, L. M., and Gougeon, M. L. (2002). Multiparametric flow cytometric analysis of biochemical and functional events associated with apoptosis and oncosis using the 7-aminoactinomycin D assay. J. Immunol. Methods 265, 81-96.
53. Li, C. F., MacDonald, J. R., Wie, R. Y., Ray, J., Lau, K., Kandel, C., et al. (2007). Human sterile alpha motif domain 9, a novel gene identified as down-regulated in aggressive fibromatosis, is absent in the mouse. BMC Genomics 8:92. doi:10.1186/1471-2164-8-92
54. Li, Q., Frank, M., Thisse, C. L., Thisse, B. V., and Uitto, J. (2011). Zebrafish: a model system to study heritable skin diseases. J. Invest. Dermatol. 131, 565-571.
55. Li, Q., Sadowski, S., Frank, M., Chai, C., Varadi, A., Ho, S. Y., et al. (2010). The abcc6a gene expression is required for normal zebrafish development. J. Invest. Dermatol. 11, 1-8.
56. Liang, D., Chang, J. R., Chin, A. J., Smith, A., Kelly, C., Weinberg, E. S., et al. (2001). The role of vascular endothelial growth factor (VEGF) in vasculogenesis, angiogenesis, and hematopoiesis in zebrafish development. Mech. Dev. 108, 29-43.
57. Lieschke, G., and Currie, P. D. (2007). Animal models of human disease: zebrafish swim into view. Nat. Rev. Genet. 8, 353-367.
58. Link, V., Shevchenko, A., and Heisenberg, C. (2006). Proteomics of early zebrafish embryos. BMC Dev. Biol. 6:1. doi:10.1186/1471-213X-6-1
59. Little, S. C., and Mullins, M. C. (2004). Twisted gastrulation promotes BMP signaling in zebrafish dorsal-ventral axial patterning. Development 13123, 5825-5835.
60. Lievremont, M., Potus, J., and Guillou, B. (1982). Use of alizarin red S for histochemical staining of Ca2+ in the mouse; some parameters of the chemical reaction in vitro. Acta Anat. (Basel) 3, 3268-3280.
61. Lobner, C., Wee, S., Ler, S. G., Li, R. H., Carnery, T., Blackstock, W., et al. (2012). Expanding the zebrafish embryo proteome using multiple fractionation approaches and tandem mass spectrometry. Proteomics 11, 1879-1882.
62. Love, D. R., Pichler, F. B., Dodd, A., Copp, B. R., and Greenwood, D. R. (2004) Technology for high-throughput screens: the present and future Curr. Opin. Biotechnol. 6:564-571.
63. Lu, J. G., Peatman, E., Tang, H. B., Lewis, J., and Liu, Z. J. (2012). Profiling of gene duplication patterns of sequenced teleost genomes: evidence for rapid lineage-specific genome expansion mediated by recent tandem duplications. BMC Genomics 13:246. doi:10.1186/1471-2164-13-246
64. Lucitt, M. B., Price, T. S., Pizarro, A., Wu, W., Yocum, A. K., Seiler, C., et al. (2008). Analysis of the zebrafish proteome during embryonic development. Mol. Cell. Proteomics 7, 981-994.
65. Mathavan, S., Lee, S. G., Mak, A., Miller, L. D., Murthy, K. R., Govindarajan, K. R., et al. (2005). Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genet. 1:e29. doi:10.1371/journal.pgen.0010029
66. McCurley, A. T., and Callard, G. V. (2008). Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol. Biol. 9:102. doi:10.1186/1471-2199-9-102
67. Megason, S. G., and Fraser, S. E. (2007). Imaging in systems biology. Cell 130, 784-795.
68. Meng, X., Noyes, M. B., Zhu, L. J., Lawson, N. D., and Wolfe, S. A. (2008). Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat. Biotechnol. 26, 695-701.
69. Metscher, B. D. (2009). MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions. Dev. Dyn. 38, 632-640.
70. Mitra, K., and Lippincott-Schwartz, J. (2010). Analysis of mitochondrial dynamics and functions using imaging approaches. Curr. Protoc. Cell Biol. 4, 1-21.
71. Morelli, L. G., Uriu, K., Ares, S., and Oates, A. C. (2012). Computational approaches to developmental patterning. Science 336, 187-191.
72. Mungrue, I. N., Zhao, P., Yao, Y., Meng, H., Rau, C., Havel, J. V., et al. (2011). Abcc6 deficiency causes increased infarct size and apoptosis in a mouse cardiac ischemia-reperfusion model. Arterioscler. Throm. Vasc. Biol. 31, 2806-2812.
73. Nasevicius, A., and Ekker, S. C. (2000). Effective targeted gene "knockdown" in zebrafish. Nat. Genet. 26, 216-220.
74. Nejati-Yazdinejad, M. (2006). Spectrophotometric determination of trace amount of copper (ii) iron based on complexation with an anthraquinone derivative. Anal. Sci. 22, 617-619.
75. Nicholls, D. G., and Budd, S. L. (2000). Mitochondria and neuronal survival. Physiol. Rev. 80, 315-360.
76. Nicoli, S., and Presta, M. (2007). The zebrafish/tumor xenograft angiogenesis assay. Nat. Protoc. 2, 2918-2923.
77. Niwa, R., and Slack, F. J. (2007). Ins and outs of RNA interference analysis. Cell 2008, 34-36.
78. Oleykowski, C. A., Bronson Mullins, C. R., Godwin, A. K., and Yeung, A. T. (1998). Mutation detection using a novel plant endonuclease. Nucleic Acids Res. 26, 4597-4602.
79. Pasqualetti, S., Banfi, G., and Mariotti, M. (2012). The zebrafish scale as model to study the bone mineralization process. J. Mol. Hist. 43, 589-595.
80. Pasquali-Ronchetti, I., Garcia-Fernandez, M. I., Boraldi, F., Quaglino, D., Gheduzzi, D., De Vincenzi Paolinelli, C., et al. (2006). Oxidative stress in fibroblasts from patients with pseudoxanthoma elasticum: possible rele in the pathogenesis of clinical manifestations. J. Pathol. 208, 54-61.
81. Peterson, R. T., Link, B. A., Dowling, J. E., and Schreiber, S. L. (2000). Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc. Natl. Acad. Sci. U.S.A. 97, 12965-12969.
82. Petzold, A. M., Balciunas, D., Sivasubbu, S., Clark, K. J., Bedell, V. M., Westcot, S. E., et al. (2009). Nicotine response genetics in the zebrafish. Proc. Natl. Acad. Sci. U.S.A. 106, 18662-18667.
83. Pichler, F. B., Dodd, A., and Love, D. R. (2004). Global gene expression analysis in the zebrafish: the challenge and the promise. Drug Discov. Today Technol. 1, 79-84.
84. Pichler, F. B., Laurenson, S., Williams, L. C., Dodd, A., Copp, B. R., and Love, D. R. (2003). Chemical discovery and global gene expression analysis in zebrafish. Nat. Biotechnol. 21, 879-883.
85. Postlethwait, J., Amores, A., Cresko, W., Singer, A., and Yan, Y. L. (2004). Subfunction partitioning, the telwost radiation and the annotation of the human genome. Trends Genet. 20, 481-490.
86. Renaud, O., Herbomel, P., and Kissa, K. (2011). Studying cell behavior in whole zebrafish embryos by confocal live imaging: application to hematopoietic stem cells. Nat. Protoc. 6, 1897-1904.
87. Rikin, A., Rosenfeld, G. E., McCartin, K., and Evans, T. (2010). A reverser genetic approach to test functional redundancy during embryogenesis. J. Vis. Exp. 11, 2020.
88. Rusanescu, G., Weissleder, R., and Aikawa, E. (2008). Notch signaling in cardiovascular disease and calcification. Curr. Cardiol. Rev. 4, 148-156.
89. Ryu, S., Beutner, G., Kinnally, K. W., Dirksen, R. T., and Sheu, S. (2011). Single channel characterization of the mitochondrial ryanodine receptor in heart mitoplasts. J. Biol. Chem. 24, 21324-21339.
90. Sander, J. D., Dahlborg, E. J., Goodwin, M. J., Cade, L., Zhang, F., Cifuentes, D., et al. (2011). Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nat. Methods 8, 67-69.
91. Sander, J. D., Maeder, M. L., Reyon, D., Voytas, D. F., Joung, J. K., and Dobbs, D. (2010). ZiFiT (Zinc Finger Targeter): an updated zinc finger engineering tool. Nucleic Acids Res. 38, W462-W468.
92. Scheffler, I. E. (2001). Mitochondria make a comeback. Adv. Drug Deliv. Rev. 49, 3-26.
93. Sehnert, A. J., and Stainier, D. Y. (2002). A window to the heart: can zebrafish mutants help us understand heart disease in humans? Trends Genet. 18, 491-494.
94. Shanahan, C. M., Crouthamel, M. H., Kapustin, A., and Giachelli, C. M. (2011). Arterial calcification in chronic kidney disease: kye roles for calcium and phosphate. Circ. Res. 6, 697-711.
95. Shawber, C. J., and Kitajewski, J. (2004). Notch function in the vasculature: insights from zebrafish, mouse and man. Bioessays 26, 225-234.
96. Shoji, W., and Sato-Maeda, M. (2008). Application of heat shock promoter in transgenic zebrafish. Dev. Growth Differ. 50, 401-406.
97. Sire, J. Y., and Akimenko, M. A. (2004). Scale development in fish: a review, with description of sonic hedgehog (shh) expression in the zebrafish. Int. J. Dev. Biol. 48, 233-247.
98. Sire, J. Y., Allizard, F., Babiar, O., Bourguingnon, J., and Quilhac, A. (1997a). Scale development in zebrafish. J. Anat. 190, 545-561.
99. Sire, J. Y., Quilhac, A., Bourguignon, J., and Allizard, F. (1997b). Evidence for participation of the epidermis in the deposition of superficial layer of scales in zebrafish (Danio rerio). J. Morphol. 231, 161-174.
100. Skromne, I., and Prince, V. E. (2008). Current perspectives in zebrafish reverse genetics: moving forward. Dev. Dyn. 137, 861-882.
101. Song, Y. Q., Selak, M. A., Watson, C. T., Coutts, C., Scherer, P. C., Panzer, J. A., et al. (2009). Mechanisms underlying metabolic and neural defects in zebrafish and human multiple Acyl-CoA dehydrogenase deficiency (MADD). PLoS ONE 4:e8329. doi:10.1371/journal.pone.0008329
102. Stainier, D. Y., Fouquet, B., Chen, J. N., Warren, K. S., Weinstein, B. M., and Meiler, S. E. (1996). Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development 123, 285-292.
103. Stephens, J. W., Khanolkar, M. P., and Bain, S. C. (2009). The biological relevance and measurement of plasma markers of oxidative stress in diabetes and cardiovascular disease. Atherosclerosis 202, 321-329.
104. Summerton, J. (1999). Morpholino antisense oligomers: the case for an RNase H-independent structural type. Biochim. Biophys. Acta 1489, 141-158.
105. Summerton, J., and Weller, D. (1997). Morpholino antisense oligomers: design, preparation and properties. Antisense Nucleic Acid Drug Dev. 7, 187-195.
106. Sun, Y., Mauerhan, D. R., Chaturvedi, D., Hanley, E. N. Jr., and Gruber, H. E. (2012). Biological effects of phosphate on fibroblast-like synoviocytes. ISRN Cell Biol. 2012, 1-6.
107. Taylor, K. L., Grant, N. J., Temperley, N. D., and Patton, E. E. (2010). Small molecule screening in zebrafish: an in vivo approach to identifying new chemical tools and drug leads. Cell Commun. Signal. 8, 1-14.
108. Thisse, C., and Thisse, B. (2008). High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 3, 59-69.
109. Tingaud-Sequeira, A., Forgue, J., Andre, M., and Babin, P. J. (2006). Epidermal transient down-regulation of retinol-binding protein 4 and mirror expression of apolipoprotein Eb and estrogen receptor 2a during zebrafish fin and scale development. Dev. Dyn. 235, 3071-3079.
110. Van Genderen, H., Kenis, H., Lux, P., Ungeth, L., Maassen, C., Deckers, N., et al. (2006). In vitro measurement of cell death with the annexin A5 affinity assay. Nat. Protoc. 1, 363-367.
111. Van Ham, T. J., Mapes, J., Kokel, D., and Peterson, R. T. (2010). Live imaging of apoptotic cells in zebrafish. FASEB J. 24, 4336-4342.
112. Varshney, G. K., Huang, H., Zhang, S., Lu, J., Gildea, D. E., Yang, Z., et al. (2013a). The zebrafish insertion collection (ZInC): a web based, searchable collection of zebrafish mutations generated by DNA insertion. Nucleic Acids Res. 41, 861-864.
113. Varshney, G. K., Lu, J., Gildea, D. E., Huang, H., Pei, W., Yang, Z., et al. (2013b). A large-scale zebrafish gene knockout resource for the genome-wide study of gene function. Genome Res. 23, 1-9.
114. Verstraeten, B., Sanders, E., and Huysseune, A. (2012). "Whole mount immunohistochemistry and in situ hybridization of larval and adult zebrafish dental tissues," in Methods in Molecular Biology, Methods in Odontogenesis, Vol. 887, ed. C. Kioussi (Totowa, NJ: Humana Press), 179-191.
115. Viegas, C. S. B., Cavaco, S., Neves, P. L., Ferreira, A., Joao, A., Williamson, M. K., et al. (2009). Gla-rich protein is a novel vitamin K-dependent protein present in serum that accumulates at sites of pathological calcifications. Am. J. Pathol. 175, 2288-2298.
116. Walker, M. B., and Kimmel, C. B. (2007). A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech. Histochem. 82, 23-28.
117. Wang, L., Zhou, J. Y., Yaho, J. H., Lu, D. R., and Qiao, X. J. (2010). U6 promoter-driven siRNA injection has nonspecific effects in zebrafish. Biochem. Biophys. Res. Commun. 39, 1363-1368.
118. Wang, Z., Gerstein, M., and Snyder, M. (2009). RNA-seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57-63.
119. Warren, K. S., and Fishman, M. C. (1998). Physiological genomics: mutant screens in zebrafish. Am. J. Physiol. 275, H1-H7.
120. Wei, L., Hoole, D., and Sun, B. (2012). Identification of apoptosis related genes and transcription variations in response to microcystin-LR in zebrafish liver. Toxicol. Ind. Health doi:10.1177/0748233712462443
121. Wetterbom, A., Ameur, A., Feuk, L., Gyllensten, U., and Cavelier, L. (2010). Identification of novel exons and transcribed regions by chimpanzee transcriptome sequencing. Genome Biol. 11, R78.
122. Wienholds, E., Koudijs, M. J., van Eeden, F. J., Cuppen, E., and Plasterk, R. H. (2003). The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nat. Genet. 35, 217-218.
123. Wienholds, E., Schulte-Merker, S., Walderich, B., and Plasterk, R. H. (2002). Target-selected inactivation of the zebrafish rag1 gene. Science 297, 99-102.
124. Woods, I. G., Kelly, P. D., Chu, F., Ngo-Hazelett, P., Yan, Y., Huang, H., et al. (2000). A comparative map of the zebrafish genome. Genome Res. 10, 1903-1914.
125. Xu, X., Meiler, S. E., Zhong, T. P., Mohideen, M., Crossley, D. A., Burggren, W. W., et al. (2002). Cardiomyopathy in zebrafish due to mutation in an alternatively spliced exon of titin. Nat. Genet. 30, 205-209.
126. Zhang, C., Huang, V. H., Simon, M., Sharma, L. K., Fan, W., Hass, R., et al. (2012). Heteroplasmic mutations of the mitochondrial genome cause paradoxical effects on mitochondrial functions. FASEB J. 26, 4914-4924.
127. Zhao, X. F., Fjose, A., Larsen, N., Helvik, J. V., and Drivenes, O. (2008). Treatment with small interfering RNA affects the microRNA pathway and causes unspecific defects in zebrafish embryos. FEBS J. 275, 2177-2184.