Live imaging early immune cell ontogeny and function in zebrafish Danio rerio

Journal of Fish Biology

Volumn 73, Issue 8, 2008, Pages 1833-1871

  Hall, C J ^a   Flores, M V ^a   Crosier, K E ^a   Crosier, P S ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Immunity; Inflammation; Live cell imaging; Transgenic; Wound healing; Zebrafish

Indexed keywords

ANIMALIA; DANIO RERIO; MUS; VERTEBRATA;

EID: 53549083612     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2008.01980.x     Document Type: Review

References (136)

1. Adams, J. M., Harris, A. W., Strasser, A., Ogilvy, S. Cory, S 1999). Transgenic models of lymphoid neoplasia and development of a pan-hematopoietic vector. Oncogene 18, 5268 5277.
2. Ai, H. W., Henderson, J. N., Remington, S. J. Campbell, R. E 2006). Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging. Biochemical Journal 400, 531 540.
3. Amsterdam, A., Lin, S. Hopkins, N 1995). The Aequorea victoria green fluorescent protein can be used as a reporter in live zebrafish embryos. Developmental Biology 171, 123 129.
4. Ando, R., Hama, H., Yamamoto-Hino, M., Mizuno, H. Miyawaki, A 2002). An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein. Proceedings of the National Academy of Sciences of the United States of America 99, 12651 12656.
5. Baumjohann, D. Lutz, M. B 2006). Non-invasive imaging of dendritic cell migration in vivo. Immunobiology 211, 587 597.
6. Bennett, C. M., Kanki, J. P., Rhodes, J., Liu, T. X., Paw, B. H., Kieran, M. W., Langenau, D. M., Delahaye-Brown, A., Zon, L. I., Fleming, M. D. Look, A. T 2001). Myelopoiesis in the zebrafish, Danio rerio. Blood 98, 643 651.
7. Berghmans, S., Jette, C., Langenau, D., Hsu, K., Stewart, R., Look, T. Kanki, J. P 2005). Making waves in cancer research: new models in the zebrafish. Biotechniques 39, 227 237.
8. Berman, J. N., Kanki, J. P. Look, A. T 2005). Zebrafish as a model for myelopoiesis during embryogenesis. Experimental Hematology 33, 997 1006.
9. Bertrand, J. Y., Giroux, S., Golub, R., Klaine, M., Jalil, A., Boucontet, L., Godin, I. Cumano, A 2005). Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin. Proceedings of the National Academy of Sciences of the United States of America 102, 134 139.
10. Bertrand, J. Y., Kim, A. D., Violette, E. P., Stachura, D. L., Cisson, J. L. Traver, D 2007). Definitive hematopoiesis initiates through a committed erythromyeloid progenitor in the zebrafish embryo. Development 134, 4147 4156.
11. Bertrand, J. Y., Kim, A. D., Teng, S. Traver, D 2008). CD41+ cmyb+ precursors colonize the zebrafish pronephros by a novel migration route to initiate adult hematopoiesis. Development 135, 1853 1862.
12. Brecher, G., Bookstein, N., Redfearn, W., Necas, E., Pallavicini, M. G. Cronkite, E. P 1993). Self-renewal of the long-term repopulating stem cell. Proceedings of the National Academy of Sciences of the United States of America 90, 6028 6031.
13. Cahalan, M. D. Parker, I 2006). Imaging the choreography of lymphocyte trafficking and the immune response. Current Opinion in Immunology 18, 476 482.
14. Carradice, D. Lieschke, G. J 2008). Zebrafish in hematology: sushi or science? Blood 111, 3331 3342.
15. Chen, J., Jette, C., Kanki, J. P., Aster, J. C., Look, A. T. Griffin, J. D 2007). NOTCH1-induced T-cell leukemia in transgenic zebrafish. Leukemia 21, 462 471.
16. Clay, H., Davis, J. M., Beery, D., Huttenlocher, A., Lyons, S. E. Ramakrishnan, L 2007). Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host & Microbe 2, 29 39.
17. Croft, B. Y 2002). Animal models for imaging. Disease Markers 18, 365 374.
18. Croix, C. S., Zipfel, W. R. Watkins, S. C 2007). Potential solutions for confocal imaging of living animals. Biotechniques 43, 14 19.
19. Crowhurst, M. O., Layton, J. E. Lieschke, G. J 2002). Developmental biology of zebrafish myeloid cells. International Journal of Developmental Biology 46, 483 492.
20. Danilov, A. V., Danilova, O. V., Klein, A. K. Huber, B. T 2006). Molecular pathogenesis of chronic lymphocytic leukemia. Current Molecular Medicine 6, 665 675.
21. Dantzig, J. A., Higuchi, H. Goldman, Y. E 1998). Studies of molecular motors using caged compounds. Methods in Enzymology 291, 307 348.
22. Davidson, A. J. Zon, L. I 2004). The 'definitive' (and 'primitive') guide to zebrafish hematopoiesis. Oncogene 23, 7233 7246.
23. Davidson, A. E., Balciunas, D., Mohn, D., Shaffer, J., Hermanson, S., Sivasubbu, S., Cliff, M. P., Hackett, P. B. Ekker, S. C 2003). Efficient gene delivery and gene expression in zebrafish using the Sleeping Beauty transposon. Developmental Biology 263, 191 202.
24. Davis, J. M., Clay, H., Lewis, J. L., Ghori, N., Herbomel, P. Ramakrishnan, L 2002). Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 17, 693 702.
25. Denk, W., Strickler, J. H. Webb, W. W 1990). Two-photon laser scanning fluorescence microscopy. Science 248, 73 76.
26. Feng, H., Langenau, D. M., Madge, J. A., Quinkertz, A., Gutierrez, A., Neuberg, D. S., Kanki, J. P. Look, A. T 2007). Heat-shock induction of T-cell lymphoma/leukaemia in conditional Cre/lox-regulated transgenic zebrafish. British Journal of Haematology 138, 169 175.
27. Ferrando, A. A., Neuberg, D. S., Staunton, J., Loh, M. L., Huard, C., Raimondi, S. C., Behm, F. G., Pui, C. H., Downing, J. R., Gilliland, D. G., Lander, E. S., Golub, T. R. Look, A. T 2002). Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 1, 75 87.
28. Gering, M. Patient, R 2005). Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos. Developmental Cell 8, 389 400.
29. Gerlich, D. Ellenberg, J 2003). 4D imaging to assay complex dynamics in live specimens. Nature Cell Biology Suppl., S14 S19.
30. Germain, R. N., Castellino, F., Chieppa, M., Egen, J. G., Huang, A. Y., Koo, L. Y. Qi, H 2005). An extended vision for dynamic high-resolution intravital immune imaging. Seminars in Immunology 17, 431 441.
31. Germain, R. N., Miller, M. J., Dustin, M. L. Nussenzweig, M. C 2006). Dynamic imaging of the immune system: progress, pitfalls and promise. Nature Reviews Immunology 6, 497 507.
32. Goessling, W., North, T. E. Zon, L. I 2007). New waves of discovery: modeling cancer in zebrafish. Journal of Clinical Oncology 25, 2473 2479.
33. Goetz, M., Fottner, C., Schirrmacher, E., Delaney, P., Gregor, S., Schneider, C., Strand, D., Kanzler, S., Memadathil, B., Weyand, E., Holtmann, M., Schirrmacher, R., Weber, M. M., Anlauf, M., Kloppel, G., Vieth, M., Galle, P. R., Bartenstein, P., Neurath, M. F. Kiesslich, R 2007). In-vivo confocal real-time mini-microscopy in animal models of human inflammatory and neoplastic diseases. Endoscopy 39, 350 356.
34. Grabher, C. Wittbrodt, J 2007). Meganuclease and transposon mediated transgenesis in medaka. Genome Biology 8 (Suppl. 1 S10.
35. Grabher, C., Joly, J. S. Wittbrodt, J 2004). Highly efficient zebrafish transgenesis mediated by the meganuclease I-SceI. Methods in Cell Biology 77, 381 401.
36. Grabher, C., von Boehmer, H. Look, A. T 2006). Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nature Reviews Cancer 6, 347 359.
37. Graf, R., Rietdorf, J. Zimmermann, T 2005). Live cell spinning disk microscopy. Advances in Biochemical Engineering/Biotechnology 95, 57 75.
38. Hall, C., Flores, M. V., Storm, T., Crosier, K. Crosier, P 2007). The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish. BMC Developmental Biology 7, 42.
39. Hanahan, D. Weinberg, R. A 2000). The hallmarks of cancer. Cell 100, 57 70.
40. Hatta, K., Tsujii, H. Omura, T 2006). Cell tracking using a photoconvertible fluorescent protein. Nature Protocols 1, 960 967.
41. Henrickson, S. E. von Andrian, U. H 2007). Single-cell dynamics of T-cell priming. Current Opinion in Immunology 19, 249 258.
42. Herbomel, P., Thisse, B. Thisse, C 1999). Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126, 3735 3745.
43. Herbomel, P., Thisse, B. Thisse, C 2001). Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Developmental Biology 238, 274 288.
44. Hermanson, S., Davidson, A. E., Sivasubbu, S., Balciunas, D. Ekker, S. C 2004). Sleeping Beauty transposon for efficient gene delivery. Methods in Cell Biology 77, 349 362.
45. Hess, G. P. Grewer, C 1998). Development and application of caged ligands for neurotransmitter receptors in transient kinetic and neuronal circuit mapping studies. Methods in Enzymology 291, 443 473.
46. Higashijima, S., Okamoto, H., Ueno, N., Hotta, Y. Eguchi, G 1997). High-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Developmental Biology 192, 289 299.
47. Hsu, K., Kanki, J. P. Look, A. T 2001). Zebrafish myelopoiesis and blood cell development. Current Opinion in Hematology 8, 245 251.
48. Hsu, K., Traver, D., Kutok, J. L., Hagen, A., Liu, T. X., Paw, B. H., Rhodes, J., Berman, J. N., Zon, L. I., Kanki, J. P. Look, A. T 2004). The pu.1 promoter drives myeloid gene expression in zebrafish. Blood 104, 1291 1297.
49. Huisken, J. Stainier, D. Y 2007). Even fluorescence excitation by multidirectional selective plane illumination microscopy (mSPIM). Optics Letters 32, 2608 2610.
50. Huisken, J., Swoger, J., Del Bene, F., Wittbrodt, J. Stelzer, E. H 2004). Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305, 1007 1009.
51. Jaffredo, T., Nottingham, W., Liddiard, K., Bollerot, K., Pouget, C. de Bruijn, M 2005). From hemangioblast to hematopoietic stem cell: an endothelial connection? Experimental Hematology 33, 1029 1040.
52. Jessen, J. R., Meng, A., McFarlane, R. J., Paw, B. H., Zon, L. I., Smith, G. R. Lin, S 1998). Modification of bacterial artificial chromosomes through chi-stimulated homologous recombination and its application in zebrafish transgenesis. Proceedings of the National Academy of Sciences of the United States of America 95, 5121 5126.
53. Jessen, J. R., Willett, C. E. Lin, S 1999). Artificial chromosome transgenesis reveals long-distance negative regulation of rag1 in zebrafish. Nature Genetics 23, 15 16.
54. Jessen, J. R., Jessen, T. N., Vogel, S. S. Lin, S 2001). Concurrent expression of recombination activating genes 1 and 2 in zebrafish olfactory sensory neurons. Genesis 29, 156 162.
55. Jin, H., Xu, J. Wen, Z 2007). Migratory path of definitive hematopoietic stem/progenitor cells during zebrafish development. Blood 109, 5208 5214.
56. Kalev-Zylinska, M. L., Horsfield, J. A., Flores, M. V., Postlethwait, J. H., Vitas, M. R., Baas, A. M., Crosier, P. S. Crosier, K. E 2002). Runx1 is required for zebrafish blood and vessel development and expression of a human RUNX1-CBF2T1 transgene advances a model for studies of leukemogenesis. Development 129, 2015 2030.
57. Kamei, M. Weinstein, B. M 2005). Long-term time-lapse fluorescence imaging of developing zebrafish. Zebrafish 2, 113 123.
58. Kamei, M., Isogai, S. Weinstein, B. M 2004). Imaging blood vessels in the zebrafish. Methods in Cell Biology 76, 51 74.
59. Kawakami, K. Shima, A 1999). Identification of the Tol2 transposase of the medaka fish Oryzias latipes that catalyzes excision of a nonautonomous Tol2 element in zebrafish Danio rerio. Gene 240, 239 244.
60. Kawakami, K., Koga, A., Hori, H. Shima, A 1998). Excision of the tol2 transposable element of the medaka fish, Oryzias latipes, in zebrafish, Danio rerio. Gene 225, 17 22.
61. Kawakami, K., Shima, A. Kawakami, N 2000). Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. Proceedings of the National Academy of Sciences of the United States of America 97, 11403 11408.
62. Kissa, K., Murayama, E., Zapata, A., Cortes, A., Perret, E., Machu, C. Herbomel, P 2008). Live imaging of emerging hematopoietic stem cells and early thymus colonization. Blood 111, 1147 1156.
63. Koo, V., Hamilton, P. W. Williamson, K 2006). Non-invasive in vivo imaging in small animal research. Cellular Oncology 28, 127 139.
64. Lam, S. H., Chua, H. L., Gong, Z., Lam, T. J. Sin, Y. M 2004). Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Developmental and Comparative Immunology 28, 9 28.
65. Langenau, D. M., Traver, D., Ferrando, A. A., Kutok, J. L., Aster, J. C., Kanki, J. P., Lin, S., Prochownik, E., Trede, N. S., Zon, L. I. Look, A. T 2003). Myc-induced T cell leukemia in transgenic zebrafish. Science 299, 887 890.
66. Langenau, D. M., Ferrando, A. A., Traver, D., Kutok, J. L., Hezel, J. P., Kanki, J. P., Zon, L. I., Look, A. T. Trede, N. S 2004). In vivo tracking of T cell development, ablation, and engraftment in transgenic zebrafish. Proceedings of the National Academy of Sciences of the United States of America 101, 7369 7374.
67. Langenau, D. M., Feng, H., Berghmans, S., Kanki, J. P., Kutok, J. L. Look, A. T 2005a). Cre/lox-regulated transgenic zebrafish model with conditional myc-induced T cell acute lymphoblastic leukemia. Proceedings of the National Academy of Sciences of the United States of America 102, 6068 6073.
68. Langenau, D. M., Jette, C., Berghmans, S., Palomero, T., Kanki, J. P., Kutok, J. L. Look, A. T 2005b). Suppression of apoptosis by bcl-2 overexpression in lymphoid cells of transgenic zebrafish. Blood 105, 3278 3285.
69. Lawson, N. D. Weinstein, B. M 2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Developmental Biology 248, 307 318.
70. Le Guyader, D., Redd, M. J., Colucci-Guyon, E., Murayama, E., Kissa, K., Briolat, V., Mordelet, E., Zapata, A., Shinomiya, H. Herbomel, P 2008). Origins and unconventional behavior of neutrophils in developing zebrafish. Blood 111, 132 141.
71. Lichanska, A. M. Hume, D. A 2000). Origins and functions of phagocytes in the embryo. Experimental Hematology 28, 601 611.
72. Lieschke, G. J. Currie, P. D 2007). Animal models of human disease: zebrafish swim into view. Nature Reviews. Genetics 8, 353 367.
73. Lieschke, G. J., Oates, A. C., Crowhurst, M. O., Ward, A. C. Layton, J. E 2001). Morphologic and functional characterization of granulocytes and macrophages in embryonic and adult zebrafish. Blood 98, 3087 3096.
74. Lin, H. F., Traver, D., Zhu, H., Dooley, K., Paw, B. H., Zon, L. I. Handin, R. I 2005). Analysis of thrombocyte development in CD41-GFP transgenic zebrafish. Blood 106, 3803 3810.
75. Lippincott-Schwartz, J., Altan-Bonnet, N. Patterson, G. H 2003). Photobleaching and photoactivation: following protein dynamics in living cells. Nature Cell Biology Suppl., S7 S14.
76. List, K., Szabo, R., Molinolo, A., Sriuranpong, V., Redeye, V., Murdock, T., Burke, B., Nielsen, B. S., Gutkind, J. S. Bugge, T. H 2005). Deregulated matriptase causes ras-independent multistage carcinogenesis and promotes ras-mediated malignant transformation. Genes & Development 19, 1934 1950.
77. Lokey, R. S 2003). Forward chemical genetics: progress and obstacles on the path to a new pharmacopoeia. Current Opinion in Chemical Biology 7, 91 96.
78. Martinez-Agosto, J. A., Mikkola, H. K., Hartenstein, V. Banerjee, U 2007). The hematopoietic stem cell and its niche: a comparative view. Genes & Development 21, 3044 3060.
79. Masters, B. R. Bohnke, M 2001). Confocal microscopy of the human cornea in vivo. International Ophthalmology 23, 199 206.
80. Mathias, J. R., Perrin, B. J., Liu, T. X., Kanki, J., Look, A. T. Huttenlocher, A 2006). Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. Journal of Leukocyte Biology 80, 1281 1288.
81. Mathias, J. R., Dodd, M. E., Walters, K. B., Rhodes, J., Kanki, J. P., Look, A. T. Huttenlocher, A 2007). Live imaging of chronic inflammation caused by mutation of zebrafish Hai1. Journal of Cell Science 120, 3372 3383.
82. Meeker, N. D. Trede, N. S 2008). Immunology and zebrafish: spawning new models of human disease. Developmental and Comparative Immunology 32, 745 757.
83. Meijer, A. H., van der Sar, A. M., Cunha, C., Lamers, G. E., Laplante, M. A., Kikuta, H., Bitter, W., Becker, T. S. Spaink, H. P 2008). Identification and real-time imaging of a myc-expressing neutrophil population involved in inflammation and mycobacterial granuloma formation in zebrafish. Developmental and Comparative Immunology 32, 36 49.
84. Mikkola, H. K. Orkin, S. H 2006). The journey of developing hematopoietic stem cells. Development 133, 3733 3744.
85. Miyamoto, T., Iwasaki, H., Reizis, B., Ye, M., Graf, T., Weissman, I. L. Akashi, K 2002). Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Developmental Cell 3, 137 147.
86. Murayama, E., Kissa, K., Zapata, A., Mordelet, E., Briolat, V., Lin, H. F., Handin, R. I. Herbomel, P 2006). Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 25, 963 975.
87. Murphey, R. D. Zon, L. I 2006). Small molecule screening in the zebrafish. Methods 39, 255 261.
88. Neely, M. N., Pfeifer, J. D. Caparon, M 2002). Streptococcus-zebrafish model of bacterial pathogenesis. Infection and Immunity 70, 3904 3914.
89. Neutra, M. R 1999). M cells in antigen sampling in mucosal tissues. Current Topics in Microbiology and Immunology 236, 17 32.
90. North, T. E., Goessling, W., Walkley, C. R., Lengerke, C., Kopani, K. R., Lord, A. M., Weber, G. J., Bowman, T. V., Jang, I. H., Grosser, T., Fitzgerald, G. A., Daley, G. Q., Orkin, S. H. Zon, L. I 2007). Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447, 1007 1011.
91. Okuda, T., van Deursen, J., Hiebert, S. W., Grosveld, G. Downing, J. R 1996). AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84, 321 330.
92. Packham, G. Stevenson, F. K 2005). Bodyguards and assassins: Bcl-2 family proteins and apoptosis control in chronic lymphocytic leukaemia. Immunology 114, 441 449.
93. Patterson, L. J., Gering, M. Patient, R 2005). Scl is required for dorsal aorta as well as blood formation in zebrafish embryos. Blood 105, 3502 3511.
94. Pawley, J. B 2002). Limitations on optical sectioning in live-cell confocal microscopy. Scanning 24, 241 246.
95. Perry, S. S., Pierce, L. J., Slayton, W. B. Spangrude, G. J 2003). Characterization of thymic progenitors in adult mouse bone marrow. Journal of Immunology 170, 1877 1886.
96. Pina, C. Enver, T 2007). Differential contributions of haematopoietic stem cells to foetal and adult haematopoiesis: insights from functional analysis of transcriptional regulators. Oncogene 26, 6750 6765.
97. Politz, J. C 1999). Use of caged fluorochromes to track macromolecular movement in living cells. Trends in Cell Biology 9, 284 287.
98. Pressley, M. E., Phelan, P. E., III., Witten, P. E., Mellon, M. T. Kim, C. H 2005). Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Developmental and Comparative Immunology 29, 501 513.
99. Rawls, J. F., Mahowald, M. A., Goodman, A. L., Trent, C. M. Gordon, J. I 2007). In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proceedings of the National Academy of Sciences of the United States of America 104, 7622 7627.
100. Redd, M. J., Kelly, G., Dunn, G., Way, M. Martin, P 2006). Imaging macrophage chemotaxis in vivo: studies of microtubule function in zebrafish wound inflammation. Cell Motility and the Cytoskeleton 63, 415 422.
101. Renshaw, S. A., Loynes, C. A., Trushell, D. M., Elworthy, S., Ingham, P. W. Whyte, M. K 2006). A transgenic zebrafish model of neutrophilic inflammation. Blood 108, 3976 3978.
102. Renshaw, S. A., Loynes, C. A., Elworthy, S., Ingham, P. W. Whyte, M. K 2007). Modeling inflammation in the zebrafish: how a fish can help us understand lung disease. Experimental Lung Research 33, 549 554.
103. Romana, S. P., Poirel, H., Leconiat, M., Flexor, M. A., Mauchauffe, M., Jonveaux, P., Macintyre, E. A., Berger, R. Bernard, O. A 1995). High frequency of t(12;21) in childhood B-lineage acute lymphoblastic leukemia. Blood 86, 4263 4269.
104. Sabaawy, H. E., Azuma, M., Embree, L. J., Tsai, H. J., Starost, M. F. Hickstein, D. D 2006). TEL-AML1 transgenic zebrafish model of precursor B cell acute lymphoblastic leukemia. Proceedings of the National Academy of Sciences of the United States of America 103, 15166 15171.
105. van der Sar, A. M., Musters, R. J., van Eeden, F. J., Appelmelk, B. J., Vandenbroucke-Grauls, C. M. Bitter, W 2003). Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell Microbiology 5, 601 611.
106. van der Sar, A. M., Stockhammer, O. W., van der Laan, C., Spaink, H. P., Bitter, W. Meijer, A. H 2006). MyD88 innate immune function in a zebrafish embryo infection model. Infection and Immunity 74, 2436 2441.
107. Sato, T., Takahoko, M. Okamoto, H 2006). HuC:Kaede, a useful tool to label neural morphologies in networks in vivo. Genesis 44, 136 142.
108. Scheinecker, C 2005). Application of in vivo microscopy: evaluating the immune response in living animals. Arthritis Research & Therapy 7, 246 252.
109. Sepich, D. S., Wegner, J., O'Shea, S. Westerfield, M 1998). An altered intron inhibits synthesis of the acetylcholine receptor alpha-subunit in the paralyzed zebrafish mutant nic1. Genetics 148, 361 372.
110. Shu, X., Shaner, N. C., Yarbrough, C. A., Tsien, R. Y. Remington, S. J 2006). Novel chromophores and buried charges control color in mFruits. Biochemistry 45, 9639 9647.
111. Smith, D. P., Bath, M. L., Metcalf, D., Harris, A. W. Cory, S 2006). MYC levels govern hematopoietic tumor type and latency in transgenic mice. Blood 108, 653 661.
112. Stoletov, K., Montel, V., Lester, R. D., Gonias, S. L. Klemke, R 2007). High-resolution imaging of the dynamic tumor cell vascular interface in transparent zebrafish. Proceedings of the National Academy of Sciences of the United States of America 104, 17406 17411.
113. Stuart, G. W., McMurray, J. V. Westerfield, M 1988). Replication, integration and stable germ-line transmission of foreign sequences injected into early zebrafish embryos. Development 103, 403 412.
114. Stuart, G. W., Vielkind, J. R., McMurray, J. V. Westerfield, M 1990). Stable lines of transgenic zebrafish exhibit reproducible patterns of transgene expression. Development 109, 577 584.
115. Swaim, L. E., Connolly, L. E., Volkman, H. E., Humbert, O., Born, D. E. Ramakrishnan, L 2006). Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infection and Immunity 74, 6108 6117.
116. Thermes, V., Grabher, C., Ristoratore, F., Bourrat, F., Choulika, A., Wittbrodt, J. Joly, J. S 2002). I-SceI meganuclease mediates highly efficient transgenesis in fish. Mechanisms of Development 118, 91 98.
117. Thompson, M. A., Ransom, D. G., Pratt, S. J., MacLennan, H., Kieran, M. W., Detrich, H. W., III., Vail, B., Huber, T. L., Paw, B., Brownlie, A. J., Oates, A. C., Fritz, A., Gates, M. A., Amores, A., Bahary, N., Talbot, W. S., Her, H., Beier, D. R., Postlethwait, J. H. Zon, L. I 1998). The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis. Developmental Biology 197, 248 269.
118. Tran, T. C., Sneed, B., Haider, J., Blavo, D., White, A., Aiyejorun, T., Baranowski, T. C., Rubinstein, A. L., Doan, T. N., Dingledine, R. Sandberg, E. M 2007). Automated, quantitative screening assay for antiangiogenic compounds using transgenic zebrafish. Cancer Research 67, 11386 11392.
119. Traver, D., Paw, B. H., Poss, K. D., Penberthy, W. T., Lin, S. Zon, L. I 2003). Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nature Immunology 4, 1238 1246.
120. Traver, D., Winzeler, A., Stern, H. M., Mayhall, E. A., Langenau, D. M., Kutok, J. L., Look, A. T. Zon, L. I 2004). Effects of lethal irradiation in zebrafish and rescue by hematopoietic cell transplantation. Blood 104, 1298 1305.
121. Trede, N. S., Langenau, D. M., Traver, D., Look, A. T. Zon, L. I 2004). The use of zebrafish to understand immunity. Immunity 20, 367 379.
122. Urasaki, A., Morvan, G. Kawakami, K 2006). Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics 174, 639 649.
123. Vogel, W. O 1985). The caudal heart of fish: not a lymph heart. Acta Anatomica (Basel) 121, 41 45.
124. Wang, Q., Stacy, T., Binder, M., Marin-Padilla, M., Sharpe, A. H. Speck, N. A 1996). Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proceedings of the National Academy of Sciences of the United States of America 93, 3444 3449.
125. Ward, A. C., McPhee, D. O., Condron, M. M., Varma, S., Cody, S. H., Onnebo, S. M., Paw, B. H., Zon, L. I. Lieschke, G. J 2003). The zebrafish spi1 promoter drives myeloid-specific expression in stable transgenic fish. Blood 102, 3238 3240.
126. Wienholds, E., Schulte-Merker, S., Walderich, B. Plasterk, R. H 2002). Target-selected inactivation of the zebrafish rag1 gene. Science 297, 99 102.
127. Willett, C. E., Cherry, J. J. Steiner, L. A 1997a). Characterization and expression of the recombination activating genes (rag1 and rag2) of zebrafish. Immunogenetics 45, 394 404.
128. Willett, C. E., Zapata, A. G., Hopkins, N. Steiner, L. A 1997b). Expression of zebrafish rag genes during early development identifies the thymus. Developmental Biology 182, 331 341.
129. Willett, C. E., Cortes, A., Zuasti, A. Zapata, A. G 1999). Early hematopoiesis and developing lymphoid organs in the zebrafish. Developmental Dynamics 214, 323 336.
130. Willett, C. E., Kawasaki, H., Amemiya, C. T., Lin, S. Steiner, L. A 2001). Ikaros expression as a marker for lymphoid progenitors during zebrafish development. Developmental Dynamics 222, 694 698.
131. Yang, Z., Jiang, H., Chachainasakul, T., Gong, S., Yang, X. W., Heintz, N. Lin, S 2006). Modified bacterial artificial chromosomes for zebrafish transgenesis. Methods 39, 183 188.
132. Yaniv, K., Isogai, S., Castranova, D., Dye, L., Hitomi, J. Weinstein, B. M 2006). Live imaging of lymphatic development in the zebrafish. Natural Medicines 12, 711 716.
133. Zapata, A., Diez, B., Cejalvo, T., Gutierrez-de Frias, C. Cortes, A 2006). Ontogeny of the immune system of fish. Fish & Shellfish Immunology 20, 126 136.
134. Zhang, X. Y. Rodaway, A. R 2007). SCL-GFP transgenic zebrafish: in vivo imaging of blood and endothelial development and identification of the initial site of definitive hematopoiesis. Developmental Biology 307, 179 194.
135. Zhu, H., Traver, D., Davidson, A. J., Dibiase, A., Thisse, C., Thisse, B., Nimer, S. Zon, L. I 2005). Regulation of the lmo2 promoter during hematopoietic and vascular development in zebrafish. Developmental Biology 281, 256 269.
136. Zipfel, W. R., Williams, R. M. Webb, W. W 2003). Nonlinear magic: multiphoton microscopy in the biosciences. Nature Biotechnology 21, 1369 1377.