Somatic gene transfer in European sea bass (Dicentrarchus labrax): Optimal fish conditions and exogenous control of foreign genes

Aquaculture

Volumn 388-391, Issue 1, 2013, Pages 60-69

  Muñoz, Iciar ^a   Zanuy, Silvia ^a   Mazón, María José ^a   Carrillo, Manuel ^a   Gómez, Ana ^a  

^a CSIC Instituto de Acuicultura de Torre de la Sal IATS   (Spain)

Author keywords

Fish; Muscle; Plasmid injection; Tetracycline regulated system

Indexed keywords

ADULT; ANTIBIOTICS; DNA; FISH CULTURE; GENE EXPRESSION; GENE TRANSFER; LOW TEMPERATURE; MARICULTURE; MUSCLE; PLASMID; REARING; VACCINATION;

DICENTRARCHUS LABRAX;

EID: 84873724513     PISSN: 00448486     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquaculture.2013.01.001     Document Type: Article

References (107)

1. Adam, A., Bartfai, R., Lele, Z., Krone, P.H., Orban, L., 2000. Heat-inducible expression of a reporter gene detected by transient assay in zebrafish. Experimental Cell Research 256, 282-290..
2. Ajiki, T., Murakami, T., Kobayashi, Y., Hakamata, Y., Wang, J., Inoue, S., et al., 2003. Longlasting gene expression by particle-mediated intramuscular transfection modified with bupivacaine: combinatorial gene therapy with IL-12 and IL-18 cDNA against rat sarcoma at a distant site. Cancer Gene Therapy 10, 318-329..
3. Alam, M.S., Lavender, F.L., Iyengar, A., Rahman, M.A., Ayad, H.H., Lathe, R., et al., 1996. Comparison of the activity of carp and rat beta-actin gene regulatory sequences in tilapia and rainbow trout embryos. Molecular Reproduction and Development 45, 117-122..
4. Alonso, M., Chiou, P.P., Leong, J.A., 2011. Development of a suicidal DNA vaccine for infectious hematopoietic necrosis virus (IHNV). Fish & Shellfish Immunology 30, 815-823..
5. Altschmied, J., Duschl, J., 1997. Set of optimized luciferase reporter gene plasmids compatible with widely used CAT vectors. Biotechniques 23, 436-438..
6. Anderson, E.D., Mourich, D.V., Fahrenkrug, S.C., LaPatra, S., Shepherd, J., Leong, J.A., 1996. Gene expression in rainbow trout (Oncorhynchus mykiss) following intramuscular injection of DNA. Molecular Marine Biology and Biotechnology 5, 105-113..
7. Andre, F.M., Cournil-Henrionnet, C., Vernerey, D., Opolon, P., Mir, L.M., 2006. Variability of naked DNA expression after direct local injection: the influence of the injection speed. Gene Therapy 13, 1619-1627..
8. Argenton, F., Arava, Y., Aronheim, A., Walker, M.D., 1996. An activation domain of the helix-loop-helix transcription factor E2A shows cell type preference in vivo in microinjected zebra fish embryos. Molecular and Cellular Biology 16, 1714-1721..
9. Ayala, M.D., Lopez-Albors, O., Gil, F., Latorre, R., Vazquez, J.M., Garcia-Alcazar, A., et al., 2000. Temperature effect on muscle growth of the axial musculature of the sea bass (Dicentrarchus labrax L.). Anatomia, Histologia, Embryologia 29, 235-241..
10. Ayala, M.D., Lopez-Albors, O., Gil, F., Garcia-Alcazar, A., Abellan, E., Alarcon, J.A., et al., 2001. Temperature effects on muscle growth in two populations (Atlantic and Mediterranean) of sea bass, Dicentrarchus labrax L. Aquaculture 202, 359-370..
11. Ayala, M., Lopez-Albors, O., Garcia-Alcazar, A., Abellan, E., Latorre, R., Vazquez, J.M., et al., 2003. Effect of two thermal regimes on the muscle growth dynamics of sea bass larvae, Dicentrarchus labrax L. Anatomia, Histologia, Embryologia 32, 271-275..
12. Baron, U., Gossen, M., Bujard, H., 1997. Tetracycline-controlled transcription in eukaryotes: novel transactivators with graded transactivation potential. Nucleic Acids Research 25, 2723-2729..
13. Boudinot, P., Blanco, M., De Kinkelin, P., Benmansour, A. 1998. Combined DNA immunization with the glycoprotein gene of viral hemorrhagic septicemia virus and infectious hematopoietic necrosis virus induces double-specific protective immunity and nonspecific response in rainbow trout. Virology 249, 297-306..
14. Braun, S., 2008. Muscular gene transfer using nonviral vectors. Current Gene Therapy 8, 391-405..
15. Byon, J.Y., Ohira, T., Hirono, I., Aoki, T., 2006. Comparative immune responses in Japanese flounder, Paralichthys olivaceus, after vaccination with viral hemorrhagic septicemia virus (VHSV) recombinant glycoprotein and DNA vaccine using a microarray analysis. Vaccine 24, 921-930..
16. Carrillo, M., Begtashi, I., Rodriguez, L., Marin, M.C., Zanuy, S., 2010. Long photoperiod on sea cages delays timing of first spermiation and enhances growth in male European sea bass (Dicentrarchus labrax). Aquaculture 299, 157-164..
17. Chan, W.K., Devlin, R.H., 1993. Polymerase chain reaction amplification and functional characterization of sockeye salmon histone H3, metallothionein-B, and protamine promoters. Molecular Marine Biology and Biotechnology 2, 308-318..
18. Chico, V., Ortega-Villaizan, M., Falco, A., Tafalla, C., Perez, L., Coll, J.M., et al., 2009. The immunogenicity of viral haemorragic septicaemia rhabdovirus (VHSV) DNA vaccines can depend on plasmid regulatory sequences. Vaccine 27, 1938-1948..
19. Corbeil, S., Kurath,G., LaPatra, S.E., 2000a. FishDNAvaccine against infectious hematopoietic necrosis virus: efficacy of various routes of immunisation. Fish & Shellfish Immunology 10, 711-723..
20. Corbeil, S., LaPatra, S.E., Anderson, E.D., Kurath, G., 2000b. Nanogram quantities of a DNA vaccine protect rainbow trout fry against heterologous strains of infectious hematopoietic necrosis virus. Vaccine 18, 2817-2824..
21. Dale, E.C., Ow, D.W., 1990. Intra- and intermolecular site-specific recombination in plant cells mediated by bacteriophage P1 recombinase. Gene 91, 79-85..
22. Dale, E.C., Ow, D.W., 1991. Gene transfer with subsequent removal of the selection gene from the host genome. Proceedings of the National Academy of Sciences of the United States of America 88, 10558-10562..
23. Danko, I., Fritz, J.D., Jiao, S.S., Hogan, K., Latendresse, J.S., Wolff, J.A., 1994. Pharmacological enhancement of in-vivo foreign gene-expression in muscle. Gene Therapy 1, 114-121..
24. Davis, H.L., Whalen, R.G., Demeneix, B.A., 1993. Direct gene transfer into skeletal muscle in vivo: factors affecting efficiency of transfer and stability of expression. Human Gene Therapy 4, 151-159..
25. Davis, H.L., Michel, M.L., Whalen, R.G., 1995. Use of plasmid DNA for direct gene transfer and immunization. Annals of the New York Academy of Sciences 772, 21-29..
26. Dhawan, J., Rando, T.A., Elson, S.L., Bujard, H., Blau, H.M., 1995. Tetracycline-regulated gene expression following direct gene transfer into mouse skeletal muscle. Somatic Cell and Molecular Genetics 21, 233-240..
27. Distel, B., Gould, S.J., Voorn-Brouwer, T., Van der, B.M., Tabak, H.F., Subramani, S. 1992. The carboxyl-terminal tripeptide serine-lysine-leucine of firefly luciferase is necessary but not sufficient for peroxisomal import in yeast. The New Biologist 4, 157-165..
28. Faurez, F., Dory, D., Le Moigne, V., Gravier, R., Jestin, A., 2010. Biosafety of DNA vaccines: new generation of DNA vectors and current knowledge on the fate of plasmid after injection. Vaccine 28, 3888-3895..
29. Fletcher, G.L., Shears, M.A., King, M.J., Davies, P.L., Hew, C.L., 1988. Evidence for antifreeze protein gene transfer in Atlantic salmon. Canadian Journal of Fisheries and Aquatic Sciences 45, 352-357..
30. Friedenreich, H., Schartl, M., 1990. Transient expression directed by homologous and heterologous promoter and enhancer sequences in fish cells. Nucleic Acids Research 18, 3299-3305..
31. Furth, P.A., St Onge, L., Boger, H., Gruss, P., Gossen, M., Kistner, A., et al., 1994. Temporal control of gene expression in transgenic mice by a tetracycline-responsive promoter. Proceedings of the National Academy of Sciences of the United States of America 91, 9302-9306..
32. Garver, K.A., Conway, C.M., Elliott, D.G., Kurath, G., 2005. Analysis of DNA-vaccinated fish reveals viral antigen in muscle, kidney and thymus, and transient histopathologic changes. Marine Biotechnology 7, 540-553..
33. Gomez-Chiarri, M., Chiaverini, L.A., 1999. Evaluation of eukaryotic promoters for the construction of DNA vaccines for aquaculture. Genetic Analysis: Biomolecular Engineering 15, 121-124..
34. Gomez-Chiarri, M., Livingston, S.K., Muro-Cacho, C., Sanders, S., Levine, R.P., 1996. Introduction of foreign genes into the tissue of live fish by direct injection and particle bombardment. Diseases of Aquatic Organisms 27, 5-12..
35. Gopalkrishnan, R.V., Christiansen, K.A., Goldstein, N.I., DePinho, R.A., Fisher, P.B., 1999. Use of the human EF-1alpha promoter for expression can significantly increase success in establishing stable cell lines with consistent expression: a study using the tetracycline-inducible system in human cancer cells. Nucleic Acids Research 27, 4775-4782..
36. Gossen, M., Bujard, H., 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proceedings of the National Academy of Sciences of the United States of America 89, 5547-5551..
37. Gossen, M., Freundlieb, S., Bender, G., Muller, G., Hillen, W., Bujard, H., 1995. Transcriptional activation by tetracyclines in mammalian cells. Science 268, 1766-1769..
38. Hans, S., Scheer, N., Riedl, I., Weizsacker, E., Blader, P., Campos-Ortega, J.A., 2004. her3, a zebrafish member of the hairy-E(spl) family, is repressed by Notch signalling. Development 131, 2957-2969..
39. Hansen, E., Fernandes, K., Goldspink, G., Butterworth, P., Umeda, P.K., Chang, K.C., 1991. Strong expression of foreign genes following direct injection into fish muscle. FEBS Letters 290, 73-76..
40. Ho, Y.L., Lin, Y.H., Tsai, W.Y., Hsieh, F.J., Tsai, H.J., 2009. Conditional antisenseknockdown of zebrafish cardiac troponin C as a new animal model for dilated cardiomyopathy. Circulation Journal 73, 1691-1697..
41. Hojman, P., 2010. Basic principles and clinical advancements of muscle electrotransfer. Current Gene Therapy 10, 128-138..
42. Howe, J.R., Skryabin, B.V., Belcher, S.M., Zerillo, C.A., Schmauss, C., 1995. The responsiveness of a tetracycline-sensitive expression system differs in different cell lines. Journal of Biological Chemistry 270, 14168-14174..
43. Huang, C.J., Jou, T.S., Ho, Y.L., Lee, W.H., Jeng, Y.T., Hsieh, F.J., et al., 2005. Conditional expression of a myocardium-specific transgene in zebrafish transgenic lines. Developmental Dynamics 233, 1294-1303..
44. Izumi, M., Gilbert, D.M., 1999. Homogeneous tetracycline-regulatable gene expression in mammalian fibroblasts. Journal of Cellular Biochemistry 76, 280-289..
45. Kanellos, T., Sylvester, I.D., Howard, C.R., Russell, P.H., 1999. DNA is as effective as protein at inducing antibody in fish. Vaccine 17, 965-972..
46. Kistner, A., Gossen, M., Zimmermann, F., Jerecic, J., Ullmer, C., Lubbert, H., et al., 1996. Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice. Proceedings of the National Academy of Sciences of the United States of America 93, 10933-10938..
47. Knopf, F., Schnabel, K., Haase, C., Pfeifer, K., Anastassiadis, K., Weidinger, G., 2010. Dually inducible TetON systems for tissue-specific conditional gene expression in zebrafish. Proceedings of the National Academy of Sciences of the United States of America 107, 19933-19938..
48. Lai, N.C., Tang, T., Gao, M.H., Sato, M., Miyanohara, A., Hammond, H.K., 2012. Improved function of the failing rat heart by regulated expression of insulinlike growth factor I via intramuscular gene transfer. Human Gene Therapy 23, 255-261..
49. Langenau, D.M., Feng, H., Berghmans, S., Kanki, J.P., Kutok, J.L., Look, A.T., 2005. Cre/loxregulated 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..
50. Lemieux, P., Guerin, N., Paradis, G., Proulx, R., Chistyakova, L., Kabanov, A., et al., 2000. A combination of poloxamers increases gene expression of plasmid DNA in skeletal muscle. Gene Therapy 7, 986-991..
51. Li, Z., Huang, X., Zhan, H., Zeng, Z., Li, C., Spitsbergen, J.M., et al., 2012. Inducible and repressable oncogene-addicted hepatocellular carcinoma in Tet-on xmrk transgenic zebrafish. Journal of Hepatology 56, 419-425..
52. Lin, S.B., Fan, T.W., Wu, J.L., Hui, C.F., Chen, J.Y., 2009. Immune response and inhibition of bacterial growth by electrotransfer of plasmid DNA containing the antimicrobial peptide, epinecidin-1, into zebrafish muscle. Fish & Shellfish Immunology 26, 451-458..
53. Liu, Z.J., Moav, B., Faras, A.J., Guise, K.S., Kapuscinski, A.R., Hackett, P.B., 1990a. Functional analysis of elements affecting expression of the beta-actin gene of carp. Molecular and Cellular Biology 10, 3432-3440..
54. Liu, Z.J., Zhu, Z.Y., Roberg, K., Faras, A., Guise, K., Kapuscinski, A.R., et al., 1990b. Isolation and characterization of beta-actin gene of carp (Cyprinus carpio). DNA Sequence 1, 125-136..
55. Liu, Z.J.,Moav, B., Faras, A.J., Guise, K.S., Kapuscinski, A.R., Hackett, P.B., 1990c. Development of expression vectors for transgenic fish. Biotechnology (N. Y) 8, 1268-1272..
56. Lopez-Albors, O., Abdel, I., Periago, M.J., Ayala, M.D., García Alcázar, A., Martínez Graciá, C., et al., 2008. Temperature influence on the white muscle growth dynamics of the sea bass Dicentrarchus labrax, L. Flesh quality implications at commercial size. Aquaculture 277, 39-51..
57. Lorenzen, N., Lorenzen, E., Einer-Jensen, K., Heppell, J., Wu, T., Davis, H., 1998. Protective immunity to VHS in rainbow trout (Oncorhynchus mykiss, Walbaum) following DNA vaccination. Fish & Shellfish Immunology 8, 261-270..
58. Lorenzen, N., Cupit, P.M., Einer-Jensen, K., Lorenzen, E., Ahrens, P., Secombes, C.J., et al., 2000. Immunoprophylaxis in fish by injection of mouse antibody genes. Nature Biotechnology 18, 1177-1180..
59. Maclean, N., Iyengar, A., Rahman, A., Sulaiman, Z., Penman, D., 1992. Transgene transmission and expression in rainbow trout and tilapia. Molecular Marine Biology and Biotechnology 1, 355-365..
60. Malvisi, J., della Roca, G., Anfssi, P., Zaguini, A., Tomasi, L., Magni, A., et al. 2003. Tissue disposition and residue kinetics of oxytetracycline, flumequine, amoxycillin and thiamphenicol in sea bream (Sparus aurata) after oral administration. Proceedings of the International Symposium of Progress and Prospect of Marine Biotechnology (ISPPMB'98) Qingdao, China, pp. 139-146..
61. Miana-Mena, F.J., Munoz, M.J., Roux, S., Ciriza, J., Zaragoza, P., Brulet, P., et al., 2004. A nonviral vector for targeting gene therapy to motoneurons in the CNS. Neurodegenerative Diseases 1, 101-108..
62. Mikalsen, A.B., Torgersen, J., Alestrom, P., Hellemann, A.L., Koppang, E.O., Rimstad, E., 2004. Protection of Atlantic salmon Salmo salar against infectious pancreatic necrosis after DNA vaccination. Diseases of Aquatic Organisms 60, 11-20..
63. Moav, B., Liu, Z., Caldovic, L.D., Gross, M.L., Faras, A.J., Hackett, P.B., 1993. Regulation of expression of transgenes in developing fish. Transgenic Research 2, 153-161..
64. Moav, B., Hinits, Y., Groll, Y., Rothbard, S., 1995. Inheritance of recombinant carp betaactin GH cDNA gene in transgenic carp. Aquaculture 137, 179-185..
65. Muller, F., Williams, D.W., Kobolak, J., Gauvry, L., Goldspink, G., Orban, L., et al., 1997. Activator effect of coinjected enhancers on the muscle-specific expression of promoters in zebrafish embryos. Molecular Reproduction and Development 47, 404-412..
66. Mumper, R.J., Duguid, J.G., Anwer, K., Barron, M.K., Nitta, H., Rolland, A.P., 1996. Polyvinyl derivatives as novel interactive polymers for controlled gene delivery to muscle. Pharmaceutical Research 13, 701-709..
67. Mumper, R.J.,Wang, J.,Klakamp, S.L., Nitta, H.,Anwer,K., Tagliaferri, F., et al.,1998.Protective interactive noncondensing (PINC) polymers for enhanced plasmid distribution and expression in rat skeletal muscle. Journal of Controlled Release 52, 191-203..
68. Munoz, I., Carrillo, M., Zanuy, S., Gómez, A., 2005. Regulation of exogenous gene in fish cells: an evaluation of several tetracycline regulated systems under the control of different promoters. Gene 363, 173-182..
69. Nathanailides, C., Lopez-Albors, O., Abellan, E., Vazquez, J.M., Tyler, D.D., Rowlerson, A., et al., 1996. Muscle cellularity in relation to somatic growth in the European sea bass Dicentrarchus labrax (L.). Aquaculture Research 27, 885-889..
70. Oliveira, N.A., Cecchi, C.R., Higuti, E., Oliveira, J.E., Jensen, T.G., Bartolini, P., et al., 2010. Long-term human growth hormone expression and partial phenotypic correction by plasmid-based gene therapy in an animal model of isolated growth hormone deficiency. The Journal of Gene Medicine 12, 580-585..
71. Prigozy, T., Dalrymple, K., Kedes, L., Shuler, C., 1993. Direct DNA injection into mouse tongue muscle for analysis of promoter function in vivo. Somatic Cell and Molecular Genetics 19, 111-122..
72. Pyun, W.B., Hahn, W., Kim, D.S., Yoo, W.S., Lee, S.D., Won, J.H., et al., 2010. Naked DNA expressing two isoforms of hepatocyte growth factor induces collateral artery augmentation in a rabbit model of limb ischemia. Gene Therapy 17, 1442-1452..
73. Rahman, A., Maclean, N., 1992. Fish transgene expression by direct injection into fish muscle. Molecular Marine Biology and Biotechnology 1, 286-289..
74. Rahman, M.A., Mak, R., Ayad, H., Smith, A., Maclean, N., 1998. Expression of a novel piscine growth hormone gene results in growth enhancement in transgenic tilapia (Oreochromis niloticus). Transgenic Research 7, 357-369..
75. Rao, N.M., Rambabu, K.M., Rao, S.H., 2008. Electroporation of adult zebrafish. Methods in Molecular Biology 423, 289-298..
76. Rastogi, S., Guerrero, M., Wang, M., Ilsar, I., Sabbah, M.S., Gupta, R.C., et al., 2011. Myocardial transfection with naked DNA plasmid encoding hepatocyte growth factor prevents the progression of heart failure in dogs. American Journal of Physiology - Heart and Circulatory Physiology 300, H1501-H1509..
77. Rizzuto, G., Cappelletti, M., Maione, D., Savino, R., Lazzaro, D., Costa, P., et al., 1999. Efficient and regulated erythropoietin production by naked DNA injection and muscle electroporation. Proceedings of the National Academy of Sciences of the United States of America 96, 6417-6422..
78. Rosato, A., Zoso, A., Milan, G., Macino, B., Dalla, S.S., Tosello, V., et al., 2003. Individual analysis of mice vaccinated against a weakly immunogenic self tumor-specific antigen reveals a correlation between CD8 T-cell response and antitumor efficacy. Journal of Immunology 171, 5172-5179..
79. Rowlerson, A., Mascarello, F., Radaelli, G., Veggetti, A., 1995. Differentiation and growth of muscle in the fish Sparus aurata (L): II. Hyperplastic and hypertrophic growth of lateral muscle from hatching to adult. Journal of Muscle Research and Cell Motility 16, 223-236..
80. Rowlerson, A., Radaelli, G., Mascarello, F., Veggetti, A., 1997. Regeneration of skeletal muscle in two teleost fish: Sparus aurata and Brachydanio rerio. Cell and Tissue Research 289, 311-322..
81. Sadeh, M., Czyzewski, K., Stern, L.Z., 1984. Calcium in bupivacaine-induced muscle necrosis. Muscle & Nerve 7, 752-753..
82. Sadowski, I., Bell, B., Broad, P., Hollis, M., 1992. GAL4 fusion vectors for expression in yeast or mammalian cells. Gene 118, 137-141..
83. Scheer, N., Campos-Ortega, J.A., 1999. Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mechanisms of Development 80, 153-158..
84. Scheer, N., Riedl, I., Warren, J.T., Kuwada, J.Y., Campos-Ortega, J.A., 2002. A quantitative analysis of the kinetics of Gal4 activator and effector gene expression in the zebrafish. Mechanisms of Development 112, 9-14..
85. Schulte, P.M., Powers, D.A., Schartl, M., 1998. Efficient gene transfer into Xiphophorus muscle and melanoma by injection of supercoiled plasmid DNA. Molecular Marine Biology and Biotechnology 7, 241-247..
86. Schulte, P.M., Glemet, H.C., Fiebig, A.A., Powers, D.A., 2000. Adaptive variation in lactate dehydrogenase-B gene expression: role of a stress-responsive regulatory element. Proceedings of the National Academy of Sciences of the United States of America 97, 6597-6602..
87. Sebestyen, M.G., Hegge, J.O., Noble, M.A., Lewis, D.L., Herweijer, H., Wolff, J.A., 2007. Progress toward a nonviral gene therapy protocol for the treatment of anemia. Human Gene Therapy 18, 269-285..
88. Shockett, P., Difilippantonio, M., Hellman, N., Schatz, D.G., 1995. A modified tetracyclineregulated system provides autoregulatory, inducible gene expression in cultured cells and transgenic mice. Proceedings of the National Academy of Sciences of the United States of America 92, 6522-6526..
89. Simionescu, A., Pavlath, G.K., 2011. Molecular mechanisms of myoblast fusion across species. In: Dittmar, T., Zänker, K.S. (Eds.), Cell Fusion in Health and Disease. Springer, Netherlands, pp. 113-135..
90. Sommer, B., Rinsch, C., Payen, E., Dalle, B., Schneider, B., Deglon, N., et al., 2002. Long-term doxycycline-regulated secretion of erythropoietin by encapsulated myoblasts. Molecular Therapy 6, 155-161..
91. Sommerset, I., Lorenzen, E., Lorenzen, N., Bleie, H., Nerland, A.H., 2003. A DNA vaccine directed against a rainbow trout rhabdovirus induces early protection against a nodavirus challenge in turbot. Vaccine 21, 4661-4667..
92. Sprengel, R., Hasan, M.T., 2007. Tetracycline-controlled genetic switches. Handbook of Experimental Pharmacology 178, 49-72..
93. Stebbins, M.J., Urlinger, S., Byrne, G., Bello, B., Hillen, W., Yin, J.C., 2001. Tetracyclineinducible systems for Drosophila. Proceedings of the National Academy of Sciences of the United States of America 98, 10775-10780..
94. Stieger, K., Belbellaa, B., Le Guiner, C., Moullier, P., Rolling, F., 2009. In vivo gene regulation using tetracycline-regulatable systems. Advanced Drug Delivery Reviews 61, 527-541..
95. Strathdee, C.A., McLeod, M.R., Hall, J.R., 1999. Efficient control of tetracyclineresponsive gene expression from an autoregulated bi-directional expression vector. Gene 229, 21-29..
96. Tafalla, C., Novoa, B., Alvarez, J.M., Figueras, A., 2003. In vivo and in vitro effect of oxytetracycline treatment on the inmune response of turbot, Scophtalmus maximus (L.). Journal of Fish Diseases 22, 271-276..
97. Tan, J.H., Chan, W.K., 1997. Efficient gene transfer into zebrafish skeletal muscle by intramuscular injection of plasmid DNA.Molecular Marine Biology and Biotechnology 6, 98-109..
98. Thummel, R., Burket, C.T., Brewer, J.L., Sarras,M.P., Li, L., Perry,M., et al., 2005. Cre-mediated site-specific recombination in zebrafish embryos. Developmental Dynamics 233, 1366-1377..
99. Tokui, M., Takei, I., Tashiro, F., Shimada, A., Kasuga, A., Ishii, M., et al., 1997. Intramuscular injection of expression plasmid DNA is an effective means of long-term systemic delivery of interleukin-5. Biochemical and Biophysical Research Communications 233, 527-531..
100. Tonheim, T.C., Leirvik, J., Lovoll, M., Myhr, A.I., Bogwald, J., Dalmo, R.A., 2007. Detection of supercoiled plasmid DNA and luciferase expression in Atlantic salmon (Salmo salar L.) 535 days after injection. Fish & Shellfish Immunology 23, 867-876..
101. Tonheim, T.C., Bøgwald, J., Dalmo, R.A., 2008a. What happens to the DNA vaccine in fish? A review of current knowledge. Fish & Shellfish Immunology 25, 1-18..
102. Tonheim, T.C., Dalmo, R.A., Bøgwald, J., Seternes, T., 2008b. Specific uptake of plasmid DNA without reporter gene expression in Atlantic salmon (Salmo salar L.) kidney after intramuscular administration. Fish & Shellfish Immunology 24, 90-101..
103. Urlinger, S., Baron, U., Thellmann, M., Hasan, M.T., Bujard, H., Hillen, W., 2000. Exploring the sequence space for tetracycline-dependent transcriptional activators: novel mutations yield expanded range and sensitivity. Proceedings of theNational Academy of Sciences of the United States of America 97, 7963-7968..
104. Verri, T., Ingrosso, L., Chiloiro, R., Danieli, A., Zonno, V., Alifano, P., et al., 2003. Assessment of DNA vaccine potential for gilthead sea bream (Sparus aurata) by intramuscular injection of a reporter gene. Fish & Shellfish Immunology 15, 283-295..
105. Wells, D.J., 1993. Improved gene transfer by direct plasmid injection associated with regeneration in mouse skeletal-muscle. FEBS Letters 332, 179-182..
106. Wolff, J.A., Malone, R.W., Williams, P., Chong, W., Acsadi, G., Jani, A., et al., 1990. Direct gene transfer into mouse muscle in vivo. Science 247, 1465-1468..
107. Zanuy, S., Carrillo, M., 1985. Annual cycles of growth, feeding rate, gross conversion efficiency and hematocrit levels of sea bass (Dicentrarchus labrax L.) adapted to two different osmotic media. Aquaculture 44, 11-25..