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Genotype-specific modifiers of transgene methylation and expression in the zebrafish, Danio rerio

Published online by Cambridge University Press:  14 April 2009

C. Cristofre Martin
Affiliation:
Department of Zoology, University of Manitoba, Winnipeg, Manitoba, R3T 2N2, Canada
Ross McGowan*
Affiliation:
Department of Zoology, University of Manitoba, Winnipeg, Manitoba, R3T 2N2, Canada
*
* Corresponding author.

Summary

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Previous reports involving mammalian systems, particularly mice, have demonstrated the existence of cis- and trans-acting modifiers of transgene methylation. These modifiers are thought to be important in dominance modification, genome imprinting and cellular expression mosaicism. Their potential role in the penetrance and severity of many complex human diseases could be of even greater significance. In the present investigation we demonstrate that modifiers that act in a similar fashion to those identified in mice also exist in a non-mammalian vertebrate, the zebrafish Danio rerio. We also provide evidence that the transgene methylation pattern may be influenced by the sex of the individual and environmental modulators such as temperature and sodium butyrate. These data support the theory that this type of dominance modification is mechanistically similar to position effect variegation in Drosophila. Furthermore, these data suggest evolutionary conservation of the modifiers, at least within vertebrates, and imply that they and their actions are important in normal vertebrate development.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1995

References

Allen, N. D., Norris, M. L., & Surani, M. A. H., (1990). Epigenetic control of transgene expression and imprinting by genotype-specific modifiers. Cell 61, 853861.Google Scholar
Braunstein, M., Rose, A. B., Holmes, S. G., Allis, C. D., & Broach, J. R., (1993). Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes & Development 7, 592604.Google Scholar
Cedar, H., (1988). DNA methylation and gene activity. Cell 53, 34.Google Scholar
Fisher, R. A., (1928). The possible modification of the response of the recurrent mutations. American Naturalist 62, 115126.Google Scholar
Forejt, J., & Gregorova, S., (1992). Genetic analysis of genomic imprinting: An Imprintor-1 gene control inactivation of the paternal copy of the mouse Tme locus. Cell 70, 443450.CrossRefGoogle ScholarPubMed
Gowen, J. W., & Gay, E. H., (1934). Chromosome constitution and behavior in ever-sporting and mottling in Drosophila melanogaster. Genetics 19, 189208.CrossRefGoogle ScholarPubMed
Henikoff, S., (1990). Position-effect variegation after 60 years. Trends in Genetics 6, 422426.CrossRefGoogle Scholar
James, T. C., & Elgin, S. C. R., (1986). Identification of a non-histone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Molecular and Cellular Biology 6, 38623872.Google ScholarPubMed
Laird, C., (1990). Proposed genetics basis of Huntington's disease. Trends in Genetics 6, 242247.Google Scholar
Lee, S., & Gross, D. S., (1993). Conditional silencing: the HMRE mating-type silencer exerts a rapidly reversible position effect on the yeast HSP82 heat shock protein. Molecular and Cellular Biology 13, 727738.Google Scholar
Levy-Wilson, B., Watson, D. C., & Dixon, G. H., (1979). Multiacetylated forms of H4 are found in a putative transcriptionally competent chromatin fraction from trout testes. Nucleic Acids Research 6, 259274.CrossRefGoogle Scholar
Martin, C., & McGowan, R., (1991). Strain-specific modifiers of transgene methylation and expression and genome imprinting in the zebrafish, Brachydanio rerio. Abstracts, Zebrafish Development and Genetics. Cold Spring Harbor Laboratory.Google Scholar
McGowan, R., Campbell, R., Peterson, A., & Sapienza, C., (1989). Cellular mosaicism in the methylation and expression of hemizygous loci in the mouse. Genes & Development 3, 16691676.CrossRefGoogle ScholarPubMed
Miller, O. J., Schedl, W., Allen, J., & Erlanger, B. F., (1974). 5′-Methyl-cytosine localized in mammalian constitutive heterochromatin. Nature 251, 636637.Google Scholar
Monk, M., (1990). Changes in DNA methylation during mouse embryonic development in relation to X-chromosome activity and imprinting. Philosophical Transactions Royal Society London B 326, 299312.Google Scholar
Monk, M., Boubelik, M., & Lehnert, S., (1987). Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99, 371382.Google Scholar
Mottus, R., Reeves, R., & Grigliatti, T. A., (1980). Butyrate suppression of position-effect variegation in Drosophila melanogaster. Molecular and General Genetics 178, 465469.Google ScholarPubMed
Paro, R., & Hogness, D. S., (1991). The Polycomb protein shares a homologous domain with a heterochromatinassociated protein of Drosophila. Proceedings of the National Academy of Sciences USA 88, 263267.Google Scholar
Peter, E., Candido, M., Reeves, R., & Davie, J. R., (1978). Sodium butyrate inhibits histone deacetylation in cultured cells. Cell 14, 105113.Google Scholar
Sapienza, C., Peterson, A., Rossant, J., & Balling, R., (1987). Degree of methylation of transgenes is dependent on gamete of origin. Nature 328, 251254.CrossRefGoogle ScholarPubMed
Sapienza, C., Paquette, J., Tran, T. H., & Peterson, A., (1989). Epigenetic and genetic factors affecting transgene methylation imprinting. Development 107, 165168.CrossRefGoogle ScholarPubMed
Sapienza, C. (1990 a). Sex-linked dosage-sensitive modifiers as imprinting genes. Development Supplement, 107113.Google ScholarPubMed
Sapienza, C. (1990 b). Genome imprinting, cellular mosaicism and carcinogenesis. Molecular Carcinogenetics 3, 118121.CrossRefGoogle ScholarPubMed
Schmid, M., Hoff, T., & Grunert, D., (1984). 5′-Azacytidine undercondensation in human chromosomes. Human Genetics 67, 257263.Google Scholar
Scrable, H., Cavenee, W., Ghavimi, F., Lovell, M., Morgan, K., & Sapienza, C., (1989). A model for embryonal rhabdomyosarcoma tumorigenesis that involves genomic imprinting. Proceedings of the National Academy of Sciences USA 86, 74807484.Google Scholar
Singh, P. B., Miller, J. R., Pearce, J., Kothary, R., Burton, R. D., Paro, R., James, T. C., & Gaunt, S. J., (1991). A sequence motif found in a Drosophila heterochromatin protein is conserved in animals and plants. Nucleic Acids Research 19, 789794.Google Scholar
Spofford, J. B., (1976). Position effect variagation in Drosophila. In: The Genetics and Biology of Drosophila (ed. Ashburner, M. and Novitski, E.), pp. 9551018. New York: Academic Press.Google Scholar
Stuart, G. W., Viclkind, J. R., McMurry, J. V., & Westerfield, M., (1990). Stable lines of transgenic zebrafish exhibit reproducible patterns of transgene expression. Development 109, 577584.CrossRefGoogle ScholarPubMed
Swain, J. L., Stewart, T. A., & Leder, P., (1987). Parental legacy determines methylation and expression of an autosomal transgene: A molecular mechanism for parental imprinting. Cell 50, 719727.Google Scholar
Varmuza, S., (1993). Gametic imprinting as a speciation mechanism in mammals. Journal of Theoretical Biology 164, 113.CrossRefGoogle ScholarPubMed
Westerfield, M., (1989). The Zebrafish Book. University of Oregon Press, Eugene, Oregon.Google Scholar
Wreggett, K. A., Hill, F., James, P. S., Hutchings, A., Butcher, G. W., & Singh, P. B., (1994). A mammalian homologue of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenetics and Cell Genetics 66, 99103.Google Scholar