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The induction of a specific pigment cell type by total genomic DNA injected into the neural crest region of fish embryos of the genus Xiphophorus

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Summary

We report genetic transformation in an intact higher organism, i.e., in xiphophorine fish. The gene to be transferred (Tu) is responsible for the formation of T-melanophores in the platyfish and is involved in the formation of melanomas in platyfish-swordtail hybrids. After injection of Tu-donor DNA into the neural crest region of embryos from Tu-free fish, some of the recipients developed T-melanophores. In a few cases, one or two single T-melanophores were formed during late embryogenesis. In most cases, many T-melanophores developed in young fish and were arranged in several colonies or in a pattern. DNase-degraded Tu-donor DNA, Tu-free fish DNA, as well as DNA from E. coli and adenovirus-2, did not induce T-melanophores. When using DNA from different strains of Tu-donor fish which differed in a regulating gene linked to Tu, the percentages of fish showing T-melanophores paralleled the degree of phenotypic expression of the Tu gene in the DNA donor. The results suggest that the Tu gene has been successfully transferred together with the linked regulating gene.

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References

  • Anders A, Anders F, Klinke K (1973a) Regulation of gene expression in the Gordon-Kosswig melanoma system. I. The distribution of the controlling genes in the genome of the xiphophorin fish, Platypoecilus maculatus and Platypoecilus variatus. In: Schröder JH (ed) Genetics and mutagenesis of fish. Springer, Berlin, Heidelberg, New York, pp 33–52

    Google Scholar 

  • Anders A, Anders F, Klinke K (1973b) Regulation of gene expression in the Gordon-Kosswig melanoma system. II. The arrangement of chromatophore determining loci and regulating elements in the sex chromosomes of Platypoecilus maculatus and Platypoecilus variatus. In: Schröder JH (ed) Genetics and mutagenesis of fish. Springer, Berlin, Heidelberg, New York, pp 53–63

    Google Scholar 

  • Anders F (1967) Tumor formation in platyfish-swordtail hybrids as a problem of gene regulation. Experientia 23:1–10

    Google Scholar 

  • Anders F, Anders A, Vielkind U (1974) Regulation of tumor expression in the Gordon-Kosswig melanoma system, and the origin of malignancy. Abstracts of the XIth International Cancer Congress, Florence, 305

  • Anders F, Diehl H, Scholl E (1980) Differentiation of normal melanophores and neoplastically transformed melanophores in the skin of fishes of genus Xiphophorus. In: Spearman RIC and Riley PA (eds) The skin of vertebrates. Academic Press, London, pp 211–224

    Google Scholar 

  • Borack LT (1972) Gene action on proliferation and migration in the developing neural crest of black and white axolotls, Ambystoma mexicanum, Shaw. J Exp Zool 179:289–298

    Google Scholar 

  • Brinster RL (1981) The effect of cells transferred into the mouse blastocyst on subsequent development. J Exp Med 140:1049–1056

    Google Scholar 

  • Brinster RL, Chen HY, Trumbauer M, Senear AW, Warren R, Palmites RD (1981) Somatic expression of herpes thymidine kinase in mice following injection of a fusion gene into eggs. Cell 27:223–231

    Google Scholar 

  • Brown DD, Gurdon JB (1977) High fidelity transcription of 5S DNA injected into Xenopus oocytes. Proc Natl Acad Sci USA 74:2064–2068

    Google Scholar 

  • Caspari EW, Friedman HS, Young EM (1975) Genetic changes induced by DNA in Ephestia. Genetics 80:s19-s20

    Google Scholar 

  • Chen ST, Wahn H, Turner WA, Taylor JD, Chen TT (1974) HSH, cyclic AMP, and melanocyte differentiation. Recent Progr Hormone Res 30:319–345

    Google Scholar 

  • Diehl HH (1975) Über die Entwicklung des embryonalen Pigmentierungsmusters bei verschiedenen Genotypen von Xiphophorus (Pisces, Poeciliidae). Diplomarbeit, Universität Giessen

  • Fahmy OG, Fahmy MJ (1965) Genetic properties of exogenous deoxyribonucleic acid at various levels of degradation in Drosophila melanogaster. Nature 207:507–510

    Google Scholar 

  • Fox AS (1977) Gene transfer in Drosophila melanogaster. In: Rubinstein I (ed) Molecular genetic modification of eukaryotes. Academic Press, New York, pp 101–131

    Google Scholar 

  • Fox AS, Yoon SB (1970) DNA-induced transformation in Drosophila: locus-specificity and the establishment of transformed stocks. Proc Natl Acad Sci USA 67:1608–1615

    Google Scholar 

  • Fox AS, Yoon SB, Duggleby WF, Gelbart WM (1971) Genetic transformation in Drosophila. In: Ledoux L (ed) Informative molecules in biological systems. North-Holland Publ Co, Amsterdam, London, pp 313–333

    Google Scholar 

  • Germeraad S (1976) Genetic transformation in Drosophila by microinjection of DNA. Nature 262:229–231

    Google Scholar 

  • Gordon H, Gordon M (1957) Maintenance of polymorphism by potentially injurious genes in eight natural populations of the platyfish, Xiphophorus maculatus. J Genet 55:1–44

    Google Scholar 

  • Gordon JW, Scangos GA, Plotkin DJ, Barbora JA, Ruddle FH (1980) Genetic transformation of mouse embryos by microinjection of purified DNA. Proc Natl Acad Sci USA 77:7380–7384

    Google Scholar 

  • Gordon M (1927) The genetics of a viviparous top minnow Platypoecilus; the inheritance of two kinds of melanophores. Genetics 12:253–283

    Google Scholar 

  • Gordon M (1948) Effects of five primary genes on the sites of melanomas in fishes and the influence of two color genes on their pigmentation. The Biology of Melanomas, NY Acad Sci Spec Publ 4:216–268

    Google Scholar 

  • Gordon M (1959) The melanoma cell as an incompletely differentiated pigment cell. In: Gordon M (ed) Pigment cell biology. Academic Press, New York, pp 215–239

    Google Scholar 

  • Gordon M, Lansing L (1943) Cutaneous melanophore eruptions in young fishes during stages preceding melanotic tumor formation. J Morphol 73:231–245

    Google Scholar 

  • Gradmann-Rebel W, Hemleben V (1976) Incorporation of T4 phage DNA into a specific DNA fraction from the higher plant Matthiola incana. Z Naturforsch 31c:558–564

    Google Scholar 

  • Haas-Andela H (1976) In vitro-Kultur und Aufzucht von Embryonen lebendgebärender Zahnkarpfen der Gattung Xiphophorus. Zool Anz (Jena) 197:1–5

    Google Scholar 

  • Humm DG, Young RS (1956) The embryological origin of pigment cells in platyfish-swordtail hybrids. Zoologica (NY) 41:1–10

    Google Scholar 

  • Illmensee K, Hoppe PC (1981) Nuclear transplantation in Mus musculus: developmental potential of nucleic from implantation embryos. Cell 23:9–18

    Google Scholar 

  • Jaenisch R, Mintz B (1974) Simian virus 40 DNA sequences in DNA of healthy adult mice derived from preimplantation blastocysts injected with viral DNA. Proc Natl Acad Sci USA 71:1250–1254

    Google Scholar 

  • Kallman KD (1975) The platyfish, Xiphophorus maculatus. In: King RC (ed) Handbook of genetics, vol 4. Plenum Press, New York, pp 81–132

    Google Scholar 

  • Klingmüller W (1976) Genmanipulation und Gentherapie. Springer, Berlin, Heidelberg, New York

    Google Scholar 

  • Martinovitch PN, Kanazir DT, Knezevitch ZA, Simitch MM (1962) Teratological changes in the offspring of chicken embryos treated with tyrode or with tyrode plus DNA. J Embryol Exp Morphol 10:167–177

    Google Scholar 

  • Mayer TC (1973) The migratory pathway of neural crest cells into the skin of mouse embryos. Devel Biol 34:39–46

    Google Scholar 

  • Mintz B, Illmensee K (1975) Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc Natl Acad Sci USA 72:3585–3589

    Google Scholar 

  • Ottolenghi-Nightingale E (1974) DNA-mediated transformation in mammalian cells. In: Cox RD (ed) Cell communication. John Wiley and Sons, New York, pp 233–254

    Google Scholar 

  • Pellicer A, Robins D, Wold B, Sweet R, Jackson J, Lowy I, Roberts JM, Sim G-K, Silverstein S, Axel R (1980) Altering genotype and phenotype by DNA-mediated gene transfer. Science 209:1414–1422

    Google Scholar 

  • Pellicer A, Wigler M, Axel R, Silverstein S (1978) The transfer and stable integration of the HSV thymidine kinase gene into mouse cells. Cell 14:133–141

    Google Scholar 

  • Schmidt ER (1978) Chromatophore development and cell interactions in the skin of xiphophorine fish. Wilhelm Roux's Arch 184:115–134

    Google Scholar 

  • Schwab M, Vielkind J (1973) A simple effective procedure for the isolation of high molecular weight DNA. IRCS Med Sci (73-3) 3-2-2

    Google Scholar 

  • Schwab M, Vielkind J, Anders F (1976) An approach to genetic transformation in xiphophorine fish. Mol Gen Genet 144:151–158

    Google Scholar 

  • Siniscalco M (1972) Correction of genetic defects in cultured mammalian cells. Adv Biosci 8:307–327

    Google Scholar 

  • Tavolga WN (1949) Embryonic development of the platyfish (Platypoecilus), the swordtail (Xiphophorus) and their hybrids. Bull Am Mus Nat Hist 94:165–229

    Google Scholar 

  • Turner WA Jr, Taylor JD, Chen TT (1975) Melanosome formation in the goldfish: the role of multivesicular bodies. J Ultrastruct Res 51:16–31

    Google Scholar 

  • Vielkind J (1971) Versuche zur genetischen Transformation bei lebendgebärenden Zalnkarpfen (Poeciliidae). Applikation heterologer DNA und ihr Schicksal in Rezipienten. Dissertation, Universität Giessen

  • Vielkind J (1979) Gentransfer mittels exogener DNA bei lebendgebärenden Zahnkarpfen (Poeciliidae). Habilitationsschrift, Universität Giessen

  • Vielkind J, Girgsdies O (1976) Evidence for uptake of exogenous DNA by fish embryo DNA. IRCS Med Sci 4:268

    Google Scholar 

  • Vielkind J, Haas-Andela H, Anders F (1976) DNA-mediated transformation in the platyfish-swordtail melanoma system. Experientia 32:1043–1044

    Google Scholar 

  • Vielkind J, Haas-Andela H, Anders F (1978) Characterization of the genetic factors involved in melanoma formation in xiphophorin fish by transformation experiments. Verh Dtsch Zool Ges Konstanz 1978, p 228

  • Vielkind J, Haas-Andela H, Anders F (1979) Xiphophorine fish as a carcinogenesis model. X. Transfer of the tumor gene (Tu) and its linked regulating gene (R). ICRDB, Special listing of current cancer research on etiology, epidemiology and biology of melanomas and other skin cancers, No. 146

  • Vielkind J, Schwab M, Anders F (1973) Fate of bacterial DNA injected into embryos of poeciliid fish. In: Schröder JH (ed) Genetics and mutagenesis of fish. Springer, Berlin, Heidelberg, New York, pp 123–137

    Google Scholar 

  • Vielkind J, Vielkind U (1982) Melanoma formation in fish of the genus Xiphophorus: a genetically-based disorder in the determination and differentiation of a specific pigment cell. Can J Genet Cytol (in press)

  • Vielkind J, Vielkind U, Anders F (1971a) Melanotic and amelanotic melanomas in xiphophorin fish. Cancer Res 31:868–875

    Google Scholar 

  • Vielkind J, Vielkind U, von Grotthuss E, Anders F (1971b) Uptake of bacterial H3-DNA into fish embryos. Experientia 27:347–348

    Google Scholar 

  • Vielkind U (1976) Genetic control of cell differentiation in platyfish-swordtail melanomas. J Exp Zool 196:197–204

    Google Scholar 

  • Weston J (1963) A radioautographic analysis of the migration and localization of trunk neural crest cells in the chick. Devel Biol 6:279–310

    Google Scholar 

  • Wigler M, Pellicer A, Silverstein S, Axel R (1978) Biochemical transfer and stable integration of the HSV thymidine kinase gene into mouse cells. Cell 14:725–731

    Google Scholar 

  • Wigler M, Sweet R, Sim GK, Wold B, Pellicer A, Lacy E, Maniatis T, Silverstein S, Axel R (1979) Transformation of mammalian cells with genes from procaryotes and eucaryotes. Cell 16:777–785

    Google Scholar 

  • Willecke K (1980) DNA mediated gene transfer between mammalian cells. In: Celis JE, Graessmann A, Loyter A (eds) Transfer of cell constituents into eukaryotic cells. Plenum Press, New York, London, pp 311–324

    Google Scholar 

  • Willecke K, Klomfass M, Mireau R, Döhmer J (1979) Intraspecific transfer via total cellular DNA of the gene for hypoxanthine phosphoribosyl transferase into cultured mouse cells. Mol Gen Genet 170:179–185

    Google Scholar 

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Communicated by J. Schell

Part of this work has been done by H.H. for her doctoral thesis

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Vielkind, J., Haas-Andela, H., Vielkind, U. et al. The induction of a specific pigment cell type by total genomic DNA injected into the neural crest region of fish embryos of the genus Xiphophorus . Mol Gen Genet 185, 379–389 (1982). https://doi.org/10.1007/BF00334128

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