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. 1986 Sep;5(9):2209–2215. doi: 10.1002/j.1460-2075.1986.tb04486.x

Sequential expression of murine homeo box genes during F9 EC cell differentiation.

G Breier, M Bućan, U Francke, A M Colberg-Poley, P Gruss
PMCID: PMC1167102  PMID: 2877873

Abstract

We have isolated and characterized a previously unknown member of the murine homeo box family. The new locus, m31, is located on chromosome 15 and is more homologous to sequences contained in the Drosophila homeotic gene, Antp, than to any other known murine homeo box. We show that this gene encodes a 2.7 kb mRNA which is expressed during mouse embryogenesis and during differentiation of F9 teratocarcinoma cells into parietal endoderm cells. The transcript appears late in this differentiation process and is most abundant at a time when the F9 cells begin to express tissue-specific markers and the expression of another murine homeo box gene, m6, has decreased.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Awgulewitsch A., Utset M. F., Hart C. P., McGinnis W., Ruddle F. H. Spatial restriction in expression of a mouse homoeo box locus within the central nervous system. 1986 Mar 27-Apr 2Nature. 320(6060):328–335. doi: 10.1038/320328a0. [DOI] [PubMed] [Google Scholar]
  2. Berstine E. G., Hooper M. L., Grandchamp S., Ephrussi B. Alkaline phosphatase activity in mouse teratoma. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3899–3903. doi: 10.1073/pnas.70.12.3899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carroll S. B., Scott M. P. Localization of the fushi tarazu protein during Drosophila embryogenesis. Cell. 1985 Nov;43(1):47–57. doi: 10.1016/0092-8674(85)90011-x. [DOI] [PubMed] [Google Scholar]
  4. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  5. Chomczynski P., Qasba P. K. Alkaline transfer of DNA to plastic membrane. Biochem Biophys Res Commun. 1984 Jul 18;122(1):340–344. doi: 10.1016/0006-291x(84)90480-7. [DOI] [PubMed] [Google Scholar]
  6. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Colberg-Poley A. M., Voss S. D., Chowdhury K., Gruss P. Structural analysis of murine genes containing homoeo box sequences and their expression in embryonal carcinoma cells. 1985 Apr 25-May 1Nature. 314(6013):713–718. doi: 10.1038/314713a0. [DOI] [PubMed] [Google Scholar]
  8. Colberg-Poley A. M., Voss S. D., Chowdhury K., Stewart C. L., Wagner E. F., Gruss P. Clustered homeo boxes are differentially expressed during murine development. Cell. 1985 Nov;43(1):39–45. doi: 10.1016/0092-8674(85)90010-8. [DOI] [PubMed] [Google Scholar]
  9. Desplan C., Theis J., O'Farrell P. H. The Drosophila developmental gene, engrailed, encodes a sequence-specific DNA binding activity. Nature. 1985 Dec 19;318(6047):630–635. doi: 10.1038/318630a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DiNardo S., Kuner J. M., Theis J., O'Farrell P. H. Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell. 1985 Nov;43(1):59–69. doi: 10.1016/0092-8674(85)90012-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dony C., Kessel M., Gruss P. Post-transcriptional control of myc and p53 expression during differentiation of the embryonal carcinoma cell line F9. Nature. 1985 Oct 17;317(6038):636–639. doi: 10.1038/317636a0. [DOI] [PubMed] [Google Scholar]
  12. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  13. Francke U., Lalley P. A., Moss W., Ivy J., Minna J. D. Gene mapping in Mus musculus by interspecific cell hybridization: assignment of the genes for tripeptidase-1 to chromosome 10, dipeptidase-2 to chromosome 18, acid phosphatase-1 to chromosome 12, and adenylate kinase-1 to chromosome 2. Cytogenet Cell Genet. 1977;19(2-3):57–84. doi: 10.1159/000130799. [DOI] [PubMed] [Google Scholar]
  14. Francke U., Taggart R. T. Assignment of the gene for cytoplasmic superoxide dismutase (Sod-1) to a region of chromosome 16 and of Hprt to a region of the X chromosome in the mouse. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5230–5233. doi: 10.1073/pnas.76.10.5230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  16. Garber R. L., Kuroiwa A., Gehring W. J. Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J. 1983;2(11):2027–2036. doi: 10.1002/j.1460-2075.1983.tb01696.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gehring W. J. The homeo box: a key to the understanding of development? Cell. 1985 Jan;40(1):3–5. doi: 10.1016/0092-8674(85)90300-9. [DOI] [PubMed] [Google Scholar]
  18. Hafen E., Levine M., Gehring W. J. Regulation of Antennapedia transcript distribution by the bithorax complex in Drosophila. Nature. 1984 Jan 19;307(5948):287–289. doi: 10.1038/307287a0. [DOI] [PubMed] [Google Scholar]
  19. Hart C. P., Awgulewitsch A., Fainsod A., McGinnis W., Ruddle F. H. Homeo box gene complex on mouse chromosome 11: molecular cloning, expression in embryogenesis, and homology to a human homeo box locus. Cell. 1985 Nov;43(1):9–18. doi: 10.1016/0092-8674(85)90007-8. [DOI] [PubMed] [Google Scholar]
  20. Hauser C. A., Joyner A. L., Klein R. D., Learned T. K., Martin G. R., Tjian R. Expression of homologous homeo-box-containing genes in differentiated human teratocarcinoma cells and mouse embryos. Cell. 1985 Nov;43(1):19–28. doi: 10.1016/0092-8674(85)90008-x. [DOI] [PubMed] [Google Scholar]
  21. Herrmann B., Bućan M., Mains P. E., Frischauf A. M., Silver L. M., Lehrach H. Genetic analysis of the proximal portion of the mouse t complex: evidence for a second inversion within t haplotypes. Cell. 1986 Feb 14;44(3):469–476. doi: 10.1016/0092-8674(86)90468-x. [DOI] [PubMed] [Google Scholar]
  22. Jackson I. J., Schofield P., Hogan B. A mouse homoeo box gene is expressed during embryogenesis and in adult kidney. Nature. 1985 Oct 24;317(6039):745–748. doi: 10.1038/317745a0. [DOI] [PubMed] [Google Scholar]
  23. Joyner A. L., Kornberg T., Coleman K. G., Cox D. R., Martin G. R. Expression during embryogenesis of a mouse gene with sequence homology to the Drosophila engrailed gene. Cell. 1985 Nov;43(1):29–37. doi: 10.1016/0092-8674(85)90009-1. [DOI] [PubMed] [Google Scholar]
  24. Joyner A. L., Lebo R. V., Kan Y. W., Tjian R., Cox D. R., Martin G. R. Comparative chromosome mapping of a conserved homoeo box region in mouse and human. Nature. 1985 Mar 14;314(6007):173–175. doi: 10.1038/314173a0. [DOI] [PubMed] [Google Scholar]
  25. Kurkinen M., Barlow D. P., Helfman D. M., Williams J. G., Hogan B. L. Isolation of cDNA clones for basal lamina components: type IV procollagen. Nucleic Acids Res. 1983 Sep 24;11(18):6199–6209. doi: 10.1093/nar/11.18.6199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kuroiwa A., Hafen E., Gehring W. J. Cloning and transcriptional analysis of the segmentation gene fushi tarazu of Drosophila. Cell. 1984 Jul;37(3):825–831. doi: 10.1016/0092-8674(84)90417-3. [DOI] [PubMed] [Google Scholar]
  27. Kuroiwa A., Kloter U., Baumgartner P., Gehring W. J. Cloning of the homeotic Sex combs reduced gene in Drosophila and in situ localization of its transcripts. EMBO J. 1985 Dec 30;4(13B):3757–3764. doi: 10.1002/j.1460-2075.1985.tb04145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Laughon A., Scott M. P. Sequence of a Drosophila segmentation gene: protein structure homology with DNA-binding proteins. Nature. 1984 Jul 5;310(5972):25–31. doi: 10.1038/310025a0. [DOI] [PubMed] [Google Scholar]
  29. Law S., Tamoaki T., Kreuzaler F., Dugaiczyk A. Molecular cloning of DNA complementary to a mouse alpha-fetoprotein mRNA sequence. Gene. 1980 Jun;10(1):53–61. doi: 10.1016/0378-1119(80)90143-2. [DOI] [PubMed] [Google Scholar]
  30. Levine M., Rubin G. M., Tjian R. Human DNA sequences homologous to a protein coding region conserved between homeotic genes of Drosophila. Cell. 1984 Oct;38(3):667–673. doi: 10.1016/0092-8674(84)90261-7. [DOI] [PubMed] [Google Scholar]
  31. McGinnis W., Garber R. L., Wirz J., Kuroiwa A., Gehring W. J. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell. 1984 Jun;37(2):403–408. doi: 10.1016/0092-8674(84)90370-2. [DOI] [PubMed] [Google Scholar]
  32. McGinnis W., Hart C. P., Gehring W. J., Ruddle F. H. Molecular cloning and chromosome mapping of a mouse DNA sequence homologous to homeotic genes of Drosophila. Cell. 1984 Oct;38(3):675–680. doi: 10.1016/0092-8674(84)90262-9. [DOI] [PubMed] [Google Scholar]
  33. McGinnis W., Levine M. S., Hafen E., Kuroiwa A., Gehring W. J. A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. 1984 Mar 29-Apr 4Nature. 308(5958):428–433. doi: 10.1038/308428a0. [DOI] [PubMed] [Google Scholar]
  34. Mlodzik M., Fjose A., Gehring W. J. Isolation of caudal, a Drosophila homeo box-containing gene with maternal expression, whose transcripts form a concentration gradient at the pre-blastoderm stage. EMBO J. 1985 Nov;4(11):2961–2969. doi: 10.1002/j.1460-2075.1985.tb04030.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Müller M. M., Carrasco A. E., DeRobertis E. M. A homeo-box-containing gene expressed during oogenesis in Xenopus. Cell. 1984 Nov;39(1):157–162. doi: 10.1016/0092-8674(84)90201-0. [DOI] [PubMed] [Google Scholar]
  36. Rabin M., Hart C. P., Ferguson-Smith A., McGinnis W., Levine M., Ruddle F. H. Two homoeo box loci mapped in evolutionarily related mouse and human chromosomes. Nature. 1985 Mar 14;314(6007):175–178. doi: 10.1038/314175a0. [DOI] [PubMed] [Google Scholar]
  37. Rackwitz H. R., Zehetner G., Frischauf A. M., Lehrach H. Rapid restriction mapping of DNA cloned in lambda phage vectors. Gene. 1984 Oct;30(1-3):195–200. doi: 10.1016/0378-1119(84)90120-3. [DOI] [PubMed] [Google Scholar]
  38. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Schnieke A., Harbers K., Jaenisch R. Embryonic lethal mutation in mice induced by retrovirus insertion into the alpha 1(I) collagen gene. 1983 Jul 28-Aug 3Nature. 304(5924):315–320. doi: 10.1038/304315a0. [DOI] [PubMed] [Google Scholar]
  40. Shepherd J. C., McGinnis W., Carrasco A. E., De Robertis E. M., Gehring W. J. Fly and frog homoeo domains show homologies with yeast mating type regulatory proteins. Nature. 1984 Jul 5;310(5972):70–71. doi: 10.1038/310070a0. [DOI] [PubMed] [Google Scholar]
  41. Strickland S., Smith K. K., Marotti K. R. Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell. 1980 Sep;21(2):347–355. doi: 10.1016/0092-8674(80)90471-7. [DOI] [PubMed] [Google Scholar]
  42. Struhl G., White R. A. Regulation of the Ultrabithorax gene of Drosophila by other bithorax complex genes. Cell. 1985 Dec;43(2 Pt 1):507–519. doi: 10.1016/0092-8674(85)90180-1. [DOI] [PubMed] [Google Scholar]
  43. Wang S. Y., Gudas L. J. Isolation of cDNA clones specific for collagen IV and laminin from mouse teratocarcinoma cells. Proc Natl Acad Sci U S A. 1983 Oct;80(19):5880–5884. doi: 10.1073/pnas.80.19.5880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. White R. A., Wilcox M. Distribution of Ultrabithorax proteins in Drosophila. EMBO J. 1985 Aug;4(8):2035–2043. doi: 10.1002/j.1460-2075.1985.tb03889.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Woychik R. P., Stewart T. A., Davis L. G., D'Eustachio P., Leder P. An inherited limb deformity created by insertional mutagenesis in a transgenic mouse. Nature. 1985 Nov 7;318(6041):36–40. doi: 10.1038/318036a0. [DOI] [PubMed] [Google Scholar]

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