Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1987 Sep 11;15(17):6773–6786. doi: 10.1093/nar/15.17.6773

A mouse homeobox containing gene on chromosome 11: sequence and tissue-specific expression.

F Meijlink 1, R de Laaf 1, P Verrijzer 1, O Destrée 1, V Kroezen 1, J Hilkens 1, J Deschamps 1
PMCID: PMC306174  PMID: 2889183

Abstract

We have molecularly cloned a mouse homeobox containing gene by isolating cDNA and genomic clones. The gene is located in a previously described cluster on chromosome 11 (Hart et al. (1985) Cell 43, 9-18) and was identified as the Hox2.3 gene. We present the complete mRNA sequence of this gene and describe similarities to other homeobox containing genes, among which its human homologue, the cl gene. High expression of the Hox2.3 gene was found in kidney, testis, and spinal cord of adult mice, in the spinal cord of 12.5-17.5 day embryos and in differentiating EC cells depending on their treatment. Three different treatments of the pluripotent EC cell line P19, each leading to the induction of a specific differentiation pathway, resulted in all cases in induction of Hox2.3; however, major quantitative differences in this response were observed.

Full text

PDF
6774

Images in this article

6781Image
on p.6781
6782Image
on p.6782

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. Bachmair A., Finley D., Varshavsky A. In vivo half-life of a protein is a function of its amino-terminal residue. Science. 1986 Oct 10;234(4773):179–186. doi: 10.1126/science.3018930. [DOI] [PubMed] [Google Scholar]
  3. Breier G., Bućan M., Francke U., Colberg-Poley A. M., Gruss P. Sequential expression of murine homeo box genes during F9 EC cell differentiation. EMBO J. 1986 Sep;5(9):2209–2215. doi: 10.1002/j.1460-2075.1986.tb04486.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bućan M., Yang-Feng T., Colberg-Poley A. M., Wolgemuth D. J., Guenet J. L., Francke U., Lehrach H. Genetic and cytogenetic localisation of the homeo box containing genes on mouse chromosome 6 and human chromosome 7. EMBO J. 1986 Nov;5(11):2899–2905. doi: 10.1002/j.1460-2075.1986.tb04585.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chen E. Y., Seeburg P. H. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA. 1985 Apr;4(2):165–170. doi: 10.1089/dna.1985.4.165. [DOI] [PubMed] [Google Scholar]
  6. 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]
  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. Deschamps J., de Laaf R., Joosen L., Meijlink F., Destrée O. Abundant expression of homeobox genes in mouse embryonal carcinoma cells correlates with chemically induced differentiation. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1304–1308. doi: 10.1073/pnas.84.5.1304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Duboule D., Baron A., Mähl P., Galliot B. A new homeo-box is present in overlapping cosmid clones which define the mouse Hox-1 locus. EMBO J. 1986 Aug;5(8):1973–1980. doi: 10.1002/j.1460-2075.1986.tb04452.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Edwards M. K., Harris J. F., McBurney M. W. Induced muscle differentiation in an embryonal carcinoma cell line. Mol Cell Biol. 1983 Dec;3(12):2280–2286. doi: 10.1128/mcb.3.12.2280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fainsod A., Bogarad L. D., Ruusala T., Lubin M., Crothers D. M., Ruddle F. H. The homeo domain of a murine protein binds 5' to its own homeo box. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9532–9536. doi: 10.1073/pnas.83.24.9532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Fellous M., Günther E., Kemler R., Wiels J., Berger R., Guenet J. L., Jakob H., Jacob F. Association of the H-Y male antigen with beta2-microglobulin on human lymphoid and differentiated mouse teratocarcinoma cell lines. J Exp Med. 1978 Jul 1;148(1):58–70. doi: 10.1084/jem.148.1.58. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gaunt S. J., Miller J. R., Powell D. J., Duboule D. Homoeobox gene expression in mouse embryos varies with position by the primitive streak stage. Nature. 1986 Dec 18;324(6098):662–664. doi: 10.1038/324662a0. [DOI] [PubMed] [Google Scholar]
  17. Gehring W. J. Homeo boxes in the study of development. Science. 1987 Jun 5;236(4806):1245–1252. doi: 10.1126/science.2884726. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Harvey R. P., Tabin C. J., Melton D. A. Embryonic expression and nuclear localization of Xenopus homeobox (Xhox) gene products. EMBO J. 1986 Jun;5(6):1237–1244. doi: 10.1002/j.1460-2075.1986.tb04352.x. [DOI] [PMC free article] [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. Hilkens J., Colombatti A., Strand M., Nichols E., Ruddle F. H., Hilgers J. Identification of a mouse gene required for binding of Rauscher MuLV envelope gp70. Somatic Cell Genet. 1979 Jan;5(1):39–49. doi: 10.1007/BF01538785. [DOI] [PubMed] [Google Scholar]
  22. Hilkens J., Cuypers H. T., Selten G., Kroezen V., Hilgers J., Berns A. Genetic mapping of Pim-1 putative oncogene to mouse chromosome 17. Somat Cell Mol Genet. 1986 Jan;12(1):81–88. doi: 10.1007/BF01560730. [DOI] [PubMed] [Google Scholar]
  23. Hilkens J., van der Zeijst B., Buijs F., Kroezen V., Bleumink N., Hilgers J. Identification of a cellular receptor for mouse mammary tumor virus and mapping of its gene to chromosome 16. J Virol. 1983 Jan;45(1):140–147. doi: 10.1128/jvi.45.1.140-147.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Jones-Villeneuve E. M., McBurney M. W., Rogers K. A., Kalnins V. I. Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J Cell Biol. 1982 Aug;94(2):253–262. doi: 10.1083/jcb.94.2.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Joyner A. L., Martin G. R. En-1 and En-2, two mouse genes with sequence homology to the Drosophila engrailed gene: expression during embryogenesis. Genes Dev. 1987 Mar;1(1):29–38. doi: 10.1101/gad.1.1.29. [DOI] [PubMed] [Google Scholar]
  29. Krumlauf R., Holland P. W., McVey J. H., Hogan B. L. Developmental and spatial patterns of expression of the mouse homeobox gene, Hox 2.1. Development. 1987 Apr;99(4):603–617. doi: 10.1242/dev.99.4.603. [DOI] [PubMed] [Google Scholar]
  30. Laughon A., Boulet A. M., Bermingham J. R., Jr, Laymon R. A., Scott M. P. Structure of transcripts from the homeotic Antennapedia gene of Drosophila melanogaster: two promoters control the major protein-coding region. Mol Cell Biol. 1986 Dec;6(12):4676–4689. doi: 10.1128/mcb.6.12.4676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Martin G. R., Wiley L. M., Damjanov I. The development of cystic embryoid bodies in vitro from clonal teratocarcinoma stem cells. Dev Biol. 1977 Dec;61(2):230–244. doi: 10.1016/0012-1606(77)90294-9. [DOI] [PubMed] [Google Scholar]
  33. Mavilio F., Simeone A., Giampaolo A., Faiella A., Zappavigna V., Acampora D., Poiana G., Russo G., Peschle C., Boncinelli E. Differential and stage-related expression in embryonic tissues of a new human homoeobox gene. Nature. 1986 Dec 18;324(6098):664–668. doi: 10.1038/324664a0. [DOI] [PubMed] [Google Scholar]
  34. McBurney M. W., Rogers B. J. Isolation of male embryonal carcinoma cells and their chromosome replication patterns. Dev Biol. 1982 Feb;89(2):503–508. doi: 10.1016/0012-1606(82)90338-4. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. Münke M., Cox D. R., Jackson I. J., Hogan B. L., Francke U. The murine Hox-2 cluster of homeo box containing genes maps distal on chromosome 11 near the tail-short (Ts) locus. Cytogenet Cell Genet. 1986;42(4):236–240. doi: 10.1159/000132284. [DOI] [PubMed] [Google Scholar]
  38. Pabo C. O., Sauer R. T. Protein-DNA recognition. Annu Rev Biochem. 1984;53:293–321. doi: 10.1146/annurev.bi.53.070184.001453. [DOI] [PubMed] [Google Scholar]
  39. Rabin M., Ferguson-Smith A., Hart C. P., Ruddle F. H. Cognate homeo-box loci mapped on homologous human and mouse chromosomes. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9104–9108. doi: 10.1073/pnas.83.23.9104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Regulski M., McGinnis N., Chadwick R., McGinnis W. Developmental and molecular analysis of Deformed; a homeotic gene controlling Drosophila head development. EMBO J. 1987 Mar;6(3):767–777. doi: 10.1002/j.1460-2075.1987.tb04819.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Rubin M. R., Toth L. E., Patel M. D., D'Eustachio P., Nguyen-Huu M. C. A mouse homeo box gene is expressed in spermatocytes and embryos. Science. 1986 Aug 8;233(4764):663–667. doi: 10.1126/science.3726554. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Schneuwly S., Klemenz R., Gehring W. J. Redesigning the body plan of Drosophila by ectopic expression of the homoeotic gene Antennapedia. 1987 Feb 26-Mar 4Nature. 325(6107):816–818. doi: 10.1038/325816a0. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Simeone A., Mavilio F., Bottero L., Giampaolo A., Russo G., Faiella A., Boncinelli E., Peschle C. A human homoeo box gene specifically expressed in spinal cord during embryonic development. Nature. 1986 Apr 24;320(6064):763–765. doi: 10.1038/320763a0. [DOI] [PubMed] [Google Scholar]
  47. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Ullrich A., Gray A., Berman C., Dull T. J. Human beta-nerve growth factor gene sequence highly homologous to that of mouse. Nature. 1983 Jun 30;303(5920):821–825. doi: 10.1038/303821a0. [DOI] [PubMed] [Google Scholar]
  49. Utset M. F., Awgulewitsch A., Ruddle F. H., McGinnis W. Region-specific expression of two mouse homeo box genes. Science. 1987 Mar 13;235(4794):1379–1382. doi: 10.1126/science.2881353. [DOI] [PubMed] [Google Scholar]
  50. Wolgemuth D. J., Engelmyer E., Duggal R. N., Gizang-Ginsberg E., Mutter G. L., Ponzetto C., Viviano C., Zakeri Z. F. Isolation of a mouse cDNA coding for a developmentally regulated, testis-specific transcript containing homeo box homology. EMBO J. 1986 Jun;5(6):1229–1235. doi: 10.1002/j.1460-2075.1986.tb04351.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES