Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1987 Oct;6(10):2965–2975. doi: 10.1002/j.1460-2075.1987.tb02602.x

Specific expression of the Hox 1.3 homeo box gene in murine embryonic structures originating from or induced by the mesoderm.

C Dony 1, P Gruss 1
PMCID: PMC553733  PMID: 2891502

Abstract

The murine Hox 1.3 homeo box-containing gene is expressed largely in mesoderm-derived or mesoderm-induced embryonal structures, as evidenced by in situ hybridization techniques. Expression is spatially limited to the thoracic region, specifically to components of segmental origin such as embryonal ribs and vertebrae and their precursors such as the equivalent sclerotomes, somites and somatic condensations. In addition, expression can be found in parts of embryonal lung, stomach tissue, gut and kidney, tissues whose formation is based on induction of region-specific mesoderm, as well as in some ectoderm-derived tissues. The expression is temporally controlled for the transcripts and can only be detected while the thoracic structures are being formed (days 8-13), but not at day 18 of gestation when the embryo is mature. These data suggest a role of Hox 1.3 gene in the generation of tissues derived from or induced by the embryonal mesoderm.

Full text

PDF
2968

Images in this article

2966Fig. 1.
on p.2966
2967Fig. 2.
on p.2967
2968Fig. 3.
on p.2968
2969Fig. 4.
on p.2969
2970Fig. 5.
on p.2970
2971Fig. 6.
on p.2971
2972Fig. 7.
on p.2972
2973Fig. 8.
on p.2973

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. Boncinelli E., Simeone A., La Volpe A., Faiella A., Fidanza V., Acampora D., Scotto L. Human cDNA clones containing homeo box sequences. Cold Spring Harb Symp Quant Biol. 1985;50:301–306. doi: 10.1101/sqb.1985.050.01.038. [DOI] [PubMed] [Google Scholar]
  3. Bopp D., Burri M., Baumgartner S., Frigerio G., Noll M. Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila. Cell. 1986 Dec 26;47(6):1033–1040. doi: 10.1016/0092-8674(86)90818-4. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Carrasco A. E., McGinnis W., Gehring W. J., De Robertis E. M. Cloning of an X. laevis gene expressed during early embryogenesis coding for a peptide region homologous to Drosophila homeotic genes. Cell. 1984 Jun;37(2):409–414. doi: 10.1016/0092-8674(84)90371-4. [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. Cox K. H., DeLeon D. V., Angerer L. M., Angerer R. C. Detection of mrnas in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev Biol. 1984 Feb;101(2):485–502. doi: 10.1016/0012-1606(84)90162-3. [DOI] [PubMed] [Google Scholar]
  10. Curran T., Peters G., Van Beveren C., Teich N. M., Verma I. M. FBJ murine osteosarcoma virus: identification and molecular cloning of biologically active proviral DNA. J Virol. 1982 Nov;44(2):674–682. doi: 10.1128/jvi.44.2.674-682.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  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. Fjose A., McGinnis W. J., Gehring W. J. Isolation of a homoeo box-containing gene from the engrailed region of Drosophila and the spatial distribution of its transcripts. Nature. 1985 Jan 24;313(6000):284–289. doi: 10.1038/313284a0. [DOI] [PubMed] [Google Scholar]
  15. Flint O. P., Ede D. A., Wilby O. K., Proctor J. Control of somite number in normal and amputated mutant mouse embryos: an experimental and a theoretical analysis. J Embryol Exp Morphol. 1978 Jun;45:189–202. [PubMed] [Google Scholar]
  16. Frigerio G., Burri M., Bopp D., Baumgartner S., Noll M. Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network. Cell. 1986 Dec 5;47(5):735–746. doi: 10.1016/0092-8674(86)90516-7. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Hafen E., Levine M., Garber R. L., Gehring W. J. An improved in situ hybridization method for the detection of cellular RNAs in Drosophila tissue sections and its application for localizing transcripts of the homeotic Antennapedia gene complex. EMBO J. 1983;2(4):617–623. doi: 10.1002/j.1460-2075.1983.tb01472.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. 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]
  24. 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]
  25. Lipton B. H., Jacobson A. G. Analysis of normal somite development. Dev Biol. 1974 May;38(1):73–90. doi: 10.1016/0012-1606(74)90260-7. [DOI] [PubMed] [Google Scholar]
  26. Macdonald P. M., Ingham P., Struhl G. Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box. Cell. 1986 Dec 5;47(5):721–734. doi: 10.1016/0092-8674(86)90515-5. [DOI] [PubMed] [Google Scholar]
  27. Macdonald P. M., Struhl G. A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature. 1986 Dec 11;324(6097):537–545. doi: 10.1038/324537a0. [DOI] [PubMed] [Google Scholar]
  28. Martin G. R. Nomenclature for homoeobox-containing genes. Nature. 1987 Jan 1;325(6099):21–22. doi: 10.1038/325021b0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
  32. 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]
  33. Meier S., Tam P. P. Metameric pattern development in the embryonic axis of the mouse. I. Differentiation of the cranial segments. Differentiation. 1982;21(2):95–108. doi: 10.1111/j.1432-0436.1982.tb01202.x. [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. Noden D. M. The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am J Anat. 1983 Nov;168(3):257–276. doi: 10.1002/aja.1001680302. [DOI] [PubMed] [Google Scholar]
  36. O'Rahilly R. The timing and sequence of events in the development of the human digestive system and associated structures during the embryonic period proper. Anat Embryol (Berl) 1978 Jun 2;153(2):123–136. doi: 10.1007/BF00343369. [DOI] [PubMed] [Google Scholar]
  37. Pearson M., Elsdale T. Somitogenesis in amphibian embryos. I. Experimental evidence for an interaction between two temporal factors in the specification of somite pattern. J Embryol Exp Morphol. 1979 Jun;51:27–50. [PubMed] [Google Scholar]
  38. Poole S. J., Kauvar L. M., Drees B., Kornberg T. The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell. 1985 Jan;40(1):37–43. doi: 10.1016/0092-8674(85)90306-x. [DOI] [PubMed] [Google Scholar]
  39. Porter S. D., Smith M. Homoeo-domain homology in yeast MAT alpha 2 is essential for repressor activity. Nature. 1986 Apr 24;320(6064):766–768. doi: 10.1038/320766a0. [DOI] [PubMed] [Google Scholar]
  40. RUDNICK D. Development of the digestive tube and its derivatives. Ann N Y Acad Sci. 1952 Aug 8;55(2):109–116. doi: 10.1111/j.1749-6632.1952.tb26526.x. [DOI] [PubMed] [Google Scholar]
  41. Regulski M., Harding K., Kostriken R., Karch F., Levine M., McGinnis W. Homeo box genes of the Antennapedia and bithorax complexes of Drosophila. Cell. 1985 Nov;43(1):71–80. doi: 10.1016/0092-8674(85)90013-3. [DOI] [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. Scott M. P., Weiner A. J. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4115–4119. doi: 10.1073/pnas.81.13.4115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Spooner B. S., Wessells N. K. Mammalian lung development: interactions in primordium formation and bronchial morphogenesis. J Exp Zool. 1970 Dec;175(4):445–454. doi: 10.1002/jez.1401750404. [DOI] [PubMed] [Google Scholar]
  45. Strickland S., Mahdavi V. The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell. 1978 Oct;15(2):393–403. doi: 10.1016/0092-8674(78)90008-9. [DOI] [PubMed] [Google Scholar]
  46. Tam P. P., Meier S., Jacobson A. G. Differentiation of the metameric pattern in the embryonic axis of the mouse. II. Somitomeric organization of the presomitic mesoderm. Differentiation. 1982;21(2):109–122. doi: 10.1111/j.1432-0436.1982.tb01203.x. [DOI] [PubMed] [Google Scholar]
  47. Tam P. P., Meier S. The establishment of a somitomeric pattern in the mesoderm of the gastrulating mouse embryo. Am J Anat. 1982 Jul;164(3):209–225. doi: 10.1002/aja.1001640303. [DOI] [PubMed] [Google Scholar]
  48. Tam P. P. The control of somitogenesis in mouse embryos. J Embryol Exp Morphol. 1981 Oct;65 (Suppl):103–128. [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. Wessells N. K. Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. J Exp Zool. 1970 Dec;175(4):455–466. doi: 10.1002/jez.1401750405. [DOI] [PubMed] [Google Scholar]
  51. 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]
  52. Youn B. W., Keller R. E., Malacinski G. M. An atlas of notochord and somite morphogenesis in several anuran and urodelean amphibians. J Embryol Exp Morphol. 1980 Oct;59:223–247. [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES