Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1994 Sep 25;22(19):3990–3996. doi: 10.1093/nar/22.19.3990

Novel HOX, POU and FKH genes expressed during bFGF-induced mesodermal differentiation in Xenopus.

M W King 1, M J Moore 1
PMCID: PMC308400  PMID: 7937122

Abstract

Cells from the cap of the animal hemisphere of the early Xenopus embryo are determined to form ectodermal lineages. When these cells are explanted and cultured in the presence of various growth factors a change in fate to cells of mesodermal lineage can be observed. Proteins of the fibroblast growth factor (FGF) family belong to this class of fate altering compounds. The ability of FGFs to change animal cap cell fate is in part due to an alteration in the program of genes expressed in these explanted cells. Several genes that are known to be pattern regulating in other systems have been shown to be induced by FGFs in the animal cap assay. We have utilized a PCR-based sib-selection and cloning protocol to identify a large number of cDNAs of the HOX, POU and FKH families that are present in animal caps very early during bFGF-induced mesodermal differentiation. A total of 11 different HOX, 7 POU and 4 FKH cDNAs were identified in an induced animal cap cDNA library. In several cases, pairs of highly related sequence variants were identified that presumably represent expression from the duplicated alleles of the ancestrally tetraploid Xenopus genome. In this report we characterize the temporal and spatial expression of three novel Xenopus genes during early development as well as during bFGF-induced mesodermal differentiation.

Full text

PDF
3990

Images in this article

Selected References

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

  1. Amaravadi L., King M. W. Characterization and expression of the Xenopus c-Myb homolog. Oncogene. 1994 Mar;9(3):971–974. [PubMed] [Google Scholar]
  2. Banker D. E., Bigler J., Eisenman R. N. The thyroid hormone receptor gene (c-erbA alpha) is expressed in advance of thyroid gland maturation during the early embryonic development of Xenopus laevis. Mol Cell Biol. 1991 Oct;11(10):5079–5089. doi: 10.1128/mcb.11.10.5079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bolce M. E., Hemmati-Brivanlou A., Harland R. M. XFKH2, a Xenopus HNF-3 alpha homologue, exhibits both activin-inducible and autonomous phases of expression in early embryos. Dev Biol. 1993 Dec;160(2):413–423. doi: 10.1006/dbio.1993.1317. [DOI] [PubMed] [Google Scholar]
  4. Chalepakis G., Fritsch R., Fickenscher H., Deutsch U., Goulding M., Gruss P. The molecular basis of the undulated/Pax-1 mutation. Cell. 1991 Sep 6;66(5):873–884. doi: 10.1016/0092-8674(91)90434-z. [DOI] [PubMed] [Google Scholar]
  5. Cho K. W., Blumberg B., Steinbeisser H., De Robertis E. M. Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell. 1991 Dec 20;67(6):1111–1120. doi: 10.1016/0092-8674(91)90288-a. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cho K. W., De Robertis E. M. Differential activation of Xenopus homeo box genes by mesoderm-inducing growth factors and retinoic acid. Genes Dev. 1990 Nov;4(11):1910–1916. doi: 10.1101/gad.4.11.1910. [DOI] [PubMed] [Google Scholar]
  7. Christian J. L., Olson D. J., Moon R. T. Xwnt-8 modifies the character of mesoderm induced by bFGF in isolated Xenopus ectoderm. EMBO J. 1992 Jan;11(1):33–41. doi: 10.1002/j.1460-2075.1992.tb05024.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dirksen M. L., Jamrich M. A novel, activin-inducible, blastopore lip-specific gene of Xenopus laevis contains a fork head DNA-binding domain. Genes Dev. 1992 Apr;6(4):599–608. doi: 10.1101/gad.6.4.599. [DOI] [PubMed] [Google Scholar]
  9. Fainsod A., Greunbaum Y. A chicken homeo box gene with developmentally regulated expression. FEBS Lett. 1989 Jul 3;250(2):381–385. doi: 10.1016/0014-5793(89)80760-4. [DOI] [PubMed] [Google Scholar]
  10. Finney M., Ruvkun G., Horvitz H. R. The C. elegans cell lineage and differentiation gene unc-86 encodes a protein with a homeodomain and extended similarity to transcription factors. Cell. 1988 Dec 2;55(5):757–769. doi: 10.1016/0092-8674(88)90132-8. [DOI] [PubMed] [Google Scholar]
  11. Frank D., Harland R. M. Localized expression of a Xenopus POU gene depends on cell-autonomous transcriptional activation and induction-dependent inactivation. Development. 1992 Jun;115(2):439–448. doi: 10.1242/dev.115.2.439. [DOI] [PubMed] [Google Scholar]
  12. Green J. B., Howes G., Symes K., Cooke J., Smith J. C. The biological effects of XTC-MIF: quantitative comparison with Xenopus bFGF. Development. 1990 Jan;108(1):173–183. doi: 10.1242/dev.108.1.173. [DOI] [PubMed] [Google Scholar]
  13. Green J. B., New H. V., Smith J. C. Responses of embryonic Xenopus cells to activin and FGF are separated by multiple dose thresholds and correspond to distinct axes of the mesoderm. Cell. 1992 Nov 27;71(5):731–739. doi: 10.1016/0092-8674(92)90550-v. [DOI] [PubMed] [Google Scholar]
  14. He X., Treacy M. N., Simmons D. M., Ingraham H. A., Swanson L. W., Rosenfeld M. G. Expression of a large family of POU-domain regulatory genes in mammalian brain development. Nature. 1989 Jul 6;340(6228):35–41. doi: 10.1038/340035a0. [DOI] [PubMed] [Google Scholar]
  15. Hinkley C. S., Martin J. F., Leibham D., Perry M. Sequential expression of multiple POU proteins during amphibian early development. Mol Cell Biol. 1992 Feb;12(2):638–649. doi: 10.1128/mcb.12.2.638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Häcker U., Grossniklaus U., Gehring W. J., Jäckle H. Developmentally regulated Drosophila gene family encoding the fork head domain. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8754–8758. doi: 10.1073/pnas.89.18.8754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jacobson A. G. Inductive processes in embryonic development. Science. 1966 Apr 1;152(3718):25–34. doi: 10.1126/science.152.3718.25. [DOI] [PubMed] [Google Scholar]
  18. Jessell T. M., Melton D. A. Diffusible factors in vertebrate embryonic induction. Cell. 1992 Jan 24;68(2):257–270. doi: 10.1016/0092-8674(92)90469-s. [DOI] [PubMed] [Google Scholar]
  19. Kappen C., Schughart K., Ruddle F. H. Early evolutionary origin of major homeodomain sequence classes. Genomics. 1993 Oct;18(1):54–70. doi: 10.1006/geno.1993.1426. [DOI] [PubMed] [Google Scholar]
  20. Kimelman D., Abraham J. A., Haaparanta T., Palisi T. M., Kirschner M. W. The presence of fibroblast growth factor in the frog egg: its role as a natural mesoderm inducer. Science. 1988 Nov 18;242(4881):1053–1056. doi: 10.1126/science.3194757. [DOI] [PubMed] [Google Scholar]
  21. Kimelman D., Maas A. Induction of dorsal and ventral mesoderm by ectopically expressed Xenopus basic fibroblast growth factor. Development. 1992 Jan;114(1):261–269. doi: 10.1242/dev.114.1.261. [DOI] [PubMed] [Google Scholar]
  22. King M. W., Blackwood E. M., Eisenman R. N. Expression of two distinct homologues of Xenopus Max during early development. Cell Growth Differ. 1993 Feb;4(2):85–92. [PubMed] [Google Scholar]
  23. Knöchel S., Lef J., Clement J., Klocke B., Hille S., Köster M., Knöchel W. Activin A induced expression of a fork head related gene in posterior chordamesoderm (notochord) of Xenopus laevis embryos. Mech Dev. 1992 Aug;38(2):157–165. doi: 10.1016/0925-4773(92)90007-7. [DOI] [PubMed] [Google Scholar]
  24. MacNicol A. M., Muslin A. J., Williams L. T. Raf-1 kinase is essential for early Xenopus development and mediates the induction of mesoderm by FGF. Cell. 1993 May 7;73(3):571–583. doi: 10.1016/0092-8674(93)90143-e. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Paterno G. D., Gillespie L. L., Dixon M. S., Slack J. M., Heath J. K. Mesoderm-inducing properties of INT-2 and kFGF: two oncogene-encoded growth factors related to FGF. Development. 1989 May;106(1):79–83. doi: 10.1242/dev.106.1.79. [DOI] [PubMed] [Google Scholar]
  27. Rosa F. M. Mix.1, a homeobox mRNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos. Cell. 1989 Jun 16;57(6):965–974. doi: 10.1016/0092-8674(89)90335-8. [DOI] [PubMed] [Google Scholar]
  28. Rosa F., Roberts A. B., Danielpour D., Dart L. L., Sporn M. B., Dawid I. B. Mesoderm induction in amphibians: the role of TGF-beta 2-like factors. Science. 1988 Feb 12;239(4841 Pt 1):783–785. doi: 10.1126/science.3422517. [DOI] [PubMed] [Google Scholar]
  29. Rosenfeld M. G. POU-domain transcription factors: pou-er-ful developmental regulators. Genes Dev. 1991 Jun;5(6):897–907. doi: 10.1101/gad.5.6.897. [DOI] [PubMed] [Google Scholar]
  30. Ruiz i Altaba A., Jessell T. M. Pintallavis, a gene expressed in the organizer and midline cells of frog embryos: involvement in the development of the neural axis. Development. 1992 Sep;116(1):81–93. doi: 10.1242/dev.116.Supplement.81. [DOI] [PubMed] [Google Scholar]
  31. Ruiz i Altaba A., Melton D. A. Interaction between peptide growth factors and homoeobox genes in the establishment of antero-posterior polarity in frog embryos. Nature. 1989 Sep 7;341(6237):33–38. doi: 10.1038/341033a0. [DOI] [PubMed] [Google Scholar]
  32. Rupp R. A., Weintraub H. Ubiquitous MyoD transcription at the midblastula transition precedes induction-dependent MyoD expression in presumptive mesoderm of X. laevis. Cell. 1991 Jun 14;65(6):927–937. doi: 10.1016/0092-8674(91)90545-a. [DOI] [PubMed] [Google Scholar]
  33. Sasaki H., Hogan B. L. Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development. 1993 May;118(1):47–59. doi: 10.1242/dev.118.1.47. [DOI] [PubMed] [Google Scholar]
  34. Slack J. M., Darlington B. G., Gillespie L. L., Godsave S. F., Isaacs H. V., Paterno G. D. The role of fibroblast growth factor in early Xenopus development. Development. 1989;107 (Suppl):141–148. doi: 10.1242/dev.107.Supplement.141. [DOI] [PubMed] [Google Scholar]
  35. Slack J. M., Darlington B. G., Heath J. K., Godsave S. F. Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. Nature. 1987 Mar 12;326(6109):197–200. doi: 10.1038/326197a0. [DOI] [PubMed] [Google Scholar]
  36. Slack J. M., Isaacs H. V., Darlington B. G. Inductive effects of fibroblast growth factor and lithium ion on Xenopus blastula ectoderm. Development. 1988 Jul;103(3):581–590. doi: 10.1242/dev.103.3.581. [DOI] [PubMed] [Google Scholar]
  37. Slack J. M. Regional biosynthetic markers in the early amphibian embryo. J Embryol Exp Morphol. 1984 Apr;80:289–319. [PubMed] [Google Scholar]
  38. Tadano T., Otani H., Taira M., Dawid I. B. Differential induction of regulatory genes during mesoderm formation in Xenopus laevis embryos. Dev Genet. 1993;14(3):204–211. doi: 10.1002/dvg.1020140307. [DOI] [PubMed] [Google Scholar]
  39. Tannahill D., Isaacs H. V., Close M. J., Peters G., Slack J. M. Developmental expression of the Xenopus int-2 (FGF-3) gene: activation by mesodermal and neural induction. Development. 1992 Jul;115(3):695–702. doi: 10.1242/dev.115.3.695. [DOI] [PubMed] [Google Scholar]
  40. Whitman M., Melton D. A. Involvement of p21ras in Xenopus mesoderm induction. Nature. 1992 May 21;357(6375):252–254. doi: 10.1038/357252a0. [DOI] [PubMed] [Google Scholar]
  41. von Dassow G., Schmidt J. E., Kimelman D. Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeo box gene. Genes Dev. 1993 Mar;7(3):355–366. doi: 10.1101/gad.7.3.355. [DOI] [PubMed] [Google Scholar]

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

RESOURCES