Abstract
In this paper, we show the conserved regulation of the homeodomain gene Distal-less-3 (Dlx-3) by analyzing the expression of a promoter from the Xenopus ortholog, Xdll-2, in transgenic mice. A 470-bp frog regulatory sequence confers appropriate expression on a lacZ reporter gene in the ectodermal component of structures derived from epithelial-mesenchymal interactions. Remarkably, this includes structures absent in Xenopus, such as the hair follicle and mammary gland, suggesting that conserved regulatory elements can be used to control the formation of structures peculiar to individual species. In addition, expression of Dlx-3 in developing limbs is highest at the most distal portion. This pattern is duplicated by the Xenopus promoter, indicating that this DNA may include sequences responsive to conserved proximodistal patterning signals in the vertebrate limb.
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- Awgulewitsch A., Jacobs D. Deformed autoregulatory element from Drosophila functions in a conserved manner in transgenic mice. Nature. 1992 Jul 23;358(6384):341–344. doi: 10.1038/358341a0. [DOI] [PubMed] [Google Scholar]
- Bulfone A., Kim H. J., Puelles L., Porteus M. H., Grippo J. F., Rubenstein J. L. The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos. Mech Dev. 1993 Mar;40(3):129–140. doi: 10.1016/0925-4773(93)90071-5. [DOI] [PubMed] [Google Scholar]
- Byrne C., Tainsky M., Fuchs E. Programming gene expression in developing epidermis. Development. 1994 Sep;120(9):2369–2383. doi: 10.1242/dev.120.9.2369. [DOI] [PubMed] [Google Scholar]
- Coelho C. N., Sumoy L., Kosher R. A., Upholt W. B. GHox-7: a chicken homeobox-containing gene expressed in a fashion consistent with a role in patterning events during embryonic chick limb development. Differentiation. 1992 Mar;49(2):85–92. doi: 10.1111/j.1432-0436.1992.tb00772.x. [DOI] [PubMed] [Google Scholar]
- Coelho C. N., Sumoy L., Rodgers B. J., Davidson D. R., Hill R. E., Upholt W. B., Kosher R. A. Expression of the chicken homeobox-containing gene GHox-8 during embryonic chick limb development. Mech Dev. 1991 Jun;34(2-3):143–154. doi: 10.1016/0925-4773(91)90051-7. [DOI] [PubMed] [Google Scholar]
- Cohen S. M., Brönner G., Küttner F., Jürgens G., Jäckle H. Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature. 1989 Mar 30;338(6214):432–434. doi: 10.1038/338432a0. [DOI] [PubMed] [Google Scholar]
- Cohen S. M., Jürgens G. Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development. EMBO J. 1989 Jul;8(7):2045–2055. doi: 10.1002/j.1460-2075.1989.tb03613.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dirksen M. L., Mathers P., Jamrich M. Expression of a Xenopus Distal-less homeobox gene involved in forebrain and cranio-facial development. Mech Dev. 1993 May;41(2-3):121–128. doi: 10.1016/0925-4773(93)90042-v. [DOI] [PubMed] [Google Scholar]
- Dirksen M. L., Morasso M. I., Sargent T. D., Jamrich M. Differential expression of a Distal-less homeobox gene Xdll-2 in ectodermal cell lineages. Mech Dev. 1994 Apr;46(1):63–70. doi: 10.1016/0925-4773(94)90038-8. [DOI] [PubMed] [Google Scholar]
- Dollé P., Price M., Duboule D. Expression of the murine Dlx-1 homeobox gene during facial, ocular and limb development. Differentiation. 1992 Mar;49(2):93–99. doi: 10.1111/j.1432-0436.1992.tb00773.x. [DOI] [PubMed] [Google Scholar]
- Ekker M., Akimenko M. A., Bremiller R., Westerfield M. Regional expression of three homeobox transcripts in the inner ear of zebrafish embryos. Neuron. 1992 Jul;9(1):27–35. doi: 10.1016/0896-6273(92)90217-2. [DOI] [PubMed] [Google Scholar]
- Gan L., Wessel G. M., Klein W. H. Regulatory elements from the related spec genes of Strongylocentrotus purpuratus yield different spatial patterns with a lacZ reporter gene. Dev Biol. 1990 Dec;142(2):346–359. doi: 10.1016/0012-1606(90)90355-m. [DOI] [PubMed] [Google Scholar]
- Hardy M. H. The secret life of the hair follicle. Trends Genet. 1992 Feb;8(2):55–61. doi: 10.1016/0168-9525(92)90350-d. [DOI] [PubMed] [Google Scholar]
- Izpisúa-Belmonte J. C., Falkenstein H., Dollé P., Renucci A., Duboule D. Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J. 1991 Aug;10(8):2279–2289. doi: 10.1002/j.1460-2075.1991.tb07764.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lawrence P. A., Morata G. Homeobox genes: their function in Drosophila segmentation and pattern formation. Cell. 1994 Jul 29;78(2):181–189. doi: 10.1016/0092-8674(94)90289-5. [DOI] [PubMed] [Google Scholar]
- MacKenzie A., Ferguson M. W., Sharpe P. T. Expression patterns of the homeobox gene, Hox-8, in the mouse embryo suggest a role in specifying tooth initiation and shape. Development. 1992 Jun;115(2):403–420. doi: 10.1242/dev.115.2.403. [DOI] [PubMed] [Google Scholar]
- Mackenzie A., Leeming G. L., Jowett A. K., Ferguson M. W., Sharpe P. T. The homeobox gene Hox 7.1 has specific regional and temporal expression patterns during early murine craniofacial embryogenesis, especially tooth development in vivo and in vitro. Development. 1991 Feb;111(2):269–285. doi: 10.1242/dev.111.2.269. [DOI] [PubMed] [Google Scholar]
- Malicki J., Cianetti L. C., Peschle C., McGinnis W. A human HOX4B regulatory element provides head-specific expression in Drosophila embryos. Nature. 1992 Jul 23;358(6384):345–347. doi: 10.1038/358345a0. [DOI] [PubMed] [Google Scholar]
- Martin P., Swanson G. J. Descriptive and experimental analysis of the epithelial remodellings that control semicircular canal formation in the developing mouse inner ear. Dev Biol. 1993 Oct;159(2):549–558. doi: 10.1006/dbio.1993.1263. [DOI] [PubMed] [Google Scholar]
- Martin P. Tissue patterning in the developing mouse limb. Int J Dev Biol. 1990 Sep;34(3):323–336. [PubMed] [Google Scholar]
- McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell. 1992 Jan 24;68(2):283–302. doi: 10.1016/0092-8674(92)90471-n. [DOI] [PubMed] [Google Scholar]
- Morasso M. I., Jamrich M., Sargent T. D. The homeodomain gene Xenopus Distal-less-like-2 (Xdll-2) is regulated by a conserved mechanism in amphibian and mammalian epidermis. Dev Biol. 1994 Mar;162(1):267–276. doi: 10.1006/dbio.1994.1084. [DOI] [PubMed] [Google Scholar]
- Oliver G., Sidell N., Fiske W., Heinzmann C., Mohandas T., Sparkes R. S., De Robertis E. M. Complementary homeo protein gradients in developing limb buds. Genes Dev. 1989 May;3(5):641–650. doi: 10.1101/gad.3.5.641. [DOI] [PubMed] [Google Scholar]
- Oliver G., Wright C. V., Hardwicke J., De Robertis E. M. A gradient of homeodomain protein in developing forelimbs of Xenopus and mouse embryos. Cell. 1988 Dec 23;55(6):1017–1024. doi: 10.1016/0092-8674(88)90246-2. [DOI] [PubMed] [Google Scholar]
- Papalopulu N., Kintner C. Xenopus Distal-less related homeobox genes are expressed in the developing forebrain and are induced by planar signals. Development. 1993 Mar;117(3):961–975. doi: 10.1242/dev.117.3.961. [DOI] [PubMed] [Google Scholar]
- Porteus M. H., Bulfone A., Ciaranello R. D., Rubenstein J. L. Isolation and characterization of a novel cDNA clone encoding a homeodomain that is developmentally regulated in the ventral forebrain. Neuron. 1991 Aug;7(2):221–229. doi: 10.1016/0896-6273(91)90260-7. [DOI] [PubMed] [Google Scholar]
- Price M., Lemaistre M., Pischetola M., Di Lauro R., Duboule D. A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature. 1991 Jun 27;351(6329):748–751. doi: 10.1038/351748a0. [DOI] [PubMed] [Google Scholar]
- Robinson G. W., Mahon K. A. Differential and overlapping expression domains of Dlx-2 and Dlx-3 suggest distinct roles for Distal-less homeobox genes in craniofacial development. Mech Dev. 1994 Dec;48(3):199–215. doi: 10.1016/0925-4773(94)90060-4. [DOI] [PubMed] [Google Scholar]
- Robinson G. W., Wray S., Mahon K. A. Spatially restricted expression of a member of a new family of murine Distal-less homeobox genes in the developing forebrain. New Biol. 1991 Dec;3(12):1183–1194. [PubMed] [Google Scholar]
- Sanes J. R., Rubenstein J. L., Nicolas J. F. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 1986 Dec 1;5(12):3133–3142. doi: 10.1002/j.1460-2075.1986.tb04620.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sargent T. D., Jamrich M., Dawid I. B. Cell interactions and the control of gene activity during early development of Xenopus laevis. Dev Biol. 1986 Mar;114(1):238–246. doi: 10.1016/0012-1606(86)90399-4. [DOI] [PubMed] [Google Scholar]
- Simeone A., Acampora D., Pannese M., D'Esposito M., Stornaiuolo A., Gulisano M., Mallamaci A., Kastury K., Druck T., Huebner K. Cloning and characterization of two members of the vertebrate Dlx gene family. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2250–2254. doi: 10.1073/pnas.91.6.2250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilkinson D. G., Nieto M. A. Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 1993;225:361–373. doi: 10.1016/0076-6879(93)25025-w. [DOI] [PubMed] [Google Scholar]