Abstract
Two zygotic genes, twist and snail, are indispensable for the correct establishment of the mesoderm primordium in the early Drosophila embryo. They are also needed for morphogenesis and differentiation of the mesoderm. Both genes code for transcription factors with different, albeit complementary, functions. Therefore, to understand the early development of the mesoderm, it will be necessary to identify and study the genes regulated by twist and snail. We have searched for downstream genes using a subtractive cDNA library enriched in sequences expressed in the mesoderm. We have isolated sequences that correspond to 13 novel early mesoderm genes. These novel genes show a variety of expression patterns and also differ in their dependence on twist and snail functions. This indicates that the regulation of early gene activity in the mesoderm is more complex than previously thought.
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- Anderson K. V., Bokla L., Nüsslein-Volhard C. Establishment of dorsal-ventral polarity in the Drosophila embryo: the induction of polarity by the Toll gene product. Cell. 1985 Oct;42(3):791–798. doi: 10.1016/0092-8674(85)90275-2. [DOI] [PubMed] [Google Scholar]
- Anderson K. V., Jürgens G., Nüsslein-Volhard C. Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell. 1985 Oct;42(3):779–789. doi: 10.1016/0092-8674(85)90274-0. [DOI] [PubMed] [Google Scholar]
- Arora K., Nüsslein-Volhard C. Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes. Development. 1992 Apr;114(4):1003–1024. doi: 10.1242/dev.114.4.1003. [DOI] [PubMed] [Google Scholar]
- Azpiazu N., Frasch M. tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev. 1993 Jul;7(7B):1325–1340. doi: 10.1101/gad.7.7b.1325. [DOI] [PubMed] [Google Scholar]
- Bodmer R., Jan L. Y., Jan Y. N. A new homeobox-containing gene, msh-2, is transiently expressed early during mesoderm formation of Drosophila. Development. 1990 Nov;110(3):661–669. doi: 10.1242/dev.110.3.661. [DOI] [PubMed] [Google Scholar]
- Boulay J. L., Dennefeld C., Alberga A. The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. 1987 Nov 26-Dec 2Nature. 330(6146):395–398. doi: 10.1038/330395a0. [DOI] [PubMed] [Google Scholar]
- Brown N. H., Kafatos F. C. Functional cDNA libraries from Drosophila embryos. J Mol Biol. 1988 Sep 20;203(2):425–437. doi: 10.1016/0022-2836(88)90010-1. [DOI] [PubMed] [Google Scholar]
- Costa M., Wilson E. T., Wieschaus E. A putative cell signal encoded by the folded gastrulation gene coordinates cell shape changes during Drosophila gastrulation. Cell. 1994 Mar 25;76(6):1075–1089. doi: 10.1016/0092-8674(94)90384-0. [DOI] [PubMed] [Google Scholar]
- Erdélyi M., Szabad J. Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. I. Mutations on the third chromosome. Genetics. 1989 May;122(1):111–127. doi: 10.1093/genetics/122.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fortini M. E., Lai Z. C., Rubin G. M. The Drosophila zfh-1 and zfh-2 genes encode novel proteins containing both zinc-finger and homeodomain motifs. Mech Dev. 1991 Jun;34(2-3):113–122. doi: 10.1016/0925-4773(91)90048-b. [DOI] [PubMed] [Google Scholar]
- Gasch A., Hinz U., Leiss D., Renkawitz-Pohl R. The expression of beta 1 and beta 3 tubulin genes of Drosophila melanogaster is spatially regulated during embryogenesis. Mol Gen Genet. 1988 Jan;211(1):8–16. doi: 10.1007/BF00338387. [DOI] [PubMed] [Google Scholar]
- Gerttula S., Jin Y. S., Anderson K. V. Zygotic expression and activity of the Drosophila Toll gene, a gene required maternally for embryonic dorsal-ventral pattern formation. Genetics. 1988 May;119(1):123–133. doi: 10.1093/genetics/119.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grau Y., Carteret C., Simpson P. Mutations and Chromosomal Rearrangements Affecting the Expression of Snail, a Gene Involved in Embryonic Patterning in DROSOPHILA MELANOGASTER. Genetics. 1984 Oct;108(2):347–360. doi: 10.1093/genetics/108.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kosman D., Ip Y. T., Levine M., Arora K. Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo. Science. 1991 Oct 4;254(5028):118–122. doi: 10.1126/science.1925551. [DOI] [PubMed] [Google Scholar]
- Lai Z. C., Fortini M. E., Rubin G. M. The embryonic expression patterns of zfh-1 and zfh-2, two Drosophila genes encoding novel zinc-finger homeodomain proteins. Mech Dev. 1991 Jun;34(2-3):123–134. doi: 10.1016/0925-4773(91)90049-c. [DOI] [PubMed] [Google Scholar]
- Lai Z. C., Rushton E., Bate M., Rubin G. M. Loss of function of the Drosophila zfh-1 gene results in abnormal development of mesodermally derived tissues. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4122–4126. doi: 10.1073/pnas.90.9.4122. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Langer-Safer P. R., Levine M., Ward D. C. Immunological method for mapping genes on Drosophila polytene chromosomes. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4381–4385. doi: 10.1073/pnas.79.14.4381. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leptin M., Casal J., Grunewald B., Reuter R. Mechanisms of early Drosophila mesoderm formation. Dev Suppl. 1992:23–31. [PubMed] [Google Scholar]
- Leptin M. twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev. 1991 Sep;5(9):1568–1576. doi: 10.1101/gad.5.9.1568. [DOI] [PubMed] [Google Scholar]
- Lilly B., Zhao B., Ranganayakulu G., Paterson B. M., Schulz R. A., Olson E. N. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science. 1995 Feb 3;267(5198):688–693. doi: 10.1126/science.7839146. [DOI] [PubMed] [Google Scholar]
- Natzle J. E., McCarthy B. J. Regulation of Drosophila alpha- and beta-tubulin genes during development. Dev Biol. 1984 Jul;104(1):187–198. doi: 10.1016/0012-1606(84)90047-2. [DOI] [PubMed] [Google Scholar]
- Pignoni F., Baldarelli R. M., Steingrímsson E., Diaz R. J., Patapoutian A., Merriam J. R., Lengyel J. A. The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell. 1990 Jul 13;62(1):151–163. doi: 10.1016/0092-8674(90)90249-e. [DOI] [PubMed] [Google Scholar]
- Rao Y., Vaessin H., Jan L. Y., Jan Y. N. Neuroectoderm in Drosophila embryos is dependent on the mesoderm for positioning but not for formation. Genes Dev. 1991 Sep;5(9):1577–1588. doi: 10.1101/gad.5.9.1577. [DOI] [PubMed] [Google Scholar]
- Ray R. P., Arora K., Nüsslein-Volhard C., Gelbart W. M. The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development. 1991 Sep;113(1):35–54. doi: 10.1242/dev.113.1.35. [DOI] [PubMed] [Google Scholar]
- Reuter R., Leptin M. Interacting functions of snail, twist and huckebein during the early development of germ layers in Drosophila. Development. 1994 May;120(5):1137–1150. doi: 10.1242/dev.120.5.1137. [DOI] [PubMed] [Google Scholar]
- Roth S., Stein D., Nüsslein-Volhard C. A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell. 1989 Dec 22;59(6):1189–1202. doi: 10.1016/0092-8674(89)90774-5. [DOI] [PubMed] [Google Scholar]
- Shishido E., Higashijima S., Emori Y., Saigo K. Two FGF-receptor homologues of Drosophila: one is expressed in mesodermal primordium in early embryos. Development. 1993 Feb;117(2):751–761. doi: 10.1242/dev.117.2.751. [DOI] [PubMed] [Google Scholar]
- Simpson P. Maternal-Zygotic Gene Interactions during Formation of the Dorsoventral Pattern in Drosophila Embryos. Genetics. 1983 Nov;105(3):615–632. doi: 10.1093/genetics/105.3.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
- St Johnston R. D., Gelbart W. M. Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J. 1987 Sep;6(9):2785–2791. doi: 10.1002/j.1460-2075.1987.tb02574.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tamkun J. W., Deuring R., Scott M. P., Kissinger M., Pattatucci A. M., Kaufman T. C., Kennison J. A. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell. 1992 Feb 7;68(3):561–572. doi: 10.1016/0092-8674(92)90191-e. [DOI] [PubMed] [Google Scholar]
- Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
- Thisse B., Stoetzel C., Gorostiza-Thisse C., Perrin-Schmitt F. Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J. 1988 Jul;7(7):2175–2183. doi: 10.1002/j.1460-2075.1988.tb03056.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thisse B., el Messal M., Perrin-Schmitt F. The twist gene: isolation of a Drosophila zygotic gene necessary for the establishment of dorsoventral pattern. Nucleic Acids Res. 1987 Apr 24;15(8):3439–3453. doi: 10.1093/nar/15.8.3439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang Z., Brown D. D. A gene expression screen. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11505–11509. doi: 10.1073/pnas.88.24.11505. [DOI] [PMC free article] [PubMed] [Google Scholar]