Advertisement
JOURNAL ARTICLES
A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila
K.P. Rehorn, H. Thelen, A.M. Michelson, R. Reuter
Development 1996 122: 4023-4031;

Summary

In vertebrates, transcriptional regulators of the GATA family appear to have a conserved function in differentiation and organ development. GATA-1, −2 and −3 are required for different aspects of hematopoiesis, while GATA-4, −5 and −6 are expressed in various organs of endodermal origin, such as intestine and liver, and are implicated in endodermal differentiation. Here we report that the Drosophila gene serpent (srp) encodes the previously described GATA factor ABF. The multiple functions of srp in Drosophila suggest that it is an ortholog of the entire vertebrate Gata family. srp is required for the differentiation and morphogenesis of the endodermal gut. Here we show that it is also essential for Drosophila hematopoiesis and for the formation of the fat body, the insect organ analogous to the liver. These findings imply that some aspects of the molecular mechanisms underlying blood cell development as well as endodermal differentiation are early acquisitions of metazoan evolution and may be common to most higher animals.

Reference

    1. Abel T.,
    2. Michelson A. M.,
    3. Maniatis T.
    (1993) A Drosophila GATA family member that binds to Adh regulatory sequences is expressed in the developing fat body. Development 119, 623–633
    OpenUrlAbstract/FREE Full Text
    1. Arceci R. J.,
    2. King A. A. J.,
    3. Simon M. C.,
    4. Orkin S. H.,
    5. Wilson D. B.
    (1993) Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol. Cell. Biol 13, 2235–2246
    OpenUrlAbstract/FREE Full Text
    1. Borkowski O. M. D.,
    2. Brown N. H.,
    3. Bate M.
    (1995) Anterior-posterior subdivision and the diversification of the mesoderm in Drosophila. Development 121, 4183–4193
    OpenUrlAbstract
    1. Brönner G.,
    2. Chu-la Graff Q.,
    3. Doe C. Q.,
    4. Cohen B.,
    5. Weigel D.,
    6. Taubert H.,
    7. Jäckle H.
    (1994) Sp1/egr-like zinc-finger protein required for endoderm specification and germ-layer formation in Drosophila. Nature 369, 664–668
    OpenUrlCrossRefPubMed
    1. Cavener D. R.
    (1987) Comparison of the consensus flanking translational start sites in Drosophila and vertebrates. Nucl. Acids Res 15, 1353–1361
    OpenUrlAbstract/FREE Full Text
    1. Cooley L.,
    2. Kelley R.,
    3. Spradling A.
    (1988) Insertional mutagenesis of the Drosophila genome with single P elements. Science 329, 1121–1128
    OpenUrl
    1. Evans T.,
    2. Felsenfeld G.
    (1989) The erythroid-specific transcription factor Eryf1: a new finger protein. Cell 58, 877–885
    OpenUrlCrossRefPubMedWeb of Science
    1. Felsenstein J.
    (1988) Phylogenies from molecular sequences: inference and reliability. Ann. Rev. Genet 22, 521–565
    OpenUrlCrossRefPubMedWeb of Science
    1. Fu Y.-H.,
    2. Marzluf G. A.
    (1990) nit-2, the major nitrogen regulatory gene of Neurosporacrassa, encodes a protein with putative zinc finger DNA-binding domain. Mol. Cell. Biol 10, 1056–1065
    OpenUrlAbstract/FREE Full Text
    1. Haas H.,
    2. Bauer B.,
    3. Redl B.,
    4. Stöffler G.,
    5. Marzluf G. A.
    (1995) Molecular cloning and analysis of nre, the major nitrogen regulatory gene of Penicillium chrysogenum. Curr. Genet 27, 150–158
    OpenUrlCrossRefPubMed
    1. Hawkins M. G.,
    2. McGhee J. D.
    (1995) elt-2, a second GATA factor from the nematode Caenorhabditis elegans. J. Biol. Chem 270, 14666–14671
    OpenUrlAbstract/FREE Full Text
    1. Hoshizaki D. K.,
    2. Blackburn T.,
    3. Price C.,
    4. Ghosh M.,
    5. Miles K.,
    6. Ragucci M.,
    7. Sweis R.
    (1994) Embryonic fat-cell lineage in Drosophila melanogaster. Development 120, 2489–2499
    OpenUrlAbstract/FREE Full Text
    1. Kelley C.,
    2. Blumberg H.,
    3. Zon L. I.,
    4. Evans T.
    (1993) GATA-4 is a novel transcription factor expressed in endocardium of the developing heart. Development 118, 817–827
    OpenUrlAbstract
    1. Ko L. J.,
    2. Yamamoto M.,
    3. Leonard M. W.,
    4. George K. M.,
    5. Ting P.,
    6. Engel J. D.
    (1991) Murine and human T-lymphocyte GATA-3 factors mediate transcription through a cis-regulatory element within the human T-cell receptorgene enhancer. Mol. Cell. Biol 11, 2778–2784
    OpenUrlAbstract/FREE Full Text
    1. Kudla B.,
    2. Caddick M. X.,
    3. Langdon T.,
    4. Martinez-Rossi N. M.,
    5. Bennett C. F.,
    6. Sibley S.,
    7. Davies R. W.,
    8. Arst H. N.
    (1990) The regulatory gene areA mediating nitrogen metabolite repression in Aspergillusnidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. EMBO J 9, 1355–1364
    OpenUrlPubMedWeb of Science
    1. Laski F. A.,
    2. Rio D. C.,
    3. Rubin G. M.
    (1986) Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44, 7–19
    OpenUrlCrossRefPubMedWeb of Science
    1. Laverriere A. C.,
    2. MacNeill C.,
    3. Mueller C.,
    4. Poelmann R. E.,
    5. Burch J. B. E.,
    6. Evans T.
    (1994) GATA-4/5/6, a subfamily of three transcription factors transcribed in developing heart and gut. J. Biol. Chem 269, 23177–23184
    OpenUrlAbstract/FREE Full Text
    1. Lin W.-H.,
    2. Huang L.-H.,
    3. Yeh J.-Y.,
    4. Hoheisel J.,
    5. Lehrach H.,
    6. Sun Y. H.,
    7. Tsai S.-F.
    (1995) Expression of a Drosophila GATA transcription factor in multiple tissues in the developing embryo. J. Biol. Chem 270, 25150–25158
    OpenUrlAbstract/FREE Full Text
    1. Lossky M.,
    2. Wensink P. C.
    (1995) Regulation of Drosophila yolk protein genes by an ovary-specific GATA factor. Mol. Cell. Biol 15, 6943–6952
    OpenUrlAbstract/FREE Full Text
    1. Minehart P. L.,
    2. Magasanik B.
    (1991) Sequence and expression of GLN3, a positive nitrogen regulatory gene of Saccharomyces cerevisiae encoding a protein with a putative zinc finger DNA-binding domain. Mol. Cell Biol 11, 6216–6228
    OpenUrlAbstract/FREE Full Text
    1. Nelson R. E.,
    2. Fessler L. I.,
    3. Takagi Y.,
    4. Blumberg B.,
    5. Keene D. R.,
    6. Olson P. F.,
    7. Parker C. G.,
    8. Fessler J. H.
    (1994) Peroxidasin: a novel enzyme-matrix protein of Drosophila development. EMBO J 13, 3438–3447
    OpenUrlPubMedWeb of Science
    1. Omichinski J. G.,
    2. Clore G. M.,
    3. Schaad O.,
    4. Felsenfeld G.,
    5. Trainor C.,
    6. Appella E.,
    7. Stahl S. J.,
    8. Gronenborn A. M.
    (1993) NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science 261, 438–446
    OpenUrlAbstract/FREE Full Text
    1. Pevny L.,
    2. Simon M. C.,
    3. Robertson E.,
    4. Klein W. H.,
    5. Tsai S.-F.,
    6. D'Agati V.,
    7. Orkin S. H.,
    8. Costantini F.
    (1991) Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 349, 257–260
    OpenUrlCrossRefPubMedWeb of Science
    1. Ramain P.,
    2. Heitzler P.,
    3. Haenlin M.,
    4. Simpson P.
    (1993) pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc finger protein with homology to the vertebrate transcription factor GATA-1. Development 119, 1277–1291
    OpenUrlAbstract
    1. Reuter R.
    (1994) The gene serpent has homeotic properties and specifies endoderm versus ectoderm within the Drosophila gut. Development 120, 1123–1135
    OpenUrlAbstract
    1. Reuter R.,
    2. Grunewald B.,
    3. Leptin M.
    (1993) A role for the mesoderm in endodermal migration and morphogenesis in Drosophila. Development 119, 1135–1145
    OpenUrlAbstract
    1. Reuter G.,
    2. Hoffmann G.,
    3. Dorn R.,
    4. Gausz J.,
    5. Saumweber H.
    (1993) Construction and characterization of a TM3 balancer carrying P[(ry[+])2-3] as a stable transposase source. Dros. Inf. Serv 72, 78–.
    OpenUrl
    1. Reuter R.,
    2. Leptin M.
    (1994) Interacting functions of snail, twist and huckebein during the early development of germ layers in Drosophila. Development 120, 1137–1150
    OpenUrlAbstract
    1. Soudais C.,
    2. Bielinska M.,
    3. Keikinheimo M.,
    4. MacArthur C. A.,
    5. Narita N.,
    6. Saffitz J. E.,
    7. Simon M. C.,
    8. Leiden J. M.,
    9. Wilson D. B.
    (1995) Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 121, 3877–3888
    OpenUrlAbstract
    1. Spieth J.,
    2. Shim Y. H.,
    3. Lea K.,
    4. Conrad R.,
    5. Blumenthal T.
    (1991) elt-1, an embryologically expressed Caenorhabditis elegans gene homologous to the GATA transcription factor family. Mol. Cell. Biol 11, 4651–4659
    OpenUrlAbstract/FREE Full Text
    1. Tamkun J. W.,
    2. Deuring R.,
    3. Scott M. P.,
    4. Kissinger M.,
    5. Pattatucci A. M.,
    6. Kaufman T. C.,
    7. Kennison J. A.
    (1992) brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68, 561–572
    OpenUrlCrossRefPubMedWeb of Science
    1. Tamura S.,
    2. Wang X.-H.,
    3. Maeda M.,
    4. Futai M.
    (1993) Gastric DNA-binding proteins recognize upstream sequence motifs of parietal cell-specific genes. Proc. Natl. Acad. Sci. USA 90, 10876–10880
    OpenUrlAbstract/FREE Full Text
    1. Tautz D.,
    2. Pfeifle C.
    (1989) 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 98, 81–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Tepass U.,
    2. Fessler L. I.,
    3. Aziz A.,
    4. Hartenstein V.
    (1994) Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120, 1829–1837
    OpenUrlAbstract
    1. Tsai F. Y.,
    2. Keller G.,
    3. Kuo F. C.,
    4. Weiss M.,
    5. Chen J. Z.,
    6. Rosenblatt M.,
    7. Alt F. W.,
    8. Orkin S. H.
    (1994) An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371, 221–226
    OpenUrlCrossRefPubMedWeb of Science
    1. Voisard C.,
    2. Weang J.,
    3. McEvoy J. L.,
    4. Xu P.,
    5. Leong S. A.
    (1993) urbS1, a gene regulating siderophore biosynthesis in Ustilago maydis, encodes a protein similar to the erythroid transcription factor GATA-1. Mol. Cell Biol 13, 7091–7100
    OpenUrlAbstract/FREE Full Text
    1. Weigel D.,
    2. Jurgens G.,
    3. Klingler M.,
    4. Jäckle H.
    (1990) Two gap genes mediate maternal terminal pattern information in Drosophila. Science 248, 495–498
    OpenUrlAbstract/FREE Full Text
    1. Winick J.,
    2. Abel T.,
    3. Leonard M. W.,
    4. Michelson A. M.,
    5. Chardon-Loriaux I.,
    6. Holmgren R. A.,
    7. Maniatis T.,
    8. Engel J. D.
    (1993) A GATA family transcription factor is expressed along the embryonic dorsoventral axis in Drosophila melanogaster. Development 119, 1055–1065
    OpenUrlAbstract
    1. Yamamoto M.,
    2. Ko L. J.,
    3. Leonard M. W.,
    4. Beug H.,
    5. Orkin S. H.,
    6. Engel J. D.
    (1990) Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev 4, 1650–1662
    OpenUrlAbstract/FREE Full Text
    1. Zon L. I.,
    2. Tsai S. F.,
    3. Burgess S.,
    4. Matsudaira P.,
    5. Bruns G. A.,
    6. Orkin S. H.
    (1990) The major human erythroid DNA-binding protein (GF-1): primary sequence and localization of the gene to the X chromosome. Proc. Natl. Acad. Sci. USA 87, 668–672
    OpenUrlAbstract/FREE Full Text
    1. Zon L. I.,
    2. Mather C.,
    3. Burgess S.,
    4. Bolce M. E.,
    5. Harland R. M.,
    6. Orkin S. H.
    (1991) Expression of GATA-binding proteins during embryonic development in Xenopus laevis. Proc. Natl. Acad. Sci. USA 88, 10642–10646
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
JOURNAL ARTICLES
A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila
K.P. Rehorn, H. Thelen, A.M. Michelson, R. Reuter
Development 1996 122: 4023-4031;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

A new society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.

Upcoming special issue: call for papers

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.