Induction of labial expression in the Drosophila endoderm: response elements for dpp signalling and for autoregulation

G. Tremml; M. Bienz

Summary

Extracellular signal proteins induce the homeotic gene labial (lab) to high levels of localised expression in the endoderm of Drosophila embryos. We aimed to identify cis-regulatory elements within the lab gene that respond to this induction by analysing the activity of stably integrated reporter gene constructs. Dissection of lab 5′ flanking sequences reveals two types of response elements. One of these mediates lab dependent activity, providing evidence that lab induction in the endoderm is autoregulatory. The other element, to a large extent independent of lab function, responds to decapentaplegic (dpp), a signal molecule related to mammalian TGF-beta. Our evidence suggests that lab induction in the endoderm reflects coordinate action of two distinct factors one of which may be lab protein itself, and another whose localised activity or expression in the midgut depends on the dpp signal.

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2. Lawrence P. A.
(1985). Parasegments and compartments in the Drosophila embryo. Nature 313, 639–642
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(1990). The transforming growth factor-β family. Ann. Rev. Cell Biol. 6, 597–641
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2. Vale W. W.
(1991). Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65, 973–982
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2. Fjose A.,
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2. Reuter R.,
3. Scott M. P.,
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2. Admon A.,
3. Patel N.,
4. Tjian R.
(1990). The Drosophila Fos-related AP-1 protein is a developmentally regulated transcription factor. Genes Dev. 4, 822–834
1. Demerec M.
1. Poulson D. F.
(1950). Histogenesis, organogenesis, and differentiation in the embryo of Drosophila melanogaster Meigen. In The Biology of Drosophila, (ed. Demerec M.), pp. 168–274, New York: Hafner.
1. Qian S.,
2. Capovilla M.,
3. Pirotta V.
(1991). The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. EMBO J. 10, 1415–1425
1. Reinitz J.,
2. Levine M.
(1990). Control of the initiation of homeotic gene expression by the gap genes giant and tailless. Dev. Biol. 140, 57–72
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2. Panganiban G. E. F.,
3. Hoffmann F. M.,
4. Scott M. P.
(1990). Homeotic genes regulate the expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development 110, 1031–1040
1. Rijsewijk F.,
2. Schuerman M.,
3. Wagenaar E.,
4. Parren P.,
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2. Karsenty G.,
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2. Hoffmann F. M.,
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2. Ghysen A.
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2. Bienz M.
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2. Bienz M.
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2. Kaufman T. C.
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[1] Akam M.
(1987). The molecular basis for metameric pattern in the Drosophila embryo. Development 101, 1–22

[2] Akam M.

[3] Attisano L.,
Wrana J. L.,
Cheifetz S.,
Massagué J.
(1992). Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 68, 97–108

[4] Attisano L.,

[5] Wrana J. L.,

[6] Cheifetz S.,

[7] Massagué J.

[8] Baker N.
(1987). Molecular cloning of sequences from wingless, a segment polarity gene of Drosophila: the spatial distribution of transcripts in embryos. EMBO J. 6, 1765–1774

[9] Baker N.

[10] Bienz M.,
Saari G.,
Tremml G.,
Müller J.,
Züst B.,
Lawrence P. A.
(1988). Differential regulation of Ultrabithorax in two germ layers of Drosophila. Cell 53, 567–576

[11] Bienz M.,

[12] Saari G.,

[13] Tremml G.,

[14] Müller J.,

[15] Züst B.,

[16] Lawrence P. A.

[17] Bienz M.,
Tremml G.
(1988). Domain of Ultrabithorax expression in Drosophila visceral mesoderm from autoregulation and exclusion. Nature 333, 576–578

[18] Bienz M.,

[19] Tremml G.

[20] Cabrera C. V.,
Alonso M. C.,
Johnston P.,
Phillips R. G.,
Lawrence P. A.
(1987). Phenocopies induced with antisense RNA identify the wingless gene. Cell 50, 659–663

[21] Cabrera C. V.,

[22] Alonso M. C.,

[23] Johnston P.,

[24] Phillips R. G.,

[25] Lawrence P. A.

[26] Campos-Ortega J. A.,
Hartenstein V.
(1985). The Embryonic Development of Drosophila melanogaster. Berlin: Springer Verlag.

[27] Campos-Ortega J. A.,

[28] Hartenstein V.

[29] Casanova J.,
Sánchez-Herrero E.,
Busturia A.,
Morata G.
(1987). Double and triple mutant combinations of the bithorax complex in Drosophila. EMBO J. 6, 3101–3109

[30] Casanova J.,

[31] Sánchez-Herrero E.,

[32] Busturia A.,

[33] Morata G.

[34] Chan L.-N.,
Gehring W. J.
(1971). Determination of blastoderm cells in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 68, 2217–2221

[35] Chan L.-N.,

[36] Gehring W. J.

[37] Cho K. W. Y.,
Blumberg B.,
Steinbeisser H.,
De Robertis E. M.
(1991). Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 67, 1111–1120

[38] Cho K. W. Y.,

[39] Blumberg B.,

[40] Steinbeisser H.,

[41] De Robertis E. M.

[42] Chouinard S.,
Kaufman T. C.
(1991). Control of expression of the homeotic labial (lab) locus of Drosophila melanogaster: evidence for both positive and negative autogenous regulation. Development 113, 1267–1280

[43] Chouinard S.,

[44] Kaufman T. C.

[45] Diederich R. J.,
Merrill V. K. L.,
Pultz M. A.,
Kaufman T. C.
(1989). Isolation, structure, and expression of labial, a homeotic gene of the Antennapedia complex involved in Drosophila head development. Genes Dev. 3, 399–414

[46] Diederich R. J.,

[47] Merrill V. K. L.,

[48] Pultz M. A.,

[49] Kaufman T. C.

[50] Driever W.,
Thoma G.,
Nüsslein-Volhard C.
(1989). Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature 340, 363–367

[51] Driever W.,

[52] Thoma G.,

[53] Nüsslein-Volhard C.

[54] Harding K.,
Levine M.
(1988). Gap genes define the limits of Antennapedia and bithorax gene expression during early development of Drosophila. EMBO J. 7, 205–214

[55] Harding K.,

[56] Levine M.

[57] Hartenstein V.,
Technau G. M.,
Campos-Ortega J. A.
(1985). Fate mapping in wild-type Drosophila melanogaster. III. A fate map of the blastoderm. Wilhelm Roux Arch. Dev. Biol. 194, 213–216

[58] Hartenstein V.,

[59] Technau G. M.,

[60] Campos-Ortega J. A.

[61] Hiromi Y.,
Gehring W. J.
(1987). Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell 50, 963–974

[62] Hiromi Y.,

[63] Gehring W. J.

[64] Hooper J. E.
(1986). Homeotic gene function in the muscles of Drosophila larvae. EMBO J. 5, 2321–2329

[65] Hooper J. E.

[66] Immerglück K.,
Lawrence P. A.,
Bienz M.
(1990). Induction across germ layers in Drosophila mediated by a genetic cascade. Cell 62, 261–268

[67] Immerglück K.,

[68] Lawrence P. A.,

[69] Bienz M.

[70] Irish V. F.,
Martinez-Arias A.,
Akam M.
(1989). Spatial regulation of the Antennapedia and Ultrabithorax homeotic genes during Drosophila early development. EMBO J. 8, 1527–1538

[71] Irish V. F.,

[72] Martinez-Arias A.,

[73] Akam M.

[74] Kim S.-J.,
Angel P.,
Lafyatis R.,
Hattori K.,
Kim K. Y.,
Sporn M. B.,
Karin M.,
Roberts A. B.
(1990). Autoinduction of TGF- 1 is mediated by the AP-1 complex. Mol. Cell. Biol. 10, 1492–1497

[75] Kim S.-J.,

[76] Angel P.,

[77] Lafyatis R.,

[78] Hattori K.,

[79] Kim K. Y.,

[80] Sporn M. B.,

[81] Karin M.,

[82] Roberts A. B.

[83] Kramer I. M.,
Koornneef I.,
de Laat S. W.,
van den Eijnden-van Raaij A. J. M.
(1991). TGF-β 1 induces phosphorylation of the cyclic AMP responsive element binding protein in ML-CCI64 cells. EMBO J. 10, 1083–1089

[84] Kramer I. M.,

[85] Koornneef I.,

[86] de Laat S. W.,

[87] van den Eijnden-van Raaij A. J. M.

[88] Lewis E. B.
(1963). Genes and developmental pathways. Am. Zool. 3, 53–56

[89] Lewis E. B.

[90] Lewis E. B.
(1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565–570

[91] Lewis E. B.

[92] Lin H. Y.,
Wang X.-F.,
Ng-Eaton E.,
Weinberg R. A.,
Lodish H. F.
(1992). Expression cloning of the TGF-β type II receptor, a functional transmembrane serine/threonine kinase. Cell 68, 775–785

[93] Lin H. Y.,

[94] Wang X.-F.,

[95] Ng-Eaton E.,

[96] Weinberg R. A.,

[97] Lodish H. F.

[98] Martinez-Arias A.,
Lawrence P. A.
(1985). Parasegments and compartments in the Drosophila embryo. Nature 313, 639–642

[99] Martinez-Arias A.,

[100] Lawrence P. A.

[101] Massagué J.
(1990). The transforming growth factor-β family. Ann. Rev. Cell Biol. 6, 597–641

[102] Massagué J.

[103] Mathews L. S.,
Vale W. W.
(1991). Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65, 973–982

[104] Mathews L. S.,

[105] Vale W. W.

[106] Mlodzik M.,
Fjose A.,
Gehring W. J.
(1988). Molecular structure and spatial expression of a homeobox gene from the labial region of the Antennapedia-complex. EMBO J. 7, 2569–2578

[107] Mlodzik M.,

[108] Fjose A.,

[109] Gehring W. J.

[110] Morata G.,
García-Bellido A.
(1976). Developmental analysis of some mutants of the bithorax system of Drosophila. Wilhelm Roux Arch. Dev. Biol. 179, 125–143

[111] Morata G.,

[112] García-Bellido A.

[113] Nüsslein-Volhard C.,
Wieschaus E.
(1980). Mutations affecting segment number and polarity in Drosophila. Nature 287, 795–801

[114] Nüsslein-Volhard C.,

[115] Wieschaus E.

[116] Padgett R. W.,
St. Johnston R. D.,
Gelbart W. M.
(1987). A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β gene family. Nature 325, 81–84

[117] Padgett R. W.,

[118] St. Johnston R. D.,

[119] Gelbart W. M.

[120] Panganiban G. E. F.,
Reuter R.,
Scott M. P.,
Hoffmann F. M.
(1990). A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. Development 110, 141–150

[121] Panganiban G. E. F.,

[122] Reuter R.,

[123] Scott M. P.,

[124] Hoffmann F. M.

[125] Perkins K. K.,
Admon A.,
Patel N.,
Tjian R.
(1990). The Drosophila Fos-related AP-1 protein is a developmentally regulated transcription factor. Genes Dev. 4, 822–834

[126] Perkins K. K.,

[127] Admon A.,

[128] Patel N.,

[129] Tjian R.

[130] Demerec M.
Poulson D. F.
(1950). Histogenesis, organogenesis, and differentiation in the embryo of Drosophila melanogaster Meigen. In The Biology of Drosophila, (ed. Demerec M.), pp. 168–274, New York: Hafner.

[131] Demerec M.

[132] Poulson D. F.

[133] Qian S.,
Capovilla M.,
Pirotta V.
(1991). The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. EMBO J. 10, 1415–1425

[134] Qian S.,

[135] Capovilla M.,

[136] Pirotta V.

[137] Reinitz J.,
Levine M.
(1990). Control of the initiation of homeotic gene expression by the gap genes giant and tailless. Dev. Biol. 140, 57–72

[138] Reinitz J.,

[139] Levine M.

[140] Reuter R.,
Panganiban G. E. F.,
Hoffmann F. M.,
Scott M. P.
(1990). Homeotic genes regulate the expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development 110, 1031–1040

[141] Reuter R.,

[142] Panganiban G. E. F.,

[143] Hoffmann F. M.,

[144] Scott M. P.

[145] Rijsewijk F.,
Schuerman M.,
Wagenaar E.,
Parren P.,
Weigel D.,
Nusse R.
(1987). The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–657

[146] Rijsewijk F.,

[147] Schuerman M.,

[148] Wagenaar E.,

[149] Parren P.,

[150] Weigel D.,

[151] Nusse R.

[152] Rosa F. M.
(1989). Mix.1, a homeobox mRNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos. Cell 57, 965–974

[153] Rosa F. M.

[154] Rossi P.,
Karsenty G.,
Roberts A. B.,
Roche N. S.,
Sporn M. B.,
de Crombrugghe B.
(1988). A nuclear factor 1 binding site mediates the transcriptional activation of a type I collagen promoter by transforming growth factor-. Cell 52, 405–414

[155] Rossi P.,

[156] Karsenty G.,

[157] Roberts A. B.,

[158] Roche N. S.,

[159] Sporn M. B.,

[160] de Crombrugghe B.

[161] Ruiz i Altaba A.,
Melton B. A.
(1989). Interaction between peptide growth factors and homeobox genes in the establishment of anteroposterior polarity in frog embryos. Nature 341, 33–38

[162] Ruiz i Altaba A.,

[163] Melton B. A.

[164] St. Johnston R. D.,
Hoffmann F. M.,
Blackman R. K.,
Segal D.,
Grimaila R.,
Padgett R. W.,
Irick H. A.,
Gelbart W. M.
(1990). Genes Dev. 4, 1114–1127

[165] St. Johnston R. D.,

[166] Hoffmann F. M.,

[167] Blackman R. K.,

[168] Segal D.,

[169] Grimaila R.,

[170] Padgett R. W.,

[171] Irick H. A.,

[172] Gelbart W. M.

[173] Struhl G.,
Struhl K.,
Macdonald P. M.
(1989). The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57, 1259–1273

[174] Struhl G.,

[175] Struhl K.,

[176] Macdonald P. M.

[177] Taira M.,
Jamrich M.,
Good P. J.,
Dawid I. B.
(1992). The LIM domain-containing homeo box gene Xlim-1 is expressed specifically in the organizer region of Xenopus gastrula embryos. Genes Dev. 6, 356–366

[178] Taira M.,

[179] Jamrich M.,

[180] Good P. J.,

[181] Dawid I. B.

[182] Teugels E.,
Ghysen A.
(1985). Domains of action of bithorax genes in Drosophila central nervous system. Nature 314, 558–561

[183] Teugels E.,

[184] Ghysen A.

[185] Tremml G.,
Bienz M.
(1989a). Homeotic gene expression in the visceral mesoderm of Drosophila embryos. EMBO J. 8, 2677–2685

[186] Tremml G.,

[187] Bienz M.

[188] Tremml G.,
Bienz M.
(1989b). An essential function of even-skipped for homeotic gene expression in the Drosophila visceral mesoderm. EMBO J. 8, 2687–2693

[189] Tremml G.,

[190] Bienz M.

[191] Wakimoto B. T.,
Kaufman T. C.
(1981). Analysis of larval segmentation in lethal genotypes associated with the Antennapedia gene complex in Drosophila. Dev. Biol. 81, 51–64

[192] Wakimoto B. T.,

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