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

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.

[1]  M. Sporn,et al.  A nuclear factor 1 binding site mediates the transcriptional activation of a type I collagen promoter by transforming growth factor-β , 1988, Cell.

[2]  M. Akam,et al.  The molecular basis for metameric pattern in the Drosophila embryo. , 1987, Development.

[3]  M. Bienz,et al.  An essential role of even‐skipped for homeotic gene expression in the Drosophila visceral mesoderm. , 1989, The EMBO journal.

[4]  M. Scott,et al.  A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. , 1990, Development.

[5]  E. Lewis Genes and Developmental Pathways , 1963 .

[6]  E. Sánchez-Herrero,et al.  Double and triple mutant combinations of bithorax complex of Drosophila. , 1987, The EMBO journal.

[7]  P. Lawrence,et al.  Phenocopies induced with antisense RNA identify the wingless gene , 1987, Cell.

[8]  Ken W. Y. Cho,et al.  Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid , 1991, Cell.

[9]  J. Hooper,et al.  Homeotic gene function in the muscles of Drosophila larvae , 1986, The EMBO journal.

[10]  T. Kaufman,et al.  Analysis of larval segmentation in lethal genotypes associated with the antennapedia gene complex in Drosophila melanogaster. , 1981, Developmental biology.

[11]  R. Lehmann,et al.  A gap gene, hunchback, regulates the spatial expression of Ultrabithorax , 1986, Cell.

[12]  J. Massagué,et al.  Novel activin receptors: Distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors , 1992, Cell.

[13]  Wolfgang Driever,et al.  Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen , 1989, Nature.

[14]  M. Bienz,et al.  Homeotic gene expression in the visceral mesoderm of Drosophila embryos. , 1989, The EMBO journal.

[15]  V. Pirrotta,et al.  The bx region enhancer, a distant cis‐control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. , 1991, The EMBO journal.

[16]  M. Sporn,et al.  Autoinduction of transforming growth factor beta 1 is mediated by the AP-1 complex , 1990, Molecular and cellular biology.

[17]  K. Struhl,et al.  The gradient morphogen bicoid is a concentration-dependent transcriptional activator , 1989, Cell.

[18]  R. Weinberg,et al.  Expression cloning of the TGF-β type II receptor, a functional transmembrane serine/threonine kinase , 1992, Cell.

[19]  T. Kaufman,et al.  Isolation, structure, and expression of labial, a homeotic gene of the Antennapedia Complex involved in Drosophila head development. , 1989, Genes & development.

[20]  E. Lewis A gene complex controlling segmentation in Drosophila , 1978, Nature.

[21]  M. Bienz,et al.  Domain of Ultrabithorax expression in Drosophila visceral mesoderm from autoregulation and exclusion , 1988, Nature.

[22]  N E Baker,et al.  Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos , 1987, The EMBO journal.

[23]  V. Hartenstein,et al.  A Fate Map of the Blastoderm , 1985 .

[24]  W. Gehring,et al.  Molecular structure and spatial expression of a homeobox gene from the labial region of the Antennapedia‐complex. , 1988, EMBO Journal.

[25]  M. Scott,et al.  Homeotic genes regulate the spatial expression of putative growth factors in the visceral mesoderm of Drosophila embryos. , 1990, Development.

[26]  W. Gelbart,et al.  A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family , 1987, Nature.

[27]  I. Kramer,et al.  TGF‐beta 1 induces phosphorylation of the cyclic AMP responsive element binding protein in ML‐CCl64 cells. , 1991, The EMBO journal.

[28]  P. Lawrence,et al.  Differential regulation of Ultrabithorax in two germ layers of drosophila , 1988, Cell.

[29]  D. Melton,et al.  Interaction between peptide growth factors and homoeobox genes in the establishment of antero-posterior polarity in frog embryos , 1989, Nature.

[30]  P. Lawrence,et al.  Induction across germ layers in Drosophila mediated by a genetic cascade , 1990, Cell.

[31]  J. Massagué,et al.  The transforming growth factor-beta family. , 1990, Annual review of cell biology.

[32]  C. Nüsslein-Volhard,et al.  Mutations affecting segment number and polarity in Drosophila , 1980, Nature.

[33]  R. Tjian,et al.  The Drosophila Fos-related AP-1 protein is a developmentally regulated transcription factor. , 1990, Genes & development.

[34]  W. Gehring,et al.  Determination of blastoderm cells in Drosophila melanogaster. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Levine,et al.  Gap genes define the limits of antennapedia and bithorax gene expression during early development in Drosophila. , 1988, The EMBO journal.

[36]  H. Jäckle,et al.  Target sequences for hunchback in a control region conferring Ultrabithorax expression boundaries. , 1991, Development.

[37]  T. Kaufman,et al.  Control of expression of the homeotic labial (lab) locus of Drosophila melanogaster: evidence for both positive and negative autogenous regulation. , 1991, Development.

[38]  Detlef Weigel,et al.  The Drosophila homology of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless , 1987, Cell.

[39]  P. Good,et al.  The LIM domain-containing homeo box gene Xlim-1 is expressed specifically in the organizer region of Xenopus gastrula embryos. , 1992, Genes & development.

[40]  M. Bienz,et al.  Segmental determination in Drosophila conferred by hunchback (hb), a repressor of the homeotic gene Ultrabithorax (Ubx). , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[41]  F. Rosa Mix.1, a homeobox mRNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos , 1989, Cell.

[42]  M. Levine,et al.  Control of the initiation of homeotic gene expression by the gap genes giant and tailless in Drosophila. , 1990, Developmental biology.

[43]  A. Ghysen,et al.  Domains of action of bithorax genes in Drosophila central nervous system , 1985, Nature.

[44]  P. Lawrence,et al.  Parasegments and compartments in the Drosophila embryo , 1985, Nature.

[45]  Walter J. Gehring,et al.  Regulation and function of the Drosophila segmentation gene fushi tarazu , 1987, Cell.

[46]  A. Martinez-Arias,et al.  Spatial regulation of the Antennapedia and Ultrabithorax homeotic genes during Drosophila early development. , 1989, The EMBO journal.