Compartment boundaries and the control of Drosopfiffa limb pattern by hedgehog protein

Drosophila limbs are subdivided into anterior and posterior compartments which derive from adjacent cell populations founded early in development. Evidence is now provided that posterior cells organize growth and cell patterning in both compartments by secreting hedgehog protein and that hedgehog protein acts indirectly by inducing neighbouring anterior cells to secrete decapentaplegic or wingless protein.

[1]  P. Lawrence,et al.  Compartments in the wing of Drosophila: a study of the engrailed gene. , 1976, Developmental biology.

[2]  A. Garcı́a-Bellido.  Genetic control of wing disc development in Drosophila. , 2008, Ciba Foundation symposium.

[3]  W. Gelbart,et al.  Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary , 1990, Mechanisms of Development.

[4]  S. Eaton,et al.  Repression of ci-D in posterior compartments of Drosophila by engrailed. , 1990, Genes & development.

[5]  Saigo Kaoru,et al.  Structure and expression of hedgehog, a Drosophila segment-polarity gene required for cell-cell communication. , 1993 .

[6]  C. Tickle,et al.  FGF-4 maintains polarizing activity of posterior limb bud cells in vivo and in vitro. , 1993, Development.

[7]  N E Baker,et al.  Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. , 1988, Development.

[8]  A. M. Arias,et al.  Secretion and movement of wingless protein in the epidermis of the Drosophila embryo , 1991, Mechanisms of Development.

[9]  M. Bate,et al.  A wingless-dependent polar coordinate system in Drosophila imaginal discs. , 1993, Science.

[10]  S. Cohen,et al.  Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila , 1993, Cell.

[11]  G. Rubin,et al.  Analysis of genetic mosaics in developing and adult Drosophila tissues. , 1993, Development.

[12]  Gerald M. Rubin,et al.  The TGFβ homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina , 1993, Cell.

[13]  Konrad Basler,et al.  Organizing activity of wingless protein in Drosophila , 1993, Cell.

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

[15]  W. Gelbart,et al.  An extensive 3' cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. , 1991, Development.

[16]  P. Ingham,et al.  A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos , 1993, Cell.

[17]  T. Tabata,et al.  Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs , 1994, Cell.

[18]  J. Mohler.  Requirements for hedgehog, a segmental polarity gene, in patterning larval and adult cuticle of Drosophila. , 1988, Genetics.

[19]  P. Lawrence,et al.  Borders of parasegments in Drosophila embryos are delimited by the fushi tarazu and even-skipped genes , 1987, Nature.

[20]  P. Beachy,et al.  Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog , 1992, Cell.

[21]  Judith A. Kassis,et al.  Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis , 1988, Nature.

[22]  C. Tickle,et al.  FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb , 1993, Cell.

[23]  T. Kornberg,et al.  Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. , 1990, Genes & development.

[24]  C. Tabin,et al.  Sonic hedgehog mediates the polarizing activity of the ZPA , 1993, Cell.

[25]  K. Kroll,et al.  Cloning and characterization of the segment polarity gene cubitus interruptus Dominant of Drosophila. , 1990, Genes & development.

[26]  F. Hoffmann,et al.  Biochemical characterization of the Drosophila dpp protein, a member of the transforming growth factor beta family of growth factors , 1990, Molecular and cellular biology.

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

[28]  Andrew P. McMahon,et al.  Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity , 1993, Cell.

[29]  P. Lawrence,et al.  Distribution of the wingless gene product in drosophila embryos: A protein involved in cell-cell communication , 1989, Cell.

[30]  H. Meinhardt.  Cell determination boundaries as organizing regions for secondary embryonic fields. , 1983, Developmental biology.

[31]  S. Blair.  Mechanisms of compartment formation: evidence that non-proliferating cells do not play a critical role in defining the D/V lineage restriction in the developing wing of Drosophila. , 1993, Development.

[32]  P. O’Farrell,et al.  Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein , 1985, Cell.

[33]  T. Jessell,et al.  Induction of floor plate differentiation by contact-dependent, homeogenetic signals. , 1993, Development.

[34]  T. Weaver,et al.  Axis specification in the developing Drosophila appendage: The role of wingless, decapentaplegic, and the homeobox gene aristaless , 1993, Cell.

[35]  K. Anderson,et al.  decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo , 1992, Cell.

[36]  K. Moses,et al.  The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye , 1993, Cell.

[37]  P. Lawrence,et al.  Control of compartment development by the engrailed gene in Drosophila , 1975, Nature.

[38]  P. Ingham,et al.  Regulation of wingless transcription in the Drosophila embryo. , 1993, Development.

[39]  N. Baker.  Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. , 1988, Developmental biology.

[40]  P. O’Farrell,et al.  Multiple modes of engrailed regulation in the progression towards cell fate determination , 1991, Nature.

[41]  S. Benzer,et al.  Development of the Drosophila retina, a neurocrystalline lattice. , 1976, Developmental biology.

[42]  F. Crick,et al.  Compartments and polyclones in insect development. , 1975, Science.

[43]  K. Golic.  Site-specific recombination between homologous chromosomes in Drosophila. , 1991, Science.

[44]  James R. Broach,et al.  Replication and recombination functions associated with the yeast plasmid, 2μ circle , 1980, Cell.

[45]  W. Gelbart,et al.  The relationship of decapentaplegic and engrailed expression in Drosophila imaginal disks: do these genes mark the anterior-posterior compartment boundary? , 1991, Development.

[46]  P. Ingham,et al.  Role of the Drosophila patched gene in positional signalling , 1991, Nature.

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

[48]  S. Carroll,et al.  Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions. , 1993, Development.

[49]  N. Perrimon,et al.  Altering the insertional specificity of a Drosophila transposable element. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[50]  G. Morata,et al.  Developmental compartmentalisation of the wing disk of Drosophila. , 1973, Nature: New biology.

[51]  M. Landry,et al.  Maintenance of ZPA signaling in cultured mouse limb bud cells. , 1993, Development.

[52]  F. Hoffmann,et al.  Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal disks is regulated by 3' cis-regulatory elements. , 1990, Genes & development.

[53]  W. Theurkauf,et al.  Tissue-specific and constitutive alpha-tubulin genes of Drosophila melanogaster code for structurally distinct proteins. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[54]  V. Chopra,et al.  Effect of the Wingless (wg1) mutation on wing and haltere development in Drosophila melanogaster. , 1976, Developmental biology.

[55]  P. O’Farrell,et al.  The engrailed locus of drosophila: In situ localization of transcripts reveals compartment-specific expression , 1985, Cell.

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

[57]  P. Ingham.  Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo , 1993, Nature.

[58]  G. Struhl.  Anterior and posterior compartments in the proboscis of Drosophila. , 1981, Developmental biology.

[59]  William M. Gelbart,et al.  Decapentaplegic: A gene complex affecting morphogenesis in Drosophila melanogaster , 1982, Cell.

[60]  P. O’Farrell,et al.  Maintenance of the engrailed expression pattern by Polycomb group genes in Drosophila. , 1992, Development.

[61]  A. Martinez Arias,et al.  Roles of wingless in patterning the larval epidermis of Drosophila. , 1991, Development.

[62]  Jean-Paul Vincent,et al.  The state of engrailed expression is not clonally transmitted during early Drosophila development , 1992, Cell.

[63]  K. G. Coleman,et al.  Expression of engrailed proteins in arthropods, annelids, and chordates , 1989, Cell.

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

[65]  P. Lawrence,et al.  Further studies of the engrailed phenotype in Drosophila. , 1982, The EMBO journal.

[66]  T. Tabata,et al.  The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. , 1992, Genes & development.

[67]  G. Morata,et al.  Minutes: mutants of drosophila autonomously affecting cell division rate. , 1975, Developmental biology.

[68]  G. Oswald,et al.  Lakes Beneath the Antarctic Ice Sheet , 1973, Nature.

[69]  A. Taylor,et al.  Contrasting distributions of patched and hedgehog proteins in the Drosophila embryo , 1993, Mechanisms of Development.

[70]  J. Mohler,et al.  Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila. , 1992, Development.

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