Eye development in Drosophila: formation of the eye field and control of differentiation.

Publisher Summary This chapter discusses the early stages of eye development in Drosophila , focusing on the mechanisms that determine the global pattern rather than those involved in the establishment of specific cell fates. It discusses the specification of the eye disk to form an eye, the control of morphogenetic furrow initiation and propagation, and the coordination of growth with differentiation. Most adult Drosophila structures, including the eye, develop from imaginal disks. These are groups of cells set aside in the embryo that grow and differentiate inside the larva and evert to become functional during metamorphosis. Differentiation in the eye disk is progressive, moving across the disk in a wavelike manner from posterior to anterior. The front of the wave is marked by an indentation in the disk known as the morphogenetic furrow. Most cell division occurs in the unpatterned cells anterior to the furrow, while on the posterior side of the furrow the cells are organized into clusters that develop into the ommatidia. The Drosophila eye disk develops in a remarkably coordinated manner. Its differentiation begins at a precisely defined point and expands at a steady rate, laying down rows of evenly spaced ommatidial founder cells.

[1]  J. Goodship,et al.  Developmental genetics of the heart. , 1996, Current opinion in genetics & development.

[2]  F. Hoffmann,et al.  Decapentaplegic restricts the domain of wingless during Drosophila limb patterning , 1996, Nature.

[3]  R. Hill,et al.  Multiple functions for Pax6 in mouse eye and nasal development. , 1996, Genes & development.

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

[5]  J. Sekelsky,et al.  Drawing a stripe in Drosophila imaginal disks: negative regulation of decapentaplegic and patched expression by engrailed. , 1995, Genetics.

[6]  Seymour Benzer,et al.  The eyes absent gene: Genetic control of cell survival and differentiation in the developing Drosophila eye , 1993, Cell.

[7]  M. Caudy,et al.  Hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. , 1994, Genes & development.

[8]  G. Struhl,et al.  Complementary and Mutually Exclusive Activities of Decapentaplegic and Wingless Organize Axial Patterning during Drosophila Leg Development , 1996, Cell.

[9]  R. Brent,et al.  roughex down-regulates G2 cyclins in G1. , 1997, Genes & development.

[10]  K. Eto,et al.  Uchida rat (rSey): a new mutant rat with craniofacial abnormalities resembling those of the mouse Sey mutant. , 1994, Differentiation; research in biological diversity.

[11]  F. Kashanchi,et al.  Transcriptional regulation of the mouse alpha A-crystallin gene: activation dependent on a cyclic AMP-responsive element (DE1/CRE) and a Pax-6-binding site , 1995, Molecular and cellular biology.

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

[13]  D. Kalderon,et al.  Genetic investigation of cAMP-dependent protein kinase function in Drosophila development. , 1993, Genes & development.

[14]  V. Hartenstein,et al.  The role of yan in mediating the choice between cell division and differentiation. , 1995, Development.

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

[16]  S. Higashijima,et al.  Dual Bar homeo box genes of Drosophila required in two photoreceptor cells, R1 and R6, and primary pigment cells for normal eye development. , 1992, Genes & development.

[17]  A. Cvekl,et al.  A complex array of positive and negative elements regulates the chicken alpha A-crystallin gene: involvement of Pax-6, USF, CREB and/or CREM, and AP-1 proteins , 1994, Molecular and cellular biology.

[18]  W. Gelbart,et al.  Characterization and relationship of dpp receptors encoded by the saxophone and thick veins genes in Drosophila , 1994, Cell.

[19]  J. Royet,et al.  hedgehog, wingless and orthodenticle specify adult head development in Drosophila. , 1996, Development.

[20]  A. Cvekl,et al.  Pax-6 and lens-specific transcription of the chicken delta 1-crystallin gene. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Jiménez,et al.  twine, a cdc25 homolog that functions in the male and female germline of drosophila , 1992, Cell.

[22]  G. Saunders,et al.  Mouse Small eye results from mutations in a paired-like homeobox-containing gene , 1991, Nature.

[23]  G M Rubin,et al.  wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. , 1995, Development.

[24]  R. Maas,et al.  Genomic structure, evolutionary conservation and aniridia mutations in the human PAX6 gene , 1992, Nature Genetics.

[25]  D. Ready,et al.  Neuronal differentiation in Drosophila ommatidium. , 1987, Developmental biology.

[26]  M. Bate,et al.  The development of Drosophila melanogaster , 1993 .

[27]  D. Lindsley,et al.  The Genome of Drosophila Melanogaster , 1992 .

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

[29]  S. Carroll,et al.  hairy gene function in the Drosophila eye: normal expression is dispensable but ectopic expression alters cell fates. , 1991, Development.

[30]  A. Tomlinson,et al.  Cellular interactions in the developing Drosophila eye. , 1988, Development.

[31]  J. Posakony,et al.  Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete. , 1994, Genes & development.

[32]  G. Rubin,et al.  Determination of neuronal cell fate: lessons from the R7 neuron of Drosophila. , 1994, Annual review of neuroscience.

[33]  L. Strong,et al.  Positional cloning and characterization of a paired box- and homeobox-containing gene from the aniridia region , 1991, Cell.

[34]  S. Benzer,et al.  Monoclonal antibody probes discriminate early and late mutant defects in development of the Drosophila retina. , 1989, Developmental biology.

[35]  S. Zipursky,et al.  Cell cycle progression in the developing Drosophila eye: roughex encodes a novel protein required for the establishment of G1 , 1994, Cell.

[36]  W. Gelbart,et al.  Drosophila Dpp signaling is mediated by the punt gene product: A dual ligand-binding type II receptor of the TGFβ receptor family , 1995, Cell.

[37]  P. Ingham,et al.  Quantitative effects of hedgehog and decapentaplegic activity on the patterning of the Drosophila wing , 1995, Current Biology.

[38]  G. Rubin,et al.  The homeo domain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. , 1990, Genes & development.

[39]  W. Brook,et al.  Antagonistic Interactions Between Wingless and Decapentaplegic Responsible for Dorsal-Ventral Pattern in the Drosophila Leg , 1996, Science.

[40]  C. Neumann,et al.  Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. , 1997, Development.

[41]  V. Hartenstein,et al.  The drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system , 1994, Neuron.

[42]  K. Basler,et al.  Hedgehog-dependent patterning in the Drosophila eye can occur in the absence of Dpp signaling. , 1996, Developmental biology.

[43]  M. Scott,et al.  The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog , 1996, Nature.

[44]  G. Rubin,et al.  Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginal discs. , 1992, Developmental biology.

[45]  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.

[46]  Roel Nusse,et al.  Wnt genes , 1992, Cell.

[47]  A. Bradley,et al.  BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. , 1995, Genes & development.

[48]  M. Affolter,et al.  Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF beta homologs during Drosophila embryogenesis. , 1994, Development.

[49]  P. Callaerts,et al.  New perspectives on eye evolution. , 1995, Current opinion in genetics & development.

[50]  P. O’Farrell,et al.  Genetic control of cell division patterns in the Drosophila embryo , 1989, Cell.

[51]  S. Zipursky,et al.  Induction of Drosophila eye development by decapentaplegic. , 1997, Development.

[52]  D. Kalderon Morphogenetic Signalling: Responses to Hedgehog , 1995, Current Biology.

[53]  David O. Morgan,et al.  Principles of CDK regulation , 1995, Nature.

[54]  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.

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

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

[57]  G. Struhl,et al.  Compartment boundarles and the control of Drosophila limb pattern by bedgebog protein , 1994 .

[58]  M. Scott,et al.  The Drosophila patched gene encodes a putative membrane protein required for segmental patterning , 1989, Cell.

[59]  P. Nurse,et al.  Animal cell cycles and their control. , 1992, Annual review of biochemistry.

[60]  D. Davidson,et al.  The role of Pax-6 in eye and nasal development. , 1995, Development.

[61]  P Gruss,et al.  Forebrain patterning defects in Small eye mutant mice. , 1996, Development.

[62]  J. Weissenbach,et al.  A human homologue of the Drosophila eyes absent gene underlies Branchio-Oto-Renal (BOR) syndrome and identifies a novel gene family , 1997, Nature Genetics.

[63]  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.

[64]  B. Edgar Cell Cycle: Cell-cycle control in a developmental context , 1994, Current Biology.

[65]  T. Lecuit,et al.  Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. , 1996, Development.

[66]  A. Felsenfeld,et al.  Positional signaling by hedgehog in Drosophila imaginal disc development. , 1995, Development.

[67]  S. Carroll,et al.  daughterless is required for Drosophila photoreceptor cell determination, eye morphogenesis, and cell cycle progression. , 1996, Developmental biology.

[68]  I. Hariharan,et al.  Uncoupling Cell Fate Determination from Patterned Cell Division in the Drosophila Eye , 1995, Science.

[69]  W. Gelbart,et al.  Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. , 1995, Genetics.

[70]  J. Sekelsky,et al.  Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. , 1995, Genetics.

[71]  A. Brand,et al.  Specificity of bone morphogenetic protein-related factors: cell fate and gene expression changes in Drosophila embryos induced by decapentaplegic but not 60A. , 1994, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[72]  Y Sun,et al.  Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. , 1995, Development.

[73]  M. Affolter,et al.  An absolute requirement for both the type II and type I receptors, punt and thick veins, for Dpp signaling in vivo , 1995, Cell.

[74]  T. Wolff,et al.  The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. , 1991, Development.

[75]  Marek Mlodzik,et al.  The regulation of hedgehog and decapentaplegic during Drosophila eye imaginal disc development , 1996, Mechanisms of Development.

[76]  N. Papalopulu,et al.  A Xenopus gene, Xbr-1, defines a novel class of homeobox genes and is expressed in the dorsal ciliary margin of the eye. , 1996, Developmental biology.

[77]  P. Ingham Signalling by hedgehog family proteins in Drosophila and vertebrate development. , 1995, Current opinion in genetics & development.

[78]  C. Tabin,et al.  The long and short of hedgehog signaling , 1995, Cell.

[79]  G. Mardon,et al.  Ectopic eye development in Drosophila induced by directed dachshund expression. , 1997, Development.

[80]  R. L. Johnson,et al.  patched overexpression alters wing disc size and pattern: transcriptional and post-transcriptional effects on hedgehog targets. , 1995, Development.

[81]  Mary Ellen Lane,et al.  Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development , 1995, Cell.

[82]  S. Hodgson,et al.  The human PAX6 gene is mutated in two patients with aniridia , 1992, Nature Genetics.

[83]  C. Tabin,et al.  The hedgehog gene family in Drosophila and vertebrate development. , 1994, Development (Cambridge, England). Supplement.

[84]  D. Schmucker,et al.  Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila: evidence for a conserved function in photoreceptors. , 1997, Genes & development.

[85]  G. Struhl,et al.  Direct and Long-Range Action of a Wingless Morphogen Gradient , 1996, Cell.

[86]  C. Zuker On the evolution of eyes: would you like it simple or compound? , 1994, Science.

[87]  W. Gelbart,et al.  Molecular organization of the decapentaplegic gene in Drosophila melanogaster. , 1990, Genes & development.

[88]  J. Posakony,et al.  The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes. , 1991, Development.

[89]  P. A. Powell,et al.  Spatial regulation of proneural gene activity: auto- and cross-activation of achaete is antagonized by extramacrochaetae. , 1992, Genes & development.

[90]  S. Zipursky,et al.  Atonal, rough and the resolution of proneural clusters in the developing Drosophila retina. , 1996, Development.

[91]  R. Maas,et al.  Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode. , 1997, Development.

[92]  G. Struhl,et al.  Protein kinase A and hedgehog signaling in drosophila limb development , 1995, Cell.

[93]  N. Copeland,et al.  Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. , 1995, Development.

[94]  P. Callaerts,et al.  Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. , 1995, Science.

[95]  P. O’Farrell,et al.  Cdks and the Drosophila cell cycle. , 1997, Current opinion in genetics & development.

[96]  S. Higashijima,et al.  Identification of a different-type homeobox gene, BarH1, possibly causing Bar (B) and Om(1D) mutations in Drosophila. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[97]  U. Heberlein,et al.  Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. , 1997, Development.

[98]  J. Massagué,et al.  Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor , 1994, Cell.

[99]  N. Baker,et al.  Proneural function of neurogenic genes in the developing Drosophila eye , 1997, Current Biology.

[100]  P. Bryant,et al.  Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster. , 1986, The Journal of experimental zoology.

[101]  Yves Grau,et al.  atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system , 1993, Cell.

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

[103]  J. O'Tousa,et al.  sine oculis is a homeobox gene required for Drosophila visual system development. , 1994, Genetics.

[104]  M. Pownall More to patterning than Sonic hedgehog. , 1994, BioEssays : news and reviews in molecular, cellular and developmental biology.

[105]  Saigo Kaoru,et al.  Induction of a mirror-image duplication of anterior wing structures by localized hedgehog expression in the anterior compartment of Drosophila melanogaster wing imaginal discs. , 1994, Gene.

[106]  P. O’Farrell,et al.  Transcriptional regulation of string (cdc25): a link between developmental programming and the cell cycle. , 1994, Development.

[107]  N. Baker,et al.  Drosophila eye development: Notch and Delta amplify a neurogenic pattern conferred on the morphogenetic furrow by scabrous , 1995, Mechanisms of Development.

[108]  Pattern Formation: Hedgehog points the way , 1994, Current Biology.

[109]  U. Heberlein,et al.  Mechanisms of drosophila retinal morphogenesis: The virtues of being progressive , 1995, Cell.

[110]  P. Lawrence,et al.  Cell lineage in the developing retina of Drosophila. , 1979, Developmental biology.

[111]  B. Edgar,et al.  Developmental Control of Cell Cycle Regulators: A Fly's Perspective , 1996, Science.

[112]  D. Strutt,et al.  Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A , 1995, Nature.

[113]  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.

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

[115]  A. Kumagai,et al.  The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system , 1991, Cell.

[116]  Y. Jan,et al.  Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence , 1989, Cell.

[117]  T. Tabata,et al.  Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. , 1995, Development.

[118]  U. Heberlein,et al.  Retinal morphogenesis in Drosophila: hints from an eye-specific decapentaplegic allele. , 1997, Developmental genetics.

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

[120]  Manuel Calleja,et al.  Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing , 1996, Nature.

[121]  T Marty,et al.  Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc. , 1995, Development.

[122]  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.

[123]  K. Lyons,et al.  A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. , 1995, Genes & development.

[124]  M. Wehrli,et al.  Epithelial planar polarity in the developing Drosophila eye. , 1995, Development.

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

[126]  S. Higashijima,et al.  Structure and expression of hedgehog, a Drosophila segment-polarity gene required for cell-cell communication. , 1993, Gene.

[127]  T. J. Donohoe,et al.  Growth and differentiation in the Drosophila eye coordinated by hedgehog , 1995, Nature.

[128]  M. Ashburner,et al.  Genetic and cytogenetic analysis of the 43A-E region containing the segment polarity gene costa and the cellular polarity genes prickle and spiny-legs in Drosophila melanogaster. , 1993, Genetics.

[129]  N. Baker,et al.  Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye , 1996, Current Biology.

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

[131]  H. Theisen,et al.  Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs. , 1997, Development.

[132]  W. Gelbart,et al.  Molecular lesions associated with alleles of decapentaplegic identify residues necessary for TGF-beta/BMP cell signaling in Drosophila melanogaster. , 1996, Genetics.

[133]  H. Theisen,et al.  Developmental territories created by mutual antagonism between Wingless and Decapentaplegic. , 1996, Development.

[134]  A. Taylor,et al.  A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched , 1989, Nature.

[135]  W. Gehring,et al.  Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. , 1994, Science.

[136]  G. Rubin,et al.  dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. , 1994, Development.

[137]  T. Matsuo,et al.  A mutation in the Pax-6 gene in rat small eye is associated with impaired migration of midbrain crest cells , 1993, Nature Genetics.

[138]  H. Horvitz,et al.  Patterning of the Caenorhabditis elegans head region by the Pax-6 family member vab-3 , 1995, Nature.

[139]  G. Struhl,et al.  Direct and Long-Range Action of a DPP Morphogen Gradient , 1996, Cell.

[140]  U. Heberlein,et al.  Role of the morphogenetic furrow in establishing polarity in the Drosophila eye. , 1995, Development.

[141]  K. Moses,et al.  Wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye. , 1995, Development.

[142]  Richard L. Maas,et al.  PAX6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects , 1994, Nature Genetics.

[143]  S. Carroll,et al.  Hairy and Emc negatively regulate morphogenetic furrow progression in the drosophila eye , 1995, Cell.

[144]  D. Strutt,et al.  Ommatidial polarity in the Drosophila eye is determined by the direction of furrow progression and local interactions. , 1995, Development.

[145]  S. Selleck,et al.  The division abnormally delayed (dally) gene: a putative integral membrane proteoglycan required for cell division patterning during postembryonic development of the nervous system in Drosophila. , 1995, Development.

[146]  S. Zipursky,et al.  Control of G1 in the developing Drosophila eye: rca1 regulates Cyclin A. , 1997, Genes & development.

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

[148]  K. White,et al.  Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. , 1991, Journal of neurobiology.

[149]  A. Cvekl,et al.  Pax-6 is essential for lens-specific expression of zeta-crystallin. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[150]  G. Rubin,et al.  cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in drosophila imaginal discs , 1995, Cell.

[151]  S. Selleck,et al.  Regulation of Cell Cycle Synchronization by decapentaplegic During Drosophila Eye Development , 1997, Science.

[152]  M. Freeman,et al.  Cell determination strategies in the Drosophila eye. , 1997, Development.

[153]  N. Bonini,et al.  Expression and function of clift in the development of somatic gonadal precursors within the Drosophila mesoderm. , 1997, Development.

[154]  Yuh Nung Jan,et al.  atonal is the proneural gene for Drosophila photoreceptors , 1994, Nature.

[155]  G. Struhl,et al.  Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. , 1995, Development.