Skip to main content

Advertisement

Log in

The lens in focus: a comparison of lens development in Drosophila and vertebrates

  • Review
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The evolution of the eye has been a major subject of study dating back centuries. The advent of molecular genetics offered the surprising finding that morphologically distinct eyes rely on conserved regulatory gene networks for their formation. While many of these advances often stemmed from studies of the compound eye of the fruit fly, Drosophila melanogaster, and later translated to discoveries in vertebrate systems, studies on vertebrate lens development far outnumber those in Drosophila. This may be largely historical, since Spemann and Mangold’s paradigm of tissue induction was discovered in the amphibian lens. Recent studies on lens development in Drosophila have begun to define molecular commonalities with the vertebrate lens. Here, we provide an overview of Drosophila lens development, discussing intrinsic and extrinsic factors controlling lens cell specification and differentiation. We then summarize key morphological and molecular events in vertebrate lens development, emphasizing regulatory factors and networks strongly associated with both systems. Finally, we provide a comparative analysis that highlights areas of research that would help further clarify the degree of conservation between the formation of dioptric systems in invertebrates and vertebrates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

CC:

Cone cell

PPC:

Primary pigment cell

MF:

Morphogenetic furrow

SMW:

Second mitotic wave

IOC:

Interommatidial cell

SPC:

Secondary pigment cell

TPC:

Tertiary pigment cell

PR:

Photoreceptor

PLE:

Presumptive lens ectoderm

AEL:

Anterior epithelial layer

PCP:

Planar cell polarity

References

  • Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284:770–776

    Article  PubMed  CAS  Google Scholar 

  • Ashery-Padan R, Marquardt T, Zhou X, Gruss P (2000) Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev 14:2701–2711

    Article  PubMed  CAS  Google Scholar 

  • Azuma N, Hirakiyama A, Inoue T, Asaka A, Yamada M (2000) Mutations of a human homologue of the Drosophila eyes absent gene (EYA1) detected in patients with congenital cataracts and ocular anterior segment anomalies. Hum Mol Genet 9:363–366

    Article  PubMed  CAS  Google Scholar 

  • Bajpe PK, van der Knaap JA, Demmers JA, Bezstarosti K, Bassett A, van Beusekom HM, Travers AA, Verrijzer CP (2008) Deubiquitylating enzyme UBP64 controls cell fate through stabilization of the transcriptional repressor tramtrack. Mol Cell Biol 28:1606–1615

    Article  PubMed  CAS  Google Scholar 

  • Baker NE, Yu SY (2001) The EGF receptor defines domains of cell cycle progression and survival to regulate cell number in the developing Drosophila eye. Cell 104:699–708

    Article  PubMed  CAS  Google Scholar 

  • Bao S (2010) Two themes on the assembly of the Drosophila eye. Curr Top Dev Biol 93:85–127

    Article  PubMed  Google Scholar 

  • Bao S, Cagan R (2005) Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev Cell 8:925–935

    Article  PubMed  CAS  Google Scholar 

  • Bao ZZ, Cepko CL (1997) The expression and function of Notch pathway genes in the developing rat eye. J Neurosci 17:1425–1434

    PubMed  CAS  Google Scholar 

  • Baonza A, Murawsky CM, Travers AA, Freeman M (2002) Pointed and Tramtrack69 establish an EGFR-dependent transcriptional switch to regulate mitosis. Nat Cell Biol 4:976–980

    Article  PubMed  CAS  Google Scholar 

  • Bateman JM, McNeill H (2004) Temporal control of differentiation by the insulin receptor/tor pathway in Drosophila. Cell 119:87–96

    Article  PubMed  CAS  Google Scholar 

  • Beatus P, Lendahl U (1998) Notch and neurogenesis. J Neurosci Res 54:125–136

    Article  PubMed  CAS  Google Scholar 

  • Beebe D, Garcia C, Wang X, Rajagopal R, Feldmeier M, Kim JY, Chytil A, Moses H, Ashery-Padan R, Rauchman M (2004) Contributions by members of the TGFbeta superfamily to lens development. Int J Dev Biol 48:845–856

    Article  PubMed  CAS  Google Scholar 

  • Belecky-Adams TL, Adler R, Beebe DC (2002) Bone morphogenetic protein signaling and the initiation of lens fiber cell differentiation. Development 129:3795–3802

    PubMed  CAS  Google Scholar 

  • Bhattacharya A, Baker NE (2009) The HLH protein Extramacrochaetae is required for R7 cell and cone cell fates in the Drosophila eye. Dev Biol 327:288–300

    Article  PubMed  CAS  Google Scholar 

  • Blanco J, Girard F, Kamachi Y, Kondoh H, Gehring WJ (2005) Functional analysis of the chicken delta1-crystallin enhancer activity in Drosophila reveals remarkable evolutionary conservation between chicken and fly. Development 132:1895–1905

    Article  PubMed  CAS  Google Scholar 

  • Blixt A, Mahlapuu M, Aitola M, Pelto-Huikko M, Enerback S, Carlsson P (2000) A forkhead gene, FoxE3, is essential for lens epithelial proliferation and closure of the lens vesicle. Genes Dev 14:245–254

    PubMed  CAS  Google Scholar 

  • Blixt A, Landgren H, Johansson BR, Carlsson P (2007) Foxe3 is required for morphogenesis and differentiation of the anterior segment of the eye and is sensitive to Pax6 gene dosage. Dev Biol 302:218–229

    Article  PubMed  CAS  Google Scholar 

  • Blochlinger K, Jan LY, Jan YN (1993) Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila. Development 117:441–450

    PubMed  CAS  Google Scholar 

  • Bogaert T, Brown N, Wilcox M (1987) The Drosophila PS2 antigen is an invertebrate integrin that, like the fibronectin receptor, becomes localized to muscle attachments. Cell 51:929–940

    Article  PubMed  CAS  Google Scholar 

  • Bonini NM, Leiserson WM, Benzer S (1998) Multiple roles of the eyes absent gene in Drosophila. Dev Biol 196:42–57

    Article  PubMed  CAS  Google Scholar 

  • Boswell BA, Lein PJ, Musil LS (2008a) Cross-talk between fibroblast growth factor and bone morphogenetic proteins regulates gap junction-mediated intercellular communication in lens cells. Mol Biol Cell 19:2631–2641

    Article  PubMed  CAS  Google Scholar 

  • Boswell BA, Overbeek PA, Musil LS (2008b) Essential role of BMPs in FGF-induced secondary lens fiber differentiation. Dev Biol 324:202–212

    Article  PubMed  CAS  Google Scholar 

  • Bottcher RT, Niehrs C (2005) Fibroblast growth factor signaling during early vertebrate development. Endocr Rev 26:63–77

    Article  PubMed  CAS  Google Scholar 

  • Brachmann CB, Cagan RL (2003) Patterning the fly eye: the role of apoptosis. Trends Genet 19:91–96

    Article  PubMed  CAS  Google Scholar 

  • Brownell I, Dirksen M, Jamrich M (2000) Forkhead Foxe3 maps to the dysgenetic lens locus and is critical in lens development and differentiation. Genesis 27:81–93

    Article  PubMed  CAS  Google Scholar 

  • Brunner D, Ducker K, Oellers N, Hafen E, Scholz H, Klambt C (1994) The ETS domain protein pointed-P2 is a target of MAP kinase in the sevenless signal transduction pathway. Nature 370:386–389

    Article  PubMed  CAS  Google Scholar 

  • Burgess D, Zhang Y, Siefker E, Vaca R, Kuracha MR, Reneker L, Overbeek PA, Govindarajan V (2010) Activated Ras alters lens and corneal development through induction of distinct downstream targets. BMC Dev Biol 10:13

    Article  PubMed  CAS  Google Scholar 

  • Cagan RL, Ready DF (1989a) The emergence of order in the Drosophila pupal retina. Dev Biol 136:346–362

    Article  PubMed  CAS  Google Scholar 

  • Cagan RL, Ready DF (1989b) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3:1099–1112

    Article  PubMed  CAS  Google Scholar 

  • Cain S, Martinez G, Kokkinos MI, Turner K, Richardson RJ, Abud HE, Huelsken J, Robinson ML, de Iongh RU (2008) Differential requirement for beta-catenin in epithelial and fiber cells during lens development. Dev Biol 321:420–433

    Article  PubMed  CAS  Google Scholar 

  • Canon J, Banerjee U (2003) In vivo analysis of a developmental circuit for direct transcriptional activation and repression in the same cell by a Runx protein. Genes Dev 17:838–843

    Article  PubMed  CAS  Google Scholar 

  • Chamberlain CG, McAvoy JW (1987) Evidence that fibroblast growth factor promotes lens fibre differentiation. Curr Eye Res 6:1165–1169

    Article  PubMed  CAS  Google Scholar 

  • Charlton-Perkins M, Cook TA (2010) Building a fly eye: terminal differentiation events of the retina, corneal lens, and pigmented epithelia. Curr Top Dev Biol 93:129–173

    Article  PubMed  Google Scholar 

  • Charlton-Perkins M, Whitaker SL, Fei Y, Xie B, Li-Kroeger D, Gebelein B, Cook T (2011) Prospero and Pax2 combinatorially control neural cell fate decisions by modulating Ras- and Notch-dependent signaling. Neural Dev 6:20

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Stump RJ, Lovicu FJ, Shimono A, McAvoy JW (2008) Wnt signaling is required for organization of the lens fiber cell cytoskeleton and development of lens three-dimensional architecture. Dev Biol 324:161–176

    Article  PubMed  CAS  Google Scholar 

  • Cheyette BN, Green PJ, Martin K, Garren H, Hartenstein V, Zipursky SL (1994) The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12:977–996

    Article  PubMed  CAS  Google Scholar 

  • Chow RL, Altmann CR, Lang RA, Hemmati-Brivanlou A (1999) Pax6 induces ectopic eyes in a vertebrate. Development 126:4213–4222

    PubMed  CAS  Google Scholar 

  • Clayton FE (1957) The effect of Lozenge Pseudoalleles on eye pigmentation in Drosophila melanogaster. I. Brown pigment and pigmentation in Lozenge males. Genetics 42:28–41

    PubMed  CAS  Google Scholar 

  • Cook T, Pichaud F, Sonneville R, Papatsenko D, Desplan C (2003) Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev Cell 4:853–864

    Article  PubMed  CAS  Google Scholar 

  • Cordero JB, Cagan RL (2010) Canonical wingless signaling regulates cone cell specification in the Drosophila retina. Dev Dyn 239:875–884

    Article  PubMed  CAS  Google Scholar 

  • Cordero J, Jassim O, Bao S, Cagan R (2004) A role for wingless in an early pupal cell death event that contributes to patterning the Drosophila eye. Mech Dev 121:1523–1530

    Article  PubMed  CAS  Google Scholar 

  • Cordero JB, Larson DE, Craig CR, Hays R, Cagan R (2007) Dynamic decapentaplegic signaling regulates patterning and adhesion in the Drosophila pupal retina. Development 134:1861–1871

    Article  PubMed  CAS  Google Scholar 

  • Cui W, Tomarev SI, Piatigorsky J, Chepelinsky AB, Duncan MK (2004) Mafs, Prox1, and Pax6 can regulate chicken betaB 1-crystallin gene expression. J Biol Chem 279:11088–11095

    Article  PubMed  CAS  Google Scholar 

  • Cvekl A, Duncan MK (2007) Genetic and epigenetic mechanisms of gene regulation during lens development. Prog Retin Eye Res 26:555–597

    Article  PubMed  CAS  Google Scholar 

  • Cvekl A, Yang Y, Chauhan BK, Cveklova K (2004) Regulation of gene expression by Pax6 in ocular cells: a case of tissue-preferred expression of crystallins in lens. Int J Dev Biol 48:829–844

    Article  PubMed  CAS  Google Scholar 

  • Daga A, Karlovich CA, Dumstrei K, Banerjee U (1996) Patterning of cells in the Drosophila eye by Lozenge, which shares homologous domains with AML1. Genes Dev 10:1194–1205

    Article  PubMed  CAS  Google Scholar 

  • de Iongh RU, Lovicu FJ, Overbeek PA, Schneider MD, Joya J, Hardeman ED, McAvoy JW (2001) Requirement for TGFbeta receptor signaling during terminal lens fiber differentiation. Development 128:3995–4010

    PubMed  Google Scholar 

  • de Iongh RU, Wederell E, Lovicu FJ, McAvoy JW (2005) Transforming growth factor-beta-induced epithelial-mesenchymal transition in the lens: a model for cataract formation. Cells Tissues Organs 179:43–55

    Article  PubMed  CAS  Google Scholar 

  • de Nooij JC, Hariharan IK (1995) Uncoupling cell fate determination from patterned cell division in the Drosophila eye. Science 270:983–985

    Article  PubMed  Google Scholar 

  • Dhanasekaran DN, Reddy EP (2008) JNK signaling in apoptosis. Oncogene 27:6245–6251

    Article  PubMed  CAS  Google Scholar 

  • Dickson B, Hafen E (1994) Genetics of signal transduction in invertebrates. Curr Opin Genet Dev 4:64–70

    Article  PubMed  CAS  Google Scholar 

  • Dickson B, Sprenger F, Hafen E (1992) Prepattern in the developing Drosophila eye revealed by an activated torso—sevenless chimeric receptor. Genes Dev 6:2327–2339

    Article  PubMed  CAS  Google Scholar 

  • Donner AL, Maas RL (2004) Conservation and non-conservation of genetic pathways in eye specification. Int J Dev Biol 48:743–753

    Article  PubMed  Google Scholar 

  • Donner AL, Lachke SA, Maas RL (2006) Lens induction in vertebrates: variations on a conserved theme of signaling events. Semin Cell Dev Biol 17:676–685

    Article  PubMed  CAS  Google Scholar 

  • Doroquez DB, Rebay I (2006) Signal integration during development: mechanisms of EGFR and Notch pathway function and cross-talk. Crit Rev Biochem Mol Biol 41:339–385

    Article  PubMed  CAS  Google Scholar 

  • Duncan MK, Cui W, Oh DJ, Tomarev SI (2002) Prox1 is differentially localized during lens development. Mech Dev 112:195–198

    Article  PubMed  CAS  Google Scholar 

  • Dziedzic K, Heaphy J, Prescott H, Kavaler J (2009) The transcription factor D-Pax2 regulates crystallin production during eye development in Drosophila melanogaster. Dev Dyn 238:2530–2539

    Article  PubMed  CAS  Google Scholar 

  • Edwards JS, Meyer MR (1990) Conservation of antigen 3G6: a crystalline cone constituent in the compound eye of arthropods. J Neurobiol 21:441–452

    Article  PubMed  CAS  Google Scholar 

  • Eiraku M, Takata N, Ishibashi H, Kawada M, Sakakura E, Okuda S, Sekiguchi K, Adachi T, Sasai Y (2011) Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472:51–56

    Article  PubMed  CAS  Google Scholar 

  • Epstein J, Cai J, Glaser T, Jepeal L, Maas R (1994) Identification of a Pax paired domain recognition sequence and evidence for DNA-dependent conformational changes. J Biol Chem 269:8355–8361

    PubMed  CAS  Google Scholar 

  • Faber SC, Robinson ML, Makarenkova HP, Lang RA (2002) Bmp signaling is required for development of primary lens fiber cells. Development 129:3727–3737

    PubMed  CAS  Google Scholar 

  • Fisher M, Grainger RM (2004) Lens induction and determination. In: Lovicu FJ, Robinson ML (eds) Development of the ocular lens. Cambridge University Press, New York, pp 27–47

    Chapter  Google Scholar 

  • Flores GV, Duan H, Yan H, Nagaraj R, Fu W, Zou Y, Noll M, Banerjee U (2000) Combinatorial signaling in the specification of unique cell fates. Cell 103:75–85

    Article  PubMed  CAS  Google Scholar 

  • Fortini ME (2009) Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 16:633–647

    Article  PubMed  CAS  Google Scholar 

  • Franciscovich AL, Mortimer AD, Freeman AA, Gu J, Sanyal S (2008) Overexpression screen in Drosophila identifies neuronal roles of GSK-3 beta/shaggy as a regulator of AP-1-dependent developmental plasticity. Genetics 180:2057–2071

    Article  PubMed  CAS  Google Scholar 

  • Frankfort BJ, Mardon G (2002) R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 129:1295–1306

    PubMed  CAS  Google Scholar 

  • Freeman M (1996) Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87:651–660

    Article  PubMed  CAS  Google Scholar 

  • Freeman M (1997) Cell determination strategies in the Drosophila eye. Development 124:261–270

    PubMed  CAS  Google Scholar 

  • Frohlich A (2001) A scanning electron-microscopic study of apical contacts in the eye during postembryonic development of Drosophila melanogaster. Cell Tissue Res 303:117–128

    Article  PubMed  CAS  Google Scholar 

  • Fu W, Noll M (1997) The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye. Genes Dev 11:2066–2078

    Article  PubMed  CAS  Google Scholar 

  • Fuhrmann S (2008) Wnt signaling in eye organogenesis. Organogenesis 4:60–67

    Article  PubMed  Google Scholar 

  • Fujita SC, Zipursky SL, Benzer S, Ferrus A, Shotwell SL (1982) Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci USA 79:7929–7933

    Article  PubMed  CAS  Google Scholar 

  • Furuta Y, Hogan BL (1998) BMP4 is essential for lens induction in the mouse embryo. Genes Dev 12:3764–3775

    Article  PubMed  CAS  Google Scholar 

  • Gehring WJ (1996) The master control gene for morphogenesis and evolution of the eye. Genes Cells 1:11–15

    Article  PubMed  CAS  Google Scholar 

  • Gehring WJ (2005) New perspectives on eye development and the evolution of eyes and photoreceptors. J Hered 96:171–184

    Article  PubMed  CAS  Google Scholar 

  • Gehring WJ, Ikeo K (1999) Pax 6: mastering eye morphogenesis and eye evolution. Trends Genet 15:371–377

    Article  PubMed  CAS  Google Scholar 

  • Glass AS, Dahm R (2004) The zebrafish as a model organism for eye development. Ophthal Res 36:4–24

    Article  Google Scholar 

  • Gorski SM, Brachmann CB, Tanenbaum SB, Cagan RL (2000) Delta and notch promote correct localization of irreC-rst. Cell Death Differ 7:1011–1013

    Article  PubMed  CAS  Google Scholar 

  • Gould DB, Smith RS, John SW (2004) Anterior segment development relevant to glaucoma. Int J Dev Biol 48:1015–1029

    Article  PubMed  Google Scholar 

  • Greenwald I, Rubin GM (1992) Making a difference: the role of cell-cell interactions in establishing separate identities for equivalent cells. Cell 68:271–281

    Article  PubMed  CAS  Google Scholar 

  • Grillo-Hill BK, Wolff T (2009) Dynamic cell shapes and contacts in the developing Drosophila retina are regulated by the Ig cell adhesion protein hibris. Dev Dyn 238:2223–2234

    Article  PubMed  Google Scholar 

  • Guo M, Jan LY, Jan YN (1996) Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17:27–41

    Article  PubMed  Google Scholar 

  • Halder G, Callaerts P, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788–1792

    Article  PubMed  CAS  Google Scholar 

  • Halder G, Callaerts P, Flister S, Walldorf U, Kloter U, Gehring WJ (1998) Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development 125:2181–2191

    PubMed  CAS  Google Scholar 

  • Han JD, Baker NE, Rubin CS (1997) Molecular characterization of a novel A kinase anchor protein from Drosophila melanogaster. J Biol Chem 272:26611–26619

    Article  PubMed  CAS  Google Scholar 

  • Hay N (2011) Interplay between FOXO, TOR, and Akt. Biochim Biophys Acta-Mol Cell Res [Epub ahead of print]

  • Hayashi T, Carthew RW (2004) Surface mechanics mediate pattern formation in the developing retina. Nature 431:647–652

    Article  PubMed  CAS  Google Scholar 

  • Hayashi T, Kojima T, Saigo K (1998) Specification of primary pigment cell and outer photoreceptor fates by BarH1 homeobox gene in the developing Drosophila eye. Dev Biol 200:131–145

    Article  PubMed  CAS  Google Scholar 

  • Hayashi T, Xu C, Carthew RW (2008) Cell-type-specific transcription of prospero is controlled by combinatorial signaling in the Drosophila eye. Development 135:2787–2796

    Article  PubMed  CAS  Google Scholar 

  • Heberlein U, Wolff T, Rubin GM (1993) The TGF beta homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75:913–926

    Article  PubMed  CAS  Google Scholar 

  • Held LI (2002) Imaginal discs: the genetic and cellular logic of pattern formation. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Higashijima S, Kojima T, Michiue T, Ishimaru S, Emori Y, Saigo K (1992) Dual Bar homeo box genes of Drosophila required in two photoreceptor cells, R1 and R6, and primary pigment cells for normal eye development. Genes Dev 6:50–60

    Article  PubMed  CAS  Google Scholar 

  • Ho HY, Chang KH, Nichols J, Li M (2009) Homeodomain protein Pitx3 maintains the mitotic activity of lens epithelial cells. Mech Dev 126:18–29

    Article  PubMed  CAS  Google Scholar 

  • Hsiung F, Moses K (2002) Retinal development in Drosophila: specifying the first neuron. Hum Mol Genet 11:1207–1214

    Article  PubMed  CAS  Google Scholar 

  • Igaki T (2009) Correcting developmental errors by apoptosis: lessons from Drosophila JNK signaling. Apoptosis 14:1021–1028

    Article  PubMed  Google Scholar 

  • Ingolia TD, Craig EA (1982) Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. Proc Natl Acad Sci USA 79:2360–2364

    Article  PubMed  CAS  Google Scholar 

  • Iyengar L, Patkunanathan B, Lynch OT, McAvoy JW, Rasko JE, Lovicu FJ (2006) Aqueous humour- and growth factor-induced lens cell proliferation is dependent on MAPK/ERK1/2 and Akt/PI3-K signalling. Exp Eye Res 83:667–678

    Article  PubMed  CAS  Google Scholar 

  • Jackson Behan K, Fair J, Singh S, Bogwitz M, Perry T, Grubor V, Cunningham F, Nichols CD, Cheung TL, Batterham P, Pollock JA (2005) Alternative splicing removes an Ets interaction domain from Lozenge during Drosophila eye development. Dev Genes Evol 215:423–435

    Article  PubMed  CAS  Google Scholar 

  • Jia J, Lin M, Zhang L, York JP, Zhang P (2007) The notch signaling pathway controls the size of the ocular lens by directly suppressing p57Kip2 expression. Mol Cell Biol 27:7236–7247

    Article  PubMed  CAS  Google Scholar 

  • Kamachi Y, Uchikawa M, Tanouchi A, Sekido R, Kondoh H (2001) Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes Dev 15:1272–1286

    Article  PubMed  CAS  Google Scholar 

  • Kanda H, Miura M (2004) Regulatory roles of JNK in programmed cell death. J Biochem 136:1–6

    Article  PubMed  CAS  Google Scholar 

  • Karsenty G, Luo G, Hofmann C, Bradley A (1996) BMP 7 is required for nephrogenesis, eye development, and skeletal patterning. Ann N Y Acad Sci 785:98–107

    Article  PubMed  CAS  Google Scholar 

  • Kauffmann RC, Li S, Gallagher PA, Zhang J, Carthew RW (1996) Ras1 signaling and transcriptional competence in the R7 cell of Drosophila. Genes Dev 10:2167–2178

    Article  PubMed  CAS  Google Scholar 

  • Kawauchi S, Takahashi S, Nakajima O, Ogino H, Morita M, Nishizawa M, Yasuda K, Yamamoto M (1999) Regulation of lens fiber cell differentiation by transcription factor c-Maf. J Biol Chem 274:19254–19260

    Article  PubMed  CAS  Google Scholar 

  • Kenyon KL, Moody SA, Jamrich M (1999) A novel fork head gene mediates early steps during Xenopus lens formation. Development 126:5107–5116

    PubMed  CAS  Google Scholar 

  • Kim JI, Li T, Ho IC, Grusby MJ, Glimcher LH (1999) Requirement for the c-Maf transcription factor in crystallin gene regulation and lens development. Proc Natl Acad Sci USA 96:3781–3785

    Article  PubMed  CAS  Google Scholar 

  • Kim E, Choi Y, Lee S, Seo Y, Yoon J, Baek K (2008) Characterization of the Drosophila melanogaster retinin gene encoding a cornea-specific protein. Insect Mol Biol 17:537–543

    Article  PubMed  CAS  Google Scholar 

  • Klesert TR, Cho DH, Clark JI, Maylie J, Adelman J, Snider L, Yuen EC, Soriano P, Tapscott SJ (2000) Mice deficient in Six5 develop cataracts: implications for myotonic dystrophy. Nat Genet 25:105–109

    Article  PubMed  CAS  Google Scholar 

  • Komori N, Usukura J, Matsumoto H (1992) Drosocrystallin, a major 52 kDa glycoprotein of the Drosophila melanogaster corneal lens. Purification, biochemical characterization, and subcellular localization. J Cell Sci 102(Pt 2):191–201

    PubMed  CAS  Google Scholar 

  • Kondoh H, Uchikawa M, Kamachi Y (2004) Interplay of Pax6 and SOX2 in lens development as a paradigm of genetic switch mechanisms for cell differentiation. Int J Dev Biol 48:819–827

    Article  PubMed  CAS  Google Scholar 

  • Kopan R, Ilagan MX (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137:216–233

    Article  PubMed  CAS  Google Scholar 

  • Kozmik Z (2005) Pax genes in eye development and evolution. Curr Opin Genet Dev 15:430–438

    Article  PubMed  CAS  Google Scholar 

  • Kozmik Z, Daube M, Frei E, Norman B, Kos L, Dishaw LJ, Noll M, Piatigorsky J (2003) Role of Pax genes in eye evolution: a cnidarian PaxB gene uniting Pax2 and Pax6 functions. Dev Cell 5:773–785

    Article  PubMed  CAS  Google Scholar 

  • Kumar JP (2001) Signalling pathways in Drosophila and vertebrate retinal development. Nat Rev Genet 2:846–857

    Article  PubMed  CAS  Google Scholar 

  • Kumar JP (2010) Retinal determination the beginning of eye development. Curr Top Dev Biol 93:1–28

    Article  PubMed  Google Scholar 

  • Kumar J, Moses K (1997) Transcription factors in eye development: a gorgeous mosaic? Genes Dev 11:2023–2028

    Article  PubMed  CAS  Google Scholar 

  • Lachke SA, Maas RL (2010) Building the developmental oculome: systems biology in vertebrate eye development and disease. Wiley Interdiscip Rev Syst Biol Med 2:305–323

    Article  PubMed  CAS  Google Scholar 

  • Lai ZC, Rubin GM (1992) Negative control of photoreceptor development in Drosophila by the product of the yan gene, an ETS domain protein. Cell 70:609–620

    Article  PubMed  CAS  Google Scholar 

  • Lai ZC, Fetchko M, Li Y (1997) Repression of Drosophila photoreceptor cell fate through cooperative action of two transcriptional repressors Yan and Tramtrack. Genetics 147:1131–1137

    PubMed  CAS  Google Scholar 

  • Lang RA (2004) Pathways regulating lens induction in the mouse. Int J Dev Biol 48:783–791

    Article  PubMed  CAS  Google Scholar 

  • Le TT, Conley KW, Brown NL (2009) Jagged 1 is necessary for normal mouse lens formation. Dev Biol 328:118–126

    Article  PubMed  CAS  Google Scholar 

  • Lee HH, Frasch M (2004) Survey of forkhead domain encoding genes in the Drosophila genome: classification and embryonic expression patterns. Dev Dyn 229:357–366 (an official publication of the American Association of Anatomists)

    Article  PubMed  CAS  Google Scholar 

  • Lee HY, Wroblewski E, Philips GT, Stair CN, Conley K, Reedy M, Mastick GS, Brown NL (2005) Multiple requirements for Hes 1 during early eye formation. Dev Biol 284:464–478

    Article  PubMed  CAS  Google Scholar 

  • Lengler J, Krausz E, Tomarev S, Prescott A, Quinlan RA, Graw J (2001) Antagonistic action of Six3 and Prox1 at the gamma-crystallin promoter. Nucleic Acids Res 29:515–526

    Article  PubMed  CAS  Google Scholar 

  • Leptin M, Aebersold R, Wilcox M (1987) Drosophila position-specific antigens resemble the vertebrate fibronectin-receptor family. EMBO J 6:1037–1043

    PubMed  CAS  Google Scholar 

  • Li S, Li Y, Carthew RW, Lai ZC (1997) Photoreceptor cell differentiation requires regulated proteolysis of the transcriptional repressor Tramtrack. Cell 90:469–478

    Article  PubMed  CAS  Google Scholar 

  • Lim HY, Tomlinson A (2006) Organization of the peripheral fly eye: the roles of Snail family transcription factors in peripheral retinal apoptosis. Development 133:3529–3537

    Article  PubMed  CAS  Google Scholar 

  • Liu W, Lagutin OV, Mende M, Streit A, Oliver G (2006) Six3 activation of Pax6 expression is essential for mammalian lens induction and specification. EMBO J 25:5383–5395

    Article  PubMed  CAS  Google Scholar 

  • Longley RL Jr, Ready DF (1995) Integrins and the development of three-dimensional structure in the Drosophila compound eye. Dev Biol 171:415–433

    Article  PubMed  CAS  Google Scholar 

  • Lovicu FJ, McAvoy JW (2005) Growth factor regulation of lens development. Dev Biol 280:1–14

    Article  PubMed  CAS  Google Scholar 

  • Lovicu FJ, Overbeek PA (1998) Overlapping effects of different members of the FGF family on lens fiber differentiation in transgenic mice. Development 125:3365–3377

    PubMed  CAS  Google Scholar 

  • Lovicu FJ, Robinson ML (2004) Development of the ocular lens. New York, Cambridge University Press

    Book  Google Scholar 

  • Luo G, Hofmann C, Bronckers AL, Sohocki M, Bradley A, Karsenty G (1995) BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev 9:2808–2820

    Article  PubMed  CAS  Google Scholar 

  • Marin R, Demers M, Tanguay RM (1996) Cell-specific heat-shock induction of Hsp23 in the eye of Drosophila melanogaster. Cell Stress Chaperones 1:40–46

    Article  PubMed  CAS  Google Scholar 

  • Martinez G, de Iongh RU (2010) The lens epithelium in ocular health and disease. Int J Biochem Cell Biol 42:1945–1963

    Article  PubMed  CAS  Google Scholar 

  • Martinez G, Wijesinghe M, Turner K, Abud HE, Taketo MM, Noda T, Robinson ML, de Iongh RU (2009) Conditional mutations of beta-catenin and APC reveal roles for canonical Wnt signaling in lens differentiation. Invest Ophthalmol Vis Sci 50:4794–4806

    Article  PubMed  Google Scholar 

  • Mathers PH, Grinberg A, Mahon KA, Jamrich M (1997) The Rx homeobox gene is essential for vertebrate eye development. Nature 387:603–607

    Article  PubMed  CAS  Google Scholar 

  • Matsuo T, Takahashi K, Kondo S, Kaibuchi K, Yamamoto D (1997) Regulation of cone cell formation by Canoe and Ras in the developing Drosophila eye. Development 124:2671–2680

    PubMed  CAS  Google Scholar 

  • Matzuk MM, Kumar TR, Vassalli A, Bickenbach JR, Roop DR, Jaenisch R, Bradley A (1995) Functional analysis of activins during mammalian development. Nature 374:354–356

    Article  PubMed  CAS  Google Scholar 

  • McAvoy JW (1978) Cell division, cell elongation and distribution of alpha-, beta- and gamma-crystallins in the rat lens. J Embryol Exp Morphol 44:149–165

    PubMed  CAS  Google Scholar 

  • McAvoy JW, Chamberlain CG (1989) Fibroblast growth factor (FGF) induces different responses in lens epithelial cells depending on its concentration. Development 107:221–228

    PubMed  CAS  Google Scholar 

  • McAvoy JW, Chamberlain CG, de Iongh RU, Hales AM, Lovicu FJ (1999) Lens development. Eye (Lond) 13(Pt 3b):425–437

    Google Scholar 

  • McNeill H (2002) Planar polarity: location, location, location. Curr Biol 12:R449–R451

    Article  PubMed  CAS  Google Scholar 

  • Medina-Martinez O, Jamrich M (2007) Foxe3 view of lens development and disease. Development 134:1455–1463

    Article  PubMed  CAS  Google Scholar 

  • Medina-Martinez O, Brownell I, Amaya-Manzanares F, Hu Q, Behringer RR, Jamrich M (2005) Severe defects in proliferation and differentiation of lens cells in Foxe3 null mice. Mol Cell Biol 25:8854–8863

    Article  PubMed  CAS  Google Scholar 

  • Medina-Martinez O, Shah R, Jamrich M (2009) Pitx3 controls multiple aspects of lens development. Dev Dyn 238:2193–2201

    Article  PubMed  CAS  Google Scholar 

  • Moses K, Ellis MC, Rubin GM (1989) The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells. Nature 340:531–536

    Article  PubMed  CAS  Google Scholar 

  • Moustakas A, Heldin CH (2009) The regulation of TGFbeta signal transduction. Development 136:3699–3714

    Article  PubMed  CAS  Google Scholar 

  • Nagaraj R, Banerjee U (2004) The little R cell that could. Int J Dev Biol 48:755–760

    Article  PubMed  CAS  Google Scholar 

  • Nagaraj R, Banerjee U (2007) Combinatorial signaling in the specification of primary pigment cells in the Drosophila eye. Development 134:825–831

    Article  PubMed  CAS  Google Scholar 

  • Nagaraj R, Banerjee U (2009) Regulation of Notch and Wingless signalling by phyllopod, a transcriptional target of the EGFR pathway. EMBO J 28:337–346

    Article  PubMed  CAS  Google Scholar 

  • Niessen CM, Leckband D, Yap AS (2011) Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation. Physiol Rev 91:691–731

    Article  PubMed  CAS  Google Scholar 

  • Nilsson DE, Kelber A (2007) A functional analysis of compound eye evolution. Arthropod Struct Dev 36:373–385

    Article  PubMed  Google Scholar 

  • Nishiguchi S, Wood H, Kondoh H, Lovell-Badge R, Episkopou V (1998) Sox1 directly regulates the gamma-crystallin genes and is essential for lens development in mice. Genes Dev 12:776–781

    Article  PubMed  CAS  Google Scholar 

  • Ogino H, Fisher M, Grainger RM (2008) Convergence of a head-field selector Otx2 and Notch signaling: a mechanism for lens specification. Development 135:249–258

    Article  PubMed  CAS  Google Scholar 

  • Onuma Y, Takahashi S, Asashima M, Kurata S, Gehring WJ (2002) Conservation of Pax 6 function and upstream activation by Notch signaling in eye development of frogs and flies. Proc Natl Acad Sci USA 99:2020–2025

    Article  PubMed  CAS  Google Scholar 

  • Pan Y, Carbe C, Powers A, Feng GS, Zhang X (2010) Sprouty2-modulated Kras signaling rescues Shp2 deficiency during lens and lacrimal gland development. Development 137:1085–1093

    Article  PubMed  CAS  Google Scholar 

  • Parks AL, Turner FR, Muskavitch MA (1995) Relationships between complex Delta expression and the specification of retinal cell fates during Drosophila eye development. Mech Dev 50:201–216

    Article  PubMed  CAS  Google Scholar 

  • Patterson JT, Muller HJ (1930) Are “Progressive” Mutations Produced by X-Rays? Genetics 15:495–577

    PubMed  CAS  Google Scholar 

  • Pauli D, Arrigo AP, Vazquez J, Tonka CH, Tissieres A (1989) Expression of the small heat shock genes during Drosophila development: comparison of the accumulation of hsp23 and hsp27 mRNAs and polypeptides. Genome 31:671–676

    Article  PubMed  CAS  Google Scholar 

  • Piatigorsky J (2003) Crystallin genes: specialization by changes in gene regulation may precede gene duplication. J Struct Funct Genomics 3:131–137

    Article  PubMed  CAS  Google Scholar 

  • Pontoriero GF, Smith AN, Miller LA, Radice GL, West-Mays JA, Lang RA (2009) Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival. Dev Biol 326:403–417

    Article  PubMed  CAS  Google Scholar 

  • Proetzel G, Pawlowski SA, Wiles MV, Yin M, Boivin GP, Howles PN, Ding J, Ferguson MW, Doetschman T (1995) Transforming growth factor-beta 3 is required for secondary palate fusion. Nat Genet 11:409–414

    Article  PubMed  CAS  Google Scholar 

  • Purcell P, Oliver G, Mardon G, Donner AL, Maas RL (2005) Pax6-dependence of Six3, Eya1 and Dach1 expression during lens and nasal placode induction. Gene Expr Patterns 6:110–118

    Article  PubMed  CAS  Google Scholar 

  • Quiring R, Walldorf U, Kloter U, Gehring WJ (1994) Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 265:785–789

    Article  PubMed  CAS  Google Scholar 

  • Rajagopal R, Dattilo LK, Kaartinen V, Deng CX, Umans L, Zwijsen A, Roberts AB, Bottinger EP, Beebe DC (2008) Functions of the type 1 BMP receptor Acvr1 (Alk2) in lens development: cell proliferation, terminal differentiation, and survival. Invest Ophthalmol Vis Sci 49:4953–4960

    Article  PubMed  Google Scholar 

  • Rajagopal R, Huang J, Dattilo LK, Kaartinen V, Mishina Y, Deng CX, Umans L, Zwijsen A, Roberts AB, Beebe DC (2009) The type I BMP receptors, Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Dev Biol 335:305–316

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen JT, Deardorff MA, Tan C, Rao MS, Klein PS, Vetter ML (2001) Regulation of eye development by frizzled signaling in Xenopus. Proc Natl Acad Sci USA 98:3861–3866

    Article  PubMed  CAS  Google Scholar 

  • Read D, Manley JL (1992) Alternatively spliced transcripts of the Drosophila tramtrack gene encode zinc finger proteins with distinct DNA binding specificities. EMBO J 11:1035–1044

    PubMed  CAS  Google Scholar 

  • Reza HM, Yasuda K (2004) Roles of Maf family proteins in lens development. Dev Dyn 229:440–448

    Article  PubMed  CAS  Google Scholar 

  • Rickenbacher J (1954) Polished (pol), a new eye mutant in the 4th chromosome in Drosophila melanogaster. Z Indukt Abstamm Vererbungsl 86:61–68

    Article  PubMed  CAS  Google Scholar 

  • Rieger DK, Reichenberger E, McLean W, Sidow A, Olsen BR (2001) A double-deletion mutation in the Pitx3 gene causes arrested lens development in aphakia mice. Genomics 72:61–72

    Article  PubMed  CAS  Google Scholar 

  • Ring BZ, Cordes SP, Overbeek PA, Barsh GS (2000) Regulation of mouse lens fiber cell development and differentiation by the Maf gene. Development 127:307–317

    PubMed  CAS  Google Scholar 

  • Robinson ML, MacMillan-Crow LA, Thompson JA, Overbeek PA (1995) Expression of a truncated FGF receptor results in defective lens development in transgenic mice. Development 121:3959–3967

    PubMed  CAS  Google Scholar 

  • Rohrbaugh M, Ramos E, Nguyen D, Price M, Wen Y, Lai ZC (2002) Notch activation of yan expression is antagonized by RTK/pointed signaling in the Drosophila eye. Curr Biol 12:576–581

    Article  PubMed  CAS  Google Scholar 

  • Roignant JY, Treisman JE (2009) Pattern formation in the Drosophila eye disc. Int J Dev Biol 53:795–804

    Article  PubMed  CAS  Google Scholar 

  • Rowan S, Conley KW, Le TT, Donner AL, Maas RL, Brown NL (2008) Notch signaling regulates growth and differentiation in the mammalian lens. Dev Biol 321:111–122

    Article  PubMed  CAS  Google Scholar 

  • Rusconi JC, Fink JL, Cagan R (2004) klumpfuss regulates cell death in the Drosophila retina. Mech Dev 121:537–546

    Article  PubMed  CAS  Google Scholar 

  • Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T (1997) TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124:2659–2670

    PubMed  CAS  Google Scholar 

  • Saravanamuthu SS, Gao CY, Zelenka PS (2009) Notch signaling is required for lateral induction of Jagged1 during FGF-induced lens fiber differentiation. Dev Biol 332:166–176

    Article  PubMed  CAS  Google Scholar 

  • Sarkar PS, Appukuttan B, Han J, Ito Y, Ai C, Tsai W, Chai Y, Stout JT, Reddy S (2000) Heterozygous loss of Six5 in mice is sufficient to cause ocular cataracts. Nat Genet 25:110–114

    Article  PubMed  CAS  Google Scholar 

  • Seimiya M, Gehring WJ (2000) The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. Development 127:1879–1886

    PubMed  CAS  Google Scholar 

  • Semina EV, Reiter RS, Murray JC (1997) Isolation of a new homeobox gene belonging to the Pitx/Rieg family: expression during lens development and mapping to the aphakia region on mouse chromosome 19. Hum Mol Genet 6:2109–2116

    Article  PubMed  CAS  Google Scholar 

  • Seo HC, Curtiss J, Mlodzik M, Fjose A (1999) Six class homeobox genes in Drosophila belong to three distinct families and are involved in head development. Mech Dev 83:127–139

    Article  PubMed  CAS  Google Scholar 

  • Seppa MJ, Johnson RI, Bao S, Cagan RL (2008) Polychaetoid controls patterning by modulating adhesion in the Drosophila pupal retina. Dev Biol 318:1–16

    Article  PubMed  CAS  Google Scholar 

  • Serikaku MA, O’Tousa JE (1994) sine oculis is a homeobox gene required for Drosophila visual system development. Genetics 138:1137–1150

    PubMed  CAS  Google Scholar 

  • Shaham O, Smith AN, Robinson ML, Taketo MM, Lang RA, Ashery-Padan R (2009) Pax6 is essential for lens fiber cell differentiation. Development 136:2567–2578

    Article  PubMed  CAS  Google Scholar 

  • Shamloula HK, Mbogho MP, Pimentel AC, Chrzanowska-Lightowlers ZM, Hyatt V, Okano H, Venkatesh TR (2002) rugose (rg), a Drosophila A kinase anchor protein, is required for retinal pattern formation and interacts genetically with multiple signaling pathways. Genetics 161:693–710

    PubMed  CAS  Google Scholar 

  • Shull MM, Doetschman T (1994) Transforming growth factor-beta 1 in reproduction and development. Mol Reprod Dev 39:239–246

    Article  PubMed  CAS  Google Scholar 

  • Siddall NA, Behan KJ, Crew JR, Cheung TL, Fair JA, Batterham P, Pollock JA (2003) Mutations in lozenge and D-Pax2 invoke ectopic patterned cell death in the developing Drosophila eye using distinct mechanisms. Dev Genes Evol 213:107–119

    PubMed  CAS  Google Scholar 

  • Siddall NA, Hime GR, Pollock JA, Batterham P (2009) Ttk69-dependent repression of lozenge prevents the ectopic development of R7 cells in the Drosophila larval eye disc. BMC Dev Biol 9:64

    Article  PubMed  CAS  Google Scholar 

  • Smith AN, Miller LA, Song N, Taketo MM, Lang RA (2005) The duality of beta-catenin function: a requirement in lens morphogenesis and signaling suppression of lens fate in periocular ectoderm. Dev Biol 285:477–489

    Article  PubMed  CAS  Google Scholar 

  • Spemann H (1938) Embryonic development and induction. Hafner, New York

    Google Scholar 

  • Strodicke M, Karberg S, Korge G (2000) Domina (Dom), a new Drosophila member of the FKH/WH gene family, affects morphogenesis and is a suppressor of position-effect variegation. Mech Dev 96:67–78

    Article  PubMed  CAS  Google Scholar 

  • Stump RJ, Ang S, Chen Y, von Bahr T, Lovicu FJ, Pinson K, de Iongh RU, Yamaguchi TP, Sassoon DA, McAvoy JW (2003) A role for Wnt/beta-catenin signaling in lens epithelial differentiation. Dev Biol 259:48–61

    Article  PubMed  CAS  Google Scholar 

  • Swanson CI, Evans NC, Barolo S (2010) Structural rules and complex regulatory circuitry constrain expression of a Notch- and EGFR-regulated eye enhancer. Dev Cell 18:359–370

    Article  PubMed  CAS  Google Scholar 

  • Tang AH, Neufeld TP, Kwan E, Rubin GM (1997) PHYL acts to down-regulate TTK88, a transcriptional repressor of neuronal cell fates, by a SINA-dependent mechanism. Cell 90:459–467

    Article  PubMed  CAS  Google Scholar 

  • Thompson B, Townsley F, Rosin-Arbesfeld R, Musisi H, Bienz M (2002) A new nuclear component of the Wnt signalling pathway. Nat Cell Biol 4:367–373

    Article  PubMed  CAS  Google Scholar 

  • Tomarev SI, Piatigorsky J (1996) Lens crystallins of invertebrates—diversity and recruitment from detoxification enzymes and novel proteins. Eur J Biochem 235:449–465

    Article  PubMed  CAS  Google Scholar 

  • Tomarev SI, Zinovieva RD, Chang B, Hawes NL (1998) Characterization of the mouse Prox1 gene. Biochem Biophys Res Commun 248:684–689

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson A, Struhl G (2001) Delta/Notch and Boss/Sevenless signals act combinatorially to specify the Drosophila R7 photoreceptor. Molecular cell 7:487–495

    Article  PubMed  CAS  Google Scholar 

  • Tsuda L, Nagaraj R, Zipursky SL, Banerjee U (2002) An EGFR/Ebi/Sno pathway promotes delta expression by inactivating Su(H)/SMRTER repression during inductive notch signaling. Cell 110:625–637

    Article  PubMed  CAS  Google Scholar 

  • Vassalli A, Matzuk MM, Gardner HA, Lee KF, Jaenisch R (1994) Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev 8:414–427

    Article  PubMed  CAS  Google Scholar 

  • Vivekanand P, Rebay I (2006) Intersection of signal transduction pathways and development. Annu Rev Genet 40:139–157

    Article  PubMed  CAS  Google Scholar 

  • Voas MG, Rebay I (2004) Signal integration during development: insights from the Drosophila eye. Dev Dyn 229:162–175

    Article  PubMed  CAS  Google Scholar 

  • Wang MC, Bohmann D, Jasper H (2005) JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121:115–125

    Article  PubMed  CAS  Google Scholar 

  • Wassarman DA, Therrien M, Rubin GM (1995) The Ras signaling pathway in Drosophila. Curr Opin Genet Dev 5:44–50

    Article  PubMed  CAS  Google Scholar 

  • Weber GF, Menko AS (2006) Phosphatidylinositol 3-kinase is necessary for lens fiber cell differentiation and survival. Invest Ophthalmol Vis Sci 47:4490–4499

    Article  PubMed  Google Scholar 

  • Wech I, Nagel AC (2005) Mutations in rugose promote cell type-specific apoptosis in the Drosophila eye. Cell Death Differ 12:145–152

    Article  PubMed  CAS  Google Scholar 

  • Wigle JT, Chowdhury K, Gruss P, Oliver G (1999) Prox1 function is crucial for mouse lens-fibre elongation. Nat Genet 21:318–322

    Article  PubMed  CAS  Google Scholar 

  • Wilcox M, Brown N, Piovant M, Smith RJ, White RA (1984) The Drosophila position-specific antigens are a family of cell surface glycoprotein complexes. EMBO J 3:2307–2313

    PubMed  CAS  Google Scholar 

  • Wildonger J, Sosinsky A, Honig B, Mann RS (2005) Lozenge directly activates argos and klumpfuss to regulate programmed cell death. Genes Dev 19:1034–1039

    Article  PubMed  CAS  Google Scholar 

  • Wolff T, Ready DF (1991) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113:841–850

    PubMed  CAS  Google Scholar 

  • Wolff T, Ready DF (1993) Pattern formation in the Drosophila retina. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Wride MA (1996) Cellular and molecular features of lens differentiation: a review of recent advances. Differentiation 61:77–93

    Article  PubMed  CAS  Google Scholar 

  • Xia Y, Karin M (2004) The control of cell motility and epithelial morphogenesis by Jun kinases. Trends Cell Biol 14:94–101

    Article  PubMed  CAS  Google Scholar 

  • Xiong WC, Montell C (1993) tramtrack is a transcriptional repressor required for cell fate determination in the Drosophila eye. Genes Dev 7:1085–1096

    Article  PubMed  CAS  Google Scholar 

  • Xu PX, Woo I, Her H, Beier DR, Maas RL (1997) Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode. Development 124:219–231

    PubMed  CAS  Google Scholar 

  • Xu C, Kauffmann RC, Zhang J, Kladny S, Carthew RW (2000) Overlapping activators and repressors delimit transcriptional response to receptor tyrosine kinase signals in the Drosophila eye. Cell 103:87–97

    Article  PubMed  CAS  Google Scholar 

  • Yan H, Canon J, Banerjee U (2003) A transcriptional chain linking eye specification to terminal determination of cone cells in the Drosophila eye. Dev Biol 263:323–329

    Article  PubMed  CAS  Google Scholar 

  • Yang XJ (2004) Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin Cell Dev Biol 15:91–103

    Article  PubMed  CAS  Google Scholar 

  • Yoon CS, Hirosawa K, Suzuki E (1997) Corneal lens secretion in newly emerged Drosophila melanogaster examined by electron microscope autoradiography. J Electron Microsc 46:243–246

    CAS  Google Scholar 

  • Yu SY, Yoo SJ, Yang L, Zapata C, Srinivasan A, Hay BA, Baker NE (2002) A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 129:3269–3278

    PubMed  CAS  Google Scholar 

  • Zhang X, Tang N, Hadden TJ, Rishi AK (2011) Akt, FoxO and regulation of apoptosis. Biochim Biophys Acta-Mol Cell Res [Epub ahead of print]

  • Zhao H, Yang T, Madakashira BP, Thiels CA, Bechtle CA, Garcia CM, Zhang H, Yu K, Ornitz DM, Beebe DC, Robinson ML (2008) Fibroblast growth factor receptor signaling is essential for lens fiber cell differentiation. Dev Biol 318:276–288

    Article  PubMed  CAS  Google Scholar 

  • Zipursky SL, Sanes JR (2010) Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 143:343–353

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Tien Le for vertebrate lens immunofluorescent images. We also wish to thank Ruth Ashery-Padan, Mike Robinson, Ross Cagan, Don Ready, and members of the Visual Systems Group at Cincinnati Children’s Hospital for many insightful discussions on this topic. This work was supported by NIH RO1-EY18097 (NLB), and the Research to Prevent Blindness Foundation, the Ziegler Foundation for the Blind and NIH R01-EY017907 (TAC).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tiffany A. Cook.

Additional information

Communicated by J. Graw.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Charlton-Perkins, M., Brown, N.L. & Cook, T.A. The lens in focus: a comparison of lens development in Drosophila and vertebrates. Mol Genet Genomics 286, 189 (2011). https://doi.org/10.1007/s00438-011-0643-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00438-011-0643-y

Keywords

Navigation