Advertisement

Cell Polarity in Drosophila Retina

  • Sang-Chul NamEmail author
Chapter

Abstract

Apical–basal cell polarity is crucial for the development of multicellular organisms and for the diverse functions of epithelial cells in diverse organs. Cell polarity in epithelial cells is characterized by differential distributions of protein components in the apical and basolateral membrane domains as well as the asymmetric distributions of intracellular materials. The cell polarity is mainly regulated by evolutionary conserved genes, which are Crumbs (Crb) complex of Crb, Stardust (Sdt), Pals-1-associated tight junction protein (Patj), and partitioning-defective (Par) complex of Par-3 (Bazooka, Baz), Par-6, and atypical protein kinase C (aPKC). These cell polarity complexes play fundamental roles in initial cell polarity establishment and its maintenance and regulation. Recently, the roles of these cell polarity genes and their regulations were identified in Drosophila retina development. Here, we review recent discoveries of the roles of Crb and Par complexes and their regulators in morphogenesis and organogenesis of Drosophila retina.

Keywords

Cell Polarity Tight Junction Protein Apical Domain Drosophila Photoreceptor Apical Membrane Domain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abd El-Aziz MM, Barragan I, O’Driscoll CA, Goodstadt L, Prigmore E, Borrego S, Mena M, Pieras JI, El-Ashry MF, Safieh LA et al (2008) EYS, encoding an ortholog of Drosophila spacemaker, is mutated in autosomal recessive retinitis pigmentosa. Nat Genet 40:1285–1287PubMedGoogle Scholar
  2. Amin N, Khan A, St Johnston D, Tomlinson I, Martin S, Brenman J, McNeill H (2009) LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye. Proc Natl Acad Sci U S A 106:8941–8946PubMedGoogle Scholar
  3. Avasthi P, Watt CB, Williams DS, Le YZ, Li S, Chen CK, Marc RE, Frederick JM, Baehr W (2009) Trafficking of membrane proteins to cone but not rod outer segments is dependent on heterotrimeric kinesin-II. J Neurosci 29:14287–14298PubMedGoogle Scholar
  4. Bachmann A, Schneider M, Theilenberg E, Grawe F, Knust E (2001) Drosophila stardust is a partner of crumbs in the control of epithelial cell polarity. Nature 414:638–643PubMedGoogle Scholar
  5. Benton R, St Johnston D (2003) Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 115:691–704PubMedGoogle Scholar
  6. Berger S, Bulgakova NA, Grawe F, Johnson K, Knust E (2007) Unraveling the genetic complexity of Drosophila stardust during photoreceptor morphogenesis and prevention of light-induced degeneration. Genetics 176:2189–2200PubMedGoogle Scholar
  7. Beronja S, Laprise P, Papoulas O, Pellikka M, Sisson J, Tepass U (2005) Essential function of Drosophila Sec6 in apical exocytosis of epithelial photoreceptor cells. J Cell Biol 169:635–646PubMedGoogle Scholar
  8. Bhat MA, Izaddoost S, Lu Y, Cho KO, Choi KW, Bellen HJ (1999) Discs lost, a novel multi-PDZ domain protein, establishes and maintains epithelial polarity. Cell 96:833–845PubMedGoogle Scholar
  9. Bilder D, Perrimon N (2000) Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403:676–680PubMedGoogle Scholar
  10. Bilder D (2001) Cell polarity: squaring the circle. Curr Biol 11:R132–135Google Scholar
  11. Bryant DM, Mostov KE (2008) From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 9:887–901PubMedGoogle Scholar
  12. Chabu C, Doe CQ (2009) Twins/PP2A regulates aPKC to control neuroblast cell polarity and self-renewal. Dev Biol 330:399–405PubMedGoogle Scholar
  13. Chartier FJ, Hardy EJ, Laprise P (2012) Crumbs limits oxidase-dependent signaling to maintain epithelial integrity and prevent photoreceptor cell death. J Cell Biol 198:991–998PubMedGoogle Scholar
  14. Chen TW, Chen G, Funkhouser LJ, Nam SC (2009) Membrane domain modulation by spectrins in Drosophila photoreceptor morphogenesis. Genesis 47:744–750PubMedGoogle Scholar
  15. Chen G, League GP, Nam SC (2010) Role of spastin in apical domain control along the rhabdomere elongation in Drosophila photoreceptor. PLoS One 5:e9480PubMedGoogle Scholar
  16. Chen G, Rogers AK, League GP, Nam SC (2011) Genetic interaction of centrosomin and bazooka in apical domain regulation in Drosophila photoreceptor. PLoS One 6:e16127PubMedGoogle Scholar
  17. Choi KW, Nam SC, Mukhopadhyay B (2007) Par-1 and PP2A: Yin-Yang of bazooka localization. Fly (Austin) 1:235–237Google Scholar
  18. Cho SH, Kim JY, Simons DL, Song JY, Le JH, Swindell EC, Jamrich M, Wu SM, Kim S (2012) Genetic ablation of Pals1 in retinal progenitor cells models the retinal pathology of Leber congenital amaurosis. Hum Mol Genet 21:2663–2676PubMedGoogle Scholar
  19. Christensen AK, Jensen AM (2008) Tissue-specific requirements for specific domains in the FERM protein Moe/Epb4.1l5 during early zebrafish development. BMC Dev Biol 8:3PubMedGoogle Scholar
  20. Collin RW, Littink KW, Klevering BJ, den Born LI van, Koenekoop RK, Zonneveld MN, Blokland EA, Strom TM, Hoyng CB, den Hollander AI, Cremers FP (2008) Identification of a 2 Mb human ortholog of Drosophila eyes shut/spacemaker that is mutated in patients with retinitis pigmentosa. Am J Hum Genet 83:594–603PubMedGoogle Scholar
  21. den Hollander AI, ten Brink JB, Kok YJ de, Soest S van, den Born LI van, Driel MA van, Pol DJ van de, Payne AM, Bhattacharya SS, Kellner U et al (1999) Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nat Genet 23:217–221PubMedGoogle Scholar
  22. den Hollander AI, Heckenlively JR, den Born LI van, Kok YJ de, Velde-Visser SD van der, Kellner U, Jurklies B, Schooneveld MJ van, Blankenagel A, Rohrschneider K et al (2001) Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene. Am J Hum Genet 69:198–203PubMedGoogle Scholar
  23. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657PubMedGoogle Scholar
  24. Drubin DG, Nelson WJ (1996) Origins of cell polarity. Cell 84:335–344PubMedGoogle Scholar
  25. Errico A, Ballabio A, Rugarli EI (2002) Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. Hum Mol Genet 11:153–163PubMedGoogle Scholar
  26. Fan SS, Ready DF (1997) Glued participates in distinct microtubule-based activities in Drosophila eye development. Development 124:1497–1507PubMedGoogle Scholar
  27. Galy A, Schenck A, Sahin HB, Qurashi A, Sahel JA, Diebold C, Giangrande A (2011) CYFIP dependent actin remodeling controls specific aspects of Drosophila eye morphogenesis. Dev Biol 359:37–46PubMedGoogle Scholar
  28. Gassama-Diagne A, Yu W, ter Beest M, Martin-Belmonte F, Kierbel A, Engel J, Mostov K (2006) Phosphatidylinositol-3,4,5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nat Cell Biol 8:963–970PubMedGoogle Scholar
  29. Grawe F, Wodarz A, Lee B, Knust E, Skaer H (1996) The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions. Development 122:951–959Google Scholar
  30. Harris TJ, Peifer M (2004) Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila. J Cell Biol 167:135–147PubMedGoogle Scholar
  31. Harris TJ, Peifer M (2005) The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila. J Cell Biol 170:813–823PubMedGoogle Scholar
  32. Hong Y, Stronach B, Perrimon N, Jan LY, Jan YN (2001) Drosophila stardust interacts with crumbs to control polarity of epithelia but not neuroblasts. Nature 414:634–638PubMedGoogle Scholar
  33. Hong Y, Ackerman L, Jan LY, Jan YN (2003) Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture. Proc Natl Acad Sci U S A 100:12712–12717PubMedGoogle Scholar
  34. Horne-Badovinac S, Lin D, Waldron S, Schwarz M, Mbamalu G, Pawson T, Jan Y, Stainier DY, Abdelilah-Seyfried S (2001) Positional cloning of heart and soul reveals multiple roles for PKC lambda in zebrafish organogenesis. Curr Biol 11:1492–1502PubMedGoogle Scholar
  35. Hsu YC, Willoughby JJ, Christensen AK, Jensen AM (2006) Mosaic eyes is a novel component of the crumbs complex and negatively regulates photoreceptor apical size. Development 133:4849–4859PubMedGoogle Scholar
  36. Hurd TW, Gao L, Roh MH, Macara IG, Margolis B (2003) Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat Cell Biol 5:137–142PubMedGoogle Scholar
  37. Husain N, Pellikka M, Hong H, Klimentova T, Choe KM, Clandinin TR, Tepass U (2006) The agrin/perlecan-related protein eyes shut is essential for epithelial lumen formation in the Drosophila retina. Dev Cell 11:483–493PubMedGoogle Scholar
  38. Hutterer A, Betschinger J, Petronczki M, Knoblich JA (2004) Sequential roles of Cdc42, Par-6, aPKC, and Lgl in the establishment of epithelial polarity during Drosophila embryogenesis. Dev Cell 6:845–854PubMedGoogle Scholar
  39. Izaddoost S, Nam SC, Bhat MA, Bellen HJ, Choi KW (2002) Drosophila crumbs is a positional cue in photoreceptor adherens junctions and rhabdomeres. Nature 416:178–183PubMedGoogle Scholar
  40. Izumi Y, Hirose T, Tamai Y, Hirai S, Nagashima Y, Fujimoto T, Tabuse Y, Kemphues KJ, Ohno S (1998) An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J Cell Biol 143:95–106PubMedGoogle Scholar
  41. Jensen AM, Westerfield M (2004) Zebrafish mosaic eyes is a novel FERM protein required for retinal lamination and retinal pigmented epithelial tight junction formation. Curr Biol 14:711–717PubMedGoogle Scholar
  42. Jimeno D, Feiner L, Lillo C, Teofilo K, Goldstein LS, Pierce EA, Williams DS (2006a) Analysis of kinesin-2 function in photoreceptor cells using synchronous Cre-loxP knockout of Kif3a with RHO-Cre. Invest Ophthalmol Vis Sci 47:5039–5046Google Scholar
  43. Jimeno D, Lillo C, Roberts EA, Goldstein LS, Williams DS (2006b) Kinesin-2 and photoreceptor cell death: requirement of motor subunits. Exp Eye Res 82:351–353Google Scholar
  44. Johnson K, Grawe F, Grzeschik N, Knust E (2002) Drosophila crumbs is required to inhibit light-induced photoreceptor degeneration. Curr Biol 12:1675–1680PubMedGoogle Scholar
  45. Karagiosis SA, Ready DF (2004) Moesin contributes an essential structural role in Drosophila photoreceptor morphogenesis. Development 131:725–732PubMedGoogle Scholar
  46. Kirby C, Kusch M, Kemphues K (1990) Mutations in the par genes of Caenorhabditis elegans affect cytoplasmic reorganization during the first cell cycle. Dev Biol 142:203–215PubMedGoogle Scholar
  47. Klebes A, Knust E (2000) A conserved motif in crumbs is required for E-cadherin localisation and zonula adherens formation in Drosophila. Curr Biol 10:76–85PubMedGoogle Scholar
  48. Krahn MP, Egger-Adam D, Wodarz A (2009) PP2A antagonizes phosphorylation of Bazooka by PAR-1 to control apical-basal polarity in dividing embryonic neuroblasts. Dev Cell 16:901–908PubMedGoogle Scholar
  49. Krahn MP, Klopfenstein DR, Fischer N, Wodarz A (2010) Membrane targeting of Bazooka/PAR-3 is mediated by direct binding to phosphoinositide lipids. Curr Biol 20:636–642PubMedGoogle Scholar
  50. Kumar JP, Ready DF (1995) Rhodopsin plays an essential structural role in Drosophila photoreceptor development. Development 121:4359–4370PubMedGoogle Scholar
  51. Land MF, Nilsson DE (2002) Animal Eyes. Oxford University Press, OxfordGoogle Scholar
  52. Laprise P, Tepass U (2011) Novel insights into epithelial polarity proteins in Drosophila. Trends Cell Biol 21:401–408PubMedGoogle Scholar
  53. Laprise P, Beronja S, Silva-Gagliardi NF, Pellikka M, Jensen AM, McGlade CJ, Tepass U (2006) The FERM protein Yurt is a negative regulatory component of the crumbs complex that controls epithelial polarity and apical membrane size. Dev Cell 11:363–374PubMedGoogle Scholar
  54. Laprise P, Lau KM, Harris KP, Silva-Gagliardi NF, Paul SM, Beronja S, Beitel GJ, McGlade CJ, Tepass U (2009) Yurt, Coracle, Neurexin IV and the Na(+),K(+)-ATPase form a novel group of epithelial polarity proteins. Nature 459:1141–1145PubMedGoogle Scholar
  55. League GP, Nam SC (2011) Role of kinesin heavy chain in crumbs localization along the rhabdomere elongation in Drosophila photoreceptor. PLoS One 6:e21218PubMedGoogle Scholar
  56. Lee S, Kolodziej PA (2002) Short stop provides an essential link between F-actin and microtubules during axon extension. Development 129:1195–1204PubMedGoogle Scholar
  57. Lee S, Harris KL, Whitington PM, Kolodziej PA (2000) Short stop is allelic to kakapo, and encodes rod-like cytoskeletal-associated proteins required for axon extension. J Neurosci 20:1096–1108Google Scholar
  58. Lee JH, Koh H, Kim M, Kim Y, Lee SY, Karess RE, Lee SH, Shong M, Kim JM, Kim J, Chung J (2007) Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature 447:1017–1020PubMedGoogle Scholar
  59. Lei Y, Warrior R (2000) The Drosophila Lissencephaly1 (DLis1) gene is required for nuclear migration. Dev Biol 226:57–72Google Scholar
  60. Li BX, Satoh AK, Ready DF (2007) Myosin V, Rab11, and dRip11 direct apical secretion and cellular morphogenesis in developing Drosophila photoreceptors. J Cell Biol 177:659–669PubMedGoogle Scholar
  61. Longley RL Jr, Ready DF (1995) Integrins and the development of three-dimensional structure in the Drosophila compound eye. Dev Biol 171:415–433PubMedGoogle Scholar
  62. Lopes VS, Jimeno D, Khanobdee K, Song X, Chen B, Nusinowitz S, Williams DS (2010) Dysfunction of heterotrimeric kinesin-2 in rod photoreceptor cells and the role of opsin mislocalization in rapid cell death. Mol Biol Cell 21:4076–4088PubMedGoogle Scholar
  63. Lumb JH, Connell JW, Allison R, Reid E (2011) The AAA ATPase spastin links microtubule severing to membrane modelling. Biochim Biophys Acta 1823:192–197PubMedGoogle Scholar
  64. Macara IG (2004a) Par proteins: partners in polarization. Curr Biol 14:R160–R162Google Scholar
  65. Macara IG (2004b) Parsing the polarity code. Nat Rev Mol Cell Biol 5:220–231Google Scholar
  66. Martin SG, St Johnston D (2003) A role for Drosophila LKB1 in anterior-posterior axis formation and epithelial polarity. Nature 421:379–384PubMedGoogle Scholar
  67. Martin-Belmonte F, Mostov K (2007) Phosphoinositides control epithelial development. Cell Cycle 6:1957–1961PubMedGoogle Scholar
  68. Medina E, Williams J, Klipfell E, Zarnescu D, Thomas G, Le Bivic A (2002) Crumbs interacts with moesin and beta (heavy)-spectrin in the apical membrane skeleton of Drosophila. J Cell Biol 158:941–951PubMedGoogle Scholar
  69. Mehalow AK, Kameya S, Smith RS, Hawes NL, Denegre JM, Young JA, Bechtold L, Haider NB, Tepass U, Heckenlively JR et al (2003) CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum Mol Genet 12:2179–2189PubMedGoogle Scholar
  70. Mirouse V, Swick LL, Kazgan N, St Johnston D, Brenman JE (2007) LKB1 and AMPK maintain epithelial cell polarity under energetic stress. J Cell Biol 177:387–392PubMedGoogle Scholar
  71. Morais-de-Sa E, Mirouse V, St Johnston D (2010) aPKC phosphorylation of Bazooka defines the apical/lateral border in Drosophila epithelial cells. Cell 141:509–523PubMedGoogle Scholar
  72. Morton DG, Roos JM, Kemphues KJ (1992) Par-4, a gene required for cytoplasmic localization and determination of specific cell types in Caenorhabditis elegans embryogenesis. Genetics 130:771–790PubMedGoogle Scholar
  73. Mosley-Bishop KL, Li Q, Patterson L, Fischer JA (1999) Molecular analysis of the klarsicht gene and its role in nuclear migration within differentiating cells of the Drosophila eye. Curr Biol 9:1211–1220PubMedGoogle Scholar
  74. Mui UN, Lubczyk CM, Nam SC (2011) Role of spectraplakin in Drosophila photoreceptor morphogenesis. PLoS One 6:e25965PubMedGoogle Scholar
  75. Mukhopadhyay B, Nam SC, Choi KW (2010) Kinesin II is required for cell survival and adherens junction positioning in Drosophila photoreceptors. Genesis 48:522–530PubMedGoogle Scholar
  76. Nam SC, Choi KW (2003) Interaction of Par-6 and crumbs complexes is essential for photoreceptor morphogenesis in Drosophila. Development 130:4363–4372PubMedGoogle Scholar
  77. Nam SC, Choi KW (2006) Domain-specific early and late function of Dpatj in Drosophila photoreceptor cells. Dev Dyn 235:1501–1507PubMedGoogle Scholar
  78. Nam SC, Mukhopadhyay B, Choi KW (2007) Antagonistic functions of Par-1 kinase and protein phosphatase 2A are required for localization of Bazooka and photoreceptor morphogenesis in Drosophila. Dev Biol 306:624–635PubMedGoogle Scholar
  79. Nelson WJ (2003) Adaptation of core mechanisms to generate cell polarity. Nature 422:766–774PubMedGoogle Scholar
  80. Nie J, Mahato S, Mustill W, Tipping C, Bhattacharya SS, Zelhof AC (2012) Cross species analysis of Prominin reveals a conserved cellular role in invertebrate and vertebrate photoreceptor cells. Dev Biol 371(2):312–320PubMedGoogle Scholar
  81. Nunbhakdi-Craig V, Machleidt T, Ogris E, Bellotto D, White CL 3rd, Sontag E (2002) Protein phosphatase 2A associates with and regulates atypical PKC and the epithelial tight junction complex. J Cell Biol 158:967–978PubMedGoogle Scholar
  82. Ogawa H, Ohta N, Moon W, Matsuzaki F (2009) Protein phosphatase 2A negatively regulates aPKC signaling by modulating phosphorylation of Par-6 in Drosophila neuroblast asymmetric divisions. J Cell Sci 122:3242–3249PubMedGoogle Scholar
  83. Ohno S (2001) Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr Opin Cell Biol 13:641–648PubMedGoogle Scholar
  84. Park B, Alves CH, Lundvig DM, Tanimoto N, Beck SC, Huber G, Richard F, Klooster J, Andlauer TF, Swindell EC et al (2011) PALS1 is essential for retinal pigment epithelium structure and neural retina stratification. J Neurosci 31:17230–17241PubMedGoogle Scholar
  85. Pellikka M, Tanentzapf G, Pinto M, Smith C, McGlade CJ, Ready DF, Tepass U (2002) Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 416:143–149PubMedGoogle Scholar
  86. Petronczki M, Knoblich JA (2001) DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila. Nat Cell Biol 3:43–49PubMedGoogle Scholar
  87. Pham H, Yu H, Laski FA (2008) Cofilin/ADF is required for retinal elongation and morphogenesis of the Drosophila rhabdomere. Dev Biol 318:82–91PubMedGoogle Scholar
  88. Pinal N, Goberdhan DC, Collinson L, Fujita Y, Cox IM, Wilson C, Pichaud F (2006) Regulated and polarized PtdIns (3,4,5) P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells. Curr Biol 16:140–149PubMedGoogle Scholar
  89. Pocha SM, Shevchenko A, Knust E (2011) Crumbs regulates rhodopsin transport by interacting with and stabilizing myosin V. J Cell Biol 195:827–838PubMedGoogle Scholar
  90. Poels J, Spasic MR, Gistelinck M, Mutert J, Schellens A, Callaerts P, Norga KK (2012) Autophagy and phagocytosis-like cell cannibalism exert opposing effects on cellular survival during metabolic stress. Cell Death Differ 19:1590–1601PubMedGoogle Scholar
  91. Ready DF (2002) Drosophila compound eye morphogenesis: blind mechanical engineers? In: Moses K (ed) Drosophila eye development (results and problems in cell differentiation). Springer, Heidelberg, pp 191–204Google Scholar
  92. Richard M, Grawe F, Knust E (2006) DPATJ plays a role in retinal morphogenesis and protects against light-dependent degeneration of photoreceptor cells in the Drosophila eye. Dev Dyn 235:895–907PubMedGoogle Scholar
  93. Roh MH, Makarova O, Liu CJ, Shin K, Lee S, Laurinec S, Goyal M, Wiggins R, Margolis B (2002) The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of crumbs and discs lost. J Cell Biol 157:161–172PubMedGoogle Scholar
  94. Roll-Mecak A, McNally FJ (2009) Microtubule-severing enzymes. Curr Opin Cell Biol 22:96–103PubMedGoogle Scholar
  95. Salinas S, Carazo-Salas RE, Proukakis C, Schiavo G, Warner TT (2007) Spastin and microtubules: functions in health and disease. J Neurosci Res 85:2778–2782PubMedGoogle Scholar
  96. Satoh AK, O’Tousa JE, Ozaki K, Ready DF (2005) Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132:1487–1497PubMedGoogle Scholar
  97. Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457:818–823PubMedGoogle Scholar
  98. Sotillos S, Diaz-Meco MT, Caminero E, Moscat J, Campuzano S (2004) DaPKC-dependent phosphorylation of crumbs is required for epithelial cell polarity in Drosophila. J Cell Biol 166:549–557PubMedGoogle Scholar
  99. Sottocornola R, Royer C, Vives V, Tordella L, Zhong S, Wang Y, Ratnayaka I, Shipman M, Cheung A, Gaston-Massuet C et al (2010) ASPP2 binds Par-3 and controls the polarity and proliferation of neural progenitors during CNS development. Dev Cell 19:126–137PubMedGoogle Scholar
  100. Spasic MR, Callaerts P, Norga KK (2008) Drosophila alicorn is a neuronal maintenance factor protecting against activity-induced retinal degeneration. J Neurosci 28:6419–6429PubMedGoogle Scholar
  101. Suzuki A, Yamanaka T, Hirose T, Manabe N, Mizuno K, Shimizu M, Akimoto K, Izumi Y, Ohnishi T, Ohno S (2001) Atypical protein kinase C is involved in the evolutionarily conserved par protein complex and plays a critical role in establishing epithelia-specific junctional structures. J Cell Biol 152:1183–1196PubMedGoogle Scholar
  102. Tepass U (2012) The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annu Rev Cell Dev Biol 28:655–685PubMedGoogle Scholar
  103. Tepass U, Knust E (1993) Crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster. Dev Biol 159:311–326PubMedGoogle Scholar
  104. Tepass U, Tanentzapf G, Ward R, Fehon R (2001) Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35:747–784PubMedGoogle Scholar
  105. Tepass U, Theres C, Knust, E (1990) Crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61:787–799Google Scholar
  106. Walther RF, Pichaud F (2010) Crumbs/DaPKC-dependent apical exclusion of bazooka promotes photoreceptor polarity remodeling. Curr Biol 20:1065–1074PubMedGoogle Scholar
  107. Watts JL, Morton DG, Bestman J, Kemphues KJ (2000) The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry. Development 127:1467–1475PubMedGoogle Scholar
  108. Wei X, Malicki J (2002) Nagie oko, encoding a MAGUK-family protein, is essential for cellular patterning of the retina. Nat Genet 31:150–157PubMedGoogle Scholar
  109. Whited JL, Cassell A, Brouillette M, Garrity PA (2004) Dynactin is required to maintain nuclear position within postmitotic Drosophila photoreceptor neurons. Development 131:4677–4686PubMedGoogle Scholar
  110. Wodarz A, Ramrath A, Grimm A, Knust E (2000) Drosophila atypical protein kinase C associates with bazooka and controls polarity of epithelia and neuroblasts. J Cell Biol 150:1361–1374PubMedGoogle Scholar
  111. Wu S, Mehta SQ, Pichaud F, Bellen HJ, Quiocho FA (2005) Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat Struct Mol Biol 12:879–885PubMedGoogle Scholar
  112. Xia H, Ready DF (2011) Ectoplasm, ghost in the R cell machine? Dev Neurobiol 71:1246–1257PubMedGoogle Scholar
  113. Xiong W, Rebay I (2011) Abelson tyrosine kinase is required for Drosophila photoreceptor morphogenesis and retinal epithelial patterning. Dev Dyn 240:1745–1755PubMedGoogle Scholar
  114. Zelhof AC, Hardy RW (2004) WASp is required for the correct temporal morphogenesis of rhabdomere microvilli. J Cell Biol 164:417–426PubMedGoogle Scholar
  115. Zelhof AC, Hardy RW, Becker A, Zuker CS (2006) Transforming the architecture of compound eyes. Nature 443:696–699PubMedGoogle Scholar
  116. Zhou W, Hong Y (2012) Drosophila Patj plays a supporting role in apical-basal polarity but is essential for viability. Development 139:2891–2896PubMedGoogle Scholar
  117. Zou J, Wang X, Wei X (2012) Crb apical polarity proteins maintain zebrafish retinal cone mosaics via intercellular binding of their extracellular domains. Dev Cell 22:1261–1274PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of BiologyTexas A&M International UniversityLaredoUSA

Personalised recommendations