Abstract
Previous chapters have introduced the core determinants of apicobasal polarity in different cell types. This chapter will examine how these determinants become localised to particular membrane domains in Drosophila. In some cell types, such as neuroblasts, polarity does not rely on transmembrane proteins or membrane trafficking. In contrast, epithelial cell polarity involves several key transmembrane proteins, such as Crumbs and E-cadherin, and their distribution depends critically on the exocytic and endocytic machinery. In addition, certain types of epithelial cells secrete an apical extracellular matrix and a basement membrane matrix, processes that must involve polarised exocytic delivery of matrix components. Disruption of membrane trafficking can therefore lead to loss of epithelial polarity and tumour-like phenotypes in Drosophila.
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References
Atwood SX, Prehoda KE (2009) aPKC phosphorylates Miranda to polarize fate determinants during neuroblast asymmetric cell division. Curr Biol 19(9):723–729. doi:10.1016/j.cub.2009.03.056
Bachmann A, Draga M, Grawe F, Knust E (2008) On the role of the MAGUK proteins encoded by Drosophila varicose during embryonic and postembryonic development. BMC Dev Biol 8:55. doi:10.1186/1471-213X-8-55
Banerjee S, Bainton RJ, Mayer N, Beckstead R, Bhat MA (2008) Septate junctions are required for ommatidial integrity and blood-eye barrier function in Drosophila. Dev Biol 317(2):585–599. doi:10.1016/j.ydbio.2008.03.007
Banerjee S, Paik R, Mino RE, Blauth K, Fisher ES, Madden VJ, Fanning AS, Bhat MA (2011) A Laminin G-EGF-Laminin G module in Neurexin IV is essential for the apico-lateral localization of Contactin and organization of septate junctions. PLoS One 6(10):e25926. doi:10.1371/journal.pone.0025926
Baumann O (2001) Posterior midgut epithelial cells differ in their organization of the membrane skeleton from other Drosophila epithelia. Exp Cell Res 270(2):176–187. doi:10.1006/excr.2001.5343
Behr M, Riedel D, Schuh R (2003) The claudin-like megatrachea is essential in septate junctions for the epithelial barrier function in Drosophila. Dev Cell 5(4):611–620
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(6):691–704
Berdnik D, Torok T, Gonzalez-Gaitan M, Knoblich JA (2002) The endocytic protein alpha-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev Cell 3(2):221–231
Betschinger J, Mechtler K, Knoblich JA (2003) The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 422(6929):326–330. doi:10.1038/nature01486
Bilder D, Perrimon N (2000) Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403(6770):676–680. doi:10.1038/35001108
Bilder D, Li M, Perrimon N (2000) Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289(5476):113–116
Blankenship JT, Fuller MT, Zallen JA (2007) The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity. J Cell Sci 120(Pt 17):3099–3110. doi:10.1242/jcs.004770
Bloor JW, Kiehart DP (2002) Drosophila RhoA regulates the cytoskeleton and cell-cell adhesion in the developing epidermis. Development 129(13):3173–3183
Bokel C, Prokop A, Brown NH (2005) Papillote and Piopio: Drosophila ZP-domain proteins required for cell adhesion to the apical extracellular matrix and microtubule organization. J Cell Sci 118(Pt 3):633–642. doi:10.1242/jcs.01619
Bryant PJ, Schmidt O (1990) The genetic control of cell proliferation in Drosophila imaginal discs. J Cell Sci Suppl 13:169–189
Campbell K, Knust E, Skaer H (2009) Crumbs stabilises epithelial polarity during tissue remodelling. J Cell Sci 122(Pt 15):2604–2612. doi:10.1242/jcs.047183
Chen CL, Gajewski KM, Hamaratoglu F, Bossuyt W, Sansores-Garcia L, Tao C, Halder G (2010) The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc Natl Acad Sci U S A 107(36):15810–15815. doi:10.1073/pnas.1004060107
Coumailleau F, Furthauer M, Knoblich JA, Gonzalez-Gaitan M (2009) Directional Delta and Notch trafficking in Sara endosomes during asymmetric cell division. Nature 458(7241):1051–1055. doi:10.1038/nature07854
Denef N, Chen Y, Weeks SD, Barcelo G, Schupbach T (2008) Crag regulates epithelial architecture and polarized deposition of basement membrane proteins in Drosophila. Dev Cell 14(3):354–364. doi:10.1016/j.devcel.2007.12.012
Deng WM, Schneider M, Frock R, Castillejo-Lopez C, Gaman EA, Baumgartner S, Ruohola-Baker H (2003) Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development 130(1):173–184
Faivre-Sarrailh C, Banerjee S, Li J, Hortsch M, Laval M, Bhat MA (2004) Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function. Development 131(20):4931–4942. doi:10.1242/dev.01372
Fernandez BG, Gaspar P, Bras-Pereira C, Jezowska B, Rebelo SR, Janody F (2011) Actin-Capping Protein and the Hippo pathway regulate F-actin and tissue growth in Drosophila. Development 138(11):2337–2346. doi:10.1242/dev.063545
Fletcher GC, Lucas EP, Brain R, Tournier A, Thompson BJ (2012) Positive feedback and mutual antagonism combine to polarize Crumbs in the Drosophila follicle cell epithelium. Curr Biol 22(12):1116–1122. doi:10.1016/j.cub.2012.04.020
Fox DT, Homem CC, Myster SH, Wang F, Bain EE, Peifer M (2005) Rho1 regulates Drosophila adherens junctions independently of p120ctn. Development 132(21):4819–4831. doi:10.1242/dev.02056
Genova JL, Fehon RG (2003) Neuroglian, Gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila. J Cell Biol 161(5):979–989. doi:10.1083/jcb.200212054
Gomez GA, McLachlan RW, Yap AS (2011) Productive tension: force-sensing and homeostasis of cell-cell junctions. Trends Cell Biol 21(9):499–505. doi:10.1016/j.tcb.2011.05.006
Guichard A, McGillivray SM, Cruz-Moreno B, van Sorge NM, Nizet V, Bier E (2010) Anthrax toxins cooperatively inhibit endocytic recycling by the Rab11/Sec15 exocyst. Nature 467(7317):854–858. doi:10.1038/nature09446
Hafezi Y, Bosch JA, Hariharan IK (2012) Differences in levels of the transmembrane protein Crumbs can influence cell survival at clonal boundaries. Dev Biol 368(2):358–369. doi:10.1016/j.ydbio.2012.06.001
Haigo SL, Bilder D (2011) Global tissue revolutions in a morphogenetic movement controlling elongation. Science 331(6020):1071–1074. doi:10.1126/science.1199424
Halbsgut N, Linnemannstons K, Zimmermann LI, Wodarz A (2011) Apical-basal polarity in Drosophila neuroblasts is independent of vesicular trafficking. Mol Biol Cell 22(22):4373–4379. doi:10.1091/mbc.E11-03-0219
Harris KP, Tepass U (2008) Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. J Cell Biol 183(6):1129–1143. doi:10.1083/jcb.200807020
Hijazi A, Masson W, Auge B, Waltzer L, Haenlin M, Roch F (2009) boudin is required for septate junction organisation in Drosophila and codes for a diffusible protein of the Ly6 superfamily. Development 136(13):2199–2209. doi:10.1242/dev.033845
Homem CC, Knoblich JA (2012) Drosophila neuroblasts: a model for stem cell biology. Development 139(23):4297–4310. doi:10.1242/dev.080515
Ile KE, Tripathy R, Goldfinger V, Renault AD (2012) Wunen, a Drosophila lipid phosphate phosphatase, is required for septate junction-mediated barrier function. Development 139(14):2535–2546. doi:10.1242/dev.077289
Izumi Y, Yanagihashi Y, Furuse M (2012) A novel protein complex, Mesh-Ssk, is required for septate junction formation in the Drosophila midgut. J Cell Sci 125(Pt 20):4923–4933. doi:10.1242/jcs.112243
Jazwinska A, Ribeiro C, Affolter M (2003) Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat Cell Biol 5(10):895–901. doi:10.1038/ncb1049
Kim S, Gailite I, Moussian B, Luschnig S, Goette M, Fricke K, Honemann-Capito M, Grubmuller H, Wodarz A (2009) Kinase-activity-independent functions of atypical protein kinase C in Drosophila. J Cell Sci 122(Pt 20):3759–3771. doi:10.1242/jcs.052514
Langevin J, Morgan MJ, Sibarita JB, Aresta S, Murthy M, Schwarz T, Camonis J, Bellaiche Y (2005) Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev Cell 9(3):365–376
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(3):363–374. doi:10.1016/j.devcel.2006.06.001
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(7250):1141–1145. doi:10.1038/nature08067
Laval M, Bel C, Faivre-Sarrailh C (2008) The lateral mobility of cell adhesion molecules is highly restricted at septate junctions in Drosophila. BMC Cell Biol 9:38. doi:10.1186/1471-2121-9-38
Lerner DW, McCoy D, Isabella AJ, Mahowald AP, Gerlach GF, Chaudhry TA, Horne-Badovinac S (2013) A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev Cell 24(2):159–168. doi:10.1016/j.devcel.2012.12.005
Letizia A, Sotillos S, Campuzano S, Llimargas M (2011) Regulated Crb accumulation controls apical constriction and invagination in Drosophila tracheal cells. J Cell Sci 124(Pt 2):240–251. doi:10.1242/jcs.073601
Letizia A, Ricardo S, Moussian B, Martin N, Llimargas M (2013) A functional role of the extracellular domain of Crumbs in cell architecture and apicobasal polarity. J Cell Sci 126(Pt 10):2157–2163. doi:10.1242/jcs.122382
Levayer R, Pelissier-Monier A, Lecuit T (2011) Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat Cell Biol 13(5):529–540. doi:10.1038/ncb2224
Ling C, Zheng Y, Yin F, Yu J, Huang J, Hong Y, Wu S, Pan D (2010) The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates Hippo signaling by binding to Expanded. Proc Natl Acad Sci U S A 107(23):10532–10537. doi:10.1073/pnas.1004279107
Llimargas M, Strigini M, Katidou M, Karagogeos D, Casanova J (2004) Lachesin is a component of a septate junction-based mechanism that controls tube size and epithelial integrity in the Drosophila tracheal system. Development 131(1):181–190. doi:10.1242/dev.00917
Lu H, Bilder D (2005) Endocytic control of epithelial polarity and proliferation in Drosophila. Nat Cell Biol 7(12):1232–1239. doi:10.1038/ncb1324
Lucas EP, Khanal I, Gaspar P, Fletcher GC, Polesello C, Tapon N, Thompson BJ (2013) The Hippo pathway polarizes the actin cytoskeleton during collective migration of Drosophila border cells. J Cell Biol 201(6):875–885. doi:10.1083/jcb.201210073
Magie CR, Meyer MR, Gorsuch MS, Parkhurst SM (1999) Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 126(23):5353–5364
Magie CR, Pinto-Santini D, Parkhurst SM (2002) Rho1 interacts with p120ctn and alpha-catenin, and regulates cadherin-based adherens junction components in Drosophila. Development 129(16):3771–3782
Mason FM, Tworoger M, Martin AC (2013) Apical domain polarization localizes actin-myosin activity to drive ratchet-like apical constriction. Nat Cell Biol 15(8):926–936. doi:10.1038/ncb2796
Meng W, Takeichi M (2009) Adherens junction: molecular architecture and regulation. Cold Spring Harb Perspect Biol 1(6):a002899. doi:10.1101/cshperspect.a002899
Menut L, Vaccari T, Dionne H, Hill J, Wu G, Bilder D (2007) A mosaic genetic screen for Drosophila neoplastic tumor suppressor genes based on defective pupation. Genetics 177(3):1667–1677. doi:10.1534/genetics.107.078360
Mirouse V, Christoforou CP, Fritsch C, St Johnston D, Ray RP (2009) Dystroglycan and perlecan provide a basal cue required for epithelial polarity during energetic stress. Dev Cell 16(1):83–92. doi:10.1016/j.devcel.2008.11.006
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(3):509–523. doi:10.1016/j.cell.2010.02.040
Moyer KE, Jacobs JR (2008) Varicose: a MAGUK required for the maturation and function of Drosophila septate junctions. BMC Dev Biol 8:99. doi:10.1186/1471-213X-8-99
Nelson KS, Furuse M, Beitel GJ (2010) The Drosophila Claudin Kune-kune is required for septate junction organization and tracheal tube size control. Genetics 185(3):831–839. doi:10.1534/genetics.110.114959
Pastor-Pareja JC, Xu T (2011) Shaping cells and organs in Drosophila by opposing roles of fat body-secreted Collagen IV and perlecan. Dev Cell 21(2):245–256. doi:10.1016/j.devcel.2011.06.026
Paul SM, Ternet M, Salvaterra PM, Beitel GJ (2003) The Na+/K+ ATPase is required for septate junction function and epithelial tube-size control in the Drosophila tracheal system. Development 130(20):4963–4974. doi:10.1242/dev.00691
Peifer M (1995) Cell adhesion and signal transduction: the Armadillo connection. Trends Cell Biol 5(6):224–229
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(6877):143–149. doi:10.1038/nature721
Pocha SM, Wassmer T, Niehage C, Hoflack B, Knust E (2011) Retromer controls epithelial cell polarity by trafficking the apical determinant Crumbs. Curr Biol 21(13):1111–1117. doi:10.1016/j.cub.2011.05.007
Robinson BS, Huang J, Hong Y, Moberg KH (2010) Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein Expanded. Curr Biol 20(7):582–590. doi:10.1016/j.cub.2010.03.019
Roeth JF, Sawyer JK, Wilner DA, Peifer M (2009) Rab11 helps maintain apical crumbs and adherens junctions in the Drosophila embryonic ectoderm. PLoS One 4(10):e7634. doi:10.1371/journal.pone.0007634
Roper K (2012) Anisotropy of Crumbs and aPKC drives myosin cable assembly during tube formation. Dev Cell 23(5):939–953. doi:10.1016/j.devcel.2012.09.013
Sarpal R, Pellikka M, Patel RR, Hui FY, Godt D, Tepass U (2012) Mutational analysis supports a core role for Drosophila alpha-catenin in adherens junction function. J Cell Sci 125(Pt 1):233–245. doi:10.1242/jcs.096644
Schneider M, Khalil AA, Poulton J, Castillejo-Lopez C, Egger-Adam D, Wodarz A, Deng WM, Baumgartner S (2006) Perlecan and Dystroglycan act at the basal side of the Drosophila follicular epithelium to maintain epithelial organization. Development 133(19):3805–3815. doi:10.1242/dev.02549
Simoes Sde M, Blankenship JT, Weitz O, Farrell DL, Tamada M, Fernandez-Gonzalez R, Zallen JA (2010) Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation. Dev Cell 19(3):377–388. doi:10.1016/j.devcel.2010.08.011
Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, Klambt C (2008) Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28(3):587–597. doi:10.1523/JNEUROSCI. 4367-07.2008
Strigini M, Cantera R, Morin X, Bastiani MJ, Bate M, Karagogeos D (2006) The IgLON protein Lachesin is required for the blood-brain barrier in Drosophila. Mol Cell Neurosci 32(1–2):91–101. doi:10.1016/j.mcn.2006.03.001
Tanentzapf G, Tepass U (2003) Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat Cell Biol 5(1):46–52. doi:10.1038/ncb896
Tepass U, Gruszynski-DeFeo E, Haag TA, Omatyar L, Torok T, Hartenstein V (1996) shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev 10(6):672–685
Thompson BJ, Mathieu J, Sung HH, Loeser E, Rorth P, Cohen SM (2005) Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev Cell 9(5):711–720. doi:10.1016/j.devcel.2005.09.020
Thompson BJ, Pichaud F, Roper K (2013) Sticking together the Crumbs—an unexpected function for an old friend. Nat Rev Mol Cell Biol 14(5):307–314. doi:10.1038/nrm3568
Vaccari T, Bilder D (2005) The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev Cell 9(5):687–698. doi:10.1016/j.devcel.2005.09.019
Vichas A, Zallen JA (2011) Translating cell polarity into tissue elongation. Semin Cell Dev Biol 22(8):858–864. doi:10.1016/j.semcdb.2011.09.013
Walther RF, Pichaud F (2010) Crumbs/DaPKC-dependent apical exclusion of Bazooka promotes photoreceptor polarity remodeling. Curr Biol 20(12):1065–1074. doi:10.1016/j.cub.2010.04.049
Wan P, Wang D, Luo J, Chu D, Wang H, Zhang L, Chen J (2013) Guidance receptor promotes the asymmetric distribution of exocyst and recycling endosome during collective cell migration. Development 140(23):4797–4806. doi:10.1242/dev.094979
Wang YC, Khan Z, Kaschube M, Wieschaus EF (2012) Differential positioning of adherens junctions is associated with initiation of epithelial folding. Nature 484(7394):390–393. doi:10.1038/nature10938
Warner SJ, Longmore GD (2009) Distinct functions for Rho1 in maintaining adherens junctions and apical tension in remodeling epithelia. J Cell Biol 185(6):1111–1125. doi:10.1083/jcb.200901029
Wilkin MB, Becker MN, Mulvey D, Phan I, Chao A, Cooper K, Chung HJ, Campbell ID, Baron M, MacIntyre R (2000) Drosophila dumpy is a gigantic extracellular protein required to maintain tension at epidermal-cuticle attachment sites. Curr Biol 10(10):559–567
Wirtz-Peitz F, Nishimura T, Knoblich JA (2008) Linking cell cycle to asymmetric division: Aurora-A phosphorylates the Par complex to regulate Numb localization. Cell 135(1):161–173. doi:10.1016/j.cell.2008.07.049
Wodarz A, Gonzalez C (2006) Connecting cancer to the asymmetric division of stem cells. Cell 124(6):1121–1123. doi:10.1016/j.cell.2006.03.004
Wodarz A, Hinz U, Engelbert M, Knust E (1995) Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82(1):67–76
Woods DF, Bryant PJ (1991) The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66(3):451–464
Woods DF, Hough C, Peel D, Callaini G, Bryant PJ (1996) Dlg protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J Cell Biol 134(6):1469–1482
Woods DF, Wu JW, Bryant PJ (1997) Localization of proteins to the apico-lateral junctions of Drosophila epithelia. Dev Genet 20(2):111–118. doi:10.1002/(SICI)1520-6408(1997)20:2<111::AID-DVG4>3.0.CO;2-A
Wu VM, Schulte J, Hirschi A, Tepass U, Beitel GJ (2004) Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control. J Cell Biol 164(2):313–323. doi:10.1083/jcb.200309134
Wu VM, Yu MH, Paik R, Banerjee S, Liang Z, Paul SM, Bhat MA, Beitel GJ (2007) Drosophila Varicose, a member of a new subgroup of basolateral MAGUKs, is required for septate junctions and tracheal morphogenesis. Development 134(5):999–1009. doi:10.1242/dev.02785
Yan J, Lu Q, Fang X, Adler PN (2009) Rho1 has multiple functions in Drosophila wing planar polarity. Dev Biol 333(1):186–199. doi:10.1016/j.ydbio.2009.06.027
Yanagihashi Y, Usui T, Izumi Y, Yonemura S, Sumida M, Tsukita S, Uemura T, Furuse M (2012) Snakeskin, a membrane protein associated with smooth septate junctions, is required for intestinal barrier function in Drosophila. J Cell Sci 125(Pt 8):1980–1990. doi:10.1242/jcs.096800
Zallen JA, Wieschaus E (2004) Patterned gene expression directs bipolar planar polarity in Drosophila. Dev Cell 6(3):343–355
Zhou B, Wu Y, Lin X (2011) Retromer regulates apical-basal polarity through recycling Crumbs. Dev Biol 360(1):87–95. doi:10.1016/j.ydbio.2011.09.009
Acknowledgements
I thank Georgina Fletcher and Eliana Lucas for helping in preparing the figures. I also apologise to my colleagues working with C. elegans, or mammalian cells in culture, whose important work could not be cited here due to space limitations.
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Thompson, B.J. (2015). Membrane Traffic and Apicobasal Polarity in Drosophila Epithelial Cells. In: Ebnet, K. (eds) Cell Polarity 1. Springer, Cham. https://doi.org/10.1007/978-3-319-14463-4_14
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