Spinster controls Dpp signaling during glial migration in the Drosophila eye

Journal of Neuroscience

Volumn 31, Issue 19, 2011, Pages 7005-7015

  Yuva Aydemir, Yeliz ^a   Bauke, Ann Christin ^a   Klämbt, Christian ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DECAPENTAPLEGIC PROTEIN; MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; ENDOCYTOSIS; ENDOSOME; EYE; GENE; GENE FUNCTION; GENETIC ANALYSIS; GLIA CELL; LYSOSOME; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINSTER GENE;

ANIMALS; CELL MOVEMENT; COMPOUND EYE, ARTHROPOD; DROSOPHILA; DROSOPHILA PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MEMBRANE PROTEINS; NEUROGLIA; SIGNAL TRANSDUCTION;

EID: 79956292584     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0459-11.2011     Document Type: Article

References (52)

1. Affolter M, Pyrowolakis G (2006) eIF4A goes beyond translation. Nat Cell Biol 8:1319-1321.
2. Aigouy B, Van de Bor V, Boeglin M, Giangrande A (2004) Time-lapse and cell ablation reveal the role of cell interactions in fly glia migration and proliferation. Development 131:5127-5138.
3. Aigouy B, Lepelletier L, Giangrande A (2008) Glial chain migration requires pioneer cells. J Neurosci 28:11635-11641.
4. Arbouzova NI, Zeidler MP (2006) JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Development 133:2605-2616.
5. Chen Y, Struhl G (1996) Dual roles for patched in sequestering and transducing Hedgehog. Cell 87:553-563.
6. Chinchore Y, Mitra A, Dolph PJ (2009) Accumulation of rhodopsin in late endosomes triggers photoreceptor cell degeneration. PLoS Genet 5:e1000377.
7. Choi KW, Benzer S (1994) Migration of glia along photoreceptor axons in the developing Drosophila eye. Neuron 12:423-431.
8. Dermaut B, Norga KK, Kania A, Verstreken P, Pan H, Zhou Y, Callaerts P, Bellen HJ (2005) Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurodegeneration in Drosophila benchwarmer. J Cell Biol 170:127-139.
9. Dudu V, Bittig T, Entchev E, Kicheva A, Jülicher F, González-Gaitán M (2006) Postsynaptic mad signaling at the Drosophila neuromuscular junction. Curr Biol 16:625-635.
10. Edenfeld G, Altenhein B, Zierau A, Cleppien D, Krukkert K, Technau G, Klämbt C (2007) Notch and Numb are required for normal migration of peripheral glia in Drosophila. Dev Biol 301:27-37.
11. Ekas LA, Baeg GH, Flaherty MS, Ayala-Camargo A, Bach EA (2006) JAK/ STAT signaling promotes regional specification by negatively regulating wingless expression in Drosophila. Development 133:4721-4729.
12. Entchev EV, Schwabedissen A, González-Gaitán M (2000) Gradient formation of the TGF-beta homolog Dpp. Cell 103:981-991.
13. Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG (2009) Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 187:733-747.
14. Fischer JA, Eun SH, Doolan BT (2006) Endocytosis, endosome trafficking, and the regulation of Drosophila development. Annu Rev Cell Dev Biol 22:181-206.
15. Franzdóttir SR, Engelen D, Yuva-Aydemir Y, Schmidt I, Aho A, Klämbt C (2009) Switch in FGF signalling initiates glial differentiation in the Drosophila eye. Nature 460:758-761.
16. González-Gaitán M (2003) Endocytic trafficking during Drosophila development. Mech Dev 120:1265-1282.
17. Halter DA, Urban J, Rickert C, Ner SS, Ito K, Travers AA, Technau GM (1995) The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121:317-332.
18. Hülsmeier J, Pielage J, Rickert C, Technau GM, Klämbt C, Stork T (2007) Distinct functions of α-Spectrin and β-Spectrin during axonal pathfinding. Development 134:713-722.
19. Hummel T, Attix S, Gunning D, Zipursky SL (2002) Temporal control of glial cell migration in the Drosophila eye requires gilgamesh, hedgehog, and eye specification genes. Neuron 33:193-203.
20. Jékely G, Rørth P (2003) Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO Rep 4:1163-1168.
21. Jékely G, Sung HH, Luque CM, Rørth P (2005) Regulators of endocytosis maintain localized receptor tyrosine kinase signaling in guided migration. Dev Cell 9:197-207.
22. Klämbt C (2009) Modes and regulation of glial migration in vertebrates and invertebrates. Nat Rev Neurosci 10:769-779.
23. Lee BP, Jones BW (2005) Transcriptional regulation of the Drosophila glial gene repo. Mech Dev 122:849-862.
24. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
25. Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, Bellen HJ (2002) Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108:261-269.
26. Lu H, Bilder D (2005) Endocytic control of epithelial polarity and proliferation in Drosophila. Nat Cell Biol 7:1232-1239.
27. Meinertzhagen IA, Hanson TE (1993) The development of the optic lobe. In: The development of Drosophila melanogaster (Bate M, Martinez Arias A, eds), pp 1363-1491. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
28. Miura S, Takeshita T, Asao H, Kimura Y, Murata K, Sasaki Y, Hanai JI, Beppu H, Tsukazaki T, Wrana JL, Miyazono K, Sugamura K (2000) Hgs (Hrs), a FYVE domain protein, is involved in Smad signaling through cooperation with SARA. Mol Cell Biol 20:9346-9355.
29. Murakami S, Umetsu D, Maeyama Y, Sato M, Yoshida S, Tabata T (2007) Focal adhesion kinase controls morphogenesis of the Drosophila optic stalk. Development 134:1539-1548.
30. Nakano Y, Fujitani K, Kurihara J, Ragan J, Usui-Aoki K, Shimoda L, Lukacsovich T, Suzuki K, Sezaki M, Sano Y, Ueda R, Awano W, Kaneda M, Umeda M, Yamamoto D (2001) Mutations in the novel membrane protein spinster interfere with programmed cell death and cause neural degeneration in Drosophila melanogaster. Mol Cell Biol 21:3775-3788.
31. Penton A, Wodarz A, Nusse R (2002) Amutational analysis of dishevelled in Drosophila defines novel domains in the dishevelled protein as well as novel suppressing alleles of axin. Genetics 161:747-762.
32. Rangarajan R, Gong Q, Gaul U (1999) Migration and function of glia in the developing Drosophila eye. Development 126:3285-3292.
33. Rangarajan R, Courvoisier H, Gaul U (2001) Dpp and Hedgehog mediate neuron-glia interactions in Drosophila eye development by promoting the proliferation and motility of subretinal glia. Mech Dev 108:93-103.
34. Sepp KJ, Auld VJ (1999) Conversion of lac Z enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151:1093-1101.
35. Sepp KJ, Schulte J, Auld VJ (2000) Developmental dynamics of peripheral glia in Drosophila melanogaster. Glia 30:122-133.
36. Silies M, Klämbt C (2010) APC/C(Fzr/Cdh1)-dependent regulation of cell adhesion controls glial migration in the Drosophila PNS. Nat Neurosci 13:1357-1364.
37. Silies M, Yuva Y, Engelen D, Aho A, Stork T, Klämbt C (2007) Glial cell migration in the eye disc. J Neurosci 27:13130-13139.
38. Silies M, Yuva-Aydemir Y, Franzdóttir SR, Klämbt C (2010) The eye imaginal disc as a model to study the coordination of neuronal and glial development. Fly (Austin) 4:71-79.
39. Simonsen A, Cumming RC, Lindmo K, Galaviz V, Cheng S, Rusten TE, Finley KD (2007) Genetic modifiers of the Drosophila blue cheese gene link defects in lysosomal transport with decreased life span and altered ubiquitinated-protein profiles. Genetics 176:1283-1297.
40. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513-525.
41. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, Klämbt C (2008) Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28:587-597.
42. Sunio A, Metcalf AB, Krämer H (1999) Genetic dissection of endocytic trafficking in Drosophila using a horseradish peroxidase-bride of sevenless chimera: hook is required for normal maturation of multivesicular endosomes. Mol Biol Cell 10:847-859.
43. Sweeney ST, Davis GW (2002) Unrestricted synaptic growth in spinster-a late endosomal protein implicated in TGF-beta-mediated synaptic growth regulation. Neuron 36:403-416.
44. Torroja C, Gorfinkiel N, Guerrero I (2004) Patched controls the Hedgehog gradient by endocytosis in a dynamin-dependent manner, but this internalization does not play a major role in signal transduction. Development 131:2395-2408.
45. Treisman JE, Rubin GM (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121:3519-3527.
46. Tsai YC, Yao JG, Chen PH, Posakony JW, Barolo S, Kim J, Sun YH (2007) Upd/Jak/STAT signaling represses wg transcription to allow initiation of morphogenetic furrow in Drosophila eye development. Dev Biol 306:760-771.
47. Ulrich F, Heisenberg CP (2009) Trafficking and cell migration. Traffic 10:811-818.
48. Vanlandingham PA, Ceresa BP (2009) Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J Biol Chem 284:12110-12124.
49. von Hilchen CM, Beckervordersandforth RM, Rickert C, Technau GM, Altenhein B (2008) Identity, origin, and migration of peripheral glial cells in the Drosophila embryo. Mech Dev 125:337-352.
50. von Hilchen CM, Hein I, Technau GM, Altenhein B (2010) Netrins guide migration of distinct glial cells in the Drosophila embryo. Development 137:1251-1262.
51. 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 82:67-76.
52. Wolff T, Ready DF (1993) Pattern formation in the Drosophila retina. In: The development of Drosophila (Bate M, Martinez Arias A, eds), pp 1277-1325. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.