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Notch Is Required in Adult Sensory Neurons for Morphological and Functional Plasticity of the Olfactory Circuit


Appropriate behavioral responses to changing environmental signals, such as odors, are essential for an organism’s survival. In Drosophila odors are detected by olfactory receptor neurons (ORNs) that synapse with second order projection neurons (PNs) and local interneurons in morphologically identifiable neuropils in the antennal lobe called glomeruli. Chronic odor exposure leads to changes in animal behavior as well as to changes in the activity of neurons in the olfactory circuit and increases in the volume of glomeruli. Here, we establish that Notch, an evolutionarily conserved transmembrane receptor that plays profound and pervasive roles in animal development, is required in adult Drosophila ORNs for functional and morphological plasticity in response to chronic odor exposure. These findings are significant because they point to a role for Notch in regulating activity dependent plasticity. Furthermore, we show that in regulating the odor dependent change in glomerular volume, Notch acts by both non-canonical, cleavage-independent and canonical, cleavage-dependent mechanisms, with the Notch ligand Delta in PNs switching the balance between the pathways. Because both the Notch pathway and the processing of olfactory information are highly conserved between flies and vertebrates these findings are likely to be of general relevance.


Vyšlo v časopise: Notch Is Required in Adult Sensory Neurons for Morphological and Functional Plasticity of the Olfactory Circuit. PLoS Genet 11(5): e32767. doi:10.1371/journal.pgen.1005244
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005244

Souhrn

Appropriate behavioral responses to changing environmental signals, such as odors, are essential for an organism’s survival. In Drosophila odors are detected by olfactory receptor neurons (ORNs) that synapse with second order projection neurons (PNs) and local interneurons in morphologically identifiable neuropils in the antennal lobe called glomeruli. Chronic odor exposure leads to changes in animal behavior as well as to changes in the activity of neurons in the olfactory circuit and increases in the volume of glomeruli. Here, we establish that Notch, an evolutionarily conserved transmembrane receptor that plays profound and pervasive roles in animal development, is required in adult Drosophila ORNs for functional and morphological plasticity in response to chronic odor exposure. These findings are significant because they point to a role for Notch in regulating activity dependent plasticity. Furthermore, we show that in regulating the odor dependent change in glomerular volume, Notch acts by both non-canonical, cleavage-independent and canonical, cleavage-dependent mechanisms, with the Notch ligand Delta in PNs switching the balance between the pathways. Because both the Notch pathway and the processing of olfactory information are highly conserved between flies and vertebrates these findings are likely to be of general relevance.


Zdroje

1. Devaud JM, Acebes A, Ferrús A (2001) Odor exposure causes central adaptation and morphological changes in selected olfactory glomeruli in Drosophila. J Neurosci 21: 6274–6282. 11487650

2. Devaud JM, Acebes A, Ramaswami M, Ferrús A (2003) Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age. J Neurobiol 56: 13–23. doi: 10.1002/neu.10215 12767029

3. Arenas A, Fernández VM, Farina WM (2009) Associative learning during early adulthood enhances later memory retention in honeybees. PLoS ONE 4: e8046. doi: 10.1371/journal.pone.0008046 19956575

4. Arenas A, Giurfa M, Farina WM, Sandoz JC (2009) Early olfactory experience modifies neural activity in the antennal lobe of a social insect at the adult stage. Eur J Neurosci 30: 1498–1508. doi: 10.1111/j.1460-9568.2009.06940.x 19821839

5. Sachse S, Rueckert E, Keller A, Okada R, Tanaka NK, et al. (2007) Activity-dependent plasticity in an olfactory circuit. Neuron 56: 838–850. doi: 10.1016/j.neuron.2007.10.035 18054860

6. Chakraborty TS, Goswami SP, Siddiqi O (2009) Sensory correlates of imaginal conditioning in Drosophila melanogaster. J Neurogenet 23: 210–219. doi: 10.1080/01677060802491559 19058083

7. Gao Q, Yuan B, Chess A (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 3: 780–785. doi: 10.1038/77680 10903570

8. Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125: 143–160. doi: 10.1016/j.cell.2006.01.050 16615896

9. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96: 725–736. 10089887

10. Wilson RI (2013) Early Olfactory Processing in Drosophila: Mechanisms and Principles. Annu Rev Neurosci 36: 217–241. doi: 10.1146/annurev-neuro-062111-150533 23841839

11. Das S, Sadanandappa MK, Dervan A, Larkin A, Lee JA, et al. (2011) Plasticity of local GABAergic interneurons drives olfactory habituation. Proc Natl Acad Sci USA 108: E646–E654. doi: 10.1073/pnas.1106411108 21795607

12. Hourcade B, Perisse E, Devaud JM, Sandoz J-C (2009) Long-term memory shapes the primary olfactory center of an insect brain. Learning & Memory 16: 607–615. doi: 10.1101/lm.1445609 19794186

13. Arenas A, Giurfa M, Sandoz JC, Hourcade B, Devaud JM, et al. (2012) Early olfactory experience induces structural changes in the primary olfactory center of an insect brain. Eur J Neurosci 35: 682–690. doi: 10.1111/j.1460-9568.2012.07999.x 22300014

14. Jones SV, Choi DC, Davis M, Ressler KJ (2008) Learning-dependent structural plasticity in the adult olfactory pathway. J Neurosci 28: 13106–13111. doi: 10.1523/JNEUROSCI.4465-08.2008 19052201

15. Davis RL (2004) Olfactory learning. Neuron 44: 31–48. doi: 10.1016/j.neuron.2004.09.008 15450158

16. Root CM, Masuyama K, Green DS, Enell LE, Nässel DR, et al. (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59: 311–321. doi: 10.1016/j.neuron.2008.07.003 18667158

17. Root CM, Ko KI, Jafari A, Wang JW (2011) Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145: 133–144. doi: 10.1016/j.cell.2011.02.008 21458672

18. Iyengar A, Chakraborty TS, Goswami SP, Wu C-F, Siddiqi O (2010) Post-eclosion odor experience modifies olfactory receptor neuron coding in Drosophila. Proc Natl Acad Sci USA 107: 9855–9860. doi: 10.1073/pnas.1003856107 20448199

19. Kass MD, Rosenthal MC, Pottackal J, McGann JP (2013) Fear Learning Enhances Neural Responses to Threat-Predictive Sensory Stimuli. Science 342: 1389–1392. doi: 10.1126/science.1244916 24337299

20. Abraham NM, Vincis R, Lagier S, Rodriguez I, Carleton A (2014) Long term functional plasticity of sensory inputs mediated by olfactory learning. eLife 3: e02109–e02109. doi: 10.7554/eLife.02109.011 24642413

21. Lieber T, Kidd S, Struhl G (2011) DSL-Notch signaling in the Drosophila brain in response to olfactory stimulation. Neuron 69: 468–481. doi: 10.1016/j.neuron.2010.12.015 21315258

22. Greenwald I (1998) LIN-12/Notch signaling: lessons from worms and flies. Genes Dev 12: 1751–1762. 9637676

23. Lai EC (2004) Notch signaling: control of cell communication and cell fate. Development 131: 965–973. doi: 10.1242/dev.01074 14973298

24. Louvi A, Artavanis-Tsakonas S (2006) Notch signalling in vertebrate neural development. Nat Rev Neurosci 7: 93–102. doi: 10.1038/nrn1847 16429119

25. Conboy L, Seymour CM, Monopoli MP, O'Sullivan NC, Murphy KJ, et al. (2007) Notch signalling becomes transiently attenuated during long-term memory consolidation in adult Wistar rats. Neurobiol Learn Mem 88: 342–351. doi: 10.1016/j.nlm.2007.04.006 17543552

26. Costa RM, Honjo T, Silva AJ (2003) Learning and memory deficits in Notch mutant mice. Curr Biol 13: 1348–1354. 12906797

27. Dahlhaus M, Hermans JM, Van Woerden LH, Saiepour MH, Nakazawa K, et al. (2008) Notch1 signaling in pyramidal neurons regulates synaptic connectivity and experience-dependent modifications of acuity in the visual cortex. J Neurosci 28: 10794–10802. doi: 10.1523/JNEUROSCI.1348-08.2008 18945887

28. Ge X, Hannan F, Xie Z, Feng C, Tully T, et al. (2004) Notch signaling in Drosophila long-term memory formation. Proc Natl Acad Sci USA 101: 10172–10176. doi: 10.1073/pnas.0403497101 15220476

29. Matsuno M, Horiuchi J, Tully T, Saitoe M (2009) The Drosophila cell adhesion molecule klingon is required for long-term memory formation and is regulated by Notch. Proc Natl Acad Sci USA 106: 310–315. doi: 10.1073/pnas.0807665106 19104051

30. Presente A, Boyles RS, Serway CN, de Belle JS, Andres AJ (2004) Notch is required for long-term memory in Drosophila. Proc Natl Acad Sci USA 101: 1764–1768. doi: 10.1073/pnas.0308259100 14752200

31. Wang Y, Chan SL, Miele L, Yao PJ, Mackes J, et al. (2004) Involvement of Notch signaling in hippocampal synaptic plasticity. Proc Natl Acad Sci USA 101: 9458–9462. doi: 10.1073/pnas.0308126101 15190179

32. Alberi L, Liu S, Wang Y, Badie R, Smith-Hicks C, et al. (2011) Activity-induced Notch signaling in neurons requires Arc/Arg3.1 and is essential for synaptic plasticity in hippocampal networks. Neuron 69: 437–444. doi: 10.1016/j.neuron.2011.01.004 21315255

33. Zhang J, Little CJ, Tremmel DM, Yin JCP, Wesley CS (2013) Notch-inducible hyperphosphorylated CREB and its ultradian oscillation in long-term memory formation. J Neurosci 33: 12825–12834. doi: 10.1523/JNEUROSCI.0783-13.2013 23904617

34. Yoon K-J, Lee H-R, Jo YS, An K, Jung S-Y, et al. (2012) Mind bomb-1 is an essential modulator of long-term memory and synaptic plasticity via the Notch signaling pathway. Mol Brain 5: 40. doi: 10.1186/1756-6606-5-40 23111145

35. Dias BG, Goodman JV, Ahluwalia R, Easton AE, Andero R, et al. (2014) Amygdala-Dependent Fear Memory Consolidation via miR-34a and Notch Signaling. Neuron: 1–13. doi: 10.1016/j.neuron.2014.07.019

36. Zheng J, Watanabe H, Wines-Samuelson M, Zhao H, Gridley T, et al. (2012) Conditional deletion of Notch1 and Notch2 genes in excitatory neurons of postnatal forebrain does not cause neurodegeneration or reduction of Notch mRNAs and proteins. J Biol Chem 287: 20356–20368. doi: 10.1074/jbc.M112.349738 22505716

37. Sato C, Turkoz M, Dearborn JT, Wozniak DF, Kopan R, et al. (2012) Loss of RBPj in postnatal excitatory neurons does not cause neurodegeneration or memory impairments in aged mice. PLoS ONE 7: e48180. doi: 10.1371/journal.pone.0048180 23110206

38. Kopan R, Ilagan MXG (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137: 216–233. doi: 10.1016/j.cell.2009.03.045 19379690

39. Hayward P, Brennan K, Sanders P, Balayo T, DasGupta R, et al. (2005) Notch modulates Wnt signalling by associating with Armadillo/beta-catenin and regulating its transcriptional activity. Development 132: 1819–1830. doi: 10.1242/dev.01724 15772135

40. Kwon C, Cheng P, King IN, Andersen P, Shenje L, et al. (2011) Notch post-translationally regulates β-catenin protein in stem and progenitor cells. Nature Cell Biology 13: 1244–1251. doi: 10.1038/ncb2313 21841793

41. Song JK, Giniger E (2011) Noncanonical Notch function in motor axon guidance is mediated by Rac GTPase and the GEF1 domain of Trio. Dev Dyn 240: 324–332. doi: 10.1002/dvdy.22525 21246649

42. Kuzina I, Song JK, Giniger E (2011) How Notch establishes longitudinal axon connections between successive segments of the Drosophila CNS. Development 138: 1839–1849. doi: 10.1242/dev.062471 21447553

43. Le Gall M, De Mattei C, Giniger E (2008) Molecular separation of two signaling pathways for the receptor, Notch. Dev Biol 313: 556–567. doi: 10.1016/j.ydbio.2007.10.030 18062953

44. Lee KS, Wu Z, Song Y, Mitra SS, Feroze AH, et al. (2013) Roles of PINK1, mTORC2, and mitochondria in preserving brain tumor-forming stem cells in a noncanonical Notch signaling pathway. Genes Dev 27: 2642–2647. doi: 10.1101/gad.225169.113 24352421

45. Perumalsamy LR, Nagala M, Banerjee P, Sarin A (2009) A hierarchical cascade activated by non-canonical Notch signaling and the mTOR-Rictor complex regulates neglect-induced death in mammalian cells. Cell Death Differ 16: 879–889. doi: 10.1038/cdd.2009.20 19265851

46. Layden MJ, Martindale MQ (2014) Non-canonical Notch signaling represents an ancestral mechanism to regulate neural differentiation. Evodevo 5: 30. doi: 10.1186/2041-9139-5-30 25705370

47. Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15: 1548–1553. doi: 10.1016/j.cub.2005.07.066 16139209

48. Couto A, Alenius M, Dickson BJ (2005) Molecular, Anatomical, and Functional Organization of the Drosophila Olfactory System. Current Biology 15: 1535–1547. doi: 10.1016/j.cub.2005.07.034 16139208

49. Berdnik D, Chihara T, Couto A, Luo L (2006) Wiring stability of the adult Drosophila olfactory circuit after lesion. J Neurosci 26: 3367–3376. doi: 10.1523/JNEUROSCI.4941-05.2006 16571743

50. Brochtrup A, Hummel T (2011) Olfactory map formation in the Drosophila brain: genetic specificity and neuronal variability. Curr Opin Neurobiol 21: 85–92. doi: 10.1016/j.conb.2010.11.001 21112768

51. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765–1768. doi: 10.1126/science.1089035 14657498

52. Scott K, Brady R, Cravchik A, Morozov P, Rzhetsky A, et al. (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104: 661–673. doi: 10.1016/S0092-8674(02)02052-4 11257221

53. Suh GSB, Wong AM, Hergarden AC, Wang JW, Simon AF, et al. (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431: 854–859. doi: 10.1038/nature02980 15372051

54. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, et al. (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Meth 6: 875–881. doi: 10.1038/nmeth.1398

55. Chen T-W, Wardill TJ, Sun Y, Pulver SR, Renninger SL, et al. (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499: 295–300. doi: 10.1038/nature12354 23868258

56. Han DD, Stein D, Stevens LM (2000) Investigating the function of follicular subpopulations during Drosophila oogenesis through hormone-dependent enhancer-targeted cell ablation. Development 127: 573–583. 10631178

57. del Álamo D, Rouault H, Schweisguth F (2011) Mechanism and significance of cis-inhibition in Notch signalling. Curr Biol 21: R40–R47. doi: 10.1016/j.cub.2010.10.034 21215938

58. Deblandre GA, Lai EC, Kintner C (2001) Xenopus neuralized is a ubiquitin ligase that interacts with XDelta1 and regulates Notch signaling. Dev Cell 1: 795–806. 11740941

59. Lai EC, Deblandre GA, Kintner C, Rubin GM (2001) Drosophila neuralized is a ubiquitin ligase that promotes the internalization and degradation of delta. Dev Cell 1: 783–794. 11740940

60. Pavlopoulos E, Pitsouli C, Klueg KM, Muskavitch MA, Moschonas NK, et al. (2001) neuralized Encodes a peripheral membrane protein involved in delta signaling and endocytosis. Dev Cell 1: 807–816. 11740942

61. Wang W, Struhl G (2004) Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 131: 5367–5380. doi: 10.1242/dev.01413 15469974

62. Overstreet E (2004) Fat facets and Liquid facets promote Delta endocytosis and Delta signaling in the signaling cells. Development 131: 5355–5366. doi: 10.1242/dev.01434 15469967

63. Francis R, McGrath G, Zhang J, Ruddy DA, Sym M, et al. (2002) aph-1 and pen-2 are required for Notch pathway signaling, gamma-secretase cleavage of betaAPP, and presenilin protein accumulation. Dev Cell 3: 85–97. 12110170

64. Goutte C, Tsunozaki M, Hale VA, Priess JR (2002) APH-1 is a multipass membrane protein essential for the Notch signaling pathway in Caenorhabditis elegans embryos. Proc Natl Acad Sci USA 99: 775–779. doi: 10.1073/pnas.022523499 11792846

65. Morel V, Schweisguth F (2000) Repression by suppressor of hairless and activation by Notch are required to define a single row of single-minded expressing cells in the Drosophila embryo. Genes Dev 14: 377–388. 10673509

66. Hsieh JJ, Henkel T, Salmon P, Robey E, Peterson MG, et al. (1996) Truncated mammalian Notch1 activates CBF1/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2. Mol Cell Biol 16: 952–959. 8622698

67. Wesley CS, Mok L-P (2003) Regulation of Notch signaling by a novel mechanism involving suppressor of hairless stability and carboxyl terminus-truncated notch. Mol Cell Biol 23: 5581–5593. 12897132

68. Kidd S, Lieber T, Young MW (1998) Ligand-induced cleavage and regulation of nuclear entry of Notch in Drosophila melanogaster embryos. Genes Dev 12: 3728–3740. 9851979

69. Wu L, Aster JC, Blacklow SC, Lake R, Artavanis-Tsakonas S, et al. (2000) MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nat Genet 26: 484–489. doi: 10.1038/82644 11101851

70. Kankel MW, Hurlbut GD, Upadhyay G, Yajnik V, Yedvobnick B, et al. (2007) Investigating the genetic circuitry of mastermind in Drosophila, a notch signal effector. Genetics 177: 2493–2505. doi: 10.1534/genetics.107.080994 18073442

71. Vied C, Kalderon D (2009) Hedgehog-stimulated stem cells depend on non-canonical activity of the Notch co-activator Mastermind. Development 136: 2177–2186. doi: 10.1242/dev.035329 19474148

72. McElhinny AS, Li J-L, Wu L (2008) Mastermind-like transcriptional co-activators: emerging roles in regulating cross talk among multiple signaling pathways. Oncogene 27: 5138–5147. doi: 10.1038/onc.2008.228 18758483

73. Sestan N, Artavanis-Tsakonas S, Rakic P (1999) Contact-dependent inhibition of cortical neurite growth mediated by notch signaling. Science 286: 741–746. 10531053

74. Franklin JL, Berechid BE, Cutting FB, Presente A, Chambers CB, et al. (1999) Autonomous and non-autonomous regulation of mammalian neurite development by Notch1 and Delta1. Curr Biol 9: 1448–1457. 10607588

75. Berezovska O, McLean P, Knowles R, Frosh M, Lu FM, et al. (1999) Notch1 inhibits neurite outgrowth in postmitotic primary neurons. Neuroscience 93: 433–439. 10465425

76. Levy OA, Lah JJ, Levey AI (2002) Notch signaling inhibits PC12 cell neurite outgrowth via RBP-J-dependent and-independent mechanisms. Dev Neurosci 24: 79–88. 12145413

77. Hassan BA, Bermingham NA, He Y, Sun Y, Jan YN, et al. (2000) atonal regulates neurite arborization but does not act as a proneural gene in the Drosophila brain. Neuron 25: 549–561. 10774724

78. Knaden M, Strutz A, Ahsan J, Sachse S, Hansson BS (2012) Spatial representation of odorant valence in an insect brain. Cell Reports 1: 392–399. doi: 10.1016/j.celrep.2012.03.002 22832228

79. Schlief ML, Wilson RI (2007) Olfactory processing and behavior downstream from highly selective receptor neurons. Nat Neurosci 10: 623–630. doi: 10.1038/nn1881 17417635

80. Carlsson MA, Diesner M, Schachtner J, Nässel DR (2010) Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits. J Comp Neurol 518: 3359–3380. doi: 10.1002/cne.22405 20575072

81. Yew JY, Wang Y, Barteneva N, Dikler S, Kutz-Naber KK, et al. (2009) Analysis of neuropeptide expression and localization in adult drosophila melanogaster central nervous system by affinity cell-capture mass spectrometry. J Proteome Res 8: 1271–1284. doi: 10.1021/pr800601x 19199706

82. Nässel DR, Winther AME (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92: 42–104. doi: 10.1016/j.pneurobio.2010.04.010 20447440

83. Heitzler P (2010) Biodiversity and noncanonical Notch signaling. Curr Top Dev Biol 92: 457–481. doi: 10.1016/S0070-2153(10)92014-0 20816404

84. Cingolani LA, Goda Y (2008) Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9: 344–356. doi: 10.1038/nrn2373 18425089

85. Dillon C, Goda Y (2005) The actin cytoskeleton: integrating form and function at the synapse. Annu Rev Neurosci 28: 25–55. doi: 10.1146/annurev.neuro.28.061604.135757 16029114

86. Lamprecht R, LeDoux J (2004) Structural plasticity and memory. Nat Rev Neurosci 5: 45–54. doi: 10.1038/nrn1301 14708003

87. Giniger E (1998) A role for Abl in Notch signaling. Neuron 20: 667–681. 9581760

88. Crowner D, Le Gall M, Gates MA, Giniger E (2003) Notch steers Drosophila ISNb motor axons by regulating the Abl signaling pathway. Curr Biol 13: 967–972. 12781136

89. Sibbe M, Förster E, Basak O, Taylor V, Frotscher M (2009) Reelin and Notch1 cooperate in the development of the dentate gyrus. J Neurosci 29: 8578–8585. doi: 10.1523/JNEUROSCI.0958-09.2009 19571148

90. Hashimoto-Torii K, Torii M, Sarkisian MR, Bartley CM, Shen J, et al. (2008) Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 60: 273–284. doi: 10.1016/j.neuron.2008.09.026 18957219

91. Huang W, Zhu PJ, Zhang S, Zhou H, Stoica L, et al. (2013) mTORC2 controls actin polymerization required for consolidation of long-term memory. Nat Neurosci 16: 441–448. doi: 10.1038/nn.3351 23455608

92. Tan Y, Yu D, Busto GU, Wilson C, Davis RL (2013) Wnt signaling is required for long-term memory formation. Cell Reports 4: 1082–1089. doi: 10.1016/j.celrep.2013.08.007 24035392

93. Twick I, Lee JA, Ramaswami M (2014) Olfactory habituation in Drosophila-odor encoding and its plasticity in the antennal lobe. Prog Brain Res 208: 3–38. doi: 10.1016/B978-0-444-63350-7.00001–2 24767477

94. Ni J-Q, Zhou R, Czech B, Liu L-P, Holderbaum L, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Meth 8: 405–407. doi: 10.1038/nmeth.1592

95. Pfeiffer BD, Ngo T-TB, Hibbard KL, Murphy C, Jenett A, et al. (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186: 735–755. doi: 10.1534/genetics.110.119917 20697123

96. Nagel AC, Maier D, Preiss A (2002) Green fluorescent protein as a convenient and versatile marker for studies on functional genomics in Drosophila. Dev Genes Evol 212: 93–98. doi: 10.1007/s00427-002-0210-y 11914941

97. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451–461. 10197526

98. Presente A, Shaw S, Nye JS, Andres AJ (2002) Transgene-mediated RNA interference defines a novel role for notch in chemosensory startle behavior. Genesis 34: 165–169. doi: 10.1002/gene.10149 12324975

99. Kennerdell JR, Carthew RW (2000) Heritable gene silencing in Drosophila using double-stranded RNA. Nat Biotechnol 18: 896–898. doi: 10.1038/78531 10932163

100. Pfeiffer BD, Truman JW, Rubin GM (2012) Using translational enhancers to increase transgene expression in Drosophila. Proc Natl Acad Sci USA 109: 6626–6631. doi: 10.1073/pnas.1204520109 22493255

101. Tanaka NK, Awasaki T, Shimada T, Ito K (2004) Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 14: 449–457. doi: 10.1016/j.cub.2004.03.006 15043809

102. Xiong WC, Okano H, Patel NH, Blendy JA, Montell C (1994) repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev 8: 981–994. 7926782

103. Das A, Sen S, Lichtneckert R, Okada R, Ito K, et al. (2008) Drosophila olfactory local interneurons and projection neurons derive from a common neuroblast lineage specified by the empty spiracles gene. Neural Dev 3: 33. doi: 10.1186/1749-8104-3-33 19055770

104. Dietzl G, Chen D, Schnorrer F, Su K-C, Barinova Y, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151–156. doi: 10.1038/nature05954 17625558

105. Merdes G, Soba P, Loewer A, Bilic MV, Beyreuther K, et al. (2004) Interference of human and Drosophila APP and APP-like proteins with PNS development in Drosophila. EMBO J 23: 4082–4095. doi: 10.1038/sj.emboj.7600413 15385958

106. Datta SR, Vasconcelos ML, Ruta V, Luo S, Wong A, et al. (2008) The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452: 473–477. doi: 10.1038/nature06808 18305480

107. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112: 271–282. 12553914

108. Caron SJC, Ruta V, Abbott LF, Axel R (2013) Random convergence of olfactory inputs in the Drosophila mushroom body. Nature 497: 113–117. doi: 10.1038/nature12063 23615618

109. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49: 833–844. doi: 10.1016/j.neuron.2006.02.008 16543132

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