Steroids as external temporal codes act via miRNAs and cooperate with cytokines in differential neurogenesis

Fly

Volumn 7, Issue 3, 2013, Pages

  Kucherenko, Mariya M ^a   Shcherbata, Halyna R ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Differential cell adhesion; Drosophila mushroom body; JAK STAT cytokine signaling; MicroRNA let 7; Steroid hormone ecdysone; Temporal identity switch

Indexed keywords

EID: 84880142820     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: None     Document Type: Article

References (106)

1. Leone DP, Srinivasan K, Chen B, Alcamo E, McConnell SK. The determination of projection neuron identity in the developing cerebral cortex. Curr Opin Neurobiol 2008; 18:28-35; PMID:18508260; http://dx.doi.org/10.1016/j.conb.2008.05.006
2. Passante L, Gaspard N, Degraeve M, Frisen J, Kullander K, De Maertelaer V, et al. Temporal regulation of ephrin/Eph signalling is required for the spatial patterning of the mammalian striatum. Development 2008; 135:3281-90; PMID:18755772; http://dx.doi.org/10.1242/dev.024778
3. Lin S, Lee T. Generating neuronal diversity in the Drosophila central nervous system. Dev Dyn 2012; 241:57-68; PMID:21932323; http://dx.doi. org/10.1002/dvdy.22739
4. Franco SJ, Muller U. Shaping our minds: stem and progenitor cell diversity in the mammalian neocortex. Neuron 2013; 77:19-34; PMID:23312513; http://dx.doi.org/10.1016/j.neuron.2012.12.022
5. Hoshino M. Neuronal subtype specification in the cerebellum and dorsal hindbrain. Dev Growth Differ 2012; 54:317-26; PMID:22404503; http://dx.doi. org/10.1111/j.1440-169X.2012.01330.x
6. Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development 1987; 101:1-22; PMID:2896587
7. Skeath JB, Thor S. Genetic control of Drosophila nerve cord development. Curr Opin Neurobiol 2003; 13:8-15; PMID:12593977; http://dx.doi. org/10.1016/S0959-4388(03)00007-2
8. Technau GM, Berger C, Urbach R. Generation of cell diversity and segmental pattern in the embryonic central nervous system of Drosophila. Dev Dyn 2006; 235:861-9; PMID:16222713; http://dx.doi. org/10.1002/dvdy.20566
9. Urbach R, Volland D, Seibert J, Technau GM. Segment-specific requirements for dorsoventral patterning genes during early brain development in Drosophila. Development 2006; 133:4315-30; PMID:17038517; http://dx.doi.org/10.1242/ dev.02605
10. von Ohlen T, Doe CQ. Convergence of dorsal, dpp, and egfr signaling pathways subdivides the drosophila neuroectoderm into three dorsal-ventral columns. Dev Biol 2000; 224:362-72; PMID:10926773; http://dx.doi.org/10.1006/dbio.2000.9789
11. Hirth F, Hartmann B, Reichert H. Homeotic gene action in embryonic brain development of Drosophila. Development 1998; 125:1579-89; PMID:9521896
12. Lee T, Lee A, Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 1999; 126:4065-76; PMID:10457015
13. Isshiki T, Pearson B, Holbrook S, Doe CQ. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 2001; 106:511-21; PMID:11525736; http://dx.doi.org/10.1016/S0092-8674(01)00465-2
14. Schmid A, Chiba A, Doe CQ. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 1999; 126:4653-89; PMID:10518486
15. Riddiford LM. Hormones and Drosophila development. In: Bate M, Arias AM, eds. The Development of Drosophila Melanogaster. Plainview, NY: Cold Spring Harbor Laboratory Press, 1993.
16. Kucherenko MM, Barth J, Fiala A, Shcherbata HR. Steroid-induced microRNA let-7 acts as a spatiotemporal code for neuronal cell fate in the developing Drosophila brain. EMBO J 2012; 31:4511-23; PMID:23160410; http://dx.doi.org/10.1038/ emboj.2012.298
17. Sempere LF, Sokol NS, Dubrovsky EB, Berger EM, Ambros V. Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-Complex gene activity. Dev Biol 2003; 259:9-18; PMID:12812784; http:// dx.doi.org/10.1016/S0012-1606(03)00208-2
18. Chawla G, Sokol NS. Hormonal activation of let-7-C microRNAs via EcR is required for adult Drosophila melanogaster morphology and function. Development 2012; 139:1788-97; PMID:22510985; http://dx.doi.org/10.1242/dev.077743
19. Wu YC, Chen CH, Mercer A, Sokol NS. Let-7-complex microRNAs regulate the temporal identity of Drosophila mushroom body neurons via chinmo. Dev Cell 2012; 23:202-9; PMID:22814608; http:// dx.doi.org/10.1016/j.devcel.2012.05.013
20. Heisenberg M. Mushroom body memoir: from maps to models. Nat Rev Neurosci 2003; 4:266-75; PMID:12671643; http://dx.doi.org/10.1038/ nrn1074
21. Riddiford LM. Hormone receptors and the regulation of insect metamorphosis. Receptor 1993; 3:203-9; PMID:8167571
22. Kozlova T, Thummel CS. Essential roles for ecdysone signaling during Drosophila mid-embryonic development. Science 2003; 301:1911-4; PMID:12958367; http://dx.doi.org/10.1126/science.1087419
23. McBrayer Z, Ono H, Shimell M, Parvy JP, Beckstead RB, Warren JT, et al. Prothoracicotropic hormone regulates developmental timing and body size in Drosophila. Dev Cell 2007; 13:857-71; PMID:18061567; http://dx.doi.org/10.1016/j.devcel. 2007.11.003
24. Shirras AD, Bownes M. Separate DNA sequences are required for normal female and ecdysoneinduced male expression of Drosophila melanogaster yolk protein 1. Mol Gen Genet 1987; 210:153-5; PMID:3123886; http://dx.doi.org/10.1007/ BF00337772
25. Gaziova I, Bonnette PC, Henrich VC, Jindra M. Cell-autonomous roles of the ecdysoneless gene in Drosophila development and oogenesis. Development 2004; 131:2715-25; PMID:15128659; http://dx.doi. org/10.1242/dev.01143
26. Buszczak M, Freeman MR, Carlson JR, Bender M, Cooley L, Segraves WA. Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila. Development 1999; 126:4581-9; PMID:10498692
27. Terashima J, Bownes M. A microarray analysis of genes involved in relating egg production to nutritional intake in Drosophila melanogaster. Cell Death Differ 2005; 12:429-40; PMID:15776001; http:// dx.doi.org/10.1038/sj.cdd.4401587
28. Schubiger M, Carre C, Antoniewski C, Truman JW. Ligand-dependent de-repression via EcR/USP acts as a gate to coordinate the differentiation of sensory neurons in the Drosophila wing. Development 2005; 132:5239-48; PMID:16267093; http://dx.doi. org/10.1242/dev.02093
29. Konig A, Yatsenko AS, Weiss M, Shcherbata HR. Ecdysteroids affect Drosophila ovarian stem cell niche formation and early germline differentiation. EMBO J 2011; 30:1549-62; PMID:21423150; http://dx.doi.org/10.1038/emboj.2011.73
30. Riddiford LM, Cherbas P, Truman JW. Ecdysone receptors and their biological actions. Vitam Horm 2000; 60:1-73; PMID:11037621; http://dx.doi. org/10.1016/S0083-6729(00)60016-X
31. Jang AC, Chang YC, Bai J, Montell D. Border-cell migration requires integration of spatial and temporal signals by the BTB protein Abrupt. Nat Cell Biol 2009; 11:569-79; PMID:19350016; http://dx.doi. org/10.1038/ncb1863
32. Francis VA, Zorzano A, Teleman AA. dDOR is an EcR coactivator that forms a feed-forward loop connecting insulin and ecdysone signaling. Curr Biol 2010; 20:1799-808; PMID:20888228; http:// dx.doi.org/10.1016/j.cub.2010.08.055
33. Zheng X, Wang J, Haerry TE, Wu AY, Martin J, O'Connor MB, et al. TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 2003; 112:303-15; PMID:12581521; http://dx.doi. org/10.1016/S0092-8674(03)00072-2
34. Lee T, Marticke S, Sung C, Robinow S, Luo L. Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 2000; 28:807-18; PMID:11163268; http://dx.doi.org/10.1016/S0896-6273(00)00155-0
35. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75:843-54; PMID:8252621; http://dx.doi. org/10.1016/0092-8674(93)90529-Y
36. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000; 403:901-6; PMID:10706289; http://dx.doi. org/10.1038/35002607
37. Gomez-Orte E, Belles X. MicroRNA-dependent metamorphosis in hemimetabolan insects. Proc Natl Acad Sci U S A 2009; 106:21678-82; PMID:19966227; http://dx.doi.org/10.1073/ pnas.0907391106
38. Caygill EE, Johnston LA. Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Curr Biol 2008; 18:943-50; PMID:18571409; http://dx.doi. org/10.1016/j.cub.2008.06.020
39. Sokol NS, Xu P, Jan YN, Ambros V. Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes Dev 2008; 22:1591-6; PMID:18559475; http://dx.doi. org/10.1101/gad.1671708
40. Varghese J, Cohen SM. microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes Dev 2007; 21:2277-82; PMID:17761811; http://dx.doi. org/10.1101/gad.439807
41. Jin H, Kim VN, Hyun S. Conserved microRNA miR-8 controls body size in response to steroid signaling in Drosophila. Genes Dev 2012; 26:1427-32; PMID:22751499; http://dx.doi.org/10.1101/ gad.192872.112
42. Boulan L, Martin D, Milan M. bantam miRNA promotes systemic growth by connecting insulin signaling and ecdysone production. Curr Biol 2013; 23:473-8; PMID:23477723; http://dx.doi. org/10.1016/j.cub.2013.01.072
43. Kawashima H, Numakawa T, Kumamaru E, Adachi N, Mizuno H, Ninomiya M, et al. Glucocorticoid attenuates brain-derived neurotrophic factor-dependent upregulation of glutamate receptors via the suppression of microRNA-132 expression. Neuroscience 2010; 165:1301-11; PMID:19958814; http://dx.doi. org/10.1016/j.neuroscience.2009.11.057
44. Vreugdenhil E, Verissimo CS, Mariman R, Kamphorst JT, Barbosa JS, Zweers T, et al. MicroRNA 18 and 124a down-regulate the glucocorticoid receptor: implications for glucocorticoid responsiveness in the brain. Endocrinology 2009; 150:2220-8; PMID:19131573; http://dx.doi. org/10.1210/en.2008-1335
45. Huang YH, Lin YH, Chi HC, Liao CH, Liao CJ, Wu SM, et al. Thyroid hormone regulation of miR-21 enhances migration and invasion of hepatoma. Cancer Res 2013; 73:2505-17; PMID:23442323; http://dx.doi.org/10.1158/0008-5472.CAN-12-2218
46. Di Leva G, Gasparini P, Piovan C, Ngankeu A, Garofalo M, Taccioli C, et al. MicroRNA cluster 221-222 and estrogen receptor alpha interactions in breast cancer. J Natl Cancer Inst 2010; 102:706-21; PMID:20388878; http://dx.doi.org/10.1093/jnci/ djq102
47. Di Leva G, Piovan C, Gasparini P, Ngankeu A, Taccioli C, Briskin D, et al. Estrogen mediatedactivation of miR-191/425 cluster modulates tumorigenicity of breast cancer cells depending on estrogen receptor status. PLoS Genet 2013; 9:e1003311; PMID:23505378; http://dx.doi.org/10.1371/journal. pgen.1003311
48. Zhao JJ, Lin J, Yang H, Kong W, He L, Ma X, et al. MicroRNA-221/222 negatively regulates estrogen receptor alpha and is associated with tamoxifen resistance in breast cancer. J Biol Chem 2008; 283:31079-86; PMID:18790736; http://dx.doi. org/10.1074/jbc.M806041200
49. Akerblom M, Sachdeva R, Barde I, Verp S, Gentner B, Trono D, et al. MicroRNA-124 is a subventricular zone neuronal fate determinant. J Neurosci 2012; 32:8879-89; PMID:22745489; http://dx.doi. org/10.1523/JNEUROSCI.0558-12.2012
50. Boissart C, Nissan X, Giraud-Triboult K, Peschanski M, Benchoua A. miR-125 potentiates early neural specification of human embryonic stem cells. Development 2012; 139:1247-57; PMID:22357933; http://dx.doi.org/10.1242/dev.073627
51. Feng W, Feng Y. MicroRNAs in neural cell development and brain diseases. Sci China Life Sci 2011; 54:1103-12; PMID:22227902; http://dx.doi. org/10.1007/s11427-011-4249-8
52. Jovičić A, Roshan R, Moisoi N, Pradervand S, Moser R, Pillai B, et al. Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J Neurosci 2013; 33:5127-37; PMID:23516279; http://dx.doi.org/10.1523/ JNEUROSCI.0600-12.2013
53. Nowakowski TJ, Fotaki V, Pollock A, Sun T, Pratt T, Price DJ. MicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain. Proc Natl Acad Sci U S A 2013; 110:7056-61; PMID:23569256; http://dx.doi. org/10.1073/pnas.1219385110
54. Parsons XH, Parsons JF, Moore DA. Genome-Scale Mapping of MicroRNA Signatures in Human Embryonic Stem Cell Neurogenesis. Mol Med Ther 2012; 1; PMID:23543894; http://dx.doi. org/10.4172/2324-8769.1000105
55. Stappert L, Borghese L, Roese-Koerner B, Weinhold S, Koch P, Terstegge S, et al. MicroRNA-based promotion of human neuronal differentiation and subtype specification. PLoS One 2013; 8:e59011; PMID:23527072; http://dx.doi.org/10.1371/journal. pone.0059011
56. Weng R, Cohen SM. Drosophila miR-124 regulates neuroblast proliferation through its target anachronism. Development 2012; 139:1427-34; PMID:22378639; http://dx.doi.org/10.1242/ dev.075143
57. Zhao C, Sun G, Li S, Shi Y. A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol 2009; 16:365-71; PMID:19330006; http://dx.doi.org/10.1038/nsmb.1576
58. Marrone AK, Edeleva EV, Kucherenko MM, Hsiao NH, Shcherbata HR. Dg-Dys-Syn1 signaling in Drosophila regulates the microRNA profile. BMC Cell Biol 2012; 13:26; PMID:23107381; http:// dx.doi.org/10.1186/1471-2121-13-26
59. Zhao C, Sun G, Li S, Lang MF, Yang S, Li W, et al. MicroRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling. Proc Natl Acad Sci U S A 2010; 107:1876-81; PMID:20133835; http://dx.doi. org/10.1073/pnas.0908750107
60. Brett JO, Renault VM, Rafalski VA, Webb AE, Brunet A. The microRNA cluster miR-106b~25 regulates adult neural stem/progenitor cell proliferation and neuronal differentiation. Aging (Albany NY) 2011; 3:108-24; PMID:21386132
61. Sun G, Ye P, Murai K, Lang MF, Li S, Zhang H, et al. miR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cells. Nat Commun 2011; 2:529; PMID:22068596; http:// dx.doi.org/10.1038/ncomms1532
62. Liu C, Teng ZQ, Santistevan NJ, Szulwach KE, Guo W, Jin P, et al. Epigenetic regulation of miR-184 by MBD1 governs neural stem cell proliferation and differentiation. Cell Stem Cell 2010; 6:433-44; PMID:20452318; http://dx.doi.org/10.1016/j. stem.2010.02.017
63. Cheng LC, Pastrana E, Tavazoie M, Doetsch F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 2009; 12:399-408; PMID:19287386; http://dx.doi.org/10.1038/ nn.2294
64. Liu XS, Chopp M, Wang XL, Zhang L, Hozeska-Solgot A, Tang T, et al. MicroRNA-17/92 cluster mediates the proliferation and survival of neural progenitor cells after stroke. J Biol Chem 2013; 288:12478-88; PMID:23511639; http://dx.doi. org/10.1074/jbc.M112.449025
65. Ishimoto H, Sakai T, Kitamoto T. Ecdysone signaling regulates the formation of long-term courtship memory in adult Drosophila melanogaster. Proc Natl Acad Sci U S A 2009; 106:6381-6; PMID:19342482; http://dx.doi.org/10.1073/pnas.0810213106
66. Zollman S, Godt D, Prive GG, Couderc JL, Laski FA. The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci U S A 1994; 91:10717-21; PMID:7938017; http://dx.doi. org/10.1073/pnas.91.22.10717
67. Perez-Torrado R, Yamada D, Defossez PA. Born to bind: the BTB protein-protein interaction domain. Bioessays 2006; 28:1194-202; PMID:17120193; http://dx.doi.org/10.1002/bies.20500
68. Stogios PJ, Downs GS, Jauhal JJ, Nandra SK, Prive GG. Sequence and structural analysis of BTB domain proteins. Genome Biol 2005; 6:R82; PMID:16207353; http://dx.doi.org/10.1186/gb-2005-6-10-r82
69. Hu S, Fambrough D, Atashi JR, Goodman CS, Crews ST. The Drosophila abrupt gene encodes a BTB-zinc finger regulatory protein that controls the specificity of neuromuscular connections. Genes Dev 1995; 9:2936-48; PMID:7498790; http://dx.doi. org/10.1101/gad.9.23.2936
70. Mitchelmore C, Kjaerulff KM, Pedersen HC, Nielsen JV, Rasmussen TE, Fisker MF, et al. Characterization of two novel nuclear BTB/POZ domain zinc finger isoforms. Association with differentiation of hippocampal neurons, cerebellar granule cells, and macroglia. J Biol Chem 2002; 277:7598-609; PMID:11744704; http://dx.doi.org/10.1074/jbc. M110023200
71. Baubet V, Xiang C, Molczan A, Roccograndi L, Melamed S, Dahmane N. Rp58 is essential for the growth and patterning of the cerebellum and for glutamatergic and GABAergic neuron development. Development 2012; 139:1903-9; PMID:22513377; http://dx.doi.org/10.1242/dev.075606
72. Xiang C, Baubet V, Pal S, Holderbaum L, Tatard V, Jiang P, et al. RP58/ZNF238 directly modulates proneurogenic gene levels and is required for neuronal differentiation and brain expansion. Cell Death Differ 2012; 19:692-702; PMID:22095278; http:// dx.doi.org/10.1038/cdd.2011.144
73. Guo M, Bier E, Jan LY, Jan YN. tramtrack acts downstream of numb to specify distinct daughter cell fates during asymmetric cell divisions in the Drosophila PNS. Neuron 1995; 14:913-25; PMID:7748559; http://dx.doi.org/10.1016/0896-6273(95)90330-5
74. Salzberg A, D'Evelyn D, Schulze KL, Lee JK, Strumpf D, Tsai L, et al. Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development. Neuron 1994; 13:269-87; PMID:8060613; http://dx.doi.org/10.1016/0896-6273(94)90346-8
75. Giniger E, Tietje K, Jan LY, Jan YN. lola encodes a putative transcription factor required for axon growth and guidance in Drosophila. Development 1994; 120:1385-98; PMID:8050351
76. Sugimura K, Satoh D, Estes P, Crews S, Uemura T. Development of morphological diversity of dendrites in Drosophila by the BTB-zinc finger protein abrupt. Neuron 2004; 43:809-22; PMID:15363392; http:// dx.doi.org/10.1016/j.neuron.2004.08.016
77. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci U S A 1996; 93:9687-92; PMID:8790392; http://dx.doi.org/10.1073/pnas.93.18.9687
78. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, et al. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 1996; 87:1079-89; PMID:8978612; http://dx.doi.org/10.1016/S0092-8674(00)81802-4
79. Zhu S, Lin S, Kao CF, Awasaki T, Chiang AS, Lee T. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 2006; 127:409-22; PMID:17055440; http://dx.doi. org/10.1016/j.cell.2006.08.045
80. Bauer S, Kerr BJ, Patterson PH. The neuropoietic cytokine family in development, plasticity, disease and injury. Nat Rev Neurosci 2007; 8:221-32; PMID:17311007; http://dx.doi.org/10.1038/ nrn2054
81. Ngo KT, Wang J, Junker M, Kriz S, Vo G, Asem B, et al. Concomitant requirement for Notch and Jak/Stat signaling during neuro-epithelial differentiation in the Drosophila optic lobe. Dev Biol 2010; 346:284-95; PMID:20692248; http://dx.doi.org/10.1016/j. ydbio.2010.07.036
82. Copf T, Goguel V, Lampin-Saint-Amaux A, Scaplehorn N, Preat T. Cytokine signaling through the JAK/STAT pathway is required for long-term memory in Drosophila. Proc Natl Acad Sci U S A 2011; 108:8059-64; PMID:21518857; http://dx.doi. org/10.1073/pnas.1012919108
83. Bauer S, Patterson PH. Leukemia inhibitory factor promotes neural stem cell self-renewal in the adult brain. J Neurosci 2006; 26:12089-99; PMID:17108182; http://dx.doi.org/10.1523/ JNEUROSCI.3047-06.2006
84. Yasugi T, Umetsu D, Murakami S, Sato M, Tabata T. Drosophila optic lobe neuroblasts triggered by a wave of proneural gene expression that is negatively regulated by JAK/STAT. Development 2008; 135:1471-80; PMID:18339672; http://dx.doi.org/10.1242/ dev.019117
85. Starz-Gaiano M, Melani M, Wang X, Meinhardt H, Montell DJ. Feedback inhibition of Jak/STAT signaling by apontic is required to limit an invasive cell population. Dev Cell 2008; 14:726-38; PMID:18477455; http://dx.doi.org/10.1016/j.devcel. 2008.03.005
86. Siegrist SE, Haque NS, Chen CH, Hay BA, Hariharan IK. Inactivation of both Foxo and reaper promotes long-term adult neurogenesis in Drosophila. Curr Biol 2010; 20:643-8; PMID:20346676; http:// dx.doi.org/10.1016/j.cub.2010.01.060
87. Grieder NC, Charlafti I, Kloter U, Jackle H, Schafer U, Gehring WJ. Misexpression screen in Drosophila melanogaster aiming to reveal novel factors involved in formation of body parts. Genetics 2007; 175:1707-18; PMID:17179072; http://dx.doi.org/10.1534/ genetics.106.064212
88. Flaherty MS, Salis P, Evans CJ, Ekas LA, Marouf A, Zavadil J, et al. chinmo is a functional effector of the JAK/STAT pathway that regulates eye development, tumor formation, and stem cell selfrenewal in Drosophila. Dev Cell 2010; 18:556-68; PMID:20412771; http://dx.doi.org/10.1016/j.devcel. 2010.02.006
89. Jontes JD, Phillips GR. Selective stabilization and synaptic specificity: a new cell-biological model. Trends Neurosci 2006; 29:186-91; PMID:16490264; http://dx.doi.org/10.1016/j.tins.2006.02.002
90. Winther M, Berezin V, Walmod PS. NCAM2/ OCAM/RNCAM: cell adhesion molecule with a role in neuronal compartmentalization. Int J Biochem Cell Biol 2012; 44:441-6; PMID:22155300; http:// dx.doi.org/10.1016/j.biocel.2011.11.020
91. Han MR, Schellenberg GD, Wang LS; Alzheimer's Disease Neuroimaging Initiative. Genome-wide association reveals genetic effects on human Aβ42 and τ protein levels in cerebrospinal fluids: a case control study. BMC Neurol 2010; 10:90; PMID:20932310; http://dx.doi.org/10.1186/1471-2377-10-90
92. Hussman JP, Chung RH, Griswold AJ, Jaworski JM, Salyakina D, Ma D, et al. A noise-reduction GWAS analysis implicates altered regulation of neurite outgrowth and guidance in autism. Mol Autism 2011; 2:1; PMID:21247446; http://dx.doi. org/10.1186/2040-2392-2-1
93. Makino T, McLysaght A. Ohnologs in the human genome are dosage balanced and frequently associated with disease. Proc Natl Acad Sci U S A 2010; 107:9270-4; PMID:20439718; http://dx.doi. org/10.1073/pnas.0914697107
94. Atz ME, Rollins B, Vawter MP. NCAM1 association study of bipolar disorder and schizophrenia: polymorphisms and alternatively spliced isoforms lead to similarities and differences. Psychiatr Genet 2007; 17:55-67; PMID:17413444; http://dx.doi. org/10.1097/YPG.0b013e328012d850
95. Bisaz R, Conboy L, Sandi C. Learning under stress: a role for the neural cell adhesion molecule NCAM. Neurobiol Learn Mem 2009; 91:333-42; PMID:19041949; http://dx.doi.org/10.1016/j. nlm.2008.11.003
96. Bisaz R, Boadas-Vaello P, Genoux D, Sandi C. Agerelated cognitive impairments in mice with a conditional ablation of the neural cell adhesion molecule. Learn Mem 2013; 20:183-93; PMID:23504516; http://dx.doi.org/10.1101/lm.030064.112
97. Fushima K, Tsujimura H. Precise control of fasciclin II expression is required for adult mushroom body development in Drosophila. Dev Growth Differ 2007; 49:215-27; PMID:17394600; http://dx.doi. org/10.1111/j.1440-169X.2007.00922.x
98. Kurusu M, Awasaki T, Masuda-Nakagawa LM, Kawauchi H, Ito K, Furukubo-Tokunaga K. Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development 2002; 129:409-19; PMID:11807033
99. Whitlock KE. Development of Drosophila wing sensory neurons in mutants with missing or modified cell surface molecules. Development 1993; 117:1251-60; PMID:8404529
100. Prabhakar S, Noonan JP, Paabo S, Rubin EM. Accelerated evolution of conserved noncoding sequences in humans. Science 2006; 314:786; PMID:17082449; http://dx.doi.org/10.1126/science. 1130738
101. Somel M, Liu X, Tang L, Yan Z, Hu H, Guo S, et al. MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates. PLoS Biol 2011; 9:e1001214; PMID:22162950; http://dx.doi.org/10.1371/journal.pbio.1001214
102. Chen S, Spletter M, Ni X, White KP, Luo L, Long M. Frequent recent origination of brain genes shaped the evolution of foraging behavior in Drosophila. Cell Rep 2012; 1:118-32; PMID:22832161; http://dx.doi. org/10.1016/j.celrep.2011.12.010
103. Albertson R, Chabu C, Sheehan A, Doe CQ. Scribble protein domain mapping reveals a multistep localization mechanism and domains necessary for establishing cortical polarity. J Cell Sci 2004; 117:6061-70; PMID:15536119; http://dx.doi.org/10.1242/ jcs.01525
104. Brown S, Hu N, Hombria JC. Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Curr Biol 2001; 11:1700-5; PMID:11696329; http://dx.doi.org/10.1016/ S0960-9822(01)00524-3
105. Bach EA, Ekas LA, Ayala-Camargo A, Flaherty MS, Lee H, Perrimon N, et al. GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr Patterns 2007; 7:323-31; PMID:17008134; http://dx.doi.org/10.1016/j. modgep.2006.08.003
106. Shcherbata HR, Yatsenko AS, Patterson L, Sood VD, Nudel U, Yaffe D, et al. Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J 2007; 26:481-93; PMID:17215867; http://dx.doi.org/10.1038/sj.emboj.7601503