MicroRNA-276a functions in ellipsoid body and mushroom body neurons for naive and conditioned olfactory avoidance in Drosophila

Journal of Neuroscience

Volumn 33, Issue 13, 2013, Pages 5821-5833

  Li, Wanhe ^a,b   Cressy, Michael ^a,b   Qin, Hongtao ^a,d   Fulga, Tudor ^c,e   van Vactor, David ^c   Dubnau, Josh ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HUNAN UNIVERSITY   (China)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE RECEPTOR; ENHANCED GREEN FLUORESCENT PROTEIN; MICRORNA; MICRORNA 276A; NEUROFIBROMIN; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN DEVELOPMENT; CONTROLLED STUDY; DIPTERA; DOPAMINERGIC NERVE CELL; DROSOPHILA; ELECTRIC SHOCK; ELLIPSOID BODY; EMBRYO; FEMALE; GENE CONTROL; IMMUNOHISTOCHEMISTRY; MALE; MUSHROOM BODY; NONHUMAN; ODOR; OLFACTORY DISCRIMINATION; OLFACTORY MEMORY; PERIKARYON; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AVOIDANCE LEARNING; DROSOPHILA; DROSOPHILA PROTEINS; ELECTROSHOCK; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HOT TEMPERATURE; MALE; MICRORNAS; MUSHROOM BODIES; MUTATION; NEURONS; ODORS; OLFACTORY PATHWAYS; RECEPTORS, DOPAMINE; TRANSCRIPTION FACTORS;

EID: 84875446774     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4004-12.2013     Document Type: Article

References (79)

1. Andretic R, Kim YC, Jones FS, Han KA, Greenspan RJ (2008) Drosophila D1 dopamine receptor mediates caffeine-induced arousal. Proc Natl Acad Sci USA105:20392-20397. CrossRef Medline
2. Aso Y, Siwanowicz I, Bräcker L, Ito K, Kitamoto T, Tanimoto H (2010) Specific dopaminergic neurons for the formation of labile aversive memory. Curr Biol 20:1445-1451. CrossRef Medline
3. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215-233. CrossRef Medline
4. Berdnik D, Fan AP, Potter CJ, Luo L (2008) MicroRNA processing pathway regulates olfactory neuron morphogenesis. Curr Biol 18:1754-1759. CrossRef Medline
5. Betel D, Koppal A, Agius P, Sander C, Leslie C (2010) Comprehensive modeling of microRNA targets predicts functional non-conserved and noncanonical sites. Genome Biol 11:R90. CrossRef Medline
6. Blum AL, Li W, Cressy M, Dubnau J (2009) Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Curr Biol 19:1341-1350. CrossRef Medline
7. Busto GU, Cervantes-Sandoval I, Davis RL (2010) Olfactory learning in Drosophila. Physiology (Bethesda) 25:338-346. CrossRef Medline
8. Cayirlioglu P, Kadow IG, Zhan X, Okamura K, Suh GS, Gunning D, Lai EC, Zipursky SL (2008) Hybrid neurons in a microRNA mutant are putative evolutionary intermediates in insect CO2 sensory systems. Science 319: 1256-1260. CrossRef Medline
9. Chandrasekar V, Dreyer JL (2009) microRNAs miR-124, let-7d and miR- 181a regulate cocaine-induced plasticity. Mol Cell Neurosci 42:350-362. CrossRef Medline
10. Chen CC, Wu JK, Lin HW, Pai TP, Fu TF, Wu CL, Tully T, Chiang AS (2012) Visualizing long-term memory formation in two neurons of the Drosophila brain. Science 335:678-685. CrossRef Medline
11. Cheng HY, Papp JW, Varlamova O, Dziema H, Russell B, Curfman JP, Nakazawa T, Shimizu K, Okamura H, Impey S, Obrietan K (2007) microRNA modulation of circadian-clock period and entrainment. Neuron 54:813-829. CrossRef Medline
12. Chiang AS, Lin CY, Chuang CC, Chang HM, Hsieh CH, Yeh CW, Shih CT, Wu JJ, Wang GT, Chen YC, Wu CC, Chen GY, Ching YT, Lee PC, Lin CY, Lin HH, Wu CC, Hsu HW, Huang YA, Chen JY, et al. (2011) Threedimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr Biol 21:1-11. CrossRef Medline
13. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H, Hirsh J, Miesenböck G (2009) Writing memories with light-addressable reinforcement circuitry. Cell 139:405-415. CrossRef Medline
14. Cuellar TL, Davis TH, Nelson PT, Loeb GB, Harfe BD, Ullian E, McManus MT (2008) Dicer loss in striatal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proc Natl Acad Sci U S A 105:5614-5619. CrossRef Medline
15. Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, Dus M, Perrimon N, Kellis M, Wohlschlegel JA, Sachidanandam R, Hannon GJ, Brennecke J (2008) An endogenous small interfering RNA pathway in Drosophila. Nature 453:798-802. CrossRef Medline
16. Davis TH, Cuellar TL, Koch SM, Barker AJ, Harfe BD, McManus MT, Ullian EM (2008) Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J Neurosci 28:4322-4330. CrossRef Medline
17. Dubnau J, Chiang AS, Grady L, Barditch J, Gossweiler S, McNeil J, Smith P, Buldoc F, Scott R, Certa U, Broger C, Tully T (2003) The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr Biol 13:286-296. CrossRef Medline
18. Ebert MS, Sharp PA (2010) MicroRNA sponges: progress and possibilities. Rna 16:2043-2050. CrossRef Medline
19. Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721-726. CrossRef Medline
20. Edbauer D, Neilson JR, Foster KA, Wang CF, Seeburg DP, Batterton MN, Tada T, Dolan BM, Sharp PA, Sheng M (2010) Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65:373-384. CrossRef Medline
21. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2003) MicroRNA targets in Drosophila. Genome Biol 5:R1. CrossRef Medline
22. Flynt AS, Lai EC (2008) Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat Rev Genet 9:831-842. CrossRef Medline
23. Gaidatzis D, van Nimwegen E, Hausser J, Zavolan M (2007) Inference of miRNA targets using evolutionary conservation and pathway analysis. BMC Bioinformatics 8:69. CrossRef Medline
24. Gao J, Wang WY, Mao YW, Gräff J, Guan JS, Pan L, Mak G, Kim D, Su SC, Tsai LH (2010) A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466:1105-1109. CrossRef Medline
25. Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM, Baskerville S, Hammond SM, Bartel DP, Schier AF (2005) MicroRNAs regulate brain morphogenesis in zebrafish. Science 308:833-838. CrossRef Medline
26. Grun D, Wang YL, Langenberger D, Gunsalus KC, Rajewsky N (2005) microRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput Biol 1:e13. CrossRef Medline
27. Hansen KF, Sakamoto K, Wayman GA, Impey S, Obrietan K (2010) Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS One 5:e15497. CrossRef Medline
28. He M, Liu Y, Wang X, Zhang MQ, Hannon GJ, Huang ZJ (2012) Cell-typebased analysis of microRNA profiles in the mouse brain. Neuron 73:35-48. CrossRef Medline
29. Herranz H, Cohen SM (2010) MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev 24:1339-1344. CrossRef Medline
30. Kadener S, Menet JS, Sugino K, Horwich MD, Weissbein U, Nawathean P, Vagin VV, Zamore PD, Nelson SB, Rosbash M (2009) A role for microRNAs in the Drosophila circadian clock. Genes Dev 23:2179-2191. CrossRef Medline
31. Kaern M, Elston TC, Blake WJ, Collins JJ (2005) Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6:451-464. CrossRef Medline
32. Karres JS, Hilgers V, Carrera I, Treisman J, Cohen SM (2007) The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell 131:136-145. CrossRef Medline
33. Keene AC, Waddell S (2007) Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 8:341-354. CrossRef Medline
34. Kim J, Krichevsky A, Grad Y, Hayes GD, Kosik KS, Church GM, Ruvkun G (2004) Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc Natl Acad Sci U S A 101:360-365. CrossRef Medline
35. Kim YC, Lee HG, Han KA (2007a) D1 dopamine receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila. J Neurosci 27:7640-7647. CrossRef Medline
36. Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, Murchison E, Hannon G, Abeliovich A (2007b) A microRNA feedback circuit in midbrain dopamine neurons. Science 317:1220-1224. CrossRef Medline
37. Kong EC, Woo K, Li H, Lebestky T, Mayer N, Sniffen MR, Heberlein U, Bainton RJ, Hirsh J, Wolf FW (2010) A pair of dopamine neurons target the D1-like dopamine receptor DopR in the central complex to promote ethanol-stimulated locomotion in Drosophila. PLoS One 5:e9954. CrossRef Medline
38. Konopka W, Kiryk A, Novak M, Herwerth M, Parkitna JR, Wawrzyniak M, Kowarsch A, Michaluk P, Dzwonek J, Arnsperger T, Wilczynski G, Merkenschlager M, Theis FJ, Köhr G, Kaczmarek L, Schutz G (2010) MicroRNA loss enhances learning and memory in mice. J Neurosci 30: 14835-14842. CrossRef Medline
39. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S (2009) A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:416-427. CrossRef Medline
40. Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS (2003) A microRNA array reveals extensive regulation of microRNAs during brain development. Rna 9:1274-1281. CrossRef Medline
41. Kye MJ, Liu T, Levy SF, Xu NL, Groves BB, Bonneau R, Lao K, Kosik KS (2007) Somatodendritic microRNAs identified by laser capture and multiplex RT-PCR. Rna 13:1224-1234. CrossRef Medline
42. Kye MJ, Neveu P, Lee YS, Zhou M, Steen JA, Sahin M, Kosik KS, Silva AJ (2011) NMDA mediated contextual conditioning changes miRNA expression. PLoS One 6:e24682. CrossRef Medline
43. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12:735-739. CrossRef Medline
44. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci ND, Hermida L, Fulci V, Chiaretti S, Foà R, Schliwka J, Fuchs U, Novosel A, Muller RU, et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129:1401-1414. CrossRef Medline
45. Lebestky T, Chang JS, Dankert H, Zelnik L, Kim YC, Han KA, Wolf FW, Perona P, Anderson DJ (2009) Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64:522-536. CrossRef Medline
46. Lin Q, Wei W, Coelho CM, Li X, Baker-Andresen D, Dudley K, Ratnu VS, Boskovic Z, Kobor MS, Sun YE, Bredy TW (2011) The brain-specific microRNA miR-128b regulates the formation of fear-extinction memory. Nat Neurosci 14:1115-1117. CrossRef Medline
47. Liu N, Landreh M, Cao K, Abe M, Hendriks GJ, Kennerdell JR, Zhu Y, Wang LS, Bonini NM (2012) The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature 482:519-523. CrossRef Medline
48. Loya CM, Lu CS, Van Vactor D, Fulga TA (2009) Transgenic microRNA inhibition with spatiotemporal specificity in intact organisms. Nat Methods 6:897-903. CrossRef Medline
49. Lundell MJ, Hirsh J (1992) The zfh-2 gene product is a potential regulator of neuron-specific dopa decarboxylase gene expression in Drosophila. Dev Biol 154:84-94. CrossRef Medline
50. Luo W, Sehgal A (2012) Regulation of circadian behavioral output via a MicroRNA-JAK/STAT circuit. Cell 148:765-779. CrossRef Medline
51. Magill ST, Cambronne XA, Luikart BW, Lioy DT, Leighton BH, Westbrook GL, Mandel G, Goodman RH (2010) MicroRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc Natl Acad Sci U S A 107:20382-20387. CrossRef Medline
52. Margulies C, Tully T, Dubnau J (2005) Deconstructing memory in Drosophila. Curr Biol 15:R700-R713. CrossRef Medline
53. McGuire SE, Mao Z, Davis RL (2004) Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE 2004:p l6. Medline
54. Mellios N, Sugihara H, Castro J, Banerjee A, Le C, Kumar A, Crawford B, Strathmann J, Tropea D, Levine SS, Edbauer D, Sur M (2011) miR-132, an experience-dependent microRNA, is essential for visual cortex plasticity. Nat Neurosci 14:1240-1242. CrossRef Medline
55. Miñones-Moyano E, Porta S, Escaramís G, Rabionet R, Iraola S, Kagerbauer B, Espinosa-Parrilla Y, Ferrer I, Estivill X, and Marti E (2011) MicroRNA profiling of Parkinson's disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function. Hum Mol Genet 20:3067-3078. CrossRef Medline
56. Miska EA, Alvarez-Saavedra E, Townsend M, Yoshii A, Sestan N, Rakic P, Constantine-Paton M, Horvitz HR (2004) Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 5:R68. CrossRef Medline
57. Nakamura M, Baldwin D, Hannaford S, Palka J, Montell C (2002) Defective proboscis extension response (DPR), a member of the Ig superfamily required for the gustatory response to salt. J Neurosci 22:3463-3472. Medline
58. Natera-Naranjo O, Aschrafi A, Gioio AE, Kaplan BB (2010) Identification and quantitative analyses of microRNAs located in the distal axons of sympathetic neurons. Rna 16:1516-1529. CrossRef Medline
59. Nudelman AS, DiRocco DP, Lambert TJ, Garelick MG, Le J, Nathanson NM, Storm DR (2010) Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo. Hippocampus 20:492-498. CrossRef Medline
60. Peláez N, Carthew RW (2012) Biological robustness and the role of microRNAs: a network perspective. Curr Top Dev Biol 99:237-255. CrossRef Medline
61. Qin H, Cressy M, Li W, Coravos JS, Izzi SA, Dubnau J (2012) Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila. Curr Biol 22:608-614. CrossRef Medline
62. Rajasethupathy P, Fiumara F, Sheridan R, Betel D, Puthanveettil SV, Russo JJ, Sander C, Tuschl T, Kandel E (2009) Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63:803-817. CrossRef Medline
63. Rajasethupathy P, Antonov I, Sheridan R, Frey S, Sander C, Tuschl T, Kandel ER (2012) A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell 149:693-707. CrossRef Medline
64. Rollmann SM, Mackay TF, Anholt RR (2005) Pinocchio, a novel protein expressed in the antenna, contributes to olfactory behavior in Drosophila melanogaster. J Neurobiol 63:146-158. CrossRef Medline
65. Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC (2007) Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 17:1850-1864. CrossRef Medline
66. Schaefer A, O'Carroll D, Tan CL, Hillman D, Sugimori M, Llinas R, Greengard P (2007) Cerebellar neurodegeneration in the absence of microRNAs. J Exp Med 204:1553-1558. CrossRef Medline
67. Schmittgen TD (2001) Real-time quantitative PCR. Methods 25:383-385. CrossRef Medline
68. Schratt G, Greenberg M (2007) MicroRNA function in the nervous system. In: MicroRNAs (Appasani K, ed), pp. 115-128. Cambridge: Cambridge UP.
69. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23: 10495-10502. Medline
70. Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V (2004) Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol 5:R13. CrossRef Medline
71. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 157:263-277. CrossRef
72. Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79:35-47. CrossRef Medline
73. Van Swinderen B, Andretic R (2011) Dopamine in Drosophila: setting arousal thresholds in a miniature brain. Proc Biol Sci 278:906-913. CrossRef Medline
74. Venken KJ, He Y, Hoskins RA, Bellen HJ (2006) P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314:1747-1751. CrossRef Medline
75. Venken KJ, Carlson JW, Schulze KL, Pan H, He Y, Spokony R, Wan KH, Koriabine M, de Jong PJ, White KP, Bellen HJ, Hoskins RA (2009) Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat Methods 6:431-434. CrossRef Medline
76. Wu CL, Xia S, Fu TF, Wang H, Chen YH, Leong D, Chiang AS, Tully T (2007) Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10:1578-1586. CrossRef Medline
77. Xia S, Miyashita T, Fu TF, Lin WY, Wu CL, Pyzocha L, Lin IR, Saitoe M, Tully T, Chiang AS (2005) NMDA receptors mediate olfactory learning and memory in Drosophila. Curr Biol 15:603-615. CrossRef Medline
78. Yang Y, Shu X, Liu D, Shang Y, Wu Y, Pei L, Xu X, Tian Q, Zhang J, Qian K, Wang YX, Petralia RS, Tu W, Zhu LQ, Wang JZ, Lu Y (2012) EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation. Neuron 73:774-788. CrossRef Medline
79. Yoon WH, Meinhardt H, Montell DJ (2011) miRNA-mediated feedback inhibition of JAK/STAT morphogen signalling establishes a cell fate threshold. Nat Cell Biol 13:1062-1069. CrossRef Medline