Open Access
Publication ahead of print
Journal
Apidologie
DOI http://dx.doi.org/10.1051/apido/2010032
Published online 22 July 2010
  • Adams H.A., Southey B.R., Robinson G.E., Rodriguez-Zas S.L. (2008) Meta-analysis ofgenome-wide expression patterns associated with behavioral maturation in honey bees, BMC Genomics 9, 503. [CrossRef] [PubMed]
  • Alaux C., Le Conte Y., Adams H.A., Rodriguez-Zas S., Grozinger C.M., Sinha S., Robinson G.E. (2009) Regulation of brain gene expression in honey bees by brood pheromone, Genes Brain Behav. 8, 309–319. [CrossRef] [PubMed]
  • Ament S.A., Corona M., Pollock H.S., Robinson G.E. (2008) Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies, Proc. Natl. Acad. Sci. USA 105, 4226–4231. [CrossRef]
  • Aoyagi N., Wassarman D.A. (2000) Genes encoding Drosophila melanogaster RNA polymerase II general transcription factors: diversity in TFIIA and TFIID components contributes to gene-specific transcriptional regulation, J. Cell Biol. 150, F45–F50. [CrossRef] [PubMed]
  • Aravin A.A., Lagos-Quintana M., Yalcin A., Zavolan M., Marks D., Snyder B., Gaasterland T., Meyer J., Tuschl T. (2003) The small RNA profile during Drosophila melanogaster development, Dev. Cell 5, 337–350. [CrossRef] [PubMed]
  • Axelrod J.D., Matsuno K., Artavanis-Tsakonas S., Perrimon N. (1996) Interaction between Wingless and Notch signaling pathways mediated by disheveled, Science 271, 1826–1832. [CrossRef] [PubMed]
  • Babak T., Zhang W., Morris Q., Blencowe B.J., Hughes T.R. (2004) Probing microRNAs with microarrays: tissue specificity and functional inference, RNA 10, 1813–1819. [CrossRef] [PubMed]
  • Baggerman G., Cerstiaens A., De Loof A., Schoofs L. (2002) Peptidomics of the larval Drosophila melanogaster central nervous system, J. Biol. Chem. 277, 40368–40374. [CrossRef] [PubMed]
  • Barik S. (2008) An intronic microRNA silences genes that are functionally antagonistic to its host gene, Nucleic Acids Res. 36, 5232–5241. [CrossRef] [PubMed]
  • Barron A.B., Robinson G.E. (2005) Selective modulation of task performance by octopamine in honey bee (Apis mellifera) division of labour, J. Comp. Physiol. A 191, 659–668. [CrossRef]
  • Bartel D.P. (2004) microRNAs: genomics, biogenesis, mechanism, and function, Cell 116, 281–297. [CrossRef] [PubMed]
  • Ben-Shahar Y. (2005) The foraging gene, behavioral plasticity, and honeybee division of labor, J. Comp. Physiol. A 191, 987–994. [CrossRef]
  • Boutla A., Delidakis C., Tabler M. (2003) Developmental defects by antisense-mediated inactivation of microRNAs 2 and 13 in Drosophila and the identification of putative target genes, Nucleic Acids Res. 31, 4973–4980. [CrossRef] [PubMed]
  • Brennecke J., Stark A., Russell R.B., Cohen S.M. (2005) Principles of microRNA-target recognition, PLoS Biol. 3, e85. [CrossRef] [PubMed]
  • Brockmann A., Annangudi S.P., Richmond T.A., Ament S.A., Xie F., Southey B.R., Rodriguez-Zas S.R., Robinson G.E., Sweedler J.V. (2009) Quantitative peptidomics reveal brain peptide signatures of behavior, Proc. Natl. Acad. Sci. USA 106, 2383–2388. [CrossRef]
  • Chu-LaGraff Q., Doe C.Q. (1993) Neuroblast specification and formation regulated by wingless in the Drosophila CNS, Science 261, 1594–1597. [CrossRef] [PubMed]
  • Daniels R.W., Collins C.A., Chen K., Gelfand M.V., Featherstone D.E., DiAntonio A. (2006) A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle, Neuron 49, 11–16. [CrossRef] [PubMed]
  • Daniels R.W., Collins C.A., Gelfand M.V., Dant J., Brooks E.S., Krantz D.E., DiAntonio A. (2004) Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content, J. Neurosci. 24, 10466–10474. [CrossRef] [PubMed]
  • Denison R., Raymond-Delpech V. (2008) Insights into the molecular basis of social behaviour from studies on the honeybee, Apis mellifera, Invert. Neurosci. 8, 1–9. [CrossRef] [PubMed]
  • Didiano D., Hobert O. (2006) Perfect seed pairing is not a generally reliable predictor for microRNA-target interactions, Nat. Struct. Mol. Biol. 13, 849–851. [CrossRef] [PubMed]
  • Fahrbach S.E., Giray T., Robinson G.E. (1995) Volume changes in the mushroom bodies of adult honey bee queens, Neurobiol. Learn. Mem. 63, 181–191. [CrossRef] [PubMed]
  • Farooqui T., Robinson K., Vaessin H., Smith B.H. (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee, J. Neurosci. 23, 5370–5380. [PubMed]
  • Fiore R., Khudayberdiev S., Christensen M., Siegel G., Flavell S.W., Kim T.K., Greenberg M.E., Schratt G. (2009) Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels, EMBO J. 28, 697–710. [CrossRef] [PubMed]
  • Ge X., Hannan F., Xie Z., Feng C., Tully T., Zhou H., Xie Z., Zhong Y. (2004) Notch signaling in Drosophila long-term memory formation, Proc. Natl. Acad. Sci. USA 101, 10172–10176. [CrossRef]
  • Griffiths-Jones S., Saini H.K., van Dongen S., Enright A.J. (2008) miRBase: tools for microRNA genomics, Nucleic Acids Res. 36, D154–158. [CrossRef] [PubMed]
  • Grün D., Wang Y-L., Langenberger D., Gunsalus K.C., Rajewsky N. (2005) microRNA target predictions across seven Drosophila species and comparison to mammalian targets, PLoS Comput. Biol. 1, e13. [CrossRef] [PubMed]
  • Hayden M.A., Akong K., Peifer M. (2007) Novel roles for APC family members and Wingless/Wnt signaling during Drosophila brain development, Dev. Biol. 305, 358–376. [CrossRef] [PubMed]
  • He L., Thomson J.M., Hemann M.T., Hernando-Monge E., Mu D., Goodson S., Powers S., Cordon-Cardo C., Lowe S.W., Hannon G.J., Hammond S.M. (2005) A microRNA polycistron as a potential human oncogene, Nature 435, 828–833. [CrossRef] [PubMed]
  • Hess C.R., McGuirl M.M., Klinman J.P. (2008) Mechanism of the insect enzyme, tyramine beta-monooxygenase, reveals differences from the mammalian enzyme, dopamine beta-monooxygenase, J. Biol. Chem. 283, 3042–3049. [CrossRef] [PubMed]
  • Heylen K., Gobin B., Billen J., Hu T.T., Arckens L., Huybrechts R. (2008) Amfor expression in the honeybee brain: a trigger mechanism for nurse-forager transition, J. Insect Physiol. 54, 1400–1403. [CrossRef] [PubMed]
  • Hildebrandt H., Müller U. (1995) Octopamine mediates rapid stimulation of protein kinase A in the antennal lobe of honeybees, J. Neurobiol. 27, 44–50. [CrossRef] [PubMed]
  • Hutchison E.R., Okun E., Mattson M.P. (2009) The therapeutic potential of microRNAs in nervous system damage, degeneration, and repair, Neuromol. Med. 11, 153–161. [CrossRef]
  • Irving P., Troxler L., Heuer T.S., Belvin M., Kopczynski C., Reichhart J.M., Hoffmann J.A., Hetru C. (2001) A genome-wide analysis of immune responses in Drosophila, Proc. Natl. Acad. Sci. USA 98, 15119–15124. [CrossRef]
  • Ji Q., Hao X., Zhang M., Tang W., Yang M., Li L., Xiang D., Desano J.T., Bommer G.T., Fan D., Fearon E.R., Lawrence T.S., Xu L. (2009) microRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells, PLoS One 4, e6816. [CrossRef] [PubMed]
  • Jung C.G., Kim H.J., Kawaguchi M., Khanna K.K., Hida H., Asai K., Nishino H., Miura Y. (2005) Homeotic factor ATBF1 induces the cell cycle arrest associated with neuronal differentiation, Development 132, 5137–5145. [CrossRef] [PubMed]
  • Karres J., Hilgers V., Carrera I., Treisman J., Cohen S. (2007) The conserved microRNA MiR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila, Cell 131, 136–145. [CrossRef] [PubMed]
  • Kheradpour P., Stark A., Roy S., Kellis M. (2007) Reliable prediction of regulator targets using 12 Drosophila genomes, Genome Res. 17, 1919–1931. [CrossRef] [PubMed]
  • Kiya T., Kunieda T., Kubo T. (2007) Increased neural activity of a mushroom body neuron subtype in the brains of forager honeybees, PLoS One 2, e371. [CrossRef] [PubMed]
  • Kosik K.S. (2006) The neuronal microRNA system, Nat. Rev. Neurosci. 7, 911–920. [CrossRef] [PubMed]
  • Krek A., Grün D., Poy M.N., Wolf R., Rosenberg L., Epstein E.J., MacMenamin P., da Piedade I., Gunsalus K.C., Stoffel M., Rajewsky N. (2005) Combinatorial microRNA target predictions, Nat. Genet. 37, 495–500. [CrossRef] [PubMed]
  • Kubo T. (2003) Molecular analysis of the honeybee sociality, in: Kikuchi T., Azuma N., Higashi S. (Eds.), Genes, Behaviors and Evolution of Social Insects, Hokkaido University Press, pp. 3–20.
  • Lai Z.C., Fortini M.E., Rubin G.M. (1991) The embryonic expression patterns of zfh-1 and zfh-2, two Drosophila genes encoding novel zinc-finger homeodomain proteins. Mech. Dev. 34, 123–134. [CrossRef] [PubMed]
  • Lehman H.K., Schulz D.J., Barron A.B., Wraight L., Hardison C., Whitney S., Takeuchi H., Paul R.K., Robinson G.E. (2006) Division of labor in the honey bee (Apis mellifera): the role of tyramine beta-hydroxylase, J. Exp. Biol. 209, 2774–2784. [CrossRef] [PubMed]
  • Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., Bartel D.P., Linsley P.S., Johnson J.M. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs, Nature 433, 769–773. [CrossRef] [PubMed]
  • Long J.E., Chen H.X. (2009) Identification and characteristics of cattle microRNAs by homology searching and small RNA cloning, Biochem. Genet. 47, 329–343. [CrossRef] [PubMed]
  • Lu C., Jeong D.H., Kulkarni K., Pillay M., Nobuta K., German R., Thatcher S.R., Maher C., Zhang L., Ware D., Liu B., Cao X., Meyers B.C., Green P.J. (2008) Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs), Proc. Natl. Acad. Sci. USA 105, 4951–4956. [CrossRef]
  • Lundell M.J., 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] [PubMed]
  • Mishima T., Takizaw T., Luo S.S., Ishibashi O., Kawahigashi Y., Mizuguchi Y., Ishikawa T., Mori M., Kanda T., Goto T., Takizawa T. (2008) MicroRNA (microRNA) cloning analysis reveals sex differences in microRNA expression profiles between adult mouse testis and ovary, Reproduction 136, 811–822. [CrossRef] [PubMed]
  • Mobbs P.G. (1982) The brain of the honeybee Apis mellifera. 1. The connections and spatial organization of the mushroom bodies, Philos. Trans. R. Soc. Lond. B 298, 309–354. [CrossRef]
  • Obernosterer G., Leuschner P.J., Alenius M., Martinez J. (2006) Post-transcriptional regulation of microRNA expression, RNA 12, 1161–1167. [CrossRef] [PubMed]
  • Oishi K., Kamakura S., Isazawa Y., Yoshimatsu T., Kuida K., Nakafuku M., Masuyama N., Gotoh Y. (2004) Notch promotes survival of neural precursor cells via mechanisms distinct from those regulating neurogenesis, Dev. Biol. 276, 172–184. [CrossRef] [PubMed]
  • Okabe M., Imai T., Kurusu M., Hiromi Y., Okano H. (2001) Translational repression determines a neuronal potential in Drosophila asymmetric cell division, Nature 411, 94–98. [CrossRef] [PubMed]
  • Orian A., Delrow J.J., Nieves A.E.R., Abed M., Metzger D., Paroush Z., Eisenman R.N., Parkhurst S.M. (2007) A Myc-Groucho complex integrates EGF and Notch signaling to regulate neural development, Proc. Natl. Acad. Sci. USA 104, 15771–15776. [CrossRef]
  • Ørom U.A., Kauppinen S., Lund A.H. (2006) LNA-modified oligonucleotides mediate specific inhibition of microRNA function, Gene 372, 137–141. [CrossRef] [PubMed]
  • Paul R.K., Takeuchi H., Kubo T. (2006) Expression of two ecdysteroid-regulated genes, Broad-Complex and E75, in the brain and ovary of the honeybee (Apis mellifera L.), Zool. Sci. 23, 1085–1092. [CrossRef] [PubMed]
  • Peyrefitte S., Kahn D., Haenlin M. (2001) New members of the Drosophila Myc transcription factor subfamily revealed by a genome-wide examination for basic helix-loop-helix genes, Mech. Dev. 104, 99–104. [CrossRef] [PubMed]
  • Preiss A., Hartley D.A., Artavanis-Tsakonas S. (1988) The molecular genetics of Enhancer of split, a gene required for embryonic neural development in Drosophila, EMBO J. 7, 3917–3927. [PubMed]
  • Reddy A.M., Zheng Y., Jagadeeswaran G., Macmil S.L., Graham W.B., Roe B.A., Desilva U., Zhang W., Sunkar R. (2009) Cloning, characterization and expression analysis of porcine microRNAs, BMC Genomics 10, 65. [CrossRef] [PubMed]
  • Richter S., Hartmann B., Reichert H. (1998) The wingless gene is required for embryonic brain development in Drosophila, Dev. Genes Evol. 208, 37–45. [CrossRef] [PubMed]
  • Robinson G.E. (2002) Genomics and integrative analyses of division of labor in honeybee colonies, Am. Nat. 6, S160–172. [CrossRef]
  • Robinson G.E., Fahrbach S.E., Winston M.L. (1997) Insect societies and the molecular biology of social behavior, Bioessays 19, 1099–1108. [CrossRef] [PubMed]
  • Ruby J.G., Stark A., Johnston W.K., Kellis M., Bartel D.P., Lai E.C. (2007) Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs, Genome Res. 17, 1850–1864. [CrossRef] [PubMed]
  • Schratt G.M., Tuebing F., Nigh E.A., Kane C.G., Sabatini M.E., Kiebler M., Greenberg M.E. (2006) A brain-specific microRNA regulates dendritic spine development, Nature 439, 283–289. [CrossRef] [PubMed]
  • Smirnova L., Gräfe A., Seiler A., Schumacher S., Nitsch R., Wulczyn F.G. (2005) Regulation of microRNA expression during neural cell specification, Eur. J. Neurosci. 21, 1469–1477. [CrossRef] [PubMed]
  • Song Q., Sun K., Shuai Y., Lin R., You W., Wang L., Zhong Y. (2009) Suppressor of Hairless is required for long-term memory formation in Drosophila, J. Neurogenet. 23, 405–411. [CrossRef] [PubMed]
  • Stark A., Kheradpour P., Parts L., Brennecke J., Hodges E., Hannon G.J., Kellis M. (2007) Systematic discovery and characterization of fly microRNAs using 12 Drosophila genomes, Genome Res. 17, 1865–1879. [CrossRef] [PubMed]
  • Stefani G., Slack F.J. (2008) Small non-coding RNAs in animal development, Nat. Rev. Mol. Cell Biol. 9, 219–230. [CrossRef] [PubMed]
  • Vester B., Wengel J. (2004) LNA (locked nucleic acid): high-affinity targeting of complementary RNA and DNA, Biochemistry 43, 13233–13241. [CrossRef] [PubMed]
  • Wayman G.A., Davare M., Ando H., Fortin D., Varlamova O., Cheng H.Y., Marks D., Obrietan K., Soderling T.R., Goodman R.H., Impey S. (2008) An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP, Proc. Natl. Acad. Sci. USA 105, 9093–9098. [CrossRef]
  • Weaver D.B., Anzola J.M., Evans J.D., Reid J.G., Reese J.T., Childs K.L., Zdobnov E.M., Samanta M.P., Miller J., Elsik C.G. (2007) Computational and transcriptional evidence for microRNAs in the honey bee genome, Genome Biol. 8, R97. [CrossRef] [PubMed]
  • Whitfield C.W., Cziko A.M., Robinson G.E. (2003) Gene expression profiles in the brain predict behavior in individual honey bees, Science 302, 296–299. [CrossRef] [PubMed]
  • Winston M.L. (1987) The Biology of the Honey bee, Harvard University Press, Cambridge, MA.
  • Yamazaki Y., Shiraia K., Paul R.K., Fujiyuki T., Wakamoto A., Takeuchi H., Kubo T. (2006) Differential expression of HR38 in the mushroom bodies of the honeybee brain depends on the caste and division of labor, FEBS Lett. 580, 2667–2670. [CrossRef] [PubMed]