Dynamically expressed single ELAV/Hu orthologue elavl2 of bees is required for learning and memory.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
28 10 2021
28 10 2021
Historique:
received:
09
02
2021
accepted:
09
10
2021
entrez:
29
10
2021
pubmed:
30
10
2021
medline:
21
12
2021
Statut:
epublish
Résumé
Changes in gene expression are a hallmark of learning and memory consolidation. Little is known about how alternative mRNA processing, particularly abundant in neuron-specific genes, contributes to these processes. Prototype RNA binding proteins of the neuronally expressed ELAV/Hu family are candidates for roles in learning and memory, but their capacity to cross-regulate and take over each other's functions complicate substantiation of such links. Honey bees Apis mellifera have only one elav/Hu family gene elavl2, that has functionally diversified by increasing alternative splicing including an evolutionary conserved microexon. RNAi knockdown demonstrates that ELAVL2 is required for learning and memory in bees. ELAVL2 is dynamically expressed with altered alternative splicing and subcellular localization in mushroom bodies, but not in other brain regions. Expression and alternative splicing of elavl2 change during memory consolidation illustrating an alternative mRNA processing program as part of a local gene expression response underlying memory consolidation.
Identifiants
pubmed: 34711922
doi: 10.1038/s42003-021-02763-1
pii: 10.1038/s42003-021-02763-1
pmc: PMC8553928
doi:
Substances chimiques
Insect Proteins
0
RNA-Binding Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1234Subventions
Organisme : Biotechnology and Biological Sciences Research Council
Pays : United Kingdom
Informations de copyright
© 2021. The Author(s).
Références
Alberini, C. M. Transcription factors in long-term memory and synaptic plasticity. Physiol. Rev. 89, 121–145 (2009).
pubmed: 19126756
doi: 10.1152/physrev.00017.2008
Alberini, C. M., Ghirardi, M., Metz, R. & Kandel, E. R. C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76, 1099–1114 (1994).
pubmed: 8137425
doi: 10.1016/0092-8674(94)90386-7
Clayton, D. F. The genomic action potential. Neurobiol. Learn Mem. 74, 185–216 (2000).
pubmed: 11031127
doi: 10.1006/nlme.2000.3967
Kandel, E. R., Dudai, Y. & Mayford, M. R. The molecular and systems biology of memory. Cell 157, 163–186 (2014).
pubmed: 24679534
doi: 10.1016/j.cell.2014.03.001
Soller, M. Pre-messenger RNA processing and its regulation: a genomic perspective. Cell Mol. Life Sci. 63, 796–819 (2006).
pubmed: 16465448
doi: 10.1007/s00018-005-5391-x
Vuong, C. K., Black, D. L. & Zheng, S. The neurogenetics of alternative splicing. Nat. Rev. Neurosci. 17, 265–281 (2016).
pubmed: 27094079
pmcid: 4861142
doi: 10.1038/nrn.2016.27
Ule, J. & Blencowe, B. J. Alternative Splicing Regulatory Networks: Functions, Mechanisms, and Evolution. Mol. Cell 76, 329–345 (2019).
pubmed: 31626751
doi: 10.1016/j.molcel.2019.09.017
Demares, F. et al. Differential involvement of glutamate-gated chloride channel splice variants in the olfactory memory processes of the honeybee Apis mellifera. Pharm. Biochem Behav. 124, 137–144 (2014).
doi: 10.1016/j.pbb.2014.05.025
Demares, F., Raymond, V. & Armengaud, C. Expression and localization of glutamate-gated chloride channel variants in honeybee brain (Apis mellifera). Insect Biochem Mol. Biol. 43, 115–124 (2013).
pubmed: 23085357
doi: 10.1016/j.ibmb.2012.10.003
Beffert, U. et al. Modulation of synaptic plasticity and memory by Reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47, 567–579 (2005).
pubmed: 16102539
doi: 10.1016/j.neuron.2005.07.007
Poplawski, S. G. et al. Contextual fear conditioning induces differential alternative splicing. Neurobiol. Learn Mem. 134 Pt B, 221–235 (2016).
pubmed: 27451143
doi: 10.1016/j.nlm.2016.07.018
Sengar, A. S. et al. Control of Long-Term Synaptic Potentiation and Learning by Alternative Splicing of the NMDA Receptor Subunit GluN1. Cell Rep. 29, 4285–4294 e4285 (2019).
pubmed: 31875540
doi: 10.1016/j.celrep.2019.11.087
Mirisis, A. A. & Carew, T. J. The ELAV family of RNA-binding proteins in synaptic plasticity and long-term memory. Neurobiol. Learn Mem. 161, 143–148 (2019).
pubmed: 30998973
pmcid: 6529270
doi: 10.1016/j.nlm.2019.04.007
Perrone-Bizzozero, N. & Bolognani, F. Role of HuD and other RNA-binding proteins in neural development and plasticity. J. Neurosci. Res 68, 121–126 (2002).
pubmed: 11948657
doi: 10.1002/jnr.10175
Soller, M. & White, K. Elav. Curr. Biol. 14, R53 (2004).
pubmed: 14738746
doi: 10.1016/j.cub.2003.12.041
Haussmann, I. U., White, K. & Soller, M. Erect wing regulates synaptic growth in Drosophila by integration of multiple signaling pathways. Genome Biol. 9, R73 (2008).
pubmed: 18419806
pmcid: 2643944
doi: 10.1186/gb-2008-9-4-r73
Ince-Dunn, G. et al. Neuronal Elav-like (Hu) proteins regulate RNA splicing and abundance to control glutamate levels and neuronal excitability. Neuron 75, 1067–1080 (2012).
pubmed: 22998874
pmcid: 3517991
doi: 10.1016/j.neuron.2012.07.009
Samson, M. L. Rapid functional diversification in the structurally conserved ELAV family of neuronal RNA binding proteins. BMC Genomics 9, 392 (2008).
pubmed: 18715504
pmcid: 2529313
doi: 10.1186/1471-2164-9-392
Watanabe, T. & Aonuma, H. Tissue-specific promoter usage and diverse splicing variants of found in neurons, an ancestral Hu/ELAV-like RNA-binding protein gene of insects, in the direct-developing insect Gryllus bimaculatus. Insect Mol. Biol. 23, 26–41 (2014).
pubmed: 24382152
doi: 10.1111/imb.12057
Okano, H. J. & Darnell, R. B. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J. Neurosci. 17, 3024–3037 (1997).
pubmed: 9096138
pmcid: 6573636
doi: 10.1523/JNEUROSCI.17-09-03024.1997
Kim, Y. J. & Baker, B. S. The Drosophila gene rbp9 encodes a protein that is a member of a conserved group of putative RNA binding proteins that are nervous system-specific in both flies and humans. J. Neurosci. 13, 1045–1056 (1993).
pubmed: 7680064
pmcid: 6576623
doi: 10.1523/JNEUROSCI.13-03-01045.1993
Samson, M. L. & Chalvet, F. found in neurons, a third member of the Drosophila elav gene family, encodes a neuronal protein and interacts with elav. Mech. Dev. 120, 373–383 (2003).
pubmed: 12591606
doi: 10.1016/S0925-4773(02)00444-6
Yao, K.-M., Samson, M.-L., Reeves, R. & White, K. Gene elav of Drosophila melanogaster: a prototype for neuronal-specific RNA binding protein gene family that is conserved in flies and humans. J. Neurobiol. 24, 723–739 (1993).
pubmed: 8331337
doi: 10.1002/neu.480240604
Zaharieva, E., Haussmann, I. U., Brauer, U. & Soller, M. Concentration and localization of co-expressed ELAV/Hu proteins control specificity of mRNA processing. Mol. Cell Biol. 35, 3104–3115 (2015).
pubmed: 26124284
pmcid: 4539368
doi: 10.1128/MCB.00473-15
Mukherjee, N. et al. Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol. Cell 43, 327–339 (2012).
doi: 10.1016/j.molcel.2011.06.007
Uren, P. J. et al. Genomic analyses of the RNA-binding protein Hu antigen R (HuR) identify a complex network of target genes and novel characteristics of its binding sites. J. Biol. Chem. 286, 37063–37066 (2012).
doi: 10.1074/jbc.C111.266882
Lebedeva, S. et al. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol. Cell 43, 340–352 (2012).
doi: 10.1016/j.molcel.2011.06.008
Haussmann, I. U., Li, M. & Soller, M. ELAV-mediated 3’-end processing of ewg transcripts is evolutionarily conserved despite sequence degeneration of the ELAV-binding site. Genetics 189, 97–107 (2011).
pubmed: 21705751
pmcid: 3176107
doi: 10.1534/genetics.111.131383
Soller, M. & White, K. ELAV multimerizes on conserved AU4-6 motifs important for ewg splicing regulation. Mol. Cell Biol. 25, 7580–7591 (2005).
pubmed: 16107705
pmcid: 1190278
doi: 10.1128/MCB.25.17.7580-7591.2005
Soller, M. & White, K. ELAV inhibits 3’-end processing to promote neural splicing of ewg pre-mRNA. Genes Dev. 17, 2526–2538 (2003).
pubmed: 14522950
pmcid: 218147
doi: 10.1101/gad.1106703
Toba, G., Qui, J., Koushika, S. P. & White, K. Ectopic expression of Drosophila ELAV and human HuD in Drosophila wing disc cells reveals functional distinctions and similarities. J. Cell Sci. 115, 2413–2421 (2002).
pubmed: 12006625
doi: 10.1242/jcs.115.11.2413
Lisbin, M. J., Qiu, J. & White, K. The neuron-specific RNA-binding protein ELAV regulates neuroglian alternative splicing in neurons and binds directly to its pre-mRNA. Genes Dev. 15, 2546–2561 (2001).
pubmed: 11581160
pmcid: 312793
doi: 10.1101/gad.903101
Koushika, S. P., Soller, M. & White, K. The neuron-enriched splicing pattern of Drosophila erect wing is dependent on the presence of ELAV protein. Mol. Cell Biol. 20, 1836–1845 (2000).
pubmed: 10669758
pmcid: 85364
doi: 10.1128/MCB.20.5.1836-1845.2000
Koushika, S. P., Lisbin, M. J. & White, K. ELAV, a Drosophila neuron-specific protein, mediates the generation of an alternatively spliced neural protein isoform. Curr. Biol. 6, 1634–1641 (1996).
pubmed: 8994828
doi: 10.1016/S0960-9822(02)70787-2
Simionato, E. et al. The Drosophila RNA-binding protein ELAV is required for commissural axon midline crossing via control of commissureless mRNA expression in neurons. Dev. Biol. 301, 166–177 (2007).
pubmed: 17049509
doi: 10.1016/j.ydbio.2006.09.028
Rogulja-Ortmann, A. et al. The RNA-binding protein ELAV regulates Hox RNA processing, expression and function within the Drosophila nervous system. Development 141, 2046–2056 (2014).
pubmed: 24803653
pmcid: 4132933
doi: 10.1242/dev.101519
Wei, L. et al. Overlapping Activities of ELAV/Hu Family RNA Binding Proteins Specify the Extended Neuronal 3’ UTR Landscape in Drosophila. Mol. Cell 80, 140–155 e146 (2020).
pubmed: 33007254
pmcid: 7546445
doi: 10.1016/j.molcel.2020.09.007
Carrasco, J. et al. ELAV and FNE Determine Neuronal Transcript Signatures through EXon-Activated Rescue. Mol. Cell 80, 156–163 e156 (2020).
pubmed: 33007255
doi: 10.1016/j.molcel.2020.09.011
Brauer, U., Zaharieva, E. & Soller, M. Regulation of ELAV/Hu RNA-binding proteins by phosphorylation. Biochem Soc. Trans. 42, 1147–1151 (2014).
pubmed: 25110017
doi: 10.1042/BST20140103
Lefer, D., Perisse, E., Hourcade, B., Sandoz, J. & Devaud, J. M. Two waves of transcription are required for long-term memory in the honeybee. Learn Mem. 20, 29–33 (2012).
pubmed: 23247252
doi: 10.1101/lm.026906.112
Villar, M. E., Marchal, P., Viola, H. & Giurfa, M. Redefining Single-Trial Memories in the Honeybee. Cell Rep. 30, 2603–2613 e2603 (2020).
pubmed: 32101739
doi: 10.1016/j.celrep.2020.01.086
Robinow, S. & White, K. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22, 443–461 (1991).
pubmed: 1716300
doi: 10.1002/neu.480220503
Haussmann, I. U. et al. CMTr cap-adjacent 2‘-O-ribose methyltransferases are required for reward learning and mRNA localization to synapses. bioRxiv, https://doi.org/10.1101/2021.1106.1124.449724 (2021).
Decio, P. et al. Acute thiamethoxam toxicity in honeybees is not enhanced by common fungicide and herbicide and lacks stress-induced changes in mRNA splicing. Sci. Rep. 9, 19196 (2019).
pubmed: 31844097
pmcid: 6915785
doi: 10.1038/s41598-019-55534-8
Hatton, A. R., Subramaniam, V. & Lopez, A. J. Generation of alternative Ultrabithorax isoforms and stepwise removal of a large intron by resplicing at exon-exon junctions. Mol. Cell 2, 787–796 (1998).
pubmed: 9885566
doi: 10.1016/S1097-2765(00)80293-2
Duff, M. O. et al. Genome-wide identification of zero nucleotide recursive splicing in Drosophila. Nature 521, 376–379 (2015).
pubmed: 25970244
pmcid: 4529404
doi: 10.1038/nature14475
Sibley, C. R. et al. Recursive splicing in long vertebrate genes. Nature 521, 371–375 (2015).
pubmed: 25970246
pmcid: 4471124
doi: 10.1038/nature14466
Borgeson, C. D. & Samson, M. L. Shared RNA-binding sites for interacting members of the Drosophila ELAV family of neuronal proteins. Nucleic Acids Res 33, 6372–6383 (2005).
pubmed: 16282587
pmcid: 1283526
doi: 10.1093/nar/gki942
Inman, M. V., Levy, S., Mock, B. A. & Owens, G. C. Gene organization and chromosome location of the neural-specific RNA binding protein Elavl4. Gene 208, 139–145 (1998).
pubmed: 9524251
doi: 10.1016/S0378-1119(97)00615-X
Yannoni, Y. M. & White, K. Domain necessary for Drosophila ELAV nuclear localization: function requires nuclear ELAV. J. Cell Sci. 112, 4501–4512 (1999).
pubmed: 10574700
doi: 10.1242/jcs.112.24.4501
Copley, R. R. Evolutionary convergence of alternative splicing in ion channels. Trends Genet 20, 171–176 (2004).
pubmed: 15101391
doi: 10.1016/j.tig.2004.02.001
Torres-Mendez, A. et al. A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons. Nat. Ecol. Evol. 3, 691–701 (2019).
pubmed: 30833759
doi: 10.1038/s41559-019-0813-6
Ray, D. et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature 499, 172–177 (2013).
pubmed: 23846655
pmcid: 3929597
doi: 10.1038/nature12311
Akamatsu, W. et al. Mammalian ELAV-like neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and the peripheral nervous systems. Proc. Natl Acad. Sci. USA 96, 9885–9890 (1999).
pubmed: 10449789
pmcid: 22305
doi: 10.1073/pnas.96.17.9885
Akamatsu, W. et al. The RNA-binding protein HuD regulates neuronal cell identity and maturation. Proc. Natl Acad. Sci. USA 102, 4625–4630 (2005).
pubmed: 15764704
pmcid: 555491
doi: 10.1073/pnas.0407523102
Bolognani, F. et al. Coordinated expression of HuD and GAP-43 in hippocampal dentate granule cells during developmental and adult plasticity. Neurochem Res 32, 2142–2151 (2007).
pubmed: 17577668
doi: 10.1007/s11064-007-9388-8
Pascale, A. et al. Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. Proc. Natl Acad. Sci. USA 101, 1217–1222 (2004).
pubmed: 14745023
pmcid: 337033
doi: 10.1073/pnas.0307674100
Quattrone, A. et al. Posttranscriptional regulation of gene expression in learning by the neuronal ELAV-like mRNA-stabilizing proteins. Proc. Natl Acad. Sci. USA 98, 11668–11673 (2001).
pubmed: 11573004
pmcid: 58787
doi: 10.1073/pnas.191388398
Menzel, R., Manz, G., Menzel, R. & Greggers, U. Massed and spaced learning in honeybees: the role of CS, US, the intertrial interval, and the test interval. Learn Mem. 8, 198–208 (2001).
pubmed: 11533223
pmcid: 311375
doi: 10.1101/lm.40001
Hourcade, B., Muenz, T. S., Sandoz, J. C., Rossler, W. & Devaud, J. M. Long-term memory leads to synaptic reorganization in the mushroom bodies: a memory trace in the insect brain? J. Neurosci. 30, 6461–6465 (2010).
pubmed: 20445072
pmcid: 6632731
doi: 10.1523/JNEUROSCI.0841-10.2010
Haussmann, I. U. & Soller, M. Differential activity of EWG transcription factor isoforms identifies a subset of differentially regulated genes important for synaptic growth regulation. Dev. Biol. 348, 224–230 (2010).
pubmed: 20854801
doi: 10.1016/j.ydbio.2010.09.006
Sommerlandt, F. M. J., Brockmann, A., Rossler, W. & Spaethe, J. Immediate early genes in social insects: a tool to identify brain regions involved in complex behaviors and molecular processes underlying neuroplasticity. Cell Mol. Life Sci. 76, 637–651 (2019).
pubmed: 30349993
doi: 10.1007/s00018-018-2948-z
Guzowski, J. F. Insights into immediate-early gene function in hippocampal memory consolidation using antisense oligonucleotide and fluorescent imaging approaches. Hippocampus 12, 86–104 (2002).
pubmed: 11918292
doi: 10.1002/hipo.10010
Minatohara, K., Akiyoshi, M. & Okuno, H. Role of Immediate-Early Genes in Synaptic Plasticity and Neuronal Ensembles Underlying the Memory Trace. Front Mol. Neurosci. 8, 78 (2015).
pubmed: 26778955
Iino, S. et al. Neural activity mapping of bumble bee (Bombus ignitus) brains during foraging flight using immediate early genes. Sci. Rep. 10, 7887 (2020).
pubmed: 32398802
pmcid: 7217898
doi: 10.1038/s41598-020-64701-1
Hirano, Y. et al. Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies. Nat. Commun. 7, 13471 (2016).
pubmed: 27841260
pmcid: 5114576
doi: 10.1038/ncomms13471
Fujita, N. et al. Visualization of neural activity in insect brains using a conserved immediate early gene, Hr38. Curr. Biol. 23, 2063–2070 (2013).
pubmed: 24120640
doi: 10.1016/j.cub.2013.08.051
Tiruchinapalli, D. M., Ehlers, M. D. & Keene, J. D. Activity-dependent expression of RNA binding protein HuD and its association with mRNAs in neurons. RNA Biol. 5, 157–168 (2008).
pubmed: 18769135
doi: 10.4161/rna.5.3.6782
Mirisis, A. A., Kopec, A. M. & Carew, T. J. ELAV proteins bind and stabilize C/EBP mRNA in the induction of long-term memory in Aplysia. J. Neurosci. 41, 947–959 (2020).
Yim, S. J. et al. Regulation of ApC/EBP mRNA by the Aplysia AU-rich element-binding protein, ApELAV, and its effects on 5-hydroxytryptamine-induced long-term facilitation. J. Neurochem. 98, 420–429 (2006).
pubmed: 16805836
doi: 10.1111/j.1471-4159.2006.03887.x
McNeill, M. S., Kapheim, K. M., Brockmann, A., McGill, T. A. & Robinson, G. E. Brain regions and molecular pathways responding to food reward type and value in honey bees. Genes Brain Behav. 15, 305–317 (2016).
pubmed: 26566901
doi: 10.1111/gbb.12275
Sanfilippo, P., Smibert, P., Duan, H. & Lai, E. C. Neural specificity of the RNA-binding protein Elav is achieved by post-transcriptional repression in non-neural tissues. Development 143, 4474–4485 (2016).
pubmed: 27802174
pmcid: 5201049
Cabirol, A., Brooks, R., Groh, C., Barron, A. B. & Devaud, J. M. Experience during early adulthood shapes the learning capacities and the number of synaptic boutons in the mushroom bodies of honey bees (Apis mellifera). Learn Mem. 24, 557–562 (2017).
pubmed: 28916631
pmcid: 5602345
doi: 10.1101/lm.045492.117
Cabirol, A., Cope, A. J., Barron, A. B. & Devaud, J. M. Relationship between brain plasticity, learning and foraging performance in honey bees. PLoS One. 13, e0196749 (2018).
pubmed: 29709023
pmcid: 5927457
doi: 10.1371/journal.pone.0196749
Luo, L., Callaway, E. M. & Svoboda, K. Genetic Dissection of Neural Circuits: A Decade of Progress. Neuron. 98, 256–281 (2018).
pubmed: 29673479
pmcid: 5912347
doi: 10.1016/j.neuron.2018.03.040
Fan, X. C. & Steitz, J. A. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. Embo J. 17, 3448–3460 (1998).
pubmed: 9628880
pmcid: 1170681
doi: 10.1093/emboj/17.12.3448
Zaharieva, E., Chipman, J. K. & Soller, M. Alternative splicing interference by xenobiotics. Toxicology. 296, 1–12 (2012).
pubmed: 22321775
doi: 10.1016/j.tox.2012.01.014
Tasman, K., Hidalgo, S., Zhu, B., Rands, S. A. & Hodge, J. J. L. Neonicotinoids disrupt memory, circadian behaviour and sleep. Sci. Rep. 11, 2061 (2021).
pubmed: 33479461
pmcid: 7820356
doi: 10.1038/s41598-021-81548-2
Decio, P. et al. Thiamethoxam exposure deregulates short ORF gene expression in the honey bee and compromises immune response to bacteria. Sci. Rep. 11, 1489 (2021).
pubmed: 33452318
pmcid: 7811001
doi: 10.1038/s41598-020-80620-7
Wang, H., Molfenter, J., Zhu, H. & Lou, H. Promotion of exon 6 inclusion in HuD pre-mRNA by Hu protein family members. Nucleic Acids Res. 38, 3760–3770 (2010).
pubmed: 20159993
pmcid: 2887941
doi: 10.1093/nar/gkq028
Hayashi, S., Yano, M., Igarashi, M., Okano, H. J. & Okano, H. Alternative role of HuD splicing variants in neuronal differentiation. J. Neurosci. Res 93, 399–409 (2015).
pubmed: 25332105
doi: 10.1002/jnr.23496
Irimia, M. et al. A highly conserved program of neuronal microexons is misregulated in autistic brains. Cell 159, 1511–1523 (2014).
pubmed: 25525873
pmcid: 4390143
doi: 10.1016/j.cell.2014.11.035
Ustaoglu, P. et al. Srrm234, but not canonical SR and hnRNP proteins, drive inclusion of Dscam exon 9 variable exons. RNA 25, 1353–1365 (2019).
pubmed: 31292260
pmcid: 6800468
doi: 10.1261/rna.071316.119
Schutt, C. & Nothiger, R. Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127, 667–677 (2000).
pubmed: 10648226
doi: 10.1242/dev.127.4.667
Gonatopoulos-Pournatzis, T. & Blencowe, B. J. Microexons: at the nexus of nervous system development, behaviour and autism spectrum disorder. Curr. Opin. Genet. Dev. 65, 22–33 (2020).
pubmed: 32535349
doi: 10.1016/j.gde.2020.03.007
Matsumoto, Y., Menzel, R., Sandoz, J. C. & Giurfa, M. Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: a step toward standardized procedures. J. Neurosci. Methods 211, 159–167 (2012).
pubmed: 22960052
doi: 10.1016/j.jneumeth.2012.08.018
Koushika, S. P., Soller, M., DeSimone, S. M., Daub, D. M. & White, K. Differential and inefficient splicing of a broadly expressed Drosophila erect wing transcript results in tissue-specific enrichment of the vital EWG protein isoform. Mol. Cell Biol. 19, 3998–4007 (1999).
pubmed: 10330140
pmcid: 104359
doi: 10.1128/MCB.19.6.3998
Sambrook, R. P. & Russell, D. V. Molecular Cloning-A Laboratory Manual. (Cold Spring Harbor Laboratory Press, 2001).
Saudan, P. et al. Ductus ejaculatorius peptide 99B (DUP99B), a novel Drosophila melanogaster sex-peptide pheromone. Eur. J. Biochem. 269, 989–997 (2002).
pubmed: 11846801
doi: 10.1046/j.0014-2956.2001.02733.x
Waterhouse, A. et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 46, W296–W303 (2018).
pubmed: 29788355
pmcid: 6030848
doi: 10.1093/nar/gky427
Drozdetskiy, A., Cole, C., Procter, J. & Barton, G. J. JPred4: a protein secondary structure prediction server. Nucleic Acids Res. 43, W389–W394 (2015).
pubmed: 25883141
pmcid: 4489285
doi: 10.1093/nar/gkv332
Tu, Q., Cameron, R. A., Worley, K. C., Gibbs, R. A. & Davidson, E. H. Gene structure in the sea urchin Strongylocentrotus purpuratus based on transcriptome analysis. Genome Res. 22, 2079–2087 (2012).
pubmed: 22709795
pmcid: 3460201
doi: 10.1101/gr.139170.112
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Cary, G. A., Cameron, R. A. & Hinman, V. F. EchinoBase: tools for echinoderm genome analyses. Methods Mol. Biol. 1757, 349–369 (2018).
pubmed: 29761464
doi: 10.1007/978-1-4939-7737-6_12
Mota, T. & Giurfa, M. Multiple reversal olfactory learning in honeybees. Front. Behav. Neurosci. 4, 48 (2010).