Expression levels of glutamate and serotonin receptor genes in the brain of different behavioural phenotypes of worker honeybee (Apis mellifera)

Year 2014, Volume: 38 Issue: 4, 431 - 441, 01.08.2014

Qiu-hong Qın Xu Han Hao Lıu Shao-wu Zhang Zhi-jiang Zeng

https://doi.org/10.16970/ted.54867

Cited By: 3

Abstract

Social insect colonies are known for their efficient system of task specialization. In this study, we analyzed the brain expression level of glutamate and serotonin receptor genes in different behavioural phenotypes of (Apis mellifera) workers by qRT-PCR. The glutamate receptor genes include the ionotropic glutamate receptor (iGluR) genes and metabotropic glutamate receptor (mGluRs) genes, and has 9 orthologous genes in honeybee, such as the N-methyl-D-aspartate receptor (NMDAR) genes, NMDAR1 and NMDAR2, the α-amino-3-hydroxy-5-methyl-4isoxazole receptor (AMPAR) genes, AMPAR ∆2-a, AMPAR ∆2-b, AMPAR ∆2-c, AMPAR ∆2-d, and the mGluR1, mGluR4 and mGluR7. Our results showed that: the relative expression level of NMDAR genes was much higher in newly emerged workers (NW) than in young nurses (YN) and “old” foragers (OF) (P < 0.001); both NW and YN had a significantly higher relative expression level of AMPAR ∆2-b, AMPAR ∆2-c and AMPAR ∆2-d than in OF (P < 0.05). than in YN and OF; the relative expression level of mGluR7 gene in OF was significantly higher than in NW (P > 0.05), but there were no significant differences among NW, YN, and OF for the relative expression level of mGluR1 and mGluR4 gene (P > 0.05); in the case of Serotonin (5-HT), the relative expression level of the 5-HT1 gene showed no significant difference between YN and OF (P > 0.05), but was higher in YN and OF than in NW (P < 0.001). Above results indicate that some glutamate and serotonin receptor genes may play important roles in honeybee age-dependent role change

Keywords

Apis mellifera, age, brain, iGluRs, mGluRs, 5-HT

Farklı davranış fenotiplerinde işçi bal arısı (Apis mellifera), beyninde glutamat ve serotonin reseptör genlerinin ekspresyon düzeyleri

Abstract

Sosyal böcekler görev dağılımının en bilinen sistemleridir. Bu çalışmada, qRT-PCR ile bal arası (Apis mellifera) işçilerinin farklı davranış fenotiplerinde beyinde bulunan glutamat ve serotonin reseptör genlerinin ekspresyon seviyeleri analiz edilmiştir. Glutamat reseptör geni; İyonotropik glutamat reseptörü (iGluR) ve metabotropik glutamat reseptörü (mGluR'ler) genlerini kapsar. Balarısında Glutamat reseptör geni, N-metil-D-aspartat reseptör (NMDAR) genleri, NMDAR1 ve NMDAR2, α-amino-3-hidroksi-5-metil-4-izoksazol reseptörü (AMPAR) genleri, AMPAR ∆2-a AMPAR ∆2-b AMPAR ∆2-c AMPAR ∆2-d ve mGluR1, mGluR4 ve mGluR7 olmak üzere 9 ortolog gene sahiptir. Sonuçlarımıza göre: NMDAR geninin ekspresyon düzeyi yeni çıkış yapmış işçilerde (NW), genç (YN) ve yaşlı bireylere (OF) oranla çok daha yüksek bulunmuşken (p<0.001); işçi arıların ve genç bireylerin her ikisinde yaşlı bireylerden belirgin bir şekilde daha yüksek oranda Ampar ∆2-b, Ampar ∆2-c ve Ampar ∆2-d gen ekspresyon düzeyi saptanmıştır (P<0.05). Yaşlı bireylerde mGluR7 geninin ekspresyon düzeyi işçi arılardan belirgin olarak daha yüksek iken (P>0.05); genç, yaşlı ve işçi arıların hepsinde mGluR1 ve mGluR4 genlerinin ekspresyon düzeyleri açısından (p>0.05) anlamlı bir fark bulunamamıştır. Serotonin (5-HT) söz konusu olduğunda, 5-HT1 geninin ekspresyon seviyesi bakımından genç ve yaşlı bireyler arasında anlamlı bir fark çıkmamıştır (P>0.05) ancak aynı genin ifadesi genç ve yaşlı bireylerde işçi arılara göre daha yüksek bulunmuştur (P<0.001). Yukarıdaki sonuçlar, bazı glutamat ve serotonin reseptör genlerinin arılarda yaşa bağlı görev değişikliğinde önemli roller oynayabileceğini göstermiştir

Keywords

Apis mellifera, yaş, beyin, iGluRs, mGluRs, 5-HT

References

• Barbas, D., L. Desgroseillers, V.F. Castellucci, T.J. Carew & S. Marinesco, 2003. Multiple serotonergic mechanisms contributing to sensitization in Aplysia: evidence of diverse serotonin receptor subtypes. Learnning & Memory 10: 373–386.
• Barbas, D., A. Campbell, V.F. Castellucci & L.L. Desgroseillers, 2005. Comparative localization of two serotonin receptors and sensor in the central nervous system of Aplysia californica. Journal of Comparative Neurology 3: 295–304.
• Barnes, N.M. & T. Sharp, 1999. A review of central 5-HT receptors and their function. Neuropharmacology 38: 1083- 1152.
• Bear, M.F., 1999. Homo synaptic long-term depression, a mechanism for memory? Proceedings of the National academy of Sciences of the United States of America 96: 9457–9458.
• Bliss, T.V. & G.L. Collingrodge, 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31–39.
• Bicker, G., 1999. Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microscopy Research and Technique 45: 174-183.
• Callaerts-vegh, Z., T. Beckers, S.M. Ball, F. Baeyens, P.F. Callaerts, J.F. Cryan, E. Molnar & R. D'hooge, 2006. Concomitant deficits in working memory and fear extinction are functionally dissociated from reduced anxiety in metabotropic glutamate receptor 7-deficient mice. Journal of Neuroscience 26: 6573-6582.
• Chen, S.L., 2001. The Apicultural Science in China. China Agriculture Press, Beijing.
• Cline, H.T., G.Y. Wu & R. Malinow, 1996. In vivo development of neuronal structure and function. Cold Spring Harbor Symposia on Quantitative Biology 61: 95–104.
• Corona, M., R.A. Velarde, S. Remolina, A. Moran-lauter, Y. Wang, K.A. Hughes & G.E. Robinson, 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honeybee longevity. Proceedings of the National academy of Sciences of the United States of America 104: 7128–7133.
• Danbolt, N.C., 2001. Glutamate Uptake. Progress in Neurobiology 65: 1-105.
• Démares. F., F. Drouard, I. Massou, C. Crattelet, A. Loeuillet, C. Bettiol, & V. Raymond, 2014. Catherine armengaud differential involvement of glutamate-gated chloride channel splice variants in the olfactorymemory processes of the honeybee Apis mellifera. Pharmacology, Biochemistry and Behavior 124:137-144.
• Démares, F., V. Raymond & C. Armengaud, 2013. Expression and localization of glutamate-gated chloride channel variants in honeybee brain (Apis mellifera). Insect Biochemistry Molecule Biology 43(1):115-24.
• Denison, R. & V. Raymond-Delpech, 2008. Insights into the molecular basis of social behaviour from studies on the honeybee, Apis mellifera. Invertebrate Neuroscience 8:1-9.
• Elhassani, A.K., S. Schuster, Y. Dyck, F. Demares, G. Leboulle & C. Armengaud, 2012. Identification, localization and function of glutamate‐gated chloride channel receptors in the honeybee brain. European Journal of Neuroscience 36: 2409-2420.
• Erreger, K., P.E. Chen, D.J. Wyllie & S.F. Traynelis, 2004. Glutamate receptor gating. Critical Reviews™ in Neurobilogy 16: 187–224.
• Fahrbach S.E. & G.E. Robinson, 1995. Behavioural development in the honeybee: toward the study of learning under natural conditions. Learnning & Memory 2: 199-224.
• French, A.S., K.L. Simcock, D. Rolke, S.E. Gartside, W. Blenau & G.A. Wright, 2004. The role of serotonin in feeding and gut contractions in the honeybee. Journal of Insect Physiology 61:8-15.
• Funada, M., S. Yasuo, T. Yoshimura, S. Ebihara, H. Sasagawa, Y. Kitagawa & T. Kadowaki, 2004. Characterization of the two distinct subtypes of metabotropic glutamate receptors from honeybee, Apis mellifera. Neuroscience Letter 359:190-194.
• Giurfa, M., J. Nşñez & W. Backhaus, 1994. Odour and colour information in the foraging choice behaviour of the honeybee. Journal of Comparative Physiology A 175: 773-779.
• Hogner, A., J. Kastrup, R. Jin, T. Liljefors, M. Mayer, J. Egebjerg, I. Larsen & E. Gouaux, 2002. Structural basis for AMPA receptor activation and ligand selectivity: crystal structures of five agonist complexes with the GluR2 ligand-binding core. Journal of Molecular Biology 322: 93-109.
• Holscher, C., S. Schmid, P.K. Pilz, G. Sansig, H. Van der putten & C.F. Plappert, 2004. Lack of the metabotropic glutamate receptor subtype 7 selectively impairs short-term working memory but not long-term memory. Behavioural Brain Research 154: 473-482.
• Hornik, K., 2011. The R FAQ. ISBN 3-900051-08-9, 2011. http://CRAN.R-project.org/doc/FAQ/ R-FAQ.html.
• Honeybee genome sequencing consortium, 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931-949.
• Hoyer, D., J.P. Hannon & G.R.Martin, 2002. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacology Biochemistry and Behavior 71: 533-554.
• Kessels, H.W. & R. Malinow, 2009. Synaptic AMPA receptor plasticity and behavior. Neuron 61: 340-350.
• Kucharski, R., C. Mitri, Y. Grau & R. Maleszka, 2007. Characterization of a metabotropic glutamate receptor in the honeybee (Apis mellifera): implications for memory formation. Invertebrate Neuroscience 7: 99-108.
• Linden, D.J. & J.A. Connor, 1995. Long-term synaptic depression. Annual Review of Neuroscience 18: 319-357.
• Liu, W. & D.A.Saint, 2002. A new quantitative method of real time reverse transcription polymerase chain reaction assay based on simulation of polymerase chain reaction kinetics. Analytical Biochemistry 302: 52-59.
• Locatelli, F., G. Bundrock & U. Muller, 2005. Focal and temporal release of glutamate in the mushroom bodies improves olfactory memory in Apis mellifera. Journal of Neuroscience 25:11614-11618.
• Lourenco, A,P., A. Mackert, A.S. Cristino, & Z.L.P. Simoes, 2008. Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie 39:372–385
• Martin, S.J., P.D. Grimwood & R.G. Morris, 2000. Synaptic plasticity and memory: anevaluation of the hypothesis. Annual Review of Neuroscience 23: 649–711.
• Meltzer, C.C., G. Smith, S.T. Dekosky, B.G. Pollock, C.A. Mathis, R.Y. Moore, D.J. Kupfer & C.F. Reynolds, 1998. Serotonin in aging, late-life depression and Alzheimer’s disease: the emerging role of functional imaging. Neuropsychopharmacology 18: 407–430.
• Meneses, A. 1999. 5-HT system and cognition. Neuroscience & Biobehavioural Reviews, 8: 1111–1125.
• Meneses, A., 2002. Tianeptine: 5-HT uptake sites and 5-HT1-7 receptors modulate memory formation in an autoshaping Pavlovian/instrumental task. Neuroscience & Biobehavioural Reviews 26: 309-320.
• Meneses, A., 2007. Do serotonin1–7 receptors modulate short and long-term memory? Neurobiol. Learning & Memory 87: 561–572.
• Menzel, R., K. Geifer, J. Joerges, U. Müller & L. Chittka, 1998. Bees travel novel homeward routes by integrating separately acquired vector memories. Animal Behaviour 55: 139-152.
• Milner, B., L.R. Squire & E.R. Kandel, 1998. Cognitive Neuroscience Review and theStudy of Memory. Neuron 20: 445-468.
• Morris, R.G.M., S. Davis & S.P. Butcher, 1991. “Hippocampal Synaptic Plasticity and NMDA Receptors: A Role in Information storage?, 267-300”. In: Long-Term Potentiation: A Debate of Current Issues (Eds. M. Baudry & J. Davis), Massachusetts: MIT Press, Cambridge.
• Nelson, C.M., K.E. Ihle, M.K. Fondrk, R.E. Page & G.V. Amdam, 2007. The gene vitellogenin has multiple coordinating effects on social organization. PLOS Biology 5: e62.
• Nicoll, R.A. & R.C. Malenka, 1995. Contrasting properties of two forms of long-termpotentiation in the hippocampus. Nature 377: 115-118.
• Rawlins, J.N.P., 1996. NMDA receptors, synaptic plasticity, and learning and memory, pp. 275–284. In: Excitatory Amino Acids and the Cerebral Cortex (F. CONTI and T.P. HICKS Eds).- Massachusetts: MIT Press, Cambridge.
• Robinson, G.E., 1987. Regulation of honeybee age polyethism by juvenile hormone. Behavioural Ecology and Sociobiology 20: 329-338.
• Ryzhova, I.V., T.G. Zachepilo, E.G. Chesnokova & N.G. Lopatina 2010. Metabotropic Glutamate Receptors in Mechanisms of Plasticity of the Central Nervous System in the Honeybee Apis mellifera. Journal of Evolutionary Biochemistry and Physiology 46(3): 251—258.
• Sanderson, C.E., B.S. Orozco, P.S.Hill & H.Wells, 2006. Honeybee (Apis mellifera ligustica) response to differences in handling time, rewards and flower colours. Ethology 112: 937-946.
• Scharlaken, B., D.C. de Graaf, K. Goossens, M. Brunain, L.J. Peelman & F.J. Jacobs, 2008. Reference gene selection for insect expression studies using quantitative real-time PCR: The honeybee, Apis mellifera, head after a bacterial challenge. Journal of Insect Science 8:1–10.
• Schlenstedt, J., S. Balfanz, J. Baumann & W. Blenau, 2006. Am5-HT7: molecular and pharmacological characterization of the first serotonin receptor of the honeybee (Apis mellifera). Journal of Neurochemistry 98:1985-1998.
• Schmitt, J.A.J., M. Winger, J.G. Ramaekers, E.A.T. Evers & W.J. Riedel, 2006. Serotonin and human cognitive performance. Current Pharmaceutical Design 12: 2473-2486.
• Si, A., P. Helliwell & R. Maleszka, 2004. Effects of NMDA receptor antagonists onolfactory learning and memory in the honeybee (Apis mellifera). Pharmacology Biochemistry and Behavior 77: 191–197.
• Simonyi, A., L.A. Miller & G.Y. Sun, 2000. Region-specific decline in the expression of metabotropic glutamate receptor 7 mRNA in rat brain during aging. Molecular Brain Research 82: 101-106.
• Spiess, A. & C. Ritz, 2010. qpcR: Modelling and analysis of real-time PCR data. R package version 1.3-2.
• Thamm, M., D. Rolke, N. Jordan, S. Balfanz, C. Schiffer, A. Baumann & W. Blenau, 2013. Function and distribution of 5-HT2 receptors in the honeybee (Apis mellifera). PLoS One 8(12):e82407.
• Wright, G.A., 2011. The role of dopamine and serotonin in conditioned food aversion learning in the honeybee. Communicative & Integrative Biology 4 (3):318–320.
• Wright, G.A., J.A. Mustard, N.K. Simcock, A.A.R. Ross-Taylor, L.D. McNicholas, A. Popescu & F. Marion-Poll, 2010. Parallel reinforcement pathways for conditioned food aversions in the honeybee. Current Biology 20:2234– 2240.
• Winston, M.L., 1987. The Biology of the Honeybee. Harverd university Press, Cambridge, MA.
• Xia, S., T. Miyashita, T.F. Fu, W.Y. Lin, C.L. Wu, L. Pyzocha, I.R. Lin, M. Saitoe, T. Tully & A.S. Chiang, 2005. NMDA receptors mediate olfactory learning and memory in Drosophila. Current Biology 15:603-615.
• Zannat, M.T., F. Locatelli, J. Rybak, R. Menzel & G. Leboulle, 2006. Identification and localisation of the NR1 sub-unit homologue of the NMDA glutamate receptor in the honeybee brain. Neuroscience Letter 398:274-279.
• Zhang, S., M. Lehrer & M. Srinivasan, 1999. Honeybee memory: navigation by associative grouping and recall of visual stimuli. Neurobiology of Learning and Memory 72: 180-201.