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Role of the GluR2 Subunit of AMPA Receptors in Associative Learning in the Honeybee Apis mellifera L.

  • T. G. Zachepilo
  • A. A. Davydova
  • A. I. Vaido
  • N. G. LopatinaEmail author
Comparative and Ontogenic Physiology
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Abstract

In the honeybee, we discovered (1) the presence of the AMPA-like receptors containing the GluR2 subunit in neurons (Kenyon cells) of the mushroom bodies responsible for olfactory learning, (2) the involvement of the GluR2 subunit in the short-term memory formation during a single training session; (3) a similarity to mammals in the regulation of functional activity of the AMPA-like receptor GluR2 subunit.

Key words

honeybee short-term memory AMPA-receptor GluR2 subunit CMPDA modulator pep2-SVKI inhibitor 

Abbreviations

STM

short-term memory

ABP

AMPA receptor-binding protein

AMPA

α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid

CMPDA

N,N’-(1,4-phenylenedi- 2,1-ethanediyl)bis-2-propanesulfonamide

DNQX

6,7-dinitroquinoxaline-2,3-dione

GluR

glutamate receptor

GRIP

glutamate (AMPA) receptor interacting protein

PDZ

PSD-95 (a 95 kDa protein involved in signaling in the postsynaptic density), Dlg (the Drosophila discs large protein), and ZO1 (the zonula occludens 1 protein involved in maintaining epithelial cell polarity), i.e. essentially, a protein–protein interaction domain

pep2-SVKI

(YNVYGIESVKI) tyrosineasparagine- valine-tyrosine-glycine-isoleucine-glutamate-serine-valine-lysine-isoleucine

PICK1

protein interacting with C-kinase 1

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References

  1. 1.
    Frisch, K., The Dancing Bees: An Account of the Life and Senses of the Honey Bee, New York, 1953.Google Scholar
  2. 2.
    Lopatina, N.G., Signal’naya deyatel’nost’ v sem’e medonosnoi pchely (Signaling in the Honeybee Family), Leningrad, 1971.Google Scholar
  3. 3.
    Menzel, R., Learning and memory, Honeybee Neurobiology and Behavior, Galizia, C.G., Eisenhardt, D., and Giurfa, M., Eds., London–New York, 2012, pp. 485–493.Google Scholar
  4. 4.
    Riedel, G., Platt, B., and Micheau, J., Glutamate receptor function in learning and memory, Behav. Brain Res., 2003, vol. 140, pp. 1–47.CrossRefGoogle Scholar
  5. 5.
    Ryzhova, I.V., Lopatina, N.G., and Chesnokova, E.G., Receptors of excitatory amino acids in associative learning of the honeybee Apis mellifera L., Trudy Russk. Entomol. Obshch., St. Petersburg, 2003, vol. 74, pp. 17–32.Google Scholar
  6. 6.
    Braithwaite, S.P., Xia, H., and Malenka, R.C., Differential roles for NSF and GRIP/ABP in AMPA receptor cycling, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, no. 10, pp. 7096–7101.CrossRefGoogle Scholar
  7. 7.
    Hanley, J.G. and Hanley, J.M., PICK1 is a calcium-sensor for NMDA-induced AMPA receptor trafficking, EMBO J., 2005, vol. 24, no. 18, pp. 3266–3278.CrossRefGoogle Scholar
  8. 8.
    Hanley, J.G., Molecular mechanisms for regulation of AMPAR trafficking by PICK1, Biochem. Soc. Trans., 2006, vol. 34, pt. 5, pp. 931–935.CrossRefGoogle Scholar
  9. 9.
    Yang, Y., Wang, X., and Zhou, Q., Perisinaptic GluR2-lacking AMPA receptors control the reversibility of synaptic and spines modifications, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, no. 26, pp. 11999–12004.CrossRefGoogle Scholar
  10. 10.
    Asrar, S. and Jia, Zh., Molecular mechanisms coordinating functional and morphological plasticity at the synapse: role of GluA2/N-cadherin interaction-mediated actin signaling in mGluR-dependent LTD, Cell. Sign., 2013, vol. 25, pp. 397–402.CrossRefGoogle Scholar
  11. 11.
    Lai, K.O. and Ip, N.Y., Structural plasticity of dendritic spines: The underlying mechanisms and its dysregulation in brain disorders, Biochim. Biophis. Acta, 2013, vol. 1832, pp. 2257–2263.CrossRefGoogle Scholar
  12. 12.
    Wu, L.-J., Wang, Y.-T., and Zhuo, M., Hook-up of GluA2, GRIP and liprin-α for cholinergic muscarinic receptor-dependent LTD in the hippocampus, Mol. Brain, 2009, vol. 2, pp. 17–20.CrossRefGoogle Scholar
  13. 13.
    Volk, L., Kim, C.-H., Takamiya, K., Yu, Y., and Huganir, R.L., Developmental regulation of protein interacting with C kinase 1 (PICK1) function in hippocampal synaptic plasticity and learning, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, no. 50, pp. 21784–21789.CrossRefGoogle Scholar
  14. 14.
    Brockie, P.J., Jensen, M., Mellem, J.E., Maxfield, D., Thacker, C., Hoerndli, F., Dunn, P.J., Tomita, S., Madsen, D.M., and Maricq, A.V., Cornichons control ER export of AMPA receptors to regulate synaptic excitability, Neuron, 2013, vol. 80, pp. 129–142.CrossRefGoogle Scholar
  15. 15.
    Isaac, J.T.R., Ashby, M.C., and McBain, C.J., The role of the GluR2 subunit in AMPA receptor funcion and synaptic plasticity, Neuron, 2007, vol. 54, pp. 859–871.CrossRefGoogle Scholar
  16. 16.
    Tikhonov, D.B. and Magazanik, L.G., Origin and molecular evolution of ionotropic glutamate receptors, Neurosci. Behav. Physiol., 2009, vol. 39, pp. 763–773.CrossRefGoogle Scholar
  17. 17.
    Kim, C.-H., Chang, H.J., Lee, H.-K., and Huganir, R.L., Interaction of the AMPA receptor subunit GluR2y3 with PDZ domains regulates hippocampal long-term depression, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, no. 20, pp. 11725–11730.CrossRefGoogle Scholar
  18. 18.
    Daw, M., Chittajallu, R., Bortolotto, Z., Dev, K.K., Duprat, F., Henley, J.M., Collingridge, G.L., and Isaac, J.T., PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses, Neuron, 2000, vol. 28, pp. 873–886.CrossRefGoogle Scholar
  19. 19.
    Dong, H., O’Brien, R.J., Fung, E.T., Lanahan, A.A., Worley, P.F., and Huganir, R.L., GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors, Nature, 1997, vol. 386, pp. 279–283.CrossRefGoogle Scholar
  20. 20.
    Hart, A.C., Sims, S., and Kaplan, J.M., Synaptic code for sensory modalities revealed by C. elegans GluR-1 glutamate receptor, Nature, 1995, vol. 378, no. 6552, pp. 82–85.CrossRefGoogle Scholar
  21. 21.
    Schuster, C.M., Ultsch, A., Schloss, P., Cox, J. A., Schmitt, B., and Betz, H., Molecular cloning of an invertebrate glutamate receptor subunit expressed in Drosophila muscle, Science, 1991, vol. 254, no. 5028, pp. 112–114.CrossRefGoogle Scholar
  22. 22.
    Lopatina, N.G., Ryzhova, I.V., and Chesnokova, E.G., The role of non-NMDA-receptors in the process of associative learning in the honeybee Apis mellifera, J. Evol. Biochem. Physiol., 2002, vol. 38, pp. 211–217.CrossRefGoogle Scholar
  23. 23.
    Lopatina, N.G., Zachepilo, T.G., Ryzhova, I.V., Smirnov, V.B., and Chesnokova, E.G., Differential participation of central L-glutamate receptors of non-NMDA-subtype in associative learning of the honeybee Apis mellifera, J. Evol. Biochem. Physiol., 2004, vol. 40, pp. 271–276.CrossRefGoogle Scholar
  24. 24.
    Timm, D.E., Benveniste, M., Weeks, A.M., Nisenbaum, E.S., and Partin, K.M., Structural and functional analysis of two new positive allosteric modulators of GluA2 desensitization and deactivation, Mol. Pharmacol., 2011, vol. 80, pp. 267–280.CrossRefGoogle Scholar
  25. 25.
    Pavlov, I.P., Lectures on the performance of cerebral hemispheres (1926), The Complete Collected Works, 1951, vol. 4, Moscow–Leningrad.Google Scholar
  26. 26.
    Hawkins, R.D., Possible contributions of a novel form of synaptic plasticity in Aplysia to reward, memory, and their dysfunctions in mammalian brain, Learn. Mem., 2013, vol. 20, pp. 580–591.CrossRefGoogle Scholar
  27. 27.
    Harris, G., Shen, Y., Ha, H., Donato, A., Wallis, S., Zhang, X., and Zhang, Y., Dissecting the signaling mechanisms underlying recognition and preference of food odors, Neurosci., 2014, vol. 34, pp. 9389–9403.CrossRefGoogle Scholar
  28. 28.
    Dahlberg, C.L. and Juo, P., The WD40-repeat proteins WDR-20 and WDR-48 bind and activate the deubiquitinating enzyme USP-46 to promote the abundance of the glutamate receptor GLR-1 in the ventral nerve cord of Caenorhabditis elegans, J. Biol. Chem., 2014, vol. 289, pp. 3444–3456.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • T. G. Zachepilo
    • 1
  • A. A. Davydova
    • 1
  • A. I. Vaido
    • 1
  • N. G. Lopatina
    • 1
    Email author
  1. 1.Pavlov Institute of PhysiologyRussian Academy of SciencesSt. PetersburgRussia

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