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

  • 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.

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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

References

  1. Frisch, K., The Dancing Bees: An Account of the Life and Senses of the Honey Bee, New York, 1953.

    Google Scholar 

  2. Lopatina, N.G., Signal’naya deyatel’nost’ v sem’e medonosnoi pchely (Signaling in the Honeybee Family), Leningrad, 1971.

    Google Scholar 

  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.

  4. Riedel, G., Platt, B., and Micheau, J., Glutamate receptor function in learning and memory, Behav. Brain Res., 2003, vol. 140, pp. 1–47.

    Article  CAS  PubMed  Google Scholar 

  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. 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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hanley, J.G., Molecular mechanisms for regulation of AMPAR trafficking by PICK1, Biochem. Soc. Trans., 2006, vol. 34, pt. 5, pp. 931–935.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Pavlov, I.P., Lectures on the performance of cerebral hemispheres (1926), The Complete Collected Works, 1951, vol. 4, Moscow–Leningrad.

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Pavlov Institute of Physiology, Russian Academy of Sciences, St. Petersburg, Russia

    T. G. Zachepilo, A. A. Davydova, A. I. Vaido & N. G. Lopatina

Authors
  1. T. G. Zachepilo
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  2. A. A. Davydova
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  3. A. I. Vaido
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  4. N. G. Lopatina
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Correspondence to N. G. Lopatina.

Additional information

Original Russian Text © T.G. Zachepilo, A.A. Davydova, A.I. Vaido, N.G. Lopatina, 2018, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2018, Vol. 54, No. 6, pp. 399–405.

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Zachepilo, T.G., Davydova, A.A., Vaido, A.I. et al. Role of the GluR2 Subunit of AMPA Receptors in Associative Learning in the Honeybee Apis mellifera L.. J Evol Biochem Phys 54, 449–456 (2018). https://doi.org/10.1134/S0022093018060042

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  • DOI: https://doi.org/10.1134/S0022093018060042

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