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Dipeptides Beta- L-Aspartyl-Serine and Beta-L-Aspartyl-Proline in Memory Regulation in the Honeybee

  • Comparative and Ontogenic Physiology
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Abstract

We report a comparative analysis of the effect of alpha- and beta- isomers of the dipeptides aspartyl-serine and aspartyl-proline on the ability of honeybees to retain the conditioned food reflex to olfactory cues in their short-term/long-term memory. Stimulatory/inhibitory effects of the alpha-dipeptides on memory processes are confined to the concentration range of 10-6–10-8 M. In contrast, beta-dipeptides exert stimulatory/inhibitory effects on memory not only within the same range but also at ultra-low (pico- and femtomolar) concentrations. At concentrations of 10-9–10-11 M, beta-dipeptides have no effect on the characteristics under study (“silence zone”). Thus, we revealed fundamental differences in the effects of alpha- and beta- dipeptide isomers on the memory regulation.

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Abbreviations

STM:

short-term memory

LTM:

long-term memory

D-1:

alpha-L-aspar-tyl-1-proline

D-7:

alpha-L-aspartyl-L-serine

AD-1:

beta-L-aspartyl-proline

AD-7:

beta-L-aspartyl-serine

sNPF:

small neuropeptide F

PBAN:

pheromone biosynthesis activation neuropeptide

FMRF:

amide-phenylalanine-methi-onyl- arginyl-phenylalanine amide

References

  1. Fairclough, S.R., Chen, Z., Kramer, E., Zeng, Q., Young, S., Robertson, H.M., Begovic, E., Richter, D.J., Russ, C, Westbrook, M.J., Manning, G., Lang, B.F., Haas, B., Nusbaum, C., and King, N., Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta, Genome Biol., 2013, vol. 14, no. 2, R15. doi: 10.1186/gb-2013-14-2-rl5

    Google Scholar 

  2. Khavinson, V. Kh., Universal evolutionary mechanism of peptide regulation of gene expression and protein synthesis in the living nature, Usp. Gerontol, 2017, vol. 30, no. 2, p. 79, Mater. Conf. Inno-vat. Russ. Technol. Gerontol. Geriatr., St. Petersburg}}, 2017.

    Google Scholar 

  3. Khavinson, V., General mechanism for peptide regulation of gene expression, protein synthesis and human vital resource, Int. Symp. Experts' Opinion on Current Approaches in Anti-ageing Medicine and Gerontology, Geneva, 2017, pp. 50–54.

    Google Scholar 

  4. Khavinson, V.Kh. and Vanyushin, B.F., Universal mechanism of epigenetic peptide regulation of gene expression and protein synthesis in the living nature, Proc. VI Int. Symp. Interact. Nerv. Immune Syst. Norm. Pathol., St. Petersburg, 2017, p. 176.

    Google Scholar 

  5. Khavinson, V.Kh., Linkova, N.S., Dudkov, A.V., Polyakova, V.O., Kvetnoy, I.M., Peptidergic regulation of expression of genes encoding antioxidant and anti-inflammatory proteins, Bull. Exp. Biol. Med., 2011, vol. 152, no. 2, pp. 615–618.

    Google Scholar 

  6. Ludwig, M., Apps, D., Menzies, J., Patel, J.C., and Rice, M.E., Dendritic release of neurotransmitters, Compr. Physiol., 2016, vol. 7, no. 2, pp. 235–252. doi: 10.1002/cphy.c 160007

    Article  PubMed  PubMed Central  Google Scholar 

  7. Schoofs, L., De Loof, A., and Van Hiel, M.B., Neuropeptides as regulators of behavior in insects, Annu. Rev. Entomol, 2017, vol. 62, pp. 35–52. doi: 10.1146/annurev-ento-031616-035500

    Article  CAS  PubMed  Google Scholar 

  8. Nachman, R.J., Holman, G.M., Hayes, T.K., and Beier, R.C., Acyl, pseudotetra-, tri- and dipeptide active-core analogs of insect neuropeptides, Int. J. Pept. Protein. Res., 1993, vol. 42, no. 2, pp. 372–377.

    CAS  PubMed  Google Scholar 

  9. Bendena, W.G., Neuropeptide physiology in insects, Adv. Exp. Med. Biol, 2010, vol. 692, pp. 166–191.

    Article  CAS  PubMed  Google Scholar 

  10. Shiotani, S., Yanai, N., Suzuki, T., Tujioka, S., Sakano, Y., Yamakawa-Kobayashi, K., and Kayashima, Y., Effect of a dipeptide-enriched diet in an adult Drosophila melanogaster laboratory strain, Biosci. Biotechnol. Biochem., 2013, vol. 77, no. 2, pp. 836–838.

    Article  CAS  PubMed  Google Scholar 

  11. Khavinson, V.Kh., Solovyov, AYu., Tarnovska-ya, S.I., and Linkova, N.S., Mechanism of biological activity of short peptides: cell penetration and epigenetic regulation of gene expression, Usp. Sovr. Biol, 2013, vol. 133, no. 2, pp. 310–316.

    CAS  Google Scholar 

  12. Nusbaum, M.P., Blitz, D.M., and Marder, E., Functional consequences of neuropeptide and small-molecule co-transmission, Nat. Rev. Neuro-sci., 2017, vol. 18, no. 2, pp. 389–403. doi: 10.1038/ nrn.2017.56

    Article  CAS  Google Scholar 

  13. Ostrovskaya, R.U., Yagubova, S.S., Gudashe-va, T.A., and Seredenin, S.B., Low-molecular-weight NGF mimetic corrects cognitive deficit and depression-like behavior in experimental diabetes, Acta naturae, 2017, vol. 9, no. 2(33), pp.100–108.

    Article  Google Scholar 

  14. Khosravi, M., Rahimi, R., Pourahmad, J., Za-rei, M. H., and Rabbani, M., Comparison of kinetic study and protective effects of biological dipeptide and two porphyrin derivatives on metal cytotoxicity toward human lymphocytes, Iran J. Pharm. Res., 2017, vol. 16, no. 2, pp. 1059–1070.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Moura, C.S., Lollo, P.C.B., Morato, P.N., Ris-so, E.M., and Amaya-Farfan, J., Bioactivity of food peptides: biological response of rats to bovine milk whey peptides following acute exercise, Food Nutr. Res., 2017, vol. 61, no. 2, pp. 1290740. doi: 10.1080/16546628.2017.1290740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Khavinson, V., Linkova, N., Kukanova, E., Bol-shakova, A., Gainullina, A., Tendler, S., Moro-zova, E., Tarnovskaya, S., Vinski, D., Bakulev, V., and Kasyanenko, N., Neuroprotective effect of EDR peptide in mouse model of Huntington's disease, J. Neurol. Neurosci., 2017, vol. 8, no. 2, pp. 1–11.

    Google Scholar 

  17. Fedoreeva, L.I., Dilovarova, T.A., Ashapkin, V.V., Martirosyan, Yu.Ts., Khavinson, V.Kh., Kharch-enko, P.N., and Vanyushin, B.F., Short exogenous peptides regulate expression of CLE, KNOX1 and GRF family genes in Nicotiana tabacum, Biochem. (Moscow), 2017, vol. 82, no. 2, pp. 521–528.

    Google Scholar 

  18. Cazzamali, G., Saxild, N., and Grimrnelikhui-jzen, C., Molecular cloning and functional expression of a Drosophila corazonin receptor, Biochem. Biophys. Res. Commun., 2002, vol. 298, no. 2, pp. 31–36.

    Article  CAS  PubMed  Google Scholar 

  19. Flicker, L.D., Neuropeptide-processing enzymes: Applications for drug discovery, AAPS J., 2005, vol. 7, no. 2, pp. E449-E455. doi: 10.1208/aap-SJ070244

    Google Scholar 

  20. Nssel, D.R. and Winther, A.M., Drosophila neuropeptides in regulation of physiology and behavior, Prog. Neurobiol, 2010, vol. 92, no. 2, pp. 42–104. doi: 10.1016/j.pneurobio.2010.04.010

    Article  CAS  Google Scholar 

  21. Avargues-Weber, A., Dyer, A.G., Ferrah, N., and Giurfa, M., The forest or the trees: preference for global over local image processing is reversed by prior experience in honeybees, Proc. Roy. Soc. Ion-don B, Biol. Sci., vol.282, no. 1799, p. 2014–2384}. doi: 10.1098/rspb.2014.2384

  22. Chalisova, N.I., Kamyshev, N.G., Lopati-na, N.G., Koncevaya, E.A., Urtyeva, S.A., and Urtyeva, T.A., Influence of encoded amino acids on associative learning in the honeybee Apis mel-lifera, Zh. Evol. Biokhim. Fiziol, 2011, vol. 47, no. 2, pp. 516–518.

    CAS  PubMed  Google Scholar 

  23. Chalisova, N.I., Lopatina, N.G., Kamyshev, N.G., Linkova, N.S., Koncevaya, E.A., Dudkov, A.V., Kozina, L.S., Khavinson, V.Kh., and Titkov, Yu.S., Influence of the tripeptide Lys-Glu-Asp on physiological activity of cells in the neuro-immuno-endocrine system, Klet. Tekhnol. Biol. Med., 2012, no. 2, pp. 98–101.

    Google Scholar 

  24. Khavinson, V.Kh., Lopatina, N.G., Chalisova, N.I., Zachepilo, T.G., Linkova, N.S., Khali-mov, R.I., and Kamyshev, N.G., Tripeptide models conditioned reflex activity in the honeybee Apis mellifera L., Fund. Issled., 2015, no. 2, pt. 3, pp. 492–496.

    Google Scholar 

  25. Chalisova, N.I., Zachepilo, T.G., Kamy-shev, N.G., and Lopatina, N.G., The regulatory effect of dipeptides on cell proliferation in mammalian nerve tissue culture and olfactory associative learning in insects, J. Evol. Biochem. Physiol, 2015, vol. 51, no. 2, pp. 495–498.

    Article  CAS  Google Scholar 

  26. Chalisova, N.I., Lopatina, N.G., Kamy-shev, N.G., Zachepilo, T.G., Kozina, L.S., and Zalomaeva, E.S., The effect of ultra-small doses of bioregulatory peptides on cell proliferation in or-ganotypical culture of mammalian nerve tissue and higher nervous activity in insects, Usp. Gerontol, 2017, vol. 30, no. 2, p. 82, Mater. Conf. Innovat. Ross. Technol Gerontol Geriatr., St. Petersburg, 2017.

    Google Scholar 

  27. Menzel, R., Hammer, M., Muller, U., and Rosen-boom, H., Behavioral, neural and cellular components underlying olfactory learning in the honeybee, J. Physiol. Paris, 1996, vol. 90, no. 2–6, pp. 395–398.

    Article  CAS  PubMed  Google Scholar 

  28. Predel, R. andNeupert, S., Social behavior and the evolution of neuropeptide genes: lessons from the honeybee genome, Bioessays, 2007, vol. 29, no. 2, pp. 416–421.

    Article  CAS  PubMed  Google Scholar 

  29. Russo, A.F., Overview of neuropeptides: awakening the senses? Headache, 2017, vol. 57, Suppl. 2, pp. 37–46. doi: 10.1111/head.l3084

    Article  PubMed  PubMed Central  Google Scholar 

  30. Shataeva, L.K., Khavinson, V.Kh., and Ryad-nova, N.Yu., Peptidnaya samoregulyatsiya zhivikh system: fakty i gipotezy (Peptide Selfregulation in Living Systems: Facts and Hypotheses), St. Petersburg, 2003.

    Google Scholar 

  31. Min-Chul, S., Masahito, W., Du-Jie, X., Toshi-taka, Y., and Satomi, I., Inhibition of membrane Na+ channels by A type botulinum toxin at fem-tomolar concentrations in central and peripheral neurons, J. Pharmacol Sci., 2012, vol. 118, pp. 33–42.

    Article  CAS  Google Scholar 

  32. Smith, C.C., Martin, S.C., Sugunan, K., Russek, S.J., Gibbs, T.T., and Farb, D.H., A role for picomolar concentrations of pregnenolone sulfate in synaptic activity-dependent Ca2+ signaling and CREB activation, Mol Pharmacol, 2014, vol. 86, no. 2, pp. 390–398. doi: 10.1124/ mol. 114.094128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rubaiy, H.N., Ludlow, M.J., Henrot, M., Gaunt, H.J., Miteva, K., Cheung, S.Y., Ta-nahashi, Y., Hamzah, N., Musialowski, K.E., Blythe, N.M., Appleby, H.L., Bailey, M.A., McKeown, L., Taylor, R., Foster, R., Wald-mann, H., Nussbaumer, P., Christmann, M., Bon, R.S., Muraki, K., and Beech, D.J., Picomolar, selective, and subtype-specific small-molecule inhibition of TRPC1/4/5 channels, J. Biol. Chem., 2017, vol. 292, no. 2, pp. 8158–8173. doi 10.1074/ jbc.M116.773556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Burlakova, E.B., Konradov, A.A., and Maltse-va, E.L., Effect of ultra-small doses of biologically active substances and low-intensity physical factors, Khim. Fiz., 2003, vol. 22, no. 2, pp. 21–40.ISSN 0013-8738, Entomological Review, 2019, Vol. 99, No. 2, pp. 143–157.

    CAS  Google Scholar 

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Authors and Affiliations

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

    N. I. Chalisova, T. G. Zachepilo, N. G. Kamyshev & N. G. Lopatina

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  1. N. I. Chalisova
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  2. T. G. Zachepilo
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  3. N. G. Kamyshev
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  4. N. G. Lopatina
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Correspondence to T. G. Zachepilo.

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Russian Text © The Author(s), 2019, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2019, Vol. 55, No. 2, pp. 115–120.

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Chalisova, N.I., Zachepilo, T.G., Kamyshev, N.G. et al. Dipeptides Beta- L-Aspartyl-Serine and Beta-L-Aspartyl-Proline in Memory Regulation in the Honeybee. J Evol Biochem Phys 55, 124–130 (2019). https://doi.org/10.1134/S0022093019020054

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