DOI QR코드

DOI QR Code

Impaired Taste Associative Memory and Memory Enhancement by Feeding Omija in Parkinson's Disease Fly Model

  • Poudel, Seeta (Department of Bio and Fermentation Convergence Technology, BK21 PLUS project, Kookmin University) ;
  • Lee, Youngseok (Department of Bio and Fermentation Convergence Technology, BK21 PLUS project, Kookmin University)
  • 투고 : 2018.01.07
  • 심사 : 2018.05.20
  • 발행 : 2018.07.31

초록

Neurodegeneration can result in memory loss in the central nervous system (CNS) and impairment of taste and smell in the peripheral nervous system (PNS). The neurodegeneration seen in Parkinson's disease (PD) is characterized by functional loss of dopaminergic neurons. Recent studies have also found a role for dopaminergic neurons in regulating taste memory rewards in insects. To investigate how taste memories and sugar sensitivity can be affected in PD, we utilized the $DJ-1{\beta}$ mutant fruit fly, $DJ-1{\beta}^{ex54}$, as a PD model. We performed binary choice feeding assays, electrophysiology and taste-mediated memory tests to explore the function of the $DJ-1{\beta}$ gene in terms of sugar sensitivity as well as associative taste memory. We found that PD flies exhibited an impaired ability to discriminate sucrose across a range of sugar concentrations, with normal responses at only very high concentrations of sugar. They also showed an impairment in associative taste memory. We highlight that the taste impairment and memory defect in $DJ-1{\beta}^{ex54}$ can be recovered by the expression of wild-type $DJ-1{\beta}$ gene in the dopaminergic neurons. We also emphasized the role of dopaminergic neurons in restoring taste memory function. This impaired memory property of $DJ-1{\beta}^{ex54}$ flies also allows them to be used as a model system for finding supplementary dietary foods that can improve memory function. Here we provide evidence that the associative taste memory of both control and $DJ-1{\beta}^{ex54}$ flies can be enhanced with dietary supplementation of the medicinal plant, omija.

키워드

참고문헌

  1. Almer, Z., Klein, K.S., Marsh, L., Gerstenhaber, M., and Repka, M.X. (2012). Ocular motor and sensory function in Parkinson's disease. Ophthalmology 119, 178-182. https://doi.org/10.1016/j.ophtha.2011.06.040
  2. Andretic, R., and Hirsh, J. (2000). Circadian modulation of dopamine receptor responsiveness in Drosophila melanogaster. Proc. Natl. Acad. Sci., USA 97, 1873-1878. https://doi.org/10.1073/pnas.97.4.1873
  3. Ansari, K.A., and Johnson, A. (1975). Olfactory function in patients with Parkinson's disease. J. Chronic Dis. 28, 493-497. https://doi.org/10.1016/0021-9681(75)90058-2
  4. Bonifati, V., Rizzu, P., Van Baren, M.J., Schaap, O., Breedveld, G.J., Krieger, E., Dekker, M.C., Squitieri, F., Ibanez, P., Joosse, M., et al. (2003). Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299, 256-259. https://doi.org/10.1126/science.1077209
  5. Chopra, A., and Doiphode, V.V. (2002). Ayurvedic medicine: core concept, therapeutic principles, and current relevance. Med. Clin. 86, 75-89.
  6. Damier, P., Hirsch, E.C., Agid, Y., and Graybiel, A.M. (1999). The substantia nigra of the human brain: II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 122, 1437-1448. https://doi.org/10.1093/brain/122.8.1437
  7. Dawson, T.M., and Dawson, V.L. (2003). Molecular pathways of neurodegeneration in Parkinson's disease. Science 302, 819-822. https://doi.org/10.1126/science.1087753
  8. Denvinsky, O., Steven, C., Shachter, S.C., and Pacia, S.V. (2005). Traditional chinese medicine. Complementary and Alternative Therapies for Epilepsy. 177-182.
  9. Dunipace, L., Meister, S., McNealy, C., and Amrein, H. (2001). Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11, 822-835. https://doi.org/10.1016/S0960-9822(01)00258-5
  10. Friggi-Grelin, F., Coulom, H., Meller, M., Gomez, D., Hirsh, J., and Birman, S. (2003). Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. Dev. Neurobiol. 54, 618-627. https://doi.org/10.1002/neu.10185
  11. Ganguly-Fitzgerald, I., Donlea, J., and Shaw, P.J. (2006). Waking experience affects sleep need in Drosophila. Science 313, 1775-1781. https://doi.org/10.1126/science.1130408
  12. Hiroi, M., Marion-Poll, F., and Tanimura, T. (2002). Differentiated response to sugars among labellar chemosensilla in Drosophila. Zool. Sci. 19, 1009-1018. https://doi.org/10.2108/zsj.19.1009
  13. Hwang, S., Song, S., Hong, Y.K., Choi, G., Suh, Y.S., Han, S.Y., Lee, M., Park, S.H., Lee, J.H., Lee, S., et al. (2013). Drosophila DJ-1 decreases neural sensitivity to stress by negatively regulating Daxx-like protein through dFOXO. PLoS Genet. 9, e1003412. https://doi.org/10.1371/journal.pgen.1003412
  14. Kim, S.H., Joo, M.H., and Yoo, S.H. (2009). Structural identification and antioxidant properties of major anthocyanin extracted from Omija (Schizandra chinensis) fruit. J. Food Sci. 74, C134-140. https://doi.org/10.1111/j.1750-3841.2009.01049.x
  15. Jung, G.T., Ju, I.O., Choi, J.S., and Hong, J.S. (2000). The antioxidative, antimicrobial and nitrite scavenging effects of Schizandra chinensis RUPRECHT (Omija) seed. Korean J. Food Sci. and Technol. 32, 928-935.
  16. Lee, Y., and Poudel, S. (2014). Taste sensation in Drosophila melanogaster. Hanyang Med. Rev. 34, 130-136. https://doi.org/10.7599/hmr.2014.34.3.130
  17. Lee, Y., Moon, S.J., and Montell, C. (2009). Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl. Acad. Sci. USA 106, 4495-4500. https://doi.org/10.1073/pnas.0811744106
  18. Masek, P., Worden, K., Aso, Y., Rubin, G.M., and Keene, A.C. (2015). A dopamine-modulated neural circuit regulating aversive taste memory in Drosophila. Curr. Biol. 25, 1535-1541. https://doi.org/10.1016/j.cub.2015.04.027
  19. Meena, H., Pandey, H.K., Pandey, P., Arya, M.C., and Ahmed, Z. (2012). Evaluation of antioxidant activity of two important memory enhancing medicinal plants Baccopa monnieri and Centella asiatica. Indian J. Pharmacol. 44, 114. https://doi.org/10.4103/0253-7613.91880
  20. Menzies, F.M., Yenisetti, S.C., and Min, K.T. (2005). Roles of Drosophila DJ-1 in survival of dopaminergic neurons and oxidative stress. Curr. Biol. 15, 1578-1582. https://doi.org/10.1016/j.cub.2005.07.036
  21. Meulener, M., Whitworth, A.J., Armstrong-Gold, C.E., Rizzu, P., Heutink, P., Wes, P.D., Pallanck, L.J., and Bonini, N.M. (2005). Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson's disease. Curr. Biol. 15, 1572-1577. https://doi.org/10.1016/j.cub.2005.07.064
  22. Panossian, A., and Wikman, G. (2008). Pharmacology of Schisandra chinensis Bail.: an overview of Russian research and uses in medicine. J. Ethnopharmacol. 118, 183-212. https://doi.org/10.1016/j.jep.2008.04.020
  23. Park, J., Kim, S.Y., Cha, G.H., Lee, S.B., Kim, S., and Chung, J. (2005). Drosophila DJ-1 mutants show oxidative stress-sensitive locomotive dysfunction. Gene 361, 133-139. https://doi.org/10.1016/j.gene.2005.06.040
  24. Poudel, S., Kim, Y., Gwak, J.S., Jeong, S., and Lee, Y. (2017). Gustatory receptor 22e is essential for sensing chloroquine and strychnine in Drosophila melanogaster. Insect Biochem. Mol. 88, 30-36. https://doi.org/10.1016/j.ibmb.2017.07.007
  25. Rice-Evans, C., Miller, N., and Paganga, G. (1997). Antioxidant properties of phenolic compounds. Trends Plant Sci. 2, 152-159. https://doi.org/10.1016/S1360-1385(97)01018-2
  26. Seiss, E., Praamstra, P., Hesse, C., and Rickards, H. (2003). Proprioceptive sensory function in Parkinson's disease and Huntington's disease: evidence from proprioception-related EEG potentials. Exp. Brain Res. 148, 308-319. https://doi.org/10.1007/s00221-002-1291-6
  27. Shah, M., Deeb, J., Fernando, M., Noyce, A., Visentin, E., Findley, L.J., and Hawkes, C.H. (2009). Abnormality of taste and smell in Parkinson's disease. Parkinsonism Relat. Disord. 15, 232-237. https://doi.org/10.1016/j.parkreldis.2008.05.008
  28. Sienkiewicz-Jarosz, H., Scinska, A., Kuran, W., Ryglewicz, D., Rogowski, A., Wrobel, E., Korkosz, A., Kostowski, W., and Bienkowski, P. (2005). Taste responses in patients with Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 76, 40-46. https://doi.org/10.1136/jnnp.2003.033373
  29. Sitaraman, D., Zars, M., LaFerriere, H., Chen, Y.C., Sable-Smith, A., Kitamoto, T., Rottinghaus, G.E., and Zars, T. (2008). Serotonin is necessary for place memory in Drosophila. Proc. Natl. Acad. Sci. USA 105, 5579-5584. https://doi.org/10.1073/pnas.0710168105
  30. Taira, T., Saito, Y., Niki, T., Iguchi-Ariga, S.M., Takahashi, K., and Ariga, H. (2004). DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep. 5, 213-218. https://doi.org/10.1038/sj.embor.7400074
  31. Tissingh, G., Berendse, H.W., Bergmans, P., DeWaard, R., Drukarch, B., Stoof, J.C., and Wolters, E.C. (2001). Loss of olfaction in de novo and treated Parkinson's disease: possible implications for early diagnosis. Mov. Disord. 16, 41-46. https://doi.org/10.1002/1531-8257(200101)16:1<41::AID-MDS1017>3.0.CO;2-M
  32. Wong, R., Piper, M.D., Wertheim, B., and Partridge, L. (2009). Quantification of food intake in Drosophila. PloS One 4, e6063. https://doi.org/10.1371/journal.pone.0006063
  33. Wu, X., Yu, X., and Jing, H. (2011). Optimization of phenolic antioxidant extraction from Wuweizi (Schisandra chinensis) pulp using random-centroid optimazation methodology. Int. J. Mol. Sci. 12, 6255-6266. https://doi.org/10.3390/ijms12096255
  34. Yokota, T., Sugawara, K., Ito, K., Takahashi, R., Ariga, H., and Mizusawa, H. (2003). Down regulation of DJ-1 enhances cell death by oxidative stress, ER stress, and proteasome inhibition. Biochem. Biophys. Res. Commun. 312, 1342-1348. https://doi.org/10.1016/j.bbrc.2003.11.056

피인용 문헌

  1. Disease model organism for Parkinson disease: Drosophila melanogaster vol.52, pp.4, 2018, https://doi.org/10.5483/bmbrep.2019.52.4.204
  2. Cucurbitacin B Activates Bitter-Sensing Gustatory Receptor Neurons via Gustatory Receptor 33a in Drosophila melanogaster vol.43, pp.6, 2018, https://doi.org/10.14348/molcells.2020.0019
  3. Cucurbitacin B Suppresses Hyperglycemia Associated with a High Sugar Diet and Promotes Sleep in Drosophila melanogaster vol.44, pp.2, 2018, https://doi.org/10.14348/molcells.2021.2245