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Ubiquitin-dependent protein degradation is necessary for long-term plasticity and memory

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Abstract

Synaptic plasticity is considered as a basis of learning and memory and, in its turn, is associated with the reconstruction of molecular complexes in the preand postsynaptic parts. One of the means of this reconstruction is ubiquitin-dependent degradation of proteins in proteasomes, which leads to local elimination of preliminarily defined proteins–targets strictly within a certain time period in order to subsequently modify molecular complexes, such as postsynaptic density, the presynaptic apparatus of neuromediator release, and the receptor apparatus of preand postsynaptic membranes. Here, we review the bases of the organization of ubiquitin-dependent protein degradation of proteins in proteasomes and its role in synaptic plasticity and consolidation, reconsolidation, and the extinction of memory. In addition, one section is focused on the analysis of novel data on the mechanisms of the regulation of ubiquitin-dependent protein degradation, because knowledge on the mechanisms of regulation helps one to better understand how the process of protein degradation interacts with other intracellular processes in the cell.

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References

  1. Sorokin, A.V., Kim, E.R., and Ovchinnikov, L.P., Usp. Biol. Khim., 2009, vol. 49, pp. 3–76.

    Google Scholar 

  2. Tai, H.-C. and Schuman, E.M., Nat. Rev., 2008, vol. 9, no. 11, pp. 826–838.

    Article  CAS  Google Scholar 

  3. Tsimokha, A.S., Tsitologiya, 2010, vol. 52, no. 4, pp. 277–300.

    CAS  Google Scholar 

  4. Vigneron, N. and Eynde, B., J, Biomolecules, 2014, vol. 4, pp. 994–1025.

    Article  Google Scholar 

  5. Pines, J. and Lindon, C., Nat. Cell Biol., 2005, vol. 7, no. 8, pp. 731–735.

    Article  CAS  PubMed  Google Scholar 

  6. Grabera, T.E., Hebert-Seropianb, S., Khoutorskyc, A., Davide, A., Yewdelle, J.W., Lacaille, J.-C., and Sossina, W.S., PNAS, vol. 110, no. 40, pp. 16205–16210.

  7. Hedge, A.N., Learn. Mem., 2010, vol. 17, no. 7, pp. 314–327.

    Article  Google Scholar 

  8. Jarome, J.T. and Helmstetter, F.J., Neurobiology of Learning and Memory, 2013, vol. 105, pp. 107–116.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Dong, C., Upadhya, S.C., Ding, L., Smith, T.K., and Hegde, A.N., Learn. Mem., 2008, vol. 15, no. 5, pp. 335–347.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Santos, A.R., Mele, M., Vaz, S.H., Kellermayer, B., Grimaldi, M., Colino-Oliveira, M., Rombo, D.M., Comprido, D., Sebastia, A.M., and Duarte, C.B., J. Neurosci., 2015, vol. 35, no. 8, pp. 3319–3329.

    Article  CAS  PubMed  Google Scholar 

  11. Karpova, A., Mikhaylova, M., Thomas, U., Knopfel, T., and Behnisch, T., J. Neurosci., 2006, vol. 26, no. 18, pp. 4949–4955.

    Article  CAS  PubMed  Google Scholar 

  12. Fonseca, R., Vabulas, R.M., Hartl, F.U., Bonhoeffer, T., and Nagerl, U.V., Neuron, 2006, vol. 52, no. 2, pp. 239–245.

    Article  CAS  PubMed  Google Scholar 

  13. Dong, C., Bach, S.V., Haynes, K.A., and Hegde, A.N., J. Neurosci., 2014, vol. 34, no. 9, pp. 3171–3182.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Fioravante, D., Liu, R.Y., and Byrne, J.H., J. Neurosci., 2008, vol. 28, no. 41, pp. 10245–10256.

    Article  Google Scholar 

  15. Citri, A., Soler-Llavina, G., Bhattacharyya, S., and Malenka, R.C., Eur. J. Neurosci., 2009, vol. 30, no. 8, pp. 1443–1450.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Maletic-Savatic, M., Malinow, R., and Svoboda, K., Science, 1999, vol. 283, no. 5409, pp. 1923–1927.

    Article  CAS  PubMed  Google Scholar 

  17. Hamilton, A.M., Oh, W.C., Vega-Ramirez, H., Stein, I.S., Hell, J.W., Patrick, G.N., and Zito, K., Neuron, vol. 74, no. 6, pp. 1023–1030.

  18. Colledge, M., Snyder, E.M., Crozier, R.A., Jacquelyn, A., Soderling, J.A., Jin, Y., Langeberg, L.K., Lu, H., Bear, M.F., John, D., and Scott, J.D., Neuron, 2003, vol. 40, no. 3, pp. 595–607.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Ehlers, M.D., Nat. Neurosci., 2003, vol. 6, no. 3, pp. 231–242.

    Article  CAS  PubMed  Google Scholar 

  20. Lee, K.J., Lee, Y., Rozeboom, A., Lee, J.Y., Udagawa, N., Hoe, H.S., and Pak, D.T., Neuron, 2011, vol. 69, no. 5, pp. 957–973.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Yao, I., Takagi, H., Ageta, H., Kahyo, T., Sato, S., Hatanaka, K., Fukuda, Y., Chiba, T., Morone, N., Yuasa, S., Inokuchi, K., Ohtsuka, T., Macgregor, G.R., Tanaka, K., and Setou, M., Cell, 2007, vol. 130, no. 5, pp. 943–957.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Guo, L. and Wang, Y., Neuroscience, 2007, vol. 145, no. 1, pp. 100–109.

    Article  CAS  PubMed  Google Scholar 

  23. Tsai, N.P., Biochim. Biophys. Acta, 2014, vol. 1843, no. 12, pp. 2838–2842.

    Article  CAS  PubMed  Google Scholar 

  24. Patrick, G.N., Bingol, B., Weld, H.A., and Schuman, E.M., Current Biology, 2003, vol. 13, no. 23, pp. 2073–2081.

    Article  CAS  PubMed  Google Scholar 

  25. Bingol, B. and Schuman, E.M., Neuropharmacology, 2004, vol. 47, no. 5, pp. 755–763.

    Article  CAS  PubMed  Google Scholar 

  26. Mao, S.-C., Lin, H.-C., and Gean, P.-W., Neuropsychopharmacology, 2008, vol. 33, no. 13, pp. 3085–3095.

    Article  CAS  PubMed  Google Scholar 

  27. Shin, S.M., Zhang, N., Hansen, J., Gerges, N.Z., Pak, D.T.S., Sheng, M., and Lee, S.H., Nat. Neurosci., 2012, vol. 15, no. 12, pp. 1655–1666.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Hung, A.Y., Sung, C.C., Brito, I.L., and Sheng, M., PLoS ONE, 2010, vol. 5, no. 3, p. e9842.

    Google Scholar 

  29. Kudryashova, I.V., Neirokhimiya, 2014, vol. 31, no. 1, pp. 1–11.

    Google Scholar 

  30. Jarome, T.J., Werner, C.T., Kwapis, J.L., and Helmstetter, F.J., PLoS ONE, 2011, vol. 6, no. 9, p. e24349.

    Google Scholar 

  31. Fustinana, M.S., de la Fuente, V., Federman, N., Freudenthal, R., and Romano, A., Learn. Mem., 2014, vol. 21, no. 9, pp. 478–487.

    Article  CAS  Google Scholar 

  32. Lee, S.-H., Choi, J.-H., Lee, N., Lee, H.-R., Kim, J.-I., Yu, N.-K., Choi, S.-L., Lee, S.-H., Kim, H., and Kaang, B.-K., Science, 2008, vol. 319, no. 1253, pp. 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  33. Da, Silva W.C., Cardosoa, G., Boninia, J.S., Benetti, F., and Izquierdoa, I., PNAS, vol. 110, no. 16, pp. 6566–6570.

  34. Banerjee, S., Neveu, P., and Kosik, K.S., Neuron, 2009, vol. 64, no. 6, pp. 871–884.

    Article  CAS  PubMed  Google Scholar 

  35. Ren, Z.-Y., Liu, M.-M., Xue, Y.-X., Ding, Z.-B., Xue, L.-F., Zhai, S.-D., and Lu, L., Neuropsychopharmacology, 2013, vol. 38, no. 5, pp. 778–790.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Puram, S.V., Kim, A.H., Ikeuchi, Y., Wilson-Grady, J.T., Merdes, A., Gygi, S.P., and Bonni, A., Nat. Neurosci., 2012, vol. 14, no. 8, pp. 973–983.

    Article  Google Scholar 

  37. Kuczera, T., Stilling, R.M., Hsia, H.-E., Bahari-Javan, S., Irniger, S., Nasmyth, K., Sananbenesi, F., and Fischer, A., Learn. Mem., 2011, vol. 18, no. 1, pp. 49–57.

    Article  CAS  PubMed  Google Scholar 

  38. Li, M., Shin, Y.-H., Hou, L., Huang, X., Wei, Z., Klann, E., and Zhang, P., Nat. Cell Biol., 2008, vol. 10, no. 9, pp. 1083–1089.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Pick, J.E., Malumbres, M., and Klann, E., Learn Mem., 2012, vol. 20, no. 1, pp. 11–20.

    Article  PubMed  Google Scholar 

  40. Huang, J., Ikeuchi, Y., Malumbres, M., and Bonni, A., Neuron, 2015, vol. 86, no. 3, pp. 1–14.

    Article  Google Scholar 

  41. Muddashetty, R.S., Nalavadi, V.C., Gross, C., Yao, X., Xing, L., Laur, O., Warren, S.T., and Bassell, G.J, Mol. Cell, 2011, vol. 42, no. 5, pp. 673–688.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Djakovic, S.N., Marquez-Lona, E.M., Jakawich, S.K., Wright, R., Chu, C., Sutton, M.A., and Patrick, G.N., J. Neurosci., 2012, vol. 32, no. 15, pp. 5126–5131.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Upadhya, S.C., Ding, L., Smith, T.K., and Hegde, A.N., Neurochem. Int., 2006, vol. 48, no. 4, pp. 296–305.

    Article  CAS  PubMed  Google Scholar 

  44. Achterberg, K.G., Buitendijk, G.H.S., Kool, M.J., Goorden, S.M.I., Post, L., Slump, D.E., Silva, A.J., van Woerden, G.M., Kushner, S.A., and Elgersma, Y., J. Neurosci., 2014, vol. 34, no. 34, pp. 11180–11187.

    Article  Google Scholar 

  45. Hell, J.W., Neuron, 2014, vol. 81, no. 2, pp. 249–265.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Otmakhov, N., Tao-Cheng, J.H., Carpenter, S., Asrican, B., Dosemeci, A., Reese, T.S., and Lisman, J., J. Neurosci., 2004, vol. 24, no. 42, pp. 9324–9331.

    Article  CAS  PubMed  Google Scholar 

  47. Rose, J., Jin, S.X., and Craig, A.M., Neuron, 2009, vol. 61, no. 3, pp. 351–358.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Jarome, T.J., Kwapis, J.L., Ruenzel, W.L., and Helmstette, F.J., Front. Behav. Neurosci., 2013, vol.7.

    Google Scholar 

  49. Bingol, B., Wang, C.-F., Arnott, D., Cheng, D., Peng, J., and Sheng, M., Cell, 2010, vol. 140, no. 4, pp. 567–578.

    Article  CAS  PubMed  Google Scholar 

  50. Bingol, B. and Schuman, E.M., Nature, 2006, vol. 441, no. 7097, pp. 1144–1148.

    Article  CAS  PubMed  Google Scholar 

  51. Naskar, S., Wan, H., and Kemenes, G., Nat. Commun., 2014, vol. 5, p. 3967.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Feng, Y., Longo, D.L., and Ferris, D.K., Cell Growth and Differentiation, 2001, vol. 12, no. 1, pp. 29–37.

    CAS  PubMed  Google Scholar 

  53. Seeburg, D.P., Pak, D., and Sheng, M., Oncogene, 2005, vol. 24, no. 2, pp. 292–298.

    Article  CAS  PubMed  Google Scholar 

  54. Chen, Y., Yuanxiang, P., Knopfel, T., Thomas, U., and Behnisch, T., Synapse, 2012, vol. 66, no. 2, pp. 142–150.

    Article  CAS  PubMed  Google Scholar 

  55. Pak, D.T.S. and Sheng, M., Science, 2003, vol. 302, no. 5649, pp. 1368–1373.

    Article  CAS  PubMed  Google Scholar 

  56. Ang, X.L., Seeburg, D.P., Sheng, M., and Harper, J.W., J. Biol. Chem., 2008, vol. 283, no. 43, pp. 29424–29432.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Iwase, K., Ishihara, A., Yoshimura, S., Andoh, Y., Kato, M., Seki, N., Matsumoto, E., Hiwasa, T., Muller, D., Fukunaga, K., and Takiguchi, M., J. Neurochem., 2014, vol. 128, no. 2, pp. 233–245.

    Article  CAS  PubMed  Google Scholar 

  58. Wiseman, S.L., Shimizu, Y., Palfrey, C., and Nairn, A.C., J. Biol. Chem., 2013, vol. 288, no. 24, pp. 17803–17811.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Verpelli, C., Piccoli, G., Zibetti, C., Zanchi, A., Gardoni, F., Huang, K., Brambilla, D., Di Luca, M., Battaglioli, E., and Sala, C., J. Neurosci., 2010, vol. 30, no. 17, pp. 5830–5842.

    Article  CAS  PubMed  Google Scholar 

  60. Fukushima, H. Zhang, Y., Archbold, G., Ishikawa, R., Nader, K., and Kida, S., eLife, 2014, vol. 3, p. e02736.

    Article  PubMed Central  PubMed  Google Scholar 

  61. Puram, S.V., Kim, A.H., Park, H.-Y., Anckar, J., and Bonni, A., Cell Reports, 2013, vol. 4, no. 1, pp. 19–30.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Schmidt, M., Hanna, J., Elsasser, S., and Finley, D., Biol. Chem., 2005, vol. 386, no. 8, pp. 725–737.

    Article  CAS  PubMed  Google Scholar 

  63. Geetha, T. and Wooten, M.W., Traffic, 2008, vol. 9, no. 7, pp. 1146–1156.

    Article  CAS  PubMed  Google Scholar 

  64. Chuang, S.M., Chen, L., Lambertson, D., Anand, M., Kinzy, T.G., and Madura, K., Mol. Cell Biol., 2005, vol. 25, no. 1, pp. 403–413.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. Moon, S., Cho, S.-J., Lee, H.-S., Seog, D.-H., Jung, Y.W., Jin, I.N., and Walikonis, R., Mol. Cells, 2008, vol. 25, no. 4, pp. 538–544.

    CAS  PubMed  Google Scholar 

  66. Tsokas, P., Grace, E.A., Chan, P., Ma, T., Sealfon, S.C., Iyengar, R., Landau, E.M., and Blitzer, R.D., J. Neurosci., 2005, vol. 25, no. 24, pp. 5833–5843.

    Article  CAS  PubMed  Google Scholar 

  67. Kwak, Y.D., Ma, T., Diao, S., Zhang, X., Chen, Y., Hsu, J., Lipton, S.A., Masliah, E., Xu, H., and Liao, F.F., Mol. Neurodegener., 2010, vol. 5, p.49.

    Article  PubMed Central  PubMed  Google Scholar 

  68. Palumbo, A., Fiore, G., Di Cristo, C., Di Cosmo, A., and d’Ischia, M., Biochem. Biophys. Res. Commun., 2002, vol. 293, no. 5, pp. 1536–1543.

    Article  CAS  PubMed  Google Scholar 

  69. Hu, R.G., Sheng, J., Qi, X., Xu, Z., Takahashi, T.T., and Varshavsky, A., Nature, 2005, vol. 437, no. 7061, pp. 981–986.

    Article  CAS  PubMed  Google Scholar 

  70. Kapadia, M.R., Eng, J.W., Jiang, Q., Stoyanovsky, D.A., and Kibbe, M.R., Nitric Oxide, 2009, vol. 20, no. 4, pp. 279–288.

    Article  CAS  PubMed  Google Scholar 

  71. Shanga, T., Kotamrajua, S., Zhaoa, H., Kalivendia, S.V., Hillardb, C.J., and Kalyanaraman, B., Free Radical Biology & Medicine, 2005, vol. 39, no. 8, pp. 1059–1074.

    Article  Google Scholar 

  72. Chung, K.K.K., Thomas, B., Pletnikova, O., Troncoso, J.C., Laura, MarshL., Dawson, V.L., Ted, M., and Dawson, T.M., Science, 2004, vol. 304, no. 5675, pp. 1328–1331.

    Article  CAS  PubMed  Google Scholar 

  73. Lipton, S.A., Nakamura, Y., Yao, D., Shi, Z.-Q., Uehara, T., and Gu, Z., Science, 2005, vol. 308, no. 5730, p. 1870.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to N. V. Bal’.

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Original Russian Text © N.V. Bal’, P.M. Balaban, 2015, published in Neirokhimiya, 2015, Vol. 32, No. 4, pp. 275–284.

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Bal’, N.V., Balaban, P.M. Ubiquitin-dependent protein degradation is necessary for long-term plasticity and memory. Neurochem. J. 9, 237–244 (2015). https://doi.org/10.1134/S1819712415040042

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