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Neurochemical Journal

, Volume 7, Issue 1, pp 1–15 | Cite as

2′,3′-cyclic nucleotide phosphodiesterase (CNPase) as a target in neurodegenerative diseases

  • Yu. L. Baburina
  • O. V. Krestinina
  • T. S. AzarashviliEmail author
Review Articles

Abstract

We review the structure, characteristics, post-translational modifications, and functioning of 2′,3′-cyclic nucleotide phosphodiesterase (CNPase) localized in the CNS myelin and Schwann cells, as well as previously unknown properties of this protein, which was identified in brain mitochondria. We summarize the data on the localization of CNPase in the cell, the specificity of its substrates, the characteristics of the N- and C-terminals of the molecule, and its interactions with proteins-partners and nucleic acids. We describe the possible role of CNPase in ageing and neurodegenerative diseases, such as Alzheimer’s disease and multiple sclerosis, with the main emphasis on the role of mitochondria in these processes.

Keywords

mitochondria phosphodiesterase neurodegeneration ageing 

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References

  1. 1.
    Uyemura, K., Tobari, C., Hirano, S., and Tsukada, Y., J. Neurochem., 1972, vol. 19, pp. 2607–2614.PubMedCrossRefGoogle Scholar
  2. 2.
    Adams, C.W., Davison, A.N., and Gregson, N.A., J. Neurochem., 1963, vol. 10, pp. 383–395.PubMedCrossRefGoogle Scholar
  3. 3.
    Whitefeld, P.R., Heppel, L.A., and Markham, R., Biochem. J., 1955, vol. 60, pp. 15–19.Google Scholar
  4. 4.
    Sims, N.R., Bernard, C.C., Horvath, L., Mackay, I.R., and Carnegie, P.R., Adv. Exp. Med. Biol., 1978, vol. 100, pp. 411–422.PubMedCrossRefGoogle Scholar
  5. 5.
    Nishizawa, Y., Kurihara, T., and Takahashi, Y., Brain Res., 1981, vol. 212, pp. 219–222.PubMedCrossRefGoogle Scholar
  6. 6.
    Yu, W.P., Collarini, E.J., Pringle, N.P., and Richardson, W.D., Neuron, 1994, vol. 12, pp. 1353–1362.PubMedCrossRefGoogle Scholar
  7. 7.
    Epand, R.M., Biochim. Biophys. Acta, 1998, vol. 1376, pp. 353–368.PubMedCrossRefGoogle Scholar
  8. 8.
    Pritzker, L.B., Joshi, S., Gowan, J.J., Harauz, G., and Moscarello, M.A., Biochemistry, 2000, vol. 39, pp. 5374–5381.PubMedCrossRefGoogle Scholar
  9. 9.
    Balendiran, G.K., Schnutgen, F., Scapin, G., Borchers, T., Xhong, N., Lim, K., Godbout, R., Spener, F., and Sacchettini, J.C., J. Biol. Chem., 2000, vol. 275, pp. 27045–27054.PubMedGoogle Scholar
  10. 10.
    Grever, W.E., Weidenheim, K.M., Tricoche, M., Rashbaum, W.K., and Lyman, W.D., J. Neurosci. Res., 1997, vol. 47, pp. 332–340.PubMedCrossRefGoogle Scholar
  11. 11.
    Garbay, B., Heape, A.M., Sargueil, F., and Cassagne, C., Prog. Neurobiol., 2000, vol. 61, pp. 267–304.PubMedCrossRefGoogle Scholar
  12. 12.
    Shapira, R., Mobley, W.C., Thiele, S.B., Wilhelmi, M.R., Wallace, A., and Kibler, R.F., J. Neurochem., 1978, vol. 30, pp. 735–744.PubMedCrossRefGoogle Scholar
  13. 13.
    Kim, S.U., McMorris, F.A., and Sprinkle, T.J., Brain Res., 1984, vol. 300, pp. 195–199.PubMedCrossRefGoogle Scholar
  14. 14.
    Yoshino, J.E., Dinneen, M.P., Sprinkle, T.J., and Devries, G.H., Brain Res., 1985, vol. 325, pp. 199–203.PubMedCrossRefGoogle Scholar
  15. 15.
    Gravel, M., Peterson, J., Yong, V.W., Kottis, V., Trapp, B., and Braun, P.E., Mol. Cell Neurosci., 1996, vol. 7, pp. 453–466.PubMedCrossRefGoogle Scholar
  16. 16.
    Yin, X., Peterson, J., Gravel, M., Braun, P.E., and Trapp, B.D., J. Neurosci. Res., 1997, vol. 50, pp. 238–247.PubMedCrossRefGoogle Scholar
  17. 17.
    Rasband, M.N., Tayler, J., Kaga, Y., Yang, Y., Lappe-Siefke, C., Nave, K.A., and Bansal, R., Glia, 2005, vol. 50, pp. 86–90.PubMedCrossRefGoogle Scholar
  18. 18.
    Lee, J., Gravel, M., Zhang, R., Thibault, P., and Braun, P.E., J. Cell Biol., 2005, vol. 170, pp. 661–673.PubMedCrossRefGoogle Scholar
  19. 19.
    Lee, J., Gravel, M., Gao, E., O’Neill, R.C., and Braun, P.E., J. Biol. Chem., 2001, vol. 276, pp. 14804–14813.PubMedCrossRefGoogle Scholar
  20. 20.
    Prinos, P., Slack, C., and Lasko, D.D., J. Cell Biochem., 1995, vol. 58, pp. 115–131.PubMedCrossRefGoogle Scholar
  21. 21.
    Sprinkle, T.J., Tippins, R.B., and Kestler, D.P., Biochem. Biophys. Res. Commun., 1987, vol. 145, pp. 686–691.PubMedCrossRefGoogle Scholar
  22. 22.
    Stingo, S., Masullo, M., Polverini, E., Laezza, C., Ruggiero, I., Arcone, R., Ruozi, E., Dal, P.F., Malfitano, A.M., D’Ursi, A.M., and Bifulco, M., Chem. Biol. Drug Des., 2007, vol. 70, pp. 502–510.PubMedCrossRefGoogle Scholar
  23. 23.
    Lajtha, A., Toth, J., Fujimoto, K., and Agrawal, H.C., Biochem. J., 1977, vol. 164, pp. 323–329.PubMedGoogle Scholar
  24. 24.
    Rothman, J.E. and Lenard, J., Science, 1977, vol. 195, pp. 743–753.PubMedCrossRefGoogle Scholar
  25. 25.
    Braun, P.E., Sandillon, F., Edwards, A., Matthieu, J.M., and Privat, A., J. Neurosci., 1988, vol. 8, pp. 3057–3066.PubMedGoogle Scholar
  26. 26.
    McMorris, F.A., Kim, S.U., and Sprinkle, T.J., Brain Res., 1984, vol. 292, pp. 123–131.PubMedCrossRefGoogle Scholar
  27. 27.
    Trapp, B.D., Bernier, L., Andrews, S.B., and Colman, D.R., J. Neurochem., 1988, vol. 51, pp. 859–868.PubMedCrossRefGoogle Scholar
  28. 28.
    Yoshino, J.E., Griffin, J.W., and Devries, G.H., J. Neurochem., 1983, vol. 41, pp. 1126–1130.PubMedCrossRefGoogle Scholar
  29. 29.
    Jones, M. and Keenan, R.W., Biochim. Biophys. Acta, 1981, vol. 678, pp. 403–407.PubMedCrossRefGoogle Scholar
  30. 30.
    Dreiling, C.E., Schilling, R.J., and Reitz, R.C., Biochim. Biophys. Acta, 1981, vol. 640, pp. 114–120.PubMedCrossRefGoogle Scholar
  31. 31.
    Muller, H.W., Clapshaw, P.A., and Seifert, W., FEBS Lett., 1981, vol. 131, pp. 37–40.PubMedCrossRefGoogle Scholar
  32. 32.
    Drummond, R.J., Hamill, E.B., and Guha, A., J. Neurochem., 1978, vol. 31, pp. 871–878.PubMedCrossRefGoogle Scholar
  33. 33.
    Kurihara, T., Nishizawa, Y., Takahashi, Y., and Odani, S., Biochem. J., 1981, vol. 195, pp. 153–157.PubMedGoogle Scholar
  34. 34.
    Sprinkle, T.J., Grimes, M.J., and Eller, A.G., J. Neurochem., 1980, vol. 34, pp. 880–887.PubMedCrossRefGoogle Scholar
  35. 35.
    Tsukada, Y., Nagai, K., and Suda, H., J. Neurochem., 1980, vol. 34, pp. 1019–1022.PubMedCrossRefGoogle Scholar
  36. 36.
    Edwards, A.M. and Braun, P.E., Dev. Neurosci., 1988, vol. 10, pp. 75–80.PubMedCrossRefGoogle Scholar
  37. 37.
    Muller, H.W., FEBS Lett., 1982, vol. 144, pp. 77–80.PubMedCrossRefGoogle Scholar
  38. 38.
    Gravel, M., DeAngelis, D., and Braun, P.E., J. Neurosci. Res., 1994, vol. 38, pp. 243–247.PubMedCrossRefGoogle Scholar
  39. 39.
    Monoh, K., Kurihara, T., Sakimura, K., and Takahashi, Y., Biochem. Biophys. Res. Commun., 1989, vol. 165, pp. 1213–1220.PubMedCrossRefGoogle Scholar
  40. 40.
    Kurihara, T., Monoh, K., Sakimura, K., and Takahashi, Y., Biochem. Biophys. Res. Commun., 1990, vol. 170, pp. 1074–1081.PubMedCrossRefGoogle Scholar
  41. 41.
    Yu, W.P., Collarini, E.J., Pringle, N.P., and Richardson, W.D., Neuron, 1994, vol. 12, pp. 1353–1362.PubMedCrossRefGoogle Scholar
  42. 42.
    Vogel, U.S. and Thompson, R.J., Nucleic Acid Res., 1987, vol. 15, p. 7204.PubMedCrossRefGoogle Scholar
  43. 43.
    Kurihara, T., Fowler, A.V., and Takahashi, Y., J. Biol. Chem., 1987, vol. 262, pp. 3256–3261.PubMedGoogle Scholar
  44. 44.
    Olafson, R.W., Drummond, G.I., and Lee, J.F., Can. J. Biochem., 1969, vol. 47, pp. 961–966.PubMedCrossRefGoogle Scholar
  45. 45.
    Hugli, T.E., Bustin, M., and Moore, S., Brain Res., 1973, vol. 58, pp. 191–203.PubMedCrossRefGoogle Scholar
  46. 46.
    Sogin, D.C., J. Neurochem., 1976, vol. 27, pp. 1333–1337.PubMedCrossRefGoogle Scholar
  47. 47.
    Whitefeld, P.R., Heppel, L.A., and Markham, R., Biochem. J., 1955, vol. 60, pp. 15–19.Google Scholar
  48. 48.
    Sprinkle, T.J., Crit. Rev. Neurobiol., 1989, vol. 4, pp. 235–301.PubMedGoogle Scholar
  49. 49.
    Heaton, P.A. and Eckstein, F., Nucleic Acid Res., 1996, vol. 24, pp. 850–853.PubMedCrossRefGoogle Scholar
  50. 50.
    Agrawal, H.C., Sprinkle, T.J., and Agrawal, D., Biochem. Biophys. Res. Commun., 1990, vol. 170, pp. 817–823.PubMedCrossRefGoogle Scholar
  51. 51.
    Kim, T. and Pfeiffer, S.E., J. Neurocytol., 1999, vol. 28, pp. 281–293.PubMedCrossRefGoogle Scholar
  52. 52.
    Braun, P.E., De, A.D., Shtybel, W.W., and Bernier, L., J. Neurosci. Res., 1991, vol. 30, pp. 540–544.PubMedCrossRefGoogle Scholar
  53. 53.
    Esposito, C., Scrima, M., Carotenuto, A., Tedeschi, A., Rovero, P., D’Errico, G., Malfitano, A.M., Bifulco, M., and D’Ursi, A.M., Biochemistry, 2008, vol. 47, pp. 308–319.PubMedCrossRefGoogle Scholar
  54. 54.
    De Angelis, D.A. and Braun, P.E., J. Neurosci. Res., 1994, vol. 39, pp. 386–397.PubMedCrossRefGoogle Scholar
  55. 55.
    Cox, M.E., Gao, E.N., and Braun, P.E., J. Neurosci. Res., 1994, vol. 39, pp. 513–518.PubMedCrossRefGoogle Scholar
  56. 56.
    Agrawal, H.C., Sprinkle, T.J., and Agrawal, D., Neurochem. Res., 1994, vol. 19, pp. 721–728.PubMedCrossRefGoogle Scholar
  57. 57.
    Vogel, U.S. and Thompson, R.J., J. Neurochem., 1988, vol. 50, pp. 1667–1677.PubMedCrossRefGoogle Scholar
  58. 58.
    Kemp, B.E. and Pearson, R.B., Trends Biochem. Sci., 1990, vol. 15, pp. 342–346.PubMedCrossRefGoogle Scholar
  59. 59.
    O’Neill, R.C. and Braun, P.E., J. Neurochem., 2000, vol. 74, pp. 540–546.PubMedCrossRefGoogle Scholar
  60. 60.
    Stricker, R., Lottspeich, F., and Reiser, G., Biol. Chem. Hoppe Seyler, 1994, vol. 375, pp. 205–209.PubMedGoogle Scholar
  61. 61.
    Cho, S.J., Jung, J.S., Jin, I., and Moon, I.S., Mol. Cells, 2003, vol. 16, pp. 128–135.PubMedGoogle Scholar
  62. 62.
    Cho, S.J., Jung, J.S., Shin, S.C., Jin, I., Ko, B.H., Kim, K.Y., Suh-Kim, H., and Moon, I.S., Exp. Mol. Med., 2003, vol. 35, pp. 486–493.PubMedCrossRefGoogle Scholar
  63. 63.
    Dyer, C.A. and Benjamins, J.A., J. Neurosci. Res., 1989, vol. 24, pp. 201–211.PubMedCrossRefGoogle Scholar
  64. 64.
    Bifulco, M., Laezza, C., Stingo, S., and Wolff, J., Proc. Natl. Acad. Sci. U.S.A., 2002, vol. 99, pp. 1807–1812.PubMedCrossRefGoogle Scholar
  65. 65.
    Bostwick, D.G., J. Cell Biochem. Suppl., 1992, vol. 16H, pp. 10–19.PubMedCrossRefGoogle Scholar
  66. 66.
    Sawaya, R., Schwer, B., and Shuman, S., J. Biol. Chem., 2003, vol. 278, pp. 43928–43938.PubMedCrossRefGoogle Scholar
  67. 67.
    Pick, L. and Hurwitz, J., J. Biol. Chem., 1986, vol. 261, pp. 6684–6693.PubMedGoogle Scholar
  68. 68.
    Phizicky, E.M., Schwartz, R.C., and Abelson, J., J. Biol. Chem., 1986, vol. 261, pp. 2978–2986.PubMedGoogle Scholar
  69. 69.
    Tyc, K., Kellenberger, C., and Filipowicz, W., J. Biol. Chem., 1987, vol. 262, pp. 12994–13000.PubMedGoogle Scholar
  70. 70.
    Genschik, P., Hall, J., and Filipowicz, W., J. Biol. Chem., 1997, vol. 272, pp. 13211–13219.PubMedCrossRefGoogle Scholar
  71. 71.
    Ballestero, R.P., Wilmot, G.R., Leski, M.L., Uhler, M.D., and Agranoff, B.W., Proc. Natl. Acad. Sci. U.S.A., 1995, vol. 92, pp. 8621–8625.PubMedCrossRefGoogle Scholar
  72. 72.
    Ballestero, R.P., Wilmot, G.R., Agranoff, B.W., and Uhler, M.D., J. Biol. Chem., 1997, vol. 272, pp. 11479–11486.PubMedCrossRefGoogle Scholar
  73. 73.
    Ballestero, R.P., Dybowski, J.A., Levy, G., Agranoff, B.W., and Uhler, M.D., J. Neurochem., 1999, vol. 72, pp. 1362–1371.PubMedCrossRefGoogle Scholar
  74. 74.
    Kozlov, G., Lee, J., Elias, D., Gravel, M., Gutierrez, P., Ekiel, I., Braun, P.E., and Gehring, K., J. Biol. Chem., 2003, vol. 278, pp. 46021–46028.PubMedCrossRefGoogle Scholar
  75. 75.
    Sakamoto, Y., Tanaka, N., Ichimiya, T., Kurihara, T., and Nakamura, K.T., J. Mol. Biol., 2005, vol. 346, pp. 789–800.PubMedCrossRefGoogle Scholar
  76. 76.
    Hofmann, A., Zdanov, A., Genschik, P., Ruvinov, S., Filipowicz, W., and Wlodawer, A., EMBO J., 2000, vol. 19, pp. 6207–6217.PubMedCrossRefGoogle Scholar
  77. 77.
    Kato, M., Shirouzu, M., Terada, T., Yamaguchi, H., Murayama, K., Sakai, H., Kuramitsu, S., and Yokoyama, S., J. Mol. Biol., 2003, vol. 329, pp. 903–911.PubMedCrossRefGoogle Scholar
  78. 78.
    Nasr, F. and Filipowicz, W., Nucleic Acid Res., 2000, vol. 28, pp. 1676–1683.PubMedCrossRefGoogle Scholar
  79. 79.
    Mazumder, R., Iyer, L.M., Vasudevan, S., and Aravind, L., Nucleic Acid Res., 2002, vol. 30, pp. 5229–5243.PubMedCrossRefGoogle Scholar
  80. 80.
    Gravel, M., Robert, F., Kottis, V., Gallouzi, I.E., Pelletier, J., and Braun, P.E., J. Neurosci. Res., 2009, vol. 87, pp. 1069–1079.PubMedCrossRefGoogle Scholar
  81. 81.
    Scherer, S.S., Braun, P.E., Grinspan, J., Collarini, E., Wang, D.Y., and Kamholz, J., Neuron, 1994, vol. 12, pp. 1363–1375.PubMedCrossRefGoogle Scholar
  82. 82.
    Halestrap, A.P. and Brenner, C., Curr. Med. Chem., 2003, vol. 10, pp. 1507–1525.PubMedCrossRefGoogle Scholar
  83. 83.
    Brdiczka, D., Beutner, G., Ruck, A., Dolder, M., and Wallimann, T., Biofactors, 1998, vol. 8, pp. 235–242.PubMedCrossRefGoogle Scholar
  84. 84.
    Giulian, D., Iwanij, V., Dean, G., and Drummond, R.J., Brain Res., 1983, vol. 265, pp. 217–225.PubMedCrossRefGoogle Scholar
  85. 85.
    Giulian, D. and Moore, S., J. Biol. Chem., 1980, vol. 255, pp. 5993–5995.PubMedGoogle Scholar
  86. 86.
    McFerran, B. and Burgoyne, R., J. Cell Sci., 1997, vol. 110, pp. 2979–2985.PubMedGoogle Scholar
  87. 87.
    Stariha, R.L. and Kim, S.U., Microsc. Res. Tech., 2001, vol. 52, pp. 680–688.PubMedCrossRefGoogle Scholar
  88. 88.
    Grunler, J. and Parmryd, I., FEBS Lett., 1999, vol. 455, pp. 233–237.PubMedCrossRefGoogle Scholar
  89. 89.
    Parmryd, I. and Dallner, G., Arch. Biochem. Biophys., 1999, vol. 364, pp. 153–160.PubMedCrossRefGoogle Scholar
  90. 90.
    De Angelis, D.A. and Braun, P.E., J. Neurochem., 1996, vol. 67, pp. 943–951.PubMedCrossRefGoogle Scholar
  91. 91.
    Laezza, C., Wolff, J., and Bifulco, M., FEBS Lett., 1997, vol. 413, pp. 260–264.PubMedCrossRefGoogle Scholar
  92. 92.
    Lappe-Siefke, C., Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P.E., Griffiths, I.R., and Nave, K.A., Nat. Genet., 2003, vol. 33, pp. 366–374.PubMedCrossRefGoogle Scholar
  93. 93.
    Yuryev, A., Ono, M., Goff, S.A., Macaluso, F., and Wennogle, L.P., Mol. Cell Biol., 2000, vol. 20, pp. 4870–4878.PubMedCrossRefGoogle Scholar
  94. 94.
    Ventura, A., Maccarana, M., Raker, V.A., and Pelicci, P.G., J. Biol. Chem., 2004, vol. 279, pp. 2299–2306.PubMedCrossRefGoogle Scholar
  95. 95.
    Bernardi, P., Physiol. Rev., 1999, vol. 79, pp. 1127–1155.PubMedGoogle Scholar
  96. 96.
    Zohar, H., Israelson, A., Hamad, S., and Shoshan-Barmatz, V., Biochem. J., 2004, vol. 377, pp. 347–355.CrossRefGoogle Scholar
  97. 97.
    Brenner, C., Cadiou, H., Vieira, H.L., Zamzami, N., Marzo, I., Xie, Z., Leber, B., Andrews, D., Duclohier, H., Reed, J.C., and Kroemer, G., Oncogene, 2000, vol. 19, pp. 329–336.PubMedCrossRefGoogle Scholar
  98. 98.
    Kokoszka, J.E., Waymire, K.G., Levy, S.E., Sligh, J.E., Cai, J., and Jones, D.P., MacGregor G.R., Wallace D.C, Nature, 2004, vol. 427, pp. 461–465.PubMedCrossRefGoogle Scholar
  99. 99.
    Baines, C.P., Kaiser, R.A., Sheiko, T., Craigen, W.J., and Molkentin, J.D., Nat. Cell Biol., 2007, vol. 9, pp. 550–555.PubMedCrossRefGoogle Scholar
  100. 100.
    Azarashvili, T.S., Tyynela, J., Odinokova, I.V., Grigorjev, P.A., Baumann, M., Evtodienko, Y.V., and Saris, N.E., J. Bioenerg. Biomembr., 2002, vol. 34, pp. 279–284.PubMedCrossRefGoogle Scholar
  101. 101.
    Azarashvili, T., Krestinina, O., Galvita, A., Grachev, D., Baburina, Y., Stricker, R., Evtodienko, Y., and Reiser, G., Am. J. Physiol. Cell Physiol., 2009, vol. 296, pp. C1428–C1439.PubMedCrossRefGoogle Scholar
  102. 102.
    Low, R.L., Mitochondrion, 2003, vol. 2, pp. 225–236.PubMedCrossRefGoogle Scholar
  103. 103.
    Peters, A., Rosene, D.L., Moss, M.B., Kemper, T.L., Abraham, C.R., Tigges, J., and Albert, M.S., J. Neuropathol. Exp. Neurol., 1996, vol. 55, pp. 861–874.PubMedGoogle Scholar
  104. 104.
    Sloane, J.A., Hinman, J.D., Lubonia, M., Hollander, W., and Abraham, C.R., J. Neurochem., 2003, vol. 84, pp. 157–168.PubMedCrossRefGoogle Scholar
  105. 105.
    Gravel, M., Peterson, J., Yong, V.W., Kottis, V., Trapp, B., and Braun, P.E., Mol. Cell Neurosci., 1996, vol. 7, pp. 453–466.PubMedCrossRefGoogle Scholar
  106. 106.
    Yin, X., Peterson, J., Gravel, M., Braun, P.E., and Trapp, B.D., J. Neurosci. Res., 1997, vol. 50, pp. 238–247.PubMedCrossRefGoogle Scholar
  107. 107.
    Schlaepfer, W.W., Brain Res., 1977, vol. 136, pp. 1–9.PubMedCrossRefGoogle Scholar
  108. 108.
    Albert, M., Neurobiol. Aging, 1993, vol. 14, pp. 623–625.PubMedCrossRefGoogle Scholar
  109. 109.
    Kiatipattanasakul, W., Nakamura, S., Hossain, M.M., Nakayama, H., Uchino, T., Shumiya, S., Goto, N., and Doi, K., Acta Neuropathol., 1996, vol. 92, pp. 242–248.PubMedCrossRefGoogle Scholar
  110. 110.
    Lintner, R.N. and Dyer, C.A., J. Neurosci. Res., 2000, vol. 60, pp. 437–449.PubMedCrossRefGoogle Scholar
  111. 111.
    Hinman, J.D., Peters, A., Cabral, H., Rosene, D.L., Hollander, W., Rasband, M.N., and Abraham, C.R., J. Comp. Neurol., 2006, vol. 495, pp. 351–362.PubMedCrossRefGoogle Scholar
  112. 112.
    Tanaka, J., Okuma, Y., Tomobe, K., and Nomura, Y., Biol. Pharm. Bull., 2005, vol. 28, pp. 615–618.PubMedCrossRefGoogle Scholar
  113. 113.
    Ames, B.N., Shigenaga, M.K., and Hagen, T.M., Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 7915–7922.PubMedCrossRefGoogle Scholar
  114. 114.
    Papa, S. and Skulachev, V.P., Mol. Cell Biochem., 1997, vol. 174, pp. 305–319.PubMedCrossRefGoogle Scholar
  115. 115.
    Wallace, D.C., Shoffner, J.M., Trounce, I., Brown, M.D., Ballinger, S.W., Corral-Debrinski, M., Horton, T., Jun, A.S., and Lott, M.T., Biochim. Biophys. Acta, 1995, vol. 1271, pp. 141–151.PubMedCrossRefGoogle Scholar
  116. 116.
    Rottenberg, H. and Wu, S., Biochem. Biophys. Res. Commun., 1997, vol. 240, pp. 68–74.PubMedCrossRefGoogle Scholar
  117. 117.
    Crompton, M., Aging Cell, 2004, vol. 3, pp. 3–6.PubMedCrossRefGoogle Scholar
  118. 118.
    Krestinina, O.V., Kruglov, A.G., Grachev, D.E., Baburina, Yu.L., Evtodienko, Yu.V., Moshkov, D.A., Santalova, I.M., and Azarashvili, T.S., Biol. Membr., 2010, vol. 27.Google Scholar
  119. 119.
    Grune, T., Jung, T., Merker, K., and Davies, K.J., Int. J. Biochem. Cell Biol., 2004, vol. 36, pp. 2519–2530.PubMedCrossRefGoogle Scholar
  120. 120.
    Crompton, M., J. Physiol., 2000, vol. 529 P.Google Scholar
  121. 121.
    Yin, X., Peterson, J., Gravel, M., Braun, P.E., and Trapp, B.D., J. Neurosci. Res., 1997, vol. 50, pp. 238–247.PubMedCrossRefGoogle Scholar
  122. 122.
    Torp, R., Head, E., and Cotman, C.W., Prog. Neuropsychopharmacol. Biol. Psychiatry, 2000, vol. 24, pp. 801–810.PubMedCrossRefGoogle Scholar
  123. 123.
    Vlkolinsky, R., Cairns, N., Fountoulakis, M., and Lubec, G., Neurobiol. Aging, 2001, vol. 22, pp. 547–553.PubMedCrossRefGoogle Scholar
  124. 124.
    Roher, A.E., Weiss, N., Kokjohn, T.A., Kuo, Y.M., Kalback, W., Anthony, J., Watson, D., Luehrs, D.C., Sue, L., Walker, D., Emmerling, M., Goux, W., and Beach, T., Biochemistry, 2002, vol. 41, pp. 11080–11090.PubMedCrossRefGoogle Scholar
  125. 125.
    Leuner, K., Hauptmann, S., Kader, R., Scherping, I., Keil, U., Strosznajder, J.B., Eckert, A., and Muller, W.E., Antioxid. Redox. Signal, 2007, vol. 9, pp. 1659–1675.PubMedCrossRefGoogle Scholar
  126. 126.
    Lopez, J.R., Lyckman, A., Oddo, S., LaFerla, F.M., Querfurth, H.W., and Shtifman, A., J. Neurochem., 2008, vol. 105, pp. 262–271.PubMedCrossRefGoogle Scholar
  127. 127.
    Baloyannis, S.J., J. Alzheimers. Dis., 2006, vol. 9, pp. 119–126.PubMedGoogle Scholar
  128. 128.
    Rosenbergova, M., Pristasova, S., and Prachar, J., Acta Virol., 1981, vol. 25, pp. 71–77.PubMedGoogle Scholar
  129. 129.
    Rosenbergova, M. and Pristasova, S., Acta Virol., 1990, vol. 34, pp. 508–516.PubMedGoogle Scholar
  130. 130.
    Rosenbergova, M. and Pristasova, S., Acta Virol., 1991, vol. 35, pp. 401–407.PubMedGoogle Scholar
  131. 131.
    Dutta, R. and Trapp, B.D., Neurology, 2007, vol. 68, pp. S22–S31.PubMedCrossRefGoogle Scholar
  132. 132.
    Caldwell, P.C., J. Physiol., 1960, vol. 152, pp. 545–560.PubMedGoogle Scholar
  133. 133.
    Craner, M.J., Newcombe, J., Black, J.A., Hartle, C., Cuzner, M.L., and Waxman, S.G., Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 8168–8173.PubMedCrossRefGoogle Scholar
  134. 134.
    Waxman, S.G., Nat. Rev. Neurosci., 2006, vol. 7, pp. 932–941.PubMedCrossRefGoogle Scholar
  135. 135.
    Smith, K.J., Brain Pathol., 2007, vol. 17, pp. 230–242.PubMedCrossRefGoogle Scholar
  136. 136.
    Waxman, S.G., J. Neurotrauma, 1992, vol. 9, pp. S105–S117.PubMedGoogle Scholar
  137. 137.
    Coleman, M., Nat. Rev. Neurosci., 2005, vol. 6, pp. 889–898.PubMedCrossRefGoogle Scholar
  138. 138.
    Stys, P.K., J. Neurol. Sci., 2005, vol. 233, pp. 3–13.PubMedCrossRefGoogle Scholar
  139. 139.
    Mahad, D., Lassmann, H., and Turnbull, D., Neuropathol. Appl. Neurobiol., 2008, vol. 34, pp. 577–589.PubMedCrossRefGoogle Scholar
  140. 140.
    Mao, P. and Reddy, P.H., Biochim. Biophys. Acta, 2010, vol. 1802, pp. 66–79.PubMedCrossRefGoogle Scholar
  141. 141.
    Forte, M., Gold, B.G., Marracci, G., Chaudhary, P., Basso, E., Johnsen, D., Yu, X., Fowlkes, J., Rahder, M., Stem, K., Bernardi, P., and Bourdette, D., Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 7558–7563.PubMedCrossRefGoogle Scholar
  142. 142.
    Scott, L.J. and Figgitt, D.P., CNS. Drugs, 2004, vol. 18, pp. 379–396.PubMedCrossRefGoogle Scholar
  143. 143.
    Zambonin, J.L., Zhao, C., Ohno, N., Campbell, G.R., Engeham, S., Ziabreva, I., Schwarz, N., Lee, S.E., Frischer, J.M., Turnbull, D.M., Trapp, B.D., Lassmann, H., Franklin, R.J., and Mahad, D.J., Brain, 2011, vol. 134, pp. 1901–1913.PubMedCrossRefGoogle Scholar
  144. 144.
    Azarashvili, T., Stricker, R., and Reiser, G., Biol. Chem., 2010, vol. 391, pp. 619–629.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2013

Authors and Affiliations

  • Yu. L. Baburina
    • 1
  • O. V. Krestinina
    • 1
  • T. S. Azarashvili
    • 1
    • 2
    Email author
  1. 1.Institute of Theoretical and Experimental BiophysicsRussian Academy of SciencesMoscowRussia
  2. 2.Pushchino, Moskovskaya obl.Russia

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