Skip to main content
SpringerLink
Log in

Cellular mechanisms of brain hypoglycemia

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Data on intracellular processes induced by a low glucose level in nerve tissue are presented. The involvement of glutamate and ade nosine receptors, mitochondria, reactive oxygen species (ROS), and calcium ions in the development of hypoglyce mia-induced damage of neurons is considered. Hypoglycemia-induced calcium overload of neuronal mitochondria is suggested to be responsible for the increased ROS production by mitochondria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AMPA:

amino-3-hydroxy-5-methyl-4-isoxazole propionate

NMDA:

N-methyl-D-aspartate

PARP-1:

poly(ADP-ribose)-polymerase-1

ROS:

reactive oxygen species

References

  1. Vorob’ev, A. I. (1991) A Guidebook for Physician [in Russian], Meditsina, Moscow.

    Google Scholar 

  2. Rozen, V. B. (1984) in Principles of Endocrinology [in Russian], Vysshaya Shkola, Moscow, pp. 310–318.

    Google Scholar 

  3. Oomura, Y., Ooyama, H., Sugimori, M., Nakamura, T., and Yamada, Y. (1974) Nature, 247, 284–286.

    Article  PubMed  CAS  Google Scholar 

  4. Levin, B. E., Routh, V. H., Kang, L., Sanders, N. M., and Dunn-Meynell, A. A. (2004) Diabetes, 53, 2521–2528.

    Article  PubMed  CAS  Google Scholar 

  5. Yang, X. J., Kow, L. M., Pfaff, D. W., and Mobbs, C. V. (2004) Diabetes, 53, 67–73.

    Article  PubMed  CAS  Google Scholar 

  6. Davidson, M. (1999) in Endocrinology [Russian translation] (Lavin, N., ed.) Praktika, Moscow.

    Google Scholar 

  7. Delgado-Esteban, M., Almeida, A., and Bolanos, J. P. (2000) J. Neurochem., 75, 1618–1624.

    Article  PubMed  CAS  Google Scholar 

  8. Moley, K. H., and Mueckler, M. M. (2000) Apoptosis, 5, 99–105.

    Article  PubMed  CAS  Google Scholar 

  9. Satoskar, R. S., and Bandarkar, S. D. (1986) Pharmacology and Pharmacotherapy [in Russian], Meditsina, Moscow.

    Google Scholar 

  10. Monyer, H., Goldberg, M. P., and Choi, D. W. (1989) Brain Res., 483, 347–354.

    Article  PubMed  CAS  Google Scholar 

  11. Ashmarin, I. P., Stukalova, P. V., and Eshchenko, N. D. (1999) in Biochemistry of Brain [in Russian] (Ashmarin, I. P., Stukalova, P. V., and Eshchenko, N. D., eds.) St. Petersburg University Publishers, St. Petersburg, pp. 124–159.

    Google Scholar 

  12. Mark, R. J., Pang, Z., Geddes, J. W., Uchida, K., and Mattson, M. P. (1997) J. Neurosci., 17, 1046–1054.

    PubMed  CAS  Google Scholar 

  13. Hoyer, S. (2000) Exp. Gerontol., 35, 1363–1372.

    Article  PubMed  CAS  Google Scholar 

  14. Singh, P., Jain, A., and Kaur, G. (2004) Mol. Cell Biochem., 260, 153–159.

    Article  PubMed  CAS  Google Scholar 

  15. Keller, J. N., Pang, Z., Geddes, J. W., Begley, J. G., Germeyer, A., Waeg, G., and Mattson, M. P. (1997) J. Neurochem., 69, 273–284.

    Article  PubMed  CAS  Google Scholar 

  16. McDermott, E., and de Silva, P. (2005) Med. Hypotheses, 65, 1076–1081.

    Article  PubMed  CAS  Google Scholar 

  17. Raevskii, K. S., and Georgiev, V. P. (1986) Amino Acid Transmitters [in Russian], Meditsina, Moscow.

    Google Scholar 

  18. Watkins, J. C., and Olverman, H. J. (1987) Trends Neurosci., 10, 265–272.

    Article  CAS  Google Scholar 

  19. Young, A. B., and Fagg, G. E. (1990) TIPS, 11, 126–133.

    PubMed  CAS  Google Scholar 

  20. Stone, T. W., and Burton, N. R. (1988) Progr. Neurobiol., 30, 333–368.

    Article  CAS  Google Scholar 

  21. Choi, D. W. (1988) Trends Neurosci., 11, 465–469.

    Article  PubMed  CAS  Google Scholar 

  22. Manev, H., Favaron, M., Guidotti, A., and Costa, E. (1989) Mol. Pharmacol., 36, 106–112.

    PubMed  CAS  Google Scholar 

  23. Miller, B., Sarantis, M., Traynelis, F. S., and Attwell, D. (1992) Nature, 355, 722–725.

    Article  PubMed  CAS  Google Scholar 

  24. Isaev, N. K., Andreeva, N. A., Stel’mashuk, E. V., and Zorov, D. B. (2005) Biochemistry (Moscow), 70, 611–618.

    Article  CAS  Google Scholar 

  25. Benveniste, H., Drejer, J., Schousboe, A., and Diemer, N. H. (1984) J. Neurochem., 43, 1369–1374.

    Article  PubMed  CAS  Google Scholar 

  26. Silverstein, F. S., Buchanan, K., and Johnston, M. V. (1986) J. Neurochem., 47, 1614–1619.

    Article  PubMed  CAS  Google Scholar 

  27. Westerberg, E., Magnusson, K., Wieloch, T., Ungerstedt, U., Speciale, C., and Schwarcz, R. (1990) Acta Physiol. Scand., 138, 417–422.

    Article  PubMed  CAS  Google Scholar 

  28. Heyes, M. P., Papagapiou, M., Leonard, C., Markey, S. P., and Auer, R. N. (1990) J. Neurochem., 54, 1027–1033.

    Article  PubMed  CAS  Google Scholar 

  29. Ichord, R. N., Johnston, M. V., and Traystman, R. J. (2001) Brain Res. Dev. Brain Res., 128, 139–148.

    Article  PubMed  CAS  Google Scholar 

  30. Aral, Y. Z., Gucuyener, K., Atalay, Y., Hasanoglu, A., Turkyilmaz, C., Sayal, A., and Biberoglu, G. (1998) Acta Paediatr. Jpn., 40, 303–306.

    PubMed  CAS  Google Scholar 

  31. Hernandez-Fonseca, K., and Massieu, L. (2005) J. Neurosci. Res., 82, 196–205.

    Article  PubMed  CAS  Google Scholar 

  32. Honegger, P., Braissant, O., Henry, H., Boulat, O., Bachmann, C., Zurich, M. G., and Pardo, B. (2002) J. Neurochem., 81, 1141–1151.

    Article  PubMed  CAS  Google Scholar 

  33. Zeevalk, G. D., and Nicklas, W. J. (2000) J. Neurochem., 75, 1027–1034.

    Article  PubMed  CAS  Google Scholar 

  34. Madl, J. E., and Royer, S. M. (1999) Neuroscience, 94, 417–430.

    Article  PubMed  CAS  Google Scholar 

  35. Gundersen, V., Fonnum, F., Ottersen, O. P., and Storm-Mathisen, J. (2001) J. Cerebr. Blood Flow Metab., 21, 41–51.

    CAS  Google Scholar 

  36. Ioudina, M., Uemura, E., and Greenlee, H. W. (2004) Brain Res., 1004, 188–192.

    Article  PubMed  CAS  Google Scholar 

  37. Vergun, O., Han, Y. Y., and Reynolds, I. J. (2003) Exp. Neurol., 183, 682–694.

    Article  PubMed  CAS  Google Scholar 

  38. Suh, S. W., Aoyama, K., Chen, Y., Garnier, P., Matsumori, Y., Gum, E., Liu, J., and Swanson, R. A. (2003) J. Neurosci., 23, 10681–10690.

    PubMed  CAS  Google Scholar 

  39. Suh, S. W., Aoyama, K., Matsumori, Y., Liu, J., and Swanson, R. A. (2005) Diabetes, 54, 1452–1458.

    Article  PubMed  CAS  Google Scholar 

  40. Kauppinen, T. M., Chan, W. Y., Suh, S. W., Wiggins, A. K., Huang, E. J., and Swanson, R. A. (2006) Proc. Natl. Acad. Sci. USA 103, 7136–7141.

    Article  PubMed  CAS  Google Scholar 

  41. Suh, S. W., Garnier, P., Aoyama, K., Chen, Y., and Swanson, R. A. (2004) Neurobiol. Disease, 16, 538–545.

    Article  CAS  Google Scholar 

  42. Simon, R. P., Schmidley, J. W., Meldrum, B. S., Swan, J. H., and Chapman, A. G. (1986) Neuropathol. Appl. Neurobiol., 12, 567–576.

    PubMed  CAS  Google Scholar 

  43. Wieloch, T. (1985) Science, 230, 681–683.

    Article  PubMed  CAS  Google Scholar 

  44. Papagapiou, M. P., and Auer, R. N. (1990) J. Cerebr. Blood Flow Metab., 10, 270–276.

    CAS  Google Scholar 

  45. Tasker, R. C., Coyle, J. T., and Vornov, J. J. (1992) J. Neurosci., 12, 4298–4308.

    PubMed  CAS  Google Scholar 

  46. Facci, L., Leon, A., and Skaper, S. D. (1990) Neuroscience, 37, 709–716.

    Article  PubMed  CAS  Google Scholar 

  47. Monyer, H., Goldberg, M. P., and Choi, D. W. (1989) Brain Res., 483, 347–354.

    Article  PubMed  CAS  Google Scholar 

  48. Monyer, H., and Choi, D. W. (1990) J. Cerebr. Blood Flow Metab., 10, 337–342.

    CAS  Google Scholar 

  49. Rego, A. C., Santos, M. S., and Oliveira, C. R. (1999) Free Rad. Biol. Med., 26, 1405–1417.

    Article  PubMed  CAS  Google Scholar 

  50. Zhang, E. T., Hansen, A. J., Wieloch, T., and Lauritzen, M. (1990) J. Cerebr. Blood Flow Metab., 10, 136–139.

    CAS  Google Scholar 

  51. Zhu, P. J., and Krnjevic, K. (1993) Neurosci. Lett., 155, 128–131.

    Article  PubMed  CAS  Google Scholar 

  52. Calabresi, P., Centonze, D., Pisani, A., and Bernardi, G. (1997) J. Cerebr. Blood Flow Metab., 17, 1121–1126.

    CAS  Google Scholar 

  53. Turner, C. P., Blackburn, M. R., and Rivkees, S. A. (2004) J. Mol. Endocrinol., 32, 129–144.

    Article  PubMed  CAS  Google Scholar 

  54. Haas, H. L., and Selbach, O. (2000) Naunyn Schmiedebergs Arch. Pharmacol., 362, 375–381.

    Article  PubMed  CAS  Google Scholar 

  55. Kim, M., Yu, Z. X., Fredholm, B. B., and Rivkees, S. A. (2005) Am. J. Physiol. Endocrinol. Metab., 289, E562–E569.

    Article  PubMed  CAS  Google Scholar 

  56. Lobner, D. (2002) Neuroreport, 13, 2075–2078.

    Article  PubMed  CAS  Google Scholar 

  57. Kristian, T., Gido, G., and Siesjo, B. K. (1993) J. Cerebr. Blood Flow Metab., 13, 955–961.

    CAS  Google Scholar 

  58. Calabresi, P., Ascone, C. M., Centonze, D., Pisani, A., Sancesario, G., D’Angelo, V., and Bernardi, G. (1997) J. Neurosci., 17, 1940–1949.

    PubMed  CAS  Google Scholar 

  59. Uematsu, D., Greenberg, J. H., Reivich, M., and Karp, A. (1989) J. Cerebr. Blood Flow Metab., 9, 149–155.

    CAS  Google Scholar 

  60. Cheng, B., and Mattson, M. P. (1992) Exp. Neurol., 117, 114–123.

    Article  PubMed  CAS  Google Scholar 

  61. Mattson, M. P., Zhang, Y., and Bose, S. (1993) Exp. Neurol., 121, 1–13.

    Article  PubMed  CAS  Google Scholar 

  62. Walev, I., Reske, K., Palmer, M., Waleva, A., and Bhakdi, S. (1995) EMBO J., 14, 1607–1614.

    PubMed  CAS  Google Scholar 

  63. Yu, S. P., Yeh, C.-H., Strasser, U., Tian, M., and Coi, D. W. (1999) Science, 284, 336–339.

    Article  PubMed  CAS  Google Scholar 

  64. Bengtsson, F., Boris-Moller, F., Hansen, A. J., and Siesjo, B. K. (1990) J. Cerebr. Blood Flow Metab., 10, 262–269.

    CAS  Google Scholar 

  65. Auer, R. N. (2004) Metab. Brain Dis., 19, 169–175.

    Article  PubMed  Google Scholar 

  66. Pelligrino, D., Almquist, L. O., and Siesjo, B. K. (1981) Brain Res., 221, 129–147.

    Article  PubMed  CAS  Google Scholar 

  67. Honegger, P., Braissant, O., Henry, H., Boulat, O., Bachmann, C., Zurich, M. G., and Pardo, B. (2002) J. Neurochem., 81, 1141–1151.

    Article  PubMed  CAS  Google Scholar 

  68. Mellergard, P. (1993) Acid-Base Homeostasis in the Mammalian Brain, Lund, pp. 52–53.

  69. Larsen, G. A., Skjellegrind, H. K., Berg-Johnsen, J., Moe, M. C., and Vinje, M. L. (2006) Brain Res., 1077, 153–160.

    Article  PubMed  CAS  Google Scholar 

  70. Friberg, H., Ferrand-Drake, M., Bengtsson, F., Halestrap, A. P., and Wieloch, T. (1998) J. Neurosci., 18, 5151–5159.

    PubMed  CAS  Google Scholar 

  71. Ferrand-Drake, M., Zhu, C., Gido, G., Hansen, A. J., Karlsson, J. O., Bahr, B. A., Zamzami, N., Kroemer, G., Chan, P. H., Wieloch, T., and Blomgren, K. (2003) J. Neurochem., 85, 1431–1442.

    Article  PubMed  CAS  Google Scholar 

  72. Patockova, J., Marhol, P., Tumova, E., Krsiak, M., Rokyta, R., Stipek, S., Crkovska, J., and Andel, M. (2003) Physiol. Res., 52, 131–135.

    PubMed  CAS  Google Scholar 

  73. Hino, K., Nishikawa, M., Sato, E., and Inoue, M. (2005) Brain Res., 1053, 77–87.

    Article  PubMed  CAS  Google Scholar 

  74. Liu, Y., Song, X. D., Liu, W., Zhang, T. Y., and Zuo, J. (2003) J. Cell Mol. Med., 7, 49–56.

    Article  PubMed  CAS  Google Scholar 

  75. Isaev, N. K., Stel’mashuk, E. V., Belyaeva, E., and Zorov, D. B. (2005) Reception and Intracellular Signalization [in Russian], Pushchino, pp. 130–132.

  76. Lesnefsky, E. J., Moghaddas, S., Tandler, B., Kerner, J., and Hoppel, C. L. (2001) J. Mol. Cell Cardiol., 33, 1065–1089.

    Article  PubMed  CAS  Google Scholar 

  77. Wallace, D. C. (2000) Am. Heart J., 139, S70–S85.

    Article  PubMed  CAS  Google Scholar 

  78. McGowan, J. E., Chen, L., Gao, D., Trush, M., and Wei, C. (2006) Neurosci. Lett., 399, 111–114.

    Article  PubMed  CAS  Google Scholar 

  79. Ballesteros, J. R., Mishra, O. P., and McGowan, J. E. (2003) Biol. Neonate, 84, 159–163.

    Article  PubMed  CAS  Google Scholar 

  80. Liu, Y., Liu, W., Song, X. D., and Zuo, J. (2005) Mol. Cell. Biochem., 268, 45–51.

    Article  PubMed  CAS  Google Scholar 

  81. Zorov, D. B., Filburn, C. R., Klotz, L. O., Zweier, J. L., and Sollott, S. J. (2000) J. Exp. Med., 192, 1001–1014.

    Article  PubMed  CAS  Google Scholar 

  82. Zorov, D. B., Juhaszova, M., and Sollott, S. J. (2006) Biochim. Biophys. Acta, 1757, 509–517.

    Article  PubMed  CAS  Google Scholar 

  83. Brady, N. R., Hamacher-Brady, A., Westerhoff, H. V., and Gottlieb, R. A. (2006) Antiox. Redox Signal., 8, 651–665.

    Google Scholar 

  84. Chinopoulos, C., and Adam-Vizi, V. (2006) FEBS J., 273, 433–450.

    Article  PubMed  CAS  Google Scholar 

  85. Sensi, S. L., Yin, H. Z., Carriedo, S. G., Rao, S. S., and Weiss, J. H. (1999) Proc. Natl. Acad. Sci. USA, 96, 2414–2419.

    Article  PubMed  CAS  Google Scholar 

  86. Sensi, S. L., Ton-That, D., Sullivan, P. G., Jonas, E. A., Gee, K. R., Kaczmarek, L. K., and Weiss, J. H. (2003) Proc. Natl. Acad. Sci. USA, 100, 6157–6162.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119992, Moscow, Russia

    N. K. Isaev & D. B. Zorov

  2. Institute of Neurology, Russian Academy of Medical Sciences, Pereulok Obukha 5, 105064, Moscow, Russia

    N. K. Isaev & E. V. Stel’mashuk

Authors
  1. N. K. Isaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. V. Stel’mashuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. B. Zorov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. K. Isaev.

Additional information

Original Russian Text © N. K. Isoev, E. V. Stel’mashuk, D. B. Zorov, 2007, published in Biokhimiyo, 2007, Vol. 72, No. 5, pp. 586–595.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Isaev, N.K., Stel’mashuk, E.V. & Zorov, D.B. Cellular mechanisms of brain hypoglycemia. Biochemistry Moscow 72, 471–478 (2007). https://doi.org/10.1134/S0006297907050021

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297907050021

Key words

Search

Navigation