Skip to main content
Log in

Neuroglobin, an oxygen-binding protein in the mammalian nervous system (localization and putative functions)

  • Reviews
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

The review summarizes current data on neuroglobin, the heme-containing protein discovered in mammalian nerve cells in 2000. It presents general characteristics of neuroglobin as well as data on its evolutionary changes and expression across different taxa. Neuroglobin distribution in specific brain structures and outside the brain is described. The issue of the occurrence of neuroglobin not only in neurons but also in astroglial cells is discussed. Subcellular localization of neuroglobin is characterized with a special focus on its detection in the nucleus of nerve cells, suggesting its involvement in nuclear functions. Current ideas on the probable functional significance of neuroglobin are reported. Neuroglobin is presumed to be involved in metabolism of reactive nitrogen and oxygen species as well as in intracellular signaling pathways. Besides, neuroglobin has neuroprotective and antiapoptotic functions. Since its expression changes during ontogenesis, its neuroprotective role in ageing is specifically highlighted. Changes in expression and localization of neuroglobin are suggested to influence the adaptive potential of an organism.

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

Access this article

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

References

  1. Burmester, T., Weich, B., Reinhardt, S., and Hankeln, T., A vertebrate globin expressed in the brain, Nature, 2000, vol. 407, pp. 520–523.

    Article  CAS  PubMed  Google Scholar 

  2. Pesce, A., Dewide, S., Nardini, M., Moens, L., Ascenzi, P., Hankeln, T., Burmester, T., and Bolognesi, M., Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity, Structure, 2003, vol. 11, pp. 1087–1095.

    Article  CAS  PubMed  Google Scholar 

  3. Dewilde, S., Kiger, L., Burmester, T., Hankeln, T., Baudin-Creuza, V., Aerts, T., Marden, M.C., Caubergs, R., and Moens, L., Biochemical characterization and ligand-binding properties of neuroglobin, a novel member of the globin family, J. Biol. Chem., 2001, vol. 276, pp. 38 949–38 955.

    Article  CAS  Google Scholar 

  4. Vallone, B., Nienhaus, K., Matthes, A., Brunori, M., and Nienhaus, G.U., The structure of carbonmonoxy neuroglobin reveals a heme-sliding mechanism for control of ligand binding, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 17 351–17 356.

    Article  CAS  Google Scholar 

  5. Vallone, B., Nienhaus, K., Brunori, M., and Nienhaus, G.U., The structure of murine neuroglobin: Novel pathways for ligand migration and binding, Proteins, 2004, vol. 56, pp. 85–92.

    Article  CAS  PubMed  Google Scholar 

  6. Trent, J.T. III, Watts, R.A., and Hargrove, M.S., Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen, J. Biol. Chem., 2001, vol. 276, pp. 30 106–30 110.

    Article  CAS  Google Scholar 

  7. Kiger, L., Uzan, J., Dewilde, S., Burmester, T., Hankeln, T., Moens, L., Hamdane, D., Baudin-Creuza, V., and Marden, M., Neuroglobin ligand binding kinetics, IUBMB Life, 2004, vol. 56, pp. 709–719.

    Article  CAS  PubMed  Google Scholar 

  8. Burmester, T. and Hankeln, T., Function and evolution of vertebrate globins, Acta Physiol., 2014, vol. 211, pp. 501–514.

    Article  CAS  Google Scholar 

  9. Blank, M. and Burmester, T., Widespread occurrence of N-terminal acylation in animal globins and possible origin of respiratory globins from a membrane-bound ancestor, Mol. Biol. Evol., 2012, vol. 29, pp. 3553–3561.

    Article  CAS  PubMed  Google Scholar 

  10. Hoffmann, F.G., Opazo, J.C., Hoogewijs, D., Hankeln, T., Ebner, B., Vinogradov, S.N., Bailly, X., and Storz, J.F., Evolution of the globin gene family in deuterostomes: lineage-specific patterns of diversification and attrition, Mol. Biol. Evol., 2012, vol. 29, pp. 1735–1745.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Burmester, T., Haberkamp, M., Mitz, S., Roesner, A., Schmidt, M., Ebner, B., Gerlach, F., Fuchs, C., and Hankeln, T., Neuroglobin and cytoglobin: genes, proteins and evolution, IUBMB Life, 2004, vol. 56, no. 11–12 pp. 703–707.

    Article  CAS  PubMed  Google Scholar 

  12. Fuchs, C., Heib, V., Kiger, L., Haberkamp, M., Roesner, A., Schmidt, M., Hamdane, D., Marden, M.C., Hankeln, T., and Burmester, T., Zebrafish reveals different and conserved features of vertebrate neuroglobin gene structure, expression pattern and ligand binding, J. Biol. Chem., 2004, vol. 279, pp. 24 116–24 122.

    Article  CAS  Google Scholar 

  13. Schwarze, K. and Burmester, T., Conservation of globin genes in the “living fossil” Latimeria chalumnae and reconstruction of the evolution of the vertebrate globin family, Biochim. Biophys. Acta, 2013, vol. 1834, pp. 1801–1812.

    Article  CAS  PubMed  Google Scholar 

  14. Wystub, S., Ebner, B., Fuchs, C., Weich, B., Burmester, T., and Hankeln, T., Interspecies comparison of neuroglobin, cytoglobin and myoglobin: sequence evolution and candidate regulatory elements, Cytogenet. Genome Res., 2004, vol. 105, pp. 65–78.

    Article  CAS  PubMed  Google Scholar 

  15. Opazo, J.C., Lee, A.P., Hoffmann, F.G., Toloza-Villalobos, J., Burmester, T., Venkatesh, B., and Storz, J.F., Ancient Duplications and Expression Divergence in the Globin Gene Superfamily of Vertebrates: Insights from the Elephant Shark Genome and Transcriptome, Mol. Biol. Evol., 2015, vol. 32, no. 7 pp. 1684–1694.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hoffmann, F.G., Opazo, J.C., and Storz, J.F., Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 14 274–14 279.

    Article  CAS  Google Scholar 

  17. Awenius, C., Hankeln, T., and Burmester, T., Neuroglobins from the zebrafish Danio rerio and the pufferfish Tetraodon nigroviridis, Biochem. Biophys. Res. Commun., 2001, vol. 287, pp. 418–421.

    Article  CAS  PubMed  Google Scholar 

  18. Kugelstadt, D., Haberkamp, M., Hankeln, T., and Burmester, T., Neuroglobin, cytoglobin, and a novel, eye-specific globin from chicken, Biochem. Biophys. Res. Commun., 2004, vol. 325, pp. 719–725.

    Article  CAS  PubMed  Google Scholar 

  19. Roesner, A., Fuchs, C., Hankeln, T., and Burmester, T., A globin gene of ancient evolutionary origin in lower vertebrates: evidence for two distinct globin families in animals, Mol. Biol. Evol., 2005, vol. 22, pp. 12–20.

    Article  CAS  PubMed  Google Scholar 

  20. Wystub, S., Laufs, T., Schmidt, M., Burmester, T., Maas, U., Saaler-Reinhardt, S., Hankeln, T., and Reuss, S., Localisation of neuroglobin protein in the mouse brain, Neurosci. Lett., 2003, vol. 346, pp. 114–116.

    Article  CAS  PubMed  Google Scholar 

  21. Hundahl, C.A., Allen, G.C., Hannibal, J., Kjaer, K., Rehfeld, J.F., Dewilde, S., Nyengaard, J.R., Kelsen, J., and Hay-Schmidt, A., Anatomical characterization of cytoglobin and neuroglobin mRNA and protein expression in the mouse brain, Brain Res., 2010, vol. 1331, pp. 58–73.

    Article  CAS  PubMed  Google Scholar 

  22. Reuss, S., Saaler-Reinhardt, S., Weich, B., Wystub, S., Reuss, M., Burmester, T., and Hankeln, T., Expression analysis of neuroglobin mRNA in rodent tissues, Neuroscience, 2002, vol. 115, no. 3 pp. 645–656.

    Article  CAS  PubMed  Google Scholar 

  23. Mammen, P.P.A., Shelton, J.M., Goetsch, S.C., Williams, S.C., Richardson, J.A., Garry, M.G., and Garry, D.J., Neuroglobin, a novel member of the globin family, is expressed in focal regions of the brain, J. Histochem. Cytochem., 2002, vol. 50, pp. 1591–1598.

    Article  CAS  PubMed  Google Scholar 

  24. Grigor’ev, I.P., Gilerovich, E.G., Kirik, O.V., Vlasov, T.D., and Korzhevskii, D.E., Di stribution of neuroglobin in structures of rat neoncephalon after transitory ischemia, Asimmetriya, 2013, vol. 7, no. 1 pp. 15–21.

    Google Scholar 

  25. Hundahl, C.A., Allen, G.C., Nyengaard, J.R., Dewilde, S., Carter, B.D., Kelsen, J., and Hay-Schmidt, A., Neuroglobin in the rat brain: localization, Neuroendocrinol., 2008, vol. 88, no. 3 pp. 173–182.

    Article  CAS  Google Scholar 

  26. Sun, Y., Jin, K., Mao, X.O., Xie, L., Peel, A., Childs, J.T., Logvinova, A., Wang, X., and Greenberg, D.A., Effect of aging on neuroglobin expression in rodent brain, Neurobiol. Aging, 2005, vol. 26, no. 2 pp. 275–278.

    Article  CAS  PubMed  Google Scholar 

  27. Avivi, A., Gerlach, F., Joel, A., Reuss, S., Burmester, T., Nevo, E., and Hankeln, T., Neuroglobin, cytoglobin, and myoglobin contribute to hypoxia adaptation of the subterranean mole rat Spalax, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, no. 50 pp. 21 570–21 575.

    Article  CAS  Google Scholar 

  28. Hundahl, C.A., Kelsen, J., and Hay-Schmidt, A., Neuroglobin and cytoglobin expression in the human brain, Brain Struct. Funct., 2013, vol. 218, no. 2 pp. 603–609.

    Article  CAS  PubMed  Google Scholar 

  29. Gilerovich, E.G., Grigor’ev, I.P., Kirik, O.V., Alekseeva, O.S., Sukhorukova, E.G., and Korzhevskii, D.E., Distribution of neuroglobin in the human cerebellar cortex (an immunohistochemical study), Morfol., 2014, vol. 146, no. 4 pp. 75–77

    CAS  Google Scholar 

  30. Di Giulio, C., Zara, S., De Colli, M., Ruffini, R., Porzionato, A., Macchi, V., De Caro, R., and Cataldi, A., Cytoglobin and neuroglobin in the human brainstem and carotid body, Adv. Exp. Med. Biol., 2013, vol. 788, pp. 59–64.

    Article  PubMed  Google Scholar 

  31. Di Giulio, C., Zara, S., Cataldi, A., Porzionato, A., Pokorski, M., and De Caro, R., Human carotid body HIF and NGB expression during human development and aging, Adv. Exp. Med. Biol., 2012, vol. 758, pp. 265–271.

    Article  PubMed  Google Scholar 

  32. Vorasubin, N., Hosokawa, S., Hosokawa, K., Ishiyama, G., Ishiyama, A., and Lopez, I.A., Neuroglobin immunoreactivity in the human cochlea, Brain Res., 2016, vol. 1630, pp. 56–63.

    Article  CAS  PubMed  Google Scholar 

  33. Burmester, T. and Hankeln, T., What is the function of neuroglobin? J. Exp. Biol., 2009, vol. 212, pp. 1423–1428.

    Article  CAS  PubMed  Google Scholar 

  34. Schmidt, M., Giessl, A., Laufs, T., Hankeln, T., Wolfrum, U., and Burmester, T., How does the eye breathe? Evidence for neuroglobin-mediated oxygen supply in the mammalian retina, J. Biol. Chem., 2003, vol. 278, pp. 1932–1935.

    Article  CAS  PubMed  Google Scholar 

  35. Chan, A.S., Saraswathy, S., Rehak, M., Ueki, M., and Rao, N.A., Neuroglobin protection in retinal ischemia, Invest. Ophthalmol. Vis. Sci., 2012, vol. 53, no. 2 pp. 704–711.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Ostojic, J., Grozdanic, S.D., Syed, N.A., Hargrove, M.S., Trent, J.T. 3rd, Kuehn, M.H., Kwon, Y.H., Kardon, R.H., and Sakaguchi, D.S., Patterns of distribution of oxygen-binding globins, neuroglobin and cytoglobin in human retina, Arch. Ophthalmol., 2008, vol. 126, no. 11 pp. 1530–1536

    Article  CAS  PubMed  Google Scholar 

  37. Ostojic, J., Sakaguchi, D.S., de Lathouder, Y., Hargrove, M.S., Trent, J.T. 3rd, Kwon, Y.H., Kardon, R.H., Kuehn, M.H., Betts, D.M., and Grozdanic, S., Neuroglobin and cytoglobin: oxygen-binding proteins in retinal neurons, Invest. Ophthalmol. Vis. Sci., 2006, vol. 47, no. 3 pp. 1016–1023.

    Article  PubMed  Google Scholar 

  38. Kamioka, Y., Fujikawa, C., Ogai, K., Sugitani, K., Watanabe, S., Kato, S., and Wakasugi, K., Functional characterization of fish neuroglobin: zebrafish neuroglobin is highly expressed in amacrine cells after optic nerve injury and can translocate into ZF4 cells, Biochim. Biophys. Acta, 2013, vol. 1834, no. 9 pp. 1779–1788.

    Article  CAS  PubMed  Google Scholar 

  39. Boron, I., Russo, R., Boechi, L., Cheng, C.H., di Prisco, G., Estrin, D.A., Verde, C., and Nadra, A.D., Structure and dynamics of Antarctic fish neuroglobin assessed by computer simulations, IUBMB Life, 2011, vol. 63, no. 3 pp. 206–213.

    Article  CAS  PubMed  Google Scholar 

  40. Lechauve, C., Augustin, S., Roussel, D., Sahel, J.A., and Corral-Debrinski, M., Neuroglobin involvement in visual pathways through the optic nerve, Biochim. Biophys. Acta, 2013, vol. 1834, no. 9 pp. 1772–1778.

    Article  CAS  PubMed  Google Scholar 

  41. Ostojic, J., Grozdanic, S.D., Syed, N.A., Hargrove, M.S., Trent, J.T. 3rd, Kuehn, M.H., Kardon, R.H., Kwon, Y.H., and Sakaguchi, D.S., Neuroglobin and cytoglobin distribution in the anterior eye segment: a comparative immunohistochemical study, J. Histochem. Cytochem., 2008, vol. 56, no. 9 pp. 863–872.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Hundahl, C.A., Kelsen, J., Dewilde, S., and Hay-Schmidt, A., Neuroglobin in the rat brain (II): colocalisation with neurotransmitters, Neuroendocrinol., 2008, vol. 88, no. 3 pp. 183–198.

    Article  CAS  Google Scholar 

  43. Hankeln, T., Wystub, S., Laufs, T., Schmidt, M., Gerlach, F., Saaler-Reinhardt, S., Reuss, S., and Burmester, T., The cellular and subcellular localization of neuroglobin and cytoglobin—a clue to their function? IUBMB Life, 2004, vol. 56, pp. 671–679.

    Article  CAS  PubMed  Google Scholar 

  44. Laufs, T.L., Wystub, S., Reuss, S., Burmester, T., Saaler-Reinhardt, S., and Hankeln, T., Neuronspecific expression of neuroglobin in mammals, Neurosci. Lett., 2004, vol. 362, pp. 83–86.

    Article  CAS  PubMed  Google Scholar 

  45. Chen, X.Q., Qin, L.Y., Zhang, C.G., Yang, L.T., Gao, Z., Liu, S., Lau, L.T., Fung, Y.W., Greenberg, D.A., and Yu, A.C., Presence of neuroglobin in cultured astrocytes, Glia, 2005, vol. 50, no. 2 pp. 182–186.

    Article  PubMed  Google Scholar 

  46. Mitz, S.A., Reuss, S., Folkow, L.P., Blix, A.S., Ramirez, J.M., Hankeln, T., and Burmester, T., When the brain goes diving: glial oxidative metabolism may confer hypoxia tolerance to the seal brain, Neuroscience, 2009, vol. 163, no. 2 pp. 552–560.

    Article  CAS  PubMed  Google Scholar 

  47. Schneuer, M., Flachsbarth, S., Czech-Damal, N.U., Folkow, L.P., Siebert, U., and Burmester, T., Neuroglobin of seals and whales: evidence for a divergent role in the diving brain, Neuroscience, 2012, vol. 223, pp. 35–44.

    Article  CAS  PubMed  Google Scholar 

  48. Chen, X., Liu, Y., Zhang, L., Zhu, P., Zhu, H., Yang, Y., and Guan, P., Long-term neuroglobin expression of human astrocytes following brain trauma, Neurosci. Lett., 2015, vol. 606, pp. 194–199.

    Article  CAS  PubMed  Google Scholar 

  49. Hümmler, N., Schneider, C., Giessl, A., Bauer, R., Walkinshaw, G., Gassmann, M., Rascher, W., and Trollmann, R., Acute hypoxia modifies regulation of neuroglobin in the neonatal mouse brain, Exp. Neurol., 2012, vol. 236, no. 1 pp. 112–121.

    Article  PubMed  Google Scholar 

  50. Geuens, E., Brouns, I., Flamez, D., Dewilde, S., Timmermans, J.P., and Moens, L., A globin in the nucleus! J. Biol. Chem., 2003, vol. 278, pp. 30 417–30 420.

    Article  CAS  Google Scholar 

  51. Grigorev, I.P., Kirik, O.V., and Syrtsova, M.A., Neuroglobin in the rat hippocampus, 4th Int. Interdiscipl. Conf. “Modern problems in systemic regulation of physiological functions”, Moscow, September 17–18, 2015, pp. 171–173. DOI:10.12737/12327

    Google Scholar 

  52. Korzhevskii, D.E., Grigor’ev, I.P., Kirik, O.V., and Alekseeva, O.S., Neuroglobin distribution in the rat cerebellar Purkinje cells, J. Evol. Biochem. Physiol., 2015, vol. 51, no. 6 pp. 517–519.

    Article  Google Scholar 

  53. Kirik, O.V., Grigor’ev, I.P., Alekseeva, O.S., and Korzhevskii, D.E., Three-dimensional organization of the cytoplasmic neuroglobin-immunopositive structures in the rat brainstem neurons, Biol. Membr.: Zh. Membr. Klet. Biol., 2016, vol. 33, no. 3 pp. 207–212.

    CAS  Google Scholar 

  54. Lechauve, C., Augustin, S., Cwerman-Thibault, H., Bouaita, A., Forster, V., Célier, C., Rustin, P., Marden, M.C., Sahel, J.A., and Corral-Debrinski, M., Neuroglobin involvement in respiratory chain function and retinal ganglion cell integrity, Biochim. Biophys. Acta, 2012, vol. 1823, no. 12 pp. 2261–2273.

    Article  CAS  PubMed  Google Scholar 

  55. Liu, Z.F., Zhang, X., Qiao, Y.X., Xu, W.Q., Ma, C.T., Gu, H.L., Zhou, X.M., Shi, L., Cui, C.X., Xia, D., and Chen, Y.G., Neuroglobin protects cardiomyocytes against apoptosis and cardiac hypertrophy induced by isoproterenol in rats, Int. J. Clin. Exp. Med., 2015, vol. 8, no. 4 pp. 5351–5360.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Kuleva, N.V. and Krasovskaya, I.E., Role of heme-containing globins in NOsignaling in cells of vertebrates under hypoxia, Tsitol., 2015, vol. 57, no. 8 pp. 563–571.

    CAS  Google Scholar 

  57. Avella, G., Ardiccioni, C., Scaglione, A., Moschetti, T., Rondinelli, C., Montemiglio, L.C., Savino, C., Giuffrè, A., Brunori, M., and Vallone, B., Engineering the internal cavity of neuroglobin demonstrates the role of the haem-sliding mechanism, Acta Crystallogr. D. Biol. Crystallogr., 2014, vol. 70, pt. 6, pp. 1640–1648.

    Article  CAS  PubMed  Google Scholar 

  58. Li, R.C., Guo, S.Z., Lee, S.K., and Gozal, D., Neuroglobin protects neurons against oxidative stress in global ischemia, J. Cereb. Blood Flow Metab., 2010, vol. 30, pp. 1874–1882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Melgarejo-Gutiérrez, M., Acosta-Peña, E., Venebra-Muñoz, A., Escobar, C., Santiago-García, J., and Garcia-Garcia, F., Sleep deprivation reduces neuroglobin immunoreactivity in the rat brain, Neuroreport, 2013, vol. 24, no. 3 pp. 120–125.

    Article  PubMed  Google Scholar 

  60. Brunori, M., Giuffre, A., Nienhaus, K., Nienhaus, G.U., Scanclurra, F.M., and Vallone, B., Neuroglobin, nitric oxide and oxygen: functional pathways and conformational changes, Proc. Nat. Acad. Sci. USA, 2005, vol. 102, pp. 8483–8488.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Tiso, M., Tejero, J., Basu, S., Azarov, I., Wang, X., Simplaceanu, V., Frizzell, S., Jayaraman, T., Geary, L., Shapiro, C., Ho, C., Shiva, S., Kim-Shapiro, D.B., and Gladwin, M.T., Human neuroglobin functions as a redox-regulated nitrite reductase, J. Biol. Chem., 2011, vol. 286, pp. 18 277–18 289.

    Article  CAS  Google Scholar 

  62. Guidolin, D., Agnati, L.F., Tortorella, C., Marcoli, M., Maura, G., Albertin, G., and Fuxe, K., Neuroglobin as a regulator of mitochondrial-dependent apoptosis: a bioinformatics analysis, Int. J. Mol. Med., 2014, vol. 33, no. 1 pp. 111–116.

    Article  CAS  PubMed  Google Scholar 

  63. Raychaudhuri, S., Skommer, J., Henty, K., Birch, N., and Brittain, T., Neuroglobin protects nerve cells from apoptosis by inhibiting the intrinsic pathway of cell death, Apoptosis, 2010, vol. 15, no. 4 pp. 401–411.

    Article  CAS  PubMed  Google Scholar 

  64. Li, Y., Dai, Y.B., Sun, J.Y., Xiang, Y., Yang, J., Dai, S.Y., and Zhang, X., Neuroglobin attenuates beta amyloid-induced apoptosis through inhibiting caspases activity by activating PI3K/Akt signaling pathway, J. Mol. Neurosci., 2016, vol. 58, no. 1 pp. 28–38.

    Article  CAS  PubMed  Google Scholar 

  65. Ascenzi, P., Gustincich, S., and Marino, M., Mammalian nerve globins in search of functions, IUBMB Life, 2014, vol. 66, no. 4 pp. 268–276.

    Article  CAS  PubMed  Google Scholar 

  66. Lima, D.C., Cossa, A.C., Perosa, S.R., de Oliveira, E.M., da Silva, J.A., Jr, da Silva Fernandes, M.J., da Silva, I.R., Higa, E.M., da Graça Naffah-Mazzacoratti, M., Cavalheiro, E.A., and Amado, D., Neuroglobin is up-regulated in the cerebellum of pups exposed to maternal epileptic seizures, Int. J. Dev. Neurosci., 2011, vol. 29, no. 8 pp. 891–897.

    Article  CAS  PubMed  Google Scholar 

  67. Cai, B., Li, W., Mao, X., Winters, A., Ryou, M.G., Liu, R., Greenberg, D.A., Wang, N., Jin, K., and Yang, S.H., Neuroglobin Overexpression Inhibits AMPK Signaling and Promotes Cell Anabolism, Mol. Neurobiol., 2016, vol. 53, no. 2 pp. 1254–1265

    Article  CAS  PubMed  Google Scholar 

  68. Li, S.Q., Cao, X.D., Yu, D.S., and Li, Y., Effects of hypoxia preconditioning on serum NGB and S-100B in patients with intracranial aneurysm surgery, Sichuan Da Xue Xue Bao Yi Xue Ban, 2013, vol. 44, no. 5 pp. 747–751

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. S. Alekseeva.

Additional information

Original Russian Text © O.S. Alekseeva, I.P. Grigor’ev, D.E. Korzhevskii, 2017, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2017, Vol. 53, No. 4, pp. 221—229.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alekseeva, O.S., Grigor’ev, I.P. & Korzhevskii, D.E. Neuroglobin, an oxygen-binding protein in the mammalian nervous system (localization and putative functions). J Evol Biochem Phys 53, 249–258 (2017). https://doi.org/10.1134/S0022093017040019

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093017040019

Keywords

Navigation