About astroglia in the brain and pathology

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Abstract

More than 140 years astrocytes were described as passive cellular elements of the brain, and their function was limited participation in providing trophic potential of neurons. It was described as doctrine of “neuronism” which supported such famous scientists as H.W. von Waldeyer and S. Ramun y Cajal, who is the author of phrases “each nerve cell – a fully autonomous physiological canton”. During last time we can see a revision of views on the role of astrocytes in the brain. Astrocyte is equal partner of the neuron in such fundamental functions of the brain, as modulation of synaptic transmission, gliotransmission and regulation of microcirculation. Discovery of a new element of glia – NG2 cells, identification of the relationship between neuronal networks and astrocyte syncytium have changed the doctrine of neuronism. New paradigm revises the role of astroglia in the brain in health and disease.

 

About the authors

S. A. Goryaynov

N.N. Burdenko Institute of Neurosurgery, Russian Academy of Medical Sciences

Author for correspondence.
Email: sergey255@yandex.ru
Russian Federation, Moscow

S. V. Protsky

Research Center of Neurology, Russian Academy of Medical Sciences

Email: sergey255@yandex.ru
Russian Federation, Moscow

V. E. Okhotin

Institute of Gene Biology, RAS

Email: sergey255@yandex.ru
Russian Federation, Moscow

G. V. Pavlova

Institute of Gene Biology, RAS

Email: sergey255@yandex.ru
Russian Federation, Moscow

A. V. Revischin

Institute of Gene Biology, RAS

Email: sergey255@yandex.ru
Russian Federation, Moscow

A. A. Potapov

N.N. Burdenko Institute of Neurosurgery, Russian Academy of Medical Sciences

Email: sergey255@yandex.ru
Russian Federation, Moscow

References

  1. Белецкий В.К. Норма и патология мезоглии. Автореф. дисс. докт. мед. наук, Москва, 1933.
  2. Боголепов Н.Н. О роли глии при сосудистых поражениях головного мозга. В кн.: Вопросы сосудистой патологии головного и спинного мозга, 1964, вып. З. Кишинев; 33–40.
  3. Охотин В.Е., Калиниченко С.Г., Дудина Ю.В. NO-эргическая трансмиссия и NO как объемный трансмиттер. Эффекты оксида азота, механизмы синаптической пластичности и эпилептогенеза. Журн. Успехи физиологических наук 2002; апрель-июнь; 33(2): 41–55.
  4. Ройтбак А.И. В кн.: Глия и ее роль в нервной деятельности.Спб.: Наука, 1993.
  5. Alvarez-Buylla A., Lim D.A. For the long run: maintaining germinal niches in the adult brain. Neuron. 2004 Mar 4; 41 (5): 683–686.
  6. Alzheimer A. 1910 Beiträge zur Kenntnis der pathologischen Neuroglia und ihrer Be ziehungen zu den Abbauvorgängen im Nervengewebe. In: Nissl, F., Alzheimer, A. (Eds.). Histologische und histopathologische Arbeiten über die Grosshirnrinde mit besonderer Berücksichtigung der pathologischen Anatomie der Geisteskrankheiten. Gustav Fischer, Jena, pp. 401–562.
  7. Alonso-Galicia M., Hudetz A.G., Shen H. et al. Contribution of 20-HETE to vasodilator actions of nitric oxide in the cerebral microcirculation. 1999. Stroke 30: 2727–2734,
  8. Anderson C.M., Nedergaard M. Astrocyte-mediated control of cerebral microcirculation. Trends Neurosci. 2003 Jul; 26 (7): 340–344; author reply 344–345.
  9. Andriezen W.L., 1893. The neuroglia elements of the brain. Br. Med. J. 2, 227–230.
  10. Araque A., Martín E.D., Perea G., Arellano J.I. et al. Synaptically released acetylcholine evokes Ca2+ elevations in astrocytes in hippocampal slices. J Neurosci. 2002 Apr 1;22(7):2443-50.
  11. Araque A., Parpura V., Sanzgiri R.P., Haydon P.G. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 1999 May; 22 (5): 208–215.
  12. Araque A. Astrocytes process synaptic information. Neuron Glia Biol. 2008 Feb; 4 (1): 3–10. Epub 2009 Feb 27.
  13. Behrens P.F., Franz P., Woodman B. et al. Impaired glutamate transport and glutamate-glutamine cycling: downstream effects of the Huntington mutation. 2002 Brain 125 (Pt 8): 1908–1922.
  14. Beschorner R., Dietz K., Schauer N. et al. Expression of EAAT1 reflects a possible neuroprotective function of reactive astrocytes and activated microglia following human traumatic brain injury. 2007 Histol Histopathol 22 (5): 515–526.
  15. Bilban M., Haschemi A., Wegiel B. et al. Heme oxygenase and carbon monoxide initiate homeostatic signaling. 2008 J Mol Med 86 (3):267–279.
  16. Burnstock G. Purinergic signalling: past, present and future. Braz J Med Biol Res 2009 42 (1): 3–8.
  17. Chvátal A., Anderová M., Neprasová H., Prajerová I. et al.Pathological potential of astroglia. Physiol Res. 2008;57 Suppl 3:S101-10. Epub 2008 May 13.
  18. D’Ambrosio R. Does glutamate released by astrocytes cause focal epilepsy? Epilepsy Curr. 2006 Sep-Oct; 6 (5): 173–176.
  19. De Keyser J., Mostert J.P., Koch M.W. Dysfunctional astrocytes as key players in the pathogenesis of central nervous system disorders. J Neurol Sci. 2008 Apr 15; 267 (1–2): 3–16. Epub 2007 Nov 1.
  20. Deiters, O., 1865. Untersuchungen über Gehirn und Rückenmark des Menschen und der Säugethiere. Vieweg, Braunschweig.
  21. Dora K.A. Does arterial myogenic tone determine blood flow distribution in vivo? Am J Physiol Heart Circ Physiol. 2005 Oct; 289 (4): H1323–5.
  22. Frommann C., 1878. Untersuchungen über die Gewebsveränderungen bei der Multiplen Sklerose des Gehirns und Rückenmarks. Verlag von Gustav Fischer, Jena.
  23. Giaume C., Kirchhoff F., Matute C. et al. Glia: the fulcrum of brain diseases. Cell Death Differ. 2007 Jul; 14 (7): 1324–1335.
  24. Girvin A.M., Gordon K.B., Welsh C.J., Clipstone N.A. et al. Differential abilities of central nervous system resident endothelial cells and astrocytes to serve as inducible antigen-presenting cells. Blood. 2002 May 15; 99 (10): 3692–3701.
  25. Halassa M.M., Fellin T., Haydon P.G. The tripartite synapse: roles for gliotransmission in health and disease. 2007 Trends Mol Med 13 (2): 54–63.
  26. Haydon P.G. Glia: listening and talking to the synapse. Nat. Rev. 2001 Neurosci 2: 185–193.
  27. Haydon P.G., Carmignoto G. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev. 2006 Jul; 86 (3):1009–1031.
  28. Haydon P.G., Blendy J., Moss S.J., Rob Jackson F. Astrocytic control of synaptic transmission and plasticity: a target for drugs of abuse? 2009 Neuropharmacology 56 Suppl 1: 83–90.
  29. Hazell A.S., Sheedy D., Oanea R. et al. Loss of astrocytic glutamate transporters in Wernicke encephalopathy. Glia. 2009 Jun 29. [Epub ahead of print].
  30. Henle J., Merkel, F., 1869. Uber die sogenannte Bindesubstanz der Centralorgane des Nervensystems. Z. Med. 34, 49–82.
  31. Hertz L., Gibbs M.E. What learning in day-old chickens can teach a neurochemist: focus on astrocyte metabolism. J Neurochem. 2009 May; 109 Suppl 1:10–16.
  32. Hertz L., Dringen R., Schousboe A., Robinson S.R. Astrocytes: glutamate producers for neurons. J. Neurosci Res. 1999 Aug 15; 57 (4):417–428.
  33. Hooke R. 1665. Micrographia: or, some physiological descriptions of minute bodies made by magnifying glasses. London: J. Martyn and J. Allestry.
  34. Iadecola C., Ross M.E. Molecular pathology of cerebral ischemia: delayed gene expression and strategies for neuroprotection. Ann N Y Acad Sci. 1997 Dec 19; 835: 203–217.
  35. Iadecola C., Nedergaard M. Glial regulation of the cerebral microvasculature. Nat Neurosci. 2007 Nov; 10 (11): 1369–1376.
  36. Iliff J.J., Wang R., Zeldin D.C., Alkayed N.J. Epoxyeicosanoids as mediators of neurogenic vasodilation in cerebral vessels. J Physiol Heart Circ Physiol. 2009 May; 296 (5): H1352–63.
  37. Kölliker A., 1893. Handbuch der Gewebelchre des menschen. Wilhelm Engelmann, Leipzig.
  38. Krawczyk A., Jaworska-Adamu J. Synantocytes: the fifth type of glia? In comparison with astrocytes. Folia Histochem Cytobiol. 2010 Jan; 48 (2): 173–177.
  39. Kumar N.M., Gilula N.B. The gap junction communication channel.Cell. 1996 Feb 9; 84 (3): 381–388.
  40. Largo C., Cuevas P., Herreras O. Is glia disfunction the initial cause of neuronal death in ischemic penumbra? Neurol Res. 1996 Oct; 18 (5):445–448.
  41. Lee W., Parpura V. Micropatterned substrates for studying astrocytes in culture. Front Neurosci. 2009 Dec 15; 3 (3): 381–387.
  42. Lenhosek M.V., 1891. Zur Kenntnis der Neuroglia des menschlichen Ruckenmarkes. Verh. Anat. Ges. 5, 193–221.
  43. Li L., Lundkvist A., Andersson D. et al. Protective role of reactive astrocytes in brain ischemia. 2008 J Cereb Blood Flow Metab 28 (3):468–481.
  44. Liauw J., Hoang S., Choi M. et al. Thrombospondins 1 and 2 are necessary for synaptic plasticity and functional recovery after stroke. J Cereb Blood Flow Metab. 2008 Oct; 28 (10): 1722–1732. Epub 2008 Jul 2.
  45. Maragakis N.J., Rothstein J.D. Glutamate transporters: animal models to neurologic disease. 2008 Neurobiol Dis 15: 461–473.
  46. Martineau M., Baux G., Mothet J.P. Gliotransmission at central glutamatergic synapses: D-serine on stage. 2006 J Physiol Paris 99 (2–3): 103–110.
  47. McKenzie J.C., Juan Y.W., Thomas C.R. et al. Atrial natriuretic peptide-like immunoreactivity in neurons and astrocytes of human cerebellum and inferior olivary complex. J. Histochem Cytochem. 2001 Nov;49 (11): 1453–1467.
  48. Metea M.R., Newman E.A. Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci. 2006 Mar 15; 26 (11): 2862–2870.
  49. Mosso A. Sulla circolazione del sangue nel cervello delluomo, Roma, 1880.
  50. Mustafa A.K., Gadalla M.M., Snyder S.H. Signaling by gasotransmitters. 2009 Sci Signal 2 (68): re2.
  51. Nakagomi T., Taguchi A., Fujimori Y. et al. Isolation and characterization of neural stem/progenitor cells from post-stroke cerebral cortex in mice. Eur J Neurosci. 2009 May; 29 (9): 1842–1852. Epub 2009 Apr 17.
  52. Nagele R.G., Wegiel J., Venkataraman V. et al. Contribution of glial cells to the development of amyloid plaques in Alzheimer’s disease. Neurobiol Aging. 2004 May-Jun; 25 (5): 663–674.
  53. Nedergaard M., Ransom B., Goldman S.A. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 2003 Oct; 26 (10): 523–530.
  54. Nedergaard M., Takano T., Hansen A.J. Beyond the role of glutamate as a neurotransmitter. Nat Rev Neurosci. 2002 Sep; 3 (9): 748–755.
  55. Newman E.A. New roles for astrocytes: regulation of synaptic transmission. 2003 Trends Neurosci. 26 (10): 536–542.
  56. Nicholls D., Attwell D. The release and uptake of excitatory amino acids. 1990. Trends Pharmacol Sci 11: 462–468.
  57. Nicholls J.G., Martin A.R., Wallace B.G. et al. From Neuron to Brain, Fifth Edition, Sunderland, Massachusetts 2001.
  58. Nishiyama A. Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist. 2007 Feb; 13 (1): 62–76.
  59. Nissl F., 1899. Ueber einige Beziehungen zwischen Nervenzellerkrankungen und gliiSsen Erscheinungen bei verschiedenen Psychosen. Arch. Psychiat. 32, 1–21.Niwa et al., 2000.
  60. Oberheim N.A., Takano T., Han X. et al. Uniquely hominid features of adult human astrocytes. J Neurosci. 2009 Mar 11; 29 (10): 3276–3287.
  61. Pangrsic T., Potokar M., Stenovec M. et al. Exocytotic release of ATP from cultured astrocytes. 2007 J Biol Chem. 282 (39): 28749–28758.
  62. Parpura V., Zorec R. Gliotransmission: Exocytotic release from astrocytes. Brain Res Rev. 2010 May; 63 (1–2): 83–92. Epub 2009 Dec 4.
  63. Pekny M., Nilsson M. Astrocyte activation and reactive gliosis. Glia. 2005 Jun; 50 (4): 427–434.
  64. Pfrieger F.W., Barres B.A. New views on synapse-glia interactions. Curr Opin Neurobiol. 1996 Oct; 6 (5): 615–621.
  65. Pfrieger F.W., Barres B.A. Synaptic efficacy enhanced by glial cells in vitro. Science. 1997 Sep 12; 277 (5332): 1684–1687.
  66. Purkinje J.E., 1837. Neueste Beobachtungen uber die Struktur des Gehirns. Opera Omnia.
  67. Qu K., Lee S.W., Bian J.S. et al. Hydrogen sulfide: neurochemistry and neurobiology. 2008 Neurochem Int 52 (1–2): 155–165.
  68. Ramуn y Cajal S., 1920. Algunas consideraciones sobre la mesoglia de Robertson y Rio-Hortega. Trab. Lab. Invest. Biol. Univ. Madrid 18,109–127.
  69. Cajal Ramon. Contribucion al conocimiento de la neuroglia del cerebro humano. 1913 Trab Lab Invest Biol 11, 255–315.
  70. Rebel A., Koehler R.C., Martin L.J. In situ immunoradiographic method for quantification of specific proteins in normal and ischemic brain regions. 2005 J. Neurosci Methods 143: 227–235.
  71. Rossi D.J., Oshima T., Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. 2000 Nature 403: 316–321.
  72. Schipke C.G., Kettenmann H. Astrocyte responses to neuronal activity. Glia. 2004 Aug 15; 47 (3): 226–232.
  73. Scolari M.J., Acosta G.B. D-serine: a new word in the glutamatergic neuro-glial language. 2007 Amino Acids 33 (4): 563–574.
  74. Sherwood C.C., Stimpson C.D., Raghanti M.A. et al. Evolution of increased glia-neuron ratios in the human frontal cortex. Proc Natl Acad Sci U S A. 2006 Sep 12; 103 (37): 13606–13611. Epub 2006 Aug 28.
  75. Simard M., Nedergaard M. The neurobiology of glia in the context of water and ion homeostasis. Neuroscience. 2004; 129 (4): 877–896.
  76. Struzynska L. A glutamatergic component of lead toxicity in adult brain: the role of astrocytic glutamate transporters. Neurochem Int. 2009 Jul-Aug; 55 (1–3): 151–156.
  77. Tian G.F., Azmi H., Takano T. et al. An astrocytic basis of epilepsy. Nat Med. 2005 Sep; 11 (9): 973–981. Epub 2005 Aug 14.
  78. Umemura K., Kimura H. Hydrogen sulfide enhances reducing activity in neurons: neurotrophic role of H2S in the brain? Antioxid Redox Signal 2007 9 (11): 2035–2041.
  79. Verkhratsky A., Parpura V. Recent advances in (patho)physiology of astroglia. Acta Pharmacol Sin. 2010 Sep; 31 (9): 1044–1054. Epub 2010 Aug 9.
  80. Verkhratsky A., Parpura V., Rodrнguez J.J. Where the thoughts dwell: the physiology of neuronal-glial «diffuse neural net». Brain Res Rev. 2011 Jan 7; 66 (1-2): 133–51. Epub 2010 Jun 9.
  81. Verkhratsky A., Toescu E.C. Neuronal-glial networks as substrate for CNS integration. J Cell Mol Med. 2006 Oct-Dec; 10 (4): 826–836.
  82. Verkhratsky A., Steinhöuser C. Ion channels in glial cells. Brain Res Brain Res Rev. 2000 Apr; 32 (2-3): 380–412.
  83. Virchow R., 1856. Gesammelte Abhandlungen zyrwissenschaftlischen Medizin. Verlag von Meidinger Sohn & Comp, Frankfurt.
  84. Webster H., Aström K.E. Gliogenesis: historical perspectives, 1839-1985. Adv Anat Embryol Cell Biol. 2009; 202: 1–109.
  85. Wigley R., Hamilton N., Nishiyama A. et al. Morphological and physiological interactions of NG2-glia with astrocytes and neurons. J Anat. 2007 Jun; 210 (6): 661–670. Epub 2007 Apr 25.
  86. Wolosker H., Blackshaw S., Snyder S.H. Serine racemase: a glial enzyme synthesizing D-serine to regulate glutamate-N-methyl-Daspartate neurotransmission.Proc Natl Acad Sci U S A. 1999 Nov 9; 96 (23): 13409–13414.
  87. Zonta M., Angulo M.C., Gobbo S. et al. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. 2003 Nat Neurosci 6: 43–50.

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Copyright (c) 2013 Goryaynov S.A., Protsky S.V., Okhotin V.E., Pavlova G.V., Revischin A.V., Potapov A.A.

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