Multimedialna platforma wiedzy medycznej Internetowa Księgarnia Medyczna Kalendarium Konferencji
Folia Morphologica
MENU
Shortcuts Submit an article Author Guidelines (new) Ahead Of Print Reviewers 2023

open access

Vol 80, No 4 (2021)
Review article
Submitted: 2021-09-27
Accepted: 2021-09-29
Published online: 2021-10-21
View PDF Download PDF file
Get Citation

Neuroglia — development and role in physiological and pathophysiological processes

M. Cichorek1, P. Kowiański2, G. Lietzau2, J. Lasek1, J. Moryś3
DOI: 10.5603/FM.a2021.0109
·
Pubmed: 34699052
·
Folia Morphol 2021;80(4):766-775.
Affiliations
  1. Department of Anatomy and Physiology, Pomeranian University of Słupsk, Poland
  2. Department of Anatomy and Neurobiology, Faculty of Medicine, Medical University of Gdansk, Poland
  3. Department of Normal Anatomy, Pomeranian Medical University, Szczecin, Poland

open access

Vol 80, No 4 (2021)
REVIEW ARTICLES
Submitted: 2021-09-27
Accepted: 2021-09-29
Published online: 2021-10-21

Abstract

The dynamic development of studies on neuroglia in recent years indicates its previously underestimated role in maintaining proper brain function, both in physiological and pathological conditions. The use of modern research methods such as single-cell techniques as well as in vivo and in vitro models enriched the state of our knowledge. The most important issues regarding the maturation and development of neuroglia include cooperation between glial cell groups and with neurons in neurogenesis, neuroregeneration, (re)myelination and how the early developmental roles of glia contribute to nervous system dysfunction in neurodevelopmental and neurodegenerative disorders.
There is still growing evidence emphasizing the importance of astroglia in maintaining the brain physiological homeostasis, regulation of immune response, cerebral blood flow, and involvement in the reactive neurogliosis, precisely adapted to the nature of pathological stimulus and the depth of tissue damage. The important issues related to the function of oligodendrocytes include explanation of the mechanisms of interaction between the glial cells and myelinated axons, important not only in myelination, but also in development of cognitive processes and memory. Further studies are required for understanding the mechanisms of demyelination occurring in several central nervous system (CNS) diseases. An interesting area of research is related with explanation of the NG2 glia function, characterised by significant proliferative potential and ability to differentiate in both in physiological conditions and in pathology, as well as the presence of synaptic neural-glial connections, which are especially numerous during development. The increasing knowledge of microglia comprises the presence of specialised subsets of microglia, their role the myelination process and neurovascular unit functioning. We are only beginning to understand how microglia enter the brain and develop distinct functional states during ontogeny.
This review summarises the current state of knowledge on the development and role in the CNS of different, heterogeneous cell populations defined by a common term neuroglia.

Abstract

The dynamic development of studies on neuroglia in recent years indicates its previously underestimated role in maintaining proper brain function, both in physiological and pathological conditions. The use of modern research methods such as single-cell techniques as well as in vivo and in vitro models enriched the state of our knowledge. The most important issues regarding the maturation and development of neuroglia include cooperation between glial cell groups and with neurons in neurogenesis, neuroregeneration, (re)myelination and how the early developmental roles of glia contribute to nervous system dysfunction in neurodevelopmental and neurodegenerative disorders.
There is still growing evidence emphasizing the importance of astroglia in maintaining the brain physiological homeostasis, regulation of immune response, cerebral blood flow, and involvement in the reactive neurogliosis, precisely adapted to the nature of pathological stimulus and the depth of tissue damage. The important issues related to the function of oligodendrocytes include explanation of the mechanisms of interaction between the glial cells and myelinated axons, important not only in myelination, but also in development of cognitive processes and memory. Further studies are required for understanding the mechanisms of demyelination occurring in several central nervous system (CNS) diseases. An interesting area of research is related with explanation of the NG2 glia function, characterised by significant proliferative potential and ability to differentiate in both in physiological conditions and in pathology, as well as the presence of synaptic neural-glial connections, which are especially numerous during development. The increasing knowledge of microglia comprises the presence of specialised subsets of microglia, their role the myelination process and neurovascular unit functioning. We are only beginning to understand how microglia enter the brain and develop distinct functional states during ontogeny.
This review summarises the current state of knowledge on the development and role in the CNS of different, heterogeneous cell populations defined by a common term neuroglia.

Full Text:

View PDF Download PDF file
Get Citation

Keywords

astrocytes, microglia, NG2 cells, neurovascular unit, oligodendrocytes

About this article
Title

Neuroglia — development and role in physiological and pathophysiological processes

Journal

Folia Morphologica

Issue

Vol 80, No 4 (2021)

Article type

Review article

Pages

766-775

Published online

2021-10-21

Page views

7423

Article views/downloads

1485

DOI

10.5603/FM.a2021.0109

Pubmed

34699052

Bibliographic record

Folia Morphol 2021;80(4):766-775.

Keywords

astrocytes
microglia
NG2 cells
neurovascular unit
oligodendrocytes

Authors

M. Cichorek
P. Kowiański
G. Lietzau
J. Lasek
J. Moryś

References (101)
  1. Abbott NJ, Patabendige AAK, Dolman DEM, et al. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010; 37(1): 13–25.
    CrossRefPubMed
  2. Anderson MA, Ao Y, Sofroniew MV. Heterogeneity of reactive astrocytes. Neurosci Lett. 2014; 565: 23–29.
    CrossRefPubMed
  3. Araque A, Parpura V, Sanzgiri RP, et al. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 1999; 22(5): 208–215.
    CrossRefPubMed
  4. Benmamar-Badel A, Owens T, Wlodarczyk A. Protective microglial subset in development, aging, and disease: lessons from transcriptomic studies. Front Immunol. 2020; 11: 430.
    CrossRefPubMed
  5. Bennett ML, Bennett FC, Liddelow SA, et al. New tools for studying microglia in the mouse and human CNS. Proc Natl Acad Sci U S A. 2016; 113(12): E1738–E1746.
    CrossRefPubMed
  6. Bergles DE, Jabs R, Steinhäuser C. Neuron-glia synapses in the brain. Brain Res Rev. 2010; 63(1-2): 130–137.
    CrossRefPubMed
  7. Bernstein HG, Keilhoff G, Dobrowolny H, et al. Perineuronal oligodendrocytes in health and disease: the journey so far. Rev Neurosci. 2019; 31(1): 89–99.
    CrossRefPubMed
  8. Bian Z, Gong Y, Huang T, et al. Deciphering human macrophage development at single-cell resolution. Nature. 2020; 582(7813): 571–576.
    CrossRefPubMed
  9. Böttcher C, Schlickeiser S, Sneeboer MAM, et al. Human microglia regional heterogeneity and phenotypes determined by multiplexed single-cell mass cytometry. Nat Neurosci. 2019; 22(1): 78–90.
    CrossRefPubMed
  10. Bramanti V, Tomassoni D, Avitabile M, et al. Biomarkers of glial cell proliferation and differentiation in culture. Front Biosci (Schol Ed). 2010; 2: 558–570.
    CrossRefPubMed
  11. Buffo A, Rite I, Tripathi P, et al. Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A. 2008; 105(9): 3581–3586.
    CrossRefPubMed
  12. Buffo A, Rolando C, Ceruti S. Astrocytes in the damaged brain: molecular and cellular insights into their reactive response and healing potential. Biochem Pharmacol. 2010; 79(2): 77–89.
    CrossRefPubMed
  13. Burda JE, Sofroniew MV. Reactive gliosis and the multicellular response to CNS damage and disease. Neuron. 2014; 81(2): 229–248.
    CrossRefPubMed
  14. Butt A, Verkhratsky A. Neuroglia: Realising their true potential. Brain Neurosci Adv. 2018; 2: 2398212818817495.
    CrossRefPubMed
  15. Butt AM, Fern RF, Matute C. Neurotransmitter signaling in white matter. Glia. 2014; 62(11): 1762–1779.
    CrossRefPubMed
  16. Butt AM, Hamilton N, Hubbard P, et al. Synantocytes: the fifth element. J Anat. 2005; 207(6): 695–706.
    CrossRefPubMed
  17. Butt AM, Ibrahim M, Berry M. Axon-myelin sheath relations of oligodendrocyte unit phenotypes in the adult rat anterior medullary velum. J Neurocytol. 1998; 27(4): 259–269.
    PubMed
  18. Butt AM, Kalsi A. Inwardly rectifying potassium channels (Kir) in central nervous system glia: a special role for Kir4.1 in glial functions. J Cell Mol Med. 2006; 10(1): 33–44.
    CrossRefPubMed
  19. Carlson BM. Nervous system. In human embriology and develomental biology. 6th ed. Elsevier, Philadelphia 2019: 216–235.
  20. Carmignoto G, Gómez-Gonzalo M. The contribution of astrocyte signalling to neurovascular coupling. Brain Res Rev. 2010; 63(1-2): 138–148.
    CrossRefPubMed
  21. Czuba E, Steliga A, Lietzau G, et al. Cholesterol as a modifying agent of the neurovascular unit structure and function under physiological and pathological conditions. Metab Brain Dis. 2017; 32(4): 935–948.
    CrossRefPubMed
  22. De Biase LM, Nishiyama A, Bergles DE. Excitability and synaptic communication within the oligodendrocyte lineage. J Neurosci. 2010; 30(10): 3600–3611.
    CrossRefPubMed
  23. Dimou L, Gallo V. NG2-glia and their functions in the central nervous system. Glia. 2015; 63(8): 1429–1451.
    CrossRefPubMed
  24. Dimou L, Simon C, Kirchhoff F, et al. Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci. 2008; 28(41): 10434–10442.
    CrossRefPubMed
  25. Dringen R, Brandmann M, Hohnholt MC, et al. Glutathione-dependent detoxification processes in astrocytes. Neurochem Res. 2015; 40(12): 2570–2582.
    CrossRefPubMed
  26. Escartin C, Galea E, Lakatos A, et al. Reactive astrocyte nomenclature, definitions, and future directions. Nat Neurosci. 2021; 24(3): 312–325.
    CrossRefPubMed
  27. Frade J, Pope S, Schmidt M, et al. Glutamate induces release of glutathione from cultured rat astrocytes--a possible neuroprotective mechanism? J Neurochem. 2008; 105(4): 1144–1152.
    CrossRefPubMed
  28. Franklin R, Gilson J, Blakemore W. Local recruitment of remyelinating cells in the repair of demyelination in the central nervous system. J Neurosci Res. 1997; 50(2): 337–344, doi: 10.1002/(sici)1097-4547(19971015)50:2<337::aid-jnr21>3.0.co;2-3.
    PubMed
  29. Fröhlich N, Nagy B, Hovhannisyan A, et al. Fate of neuron-glia synapses during proliferation and differentiation of NG2 cells. J Anat. 2011; 219(1): 18–32.
    CrossRefPubMed
  30. Giotakos O. Is psychosis a dysmyelination-related information-processing disorder? Psychiatriki. 2019; 30(3): 245–255.
    CrossRefPubMed
  31. Girouard H, Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol (1985). 2006; 100(1): 328–335.
    CrossRefPubMed
  32. Goldmann T, Wieghofer P, Jordão MJ, et al. Origin, fate and dynamics of macrophages at central nervous system interfaces. Nat Immunol. 2016; 17(7): 797–805.
    CrossRefPubMed
  33. Hackett AR, Yahn SL, Lyapichev K, et al. Injury type-dependent differentiation of NG2 glia into heterogeneous astrocytes. Exp Neurol. 2018; 308: 72–79.
    CrossRefPubMed
  34. Halassa MM, Fellin T, Haydon PG. Tripartite synapses: roles for astrocytic purines in the control of synaptic physiology and behavior. Neuropharmacology. 2009; 57(4): 343–346.
    CrossRefPubMed
  35. Hanisch UK. Functional diversity of microglia - how heterogeneous are they to begin with? Front Cell Neurosci. 2013; 7: 65.
    CrossRefPubMed
  36. Henneke P, Kierdorf K, Hall LJ, et al. Perinatal development of innate immune topology. Elife. 2021; 10.
    CrossRefPubMed
  37. Honsa P, Pivonkova H, Dzamba D, et al. Polydendrocytes display large lineage plasticity following focal cerebral ischemia. PLoS One. 2012; 7(5): e36816.
    CrossRefPubMed
  38. Honsa P, Valny M, Kriska J, et al. Generation of reactive astrocytes from NG2 cells is regulated by sonic hedgehog. Glia. 2016; 64(9): 1518–1531.
    CrossRefPubMed
  39. Hsuan YCY, Lin CH, Chang CP, et al. Mesenchymal stem cell-based treatments for stroke, neural trauma, and heat stroke. Brain Behav. 2016; 6(10): e00526.
    CrossRefPubMed
  40. Hughes EG, Kang SH, Fukaya M, et al. Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat Neurosci. 2013; 16(6): 668–676.
    CrossRefPubMed
  41. Iadecola C. The neurovascular unit coming of age: a journey through neurovascular coupling in health and disease. Neuron. 2017; 96(1): 17–42.
    CrossRefPubMed
  42. Kana V, Desland F, Casanova-Acebes M, et al. CSF-1 controls cerebellar microglia and is required for motor function and social interaction. J Exp Med. 2019; 216(10): 2265–2281.
    CrossRefPubMed
  43. Khakh BS, Deneen B. The emerging nature of astrocyte diversity. Annu Rev Neurosci. 2019; 42: 187–207.
    CrossRefPubMed
  44. Khakh BS, Sofroniew MV. Diversity of astrocyte functions and phenotypes in neural circuits. Nat Neurosci. 2015; 18(7): 942–952.
    CrossRefPubMed
  45. Khoshnam SE, Winlow W, Farbood Y, et al. Pathogenic mechanisms following ischemic stroke. Neurol Sci. 2017; 38(7): 1167–1186.
    CrossRefPubMed
  46. Kimelberg HK, Nedergaard M. Functions of astrocytes and their potential as therapeutic targets. Neurotherapeutics. 2010; 7(4): 338–353.
    CrossRefPubMed
  47. Kimelberg HK. Functions of mature mammalian astrocytes: a current view. Neuroscientist. 2010; 16(1): 79–106.
    CrossRefPubMed
  48. Kimelberg HK. The problem of astrocyte identity. Neurochem Int. 2004; 45(2-3): 191–202.
    CrossRefPubMed
  49. Köhler S, Winkler U, Hirrlinger J. Heterogeneity of astrocytes in grey and white matter. Neurochem Res. 2021; 46(1): 3–14.
    CrossRefPubMed
  50. Kowiański P, Lietzau G, Steliga A, et al. The astrocytic contribution to neurovascular coupling--still more questions than answers? Neurosci Res. 2013; 75(3): 171–183.
    CrossRefPubMed
  51. Kuhn S, Gritti L, Crooks D, et al. Oligodendrocytes in development, myelin generation and beyond. Cells. 2019; 8(11).
    CrossRefPubMed
  52. Lago-Baldaia I, Fernandes VM, Ackerman SD. More than mortar: glia as architects of nervous system development and disease. Front Cell Dev Biol. 2020; 8: 611269.
    CrossRefPubMed
  53. Lawson LJ, Perry VH, Dri P, et al. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience. 1990; 39(1): 151–170.
    CrossRefPubMed
  54. Li Q, Barres BA. Microglia and macrophages in brain homeostasis and disease. Nat Rev Immunol. 2018; 18(4): 225–242.
    CrossRefPubMed
  55. Liddelow SA, Barres BA. Reactive astrocytes: production, function, and therapeutic potential. Immunity. 2017; 46(6): 957–967.
    CrossRefPubMed
  56. Liddelow SA, Guttenplan KA, Clarke LE, et al. Neurotoxic reactive astrocytes are induced by activated microglia. Nature. 2017; 541(7638): 481–487.
    CrossRefPubMed
  57. Liebner S, Dijkhuizen RM, Reiss Y, et al. Functional morphology of the blood-brain barrier in health and disease. Acta Neuropathol. 2018; 135(3): 311–336.
    CrossRefPubMed
  58. Liu LR, Liu JC, Bao JS, et al. Interaction of microglia and astrocytes in the neurovascular unit. Front Immunol. 2020; 11: 1024.
    CrossRefPubMed
  59. Magistretti PJ, Allaman I. A cellular perspective on brain energy metabolism and functional imaging. Neuron. 2015; 86(4): 883–901.
    CrossRefPubMed
  60. Martins-Macedo J, Lepore AC, Domingues HS, et al. Glial restricted precursor cells in central nervous system disorders: current applications and future perspectives. Glia. 2021; 69(3): 513–531.
    CrossRefPubMed
  61. Masuda T, Sankowski R, Staszewski O, et al. Microglia heterogeneity in the single-cell era. Cell Rep. 2020; 30(5): 1271–1281.
    CrossRefPubMed
  62. Matcovitch-Natan O, Winter DR, Giladi A, et al. Microglia development follows a stepwise program to regulate brain homeostasis. Science. 2016; 353(6301): aad8670.
    CrossRefPubMed
  63. Matyash V, Kettenmann H. Heterogeneity in astrocyte morphology and physiology. Brain Res Rev. 2010; 63(1-2): 2–10.
    CrossRefPubMed
  64. Menassa DA, Gomez-Nicola D. Microglial dynamics during human brain development. Front Immunol. 2018; 9: 1014.
    CrossRefPubMed
  65. Moshrefi-Ravasdjani B, Dublin P, Seifert G, et al. Changes in the proliferative capacity of NG2 cell subpopulations during postnatal development of the mouse hippocampus. Brain Struct Funct. 2017; 222(2): 831–847.
    CrossRefPubMed
  66. Murtie JC, Macklin WB, Corfas G. Morphometric analysis of oligodendrocytes in the adult mouse frontal cortex. J Neurosci Res. 2007; 85(10): 2080–2086.
    CrossRefPubMed
  67. Nishiyama A, Komitova M, Suzuki R, et al. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci. 2009; 10(1): 9–22.
    CrossRefPubMed
  68. Parri HR, Crunelli V. The role of Ca2+ in the generation of spontaneous astrocytic Ca2+ oscillations. Neuroscience. 2003; 120(4): 979–992.
    CrossRefPubMed
  69. Pelvig DP, Pakkenberg H, Stark AK, et al. Neocortical glial cell numbers in human brains. Neurobiol Aging. 2008; 29(11): 1754–1762.
    CrossRefPubMed
  70. Ransom BR, Butt AM, Black JA. Ultrastructural identification of HRP-injected oligodendrocytes in the intact rat optic nerve. Glia. 1991; 4(1): 37–45.
    CrossRefPubMed
  71. Richardson WD, Young KM, Tripathi RB, et al. NG2-glia as multipotent neural stem cells: fact or fantasy? Neuron. 2011; 70(4): 661–673.
    CrossRefPubMed
  72. Rivera AD, Chacon-De-La-Rocha I, Pieropan F, et al. Keeping the ageing brain wired: a role for purine signalling in regulating cellular metabolism in oligodendrocyte progenitors. Pflugers Arch. 2021; 473(5): 775–783.
    CrossRefPubMed
  73. Rivers LE, Young KM, Rizzi M, et al. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci. 2008; 11(12): 1392–1401.
    CrossRefPubMed
  74. Robins SC, Kokoeva MV. NG2-Glia, a new player in energy balance. Neuroendocrinology. 2018; 107(3): 305–312.
    CrossRefPubMed
  75. Schaeffer S, Iadecola C. Revisiting the neurovascular unit. Nat Neurosci. 2021; 24(9): 1198–1209.
    CrossRefPubMed
  76. Schirmer L, Schafer DP, Bartels T, et al. Diversity and function of glial cell types in multiple sclerosis. Trends Immunol. 2021; 42(3): 228–247.
    CrossRefPubMed
  77. Schoenwolf GC, Bleyl SB, Brauer PR, Francis-West PH. Develoment of the central nervous system. Larsen's human embryology. 6th ed. Elsevier, Philadelphia 2020: 191–227.
  78. Sharma K, Bisht K, Eyo UB. A comparative biology of microglia across species. Front Cell Dev Biol. 2021; 9: 652748.
    CrossRefPubMed
  79. Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol. 2010; 119(1): 7–35.
    CrossRefPubMed
  80. Sofroniew MV. Astrocyte reactivity: subtypes, states, and functions in CNS innate immunity. Trends Immunol. 2020; 41(9): 758–770.
    CrossRefPubMed
  81. Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009; 32(12): 638–647.
    CrossRefPubMed
  82. Staszewski O, Hagemeyer N. Unique microglia expression profile in developing white matter. BMC Res Notes. 2019; 12(1): 367.
    CrossRefPubMed
  83. Steliga A, Kowiański P, Czuba E, et al. Neurovascular unit as a source of ischemic stroke biomarkers-limitations of experimental studies and perspectives for clinical application. Transl Stroke Res. 2020; 11(4): 553–579.
    CrossRefPubMed
  84. Stremmel C, Schuchert R, Wagner F, et al. Yolk sac macrophage progenitors traffic to the embryo during defined stages of development. Nat Commun. 2018; 9(1): 75.
    CrossRefPubMed
  85. Takano T, Tian GF, Peng W, et al. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci. 2006; 9(2): 260–267.
    CrossRefPubMed
  86. Thion MS, Low D, Silvin A, et al. Microbiome influences prenatal and adult microglia in a sex-specific manner. Cell. 2018; 172(3): 500–516.e16.
    CrossRefPubMed
  87. Torper O, Götz M. Brain repair from intrinsic cell sources: turning reactive glia into neurons. Prog Brain Res. 2017; 230: 69–97.
    CrossRefPubMed
  88. Torper O, Ottosson DR, Pereira M, et al. In vivo reprogramming of striatal NG2 glia into functional neurons that integrate into local host circuitry. Cell Rep. 2015; 12(3): 474–481.
    CrossRefPubMed
  89. Utz SG, See P, Mildenberger W, et al. Early fate defines microglia and non-parenchymal brain macrophage development. Cell. 2020; 181(3): 557–573.e18.
    CrossRefPubMed
  90. Valny M, Honsa P, Kriska J, et al. Multipotency and therapeutic potential of NG2 cells. Biochem Pharmacol. 2017; 141: 42–55.
    CrossRefPubMed
  91. Valny M, Honsa P, Waloschkova E, et al. A single-cell analysis reveals multiple roles of oligodendroglial lineage cells during post-ischemic regeneration. Glia. 2018; 66(5): 1068–1081.
    CrossRefPubMed
  92. Verkhratsky A, Ho MS, Zorec R, et al. The concept of neuroglia. Adv Exp Med Biol. 2019; 1175: 1–13.
    CrossRefPubMed
  93. Verkhratsky A, Kettenmann H. Calcium signalling in glial cells. Trends Neurosci. 1996; 19(8): 346–352.
    CrossRefPubMed
  94. Verkhratsky A, Sofroniew MV, Messing A, et al. Neurological diseases as primary gliopathies: a reassessment of neurocentrism. ASN Neuro. 2012; 4(3).
    CrossRefPubMed
  95. Werner Y, Mass E, Ashok Kumar P, et al. Cxcr4 distinguishes HSC-derived monocytes from microglia and reveals monocyte immune responses to experimental stroke. Nat Neurosci. 2020; 23(3): 351–362.
    CrossRefPubMed
  96. Wlodarczyk A, Holtman IR, Krueger M, et al. A novel microglial subset plays a key role in myelinogenesis in developing brain. EMBO J. 2017; 36(22): 3292–3308.
    CrossRefPubMed
  97. Zhao JW, Raha-Chowdhury R, Fawcett JW, et al. Astrocytes and oligodendrocytes can be generated from NG2+ progenitors after acute brain injury: intracellular localization of oligodendrocyte transcription factor 2 is associated with their fate choice. Eur J Neurosci. 2009; 29(9): 1853–1869.
    CrossRefPubMed
  98. Zhou YD. Glial regulation of energy metabolism. Adv Exp Med Biol. 2018; 1090: 105–121.
    CrossRefPubMed
  99. Zhu X, Hill RA, Dietrich D, et al. Age-dependent fate and lineage restriction of single NG2 cells. Development. 2011; 138(4): 745–753.
    CrossRefPubMed
  100. Zonta M, Angulo MC, Gobbo S, et al. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci. 2003; 6(1): 43–50.
    CrossRefPubMed
  101. Zonta M, Carmignoto G. Calcium oscillations encoding neuron-to-astrocyte communication. J Physiol Paris. 2002; 96(3-4): 193–198.
    CrossRefPubMed

Regulations

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

By VM Media Group sp. z o.o., Grupa Via Medica, Świętokrzyska 73, 80–180 Gdańsk, Poland

tel.: +48 58 320 94 94, faks: +48 58 320 94 60, e-mail: viamedica@viamedica.pl