The glia doctrine: Addressing the role of glial cells in healthy brain ageing

Mechanisms of Ageing and Development

Volumn 134, Issue 10, 2013, Pages 449-459

  Nagelhus, Erlend A ^a,b   Amiry Moghaddam, Mahmood ^a   Bergersen, Linda H ^a   Bjaalie, Jan G ^a   Eriksson, Jens ^b   Gundersen, Vidar ^a,b   Leergaard, Trygve B ^a   Morth, J Preben ^a   Storm Mathisen, Jon ^a   Torp, Reidun ^a   Walhovd, Kristine B ^a   Tønjum, Tone ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Ageing; Alzheimer's disease; Astrocytes; Brain imaging; Exosomes; Glial cells

Indexed keywords

DNA; MEMBRANE PROTEIN;

AGING; ARTICLE; ASTROCYTE; BRAIN FUNCTION; CELL DEGENERATION; CELL FUNCTION; CELL STRUCTURE; CELLULAR DISTRIBUTION; DNA POLYMORPHISM; DNA REPAIR; EXERCISE; EXOSOME; GLIA CELL; HUMAN; HUMAN CELL; MEMBRANE VESICLE; MICROGLIA; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ANIMALIA;

AGEING; ALZHEIMER'S DISEASE; ASTROCYTES; BRAIN IMAGING; EXOSOMES; GLIAL CELLS;

AGING; ASTROCYTES; BRAIN; BRAIN DISEASES; CELL COMMUNICATION; EXOSOMES; HUMANS;

EID: 84888131085     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2013.10.001     Document Type: Article

References (143)

1. Abbott N.J., Ronnback L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7:41-53.
2. Adlard P.A., Engesser-Cesar C., Cotman C.W. Mild stress facilitates learning and exercise improves retention in aged mice. Exp. Gerontol. 2011, 46:53-59.
3. 2+ signaling. Science 2010, 327:1250-1254.
4. Akil H., Martone M.E., Van Essen D.C. Challenges and opportunities in mining neuroscience data. Science 2011, 331:708-712.
5. Alvarez-Erviti L., Seow Y., Yin H., Betts C., Lakhal S., Wood M.J. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol. 2011, 29:341-345.
6. Alvestad S., Hammer J., Hoddevik E.H., Skare O., Sonnewald U., Amiry-Moghaddam M., Ottersen O.P. Mislocalization of AQP4 precedes chronic seizures in the kainate model of temporal lobe epilepsy. Epilepsy Res. 2013, 105:30-41.
7. Amiry-Moghaddam M., Ottersen O.P. The molecular basis of water transport in the brain. Nat. Rev. Neurosci. 2003, 4:991-1001.
8. Amiry-Moghaddam M., Otsuka T., Hurn P.D., Traystman R.J., Haug F.M., Froehner S.C., Adams M.E., Neely J.D., Agre P., Ottersen O.P., Bhardwaj A. An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:2106-2111.
9. Amiry-Moghaddam M., Xue R., Haug F.M., Neely J.D., Bhardwaj A., Agre P., Adams M.E., Froehner S.C., Mori S., Ottersen O.P. Alpha-syntrophin deletion removes the perivascular but not endothelial pool of aquaporin-4 at the blood-brain barrier and delays the development of brain edema in an experimental model of acute hyponatremia. FASEB J. 2004, 18:542-544.
10. Attwell D., Buchan A.M., Charpak S., Lauritzen M., Macvicar B.A., Newman E.A. Glial and neuronal control of brain blood flow. Nature 2010, 468:232-243.
11. Barzilai A. DNA damage, neuronal and glial cell death and neurodegeneration. Apoptosis 2010, 15:1371-1381.
12. Barzilai A. The interrelations between malfunctioning DNA damage response (DDR) and the functionality of the neuro-glio-vascular unit. DNA Repair (Amst) 2013, 12:543-557.
13. Barzilai A., Biton S., Shiloh Y. The role of the DNA damage response in neuronal development, organization and maintenance. DNA Repair (Amst) 2008, 7:1010-1027.
14. Benfenati V., Caprini M., Dovizio M., Mylonakou M.N., Ferroni S., Ottersen O.P., Amiry-Moghaddam M. An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cell-volume control in astrocytes. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2563-2568.
15. Berchtold N.C., Castello N., Cotman C.W. Exercise and time-dependent benefits to learning and memory. Neuroscience 2010, 167:588-597.
16. Bergersen L.H., Gjedde A. Is lactate a volume transmitter of metabolic states of the brain?. Front. Neuroenerg. 2012, 4:5.
17. Bezzi P., Gundersen V., Galbete J.L., Seifert G., Steinhauser C., Pilati E., Volterra A. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat. Neurosci. 2004, 7:613-620.
18. Bishop N.A., Lu T., Yankner B.A. Neural mechanisms of ageing and cognitive decline. Nature 2010, 464:529-535.
19. Bjaalie J.G. Understanding the brain through neuroinformatics. Front. Neurosci. 2008, 2:19-21.
20. Bjaalie J.G., Grillner S. Global neuroinformatics: the International Neuroinformatics Coordinating Facility. J. Neurosci. 2007, 27:3613-3615.
21. Blumenfeld-Katzir T., Pasternak O., Dagan M., Assaf Y. Diffusion MRI of structural brain plasticity induced by a learning and memory task. PLoS ONE 2011, 6:e20678.
22. Bohr V.A. Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem. Sci. 2008, 33:609-620.
23. Bohr V.A., Ottersen O.P., Tonjum T. Genome instability and DNA repair in brain, ageing and neurological disease. Neuroscience 2007, 145:1183-1186.
24. Bourne J.N., Harris K.M. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 2011, 21:354-373.
25. Busche M.A., Eichhoff G., Adelsberger H., Abramowski D., Wiederhold K.H., Haass C., Staufenbiel M., Konnerth A., Garaschuk O. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 2008, 321:1686-1689.
26. Chen J., Tan Z., Zeng L., Zhang X., He Y., Gao W., Wu X., Li Y., Bu B., Wang W., Duan S. Heterosynaptic long-term depression mediated by ATP released from astrocytes. Glia 2013, 61:178-191.
27. Chesler M. Regulation and modulation of pH in the brain. Physiol. Rev. 2003, 83:1183-1221.
28. Coco M., Caggia S., Musumeci G., Perciavalle V., Graziano A.C., Pannuzzo G., Cardile V. Sodium l-lactate differently affects brain-derived neurothrophic factor, inducible nitric oxide synthase, and heat shock protein 70kDa production in human astrocytes and SH-SY5Y cultures. J. Neurosci. Res. 2013, 91:313-320.
29. Davidsen T., Koomey M., Tonjum T. Microbial genome dynamics in CNS pathogenesis. Neuroscience 2007, 145:1375-1387.
30. +-ATPase alpha3 gene ATP1A3 are associated with rapid-onset dystonia parkinsonism. Neuron 2004, 43:169-175.
31. + pump alpha2 subunit associated with familial hemiplegic migraine type 2. Nat. Genet. 2003, 33:192-196.
32. De Pitta M., Volman V., Berry H., Ben-Jacob E. A tale of two stories: astrocyte regulation of synaptic depression and facilitation. PLoS Comput. Biol. 2011, 7:e1002293.
33. De Pitta M., Volman V., Berry H., Parpura V., Volterra A., Ben-Jacob E. Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity. Front. Comput. Neurosci. 2012, 6:98.
34. Desler C., Marcker M.L., Singh K.K., Rasmussen L.J. The importance of mitochondrial DNA in aging and cancer. J. Aging Res. 2011, 2011:407536.
35. Duan Z., Qu Y., Zhao F., Tang B., Li J., Mu D. [Protective effect of conditioned medium from astrocytes transfected with telomerase reverse transcriptase on hypoxia-ischemia neurons]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2010, 24:1217-1223.
36. Eid T., Lee T.S., Thomas M.J., Amiry-Moghaddam M., Bjornsen L.P., Spencer D.D., Agre P., Ottersen O.P., de Lanerolle N.C. Loss of perivascular aquaporin 4 may underlie deficient water and K+ homeostasis in the human epileptogenic hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1193-1198.
37. Engvig A., Fjell A.M., Westlye L.T., Moberget T., Sundseth O., Larsen V.A., Walhovd K.B. Effects of memory training on cortical thickness in the elderly. Neuroimage 2010, 52:1667-1676.
38. Engvig A., Fjell A.M., Westlye L.T., Moberget T., Sundseth O., Larsen V.A., Walhovd K.B. Memory training impacts short-term changes in aging white matter: a longitudinal diffusion tensor imaging study. Hum. Brain Mapp. 2012, 33:2390-2406.
39. Engvig A., Fjell A.M., Westlye L.T., Skaane N.V., Sundseth O., Walhovd K.B. Hippocampal subfield volumes correlate with memory training benefit in subjective memory impairment. Neuroimage 2012, 61:188-194.
40. Erickson K.I., et al. Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3017-3022.
41. Fields R.D. Myelination: an overlooked mechanism of synaptic plasticity?. Neuroscientist 2005, 11:528-531.
42. Finch C.E. Evolution in health and medicine Sackler colloquium: evolution of the human lifespan and diseases of aging: roles of infection, inflammation, and nutrition. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(Suppl. 1):1718-1724.
43. Fjell A.M., Walhovd K.B., Fennema-Notestine C., McEvoy L.K., Hagler D.J., Holland D., Brewer J.B., Dale A.M. One-year brain atrophy evident in healthy aging. J. Neurosci. 2009, 29:15223-15231.
44. Fjell A.M., Westlye L.T., Amlien I., Espeseth T., Reinvang I., Raz N., Agartz I., Salat D.H., Greve D.N., Fischl B., Dale A.M., Walhovd K.B. High consistency of regional cortical thinning in aging across multiple samples. Cereb. Cortex 2009, 19:2001-2012. 10.1093/cercor/bhn232.
45. Fjell A.M., Westlye L.T., Amlien I., Espeseth T., Reinvang I., Raz N., Agartz I., Salat D.H., Greve D.N., Fischl B., Dale A.M., Walhovd K.B. High consistency of regional cortical thinning in aging across multiple samples. Cereb. Cortex 2009, 19:2001-2012.
46. Fjell A.M., Walhovd K.B., Fennema-Notestine C., McEvoy L.K., Hagler D.J., Holland D., Blennow K., Brewer J.B., Dale A.M. Brain atrophy in healthy aging is related to CSF levels of Abeta1-42. Cereb. Cortex 2010, 20:2069-2079.
47. Fjell A.M., Walhovd K.B., Fennema-Notestine C., McEvoy L.K., Hagler D.J., Holland D., Brewer J.B., Dale A.M. CSF biomarkers in prediction of cerebral and clinical change in mild cognitive impairment and Alzheimer's disease. J. Neurosci. 2010, 30:2088-2101.
48. Folmer D.E., Elferink R.P., Paulusma C.C. P4 ATPases - lipid flippases and their role in disease. Biochim. Biophys. Acta 2009, 1791:628-635.
49. Foster P.P., Rosenblatt K.P., Kuljis R.O. Exercise-induced cognitive plasticity, implications for mild cognitive impairment and Alzheimer's disease. Front. Neurol. 2011, 2:28.
50. Frydenlund D.S., Bhardwaj A., Otsuka T., Mylonakou M.N., Yasumura T., Davidson K.G., Zeynalov E., Skare O., Laake P., Haug F.M., Rash J.E., Agre P., Ottersen O.P., Amiry-Moghaddam M. Temporary loss of perivascular aquaporin-4 in neocortex after transient middle cerebral artery occlusion in mice. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13532-13536.
51. Fu W., Lu C., Mattson M.P. Telomerase mediates the cell survival-promoting actions of brain-derived neurotrophic factor and secreted amyloid precursor protein in developing hippocampal neurons. J. Neurosci. 2002, 22:10710-10719.
52. Giaume C., Liu X. From a glial syncytium to a more restricted and specific glial networking. J. Physiol. Paris 2012, 106:34-39.
53. Giaume C., Leybaert L., Naus C.C., Sáez J.C. Connexin and pannexin hemichannels in brain glial cells: properties, pharmacology, and roles. Front. Pharmacol. 2013, 4:88.
54. Girgenti M.J., Hunsberger J., Duman C.H., Sathyanesan M., Terwilliger R., Newton S.S. Erythropoietin induction by electroconvulsive seizure, gene regulation, and antidepressant-like behavioral effects. Biol. Psychiatry 2009, 66:267-274.
55. Gordon G.R., Mulligan S.J., MacVicar B.A. Astrocyte control of the cerebrovasculature. Glia 2007, 55:1214-1221.
56. Gredilla R., Garm C., Stevnsner T. Nuclear and mitochondrial DNA repair in selected eukaryotic aging model systems. Oxid. Med. Cell Longev. 2012, 2012:282438.
57. Griffin R., Nally R., Nolan Y., McCartney Y., Linden J., Lynch M.A. The age-related attenuation in long-term potentiation is associated with microglial activation. J. Neurochem. 2006, 99:1263-1272.
58. Grolla A.A., Fakhfouri G., Balzaretti G., Marcello E., Gardoni F., Canonico P.L., DiLuca M., Genazzani A.A., Lim D. Abeta leads to Ca(2)(+) signaling alterations and transcriptional changes in glial cells. Neurobiol. Aging 2013, 34:511-522.
59. Guescini M., Genedani S., Stocchi V., Agnati L.F. Astrocytes and glioblastoma cells release exosomes carrying mtDNA. J. Neural Transm. 2010, 117:1-4.
60. Haj-Yasein N.N., Vindedal G.F., Eilert-Olsen M., Gundersen G.A., Skare O., Laake P., Klungland A., Thoren A.E., Burkhardt J.M., Ottersen O.P., Nagelhus E.A. Glial-conditional deletion of aquaporin-4 (Aqp4) reduces blood-brain water uptake and confers barrier function on perivascular astrocyte endfeet. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17815-17820.
61. Haj-Yasein N.N., Jensen V., Ostby I., Omholt S.W., Voipio J., Kaila K., Ottersen O.P., Hvalby O., Nagelhus E.A. Aquaporin-4 regulates extracellular space volume dynamics during high-frequency synaptic stimulation: a gene deletion study in mouse hippocampus. Glia 2012, 60:867-874.
62. Hamilton D.J., Shepherd G.M., Martone M.E., Ascoli G.A. An ontological approach to describing neurons and their relationships. Front. Neuroinform. 2012, 6:15.
63. Han K.S., Woo J., Park H., Yoon B.J., Choi S., Lee C.J. Channel-mediated astrocytic glutamate release via Bestrophin-1 targets synaptic NMDARs. Mol. Brain. 2013, 6:4.
64. Han X., Chen M., Wang F., Windrem M., Wang S., Shanz S., Xu Q., Oberheim N.A., Bekar L., Betstadt S., Silva A.J., Takano T., Goldman S.A., Nedergaard M. Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 2013, 12:342-353.
65. Haydon P.G., Carmignoto G. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol. Rev. 2006, 86:1009-1031.
66. Heuser K., Eid T., Lauritzen F., Thoren A.E., Vindedal G.F., Tauboll E., Gjerstad L., Spencer D.D., Ottersen O.P., Nagelhus E.A., de Lanerolle N.C. Loss of perivascular Kir4.1 potassium channels in the sclerotic hippocampus of patients with mesial temporal lobe epilepsy. J. Neuropathol. Exp. Neurol. 2012, 71:814-825.
67. Hjornevik T., Leergaard T.B., Darine D., Moldestad O., Dale A.M., Willoch F., Bjaalie J.G. Three-dimensional atlas system for mouse and rat brain imaging data. Front. Neuroinform. 2007, 1:4. 10.3389/neuro.11.004.
68. Hsu K.S., Huang C.C., Liang Y.C., Wu H.M., Chen Y.L., Lo S.W., Ho W.C. Alterations in the balance of protein kinase and phosphatase activities and age-related impairments of synaptic transmission and long-term potentiation. Hippocampus 2002, 12:787-802.
69. Iadecola C., Nedergaard M. Glial regulation of the cerebral microvasculature. Nat. Neurosci. 2007, 10:1369-1376.
70. Iliff J.J., Wang M., Liao Y., Plogg B.A., Peng W., Gundersen G.A., Benveniste H., Vates G.E., Deane R., Goldman S.A., Nagelhus E.A., Nedergaard M. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci. Transl. Med. 2012, 4:147ra111.
71. Johansen-Berg H., Baptista C.S., Thomas A.G. Human structural plasticity at record speed. Neuron 2012, 73:1058-1060.
72. Jourdain P., Bergersen L.H., Bhaukaurally K., Bezzi P., Santello M., Domercq M., Matute C., Tonello F., Gundersen V., Volterra A. Glutamate exocytosis from astrocytes controls synaptic strength. Nat. Neurosci. 2007, 10:331-339.
73. Kalisman N., Silberberg G., Markram H. The neocortical microcircuit as a tabula rasa. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:880-885.
74. Kalra H., et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 2012, 10:e1001450.
75. Kettenmann H., Hanisch U.K., Noda M., Verkhratsky A. Physiology of microglia. Physiol. Rev. 2011, 91:461-553.
76. Kida S. A Functional role for CREB as a positive regulator of memory formation and LTP. Exp. Neurobiol. 2012, 21:136-140.
77. Klika E., Antalikova L. The membrana limitans gliae superficialis in vertebrates. Folia Morphol. (Praha) 1969, 17:342-347.
78. Komulainen P., Pedersen M., Hanninen T., Bruunsgaard H., Lakka T.A., Kivipelto M., Hassinen M., Rauramaa T.H., Pedersen B.K., Rauramaa R. BDNF is a novel marker of cognitive function in ageing women: the DR's EXTRA study. Neurobiol. Learn. Mem. 2008, 90:596-603.
79. Lachenal G., Pernet-Gallay K., Chivet M., Hemming F.J., Belly A., Bodon G., Blot B., Haase G., Goldberg Y., Sadoul R. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol. Cell. Neurosci. 2010, 46:409-418.
80. LaRocca T.J., Seals D.R., Pierce G.L. Leukocyte telomere length is preserved with aging in endurance exercise-trained adults and related to maximal aerobic capacity. Mech. Ageing Dev. 2010, 131:165-167.
81. Laske C., Stransky E., Leyhe T., Eschweiler G.W., Wittorf A., Richartz E., Bartels M., Buchkremer G., Schott K. Stage-dependent BDNF serum concentrations in Alzheimer's disease. J. Neural Transm. 2006, 113:1217-1224.
82. Latimer C.S., Searcy J.L., Bridges M.T., Brewer L.D., Popovic J., Blalock E.M., Landfield P.W., Thibault O., Porter N.M. Reversal of glial and neurovascular markers of unhealthy brain aging by exercise in middle-aged female mice. PLoS ONE 2011, 6:e26812.
83. Lauritzen K.H., Morland C., Puchades M., Holm-Hansen S., Hagelin E.M., Lauritzen F., Attramadal H., Storm-Mathisen J., Gjedde A., Bergersen L.H. Lactate receptor sites link neurotransmission, neurovascular coupling, and brain energy metabolism. Cereb. Cortex 2013, (in press). 10.1093/cercor/bht136.
84. Lee S.H., Kim W.T., Cornell-Bell A.H., Sontheimer H. Astrocytes exhibit regional specificity in gap-junction coupling. Glia 1994, 11:315-325.
85. Lee S., Yoon B.E., Berglund K., Oh S.J., Park H., Shin H.S., Augustine G.J., Lee C.J. Channel-mediated tonic GABA release from glia. Science 2010, 330:790-796.
86. Leergaard T.B., White N.S., de Crespigny A., Bolstad I., D'Arceuil H., Bjaalie J.G., Dale A.M. Quantitative histological validation of diffusion MRI fiber orientation distributions in the rat brain. PLoS One 2010, 5:e8595. 10.1371/journal.pone.0008595.
87. Lillenes M.S., Espeseth T., Stoen M., Lundervold A.J., Frye S.A., Rootwelt H., Reinvang I., Tonjum T. DNA base excision repair gene polymorphisms modulate human cognitive performance and decline during normal life span. Mech. Ageing Dev. 2011, 132:449-458.
88. Lillenes M.S., Støen M., Munoz M.G., Torp R., Günther C.C., Nilsson L.N.G., Tønjum T. Transient changes in expression of OGG1, APE1 and Polβ in the brains of mice expressing mutant amyloid-β precursor protein (AβPP). Mech. Ageing Dev. 2013, 134. pii: S0047-6374(13)00109-7. 10.1016/j.mad.2013.09.002.
89. Marambaud P., Wen P.H., Dutt A., Shioi J., Takashima A., Siman R., Robakis N.K. A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 2003, 114:635-645.
90. Marchetto M.C., Muotri A.R., Mu Y., Smith A.M., Cezar G.G., Gage F.H. Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell 2008, 3:649-657.
91. Mathiisen T.M., Lehre K.P., Danbolt N.C., Ottersen O.P. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 2010, 58:1094-1103.
92. McKenzie J.R., Palubinsky A.M., Brown J.E., McLaughlin B., Cliffel D.E. Metabolic multianalyte microphysiometry reveals extracellular acidosis is an essential mediator of neuronal preconditioning. ACS Chem. Neurosci. 2012, 3:510-518.
93. Molina-Holgado E., Molina-Holgado F. Mending the broken brain: neuroimmune interactions in neurogenesis. J. Neurochem. 2010, 114:1277-1290.
94. +-ATPase and mapping of isoform differences and disease-related mutations. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2009, 364:217-227.
95. Nagamatsu L.S., Chan A., Davis J.C., Beattie B.L., Graf P., Voss M.W., Sharma D., Liu-Ambrose T. Physical activity improves verbal and spatial memory in older adults with probable mild cognitive impairment: a 6-month randomized controlled trial. J. Aging Res. 2013, 2013:861893.
96. Nagelhus E.A., Horio Y., Inanobe A., Fujita A., Haug F.M., Nielsen S., Kurachi Y., Ottersen O.P. Immunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Muller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains. Glia 1999, 26:47-54.
97. Nagelhus E.A., Ottersen O.P. Physiological roles of aquaporin-4 in brain. Physiol. Rev. 2013, 93:1543-1562.
98. Nase G., Helm P.J., Enger R., Ottersen O.P. Water entry into astrocytes during brain edema formation. Glia 2008, 56:895-902.
99. Nielsen S., Nagelhus E.A., Amiry-Moghaddam M., Bourque C., Agre P., Ottersen O.P. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 1997, 17:171-180.
100. Niu C., Yip H.K. Neuroprotective signaling mechanisms of telomerase are regulated by brain-derived neurotrophic factor in rat spinal cord motor neurons. J. Neuropathol. Exp. Neurol. 2011, 70:634-652.
101. Oliet S.H., Piet R., Poulain D.A. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 2001, 292:923-926.
102. Østby Y., Tamnes C.K., Fjell A.M., Westlye L.T., Due-Tønnessen P., Walhovd K.B. Heterogeneity in subcortical brain development: a structural magnetic resonance imaging study of brain maturation from 8 to 30 years. J. Neurosci. 2009, 29:11772-11782. 29/38/11772. 10.1523/JNEUROSCI.1242-09.2009.
103. Osthus I.B., Sgura A., Berardinelli F., Alsnes I.V., Bronstad E., Rehn T., Stobakk P.K., Hatle H., Wisloff U., Nauman J. Telomere length and long-term endurance exercise: does exercise training affect biological age? A pilot study. PLoS ONE 2012, 7:e52769.
104. Palmer A.M. The role of the blood brain barrier in neurodegenerative disorders and their treatment. J. Alzheimers Dis. 2011, 24:643-656.
105. Panatier A., Theodosis D.T., Mothet J.P., Touquet B., Pollegioni L., Poulain D.A., Oliet S.H. Glia-derived d-serine controls NMDA receptor activity and synaptic memory. Cell 2006, 125:775-784.
106. Papadopoulos M.C., Verkman A.S. Aquaporin water channels in the nervous system. Nat. Rev. Neurosci. 2013, 14:265-277.
107. Papadopoulos M.C., Manley G.T., Krishna S., Verkman A.S. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 2004, 18:1291-1293.
108. Papp E.A., Kjonigsen L., Lillehaug S., Johnson G.A., Witter M.P., Leergaard T.B., Bjaalie J.G. Volumetric Waxholm space atlas of the rat brain for spatial integration of experimental image data. Conference abstract. Neuroinformatics 2013, P36.
109. Pasantes-Morales H., Lezama R.A., Ramos-Mandujano G., Tuz K.L. Mechanisms of cell volume regulation in hypo-osmolality. Am. J. Med. 2006, 119:S4-S11.
110. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2005, Elsevier Academic Press, San Diego.
111. Qu Y., Duan Z., Zhao F., Wei D., Zhang J., Tang B., Li J., Yang C., Mu D. Telomerase reverse transcriptase upregulation attenuates astrocyte proliferation and promotes neuronal survival in the hypoxic-ischemic rat brain. Stroke 2011, 42:3542-3550.
112. Rasmussen P., Brassard P., Adser H., Pedersen M.V., Leick L., Hart E., Secher N.H., Pedersen B.K., Pilegaard H. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp. Physiol. 2009, 94:1062-1069.
113. Rodriguez J.J., Olabarria M., Chvatal A., Verkhratsky A. Astroglia in dementia and Alzheimer's disease. Cell Death Differ. 2009, 16:378-385.
114. Sagi Y., Tavor I., Hofstetter S., Tzur-Moryosef S., Blumenfeld-Katzir T., Assaf Y. Learning in the fast lane: new insights into neuroplasticity. Neuron 2012, 73:1195-1203.
115. Saha R.N., Liu X., Pahan K. Up-regulation of BDNF in astrocytes by TNF-alpha: a case for the neuroprotective role of cytokine. J. Neuroimmune Pharmacol. 2006, 1:212-222.
116. Santello M., Cali C., Bezzi P. Gliotransmission and the tripartite synapse. Adv. Exp. Med. Biol. 2012, 970:307-331.
117. Schuler B., Vogel J., Grenacher B., Jacobs R.A., Arras M., Gassmann M. Acute and chronic elevation of erythropoietin in the brain improves exercise performance in mice without inducing erythropoiesis. FASEB J. 2012, 26:3884-3890.
118. Seifert T., Brassard P., Wissenberg M., Rasmussen P., Nordby P., Stallknecht B., Adser H., Jakobsen A.H., Pilegaard H., Nielsen H.B., Secher N.H. Endurance training enhances BDNF release from the human brain. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R372-R377.
119. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
120. Sun W., McConnell E., Pare J.F., Xu Q., Chen M., Peng W., Lovatt D., Han X., Smith Y., Nedergaard M. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 2013, 339:197-200.
121. Tamnes C.K., Ostby Y., Fjell A.M., Westlye L.T., Due-Tonnessen P., Walhovd K.B. Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb. Cortex 2010, 20:534-548. 10.1093/cercor/bhp118.
122. Thery C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 2009, 9:581-593.
123. 2+ signaling events elicited by cerebral edema. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:846-851.
124. Thrane A.S., Takano T., Rangroo Thrane V., Wang F., Peng W., Ottersen O.P., Nedergaard M., Nagelhus E.A. In vivo NADH fluorescence imaging indicates effect of aquaporin-4 deletion on oxygen microdistribution in cortical spreading depression. J. Cereb. Blood Flow Metab. 2013, 2013:63.
125. Tønjum T., Freitag N.E., Namork E., Koomey M. Identification and characterization of pilG, a highly conserved pilus-assembly gene in pathogenic Neisseria. Mol. Microbiol. 1995, 16:451-464.
126. Tremblay M.E. The role of microglia at synapses in the healthy CNS: novel insights from recent imaging studies. Neuron Glia Biol. 2011, 7:67-76.
127. Unden J., Sjolund C., Lansberg J.K., Wieloch T., Ruscher K., Romner B. Post-ischemic continuous infusion of erythropoeitin enhances recovery of lost memory function after global cerebral ischemia in the rat. BMC Neurosci. 2013, 14:27.
128. van de Waterbeemd B., Mommen G.P., Pennings J.L., Eppink M.H., Wijffels R.H., van der Pol L.A., de Jong A.P. Quantitative proteomics reveals distinct differences in the protein content of outer membrane vesicle vaccines. J. Proteome Res. 2013, 2013:25.
129. Ventura R., Harris K.M. Three-dimensional relationships between hippocampal synapses and astrocytes. J. Neurosci. 1999, 19:6897-6906.
130. + ion imbalances in Alzheimer's disease. Biochim. Biophys. Acta 2012, 1822:1671-1681.
131. Walhovd K.B., Fjell A.M., Reinvang I., Lundervold A., Dale A.M., Eilertsen D.E., Quinn B.T., Salat D., Makris N., Fischl B. Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol. Aging 2005, 26:1261-1270. (discussion 1275-1268). 10.1016/j.neurobiolaging.2005.05.020.
132. Walhovd K.B., Fjell A.M., Amlien I., Grambaite R., Stenset V., Bjornerud A., Reinvang I., Gjerstad L., Cappelen T., Due-Tonnessen P., Fladby T. Multimodal imaging in mild cognitive impairment: Metabolism, morphometry and diffusion of the temporal-parietal memory network. Neuroimage 2009, 45:215-223.
133. Walhovd K.B., Fjell A.M., Brewer J., McEvoy L.K., Fennema-Notestine C., Hagler D.J., Jennings R.G., Karow D., Dale A.M. Combining MR imaging, positron-emission tomography, and CSF biomarkers in the diagnosis and prognosis of Alzheimer disease. Am. J. Neuroradiol. 2010, 31:347-354.
134. Walhovd K.B., Fjell A.M., Dale A.M., McEvoy L.K., Brewer J., Karow D.S., Salmon D.P., Fennema-Notestine C. Multi-modal imaging predicts memory performance in normal aging and cognitive decline. Neurobiol. Aging 2010, 31:1107-1121.
135. Walhovd K.B., Westlye L.T., Amlien I., Espeseth T., Reinvang I., Raz N., Agartz I., Salat D.H., Greve D.N., Fischl B., Dale A.M., Fjell A.M. Consistent neuroanatomical age-related volume differences across multiple samples. Neurobiol. Aging 2011, 32:916-932. 10.1016/j.neurobiolaging.2009.05.013.
136. Wang G., Dinkins M., He Q., Zhu G., Poirier C., Campbell A., Mayer-Proschel M., Bieberich E. Astrocytes secrete exosomes enriched with proapoptotic ceramide and prostate apoptosis response 4 (PAR-4): potential mechanism of apoptosis induction in Alzheimer disease (AD). J. Biol. Chem. 2012, 287:21384-21395.
137. Weiner M.W., et al. The Alzheimer's disease neuroimaging initiative: progress report and future plans. Alzheimers Dement. 2010, 6. 202-211, e207.
138. Westlye L.T., Walhovd K.B., Dale A.M., Bjornerud A., Due-Tonnessen P., Engvig A., Grydeland H., Tamnes C.K., Ostby Y., Fjell A.M. Differentiating maturational and aging-related changes of the cerebral cortex by use of thickness and signal intensity. Neuroimage 2010, 52:172-185.
139. White N.S., Leergaard T.B., D'Arceuil H., Bjaalie J.G., Dale A.M. Probing tissue microstructure with restriction spectrum imaging: histological and theoretical validation. Hum. Brain Mapp. 2013, 34:327-346.
140. Wisloff U., et al. Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: a randomized study. Circulation 2007, 115:3086-3094.
141. Yang J., Lunde L.K., Nuntagij P., Oguchi T., Camassa L.M., Nilsson L.N., Lannfelt L., Xu Y., Amiry-Moghaddam M., Ottersen O.P., Torp R. Loss of astrocyte polarization in the tg-ArcSwe mouse model of Alzheimer's disease. J. Alzheimers Dis. 2011, 27:711-722.
142. Zhao J., O'Connor T., Vassar R. The contribution of activated astrocytes to Abeta production: implications for Alzheimer's disease pathogenesis. J. Neuroinflam. 2011, 8:150.
143. Zschucke E., Gaudlitz K., Strohle A. Exercise and physical activity in mental disorders: clinical and experimental evidence. J. Prev. Med. Public Health 2013, 46(Suppl. 1):S12-S21.