Ischemic tolerance in pre-myelinated white matter: The role of astrocyte glycogen in brain pathology

Journal of Cerebral Blood Flow and Metabolism

Volumn 35, Issue 6, 2015, Pages 951-958

  Fern, Robert ^a  

^a PLYMOUTH UNIVERSITY PENINSULA SCHOOLS OF MEDICINE AND DENTISTRY   (United Kingdom)

Author keywords

astrocyte; axon; glia; glycogen; ischemia; white matter

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM CHANNEL; CARRIER PROTEIN; DEOXYGLUCOSE; GLUCOSE; GLYCOGEN; IONOTROPIC RECEPTOR; LACTIC ACID; TRICARBOXYLIC ACID;

ACTION POTENTIAL; ALPHA RADIATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ELECTROPHYSIOLOGY; BRAIN ISCHEMIA; BRAIN METABOLISM; CELL DENSITY; CELL MATURATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENERGY RESOURCE; FEMALE; GLUCOSE TOLERANCE; GLYCOGEN METABOLISM; GLYCOLYSIS; MALE; METABOLIC RATE; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL VOLUME; MYELINATION; NERVE FIBER; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RAT; WHITE MATTER; ANIMAL; BRAIN; BRAIN DISEASE; ENERGY METABOLISM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MYELIN SHEATH; PATHOLOGY;

ANIMALS; ASTROCYTES; AXONS; BRAIN; BRAIN DISEASES; BRAIN ISCHEMIA; ENERGY METABOLISM; FEMALE; GLYCOGEN; MALE; MYELIN SHEATH; RATS; WHITE MATTER;

EID: 84930181607     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2015.3     Document Type: Article

References (43)

1. Fern RF, Matute C, Stys PK. White matter injury: Ischemic and nonischemic. Glia 2014; 62: 1780-1789.
2. Back SA, Luo NL, Borenstein NS, Levine JM, Volpe JJ, Kinney HC. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 2001; 21: 1302-1312.
3. Khwaja O, Volpe JJ. Pathogenesis of cerebral white matter injury of prematurity. Arch Dis Child Fetal Neonatal Ed 2008; 93: F153-F161.
4. Roessmann U, Gambetti P. Astrocytes in the developing human brain. An immunohistochemical study. Acta Neuropathol 1986; 70: 308-313.
5. Takashima S, Becker LE. Developmental changes of glial fibrillary acidic protein in cerebral white matter. Arch Neurol 1983; 40: 14-18.
6. Vaughn JE. An electron microscopic analysis of gliogenesis in rat optic nerves. Z Zellforsch Mikrosk Anat 1969; 94: 293-324.
7. Skoff RP, Price DL, Stocks A. Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. II. Time of origin. J Comp Neurol 1976; 169: 313-334.
8. Fern R, Davis P, Waxman SG, Ransom BR. Axon conduction and survival in CNS white matter during energy deprivation: a developmental study. J Neurophysiol 1998; 79: 95-105.
9. Cataldo AM, Broadwell RD. Cytochemical identification of cerebral glycogen and glucose-6-phosphatase activity under normal and experimental conditions. II. Choroid plexus and ependymal epithelia, endothelia and pericytes. J Neurocytol 1986; 15: 511-524.
10. Wender R, Brown AM, Fern R, Swanson RA, Farrell K, Ransom BR. Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci 2000; 20: 6804-6810.
11. Alix JJ, Dolphin AC, Fern R. Vesicular apparatus, including functional calcium channels, are present in developing rodent optic nerve axons and are required for normal node of Ranvier formation. J Physiol 2008; 586: 4069-4089.
12. Dringen R, Hamprecht B. Inhibition by 2-deoxyglucose and 1, 5-gluconolactone of glycogen mobilization in astroglia-rich primary cultures. J Neurochem 1993; 60: 1498-1504.
13. Alix JJ, Fern R. Glutamate receptor-mediated ischemic injury of premyelinated central axons. Ann Neurol 2009; 66: 682-693.
14. Swanson RA. Astrocyte glutamate uptake during chemical hypoxia in vitro. Neurosci Lett 1992; 147: 143-146.
15. Perge JA, Niven JE, Mugnaini E, Balasubramanian V, Sterling P. Why do axons differ in caliber? J Neurosci 2012; 32: 626-638.
16. Sturrock RR. A light and electron microscopic study of proliferation and maturation of fibrous astrocytes in the optic nerve of the human embryo. J Anat 1975; 119: 223-234.
17. Jakovcevski I, Filipovic R, Mo Z, Rakic S, Zecevic N. Oligodendrocyte development and the onset of myelination in the human fetal brain. Front Neuroanat 2009; 3: 5.
18. Wierzba-Bobrowicz T, Lechowicz W, Kosno-Kruszewska E. A morphometric evaluation of morphological types of microglia and astroglia in human fetal mesencephalon. Folia Neuropathol 1997; 35: 29-35.
19. Spreafico R, Arcelli P, Frassoni C, Canetti P, Giaccone G, Rizzuti T et al. Development of layer I of the human cerebral cortex after midgestation: architectonic findings, immunocytochemical identification of neurons and glia, and in situ labeling of apoptotic cells. J Comp Neurol 1999; 410: 126-142.
20. Howard BM, Zhicheng M, Filipovic R, Moore AR, Antic SD, Zecevic N. Radial glia cells in the developing human brain. Neuroscientist 2008; 14: 459-473.
21. Mi H, Barres BA. Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J Neurosci 1999; 19: 1049-1061.
22. Matheson DF. Some quantitative aspects of myelination of the optic nerve in rat. Brain Res 1970; 24: 257-269.
23. Black JA, Waxman SG, Ransom BR, Feliciano MD. A quantitative study of developing axons and glia following altered gliogenesis in rat optic nerve. Brain Res 1986; 380: 122-135.
24. Zhang MZ, McKanna JA. Gliogenesis in postnatal rat optic nerve: LC1+microglia and S100-beta+astrocytes. Brain Res Dev Brain Res 1997; 101: 27-36.
25. David S, Miller RH, Patel R, Raff MC. Effects of neonatal transection on glial cell development in the rat optic nerve: evidence that the oligodendrocyte-Type 2 astrocyte cell lineage depends on axons for its survival. J Neurocytol 1984; 13: 961-974.
26. Jacque C, Lachapelle F, Collier P, Raoul M, Baumann N. Accumulation of GFA, the monomeric precursor of the gliofilaments, during development in normal mice and dysmyelinating mutants. J Neurosci Res 1980; 5: 379-385.
27. Nehlig A, Pereira de Vasconcelos A, Boyet S. Postnatal changes in local cerebral blood flow measured by the quantitative autoradiographic [14C]iodoantipyrine technique in freely moving rats. J Cereb Blood Flow Metab 1989; 9: 579-588.
28. Chugani HT, Hovda DA, Villablanca JR, Phelps ME, Xu WF. Metabolic maturation of the brain: a study of local cerebral glucose utilization in the developing cat. J Cereb Blood Flow Metab 1991; 11: 35-47.
29. Orgul S, Cioffi GA. Embryology, anatomy, and histology of the optic nerve vasculature. J Glaucoma 1996; 5: 285-294.
30. Blankenship AG, Hamby AM, Firl A, Vyas S, Maxeiner S, Willecke K et al. The role of neuronal connexins 36 and 45 in shaping spontaneous firing patterns in the developing retina. J Neurosci 2011; 31: 9998-10008.
31. Foster RE, Connors BW, Waxman SG. Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development. Brain Res 1982; 255: 371-386.
32. Waxman SG, Black JA, Kocsis JD, Ritchie JM. Low density of sodium channels supports action potential conduction in axons of neonatal rat optic nerve. Proc Natl Acad Sci USA 1989; 86: 1406-1410.
33. Black JA, Foster RE, Waxman SG. Rat optic nerve: freeze-fracture studies during development of myelinated axons. Brain Res 1982; 250: 1-20.
34. Perge JA, Koch K, Miller R, Sterling P, Balasubramanian V. How the optic nerve allocates space, energy capacity, and information. J Neurosci 2009; 29: 7917-7928.
35. Hildebrand C, Waxman SG. Postnatal differentiation of rat optic nerve fibers: electron microscopic observations on the development of nodes of Ranvier and axoglial relations. J Comp Neurol 1984; 224: 25-37.
36. Rasband MN, Shrager P. Ion channel sequestration in central nervous system axons. J Physiol 2000; 525: 63-73.
37. Fern R. Intracellular calcium and cell death during ischemia in neonatal rat white matter astrocytes in situ. J Neurosci 1998; 18: 7232-7243.
38. Thomas R, Salter MG, Wilke S, Husen A, Allcock N, Nivison M et al. Acute ischemic injury of astrocytes is mediated by Na-K-Cl cotransport and not Ca2+ influx at a key point in white matter development. J Neuropathol Exp Neurol 2004; 63: 856-871.
39. Salter MG, Fern R. The mechanisms of acute ischemic injury in the cell processes of developing white matter astrocytes. J Cereb Blood Flow Metab 2008; 28: 588-601.
40. Choi I, Chiu SY. Expression of high-Affinity neuronal and glial glutamate transporters in the rat optic nerve. Glia 1997; 20: 184-192.
41. Huria R, Murthy B, Al-Ghamdi B, Fern R. Pre-myelinated central axons express neurotoxic NMDA-receptors: relevance to white matter injury. J Cereb Blood Flow Metab 2015. doi10.1038/jcbfm.2014.227.
42. Mansour H, Chamberlain CG, Weible MW, 2nd, Hughes S, Chu Y, Chan-Ling T. Aging-related changes in astrocytes in the rat retina: imbalance between cell proliferation and cell death reduces astrocyte availability. Aging Cell 2008; 7: 526-540.
43. Boumezbeur F, Mason GF, de Graaf RA, Behar KL, Cline GW, Shulman GI et al. Altered brain mitochondrial metabolism in healthy aging as assessed by in vivo magnetic resonance spectroscopy. J Cereb Blood Flow Metab 2010; 30: 211-221.