Antagonists of the vasopressin V1 receptor and of the β1-adrenoceptor inhibit cytotoxic brain edema in stroke by effects on astrocytes – But the mechanisms differ

Current Neuropharmacology

Volumn 12, Issue 4, 2014, Pages 308-323

  Hertz, Leif ^a   Xu, Junnan ^a   Chen, Ye ^b   Gibbs, Marie E ^c   Du, Ting ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Astrocyte; Brain edema; MCAO; Memory; Na+,K+ ATPase; NKCC1; Vasopressin; 1 adrenoceptor

Indexed keywords

BETA 1 ADRENERGIC RECEPTOR; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1; VASOPRESSIN V1 RECEPTOR;

ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN EDEMA; CEREBROVASCULAR ACCIDENT; HUMAN; NONHUMAN; PHOSPHORYLATION; PROTEIN EXPRESSION; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

EID: 84911481059     PISSN: 1570159X     EISSN: 18756190     Source Type: Journal    
DOI: 10.2174/1570159X12666140828222723     Document Type: Article

References (109)

1. Hossmann, K. A.; Sakaki, S.; Zimmermann, V. Ion activities in reversible ischemia of the cat brain. Acta Neurol. Scand. Suppl., 1977, 64, 108-109. PubMed ID: 268751.
2. Hansen, A. J.; Nedergaard, M. Brain ion homeostasis in cerebral ischemia. Neurochem. Pathol., 1988, 9, 195-209. DOI 10. 1007/BF03160362.
3. - cotransporter NKCC1 in mammalian epithelial cells. J. Physiol, 2010, 555(Pt 21), 4089-4101. doi: 10. 1113/jphysiol. 2010. 194738.
4. Zeuthen, T.; Macaulay, N. Cotransport of water by Na+-K+-2Cl" cotransporters expressed in Xenopus oocytes: NKCC1 versus NKCC2. J. Physiol., 2012, 590(Pt 5), 1139-1154. doi: 10. 1113/jphysiol. 2011. 226316.
5. + homeostasis and glycogen usage in brain. Neurochem. Res., 2013, 35(3), 472-485. DOI 10. 1007/s11064-012-0938-3.
6. - cotransport in the heart, brain, and blood. Am. J. Physiol Regul. Integr. Comp. Physiol, 2006, 291(1), R1-25. DOI http://dx. doi. org/10. 1152/ajpregu. 00782. 2005.
7. - cotransporter expression and inhibitory synaptogenesis in the rat hippocampus: an immuno-cytochemical analysis. Eur. J. Neurosci., 2002, 15(2), 233-245. DOI: 10. 1046/j. 0953-816x. 2001. 01854. x.
8. Deisz, R. A.; Lehmann, T. N.; Horn, P.; Dehnicke, C.; Nitsch, R. Components of neuronal chloride transport in rat and human neocortex. J. Physiol, 2011, 559(Pt 6), 1317-1347. DOI: 10. 1113/jphysiol. 2010. 201830.
9. Kanaka, C.; Ohno, K.; Okabe, A., et al. The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1, 2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience, 2001, 104(4), 933-946. DOI: 10. 1016/S0306-4522(01)00149-X.
10. Yan, Y.; Dempsey, R. J.; Sun, D. Expression of Na+-K+-Cl" cotransporter in rat brain during development and its localization in mature astrocytes. Brain Res., 2001, 911(1), 43-55. DOI: 10. 1016/S0006-8993(01)02649-X.
11. Abbruscato, T. J.; Lopez, S. P.; Roder, K.; Paulson, J. R. Regulation of blood-brain barrier Na, K, 2Cl-cotransporter through phosphorylation during in vitro stroke conditions and nicotine exposure. J. Pharmacol. Exp. Ther., 2004, 310(2), 459-468. doi: 10. 1124/jpet. 104. 066274.
12. Yuen, N.; Lam, T. I.; Wallace, B. K.; Klug, N. R.; Anderson, S. E.; O'Donnell, M. E. Ischemic factor-induced increases in cerebral micro vascular endothelial cell Na/H exchange activity and abundance: evidence for involvement of ERK1/2 MAP kinase. Am. J. Physiol Cell Physiol, 2014, 306(10): C931-942. DOI: 10. 1152/ajpcell. 00021. 2013.
13. Chen, Y.; McNeill, J. R.; Hajek, I.; Hertz, L. Effect of vasopressin on brain swelling at the cellular level: do astrocytes exhibit a furosemide vasopressin sensitive mechanism for volume regulation? Can. J. Physiol. Pharmacol, 1992, 70 Suppl, S367-373. PMID: 1295687 [PubMed-indexed for MEDLINE].
14. 2+]i in differentiated astrocytes by activation of V1b/V3 receptors but has no effect in mature cortical neurons. J. Neurosci. Res., 2000, 60(6), 761-766. DOI: 10. 1002/1097-4547(20000615)60: 6<761:: AID-JNR>8 3. 0. CO; 2-R.
15. Zadunaisky, J. A.; Curran, P. F. Sodium fluxes in isolated frog brain. Am. J. Physiol, 1963, 205(5), 949-956. PMID: 5877423.
16. Bourke, R. S.; Nelson, K. M. Further studies on the K+-dependent swelling of primate cerebral cortex in vivo: the enzymatic basis of the K+-dependent transport of chloride. J. Neurochem., 1972, 19(3), 663-685. DOI: 10. 1111/j. 1471-4159. 1972. tb01383. x.
17. Kahle, K. T.; Barnett, S. M.; Sassower, K. C.; Staley, K. J. Decreased seizure activity in a human neonate treated with bumetanide, an inhibitor of the Na+-K+-2Cl" cotransporter NKCC1. J. Child Neurol., 2009, 24(5), 572-576. doi: 10. 1177/0883073809333526.
18. Khanna, A.; Kahle, K. T.; Walcott, B. P.; Gerzanich, V.; Simard, J. M. Disruption of ion homeostasis in the neurogliovascular unit underlies the pathogenesis of ischemic cerebral edema. Transl Stroke Res., 2014, 5(1), 3-16. DOI 10. 1007/s12975-013-0307-9.
19. +-dependent chloride transporter (NKCC1)-null mice exhibit less gray and white matter damage after focal cerebral ischemia. J Cereb Blood Flow Metab., 2005, 25(1), 54-66. doi: 10. 1038/sj. jcbfm. 9600006.
20. 3-stimulated swelling and ion uptake of monkey cerebral cortex. Brain Res., 1976, 105(2), 309-323. DOI: 10. 1016/0006-8993(76)90427-3.
21. Moller, M.; Mollgård, K.; Lund-Andersen, H.; Hertz, L. Concordance between morphological and biochemical estimates of fluid spaces in rat brain cortex slices. Exp. Brain Res., 1974, 21(3), 299-314. DOI 10. 1007/BF00235749.
22. Lund-Andersen, H.; Hertz, L. Effects of potassium and of glutamate on swelling and on sodium and potassium content in brain-cortex slices from adult rats. Exp. Brain Res., 1970, 11(2), 199-212. DOI 10. 1007/BF00234323.
23. Hertz, L.; Bender, A. S.; Woodbury, D. M.; White, H. S. Potassium-stimulated calcium uptake in astrocytes and its potent inhibition by nimodipine. J. Neurosci. Res., 1989, 22(2), 209-215. DOI: 10. 1002/jnr. 490220215.
24. 2+]i and its reduction by anti-bipolar drugs in cultured astrocytes combined with its mRNA expression in freshly isolated cells support the importance of astrocytic L-channels. Cell Calcium., 2013, 54(5), 335-342. DOI: 10. 1016/j. ceca. 2013. 08. 002.
25. Hara, H.; Nagasawa, H.; Kogure, K. Nimodipine attenuates both ischaemia-induced brain oedema and mortality in a rat novel transient middle cerebral artery occlusion model. Acta Neurochir. Suppl., (Wien)., 1990, 51, 251-253. DOI 10. 1007/978-3-7091-9115-6_84.
26. Campbell, C. A.; Mackay, K. B.; Patel, S.; King, P. D.; Stretton, J. L.; Hadingham, S. J.; Hamilton, T. C. Effects of isradipine, an L-type calcium channel blocker on permanent and transient focal cerebral ischemia in spontaneously hypertensive rats. Exp. Neurol., 1997, 148(1), 45-50. DOI: 10. 1006/exnr. 1997. 6611.
27. Deguchi, K.; Yamashita, T.; Abe, K. Prevention of neuronal damage by calcium channel blockers with antioxidative effects after transient focal ischemia in rats. Brain Res., 2007, 1176, 143-150. DOI: 10. 1016/j. brainres. 2007. 07. 038.
28. +-induced swelling but follows hypotonicity-induced swelling. Neuropathology, 2011, 31(3), 250-264. DOI: 10. 1111/j. 1440-1789. 2010. 01172. x.
29. Lang, F.; Ritter, M.; Wöll, E, et al. Altered cell volume regulation in ras oncogene expressing NIH fibroblasts. Pflugers Arch., 1992, 420(5-6), 424-427. DOI 10. 1007/BF00374615.
30. Lytle, C.; Forbush, B 3rd. The Na-K-Cl cotransport protein of shark rectal gland. II. Regulation by direct phosphorylation. J. Biol Chem., 1992, 267(35), 25438-25443. PMID: 1334094.
31. - cotransporter. Am. J. Physiol, 1999, 277(6 Pt 1), C1184-1193. PubMed ID 10600770.
32. Vitari, A. C.; Thastrup, J.; Rafiqi, F. H. et al. Functional interactions of the SPAK/OSR1 kinases with their upstream activator WNK1 and downstream substrate NKCC1. Biochem. J., 2006, 397(1), 223-231. doi: 10. 1042/BJ20060220.
33. Delpire, E.; Gagnon, K. B. SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem. J., 2008, 409(2), 321-331. doi: 10. 1042/BJ20071324.
34. Hertz, L.; Xu, J.; Song, D.; Yan, E.; Gu, L.; Peng, L. Astrocytic and neuronal accumulation of elevated extracellular K+ with a 2/3 K+/Na+ flux ratio-consequences for energy metabolism, osmolarity and higher brain function. Front. Comput. Neurosci., 2013, 7, 114. doi: 10. 3389/fncom. 2013. 00114.
35. +. Sci. Signal. 2012, 5(218), ra26. DOI: 10. 1126/scisignal. 2002334.
36. Song, Y.; Gunnarson, E. Potassium dependent regulation of astrocyte water permeability is mediated by cAMP signaling. PLoS One, 2012, 7(4): e34936. DOI: 10. 1371/journal. pone. 0034936.
37. Peng, L.; Du, T.; Xu, J, et al. Adrenergic and V1-ergic Agonists/Antagonists Affecting Recovery from Brain Trauma in the Lund Project Act on Astrocytes. Curr. Signal. Transduct. Ther., 2012, 7, 43-55. DOI: 10. 2174/157436212799278115.
38. Raggenbass, M. Vasopressin-and oxytocin-induced activity in the central nervous system: electrophysiological studies using in-vitro systems. Prog. Neurobiol., 2001, 64(3), 307-326. DOI: 10. 1016/S0301-0082(00)00064-2.
39. Hösli, E.; Hösli, L. Autoradiographic localization of binding sites for second messengers on neurones and astrocytes of cultured rat cerebellum. Neurosci. Lett., 1991, 125(1), 49-52. DOI: 10. 1016/0304-3940(91)90128-G.
40. Hösli, E.; Hösli, L. Autoradiographic localization of binding sites for arginine vasopressin and atrial natriuretic peptide on astrocytes and neurons of cultured rat central nervous system. Neuroscience, 1992, 51(1), 159-166. DOI: 10. 1016/0306-4522(92)90480-P.
41. Hatton, G. I.; Bicknell, R. J.; Hoyland, J.; Bunting, R.; Mason, W. T. Arginine vasopressin mobilises intracellular calcium via V1-receptor activation in astrocytes (pituicytes) cultured from adult rat neural lobes. Brain Res., 1992, 588(1), 75-83. DOI: 10. 1016/0006-8993(92)91346-G.
42. Holmes, C. L.; Landry, D. W.; Granton, J. T. Science review: Vasopressin and the cardiovascular system part 1--receptor physiology. Crit. Care, 2003, 7(6), 427-434. PubMed ID: 14624682.
43. Thibonnier, M.; Auzan, C.; Madhun, Z.; Wilkins, P.; Berti-Mattera, L.; Clauser, E. Molecular cloning, sequencing, and functional expression of a cDNA encoding the human V1a vasopressin receptor. J. Biol. Chem., 1994, 269(5), 3304-3310. PMID: 8106369.
44. Briley, E. M.; Lolait, S. J.; Axelrod, J.; Felder, C. C. The cloned vasopressin V1a receptor stimulates phospholipase A2, phospholipase C, and phospholipase D through activation of receptor-operated calcium channels. Neuropeptides, 1994, 27(1), 63-74. DOI: 10. 1016/0143-4179(94)90017-5.
45. Thibonnier, M.; Preston, J. A.; Dulin, N.; Wilkins, P. L.; Berti-Mattera, L. N.; Mattera, R. The human V3 pituitary vasopressin receptor: ligand binding profile and density-dependent signaling pathways. Endocrinology, 1997, 138(10), 4109-4122. http://dx. doi. org/10. 1210/en. 138. 10. 4109.
46. Vakili, A.; Kataoka, H.; Plesnila, N. Role of arginine vasopressin V1 and V2 receptors for brain damage after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab., 2005, 25(8), 1012-1019. doi: 10. 1038/sjjcbfm. 9600097.
47. Liu, X.; Nakayama, S.; Amiry-Moghaddam, M.; Ottersen, O. P.; Bhardwaj, A. Arginine-vasopressin V1 but not V2 receptor antago nism modulates infarct volume, brain water content, and aquaporin-4 expression following experimental stroke. Neurocrit. Care, 2010, 12(1), 124-131. doi: 10. 1007/s12028-009-9277-x.
48. Shuaib, A.; Xu Wang, C.; Yang, T.; Noor, R. Effects of nonpeptide V(1) vasopressin receptor antagonist SR-49059 on infarction volume and recovery of function in a focal embolic stroke model. Stroke, 2002, 33(12), 3033-3037. PMID: 12468809.
49. Kleindienst, A.; Fazzina, G.; Dunbar, J. G.; Glisson, R.; Marmarou, A. Protective effect of the V1a receptor antagonist SR49059 on brain edema formation following middle cerebral artery occlusion in the rat. Acta Neurochir. Suppl., 2006, 96, 303-306. DOI 10. 1007/3-211-30714-1_65.
50. Kleindienst, A.; Dunbar, J. G.; Glisson, R.; Marmarou, A. The role of vasopressin V1A receptors in cytotoxic brain edema formation following brain injury. Acta Neurochir (Wien)., 2013, 155(1), 151-164. DOI 10. 1007/s00701-012-1558-z.
51. Matsuoka, Y.; Hossmann, K. A. Cortical impedance and extracellular volume changes following middle cerebral artery occlusion in cats. J. Cereb. Blood Flow Metab., 1982, 2(4), 466-474. doi: 10. 1038/jcbfm. 1982. 53.
52. Nielsen, T. H.; Ståhl, N.; Schalén, W.; Reinstrup, P.; Toft, P.; Nordström, C-H. Recirculation usually precedes malignant edema in middle cerebral artery infarcts. Acta Neurol. Scand., 2012, 126(6), 404-410. DOI: 10. 1111/j. 1600-0404. 2012. 01664. x.
53. Manaenko, A.; Fathali, N.; Khatibi, N. H. et al. Post-treatment with SR49059 improves outcomes following an intracerebral hemorrhagic stroke in mice. Acta Neurochir. Suppl., 2011, 111, 191-196. DOI 10. 1007/978-3-7091-0693-8_32.
54. Barreca, T.; Gandolfo, C.; Corsini, G, et al. Evaluation of the secretory pattern of plasma arginine vasopressin in stroke patients. Cerebrovasc. Dis., 2001, 11(2), 113-118. DOI: 10. 1159/000047622.
55. Liu, X. F.; Shi, Y. M.; Lin, B. C. Mechanism of action of arginine vasopressin on acute ischemic brain edema. Chin Med (Engl)., 1991, 104(6), 490-493. PMID: 1651829.
56. Dickinson, L. D.; Betz, A. L. Attenuated development of ischemic brain edema in vasopressin-deficient rats. J. Cereb. Blood Flow Metab., 1992, 12(4), 681-690. doi: 10. 1038/jcbfm. 1992. 93.
57. Del Bigio, M. R.; Fedoroff, S. Swelling of astroglia in vitro and the effect of arginine vasopressin and atrial natriuretic peptide. Acta Neurochir. Suppl (Wien)., 1990, 51, 14-16. DOI 10. 1007/978-3-7091-9115-6_5.
58. Sarfaraz, D.; Fraser, C. L. Effects of arginine vasopressin on cell volume regulation in brain astrocyte in culture. Am. J. Physiol, 1999, 276(3Pt1), E596-601. PubMed 10070029.
59. Du, T.; Song, D.; Li, H.; Li, B.; Cai, L.; Hertz, L.; Peng, L. Stimulation by vasopressin of ERK phosphorylation and vector-driven water flux in astrocytes is transactivation-dependent. Eur. J. Pharmacol, 2008, 587(1-3), 73-77. DOI: 10. 1016/j. ejphar. 2008. 03. 030.
60. 2+ transients in cells cultured from rat circumventricular organs. Brain Res., 1995, 673(2), 349-355. DOI: 10. 1016/0006-8993(95)00017-K.
61. 2+ concentration responses in non-neuronal cells of the rat dorsal root ganglion. Brain Res., 2012, 1483, 1-12. DOI: 10. 1016/j. brainres. 2012. 08. 028.
62. Gunnarson, E.; Zelenina, M.; Axehult, G., et al. Identification of a molecular target for glutamate regulation of astrocyte water permeability. Glia, 2008, 56(6), 587-596. DOI: 10. 1002/glia. 20627.
63. Niermann, H.; Amiry-Moghaddam, M.; Holthoff, K.; Witte, O. W.; Ottersen, O. P. A novel role of vasopressin in the brain: modulation of activity-dependent water flux in the neocortex. J. Neurosci., 2001, 21(9), 3045-3051. PMID: 11312289.
64. 2+-dependent glycogen hydrolysis in mouse cerebral cortex. J. Neurosci., 1988, 5(6), 1922-1928. PMID: 3385482.
65. + concentrations, or GABA. Neurochem Res., 2014, 39(4), 661-667. DOI 10. 1007/s11064-014-1244-z.
66. 2+ concentration in hippocampal and cortical astrocytes through two distinct receptors. J. Neurochem., 2007, 103(1), 229-237. DOI: 10. 1111/j. 1471-4159. 2007. 04737. x.
67. Goyagi, T.; Kimura, T.; Nishikawa, T.; Tobe, Y.; Masaki, Y. Beta-adrenoreceptor antagonists attenuate brain injury after transient focal ischemia in rats. Anesth. Analg., 2006, 103(3), 658-663. PMID: 16931677.
68. Goyagi, T.; Tobe, Y.; Nishikawa, T. Long-term and spatial memory effects of selective β1-antagonists after transient focal ischaemia in rats. Br. J. Anaesth., 2012, 109(3), 399-406. DOI: 10. 1093/bja/aes134.
69. Goyagi, T.; Horiguchi, T.; Nishikawa, T.; Tobe, Y. Post-treatment with selective β1 adrenoceptor antagonists provides neuroprotection against transient focal ischemia in rats. Brain Res., 2010, 1343, 213-217. DOI: 10. 1016/j. brainres. 2010. 04. 079.
70. Iwata, M.; Inoue, S.; Kawaguchi, M.; Nakamura, M.; Konishi, N.; Furuya, H. Posttreatment but not pretreatment with selective beta-adrenoreceptor 1 antagonists provides neuroprotection in the hippocampus in rats subjected to transient forebrain ischemia. Anesth. Analg., 2010, 110(4), 1126-1132. doi: 10. 1213/ANE. 0b013e3181d278f7.
71. Umehara, S.; Goyagi, T.; Nishikawa, T.; Tobe, Y.; Masaki, Y. Esmolol and landiolol, selective beta1-adrenoreceptor antagonists, provide neuroprotection against spinal cord ischemia and reperfusion in rats. Anesth. Analg, 2010, 110(4), 1133-1137. doi: 10. 1213/ANE. 0b013e3181cdb06b.
72. - cotransporter NKCC1 and the Na+, K+-ATPase and interacts with endogenous ouabain. Neurochem. Res., 2014, (in press). DOI: 10. 1007/s11064-014-1352-9.
73. Du, T.; Li, B.; Li, H.; Li, M.; Hertz, L.; Peng, L. Signaling pathways of isoproterenol-induced ERK1/2 phosphorylation in primary cultures of astrocytes are concentration-dependent. J. Neurochem., 2010, 115(4), 1007-1023. DOI: 10. 1111/j. 1471-4159. 2010. 06995. x.
74. +-ATPase activity in cultured mouse neurons and astrocytes. Neurochem. Int., 1996, 25(3), 335-342. DOI: 10. 1016/0197-0186(95)00081-X.
75. McGrail, K. M.; Phillips, J. M.; Sweadner, K. J. Immunofluorescent localization of three Na, K-ATPase isozymes in the rat central nervous system: both neurons and glia can express more than one Na, K-ATPase. J. Neurosci, 1991, 11(2), 381-391. PMID: 1846906.
76. +, K+-ATPase α and β isoforms and FXYD in mice treated chronically with carbamazepine, an anti-bipolar drug. Neurochem. Res., 2013, 35(4), 834-841. DOI 10. 1007/s11064-013-0986-3.
77. + concentration. Brain Res., 1972, 43(2), 437-443. DOI: 10. 1016/0006-8993(72)90399-X.
78. +)-ATPase (EC 3. 6. 1. 3) of bulk isolated glial cells, perikarya and synaptosomes from rabbit brain cortex. Brain Res., 1979, 165(1), 87-103. DOI: 10. 1016/0006-8993(79) 90047-7.
79. Bekar, L. K.; He, W.; Nedergaard, M. Locus coeruleus alpha-adrenergic-mediated activation of cortical astrocytes in vivo. Cereb. Cortex., 2008, 15(12), 2789-2795. doi: 10. 1093/cercor/bhn040.
80. Bay, V.; Butt, A. M. Relationship between glial potassium regulation and axon excitability: a role for glial Kir4. 1 channels. Glia, 2012, 60(4), 651-660. DOI: 10. 1002/glia. 22299.
81. Siesjö, B. K.; Bengtsson, F. Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: a unifying hypothesis. J. Cereb. Blood Flow Metab., 1989, 9(2), 127-140. doi: 10. 1038/jcbfm. 1989. 20.
82. Pérez-Pinzón, M. A.; Mumford, P. L.; Carranza, V.; Sick, T. J. Calcium influx from the extracellular space promotes NADH hyperoxidation and electrical dysfunction after anoxia in hippocampal slices. J. Cereb. Blood Flow Metab., 1998, 15(2), 215-221. doi: 10. 1097/00004647-199802000-00013.
83. 2+ exchange in hypoxia-related acute astrocyte death. Glia, 2005, 49(1), 143-152. DOI: 10. 1002/glia. 20107.
84. + homeostasis? Neuron Glia Biol., 2010, 6(2), 127-135. DOI: http://dx. doi. org/10. 1017/S1740925X10000013.
85. Darbin, O.; Carre, E.; Naritoku, D.; Risso, J. J.; Lonjon, M.; Patrylo, P. R. Glucose metabolites in the striatum of freely behaving rats following infusion of elevated potassium. Brain Res., 2006, 1116(1), 127-131. DOI: 10. 1016/j. brainres. 2006. 06. 095.
86. Ashford, C. A.; Dixon, K. C. The effect of potassium on the glucolysis of brain tissue with reference to the Pasteur effect. Biochem J., 1935, 29(1), 157-168. PMCID: PMC1266469.
87. Hertz, L.; Schou, M.; Univalent cations and the respiration of brain-cortex slices. Biochem. J., 1962, 55, 93-104. PMCID: PMC1243915.
88. Hertz, L., Peng, L., Kjeldsen, C. C., O'Dowd, B. S. and Dienel, G. A. Ion, Transmitter and Drug Effects on Energy Metabolism in Astrocytes. In Hertz, L. ed., Non-Neuronal Cells of the Nervous System: Function and Dysfunction, Elsevier, Amsterdam, 2004, pp. 435-460. DOI: 10. 1016/S 1569-2558(03)31019-7.
89. Keep, R. F.; Xiang, J.; Ennis, S. R.; Beer, M. E.; Betz, A. L. Brain volume regulation during development: the role of blood-brain barrier potassium transport. Adv. Exp. Med. Biol., 1993, 331, 65-69. DOI 10. 1007/978-1-4615-2920-0_11.
90. - cotransport through ETA receptors and protein kinase C-dependent pathway in cerebral capillary endothelium. J. Neurochem., 1995, 65(4), 1588-1596. DOI: 10. 1046/j. 1471-4159. 1995. 65041588. x.
91. Siemkowicz, E.; Hansen, A. J. Brain extracellular ion composition and EEG activity following 10 minutes ischemia in normo-and hyperglycemic rats. Stroke, 1981, 12(2), 236-240. doi: 10. 1161/01. STR. 12. 2. 236.
92. Frieder, B.; Allweis, C. Memory consolidation: further evidence for the four-phase model from the time-courses of diethyldithiocarbamate and ethacrynic acid amnesias. Physiol Behav., 1982, 29(6), 1071-1075. DOI: 10. 1016/0031-9384(82)90300-6.
93. Gibbs, M. E.; Bowser, D. N.; Hutchinson, D. S.; Loiacono, R. E.; Summers, R. J. Memory processing in the avian hippocampus involves interactions between beta-adrenoceptors, glutamate receptors, and metabolism. Neuropsychopharmacology, 2008, 33(12), 2831-2846. doi: 10. 1038/npp. 2008. 5.
94. Gibbs, M. E.; Ng, K. T. Psychobiology of memory: Towards a model of memory formation. Biobehav. Rev., 1977, 1, 113-136. DOI: 10. 1016/0147-7552(77)90017-1.
95. Daisley, J. N.; Gruss, M.; Rose, S. P.; Braun, K. Passive avoidance training and recall are associated with increased glutamate levels in the intermediate medial hyperstriatum ventrale of the day-old chick. Neural Plast., 1998, 6(3), 53-61. http://dx. doi. org/10. 1155/ NP. 1998. 53.
96. Daisley, J. N.; Rose, S. P. Amino acid release from the intermediate medial hyperstriatum ventrale (IMHV) of day-old chicks following a one-trial passive avoidance task. Neurobiol. Learn Mem., 2002, 77(2), 185-201. DOI: 10. 1006/nlme. 2001. 4011.
97. Gibbs, M. E.; Hutchinson, D.; Hertz, L. Astrocytic involvement in learning and memory consolidation. Neurosci. Biobehav., Rev., 2008, 32(5), 927-944. DOI: 10. 1016/j. neubiorev. 2008. 02. 001.
98. Gibbs, M. E.; Shleper, M.; Mustafa, T.; Burnstock, G.; Bowser, D. N. ATP derived from astrocytes modulates memory in the chick. Neuron Glia Biol., 2011, 7(2-4), 177-86. DOI: http://dx. doi. org/ 10. 1017/S1740925X12000117.
99. Khanna, A.; Kahle, K. T.; Walcott, B. P.; Gerzanich, V.; Simard, J. M. Disruption of ion homeostasis in the neurogliovascular unit underlies the pathogenesis of ischemic cerebral edema. Transl. Stroke Res., 2014, 5(1), 3-16. DOI 10. 1007/s12975-013-0307-9.
100. Thomas, R. C. Electrogenic sodium pump in nerve and muscle cells. Physiol. Rev., 1972, 52(3), 563-594. PMID: 4555514.
101. +-ATPase in reconstituted lipid vesicles. Biochim. Biophys. Acta., 1989, 981(2), 326-336. DOI: 10. 1016/0005-2736(89)90044-8.
102. Schuier, F. J.; Hossmann, K. A. Experimental brain infarcts in cats. II. Ischemic brain edema. Stroke., 1980, 11(6), 593-601. doi: 10. 1161/01. STR. 11. 6. 593.
103. Asgeirsson, B.; Grände P. O.; Nordström, C-H. A new therapy of post-trauma brain oedema based on haemodynamic principles for brain volume regulation. Intens. Care Med., 1994, 20(4), 260-267. DOI 10. 1007/BF01708961.
104. De Raedt, S.; Haentjens, P.; De Smedt, A. et al. Pre-stroke use of beta-blockers does not affect ischaemic stroke severity and outcome. Eur. J. Neurol., 2012, 19(2), 234-240. DOI: 10. 1111/j. 1468-1331. 2011. 03475. x.
105. Duncan, G. E.; Little, K. Y.; Koplas, P. A.; Kirkman, J. A.; Breese, G. R.; Stumpf, W. E. Beta-adrenergic receptor distribution in human and rat hippocampal formation: marked species differences. Brain Res., 1991, 561(1), 84-92. DOI: 10. 1016/0006-8993(91)90752-H.
106. Little, K. Y.; Duncan, G. E.; Breese, G. R.; Stumpf, W. E. Beta-adrenergic receptor binding in human and rat hypothalamus. Biol Psychiatry., 1992, 32(6): 512-522. PMID: 1332783.
107. Russo-Neustadt, A.; Cotman, C. W. Adrenergic receptors in Alzheimer's disease brain: selective increases in the cerebella of aggressive patients. J. Neurosci., 1997, 17(14), 5573-5580. PMID: 9204938.
108. 2+]i. Neurochem. Int., 2010, 57(4), 411-420. DOI: 10. 1016/j. neuint. 2010. 03. 019.
109. 3H]dihydroalprenolol binding to beta adrenergic receptors in multiple sclerosis brain. Neurosci. Lett., 2000, 289(1), 75-77. DOI: 10. 1016/S0304-3940 (00)01254-4.