Pathological alterations of astrocytes in stroke-prone spontaneously hypertensive rats under ischemic conditions

Neurochemistry International

Volumn 60, Issue 1, 2012, Pages 91-98

  Yamagata, Kazuo ^a  

^a NIHON UNIVERSITY   (Japan)

Author keywords

Astrocytes; GDNF; Ischemia; Lactate; SHRSP; Stroke

Indexed keywords

CELL ADHESION MOLECULE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NITRIC OXIDE; SERINE; VASCULAR CELL ADHESION MOLECULE 1;

ASTROCYTE; HYPOXIA; ISCHEMIA; NERVE CELL; NERVE CELL NECROSIS; NEUROLOGIC DISEASE; NONHUMAN; NUTRITIONAL STATUS; PRIORITY JOURNAL; RAT; REOXYGENATION; REVIEW; STROKE; TIGHT JUNCTION;

RATTUS;

EID: 83455211541     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.11.002     Document Type: Short Survey

References (102)

1. N.J. Abbott, L. Ronnback, and E. Hansson Astrocyte-endothelial interactions at the blood-brain barrier Nat. Rev. Neurosci. 7 2006 41 53 (Pubitemid 41828930)
2. I. Allaman, M. Belanger, and P.J. Magistretti Astrocyte-neuron metabolic relationships: for better and for worse Trends Neurosci. 34 2011 76 87
3. G. Azarias, H. Perreten, S. Lengacher, D. Poburko, N. Demaurex, P.J. Magistretti, and J.Y. Chatton Glutamate transport decreases mitochondrial pH and modulates oxidative metabolism in astrocytes J. Neurosci. 31 2011 3550 3559
4. Barreto, G., White, R.E., Ouyang, Y., Xu, L., Giffard, R.G., Astrocytes: targets for neuroprotection in stroke. Cent. Nerv. Syst. Agents Med. Chem. 2011 Apr 27. (in press).
5. J. Beck, B. Lenart, D.B. Kintner, and D. Sun Na-K-Cl cotransporter contributes to glutamate-mediated excitotoxicity J. Neurosci. 23 2003 5061 5068 (Pubitemid 36793233)
6. P.G. Bittar, Y. Charnay, L. Pellerin, C. Bouras, and P.J. Magistretti Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain J. Cereb. Blood Flow Metab. 16 1996 1079 1089 (Pubitemid 26365358)
7. A.K. Bouzier-Sore, P. Voisin, P. Canioni, P.J. Magistretti, and L. Pellerin Lactate is a preferential oxidative energy substrate over glucose for neurons in culture J. Cereb. Blood Flow Metab. 23 2003 1298 1306 (Pubitemid 37409793)
8. V. Bramanti, D. Tomassoni, M. Avitabile, F. Amenta, and R. Avola Biomarkers of glial cell proliferation and differentiation in culture Front Biosci. 2 2010 558 570
9. S. Broer, B. Rahman, G. Pellegri, L. Pellerin, J.L. Martin, S. Verleysdonk, B. Hamprecht, and P.J. Magistretti Comparison of lactate transport in astroglial cells and monocarboxylate transporter 1 (MCT1) expressing Xenopus laevis oocytes. Expression of two different monocarboxylate transporters in astroglial cells and neurons J. Biol. Chem. 272 1997 30096 30102 (Pubitemid 27512206)
10. P. Cao, O. Ito, Q. Guo, D. Ito, Y. Muroya, R. Rong, T. Mori, S. Ito, and M. Kohzuki Endogenous hydrogen peroxide up-regulates the expression of nitric oxide synthase in the kidney of SHR J. Hypertens. 29 2011 1167 1174
11. Y. Chen, and R.A. Swanson Astrocytes and brain injury J. Cereb. Blood Flow Metab. 23 2003 137 149 (Pubitemid 36188452)
12. R. Ciccarelli, P. Di Iorio, V. Bruno, G. Battaglia, I. D'Alimonte, M. D'Onofrio, F. Nicoletti, and F. Caciagli Activation of A(1) adenosine or mGlu3 metabotropic glutamate receptors enhances the release of nerve growth factor and S-100beta protein from cultured astrocytes Glia 27 1999 275 281 (Pubitemid 29413918)
13. D.B. Clemow, J.M. Spitsbergen, R. McCarty, W.D. Steers, and J.B. Tuttle Arterial nerve growth factor (NGF) mRNA, protein, and vascular smooth muscle cell NGF secretion in hypertensive and hyperactive rats Exp. Cell Res. 244 1998 196 205 (Pubitemid 28480867)
14. R. Dringen, H. Peters, H. Wiesinger, and B. Hamprecht Lactate transport in cultured glial cells Dev. Neurosci. 17 1995 63 69
15. L.C. Edsall, G.G. Pirianov, and S. Spiegel Involvement of sphingosine 1-phosphate in nerve growth factor-mediated neuronal survival and differentiation J. Neurosci. 17 1997 6952-6269
16. M. Furuse, H. Sasaki, K. Fujimoto, and S. Tsukita A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts J. Cell Biol. 143 1998 391 401 (Pubitemid 28487858)
17. T. Gemba, M. Ninomiya, K. Matsunaga, and M. Ueda Changes in extracellular concentration of amino acids in the hippocampus during cerebral ischemia in stroke-prone SHR, stroke-resistant SHR and normotensive rats Neurosci. Lett. 135 1992 184 188
18. K. Gotoh, H. Kikuchi, H. Kataoka, I. Nagata, K. Nozaki, J.C. Takahashi, and F. Hazama Altered nitric oxide synthase immunoreactivity in the brain of stroke-prone spontaneously hypertensive rats Acta. Neuropathol. 92 1996 123 129 (Pubitemid 26248454)
19. E. Gouix, F. Leveille, O. Nicole, C. Melon, L. Had-Aissouni, and A. Buisson Reverse glial glutamate uptake triggers neuronal cell death through extrasynaptic NMDA receptor activation Mol. Cell Neurosci. 40 2009 463 473
20. 2 production contributes to chronic glutamate toxicity in primary cortical neurons Exp. Cell Res. 316 2010 1651 1661
21. A. Haberg, H. Qu, and U. Sonnewald Glutamate and GABA metabolism in transient and permanent middle cerebral artery occlusion in rat: importance of astrocytes for neuronal survival Neurochem. Int. 48 2006 531 540
22. N. Hagen, M. Hans, D. Hartmann, D. Swandulla, and G. van Echten-Deckert. Sphingosine-1-phosphate links glycosphingolipid metabolism to neurodegeneration via a calpain-mediated mechanism Cell Death Differ 18 2011 1356 1365
23. Y.A. Hannun, and L.M. Obeid Principles of bioactive lipid signalling: lessons from sphingolipids Nat. Rev. Mol. Cell Biol. 9 2008 139 150 (Pubitemid 351158911)
24. K. Hayakawa, T. Nakano, K. Irie, S. Higuchi, M. Fujioka, K. Orito, K. Iwasaki, G. Jin, E.H. Lo, K. Mishima, and M. Fujiwara Inhibition of reactive astrocytes with fluorocitrate retards neurovascular remodeling and recovery after focal cerebral ischemia in mice J. Cereb. Blood Flow Metab. 30 2010 871 882
25. C.E. Henderson, H.S. Phillips, R.A. Pollock, A.M. Davies, C. Lemeulle, M. Armanini, L. Simmons, B. Moffet, R.A. Vandlen, and L.C. Simpson GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle Science 266 1994 1062 1064 (Pubitemid 24373728)
26. H. Kitagawa, T. Hayashi, Y. Mitsumoto, N. Koga, Y. Itoyama, and K. Abe Reduction of ischemic brain injury by topical application of glial cell line-derived neurotrophic factor after permanent middle cerebral artery occlusion in rats Stroke 29 1998 1417 1422 (Pubitemid 28300081)
27. Z. Kokaia, M.S. Airaksinen, A. Nanobashvili, E. Larsson, E. Kujamaki, O. Lindvall, and M. Saarma GDNF family ligands and receptors are differentially regulated after brain insults in the rat Eur.J. Neurosci. 11 1999 1202 1216 (Pubitemid 29142180)
28. L.F. Lin, D.H. Doherty, J.D. Lile, S. Bektesh, and F. Collins GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons Science 260 1993 1130 1132 (Pubitemid 23186789)
29. T.N. Lin, Y.P. Wong, J.J. Chen, J.T. Cheng, S.F. Yu, S.H. Sun, S.I. Chi, and C.Y. Chai Elevated basic fibroblast growth factor levels in stroke-prone spontaneously hypertensive rats Neuroscience. 76 1997 557 570 (Pubitemid 27008484)
30. C.H. Lin, F.C. Cheng, Y.Z. Lu, L.F. Chu, C.H. Wang, and C.M. Hsueh Protection of ischemic brain cells is dependent on astrocyte-derived growth factors and their receptors Exp. Neurol. 201 2006 225 233
31. M. Maceyka, S.G. Payne, S. Milstien, and S. Spiegel Sphingosine kinase, sphingosine-1-phosphate, and apoptosis Biochim. Biophys. Acta. 1585 2002 193 201 (Pubitemid 36096858)
32. P.J. Magistretti Cellular bases of functional brain imaging: insights from neuron-glia metabolic coupling Brain Res. 886 2000 108 112
33. S. Matsuda, T.C. Wen, F. Morita, H. Otsuka, K. Igase, H. Yoshimura, and M. Sakanaka Interleukin-6 prevents ischemia-induced learning disability and neuronal and synaptic loss in gerbils Neurosci. Lett. 204 1996 109 112 (Pubitemid 26053684)
34. C. McNeill-Blue, B.A. Wetmore, J.F. Sanchez, W.J. Freed, and B.A. Merrick Apoptosis mediated by p53 in rat neural AF5 cells following treatment with hydrogen peroxide and staurosporine Brain Res. 1112 2006 1 15 (Pubitemid 44363064)
35. J. Mitoma, S. Furuya, and Y. Hirabayashi A novel metabolic communication between neurons and astrocytes: non-essential amino acid l-serine released from astrocytes is essential for developing hippocampal neurons Neurosci. Res. 30 1998 195 199 (Pubitemid 28127840)
36. H. Miyazaki, Y. Okuma, Y. Fujii, K. Nagashima, and Y. Nomura Glial cell line-derived neurotrophic factor protects against delayed neuronal death after transient forebrain ischemia in rats Neuroscience 89 1999 643 647 (Pubitemid 29070992)
37. B. Moffet, R.A. Vandlen, and L.C. Simpson GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle Science 266 1994 1062 1064 (Pubitemid 24373728)
38. H.W. Muller, U. Junghans, and J. Kappler Astroglial neurotrophic and neurite-promoting factors Pharmacol. Ther. 65 1995 1 18 (Pubitemid 24381834)
39. A. Nagaoka, H. Iwatsuka, Z. Suzuoki, and K. Okamoto Genetic predisposition to stroke in spontaneously hypertensive rats Am. J. Physiol. 230 1976 1354 1359
40. M. Nedergaard, and U. Dirnagl Role of glial cells in cerebral ischemia Glia 50 2005 281 286 (Pubitemid 40780834)
41. J. O'Brien, K.M. Kla, I.B. Hopkins, E.A. Malecki, and M.C. McKenna Kinetic parameters and lactate dehydrogenase isozyme activities support possible lactate utilization by neurons Neurochem Res. 32 2007 597 607 (Pubitemid 46481292)
42. K. Okamoto, Y. Yamori, and K. Nagaoka Establishment of the stroke-prone spontaneously hypertensive rats (SHR) Circ. Res. 35 suppl 1 1974 1143 1153
43. Y. Ou, S. Yu, Y. Kaneko, N. Tajiri, E.C. Bae, S.H. Chheda, C.E. Stahl, T. Yang, L. Fang, K. Hu, C.V. Borlongan, and G. Yu Intravenous infusion of GDNF gene-modified human umbilical cord blood CD34+ cells protects against cerebral ischemic injury in spontaneously hypertensive rats Brain Res. 1366 2010 217 225
44. M. Pekny, and M. Nilsson Astrocyte activation and reactive gliosis Glia 50 2005 427 434 (Pubitemid 40780846)
45. L. Pellerin How astrocytes feed hungry neurons Mol. Neurobiol. 32 2005 59 72 (Pubitemid 41113209)
46. L. Pellerin, and P.J. Magistretti Glutamate uptake into astrocytes stimulates aerobic glycolysis:a mechanism coupling neuronal activity to glucose utilization Proc. Natl. Acad. Sci. U S A. 91 1994 10625 10629 (Pubitemid 24329051)
47. L. Pellerin, G. Pellegri, P.G. Bittar, Y. Charnay, C. Bouras, J.L. Martin, N. Stella, and P.J. Magistretti Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle Dev. Neurosci. 20 1998 291 299 (Pubitemid 28495523)
48. J.W. Phillis, D. Song, L.L. Guyot, and M.H. O'Regan Lactate reduces amino acid release and fuels recovery of function in the ischemic brain Neurosci. Lett. 272 1999 195 198 (Pubitemid 29412976)
49. A.M. Planas, C. Justicia, M.A. Soriano, and I. Ferrer Epidermal growth factor receptor in proliferating reactive glia following transient focal ischemia in the rat brain Glia 23 1998 120 129 (Pubitemid 28229085)
50. Y. Qiu, J. Pan, Y. Li, X. Li, M. Li, I. Abukhousa, and Y. Wang Relationship between activated astrocytes and hypoxic cerebral tissue in a rat model of cerebral ischemia/reperfusion Int. J. Neurosci. 121 2011 1 7
51. C. Saha, S.K. Nigam, and B.M. Denker Involvement of Galphai2 in the maintenance and biogenesis of epithelial cell tight junctions J. Biol. Chem. 273 1998 21629 21633 (Pubitemid 28405334)
52. M. Sakurai, T. Hayashi, K. Abe, G. Yaginuma, T. Meguro, Y. Itoyama, and K. Tabayashi Induction of glial cell line-derived neurotrophic factor and c-ret porto-oncogene-like immunoreactivity in rabbit spinal cord after transient ischemia Neurosci. Lett. 276 1999 123 126 (Pubitemid 29525505)
53. Y. Sakurai-Yamashita, K. Shigematsu, K. Yamashita, and M. Niwa Expression of MCP-1 in the hippocampus of SHRSP with ischemia-related delayed neuronal death Cell Mol. Neurobiol. 26 2006 823 831
54. E. Sánchez-Mendoza, M.C. Burguete, M. Castelló-Ruiz, M.P. González, C. Roncero, J.B. Salom, C. Arce, S. Cañadas, G. Torregrosa, E. Alborch, and M.J. Oset-Gasque Transient focal cerebral ischemia significantly alters not only EAATs but also VGLUTs expression in rats: relevance of changes in reactive astroglia J. Neurochem. 113 2010 1343 1355
55. R. Savoca, U. Ziegler, and P. Sonderegger Effects of l-serine on neurons in vitro J. Neurosci. Methods 61 1995 159 167 (Pubitemid 3000693)
56. A. Schurr, R.S. Payne, J.J. Miller, and B.M. Rigor Glia are the main source of lactate utilized by neurons for recovery of function post hypoxia Brain Res. 774 1997 221 224 (Pubitemid 28007904)
57. A. Schurr, R.S. Payne, J.J. Miller, and B.M. Rigor Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation J. Neurochem 69 1997 423 426 (Pubitemid 27274200)
58. M. Schwaninger, N. Petersen, S. Prinz, S. Sallmann, M. Neher, and M. Spranger Adenosine-induced expression of interleukin-6 in astrocytes through protein kinase A and NF-IL-6 Glia 31 2000 51 58 (Pubitemid 30410873)
59. M. Simard, and M. Nedergaard The neurobiology of glia in the context of water and ion homeostasis Neuroscience 129 2004 877 896 (Pubitemid 39556241)
60. S.M. Stamatovic, R.F. Keep, and A.V. Andjelkovic Brain endothelial cell-cell junctions: how to "open" the blood brain barrier Curr. Neuropharmacol. 6 2008 179 192
61. E. Steed, M.S. Balda, and K. Matter Dynamics and functions of tight junctions Trends Cell Biol. 20 2010 142 149
62. A. Suzumura, H. Takeuchi, G. Zhang, R. Kuno, and T. Mizuno Roles of glia-derived cytokines on neuronal degeneration and regeneration Ann. NY Acad. Sci. 1088 2006 219 229 (Pubitemid 47092033)
63. R.A. Swanson, W. Ying, and T.M. Kauppinen Astrocyte influences on ischemic neuronal death Curr. Mol. Med. 4 2004 193 205 (Pubitemid 38425914)
64. M. Tagami, Y. Nara, A. Kubota, T. Sunaga, H. Maezawa, H. Fujino, and Y. Yamori Ultrastructural characteristics of occluded perforating arteries in stroke-prone spontaneously hypertensive rats Stroke 18 1987 733 740 (Pubitemid 17093864)
65. M. Tagami, Y. Nara, A. Kubota, H. Fujino, and Y. Yamori Ultrastructural changes in cerebral pericytes and astrocytes of stroke-prone spontaneously hypertensive rats Stroke 21 1990 1064 1071 (Pubitemid 20218172)
66. M. Tagami, K. Yamagata, K. Ikeda, Y. Nara, H. Fujino, A. Kubota, F. Numano, and Y. Yamori Vitamin E prevents apoptosis in cortical neurons during hypoxia and oxygen reperfusion Lab. Invest. 78 1998 1415 1429 (Pubitemid 28546085)
67. M. Tagami, K. Ikeda, K. Yamagata, Y. Nara, H. Fujino, A. Kubota, F. Numano, and Y. Yamori Vitamin E prevents apoptosis in hippocampal neurons caused by cerebral ischemia and reperfusion in stroke-prone spontaneously hypertensive rats Lab. Invest. 79 1999 609 615 (Pubitemid 29228219)
68. T. Takano, N. Oberheim, M.L. Cotrina, and M. Nedergaard Astrocytes and ischemic injury Stroke Suppl. 3 2009 S 8 12
69. E. Tani, S. Yamagata, and Y. Ito Freeze-fracture of capillary endothelium in rat brain Cell Tissue Res. 176 1977 157 165
70. D. Tomassoni, V. Bramanti, and F. Amenta Expression of aquaporins 1 and 4 in the brain of spontaneously hypertensive rats Brain Res. 1325 2010 155 163
71. A.B. Tonchev The nerve growth factor in health and unhealth neurons Arch. Ital. Biol. 2011 225 231 10.4449/aib.v149i2.1368
72. G. Trendelenburg, and U. Dirnagl Neuroprotective role of astrocytes in cerebral ischemia: focus on ischemic preconditioning Glia 50 2005 307 320 (Pubitemid 40780837)
73. M. Ueno, H. Sakamoto, H. Tomimoto, I. Akiguchi, M. Onodera, C.L. Huang, and K. Kanenishi Blood-brain barrier is impaired in the hippocampus of young adult spontaneously hypertensive rats Acta. Neuropathol. 107 2004 532 538 (Pubitemid 38779704)
74. M. Ueno, T. Nakagawa, C.L. Huang, M. Ueki, T. Kusaka, N. Hosomi, K. Kanenishi, M. Onodera, B. Wu, and H. Sakamoto The expression of P-glycoprotein is increased in vessels with blood-brain barrier impairment in a stroke-prone hypertensive model Neuropathol. Appl. Neurobiol. 35 2009 147 155
75. M. Ueno, T. Nakagawa, Y. Nagai, N. Nishi, T. Kusaka, K. Kanenishi, M. Onodera, N. Hosomi, C.L. Huang, H. Yokomise, H. Tomimoto, and H. Sakamoto The expression of CD36 in vessels with blood-brain barrier impairment in a stroke-prone hypertensive model Neuropathol. Appl. Neurobiol. 2011 1365 2990 2011.011
76. U. Vollgraf, M. Wegner, and C. Richter-Landsberg Activation of AP-1 and nuclear factor-kappaB transcription factors is involved in hydrogen peroxide-induced apoptotic cell death of oligodendrocytes J. Neurochem. 73 1999 2501 2509
77. Y. Wang, S.Z. Lin, A.L. Chiou, L.R. Williams, and B.J. Hoffer Glial cell line-derived neurotrophic factor protects against ischemia-induced injury in the cerebral cortex J. Neurosci. 17 1997 4341 4348 (Pubitemid 27220624)
78. E.R. Whittemore, D.T. Loo, J.A. Watt, and C.W. Cotman A detailed analysis of hydrogen peroxide-induced cell death in primary neuronal culture Neuroscience 67 1995 921 932
79. H. Wolburg, S. Noell, A. Mack, K. Wolburg-Buchholz, and P. Fallier-Becker Brain endothelial cells and the glio-vascular complex Cell Tissue Res. 335 2009 75 96
80. L. Xu, J.F. Emery, Y.B. Ouyang, L.A. Voloboueva, and R.G. Giffard Astrocyte targeted overexpression of Hsp72 or SOD2 reduces neuronal vulnerability to forebrain ischemia Glia. 58 2010 1042 1049
81. K. Yamagata, Y. Nara, M. Tagami, and Y. Yamori Demonstration of hereditarily accelerated proliferation in astrocytes derived from spontaneously hypertensive rats Clin. Exp. Pharmacol. Physiol. 22 1995 605 609
82. K. Yamagata, M. Tagami, Y. Nara, H. Fujino, A. Kubota, F. Numano, T. Kato, and Y. Yamori Faulty induction of blood-brain barrier functions by astrocytes isolated from stroke-prone spontaneously hypertensive rats Clin. Exp. Pharmacol. Physiol. 24 1997 686 691 (Pubitemid 27376226)
83. K. Yamagata, M. Tagami, Y. Nara, M. Mitani, A. Kubota, H. Fujino, F. Numano, T. Kato, and Y. Yamori Astrocyte-conditioned medium induces blood-brain barrier properties in endothelial cells Clin. Exp. Pharmacol. Physiol. 24 1997 710 713 (Pubitemid 27376230)
84. K. Yamagata, M. Tagami, K. Ikeda, T. Noguchi, Y. Yamori, and Y. Nara Reduced production of lactate during hypoxia and reoxygenation in astrocytes isolated from stroke-prone spontaneously hypertensive rats Neurosci. Lett. 296 2000 113 116
85. K. Yamagata, M. Tagami, K. Ikeda, S. Tsumagari, Y. Yamori, and Y. Nara Differential regulation of glial cell line-derived neurotrophic factor (GDNF) mRNA expression during hypoxia and reoxygenation in astrocytes isolated from stroke-prone spontaneously hypertensive rats Glia 37 2002 1 7 (Pubitemid 34103089)
86. K. Yamagata, M. Tagami, Y. Torii, F. Takenaga, S. Tsumagari, S. Itoh, Y. Yamori, and Y. Nara Sphingosine 1-phosphate induces the production of glial cell line-derived neurotrophic factor and cellular proliferation in astrocytes Glia 41 2003 199 206 (Pubitemid 36262197)
87. K. Yamagata, Y. Shoji, T. Terashima, and H. Yokogoshi Glutamate reduces secretion of l-serine in astrocytes isolated from stroke-prone spontaneously hypertensive rats Neuroscience 143 2006 729 737 (Pubitemid 44781283)
88. K. Yamagata, K. Hakata, A. Maeda, C. Mochizuki, H. Matsufuji, M. Chino, and Y. Yamori Adenosine induces expression of glial cell line-derived neurotrophic factor (GDNF) in primary rat astrocytes Neurosci. Res. 59 2007 467 474 (Pubitemid 350007817)
89. K. Yamagata, M. Tagami, and Y. Yamori Nitric oxide reduces astrocytic lactate production and induces neuronal vulnerability in stroke-prone spontaneously hypertensive rats Glia 56 2008 387 393 (Pubitemid 351212948)
90. K. Yamagata, M. Tagami, and Y. Yamori Neuronal vulnerability of stroke-prone spontaneously hypertensive rats to ischemia and its prevention with antioxidants such as vitamin E Neuroscience 170 2010 1 7
91. Yamagata, K., Kitazawa, T., Shinoda, M., Tagawa, C., Chino, M., Matsufuji, H., 2010b. Stroke status evoked adhesion molecule genetic alterations in astrocytes isolated from stroke-prone spontaneously hypertensive rats and the apigenin inhibition of their expression. Stroke Res. Treat. pii:386389.
92. M. Yamasaki, K. Yamada, S. Furuya, J. Mitoma, Y. Hirabayashi, and M. Watanabe 3-Phosphoglycerate dehydrogenase, a key enzyme for l-serine biosynthesis, is preferentially expressed in the radial glia/astrocyte lineage and olfactory ensheathing glia in the mouse brain J. Neurosci. 21 2001 7691 7704 (Pubitemid 32904968)
93. K. Yamashita, Y. Kataoka, Y.S. Yamashita, A. Himeno, K. Tsutsumi, M. Niwa, and K. Taniyama Glial endothelin/nitric oxide system participates in hippocampus CA1 neuronal death of SHRSP following transient forebrain ischaemia Clin. Exp. Pharmacol. Physiol. Suppl. 22 1995 S277 S278
94. K. Yamashita, Y. Kataoka, Y. Sakurai-Yamashita, K. Shigematsu, A. Himeno, M. Niwa, and K. Taniyama Involvement of glial endothelin/nitric oxide in delayed neuronal death of rat hippocampus after transient forebrain ischemia Cell Mol. Neurobiol. 20 2000 541 551 (Pubitemid 30481892)
95. Y. Yamori, and R. Horie Developmental course of hypertension and regional cerebral blood flow in stroke-prone spontaneously hypertensive rats Stroke 8 1977 456 461 (Pubitemid 8148566)
96. Y. Yamori, A. Nagaoka, and K. Okamoto Importance of genetic factors in hypertensive cerebrovascular lesions: an evidence obtained by successive selective breeding of stroke-prone and-resistant SHR Jpn. Circ. J. 38 1974 1095 1100
97. Y. Yamori, T. Igawa, T. Kanbe, Y. Nara, and M. Tagami Enhanced growth rate of cultured smooth muscle cells from spontaneously hypertensive rats Heart Vessels 4 1988 94 99 (Pubitemid 19009503)
98. Q. Yang, E.Y. Wang, X.J. Huang, W.S. Qu, L. Zhang, J.Z. Xu, W. Wang, and D.S. Tian Blocking epidermal growth factor receptor attenuates reactive astrogliosis through inhibiting cell cycle progression and protects against ischemic brain injury in rats J. Neurochem. 119 2011 644 653
99. Y. Yatomi, F. Ruan, S. Hakomori, and Y. Igarashi Sphingosine-1-phosphate: a platelet-activating sphingolipid released from agonist-stimulated human platelets Blood 86 1995 193 202
100. N. Zerangue, and M.P. Kavanaugh ASCT-1 is a neutral amino acid exchanger with chloride channel activity J. Biol. Chem. 271 1996 27991 27994 (Pubitemid 26374599)
101. F. Zhang, S.J. Vannucci, N.J. Philp, and I.A. Simpson Monocarboxylate transporter expression in the spontaneous hypertensive rat: effect of stroke J. Neurosci. Res. 79 2005 139 145 (Pubitemid 40116428)
102. Y. Zhou, H.L. Li, R. Zhao, L.T. Yang, Y. Dong, X. Yue, Y.Y. Ma, Z. Wang, J. Chen, C.L. Cui, and A.C. Yu Astrocytes express N-methyl-D-aspartate receptor subunits in development, ischemia and post-ischemia Neurochem. Res. 35 2010 2124 2134