Mechanisms underlying the protective effects of myricetin and quercetin following oxygen-glucose deprivation-induced cell swelling and the reduction in glutamate uptake in glial cells

Neuroscience

Volumn 183, Issue , 2011, Pages 1-14

  Panickar, K S ^a   Anderson, R A ^a  

^a BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

Author keywords

Brain edema; Calcium; Flavonoids; Ischemia; Mitochondria; Polyphenols

Indexed keywords

CYCLOSPORIN A; DANTROLENE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; FLAVONOID; GLUTAMIC ACID; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MYRICETIN; NIFEDIPINE; NIMODIPINE; QUERCETIN; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TACROLIMUS; VERAPAMIL;

ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN EDEMA; BRAIN ISCHEMIA; BRAIN PROTECTION; CALCIUM CELL LEVEL; CELL CULTURE; CELL MEMBRANE DEPOLARIZATION; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; CULTURE MEDIUM; DRUG STRUCTURE; GLIA CELL; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL;

ANIMALS; ANOXIA; CALCIUM; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; EDEMA; FLAVONOIDS; GLIOMA; GLUCOSE; GLUTAMIC ACID; INTRACELLULAR FLUID; MEMBRANE POTENTIAL, MITOCHONDRIAL; NEUROGLIA; NEUROPROTECTIVE AGENTS; QUERCETIN; RATS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; TIME FACTORS;

EID: 79955581589     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.03.064     Document Type: Article

References (97)

1. Abib R.T., Quincozes-Santos A., Nardin P., Wofchuk S.T., Perry M.L., Gonçalves C.A. Epicatechin gallate increases glutamate uptake and S100B secretion in C6 cell lineage. Mol Cell Biochem 2008, 310(1-2):153-158.
2. Akimova O.A., Grygorczyk A., Bundey R.A., Bourcier N., Gekle M., Insel P.A., Orlov S.N. Transient activation and delayed inhibition of Na+,K+,Cl- cotransport in ATP-treated C11-MDCK cells involve distinct P2Y receptor subtypes and signaling mechanisms. J Biol Chem 2006, 281(42):31317-31325.
3. Albers G.W. Diffusion-weighted MRI for evaluation of acute stroke. Neurology 1998, 51(3 Suppl 3):S47-S49.
4. ArunaDevi R., Lata S., Bhadoria B.K., Ramteke V.D., Kumar S., Sankar P., Kumar D., Tandan S.K. Neuroprotective effect of 5,7,3',4',5'-pentahydroxy dihydroflavanol-3-O-(2''-O-galloyl)-beta-D-glucopyranoside, a polyphenolic compound in focal cerebral ischemia in rat. Eur J Pharmacol 2010, 626(2-3):205-212.
5. Bastianetto S., Zheng W.H., Quirion R. Neuroprotective abilities of resveratrol and other red wine constituents against nitric oxide-related toxicity in cultured hippocampal neurons. Br J Pharmacol 2000, 131(4):711-720.
6. Bernardi P., Krauskopf A., Basso E., Petronilli V., Blachly-Dyson E., Di Lisa F., Forte M.A. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J 2006, 273(10):2077-2099.
7. Bravo L. Polyphenols: chemistry, dietary sources, metabolism, and nutritional significance. Nutr Rev 1998, 56:317-333.
8. Brott T., Bogousslavsky J. Treatment of acute ischemic stroke. N Engl J Med 2000, 343(10):710-722.
9. Cho J.Y., Kim I.S., Jang Y.H., Kim A.R., Lee S.R. Protective effect of quercetin, a natural flavonoid against neuronal damage after transient global cerebral ischemia. Neurosci Lett 2006, 404(3):330-335.
10. Connern C.P., Halestrap A.P. Recruitment of mitochondrial cyclophilin to the mitochondrial inner membrane under conditions of oxidative stress that enhance the opening of a calcium-sensitive non-specific channel. Biochem J 1994, 302(Pt 2):321-324.
11. Cushnie T.P., Lamb A.J. Antimicrobial activity of flavonoids. Int J Antimicrob Agents 2005, 26(5):343-356.
12. Dajas F., Rivera F., Blasina F., Arredondo F., Echeverry C., Lafon L., Morquio A., Heizen H. Cell culture protection and in vivo neuroprotective capacity of flavonoids. Neurotox Res 2003, 5(6):425-432.
13. Dajas F., Rivera-Megret F., Blasina F., Arredondo F., Abin-Carriquiry J.A., Costa G., Echeverry C., Lafon L., Heizen H., Ferreira M., Morquio A. Neuroprotection by flavonoids. Braz J Med Biol Res 2003, 36(12):1613-1620.
14. Danbolt N.C. Glutamate uptake. Prog Neurobiol 2001, 65(1):1-105.
15. de Almeida L.M., Piñeiro C.C., Leite M.C., Brolese G., Tramontina F., Feoli A.M., Gottfried C., Gonçalves C.A. Resveratrol increases glutamate uptake, glutathione content, and S100B secretion in cortical astrocyte cultures. Cell Mol Neurobiol 2007, 27(5):661-668.
16. de Almeida L.M., Piñeiro C.C., Leite M.C., Brolese G., Leal R.B., Gottfried C., Gonçalves C.A. Protective effects of resveratrol on hydrogen peroxide induced toxicity in primary cortical astrocyte cultures. Neurochem Res 2008, 33(1):8-15.
17. Domańska-Janik K., Lazarewicz J., Noremberg K., Strosznajder J., Zalewska T. Metabolic disturbances of synaptosomes isolated from ischemic gerbil brain. Neurochem Res 1985, 10(5):649-665.
18. Drejer J., Larsson O.M., Schousboe A. Characterization of l-glutamate uptake into and release from astrocytes and neurons cultured from different brain regions. Exp Brain Res 1982, 47(2):259-269.
19. Drejer J., Benveniste H., Diemer N.H., Schousboe A. Cellular origin of ischemia-induced glutamate release from brain tissue in vivo and in vitro. J Neurochem 1985, 45(1):145-151.
20. Fischer R., Schliess F., Häussinger D. Characterization of the hypo-osmolarity-induced Ca2+ response in cultured rat astrocytes. Glia 1997, 20(1):51-58.
21. Franceschini D., Giusti P., Skaper S.D. MEK inhibition exacerbates ischemic calcium imbalance and neuronal cell death in rat cortical cultures. Eur J Pharmacol 2006, 553(1-3):18-27.
22. Garcia J.H., Kalimo H., Kamijyo Y., Trump B.F. Cellular events during partial cerebral ischemia. I. Electron microscopy of feline cerebral cortex after middle-cerebral-artery occlusion. Virchows Arch B Cell Pathol 1977, 25(3):191-206.
23. Gassen M., Youdim M.B. Free radical scavengers: chemical concepts and clinical relevance. J Neural Transm Suppl 1999, 56:193-210.
24. Gegelashvili G., Schousboe A. High affinity glutamate transporters: regulation of expression and activity. Mol Pharmacol 1997, 52:6-15.
25. Gunter T.E., Pfeiffer D.R. Mechanisms by which mitochondria transport calcium. Am J Physiol 1990, 258(5 Pt 1):C755-C786.
26. Gutierrez-Diaz J.A., Cuevas P., Reimers D., Dujovny M., Diaz F.G., Ausman J.I. Quantitative electron microscopic study of calcium accumulation in cerebral ischemia mitochondria. Surg Neurol 1985, 24(1):67-72.
27. Ha H.J., Kwon Y.S., Park S.M., Shin T., Park J.H., Kim H.C., Kwon M.S., Wie M.B. Quercetin attenuates oxygen-glucose deprivation- and excitotoxin-induced neurotoxicity in primary cortical cell cultures. Biol Pharm Bull 2003, 26(4):544-546.
28. Häkkinen S.H., Kärenlampi S.O., Heinonen I.M., Mykkänen H.M., Törrönen A.R. Content of the flavonols quercetin, myricetin, and kaempferol in 25 edible berries. J Agric Food Chem 1999, 47(6):2274-2279.
29. Hamaguchi T., Ono K., Murase A., Yamada M. Phenolic compounds prevent Alzheimer's pathology through different effects on the amyloid-beta aggregation pathway. Am J Pathol 2009, 75(6):2557-2565.
30. Hou Y., Aboukhatwa M.A., Lei D.L., Manaye K., Khan I., Luo Y. Anti-depressant natural flavonols modulate BDNF and beta amyloid in neurons and hippocampus of double TgAD mice. Neuropharmacology 2010, 58(6):911-920.
31. Hwang I.K., Lee C.H., Yoo K.Y., Choi J.H., Park O.K., Lim S.S., Kang I.J., Kwon D.Y., Park J., Yi J.S., Bae Y.S., Won M.H. Neuroprotective effects of onion extract and quercetin against ischemic neuronal damage in the gerbil hippocampus. J Med Food 2009, 12(5):990-995.
32. Inanami O., Watanabe Y., Syuto B., Nakano M., Tsuji M., Kuwabara M. Oral administration of (-)catechin protects against ischemia-reperfusion-induced neuronal death in the gerbil. Free Radic Res 1998, 29(4):359-365.
33. Ito U., Go K.G., Walker J.T., Spatz M., Klatzo I. Experimental cerebral ischemia in Mongolian gerbils III. Behaviour of the blood-brain barrier. Acta Neuropathol 1976, 34(1):1-6.
34. Ito U., Ohno K., Nakamura R., Suganuma F., Inaba Y. Brain edema during ischemia and after restoration of blood flow. Measurement of water, sodium, potassium content and plasma protein permeability. Stroke 1979, 10(5):542-547.
35. Jayakumar A.R., Panickar K.S., Murthy ChR., Norenberg M.D. Oxidative stress and mitogen-activated protein kinase phosphorylation mediate ammonia-induced cell swelling and glutamate uptake inhibition in cultured astrocytes. J Neurosci 2006, 26(18):4774-4784.
36. Jayakumar A.R., Rao K.V., Panickar K.S., Moriyama M., Reddy P.V., Norenberg M.D. Trauma-induced cell swelling in cultured astrocytes. J Neuropathol Exp Neurol 2008, 67(5):417-427.
37. Kääriäinen T.M., Piltonen M., Ossola B., Kekki H., Lehtonen S., Nenonen T., Lecklin A., Raasmaja A., Männistö P.T. Lack of robust protective effect of quercetin in two types of 6-hydroxydopamine-induced parkinsonian models in rats and dopaminergic cell cultures. Brain Res 2008, 1203:149-159.
38. Kempuraj D., Madhappan B., Christodoulou S., Boucher W., Cao J., Papadopoulou N., Cetrulo C.L., Theoharides T.C. Flavonols inhibit proinflammatory mediator release, intracellular calcium ion levels and protein kinase C theta phosphorylation in human mast cells. Br J Pharmacol 2005, 145(7):934-944.
39. Kimelberg H.K. Current concepts of brain edema. Review of laboratory investigations. J Neurosurg 1995, 83(6):1051-1059.
40. Kimelberg H.K., Rutledge E., Goderie S., Charniga C. Astrocytic swelling due to hypotonic or high K+ medium causes inhibition of glutamate and aspartate uptake and increases their release. J Cereb Blood Flow Metab 1995, 15(3):409-416.
41. Kimelberg H.K. Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy. Glia 2005, 50(4):389-397.
42. Klatzo I. Presidental address. Neuropathological aspects of brain edema. J Neuropathol Exp Neurol 1967, 26(1):1-14.
43. Kletzien R.F., Pariza M.W., Becker J.E., Potter V.R. A method using 3-O-methyl-d-glucose and phloretin for the determination of intracellular water space of cells in monolayer culture. Anal Biochem 1975, 68(2):537-544.
44. Kovalenko T.M., Osadchenko I.O., Tsupykov O.M., Pivneva T.A., Shalamai A.S., Moibenko O.O., Skybo H.H. Neuroprotective effect of quercetin during experimental brain ischemia. Fiziol Zh 2006, 52(5):21-27. [Article in Ukrainian].
45. Kuroiwa T., Ueki M., Chen Q., Suemasu H., Taniguchi I., Okeda R. Biomechanical characteristics of brain edema: the difference between vasogenic-type and cytotoxic-type edema. Acta Neurochir Suppl (Wien) 1994, 60:158-161.
46. Lee H., Bae J.H., Lee S.R. Protective effect of green tea polyphenol EGCG against neuronal damage and brain edema after unilateral cerebral ischemia in gerbils. J Neurosci Res 2004, 77(6):892-900.
47. Lee S., Suh S., Kim S. Protective effects of the green tea polyphenol (-)-epigallocatechin gallate against hippocampal neuronal damage after transient global ischemia in gerbils. Neurosci Lett 2000, 287(3):191-194.
48. Lipski J., Park T.I., Li D., Lee S.C., Trevarton A.J., Chung K.K., Freestone P.S., Bai J.Z. Involvement of TRP-like channels in the acute ischemic response of hippocampal CA1 neurons in brain slices. Brain Res 2006, 1077(1):187-199.
49. Lytle C., McManus T. Coordinate modulation of Na-K-2Cl cotransport and K-Cl cotransport by cell volume and chloride. Am J Physiol Cell Physiol 2002, 283(5):C1422-C1431.
50. Ma Z.G., Wang J., Jiang H., Liu T.W., Xie J.X. Myricetin reduces 6-hydroxydopamine-induced dopamine neuron degeneration in rats. Neuroreport 2007, 18(11):1181-1185.
51. MacGregor D.G., Avshalumov M.V., Rice M.E. Brain edema induced by in vitro ischemia: causal factors and neuroprotection. J Neurochem 2003, 85(6):1402-1411.
52. Mellergård P., Bengtsson F., Smith M.L., Riesenfeld V., Siesjö B.K. Time course of early brain edema following reversible forebrain ischemia in rats. Stroke 1989, 20(11):1565-1570.
53. Nagai K., Jiang M.H., Hada J., Nagata T., Yajima Y., Yamamoto S., Nishizaki T. (-)-Epigallocatechin gallate protects against NO stress-induced neuronal damage after ischemia by acting as an anti-oxidant. Brain Res 2002, 956(2):319-322.
54. Nagao A., Seki M., Kobayashi H. Inhibition of xanthine oxidase by flavonoids. Biosci Biotechnol Biochem 1999, 63(10):1787-1790.
55. Namura S., Maeno H., Takami S., Jiang X.F., Kamichi S., Wada K., Nagata I. Inhibition of glial glutamate transporter GLT-1 augments brain edema after transient focal cerebral ischemia in mice. Neurosci Lett 2002, 324(2):117-120.
56. Norenberg M.D., Baker L., Norenberg L.O., Blicharska J., Bruce-Gregorios J.H., Neary J.T. Ammonia-induced astrocyte swelling in primary culture. Neurochem Res 1991, 16(7):833-836.
57. Olson J.E., Fleischhacker D., Murray W.B., Holtzman D. Control of astrocyte volume by intracellular and extracellular Ca2+. Glia 1990, 3(5):405-412.
58. Oyama Y., Fuchs P.A., Katayama N., Noda K. Myricetin and quercetin, the flavonoid constituents of Ginkgo biloba extract, greatly reduce oxidative metabolism in both resting and Ca(2+)-loaded brain neurons. Brain Res 1994, 635(1-2):125-129.
59. Panickar K.S., Jayakumar A.R., Norenberg M.D. Differential response of neural cells to trauma-induced free radical production in vitro. Neurochem Res 2002, 27(1-2):161-166.
60. Panickar K.S., Norenberg M.D. Astrocytes in cerebral ischemic injury: general and morphological considerations. Glia 2005, 50(4):287-298.
61. Panickar K.S., Nonner D., Barrett J.N. Overexpression of Bcl-xl protects septal neurons from prolonged hypoglycemia and from acute ischemia-like stress. Neuroscience 2005, 135(1):73-80.
62. Panickar K.S., Jayakumar A.R., Norenberg M.D. The mitochondrial permeability transition and MAP kinase phosphorylation in the mechanism of astrocyte swelling following in vitro trauma. Soc Neurosci Abstr 2006, 180:14.
63. Panickar K.S., Jayakumar A.R., Rama Rao K.V., Norenberg M.D. Downregulation of the 18-kDa translocator protein: effects on the ammonia-induced mitochondrial permeability transition and cell swelling in cultured astrocytes. Glia 2007, 55(16):1720-1727.
64. Panickar K.S., Polansky M.M., Anderson R.A. Cinnamon polyphenols attenuate cell swelling and mitochondrial dysfunction following oxygen-glucose deprivation in glial cells. Exp Neurol 2009, 216:420-427.
65. Panickar K.S., Polansky M.M., Anderson R.A. Green tea polyphenols attenuate glial swelling and mitochondrial dysfunction following oxygen-glucose deprivation in cultures. Nutr Neurosci 2009, 12(3):105-113.
66. Panickar K.S., Jayakumar A.R., Rama Rao K.V., Norenberg M.D. Ammonia-induced activation of p53 in cultured astrocytes: role in cell swelling and glutamate uptake. Neurochem Int 2009, 55(1-3):98-105.
67. Park H.H., Lee S., Son H.Y., Park S.B., Kim M.S., Choi E.J., Singh T.S., Ha J.H., Lee M.G., Kim J.E., Hyun M.C., Kwon T.K., Kim Y.H., Kim S.H. Flavonoids inhibit histamine release and expression of proinflammatory cytokines in mast cells. Arch Pharm Res 2008, 31(10):1303-1311.
68. Pasantes-Morales H., Cardin V., Tuz K. Signaling events during swelling and regulatory volume decrease. Neurochem Res 2000, 25(9-10):1301-1314.
69. Petito C.K., Pulsinelli W.A., Jacobson G., Plum F. Edema and vascular permeability in cerebral ischemia: comparison between ischemic neuronal damage and infarction. J Neuropathol Exp Neurol 1982, 141(4):423-436.
70. Plesnila N., Ringel F., Chang R.C., Staub F., Baethmann A. Relevance of calcium homeostasis in glial cell swelling from acidosis. Acta Neurochir Suppl 1998, 71:203-205.
71. Rama Rao K.V., Chen M., Simard J.M., Norenberg M.D. Suppression of ammonia-induced astrocyte swelling by cyclosporin A. J Neurosci Res 2003, 74(6):891-897.
72. Reichert S.A., Kim-Han J.S., Dugan L.L. The mitochondrial permeability transition pore and nitric oxide synthase mediate early mitochondrial depolarization in astrocytes during oxygen-glucose deprivation. J Neurosci 2001, 21(17):6608-6616.
73. Ringel F., Baethmann A., Plesnila N. Lactacidosis-induced glial cell swelling depends on extracellular Ca2+. Neurosci Lett 2006, 398(3):306-309.
74. Ross J.A., Kasum C.M. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu Rev Nutr 2002, 22:19-34.
75. Rossi D.J., Oshima T., Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 2000, 403:316-321.
76. Saito N., Chang C., Kawai K., Joó F., Nowak T.S., Mies G., Ikeda J., Nagashima G., Ruetzler C., Lohr J., et al. Role of neuroexcitation in development of blood-brain barrier and oedematous changes following cerebral ischaemia and traumatic brain injury. Acta Neurochir Suppl (Wien) 1990, 51:186-188.
77. Sakata Y., Zhuang H., Kwansa H., Koehler R.C., Doré S. Resveratrol protects against experimental stroke: putative neuroprotective role of heme oxygenase. Exp Neurol 2010, 224(1):325-329.
78. Scarabelli T.M., Mariotto S., Abdel-Azeim S., Shoji K., Darra E., Stephanou A., Chen-Scarabelli C., Marechal J.D., Knight R., Ciampa A., Saravolatz L., de Prati A.C., Yuan Z., Cavalieri E., Menegazzi M., Latchman D., Pizza C., Perahia D., Suzuki H. Targeting STAT1 by myricetin and delphinidin provides efficient protection of the heart from ischemia/reperfusion-induced injury. FEBS Lett 2009, 583(3):531-541.
79. Schültke E., Kamencic H., Zhao M., Tian G.F., Baker A.J., Griebel R.W., Juurlink B.H. Neuroprotection following fluid percussion brain trauma: a pilot study using quercetin. J Neurotrauma 2005, 22(12):1475-1484.
80. Schweizer M., Schlegel J., Baumgartner D., Richter C. Sensitivity of mitochondrial peptidyl-prolyl cis-trans isomerase, pyridine nucleotide hydrolysis and Ca2+ release to cyclosporine A and related compounds. Biochem Pharmacol 1993, 45(3):641-646.
81. Shimmyo Y., Kihara T., Akaike A., Niidome T., Sugimoto H. Three distinct neuroprotective functions of myricetin against glutamate-induced neuronal cell death: involvement of direct inhibition of caspase-3. J Neurosci Res 2008, 86(8):1836-1845.
82. Shutenko Z., Henry Y., Pinard E., Seylaz J., Potier P., Berthet F., Girard P., Sercombe R. Influence of the antioxidant quercetin in vivo on the level of nitric oxide determined by electron paramagnetic resonance in rat brain during global ischemia and reperfusion. Biochem Pharmacol 1999, 57(2):199-208.
83. Siesjö B.K. Cerebral circulation and metabolism. J Neurosurg 1984, 60(5):883-908.
84. Siesjö B.K. Mechanisms of ischemic brain damage. Crit Care Med 1988, 16(10):954-963.
85. Sims N.R., Finegan J.M., Blass J.P. Effects of postdecapitative ischemia on mitochondrial respiration in brain tissue homogenates. J Neurochem 1986, 47(2):506-511.
86. Swanson R.A., Choi D.W. Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J Cereb Blood Flow Metab 1993, 13(1):162-169.
87. Wang H., Joseph J.A. Structure-activity relationships of quercetin in antagonizing hydrogen peroxide-induced calcium dysregulation in PC12 cells. Free Radic Biol Med 1999, 27(5-6):683-694.
88. Wang Y.J., He F., Li X.L. The neuroprotection of resveratrol in the experimental cerebral ischemia. Zhonghua Yi Xue Za Zhi 2003, 83(7):534-536. [Article in Chinese].
89. Wedworth S.M., Lynch S. Dietary flavonoids in atherosclerosis prevention. Ann Pharmacother 1995, 29(6):627-628.
90. Weinberger J., Cohen G. The differential effect of ischemia on the active uptake of dopamine, gamma-aminobutyric acid, and glutamate by brain synaptosomes. J Neurochem 1982, 38(4):963-968.
91. Wu B.Y., Yu A.C. Quercetin inhibits c-fos, heat shock protein, and glial fibrillary acidic protein expression in injured astrocytes. J Neurosci Res 2000, 62(5):730-736.
92. Yamamoto M., Shima T., Uozumi T., Sogabe T., Yamada K., Kawasaki T. A possible role of lipid peroxidation in cellular damages caused by cerebral ischemia and the protective effect of alpha-tocopherol administration. Stroke 1983, 14(6):977-982.
93. Yao Y., Han D.D., Zhang T., Yang Z. Quercetin improves cognitive deficits in rats with chronic cerebral ischemia and inhibits voltage-dependent sodium channels in hippocampal CA1 pyramidal neurons. Phytother Res 2010, 24(1):136-140.
94. Zamzami N., Hirsch T., Dallaporta B., Petit P.X., Kroemer G. Mitochondrial implication in accidental and programmed cell death: apoptosis and necrosis. J Bioenerg Biomembr 1997, 29(2):185-193.
95. Zbarsky V., Datla K.P., Parkar S., Rai D.K., Aruoma O.I., Dexter D.T. Neuroprotective properties of the natural phenolic antioxidants curcumin and naringenin but not quercetin and fisetin in a 6-OHDA model of Parkinson's disease. Free Radic Res 2005, 39(10):1119-1125.
96. Zhu W.Z., Gao B.B., Li H.W., Zhang Y.Y., Han Q.D. Tyrosine kinase participates in alpha 1A-adrenoceptor-mediated increase of intracellular calcium in human embryo kidney 293 cells. Zhongguo Yao Li Xue Bao 1999, 20(11):1025-1230.
97. Zoratti M., Szabò I. The mitochondrial permeability transition. Biochim Biophys Acta 1995, 1241(2):139-176.