Inhibitors of the mitochondrial permeability transition reduce ammonia-induced cell swelling in cultured astrocytes

Journal of Neuroscience Research

Volumn 87, Issue 12, 2009, Pages 2677-2685

  Reddy, Pichili V B ^a   Rama Rao, Kakulavarapu V ^a   Norenberg, Michael D ^a,b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Ammonia; Astrocyte swelling; Brain edema; Mitochondrial permeability transition

Indexed keywords

AMMONIA; CYCLOSPORIN A; MAGNESIUM; MINOCYCLINE; PYRUVATE SODIUM; PYRUVIC ACID; TRIFLUOPERAZINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN EDEMA; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; NERVE CELL CULTURE; NONHUMAN; POTENTIOMETRY; PRIORITY JOURNAL; RAT;

AMMONIA; ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN; BRAIN EDEMA; CELL SIZE; CELLS, CULTURED; CYCLOSPORINE; HEPATIC ENCEPHALOPATHY; HYPERAMMONEMIA; MAGNESIUM; MINOCYCLINE; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; PYRUVIC ACID; RATS; TRIFLUOPERAZINE; WATER-ELECTROLYTE BALANCE;

EID: 70449497896     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22097     Document Type: Article

References (86)

1. Albrecht J, Jones EA. 1999. Hepatic encephalopathy: molecular mechanisms underlying the clinical syndrome. J Neurol Sci 170:138-146.
2. Albrecht J, Norenberg MD. 2006. Glutamine: a Trojan horse in ammonia neurotoxicity. Hepatology 44:788-794. (Pubitemid 46489541)
3. Aronson AL. 1980. Pharmacotherapeutics of the newer tetracyclines. J Am Vet Med Assoc 176:1061-1068.
4. Bai G, Rama Rao KV, Murthy CR, Panickar KS, Jayakumar AR, Norenberg MD. 2001. Ammonia induces the mitochondrial permeability transition in primary cultures of rat astrocytes. J Neurosci Res 66:981-991.
5. Begley DJ, Squires LK, Zlokovic BV, Mitrovic DM, Hughes CC, Revest PA, Greenwood J. 1990. Permeability of the blood-brain barrier to the immunosuppressive cyclic peptide cyclosporin A. J Neurochem 55:1222-1230. (Pubitemid 20306022)
6. Bernardi P. 1996. The permeability transition pore. Control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death. Biochim Biophys Acta 1275:5-9.
7. Bernardi P, Vassanelli S, Veronese P, Colonna R, Szabo I, Zoratti M. 1992. Modulation of the mitochondrial permeability transition pore. Effect of protons and divalent cations. J Biol Chem 267:2934-2939.
8. Blei AT. 1991. Cerebral edema and intracranial hypertension in acute liver failure: distinct aspects of the same problem. Hepatology 13:376-379.
9. Blei AT. 2005. The pathophysiology of brain edema in acute liver failure. Neurochem Int 47:71-77. (Pubitemid 40848695)
10. Brahma B, Forman RE, Stewart EE, Nicholson C, Rice ME. 2000. Ascorbate inhibits edema in brain slices. J Neurochem 74:1263-1270. (Pubitemid 30104325)
11. Broekemeier KM, Pfeiffer DR. 1995. Inhibition of the mitochondrial permeability transition by cyclosporin A during long time frame experiments: relationship between pore opening and the activity of mitochondrial phospholipases. Biochemistry 34:16440-16449.
12. Capocaccia L, Angelico M. 1991. Fulminant hepatic failure. Clinical features, etiology, epidemiology, and current management. Dig Dis Sci 36:775-779.
13. 2+ ions is stimulated by t-butyl hydroperoxide and mediated by reactive oxygen species generated by mitochondria. Free Radic Biol Med 18:479-486.
14. Chan PH, Longar S, Chen S, Yu AC, Hillered L, Chu L, Imaizumi S, Pereira B, Moore K, Woolworth V. 1989. The role of arachidonic acid and oxygen radical metabolites in the pathogenesis of vasogenic brain edema and astrocytic swelling. Ann N Y Acad Sci 559:237-247. (Pubitemid 19215841)
15. Chen CJ, Liao SL, Kuo JS. 2000. Gliotoxic action of glutamate on cultured astrocytes. J Neurochem 75:1557-1565.
16. Cordoba J, Blei AT. 1994. Brain edema and fulminant hepatic failure. Trop Gastroenterol 15:45-54.
17. Desagher S, Glowinski J, Premont J. 1997. Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J Neurosci 17:9060-9067. (Pubitemid 27498433)
18. Dickens BF, Weglicki WB, Li YS, Mak IT. 1992. Magnesium deficiency in vitro enhances free radical-induced intracellular oxidation and cytotoxicity in endothelial cells. FEBS Lett 311:187-191.
19. Dommergues MA, Plaisant F, Verney C, Gressens P. 2003. Early microglial activation following neonatal excitotoxic brain damage in mice: a potential target for neuroprotection. Neuroscience 121:619-628. (Pubitemid 38367501)
20. Ducis I, Norenberg LO, Norenberg MD. 1990. The benzodiazepine receptor in cultured astrocytes from genetically epilepsy-prone rats. Brain Res 531:318-321. (Pubitemid 20348641)
21. Feng DF, Zhu ZA, Lu YC. 2004. Effects of magnesium sulfate on traumatic brain edema in rats. Chin J Traumatol 7:148-152. (Pubitemid 38786902)
22. Ganz R, Swain M, Traber P, DalCanto M, Butterworth RF, Blei AT. 1989. Ammonia-induced swelling of rat cerebral cortical slices: implications for the pathogenesis of brain edema in acute hepatic failure. Metab Brain Dis 4:213-223. (Pubitemid 19231231)
23. Gieseler A, Schultze AT, Kupsch K, Haroon MF, Wolf G, Siemen D, Kreutzmann P. 2009. Inhibitory modulation of the mitochondrial permeability transition by minocycline. Biochem Pharmacol 77:886-896.
24. Halestrap AP, Woodfield KY, Connern CP. 1997. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J Biol Chem 272:3346-3354. (Pubitemid 27066829)
25. Hindfelt B, Plum F, Duffy TE. 1977. Effect of acute ammonia intoxication on cerebral metabolism in rats with portacaval shunts. J Clin Invest 59:386-396. (Pubitemid 8061207)
26. Hoyt KR, Sharma TA, Reynolds IJ. 1997. Trifluoperazine and dibucaine- induced inhibition of glutamate-induced mitochondrial depolarization in rat cultured forebrain neurones. Br J Pharmacol 122:803-808.
27. Izumi Y, Roussel S, Pinard E, Seylaz J. 1991. Reduction of infarct volume by magnesium after middle cerebral artery occlusion in rats. J Cereb Blood Flow Metab 11:1025-1030.
28. Jayakumar AR, Panickar KS, Murthy Ch R, Norenberg MD. 2006. Oxidative stress and mitogen-activated protein kinase phosphorylation mediate ammonia-induced cell swelling and glutamate uptake inhibition in cultured astrocytes. J Neurosci 26:4774-4784.
29. Jayakumar AR, Rama Rao KV, Tong XY, Norenberg MD. 2009. Calcium in the mechanism of ammonia-induced astrocyte swelling. J Neurochem (in press).
30. Jones EA, Weissenborn K. 1997. Neurology and the liver. J Neurol Neurosurg Psychiatry 63:279-293.
31. Juurlink BH, Hertz L. 1985. Plasticity of astrocytes in primary cultures: an experimental tool and a reason for methodological caution. Dev Neurosci 7:263-277. (Pubitemid 16120574)
32. Kaptanoglu E, Beskonakli E, Okutan O, Selcuk Surucu H, Taskin Y. 2003. Effect of magnesium sulphate in experimental spinal cord injury: evaluation with ultrastructural findings and early clinical results. J Clin Neurosci 10:329-334. (Pubitemid 36713405)
33. Kato M, Hughes RD, Keays RT, Williams R. 1992. Electron microscopic study of brain capillaries in cerebral edema from fulminant hepatic failure. Hepatology 15:1060-1066.
34. Kerr PM, Suleiman MS, Halestrap AP. 1999. Reversal of permeability transition during recovery of hearts from ischemia and its enhancement by pyruvate. Am J Physiol 276:H496-502.
35. Kim HS, Suh YH. 2009. Minocycline and neurodegenerative diseases. Behav Brain Res 196:168-179.
36. Kimelberg HK. 1987. Anisotonic media and glutamate-induced ion transport and volume responses in primary astrocyte cultures. J Physiol (Paris) 82:294-303.
37. Kimelberg HK. 1995. Current concepts of brain edema. Review of laboratory investigations. J Neurosurg 83:1051-1059.
38. Kletzien RF, Pariza MW, Becker JE, Potter VR. 1975. A method using 3-O-methyl-D-glucose and phloretin for the determination of intracellular water space of cells in monolayer culture. Anal Biochem 68:537-544.
39. 2+. Arch Biochem Biophys 359:77-81.
40. Kuroda S, Nakai A, Kristian T, Siesjo BK. 1997. The calmodulin antagonist trifluoperazine in transient focal brain ischemia in rats. Anti-ischemic effect and therapeutic window. Stroke 28:2539-2544.
41. Landar A, Shiva S, Levonen AL, Oh JY, Zaragoza C, Johnson MS, Darley- Usmar VM. 2006. Induction of the permeability transition and cytochrome c release by 15-deoxy-Delta12,14-prostaglandin J2 in mitochondria. Biochem J 394:185-195. (Pubitemid 43259668)
42. Mallet RT, Sun J. 2003. Antioxidant properties of myocardial fuels. Mol Cell Biochem 253:103-111.
43. Marinov MB, Harbaugh KS, Hoopes PJ, Pikus HJ, Harbaugh RE. 1996. Neuroprotective effects of preischemia intraarterial magnesium sulfate in reversible focal cerebral ischemia. J Neurosurg 85:117-124.
44. Martinez A. 1968. Electron microscopy in human hepatic encephalopathy. Acta Neuropathol 11:82-86.
45. Muir KW. 2001. Magnesium for neuroprotection in ischaemic stroke: rationale for use and evidence of effectiveness. CNS Drugs 15:921-930.
46. Neumann-Haefelin T, Kastrup A, de Crespigny A, Yenari MA, Ringer T, Sun GH, Moseley ME. 2000. Serial MRI after transient focal cerebral ischemia in rats: dynamics of tissue injury, blood-brain barrier damage, and edema formation. Stroke 31:1965-1972. (Pubitemid 30620481)
47. Norenberg MD. 1977. A light and electron microscopic study of experimental portal-systemic (ammonia) encephalopathy. Progression and reversal of the disorder. Lab Invest 36:618-627.
48. Norenberg MD. 2003. Oxidative and nitrosative stress in ammonia neurotoxicity. Hepatology 37:245-248.
49. Norenberg MD, Rao KV. 2007. The mitochondrial permeability transition in neurologic disease. Neurochem Int 50:983-997. (Pubitemid 46962816)
50. Norenberg MD, Baker L, Norenberg LO, Blicharska J, Bruce-Gregorios JH, Neary JT. 1991. Ammonia-induced astrocyte swelling in primary culture. Neurochem Res 16:833-836.
51. Norenberg MD, Jayakumar AR, Rama Rao KV. 2004. Oxidative stress in the pathogenesis of hepatic encephalopathy. Metab Brain Dis 19:313-329. (Pubitemid 39361190)
52. Norenberg MD, Jayakumar AR, Rama Rao KV, Panickar KS. 2007. New concepts in the mechanism of ammonia-induced astrocyte swelling. Metab Brain Dis 22:219-234.
53. Norenberg MD, Rama Rao KV, Jayakumar AR. 2009. Signaling factors in the mechanism of ammonia neurotoxicity. Metab Brain Dis 24:103-117.
54. Novgorodov SA, Gudz TI, Brierley GP, Pfeiffer DR. 1994. Magnesium ion modulates the sensitivity of the mitochondrial permeability transition pore to cyclosporin A and ADP. Arch Biochem Biophys 311:219-228. (Pubitemid 24220137)
55. Oldendorf WH. 1973. Carrier-mediated blood-brain barrier transport of short-chain monocarboxylic organic acids. Am J Physiol 224:1450-1453.
56. Olson JE, Evers JA, Holtzman D. 1992. Astrocyte volume regulation and ATP and phosphocreatine concentrations after exposure to salicylate, ammonium, and fatty acids. Metab Brain Dis 7:183-196. (Pubitemid 23099620)
57. Peker S, Abacioglu U, Sun I, Konya D, Yuksel M, Pamir NM. 2004. Prophylactic effects of magnesium and vitamin E in rat spinal cord radiation damage: evaluation based on lipid peroxidation levels. Life Sci 75:1523-1530. (Pubitemid 38887279)
58. Pichili VB, Rao KV, Jayakumar AR, Norenberg MD. 2007. Inhibition of glutamine transport into mitochondria protects astrocytes from ammonia toxicity. Glia 55:801-809.
59. Racay P. 2008. Effect of magnesium on calcium-induced depolarisation of mitochondrial transmembrane potential. Cell Biol Int 32:136-145. (Pubitemid 351249151)
60. Rama Rao KV, Chen M, Simard JM, Norenberg MD. 2003. Suppression of ammonia-induced astrocyte swelling by cyclosporin A. J Neurosci Res 74:891-897. (Pubitemid 37490422)
61. Rama Rao KV, Jayakumar AR, Norenberg MD. 2005. Role of oxidative stress in the ammonia-induced mitochondrial permeability transition in cultured astrocytes. Neurochem Int 47:31-38. (Pubitemid 40848690)
62. Rao KV, Norenberg MD. 2004. Manganese induces the mitochondrial permeability transition in cultured astrocytes. J Biol Chem 279:32333-32338. (Pubitemid 39014685)
63. Saldeen J. 2000. Cytokines induce both necrosis and apoptosis via a common Bcl-2-inhibitable pathway in rat insulin-producing cells. Endocrinology 141:2003-2010. (Pubitemid 32274349)
64. Sato T, Morishima Y, Shirasaki Y. 2003. 3-[2-[4-(3-chloro-2-methylphenyl) - 1-piperazinyl] ethyl]-5,6-dimethoxy-1-(4-imidazolylmethyl)- 1H-in dazoledihydro chloride 3.5 hydrate (DY-9760e), a novel calmodulin antagonist, reduces brain edema through the inhibition of enhanced blood-brain barrier permeability after transient focal ischemia. J Pharmacol Exp Ther 304:1042-1047. (Pubitemid 36254416)
65. Scorrano L, Penzo D, Petronilli V, Pagano F, Bernardi P. 2001. Arachidonic acid causes cell death through the mitochondrial permeability transition. Implications for tumor necrosis factor-alpha aopototic signaling. J Biol Chem 276:12035-12040. (Pubitemid 37385366)
66. Staub F, Winkler A, Peters J, Kempski O, Baethmann A. 1994. Mechanisms of glial swelling by arachidonic acid. Acta Neurochir Suppl (Wien) 60:20-23.
67. Stirling DP, Koochesfahani KM, Steeves JD, Tetzlaff W. 2005. Minocycline as a neuroprotective agent. Neuroscientist 11:308-322.
68. Sullivan PG, Thompson MB, Scheff SW. 1999. Cyclosporin A attenuates acute mitochondrial dysfunction following traumatic brain injury. Exp Neurol 160:226-234.
69. Swain M, Butterworth RF, Blei AT. 1992. Ammonia and related amino acids in the pathogenesis of brain edema in acute ischemic liver failure in rats. Hepatology 15:449-453.
70. Tanno H, Nockels RP, Pitts LH, Noble LJ. 1992. Breakdown of the blood-brain barrier after fluid percussive brain injury in the rat. Part 1: distribution and time course of protein extravasation. J Neurotrauma 9:21-32.
71. Theruvath TP, Zhong Z, Pediaditakis P, Ramshesh VK, Currin RT, Tikunov A, Holmuhamedov E, Lemasters JJ. 2008. Minocycline and N-methyl-4-isoleucine cyclosporin (NIM811) mitigate storage/reperfusion injury after rat liver transplantation through suppression of the mitochondrial permeability transition. Hepatology 47:236-246.
72. Traber PG, Dal Canto M, Ganger DR, Blei AT. 1987. Electron microscopic evaluation of brain edema in rabbits with galactosamine-induced fulminant hepatic failure: ultrastructure and integrity of the blood-brain barrier. Hepatology 7:1272-1277. (Pubitemid 18014201)
73. Uchino H, Elmer E, Uchino K, Lindvall O, Siesjo BK. 1995. Cyclosporin A dramatically ameliorates CA1 hippocampal damage following transient forebrain ischaemia in the rat. Acta Physiol Scand 155:469-471. (Pubitemid 26017516)
74. Voorhies TM, Ehrlich ME, Duffy TE, Petito CK, Plum F. 1983. Acute hyperammonemia in the young primate: physiologic and neuropathologic correlates. Pediatr Res 17:970-975.
75. 2+-induced permeabilization promotes free radical release from rat brain mitochondria with partially inhibited complex I. J Neurochem 93:526-537.
76. Waagepetersen HS, Sonnewald U, Larsson OM, Schousboe A. 2000. A possible role of alanine for ammonia transfer between astrocytes and glutamatergic neurons. J Neurochem 75:471-479. (Pubitemid 30485427)
77. 19F NMR study of trifluoperazine crossing blood-brain-barrier due to P-glycoprotein modulation. Proc Intl Sot Mag Reson Med 8:1083.
78. Wang X, Perez E, Liu R, Yan LJ, Mallet RT, Yang SH. 2007. Pyruvate protects mitochondria from oxidative stress in human neuroblastoma SK-N-SH cells. Brain Res 1132:1-9. (Pubitemid 46096455)
79. Willard-Mack CL, Koehler RC, Hirata T, Cork LC, Takahashi H, Traystman RJ, Brusilow SW. 1996. Inhibition of glutamine synthetase reduces ammonia-induced astrocyte swelling in rat. Neuroscience 71:589-599. (Pubitemid 26067021)
80. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, Choi DK, Ischiropoulos H, Przedborski S. 2002. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of parkinson disease. J Neurosci 22:1763-1771
81. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J. 1998. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA. 95:15769-15774. (Pubitemid 29018775)
82. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu DC, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM. 2002. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417:74-78. (Pubitemid 34498818)
83. Zivin JA, Kochhar A, Saitoh T. 1989. Phenothiazines reduce ischemic damage to the central nervous system. Brain Res 482:189-193. (Pubitemid 19063168)
84. Zoratti M, Szabo I. 1995. The mitochondrial permeability transition. Biochim Biophys Acta 1241:139-176.
85. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. 2000. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192:1001-1014.
86. Zwingmann C, Flogel U, Pfeuffer J, Leibfritz D. 2000. Effects of ammonia exposition on glioma cells: changes in cell volume and organic osmolytes studied by diffusion-weighted and high-resolution NMR spectroscopy. Dev Neurosci 22:463-471.