Downregulation of the 18-kDa translocator protein: Effects on the ammonia-induced mitochondrial permeability transition and cell swelling in cultured astrocytes

GLIA

Volumn 55, Issue 16, 2007, Pages 1720-1727

  Panickar, K S ^a,b   Jayakumar, A R ^a   Rama Rao, K V ^a   Norenberg, Michael D ^a  

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

^b BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

Author keywords

18 kDa translocator protein; Ammonia toxicity; Astrocytes; Cell swelling; Hepatic encephalopathy; Mitochondrial permeability transition; Peripheral benzodiazepine receptor

Indexed keywords

18 KDA TRANSLOCATOR PROTEIN; AMMONIA; ANTISENSE OLIGONUCLEOTIDE; CARRIER PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL CULTURE; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; DOWN REGULATION; HEPATIC ENCEPHALOPATHY; MITOCHONDRIAL PERMEABILITY; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT;

AMMONIA; AMMONIUM CHLORIDE; ANIMALS; ASTROCYTES; CARRIER PROTEINS; CELL SIZE; CELLS, CULTURED; DOWN-REGULATION; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; OLIGONUCLEOTIDES, ANTISENSE; PERMEABILITY; RATS; RECEPTORS, GABA-A;

EID: 35348973583     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20584     Document Type: Article

References (77)

1. Albrecht J, Jones EA. 1999. Hepatic encephalopathy: Molecular mechanisms underlying the clinical syndrome. J Neurol Sci 170:138-146.
2. Anholt RR, Pedersen PL, De Souza EB, Snyder SH. 1986. The peripheral-type benzodiazepine receptor. Localization to the mitochondrial outer membrane. J Biol Chem 261:576-583.
3. 2+-induced permeability transition pore opening in rat brain mitochondria. Cell Calcium 42:27-39.
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. Belanger M, Desjardins P, Chatauret N, Rose C, Butterworth RF. 2005. Mild hypothermia prevents brain edema and attenuates up-regulation of the astrocytic benzodiazepine receptor in experimental acute liver failure. J Hepatol 42:694-699.
6. Bender AS, Norenberg MD. 1998. Effect of benzodiazepines and neurosteroids on ammonia-induced swelling in cultured astrocytes. J Neurosci Res 54:673-680.
7. Bernardi P, Colonna R, Costantini P, Eriksson O, Fontaine E, Ichas F, Massari S, Nicolli A, Petronilli V, Scorrano L. 1998. The mitochondrial permeability transition. Biofactors 8:273-281.
8. Bernardi P, Krauskopf A, Basso E, Petronilli V, Blachly-Dyson E, Di Lisa F, Forte MA. 2006. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J 273:2077-2099.
9. Berson A, Descatoire V, Sutton A, Fau D, Maulny B, Vadrot N, Feldmann G, Berthon B, Tordjmann T, Pessayre D. 2001. Toxicity of alpidem, a peripheral benzodiazepine receptor ligand, but not zolpidem, in rat hepatocytes: Role of mitochondrial permeability transition and metabolic activation. J Pharmacol Exp Ther 299:793-800.
10. Blei A. 2000. Hypothermia for fulminant hepatic failure: A cool approach to a burning problem. Liver Transpl 6:245-247.
11. Brahma B, Forman RE, Stewart EE, Nicholson C, Rice ME. 2000. Ascorbate inhibits edema in brain slices. J Neurochem 74:1263-70.
12. Butterworth RF. 2000. The astrocytic ("peripheral-type") benzodiazepine receptor: Role in the pathogenesis of portal-systemic encephalopathy. Neurochem Int 36:411-416.
13. Capocaccia L, Angelico M. 1991. Fulminant hepatic failure. Clinical features, etiology, epidemiology, and current management. Dig Dis Sci 36:775-779.
14. Chan PH, Yurko M, Fishman RA. 1982. Phospholipid degradation and cellular edema induced by free radicals in brain cortical slices. J Neurochem 38:525-531.
15. Chatauret N, Rose C, Butterworth RF. 2002. Mild hypothermia in the prevention of brain edema in acute liver failure: Mechanisms and clinical prospects. Metab Brain Dis 17:445-451.
16. Chelli B, Falleni A, Salvetti F, Gremigni V, Lucacchini A, Martini C. 2001. Peripheral-type benzodiazepine receptor ligands: Mitochondrial permeability transition induction in rat cardiac tissue. Biochem Pharmacol 61:695-705.
17. Clemmesen JO, Larsen FS, Kondrup J, Hansen BA, Ott P. 1999. Cerebral herniation in patients with acute liver failure is correlated with arterial ammonia concentration. Hepatology 29:648-653.
18. Córdoba J, Crespin J, Gottstein J, Blei AT. 1999. Mild hypothermia modifies ammonia-induced brain edema in rats after portacaval anastomosis. Gastroenterology 116:686-693.
19. Ducis I, Norenberg LO, Norenberg MD. 1989. Effect of ammonium chloride on the astrocyte benzodiazepine receptor. Brain Res 493:362-365.
20. Giguere JF, Hamel E, Butterworth RF. 1992. Increased densities of binding sites for the 'peripheral-type' benzodiazepine receptor ligand [3H]PK 11195 in rat brain following portacaval anastomosis. Brain Res 585:295-298.
21. Gonzalez-Polo RA, Carvalho G, Braun T, Decaudin D, Fabre C, Larochette N, Perfettini JL, Djavaheri-Mergny M, Youlyouz-Marfak I, Codogno P, Raphael M, Feuillard J, Kroemer G. 2005. PK 11195 potently sensitizes to apoptosis induction independently from the peripheral benzodiazepin receptor. Oncogene 24:7503-7513.
22. Green DR, Reed JC. 1998. Mitochondria and apoptosis. Science 281:1309-1312.
23. Hans G, Wislet-Gendebien S, Lallemend F, Robe P, Rogister B, Belachew S, Nguyen L, Malgrange B, Moonen G, Rigo JM. 2005. Peripheral benzodiazepine receptor (PBR) ligand cytotoxicity unrelated to PBR expression. Biochem Pharmacol 69:819-830.
24. Hauet T, Yao ZX, Bose HS, Wall CT, Han Z, Li W, Hales DB, Miller WL, Culty M, Papadopoulos V. 2005. Peripheral-type benzodiazepine receptor-mediated action of steroidogenic acute regulatory protein on cholesterol entry into Leydig cell mitochondria. Mol Endocrinol 19:540-554.
25. Häussinger D. 2006. Low grade cerebral edema and the pathogenesis of hepatic encephalopathy in cirrhosis. Hepatology 43:1187-1190.
26. Hazell AS, Butterworth RF. 1999. Hepatic encephalopathy: An update of pathophysiologic mechanisms. Proc Soc Exp Biol Med 222:99-112.
27. Itzhak Y, Norenberg MD. 1994. Ammonia-induced upregulation of peripheral-type benzodiazepine receptors in cultured astrocytes labeled with [3H] 11195. Neurosci Lett 177:35-38.
28. Itzhak Y, Roig-Cantisano A, Dombro RS, Norenberg MD. 1995. Acute liver failure and hyperammonemia increase peripheral-type benzodiazepine receptor binding and pregnenolone synthesis in mouse brain. Brain Res 705:345-348.
29. Jalan R, Olde Damink SW, Deutz NE, Hayes PC, Lee A. 2004. Moderate hypothermia in patients with acute liver failure and uncontrolled intracranial hypertension. Gastroenterology 127:1338-1346.
30. Jayakumar AR, Panickar KS, Murthy ChR, 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 26:4774-84.
31. Jayakumar AR, Panickar KS, Norenberg MD. 2002. Peripheral benzodiazepine receptor ligands induce the formation of free radicals in cultured neural cells. J Neurochem 83:1226-1234.
32. Jefcoate CR, McNamara BC, Artemenko I, Yamazaki T. 1992. Regulation of cholesterol movement to mitochondrial cytochrome P450scc in steroid hormone synthesis. J Steroid Biochem Mol Biol 43:751-767.
33. Jones EA, Weissenborn K. 1997. Neurology and the liver. J Neurol Neurosurg Psychiatry 63:279-293.
34. Kelly-Hershkovitz E, Weizman R, Spanier I, Leschiner S, Lahav M, Weisinger G, Gavish M. 1998. Effects of peripheral-type benzodiazepine receptor antisense knockout on MA-10 Leydig cell proliferation and steroidogenesis. J Biol Chem 6273:5478-5483.
35. Kimelberg HK. 1987. Anisotonic media and glutamate-induced ion transport and volume responses in primary astrocyte cultures. J Physiol (Paris) 82:294-303.
36. Kimelberg HK, Goderie S, Higman S, Pang S. 1989. Swelling-induced membrane transport changes in astrocytes. Acta Physiol Scand 582 (Suppl):26.
37. Kimelberg HK, Mongin AA. 1998. Swelling-activated release of excitatory amino acids in the brain: Relevance for pathophysiology. Contrib Nephrol 123:240-257.
38. + medium causes inhibition of glutamate and aspartate uptake and increases their release. J Cereb Blood Flow Metab 15:409-416.
39. 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.
40. Kroemer G, Galluzzi L, Brenner C. 2007. Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99-163.
41. Krueger KE. 1995. Molecular and functional properties of mitochondrial benzodiazepine receptors. Biochim Biophys Acta 1241:453-470.
42. Lavoie J, Layrargues GP, Butterworth RF. 1990. Increased densities of peripheral-type benzodiazepine receptors in brain autopsy samples from cirrhotic patients with hepatic encephalopathy. Hepatology 11:874-878.
43. Levin E, Premkumar A, Veenman L, Kugler W, Leschiner S, Spanier I, Weisinger G, Lakomek M, Weizman A, Snyder SH, Pasternak GW, Gavish M. 2005. The peripheral-type benzodiazepine receptor and tumorigenicity: Isoquinoline binding protein (IBP) antisense knockdown in the C6 glioma cell line. Biochemistry 44:9924-9935.
44. Li J, Wang J, Zeng Y. 2007. Peripheral benzodiazepine receptor ligand, PK 11195 induces mitochondria cytochrome c release and dissipation of mitochondria potential via induction of mitochondria permeability transition Eur J Pharmacol 560:117-122.
45. Martinez A. 1968. Electron microscopy in human hepatic encephalopathy. Acta Neuropathol (Berl) 11:82-86.
46. McEnery MW, Snowman AM, Trifiletti RR, Snyder SH. 1992. Isolation of the mitochondrial benzodiazepine receptor: Association with the voltage-dependent anion channel and the adenine nucleotide carrier. Proc Natl Acad Sci USA 89:3170-3174.
47. Murthy ChRK, Rama Rao KV, Bai G, Norenberg MD. 2001. Ammonia induced production of free radicals in primary cultures of rat astrocytes. J Neurosci Res 66:282-288.
48. 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.
49. Norenberg MD. 1987. The role of astrocytes in hepatic encephalopathy. Neurochem Pathol 6:13-33.
50. Norenberg MD. 1996. Astrocytic-ammonia interactions in hepatic encephalopathy. Semin Liver Dis 16:245-253.
51. Norenberg MD. 1998. Astroglial dysfunction in hepatic encephalopathy. Metab Brain Dis 13:319-335.
52. 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.
53. Norenberg MD, Itzhak Y, Bender AS. 1997. The peripheral benzodiazepine receptor and neurosteroids in hepatic encephalopathy. Adv Exp Med Biol 420:95-111.
54. Norenberg MD, Jayakumar AR, Rama Rao KV, Panickar KS. 2006. The peripheral benzodiazepine receptor and neurosteroids in the pathogenesis of hepatic encephalopathy and ammonia neurotoxicity. In: Häussinger D, Kircheis G, Schliess F, editors. Hepatic encephalopathy and nitrogen metabolism. Dordtrecht: Springer. pp 143-160.
55. Norenberg MD, Rama Rao KV, Jayakumar AR. 2003. The mitochondrial permeability transition in ammonia neurotoxicity. In: Jones E, Meijer AJ, Chamuleau AF, editors. Encephalopathy and nitrogen metabolism in liver failure. Dordrecht: Kluwer. pp 267-286.
56. Norenberg MD, Rao KV, Jayakumar AR. 2005. Mechanisms of ammonia-induced astrocyte swelling. Metab Brain Dis 20:303-318.
57. Papadopoulos V. 1993. Peripheral-type benzodiazepine/diazepam binding inhibitor receptor: Biological role in steroidogenic cell function. Endocr Rev 14:222-240.
58. Papadopoulos V, Amri H, Boujrad N, Cascio C, Culty M, Garnier M, Hardwick M, Li H, Vidic B, Brown AS, Reversa JL, Bernassau JM, Drieu K. 1997. Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids 62:21-28.
59. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapere JJ, Lindemann P, Norenberg MD, Nutt D, Weizman A, Zhang MR, Gavish M. 2006. Translocator protein (18 kDa): New nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 27:402-409.
60. Park SY, Cho N, Chang I, Chung JH, Min YK, Lee MK, Kim KW, Kim SJ, Lee MS. 2005. Effect of PK 11195, a peripheral benzodiazepine receptor agonist, on insulinoma cell death and insulin secretion. Apoptosis 10:537-544.
61. Pastorino JG, Simbula G, Gilfor E, Hoek JB, Farber JL. 1994. Protoporphyrin IX, an endogenous ligand of the peripheral benzodiazepine receptor, potentiates induction of the mitochondrial permeability transition and the killing of cultured hepatocytes by rotenone. J Biol Chem 269:31041-31046.
62. Pichili VB, Rao KV, Jayakumar AR, Norenberg MD. 2007. Inhibition of glutamine transport into mitochondria protects astrocytes from ammonia toxicity. Glia 55:801-809.
63. Rama Rao KV, Chen M, Simard JM, Norenberg MD. 2003a. Suppression of ammonia-induced astrocyte swelling by cyclosporin A. J Neurosci Res 74:891-897.
64. Rama Rao KV, Jayakumar AR, Norenberg DM. 2003b. Ammonia neurotoxicity: Role of the mitochondrial permeability transition. Metab Brain Dis 18:113-127.
65. 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.
66. Rao KV, Norenberg MD. 2004. Manganese induces the mitochondrial permeability transition in cultured astrocytes. J Biol Chem 279:32333-32338.
67. Rao KVR, Bai G, Jayakumar AR, Norenberg MD. 2001. Role of the peripheral benzodiazepine receptor and neurosteroids in the induction of the mitochondrial permeability transition in cultured astrocytes. J Neurochem 78 (Suppl 1): 25-25.
68. Reinehr R, Görg B, Becker S, Qvartskhava N, Bidmon HJ, Selbach O, Haas HL, Schliess F, Häussinger D. 2007. Hypoosmotic swelling and ammonia increase oxidative stress by NADPH oxidase in cultured astrocytes and vital brain slices. Glia 55:758-771.
69. Simpson ER, Waterman MR. 1983. Regulation by ACTH of steroid hormone biosynthesis in the adrenal cortex. Can J Biochem Cell Biol 61:692-707.
70. Traber P, DalCanto M, Ganger D, Blei AT. 1989. Effect of body temperature on brain edema and encephalopathy in the rat after hepatic devascularization. Gastroenterology 96:885-891.
71. Vaquero J, Chung C, Blei AT. 2003. Brain edema in acute liver failure. A window to the pathogenesis of hepatic encephalopathy. Ann Hepatol 2:12-22.
72. Walter RB, Pirga JL, Cronk MR, Mayer S, Appelbaum FR, Banker DE. 2005. PK 11195, a peripheral benzodiazepine receptor (pBR) ligand, broadly blocks drug efflux to chemosensitize leukemia and myeloma cells by a pBR-independent, direct transporter-modulating mechanism. Blood 106:3584-3593.
73. Weisinger G, Kelly-Hershkovitz E, Veenman L, Spanier I, Leschiner S, Gavish M. 2004. Peripheral benzodiazepine receptor antisense knockout increases tumorigenicity of MA-10 Leydig cells in vivo and in vitro. Biochemistry 43:12315-12321.
74. Woods MJ, Zisterer DM, Williams DC. 1996. Two cellular and subcellular locations for the peripheral-type benzodiazepine receptor in rat liver. Biochem Pharmacol 51:1283-1292.
75. Zoratti M, Szabo I. 1995. The mitochondrial permeability transition. Biochim Biophys Acta 1241:139-176.
76. Zoratti M, Szabo I, De Marchi U. 2005. Mitochondrial permeability transitions: How many doors to the house? Biochim Biophys Acta 1706:40-52.
77. 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.