Biapigenin modulates the activity of the adenine nucleotide translocator in isolated rat brain mitochondria

Neurotoxicity Research

Volumn 17, Issue 1, 2010, Pages 75-90

  Silva, Bruno A ^a,d   Oliveira, Paulo J ^a   Cristóvão, Armando ^a,c   Dias, Alberto C P ^d   Malva, João O ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF MINHO   (Portugal)

Author keywords

Biapigenin; Calcium homeostasis; Hypericum perforatum; Mitochondria; Mitochondrial permeability transition pore

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATASE; ATRACTYLOSIDE; BIAPIGENIN; BONGKREKIC ACID; CALCIUM; FLAVONE; HYPERICUM PERFORATUM EXTRACT; OLIGOMYCIN; UNCLASSIFIED DRUG; APIGENIN; BIFLAVONOID; ENZYME INHIBITOR;

ANIMAL CELL; ARTICLE; BIOENERGY; BRAIN MITOCHONDRION; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVITY; FEMALE; MALE; MEMBRANE PERMEABILITY; MEMBRANE STEADY POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; RAT; REPOLARIZATION; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; DOSE RESPONSE; DRUG EFFECT; DRUG INTERACTION; ELECTRON TRANSPORT; HOMEOSTASIS; METABOLISM; MITOCHONDRION; ULTRASTRUCTURE; WISTAR RAT;

HYPERICUM PERFORATUM; RATTUS;

ADENOSINE TRIPHOSPHATASES; ANALYSIS OF VARIANCE; ANIMALS; APIGENIN; BIFLAVONOIDS; BRAIN; CALCIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRON TRANSPORT; ENZYME INHIBITORS; FEMALE; HOMEOSTASIS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL ADP, ATP TRANSLOCASES; OLIGOMYCINS; RATS; RATS, WISTAR;

EID: 77449110345     PISSN: 10298428     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12640-009-9082-5     Document Type: Article

References (64)

1. Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry 70:200-214
2. Belisle E, Kowaltowski AJ (2002) Opening of mitochondrial K+ channels increases ischemic ATP levels by preventing hydrolysis. J Bioenerg Biomembr 34:285-298
3. Bravo C, Vargas-Suárez M, Rodríguez-Enríquez S, Lova-Tavera H, Moreno-Sánchez R (2001) Metabolic changes induced by cold stress in rat liver mitochondria. J Bioenerg Biomembr 33:289-301
4. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287:C817-C833
5. Bruni A, Luciani S, Contessa AR (1964) Inhibition by atractyloside of the binding of adenine-nucleotides to rat-liver mitochondria. Nature 201:1219-1220
6. Bruni A, Luciani S, Bortignon C (1965) Competitive reversal by adenine nucleotides of atractyloside effect on mitochondrial energy transfer. Biochim Biophys Acta 97:434-441
7. Brustovetsky N, Dubinsky JM (2000) Dual responses of CNS mitochondria to elevated calcium. J Neurosci 20:103-113
8. Brustovetsky N, Klingenberg M (1994) The reconstituted ADP/ATP carrier can mediate H+ transport by free fatty acids, which is further stimulated by mersalyl. J Biol Chem 269:27329-27336
9. Brustovetsky NN, Dedukhova VI, Egorova MV, Mokhova EN, Skulachev VP (1990) Inhibitors of the ATP/ADP antiporter suppress stimulation of mitochondrial respiration and H+ permeability by palmitate and anionic detergents. FEBS Lett 272:187-189
10. Chen C, Ko Y, Delannoy M, Ludtke SJ, Chiu W, Pedersen PL (2004) Mitochondrial ATP synthasome: three-dimensional structure by electron microscopy of the ATP synthase in complex formation with carriers for Pi and ADP/ATP. J Biol Chem 279:31761-31768
11. Cho J, Lee HK (2004) Wogonin inhibits excitotoxic and oxidative neuronal damage in primary cultured rat cortical cells. Eur J Pharmacol 485:105-110 (Pubitemid 38134403)
12. Comelli M, Metelli G, Mavelli I (2007) Downmodulation of mitochondrial F0F1 ATP synthase by diazoxide in cardiac myoblasts: a dual effect of the drug. Am J Physiol Heart Circ Physiol 292:H820-H829
13. Dahout-Gonzalez C, Ramus C, Dassa EP, Dianoux AC, Brandolin G (2005) Conformation-dependent swinging of the matrix loop m2 of the mitochondrial Saccharomyces cerevisiae ADP/ATP carrier. Biochemistry 44:16310-16320
14. Dahout-Gonzalez C, Nury H, Trezeguet V, Lauquin GJ, Pebay-Peyroula E, Brandolin G (2006) Molecular, functional, and pathological aspects of the mitochondrial ADP/ATP carrier. Physiology 21:242-249
15. De Paola R, Muia C, Mazzon E, Genovese T, Crisafulli C, Menegazzi M, Caputi AP, Suzuki H, Cuzzocrea S (2005) Effect of Hypericum perforatum extract in a rat model of ischemia and reperfusion injury. Shock 24:255-263
16. Di Carlo G, Borrelli F, Ernst E, Izzo AA (2001) St John's wort: Prozac from the plant kingdom. Trends Pharmacol Sci 22:292-297
17. Dias ACP, Tomas-Barberan FA, Fernandes-Ferreira FA, Ferreres F (1998) Unusual flavonoids produced by callus of Hypericum perforatum. Phytochemistry 48:1165-1168
18. Dorner A, Olesch M, Giessen S, Pauschinger M, Schultheiss HP (1999) Transcription of the adenine nucleotide translocase isoforms in various types of tissues in the rat. Biochim Biophys Acta 1417:16-24
19. Dubinsky JM, Brustovetsky N, LaFrance R (2004) Protective roles of CNS mitochondria. J Bioenerg Biomembr 36:299-302
20. Duchen MR (2004) Mitochondria in health and disease: perspectives on a new mitochondrial biology. Mol Aspects Med 25:365-451
21. Estabrook RW (1967) Mitochondrial respiratory control and the polarographic measurement of ADP: O ratios. Methods Enzymol 10:41-47
22. Fernandez-Gomez FJ, Galindo MF, Gomez-Lazaro M, González-Garcia C, Ceña V, Aguirre N, Jordán J (2005) Involvement of mitochondrial potential and calcium buffering capacity in minocycline cytoprotective actions. Neuroscience 133:959-967
23. Ferreira FM, Madeira VM, Moreno AJ (1997) Interactions of 2, 2-bis(p-chlorophenyl)-1, 1-dichloroethylene with mitochondrial oxidative phosphorylation. Biochem Pharmacol 53:299-308
24. Halestrap AP (2006) Calcium, mitochondria and reperfusion injury: a pore way to die. Biochem Soc Trans 34:232-237
25. Halestrap AP, Brenner C (2003) The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr Med Chem 10:1507-1525
26. Halestrap AP, McStay GP, Clarke SJ (2002) The permeability transition pore complex: another view. Biochimie 84:153-166
27. Halestrap AP, Clarke SJ, Khaliulin I (2007) The role of mitochondria in protection of the heart by preconditioning. Biochim Biophys Acta 1767:1007-1031
28. He L, Lemasters JJ (2002) Regulated and unregulated mitochondrial permeability transition pores: a new paradigm of pore structure and function? FEBS Lett 512:1-7
29. Henderson PJ, Lardy HA (1970) Bongkrekic acid. An inhibitor of the adenine nucleotide translocase of mitochondria. J Biol Chem 245:1319-1326
30. Ichas F, Mazat JP (1998) From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1366:33-50
31. Ishige K, Schubert D, Sagara Y (2001) Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms. Free Radic Biol Med 30:433-446
32. Kamo N, Muratsugu M, Hongoh R, Kobatake Y (1979) Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J Membr Biol 49:105-121
33. Ko YH, Delannoy M, Hullihen J, Chiu W, Pedersen PL (2003) Mitochondrial ATP synthasome. Cristae-enriched membranes and a multiwell detergent screening assay yield dispersed single complexes containing the ATP synthase and carriers for Pi and ADP/ATP. J Biol Chem 278:12305-12309
34. Kowaltowski AJ, Maciel EN, Fornazari M, Castilho RF (2006) Diazoxide protects against methylmalonate-induced neuronal toxicity. Exp Neurol 201:165-171
35. Kristal BS, Stavrovskaya IG, Narayanan MV, Krasnikov BF, Brown AM, Beal MF, Friedlander RM (2004) The mitochondrial permeability transition as a target for neuroprotection. J Bioenerg Biomembr 36:309-312
36. Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99-163 (Pubitemid 46209992)
37. Kumar V, Mdzinarishvili A, Kiewert C, Abbruscato T, Bickel U, van der Schyf CJ, Klein J (2006) NMDA receptor-antagonistic properties of hyperforin, a constituent of St. John's Wort. J Pharmacol Sci 102:47-54
38. Lee H, Bae JH, Lee SR (2004) Protective effect of green tea polyphenol EGCG against neuronal damage and brain edema after unilateral cerebral ischemia in gerbils. J Neurosci Res 77:892-900
39. Madeira VM, Antunes-Madeira MC, Carvalho AP (1974) Activation energies of the ATPase activity of sarcoplasmic reticulum. Biochem Biophys Res Commun 58:897-904
40. Mansson R, Hansson MJ, Morota S, Uchino H, Ekdhal CT, Elmér E (2007) Re-evaluation of mitochondrial permeability as a primary neuroprotective target of minocycline. Neurobiol Dis 25:198-205
41. Montero M, Lobaton CD, Hernandez-Sanmiguel E, Santodomingo J, Vay L, Moreno A, Alvarez J (2004) Direct activation of the mitochondrial calcium uniporter by natural plant flavonoids. Biochem J 384:19-24
42. Moreira PI, Santos MS, Sena C, Seica R, Oliveira CR (2005) Insulin protects against amyloid beta-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol Dis 18:628-637 (Pubitemid 40332720)
43. Murata M, Akao M, O'Rourke B, Marban E (2001) Mitochondrial ATP-sensitive potassium channels attenuate matrix Ca(2+) overload during simulated ischemia and reperfusion: possible mechanism of cardioprotection. Circ Res 89:891-898
44. Oliveira PJ, Seica R, Coxito PM, Rolo AP, Palmeira CM, Santos MS, Moreno AJ (2003) Enhanced permeability transition explains the reduced calcium uptake in cardiac mitochondria from streptozotocin-induced diabetic rats. FEBS Lett 554:511-514
45. Oliveira PJ, Bjork Já , Santos MS, Leino RL, Froberg MK, Moreno AJ, Wallace KB (2004) Carvedilol-mediated antioxidant protection against doxorubicin-induced cardiac mitochondrial toxicity. Toxicol Appl Pharmacol 200:159-168
46. Parihar MS, Brewer GJ (2007) Mitoenergetic failure in Alzheimer disease. Am J Physiol Cell Physiol 292:C8-C23
47. Park C, So HS, Shin CH, Baek SH, Moon BS, Shin SH, Lee HS, Lee DW, Park R (2003) Quercetin protects the hydrogen peroxide-induced apoptosis via inhibition of mitochondrial dysfunction in H9c2 cardiomyoblast cells. Biochem Pharmacol 66:1287-1295
48. Pietrobon D, Luvisetto S, Azzone GF (1987) Uncoupling of oxidative phosphorylation. Alternative mechanisms: intrinsic uncoupling or decoupling? Biochemistry 26:7339-7347
49. Rasola A, Bernardi P (2007) The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 12:815-833
50. Rice-Evans C (2001) Flavonoid antioxidants. Curr Med Chem 8:797-807
51. Santos AC, Uyemura SA, Lopes JL, Bazon JN, Mingatto FE, Curti C (1998) Effect of naturally occurring flavonoids on lipid peroxidation and membrane permeability transition in mitochondria. Free Radic Biol Med 24:1455-1461
52. Schroeter H, Williams RJ, Matin R, Iversen L, Rice-Evans CA (2000) Phenolic antioxidants attenuate neuronal cell death following uptake of oxidized low-density lipoprotein. Free Radic Biol Med 29:1222-1233
53. Shabalina IG, Kramarova TV, Nedergaard J, Cannon B (2006) Carboxyatractyloside effects on brown-fat mitochondria imply that the adenine nucleotide translocator isoforms ANT1 and ANT2 may be responsible for basal and fatty-acid-induced uncoupling respectively. Biochem J 399:405-414
54. Shin DH, Bae YC, Kim-Han JS, Lee JH, Choi IY, Son KH, Kang SS, Kim WK, Han BH (2006a) Polyphenol amentoflavone affords neuroprotection against neuronal hypoxic-ischemic brain damage via multiple mechanisms. J Neurochem 96:561-572
55. Shin WH, Park SJ, Kim EJ (2006b) Protective effects of anthocyanins in middle cerebral artery occlusion and reperfusion model of cerebral ischemia in rats. Life Sci 79:286-296
56. Silva B, Oliveira PJ, Dias ACP, Malva JO (2008) Quercetin, kaempferol and biapigenin from Hypericum perforatum are neuroprotective against excitotoxic insults. Neurotoxicity Res 13:265-279
57. Stocchi V, Cucchiarini L, Magnani M, Chiarantini L, Palma P, Crescentini G (1985) Simultaneous extraction and reverse-phase high-performance liquid chromatographic determination of adenine and pyridine nucleotides in human red blood cells. Anal Biochem 146:118-124
58. Stout AK, Raphael HM, Kanterewicz BI, Klann E, Reynolds IJ (1998) Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat Neurosci 1:366-373
59. Teshima Y, Akao M, Li RA, Chong TH, Baumgartner WA, Johnston MV, Marbán E (2003) Mitochondrial ATP-sensitive potassium channel activation protects cerebellar granule neurons from apoptosis induced by oxidative stress. Stroke 34:1796-1802
60. Urushitani M, Nakamizo T, Inoue R, Sawada H, Kihara T, Honda K, Akaike A, Shimohama S (2001) N-methyl-D-aspartate receptor-mediated mitochondrial Ca(2+) overload in acute excitotoxic motor neuron death: a mechanism distinct from chronic neurotoxicity after Ca(2+) influx. J Neurosci Res 63:377-387
61. Vieira HL, Haouzi D, El-Hamel C, Jacotot E, Belzacq AS, Brenner C, Kroemer G (2000) Permeabilization of the mitochondrial inner membrane during apoptosis: impact of the adenine nucleotide translocator. Cell Death Differ 7:1146-1154
62. Wu L, Shen F, Lin L, Zhang X, Bruce IC, Xia Q (2006) The neuroprotection conferred by activating the mitochondrial ATP-sensitive K+ channel is mediated by inhibiting the mitochondrial permeability transition pore. Neurosci Lett 402:184-189
63. Yazawa K, Kihara T, Shen H, Shimmyo Y, Niidome T, Sugimoto H (2006) Distinct mechanisms underlie distinct polyphenol-induced neuroprotection. FEBS Lett 580:6623-6628
64. Zanotti F, Guerrieri F, Capozza G, Fiermonte M, Berden J, Papa S (1992) Role of F0 and F1 subunits in the gating and coupling function of mitochondrial H(+)-ATP synthase. The effect of dithiol reagents. Eur J Biochem 208:9-16