Dibenzofuran-induced mitochondrial dysfunction: Interaction with ANT carrier

Toxicology in Vitro

Volumn 27, Issue 8, 2013, Pages 2160-2168

  Duarte, F V ^a,b   Gomes, A P ^a,b   Teodoro, J S ^a,b   Varela, A T ^a,b   Moreno, A J M ^b   Rolo, A P ^a,c   Palmeira, C M ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

Adenine nucleotide translocator (ANT); Cyclophilin D (CypD); Dibenzofuran (DBF); Mitochondria; Mitochondrial permeability transition (MPT)

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE DIPHOSPHATE; CALCIUM ION; CYCLOPHILIN D; DIBENZOFURAN; POLYCYCLIC AROMATIC HYDROCARBON;

ARTICLE; BIOACCUMULATION; BIOENERGY; CARCINOGENICITY; CELL DEATH; DEPOLARIZATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENVIRONMENTAL EXPOSURE; IMMUNOPRECIPITATION; LIVER MITOCHONDRION; MITOCHONDRIAL PERMEABILITY; PATHOPHYSIOLOGY; POLLUTANT; PROTEIN BINDING; PROTEIN PHOSPHORYLATION;

ADENINE NUCLEOTIDE TRANSLOCATOR (ANT); CYCLOPHILIN D (CYPD); DIBENZOFURAN (DBF); MITOCHONDRIA; MITOCHONDRIAL PERMEABILITY TRANSITION (MPT);

ADENOSINE TRIPHOSPHATASES; ANIMALS; BENZOFURANS; CYCLOPHILINS; ENVIRONMENTAL POLLUTANTS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, LIVER; MITOCHONDRIAL ADP, ATP TRANSLOCASES; OXYGEN; RATS; RATS, WISTAR;

EID: 84885795993     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2013.08.009     Document Type: Article

References (51)

1. Ahmed S., Shibazaki M., Takeuchi T., Kikuchi H. Protein kinase Ctheta activity is involved in the 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced signal transduction pathway leading to apoptosis in L-MAT, a human lymphoblastic T-cell line. FEBS J. 2005, 272:903-915.
2. Aly H.A.A., Domènech O. Cytotoxicity and mitochondrial dysfunction of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in isolated rat hepatocytes. Toxicol. Lett. 2009, 191:79-87.
3. 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.
4. Chance B., Williams G. The respiratory chain and oxidative phosphorylation. Adv. Enzymol. Relat. Subjects Biochem. 1956, 17:65-134.
5. Chiara, F., Gambalunga, A., Sciacovelli, M., Nicolli, A., Ronconi, L., Fregona, D., Bernardi, P., Rasola, A., Trevisan, A., 2012. Chemotherapeutic induction of mitochondrial oxidative stress activates GSK-3α/β and Bax, leading to permeability transition pore opening and tumor cell death. Cell Death and Disease, 3, e444. http://dx.doi.org/10.1038/cddis.2012.184.
6. Chiba T., Uchi H., Tsuji G., Gondo H., Moroi Y., Furue M. Arylhydrocarbon receptor (AhR) activation in airway epithelial cells induces MUC5AC via reactive oxygen species (ROS) production. Pulm. Pharmacol. Ther. 2011, 24:133-140.
7. Contreras L., Drago I., Zampese E., Pozzan T. Mitochondria: the calcium connection. Biochim. Biophys. Acta 2010, 1797(6-7):607-618.
8. Dimitrova-Shumkovska J., Veenman L., Ristoski T., Leschiner S., Gavish M. Decreases in binding capacity of the mitochondrial 18 kDa translocator protein accompany oxidative stress and pathological signs in rat liver after DMBA exposure. Toxicol. Pathol. 2010, 38:957-968.
9. Duarte F.V., Simões A.M., Teodoro J.S., Rolo A.P., Palmeira C.M. Exposure to dibenzofuran affects lung mitochondrial function in vitro. Toxicol. Mech. Methods 2011, 21(8):571-576.
10. Duarte F.V., Teodoro J.S., Rolo A.P., Palmeira C.M. Exposure to dibenzofuran triggers autophagy in lung cells. Toxicol. Lett. 2012, 209(1):35-42.
11. Estabrook R. Mitochondrial respiratory control and the polarographic measurement of ADP/O ratios. Methods Enzymol 1967, 10:41-47.
12. Geier D.A., King P.G., Geier M.R. Mitochondrial dysfunction, impaired oxidative-reduction activity, degeneration, and death in human neuronal and fetal cells induced by low-level exposure to thimerosal and other metal compounds. Toxicol. Environ. Chem. 2009, 1-15. iFirst.
13. Gomes A.P., Duarte F.V., Nunes P., Hubbard B.P., Teodoro J.S., Varela A.T., Jones J.G., Sinclair D.A., Palmeira C.M., Rolo A.P. Berberine protects against high fat diet-induced dysfunction in muscle mitochondria by inducing SIRT1-dependent mitochondrial biogenesis. Biochim. Biophys. Acta 2012, 1822(2):185-195.
14. Gornall A., Bardawill C., David M. Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 1949, 177(2):751-766.
15. Halestrap A.P., Pasdois P. The role of the mitochondrial permeability transition pore in heart disease. Biochim. Biophys. Acta 2009, 1787(11):1402-1415.
16. Hansson M.J., Morota S., Chen L., Matsuyama N., Suzuki Y., Nakajima S., Tanoue T., Omi A., Shibasaki F., Shimazu M., Ikeda Y., Uchino H., Elmér E. Cyclophilin D-sensitive mitochondrial permeability transition in adult human brain and liver mitochondria. J. Neurotrauma 2011, 28(1):143-153.
17. m) and G1 arrest in human hepatoma cell line. Toxicol. Lett. 2012, 214(2):137-144.
18. Kamo N., Muratsugu M., Hongoh R., Kobatake Y. 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. 1979, 49(2):105-121.
19. Kinnally K.W., Peixoto P.M., Ryu S.Y., Dejean L.M. Is mPTP the gatekeeper for necrosis, apoptosis, or both?. Biochim. Biophys. Acta 2011, 1813(4):616-622.
20. Kopf P.G., Walker M.K. 2,3,7,8-tetrachlorodibenzo-p-dioxin increases reactive oxygen species production in human endothelial cells via induction of cytochrome P4501A1. Toxicol. Appl. Pharmacol. 2010, 245:91-99.
21. Lecureur V., Arzel M., Ameziane S., Houlbert N., Le Vee M., Jouneau S., Fardel O. MAPK- and PKC/CREB-dependent induction of interleukin-11 by the environmental contaminant formaldehyde in human bronchial epithelial cells. Toxicology 2012, 292(1):13-22.
22. ++ movements across biological membranes. Biochem. Biophys. Res. Commun. 1975, 64(3):870-876.
23. Madeira V.M., Antunes-Madeira M.C., Carvalho A.P. Activation energies of the ATPase activity of sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 1974, 58(4):897-904.
24. Mandal P.K. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J. Comp. Physiol. [B] 2005, 175(4):221-230.
25. Masini A., Ceccarelli-Stanzani D., Muscatello U. An investigation on the effect of oligomycin on state-4 respiration in isolated rat-liver mitochondria. Biochim. Biophys. Acta 1984, 767(1):130-137.
26. Mbye L.H., Singh I.N., Carrico K.M., Saatman K.E., Hall E.D. Comparative neuroprotective effects of cyclosporin A and NIM811, a nonimmunosuppressive cyclosporin A analog, following traumatic brain injury. J. Cereb. Blood Flow Metab. 2009, 29(1):87-97.
27. McGwin G., Lienert J., Kennedy J.I. Formaldehyde exposure and asthma in children: a systematic review. Environ. Health Perspect. 2010, 118(3):313-317.
28. Millay D.P., Sargent M.A., Osinska H., Baines C.P., Barton E.R., Vuagniaux G., Sweeney H.L., Robbins J., Molkentin J.D. Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat. Med. 2008, 14(4):442-447.
29. Mohammadi-Bardbori A., Ghazi-Khansari M. Alternative electron acceptors: proposed mechanism of paraquat mitochondrial toxicity. Environ. Toxicol. Pharmacol. 2008, 26:1-5.
30. Nicholls D.G. Mitochondrial calcium function and dysfunction in the central nervous system. Biochim. Biophys. Acta 2009, 1787(11):1416-1424.
31. Orrenius S., Gogvadze V., Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu. Rev. Pharmacol. Toxicol. 2007, 47:143-183.
32. Palmeira C.M., Madeira V.M. Mercuric chloride toxicity in rat liver mitochondria and isolated hepatocytes. Environ. Toxicol. Pharmacol. 1997, 3(3):229-235.
33. Palmeira C.M., Wallace K.B. Benzoquinone inhibits the voltage-dependent induction of the mitochondrial permeability transition caused by redox-cycling naphthoquinones. Toxicol. Appl. Pharmacol. 1997, 143(2):338-347.
34. Palmeira C.M., Moreno A.J., Madeira V.M. Interactions of herbicides 2,4-D and dinoseb with liver mitochondrial bioenergetics. Toxicol. Appl. Pharmacol. 1994, 127(1):50-57.
35. Pastorino J.G., Hoek J.B. Regulation of hexokinase binding to VDAC. J. Bioenerg. Biomembr. 2008, 40(3):171-182.
36. Raaschou-Nielsen O., Andersen Z.J., Hvidberg M., Jensen S.S., Ketzel M., Sørensen M., Loft S., Overvad K., Tjønneland A. Lung cancer incidence and long-term exposure to air pollution from traffic. Environ. Health Perspect. 2011, 119(6):860-865.
37. Rasola A., Sciacovelli M., Pantic B., Bernardi P. Signal transduction to the permeability transition pore. FEBS Lett. 2010, 584(10):1989-1996.
38. Rico de Souza A., Zago M., Pollock S.J., Sime P.J., Phipps R.P., Baglole C.J. Genetic ablation of the aryl hydrocarbon receptor causes cigarette smoke-induced mitochondrial dysfunction and apoptosis. J. Biol. Chem. 2011, 286:43214-43228.
39. Rolo A.P., Teodoro J.S., Peralta C., Rosello-Catafau J., Palmeira C.M. Prevention of I/R injury in fatty livers by ischemic preconditioning is associated with increased mitochondrial tolerance. the key role of ATPsynthase and mitochondrial permeability transition. Transpl. Int. 2009, 22(11):1081-1090.
40. Roos D.H., Puntel R.L., Farina M., Aschner M., Bohrer D., Roca J.B., de Vargas Barbosa N.B. Modulation of methylmercury uptake by methionine: prevention of mitochondrial dysfunction in rat liver slices by a mimicry mechanism. Toxicol. Appl. Pharmacol. 2011, 252(1):28-35.
41. Russmann S., Kullak-Ublick G.A., Grattagliano I. Current concepts of mechanisms in drug-induced hepatotoxicity. Curr. Med. Chem. 2009, 16(23):3041-3053.
42. Sang H., Zhang L., Li J. Anti-benzopyrene-7,8-diol-9,10-epoxide induces apoptosis via mitochondrial pathway in human bronchiolar epithelium cells independent of the mitochondria permeability transition pore. Food Chem. Toxicol. 2012, 50(7):2417-2423.
43. Shertzer H.G., Genter M.B., Shen D., Nebert D.W., Chen Y., Dalton T.P. TCDD decreases ATP levels and increases reactive oxygen production through changes in mitochondrial F(0)F(1)-ATP synthase and ubiquinone. Toxicol. Appl. Pharmacol. 2006, 217:363-374.
44. Sileikyte J., Petronilli V., Zulian A., Dabbeni-Sala F., Tognon G., Nikolov P., Bernardi P., Ricchelli F. Regulation of the inner membrane mitochondrial permeability transition by the outer membrane translocator protein (peripheral benzodiazepine receptor). J. Biol. Chem. 2011, 286(2):1046-1053.
45. Silva F.S.G., Ribeiro M.P.C., Santos M.S., Rocha-Pereira P., Santos-Silva A., Custódio J.B.A. Acitretin affects bioenergetics of liver mitochondria and promotes mitochondrial permeability transition: potential mechanisms of hepatotoxicity. Toxicology 2013, 306:93-100.
46. Simões A.M., Duarte F.V., Teodoro J.S., Rolo A.P., Palmeira C.M. Exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin and tetraethyl-lead affects lung mitochondria bioenergetics. Toxicol. Mech. Methods 2010, 20(1):1-6.
47. Tang Y., Wang F., Jin C., Liang H., Zhong X., Yang Y. Mitochondrial injury induced by nanosized titaniumdioxide in A549 cells and rats. Environ. Toxicol. Pharmacol 2013.
48. Teodoro J.S., Simões A.M., Duarte F.V., Rolo A.P., Murdoch R.C., Hussain S.M., Palmeira C.M. Assessment of the toxicity of silver nanoparticles in vitro: a mitochondrial perspective. Toxicol. In Vitro 2011, 25(3):664-670.
49. Varela A.T., Gomes A.P., Simões A.M., Teodoro J.S., Duarte F.V., Rolo A.P., Palmeira C.M. Indirubin-3'-oxime impairs mitochondrial oxidative phosphorylation and prevents mitochondrial permeability transition induction. Toxicol. Appl. Pharmacol. 2008, 233(2):179-185.
50. Varela A.T., Simões A.M., Teodoro J.S., Duarte F.V., Gomes A.P., Palmeira C.M., Rolo A.P. Indirubin-3'-oxime prevents hepatic I/R damage by inhibiting GSK-3beta and mitochondrial permeability transition. Mitochondrion 2010, 10(5):456-463.
51. Yoshioka W., Peterson R.E., Tohyama C. Molecular targets that link dioxin exposure to toxicity phenotypes. J. Steroid Biochem. Mol. Biol. 2011, 127(1-2):96-101.