Cyclosporine A-induced apoptosis in renal tubular cells is related to oxidative damage and mitochondrial fission

Toxicology Letters

Volumn 218, Issue 1, 2013, Pages 30-38

  de Arriba, Gabriel ^a,b,c   Calvino, Miryam ^a,d   Benito, Selma ^a,d   Parra, Trinidad ^a,d  

^a HOSPITAL UNIVERSITARIO DE GUADALAJARA   (Spain)

^b UNIVERSITY OF ALCALÁ   (Spain)

^c Grupo Español de Estudio de la Nefropatía Diabética GEENDIAB   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Apoptosis; Cyclosporine; Mitochondrial fission; Mitochondrial fusion; Reactive oxygen species

Indexed keywords

ALPHA TOCOPHEROL; CYCLOSPORIN A; CYTOCHROME C; DYNAMIN RELATED PROTEIN 1; GLUTATHIONE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOFUSIN 2; OPTIC ATROPHY PROTEIN 1; PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BIOSYNTHESIS; CELL FUNCTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; INTRACELLULAR SPACE; KIDNEY TUBULE CELL; MITOCHONDRIAL FISSION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MOLECULAR DYNAMICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CYCLOSPORINE; DRUG ANTAGONISM; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLUTATHIONE; KIDNEY TUBULES; LLC-PK1 CELLS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; PERMEABILITY; REACTIVE OXYGEN SPECIES; SWINE; VITAMIN E;

EID: 84873324504     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.01.007     Document Type: Article

References (46)

1. Bass D.A., Parce J.W., Dechatelet L.R., Szejda P., Seeds M.C., Thomas M. Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. Journal of Immunology 1983, 130:1910-1917.
2. Berman S.B., Pineda F.J., Hardwick J.M. Mitochondrial fission and fusion dynamics: the long and short of it. Cell Death and Differentiation 2008, 15:1147-1152.
3. Bernardi P. The permeability transition pore. Control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death. Biochimica et Biophysica Acta 1996, 1275:5-9.
4. Brady N.R., Elmore S.P., van Beek J.J., Krab K., Courtoy P.J., Hue L., Westerhoff H.V. Coordinated behavior of mitochondria in both space and time: a reactive oxygen species-activated wave of mitochondrial depolarization. Biophysical Journal 2004, 87:2022-2034.
5. Brooks C., Wei Q., Cho S.G., Dong Z. Regulation of mitochondrial dynamics in acute kidney injury in cell culture and rodent models. Journal of Clinical Investigation 2009, 119:1275-1285.
6. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochemical Journal 1999, 341(Pt 2):233-249.
7. Chan D.C. Mitochondrial fusion and fission in mammals. Annual Review of Cell and Developmental Biology 2006, 22:79-99.
8. de Arriba G., de Hornedo J.P., Rubio S.R., Fernandez M.C., Martinez S.B., Camarero M.M., Cid T.P. Vitamin E protects against the mitochondrial damage caused by cyclosporin A in LLC-PK1 cells. Toxicology and Applied Pharmacology 2009, 239:241-250.
9. Fournier N., Ducet G., Crevat A. Action of cyclosporine on mitochondrial calcium fluxes. Journal of Bioenergetics and Biomembranes 1987, 19:297-303.
10. Galindo M.F., Jordan J., Gonzalez-Garcia C., Cena V. Reactive oxygen species induce swelling and cytochrome c release but not transmembrane depolarization in isolated rat brain mitochondria. British Journal of Pharmacology 2003, 139:797-804.
11. He L., Lemasters J.J. Regulated and unregulated mitochondrial permeability transition pores: a new paradigm of pore structure and function?. FEBS Letters 2002, 512:1-7.
12. Hoppins S., Lackner L., Nunnari J. The machines that divide and fuse mitochondria. Annual Review of Biochemistry 2007, 76:751-780.
13. Hoppins S., Nunnari J. The molecular mechanism of mitochondrial fusion. Biochimica et Biophysica Acta 2009, 1793:20-26.
14. Iverson S.L., Orrenius S. The cardiolipin-cytochrome c interaction and the mitochondrial regulation of apoptosis. Archives of Biochemistry and Biophysics 2004, 423:37-46.
15. Jackson M.J., Papa S., Bolanos J., Bruckdorfer R., Carlsen H., Elliott R.M., Flier J., Griffiths H.R., Heales S., Holst B., Lorusso M., Lund E., Oivind Moskaug J., Moser U., Di Paola M., Polidori M.C., Signorile A., Stahl W., Vina-Ribes J., Astley S.B. Antioxidants, reactive oxygen and nitrogen species, gene induction and mitochondrial function. Molecular Aspects of Medicine 2002, 23:209-285.
16. Jezek P., Hlavata L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. International Journal of Biochemistry and Cell Biology 2005, 37:2478-2503.
17. Justo P., Lorz C., Sanz A., Egido J., Ortiz A. Intracellular mechanisms of cyclosporin A-induced tubular cell apoptosis. Journal of the American Society of Nephrology 2003, 14:3072-3080.
18. Karbowski M., Lee Y.J., Gaume B., Jeong S.Y., Frank S., Nechushtan A., Santel A., Fuller M., Smith C.L., Youle R.J. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. Journal of Cell Biology 2002, 159:931-938.
19. Karbowski M., Norris K.L., Cleland M.M., Jeong S.Y., Youle R.J. Role of Bax and Bak in mitochondrial morphogenesis. Nature 2006, 443:658-662.
20. Kim J.S., He L., Lemasters J.J. Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochemical and Biophysical Research Communications 2003, 304:463-470.
21. Kinnally K.W., Antonsson B. A tale of two mitochondrial channels, MAC and PTP, in apoptosis. Apoptosis 2007, 12:857-868.
22. Lee Y.J., Jeong S.Y., Karbowski M., Smith C.L., Youle R.J. Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Molecular Biology of the Cell 2004, 15:5001-5011.
23. Lovell J.F., Billen L.P., Bindner S., Shamas-Din A., Fradin C., Leber B., Andrews D.W. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 2008, 135:1074-1084.
24. Mannella C.A. Structural diversity of mitochondria: functional implications. Annals of the New York Academy of Sciences 2008, 1147:171-179.
25. McMillin J.B., Dowhan W. Cardiolipin and apoptosis. Biochimica et Biophysica Acta 2002, 1585:97-107.
26. Naesens M., Kuypers D.R., Sarwal M. Calcineurin inhibitor nephrotoxicity. Clinical Journal of the American Society of Nephrology 2009, 4:481-508.
27. Nunnari J., Suomalainen A. Mitochondria: in sickness and in health. Cell 2012, 148:1145-1159.
28. Orrenius S. Reactive oxygen species in mitochondria-mediated cell death. Drug Metabolism Reviews 2007, 39:443-455.
29. Paradies G., Petrosillo G., Pistolese M., Ruggiero F.M. Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 2002, 286:135-141.
30. Parra Cid T., Conejo Garcia J.R., Carballo Alvarez F., de Arriba G. Antioxidant nutrients protect against cyclosporine A nephrotoxicity. Toxicology 2003, 189:99-111.
31. Parra T., de Arriba G., Conejo J.R., Cantero M., Arribas I., Rodriguez-Puyol D., Rodriguez-Puyol M., Carballo F. Cyclosporine increases local glomerular synthesis of reactive oxygen species in rats: effect of vitamin E on cyclosporine nephrotoxicity. Transplantation 1998, 66:1325-1329.
32. Perez de Hornedo J., de Arriba G., Calvino M., Benito S., Parra T. Cyclosporin A causes oxidative stress and mitochondrial dysfunction in renal tubular cells. Nefrologia 2007, 27:565-573.
33. Perkins G., Bossy-Wetzel E., Ellisman M.H. New insights into mitochondrial structure during cell death. Experimental Neurology 2009, 218:183-192.
34. Poot M., Pierce R.H. Detection of changes in mitochondrial function during apoptosis by simultaneous staining with multiple fluorescent dyes and correlated multiparameter flow cytometry. Cytometry 1999, 35:311-317.
35. Redondo-Horcajo M., Romero N., Martinez-Acedo P., Martinez-Ruiz A., Quijano C., Lourenco C.F., Movilla N., Enriquez J.A., Rodriguez-Pascual F., Rial E., Radi R., Vazquez J., Lamas S. Cyclosporine A-induced nitration of tyrosine 34 MnSOD in endothelial cells: role of mitochondrial superoxide. Cardiovascular Research 2010, 87:356-365.
36. Sheridan C., Martin S.J. Mitochondrial fission/fusion dynamics and apoptosis. Mitochondrion 2010, 10:640-648.
37. Soubannier V., McBride H.M. Positioning mitochondrial plasticity within cellular signaling cascades. Biochimica et Biophysica Acta 2009, 1793:154-170.
38. Taguchi N., Ishihara N., Jofuku A., Oka T., Mihara K. Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. Journal of Biological Chemistry 2007, 282:11521-11529.
39. Ulivieri C. Cell death: insights into the ultrastructure of mitochondria. Tissue and Cell 2010, 42:339-347.
40. Wang C., Salahudeen A.K. Cyclosporine nephrotoxicity: attenuation by an antioxidant-inhibitor of lipid peroxidation in vitro and in vivo. Transplantation 1994, 58:940-946.
41. Westermann B. Molecular machinery of mitochondrial fusion and fission. Journal of Biological Chemistry 2008, 283:13501-13505.
42. Wiswedel I., Gardemann A., Storch A., Peter D., Schild L. Degradation of phospholipids by oxidative stress-exceptional significance of cardiolipin. Free Radical Research 2010, 44:135-145.
43. Wu S., Zhou F., Zhang Z., Xing D. Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins. The FEBS Journal 2011, 278:941-954.
44. Yamada K., Arita K., Kobuchi H., Yamamoto S., Yoshioka T., Tamai H., Utsumi K. Cholesteryl-hemisuccinate-induced apoptosis of promyelocytic leukemia HL-60 cells through a cyclosporin A-insensitive mechanism. Biochemical Pharmacology 2003, 65:339-348.
45. Yamaguchi R., Perkins G. Dynamics of mitochondrial structure during apoptosis and the enigma of Opa1. Biochimica et Biophysica Acta 2009, 1787:963-972.
46. Zoratti M., Szabo I. The mitochondrial permeability transition. Biochimica et Biophysica Acta 1995, 1241:139-176.