Trolox-sensitive reactive oxygen species regulate mitochondrial morphology, oxidative phosphorylation and cytosolic calcium handling in healthy cells

Antioxidants and Redox Signaling

Volumn 17, Issue 12, 2012, Pages 1657-1669

  Distelmaier, Felix ^a,b,c   Valsecchi, Federica ^a,b,d   Forkink, Marleen ^a   Van Emst De Vries, Sjenet ^a   Swarts, Herman G ^a   Rodenburg, Richard J T ^b   Verwiel, Eugène T P ^b   Smeitink, Jan A M ^b   Willems, Peter H G M ^a   Koopman, Werner J H ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYKININ; CALCIUM; CITRATE SYNTHASE; DICHLORODIHYDROFLUORESCEIN; GLUTATHIONE DISULFIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TROLOX C;

ARTICLE; CALCIUM CELL LEVEL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; FIBROBLAST; GENE EXPRESSION PROFILING; HUMAN; HUMAN TISSUE; LIPID PEROXIDATION; MEMBRANE PERMEABILITY; MITOCHONDRION; MORPHOLOGY; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CALCIUM; CELLS, CULTURED; CHO CELLS; CHROMANS; CRICETINAE; CYTOSOL; HELA CELLS; HUMANS; LIPID PEROXIDATION; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; REACTIVE OXYGEN SPECIES;

EID: 84867710651     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4294     Document Type: Article

References (52)

1. Benard G and Rossignol R. Ultrastructure of the mitochondrion and its bearing on functions and bioenergetics. Antioxid Redox Signal 10: 1313-1342, 2008..
2. Brown GC and Borutaite V. There is no evidence that mitochondria are the main source of reactive oxygen species in mammalian cells. Mitochondrion 12: 1-4, 2011..
3. D'Autréaux B and Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeo-stasis. Nat Rev Mol Cell Biol 8: 813-824, 2007.. (Pubitemid 47462134)
4. Davies MJ, Forni LG, and Willson RL. Vitamin E analogue Trolox C. E.s.r. and pulse-radiolysis studies of free-radical reactions. Biochem J 255: 513-522, 1988..
5. DeBrito OMand Scorrano L.Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456: 605-610, 2008..
6. Distelmaier F, Koopman WJ, Testa ER, de Jong AS, Swarts HG, Mayatepek E, Smeitink JA, and Willems PH. Life cell quantification of mitochondrial membrane potential at the single organelle level. Cytometry A 73A: 129-138, 2008..
7. 2+-stimulated ATP production in human complex I deficiency. J Mol Med 87: 515-522, 2009..
8. 2-induced mito-chondrial fragmentation in C2C12 myocytes. Free Radic Biol Med 49: 1646-1654, 2010..
9. 2+ entry in vascular endo-thelial cells. Cell Calcium 43: 405-415, 2008.. (Pubitemid 351298573)
10. Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 194: 7-15, 2011..
11. Forkink M, Smeitink JA, Brock R, Willems PH, and Koopman WJ. Detection and manipulation of mitochondrial reactive oxygen species in mammalian cells. Biochim. Biophys Acta Bioenergetics 1797: 1034-1044, 2010..
12. Gibson GE and Huang HM. Mitochondrial enzymes and endoplasmic reticulum calcium stores as targets of oxidative stress in neurodegenerative diseases. J Bioenerg Biomembr 36: 335-340, 2004.. (Pubitemid 39619837)
13. Gomes LC, Di Benedetto G, and Scorrano L. During autop-hagy mitochondria elongate, are spared from degradation and sustain cell viability. Nature Cell Biol 13: 589-598, 2011..
14. 2+ pump isoform SERCA3 is more resistant than SERCA2b to peroxide. Am J Physiol. 273: 420-425, 1997..
15. 2 in cell cultures: impact of cell concentration and exposure time. Free Rad Biol Med 49: 1298-1305, 2010..
16. Hempel SL, Buettner GR, O'Malley YQ, Wessels DA, and Flaherty DM. Dihydrofluorescein diacetate is superior for detecting intracellular oxidants: comparison with 2', 7¢-dichlorodihydrofluorescein diacetate, 5(and 6)-carboxy-2¢, 7'-dichlorodihydrofluorescein diacetate, and dihydrorhodamine 123. Free Radic Biol Med 27: 146-159, 1999.. (Pubitemid 29353095)
17. Houtkooper RH and Vaz FM. Cardiolipin, the heart of mi-tochondrial metabolism. Cell Mol Life Sci 65: 2493-2506, 2008..
18. Jendrach M, Mai S, Pohl S, Vöth M, and Bereiter-Hahn J. Short-and long-term alterations of mitochondrial morphology, dynamics and mtDNA after transient oxidative stress. Mitochondrion 8: 293-304, 2008..
19. Keller A, Mohamed A, Dröse S, Brandt U, Fleming I, and Brandes RP. Analysis of dichlorodihydrofluorescein and dihydrocalcein as probes for the detection of intracellular reactive oxygen species. Free Radic Res 38: 1257-1267, 2004.. (Pubitemid 40045478)
20. 2-dependent oxidation of dichlorodihydrofluorescein. Mol Cells 21: 161-165, 2006..
21. Koopman WJH, Grefte S, Smeitink JA, and Willems PH. Simultaneous quantification of oxidative stress and cell spreading using 5-(and-6)- chloromethyl-2', 7'-dichlorofluorescein. Cyto-metry A 69A: 1184-1192, 2006.. (Pubitemid 46036175)
22. Koopman WJH, Nijtmans LG, Dieteren CE, Roestenberg P, Valsecchi F, Smeitink JA, and Willems PH. Mammalian mito-chondrial complex I: biogenesis, regulation and reactive oxygen species generation. Antioxid Redox Signal 12: 1431-1470, 2010..
23. Koopman WJH, Verkaart S, van Emst-de Vries SE, Grefte S, Smeitink JA, Nijtmans LG, and Willems PH. Mitigation of NADH: ubiquinone oxidoreductase deficiency by chronic Trolox treatment. Biochim Biophys Acta 1777: 853-859, 2008..
24. Koopman WJH, Verkaart S, Visch HJ, van der Westhuizen FH, Murphy MP, van den Heuvel LW, Smeitink JA, and Willems PH. Inhibition of complex I of the electron transport chain causes oxygen radical-mediated mitochondrial outgrowth. Am J Physiol Cell Physiol 288: C1440-C1450, 2005.. (Pubitemid 40991081)
25. Koopman WJH, Verkaart S, Visch HJ, van Emst-de Vries SE, Nijtmans LG, Smeitink JA, and Willems PH. Human NADH: ubiquinone oxidoreductase deficiency: radical changes in mitochondrial morphology? Am J Physiol Cell Physiol 293: C22-C29, 2007.. (Pubitemid 47105004)
26. Koopman WJH, Visch HJ, Smeitink JA, and Willems PH. Simultaneous quantitative measurement and automated analysis of mitochondrial morphology, mass, potential, and motility in living human skin fibroblasts. Cytometry A 69A: 1-12, 2006.. (Pubitemid 43062691)
27. Koopman WJH, Willems PHGM, and Smeitink JAM. Monogenic mitochondrial disorders. N Engl J Med 366: 1132-1141, 2012..
28. Mahon KP, Potocky TB, Blair D, Roy MD, Stewart KM, Chiles TC, and Kelley SO. Deconvolution of the cellular oxidative stress response with organelle-specific peptide conjugates. Chem Biol 14: 923-930, 2007.. (Pubitemid 47268781)
29. Mai S, Klinkenberg M, Auburger G, Bereiter-Hahn J, and Jendrach M. Decreased expression of Drp1 and Fis1 mediates mitochondrial elongation in senescent cells and enhances resistance to oxidative stress through PINK1. J Cell Sci 123: 917-926, 2010..
30. Murphy MP, Holmgren A, Larsson NG, Halliwell B, Chang CJ, Kalyanaraman B, Rhee SG, Thornalley PJ, Partridge L, Gems D, Nyström T, Belousov V, Schumacker PT, and Winterbourn CC. Unraveling the biological roles of reactive oxygen species. Cell Metab 13: 361-366, 2011..
31. Parone PA, Da Cruz S, Tondera D, Mattenberger Y, James DI, Maechler P, Barja F, and Martinou JC. Preventing mi-tochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS One 3: e3257, 2008..
32. Qi X, Disatnik MH, Shen N, Sobel RA, and Mochly-Rosen D. Aberrant mitochondrial fission in neurons induced by delta protein kinase C under oxidative stress conditions, in vivo. Mol Biol Cell 22: 256-265, 2010..
33. Rakovic A, Grünewald A, Kottwitz J, Brü ggemann N, Pramstaller P, Lohmann K, and Klein C. Mutations in PINK1 and Parkin impair ubiquitination of mitofusins in human fibroblasts. PLoS One 6: e16746, 2011..
34. Raspor P, Plesnicar S, Gazdag Z, Pesti M, Miklavcic M, Lah B, Logar-Marinsek R, and Poljsak B. Prevention of intracellular oxidation in yeast: the role of vitamin E analogue, Trolox (6-hydroxy-2, 5, 7, 8-tetramethylkroman- 2-carboxyl acid). Cell Biol Int 29: 57-63, 2005.. (Pubitemid 40353728)
35. Rodenburg RJ. Biochemical diagnosis of mitochondrial disorders. J. Inherit Metab Dis 34: 283-92, 2011..
36. Schafer FQ and Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30: 1191-1212, 2001.. (Pubitemid 32463931)
37. Storz P. Forkhead homeobox type O transcription factors in the responses to oxidative stress. Antioxid Redox Signal 14: 593-605, 2011..
38. Tafazoli S, Wright JS, and O'Brien PJ. Prooxidant and anti-oxidant activity of vitamin E analogues and troglitazone. Chem Res Toxicol 18: 1567-1574, 2005.. (Pubitemid 41504477)
39. Tanaka A, Cleland MM, Xu S, Narendra DP, Suen DF, Karbowski M, and Youle RJ. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol 191: 1367-1380, 2010..
40. Twig G and Shirihai OS. The interplay between mitochon-drial dynamics and mitophagy. Antioxid Redox Signal 14: 1939-1951, 2011..
41. Umansky V, Ratter F, Lampel S, Bucur M, Schirrmacher V, and Ushmorov A. Inhibition of nitric-oxide-mediated apo-ptosis in Jurkat leukemia cells despite cytochrome c release. Exp Cell Res 265: 274-282, 2001.. (Pubitemid 32980215)
42. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, and Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39: 44-84, 2007.. (Pubitemid 44566469)
43. Verkaart S, Koopman WJ, Cheek J, van Emst-de Vries SE, van den Heuvel LW, Smeitink JA, and Willems PH. Mi-tochondrial and cytosolic thiol redox state are not detectably altered in isolated human NADH: ubiquinone oxidoreduc-tase deficiency. Biochim Biophys Acta 1772: 1041-1051, 2007.. (Pubitemid 47314228)
44. Verkaart S, Koopman WJ, Nijtmans LG, van den Heuvel LW, Smeitink JA, and Willems PH Superoxide activity is inversely related to complex I activity in inherited complex I deficiency. Biochim Biophys Acta 1772: 373-381, 2007.. (Pubitemid 46275438)
45. Visch HJ, Koopman WJ, Leusink A, van Emst-de Vries SE, van den Heuvel LW, Willems PH, and Smeitink JA. Decreased agonist-stimulated mitochondrial ATP production caused by a pathological reduction in endoplasmic reticu-lum calcium content in human complex I deficiency. Biochim Biophys Acta 1762: 115-123, 2006.. (Pubitemid 43021094)
46. 2+ handling in human complex I deficiency. J Biol Chem 279: 40328-40336, 2004.. (Pubitemid 39287618)
47. Westermann B. Bioenergetic role of mitochondrial fusion and fission. Biochim Biophys Acta PMID: 22409868, 2012; [Epub ahead of print]; DOI: 10.1016/j.bbabio.2012.02.033..
48. Winterbourn CC. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 4: 278-286, 2008.. (Pubitemid 351550893)
49. Wu S, Zhou F, and Zhang Z. Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins. FEBS J 278: 941-954, 2011..
50. Yu T, Jhun BS, and Yoon Y. High-glucose stimulation increases reactive oxygen species production through the calcium and mitogen-activated protein kinase-mediated activation of mito-chondrial fission. Antioxid Redox Signal 14: 524-437, 2011..
51. Yu T, Robotham JL, and Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci U S A 103: 2653-2658, 2006..
52. Zorzano A, Liesa M, Sebastian D, Segales J, and Palacin M. Mitochondrial fusion proteins: dual regulators of morphology and metabolism. Semin Cell Dev Biol 21: 566-574, 2010..