Mitochondrial hyperpolarization during chronic complex i inhibition is sustained by low activity of complex II, III, IV and v

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1837, Issue 8, 2014, Pages 1247-1256

  Forkink, Marleen ^a   Manjeri, Ganesh R ^a   Liemburg Apers, Dania C ^a   Nibbeling, Esther ^a   Blanchard, Maxime ^a   Wojtala, Aleksandra ^b   Smeitink, Jan A M ^c   Wieckowski, Mariusz R ^b   Willems, Peter H G M ^a   Koopman, Werner J H ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

ATeam; Live cell microscopy; Respirometry; SypHer; TMRM

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; COMPLEX V; CYTOCHROME C OXIDASE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE STEADY POTENTIAL; CONTROLLED STUDY; CYTOSOL; ELECTRON TRANSPORT; ENZYME INHIBITION; FLUORESCENCE IMAGING; HEK293 CELL LINE; HYPERPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ATEAM; LIVE-CELL MICROSCOPY; RESPIROMETRY; SYPHER; TMRM;

CELL RESPIRATION; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; HEK293 CELLS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL ADP, ATP TRANSLOCASES; MITOCHONDRIAL MEMBRANES; OXIDATIVE PHOSPHORYLATION;

EID: 84901101784     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2014.04.008     Document Type: Article

References (43)

1. W.J.H. Koopman, P.H.G.M. Willems, and J.A.M. Smeitink Monogenic mitochondrial disorders N. Engl. J. Med. 366 2012 1132 1141
2. D.G. Nicholls, and O. Lindberg Inhibited respiration and ATPase activity of rat liver mitochondria under conditions of matrix condensation FEBS Lett. 25 1972 61 64
3. C. Chinopoulos Mitochondrial consumption of cytosolic ATP: not so fast FEBS Lett. 585 2011 1255 1259
4. F. Palmieri Diseases caused by defects of mitochondrial carriers: a review Biochim. Biophys. Acta 1777 2008 564 578
5. W.J.H. Koopman, L.G.J. Nijtmans, C.E.J. Dieteren, P. Roestenberg, F. Valsecchi, and J.A.M. Smeitink et al. Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation Antioxid. Redox Signal. 12 2010 1431 1470
6. F. Fischer, A. Hamann, and H.D. Osiewacz Mitochondrial quality control: an integrated network of pathways Trends Biochem. Sci. 37 2012 284 292
7. J. Nunnari, and A. Suomalainen Mitochondria: in sickness and in health Cell 148 2012 1145 1159
8. E.I. Rugarli, and T. Langer Mitochondrial quality control: a matter of life and death for neurons EMBO J. 31 2012 1336 1349
9. E.A. Schon, S. DiMauro, and M. Hirano Human mitochondrial DNA: roles of inherited and somatic mutations Nat. Rev. Genet. 13 2012 878 890
10. R.A.J. Smith, R.C. Hartley, H.M. Cochemé, and M.P. Murphy Mitochondrial pharmacology Trends Pharmacol. Sci. 33 2012 341 352
11. S.B. Vafai, and V.K. Mootha Mitochondrial disorders as windows into an ancient organelle Nature 491 2012 374 383
12. W.J.H. Koopman, F. Distelmaier, J.A.M. Smeitink, and P.H.G.M. Willems OXPHOS mutations and neurodegeneration EMBO J. 32 2013 9 29
13. G. Solaini, G. Sgarbi, G. Lenaz, and A. Baracca Evaluating mitochondrial membrane potential in cells Biosci. Rep. 27 2007 11 21 (Pubitemid 46940934)
14. A.I. Jonckheere, M. Huigsloot, M. Lammens, J. Jansen, L.P. van den Heuvel, and U. Spiekerkoetter et al. Restoration of complex V deficiency caused by a novel deletion in the human TMEM70 gene normalizes mitochondrial morphology Mitochondrion 11 2011 954 963
15. 2 +-stimulated ATP production in human complex I deficiency J. Mol. Med. 87 2009 515 522
16. F. Distelmaier, W.J.H. Koopman, L.P. van den Heuvel, R.J. Rodenburg, E. Mayatepek, and P.H.G.M. Willems et al. Mitochondrial complex I deficiency: from organelle dysfunction to clinical disease Brain 132 2009 833 842
17. ·--mediated mitochondrial outgrowth Am. J. Physiol. Cell Physiol. 288 2005 C1440 C1450
18. F. Valsecchi, C. Monge, M. Forkink, A.J.C. de Groof, G. Benard, and R. Rossignol et al. Metabolic consequences of NDUFS4 gene deletion in immortalized mouse embryonic fibroblasts Biochim. Biophys. Acta 1817 2012 1925 1936
19. A.Y. Abramov, T.K. Smulders-Srinivasan, D.M. Kirby, R. Acin-Perez, J.A. Enriquez, and R.N. Lightowlers et al. Mechanism of neurodegeneration of neurons with mitochondrial DNA mutations Brain 133 2010 797 807
20. A. Barrientos, and C.T. Moraes Titrating the effects of mitochondrial complex I impairment in the cell physiology J. Biol. Chem. 274 1999 16188 16197
21. A. Mehta, and C. Shaha Apoptotic death in Leishmania donovani promastigotes in response to respiratory chain inhibition: complex II inhibition results in increased pentamidine cytotoxicity J. Biol. Chem. 279 2004 11798 11813 (Pubitemid 38401685)
22. Q. Gao, and M.S. Wolin Effects of hypoxia on relationships between cytosolic and mitochondrial NAD(P)H redox and superoxide generation in coronary arterial smooth muscle Am. J. Physiol. Heart Circ. Physiol. 295 2008 H978 H989
23. B.J. Van Raam, W. Sluiter, E. De Wit, D. Roos, A.J. Verhoeven, and T.W. Kuijpers Mitochondrial membrane potential in human neutrophils is maintained by complex III activity in the absence of supercomplex organisation PLoS One 3 2008 12
24. C.E.J. Dieteren, P.H.G.M. Willems, R.O. Vogel, H.G. Swarts, J. Fransen, and R. Roepman et al. Subunits of mitochondrial complex I exist as part of matrix- and membrane-associated subcomplexes in living cells J. Biol. Chem. 283 2008 34753 34761
25. C.E.J. Dieteren, S.C.A.M. Gielen, L.G.J. Nijtmans, J.A.M. Smeitink, H.G. Swarts, and R. Brock et al. Solute diffusion is hindered in the mitochondrial matrix Proc. Natl. Acad. Sci. U. S. A. 108 2011 8657 8662
26. C.E.J. Dieteren, W.J.H. Koopman, H.G. Swarts, J.G.P. Peters, P. Maczuga, and J.J. van Gemst et al. Subunit-specific incorporation efficiency and kinetics in mitochondrial complex I homeostasis J. Biol. Chem. 287 2012 41851 41860
27. S.J.G. Hoefs, C.E.J. Dieteren, F. Distelmaier, R.J.R.J. Janssen, A. Epplen, and H.G.P. Swarts et al. NDUFA2 complex I mutation leads to Leigh disease Am. J. Hum. Genet. 82 2008 1306 1315
28. D. Poburko, J. Santo-Domingo, and N. Demaurex Dynamic regulation of the mitochondrial proton gradient during cytosolic calcium elevations J. Biol. Chem. 286 2011 11672 11684
29. H. Imamura, K.P.H. Nhat, H. Togawa, K. Saito, R. Iino, and Y. Kato-Yamada et al. Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators Proc. Natl. Acad. Sci. U. S. A. 106 2009 15651 15656
30. E. Hütter, H. Unterluggauer, A. Garedew, P. Jansen-Dürr, and E. Gnaiger High-resolution respirometry - a modern tool in aging research Exp. Gerontol. 41 2006 103 109 (Pubitemid 43031375)
31. E. Gnaiger, A. Kuznetsov, S. Schneeberger, R. Seiler, G. Brandacher, and W. Steurer et al. Mitochondria in the cold G. Heldmaier, M. Klingenspor, Life Cold 2000 Springer Heidelberg, Berlin, New York 431 438
32. M. Nooteboom, M. Forkink, P.H.G.M. Willems, and W.J.H. Koopman Live-cell quantification of mitochondrial functional parameters E. Badoer, Neuromethods Vis. Tech. - From Immunohistochem. to Magn. Reson. Imaging 2012 Humana Press Inc. 111 127
33. J.S. Fan, and P. Palade Perforated patch recording with beta-escin Pflugers Arch. 436 1998 1021 1023
34. W.J.H. Koopman, H.-J. Visch, S. Verkaart, L.W.P.J. van den Heuvel, J.A.M. Smeitink, and P.H.G.M. Willems Mitochondrial network complexity and pathological decrease in complex I activity are tightly correlated in isolated human complex I deficiency Am. J. Physiol. Cell Physiol. 289 2005 C881 C890
35. P. Srivastava, and D. Panda Rotenone inhibits mammalian cell proliferation by inhibiting microtubule assembly through tubulin binding FEBS J. 274 2007 4788 4801 (Pubitemid 47353128)
36. E.N. Maldonado, J. Patnaik, M.R. Mullins, and J.J. Lemasters Free tubulin modulates mitochondrial membrane potential in cancer cells Cancer Res. 70 2010 10192 10201
37. A.V. Kuznetsov, S. Javadov, R. Guzun, M. Grimm, and V. Saks Cytoskeleton and regulation of mitochondrial function: the role of beta-tubulin II Front. Physiol. 4 2013 82
38. J.G. Okun, P. Lümmen, and U. Brandt Three classes of inhibitors share a common binding domain in mitochondrial complex I (NADH:ubiquinone oxidoreductase) J. Biol. Chem. 274 1999 2625 2630 (Pubitemid 29075339)
39. D.G. Nicholls Simultaneous monitoring of ionophore- and inhibitor-mediated plasma and mitochondrial membrane potential changes in cultured neurons J. Biol. Chem. 281 2006 14864 14874 (Pubitemid 43855191)
40. D.G. Nicholls, and S.J. Ferguson 3rd ed. Bioenergetics 3 2002 Academic Press London
41. I. Goehring, A.A. Gerencser, S. Schmidt, M.D. Brand, H. Mulder, and D.G. Nicholls Plasma membrane potential oscillations in insulin secreting Ins-1 832/13 cells do not require glycolysis and are not initiated by fluctuations in mitochondrial bioenergetics J. Biol. Chem. 287 2012 15706 15717
42. G. Cannino, R. El-Khoury, M. Pirinen, B. Hutz, P. Rustin, and H.T. Jacobs et al. Glucose modulates respiratory complex I activity in response to acute mitochondrial dysfunction J. Biol. Chem. 287 2012 38729 38740
43. C. Chinopoulos, A.A. Gerencser, M. Mandi, K. Mathe, B. Töröcsik, and J. Doczi et al. Forward operation of adenine nucleotide translocase during F0F1-ATPase reversal: critical role of matrix substrate-level phosphorylation FASEB J. 24 2010 2405 2416