Identification of a novel mitochondrial uncoupler that does not depolarize the plasma membrane

Molecular Metabolism

Volumn 3, Issue 2, 2014, Pages 114-123

  Kenwood, Brandon M ^a   Weaver, Janelle L ^a   Bajwa, Amandeep ^a   Poon, Ivan K ^a   Byrne, Frances L ^a   Murrow, Beverley A ^a   Calderone, Joseph A ^h   Huang, Liping ^a   Divakaruni, Ajit S ^b   Tomsig, Jose L ^a   Okabe, Kohki ^f   Lo, Ryan H ^e   Cameron Coleman, G ^a   Columbus, Linda ^e   Yan, Zhen ^a,e   Saucerman, Jeffrey J ^c,e   Smith, Jeffrey S ^c   Holmes, Jeffrey W ^c,e   Lynch, Kevin R ^a   Ravichandran, Kodi S ^a   Uchiyama, Seiichi ^f   Santos, Webster L ^h   Rogers, George W ^d   Okusa, Mark D ^a   Bayliss, Douglas A ^a   Hoehn, Kyle L ^a,e,g   more..

^a UNIVERSITY OF VIRGINIA   (United States)

^b San Diego   (United States)

^c University of Virginia   (United States)

^d Seahorse Bioscience   (United States)

^e UNIVERSITY OF VIRGINIA   (United States)

^f UNIVERSITY OF TOKYO   (Japan)

^g UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^h VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Bioenergetics; CCCP; DNP; FCCP; Ischemia; Mitochondria

Indexed keywords

(2 FLUOROPHENYL) [6 [(2 FLUOROPHENYL)AMINO](1,2,5 OXADIAZOLO[3,4 E]PYRAZIN 5 YL)]AMINE; BAM 15; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; IONOPHORE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL STIMULATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DOSE COMPARISON; DRUG MECHANISM; FLUORESCENCE ACTIVATED CELL SORTING; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRACELLULAR SIGNALING; KIDNEY ISCHEMIA; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION SWELLING; MOUSE; MYOBLAST; NEWBORN; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PRIORITY JOURNAL; RAT; RENAL PROTECTION; REPERFUSION INJURY;

MUS;

EID: 84895800631     PISSN: 22128778     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmet.2013.11.005     Document Type: Article

References (33)

1. Rousset S., Alves-Guerra M.C., Mozo J., Miroux B., Cassard-Doulcier A.M., Bouillaud F., et al. The biology of mitochondrial uncoupling proteins. Diabetes 2004, 53(Suppl 1):S130-S135.
2. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Letters 1997, 416:15-18.
3. Turrens J.F. Superoxide production by the mitochondrial respiratory chain. Bioscience Reports 1997, 17:3-8.
4. Lambert A.J., Brand M.D. Reactive oxygen species production by mitochondria. Methods in Molecular Biology 2009, 554:165-181.
5. Sack M.N. Mitochondrial depolarization and the role of uncoupling proteins in ischemia tolerance. Cardiovascular Research 2006, 72:210-219.
6. McLeod C.J., Aziz A., Hoyt R.F., McCoy J.P., Sack M.N. Uncoupling proteins 2 and 3 function in concert to augment tolerance to cardiac ischemia. Journal of Biological Chemistry 2005, 280:33470-33476.
7. Korde A.S., Pettigrew L.C., Craddock S.D., Maragos W.F. The mitochondrial uncoupler 2,4-dinitrophenol attenuates tissue damage and improves mitochondrial homeostasis following transient focal cerebral ischemia. Journal of Neurochemistry 2005, 94:1676-1684.
8. Modriansky M., Gabrielova E. Uncouple my heart: the benefits of inefficiency. Journal of Bioenergetics and Biomembranes 2009, 41:133-136.
9. Wu Y.N., Munhall A.C., Johnson S.W. Mitochondrial uncoupling agents antagonize rotenone actions in rat substantia nigra dopamine neurons. Brain Research 2011, 1395:86-93.
10. Anderson E.J., Lustig M.E., Boyle K.E., Woodlief T.L., Kane D.A., Lin C.T., et al. Mitochondrial h2o2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. Journal of Clinical Investigation 2009, 119:573-581.
11. Hoehn K.L., Salmon A.B., Hohnen-Behrens C., Turner N., Hoy A.J., Maghzal G.J., et al. Insulin resistance is a cellular antioxidant defense mechanism. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:17787-17792.
12. Caldeira da Silva C.C., Cerqueira F.M., Barbosa L.F., Medeiros M.H., Kowaltowski A.J. Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity. Aging Cell 2008, 7:552-560.
13. Brennan J.P., Southworth R., Medina R.A., Davidson S.M., Duchen M.R., Shattock M.J. Mitochondrial uncoupling, with low concentration FCCP, induces ROS-dependent cardioprotection independent of KATP channel activation. Cardiovascular Research 2006, 72:313-321.
14. Tseng Y.H., Cypess A.M., Kahn C.R. Cellular bioenergetics as a target for obesity therapy. Nature Reviews Drug Discovery 2010, 9:465-482.
15. + currents in bovine aortic endothelial cells. Pflügers Archiv 2002, 443:344-352.
16. Juthberg S.K., Brismar T. Effect of metabolic inhibitors on membrane potential and ion conductance of rat astrocytes. Cellular and Molecular Neurobiology 1997, 17:367-377.
17. Brismar T., Collins V.P. Effect of external cation concentration and metabolic inhibitors on membrane potential of human glial cells. Journal of Physiology 1993, 460:365-383.
18. Buckler K.J., Vaughan-Jones R.D. Effects of mitochondrial uncouplers on intracellular calcium, pH and membrane potential in rat carotid body type I cells. Journal of Physiology 1998, 513(Pt 3):819-833.
19. Rogers G.W., Brand M.D., Petrosyan S., Ashok D., Elorza A.A., Ferrick D.A., et al. High throughput microplate respiratory measurements using minimal quantities of isolated mitochondria. PLoS One 2011, 6:e21746.
20. Divakaruni A.S., Wiley S.E., Rogers G.W., Andreyev A.Y., Petrosyan S., Loviscach M., et al. Thiazolidinediones are acute, specific inhibitors of the mitochondrial pyruvate carrier. Proceedings of the National Academy of Sciences of the United States of America 2013, 110:5422-5427.
21. Shchepinova M.M., Denisov S.S., Kotova E.A., Khailova L.S., Knorre D.A., Korshunova G.A., et al. Dodecyl and octyl esters of fluorescein as protonophores and uncouplers of oxidative phosphorylation in mitochondria at submicromolar concentrations. Biochimica et Biophysica Acta 2013, 1837:149-158.
22. Li L., Huang L., Ye H., Song S.P., Bajwa A., Lee S.J., et al. Dendritic cells tolerized with adenosine A(2)AR agonist attenuate acute kidney injury. Journal of Clinical Investigation 2012, 122:3931-3942.
23. Bajwa A., Jo S.K., Ye H., Huang L., Dondeti K.R., Rosin D.L., et al. Activation of sphingosine-1-phosphate 1 receptor in the proximal tubule protects against ischemia-reperfusion injury. Journal of the American Society of Nephrology 2010, 21:955-965.
24. Li L., Huang L., Sung S.S., Lobo P.I., Brown M.G., Gregg R.K., et al. Nkt cell activation mediates neutrophil ifn-gamma production and renal ischemia-reperfusion injury. Journal of Immunology 2007, 178:5899-5911.
25. Nicholls D.G., Ferguson S.J. Bioenergetics 2002, 3:297. (xviii, 297 p.).
26. Lou P.H., Hansen B.S., Olsen P.H., Tullin S., Murphy M.P., Brand M.D. Mitochondrial uncouplers with an extraordinary dynamic range. Biochemical Journal 2007, 407:129-140.
27. Minners J., van den Bos E.J., Yellon D.M., Schwalb H., Opie L.H., Sack M.N. Dinitrophenol, cyclosporin a, and trimetazidine modulate preconditioning in the isolated rat heart: support for a mitochondrial role in cardioprotection. Cardiovascular Research 2000, 47:68-73.
28. Brand M.D., Nicholls D.G. Assessing mitochondrial dysfunction in cells. Biochemical Journal 2011, 435:297-312.
29. Murphy M.P. How mitochondria produce reactive oxygen species. Biochemical Journal 2009, 417:1-13.
30. Pandya J.D., Pauly J.R., Sullivan P.G. The optimal dosage and window of opportunity to maintain mitochondrial homeostasis following traumatic brain injury using the uncoupler FCCP. Experimental Neurology 2009, 218:381-389.
31. Stout A.K., Raphael H.M., Kanterewicz B.I., Klann E., Reynolds I.J. Glutamate-induced neuron death requires mitochondrial calcium uptake. Nature Neuroscience 1998, 1:366-373.
32. Maragos W.F., Rockich K.T., Dean J.J., Young K.L. Pre- or post-treatment with the mitochondrial uncoupler 2,4-dinitrophenol attenuates striatal quinolinate lesions. Brain Research 2003, 966:312-316.
33. Brennan J.P., Berry R.G., Baghai M., Duchen M.R., Shattock M.J. FCCP is cardioprotective at concentrations that cause mitochondrial oxidation without detectable depolarisation. Cardiovascular Research 2006, 72:322-330.