A carbon monoxide-releasing molecule (CORM-3) uncouples mitochondrial respiration and modulates the production of reactive oxygen species

Free Radical Biology and Medicine

Volumn 50, Issue 11, 2011, Pages 1556-1564

  Lo Iacono, Luisa ^a   Boczkowski, Jorge ^b   Zini, Roland ^b   Salouage, Issam ^b   Berdeaux, Alain ^b   Motterlini, Roberto ^a,b   Morin, Didier ^b  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

Author keywords

Carbon monoxide; CO releasing molecules; Free radicals; Mitochondrial respiration; Reactive oxygen species; Uncoupling agents

Indexed keywords

5 HYDROXYDECANOIC ACID; ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE DIPHOSPHATE; CARBON MONOXIDE; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; CARBOXYATRACTYLOSIDE; CYTOCHROME C OXIDASE; GUANOSINE DIPHOSPHATE; HYDROGEN PEROXIDE; MALIC ACID; MALONIC ACID; MYOGLOBIN; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RHODAMINE; RUTHENIUM DERIVATIVE; SUCCINIC ACID; TRICARBONYLCHLORO(GLYCINATO)RUTHENIUM; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HEART MITOCHONDRION; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RAT;

ANIMALS; CARBON MONOXIDE; CELL RESPIRATION; ELECTRON TRANSPORT COMPLEX II; HEART; HYDROGEN PEROXIDE; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, HEART; ORGANOMETALLIC COMPOUNDS; OXIDATIVE COUPLING; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES;

MAMMALIA;

EID: 79955598078     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.02.033     Document Type: Article

References (51)

1. C.A. Piantadosi Biological chemistry of carbon monoxide Antioxid. Redox Signaling 4 2002 259 270 (Pubitemid 34517177)
2. R. Foresti, M.G. Bani-Hani, and R. Motterlini Use of carbon monoxide as a therapeutic agent: promises and challenges Intensive Care Med. 34 2008 649 658
3. C.A. Piantadosi Carbon monoxide, reactive oxygen signaling, and oxidative stress Free Radic. Biol. Med. 45 2008 562 569
4. J. Boczkowski, J.J. Poderoso, and R. Motterlini CO-metal interaction: vital signaling from a lethal gas Trends Biochem. Sci. 31 2006 614 621 (Pubitemid 44740399)
5. S.W. Ryter, J. Alam, and A.M. Choi Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications Physiol. Rev. 86 2006 583 650
6. J.E. Clark, R. Foresti, C.J. Green, and R. Motterlini Dynamics of haem oxygenase-1 expression and bilirubin production in cellular protection against oxidative stress Biochem. J. 348 2000 615 619 (Pubitemid 30410252)
7. R. Foresti, H. Goatly, C.J. Green, and R. Motterlini Role of heme oxygenase-1 in hypoxia-reoxygenation: requirement of substrate heme to promote cardioprotection Am. J. Physiol. Heart Circ. Physiol. 281 2001 H1976 H1984
8. R. Motterlini, and L.E. Otterbein Therapeutic potential of carbon monoxide Nat. Rev. Drug Discovery 9 2010 728 743
9. R. Motterlini, J.E. Clark, R. Foresti, P. Sarathchandra, B.E. Mann, and C.J. Green Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities Circ. Res. 90 2002 E17 E24
10. J.E. Clark, P. Naughton, S. Shurey, C.J. Green, T.R. Johnson, B.E. Mann, R. Foresti, and R. Motterlini Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule Circ. Res. 93 2003 e2 e8
11. P. Sawle, R. Foresti, B.E. Mann, T.R. Johnson, C.J. Green, and R. Motterlini Carbon monoxide-releasing molecules (CO-RMs) attenuate the inflammatory response elicited by lipopolysaccharide in RAW264.7 murine macrophages Br. J. Pharmacol. 145 2005 800 810 (Pubitemid 41076287)
12. M.J. Alcaraz, M.I. Guillen, M.L. Ferrandiz, J. Megias, and R. Motterlini Carbon monoxide-releasing molecules: a pharmacological expedient to counteract inflammation Curr. Pharm. Des. 14 2008 465 472 (Pubitemid 351516851)
13. H.B. Suliman, M.S. Carraway, A.S. Ali, C.M. Reynolds, K.E. Welty-Wolf, and C.A. Piantadosi The CO/HO system reverses inhibition of mitochondrial biogenesis and prevents murine doxorubicin cardiomyopathy J. Clin. Invest. 117 2007 3730 3741 (Pubitemid 350224084)
14. S. Lancel, S.M. Hassoun, R. Favory, B. Decoster, R. Motterlini, and R. Neviere Carbon monoxide rescues mice from lethal sepsis by supporting mitochondrial energetic metabolism and activating mitochondrial biogenesis J. Pharmacol. Exp. Ther. 1329 2009 641 648
15. D.C. Wallace, W. Fan, and V. Procaccio Mitochondrial energetics and therapeutics Annu. Rev. Pathol. 5 2010 297 348
16. S. Raha, and B.H. Robinson Mitochondria, oxygen free radicals, disease and ageing Trends Biochem. Sci. 25 2000 502 508
17. A.J. Lambert, and M.D. Brand Superoxide production by NADH:ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane Biochem. J. 382 2004 511 517 (Pubitemid 39243917)
18. M.D. Brand, C. Affourtit, T.C. Esteves, K. Green, A.J. Lambert, S. Miwa, J.L. Pakay, and N. Parker Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins Free Radic. Biol. Med. 37 2004 755 767 (Pubitemid 39078548)
19. M.D. Brand Uncoupling to survive? The role of mitochondrial inefficiency in ageing Exp. Gerontol. 35 2000 811 820
20. S. Krauss, C.Y. Zhang, and B.B. Lowell The mitochondrial uncoupling-protein homologues Nat. Rev. Mol. Cell Biol. 6 2005 248 261 (Pubitemid 40314925)
21. M.D. Brand, J.L. Pakay, A. Ocloo, J. Kokoszka, D.C. Wallace, P.S. Brookes, and E.J. Cornwall The basal proton conductance of mitochondria depends on adenine nucleotide translocase content Biochem. J. 392 2005 353 362 (Pubitemid 41796524)
22. G. Mattiasson, and P.G. Sullivan The emerging functions of UCP2 in health, disease, and therapeutics Antioxid. Redox Signaling 8 2006 1 38 (Pubitemid 43324527)
23. J.D. Sharer The adenine nucleotide translocase type 1 (ANT1): a new factor in mitochondrial disease IUBMB Life 57 2005 607 614 (Pubitemid 41530548)
24. Y. Emre, C. Hurtaud, M. Karaca, T. Nubel, F. Zavala, and D. Ricquier Role of uncoupling protein UCP2 in cell-mediated immunity: how macrophage-mediated insulitis is accelerated in a model of autoimmune diabetes Proc. Natl Acad. Sci. U. S. A. 104 2007 19085 19090
25. R. Motterlini, P. Sawle, S. Bains, J. Hammad, R. Alberto, R. Foresti, and C.J. Green CORM-A1: a new pharmacologically active carbon monoxide-releasing molecule FASEB J. 19 2005 284 286 (Pubitemid 40189283)
26. O.H. Lowry, N.J. Rosenbrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
27. R.K. Emaus, R. Grunwald, and J.J. Lemasters Rhodamine 123 as a probe of transmembrane potential in isolated rat-liver mitochondria: spectral and metabolic properties Biochim. Biophys. Acta 850 1986 436 448 (Pubitemid 16077550)
28. A. Barrientos In vivo and in organello assessment of OXPHOS activities Methods 26 2002 307 316 (Pubitemid 34971570)
29. R. Foresti, J. Hammad, J.E. Clark, R.A. Johnson, B.E. Mann, A. Friebe, C.J. Green, and R. Motterlini Vasoactive properties of CORM-3, a novel water-soluble carbon monoxide-releasing molecule Br. J. Pharmacol. 142 2004 453 460 (Pubitemid 38869858)
30. P.A. Townsend, S.M. Davidson, S.J. Clarke, I. Khaliulin, C.J. Carroll, T.M. Scarabelli, R.A. Knight, A. Stephanou, D.S. Latchman, and A.P. Halestrap Urocortin prevents mitochondrial permeability transition in response to reperfusion injury indirectly by reducing oxidative stress Am. J. Physiol. Heart Circ. Physiol. 293 2007 H928 H938
31. B.S. Zuckerbraun, B.Y. Chin, M. Bilban, D.J. de Costa, J. Rao, T.R. Billiar, and L.E. Otterbein Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species FASEB J. 21 2007 1099 1106 (Pubitemid 46495699)
32. S.S. Korshunov, V.P. Skulachev, and A.A. Starkov High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria FEBS Lett. 416 1997 15 18 (Pubitemid 27470791)
33. A.J. Lambert, and M.D. Brand Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I) J. Biol. Chem. 279 2004 39414 39420 (Pubitemid 39258206)
34. A. Sandouka, E. Balogun, R. Foresti, B.E. Mann, T.R. Johnson, Y. Tayem, C.J. Green, B. Fuller, and R. Motterlini Carbon monoxide-releasing molecules (CO-RMs) modulate respiration in isolated mitochondria Cell. Mol. Biol. 51 2005 425 432 (Pubitemid 41596320)
35. M. Desmard, J. Boczkowski, J. Poderoso, and R. Motterlini Mitochondrial and cellular heme-dependent proteins as targets for the bioactive function of the heme oxygenase/carbon monoxide system Antioxid. Redox Signaling 9 2007 2139 2155 (Pubitemid 350059023)
36. J.A. Harper, K. Dickinson, and M.D. Brand Mitochondrial uncoupling as a target for drug development for the treatment of obesity Obes. Rev. 2 2001 255 265 (Pubitemid 33755901)
37. V.P. Skulachev Uncoupling new approaches to an old problem of bioenergetics Biochim. Biophys. Acta 1363 1998 100 124 (Pubitemid 28129344)
38. A.A. Starkov, V.I. Dedukhova, and V.P. Skulachev 6-Ketocholestanol abolishes the effect of the most potent uncouplers of oxidative phosphorylation in mitochondria FEBS Lett. 355 1994 305 308 (Pubitemid 24359928)
39. K.S. Echtay Mitochondrial uncoupling proteins-what is their physiological role? Free Radic. Biol. Med. 43 2007 1351 1371 (Pubitemid 47532367)
40. A.Y. Andreyev, T.O. Bondareva, V.I. Dedukhova, E.N. Mokhova, V.P. Skulachev, L.M. Tsofina, N.I. Volkov, and T.V. Vygodina The ATP/ADP-antiporter is involved in the uncoupling effect of fatty acids on mitochondria Eur. J. Biochem. 182 1989 585 592 (Pubitemid 19169954)
41. C.S. Queiroga, A.S. Almeida, C. Martel, C. Brenner, P.M. Alves, and H.L. Vieira Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilization and apoptosis J. Biol. Chem. 285 2010 17077 17088
42. M.A. Di Noia, S. Van Driesche, F. Palmieri, L.M. Yang, S. Quan, A.I. Goodman, and N.G. Abraham Heme oxygenase-1 enhances renal mitochondrial transport carriers and cytochrome C oxidase activity in experimental diabetes J. Biol. Chem. 281 2006 15687 15693 (Pubitemid 43848455)
43. P. Rustin, A. Munnich, and A. Rotig Succinate dehydrogenase and human diseases: new insights into a well-known enzyme Eur. J. Hum. Genet. 10 2002 289 291 (Pubitemid 34778046)
44. O. Miro, J.R. Alonso, D. Jarreta, J. Casademont, A. Urbano-Marquez, and F. Cardellach Smoking disturbs mitochondrial respiratory chain function and enhances lipid peroxidation on human circulating lymphocytes Carcinogenesis 20 1999 1331 1336 (Pubitemid 29341457)
45. L. Susheela, K. Venkatesan, and T. Ramasarma Structural and kinetic studies on the activators of succinate dehydrogenase Biochim. Biophys. Acta 480 1977 47 55 (Pubitemid 8006370)
46. 2 by mitochondria in the resting state FEBS Lett. 435 1998 215 218 (Pubitemid 28435003)
47. Q. Chen, S. Moghaddas, C.L. Hoppel, and E.J. Lesnefsky Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria Am. J. Physiol. Cell Physiol. 294 2008 C460 C466
48. Y.R. Chen, C.L. Chen, D.R. Pfeiffer, and J.L. Zweier Mitochondrial complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation J. Biol. Chem. 282 2007 32640 32654 (Pubitemid 350159288)
49. C. Taille, J. El-Benna, S. Lanone, J. Boczkowski, and R. Motterlini Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle J. Biol. Chem. 280 2005 25350 25360 (Pubitemid 40962237)
50. 2+ channels via redox modulation of key cysteine residues by mitochondrial reactive oxygen species J. Biol. Chem. 283 2008 24412 24419
51. G. Wang, T. Hamid, R.J. Keith, G. Zhou, C.R. Partridge, X. Xiang, J.R. Kingery, R.K. Lewis, Q. Li, D.G. Rokosh, R. Ford, F.G. Spinale, D.W. Riggs, S. Srivastava, A. Bhatnagar, R. Bolli, and S.D. Prabhu Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart Circulation 121 2010 1912 1925