Rapid uptake of lipophilic triphenylphosphonium cations by mitochondria in vivo following intravenous injection: Implications for mitochondria-specific therapies and probes

Biochimica et Biophysica Acta - General Subjects

Volumn 1800, Issue 9, 2010, Pages 1009-1017

  Porteous, Carolyn M ^a   Logan, Angela ^b   Evans, Cameron ^a   Ledgerwood, Elizabeth C ^a   Menon, David K ^c   Aigbirhio, Franklin ^d   Smith, Robin A J ^a   Murphy, Michael P ^b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Antioxidant; Mitochondrion; MitoQ; Oxidative stress; Phosphonium cation

Indexed keywords

PHOSPHONIUM DERIVATIVE; TRIPHENYLPHOSPHONIUM; UNCLASSIFIED DRUG; ANTIOXIDANT; CATION; ORGANOPHOSPHORUS COMPOUND;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL FUNCTION; CHEMICAL STRUCTURE; CONTROLLED STUDY; FEMALE; HYDROPHOBICITY; IN VIVO STUDY; LIPOPHILICITY; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; SYNTHESIS; TISSUE DISTRIBUTION; ANIMAL; DRUG DELIVERY SYSTEM; DRUG EFFECTS; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; MITOCHONDRIAL DISEASES; MITOCHONDRION; PATHOLOGY;

MUS;

ANIMALS; ANTIOXIDANTS; CATIONS; DRUG DELIVERY SYSTEMS; FEMALE; INJECTIONS, INTRAVENOUS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MITOCHONDRIAL DISEASES; ORGANOPHOSPHORUS COMPOUNDS;

EID: 77955266918     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2010.06.001     Document Type: Article

References (51)

1. Ross M.F., Kelso G.F., Blaikie F.H., James A.M., Cocheme H.M., Filipovska A., et al. Lipophilic triphenylphosphonium cations as tools in mitochondrial bioenergetics and free radical biology. Biochemistry (Mosc.) 2005, 70:222-230.
2. Murphy M.P. Targeting bioactive compounds to mitochondria. Trends Biotechnol. 1997, 15:326-330.
3. Murphy M.P., Smith R.A.J. Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu. Rev. Pharmacol. Toxicol. 2007, 47:629-656.
4. Smith R.A.J., Porteous C.M., Coulter C.V., Murphy M.P. Targeting an antioxidant to mitochondria. Eur. J. Biochem. 1999, 263:709-716.
5. Kelso G.F., Porteous C.M., Coulter C.V., Hughes G., Porteous W.K., Ledgerwood E.C., et al. Selective targeting of a redox-active ubiquinone to mitochondria within cells. J. Biol. Chem. 2001, 276:4588-4596.
6. Plotnikov E.Y., Vasileva A.K., Arkhangelskaya A.A., Pevzner I.B., Skulachev V.P., Zorov D.B. Interrelations of mitochondrial fragmentation and cell death under ischemia/reoxygenation and UV-irradiation: protective effects of SkQ1, lithium ions and insulin. FEBS Lett. 2008, 582:3117-3124.
7. Dhanasekaran A., Kotamraju S., Karunakaran C., Kalivendi S.V., Thomas S., Joseph J., et al. Mitochondria superoxide dismutase mimetic inhibits peroxide-induced oxidative damage and apoptosis: role of mitochondrial superoxide. Free Radic. Biol. Med. 2005, 39:567-583.
8. Burns R.J., Smith R.A.J., Murphy M.P. Synthesis and characterization of thiobutyltriphenylphosphonium bromide, a novel thiol reagent targetted to the mitochondrial matrix. Arch. Biochem. Biophys. 1995, 322:60-68.
9. Lin T.K., Hughes G., Muratovska A., Blaikie F.H., Brookes P.S., Darley-Usmar V., et al. Specific modification of mitochondrial protein thiols in response to oxidative stress: a proteomics approach. J. Biol. Chem. 2002, 277:17048-17056.
10. Murphy M.P., Echtay K.S., Blaikie F.H., Asin-Cayuela J., Cocheme H.M., Green K., et al. Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation: studies using a mitochondria-targeted spin trap derived from alpha-phenyl-N-tert-butylnitrone. J. Biol. Chem. 2003, 278:48534-48545.
11. Xu Y., Kalyanaraman B. Synthesis and ESR studies of a novel cyclic nitrone spin trap attached to a phosphonium group-a suitable trap for mitochondria-generated ROS?. Free Radic. Res. 2007, 41:1-7.
12. Hardy M., Rockenbauer A., Vasquez-Vivar J., Felix C., Lopez M., Srinivasan S., et al. Detection, characterization, and decay kinetics of ROS and thiyl adducts of mito-DEPMPO spin trap. Chem. Res. Toxicol. 2007, 20:1053-1060.
13. Hardy M., Chalier F., Ouari O., Finet J.P., Rockenbauer A., Kalyanaraman B., et al. Mito-DEPMPO synthesized from a novel NH2-reactive DEPMPO spin trap: a new and improved trap for the detection of superoxide. Chem. Commun. 2007, 1083-1085.
14. Robinson K.M., Janes M.S., Pehar M., Monette J.S., Ross M.F., Hagen T.M., et al. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15038-15043.
15. Dickinson B.C., Chang C.J. A targetable fluorescent probe for imaging hydrogen peroxide in the mitochondria of living cells. J. Am. Chem. Soc. 2008, 130:9638-9639.
16. Patel J., Rideout D., McCarthy M.R., Calogeropoulou T., Wadwa K.S., Oseroff A.R. Antineoplastic activity, synergism and antagonism of trialkylphsphonium salts and their combinations. Anticancer Res. 1994, 14:21-28.
17. Manetta A., Gamboa G., Nasseri A., Podnos Y.D., Ema D., Dorion G., et al. Novel phosphonium salts display in vitro and in vivo cytotoxic activity against ovarian cancer cell lines. Gynecol. Oncol. 1996, 60:203-212.
18. James A.M., Blaikie F.H., Smith R.A.J., Lightowlers R.N., Smith P.M., Murphy M.P. Specific targeting of a DNA-alkylating reagent to mitochondria. Synthesis and characterization of [4-((11aS)-7-methoxy-1, 2, 3, 11a-tetrahydro-5H-pyrrolo[2, 1-c][1, 4]benzodiaze pin-5-on-8-oxy)butyl]-triphenylphosphonium iodide. Eur. J. Biochem. 2003, 270:2827-2836.
19. Prime T.A., Blaikie F.H., Evans C., Nadtochiy S.M., James A.M., Dahm C.C., et al. A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:10764-10769.
20. Smith R.A.J., Porteous C.M., Gane A.M., Murphy M.P. Delivery of bioactive molecules to mitochondria in vivo. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:5407-5412.
21. Esplugues J.V., Rocha M., Nunez C., Bosca I., Ibiza S., Herance J.R., et al. Complex I dysfunction and tolerance to nitroglycerin: an approach based on mitochondrial-targeted antioxidants. Circ. Res. 2006, 99:1067-1075.
22. Adlam V.J., Harrison J.C., Porteous C.M., James A.M., Smith R.A.J., Murphy M.P., et al. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J. 2005, 19:1088-1095.
23. Neuzil J., Widen C., Gellert N., Swettenham E., Zobalova R., Dong L.F., et al. Mitochondria transmit apoptosis signalling in cardiomyocyte-like cells and isolated hearts exposed to experimental ischemia-reperfusion injury. Redox Rep. 2007, 12:148-162.
24. Lowes D.A., Thottakam B.M., Webster N.R., Murphy M.P., Galley H.F. The mitochondria-targeted antioxidant MitoQ protects against organ damage in a lipopolysaccharide-peptidoglycan model of sepsis. Free Radic. Biol. Med. 2008, 45:1559-1565.
25. Chandran K., et al. Doxorubicin inactivates myocardial cytochrome c oxidase in rats: cardioprotection by MitoQ. Biophys. J. 2009, 96:1388-1398.
26. Graham D., Huynh N.N., Hamilton C.A., Beattie E., Smith R.A.J., Cochemé H.M., et al. The mitochondria targeted antioxidant MitoQ10 improves endothelial function and attenuates cardiac hypertrophy. Hypertension 2009, 54:322-328.
27. Rodriguez-Cuenca S., Cochemé H.M., Logan A., Abakumova I., Prime T.A., Rose C., et al. Consequences of long-term oral administration of the mitochondria-targeted antioxidant MitoQ to wild-type mice. Free Radic. Biol. Med. 2010, 48:161-172.
28. B.J. Snow, F.L. Rolfe, M.M. Lockhart, C.M. Frampton, J. O'Sullivan, V. Fung, et al. A double-blind, placebo-controlled study to assess the mitochondria-targeted antioxidant mitoQ as a disease modifying therapy in Parkinson's disease. Mov. Disord. in press.
29. E.J.Gane, F. Weilert, D.W. Orr, G.F. Keogh, M. Gibson, M. Gibson, et al. The mitochondria-targeted antioxidant mitoquinone decreases liver damage in a phase II study of hepatitis C patients. Liver Int. in press. http://doi:10.1111/j.1478-3231.2010.02250.x.
30. Piot C., Croisille P., Staat P., Thibault H., Rioufol G., Mewton N., et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N. Engl. J. Med. 2008, 359:473-481.
31. 11C]TPMP in canine brain tumor: a PET study. J. Nucl. Med. 1999, 40:1180-1185.
32. Madar I., Ravert H.T., Du Y., Hilton J., Volokh L., Dannals R.F., et al. Characterization of uptake of the new PET imaging compound 18F-fluorobenzyl triphenylphosphonium in dog myocardium. J. Nucl. Med. 2006, 47:1359-1366.
33. Ross M.F., Prime T.A., Abakumova I., James A.M., Porteous C.M., Smith R.A.J., et al. Rapid and extensive uptake and activation of hydrophobic triphenylphosphonium cations within cells. Biochem. J. 2008, 411:633-645.
34. Albanese D., Landini D., Penso M. Hydrated tetrabutylammonium fluoride as a powerful nucleophilic fluorinating agent. J. Org. Chem. 1998, 63:9587-9589.
35. Pattison F.L.M., Howell W.C., McNamara A.J., Schneider J.C., Walker J.F. Toxic fluorine compoundsIII. ω-Fluoro alcohols. J. Org. Chem. 1956, 21:739-747.
36. Shimizu M., Nakahara Y., Yoshioka H. Chemoselective fluorination for primary alcohols. Tetrahedron Lett. 1985, 26:4207-4210.
37. Smith R.A.J., Kelso G.F., James A.M., Murphy M.P. Targeting coenzyme Q derivatives to mitochondria. Meth. Enzymol. 2004, 382:45-67.
38. McAllister P.R., Dotson M.J., Grim S.O., Hillman G.R. Effects of phosphonium compounds on Schistosoma mansoni. J. Med. Chem. 1980, 23:862-865.
39. Trujillo J.G., Ceballos G., Yanez R., Joseph-Nathan P. Regioselective synthesis of (+)-(S)-2-amino-5-(iodoacetamido)pentanoic and (+)-(S)-2-amino-6-(iodoacetamido)hexanoic acids. Synth. Commun. 1991, 21:683-691.
40. Asin-Cayuela J., Manas A.R., James A.M., Smith R.A.J., Murphy M.P. Fine-tuning the hydrophobicity of a mitochondria-targeted antioxidant. FEBS Lett. 2004, 571:9-16.
41. James A.M., Cocheme H.M., Smith R.A.J., Murphy M.P. Interactions of mitochondria-targeted and untargeted ubiquinones with the mitochondrial respiratory chain and reactive oxygen species. Implications for the use of exogenous ubiquinones as therapies and experimental tools. J. Biol. Chem. 2005, 280:21295-21312.
42. Chappell J.B., Hansford R.G. Preparation of mitochondria from animal tissues and yeasts. Subcellular Components: Preparation and Fractionation 1972, 77-91. Butterworths, London. G.D. Birnie (Ed.).
43. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., et al. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150:76-85.
44. Ross M.F., Filipovska A., Smith R.A.J., Gait M.J., Murphy M.P. Cell-penetrating peptides do not cross mitochondrial membranes even when conjugated to a lipophilic cation: evidence against direct passage through phospholipid bilayers. Biochem. J. 2004, 383:457-468.
45. Li Y., Zhang H., Fawcett J.P., Tucker I.G. Quantitation and metabolism of mitoquinone, a mitochondria-targeted antioxidant, in rat by liquid chromatography/tandem mass spectrometry. Rapid. Commun. Mass. Spectrom. 2007, 21:1958-1964.
46. Ross M.F., Da Ros T., Blaikie F.H., Prime T.A., Porteous C.M., Severina I.I., et al. Accumulation of lipophilic dications by mitochondria and cells. Biochem. J. 2006, 400:199-208.
47. 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. J. Neurochem. 2005, 94:1676-1684.
48. Korde A.S., Sullivan P.G., Maragos W.F. The uncoupling agent 2, 4-dinitrophenol improves mitochondrial homeostasis following striatal quinolinic acid injections. J. Neurotrauma 2005, 22:1142-1149.
49. Pandya J.D., Pauly J.R., Nukala V.N., Sebastian A.H., Day K.M., Korde A.S., et al. Post-injury administration of mitochondrial uncouplers increases tissue sparing and improves behavioral outcome following traumatic brain injury in rodents. J. Neurotrauma 2007, 24:798-811.
50. Chen L.B. Mitochondrial membrane potential in living cells. Ann. Rev. Cell Biol. 1988, 4:155-181.
51. Murphy M.P., Smith R.A.J. Drug delivery to mitochondria: the key to mitochondrial medicine. Adv. Drug Deliv. Rev. 2000, 41:235-250.