P-glycoprotein (Mdr1a/1b) and breast cancer resistance protein (Bcrp) decrease the uptake of hydrophobic alkyl triphenylphosphonium cations by the brain

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 6, 2013, Pages 3458-3465

  Porteous, Carolyn M ^a   Menon, David K ^b   Aigbirhio, Franklin I ^c   Smith, Robin A J ^a   Murphy, Michael P ^d  

^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

ABC transporters; Blood brain barrier; Lipophilic cation; Mitochondria; MitoQ

Indexed keywords

11 FLUORODECYLTRIPHENYLPHOSPHONIUM MESYLATE; BREAST CANCER RESISTANCE PROTEIN; CYCLOSPORIN A; METHYLTRIPHENYLPHOSPHONIUM; MITOQ; MITOQUINONE; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 1A; MULTIDRUG RESISTANCE PROTEIN 1B; PHOSPHONIUM DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG BRAIN LEVEL; DRUG DISTRIBUTION; DRUG LIVER LEVEL; DRUG STRUCTURE; DRUG TRANSPORT; DRUG UPTAKE; FEMALE; IN VIVO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BLOOD-BRAIN BARRIER; HETEROCYCLIC COMPOUNDS; LIVER; MICE; MICE, KNOCKOUT; MITOCHONDRIAL DISEASES; NERVE TISSUE PROTEINS; ORGANOPHOSPHORUS COMPOUNDS; ORGANOSELENIUM COMPOUNDS; P-GLYCOPROTEINS;

MUS; MUS MUSCULUS;

EID: 84875978344     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.02.005     Document Type: Article

References (57)

1. R.A.J. Smith, R.C. Hartley, H.M. Cochemé, and M.P. Murphy Mitochondrial pharmacology Trends Pharmacol. Sci. 33 2012 341 352
2. P. Coskun, J. Wyrembak, S.E. Schriner, H.W. Chen, C. Marciniack, F. Laferla, and D.C. Wallace A mitochondrial etiology of Alzheimer and Parkinson disease Biochim. Biophys. Acta Gen. Subj. 1820 2012 553 564
3. D.C. Wallace, W. Fan, and V. Procaccio Mitochondrial energetics and therapeutics Annu. Rev. Pathol. 5 2010 297 348
4. M.R. Duchen, and G. Szabadkai Roles of mitochondria in human disease Essays Biochem. 47 2010 115 137
5. M.P. Murphy, and R.A.J. Smith Targeting antioxidants to mitochondria by conjugation to lipophilic cations Annu. Rev. Pharmacol. Toxicol. 47 2007 629 656
6. R.A.J. Smith, R.C. Hartley, and M.P. Murphy Mitochondria-targeted small molecule therapeutics and probes Antioxid. Redox Signal. 15 2011 3021 3038
7. M.F. Ross, G.F. Kelso, F.H. Blaikie, A.M. James, H.M. Cochemé, A. Filipovska, T. Da Ros, T.R. Hurd, R.A.J. Smith, and M.P. Murphy Lipophilic triphenylphosphonium cations as tools in mitochondrial bioenergetics and free radical biology Biochemistry (Mosc) 70 2005 222 230
8. M.P. Murphy Targeting bioactive compounds to mitochondria Trends Biotechnol. 15 1997 326 330
9. R.A.J. Smith, C.M. Porteous, C.V. Coulter, and M.P. Murphy Targeting an antioxidant to mitochondria Eur. J. Biochem. 263 1999 709 716
10. G.F. Kelso, C.M. Porteous, C.V. Coulter, G. Hughes, W.K. Porteous, E.C. Ledgerwood, R.A.J. Smith, and M.P. Murphy Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties J. Biol. Chem. 276 2001 4588 4596
11. A. Dhanasekaran, S. Kotamraju, C. Karunakaran, S.V. Kalivendi, S. Thomas, J. Joseph, and B. Kalyanaraman Mitochondria superoxide dismutase mimetic inhibits peroxide-induced oxidative damage and apoptosis: role of mitochondrial superoxide Free Radic. Biol. Med. 39 2005 567 583
12. R.J. Burns, R.A.J. Smith, and M.P. Murphy Synthesis and characterization of thiobutyltriphenylphosphonium bromide, a novel thiol reagent targeted to the mitochondrial matrix Arch. Biochem. Biophys. 322 1995 60 68
13. T.K. Lin, G. Hughes, A. Muratovska, F.H. Blaikie, P.S. Brookes, V. Darley-Usmar, R.A.J. Smith, and M.P. Murphy Specific modification of mitochondrial protein thiols in response to oxidative stress: a proteomics approach J. Biol. Chem. 277 2002 17048 17056
14. M.P. Murphy, K.S. Echtay, F.H. Blaikie, J. Asin-Cayuela, H.M. Cochemé, K. Green, J.A. Buckingham, E.R. Taylor, F. Hurrell, G. Hughes, S. Miwa, C.E. Cooper, D.A. Svistunenko, R.A.J. Smith, and M.D. Brand 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. 278 2003 48534 48545
15. Y. Xu, and B. Kalyanaraman 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. 41 2007 1 7
16. M. Hardy, A. Rockenbauer, J. Vasquez-Vivar, C. Felix, M. Lopez, S. Srinivasan, N. Avadhani, P. Tordo, and B. Kalyanaraman Detection, characterization, and decay kinetics of ROS and thiol adducts of mito-DEPMPO spin trap Chem. Res. Toxicol. 20 2007 1053 1060
17. 2-reactive DEPMPO spin trap: a new and improved trap for the detection of superoxide Chem. Commun. 2007 1083 1085
18. K.M. Robinson, M.S. Janes, M. Pehar, J.S. Monette, M.F. Ross, T.M. Hagen, M.P. Murphy, and J.S. Beckman Selective fluorescent imaging of superoxide in vivo using ethidium-based probes Proc. Natl. Acad. Sci. U. S. A. 103 2006 15038 15043
19. B.C. Dickinson, and C.J. Chang A targetable fluorescent probe for imaging hydrogen peroxide in the mitochondria of living cells J. Am. Chem. Soc. 130 2008 9638 9639
20. 2 within living Drosophila during aging using a ratiometric mass spectrometry probe targeted to the mitochondrial matrix Cell Metab. 13 2011 340 350
21. T.A. Prime, M. Forkink, A. Logan, P. Finichiu, J. McLachlan, P.B. Li Pun, W.J. Koopman, L. Larsen, M.J. Latter, R.A.J. Smith, and M.P. Murphy A ratiometric fluorescent probe for assessing mitochondrial phospholipid peroxidation within living cells Free Radic. Biol. Med. 53 2012 544 553
22. J. Patel, D. Rideout, M.R. McCarthy, T. Calogeropoulou, K.S. Wadwa, and A.R. Oseroff Antineoplastic activity, synergism and antagonism of trialkylphsphonium salts and their combinations Anticancer. Res. 14 1994 21 28
23. A. Manetta, G. Gamboa, A. Nasseri, Y.D. Podnos, D. Ema, G. Dorion, L. Rawlings, P.M. Carpenter, A. Bustamante, J. Patel, and D. Rideout Novel phosphonium salts display in vitro and in vivo cytotoxic activity against ovarian cancer cell lines Gynecol. Oncol. 60 1996 203 212
24. A.M. James, F.H. Blaikie, R.A.J. Smith, R.N. Lightowlers, P.M. Smith, and M.P. Murphy 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. 270 2003 2827 2836
25. T.A. Prime, F.H. Blaikie, C. Evans, S.M. Nadtochiy, A.M. James, C.C. Dahm, D.A. Vitturi, R.P. Patel, C.R. Hiley, I. Abakumova, R. Requejo, E.T. Chouchani, T.R. Hurd, J.F. Garvey, C.T. Taylor, P.S. Brookes, R.A.J. Smith, and M.P. Murphy A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury Proc. Natl. Acad. Sci. U. S. A. 106 2009 10764 10769
26. J.V. Esplugues, M. Rocha, C. Nunez, I. Bosca, S. Ibiza, J.R. Herance, A. Ortega, J.M. Serrador, P. D'Ocon, and V.M. Victor Complex I dysfunction and tolerance to nitroglycerin: an approach based on mitochondrial-targeted antioxidants Circ. Res. 99 2006 1067 1075
27. V.J. Adlam, J.C. Harrison, C.M. Porteous, A.M. James, R.A.J. Smith, M.P. Murphy, and I.A. Sammut Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury FASEB J. 19 2005 1088 1095
28. J. Neuzil, C. Widen, N. Gellert, E. Swettenham, R. Zobalova, L.F. Dong, X.F. Wang, C. Lidebjer, H. Dalen, J.P. Headrick, and P.K. Witting Mitochondria transmit apoptosis signalling in cardiomyocyte-like cells and isolated hearts exposed to experimental ischemia-reperfusion injury Redox Rep. 12 2007 148 162
29. D.A. Lowes, B.M. Thottakam, N.R. Webster, M.P. Murphy, and H.F. Galley The mitochondria-targeted antioxidant MitoQ protects against organ damage in a lipopolysaccharide-peptidoglycan model of sepsis Free Radic. Biol. Med. 45 2008 1559 1565
30. K. Chandran, D. Aggarwal, R.Q. Migrino, J. Joseph, D. McAllister, E.A. Konorev, W.E. Antholine, J. Zielonka, S. Srinivasan, N.G. Avadhani, and B. Kalyanaraman Doxorubicin inactivates myocardial cytochrome c oxidase in rats: cardioprotection by MitoQ Biophys. J. 96 2009 1388 1398
31. 10 improves endothelial function and attenuates cardiac hypertrophy Hypertension 54 2009 322 328
32. S. Rodriguez-Cuenca, H.M. Cochemé, A. Logan, I. Abakumova, T.A. Prime, C. Rose, A. Vidal-Puig, A.C. Smith, D.C. Rubinsztein, I.M. Fearnley, B.A. Jones, S. Pope, S.J. Heales, B.Y. Lam, S.G. Neogi, I. McFarlane, A.M. James, R.A.J. Smith, and M.P. Murphy Consequences of long-term oral administration of the mitochondria-targeted antioxidant MitoQ to wild-type mice Free Radic. Biol. Med. 48 2010 161 172
33. B.J. Snow, F.L. Rolfe, M.M. Lockhart, C.M. Frampton, J.D. O'Sullivan, V. Fung, R.A.J. Smith, M.P. Murphy, and K.M. Taylor A double-blind, placebo-controlled study to assess the mitochondria-targeted antioxidant MitoQ as a disease-modifying therapy in Parkinson's disease Mov. Disord. 25 2010 1670 1674
34. E.J. Gane, F. Weilert, D.W. Orr, G.F. Keogh, M. Gibson, M.M. Lockhart, C.M. Frampton, K.M. Taylor, R.A.J. Smith, and M.P. Murphy The mitochondria-targeted anti-oxidant mitoquinone decreases liver damage in a phase II study of hepatitis C patients Liver Int. 30 2010 1019 1026
35. R.A.J. Smith, C.M. Porteous, A.M. Gane, and M.P. Murphy Delivery of bioactive molecules to mitochondria in vivo Proc. Natl. Acad. Sci. U. S. A. 100 2003 5407 5412
36. C.M. Porteous, A. Logan, C. Evans, E.C. Ledgerwood, D.K. Menon, F. Aigbirhio, R.A.J. Smith, and M.P. Murphy Rapid uptake of lipophilic triphenylphosphonium cations by mitochondria in vivo following intravenous injection: implications for mitochondria-specific therapies and probes Biochim. Biophys. Acta 1800 2010 1009 1017
37. A. Ghosh, K. Chandran, S.V. Kalivendi, J. Joseph, W.E. Antholine, C.J. Hillard, A. Kanthasamy, A. Kanthasamy, and B. Kalyanaraman Neuroprotection by a mitochondria-targeted drug in a Parkinson's disease model Free Radic. Biol. Med. 49 2010 1674 1684
38. M.J. McManus, M.P. Murphy, and J.L. Franklin The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer's disease J. Neurosci. 31 2011 15703 15715
39. M.F. Ross, T.A. Prime, I. Abakumova, A.M. James, C.M. Porteous, R.A.J. Smith, and M.P. Murphy Rapid and extensive uptake and activation of hydrophobic triphenylphosphonium cations within cells Biochem. J. 411 2008 633 645
40. A.M. James, M.S. Sharpley, A.R. Manas, F.E. Frerman, J. Hirst, R.A.J. Smith, and M.P. Murphy Interaction of the mitochondria-targeted antioxidant MitoQ with phospholipid bilayers and ubiquinone oxidoreductases J. Biol. Chem. 282 2007 14708 14718
41. D.S. Miller Regulation of P-glycoprotein and other ABC drug transporters at the blood-brain barrier Trends Pharmacol. Sci. 31 2010 246 254
42. A. Reichel Addressing central nervous system (CNS) penetration in drug discovery: basics and implications of the evolving new concept Chem. Biodivers. 6 2009 2030 2049
43. F. Klepsch, T. Stockner, T. Erker, M. Muller, P. Chiba, and G.F. Ecker Using structural and mechanistic information to design novel inhibitors/substrates of P-glycoprotein Curr. Top. Med. Chem. 10 2010 1769 1774
44. Y. Raviv, H.B. Pollard, E.P. Bruggemann, I. Pastan, and M.M. Gottesman Photosensitized labeling of a functional multidrug transporter in living drug-resistant tumor cells J. Biol. Chem. 265 1990 3975 3980
45. S.G. Aller, J. Yu, A. Ward, Y. Weng, S. Chittaboina, R. Zhuo, P.M. Harrell, Y.T. Trinh, Q. Zhang, I.L. Urbatsch, and G. Chang Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding Science 323 2009 1718 1722
46. 10, a mitochondria-targeted antioxidant, in Caco-2 cell monolayers J. Pharm. Pharmacol. 59 2007 503 511
47. n) in Caco-2 cell monolayers Eur. J. Drug Metab. Pharmacokinet. 33 2008 199 204
48. 10), a mitochondria-targeted antioxidant, in rat Asian J. Pharm. Sci. 5 2010 106 113
49. J.W. Jonker, J. Freeman, E. Bolscher, S. Musters, A.J. Alvi, I. Titley, A.H. Schinkel, and T.C. Dale Contribution of the ABC transporters Bcrp1 and Mdr1a/1b to the side population phenotype in mammary gland and bone marrow of mice Stem Cells 23 2005 1059 1065
50. L. Zhou, K. Schmidt, F.R. Nelson, V. Zelesky, M.D. Troutman, and B. Feng The effect of breast cancer resistance protein and P-glycoprotein on the brain penetration of flavopiridol, imatinib mesylate (Gleevec), prazosin, and 2-methoxy-3-(4-(2-(5-methyl-2-phenyloxazol-4-yl)ethoxy)phenyl)propanoic acid (PF-407288) in mice Drug Metab. Dispos. 37 2009 946 955
51. J. Asin-Cayuela, A.R. Manas, A.M. James, R.A.J. Smith, and M.P. Murphy Fine-tuning the hydrophobicity of a mitochondria-targeted antioxidant FEBS Lett. 571 2004 9 16
52. Y. Li, H. Zhang, J.P. Fawcett, and I.G. Tucker Quantitation and metabolism of mitoquinone, a mitochondria-targeted antioxidant, in rat by liquid chromatography/tandem mass spectrometry Rapid Commun. Mass Spectrom. 21 2007 1958 1964
53. J.M. Croop, M. Raymond, D. Haber, A. Devault, R.J. Arceci, P. Gros, and D.E. Housman The three mouse multidrug resistance (MDR) genes are expressed in a tissue-specific manner in normal mouse tissues Mol. Cell. Biochem. 9 1989 1346 1350
54. M. Huls, C.D.A. Brown, A.S. Windass, R. Sayer, J.J.M.W. van den Heuvel, S. Heemskerk, F.G.M. Russel, and R. Masereeuw The breast cancer resistance protein transporter ABCG2 is expressed in the human kidney proximal tubule apical membrane Kidney Int. 73 2008 220 225
55. A.H. Schinkel, E. Wagenaar, L. van Deemter, C.A.A.M. Mol, and P. Borst Absence of the Mdr1a P-glycoprotein in mice affects tissue distribution and pharmacokinetics of dexamethasone, digoxin, and Cyclosporin A J. Clin. Invest. 96 1995 1698 1705
56. D.S. Cox, K.R. Scott, H. Gao, and N.D. Eddington Effect of P-glycoprotein on the pharmacokinetics and tissue distribution of enaminone anticonvulsants: analysis by population and physiological approaches J. Pharmacol. Exp. Ther. 302 2002 1096 1104
57. A. Swed, S. Eyal, I. Madar, H. Zohar-Kontante, L. Weiss, and A. Hoffman The role of P-glycoprotein in intestinal transport versus the BBB transport of tetraphenylphosphonium Mol. Pharm. 6 2009 1883 1890