Drug delivery to mitochondria: The key to mitochondrial medicine

Advanced Drug Delivery Reviews

Volumn 41, Issue 2, 2000, Pages 235-250

  Murphy, Michael P ^a   Smith, Robin A J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Ageing; Antioxidants; Apoptosis; Diabetes; Lipophilic cations; Membrane potential; Neurodegenerative diseases; Obesity; Target peptide

Indexed keywords

CALCIUM; CELLS; CYTOLOGY; DISEASES; ESTERIFICATION; GENETIC ENGINEERING; MOLECULES; PHOSPHORIC ACID;

BIOACTIVE MOLECULES; DIABETES; DRUG DELIVERY; ISCHAEMIA REPERFUSION INJURY; MITOCHONDRIA; MITOCHONDRIAL RESPIRATORY CHAIN; NEURODEGENERATIVE DISEASES; OBESITY; OXIDATIVE PHOSPHORYLATION;

CONTROLLED DRUG DELIVERY;

ADENOSINE TRIPHOSPHATE; MITOCHONDRIAL DNA;

AGING; APOPTOSIS; DEGENERATIVE DISEASE; DIABETES MELLITUS; GENE THERAPY; HUMAN; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW;

EID: 0343986284     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-409X(99)00069-1     Document Type: Article

References (174)

1. Langer R. Drug delivery and targeting. Nature. 392:(suppl.):1998;5-10.
2. Murphy M.P. Targeting bioactive compounds to mitochondria. Trends Biotechnol. 15:1997;326-330.
3. Wallace D.C. Mitochondrial diseases in man and mouse. Science. 283:1999;1482-1488.
4. Saraste M. Oxidative phosphorylation at the fin de siecle. Science. 283:1999;1488-1493.
5. Nicholls D.G., Ferguson S.J. Bioenergetics 2. 1992;Academic Press, London.
6. Palmieri F., Bisaccia F., Capobianco L., Dolce V., Fiermonte G., Iacobazzi V., Indiveri C., Palmieri L. Mitochondrial metabolite transporters. Biochim. Biophys. Acta. 1275:1996;127-132.
7. Tyler D. The Mitochondrion in Health and Disease. 1992;VCH, New York.
8. Neupert W. Protein import into mitochondria. Annu. Rev. Biochem. 66:1997;863-917.
9. Schatz G. The protein import system of mitochondria. J. Biol. Chem. 271:1996;31763-31766.
10. Wallace D.C. Mitochondrial DNA variation in human evolution, degenerative disease and aging. Am. J. Hum. Genet. 57:1995;201-223.
11. Yaffe M.P. The machinery of mitochondrial inheritance and behavior. Science. 283:1999;1493-1497.
12. 2+ responses. Science. 280:1998;1763-1766.
13. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59:1979;527-605.
14. Beckman K.B., Ames B.N. The free radical theory of aging matures. Physiol. Rev. 78:1998;547-581.
15. Shigenaga M.K., Hagen T.M., Ames B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. USA. 91:1994;19771-19778.
16. Lenaz G. Role of mitochondria in oxidative stress and ageing. Biochim. Biophys. Acta. 1366:1998;53-67.
17. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA. 87:1990;1620-1624.
18. Murphy M.P., Packer M.A., Scarlett J.L., Martin S.W. Peroxynitrite: a biologically significant oxidant. Gen. Pharmacol. 31:1998;179-186.
19. Richter C., Park J.-W., Ames B.N. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc. Natl. Acad. Sci. USA. 85:1988;6465-6467.
20. Ames B.N., Shigenaga M.K., Hagen T.M. Mitochondrial decay in aging. Biochim. Biophys. Acta. 1271:1995;165-170.
21. Ames B.N., Shigenaga M.K., Hagen T.M. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. USA. 90:1993;7915-7922.
22. Reed D. Glutathione: toxicological implications. Annu. Rev. Pharmacol. Toxicol. 30:1990;603-631.
23. Sies H. Strategies of antioxidant defense. Eur. J. Biochem. 215:1993;213-219.
24. Li Y., Huang T.-T., Carlson E.J., Melov S., Ursell P.C., Olson J.L., Noble L.J., Yoshimura M.P., Berger C., Chan P.H., Wallace D.C., Epstein C.J. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11:1995;376-381.
25. Lebovitz R.M., Zhang H., Vogel H., Cartwright J., Dionne L., Lu N., Huang S., Matzuk M.M. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc. Natl. Acad. Sci. USA. 93:1996;9782-9787.
26. Reaume A.G., Elliott J.L., Hoffman E.K., Kowall N.W., Ferrante R.J., Siwek D.F., Wilcox H.M., Flood D.G., Beal M.F., Brown R.H., Scott R.W., Snider W.D. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 13:1996;43-47.
27. Zoratti M., Zabo I. The mitochondrial permeability transition. Biochim. Biophys. Acta. 1241:1995;139-176.
28. Halestrap A.P., Kerr P.M., Javadov S., Woodfield K.-Y. Elucidating the molecular mechanism of the permeability transition pore and its role in reperfusion injury. Biochim. Biophys. Acta. 1366:1998;79-94.
29. Lemasters J.J., Nieminen A.-L., Qian T., Trost L.C., Elmore S.P., Nishimura Y., Crowe R.A., Cascio W.E., Bradham C.A., Brenner D.A., Herman B. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta. 1366:1998;177-196.
30. Halestrap A.P., Woodfield K.-Y., Connern C.P. Oxidative stress, thiol reagents and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide carrier. J. Biol. Chem. 272:1997;3346-3354.
31. Kroemer G., Zamzami N., Susin S.A. Mitochondrial control of apoptosis. Immunol. Today. 18:1997;44-51.
32. Kroemer G., Petit P., Zamami N., Vayssiere J.-L., Mignotte B. The biochemistry of programmed cell death. FASEB J. 9:1995;1277-1287.
33. Lucas D.T., Szweda L.I. Cardiac reperfusion injury: aging, lipid peroxidation, and mitochondrial dysfunction. Proc. Natl. Acad. Sci. USA. 95:1998;510-514.
34. Sohol R.S., Weindruch R. Oxidative stress, caloric restriction and aging. Science. 273:1996;59-63.
35. Bernardi P.E. Mitochondria in cell death - special issue. Biochim. Biophys. Acta. 1366:1998;1-234.
36. Vaux D.L., Strasser A. The molecular biology of apoptosis. Proc. Natl. Acad. Sci. USA. 93:1996;2239-2244.
37. Kerr J.F.R., Wyllie A.H., Currie A.R. Apoptosis: A basic biological phenomenon with wide ranging implications in tissue kinetics. Br. J. Cancer. 26:1972;239-257.
38. Hale A.J., Smith C.A., Sutherland L.C., Stoneman V.E.A., Longthorne V.L., Culhane A.C., Williams G.T. Apoptosis: molecular regulation of cell death. Eur. J. Biochem. 236:1996;1-26.
39. Wyllie A.H., Kerr J.F.R., Currie A.R. Cell death: The significance of apoptosis. Int. Rev. Cytol. 68:1980;251-306.
40. Nicotera P., Bellomo G., Orrenius S. Calcium-mediated mechanisms in chemically induced cell death. Annu. Rev. Pharmacol. Toxicol. 32:1992;449-470.
41. Leist M., Nicotera P. Apoptosis, excitotoxicity, and neuropathology. Exp. Cell Res. 239:1998;183-201.
42. Leist M., Nicotera P. The shape of cell death. Biochem. Biophys. Res. Commun. 236:1997;1-9.
43. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
44. Kroemer G., Dallaporta B., Resche-Rignon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60:1998;619-642.
45. Salvesen G.S., Dixit V.M. Caspases: intracellular signalling by proteolysis. Cell. 91:1997;443-446.
46. Cohen G.M. Caspases: the executioners of apoptosis. Biochem. J. 326:1997;1-16.
47. Nicholson D.W., Thornberry N.A. Caspases: Killer proteases. Trends Biochem. Sci. 22:1997;299-306.
48. Yang J., Liu X., Bhalla K., Kim C.N., Ibrado A.M., Cai J., Peng T.-I., Jones D.P., Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 275:1997;1129-1132.
49. Kluck R.M., Martin S.J., Hoffman B.M., Zhou J.S., Green D.R., Newmeyer D.D. Cytochrome c activation of CPP32-like proteolysis plays a critical role in Xenopus cell-free apoptosis system. EMBO J. 16:1997;4639-4649.
50. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science. 275:1997;1132-1136.
51. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397:1999;441-446.
52. Li P., Nijhawan I., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/Caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:1997;479-489.
53. Zou H., Henzel W.J., Liu X., Lutschg A., Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in Cytochrome c-dependent activation of caspase-3. Cell. 90:1997;405-413.
54. L prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol. Cell. 3:1999;159-167.
55. L regulates the membrane potential and volume homeostasis of mitochondria. Cell. 91:1997;627-637.
56. Samali A., Cai J., Zhivotovsky B., Jones D.P., Orrenius S. Presence of a pre-apoptotic complex of pro-caspase-3, Hsp-60 and Hsp 10 in the mitochondrial fraction of Jurkat cells. EMBO J. 18:1999;2040-2048.
57. Reed J.C., Jurgensmeier J., Matsuyama S. Bcl-2 family proteins and mitochondria. Biochim. Biophys. Acta. 1366:1998;127-137.
58. Susin S.A., Zamzami N., Castedo M., Hirsch T., Marchetti P., Macho A., Daugas E., Geuskens M., Kroemer G. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184:1996;1-11.
59. Hockenberry E.A. Bcl-2, a novel regulator of cell death. BioEssays. 17:1995;631-638.
60. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:1998;481-490.
61. Marzo I., Brenner C., Zamzami N., Jurgensmeier J.M., Susin S.A., Vieira H.L.A., Prevost M.-C., Xie Z., Matsuyama S., Reed J.C., Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science. 281:1998;2027-2031.
62. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science. 284:1999;339-343.
63. Scarlett J.L., Murphy M.P. Release of apoptogenic proteins from the mitochondrial intermembrane space during the mitochondrial permeability transition. FEBS Lett. 418:1997;282-286.
64. Gunter T.E., Gunter K.K., Sheu S.-S., Gavin C.E. Mitochondrial calcium transport: physiology and pathological relevance. Am. J. Physiol. 267:1994;C313-C339.
65. Babcock D.F., Hille B. Mitochondrial oversight of cellular calcium signalling. Curr. Opin. Neurobiol. 8:1998;398-404.
66. Robb-Gaspers L.D., Rutter G.A., Burnett P., Hajnoczky G., Denton R.M., Thomas A.P. Coupling between cytosolic and mitochondrial calcium oscillations: role in the regulation of hepatic metabolism. Biochim. Biophys. Acta. 1366:1998;17-32.
67. Pozzan T., Rizzuto R., Volpe P., Meldolesi J. Molecular and cellular physiology of intracellular calcium stores. Physiol. Rev. 74:1994;595-636.
68. Guo Q., Christakos S., Robinson N., Mattson M.P. Calbindin D28K blocks the proapoptotic actions of mutant presenilin 1: reduced oxidative stress and preserved mitochondrial function. Proc. Natl. Acad. Sci. USA. 95:1998;3227-3232.
69. Ichas F., Mazat J.-P. From calcium signalling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim. Biophys. Acta. 1366:1998;33-50.
70. Jouaville L.S., Ichas F., Holmuhamedov E.L., Camacho P., Lechleiter J.D. Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature. 377:1995;438-441.
71. Ichas F., Jouaville L.S., Mazat J.-P. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell. 89:1997;1145-1153.
72. Wallace D.C. Diseases of the mitochondrial DNA. Annu. Rev. Biochem. 61:1992;1175-1212.
73. Wallace D.C. Mitochondrial genetics: A paradigm for aging and degenerative diseases? Science. 256:1992;628-632.
74. Wallace D.C. Mitochondrial DNA sequence variation in human evolution and disease. Proc. Natl. Acad. Sci. USA. 91:1994;8739-8746.
75. Nishino I., Spinazzola A., Hirano M. Thymidine phosphorylase gene mutations in MNGIE, a human mitochondrial disorder. Science. 283:1999;1.
76. Porteous W.K., James A.M., Sheard P.W., Porteous C.M., Packer M.A., Hyslop S.J., Melton J.V., Pang C.-Y., Wei Y.-H., Murphy M.P. Bioenergetic consequences of accumulating the common 4,977 bp mitochondrial DNA deletion. Eur. J. Biochem. 257:1998;192-201.
77. Hayashi J.I., Ohta S., Kiruchi A., Takemitsu M., Goto Y., Nonaka I. Introduction of disease related mitochondrial DNA deletions into Hela cells lacking mitochondrial DNA results in mitochondrial dysfunction. Proc. Natl. Acad. Sci. USA. 88:1991;10614-10618.
78. Holt I.J., Harding A.E., Cooper J.M., Schapira A.H.V., Toscano A., Clark J.B., Morgan-Hughes J.A. Mitochondrial myopathies: clinical and biochemical features of 30 patients with major deletions of muscle mitochondrial DNA. Ann. Neurol. 26:1989;699-708.
79. Wei Y.-H. Mitochondrial DNA alterations as ageing associated molecular events. Mutat. Res. 275:1992;145-155.
80. Corral-Debrinski M., Shoffner J.M., Lott M.T., Wallace D.C. Association of mitochondrial DNA damage with ageing and coronary atherosclerotic disease. Mutat. Res. 275:1992;169-180.
81. Pitkanen S., Robinson B.H. Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J. Clin. Invest. 98:1996;345-351.
82. Rotig A., de Lonlay P., Chretien D., Foury F., Koenig M., Sidi D., Munnich A., Rustin P. Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet. 17:1997;215-217.
83. Lutsenko S., Cooper M.J. Localization of the Wilson's disease protein product to mitochondria. Proc. Natl. Acad. Sci. USA. 95:1998;6004-6009.
84. Koehler C.M., Leuenberger D., Merchant S., Renold A., Junne T., Schatz G. Human deafness dystonia syndrome is a mitochondrial disease. Proc. Natl. Acad. Sci. USA. 96:1999;2141-2146.
85. Boss O., Muzzin P., Giacobino J.-P. The uncoupling proteins, a review. Eur. J. Endocrinol. 139:1998;1-9.
86. Skulachev V.P. Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Q. Rev. Biophys. 29:1996;169-202.
87. Enerback S., Jacobsson A., Simpson E.M., Guerra C., Yamashita H., Harper M.E., Kozak L.P. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature. 387:1997;90-94.
88. Solanes G., Vidal-Puig A., Grujic D., Flier J.S., Lowell B.B. The human uncoupling protein-3 gene. J. Biol. Chem. 272:1997;25433-25436.
89. Boss O., Samec S., Paolini-Giacobino A., Rossier C., Dulloo A., Seydoux J., Muzzin P., Giacobino J.-P. Uncoupling protein 3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett. 408:1997;39-42.
90. Mao W., Yu X.X., Zhong A., Wu L., Bruch J., Sherwood S.W., Adams S.H., Pan G. UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells. FEBS Lett. 443:1999;326-330.
91. Eto K., Tsubamoto Y., Terauchi Y., Sugiyama T., Kishimoto T., Takahashi N., Yamauchi N., Kobota N., Murayama S., Aizawa T., Akanuma Y., Aizawa S., Kasai H., Yazaki Y., Kadowaki T. Role of NADH shuttle system in glucose-induced activation of mitochondrial metabolism and insulin secretion. Nature. 283:1999;981-985.
92. Ghafourifar P., Richter C. Nitric oxide synthase activity in mitochondria. FEBS Lett. 418:1997;291-296.
93. Tatoyan A., Giulivi C. Purification and characterization of a nitric-oxide synthase from rat liver mitochondria. J. Biol. Chem. 273:1998;11044-11048.
94. Brown G.C. Nitric oxide regulates mitochondrial respiration and cell functions by inhibiting cytochrome oxidase. FEBS Lett. 369:1995;136-139.
95. Arnold S., Goglia F., Kadenbach B. 3,5-Diiodothyronine binds to subunit Va of cytochrome c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur. J. Biochem. 252:1998;325-330.
96. Heine U.I., Burmester J.K., Flanders K.C., Danielpour D., Munoz E.F., Roberts A.B., Sporn M.B. Localization of transforming growth factor-beta 1 in mitochondria of murine heart and liver. Cell. Regul. 2:1991;467-477.
97. Decaudin D., Marzo I., Brennner C., Kroemer G. Mitochondria in chemotherapy-indiced apoptosis: a prospective novel target of cancer therapy. Int. J. Oncol. 12:1998;141-152.
98. Murphy M.P. Slip and leak in mitochondrial oxidative phosphorylation. Biochim. Biophys. Acta. 977:1989;123-141.
99. Brand M.D. Measurement of mitochondrial protonmotive force. Brown G.C., Cooper C.E. Bioenergetics - A Practical Approach. 1995;39-62 IRL, Oxford.
100. Azzone G.F., Pietrobon D., Zoratti M. Determination of the proton electrochemical gradient across biological membranes. Curr. Top. Bioenerg. 13:1984;1-77.
101. Rottenberg H. The measurement of membrane potential and ΔpH in cells, organelles, and vesicles. Methods Enzymol. 55:1979;547-569.
102. Chen L.B. Mitochondrial membrane potential in living cells. Annu. Rev. Cell Biol. 4:1988;155-181.
103. Liberman E.A., Topali V.P., Tsofina L.M., Jasaitis A.A., Skulachev V.P. Mechanism of coupling of oxidative phosphorylation and the membrane potential of mitochondria. Nature. 222:1969;1076-1078.
104. Smith J.C. Potential-sensitive probes in membranes of bioenergetic relevance. Biochim. Biophys. Acta. 1016:1990;1-28.
105. Davey G.P., Tipton K.F., Murphy M.P. Uptake and accumulation of 1-methyl-4-phenylpyridinium by rat liver mitochondria measured using an ion-selective electrode. Biochem. J. 288:1992;439-443.
106. Tipton K.F., Singer T.P. Advances in our understanding of the mechanism of the neurotoxicity of MPTP and related compounds. J. Neurochem. 61:1993;1191-1206.
107. Berry M.N., Edwards A.M., Barrit G.J., Grivell M.B., Halls H.J., Gannon B.J., Friend D.S. Isolated hepatocytes preparation, properties and applications. Burdon R.H., van Knippenberg P.H. Laboratory Techniques in Biochemistry and Molecular Biology. 1991;386-390 Elsevier, Amsterdam.
108. Burns R.J., Murphy M.P. Labeling of mitochondrial proteins in living cells by the thiol probe thiobutyltriphenylphosphonium bromide. Arch. Biochem. Biophys. 339:1997;33-39.
109. Rideout D.C., Calogeropoulou T., Jaworski J.S., Dagnino R., McCarthy M.R. Phosphonium salts exhibiting selective anti-carcinoma activity in vitro. Anti-Cancer Drug Design. 4:1989;265-280.
110. Nocentini S., Moreno G., Petit P.X., Guggiari M., Salet C., Demerseman P., Dodin G. Induction of mitochondrial dysfunction and apoptosis in HeLa cells by bis-pyridinium oximes, a newly synthesised family of lipophilic biscations. Biochem. Pharmacol. 53:1997;1543-1552.
111. Morgan J., Whitaker J.E., Oseroff A.R. GRP78 induction by calcium ionophore potentiates photodynamic therapy using the mitochondrial targeting dye victoria blue BO. Photochem. Photobiol. 67:1998;155-164.
112. Teicher B.A., Holden S.A., Cathcart K.N.S. Efficacy of Pt(Rh-123)2 as a radiosensitizer with fractionated X rays. Int. J. Radiat. Oncol. Biol. Phys. 13:1987;1217-1224.
113. Manetta G., Nasseeri A., Podnos Y.D., Emma D., Dorion G., Rawlings L., Carpenter P.M., Bustamante A., Patel J., Rideout D. Novel phosphonium salts display in vitro and in vivo cytotoxic activity against human ovarian cancer cell lines. Gynacol. Oncol. 60:1996;203-212.
114. 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. 14:1994;21-28.
115. Rideout D., Bustamante A., Patel J. Mechanism of inhibition of FaDu hypopharyngeal carcinoma cell growth by tetraphenylphosphnium chloride. Int. J. Cancer. 57:1994;247-253.
116. Rideout D. Self assembling drugs: a new approach to biochemical modulation in cancer chemotherapy. Cancer Invest. 12:1994;189-202.
117. 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. 322:1995;60-68.
118. Smith R.A.J., Porteous C.M., Coulter C.V., Murphy M.P. Selective targeting of an antioxidant to mitochondria. Eur. J. Biochem. 263:1999;709-716.
119. Matthews R.T., Yang L., Browne S., Bail M., Beal M.F. Coenzyme Q10 administration increases brain mitochondrial concentrations and exerts neurprotective effects. Proc. Natl. Acad. Sci. USA. 95:1998;8892-8897.
120. Miquel J., Ferraniz M.L., De Juan E., Sevilla I., Martinez M. N-acetylcysteine protects against age-related decline of oxidative phosphorylation in liver mitochondria. Eur. J. Pharmacol. 292:1995;333-335.
121. Sokol R.J., McKim J.M., Goff M.C., Ruyle S.Z., Devereaux M.W., Han D., Packer L., Everson G. Vitamin E reduces oxidant injury to mitochondria and the hepatoxicity of taurochenodeoxycholic acid in the rat. Gastroenterology. 114:1998;164-174.
122. Melov S., Schneider J.A., Day B.J., Hinerfeld D., Coskun P., Mira S.S., Crapo J.D., Wallace D.C. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat. Genet. 18:1998;159-163.
123. Kauppinen R. Proton electrochemical potential of the inner mitochondrial membrane in isolated perfused rat hearts, as measured by exogenous probes. Biochim. Biophys. Acta. 725:1983;131-137.
124. 11C-triphenylmethylphosphonium for the evaluation of membrane potential in the heart by positron-emission tomography. Eur. J. Nucl. Med. 11:1986;478-483.
125. Wan B., Doumen C., Duszynski J., Salama G., LaNoue K.F. A method of determining electrical potential gradient across mitochondrial membrane in perfused rat hearts. Am. J. Physiol. 265:1993;H445-H452.
126. Steen H., Maring J.G., Meijer D.K. Differential effects of metabolic inhibitors on cellular and mitochondrial uptake of organic cations in rat liver. Biochem. Pharmacol. 45:1993;809-818.
127. Evans D., Smith J.C. Seizure activity and cortical spreading depression monitored by an extrinsic potential-sensitive molecular probe. Brain Res. 409:1987;350-357.
128. Srivastava P.C., Hay H.G., Knapp F.F. Effects of alkyl and aryl substitution on the myocardial specificity of radioiodinated phosphonium, arsonium, and ammonium cations. J. Med. Chem. 28:1985;901-904.
129. Lampidis T.J., Shi Y.F., Calderon C.L., Kolonias D., Tapiero H., Savaraj N. Accumulation of simple organic cations correlates with differential cytotoxicity in multidrug-resistant and -sensitive human and rodent cells. Leukemia. 11:1997;1156-1159.
130. Gottesman M.M., Pastan I. Biochemistry of the multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62:1993;385-427.
131. Pfanner N., Craig E.A., Honlinger A. Mitochondrial preprotein translocase. Annu. Rev. Cell Cell. Biol. 13:1997;25-51.
132. Pfanner N., Craig E.A., Meijer M. The protein import machinery of the mitochondrial inner membrane. Trends Biochem. Sci. 19:1994;368-372.
133. Hurt E.C., Pesold-Hurt B., Suda K., Oppliger W., Schatz G. The first 12 amino acids (less than half of the presequence) can direct mouse cytosolic dihydrofolate reductase in to the yeast mitochondrial matrix. EMBO J. 4:1985;2061-2068.
134. Hurt E.C., Pesold-Hurt B., Schatz G. The cleavable prepiece of an imported mitochondrial protein is sufficient to direct cytosolic dihydrofolate reductase into the mitochondrial matrix. FEBS Lett. 178:1984;306-310.
135. Horwich A.L., Kalousek F., Mellman I., Rosenberg L.E. A leader peptide is sufficient to direct mitochondrial import of a chimeric protein. EMBO J. 4:1985;1129-1135.
136. Rizzuto R., Simpson A.W.M., Brini M., Pozzan T. Rapid changes of mitochondrial Ca revealed by specifically targeted recombinant aequorin. Nature. 358:1992;325-327.
137. Rizzuto R., Brini M., De Giorgi F., Rossi R., Heim R., Tsien R.Y., Pozzan T. Double labeling of subcellular structures with organelle-targeted GFP mutants in vivo. Curr. Biol. 6:1996;183-188.
138. Vestweber D., Schatz G. Mitochondria can import artificial precursor proteins containing a branched polypeptide chain or a carboxy-terminal stilbene derivative. J. Cell Biol. 107:1988;2045-2049.
139. Vestweber D., Schatz G. DNA-protein conjugates can enter mitochondria via the protein import pathway. Nature. 338:1989;170-172.
140. Seibel P.E.A., Trappe J., Villani G., Klopstock T., Papa S., Reichmann H. Transfection of mitochondria: strategy towards a gene therapy of mitchondrial DNA diseases. Nucleic Acids Res. 23:1995;10-17.
141. Mueller G.M., McKenzie L.R., Homaniacs G.E., Watkins S.C., Robbins P.D., Paul H.S. Complementation of defective leucine decaroboxylation in fibroblasts from a maple syrup urine disease patient by retrovirus-mediated gene transfer. Gene Ther. 2:1995;461-468.
142. Palu G., Bonaguro R., Marcello A. In pursuit of new developments for gene therapy of human diseases. J. Biotechnol. 68:1999;1-13.
143. Chrzanowska-Lightowlers Z.M.A., Lightowlers R.N., Turnbull D.M. Gene therapy for mitochondrial DNA defects: is it possible? Gene Ther. 2:1995;311-316.
144. Taylor R.W., Chinnery P.F., Clark K.M., Lightowlers R.N., Turnbull D.M. Treatment of mitochondrial disease. J. Bioenerg. Biomembr. 29:1997;195-205.
145. Collombet J.M., Coutelle C. Towards gene therapy of mitochondrial dissorders. Mol. Med. Today. 4:1998;31-38.
146. Butow R.A., Fox T.D. Organelle transformation: shoot first, ask questions later. Trends Biochem. Sci. 15:1990;465-468.
147. King M.P., Attardi G. Injection of mitochondria into human cells leads to a rapid replacement of the endogenous mitochondrial DNA. Cell. 52:1988;811-819.
148. King M.P., Attardi G. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science. 246:1989;500-503.
149. Schneider A. Import of RNA into mitochondria. Trends Cell. Biol. 4:1994;282-286.
150. Chang D.D., Clayton D.A. Mouse RNAase MRP RNA is encoded by a nuclear gene and contains a decamer sequence complementary to a conserved region of mitochondrial RNA substrate. Cell. 56:1989;131-139.
151. Nagley P., Farrell L.B., Gearing D.P., Nero D., Meltzer G., Devenish R.J. Assembly of functional proton-translocating ATPase complex in yeast mitochondria with cytoplasmically synthesised subunit 8, a polypeptide normally encoded by the organelle. Proc. Natl. Acad. Sci. USA. 85:1988;2091-2095.
152. Taylor R.W., Chinnery P.F., Turnbull D.M., Lightowlers R.N. Selective inhibition of mutant human mitochondrial DNA replication in vitro by peptide nucleotide acids. Nat. Genet. 15:1997;212-215.
153. Buchardt O., Egholm M., Berg R.H., Nielsen P.E. Peptide nucleic acids and their potential applications in biotechnology. Trends Biotechnol. 11:1993;384-386.
154. Walker J.E. The NADH:Ubiquinone oxidoreductase (Complex I) of respiratory chains. Q. Rev. Biophys. 25:1992;253-321.
155. Seo B.B., Kitajima-Ihara T., Chan E.K., Scheffler I.E., Matsuno-Yagi A., Yagi T. Molecular remedy of Complex I defects: rotenone insensitive internal NADH-quinone oxidreductase of Saccharomyces cerevisiae mitochondria restores the NADH oxidase activity of complex-1 deficient mammalian cells. Proc. Natl. Acad. Sci. USA. 95:1998;167-171.
156. Wispe J.R., Warner B.B., Clark J.C., Dey C.R., Neumann J., Glasser S.W., Crapo J.D., Chang L.Y., Whitsett J.A. Human Mn-superoxide dismutase in pulmonary epithelial cells of transgenic mice confers protection from oxygen injury. J. Biol. Chem. 267:1992;23937-23941.
157. Zwacka R.A., Zhou W., Zhand Y., Darby C.J., Dudus L., Halldorson J., Oberly L., Engelhardt J.F. Redox gene therapy for ischemia/reperfusion injury of the liver reduces AP-1 and NF-KB activation. Nat. Med. 4:1998;698-704.
158. Zhang C., Sriratana A., Miniamikawa T., Nagley P. Photosensitisation properties of mitochondrially targeted green fluorescent protein. Biochem. Biophys. Res. Commun. 242:1998;390-395.
159. Wheeler V.C., Prodromou C., Pearl L.H., Williamson R., Coutelle C. Synthesis of a modified gene encoding human ornithine transcarbamoylase for expression in mammalian mitochondrial translation systems: a novel approach towards correction of a genetic defect. Gene. 169:1996;251-255.
160. Collombet J.M., Coutelle C. Towards a gene therapy of mitochondrial disorders. Mol. Med. Today. 4:1998;31-38.
161. Daum G. Lipids of mitochondria. Biochim. Biophys. Acta. 822:1985;1-42.
162. Maftah A., Petit J.M., Julien R. Specific interaction of the new fluorescent dye 10-N-nonyl acridine orange with inner mitochondrial membrane. A lipid-mediated inhibition of oxidative phosphorylation. FEBS Lett. 260:1990;236-240.
163. Verma A., Facchina S.L., Hirsch D.J., Song S.-Y., Dillahey L.F., Williams J.R., Snyder S.H. Photodynamic tumor therapy: mitochondrial benzodiazapine receptors as a therapeutic target. Mol. Med. 4:1998;40-45.
164. Derossi D., Chassaing G. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell. Biol. 8:1998;84-87.
165. Rojas M., Donahue J.P., Tan Z., Lin Y.-Z. Genetic engineering of proteins with cell membrane permeability. Nat. Biotechnol. 16:1998;370-375.
166. Phelan A., Elliott G., O'Hare P. Intercellular delivery of functional p53 by the herpesvirus protein VP22. Nat. Biotechnol. 16:1998;440-443.
167. Pooga M., Soomets U., Hallbrink M., Valkna A., Saar K., Rezaei K., Kahl U., Hao J.-X., Xu X.-J., Wiesnfeld-Hallin Z., Hokfelt T., Bartfai T., Langel U. Cell penetrating PNA constructs regulate galanin receptor levels and modify pain transmission in vivo. Nat. Biotechnol. 16:1998;857-861.
168. Hawiger J. Noninvasive intracellular delivery of functional peptides and proteins. Curr. Opin. Chem. Biol. 3:1998;89-94.
169. Melov S., Coskun P., Patel M., Tuinstra R., Cottrell B., Jun A.S., Zastawny T.H., Dizdaroglu M., Goodman S.I., Huang T.T., Miziorko H., Epstein C.J., Wallace D.C. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc. Natl. Acad. Sci. USA. 96:1999;846-851.
170. Williams M.D., Van Remmen H., Conrad C.G., Huang T.-T., Epstein C.J., Richardson A. Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J. Biol. Chem. 273:1998;28510-28515.
171. Price D.L., Sisodia S.S., Borchelt D.R. Genetic neurodegenerative diseases: the human illness and transgenic models. Science. 282:1998;1079-1083.
172. Odagiri Y., Uchida H., Hosokawa M., Takemoto K., Morley A.A., Takeda T. Accelerated accumulation of somatic mutations in the senesence accelerated mouse. Nat. Genet. 19:1998;116-117.
173. Esposito L.A., Melov S., Panov A., Cottrell B.A., Wallace D.C. Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl. Acad. Sci. USA. 96:1999;4820-4825.
174. Graham B.H., Waymire K.G., Cottrell B., Trounce I.A., MacGregor G.R., Wallace D.C. A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nat. Genet. 16:1997;226-234.