Therapeutic role of coenzyme Q10 in Parkinson's disease

Pharmacology and Therapeutics

Volumn 107, Issue 1, 2005, Pages 120-130

  Shults, Clifford W ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Coenzyme Q10; Mitochondria; Neuroprotection; Parkinson's disease

Indexed keywords

ALPHA TOCOPHEROL; DOPAMINE RECEPTOR STIMULATING AGENT; LEVODOPA; REMACEMIDE; SELEGILINE; UBIDECARENONE;

APOPTOSIS; BIOENERGY; BRAIN MITOCHONDRION; CLINICAL TRIAL; DOPAMINERGIC SYSTEM; DRUG BLOOD LEVEL; ELECTRON TRANSPORT; HUMAN; NEUROPATHOLOGY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SIDE EFFECT; URINALYSIS;

ANIMALS; APOPTOSIS; CLINICAL TRIALS; ENERGY METABOLISM; HUMANS; MITOCHONDRIA; OXIDATIVE STRESS; PARKINSON DISEASE; UBIQUINONE;

EID: 20444365828     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2005.02.002     Document Type: Review

References (108)

1. Y. Akaneya, M. Takahashi, and H. Hatanaka Involvement of free radicals in MPP+ neurotoxicity against rat dopaminergic neurons in culture Neurosci Lett 193 1 1995 53 56
2. Z.I. Alam, S.E. Daniel, A.J. Lees, D.C. Marsden, P. Jenner, and B. Halliwell A generalised increase in protein carbonyls in the brain in Parkinson's but not incidental Lewy body disease J Neurochem 69 3 1997 1326 1329
3. Z.I. Alam, A. Jenner, S.E. Daniel, A.J. Lees, N. Cairns, and C.D. Marsden Oxidative DNA damage in the parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra J Neurochem 69 3 1997 1196 1203
4. J.K. Andersen Does neuronal loss in Parkinson's disease involve programmed cell death? Bioessays 23 7 2001 640 646
5. J.J. Anderson, D. Bravi, R. Ferrari, T.L. Davis, F. Baronti, and T.N. Chase No evidence for altered muscle mitochondrial function in Parkinson's disease J Neurol Neurosurg Psychiatry 5 5 1993 477 480
6. D. Arsenijevic, H. Onuma, C. Pecqueur, S. Raimbault, B.S. Manning, and B. Miroux Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production Nat Genet 26 4 2000 435 439
7. N. Barroso, Y. Campos, R. Huertas, J. Esteban, J.A. Molina, and A. Alonso Respiratory chain enzyme activities in lymphocytes from untreated patients with Parkinson disease Clin Chem 39 4 1993 667 669
8. M. Battino, A. Gorini, R.F. Villa, M.L. Genova, C. Bovina, and S. Sassi Coenzyme Q content in synaptic and non-synaptic mitochondria from different brain regions in the ageing rat. Mech Ageing Dev 78 3 1995 173 187
9. M.F. Beal Neurochemistry and toxin models in Huntington's disease Curr Opin Neurol 7 6 1994 542 547
10. 10 attenuates the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP) induced loss of striatal dopamine and dopaminergic axons in aged mice Brain Res 783 1998 109 114
11. R. Benecke, P. Strümper, and H. Weiss Electron transfer complexes I and IV of platelets are abnormal in Parkinson's disease but normal in Parkinson-plus syndromes Brain 116 1993 1451 1463
12. L.A. Bindoff, M.A. Birch-Machin, N.E. Cartlidge, W.D. Parker Jr., and D.M. Turnbull Respiratory chain abnormalities in skeletal muscle from patients with Parkinson's disease J Neurol Sci 104 2 1991 203 208
13. O. Blin, C. Desnuelle, O. Rascol, M. Borg, H. Peyro Saint Paul, and J.P. Azulay Mitochondrial respiratory failure in skeletal muscle from patients with Parkinson's disease and multiple system atrophy J Neurol Sci 125 1 1994 95 101
14. C. Bogentoft, P.O. Edelund, B. Olsson, L. Widlund, and K. Westensen Biopharmaceutical aspects of intravenous and oral administration of coenzyme Q10 Q.K. Folkers G.P. Littarru T. Yamagami Biomedical and Clinical Aspects of Coenzyme 1991 Elsevier Science Publishers Amsterdam 215 224
15. F. Cardellach, M.J. Marti, J. Fernandez-Sola, C. Marin, J.B. Hoek, and E. Tolosa Mitochondrial respiratory chain activity in skeletal muscle from patients with Parkinson's disease Neurology 43 11 1993 2258 2262
16. F.L. Crane Biochemical functions of coenzyme Q10 J Am Coll Nutr 20 6 2001 591 598
17. I. Dalle-Donne, D. Giustarini, R. Colombo, R. Rossi, and A. Milzani Protein carbonylation in human diseases Trends Mol Med 9 4 2003 169 176
18. M. Degali Esposti Inhibitors of NADH-ubiquinone reductase: an overview Biochim Biophys Acta 1364 2 1998 222 235
19. D.T. Dexter, C.J. Carter, F.R. Wells, F. Javoy-Agid, Y. Agid, and A. Lees Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease J Neurochem 52 2 1989 381 389
20. D.T. Dexter, A.E. Holley, W.D. Flitter, T.F. Slater, F.R. Wells, and S.E. Daniel Increased levels of lipid hydroperoxides in the parkinsonian substantia nigra: an HPLC and ESR study Mov Disord 9 1 1994 92 97 (Erratum in: Mov Disord 9(3), 380)
21. S. DiDonato, M. Zeviani, P. Giovannini, N. Savarese, M. Rimoldi, and C. Mariotti Respiratory chain and mitochondrial DNA in muscle and brain in Parkinson's disease patients Neurology 43 11 1993 2262 2268
22. K.S. Echtay, E. Winkler, and M. Klingenberg Coenzyme Q is an obligatory cofactor for uncoupling protein function Nature 408 6812 2000 609 613
23. K.S. Echtay, E. Winkler, K. Frischmuth, and M. Klingenberg Uncoupling proteins 2 and 3 are highly active H(+) transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone) Proc Natl Acad Sci U S A 98 4 2001 1416 1421
24. K.S. Echtay, D. Roussel, J. St-Pierre, M.B. Jekabsons, S. Cadenas, and J. Stuart Superoxide activates mitochondrial uncoupling proteins Nature 415 6867 2002 96 99
25. C. Edlund, M. Söderberg, K. Kristensson, and G. Dallner Ubiquinone, dolichol, and cholesterol metabolism in aging and Alzheimer's disease Biochem Cell Biol 70 6 1992 422 428
26. B.I. Giasson, J.E. Duda, I.V. Murray, Q. Chen, J.M. Souza, and H.I. Hurtig Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions Science 290 5493 2000 985 989
27. G. Gille, S.T. Hung, H. Reichmann, and W.D. Rausch Oxidative stress to dopaminergic neurons as models of Parkinson's disease Ann N Y Acad Sci 1018 2004 533 540
28. C.G. Goetz, S. Leurgans, R. Raman Parkinson Study Group Placebo-associated improvements in motor function: comparison of subjective and objective sections of the UPDRS in early Parkinson's disease Mov Disord 17 2 2002 283 288
29. M.J. Goldenthal, and J. Marín-García Mitochondrial signaling pathways: a receiver/integrator organelle Mol Cell Biochem 262 2004 1 16
30. D.R. Green, and G. Kroemer The pathophysiology of mitochondrial cell death Science 305 5684 2004 626 629
31. J.T. Greenamyre, T.B. Sherer, R. Betarbet, and A.V. Panov Complex I and Parkinson's disease IUBMB Life 52 3-5 2001 135 141
32. M. Gu, J.M. Cooper, J.W. Taanman, and A.H. Schapira Mitochondrial DNA transmission of the mitochondrial defect in Parkinson's disease Ann Neurol 44 2 1998 177 186
33. R. Haas, F. Nasirian, K. Nakano, D. Ward, M. Pay, and R. Hill Low platelet mitochondrial Complex I and Complex II/III activity in early untreated Parkinson's disease Ann Neurol 37 1995 714 722
34. B. Halliwell Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment Drugs Aging 18 9 2001 685 716
35. R.E. Heikkila, F.S. Cabbat, L. Manzino, and R.C. Duvoisin Effects of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine on neostriatal dopamine in mice Neuropharmacology 23 6 1984 711 713
36. M.W. Horstink, and B.G. van Engelen The effect of coenzyme Q10 therapy in Parkinson disease could be symptomatic Arch Neurol 60 8 2003 1170 1172
37. T.L. Horvath, S. Diano, C. Leranth, L.M. Garcia-Segura, M.A. Cowley, and M. Shanabrough Coenzyme Q induces nigral mitochondrial uncoupling and prevents dopamine cell loss in a primate model of Parkinson's disease Endocrinology 144 7 2003 2757 2760
38. H. Ischiropoulos, and J.S. Beckman Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J Clin Invest 11 2 2003 163 169
39. N. Ishii, N. Senoo-Matsuda, K. Miyake, K. Yasuda, T. Ishii, and P.S. Hartman Coenzyme Q10 can prolong C. elegans lifespan by lowering oxidative stress Mech Ageing Dev 125 1 2004 41 46
40. M.D. Jacobson, J.F. Burne, M.P. King, T. Miyashita, J.C. Reed, and M.C. Raff Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA Nature 361 1993 365 369
41. B. Janetzky, S. Hauck, M.B.H. Youdim, P. Riederer, K. Jellinger, and F. Pantucek Unaltered aconitase activity, but decreased complex I activity in substantia nigra pars compacta of patients with Parkinson's disease Neurosci Lett 169 1994 126 128
42. P. Jenner Oxidative stress in Parkinson's disease Ann Neurol 53 3 2003 S26 S361 (discussion S36-8)
43. F.J. Jiménez-Jiménez, J.A. Molina, F. de Bustos, A. García-Redondo, C. Gómez-Escalonilla, and A. Martínez-Salio Serum levels of coenzyme Q10 in patients with Parkinson's disease J Neural Transm 107 2 2000 177 181
44. A. Kikuchi, A. Takeda, H. Onodera, T. Kimpara, K. Hisanaga, and N. Sato Systemic increase of oxidative nucleic acid damage in Parkinson's disease and multiple system atrophy Neurobiol Dis 9 2 2002 244 248
45. A.E. Kingsbury, C.D. Mardsen, and O.J. Foster DNA fragmentation in human substantia nigra: apoptosis or perimortem effect? Mov Disord 13 6 1998 877 884
46. D. Krige, M.T. Carroll, J.M. Cooper, C.D. Marsden, and A.H.V. Schapira Platelet mitochondrial function in Parkinson's disease Ann Neurol 32 1992 782 788
47. G. Kroemer Mitochondrial control of apoptosis: an introduction Biochem Biophys Res Commun 304 3 2003 433 435
48. J.W. Langston, P. Ballard, J.W. Tetrud, and I. Irwin Chronic parkinsonism in humans due to a produce of meperidine-analog synthesis Science 219 1983 979 980
49. J.W. Langston, L.S. Forno, C.S. Rebert, and I. Irwin Selective nigral toxicity after systemic administration of 1-methyl-4-phenyl-1,2,5,6- tetrahydropyrine (MPTP) in the squirrel monkey Brain Res 292 2 1984 390 394
50. P.L. Larsen, and C.F. Clarke Extension of life-span in Caenorhabditis elegans by a diet lacking coenzyme Q Science 295 5552 2002 120 123
51. A. Lass, and R.S. Sohal Electron transport-linked ubiquinone-dependent recycling of α-tocopherol inhibits autooxidation of mitochondrial membranes Arch Biochem Biophys 352 1998 229 236
52. A. Lass, L. Kwong, and R.S. Sohal Mitochondrial coenzyme Q content and aging Biofactors 9 2-4 1999 199 205
53. M. Le Bras, M.V. Clement, S. Pervaiz, and C. Brenner Reactive oxygen species and the mitochondrial signaling pathway of cell death Histol Histopathol 20 1 2005 205 219
54. K. Lönnrot, P. Holm, A. Lagerstedt, H. Huhtala, and H. Alho The effects of lifelong ubiquinone Q10 supplementation on the Q9 and Q10 tissue concentrations and life span of male rats and mice Biochem Mol Biol Int 44 4 1998 727 737
55. P.W. Lucker, N. Wetselsberger, G. Hennings, and D. Rehn Pharmacokinetics of coenzyme ubidecarenone in healthy volunteers Q.K. Folkers G.P. Littarru T. Yamagami Biomedical and Clinical Aspects of Coenzyme 1984 Elsevier Science Publishers Amsterdam 143 151
56. J.D. Ly, D. Grubb, and R. Lawen The mitochondrial membrane potential (ΔΨm) in apoptosis; an update Apoptosis 8 2003 115 128
57. M. Madesh, and G. Hajnoczky VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release J Cell Biol 155 6 2001 1003 1015
58. M.A. Martin, J.A. Molina, F.J. Jimenez-Jimenez, J. Benito-Leon, M. Orti-Pareja, and Y. Campos Respiratory-chain enzyme activities in isolated mitochondria of lymphocytes from untreated Parkinson's disease patients. Grupo-Centro de Trastornos del Movimiento Neurology 46 5 1996 1343 1346
59. T. Matsubara, T. Azuma, S. Yoshida, and T. Yamagami Serum coenzyme Q-10 level in Parkinson syndrome K. Folkers P. Littarru T. Yamagami Biomedical and Clinical Aspects of Coenzyme Q 1991 Elsevier Science Publishers BV Amsterdam 159 166
60. R.T. Matthews, L. Yang, S. Browne, M. Baik, and M.F. Beal Coenzyme Q10 administration increases brain mitochondrial concentrations and exerts neuroprotective effects Proc Natl Acad Sci U S A 95 15 1998 8892 8897
61. G. Mattiasson, M. Shamloo, G. Gido, K. Mathi, G. Tomasevic, and S. Yi Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma Nat Med 9 8 2003 1062 1068
62. M.P. Mattson, and G. Kroemer Mitochondria in cell death: novel targets for neuroprotection and cardioprotection Trends Mol Med 9 5 2003 196 205
63. T. Menke, G. Gille, F. Reber, B. Janetzky, W. Andler, and R.H. Funk Coenzyme Q10 reduces the toxicity of rotenone in neuronal cultures by preserving the mitochondrial membrane potential Biofactors 18 1-4 2003 65 72
64. D. Mohr, V.W. Bowry, and R. Stocker Dietary supplementation with coenzyme Q10 results in increased levels of ubiquinol-10 within circulating lipoproteins and increased resistance of human low-density lipoprotein to the initiation of lipid peroxidation Biochim Biophys Acta 1126 1992 247 254
65. J.A. Molina, F. de Bustos, S. Ortiz, T. Del Ser, M. Seijo, and J. Benito-Léon Serum levels of coenzyme Q in patients with Lewy body disease J Neural Transm 109 9 2002 1195 1201
66. T. Müller, T. Büttner, A.F. Gholipour, and W. Kuhn Coenzyme Q10 supplementation provides mild symptomatic benefit in patients with Parkinson's disease Neurosci Lett 341 3 2003 201 204
67. Y. Nakagawa-Hattori, H. Yoshino, T. Kondo, Y. Mizuno, and S. Horai Is Parkinson's disease a mitochondrial disorder? J Neurol Sci 107 1 1992 29 33
68. P. Navas, D.M. Fernandez-Ayala, S.F. Martin, G. Lopez-Lluch, R. De Caboa, and J.C. Rodriguez-Aguilera Ceramide-dependent caspase 3 activation is prevented by coenzyme Q from plasma membrane in serum-deprived cells Free Radic Res 36 4 2002 369 374
69. A. Nègre-Salvayre, C. Hirtz, G. Carrera, R. Cazenave, M. Troly, and R. Salvayre A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation FASEB J 11 10 1997 809 815
70. D. Nijhawan, N. Honarpour, and X. Wang Apoptosis in neural development and disease Ann Rev Neurosci 23 2000 73 87
71. H. Noack, U. Kube, and W. Augustin Relations between tocopherol depletion and coenzyme Q during lipid peroxidation in rat liver mitochondria Free Radic Res 20 6 1994 375 386
72. T. Okamoto, T. Matusuya, Y. Fukunaga, T. Kishi, and T. Yamagami Human serum ubiquinol-10 levels and relationship to serum lipids Int J Vitam Nutr Res 59 1989 288 292
73. L. Papucci, N. Schiavone, E. Witort, M. Donnini, A. Lapucci, and A. Tempestini Coenzyme q10 prevents apoptosis by inhibiting mitochondrial depolarization independently of its free radical scavenging property J Biol Chem 278 30 2003 28220 28228
74. E. Paradis, S. Clavel, F. Bouillaud, D. Ricquier, and D. Richard Uncoupling protein 2: a novel player in neuroprotection Trends Mol Med 9 12 2003 522 525
75. W.D. Parker Jr., S.J. Boyson, and J.K. Parks Abnormalities of the electron transport chain in idiopathic Parkinson's disease Ann Neurol 26 1989 719 723
76. W.D. Parker Jr., and J.K. Parks Mitochondrial ND5 mutations in idiopathic Parkinson's disease Biochem Biophys Res Commun 326 3 2005 667 669
77. Parkinson Study Group Effects of tocopherol and deprenyl on the progression of disability in early Parkinson's disease New Engl J Med 328 1993 176 183
78. S. Przedborski, V. Jackson-Lewis, R. Djaldetti, G. Liberatore, M. Vila, and S. Vukosavic The parkinsonian toxin MPTP: action and mechanism Restor Neurol Neurosci 16 2 2000 135 142
79. J.C. Reed Apoptosis-based therapies Nat Rev Drug Discov 1 2002 111 121
80. J.R. Sanchez-Ramos, E. Overvil, and B.N. Ames A marker of oxyradical-mediated DNA damage (8-hydroxy-2′ deoxyguanosine) is increased in nigro-striatum of Parkinson's disease brain Neurodegeneration 3 1994 197 204
81. J.K. Sandhu, S. Pandey, M. Ribecco-Lutkiewicz, R. Monette, H. Borowy-Borowski, and P.R. Walker Molecular mechanisms of glutamate neurotoxicity in mixed cultures of NT2-derived neurons and astrocytes: protective effects of coenzyme Q10 J Neurosci Res 72 6 2003 691 703
82. A.H. Schapira, J.M. Cooper, D. Dexter, P. Jenner, J.B. Clark, and C.D. Marsden Mitochondrial complex I deficiency in Parkinson's disease Lancet 1 8649 1989 1269
83. A.H. Schapira, V.M. Mann, J.M. Cooper, D. Dexter, S.E. Daniel, and P. Jenner Anatomic and disease specificity of NADH CoQ1 reductase complex I deficiency in parkinson's disease J Neurochem 55 1990 2142 2145
84. J.B. Schulz, D.R. Henshaw, R.T. Matthews, and M.F. Beal Coenzyme Q10 and nicotinamide and a free radical spin trap protect against MPTP neurotoxicity Exp Neurol 132 2 1995 279 283
85. S. Shavali, E.C. Carlson, J.C. Swinscoe, and M. Ebadi 1-Benzyl-1,2,3,4-tetrahydroisoquinoline, a Parkinsonism-inducing endogenous toxin, increases alpha-synuclein expression and causes nuclear damage in human dopaminergic cells J Neurosci Res 76 4 2004 563 571
86. T.B. Sherer, R. Betarbet, C.M. Testa, B.B. Seo, J.R. Richardson, and J.H. Kim Mechanism of toxicity in rotenone models of Parkinson's disease J Neurosci 23 34 2003 10756 10764
87. J.M. Shoffner, R.L. Watts, J.L. Juncos, A. Torroni, and D.C. Wallace Mitochondrial oxidative phosphorylation defects in Parkinson's disease Ann Neurol 30 3 1991 332 339
88. C.W. Shults, F. Nasirian, D.M. Ward, K. Nakano, M. Pay, and L.R. Hill Carbidopa/levodopa and selegiline do not affect platelet mitochondrial function in early parkinsonism Neurology 45 1995 344 348
89. C.W. Shults, R.H. Haas, D. Passov, and M.F. Beal Coenzyme Q10 levels correlate with the activities of complexes I and II/III in mitochondria from parkinsonian and nonparkinsonian subjects Ann Neurol 42 1997 261 264
90. C.W. Shults, M.F. Beal, D. Fontaine, K. Nakano, and R.H. Haas Absorption, tolerability, and effects on mitochondrial activity of oral coenzyme Q10 in parkinsonian patients Neurology 50 3 1998 793 795
91. C.W. Shults, D. Oakes, K. Kieburtz, M.F. Beal, R. Haas, and S. Plumb Effects of coenzyme Q10 in early Parkinson disease - evidence of slowing of the functional decline Arch Neurol 59 2002 1541 1550
92. C.W. Shults, M.F. Beal, D. Song, and D. Fontaine Pilot trial of high dosages of coenzyme Q10 in patients with Parkinson's disease Exp Neurol 188 2 2004 491 494
93. T.P. Singer, N. Castagnoli Jr., R.R. Ramsay, and A.J. Trevor Biochemical events in the development of parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine J Neurochem 49 1987 1 8
94. R. Smigrodzki, J. Parks, and W.D. Parker High frequency of mitochondrial complex I mutations in Parkinson's disease and aging Neurobiol Aging 25 10 2004 1273 1281
95. M. Sohmiya, M. Tanaka, N.W. Tak, M. Yanagisawa, Y. Tanino, and Y. Suzuki Redox status of plasma coenzyme Q10 indicates elevated systemic oxidative stress in Parkinson's disease J Neurol Sci 223 2 2004 161 166
96. R.H. Swerdlow, J.K. Parks, S.W. Miller, J.B. Tuttle, P.A. Trimmer, and J.P. Sheehan Origin and functional consequences of the complex I defect in Parkinson's disease Ann Neurol 40 4 1996 663 671
97. Y. Teshima, M. Akao, S.P. Jones, and E. Marbán Uncoupling protein-2 overexpression inhibits mitochondrial death pathway in cardiomyocytes Circ Res 93 3 2003 192 200
98. The Huntington Study Group A randomized, placebo-controlled trial of coenzyme Q10 and remacemide in Huntington's disease Neurology 57 3 2001 397 404
99. Y. Tomono, J. Hasegawa, T. Seki, K. Motegi, and N. Morishita Pharmacokinetic study of deuterium-labelled coenzyme Q10 in man Int J Clin Pharmacol Ther Toxicol 24 1986 536 541
100. Y. Tsujimoto Cell death regulation by the Bcl-2 protein family in the mitochondria J Cell Physiol 195 2 2003 158 167
101. E.M. Valente, P.M. Abou-Sleiman, V. Caputo, M.M. Muqit, K. Harvey, and S. Gispert Hereditary early-onset Parkinson's disease caused by mutations in PINK1 Science 304 2004 1158 1160
102. M. van Gurp, N. Festjens, G. van Loo, X. Saelens, and P. Vandenabeele Mitochondrial intermembrane proteins in cell death Biochem Biophys Res Commun 304 3 2003 487 497
103. L. Walter, V. Nogueira, X. Leverve, M.P. Heitz, P. Bernardi, and E. Fontaine Three classes of ubiquinone analogs regulate the mitochondrial permeability transition pore through a common site J Biol Chem 275 2000 29521 29527
104. T. Yamagami, T. Okishio, S. Toyama, and T. Kishi Correlation of serum coenzyme Q10 level and leukocute complex II activity in normal and cardiovascular patients K. Folkers T. Yamagami Biomedical and Clinical Aspects of Coenzyme Q 1981 Elsevier Science Publishers Amsterdam 79 89
105. H. Yoshino, Y. Nakagawa-Hattori, T. Kondo, and Y. Mizuno Mitochondrial complex I and II activities of lymphocytes and platelets in Parkinson's disease J Neural Transm Parkinson's Dis Dement Sect 4 1 1992 27 34
106. N. Zamzami, P. Marchetti, M. Castedo, C. Zanin, J.L. Vayssiere, and P.X. Petit Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo J Exp Med 181 1995 1661 1672
107. N. Zamzami, P. Marchetti, M. Castedo, D. Decaudin, A. Macho, and T. Hirsch Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death J Exp Med 182 1995 367 377
108. K.C. Zimmermann, C. Bonzon, and D.R. Green The machinery of programmed cell death Pharmacol Ther 92 2001 57 70