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Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: Synthesis and in vitro studies

Biochemistry (Moscow) volume 73, pages 1273–1287 (2008)Cite this article

Abstract

Synthesis of cationic plastoquinone derivatives (SkQs) containing positively charged phosphonium or rhodamine moieties connected to plastoquinone by decane or pentane linkers is described. It is shown that SkQs (i) easily penetrate through planar, mitochondrial, and outer cell membranes, (ii) at low (nanomolar) concentrations, posses strong antioxidant activity in aqueous solution, BLM, lipid micelles, liposomes, isolated mitochondria, and cells, (iii) at higher (micromolar) concentrations, show pronounced prooxidant activity, the “window” between anti- and prooxidant concentrations being very much larger than for MitoQ, a cationic ubiquinone derivative showing very much lower antioxidant activity and higher prooxidant activity, (iv) are reduced by the respiratory chain to SkQH2, the rate of oxidation of SkQH2 being lower than the rate of SkQ reduction, and (v) prevent oxidation of mitochondrial cardiolipin by OH·. In HeLa cells and human fibroblasts, SkQs operate as powerful inhibitors of the ROS-induced apoptosis and necrosis. For the two most active SkQs, namely SkQ1 and SkQR1, C 1/2 values for inhibition of the H2O2-induced apoptosis in fibroblasts appear to be as low as 1·10−11 and 8·10−13 M, respectively. SkQR1, a fluorescent representative of the SkQ family, specifically stains a single type of organelles in the living cell, i.e. energized mitochondria. Such specificity is explained by the fact that it is the mitochondrial matrix that is the only negatively-charged compartment inside the cell. Assuming that the Δψ values on the outer cell and inner mitochondrial membranes are about 60 and 180 mV, respectively, and taking into account distribution coefficient of SkQ1 between lipid and water (about 13,000: 1), the SkQ1 concentration in the inner leaflet of the inner mitochondrial membrane should be 1.3·108 times higher than in the extracellular space. This explains the very high efficiency of such compounds in experiments on cell cultures. It is concluded that SkQs are rechargeable, mitochondria-targeted antioxidants of very high efficiency and specificity. Therefore, they might be used to effectively prevent ROS-induced oxidation of lipids and proteins in the inner mitochondrial membrane in vivo.

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Abbreviations

Δψ:

transmembrane electric potential difference

AAPH:

2,2′-azobis(2-amidinopropane) dihydrochloride

BLM:

bilayer planar phospholipid membrane

BSA:

bovine serum albumin

CCCP:

carbonyl cyanide m-chlorophenylhydrazone

CM-DCF-DA:

5-(-6)-chloromethyl-2′,7′-dichlorodihydrofluorescein diacetate

C12TPP:

dodecyltriphenylphosphonium

DMQ:

demethoxy-derivative of CoQ0 lacking one of the methoxy groups

DPQ:

decylplastoquinone

FCCP:

carbonyl cyanide p-trifluo-romethoxyphenylhydrazone

MDA:

malondialdehyde

MitoQ:

10-(6′-ubiquinonyl) decyltriphenylphosphonium

NAC:

N-acetyl cysteine

PQ:

plastoquinone

ROS:

reactive oxygen species

SF6846:

3,5-di(tert)butyl-4-hydroxybenzylidene malononitrile

SkQ:

cationic derivative of plastoquinone or methyl plastoquinone

SkQ1:

10-(6′-plastoquinonyl) decyltriphenylphosphonium

SkQ2:

10-(6′-plastoquinonyl) decylcarnitine

SkQ2M:

10-(6t′-plastoquinonyl) decylmethylcarnitine

SkQ3:

10-(6′-methylplasto-quinonyl) decyltriphenylphosphonium

SkQ4:

10-(6′-plastoquinonyl) decyltributylammonium

SkQ5:

5-(6′-plastoquinonyl) amyltriphenylphosphonium

SkQR1:

10-(6′-plastoquinonyl) decylrhodamine 19

TMRE:

tetramethylrhodamine ethyl ester

TPB:

tetraphenylborate

TPP:

tetraphenylphosphonium

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Authors and Affiliations

  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    Y. N. Antonenko, A. V. Avetisyan, L. E. Bakeeva, B. V. Chernyak, L. V. Domnina, O. Yu. Ivanova, D. S. Izyumov, L. S. Khailova, S. S. Klishin, G. A. Korshunova, K. G. Lyamzaev, M. S. Muntyan, O. K. Nepryakhina, A. A. Pashkovskaya, O. Yu. Pletjushkina, A. V. Pustovidko, T. I. Rokitskaya, V. B. Saprunova, R. A. Simonyan, J. M. Vassiliev, M. Yu. Vyssokikh, L. S. Yaguzhinsky & V. P. Skulachev

  2. Chemical Faculty, Lomonosov Moscow State University, 119991, Moscow, Russia

    V. A. Chertkov, N. V. Sumbatyan & V. N. Tashlitsky

  3. Institute of Chemical Physics, ul. Kosygina 4, 119977, Moscow, Russia

    V. A. Roginsky

  4. Institute of Experimental Cardiology, Cardiology Research Center, 3-ya Cherepkovskaya ul. 15A, 121552, Moscow, Russia

    E. K. Ruuge & I. V. Sviryaeva

  5. Biological Faculty, Lomonosov Moscow State University, 119991, Moscow, Russia

    I. I. Severina

  6. Mitoengineering Center, Lomonosov Moscow State University, 119991, Moscow, Russia

    I. V. Skulachev, M. V. Skulachev, A. A. Zamyatnin Jr. & V. P. Skulachev

  7. Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119991, Moscow, Russia

    V. P. Skulachev

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  2. A. V. Avetisyan
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  18. V. A. Roginsky
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  25. M. V. Skulachev
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  33. V. P. Skulachev
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Correspondence to V. P. Skulachev.

Additional information

Published in Russian in Biokhimiya, 2008, Vol. 73, No. 12, pp. 1589–1606.

This and the following four articles were written by the request of the Editorial Board of Biochemistry (Moscow).

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Antonenko, Y.N., Avetisyan, A.V., Bakeeva, L.E. et al. Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: Synthesis and in vitro studies. Biochemistry Moscow 73, 1273–1287 (2008). https://doi.org/10.1134/S0006297908120018

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  • DOI: https://doi.org/10.1134/S0006297908120018

Key words

  • SkQ1
  • penetrating cations
  • plastoquinone
  • antioxidants
  • mitochondria
  • apoptosis