Abstract
Oxidative stress is considered a major contributor to etiology of both “normal” senescence and severe pathologies with serious public health implications. Mitochondria generate reactive oxygen species (ROS) that are thought to augment intracellular oxidative stress. Mitochondria possess at least nine known sites that are capable of generating superoxide anion, a progenitor ROS. Mitochondria also possess numerous ROS defense systems that are much less studied. Studies of the last three decades shed light on many important mechanistic details of mitochondrial ROS production, but the bigger picture remains obscure. This review summarizes the current knowledge about major components involved in mitochondrial ROS metabolism and factors that regulate ROS generation and removal. An integrative, systemic approach is applied to analysis of mitochondrial ROS metabolism, which is now dissected into mitochondrial ROS production, mitochondrial ROS removal, and mitochondrial ROS emission. It is suggested that mitochondria augment intracellular oxidative stress due primarily to failure of their ROS removal systems, whereas the role of mitochondrial ROS emission is yet to be determined and a net increase in mitochondrial ROS production in situ remains to be demonstrated.
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REFERENCES
Skulachev, V. P. (1996) Q. Rev. Biophys., 29, 169–202.
Fiskum, G., Murphy, A. N., and Beal, M. F. (1999) J. Cerebr. Blood Flow Metab., 19, 351–369.
Murphy, A. N., Fiskum, G., and Beal, M. F. (1999) J. Cerebr. Blood Flow Metab., 19, 231–245.
Beal, M. F. (1996) Curr. Opin. Neurobiol., 6, 661–666.
Bossy Wetzel, E., Schwarzenbacher, R., and Lipton, S. A. (2004) Nat. Med., 10(Suppl.), S2–9.
Dawson, T. M., and Dawson, V. L. (2003) Science, 302, 819–822.
Shen, J., and Cookson, M. R. (2004) Neuron, 43, 301–304.
Lenaz, G. (2001) IUBMB Life, 52, 159–164.
Jensen, P. K. (1966) Biochim. Biophys. Acta, 122, 157–166.
Loschen, G., Flohe, L., and Chance, B. (1971) FEBS Lett., 18, 261–264.
Boveris, A., and Chance, B. (1973) Biochem. J., 134, 707–716.
Sawyer, D. T., and Valentine, J. S. (1981) Acc. Chem. Res., 14, 393–400.
Turrens, J. F. (2003) J. Physiol., 552, 335–344.
Tolkien, J. R. R. (1954) The Lord of the Rings, George Allen & Unwin.
Nishino, H., and Ito, A. (1986) J. Biochem. (Tokyo), 100, 1523–1531.
Whatley, S. A., Curti, D., and Marchbanks, R. M. (1996) Neurochem. Res., 21, 995–1004.
Whatley, S. A., Curti, D., Das Gupta, F., Ferrier, I. N., Jones, S., Taylor, C., and Marchbanks, R. M. (1998) Mol. Psychiatry, 3, 227–237.
Hauptmann, N., Grimsby, J., Shih, J. C., and Cadenas, E. (1996) Arch. Biochem. Biophys., 335, 295–304.
Simonson, S. G., Zhang, J., Canada, A. T., Jr., Su, Y. F., Benveniste, H., and Piantadosi, C. A. (1993) J. Cerebr. Blood Flow Metab., 13, 125–134.
Kunduzova, O. R., Bianchi, P., Parini, A., and Cambon, C. (2002) Eur. J. Pharmacol., 448, 225–230.
Maurel, A., Hernandez, C., Kunduzova, O., Bompart, G., Cambon, C., Parini, A., and Frances, B. (2003) Am. J. Physiol. Heart Circ. Physiol., 284, H1460–1467.
Carvalho, F., Duarte, J. A., Neuparth, M. J., Carmo, H., Fernandes, E., Remiao, F., and Bastos, M. L. (2001) Arch. Toxicol., 75, 465–469.
Kumar, M. J., Nicholls, D. G., and Andersen, J. K. (2003) J. Biol. Chem., 278, 46432–46439.
Loffler, M., Becker, C., Wegerle, E., and Schuster, G. (1996) Histochem. Cell Biol., 105, 119–128.
Forman, J. H., and Kennedy, J. (1975) J. Biol. Chem., 250, 4322–4326.
Forman, H. J., and Kennedy, J. (1976) Arch. Biochem. Biophys., 173, 219–224.
Dileepan, K. N., and Kennedy, J. (1985) Biochem. J., 225, 189–194.
Koza, R. A., Kozak, U. C., Brown, L. J., Leiter, E. H., MacDonald, M. J., and Kozak, L. P. (1996) Arch. Biochem. Biophys., 336, 97–104.
Lee, Y. P., and Lardy, H. A. (1965) J. Biol. Chem., 240, 1427–1436.
Dummler, K., Muller, S., and Seitz, H. J. (1996) Biochem. J., 317 (Pt. 3), 913–918.
Kwong, L. K., and Sohal, R. S. (1998) Arch. Biochem. Biophys., 350, 118–126.
Miwa, S., St Pierre, J., Partridge, L., and Brand, M. D. (2003) Free Rad. Biol. Med., 35, 938–948.
Zhang, L., Yu, L., and Yu, C. A. (1998) J. Biol. Chem., 273, 33972–33976.
McLennan, H. R., and Degli Esposti, M. (2000) J. Bioenerg. Biomembr., 32, 153–162.
Gardner, P. R. (2002) Meth. Enzymol., 349, 9–23.
Vasquez Vivar, J., Kalyanaraman, B., and Kennedy, M. C. (2000) J. Biol. Chem., 275, 14064–14069.
Maas, E., and Bisswanger, H. (1990) FEBS Lett., 277, 189–190.
Tretter, L., and Adam Vizi, V. (2004) J. Neurosci., 24, 7771–7778.
Starkov, A. A., Fiskum, G., Chinopoulos, C., Lorenzo, B. J., Browne, S. E., Patel, M. S., and Beal, M. F. (2004) J. Neurosci., 24, 7779–7788.
Bunik, V. I., and Sievers, C. (2002) Eur. J. Biochem., 269, 5004–5015.
Skulachev, V. P. (1988) Membrane Bioenergetics, Springer Verlag, New York.
Cadenas, E., Boveris, A., Ragan, C. I., and Stoppani, A. O. (1977) Arch. Biochem. Biophys., 180, 248–257.
Kushnareva, Y., Murphy, A. N., and Andreyev, A. (2002) Biochem. J., 368, 545–553.
Liu, Y., Fiskum, G., and Schubert, D. (2002) J. Neurochem., 80, 780–787.
Takeshige, K., and Minakami, S. (1979) Biochem. J., 180, 129–135.
Hinkle, P. C., Butow, R. A., Racker, E., and Chance, B. (1967) J. Biol. Chem., 242, 5169–5173.
Herrero, A., and Barja, G. (2000) J. Bioenerg. Biomembr., 32, 609–615.
Genova, M. L., Ventura, B., Giuliano, G., Bovina, C., Formiggini, G., Parenti Castelli, G., and Lenaz, G. (2001) FEBS Lett., 505, 364–368.
Kang, D., Narabayashi, H., Sata, T., and Takeshige, K. (1983) J. Biochem. (Tokyo), 94, 1301–1306.
Kudin, A. P., Bimpong Buta, N. Y., Vielhaber, S., Elger, C. E., and Kunz, W. S. (2004) J. Biol. Chem., 279, 4127–4135.
Krishnamoorthy, G., and Hinkle, P. C. (1988) J. Biol. Chem.., 263, 17566–17575.
Genova, M. L., Pich, M. M., Biondi, A., Bernacchia, A., Falasca, A., Bovina, C., Formiggini, G., Parenti Castelli, G., and Lenaz, G. (2003) Exp. Biol. Med. (Maywood), 228, 506–513.
Chance, B., and Williams, G. R. (1956) Adv. Enzymol. Relat. Subj. Biochem., 17, 65–134.
Korshunov, S. S., Skulachev, V. P., and Starkov, A. A. (1997) FEBS Lett., 416, 15–18.
Starkov, A. A., and Fiskum, G. (2003) J. Neurochem., 86, 1101–1107.
Hansford, R. G., Hogue, B. A., and Mildaziene, V. (1997) J. Bioenerg. Biomembr., 29, 89–95.
Starkov, A. A., Polster, B. M., and Fiskum, G. (2002) J. Neurochem., 83, 220–228.
Lambert, A. J., and Brand, M. D. (2004) Biochem. J., 382, 511–517.
Turrens, J. F., and Boveris, A. (1980) Biochem. J., 191, 421–427.
Sipos, I., Tretter, L., and Adam Vizi, V. (2003) J. Neurochem., 84, 112–118.
Barja, G. (1999) J. Bioenerg. Biomembr., 31, 347–366.
Herrero, A., and Barja, G. (2000) J. Bioenerg. Biomembr., 32, 609–615.
Ramsay, R. R., and Singer, T. P. (1992) Biochem. Biophys. Res. Commun., 189, 47–52.
Dykens, J. A. (1994) J. Neurochem., 63, 584–591.
Kowaltowski, A. J., Castilho, R. F., and Vercesi, A. E. (1995) Am. J. Physiol., 269, C141–147.
Kowaltowski, A. J., Castilho, R. F., and Vercesi, A. E. (1996) FEBS Lett., 378, 150–152.
Kowaltowski, A. J., Naia da Silva, E. S., Castilho, R. F., and Vercesi, A. E. (1998) Arch. Biochem. Biophys., 359, 77–81.
Kowaltowski, A. J., Netto, L. E., and Vercesi, A. E. (1998) J. Biol. Chem., 273, 12766–12769.
Trumpower, B. L. (1990) J. Biol. Chem., 265, 11409–11412.
Grigolava, I. V., Ksenzenko, M., Konstantinov, A. A., Tikhonov, A. N., and Kerimov, T. M. (1980) Biokhimiya, 45, 75–82.
Loschen, G., Azzi, A., Richter, C., and Flohe, L. (1974) FEBS Lett., 42, 68–72.
Dionisi, O., Galeotti, T., Terranova, T., and Azzi, A. (1975) Biochim. Biophys. Acta, 403, 292–300.
Boveris, A., Cadenas, E., and Stoppani, A. O. (1976) Biochem. J., 156, 435–444.
Ksenzenko, M., Konstantinov, A. A., Khomutov, G. B., Tikhonov, A. N., and Ruuge, E. K. (1983) FEBS Lett., 155, 19–24.
Turrens, J. F., Alexandre, A., and Lehninger, A. L. (1985) Arch. Biochem. Biophys., 237, 408–414.
Rich, P. R., and Bonner, W. D. (1978) Arch. Biochem. Biophys., 188, 206–213.
Junemann, S., Heathcote, P., and Rich, P. R. (1998) J. Biol. Chem., 273, 21603–21607.
Turrens, J. F. (1997) Biosci. Rep., 17, 3–8.
Crofts, A. R., Barquera, B., Gennis, R. B., Kuras, R., Guergova Kuras, M., and Berry, E. A. (1999) Biochemistry, 38, 15807–15826.
Zoccarato, F., Cavallini, L., Deana, R., and Alexandre, A. (1988) Biochem. Biophys. Res. Commun., 154, 727–734.
Konstantinov, A. A., Peskin, A. V., Popova, E., Khomutov, G. B., and Ruuge, E. K. (1987) Biochim. Biophys. Acta, 894, 1–10.
Raha, S., McEachern, G. E., Myint, A. T., and Robinson, B. H. (2000) Free Rad. Biol. Med., 29, 170–180.
Starkov, A. A., and Fiskum, G. (2001) Biochem. Biophys. Res. Commun., 281, 645–650.
Ksenzenko, M., Konstantinov, A. A., Khomutov, G. B., Tikhonov, A. N., and Ruuge, E. K. (1984) FEBS Lett., 175, 105–108.
Nohl, H., and Hegner, D. (1978) Eur. J. Biochem., 82, 563–567.
St Pierre, J., Buckingham, J. A., Roebuck, S. J., and Brand, M. D. (2002) J. Biol. Chem., 277, 44784–44790.
Han, D., Williams, E., and Cadenas, E. (2001) Biochem. J., 353, 411–416.
Mao, G. D., and Poznansky, M. J. (1992) FEBS Lett., 305, 233–236.
Gus ‘kova, R. A., Ivanov, II, Kol ‘tover, V. K., Akhobadze, V. V., and Rubin, A. B. (1984) Biochim. Biophys. Acta, 778, 579–585.
Lynch, R. E., and Fridovich, I. (1978) J. Biol. Chem., 253, 4697–4699.
Frimer, A. A., Strul, G., Buch, J., and Gottlieb, H. E. (1996) Free Rad. Biol. Med., 20, 843–852.
Takahashi, M. A., and Asada, K. (1983) Arch. Biochem. Biophys., 226, 558–566.
Echtay, K. S., Murphy, M. P., Smith, R. A., Talbot, D. A., and Brand, M. D. (2002) J. Biol. Chem., 277, 47129–47135.
Bulteau, A. L., Ikeda Saito, M., and Szweda, L. I. (2003) Biochemistry, 42, 14846–14855.
Muller, F. L., Liu, Y., and van Remmen, H. (2004) J. Biol. Chem., 279, 49064–49073.
Packer, L., Weber, S. U., and Rimbach, G. (2001) J. Nutr., 131, 369S–373S.
Lass, A., Forster, M. J., and Sohal, R. S. (1999) Free Rad. Biol. Med., 26, 1375–1382.
Maiorino, M., Thomas, J. P., Girotti, A. W., and Ursini, F. (1991) Free Rad. Res. Commun., 12/13, 131–135.
Thomas, J. P., Maiorino, M., Ursini, F., and Girotti, A. W. (1990) J. Biol. Chem., 265, 454–461.
Bao, Y., Jemth, P., Mannervik, B., and Williamson, G. (1997) FEBS Lett., 410, 210–212.
Imai, H., and Nakagawa, Y. (2003) Free Rad. Biol. Med., 34, 145–169.
Yant, L. J., Ran, Q., Rao, L., van Remmen, H., Shibatani, T., Belter, J. G., Motta, L., Richardson, A., and Prolla, T. A. (2003) Free Rad. Biol. Med., 34, 496–502.
Arai, M., Imai, H., Koumura, T., Yoshida, M., Emoto, K., Umeda, M., Chiba, N., and Nakagawa, Y. (1999) J. Biol. Chem., 274, 4924–4933.
Esposito, L. A., Kokoszka, J. E., Waymire, K. G., Cottrell, B., MacGregor, G. R., and Wallace, D. C. (2000) Free Rad. Biol. Med., 28, 754–766.
Knopp, E. A., Arndt, T. L., Eng, K. L., Caldwell, M., LeBoeuf, R. C., Deeb, S. S., and O ‘Brien, K. D. (1999) Mamm. Genome, 10, 601–605.
Pushpa Rekha, T. R., Burdsall, A. L., Oleksa, L. M., Chisolm, G. M., and Driscoll, D. M. (1995) J. Biol. Chem., 270, 26993–26999.
Gardner, P. R., Raineri, I., Epstein, L. B., and White, C. W. (1995) J. Biol. Chem., 270, 13399–13405.
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., et al. (1995) Nat. Genet., 11, 376–381.
Lebovitz, R. M., Zhang, H., Vogel, H., Cartwright, J., Jr., Dionne, L., Lu, N., Huang, S., and Matzuk, M. M. (1996) Proc. Natl. Acad. Sci. USA, 93, 9782–9787.
Tsan, M. F., White, J. E., Caska, B., Epstein, C. J., and Lee, C. Y. (1998) Am. J. Respir. Cell Mol. Biol., 19, 114–120.
Jackson, R. M., Helton, E. S., Viera, L., and Ohman, T. (1999) Exp. Lung Res., 25, 631–646.
Van Remmen, H., Ikeno, Y., Hamilton, M., Pahlavani, M., Wolf, N., Thorpe, S. R., Alderson, N. L., Baynes, J. W., Epstein, C. J., Huang, T. T., Nelson, J., Strong, R., and Richardson, A. (2003) Physiol. Genomics, 16, 29–37.
Van Remmen, H., Williams, M. D., Guo, Z., Estlack, L., Yang, H., Carlson, E. J., Epstein, C. J., Huang, T. T., and Richardson, A. (2001) Am. J. Physiol. Heart Circ. Physiol., 281, H1422–1432.
Williams, M. D., van Remmen, H., Conrad, C. C., Huang, T. T., Epstein, C. J., and Richardson, A. (1998) J. Biol. Chem., 273, 28510–28515.
Van Remmen, H., Salvador, C., Yang, H., Huang, T. T., Epstein, C. J., and Richardson, A. (1999) Arch. Biochem. Biophys., 363, 91–97.
Raineri, I., Carlson, E. J., Gacayan, R., Carra, S., Oberley, T. D., Huang, T. T., and Epstein, C. J. (2001) Free Rad. Biol. Med., 31, 1018–1030.
Hackenbrock, C. R., Chazotte, B., and Gupte, S. S. (1986) J. Bioenerg. Biomembr., 18, 331–368.
McCord, J. M., and Fridovich, I. (1970) J. Biol. Chem., 245, 1374–1377.
Korshunov, S. S., Krasnikov, B. F., Pereverzev, M. O., and Skulachev, V. P. (1999) FEBS Lett., 462, 192–198.
Pereverzev, M. O., Vygodina, T. V., Konstantinov, A. A., and Skulachev, V. P. (2003) Biochem. Soc. Trans., 31, 1312–1315.
Mailer, K. (1990) Biochem. Biophys. Res. Commun., 170, 59–64.
Ho, Y. S., Xiong, Y., Ma, W., Spector, A., and Ho, D. S. (2004) J. Biol. Chem., 279, 32804–32812.
Radi, R., Turrens, J. F., Chang, L. Y., Bush, K. M., Crapo, J. D., and Freeman, B. A. (1991) J. Biol. Chem., 266, 22028–22034.
Antunes, F., Han, D., and Cadenas, E. (2002) Free Rad. Biol. Med., 33, 1260–1267.
Pastore, A., Federici, G., Bertini, E., and Piemonte, F. (2003) Clin. Chim. Acta, 333, 19–39.
Dringen, R. (2000) Progr. Neurobiol., 62, 649–671.
Wahllander, A., Soboll, S., Sies, H., Linke, I., and Muller, M. (1979) FEBS Lett., 97, 138–140.
Griffith, O. W., and Meister, A. (1985) Proc. Natl. Acad. Sci. USA, 82, 4668–4672.
Martensson, J., Lai, J. C., and Meister, A. (1990) Proc. Natl. Acad. Sci. USA, 87, 7185–7189.
Chen, Z., and Lash, L. H. (1998) J. Pharmacol. Exp. Ther., 285, 608–618.
Rebrin, I., Kamzalov, S., and Sohal, R. S. (2003) Free Rad. Biol. Med., 35, 626–635.
Vogel, R., Wiesinger, H., Hamprecht, B., and Dringen, R. (1999) Neurosci. Lett., 275, 97–100.
Boveris, A., and Cadenas, E. (1997) Cellular Sources and Steady State Levels of Reactive Oxygen Species, Marcel Dekker.
Han, D., Canali, R., Rettori, D., and Kaplowitz, N. (2003) Mol. Pharmacol., 64, 1136–1144.
Raza, H., Robin, M. A., Fang, J. K., and Avadhani, N. G. (2002) Biochem. J., 366, 45–55.
Olafsdottir, K., and Reed, D. J. (1988) Biochim. Biophys. Acta, 964, 377–382.
Kozhemiakin, L. A., Bulavin, D. V., Udintsev, A. V., and Smirnov, V. V. (1993) Tsitologiya, 35, 58–63.
Zoccarato, F., Cavallini, L., and Alexandre, A. (2004) J. Biol. Chem., 279, 4166–4174.
Panfili, E., Sandri, G., and Ernster, L. (1991) FEBS Lett., 290, 35–37.
Kelner, M. J., and Montoya, M. A. (2000) Biochem. Biophys. Res. Commun., 269, 366–368.
Hoek, J. B., and Rydstrom, J. (1988) Biochem. J., 254, 1–10.
Kirsch, M., and De Groot, H. (2001) FASEB J., 15, 1569–1574.
Tischler, M. E., Hecht, P., and Williamson, J. R. (1977) FEBS Lett., 76, 99–104.
Skulachev, V. P. (2001) FEBS Lett., 492, 1–3.
Lenzen, S., Drinkgern, J., and Tiedge, M. (1996) Free Rad. Biol. Med., 20, 463–466.
Asayama, K., Yokota, S., Dobashi, K., Hayashibe, H., Kawaoi, A., and Nakazawa, S. (1994) Histochemistry, 102, 213–219.
Utsunomiya, H., Komatsu, N., Yoshimura, S., Tsutsumi, Y., and Watanabe, K. (1991) J. Histochem. Cytochem., 39, 1167–1174.
Esworthy, R. S., Ho, Y. S., and Chu, F. F. (1997) Arch. Biochem. Biophys., 340, 59–63.
Ho, Y. S., Magnenat, J. L., Bronson, R. T., Cao, J., Gargano, M., Sugawara, M., and Funk, C. D. (1997) J. Biol. Chem., 272, 16644–16651.
Spector, A., Yang, Y., Ho, Y. S., Magnenat, J. L., Wang, R. R., Ma, W., and Li, W. C. (1996) Exp. Eye Res., 62, 521–540.
Cheng, W. H., Ho, Y. S., Valentine, B. A., Ross, D. A., Combs, G. F., Jr., and Lei, X. G. (1998) J. Nutr., 128, 1070–1076.
Cheng, W. H., Ho, Y. S., Ross, D. A., Valentine, B. A., Combs, G. F., and Lei, X. G. (1997) J. Nutr., 127, 1445–1450.
De Haan, J. B., Bladier, C., Griffiths, P., Kelner, M., O ‘Shea, R. D., Cheung, N. S., Bronson, R. T., Silvestro, M. J., Wild, S., Zheng, S. S., Beart, P. M., Hertzog, P. J., and Kola, I. (1998) J. Biol. Chem., 273, 22528–22536.
Zhang, J., Graham, D. G., Montine, T. J., and Ho, Y. S. (2000) J. Neuropathol. Exp. Neurol., 59, 53–61.
Klivenyi, P., Andreassen, O. A., Ferrante, R. J., Dedeoglu, A., Mueller, G., Lancelot, E., Bogdanov, M., Andersen, J. K., Jiang, D., and Beal, M. F. (2000) J. Neurosci., 20, 1–7.
Fujii, J., and Ikeda, Y. (2002) Redox Rep., 7, 123–130.
Wood, Z. A., Schroder, E., Robin Harris, J., and Poole, L. B. (2003) Trends Biochem. Sci., 28, 32–40.
Chae, H. Z., Kim, H. J., Kang, S. W., and Rhee, S. G. (1999) Diabetes Res. Clin. Pract., 45, 101–112.
Leyens, G., Donnay, I., and Knoops, B. (2003) Comp. Biochem. Physiol. B. Biochem. Mol. Biol., 136, 943–955.
Araki, M., Nanri, H., Ejima, K., Murasato, Y., Fujiwara, T., Nakashima, Y., and Ikeda, M. (1999) J. Biol. Chem., 274, 2271–2278.
Hattori, F., Murayama, N., Noshita, T., and Oikawa, S. (2003) J. Neurochem., 86, 860–868.
Banmeyer, I., Marchand, C., Verhaeghe, C., Vucic, B., Rees, J. F., and Knoops, B. (2004) Free Rad. Biol. Med., 36, 65–77.
Johansson, C., Lillig, C. H., and Holmgren, A. (2004) J. Biol. Chem., 279, 7537–7543.
Gromer, S., Urig, S., and Becker, K. (2004) Med. Res. Rev., 24, 40–89.
Fernandes, A. P., and Holmgren, A. (2004) Antioxid. Redox Signal, 6, 63–74.
Nonn, L., Williams, R. R., Erickson, R. P., and Powis, G. (2003) Mol. Cell Biol., 23, 916–922.
Patenaude, A., Murthy, M. R., and Mirault, M. E. (2004) J. Biol. Chem., 279, 27302–27314.
Staniek, K., and Nohl, H. (1999) Biochim. Biophys. Acta, 1413, 70–80.
Savage, M. K., Jones, D. P., and Reed, D. J. (1991) Arch. Biochem. Biophys., 290, 51–56.
Nicholls, D. G., and Budd, S. L. (2000) Physiol. Rev., 80, 315–360.
Fiskum, G. (2000) J. Neurotrauma, 17, 843–855.
Maciel, E. N., Vercesi, A. E., and Castilho, R. F. (2001) J. Neurochem., 79, 1237–1245.
Perez Velazquez, J. L., Frantseva, M. V., and Carlen, P. L. (1997) J. Neurosci., 17, 9085–9094.
Anderson, M. F., and Sims, N. R. (2002) J. Neurochem., 81, 541–549.
Starkov, A. A. (1997) Biosci. Rep., 17, 273–279.
Zhang, Z., Huang, L., Shulmeister, V. M., Chi, Y. I., Kim, K. K., Hung, L. W., Crofts, A. R., Berry, E. A., and Kim, S. H. (1998) Nature, 392, 677–684.
Novgorodov, S. A., Gudz, T. I., Kushnareva, Y. E., Roginsky, V. A., and Kudrjashov, Y. B. (1991) Biochim. Biophys. Acta, 1058, 242–248.
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Translated from Biokhimiya, Vol. 70, No. 2, 2005, pp. 246–264.
Original Russian Text Copyright © 2005 by Andreyev, Kushnareva, Starkov.
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Andreyev, A.Y., Kushnareva, Y.E. & Starkov, A.A. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Moscow) 70, 200–214 (2005). https://doi.org/10.1007/s10541-005-0102-7
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DOI: https://doi.org/10.1007/s10541-005-0102-7