Abstract
Phenoptosis is the death of an organism programmed by its genome. Numerous examples of phenoptosis are described in prokaryotes, unicellular eukaryotes, and all kingdoms of multicellular eukaryotes (animals, plants, and fungi). There are very demonstrative cases of acute phenoptosis when actuation of a specific biochemical or behavioral program results in immediate death. Rapid (taking days) senescence of semelparous plants is described as phenoptosis controlled by already known genes and mediated by toxic phytohormones like abscisic acid. In soya, the death signal is transmitted from beans to leaves via xylem, inducing leaf fall and death of the plant. Mutations in two genes of Arabidopsis thaliana, required for the flowering and subsequent formation of seeds, prevent senescence, strongly prolonging the lifespan of this small semelparous grass that becomes a big bush with woody stem, and initiate substitution of vegetative for sexual reproduction. The death of pacific salmon immediately after spawning is surely programmed. In this case, numerous typical traits of aging, including amyloid plaques in the brain, appear on the time scale of days. There are some indications that slow aging of higher animals and humans is also programmed, being the final step of ontogenesis. It is assumed that stepwise decline of many physiological functions during such aging increases pressure of natural selection on organisms stimulating in this way biological evolution. As a working hypothesis, the biochemical mechanism of slow aging is proposed. It is assumed that mitochondria-generated reactive oxygen species (ROS) is a tool to stimulate apoptosis, an effect decreasing with age the cell number (cellularity) of organs and tissues. A group of SkQ-type substances composed of plastoquinone and a penetrating cation were synthesized to target an antioxidant into mitochondria and to prevent the age-linked rise of the mitochondrial ROS level. Such targeting is due to the fact that mitochondria are the only cellular organelles that are negatively charged compared to the cytosol. SkQs are shown to strongly decrease concentration of ROS in mitochondria, prolong lifespan of fungi, invertebrates, fish, and mammals, and retard appearance of numerous traits of aging. Clinical trials of SkQ1 (plastoquinonyl decyltriphenylphosphonium) have been successfully completed so that the Ministry of Health of the Russian Federation recommends drops of very dilute (0.25 μM) solution of this antioxidant as a medicine to treat the syndrome of dry eye, which was previously considered an incurable disease developing with age. These drops are already available in drugstores. Thus, SkQ1 is the first mitochondria-targeted drug employed in medical practice.
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Abbreviations
- Δψ:
-
transmembrane difference of electric potentials
- BLM:
-
bilayer planar phospholipid membrane
- C12TPP:
-
dodecyltriphenylphosphonium
- MitoQ:
-
ubiquinonyl decyltriphenylphosphonium
- ROS:
-
reactive oxygen species
- SkQ:
-
derivatives of plastoquinone and penetrating cations (Sk+)
- SkQ1:
-
plastoquinonyl decyltriphenylphosphonium
- SkQR1:
-
plastoquinonyl decylrhodamine 19
References
Skulachev, V. P., and Ozrina, R. D. (2011) Biochemistry (Moscow), 76, 1–2.
Skulachev, V. P. (1997) Biochemistry (Moscow), 62, 1191–1195.
Skulachev, V. P. (1999) Biochemistry (Moscow), 64, 1418–1426.
Longo, V. D., Mitteldorf, J., and Skulachev, V. P. (2005) Nat. Rev. Genet., 6, 866–872.
Libertini, G. (2012) Biochemistry (Moscow), 77, 707–715.
Koonin, E. V., and Aravind, L. (2002) Cell Death Differ., 9, 394–404.
Lewis, K. (2000) Microbiol. Mol. Biol. Rev., 64, 503–514.
Skulachev, V. P. (2003) in Model Systems in Aging (Nystrom, T., and Osiewacz, H. D., eds.) Springer-Verlag, Berlin-Heidelberg, pp. 191–238.
Severin, F. F., and Hyman, A. A. (2002) Curr. Biol., 12, R233–R235.
Pozniakovsky, A. I., Knorre, D. A., Markova, O. V., Hyman, A. A., Skulachev, V. P., and Severin, F. F. (2005) J. Cell Biol., 168, 257–269.
Skulachev, V. P. (2002) Ann. N.Y. Acad. Sci., 959, 214–237.
Severin, F. F., and Skulachev, V. P. (2009) Advances Gerontol. (Russ.), 22, 37–48.
Skulachev, V. P. (2009) Rus. Chem. J. (Russ.), LIII, 125–140.
Sukhanova, E. I., Rogov, A. G., Severin, F. F., and Zvyagilskaya, R. A. (2012) Biochemistry (Moscow), 77, 761–775.
Nooden, L. D., Guiamet, J. J., and John, I. (1997) Physiol. Plant., 101, 746–753.
Leopold, A. C., Niedergangkamien, E., and Janick, J. (1959) Plant Physiol., 34, 570–573.
Lindoo, S. J., and Nooden, L. D. (1977) Plant Physiol., 59, 1136–1140.
Nooden, L. D., and Murray, B. J. (1982) Plant Physiol., 69, 754–756.
Skulachev, V. P. (2011) Aging (Albany, N.Y.), 3, 1120–1123.
Kirkwood, T. B. L., and Melov, S. (2011) Curr. Biol., 21, R701–R707.
Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R., and Abrams, S. R. (2010) Ann. Rev. Plant Biol., 61, 651–679.
Cho, D., Shin, D. J., Jeon, B. W., and Kwak, J. M. (2009) J. Plant Biol., 52, 102–113.
Melzer, S., Lens, F., Gennen, J., Vanneste, S., Rohde, A., and Beeckman, T. (2008) Nature Genet., 40, 1489–1492.
Weismann, A. (1889) Essays upon Heredity and Kindred Biological Problems, Clarendon Press, Oxford.
Carlquist, S. J. (1974) Island Biology, Columbia University Press, New York.
Groover, A. T. (2005) Trends Plant Sci., 10, 210–214.
Kim, S. C., Crawford, D. J., FranciscoOrtega, J., and SantosGuerra, A. (1996) PNAS, 93, 7743–7748.
Bohle, U. R., Hilger, H. H., and Martin, W. F. (1996) PNAS, 93, 11740–11745.
Libbert, A. (1976) Physiology of Plants [Russian translation], Mir, Moscow.
Wodinsky, J. (1977) Science, 198, 948–951.
Nesis, K. N. (1997) in Russian Science: to Persevere and Be Reborn (Byalko, A. V., ed.) [in Russian], Fizmatizdat, Moscow, pp. 358–365.
Dawkins, R. (1976) The Selfish Gene, Oxford University Press, New York.
Bradley, A. J., McDonald, I. R., and Lee, A. K. (1980) General Comparat. Endocrinol., 40, 188–200.
Skulachev, V. P. (2005) Vestnik RAN (Russ.), 75, 831–843.
Austad, S. N. (2004) Aging Cell, 3, 249–251.
Maldonado, T. A., Jones, R. E., and Norris, D. O. (2000) Brain Res., 858, 237–251.
Maldonado, T. A., Jones, R. E., and Norris, D. O. (2002) J. Neurobiol., 53, 11–20.
Maldonado, T. A., Jones, R. E., and Norris, D. O. (2002) J. Neurobiol., 53, 21–35.
Kipling, D., Davis, T., Ostler, E. L., and Faragher, R. G. A. (2004) Science, 305, 1426–1431.
Terzibasi, E., Valenzano, D. R., and Cellerino, A. (2007) Exp. Gerontol., 42, 81–89.
Comfort, A. (1979) The Biology of Senescence, Elsevier, New York.
Schopenhauer, A. (1993) The World as Will and Representation [Russian translation], Moskovskii Klub, Moscow.
Darwin, C. (1871) The Descent of Man, and Selection in Relation to Sex, D. Appleton and Company, New York.
Medawar, P. B. (1952) An Unsolved Problem of Biology, Published for the College by H. K. Lewis, London.
Bowles, J. T. (1998) Med. Hypotheses, 51, 179–221.
Bowles, J. T. (2000) Med. Hypotheses, 54, 236–339.
Loison, A., Festa-Bianchet, M., Gaillard, J. M., Jorgenson, J. T., and Jullien, J. M. (1999) Ecology, 80, 2539–2554.
Bonduriansky, R., and Brassil, C. E. (2002) Nature, 420, 377–377.
Gavrilova, N. S., Gavrilov, L. A., Severin, F. F., and Skulachev, V. P. (2012) Biochemistry (Moscow), 77, 754–760.
Khokhlov, A. N. (2009) Ros. Khim. Zh., LIII, 111–117.
Vreeland, R. H., Rosenzweig, W. D., and Powers, D. W. (2000) Nature, 407, 897–900.
George, J. C., Bada, J., Zeh, J., Scott, L., Brown, S. E., O’Hara, T., and Suydam, R. (1999) Canad. J. Zool., 77, 571–580.
Buffenstein, R. (2005) J. Gerontol. A. Biol. Sci. Med. Sci., 60, 1369–1377.
Dawkins, R. (1989) in Artificial Life Proceedings Reading (Langton, C., ed.) Addison Wesley, Massachusetts, pp. 201–220.
Kirschner, M., and Gerhart, J. (1998) PNAS, 95, 8420–8427.
Skulachev, V. P., Bogachev, A. V., and Kasparinsky, F. O. (2010) Membrane Bioenergetics [in Russian], Moscow University Publishers, Moscow.
Mufazalov, I. A., Penkov, D. N., Chernyak, B. V., Pletyushkina, O. Yu., Vyssokih, M. Yu., Kirpichnikov, M. P., Dolgikh, D. A., Kruglov, A. A., Kuprash, D. V., Skulachev, V. P., and Nedospasov, S. A. (2009) Mol. Biol. (Moscow), 43, 648–656.
Sharonov, G. V., Feofanov, A. V., Bocharova, O. V., Astapova, M. V., Dedukhova, V. I., Chernyak, B. V., Dolgikh, D. A., Arseniev, A. S., Skulachev, V. P., and Kirpichnikov, M. P. (2005) Apoptosis, 10, 797–808.
Mott, J. L., Zhang, D., Freeman, J. C., Mikolajczak, P., Chang, S. W., and Zassenhaus, H. P. (2004) Biochem. Biophys. Res. Commun., 319, 1210–1215.
Trifunovic, A., Wredenberg, A., Falkenberg, M., Spelbrink, J. N., Rovio, A. T., Bruder, C. E., Bohlooly, Y. M., Gidlof, S., Oldfors, A., Wibom, R., Tornell, J., Jacobs, H. T., and Larsson, N. G. (2004) Nature, 429, 417–423.
Kujoth, G. C., Hiona, A., Pugh, T. D., Someya, S., Panzer, K., Wohlgemuth, S. E., Hofer, T., Seo, A. Y., Sullivan, R., Jobling, W. A., Morrow, J. D., van Remmen, H., Sedivy, J. M., Yamasoba, T., Tanokura, M., Weindruch, R., Leeuwenburgh, C., and Prolla, T. A. (2005) Science, 309, 481–484.
Harman, D. (1956) J. Gerontol., 11, 298–300.
Emanuel, N. M. (1975) Izv. AN SSSR, 785–794.
Szilard, L. (1959) PNAS, 45, 30–45.
Skulachev, V. P., and Longo V. D. (2005) Ann. N. Y. Acad. Sci., 1057, 145–164.
Szczesny, B., Tann, A. W., and Mitra, S. (2010) Mech. Ageing Develop., 131, 330–337.
Brunet-Rossinni, A. K., and Austad, S. N. (2004) Biogerontology, 5, 211–222.
Ku, H. H., Brunk, U. T., and Sohal, R. S. (1993) Free Radic. Biol. Med., 15, 621–627.
Barja, G. (1998) Ann. N. Y. Acad. Sci., 854, 224–238.
Barja, G., and Herrero, A. (2000) FASEB J., 14, 312–318.
Lambert, A. J., Boysen, H. M., Buckingham, J. A., Yang, T., Podlutsky, A., Austad, S. N., Kunz, T. H., Buffenstein, R., and Brand, M. D. (2007) Aging Cell, 6, 607–618.
Dilman, V. M. (1978) Mech. Ageing Dev., 8, 153–173.
Dilman, V. M. (1982) Large Biological Clock [in Russian], Znaniye, Moscow.
Longo, V. D., and Finch, C. E. (2003) Science, 299, 1342–1346.
Kim, E. B., Fang, X. D., Fushan, A. A., Huang, Z. Y., Lobanov, A. V., Han, L. J., Marino, S. M., Sun, X. Q., Turanov, A. A., Yang, P. C., Yim, S. H., Zhao, X., Kasaikina, M. V., Stoletzki, N., Peng, C. F., Polak, P., Xiong, Z. Q., Kiezun, A., Zhu, Y. B., Chen, Y. X., Kryukov, G. V., Zhang, Q., Peshkin, L., Yang, L., Bronson, R. T., Buffenstein, R., Wang, B., Han, C. L., Li, Q. Y., Chen, L., Zhao, W., Sunyaev, S. R., Park, T. J., Zhang, G. J., Wang, J., and Gladyshev, V. N. (2011) Nature, 479, 223–227.
Liberman, E. A., Topaly, V. P., Tsofina, L. M., Jasaitis, A. A., and Skulachev, V. P. (1969) Nature, 222, 1076–1078.
Green, D. E. (1974) Biochim. Biophys. Acta, 346, 27–78.
Liberman, E. A., and Skulachev, V. P. (1970) Biochim. Biophys. Acta, 216, 30–42.
Severin, S. Ye., Skulachev, V. P., and Yaguzhinsky, L. S. (1970) Biokhimiya, 35, 1250–1257.
Burns, R. J., Smith, R. A., and Murphy, M. P. (1995) Arch. Biochem. Biophys., 322, 60–68.
Smith, R. A., Porteous, C. M., Coulter, C. V., and Murphy, M. P. (1999) Eur. J. Biochem., 263, 709–716.
Kelso, G. F., Porteous, C. M., Coulter, C. V., Hughes, G., Porteous, W. K., Ledgerwood, E. C., Smith, R. A., and Murphy, M. P. (2001) J. Biol. Chem., 276, 4588–4596.
Murphy, M. P., and Smith, R. A. (2007) Annu. Rev. Pharmacol. Toxicol., 47, 629–656.
Antonenko, Y. N., Avetisyan, A. V., Bakeeva, L. E., Chernyak, B. V., Chertkov, V. A., Domnina, L. V., Ivanova, O. Y., Izyumov, D. S., Khailova, L. S., Klishin, S. S., Korshunova, G. A., Lyamzaev, K. G., Muntyan, M. S., Nepryakhina, O. K., Pashkovskaya, A. A., Pletjushkina, O. Y., Pustovidko, A. V., Roginsky, V. A., Rokitskaya, T. I., Ruuge, E. K., Saprunova, V. B., Severina, I. I., Simonyan, R. A., Skulachev, I. V., Skulachev, M. V., Sumbatyan, N. V., Sviryaeva, I. V., Tashlitsky, V. N., Vassiliev, J. M., Vyssokikh, M. Y., Yaguzhinsky, L. S., Zamyatnin, A. A., Jr., and Skulachev, V. P. (2008) Biochemistry (Moscow), 73, 1273–1287.
Skulachev, V. P., Anisimov, V. N., Antonenko, Y. N., Bakeeva, L. E., Chernyak, B. V., Erichev, V. P., Filenko, O. F., Kalinina, N. I., Kapelko, V. I., Kolosova, N. G., Kopnin, B. P., Korshunova, G. A., Lichinitser, M. R., Obukhova, L. A., Pasyukova, E. G., Pisarenko, O. I., Roginsky, V. A., Ruuge, E. K., Senin, I. I., Severina, I. I., Skulachev, M. V., Spivak, I. M., Tashlitsky, V. N., Tkachuk, V. A., Vyssokikh, M. Y., Yaguzhinsky, L. S., and Zorov, D. B. (2009) Biochim. Biophys. Acta, 1787, 437–461.
James, A. M., Cocheme, H. M., Smith, R. A., and Murphy, M. P. (2005) J. Biol. Chem., 280, 21295–21312.
O’Malley, Y., Fink, B. D., Ross, N. C., Prisinzano, T. E., and Sivitz, W. I. (2006) J. Biol. Chem., 281, 39766–39775.
Doughan, A. K., and Dikalov, S. I. (2007) Antioxid. Redox. Signal., 9, 1825–1836.
Kruk, J., Jemiola-Rzeminska, M., and Strzalka, K. (1997) Chem. Phys. Lipids, 87, 73–80.
Roginsky, V., Barsukova, T., Loshadkin, D., and Pliss, E. (2003) Chem. Phys. Lipids, 125, 49–58.
Skulachev, V. P. (2007) Biochemistry (Moscow), 72, 1385–1396.
Fink, B. D., Herlein, J. A., Yorek, M. A., Fenner, A. M., Kerns, R. J., and Sivitz, W. I. (2012) J. Pharm. Exp. Therap., DOI: 10.1124/jpet.112.195586.
Skulachev, V. P., Antonenko, Y. N., Cherepanov, D. A., Chernyak, B. V., Izyumov, D. S., Khailova, L. S., Klishin, S. S., Korshunova, G. A., Lyamzaev, K. G., Pletjushkina, O. Y., Roginsky, V. A., Rokitskaya, T. I., Severin, F. F., Severina, I. I., Simonyan, R. A., Skulachev, M. V., Sumbatyan, N. V., Sukhanova, E. I., Tashlitsky, V. N., Trendeleva, T. A., Vyssokikh, M. Y., and Zvyagilskaya, R. A. (2010) Biochim. Biophys. Acta, 1797, 878–889.
Roginsky, V. A., Tashlitsky, V. N., and Skulachev, V. P. (2009) Aging (Albany, NY), 1, 481–489.
Skulachev, M. V., Antonenko, Y. N., Anisimov, V. N., Chernyak, B. V., Cherepanov, D. A., Chistyakov, V. A., Egorov, M. V., Kolosova, N. G., Korshunova, G. A., Lyamzaev, K. G., Plotnikov, E. Y., Roginsky, V. A., Savchenko, A. Y., Severina, I. I., Severin, F. F., Shkurat, T. P., Tashlitsky, V. N., Shidlovsky, K. M., Vyssokikh, M. Y., Zamyatnin, A. A., Zorov, D. B., and Skulachev, V. P. (2011) Curr. Drug Targets, 12, 800–826.
Severin, F. F., Severina, I. I., Antonenko, Y. N., Rokitskaya, T. I., Cherepanov, D. A., Mokhova, E. N., Vyssokikh, M. Y., Pustovidko, A. V., Markova, O. V., Yaguzhinsky, L. S., Korshunova, G. A., Sumbatyan, N. V., Skulachev, M. V., and Skulachev, V. P. (2010) PNAS, 107, 663–668.
Anisimov, V. N., Egorov, M. V., Krasilshchikova, M. S., Lyamzaev, K. G., Manskikh, V. N., Moshkin, M. P., Novikov, E. A., Popovich, I. G., Rogovin, K. A., Shabalina, I. G., Shekarova, O. N., Skulachev, M. V., Titova, T. V., Vygodin, V. A., Vyssokikh, M. Y., Yurova, M. N., Zabezhinsky, M. A., and Skulachev, V. P. (2011) Aging (Albany NY), 3, 1110–1119.
Anisimov, V. N., Bakeeva, L. E., Egormin, P. A., Filenko, O. F., Isakova, E. F., Manskikh, V. N., Mikhelson, V. M., Panteleeva, A. A., Pasyukova, E. G., Pilipenko, D. I., Piskunova, T. S., Popovich, I. G., Roshchina, N. V., Rybina, O. Y., Saprunova, V. B., Samoylova, T. A., Semenchenko, A. V., Skulachev, M. V., Spivak, I. M., Tsybul’ko, E. A., Tyndyk, M. L., Vyssokikh, M. Y., Yurova, M. N., Zabezhinsky, M. A., and Skulachev, V. P. (2008) Biochemistry (Moscow), 73, 1329–1342.
Stefanova, N. A., Fursova, A., and Kolosova, N. G. (2010) J. Alzheimer’s Dis., 21, 479–491.
Skulachev, V. P. (2012) J. Alzheimer’s Dis., 28, 283–289.
Neroev, V. V., Archipova, M. M., Bakeeva, L. E., Fursova, A., Grigorian, E. N., Grishanova, A. Y., Iomdina, E. N., Ivashchenko, Zh. N., Katargina, L. A., Khoroshilova-Maslova, I. P., Kilina, O. V., Kolosova, N. G., Kopenkin, E. P., Korshunov, S. S., Kovaleva, N. A., Novikova, Y. P., Philippov, P. P., Pilipenko, D. I., Robustova, O. V., Saprunova, V. B., Senin, I. I., Skulachev, M. V., Sotnikova, L. F., Stefanova, N. A., Tikhomirova, N. K., Tsapenko, I. V., Shchipanova, A. I., Zinovkin, R. A., and Skulachev, V. P. (2008) Biochemistry (Moscow), 73, 1317–1328.
Bakeeva, L. E., Barskov, I. V., Egorov, M. V., Isaev, N. K., Kapelko, V. I., Kazachenko, A. V., Kirpatovsky, V. I., Kozlovsky, S. V., Lakomkin, V. L., Levina, S. B., Pisarenko, O. I., Plotnikov, E. Y., Saprunova, V. B., Serebryakova, L. I., Skulachev, M. V., Stelmashook, E. V., Studneva, I. M., Tskitishvili, O. V., Vasilyeva, A. K., Victorov, I. V., Zorov, D. B., and Skulachev, V. P. (2008) Biochemistry (Moscow), 73, 1288–1299.
Plotnikov, E. Y., Silachev, D. N., Chupyrkina, A. A., Danshina, M. I., Jankauskas, S. S., Morosanova, M. A., Stelmashook, E. V., Vasileva, A. K., Goryacheva, E. S., Pirogov, Y. A., Isaev, N. K., and Zorov, D. B. (2010) Biochemistry (Moscow), 75, 145–150.
Plotnikov, E. Y., Chupyrkina, A. A., Jankauskas, S. S., Pevzner, I. B., Silachev, D. N., Skulachev, V. P., and Zorov, D. B. (2011) Biochim. Biophys. Acta, 1812, 77–86.
Zorov, D. B., Plotnikov, E. Y., Yankauskas, S. S., Isaev, N. K., Silachev, D. N., Zorova, L. D., Pevzner, I. B., Pul’kova, N. V., Zorov, S. D., and Morosanova, M. A. (2012) Biochemistry (Moscow), 77, 742–753.
Agapova, L. S., Chernyak, B. V., Domnina, L. V., Dugina, V. B., Efimenko, A. Y., Fetisova, E. K., Ivanova, O. Y., Kalinina, N. I., Khromova, N. V., Kopnin, B. P., Kopnin, P. B., Korotetskaya, M. V., Lichinitser, M. R., Lukashev, A. L., Pletjushkina, O. Y., Popova, E. N., Skulachev, M. V., Shagieva, G. S., Stepanova, E. V., Titova, E. V., Tkachuk, V. A., Vasiliev, J. M., and Skulachev, V. P. (2008) Biochemistry (Moscow), 73, 1300–1316.
Sommer, S. S. (1994) Hum. Mutat., 3, 166–169.
Manskikh, V. N. (2004) Essays on Evolutionary Oncology [in Russian], SibGMU, Tomsk.
Lihtenstein, A. V. (2005) Biochemistry (Moscow), 70, 1055–1064.
Manskikh, V. N. (2009) Ros. Khim. Zh. (Russ.), LIII, 57–63.
MacCay, C. M., and Crowell, M. F. (1934) Sci. Mon., 39, 405–414.
MacCay, C. M., Crowell, M. F., and Maynard, L. A. (1935) J. Nutr., 10, 63–79.
MacCay, C. M., Maynard, L. A., and Barnes, L. L. (1943) Arch. Biochem., 2, 469–479.
Robertson, T. B., Marston, R., and Walters, J. W. (1934) Aust. J. Exp. Biol. Med. Sci., 12, 33.
Will, L. C., and MacCay, C. M. (1943) Arch. Biochem., 2, 481–484.
Mair, W., Goymer, P., Pletcher, S. D., and Partridge, L. (2003) Science, 301, 1731–1733.
Libert, S., and Pletcher, S. D. (2007) Cell, 131, 1231–1234.
Libert, S., Zwiener, J., Chu, X., Vanvoorhies, W., Roman, G., and Pletcher, S. D. (2007) Science, 315, 1133–1137.
Carr, C. J., King, J. T., and Visscher, B. (1949) Proc. Fedn. Am. Soc. Exp. Biol., 8, 22.
Stuchlikova, E., Juricova-Horakova, M., and Deyl, Z. (1975) Exp. Gerontol., 10, 141–144.
Richie, J. P., Jr., Leutzinger, Y., Parthasarathy, S., Malloy, V., Orentreich, N., and Zimmerman, J. A. (1994) FASEB J., 8, 1302–1307.
Miller, R. A., Buehner, G., Chang, Y., Harper, J. M., Sigler, R., and Smith-Wheelock, M. (2005) Aging Cell, 4, 119–125.
Sanz, A., Caro, P., Ayala, V., Portero-Otin, M., Pamplona, R., and Barja, G. (2006) FASEB J., 20, 1064–1073.
Caro, P., Gomez, J., Sanchez, I., Garcia, R., Lopez-Torres, M., Naudi, A., Portero-Otin, M., Pamplona, R., and Barja, G. (2009) Biogerontology, 10, 579–592.
Edman, U., Garcia, A. M., Busuttil, R. A., Sorensen, D., Lundell, M., Kapahi, P., and Vijg, J. (2009) Aging Cell, 8, 331–338.
Skulachev, V. P. (2011) Aging (Albany, NY), 3, 1045–1050.
Colman, R. J., Anderson, R. M., Johnson, S. C., Kastman, E. K., Kosmatka, K. J., Beasley, T. M., Allison, D. B., Cruzen, C., Simmons, H. A., Kemnitz, J. W., and Weindruch, R. (2009) Science, 325, 201–204.
Sun, D., Muthukumar, A. R., Lawrence, R. A., and Fernandes, G. (2001) Clin. Diagn. Lab. Immunol., 8, 1003–1011.
Gardner, E. M. (2005) J. Gerontol. A. Biol. Sci. Med. Sci., 60, 688–694.
Obukhova, L. A., Skulachev, V. P., and Kolosova, N. G. (2009) Aging (Albany NY), 1, 389–401.
Demianenko, I. A., Vasilieva, T. V., Domnina, L. V., Dugina, V. B., Yegorov, M. V., Ivanova, O. Yu., Ilinskaya, O. P., Pletiushkina, O. Yu., Popova, E. N., Saharov, I. Yu., Fedorov, A. V., and Chernyak, B. V. (2010) Biochemistry (Moscow), 75, 274–280.
Hopkin, K. (2003) Sci. Aging Knowledge Environ., 2003, NS4.
Hamilton, W. D. (1964) J. Theor. Biol., 7, 1–16.
Hamilton, W. D. (1964) J. Theor. Biol., 7, 17–52.
Dawkins, R. (2010) Extended Phenotype. Long Arm of the Gene [Russian translation], Astrel, Moscow.
Eng, P. M., Rimm, E. B., Fitzmaurice, G., and Kawachi, I. (2002) Am. J. Epidemiol., 155, 700–709.
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Original Russian Text © V. P. Skulachev, 2012, published in Biokhimiya, 2012, Vol. 77, No. 7, pp. 827–846.
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Skulachev, V.P. What is “phenoptosis” and how to fight it?. Biochemistry Moscow 77, 689–706 (2012). https://doi.org/10.1134/S0006297912070012
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DOI: https://doi.org/10.1134/S0006297912070012