Abstract
Programmed cell death (PCD)is a major component of normal development, preservation of tissue homeostasis, and elimination of damaged cells. Many studies have subdivided PCD into the three categories of apoptosis, autophagy, and necrosis based on criteria such as morphological alterations, initiating death signal, or the implication of caspases. However, these classifications fail to address the interplay between the three types of PCD. In this review, we will discuss the central role of the mitochondrion in the integration of the cell death pathways. Mitochondrial alterations such as the release of sequestered apoptogenic proteins, loss of transmembrane potential, production of reactive oxygen species (ROS), disruption of the electron transport chain, and decreases in ATP synthesis have been shown to be involved in, and possibly responsible for, the different manifestations of cell death. Thus, the mitochondria can be viewed as a central regulator of the decision between cellular survival and demise.
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Abbreviations
- AIF:
-
apoptosis inducing factor
- BH:
-
Bcl-2 homology domain
- HtrA2:
-
high temperature requirement protein A2
- OPA1:
-
optic atrophy type 1 protein
- Smac/DIABLO:
-
second mitochondria derived activator of caspase/direct IAP binding protein with low pI
- TNF:
-
tumor necrosis factor
- TRAIL:
-
TNF related apoptosis inducing ligand
- XIAP:
-
X-linked inhibitor of apoptosis
REFERENCES
Clarke, P. G., and Clarke, S. (1995) Nature, 378, 230.
Virchow, R. (1871) Die Cellularpathologie in ihrer Begrundung auf physiologische Gewebelehre, 4, Auflage. Hirschwald, Berlin.
Glucksmann, A. (1951) Biol. Rev. Cambridge Phil. Soc., 26, 59–86.
Saunders, J. W. (1966) Science, 154, 604–612.
Lockshin, R. A., and Williams, C. M. (1964) J. Insect Physiol., 10, 643–649.
Lockshin, R. A., and Williams, C. M. (1965) J. Insect Physiol., 11, 123–133.
Kerr, J. F. R., Wyllie, A. H., and Currie, A. R. (1972) Br. J. Cancer, 26, 239–257.
Jaattela, M. (2004) Oncogene, 23, 2746–2756.
Bursch, W., Ellinger, A., Gerner, C. H., Frohwein, U., and Schulte Hermann, R. (2000) Ann. NY Acad. Sci., 926, 1–12.
Ferri, K. F., and Kroemer, G. (2001) Nat. Cell Biol., 3, E255–263.
Clarke, P. G. H. (1990) Anat. Embryol., 181, 195–213.
Schweichel, J. U., and Merker, H. J. (1973) Teratology, 7, 253–266.
Ogier Denis, E., and Codogno, P. (2003) Biochim. Biophys. Acta, 1603, 113–128.
Jacobsen, J., and Duchen, M. R. (2001) Cell Death Diff., 8, 963–966.
Scorrano, L., Ashiya, M., Buttle, K., Weiler, S., Oakes, S. A., Mannella, C. A., and Korsmeyer, S. J. (2002) Dev. Cell., 2, 55–67.
Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. (1996) Cell, 86, 147–157.
Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. (1997) Cell, 91, 479–489.
Zou, H., Henzel, W. J., Liu, X., Lutschg, A., and Wang, X. (1997) Cell, 90, 405–413.
Cain, K., Brown, D. G., Langlais, C., and Cohen, G. M. (1999) J. Biol. Chem., 274, 22686–22692.
Cain, K., Bratton, S. B., Langlais, C., Walker, G., Brown, D. G., Sun, X. M., and Cohen, G. M. (2000) J. Biol. Chem., 275, 6067–6070.
Acehan, D., Jiang, X., Morgan, D. G., Heuser, J. E., Wang, X., and Akey, C. W. (2002) Mol. Cell., 9, 423–432.
Slee, E. A., Harte, M. T., Kluck, R. M., Wolf, B. B., Casiano, C. A., Newmeyer, D. D., Wang, H. G., Reed, J. C., Nicholson, D. W., Alnemri, E. S., Green, D. R., and Martin, S. J. (1999) J. Cell Biol., 144, 281–292.
Van de Craen, M., Declercq, W., van den brande, I., Fiers, W., and Vandenabeele, P. (1999) Cell Death Diff., 6, 1117–1124.
Bratton, S. B., Walker, G., Srinivasula, S. M., Sun, X. M., Butterworth, M., Alnemri, E. S., and Cohen, G. M. (2001) EMBO J., 20, 998–1009.
Verhagen, A. M., Ekert, P. G., Pakusch, M., Silke, J., Connolly, L. M., Reid, G. E., Moritz, R. L., Simpson, R. J., and Vaux, D. L. (2000) Cell, 102, 43–53.
Du, C., Fang, M., Li, Y., Li, L., and Wang, X. (2000) Cell, 102, 33–42.
Suzuki, Y., Imai, Y., Nakayama, H., Takahashi, K., Takio, K., and Takahashi, R. (2001) Mol. Cell, 8, 613–621.
Verhagen, A. M., Silke, J., Ekert, P. G., Pakusch, M., Kaufmann, H., Connolly, L. M., Day, C. L., Tikoo, A., Burke, R., Wrobel, C., Moritz, R. L., Simpson, R. J., and Vaux, D. L. (2002) J. Biol. Chem., 277, 445–454.
Van Loo, G., van Gurp, M., Depuydt, B., Srinivasula, S. M., Rodriguez, I., Alnemri, E. S., Gevaert, K., Vandekerckhove, J., Declercq, W., and Vandenabeele, P. (2002) Cell Death Differ., 9, 20–26.
Blink, E., Maianski, N. A., Alnemri, E. S., Zervos, A. S., Roos, D., and Kuijpers, T. W. (2004) Cell Death Differ., 8, 937–939.
Li, W., Srinivasula, S. M., Chai, J., Li, P., Wu, J. W., Zhang, Z., Alnemri, E. S., and Shi, Y. (2002) Nat. Struct. Biol., 9, 436–441.
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., and Kroemer, G. (1999) Nature, 397, 441–446.
Susin, S. A., Daugas, E., Ravagnan, L., Samejima, K., Zamzami, N., Loeffler, M., Costantini, P., Ferri, K. F., Irinopoulou, T., Prevost, M. C., Brothers, G., Mak, T. W., Penninger, J., Earnshaw, W. C., and Kroemer, G. (2000) J. Exp. Med., 192, 571–580.
Li, L. Y., Luo, X., and Wang, X. (2001) Nature, 412, 95–99.
Widlak, P., Li, L. Y., Wang, X., and Garrard, W. T. (2001) J. Biol. Chem., 276, 48404–48409.
Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A., and Nagata, S. (1998) Nature, 391, 43–50.
Kim, J. S., He, L., and Lemasters, J. J. (2003) Biochem. Biophys. Res. Commun., 304, 463–470.
Belzacq, A. S., Vieira, H. L., Kroemer, G., and Brenner, C. (2002) Biochimie, 84, 167–176.
Zamzami, N., Susin, S. A., Marchetti, P., Hirsch, T., Gomez Monterrey, I., Castedo, M., and Kroemer, G. (1996) J. Exp. Med., 183, 1533–1544.
Marzo, I., Brenner, C., Zamzami, N., Jurgensmeier, J. M., Susin, S. A., Vieira, H. L., Prevost, M. C., Xie, Z., Matsuyama, S., Reed, J. C., and Kroemer, G. (1998) Science, 281, 2027–2031.
Shimizu, S., Narita, M., and Tsujimoto, Y. (1999) Nature, 399, 483–487.
Rostovtseva, T. K., Antonsson, B., Suzuki, M., Youle, R. J., Colombini, M., and Bezrukov, S. M. (2004) J. Biol. Chem., 279, 13575–13583.
Borner, C., Martinou, I., Mattmann, C., Irmler, M., Schaerer, E., Martinou, J. C., and Tschopp, J. (1994) J. Cell Biol., 126, 1059–1068.
Hanada, M., Aime Sempe, C., Sato, T., and Reed, J. C. (1995) J. Biol. Chem., 270, 11962–11969.
Hunter, J. J., Bond, B. L., and Parslow, T. G. (1996) Mol. Cell. Biol., 16, 877–883.
Huang, D. C., Adams, J. M., and Cory, S. (1998) EMBO J., 17, 1029–1039.
Shimizu, S., Konishi, A., Kodama, T., and Tsujimoto, Y. (2000) Proc. Natl. Acad. Sci. USA, 97, 3100–3105.
Shimizu, S., Ide, T., Yanagida, T., and Tsujimoto, Y. (2000) J. Biol. Chem., 275, 12321–12325.
Muchmore, S. W., Sattler, M., Liang, H., Meadows, R. P., Harlan, J. E., Yoon, H. S., Nettesheim, D., Chang, B. S., Thompson, C. B., Wong, S. L., Ng, S. L., and Fesik, S. W. (1996) Nature, 381, 335–341.
Sattler, M., Liang, H., Nettesheim, D., Meadows, R. P., Harlan, J. E., Eberstadt, M., Yoon, H. S., Shuker, S. B., Chang, B. S., Minn, A. J., Thompson, C. B., and Fesik, S. W. (1997) Science, 275, 983–986.
Minn, A. J., Velez, P., Schendel, S. L., Liang, H., Muchmore, S. W., Fesik, S. W., Fill, M., and Thompson, C. B. (1997) Nature, 385, 353–357.
Antonsson, B., Conti, F., Ciavatta, A., Montessuit, S., Lewis, S., Martinou, I., Bernasconi, L., Bernard, A., Mermod, J. J., Mazzei, G., Maundrell, K., Gambale, F., Sadoul, R., and Martinou, J. C. (1997) Science, 277, 370–372.
Schlesinger, P. H., Gross, A., Yin, X. M., Yamamoto, K., Saito, M., Waksman, G., and Korsmeyer, S. J. (1997) Proc. Natl. Acad. Sci. USA, 94, 11357–11362.
Schendel, S. L., Xie, Z., Montal, M. O., Matsuyama, S., Montal, M., and Reed, J. C. (1997) Proc. Natl. Acad. Sci. USA, 94, 5113–5118.
Schendel, S. L., Azimov, R., Pawlowski, K., Godzik, A., Kagan, B. L., and Reed, J. C. (1999) J. Biol. Chem., 274, 21932–21936.
Eskes, R., Desagher, S., Antonsson, B., and Martinou, J. C. (2000) Mol. Cell Biol., 20, 929–935.
Wei, M. C., Lindsten, T., Mootha, V. K., Weiler, S., Gross, A., Ashiya, M., Thompson, C. B., and Korsmeyer, S. J. (2000) Genes Dev., 14, 2060–2071.
Korsmeyer, S. J. (1999) Cancer Res., 59, 1693s–1700s.
Scorrano, L., and Korsmeyer, S. J. (2003) Biochem. Biophys. Res. Commun., 304, 437–444.
Murphy, K. M., Streips, U. N., and Lock, R. B. (2000) J. Biol. Chem., 275, 17225–17228.
Mikhailov, V., Mikhailova, M., Pulkrabek, D. J., Dong, Z., Venkatachalam, M. A., and Saikumar, P. (2001) J. Biol. Chem., 276, 18361–18374.
Kuwana, T., Mackey, M. R., Perkins, G., Ellisman, M. H., Latterich, M., Schneiter, R., Green, D. R., and Newmeyer, D. D. (2002) Cell, 111, 331–342.
May, P., and May, E. (1999) Oncogene, 18, 7621–7636.
Bourdon, J. C., Laurenzi, V. D., Melino, G., and Lane, D. (2003) Cell Death Differ., 10, 397–399.
Schuler, M., and Green, D. R. (2001) Biochem. Soc. Trans., 29, 684–688.
Chipuk, J. E., Kuwana, T., Bouchier Hayes, L., Droin, N. M., Newmeyer, D. D., Schuler, M., and Green, D. R. (2004) Science, 303, 1010–1014.
Petrosillo, G., Ruggiero, F. M., and Paradies, G. (2003) FASEB J., 17, 2202–2208.
Ott, M., Robertson, J. D., Gogvadze, V., Zhivotovsky, B., and Orrenius, S. (2002) Proc. Natl. Acad. Sci. USA, 99, 1259–1263.
Karbowski, M., and Youle, R. J. (2003) Cell Death Differ., 10, 870–880.
Bossy Wetzel, E., Barsoum, M. J., Godzik, A., Schwarzenbacher, R., and Lipton, S. A. (2003) Curr. Opin. Cell Biol., 15, 706–716.
Praefcke, G. J., and McMahon, H. T. (2004) Nat. Rev. Mol. Cell Biol., 5, 133–147.
Smirnova, E., Griparic, L., Shurland, D. L., and van der Bliek, A. M. (2001) Mol. Biol. Cell, 12, 2245–2256.
Griparic, L., van der Wel, N. N., Orozco, I. J., Peters, P. J., and van der Bliek, A. M. (2004) J. Biol. Chem., 279, 18792–18798.
Olichon, A., Baricault, L., Gas, N., Guillou, E., Valette, A., Belenguer, P., and Lenaers, G. (2003) J. Biol. Chem., 278, 7743–7746.
Frank, S., Gaume, B., Bergmann Leitner, E. S., Leitner, W. W., Robert, E. G., Catez, F., Smith, C. L., and Youle, R. J. (2001) Dev. Cell., 1, 515–525.
Hirsch, T., Susin, S. A., Marzo, I., Marchetti, P., Zamzami, N., and Kroemer, G. (1998) Cell. Biol. Toxicol., 14, 141–145.
Ricci, J. E., Waterhouse, N., and Green, D. R. (2003) Cell Death Differ., 10, 488–492.
Fleury, C., Mignotte, B., and Vayssiere, J. L. (2002) Biochimie, 842, 131–141.
Saybasili, H., Yuksel, M., Haklar, G., and Yalcin, A. S. (2001) Antioxid. Redox Signal., 3, 1099–1104.
Bergamini, C. M., Gambetti, S., Dondi, A., and Cervellati, C. (2004) Curr. Pharm. Des., 10, 1611–1626.
Huang, P., Feng, L., Oldham, E. A., Keating, M. J., and Plunkett, W. (2000) Nature, 407, 390–395.
Roue, G., Bitton, N., Yuste, V. J., Montange, T., Rubio, M., Dessauge, F., Delettre, C., Merle Beral, H., Sarfati, M., and Susin, S. A. (2003) Biochimie, 85, 741–746.
Manna, P. P., and Frazier, W. A. (2004) Cancer Res., 64, 1026–1036.
Mate, M. J., Ortiz Lombardia, M., Boitel, B., Haouz, A., Tello, D., Susin, S. A., Penninger, J., Kroemer, G., and Alzari, P. M. (2002) Nat. Struct. Biol., 9, 442–446.
Ye, H., Cande, C., Stephanou, N. C., Jiang, S., Gurbuxani, S., Larochette, N., Daugas, E., Garrido, C., Kroemer, G., and Wu, H. (2002) Nat. Struct. Biol., 9, 680–684.
Miramar, M. D., Costantini, P., Ravagnan, L., Saraiva, L. M., Haouzi, D., Brothers, G., Penninger, J. M., Peleato, M. L., Kroemer, G., and Susin, S. A. (2001) J. Biol. Chem., 276, 16391–16398.
Klein, J. A., Longo Guess, C. M., Rossmann, M. P., Seburn, K. L., Hurd, R. E., Frankel, W. N., Bronson, R. T., and Ackerman, S. L. (2002) Nature, 419, 367–374.
Lipton, S. A., and Bossy Wetzel, E. (2002) Cell, 111, 147–150.
Pelicano, H., Feng, L., Zhou, Y., Carew, J. S., Hileman, E. O., Plunkett, W., Keating, M. J., and Huang, P. (2003) J. Biol. Chem., 278, 37832–37839.
Ricci, J. E., Munoz Pinedo, C., Fitzgerald, P., Bailly Maitre, B., Perkins, G. A., Yadava, N., Scheffler, I. E., Ellisman, M. H., and Green, D. R. (2004) Cell, 117, 773–786.
Izyumov, D. S., Avetisyan, A. V., Pletjushkina, O. Y., Sakharov, D. V., Wirtz, K. W., Chernyak, B. V., and Skulachev, V. P. (2004) Biochim. Biophys. Acta, 1658, 141–147.
Leist, M., Single, B., Castoldi, A. F., Kuhnle, S., and Nicotera, P. (1997) J. Exp. Med., 185, 1481–1486.
Formigli, L., Papucci, L., Tani, A., Schiavone, N., Tempestini, A., Orlandini, G. E., Capaccioli, S., and Orlandini, S. Z. (2000) J. Cell. Phys., 182, 41–49.
Danial, N. N., Gramm, C. F., Scorrano, L., Zhang, C. Y., Krauss, S., Ranger, A. M., Datta, S. R., Greenberg, M. E., Licklider, L. J., Lowell, B. B., Gygi, S. P., and Korsmeyer, S. J. (2003) Nature, 424, 952–956.
Plomp, P. J., Gordon, P. B., Meijer, A. J., Hoyvik, H., and Seglen, P. O. (1989) J. Biol. Chem., 264, 6699–6704.
Seglen, P. O., and Bohley, P. (1992) Experientia, 48, 158–172.
Paglin, S., Hollister, T., Delohery, T., Hackett, N., McMahill, M., Sphicas, E., Domingo, D., and Yahalom, J. (2001) Cancer Res., 61, 439–444.
Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. (1999) Nature, 402, 672–676.
Yanagisawa, H., Miyashita, T., Nakano, Y., and Yamamoto, D. (2003) Cell Death Differ., 10, 798–807.
Priault, M., Camougrand, N., Kinnally, K. W., Vallette, F. M., and Manon, S. (2003) FEMS Yeast Res., 4, 15–27.
Guimaraes, C. A., and Linden, R. (2004) Eur. J. Biochem., 271, 1638–1650.
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., and Herman, B. (1998) Biochim. Biophys. Acta, 1366, 177–196.
Burlacu, A., Jinga, V., Gafencu, A. V., and Simionescu, M. (2001) Cell Tissue Res., 306, 409–416.
Seoane, A., Dememes, D., and Llorens, J. (2001) J. Comp. Neurol., 439, 385–399.
Kawahara, A., Ohsawa, Y., Matsumura, H., Uchiyama, Y., and Nagata, S. (1998) J. Cell Biol., 143, 1353–1360.
Shimizu, S., Eguchi, Y., Kamiike, W., Waguri, S., Uchiyama, Y., Matsuda, H., and Tsujimoto, Y. (1996) Oncogene, 12, 2045–2050.
Vande Velde, C., Cizeau, J., Dubik, D., Alimonti, J., Brown, T., Israels, S., Hakem, R., and Greenberg, A. H. (2000) Mol. Cell. Biol., 20, 5454–5468.
Oppenheim, R. W., Flavell, R. A., Vinsant, S., Prevette, D., Kuan, C. Y., and Rakic, P. (2001) J. Neurosci., 21, 4752–4760.
Bauvy, C., Gane, P., Arico, S., Codogno, P., and Ogier Denis, E. (2001) Exp. Cell Res., 268, 139–149.
Mills, K. R., Reginato, M., Debnath, J., Queenan, B., and Brugge, J. S. (2004) Proc. Natl. Acad. Sci. USA, 101, 3438–3443.
Jia, L., Dourmashkin, R. R., Allen, P. D., Gray, A. B., Newland, A. C., and Kelsey, S. M. (1997) Br. J. Haematol., 98, 673–685.
Bursch, W., Ellinger, A., Kienzl, H., Torok, L., Pandey, S., Sikorska, M., Walker, R., and Hermann, R. S. (1996) Carcinogenesis, 17, 1595–1607.
Inbal, B., Bialik, S., Sabanay, I., Shani, G., and Kimchi, A. (2002) J. Cell Biol., 157, 455–468.
Marsden, V. S., O ‘Connor, L., O ‘Reilly, L. A., Silke, J., Metcalf, D., Ekert, P. G., Huang, D. C., Cecconi, F., Kuida, K., Tomaselli, K. J., Roy, S., Nicholson, D. W., Vaux, D. L., Bouillet, P., Adams, J. M., and Strasser, A. (2002) Nature, 419, 634–637.
Cory, S., Huang, D. C., and Adams, J. M. (2003) Oncogene, 22, 8590–8607.
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Translated from Biokhimiya, Vol. 70, No. 2, 2005, pp. 284 293.
Original Russian Text Copyright ¢ 2005 by Bras, Queenan, Susin.
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Bras, M., Queenan, B. & Susin, S.A. Programmed cell death via mitochondria: Different modes of dying. Biochemistry (Moscow) 70, 231–239 (2005). https://doi.org/10.1007/s10541-005-0105-4
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DOI: https://doi.org/10.1007/s10541-005-0105-4