Skip to main content
SpringerLink
Log in

Programmed cell death via mitochondria: Different modes of dying

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

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

  1. Clarke, P. G., and Clarke, S. (1995) Nature, 378, 230.

    PubMed  CAS  Google Scholar 

  2. Virchow, R. (1871) Die Cellularpathologie in ihrer Begrundung auf physiologische Gewebelehre, 4, Auflage. Hirschwald, Berlin.

  3. Glucksmann, A. (1951) Biol. Rev. Cambridge Phil. Soc., 26, 59–86.

    Article  Google Scholar 

  4. Saunders, J. W. (1966) Science, 154, 604–612.

    PubMed  Google Scholar 

  5. Lockshin, R. A., and Williams, C. M. (1964) J. Insect Physiol., 10, 643–649.

    CAS  Google Scholar 

  6. Lockshin, R. A., and Williams, C. M. (1965) J. Insect Physiol., 11, 123–133.

    PubMed  CAS  Google Scholar 

  7. Kerr, J. F. R., Wyllie, A. H., and Currie, A. R. (1972) Br. J. Cancer, 26, 239–257.

    PubMed  CAS  Google Scholar 

  8. Jaattela, M. (2004) Oncogene, 23, 2746–2756.

    PubMed  Google Scholar 

  9. Bursch, W., Ellinger, A., Gerner, C. H., Frohwein, U., and Schulte Hermann, R. (2000) Ann. NY Acad. Sci., 926, 1–12.

    Article  PubMed  CAS  Google Scholar 

  10. Ferri, K. F., and Kroemer, G. (2001) Nat. Cell Biol., 3, E255–263.

    PubMed  CAS  Google Scholar 

  11. Clarke, P. G. H. (1990) Anat. Embryol., 181, 195–213.

    PubMed  CAS  Google Scholar 

  12. Schweichel, J. U., and Merker, H. J. (1973) Teratology, 7, 253–266.

    Google Scholar 

  13. Ogier Denis, E., and Codogno, P. (2003) Biochim. Biophys. Acta, 1603, 113–128.

    PubMed  CAS  Google Scholar 

  14. Jacobsen, J., and Duchen, M. R. (2001) Cell Death Diff., 8, 963–966.

    Google Scholar 

  15. Scorrano, L., Ashiya, M., Buttle, K., Weiler, S., Oakes, S. A., Mannella, C. A., and Korsmeyer, S. J. (2002) Dev. Cell., 2, 55–67.

    PubMed  CAS  Google Scholar 

  16. Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. (1996) Cell, 86, 147–157.

    PubMed  CAS  Google Scholar 

  17. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. (1997) Cell, 91, 479–489.

    PubMed  CAS  Google Scholar 

  18. Zou, H., Henzel, W. J., Liu, X., Lutschg, A., and Wang, X. (1997) Cell, 90, 405–413.

    PubMed  CAS  Google Scholar 

  19. Cain, K., Brown, D. G., Langlais, C., and Cohen, G. M. (1999) J. Biol. Chem., 274, 22686–22692.

    PubMed  CAS  Google Scholar 

  20. 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.

    PubMed  CAS  Google Scholar 

  21. Acehan, D., Jiang, X., Morgan, D. G., Heuser, J. E., Wang, X., and Akey, C. W. (2002) Mol. Cell., 9, 423–432.

    PubMed  CAS  Google Scholar 

  22. 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.

    PubMed  CAS  Google Scholar 

  23. Van de Craen, M., Declercq, W., van den brande, I., Fiers, W., and Vandenabeele, P. (1999) Cell Death Diff., 6, 1117–1124.

    Google Scholar 

  24. 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.

    PubMed  CAS  Google Scholar 

  25. 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.

    PubMed  CAS  Google Scholar 

  26. Du, C., Fang, M., Li, Y., Li, L., and Wang, X. (2000) Cell, 102, 33–42.

    PubMed  CAS  Google Scholar 

  27. Suzuki, Y., Imai, Y., Nakayama, H., Takahashi, K., Takio, K., and Takahashi, R. (2001) Mol. Cell, 8, 613–621.

    PubMed  CAS  Google Scholar 

  28. 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.

    PubMed  CAS  Google Scholar 

  29. 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.

    PubMed  Google Scholar 

  30. Blink, E., Maianski, N. A., Alnemri, E. S., Zervos, A. S., Roos, D., and Kuijpers, T. W. (2004) Cell Death Differ., 8, 937–939.

    Google Scholar 

  31. 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.

    PubMed  CAS  Google Scholar 

  32. 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.

    PubMed  CAS  Google Scholar 

  33. 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.

    PubMed  CAS  Google Scholar 

  34. Li, L. Y., Luo, X., and Wang, X. (2001) Nature, 412, 95–99.

    PubMed  CAS  Google Scholar 

  35. Widlak, P., Li, L. Y., Wang, X., and Garrard, W. T. (2001) J. Biol. Chem., 276, 48404–48409.

    PubMed  CAS  Google Scholar 

  36. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A., and Nagata, S. (1998) Nature, 391, 43–50.

    PubMed  CAS  Google Scholar 

  37. Kim, J. S., He, L., and Lemasters, J. J. (2003) Biochem. Biophys. Res. Commun., 304, 463–470.

    PubMed  CAS  Google Scholar 

  38. Belzacq, A. S., Vieira, H. L., Kroemer, G., and Brenner, C. (2002) Biochimie, 84, 167–176.

    PubMed  CAS  Google Scholar 

  39. Zamzami, N., Susin, S. A., Marchetti, P., Hirsch, T., Gomez Monterrey, I., Castedo, M., and Kroemer, G. (1996) J. Exp. Med., 183, 1533–1544.

    PubMed  CAS  Google Scholar 

  40. 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.

    PubMed  CAS  Google Scholar 

  41. Shimizu, S., Narita, M., and Tsujimoto, Y. (1999) Nature, 399, 483–487.

    PubMed  CAS  Google Scholar 

  42. Rostovtseva, T. K., Antonsson, B., Suzuki, M., Youle, R. J., Colombini, M., and Bezrukov, S. M. (2004) J. Biol. Chem., 279, 13575–13583.

    PubMed  CAS  Google Scholar 

  43. Borner, C., Martinou, I., Mattmann, C., Irmler, M., Schaerer, E., Martinou, J. C., and Tschopp, J. (1994) J. Cell Biol., 126, 1059–1068.

    PubMed  CAS  Google Scholar 

  44. Hanada, M., Aime Sempe, C., Sato, T., and Reed, J. C. (1995) J. Biol. Chem., 270, 11962–11969.

    PubMed  CAS  Google Scholar 

  45. Hunter, J. J., Bond, B. L., and Parslow, T. G. (1996) Mol. Cell. Biol., 16, 877–883.

    PubMed  CAS  Google Scholar 

  46. Huang, D. C., Adams, J. M., and Cory, S. (1998) EMBO J., 17, 1029–1039.

    PubMed  CAS  Google Scholar 

  47. Shimizu, S., Konishi, A., Kodama, T., and Tsujimoto, Y. (2000) Proc. Natl. Acad. Sci. USA, 97, 3100–3105.

    PubMed  CAS  Google Scholar 

  48. Shimizu, S., Ide, T., Yanagida, T., and Tsujimoto, Y. (2000) J. Biol. Chem., 275, 12321–12325.

    PubMed  CAS  Google Scholar 

  49. 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.

    PubMed  CAS  Google Scholar 

  50. 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.

    PubMed  CAS  Google Scholar 

  51. 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.

    PubMed  CAS  Google Scholar 

  52. 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.

    PubMed  CAS  Google Scholar 

  53. 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.

    PubMed  CAS  Google Scholar 

  54. 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.

    PubMed  CAS  Google Scholar 

  55. Schendel, S. L., Azimov, R., Pawlowski, K., Godzik, A., Kagan, B. L., and Reed, J. C. (1999) J. Biol. Chem., 274, 21932–21936.

    PubMed  CAS  Google Scholar 

  56. Eskes, R., Desagher, S., Antonsson, B., and Martinou, J. C. (2000) Mol. Cell Biol., 20, 929–935.

    PubMed  CAS  Google Scholar 

  57. 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.

    PubMed  CAS  Google Scholar 

  58. Korsmeyer, S. J. (1999) Cancer Res., 59, 1693s–1700s.

    PubMed  CAS  Google Scholar 

  59. Scorrano, L., and Korsmeyer, S. J. (2003) Biochem. Biophys. Res. Commun., 304, 437–444.

    PubMed  CAS  Google Scholar 

  60. Murphy, K. M., Streips, U. N., and Lock, R. B. (2000) J. Biol. Chem., 275, 17225–17228.

    PubMed  CAS  Google Scholar 

  61. Mikhailov, V., Mikhailova, M., Pulkrabek, D. J., Dong, Z., Venkatachalam, M. A., and Saikumar, P. (2001) J. Biol. Chem., 276, 18361–18374.

    PubMed  CAS  Google Scholar 

  62. 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.

    PubMed  CAS  Google Scholar 

  63. May, P., and May, E. (1999) Oncogene, 18, 7621–7636.

    PubMed  CAS  Google Scholar 

  64. Bourdon, J. C., Laurenzi, V. D., Melino, G., and Lane, D. (2003) Cell Death Differ., 10, 397–399.

    PubMed  CAS  Google Scholar 

  65. Schuler, M., and Green, D. R. (2001) Biochem. Soc. Trans., 29, 684–688.

    PubMed  CAS  Google Scholar 

  66. 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.

    PubMed  CAS  Google Scholar 

  67. Petrosillo, G., Ruggiero, F. M., and Paradies, G. (2003) FASEB J., 17, 2202–2208.

    PubMed  CAS  Google Scholar 

  68. Ott, M., Robertson, J. D., Gogvadze, V., Zhivotovsky, B., and Orrenius, S. (2002) Proc. Natl. Acad. Sci. USA, 99, 1259–1263.

    PubMed  CAS  Google Scholar 

  69. Karbowski, M., and Youle, R. J. (2003) Cell Death Differ., 10, 870–880.

    PubMed  CAS  Google Scholar 

  70. Bossy Wetzel, E., Barsoum, M. J., Godzik, A., Schwarzenbacher, R., and Lipton, S. A. (2003) Curr. Opin. Cell Biol., 15, 706–716.

    PubMed  CAS  Google Scholar 

  71. Praefcke, G. J., and McMahon, H. T. (2004) Nat. Rev. Mol. Cell Biol., 5, 133–147.

    PubMed  CAS  Google Scholar 

  72. Smirnova, E., Griparic, L., Shurland, D. L., and van der Bliek, A. M. (2001) Mol. Biol. Cell, 12, 2245–2256.

    PubMed  CAS  Google Scholar 

  73. 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.

    PubMed  CAS  Google Scholar 

  74. Olichon, A., Baricault, L., Gas, N., Guillou, E., Valette, A., Belenguer, P., and Lenaers, G. (2003) J. Biol. Chem., 278, 7743–7746.

    PubMed  CAS  Google Scholar 

  75. 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.

    PubMed  CAS  Google Scholar 

  76. Hirsch, T., Susin, S. A., Marzo, I., Marchetti, P., Zamzami, N., and Kroemer, G. (1998) Cell. Biol. Toxicol., 14, 141–145.

    PubMed  CAS  Google Scholar 

  77. Ricci, J. E., Waterhouse, N., and Green, D. R. (2003) Cell Death Differ., 10, 488–492.

    PubMed  CAS  Google Scholar 

  78. Fleury, C., Mignotte, B., and Vayssiere, J. L. (2002) Biochimie, 842, 131–141.

    Google Scholar 

  79. Saybasili, H., Yuksel, M., Haklar, G., and Yalcin, A. S. (2001) Antioxid. Redox Signal., 3, 1099–1104.

    PubMed  CAS  Google Scholar 

  80. Bergamini, C. M., Gambetti, S., Dondi, A., and Cervellati, C. (2004) Curr. Pharm. Des., 10, 1611–1626.

    PubMed  CAS  Google Scholar 

  81. Huang, P., Feng, L., Oldham, E. A., Keating, M. J., and Plunkett, W. (2000) Nature, 407, 390–395.

    PubMed  CAS  Google Scholar 

  82. 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.

    PubMed  CAS  Google Scholar 

  83. Manna, P. P., and Frazier, W. A. (2004) Cancer Res., 64, 1026–1036.

    PubMed  CAS  Google Scholar 

  84. 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.

    PubMed  CAS  Google Scholar 

  85. 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.

    PubMed  CAS  Google Scholar 

  86. 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.

    PubMed  CAS  Google Scholar 

  87. 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.

    PubMed  CAS  Google Scholar 

  88. Lipton, S. A., and Bossy Wetzel, E. (2002) Cell, 111, 147–150.

    PubMed  CAS  Google Scholar 

  89. 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.

    PubMed  CAS  Google Scholar 

  90. 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.

    PubMed  CAS  Google Scholar 

  91. 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.

    PubMed  CAS  Google Scholar 

  92. Leist, M., Single, B., Castoldi, A. F., Kuhnle, S., and Nicotera, P. (1997) J. Exp. Med., 185, 1481–1486.

    PubMed  CAS  Google Scholar 

  93. 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.

    CAS  Google Scholar 

  94. 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.

    PubMed  CAS  Google Scholar 

  95. Plomp, P. J., Gordon, P. B., Meijer, A. J., Hoyvik, H., and Seglen, P. O. (1989) J. Biol. Chem., 264, 6699–6704.

    PubMed  CAS  Google Scholar 

  96. Seglen, P. O., and Bohley, P. (1992) Experientia, 48, 158–172.

    PubMed  CAS  Google Scholar 

  97. Paglin, S., Hollister, T., Delohery, T., Hackett, N., McMahill, M., Sphicas, E., Domingo, D., and Yahalom, J. (2001) Cancer Res., 61, 439–444.

    PubMed  CAS  Google Scholar 

  98. Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. (1999) Nature, 402, 672–676.

    PubMed  CAS  Google Scholar 

  99. Yanagisawa, H., Miyashita, T., Nakano, Y., and Yamamoto, D. (2003) Cell Death Differ., 10, 798–807.

    PubMed  CAS  Google Scholar 

  100. Priault, M., Camougrand, N., Kinnally, K. W., Vallette, F. M., and Manon, S. (2003) FEMS Yeast Res., 4, 15–27.

    PubMed  CAS  Google Scholar 

  101. Guimaraes, C. A., and Linden, R. (2004) Eur. J. Biochem., 271, 1638–1650.

    CAS  Google Scholar 

  102. 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.

    PubMed  CAS  Google Scholar 

  103. Burlacu, A., Jinga, V., Gafencu, A. V., and Simionescu, M. (2001) Cell Tissue Res., 306, 409–416.

    PubMed  CAS  Google Scholar 

  104. Seoane, A., Dememes, D., and Llorens, J. (2001) J. Comp. Neurol., 439, 385–399.

    PubMed  CAS  Google Scholar 

  105. Kawahara, A., Ohsawa, Y., Matsumura, H., Uchiyama, Y., and Nagata, S. (1998) J. Cell Biol., 143, 1353–1360.

    PubMed  CAS  Google Scholar 

  106. Shimizu, S., Eguchi, Y., Kamiike, W., Waguri, S., Uchiyama, Y., Matsuda, H., and Tsujimoto, Y. (1996) Oncogene, 12, 2045–2050.

    PubMed  CAS  Google Scholar 

  107. 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.

    PubMed  CAS  Google Scholar 

  108. Oppenheim, R. W., Flavell, R. A., Vinsant, S., Prevette, D., Kuan, C. Y., and Rakic, P. (2001) J. Neurosci., 21, 4752–4760.

    PubMed  CAS  Google Scholar 

  109. Bauvy, C., Gane, P., Arico, S., Codogno, P., and Ogier Denis, E. (2001) Exp. Cell Res., 268, 139–149.

    PubMed  CAS  Google Scholar 

  110. Mills, K. R., Reginato, M., Debnath, J., Queenan, B., and Brugge, J. S. (2004) Proc. Natl. Acad. Sci. USA, 101, 3438–3443.

    PubMed  CAS  Google Scholar 

  111. 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.

    PubMed  CAS  Google Scholar 

  112. Bursch, W., Ellinger, A., Kienzl, H., Torok, L., Pandey, S., Sikorska, M., Walker, R., and Hermann, R. S. (1996) Carcinogenesis, 17, 1595–1607.

    PubMed  CAS  Google Scholar 

  113. Inbal, B., Bialik, S., Sabanay, I., Shani, G., and Kimchi, A. (2002) J. Cell Biol., 157, 455–468.

    PubMed  CAS  Google Scholar 

  114. 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.

    PubMed  CAS  Google Scholar 

  115. Cory, S., Huang, D. C., and Adams, J. M. (2003) Oncogene, 22, 8590–8607.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Apoptose et Systeme Immunitaire, Institut Pasteur, CNRS-URA 1961, 25 rue du Dr. Roux, 75015, Paris, France

    M. Bras, B. Queenan & S. A. Susin

Authors
  1. M. Bras
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Queenan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. A. Susin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. A. Susin.

Additional information

Translated from Biokhimiya, Vol. 70, No. 2, 2005, pp. 284 293.

Original Russian Text Copyright ¢ 2005 by Bras, Queenan, Susin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10541-005-0105-4

Key words

Search

Navigation