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Journal of Bioenergetics and Biomembranes

, Volume 37, Issue 3, pp 155–164 | Cite as

The Role of the Mitochondrial Apoptosis Induced Channel MAC in Cytochrome c Release

  • Sonia Martinez-Caballero
  • Laurent M. Dejean
  • Elizabeth A. Jonas
  • Kathleen W. KinnallyEmail author
Article

Abstract

Permeabilization of the mitochondrial outer membrane is a crucial event during apoptosis. It allows the release of proapoptotic factors, like cytochrome c, from the intermembrane space, and represents the commitment step in apoptosis. The mitochondrial apoptosis-induced channel, MAC, is a high-conductance channel that forms during early apoptosis and is the putative cytochrome c release channel. Unlike activation of the permeability transition pore, MAC formation occurs without loss of outer membrane integrity and depolarization. The single channel behavior and pharmacology of reconstituted MAC has been characterized with patch-clamp techniques. Furthermore, MAC’s activity is compared to that detected in mitochondria inside the cells at the time cytochrome c is released. Finally, the regulation of MAC by the Bcl-2 family proteins and insights concerning its molecular composition are also discussed.

Keywords

Mitochondrial apoptosis-induced channel MAC patch clamp cytochrome c Bax 

Abbreviations:

MAC

Mitochondrial apoptosis-induced channel

PTP

Permeability transition pore

TOM

Translocase of the outer membrane

VDAC

Voltage-dependent anion-selective channel

IL-3

Interleukin 3

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References

  1. Akeson, M., Branton, D., Kasianowicz, J. J., Brandin, E., and Deamer, D. W. (1999). Biophys. J. 77, 3227–3233.PubMedGoogle Scholar
  2. Antonsson, B. (2004). Mol. Cell Biochem. 256/257, 141–155.CrossRefGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. Antonsson, B., Montessuit, S., Lauper, S., Eskes, R., and Martinou, J. C. (2000). Biochem. J. 345, 271–278.CrossRefPubMedGoogle Scholar
  5. Antonsson, B., Montessuit, S., Sanchez, B., and Martinou, J. C. (2001). J. Biol. Chem. 276, 11615–11623.CrossRefPubMedGoogle Scholar
  6. Baines, C. P., Kaiser, R. A., Purcell, N. H., Blair, N. S., Osinska, H., Hambleton, M. A., Brunskill, E. W., Sayen, M. R., Gottlieb, R. A., Dorn, G. W., II, Robbins, J., and Molkentin, J. D. (2005). Nature 434, 658–662.PubMedGoogle Scholar
  7. Basanez, G., Nechushtan, A., Drozhinin, O., Chanturiya, A., Choe, E., Tutt, S., Wood, K. A., Hsu, Y., Zimmerberg, J., and Youle, R. J. (1999). Proc. Natl. Acad. Sci. USA 96, 5492–5497.PubMedGoogle Scholar
  8. Basso, E., Fante, L., Fowlkes, J., Petronilli, V., Forte, M. A., and Bernardi, P. (2005). J. Biol. Chem. 280, 18558–18561.CrossRefPubMedGoogle Scholar
  9. Baumann, G., and Mueller, P. (1974). J. Supramol. Struct. 2, 538–557.CrossRefPubMedGoogle Scholar
  10. Bezrukov, S. M., and Kasianowicz, J. J. (1997). Eur. Biophys. J. 26, 471–476.CrossRefPubMedGoogle Scholar
  11. Brenner, C., and Kroemer, G. (2000). Science 289, 1150–1151.Google Scholar
  12. Broekemeier, K. M., Carpenter-Deyo, L., Reed, D. J., and Pfeiffer, D. R. (1992). FEBS Lett. 304, 192–194.CrossRefPubMedGoogle Scholar
  13. Cartron, P. F., Priault, M., Oliver, L., Meflah, K., Manon, S., and Vallette, F. M. (2003). J. Biol. Chem. 278, 11633–11641.CrossRefPubMedGoogle Scholar
  14. Cheng, E. H., Sheiko, T. V., Fisher, J. K., Craigen, W. J., and Korsmeyer, S. J. (2003). Science. 301, 513–517.CrossRefPubMedGoogle Scholar
  15. Cheng, E. H., Wei, M. C., Weiler, S., Flavell, R. A., Mak, T. W., Lindsten, T., and Korsmeyer, S. J. (2001). Mol. Cell. 8, 705–711.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefPubMedGoogle Scholar
  17. Chittenden, T., Flemington, C., Houghton, A. B., Ebb, R. G., Gallo, G. J., Elangovan, B., Chinnadurai, G., and Lutz, R. J. (1995). EMBO J. 14, 5589–5596.PubMedGoogle Scholar
  18. Cory, S., Huang, D. C., and Adams, J. M. (2003). Oncogene 22, 8590–8607.CrossRefPubMedGoogle Scholar
  19. Danial, N. N., and Korsmeyer, S. J. (2004). Cell 116, 205–219.PubMedGoogle Scholar
  20. De Giorgi, F., Lartigue, L., Bauer, M. K., Schubert, A., Grimm, S., Hanson, G. T., Remington, S. J., Youle, R. J., and Ichas, F. (2002). FASEB J. 16, 607–609.PubMedGoogle Scholar
  21. Dejean, L. M., Martinez-Caballero, S., Guo, L., Hughes, C., Teijido, O., Ducret, T., Ichas, F., Korsmeyer, S. J., Antonsson, B., Jonas, E. A., and Kinnally, K. W. (2005). Mol. Biol. Cell. 16, 2424–2432.CrossRefPubMedGoogle Scholar
  22. Dejean, L. M., Martinez-Caballero, S., Manon, S., and Kinnally, K. W. (2005). Biochim. Biophys. Acta.Google Scholar
  23. Freedman, A. M., Kramer, J. H., Mak, I. T., Cassidy, M. M., and Weglicki, W. B. (1991). Free Radic. Biol. Med. 11, 197–206.CrossRefPubMedGoogle Scholar
  24. Goldstein, J. C., Waterhouse, N. J., Juin, P., Evan, G. I., and Green, D. R. (2000). Nat. Cell Biol. 2, 156–162.CrossRefPubMedGoogle Scholar
  25. Green, D. R., Knight, R. A., Melino, G., Finazzi-Agro, A., and Orrenius, S. (2004). Cell Death Differ. 11, 2–3.CrossRefPubMedGoogle Scholar
  26. Grigoriev, S. M., Muro, C., Dejean, L. M., Campo, M. L., Martinez-Caballero, S., and Kinnally, K. W. (2004). Int. Rev. Cytol. 238, 227–274.PubMedGoogle Scholar
  27. Gross, A., Jockel, J., Wei, M. C., and Korsmeyer, S. J. (1998). EMBO J. 17, 3878–3885.CrossRefPubMedGoogle Scholar
  28. Guihard, G., Bellot, G., Moreau, C., Pradal, G., Ferry, N., Thomy, R., Fichet, P., Meflah, K., and Vallette, F. M. (2004). J. Biol. Chem. 279, 46542–46550.CrossRefPubMedGoogle Scholar
  29. Guo, L., Pietkiewicz, D., Pavlov, E. V., Grigoriev, S. M., Kasianowicz, J. J., Dejean, L. M., Korsmeyer, S. J., Antonsson, B., and Kinnally, K. W. (2004). Am. J. Physiol. Cell Physiol. 286, C1109–C1117.CrossRefPubMedGoogle Scholar
  30. Gupte, S., and Hackenbrock, C. (1988). J. Biol. Chem. 263, 5241–5247.PubMedGoogle Scholar
  31. Heiskanen, K. M., Bhat, M. B., Wang, H. W., Ma, J., and Nieminen, A. L. (1999). J. Biol. Chem. 274, 5654–5658.CrossRefPubMedGoogle Scholar
  32. Hille, B. (2001). Ionic Channels of Excitable Membranes, Sinauer, Sunderland, MA.Google Scholar
  33. Hirotani, M., Zhang, Y., Fujita, N., Naito, M., and Tsuruo, T. (1999). J. Biol. Chem. 274, 20415–20420.CrossRefPubMedGoogle Scholar
  34. Hoyt, K. R., Sharma, T. A., and Reynolds, I. J. (1997). Br. J. Pharmacol. 122, 803–808.CrossRefPubMedGoogle Scholar
  35. Jonas, E. A., Hickman, J. A., Chachar, M., Polster, B. M., Brandt, T. A., Fannjiang, Y., Ivanovska, I., Basanez, G., Kinnally, K. W., Zimmerberg, J., Hardwick, J. M., and Kaczmarek, L. K. (2004). Proc. Natl. Acad. Sci. USA 101, 13590–13595.CrossRefPubMedGoogle Scholar
  36. Jonas, E. A., Hickman, J. A., Hardwick, J. M., and Kaczmarek, L. K. (2005). J. Biol. Chem. 280, 4491–4497.CrossRefPubMedGoogle Scholar
  37. Jutila, A., Rytomaa, M., and Kinnunen, P. K. (1998). Mol. Pharmacol. 54, 722–732.PubMedGoogle Scholar
  38. Kasianowicz, J. J., Henrickson, S. E., Weetall, H. H., and Robertson, B. (2001). Anal. Chem. 73, 2268–2272.CrossRefPubMedGoogle Scholar
  39. Kingston, C. A., Ladha, S., Manning, R., and Bowler, K. (1993). Anticancer Res. 13, 2335–2340.PubMedGoogle Scholar
  40. Korchev, Y. E., Bashford, C. L., Alder, G. M., Kasianowicz, J. J., and Pasternak, C. A. (1995). J. Membr. Biol. 147, 233–239.PubMedGoogle Scholar
  41. Krasilnikov, O., Sabirov, R., Ternovsky, V., Merzliak, P., and Muratkhodjaev, J. (1992). FEMS Microbiol. Immunol. 105, 93–100.CrossRefGoogle Scholar
  42. Krasilnikov, O. V., Carneiro, C. M., Yuldasheva, L. N., Campos-de-Carvalho, A. C., and Nogueira, R. A. (1996). Braz. J. Med. Biol. Res. 29, 1691–1697.PubMedGoogle Scholar
  43. Krasilnikov, O. V., Da Cruz, J. B., Yuldasheva, L. N., Varanda, W. A., and Nogueira, R. A. (1998). J. Membr. Biol. 161, 83–92.CrossRefPubMedGoogle Scholar
  44. Kroemer, G., and Reed, J. C. (2000). Nat. Med. 6, 513–519.CrossRefPubMedGoogle Scholar
  45. Kuwana, T., Mackey, M., Perkins, G., Ellisman, M., Latterich, M., Schneiter, R., Green, D., and Newmeyer, D. (2002). Cell 111, 331–342.CrossRefPubMedGoogle Scholar
  46. Lenartowicz, E., Bernardi, P., and Azzone, G. F. (1991). J. Bioenerg. Biomembr. 23, 679–688.CrossRefPubMedGoogle Scholar
  47. Lewis, S., Bethell, S. S., Patel, S., Martinou, J. C., and Antonsson, B. (1998). Protein Expr. Purif. 13, 120–126.CrossRefPubMedGoogle Scholar
  48. Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. (1996). Cell. 86, 147–157.CrossRefPubMedGoogle Scholar
  49. Margoliash, E., Smith, E. L., Kreil, G., and Tuppy, H. (1961). Nature 192, 1121–1127.PubMedGoogle Scholar
  50. Martinez-Caballero, S., Dejean, L. M., and Kinnally, K. W. (2004). FEBS Lett. 568, 35–38.CrossRefPubMedGoogle Scholar
  51. Motz, C., Martin, H., Krimmer, T., and Rassow, J. (2002). J. Mol. Biol. 323, 729–738.CrossRefPubMedGoogle Scholar
  52. Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., Inohara, H., Kubo, T., and Tsujimoto, Y. (2005). Nature 434, 652–658.CrossRefPubMedGoogle Scholar
  53. Newmeyer, D. D., and Ferguson-Miller, S. (2003). Cell 112, 481–490.CrossRefPubMedGoogle Scholar
  54. Nieminen, A. L., Saylor, A. K., Tesfai, S. A., Herman, B., and Lemasters, J. J. (1995). Biochem. J. 307, Pt 1, 99–106.PubMedGoogle Scholar
  55. Pastorino, J. G., Shulga, N., and Hoek, J. B. (2002). J. Biol. Chem. 277, 7610–7618.CrossRefPubMedGoogle Scholar
  56. Pavlov, E. V., Priault, M., Pietkiewicz, D., Cheng, E. H.-Y., Antonsson, B., Manon, S., Korsmeyer, S. J., Mannella, C. A., and Kinnally, K. W. (2001). J. Cell Biol. 155, 725–732.CrossRefPubMedGoogle Scholar
  57. Pavlov, P. F., and Glaser, E. (1998). Biochem. Biophys. Res. Commun. 252, 84–91.CrossRefPubMedGoogle Scholar
  58. Polcic, P., and Forte, M. (2003). Biochem. J. 374, 393–402.CrossRefPubMedGoogle Scholar
  59. Polster, B. M., Basanez, G., Young, M., Suzuki, M., and Fiskum, G. (2003). J. Neurosci. 23, 2735–2743.PubMedGoogle Scholar
  60. Polster, B. M., Kinnally, K. W., and Fiskum, G. (2001). J. Biol. Chem. 276, 37887–37894.PubMedGoogle Scholar
  61. Priault, M., Camougrand, N., Kinnally, K. W., Vallette, F. M., and Manon, S. (2003). FEMS Yeast Res. 4, 15–27.CrossRefPubMedGoogle Scholar
  62. Reed, J. C., Doctor, K. S., and Godzik, A. (2004). Sci. STKE 2004:re9 1–29.Google Scholar
  63. Rostovtseva, T., and Colombini, M. (1997). Biophys. J. 72, 1954–1962.Google Scholar
  64. Rostovtseva, T. K., and Bezrukov, S. M. (1998). Biophys. J. 74, 2365–2373.PubMedGoogle Scholar
  65. Rostovtseva, T. K., Komarov, A., Bezrukov, S. M., and Colombini, M. (2002). Biophys. J. 82, 193–205.PubMedGoogle Scholar
  66. Roucou, X., Rostovtseva, T., Montessuit, S., Martinou, J. C., and Antonsson, B. (2002). Biochem J. 363, 547–552.CrossRefPubMedGoogle Scholar
  67. Saito, M., Korsmeyer, S. J., and Schlesinger, P. H. (2000). Nat. Cell Biol. 2, 553–555.CrossRefPubMedGoogle Scholar
  68. 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.CrossRefPubMedGoogle Scholar
  69. Schlesinger, P. H., Gross, A., Yin, X.-M., Yamamoto, K., Saito, M., Waksman, G., and Korsmeyer, S. J. (1997). PNAS 94, 11357–11362.CrossRefPubMedGoogle Scholar
  70. Scorrano, L., Ashiya, M., Buttle, K., Weiler, S., Oakes, S. A., Mannella, C. A., and Korsmeyer, S. J. (2002). Dev. Cell 2, 55–67.CrossRefPubMedGoogle Scholar
  71. Scorrano, L., and Korsmeyer, S. J. (2003). BBRC 304, 437–444.PubMedGoogle Scholar
  72. Siskind, L., Kolesnick, R., and Colombini, M. (2002). J. Biol. Chem. 277, 26796–26803.CrossRefPubMedGoogle Scholar
  73. Siskind, L. J., Davoody, A., Lewin, N., Marshall, S., and Colombini, M. (2003). Biophys. J. 85, 1560–1575.PubMedGoogle Scholar
  74. Skulachev, V. P. (1996). FEBS Lett. 397, 7–10.CrossRefPubMedGoogle Scholar
  75. Sobko, A. A., Kotova, E. A., Antonenko, Y. N., Zakharov, S. D., and Cramer, W. A. (2004). FEBS Lett. 576, 205–210.CrossRefPubMedGoogle Scholar
  76. Szabo, I., Bernardi, P., and Zoratti, M. (1992). J. Biol. Chem. 267, 2940–2946.PubMedGoogle Scholar
  77. Terrones, O., Antonsson, B., Yamaguchi, H., Wang, H. G., Liu, J., Lee, R. M., Herrmann, A., and Basanez, G. (2004). J. Biol. Chem. 279, 30081–30091.CrossRefPubMedGoogle Scholar
  78. Truscott, K. N., Kovermann, P., Geissler, A., Merlin, A., Meijer, M., Driessen, A. J., Rassow, J., Pfanner, N., and Wagner, R. (2001). Nat. Struct. Biol. 8, 1074–1082.CrossRefPubMedGoogle Scholar
  79. Vander Heiden, M. G., Li, X. X., Gottleib, E., Hill, R. B., Thompson, C. B., and Colombini, M. (2001). J. Biol. Chem. 276, 19414–19419.CrossRefPubMedGoogle Scholar
  80. Varga, E., Szollosi, J., Antal, K., Kovacs, P., and Szabo, J. Z. (1999). Pharmazie 54, 380–384.PubMedGoogle Scholar
  81. Wang, X. (2001). Genes Dev. 15, 2922–2933.PubMedGoogle Scholar
  82. Wei, M. C., Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B., and Korsmeyer, S. J. (2001). Science 292, 727–730.Google Scholar
  83. Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T. I., Jones, D. P., and Wang, X. (1997). Science 275, 1129–1132.Google Scholar
  84. Yang, L., Harroun, T. A., Weiss, T. M., Ding, L., and Huang, H. W. (2001). Biophys. J. 81, 1475–1485.PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Sonia Martinez-Caballero
    • 1
  • Laurent M. Dejean
    • 1
  • Elizabeth A. Jonas
    • 2
  • Kathleen W. Kinnally
    • 1
    • 3
    Email author
  1. 1.Department of Basic SciencesNew York University, College of DentistryNew York
  2. 2.Department of Internal MedicineYale University School of MedicineNew Haven
  3. 3.Department of Basic SciencesNew York University, College of DentistryNew York

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