Abstract
The fundamental contribution of the mitochondria and ER to the decision made on the cell’s fate has been increasingly recognized. This progress has illuminated the need for the mechanisms these organelles use to initiate and to propagate apoptotic signals. The toolbox of the mitochondria and ER is evolutionary conserved, overlapping and complementary. Furthermore, mitochondria are often closely associated with the ER providing the conditions for a local and privileged communication between the two organelles. The present review is concerned with the spatially and temporally coordinated utilization of Bcl-2 family proteins and Ca2+ by the mitochondria and ER to control the membrane permeabilization in the mitochondria and to regulate Ca2+ distribution and the activity of apoptotic proteins in the ER. The apoptotic means of the mitochondria and ER will eventually come together to control the dismantling of the cell by the caspases and other enzymes.
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Annis, M. G., Yethon, J. A., Leber, B., and Andrews, D. W. (2004). Biochim. Biophys. Acta 1644, 115–123.
Annis, M. G., Zamzami, N., Zhu, W., Penn, L. Z., Kroemer, G., Leber, B., and Andrews, D. W. (2001). Oncogene 20, 1939–1952.
Arnaudeau, S., Frieden, M., Nakamura, K., Castelbou, C., Michalak, M., and Demaurex, N. (2002). J. Biol. Chem. 277, 46696–46705.
Assefa, Z., Bultynck, G., Szlufcik, K., Nadif Kasri, N., Vermassen, E., Goris, J., Missiaen, L., Callewaert, G., Parys, J. B., and De Smedt, H. (2004). J. Biol. Chem. 279, 43227–43236.
Bae, J. H., Park, J. W., and Kwon, T. K. (2003). Biochem. Biophys. Res. Commun. 303, 1073–1079.
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., Robbins, J., and Molkentin, J. D. (2005). Nature 434, 658–662.
Barry, M., Heibein, J. A., Pinkoski, M. J., Lee, S. F., Moyer, R. W., Green, D. R., and Bleackley, R. C. (2000). Mol. Cell. Biol. 20, 3781–3794.
Bassik, M. C., Scorrano, L., Oakes, S. A., Pozzan, T., and Korsmeyer, S. J. (2004). Embo J. 23, 1207–1216.
Basso, E., Fante, L., Fowlkes, J., Petronilli, V., Forte, M. A., and Bernardi, P. (2005). J. Biol. Chem. 280, 18558–18561.
Bernardi, P., and Petronilli, V. (1996). J. Bioenerg. Biomembr. 28, 131–138.
Beutner, G., Ruck, A., Riede, B., Welte, W., and Brdiczka, D. (1996). FEBS Lett. 396, 189–195.
Bionda, C., Portoukalian, J., Schmitt, D., Rodriguez-Lafrasse, C., and Ardail, D. (2004). Biochem. J. 382, 527–533.
Birbes, H., El Bawab, S., Hannun, Y. A., and Obeid, L. M. (2001). Faseb J. 15, 2669–2679.
Blackstone, N. W., and Green, D. R. (1999). Bioessays 21, 84–88.
Boehning, D., Patterson, R. L., Sedaghat, L., Glebova, N. O., Kurosaki, T., and Snyder, S. H. (2003). Nat. Cell. Biol. 5, 1051–1061.
Bowser, D. N., Petrou, S., Panchal, R. G., Smart, M. L., and Williams, D. A. (2002). Faseb J. 16, 1105–1107.
Boya, P., Cohen, I., Zamzami, N., Vieira, H. L., and Kroemer, G. (2002). Cell Death Differ. 9, 465–467.
Breckenridge, D. G., Stojanovic, M., Marcellus, R. C., and Shore, G. C. (2003a). J. Cell. Biol. 160, 1115–1127.
Breckenridge, D. G., Nguyen, M., Kuppig, S., Reth, M., and Shore, G. C. (2002). Proc. Natl. Acad. Sci. USA 99, 4331–4336.
Breckenridge, D. G., Germain, M., Mathai, J. P., Nguyen, M., and Shore, G. C. (2003b). Oncogene 22, 8608–8618.
Broekemeier, K. M., Dempsey, M. E., and Pfeiffer, D. R. (1989). J. Biol. Chem. 264, 7826–7830.
Camacho, P., and Lechleiter, J. D. (1995). Cell 82, 765–771.
Chen, M., He, H., Zhan, S., Krajewski, S., Reed, J. C., and Gottlieb, R. A. (2001). J. Biol. Chem. 276, 30724–30728.
Chen, R., Valencia, I., Zhong, F., McColl, K. S., Roderick, H. L., Bootman, M. D., Berridge, M. J., Conway, S. J., Holmes, A. B., Mignery, G. A., Velez, P., and Distelhorst, C. W. (2004). J. Cell. Biol. 166, 193–203.
Cheng, E. H., Sheiko, T. V., Fisher, J. K., Craigen, W. J., and Korsmeyer, S. J. (2003). Science 301, 513–517.
Chen-Levy, Z., Nourse, J., and Cleary, M. L. (1989). Mol. Cell. Biol. 9, 701–710.
Crompton, M., Ellinger, H., and Costi, A. (1988). Biochem. J. 255, 357–360.
Csordas, G., Thomas, A. P., and Hajnoczky, G. (1999). Embo J. 18, 96–108.
Csordas, G., Madesh, M., Antonsson, B., and Hajnoczky, G. (2002). Embo J. 21, 2198–2206.
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.
De Giorgi, F., Lartigue, L., and Ichas, F. (2000). Cell Calcium 28, 365–370.
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.
De Marchi, U., Campello, S., Szabo, I., Tombola, F., Martinou, J. C., and Zoratti, M. (2004). J. Biol. Chem. 279, 37415–37422.
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.
Dessi, F., Ben-Ari, Y., and Charriaut-Marlangue, C. (1995). Neurosci. Lett. 201, 53–56.
Distelhorst, C. W., and Shore, G. C. (2004). Oncogene 23, 2875–2880.
Ferrari, D., Pinton, P., Szabadkai, G., Chami, M., Campanella, M., Pozzan, T., and Rizzuto, R. (2002). Cell Calcium 32, 413–420.
Ferri, K. F., and Kroemer, G. (2001). Nat. Cell. Biol. 3, E255–E263.
Fontaine, E., and Bernardi, P. (1999). J. Bioenerg. Biomembr. 31, 335–345.
Fournier, N., Ducet, G., and Crevat, A. (1987). J. Bioenerg. Biomembr. 19, 297–303.
Germain, M., Mathai, J. P., and Shore, G. C. (2002). J. Biol. Chem. 277, 18053–18060.
Germain, M., Mathai, J. P., McBride, H. M., and Shore, G. C. (2005). Embo J.
Green, D. R., and Kroemer, G. (2004). Science 305, 626–629.
Groskreutz, J. L., Bronk, S. F., and Gores, G. J. (1992). Gastroenterology 102, 1030–1038.
Hacki, J., Egger, L., Monney, L., Conus, S., Rosse, T., Fellay, I., and Borner, C. (2000). Oncogene 19, 2286–2295.
Hajnoczky, G., Robb-Gaspers, L. D., Seitz, M. B., and Thomas, A. P. (1995). Cell 82, 415–424.
Halestrap, A. P., Connern, C. P., Griffiths, E. J., and Kerr, P. M. (1997). Mol. Cell. Biochem. 174, 167–172.
Haworth, R. A., and Hunter, D. R. (1979). Arch. Biochem. Biophys. 195, 460–467.
Haworth, R. A., and Hunter, D. R. (2000). J. Bioenerg. Biomembr. 32, 91–96.
He, L., and Lemasters, J. J. (2002). FEBS Lett. 512, 1–7.
Hetz, C., Russelakis-Carneiro, M., Maundrell, K., Castilla, J., and Soto, C. (2003). Embo J. 22, 5435–5445.
Hunter, D. R., and Haworth, R. A. (1979a). Arch. Biochem. Biophys. 195, 453–459.
Hunter, D. R., and Haworth, R. A. (1979b). Arch. Biochem. Biophys. 195, 468–477.
Hunter, D. R., Haworth, R. A., and Southard, J. H. (1976). J. Biol. Chem. 251, 5069–5077.
Ichas, F., Jouaville, L. S., and Mazat, J. P. (1997). Cell 89, 1145–1153.
Ito, Y., Pandey, P., Mishra, N., Kumar, S., Narula, N., Kharbanda, S., Saxena, S., and Kufe, D. (2001). Mol. Cell. Biol. 21, 6233–6242.
Jayaraman, T., and Marks, A. R. (1997). Mol. Cell. Biol. 17, 3005–3012.
Jimbo, A., Fujita, E., Kouroku, Y., Ohnishi, J., Inohara, N., Kuida, K., Sakamaki, K., Yonehara, S., and Momoi, T. (2003). Exp. Cell. Res. 283, 156–166.
Kessel, D., Castelli, M., and Reiners, J. J. (2005). Cell. Death Differ. 12, 502–511.
Khan, A. A., Soloski, M. J., Sharp, A. H., Schilling, G., Sabatini, D. M., Li, S. H., Ross, C. A., and Snyder, S. H. (1996). Science 273, 503–507.
Kitamura, Y., Miyamura, A., Takata, K., Inden, M., Tsuchiya, D., Nakamura, K., and Taniguchi, T. (2003). J. Pharmacol. Sci. 92, 228–236.
Klee, M., and Pimentel-Muinos, F. X. (2005). J. Cell. Biol. 168, 723–734.
Kokoszka, J. E., Waymire, K. G., Levy, S. E., Sligh, J. E., Cai, J., Jones, D. P., MacGregor, G. R., and Wallace, D. C. (2004). Nature 427, 461–465.
Koya, R. C., Fujita, H., Shimizu, S., Ohtsu, M., Takimoto, M., Tsujimoto, Y., and Kuzumaki, N. (2000). J. Biol. Chem. 275, 15343–15349.
Li, C., Fox, C. J., Master, S. R., Bindokas, V. P., Chodosh, L. A., and Thompson, C. B. (2002). Proc. Natl. Acad. Sci. USA 99, 9830–9835.
Li, H., Zhu, H., Xu, C. J., and Yuan, J. (1998). Cell 94, 491–501.
Lithgow, T. (2000). FEBS Lett. 476, 22–26.
Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. (1996). Cell 86, 147–157.
Lucken-Ardjomande, S., and Martinou, J. C. (2005). J. Cell. Sci. 118, 473–483.
Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998). Cell 94, 481–490.
Madesh, M., and Hajnoczky, G. (2001). J. Cell. Biol. 155, 1003–1015.
Madesh, M., Antonsson, B., Srinivasula, S. M., Alnemri, E. S., and Hajnoczky, G. (2002). J. Biol. Chem. 277, 5651–5659.
Majewski, N., Nogueira, V., Bhaskar, P., Coy, P. E., Skeen, J. E., Gottlob, K., Chandel, N. S., Thompson, C. B., Robey, R. B., and Hay, N. (2004). Mol. Cell. 16, 819–830.
Mannella, C. A., Buttle, K., Rath, B. K., and Marko, M. (1998). Biofactors 8, 225–228.
Martinou, J. C., and Green, D. R. (2001). Nat. Rev. Mol. Cell. Biol. 2, 63–67.
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.
Mathai, J. P., Germain, M., and Shore, G. C. (2005). J. Biol. Chem. 280, 23829–23836.
Mathai, J. P., Germain, M., Marcellus, R. C., and Shore, G. C. (2002). Oncogene 21, 2534–2544.
McEnery, M. W., Snowman, A. M., Trifiletti, R. R., and Snyder, S. H. (1992). Proc. Natl. Acad. Sci. USA 89, 3170–3174.
Mesaeli, N., and Phillipson, C. (2004). Mol. Biol. Cell. 15, 1862–1870.
Mignery, G. A., Sudhof, T. C., Takei, K., and De Camilli, P. (1989). Nature 342, 192–195.
Mikhailov, V., Mikhailova, M., Degenhardt, K., Venkatachalam, M. A., White, E., and Saikumar, P. (2003). J. Biol. Chem. 278, 5367–5376.
Miyashita, T., and Reed, J. C. (1995). Cell 80, 293–299.
Morishima, N., Nakanishi, K., Tsuchiya, K., Shibata, T., and Seiwa, E. (2004). J. Biol. Chem. 279, 50375–50381.
Mund, T., Gewies, A., Schoenfeld, N., Bauer, M. K., and Grimm, S. (2003). Faseb J. 17, 696–698.
Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J., Yankner, B. A., and Yuan, J. (2000). Nature 403, 98–103.
Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., Inohara, H., Kubo, T., and Tsujimoto, Y. (2005). Nature 434, 652–658.
Nakamura, K., Bossy-Wetzel, E., Burns, K., Fadel, M. P., Lozyk, M., Goping, I. S., Opas, M., Bleackley, R. C., Green, D. R., and Michalak, M. (2000). J. Cell. Biol. 150, 731–740.
Nakano, K., and Vousden, K. H. (2001). Mol. Cell. 7, 683–694.
Ng, F. W., Nguyen, M., Kwan, T., Branton, P. E., Nicholson, D. W., Cromlish, J. A., and Shore, G. C. (1997). J. Cell. Biol. 139, 327–338.
Nicholls, D. G., and Budd, S. L. (2000). Physiol. Rev. 80, 315–360.
Oakes, S. A., Opferman, J. T., Pozzan, T., Korsmeyer, S. J., and Scorrano, L. (2003). Biochem. Pharmacol. 66, 1335–1340.
Oakes, S. A., Scorrano, L., Opferman, J. T., Bassik, M. C., Nishino, M., Pozzan, T., and Korsmeyer, S. J. (2005). Proc. Natl. Acad. Sci. USA 102, 105–110.
Oda, E., Ohki, R., Murasawa, H., Nemoto, J., Shibue, T., Yamashita, T., Tokino, T., Taniguchi, T., and Tanaka, N. (2000). Science 288, 1053–1058.
Oh, K. J., Barbuto, S., Meyer, N., Kim, R. S., Collier, R. J., and Korsmeyer, S. J. (2005). J. Biol. Chem. 280, 753–767.
Pacher, P., and Hajnoczky, G. (2001). Embo J. 20, 4107–4121.
Pacher, P., Csordas, P., Schneider, T., and Hajnoczky, G. (2000). J. Physiol. 529(3), 553–564.
Palmer, A. E., Jin, C., Reed, J. C., and Tsien, R. Y. (2004). Proc. Natl. Acad. Sci. USA 101, 17404–17409.
Pastorino, J. G., Shulga, N., and Hoek, J. B. (2002). J. Biol. Chem. 277, 7610–7618.
Pastorino, J. G., Tafani, M., Rothman, R. J., Marcinkeviciute, A., Hoek, J. B., and Farber, J. L. (1999). J. Biol. Chem. 274, 31734–31739.
Puthalakath, H., Huang, D. C., O’Reilly, L. A., King, S. M., and Strasser, A. (1999). Mol. Cell. 3, 287–296.
Rao, R. V., Castro-Obregon, S., Frankowski, H., Schuler, M., Stoka, V., del Rio, G., Bredesen, D. E., and Ellerby, H. M. (2002). J. Biol. Chem. 277, 21836–21842.
Rapizzi, E., Pinton, P., Szabadkai, G., Wieckowski, M. R., Vandecasteele, G., Baird, G., Tuft, R. A., Fogarty, K. E., and Rizzuto, R. (2002). J. Cell. Biol. 159, 613–624.
Reed, J. C., Doctor, K. S., and Godzik, A. (2004). Sci. STKE. 2004, re9.
Rizzuto, R., Brini, M., Murgia, M., and Pozzan, T. (1993). Science 262, 744–747.
Rizzuto, R., Pinton, P., Carrington, W., Fay, F. S., Fogarty, K. E., Lifshitz, L. M., Tuft, R. A., and Pozzan, T. (1998). Science 280, 1763–1766.
Rosemblit, N., Moschella, M. C., Ondriasa, E., Gutstein, D. E., Ondrias, K., and Marks, A. R. (1999). Dev. Biol. 206, 163–177.
Scorrano, L., Penzo, D., Petronilli, V., Pagano, F., and Bernardi, P. (2001). J. Biol. Chem. 276, 12035–12040.
Scorrano, L., Oakes, S. A., Opferman, J. T., Cheng, E. H., Sorcinelli, M. D., Pozzan, T., and Korsmeyer, S. J. (2003). Science 300, 135–139.
Sharpe, J. C., Arnoult, D., and Youle, R. J. (2004). Biochim. Biophys. Acta 1644, 107–113.
Shimizu, S., Ide, T., Yanagida, T., and Tsujimoto, Y. (2000). J. Biol. Chem. 275, 12321–12325.
Simmen, T., Aslan, J. E., Blagoveshchenskaya, A. D., Thomas, L., Wan, L., Xiang, Y., Feliciangeli, S. F., Hung, C. H., Crump, C. M., and Thomas, G. (2005). Embo J. 24, 717–729.
Simpson, P. B., Mehotra, S., Lange, G. D., and Russell, J. T. (1997). J. Biol. Chem. 272, 22654–22661.
Sugawara, H., Kurosaki, M., Takata, M., and Kurosaki, T. (1997). Embo J. 16, 3078–3088.
Szabadkai, G., Simoni, A. M., Chami, M., Wieckowski, M. R., Youle, R. J., and Rizzuto, R. (2004). Mol. Cell. 16, 59–68.
Szalai, G., Krishnamurthy, R., and Hajnoczky, G. (1999). Embo J. 18, 6349–6361.
Takeyama, N., Miki, S., Hirakawa, A., and Tanaka, T. (2002). Exp. Cell. Res. 274, 16–24.
Tenev, T., Zachariou, A., Wilson, R., Paul, A., and Meier, P. (2002). Embo J. 21, 5118–5129.
Thomenius, M. J., Wang, N. S., Reineks, E. Z., Wang, Z., and Distelhorst, C. W. (2003). J. Biol. Chem. 278, 6243–6250.
Vance, J. E. (1988). Biochim. Biophys. Acta 963, 10–20.
Vance, J. E. (1990). J. Biol. Chem. 265, 7248–7256.
Wang, H. G., Pathan, N., Ethell, I. M., Krajewski, S., Yamaguchi, Y., Shibasaki, F., McKeon, F., Bobo, T., Franke, T. F., and Reed, J. C. (1999). Science 284, 339–343.
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.
Welihinda, A. A., Tirasophon, W., and Kaufman, R. J. (1999). Gene Expr. 7, 293–300.
Wood, D. E., Thomas, A., Devi, L. A., Berman, Y., Beavis, R. C., Reed, J. C., and Newcomb, E. W. (1998). Oncogene 17, 1069–1078.
Yi, M., Weaver, D., and Hajnoczky, G. (2004). J. Cell. Biol. 167, 661–672.
Yoneda, T., Imaizumi, K., Oono, K., Yui, D., Gomi, F., Katayama, T., and Tohyama, M. (2001). J. Biol. Chem. 276, 13935–13940.
Zamzami, N., and Kroemer, G. (2001). Nat. Rev. Mol. Cell. Biol. 2, 67–71.
Zha, J., Harada, H., Yang, E., Jockel, J., and Korsmeyer, S. J. (1996). Cell 87, 619–628.
Zong, W. X., Li, C., Hatzivassiliou, G., Lindsten, T., Yu, Q. C., Yuan, J., and Thompson, C. B. (2003). J. Cell. Biol. 162, 59–69.
Zoratti, M., and Szabo, I. (1995). Biochim. Biophys. Acta 1241, 139–176.
Zorov, D. B., Filburn, C. R., Klotz, L. O., Zweier, J. L., and Sollott, S. J. (2000). J. Exp. Med. 192, 1001–1014.
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Walter, L., Hajnóczky, G. Mitochondria and Endoplasmic Reticulum: The Lethal Interorganelle Cross-Talk. J Bioenerg Biomembr 37, 191–206 (2005). https://doi.org/10.1007/s10863-005-6600-x
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DOI: https://doi.org/10.1007/s10863-005-6600-x