Biochemistry (Moscow)

, Volume 77, Issue 7, pp 761–775 | Cite as

Phenoptosis in yeasts

  • E. I. Sukhanova
  • A. G. Rogov
  • F. F. Severin
  • R. A. Zvyagilskaya
Review

Abstract

The current view on phenoptosis and apoptosis as genetic programs aimed at eliminating potentially dangerous organisms and cells, respectively, is given. Special emphasis is placed on apoptosis (phenoptosis) in yeasts: intracellular defects and a plethora of external stimuli inducing apoptosis in yeasts; distinctive morphological and biochemical hallmarks accompanying apoptosis in yeasts; pro- and antiapoptotic factors involved in yeast apoptosis signaling; consecutive stages of apoptosis from external stimulus to the cell death; a prominent role of mitochondria and other organelles in yeast apoptosis; possible pathways for release of apoptotic factors from the intermembrane mitochondrial space into the cytosol are described. Using some concrete examples, the obvious physiological importance and expediency of altruistic death of yeast cells is shown. Poorly known aspects of yeast apoptosis and prospects for yeast apoptosis study are defined.

Key words

yeasts phenoptosis apoptosis mitochondria endoplasmic reticulum vacuole 

Abbreviations

AIF

apoptosis inducing factor

AMID

AIF-homologous mitochondrion-associated inducer of death

CsA

cyclosporin A

ER

endoplasmic reticulum

HtrA

located in the intermembrane space high temperature required protease A

IAP

protein, inhibitor of apoptosis

mPTP (mitochondrial permeability transition pore)

nonspecific permeability of the inner mitochondrial membrane

OST

oligosaccharyl transferase

Pi

inorganic phosphate

ROS

reactive oxygen species

SOD

superoxide dismutase

YMUC

yeast mitochondrial unspecific channel

Ysp1p and Ysp2p

mitochondrial yeast suicide proteins

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References

  1. 1.
    Weismann, A. (1882) Uber die Dauer des Lebens, Verlag von Gustav Fisher, Jena, Germany.Google Scholar
  2. 2.
    Weismann, A. (1884) Leben and Tod, Verlag von Gustav Fisher, Jena, Germany.Google Scholar
  3. 3.
    Skulachev, V. P. (1999) Biochemistry (Moscow), 64, 1418–1426.Google Scholar
  4. 4.
    Skulachev, V. P. (2002) Ann. N. Y. Acad Sci., 959, 214–237.PubMedCrossRefGoogle Scholar
  5. 5.
    Skulachev, V. P. (2006) Apoptosis, 11, 473–485.PubMedCrossRefGoogle Scholar
  6. 6.
    Tinari, A., Garofalo, T., Sorice, M., Esposti, M. D., and Malorni, W. (2007), 3, 282–284.Google Scholar
  7. 7.
    Lyamzaev, K. G., Nepryakhina, O. K., Saprunova, V. B., Bakeeva, L. E., Pletjushkina, O. Y., Chernyak, B. V., and Skulachev, V. P. (2008) Biochim. Biophys. Acta, 1777, 817–825.PubMedCrossRefGoogle Scholar
  8. 8.
    Mijaljica, D., Prescott, M., and Devenish, R. J. (2010) Methods Mol. Biol., 648, 93–106.PubMedCrossRefGoogle Scholar
  9. 9.
    Galluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S., Gottlieb, E., Green, D. R., Hengartner, M. O., Kepp, O., Knight, R. A., Kumar, S., Lipton, S. A., Lu, X., Madeo, F., Malorni, W., Mehlen, P., Nunez, G., Peter, M. E., Piacentini, M., Rubinsztein, D. C., Shi, Y., Simon, H. U., Vandenabeele, P., White, E., Yuan, J., Zhivotovsky, B., Melino, G., and Kroemer, G. (2012) Cell Death Differ., 19, 107–120.PubMedCrossRefGoogle Scholar
  10. 10.
    Daugas, E., Nochy, D., Ravagnan, L., Loeffler, M., Susin, S. A., Zamzami, N., and Kroemer, G. (2000) FEBS Lett., 476, 118–123.PubMedCrossRefGoogle Scholar
  11. 11.
    Punj, V., and Chakrabarty, A. M. (2003) Cell Microbiol., 5, 225–231.PubMedCrossRefGoogle Scholar
  12. 12.
    Hedge, V. L., and Williams, G. T. (2002) Apoptosis, 7, 123–132.PubMedCrossRefGoogle Scholar
  13. 13.
    Zou, H., Li, Y., Liu, X., and Wang, X. (1999) J. Biol. Chem., 274, 11549–11556.PubMedCrossRefGoogle Scholar
  14. 14.
    Hanada, M., Aime-Sempe, C., Sato, T., and Reed, J. C. (1995) J. Biol. Chem., 270, 11962–11969.PubMedCrossRefGoogle Scholar
  15. 15.
    Priault, M., Camougrand, N., Kinnally, K. W., Vallette, F. M., and Manon, S. (2003) FEMS Yeast Res., 4, 15–27.PubMedCrossRefGoogle Scholar
  16. 16.
    Greenhalf, W., Stephan, C., and Chaudhuri, B. (1996) FEBS Lett., 380, 169–175.PubMedCrossRefGoogle Scholar
  17. 17.
    Manon, S. (2004) Antioxid. Redox. Signal., 6, 259–267.PubMedCrossRefGoogle Scholar
  18. 18.
    Ink, B., Zornig, M., Baum, B., Hajibagheri, N., James, C., and Chittenden, T. (1997) Mol. Cell. Biol., 17, 2468–2474.PubMedGoogle Scholar
  19. 19.
    Jurgensmeier, J. M., Krajewski, S., Armstrong, R. C., Wilson, G. M., Oltersdorf, T., and Fritz, L. C. (1997) Mol. Biol. Cell, 8, 325–339.PubMedGoogle Scholar
  20. 20.
    Martinet, W., van den Plas, D., Raes, H., Reekmans, R., and Contreras, R. (1999) Biotechnol. Lett., 21, 821–829.CrossRefGoogle Scholar
  21. 21.
    Poliakova, D., Sokolikova, B., Kolarov, J., and Sabova, L. (2002) Microbiology, 148, 2789–2795.PubMedGoogle Scholar
  22. 22.
    De Smet, K., Eberhardt, I., Reekmans, R., and Contreras, R. (2004) Yeast, 21, 1325–1334.PubMedCrossRefGoogle Scholar
  23. 23.
    Madeo, F., Frohlich, E., and Frohlich, K. U. (1997) J. Cell Biol., 139, 729–734.PubMedCrossRefGoogle Scholar
  24. 24.
    Madeo, F., Herker, E., Maldener, C., Wissing, S., Lachelt, S., Herlan, M., Fehr, M., Lauber, K., Sigrist, S. J., Wesselborg, S., and Frohlich, K. U. (2002) Mol. Cell, 9, 911–917.PubMedCrossRefGoogle Scholar
  25. 25.
    Webb, J. S., Givskov, M., and Kjelleberg, S. (2003) Curr. Opin. Microbiol., 6, 578–585.PubMedCrossRefGoogle Scholar
  26. 26.
    Vachova, L., and Palkova, Z. (2005) J. Cell. Biol., 169, 711–717.PubMedCrossRefGoogle Scholar
  27. 27.
    Palkova, Z., Vachova, L., Gaskova, D., and Kucerova, H. (2009) Mol. Membr. Biol., 26, 228–235.PubMedCrossRefGoogle Scholar
  28. 28.
    Vachova, L., Chernyavskiy, O., Strachotova, D., Bianchini, P., Burdikova, Z., Fercikova, I., Kubinova, L., and Palkova, Z. (2009) Environ. Microbiol., 11, 1866–1877.PubMedCrossRefGoogle Scholar
  29. 29.
    Vachova, L., Kucerova, H., Devaux, F., Ulehlova, M., and Palkova, Z. (2009) Environ. Microbiol., 11, 494–504.PubMedCrossRefGoogle Scholar
  30. 30.
    Chen, H., and Fink, G. R. (2006) Genes Dev., 20, 1150–1161.PubMedCrossRefGoogle Scholar
  31. 31.
    Palkova, Z., and Vachova, L. (2006) FEMS Microbiol. Rev., 30, 806–824.PubMedCrossRefGoogle Scholar
  32. 32.
    Cap, M., Vachova, L., and Palkova, Z. (2010) Commun. Integr. Biol., 3, 198–200.PubMedCrossRefGoogle Scholar
  33. 33.
    Lee, R. E., Brunette, S., Puente, L. G., and Megeney, L. A. (2010) Proc. Natl. Acad. Sci. USA, 107, 13348–13353.PubMedCrossRefGoogle Scholar
  34. 34.
    Cheng, W. C., Leach, K. M., and Hardwick, J. M. (2008) Biochim. Biophys. Acta, 1783, 1272–1279.PubMedCrossRefGoogle Scholar
  35. 35.
    Belanger, K. D., Walter, D., Henderson, T. A., Yelton, A. L., O’Brien, T. G., Belanger, K. G., Geier, S. J., and Fahrenkrog, B. (2009) J. Cell Sci., 122, 3931–3941.PubMedCrossRefGoogle Scholar
  36. 36.
    Fahrenkrog, B. (2011) Biochem. Soc. Trans., 39, 1499–1501.PubMedCrossRefGoogle Scholar
  37. 37.
    Wissing, S., Ludovico, P., Herker, E., Buttner, S., Engelhardt, S. M., Decker, T., Link, A., Proksch, A., Rodrigues, F., Corte-Real, M., Frohlich, K. U., Manns, J., Cande, C., Sigrist, S. J., Kroemer, G., and Madeo, F. (2004) J. Cell. Biol., 166, 969–974.PubMedCrossRefGoogle Scholar
  38. 38.
    Li, W., Sun, L., Liang, Q., Wang, J., Mo, W., and Zhou, B. (2006) Mol. Biol. Cell, 17, 1802–1811.PubMedCrossRefGoogle Scholar
  39. 39.
    Fannjiang, Y., Cheng, W. C., Lee, S. J., Qi, B., Pevsner, J., McCaffer, J. M., Hill, R. B., Basanez, G., and Hardwick, J. M. (2004) Genes Dev., 18, 2785–2797.PubMedCrossRefGoogle Scholar
  40. 40.
    Ludovico, P., Rodrigues, F., Almeida, A., Silva, M. T., Barrientos, A., and Corte-Real, M. (2002) Mol. Biol. Cell, 13, 2598–2606.PubMedCrossRefGoogle Scholar
  41. 41.
    Silva, R. D., Sotoca, R., Johansson, B., Ludovico, P., Sansonetty, F., Silva, M. T., Peinado, J. M., and Corte-Real, M. (2005) Mol. Microbiol., 58, 824–834.PubMedCrossRefGoogle Scholar
  42. 42.
    Buttner, S., Eisenberg, T., Carmona-Gutierrez, D., Ruli, D., Knauer, H., Ruckenstuhl, C., Sigrist, C., Wissing, S., Kollroser, M., Frohlich, K. U., Sigrist, S., and Madeo, F. (2007) Mol. Cell., 25, 233–246.PubMedCrossRefGoogle Scholar
  43. 43.
    Cymerman, I. A., Chung, I., Beckmann, B. M., Bujnicki, J. M., and Meiss, G. (2008) Nucleic Acids Res., 36, 1369–1379.PubMedCrossRefGoogle Scholar
  44. 44.
    Qiu, J., Yoon, J. H., and Shen, B. (2005) J. Biol. Chem., 280, 15370–15379.PubMedCrossRefGoogle Scholar
  45. 45.
    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.PubMedCrossRefGoogle Scholar
  46. 46.
    Sokolov, S., Pozniakovsky, A., Bocharova, N., Knorre, D., and Severin, F. (2006) Biochim. Biophys. Acta, 1757, 660–666.PubMedCrossRefGoogle Scholar
  47. 47.
    Singh, K., Kang, P. J., and Park, H. O. (2008) Proc. Natl. Acad. Sci. USA, 105, 1522–1527.PubMedCrossRefGoogle Scholar
  48. 48.
    Yang, H., Ren, Q., and Zhang, Z. (2008) Mol. Biol. Cell., 19, 2127–2134.PubMedCrossRefGoogle Scholar
  49. 49.
    Buttner, S., Ruli, D., Vogtle, F. N., Galluzzi, L., Moitzi, B., Eisenberg, T., Kepp, O., Habernig, L, Carmona-Gutierrez, D., Rockenfeller, P., Laun, P., Breitenbach, M., Khoury, C., Frohlich, K. U., Rechberger, G., Meisinger, C., Kroemer, G., and Madeo, F. (2011) EMBO J., 30, 2779–2792.PubMedCrossRefGoogle Scholar
  50. 50.
    Eisenberg, T., Buttner, S., Kroemer, G., and Madeo, F. (2007) Apoptosis, 12, 1011–1023.PubMedCrossRefGoogle Scholar
  51. 51.
    Greenwood, M. T., and Ludovico, P. (2010) Cell Death Differ., 17, 737–745.PubMedCrossRefGoogle Scholar
  52. 52.
    Walter, D., Matter, A., and Fahrenkrog, B. M. E. (2010) J. Cell Sci., 123, 1931–1939.PubMedCrossRefGoogle Scholar
  53. 53.
    Cebulski, J., Malouin, J., Pinches, N., Cascio, V., and Austriaco, N. (2011) PLoS One, 6, e20882.PubMedCrossRefGoogle Scholar
  54. 54.
    Williams, D., Norman, G., Khoury, C., Metcalfe, N., Briard, J., Laporte, A., Sheibani, S., Portt, L., Mandato, C. A., and Greenwood, M. T. (2011) Biochim. Biophys. Acta, 1813, 315–321.PubMedCrossRefGoogle Scholar
  55. 55.
    Goldberg, A. A., Richard, V. R., Kyryakov, P., Bourque, S. D., Beach, A., Burstein, M. T., Glebov, A., Koupaki, O., Boukh-Viner, T., Gregg, C., Juneau, M., English, A. M., Thomas, D. Y., and Titorenko, V. I. (2010) Aging (Albany N.Y.), 2, 393–414.Google Scholar
  56. 56.
    Low, C. P., Shui, G., Liew, L. P., Buttner, S., Madeo, F., Dawes, I. W., Wenk, M. R., and Yang, H. (2008) J. Cell. Sci., 121, 2671–2684.PubMedCrossRefGoogle Scholar
  57. 57.
    Perez, P., and Cansado, J. (2010) Curr. Protein Pept. Sci., 11, 680–692.PubMedCrossRefGoogle Scholar
  58. 58.
    Almeida, B., Buttner, S., Ohlmeier, S., Silva, A., Mesquita, A., Sampaio-Marques, B., Osorio, N. S., Kollau, A., Mayer, B., Leao, C., Laranjinha, J., Rodrigues, F., Madeo, F., and Ludovico, P. (2007) J. Cell. Sci., 120, 3279–3288.PubMedCrossRefGoogle Scholar
  59. 59.
    Almeida, B., Silva, A., Mesquita, A., Sampaio-Marques, B., Rodrigues, F., and Ludovico, P. (2008) Biochim. Biophys. Acta, 1783, 1436–1448.PubMedCrossRefGoogle Scholar
  60. 60.
    Madeo, F., and Frohlich, K. U. (2008) Biochim. Biophys. Acta, 1783, 1271.PubMedCrossRefGoogle Scholar
  61. 61.
    Schmitt, M. J., and Reiter, J. (2008) Biochim. Biophys. Acta, 1783, 1413–1417.PubMedCrossRefGoogle Scholar
  62. 62.
    Severin, F. F., Meer, M. V., Smirnova, E. A., Knorre, D. A., and Skulachev, V. P. (2008) Biochim. Biophys. Acta, 1783, 1350–1353.PubMedCrossRefGoogle Scholar
  63. 63.
    Weinberger, M., Ramachandran, L., Feng, L., Sharma, K., Sun, X., Marchetti, M., Huberman, J. A., and Burhans, W. C. (2005) J. Cell. Sci., 118, 3543–3553.PubMedCrossRefGoogle Scholar
  64. 64.
    Weinberger, M., Feng, L., Paul, A., Smith, D. L., Jr., Hontz, R. D., Smith, J. S., Vujcic, M., Singh, K. K., Huberman, J. A., and Burhans, W. C. (2007) PLoS One, 2, e748.PubMedCrossRefGoogle Scholar
  65. 65.
    Yamaki, M., Umehara, T., Chimura, T., and Horikoshi, M. (2001) Genes Cells, 6, 1043–1054.PubMedCrossRefGoogle Scholar
  66. 66.
    Ren, Q., Yang, H., Rosinski, M., Conrad, M. N., Dresser, M. E., Guacci, V., and Zhang, Z. (2005) Mutat. Res., 570, 163–173.PubMedCrossRefGoogle Scholar
  67. 67.
    Caron, P., Aymard, F., Iacovoni, J. S., Briois, S., Canitrot, Y., Bugler, B., Massip, L., Losada, A., and Legube, G. (2012) PLoS Genet., 8, e1002460.PubMedCrossRefGoogle Scholar
  68. 68.
    Mazzoni, C., Herker, E., Palermo, V., Jungwirth, H., Eisenberg, T., Madeo, F., and Falcone, C. (2005) EMBO Rep., 6, 1076–1081.PubMedCrossRefGoogle Scholar
  69. 69.
    Gourlay, C. W., and Ayscough, K. R. (2006) Mol. Cell. Biol., 26, 6487–6501.PubMedCrossRefGoogle Scholar
  70. 70.
    Narasimhan, M. L., Damsz, B., Coca, M. A., Ibeas, J. I., Yun, D. J., Pardo, J. M., Hasegawa, P. M., and Bressan, R. A. (2001) Mol. Cell., 8, 921–930.PubMedCrossRefGoogle Scholar
  71. 71.
    Gourlay, C. W., and Ayscough, K. R. (2005) J. Cell. Sci., 118, 2119–2132.PubMedCrossRefGoogle Scholar
  72. 72.
    Hauptmann, P., Riel, C., Kunz-Schughart, L. A., Frohlich, K. U., Madeo, F., and Lehle, L. (2006) Mol. Microbiol., 59, 765–778.PubMedCrossRefGoogle Scholar
  73. 73.
    Kang, M. S., Lee, S. K., Park, C. S., Kang, J. H., Bae, S. H., and Yu, S. L. (2008) Biochem. Biophys. Res. Commun., 376, 305–309.PubMedCrossRefGoogle Scholar
  74. 74.
    Hong, J., Zhang, J., Liu, Z., Qin, S., Wu, J., and Shi, Y. (2009) Biochemistry, 48, 6824–6834.PubMedCrossRefGoogle Scholar
  75. 75.
    Walling, H. W., Baldassare, J. J., and Westfall, T. C. (1998) J. Neurosci. Res., 54, 301–308.PubMedCrossRefGoogle Scholar
  76. 76.
    Madeo, F., Frohlich, E., Ligr, M., Grey, M., Sigrist, S. J., Wolf, D. H., and Frohlich, K. U. (1999) J. Cell. Biol., 145, 757–767.PubMedCrossRefGoogle Scholar
  77. 77.
    Silva, R. D., Manon, S., Goncalves, J., Saraiva, L., and Corte-Real, M. (2011) Exp. Cell Res., 317, 781–790.PubMedCrossRefGoogle Scholar
  78. 78.
    Guerin, R., Beauregard, P. B., Leroux, A., and Rokeach, L. A. (2009) PLoS One, 4, e6244.PubMedCrossRefGoogle Scholar
  79. 79.
    Arcangioli, B., and Ben Hassine, S. (2009) Cell Cycle, 8, 2326–2331.PubMedCrossRefGoogle Scholar
  80. 80.
    Kochmak, S. A., Knorre, D. A., Sokolov, S. S., and Severin, F. F. (2011) Biochemistry (Moscow), 76, 167–171.CrossRefGoogle Scholar
  81. 81.
    Godon, C., Lagniel, G., Lee, J., Buhler, J. M., Kieffer, S., Perrot, M., Boucherie, H., Toledano, M. B., and Labarre, J. (1998) J. Biol. Chem., 273, 22480–22489.PubMedCrossRefGoogle Scholar
  82. 82.
    Costa, V. M., Amorim, M. A., Quintanilha, A., and Moradas-Ferreira, P. (2002) Free Radic. Biol. Med., 33, 1507–1515.PubMedCrossRefGoogle Scholar
  83. 83.
    Magherini, F., Tani, C., Gamberi, T., Caselli, A., Bianchi, L., Bini, L., and Modesti, A. (2007) Proteomics, 7, 1434–1445.PubMedCrossRefGoogle Scholar
  84. 84.
    Sollner, S., Durchschlag, M., Frohlich, K. U., and Macheroux, P. (2009) FEMS Yeast Res., 9, 885–891.PubMedCrossRefGoogle Scholar
  85. 85.
    Gruhlke, M. C., Portz, D., Stitz, M., Anwar, A., Schneider, T., Jacob, C., Schlaich, N. L., and Slusarenko, A. J. (2010) Free Radic. Biol. Med., 49, 1916–1924.PubMedCrossRefGoogle Scholar
  86. 86.
    Del Carratore, R., Della Croce, C., Simili, M., Taccini, E., Scavuzzo, M., and Sbrana, S. (2002) Mutat. Res., 513, 183–191.PubMedCrossRefGoogle Scholar
  87. 87.
    Gao, Q., Ren, Q., Liou, L. C., Bao, X., and Zhang, Z. (2011) FEBS Lett., 585, 2507–2512.PubMedCrossRefGoogle Scholar
  88. 88.
    Gourlay, C. W., Du, W., and Ayscough, K. R. (2006) Mol. Microbiol., 62, 1515–1521.PubMedCrossRefGoogle Scholar
  89. 89.
    Severin, F. F., and Hyman, A. A. (2002) Curr. Biol., 12, R233–R235.PubMedCrossRefGoogle Scholar
  90. 90.
    Knorre, D. A., Smirnova, E. A., and Severin, F. F. (2005) Biochemistry (Moscow), 70, 264–266.CrossRefGoogle Scholar
  91. 91.
    Rodriguez-Cousino, N., Maqueda, M., Ambrona, J., Zamora, E., Esteban, R., and Ramirez, M. (2011) Appl. Environ. Microbiol., 77, 1822–1832.PubMedCrossRefGoogle Scholar
  92. 92.
    Weiler, F., Rehfeldt, K., Bautz, F., and Schmitt, M. J. (2002) Mol. Microbiol., 46, 1095–1105.PubMedCrossRefGoogle Scholar
  93. 93.
    Weiler, F., and Schmitt, M. J. (2003) FEMS Yeast Res., 3, 69–76.PubMedGoogle Scholar
  94. 94.
    Klassen, R., and Meinhardt, F. (2005) Cell. Microbiol., 7, 393–401.PubMedCrossRefGoogle Scholar
  95. 95.
    Reiter, J., Herker, E., Madeo, F., and Schmitt, M. J. (2005) J. Cell Biol., 168, 353–358.PubMedCrossRefGoogle Scholar
  96. 96.
    Ivanovska, I., and Hardwick, J. M. (2005) J. Cell Biol., 170, 391–399.PubMedCrossRefGoogle Scholar
  97. 97.
    Baeza, M. E., Sanhueza, M. A., and Cifuentes, V. H. (2008) Biol. Res., 41, 173–182.PubMedCrossRefGoogle Scholar
  98. 98.
    Josse, L., Li, X., Coker, R. D., Gourlay, C. W., and Evans, I. H. (2011) FEMS Yeast Res., 11, 133–150.PubMedCrossRefGoogle Scholar
  99. 99.
    Wu, X. Z., Chang, W. Q., Cheng, A. X., Sun, L. M., and Lou, H. X. (2010) Biochim. Biophys. Acta, 1800, 439–447.PubMedCrossRefGoogle Scholar
  100. 100.
    Al-Dhaheri, R. S., and Douglas, L. J. (2010) J. Med. Microbiol., 59, 149–157.PubMedCrossRefGoogle Scholar
  101. 101.
    Keyhani, E., and Keyhani, J. (2004) Ann. N. Y. Acad. Sci., 1030, 369–376.PubMedCrossRefGoogle Scholar
  102. 102.
    Dai, B. D., Cao, Y. Y., Huang, S., Xu, Y. G., Gao, P. H., Wang, Y., and Jiang, Y. Y. (2009) J. Microbiol. Biotechnol., 19, 803–809.PubMedGoogle Scholar
  103. 103.
    Kang, K., Fong, W. P., and Tsang, P. W. (2010) Mycopathology, 170, 391–396.CrossRefGoogle Scholar
  104. 104.
    Keyhani, E., Khavari-Nejad, S., Keyhani, J., and Attar, F. (2009) Ann. N. Y. Acad. Sci., 1171, 284–291.PubMedCrossRefGoogle Scholar
  105. 105.
    Kang, K., Wong, K. S., Fong, W. P., and Tsang, P. W. (2011) Fungal Biol., 115, 302–309.PubMedCrossRefGoogle Scholar
  106. 106.
    Bink, A., Govaert, G., Francois, I. E., Pellens, K., Meerpoel, L., Borgers, M., van Minnebruggen, G., Vroome, V., Cammue, B. P., and Thevissen, K. (2010) FEMS Yeast Res., 10, 812–818.PubMedCrossRefGoogle Scholar
  107. 107.
    Mears, J. A., Lackner, L. L., Fang, S., Ingerman, E., Nunnari, J., and Hinshaw, J. E. (2011) Nat. Struct. Mol. Biol., 18, 20–26.PubMedCrossRefGoogle Scholar
  108. 108.
    Singh, N. K., Bracker, C. A., Hasegawa, P. M., Handa, A. K., Buckel, S., Hermodson, M. A., Pfankoch, E., Regnier, F. E., and Bressan, R. A. (1987) Plant. Physiol., 85, 529–536.PubMedCrossRefGoogle Scholar
  109. 109.
    Narasimhan, M. L., Coca, M. A., Jin, J., Yamauchi, T., Ito, Y., Kadowaki, T., Kim, K. K., Pardo, J. M., Damsz, B., Hasegawa, P. M., Yun, D. J., and Bressan, R. A. (2005) Mol. Cell, 17, 171–180.PubMedCrossRefGoogle Scholar
  110. 110.
    Xu, C., Wang, J., Gao, Y., Lin, H., Du, L., Yang, S., Long, S., She, Z., Cai, X., Zhou, S., and Lu, Y. (2010) FEMS Yeast Res., 10, 297–308.PubMedCrossRefGoogle Scholar
  111. 111.
    Hwang, B., Hwang, J. S., Lee, J., and Lee, D. G. (2011) Biochem. Biophys. Res. Commun., 405, 267–271.PubMedCrossRefGoogle Scholar
  112. 112.
    Cho, J., and Lee, D. G. (2011) Biochimie, 93, 1873–1879.PubMedCrossRefGoogle Scholar
  113. 113.
    Hwang, B., Hwang, J. S., Lee, J., Kim, J. K., Kim, S. R., Kim, Y., and Lee, D. G. (2011) Biochem. Biophys. Res. Commun., 408, 89–93.PubMedCrossRefGoogle Scholar
  114. 114.
    Park, C., and Lee, D. G. (2010) Biochem. Biophys. Res. Commun., 394, 170–172.PubMedCrossRefGoogle Scholar
  115. 115.
    Liang, Q., and Zhou, B. (2007) Mol. Biol. Cell, 18, 4741–4749.PubMedCrossRefGoogle Scholar
  116. 116.
    Bussche, J. V., and Soares, E. V. (2011) Appl. Microbiol. Biotechnol., 90, 679–687.PubMedCrossRefGoogle Scholar
  117. 117.
    Gardarin, A., Chedin, S., Lagniel, G., Aude, J. C., Godat, E., Catty, P., and Labarre, J. (2010) Mol. Microbiol., 76, 1034–1048.PubMedCrossRefGoogle Scholar
  118. 118.
    Buttner, S., Eisenberg, T., Herker, E., Carmona-Gutierrez, D., Kroemer, G., and Madeo, F. (2006) J. Cell Biol., 175, 521–525.PubMedCrossRefGoogle Scholar
  119. 119.
    Lewinska, A., Macierzynska, E., Grzelak, A., and Bartosz, G. (2011) Biogerontology, 12, 309–320.PubMedCrossRefGoogle Scholar
  120. 120.
    Ruckenstuhl, C., Carmona-Gutierrez, D., and Madeo, F. (2010) Aging (Albany N.Y.), 2, 643–649.Google Scholar
  121. 121.
    Kitagaki, H., Araki, Y., Funato, K., and Shimoi, H. (2007) FEBS Lett., 581, 2935–2942.PubMedCrossRefGoogle Scholar
  122. 122.
    Shirtliff, M. E., Krom, B. P., Meijering, R. A., Peters, B. M., Zhu, J., Scheper, M. A., Harris, M. L., and Jabra-Rizk, M. A. (2009) Antimicrob. Agents. Chemother., 53, 2392–2401.PubMedCrossRefGoogle Scholar
  123. 123.
    Aoshima, H., Kadoya, K., Taniguchi, H., Satoh, T., and Hatanaka, H. (1999) Biosci. Biotechnol. Biochem., 63, 1025–1031.PubMedCrossRefGoogle Scholar
  124. 124.
    Du, L., Su, Y., Sun, D., Zhu, W., Wang, J., Zhuang, X., Zhou, S., and Lu, Y. (2008) FEMS Yeast Res., 8, 531–539.PubMedCrossRefGoogle Scholar
  125. 125.
    Ludovico, P., Sansonetty, M. T., and Corte-Real, M. (2003) FEMS Yeast Res., 3, 91–96.PubMedGoogle Scholar
  126. 126.
    Giannattasio, S., Guaragnella, N., Corte-Real, M., Passarella, S., and Marra, E. (2005) Gene, 354, 93–98.PubMedCrossRefGoogle Scholar
  127. 127.
    Burhans, W. C., and Weinberger, M. (2009) Cell Cycle, 8, 2300–2302.PubMedCrossRefGoogle Scholar
  128. 128.
    Guaragnella, N., Passarella, S., Marra, E., and Giannattasio, S. (2010) FEBS Lett., 584, 3655–3660.PubMedCrossRefGoogle Scholar
  129. 129.
    Mitsui, K., Nakagawa, D., Nakamura, M., Okamoto, T., and Tsurugi, K. (2005) FEBS Lett., 579, 723–727.PubMedCrossRefGoogle Scholar
  130. 130.
    Mutoh, N., Kitajima, S., and Ichihara, S. (2011) Biosci. Biotechnol. Biochem., 75, 1113–1118.PubMedCrossRefGoogle Scholar
  131. 131.
    Sapienza, K., Bannister, W., and Balzan, R. (2008) Microbiology, 154, 2740–2747.PubMedCrossRefGoogle Scholar
  132. 132.
    Carmona-Gutierrez, D., Reisenbichler, A., Heimbucher, P., Bauer, M. A., Braun, R. J., Ruckenstuhl, C., Buttner, S., Eisenberg, T., Rockenfeller, P., Frohlich, K. U., Kroemer, G., and Madeo, F. (2011) Cell Cycle, 10, 3973–3978.PubMedCrossRefGoogle Scholar
  133. 133.
    De Castro, P. A., Savoldi, M., Bonatto, D., Barros, M. H., Goldman, M. H., Berretta, A. A., and Goldman, G. H. (2011) Eukaryot. Cell, 10, 398–411.PubMedCrossRefGoogle Scholar
  134. 134.
    Chahomchuen, T., Akiyama, K., Sekito, T., Sugimoto, N., Okabe, M., Nishimoto, S., Sugahara, T., and Kakinuma, Y. (2009) J. Toxicol. Sci., 34, 541–545.PubMedCrossRefGoogle Scholar
  135. 135.
    Ozhovan, S. M., Knorre, D. A., Severin, F. F., and Bakeeva, L. E. (2009) Tsitologiya, 51, 911–916.Google Scholar
  136. 136.
    Wu, J., Min, R., Wu, M., and Chen, W. (2011) Mol. Med. Rept., 4, 357–362.Google Scholar
  137. 137.
    Stoodley, P., Sauer, K., Davies, D. G., and Costerton, J. W. (2002) Annu. Rev. Microbiol., 56, 187–209.PubMedCrossRefGoogle Scholar
  138. 138.
    Vopalenska, I., Hulkova, M., Janderova, B., and Palkova, Z. (2005) Res. Microbiol., 156, 921–931.PubMedCrossRefGoogle Scholar
  139. 139.
    Pereira, C., Silva, R. D., Saraiva, L., Johansson, B., Sousa, M. J., and Corte-Real, M. (2008) Biochim. Biophys. Acta, 1783, 1286–1302.PubMedCrossRefGoogle Scholar
  140. 140.
    Aerts, A. M., Zabrocki, P., Govaert, G., Mathys, J., Carmona-Gutierrez, D., Madeo, F., Winderickx, J., Cammue, B. P., and Thevissen, K. (2009) FEBS Lett., 583, 113–117.PubMedCrossRefGoogle Scholar
  141. 141.
    Kissova, I., Plamondon, L. T., Brisson, L., Priault, M., Renouf, V., Schaeffer, J., Camougrand, N., and Manon, S. (2006) J. Biol. Chem., 281, 36187–36197.PubMedCrossRefGoogle Scholar
  142. 142.
    Pineau, L., and Ferreira, T. (2010) FEMS Yeast Res., 10, 1035–1045.PubMedCrossRefGoogle Scholar
  143. 143.
    Sousa, M. J., Azevedo, F., Pedras, A., Marques, C., Coutinho, O. P., Preto, A., Geros, H., Chaves, S. R., and Corte-Real, M. (2011) Biochem. Soc. Trans., 39, 1533–1537.PubMedCrossRefGoogle Scholar
  144. 144.
    Sheridan, C., Delivani, P., Cullen, S. P., and Martin, S. J. (2008) Mol. Cell, 31, 570–585.PubMedCrossRefGoogle Scholar
  145. 145.
    Yamaguchi, R., Lartigue, L., Perkins, G., Scott, R. T., Dixit, A., Kushnareva, Y., Kuwana, T., Ellisman, V. Y., and Newmeyer, D. D. (2008) Mol. Cell, 31, 557–569.PubMedCrossRefGoogle Scholar
  146. 146.
    Colin, J., Garibal, J., Mignotte, B., and Guenal, I. (2009) Biochem. Biophys. Res. Commun., 379, 931–943.CrossRefGoogle Scholar
  147. 147.
    Lucken-Ardjomande, S., Montessuit, S., and Martinou, J. C. (2008) Cell Death Differ., 15, 923–937.Google Scholar
  148. 148.
    Bernardi, P., Krauskopf, A., Basso, E., Petronilli, V., Blachly-Dyson, E., Di Lisa, F., and Forte, M. A. (2006) FEBS J., 273, 2077–2099.PubMedCrossRefGoogle Scholar
  149. 149.
    Leung, A. W., and Halestrap, A. P. (2008) Biochim. Biophys. Acta, 1777, 946–952.PubMedCrossRefGoogle Scholar
  150. 150.
    Halestrap, A. P. (2009) J. Mol. Cardiol., 46, 821–831.CrossRefGoogle Scholar
  151. 151.
    Sultan, A., and Sokolove, P. (2001) Arch. Biochem. Biophys., 386, 52–61.PubMedCrossRefGoogle Scholar
  152. 152.
    Mironova, G. D., Gateau-Roesch, O., Levrat, C., Gritsenko, E., Pavlov, E., Lazareva, A. V., Limarenko, E., Rey, P., Louisot, P., and Saris, N.-E. L. (2001) J. Bioenerg. Biomembr., 33, 319–331.PubMedCrossRefGoogle Scholar
  153. 153.
    Kristian, T., Bernardi, P., and Siesjo, B. K. (2001) J. Neurotrauma, 18, 1059–1074.PubMedCrossRefGoogle Scholar
  154. 154.
    Knorre, D. A., Dedukhova, V. I., Vyssokikh, M. Y., and Mokhova, E. N. (2003) Biosci. Rep., 23, 67–75.PubMedCrossRefGoogle Scholar
  155. 155.
    Chavez, E., Moreno-Sanchez, R., Zazueta, C., Rodriguez, J. S., Bravo, C., and Reyes-Vivas, H. (1997) J. Bioenerg. Biomembr., 29, 571–577.PubMedCrossRefGoogle Scholar
  156. 156.
    Kuzminova, A. E., Zhuravlyova, A. V., Vyssokikh, M. Yu., Zorova, L. D., Krasnikov, B. F., and Zorov, D. B. (1998) FEBS Lett., 434, 313–316.PubMedCrossRefGoogle Scholar
  157. 157.
    Kovaleva, M. V., Sukhanova, E. I., Trendeleva, T. A., Zyl’kova, M. V., Ural’skaya, L. A., Popova, K. M., Saris, N. E., and Zvyagilskaya, R. A. (2009) J. Bioenerg. Biomembr., 41, 239–249.PubMedCrossRefGoogle Scholar
  158. 158.
    Kovaleva, M. V., Sukhanova, E. I., Trendeleva, T. A., Popova, K. M., Zylkova, M. V., Uralskaya, L. A., and Zvyagilsksya, R. A. (2010) Biochemistry (Moscow), 75, 297–303.CrossRefGoogle Scholar
  159. 159.
    Trendeleva, T., Sukhanova, E., Ural’skaya, L., Saris, N.-E., and Zvyagilskaya, R. (2011) J. Bienerg. Biomembr., 43, 623–631.CrossRefGoogle Scholar
  160. 160.
    Trendeleva, T., Sukhanova, E., Ural’skaya, L., Saris, N.-E., and Zvyagilskaya, R. (2011) J. Bienerg. Biomembr., 43, 633–644.CrossRefGoogle Scholar
  161. 161.
    Holman, J. D., and Hand, S. C. (2009) J. Exp. Mar. Bio. Ecol., 376, 85–93.PubMedCrossRefGoogle Scholar
  162. 162.
    Prieto, S., Bouillaud, F., Ricquier, D., and Rial, E. (1992) Eur. J. Biochem., 208, 487–491.PubMedCrossRefGoogle Scholar
  163. 163.
    Prieto, S., Bouillaud, F., and Rial, E. (1995) Biochem. J., 307, 657–661.PubMedGoogle Scholar
  164. 164.
    Prieto, S., Bouillaud, F., and Rial, E. (1996) Arch. Biochem. Biophys., 334, 43–49.PubMedCrossRefGoogle Scholar
  165. 165.
    Roucou, X., Manon, S., and Guerin, M. (1997) Biochem. Mol. Biol. Int., 43, 53–61.PubMedGoogle Scholar
  166. 166.
    Manon, S., and Guerin, M. (1998) Biochem. Mol. Biol. Int., 44, 565–575.PubMedGoogle Scholar
  167. 167.
    Manon, S., Roucou, X., Guerin, M., Rigoulet, M., and Guerin, B. (1998) J. Bioenerg. Biomembr., 30, 419–429.PubMedCrossRefGoogle Scholar
  168. 168.
    Gutierrez-Aguilar, M., Perez-Vazquez, V., Bunoust, O., Manon, S., Rigoulet, M., and Uribe, S. (2007) Biochim. Biophys. Acta, 1767, 1245–1251.PubMedCrossRefGoogle Scholar
  169. 169.
    Trendeleva, T., Sukhanova, E. I., Kovaleva, M. V., Uralskaya, L. A., and Zvyagilskaya, R. A. (2011) Papers Int. Conf. “Receptors and Intercellular Signaling” (Zinchenko, V. P., Kolesnikova, S. S., and Berezhnova, A. V., eds.) Pushchino, Vol. 2, pp. 732–737.Google Scholar
  170. 170.
    Madeo, F., Herker, E., Wissing, S., Jungwirth, H., Eisenberg, T., and Frohlich, K. U. (2004) Curr. Opin. Microbiol., 7, 655–660.PubMedCrossRefGoogle Scholar
  171. 171.
    Ludovico, P., Madeo, F., and Silva, M. (2005) IUBMB Life, 57, 129–135.PubMedCrossRefGoogle Scholar
  172. 172.
    Lisa-Santamaria, P., Neiman, A. M., Cuesta-Marban, A., Mollinedo, F., Revuelta, J. L., and Jimenez, A. (2009) Biochim. Biophys. Acta, 1793, 561–571.PubMedCrossRefGoogle Scholar
  173. 173.
    Silva, R. D., Manon, S., Goncalves, J., Saraiva, L., and Corte-Real, M. (2011) Curr. Pharm. Des., 17, 246–255.PubMedCrossRefGoogle Scholar
  174. 174.
    Flower, T. R., Chesnokova, L. S., Froelich, C. A., Dixon, C., and Witt, S. N. (2005) J. Mol. Biol., 351, 1081–1100.PubMedCrossRefGoogle Scholar
  175. 175.
    Bocharova, N., Chave-Cox, R., Sokolov, S., Knorre, D., and Severin, F. (2009) Biochemistry (Moscow), 74, 231–234.CrossRefGoogle Scholar
  176. 176.
    Owsianowski, E., Walter, D., and Fahrenkrog, B. (2008) Biochim. Biophys. Acta, 1783, 1303–1310.PubMedCrossRefGoogle Scholar
  177. 177.
    Perrone, G. G., Tan, S. X., and Dawes, I. W. (2008) Biochim. Biophys. Acta, 1783, 1354–1368.PubMedCrossRefGoogle Scholar
  178. 178.
    Huh, G. H., Damsz, B., Matsumoto, T. K., Reddy, M. P., Rus, A. M., Ibeas, J. I., Narasimhan, M. L., Bressan, R. A., and Hasegawa, P. M. (2002) Plant J., 29, 649–659.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  • E. I. Sukhanova
    • 1
  • A. G. Rogov
    • 1
  • F. F. Severin
    • 2
  • R. A. Zvyagilskaya
    • 1
  1. 1.Bach Institute of BiochemistryRussian Academy of SciencesMoscowRussia
  2. 2.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia

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