Skip to main content
SpringerLink
Log in

Apoptosis in Unicellular Organisms: Mechanisms and Evolution

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

Abstract

Data about the programmed death (apoptosis) in unicellular organisms, from bacteria to ciliates, are discussed. Firstly apoptosis appeared in lower eukaryotes, but its mechanisms in these organisms are different from the classical apoptosis. During evolution, the apoptotic process has been improving gradually, with reactive oxygen species and Ca2+ playing an essential role in triggering apoptosis. All eukaryotic organisms have apoptosis inhibitors, which might be introduced by viruses. In the course of evolution, caspases and apoptosis-inducing factor appeared before other apoptotic proteins, with socalled death receptors being the last among them. The functional analogs of eukaryotic apoptotic proteins take parts in the programmed death of bacteria.

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

REFERENCES

  1. Samuilov, V.D., Oleskin, A.V., and Lagunova, E.M. (2000) Biochemistry(Moscow), 65,873–887.

    Google Scholar 

  2. Ameisen, J.C. (1996) Science,272,1278–1279.

    Google Scholar 

  3. Lewis, K. (2000) Microbiol. Mol. Rev.,64,503–514.

    Google Scholar 

  4. Proskuryakov, S.Y., Gabaj, V.L., and Konoplyannikov, A. G. (2002) Biochemistry(Moscow), 67,387–408.

    Google Scholar 

  5. Mills, J.C., Stone, N.L., and Pittman, R.N. (1999) J. Cell. Biol.,146,703–708.

    Google Scholar 

  6. Hanayama, R., Tanaka, M., Miwa, K., Shinohara, A., Iwamatsu, A., and Nagata, S. (2002) Nature,417,182–187.

    Google Scholar 

  7. Strasser, A., O'Connor, L., and Vishva, M.D. (2002) Annu. Rev. Biochem.,69,217–245.

    Google Scholar 

  8. Kruman, I.I., and Mattson, M.P. (1999) J. Neurochem., 72,529–540.

    Google Scholar 

  9. Tonshin, A.A., Saprunova, V.B., Solodovnikova, I.M., Bakeeva, L.E., and Yagughinsky, L.S. (2003) Biochemistry(Moscow), 68,875–881.

    Google Scholar 

  10. Oleinick, N.L., Morris, R.L., and Belichenko, I. (2002) Photochem. Photobiol. Sci.,1,1–21.

    Google Scholar 

  11. Kamata, H., and Hirata, H. (1999) Cell. Signal.,11,1–14.

    Google Scholar 

  12. Earnshaw, W.C., Martins, L.M., and Kaufmann, S.H. (1999) Annu. Rev. Biochem.,68,383–424.

    Google Scholar 

  13. Liang, H., and Fesik, S.W. (1997) J. Mol. Biol.,274,291–302.

    Google Scholar 

  14. Köhler, C., Orrenius, S., and Zhivotovsky, B. (2002) J. Immunol. Meth.,265,97–110.

    Google Scholar 

  15. Grossmann, J., Mohr, S., Lapentina, E.G., Fiocchi, C., and Levine, A.D. (1998) Am. J. Physiol.,274,G1117–G1124.

    Google Scholar 

  16. Salvesen, G.S., and Dixit, V.M. (1999) Proc. Natl. Acad. Sci. USA, 96,10964–10967.

    Google Scholar 

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

    Google Scholar 

  18. Philchenkov, A.A. (2003) Biochemistry (Moscow), 68,365–376.

    Google Scholar 

  19. Hirata, H., Takahashi, A., Kobayashi, S., Yonehara, S., Sawai, H., Okazaki, T., Yamamoto, K., and Sasada, M. (1998) J. Exp. Med.,187,587–600.

    Google Scholar 

  20. 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.

    Google Scholar 

  21. Crompton, M. (1999) Biochem. J.,341,233–249.

    Google Scholar 

  22. Pozzan, T., and Rizzuto, R. (2000) Eur. J. Biochem.,267, 5269–5273.

    Google Scholar 

  23. Bernardi, P. (1999) Phys. Rev.,79,1127–1155.

    Google Scholar 

  24. Ichas, F., and Mazat, J.-P. (1998) Biochim. Biophys. Acta, 1366,33–50.

    Google Scholar 

  25. Novgorodov, S.A., Gudz, T.I., Brierley, G.P., and Pfeiffer, D.R. (1994) Arch. Biochem. Biophys.,311,219–228.

    Google Scholar 

  26. Lapidus, R.G., and Sokolove, P.M. (1994) J. Biol. Chem., 269,18931–18936.

    Google Scholar 

  27. Broekemeier, K.M., Dempsey, M.E., and Pfeiffer, D.R. (1989) J.Biol.Chem.,264,7826–7830.

    Google Scholar 

  28. Halestrap, A.P., McStay, G.P., and Clarke, S.J. (2002) Biochimie,84,153–166.

    Google Scholar 

  29. Kim, J.S., He, L., Qian, T., and Lemaster, J.J. (2003) Curr. Mol. Med.,3,527–535.

    Google Scholar 

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

    Google Scholar 

  31. Budihardjo, I., Oliver, H., Lutter,M., Luo, X., and Wang, X. (1999) Annu. Rev. Cell. Dev. Biol.,15,269–290.

    Google Scholar 

  32. Robertson, J.D., Orrenius, S., and Zhivotovsky, B. (2000) J. Struct. Biol.,129,346–358.

    Google Scholar 

  33. Nichols, P. (1974) Biochim. Biophys. Acta,346,261–310.

    Google Scholar 

  34. Gorbenko, G.P. (1999) Biochim. Biophys. Acta,1420,1–13.

    Google Scholar 

  35. Rytömaa, M., and Kinnunen, P.K.J. (1995) J. Biol. Chem., 270,3197–3202.

    Google Scholar 

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

    Google Scholar 

  37. Lorenzo, H.K., Susin, S.A., Penninger, J., and Kroemer, G. (1999) Cell Death Differ.,6,516–524.

    Google Scholar 

  38. Punj, V., and Chakrabarty, A.M. (2003) Cell. Microbiol.,5, 225–231.

    Google Scholar 

  39. Morishima, N., Nakanishi, K., Takenouchi, H., Shibata, T., and Yasuhiko, Y. (2002) J. Biol. Chem.,277,34287–34294.

    Google Scholar 

  40. Gogvadze, V., Robertson, J.D., Zhivotovsky, B., and Orrenius, S. (2001) J. Biol. Chem.,276,19066–19701.

    Google Scholar 

  41. Skulachev, V.P. (2000) IUBMB Life,49,365–373.

    Google Scholar 

  42. Guicciardi, M.E., Deussing, J., Miyoshi, H., Bronk, S.F., Svingen, P.A., Peters, C., Kaufmann, S.H., and Gores, G. J. (2000) J. Clin. Invest.,106,1127–1136.

    Google Scholar 

  43. Vousden, K.H., and Vande Woude, G.F. (2000) Nature Cell. Biol.,2,E178–E180.

    Google Scholar 

  44. Nakano, K., and Vousden, K.H. (2001) Mol. Cell,7,683–694.

    Google Scholar 

  45. Chatellard Causse, C., Blot, B., Cristina, N., Torch, S., Missotten, M., and Sadoul, R. (2002) J. Biol. Chem.,277, 29108–29115.

    Google Scholar 

  46. Aubry, L., Mattei, S., Blot, B., Sadoul, R., Satre, M., and Klein, G. (2002) J. Biol. Chem.,277,21947–21954.

    Google Scholar 

  47. Carafoli, E., and Molinari, M. (1998) Biochem. Biophys. Res. Commun.,247,193–203.

    Google Scholar 

  48. Bordone, L., and Campbell, C. (2002) J. Biol. Chem.,277, 26673–26680.

    Google Scholar 

  49. Kobayashi, S., Yamashita, K., Takeoka, T., Ohtsuki, T., Suzuki, Y., Takahashi, R., Yamamoto, K., Kaufmann, S. H., Uchiyama, T., Sasada, M., and Takahashi, A. (2002) J. Biol. Chem.,277,33968–33977.

    Google Scholar 

  50. Grook, N.E., Clem, R.J., and Miller, L.K. (1994) J. Virol.,67,2168–2174.

    Google Scholar 

  51. Hay, B.A., Wassarman, D.A., and Rubin, G.M. (1995) Cell,83,1253–1262.

    Google Scholar 

  52. Uren, A.G., Pakusch, M., Hawkins, C.J., Puls, K.L., and Vaux, D.L. (1996) Proc. Natl. Acad. Sci. USA,93,4974–4978.

    Google Scholar 

  53. Miller, L.K. (1999) Trends Cell. Biol.,9,323–328.

    Google Scholar 

  54. Joazeiro, C.A., and Weissman, A.M. (2000) Cell,102, 549–552.

    Google Scholar 

  55. Deveraux, Q.L., Takahashi, R., Salvesen, G.S., and Reed, J.S. (1997) Nature,388,300–304.

    Google Scholar 

  56. Huang, Y., Park, Y.C., Rich, R.L., Segal, D., Myszka, D. G., and Wu, H. (2001) Cell,104,781–790.

    Google Scholar 

  57. Yang, Y., and Yu, X. (2003) FASEB J.,17,790–799.

    Google Scholar 

  58. Suzuki, Y., Kakabayashi, Y., and Takahashi, R. (2001) Proc. Natl.Acad.Sci.USA,98,8662–8667.

    Google Scholar 

  59. Srinivasula, S.M., Hedge, R., Saleh, A., Datta,P., Shiozaki, E., Chal, J., Lee, R.A., Robbins, P.D., Fernandes-Alnemri, T., Shi, Y., and Alnemri, E.S. (2001) Nature,410,112–116.

    Google Scholar 

  60. Nicholson, D.W. (2001) Nature,410,33–34.

    Google Scholar 

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

    Google Scholar 

  62. MacFarlane, M., Merrison, W., Bratton, S.B., and Cohen, G.M. (2002) J. Biol. Chem.,277,36611–36616.

    Google Scholar 

  63. Hu, S., and Yang, X. (2003) J. Biol. Chem.,278,10055–10060.

    Google Scholar 

  64. Fu, J., Jin, Y., and Arend, L.J. (2003) J. Biol. Chem.,278, 52660–52672.

    Google Scholar 

  65. Deveraux, Q.L., Leo, E., Stennicke, H.R., Welsh, K., Salvesen, G.S., and Reed, J.C. (1999) EMBO J.,18,5242–5251.

    Google Scholar 

  66. Fleury, C., Mignotte, B., and Vayssiere, J.L. (2002) Biochimie,84,131–141.

    Google Scholar 

  67. Maulik, N., Yoshida, T., and Das, D.K. (1998) Free Rad. Biol. Med.,24,869–875.

    Google Scholar 

  68. Tan, S., Sagara, Y., Liu, Y., Maher, P., and Schubert, D. (1998) J. Cell Biol.,141,1423–1432.

    Google Scholar 

  69. Schulz, J.B., Weller, M., and Klockgether, T. (1996) J. Neurosci.,16,4696–4706.

    Google Scholar 

  70. Schulz, J.B., Bremen, D., Reed, J.C., Lommatzsch, J., Takayama, S., Wüllner, U., Löschmann, P.A., Klockgether, T., and Weller, M. (1997) J. Neurochem.,69, 2075–2086.

    Google Scholar 

  71. Gordeeva, A.V., Zvyagilskaja, R.A., and Labas, Y.A. (2003) Biochemistry(Moscow), 68,1077–1080.

    Google Scholar 

  72. Keller, J.N., Guo, Q., Holtsberg, F.W., Bruce-Keller, A. J., and Mattson, M.P. (1998) J.Neurosci.,18,4439–4450.

    Google Scholar 

  73. Zoratti, M., and Szabo, I. (1995) Biochim. Biophys. Acta, 1241,139–176.

    Google Scholar 

  74. Vercesi, A.E., Kowaltowski, A.J., Grijalba, M.T., Meinicke, A.R., and Castilho, R.F. (1997) Biosci. Rep., 17,43–52.

    Google Scholar 

  75. Yuan, J. (1996) J. Cell. Biochem.,60,4–11.

    Google Scholar 

  76. Seipp, S., Schmich, J., and Leitz, T. (2001) Development, 128,4891–4898.

    Google Scholar 

  77. Skulachev, V.P. (1999) Biochemistry(Moscow), 64,1418–1426.

    Google Scholar 

  78. Vardi, A., Berman-Frank, I., Rozenberg, T., Hadas, O., Kaplan, A., and Levine, A. (1999) Curr. Biol.,l9,1061–1064.

    Google Scholar 

  79. Segovia, M., Haramaty, L., Berges, J.A., and Falkowski, P. G. (2003) Plant Physiol.,132,99–105.

    Google Scholar 

  80. Ha, M.W., Hou, K.Z., Liu, Y.P., and Yuan, Y. (2003) Ai Zheng,22,691–694.

    Google Scholar 

  81. Arnoult, D., Akarid, K., Grodet, A., Petit, P.X., Estaquier, J., and Ameisen, J.C. (2002) Cell Death Differ.,9,65–81.

    Google Scholar 

  82. Das, M., Mukherjee, S.B., and Shaha, C. (2001) J. Cell. Sci.,114,2461–2469.

    Google Scholar 

  83. Liu, J., Shen, H.M., and Ong, C.N. (2001) Life Sci.,69, 1833–1850.

    Google Scholar 

  84. Mukherjee, S.B., Das, M., Sudhandiran, G., and Shaha, C. (2002) J. Biol. Chem.,277,24717–24727.

    Google Scholar 

  85. Al-Olayan, E.M., Williams, G.T., and Hurd, H. (2002) Int. J. Parasitol.,32,1133–1143.

    Google Scholar 

  86. Ouaissi, A. (2003) Kinetoplastid. Biol. Dis.,2,5.

    Google Scholar 

  87. Goffeau, A., Barrell, B.G., Bussey, H., Davis, R.W., Dujon, B., Feldmann, H., Galibert, F., Hoheisel, J.D., Jacq, C., Johnston, M., Louis, E.J., Mewes, H.W., Murakami, Y., Philippsen, P., Tettelin, H., and Oliver, S. G. (1996) Science,274 (5287),563–567.

    Google Scholar 

  88. Madeo, F., Engelhardt, S., Herker, E., Lehmann, N., Maldener, C., Proksch, A., Wissing, S., and Frohlich, K.-U. (2002) Curr. Genet.,41,208–216.

    Google Scholar 

  89. Yamaki, M., Umehara, T., Chimura, T., and Horikoshi, M. (2001) Genes Cells,6,1043–1054.

    Google Scholar 

  90. Madeo, F., Fröhlich, E., Ligr, M., Grey, M., Sigrist, S.J., Wolf, D.H., and Fröhlich, K.U. (1999) J. Cell. Biol.,145, 757–767.

    Google Scholar 

  91. Laun, P., Pichova, A., Madeo, F., Fuchs, J., Ellinger, A., Kohlwein, S., Dawes, I., Fröhlich, K.-U., and Breitenbach, M. (2001) Mol. Microbiol.,39,1166–1173.

    Google Scholar 

  92. 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.

    Google Scholar 

  93. Skulachev, V.P. (2002) FEBS Lett.,528,23–26.

    Google Scholar 

  94. Manon, S., Chaudhuri, B., and Guerin, M. (1997) FEBS Lett.,415,29–32.

    Google Scholar 

  95. Xu, Q., and Reed, J.C. (1998) Mol. Cell,1,337–346.

    Google Scholar 

  96. Qi, H., Li, T.K., Kuo, D., Nur-E-Kamal, A., and Liu, L. F. (2003) J. Biol. Chem.,278,15136–15141.

    Google Scholar 

  97. Zha, H., Fisk, H.A., Yaffe, M.P., Mahajan, N., Herman, B., and Reed, J.C. (1996) Mol Cell Biol.,16,6494–6508.

    Google Scholar 

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

    Google Scholar 

  99. Sawada, M., Sun, W., Hayes, P., Leskov, K., Bootman, D. A., and Matsuyama, S. (2003) Nat. Cell Biol.,5,320–329.

    Google Scholar 

  100. Fraser, A., and James, C. (1998) Trends Cell. Biol.,8,219–221.

    Google Scholar 

  101. Fröhlich, K.-U., and Madeo, F. (2000) FEBS Lett.,473,6–9.

    Google Scholar 

  102. Chen, S.R., Dunigan, D.D., and Dickman, M.B. (2003) Free Rad. Biol. Med.,34,1315–1325.

    Google Scholar 

  103. Camougrand, N., Grelaud-Coq, A., Marza, E., Priault, M., Bessoule, J.J., and Manon, S. (2003) Mol.Microbiol., 47,495–506.

    Google Scholar 

  104. Komatsu, K., Hopkins, K.M., Lieberman, H.B., and Wang, H.-G. (2000) FEBS Lett.,481,122–126.

    Google Scholar 

  105. Weinberger, M., Ramachandran, L., and Burchans,W. (2003) IUBMB Life,55,467–472.

    Google Scholar 

  106. Uren, A.G., Beilharz,T., O'Connell, M.J., Bugg, S.J., van Driel, R., Vaux, D.L., and Lithgow, T. (1999) Proc. Natl. Acad. Sci. USA,96,10170–10175.

    Google Scholar 

  107. Fahrenkrog, B., Sauder, U., and Aebi, U. (2004) J. Cell. Sci.,117,15–26.

    Google Scholar 

  108. Ludovico, P., Sousa, M.J., Silva, M.T., Leao, C., and Corte-Real, M. (2001) Microbiology,147,2409–2415.

    Google Scholar 

  109. Ludovico, P., Rodrigues, F., Almeida, A., Silva, M.T., Barrientos, A., and Corte-Real, M. (2002) Mol. Biol. Cell, 13,2598–2606.

    Google Scholar 

  110. Phillips, A.J., Sudbery, I., and Ramsdale, M. (2003) Proc. Natl. Acad. Sci. USA,100,14327–14332.

    Google Scholar 

  111. Ludovico, P., Sansonetty, F., Silva, M.T., and Corte-Real, M. (2003) FEMS Yeast Res.,3,91–96.

    Google Scholar 

  112. Severin, F.F., and Hyman, A.A. (2002) Curr Biol.,12, R233–235.

    Google Scholar 

  113. Abdullaev, Z.Kh., Bodrova, M.E., Chernyak, B.V., Dolgikh, D.A., Kluck, R.M., Pereverzev, M.O., Arseniev, A.S., Efremov, R.G., Kirpichnikov, M.P., Mokhova, E. N., Newmeyer, D.D., Roder, H., and Skulachev, V.P. (2002) Biochem. J.,362,749–754.

    Google Scholar 

  114. Roucou, X., Prescott, M., Devenish, R.J., and Nagley, P. (2000) FEBS Lett.,471,235–239.

    Google Scholar 

  115. Stanger, B.Z., Leder, P., Lee, T.H., Kim, E., and Seed, B. (1995) Cell,81,513–523.

    Google Scholar 

  116. Cornillon, S., Foa, C., Davoust, J., Buonavista, N., Gross, J.D., and Golstein, P. (1994) J. Cell Sci.,107,2691–2704.

    Google Scholar 

  117. Olie, R.A., Durrieu, F., Cornillon, S., Loughran, G., Gross, J., Earnshaw, W.C., and Golstein, P. (1998) Curr. Biol.,8,955–958.

    Google Scholar 

  118. Arnoult, D., Tatischeff, I., Estaquier, J., Girard, M., Sureau, F., Tissier, J.P., Grodet, A., Dellinger, M., Traincard, F., Kahn, A., Ameisen, J.-C., and Petit, P.X. (2001) Mol. Biol. Cell,12,3016–3030.

    Google Scholar 

  119. Tatischeff, I., Petit, P.X., Grodet, A., Tissier, J.P., Duband Goulet, I., and Ameisen, J.C. (2001) Eur. J. Cell. Biol.,80,428–441.

    Google Scholar 

  120. Maercker, C., Kortwig, H., Nikiforov, M.A., Allis, C.D., and Lipps, H.J. (1999) Mol. Biol. Cell,10,3003–3014.

    Google Scholar 

  121. Kobayashi, T., and Endoh, H. (2003) Cell Death Differ.,10, 634–640.

    Google Scholar 

  122. Jaso Friedmann, L., Leary, J.H.,3rd, and Evans, D.L. (2000) Exp.Parasitol.,96,75–88.

    Google Scholar 

  123. Volkel, H., Kurz, U., Linder, J., Klumpp, S., Gnau, V., Jung, G., and Schultz, J.E. (1996) Eur. J. Biochem.,238, 198–206.

    Google Scholar 

  124. Maubach, G., Schilling, K., Rommerskirch, W., Wenz, I., Schultz, J.E., Weber, E., and Wiederanders, B. (1997) Eur. J. Biochem.,250,745–750.

    Google Scholar 

  125. Banno, Y., Yano, K., and Nozawa, Y. (1983) Eur. J. Biochem.,132,563–568.

    Google Scholar 

  126. Christensen, S.T., Chemnitz, J., Straarup, E.M., Kristiansen, K., Wheatley, D.N., and Rasmussen, L. (1998) Cell. Biol. Int.,22,591–598.

    Google Scholar 

  127. Heussler, V.T., Machado, J.,Jr., Fernandez, P.C., Botteron, C., Chen, C.G., Pearse, M.J., and Dobbelaere, D.A. (1999) Proc. Natl. Acad. Sci. USA,96,7312–7317.

    Google Scholar 

  128. Aga, E., Katschinski, D.M., van Zandbergen, G., Laufs, H., Hansen, B., Muller,K., Solbach, W., and Laskay, T. (2002) J.Immunol.,169,898–905.

    Google Scholar 

  129. Chose, O., Noel, C., Gerbod, D., Brenner, C., Viscogliosi, E., and Roseto, A. (2002) Exp. Cell. Res.,276,32–39.

    Google Scholar 

  130. Christensen, S.T., Sorensen, H., Beyer, N.H., Kristiansen, K., Rasmussen, L., and Rasmussen, M.I. (2001) Cell. Biol. Int.,25,509–519.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Bach Institute of Biochemistry, Russian Academy of Sciences, Leninsky pr. 33, Moscow, 119071, Russia

    A. V. Gordeeva, Y. A. Labas & R. A. Zvyagilskaya

Authors
  1. A. V. Gordeeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. A. Labas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. A. Zvyagilskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gordeeva, A.V., Labas, Y.A. & Zvyagilskaya, R.A. Apoptosis in Unicellular Organisms: Mechanisms and Evolution. Biochemistry (Moscow) 69, 1055–1066 (2004). https://doi.org/10.1023/B:BIRY.0000046879.54211.ab

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:BIRY.0000046879.54211.ab

Search

Navigation