Skip to main content
SpringerLink
Log in

Principles of control over formation of structures responsible for respiratory functions of mitochondria

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

Abstract

Topogenesis of mitochondrial proteins includes their synthesis in cytosol and mitochondria, their translocation across the outer and inner membranes, sorting to various mitochondrial compartments, and assembly of different protein complexes. These complexes are involved in transport functions, electron transfer through the respiratory chain, generation of transmembrane electrochemical potential, oxidative phosphorylation of ADP into ATP, etc. To perform these functions, a special stringent control is required over formation of submitochondrial structures and the mitochondrion as a whole. Such control is expected to rigorously eliminate not only misfolded proteins but also incorrectly incorporated subunits and is realized in mitochondria by means of numerous proteases with different functions and localizations. In the case of more complicated protein formations, e.g. supercomplexes, the protein quality is assessed by their ability to realize the integral function of the respiratory chain and, thus, ensure the stability of the whole system. Considering supercomplexes of the mitochondrial respiratory chain, the present review clearly demonstrates that this control is realized by means of various (mainly vacuolar) proteases with different functions and localizations. The contemporary experimental data also confirm the author’s original idea that the general mechanism of assembly of subcellular structures is based on the “selection by performance criterion” and “stabilization by functioning”.

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. Zorov, D. B., Isaev, N. K., Plotnikov, E. Yu., Zorova, L. D., Stelmashook, E. V., Vasileva, A. K., Arkhangelskaya, A. A., and Khrjapenkova, T. G. (2007) Biochemistry (Moscow), 72, 1115–1126.

    Article  CAS  Google Scholar 

  2. Suen, D. G., Norris, K. L., and Youle, R. J. (2008) Genes Dev., 22, 1577–1590.

    Article  CAS  PubMed  Google Scholar 

  3. Neupert, W., and Herrmann, J. M. (2007) Annu. Rev. Biochem., 76, 723–749.

    Article  CAS  PubMed  Google Scholar 

  4. Boekema, E. J., and Braun, H.-P. (2007) J. Biol. Chem., 282, 1–4.

    Article  CAS  PubMed  Google Scholar 

  5. Luzikov, V. N. (1980) Regulation of Mitochondria Formation [in Russian], Nauka, Moscow.

    Google Scholar 

  6. Shwerzmann, K., Cruz-Orive, L. M., Eggman, R., Sanger, A., and Weibel, E. R. (1986) J. Cell Biol., 102, 97–103.

    Article  Google Scholar 

  7. Wallace, D. C. (2005) Ann. Rev. Genet., 39, 359–407.

    Article  CAS  PubMed  Google Scholar 

  8. Poyton, R. O., and McEwen, J. E. (1996) Annu. Rev. Biochem., 65, 563–607.

    Article  CAS  PubMed  Google Scholar 

  9. Fontanesi, F., Soto, I. C., and Barrientos, A. (2008) IUBMB Life, 60, 557–568.

    Article  CAS  PubMed  Google Scholar 

  10. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1996) Science, 272, 1136–1144.

    Article  CAS  PubMed  Google Scholar 

  11. Capaldi, R. A., Malatesta, F., and Darley-Usmar, V. M. (1983) Biochim. Biophys. Acta, 726, 135–148.

    CAS  PubMed  Google Scholar 

  12. Church, C., Goehring, B., Forsha, D., Wazny, P., and Poyton, R. O. (2005) J. Biol. Chem., 280, 1854–1863.

    Article  CAS  PubMed  Google Scholar 

  13. Zara, V., Palmisano, I., Conte, L., and Trumpower, B. L. (2004) Eur. J. Biochem., 271, 1209–1218.

    Article  CAS  PubMed  Google Scholar 

  14. Cruciat, C.-M., Hell, K., Folsch, H., Neupert, W., and Stuart, R. A. (1999) EMBO J., 18, 5226–5233.

    Article  CAS  PubMed  Google Scholar 

  15. Sazanov, L. A., Peak-Chew, S. Y., Fearnley, I. M., and Walker, J. E. (2000) Biochemistry, 39, 7229–7235.

    Article  CAS  PubMed  Google Scholar 

  16. Grivennikova, V. G., and Vinogradov, A. D. (2003) Usp. Biol. Khim., 43, 19–58.

    CAS  Google Scholar 

  17. Duarte, M., Sousa, R., and Videira, A. (1995) Genetics, 139, 1211–1221.

    CAS  PubMed  Google Scholar 

  18. Boyer, P. D. (1997) Annu. Rev. Biochem., 66, 717–749.

    Article  CAS  PubMed  Google Scholar 

  19. Weber, J. (2007) Trends Biochem. Sci., 32, 53–56.

    Article  CAS  PubMed  Google Scholar 

  20. Lau, W. C., Baker, L. A., and Rubinstein, J. L. (2008) J. Mol. Biol., 382, 1256–1264.

    Article  CAS  PubMed  Google Scholar 

  21. Devenish, R. J., Prescott, M., and Rodgers, A. J. (2008) Int. Rev. Cell Mol. Biol., 267, 1–58.

    Article  CAS  PubMed  Google Scholar 

  22. Tzagoloff, A., Barrientos, A., Neupert, W., and Herrmann, J. M. (2004) J. Biol. Chem., 279, 19775–19780.

    Article  CAS  PubMed  Google Scholar 

  23. Wang, Z. G., White, P. S., and Ackerman, S. H. (2001) J. Biol. Chem., 276, 30773–30778.

    Article  CAS  PubMed  Google Scholar 

  24. Green, D. E., and Hechter, O. (1965) Proc. Natl. Acad. Sci. USA, 53, 318–325.

    Article  CAS  PubMed  Google Scholar 

  25. Schagger, H., and Pfeiffer, K. (2000) EMBO J., 19, 1777–1783.

    Article  CAS  PubMed  Google Scholar 

  26. Cruciat, C.-M., Brunner, S., Baumann, F., Neupert, W., and Stuart, R. A. (2000) J. Biol. Chem., 275, 18093–18098.

    Article  CAS  PubMed  Google Scholar 

  27. Schafer, E., Seelert, H., Reifschneider, N. H., Krause, F., Dencher, N. A., and Vonck, J. (2006) J. Biol. Chem., 281, 15370–15375.

    Article  PubMed  Google Scholar 

  28. Schagger, H. (2001) IUBMB Life, 52, 119–128.

    Article  CAS  PubMed  Google Scholar 

  29. Luzikov, V. N. (1973) Subcell. Biochem., 2, 1–31.

    CAS  PubMed  Google Scholar 

  30. Ko, Y. H., Delannoy, M., Hullihen, J., Chiu, W., and Pedersen, P. L. (2003) J. Biol. Chem., 278, 12305–12309.

    Article  CAS  PubMed  Google Scholar 

  31. Chen, C., Ko, Y., Delannoy, M., Ludtke, S. J., Chiu, W., and Pedersen, P. L. (2004) J. Biol. Chem., 279, 31761–31768.

    Article  CAS  PubMed  Google Scholar 

  32. Shutt, T. E., and Gray, M. W. (2006) Trends Gen., 22, 90–95.

    Article  CAS  Google Scholar 

  33. Ryan, M. T., and Hoogenraad, N. J. (2007) Annu. Rev. Biochem., 76, 701–722.

    Article  CAS  PubMed  Google Scholar 

  34. Scarpulla, R. C. (2008) Physiol. Rev., 88, 611–638.

    Article  CAS  PubMed  Google Scholar 

  35. Wu, Z., Puigserver, P., Andersson, U., Zhang, G., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., and Spiegelman, B. M. (1999) Cell, 98, 115–124.

    Article  CAS  PubMed  Google Scholar 

  36. Arny, Z., Wagner, B. K., Ma, Y., Chinsomboom, J., Laznik, D., and Spiegelman, B. M. (2008) Proc. Natl. Acad. Sci. USA, 105, 4721–4725.

    Article  Google Scholar 

  37. Kutik, S., Guiarad, B., Meyer, H., Wiedemann, N., and Pfanner, N. (2007) J. Biol. Chem., 179, 585–591.

    CAS  Google Scholar 

  38. Neupert, W. (1997) Annu. Rev. Biochem., 66, 863–917.

    Article  CAS  PubMed  Google Scholar 

  39. Van Dyck, L., and Langer, T. (1999) Cell Mol. Life Sci., 56, 825–842.

    Article  PubMed  Google Scholar 

  40. Young, L., Leonhard, K., Tatsuta, T., Trowsdale, J., and Langer, T. (2001) Science, 291, 2135–2138.

    Article  CAS  PubMed  Google Scholar 

  41. Steglich, G., Neupert, W., and Langer, T. (1999) Mol. Cell. Biol., 19, 3435–3442.

    CAS  PubMed  Google Scholar 

  42. Langer, T. (2000) Trends Biochem. Sci., 25, 247–251.

    Article  CAS  PubMed  Google Scholar 

  43. Kaser, M., Kambacheld, M., Kisters-Woike, B., and Langer, T. (2003) J. Biol. Chem., 278, 46414–46423.

    Article  PubMed  Google Scholar 

  44. Kambacheld, M., Augustin, S., Tatsuta, T., Muller, S., and Langer, T. (2005) J. Biol. Chem., 280, 20132–20139.

    Article  CAS  PubMed  Google Scholar 

  45. Wheeldon, L. W., Dianoux, A. C., Bof, M., and Vignais, P. V. (1974) Eur. J. Biochem., 46, 189–199.

    Article  CAS  PubMed  Google Scholar 

  46. Kalnov, S. L., Novikova, L. A., Zubatov, A. S., and Luzikov, V. N. (1979) Biochem. J., 182, 195–202.

    CAS  PubMed  Google Scholar 

  47. Kalnov, S. L., Novikova, L. A., Zubatov, A. S., and Luzikov, V. N. (1979) FEBS Lett., 101, 355–358.

    Article  CAS  PubMed  Google Scholar 

  48. Suzuki, C. K., Rep, M., van Dijl, J. M., Suda, K., Grivell, L. A., and Schatz, G. (1997) Trends Biochem. Sci., 22, 118–123.

    Article  CAS  PubMed  Google Scholar 

  49. Guelin, E., Rep, M., and Grivell, L. A. (1996) FEBS Lett., 381, 42–46.

    Article  CAS  Google Scholar 

  50. Savel’ev, A. S., Novikova, L. A., Kovaleva, I. E., Luzikov, V. N., Neupert, W., and Langer, T. (1998) J. Biol. Chem., 273, 20596–20602.

    Article  PubMed  Google Scholar 

  51. Weber, E. R., Hanekamp, T., and Thorsness, P. E. (1996) Mol. Biol. Cell., 7, 307–317.

    CAS  PubMed  Google Scholar 

  52. Pearce, D. A., and Sherman, F. (1997) J. Biol. Chem., 272, 31829–31836.

    Article  CAS  PubMed  Google Scholar 

  53. Wagner, I., Arlt, H., van Dyck, L., Langer, T., and Neupert, W. (1994) EMBO J., 13, 5135–5145.

    CAS  PubMed  Google Scholar 

  54. Kovaleva, I. E., Novikova, L. A., Nazarov, P. A., Grivennikov, S. I., and Luzikov, V. N. (2003) Eur. J. Biochem., 270, 222–229.

    Article  CAS  PubMed  Google Scholar 

  55. Stuart, R. A., Cyr, D. M., Craig, E. A., and Neupert, W. (1994) Trends Biochem. Sci., 19, 87–92.

    Article  CAS  PubMed  Google Scholar 

  56. Rottgers, K., Zufall, N., Guiard, B., and Voos, W. (2002) J. Biol. Chem., 277, 45829–45837.

    Article  CAS  PubMed  Google Scholar 

  57. Von Janovsky, B., Major, T., Knapp, K., and Koos, W. (2006) J. Mol. Biol., 31, 799–807.

    Google Scholar 

  58. Arlt, H., Tauer, R., Feldmann, H., Neupert, W., and Langer, T. (1996) Cell, 85, 875–885.

    Article  CAS  PubMed  Google Scholar 

  59. Leonhard, K., Sriegler, A., Neupert, W., and Langer, T. (1999) Nature, 398, 348–351.

    Article  CAS  PubMed  Google Scholar 

  60. Graef, M., Seewald, G., and Langer, T. (2007) Mol. Cell. Biol., 27, 2476–2485.

    Article  CAS  PubMed  Google Scholar 

  61. Arlt, H., Steglich, G., Perryman, R., Guiard, B., Neupert, W., and Langer, T. (1998) EMBO J., 17, 4837–4847.

    Article  CAS  PubMed  Google Scholar 

  62. Augustin, S., Nolden, M., Muller, S., Hardt, O., Arnold, I., and Langer, T. (2005) J. Biol. Chem., 280, 2691–2699.

    Article  CAS  PubMed  Google Scholar 

  63. Arnold, I., Wagner-Ecker, M., Ansorge, W., and Langer, T. (2006) Gene, 367, 74–88.

    Article  CAS  PubMed  Google Scholar 

  64. Dubaquie, Y., Looser, R., Funfschilling, U., Jeno, P., and Rospert, S. (1998) EMBO J., 17, 5868–5876.

    Article  CAS  PubMed  Google Scholar 

  65. Voisine, C., Schilke, B., Ohlson, M., Beinert, H., Marszalek, J., and Craig, E. A. (2000) Mol. Cell. Biol., 20, 3677–3684.

    Article  CAS  PubMed  Google Scholar 

  66. Schmidt, S., Strub, A., Rottgers, K., Zufall, N., and Voos, W. (2001) J. Mol. Biol., 313, 13–26.

    Article  CAS  PubMed  Google Scholar 

  67. Rep, M., van Dijl, J. M., Suda, K., Schatz, G., Grivell, L. A., and Suzuki, C. K. (1996) Science, 274, 103–106.

    Article  CAS  PubMed  Google Scholar 

  68. Rep, M., Nooy, J., Guelin, E., and Grivell, L. A. (1996) Curr. Genet., 30, 206–211.

    Article  CAS  PubMed  Google Scholar 

  69. Galkin, A. V., Tsoi, T. V., and Luzikov, V. N. (1980) Biochem. J., 190, 145–156.

    CAS  PubMed  Google Scholar 

  70. Luzikov, V. N., Zubatov, A. S., and Rainina, E. I. (1973) J. Bioenerg. Biomembr., 5, 129–149.

    Article  CAS  Google Scholar 

  71. Parry, G. (1978) Subcell. Biochem., 5, 261–325.

    CAS  PubMed  Google Scholar 

  72. Baba, M., Takeshige, K., Baba, N., and Ohsumi, Y. (1994) J. Cell Biol., 124, 903–913.

    Article  CAS  PubMed  Google Scholar 

  73. Ziegler, D. M., Linnane, A. W., Green, D. E., Dass, C. M., and Ris, H. (1958) Biochim. Biophys. Acta, 28, 524–538.

    Article  CAS  PubMed  Google Scholar 

  74. Luzikov, V. N. (1985) Mitochondrial Biogenesis and Breakdown, Plenum Publisher Corporation, New York-London.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    V. N. Luzikov

Authors
  1. V. N. Luzikov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. N. Luzikov.

Additional information

Original Russian Text © V. N. Luzikov, 2009, published in Uspekhi Biologicheskoi Khimii, 2009, Vol. 49, pp. 77–106.

The Editorial Board is deeply grateful to Academician A. A. Bogdanov for editing this review.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Luzikov, V.N. Principles of control over formation of structures responsible for respiratory functions of mitochondria. Biochemistry Moscow 74, 1443–1456 (2009). https://doi.org/10.1134/S0006297909130021

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297909130021

Key words

Search

Navigation