Advertisement

EJB Reviews pp 75-85 | Cite as

Homologous nuclear-encoded mitochondrial and cytosolic isoproteins

A review of structure, biosynthesis and genes
  • Rolf Jaussi
Part of the European Journal of Biochemistry book series (EJB REVIEWS, volume 1995)

Abstract

Mitochondrial and cytosolic proteins may be expected to differ in specific traits due to their different intracellular location. However, the identification of these differences between mitochondrial and cytosolic proteins is complicated by the heterogeneity of the two protein groups. These difficulties have been overcome by comparing traits of homologous genes, which are derived from a common ancestor gene, and their gene products.

Keywords

Mitochondrial protein import mitochondria isoelectric point evolution protein charge 

Abbreviations

pI

isoelectric point

ΔpI

pI of mitochondrial isoprotein minus pI of cytosolic isoprotein

Δplpp

pI precursor protein minus pI mature protein

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Walker, M. E., Val, D. L., Rohde, M., Devenish, R. J. & Wallace, J. C. (1991) Yeast pyruvate carboxylase: identification of two genes encoding isoenzymes, Biochem. Biophys. Res. Commun. 176, 1210–1217.PubMedGoogle Scholar
  2. 2.
    Ahmad, P. M. & Ahmad, E (1991) Mammalian pyruvate carboxylase: effect of biotin on the synthesis and translocation of apoenzyme into 3T3-L adipocyte mitochondria, FASEB J. 5, 24822485.Google Scholar
  3. 3.
    Fukushima, T., Decker, R. V., Anderson, W. M. & Spivey, H. O. (1989) Substrate channeling of NADH and binding of dehydrogenases to complex I, J. Biol. Chem. 264, 16483–16488.PubMedGoogle Scholar
  4. 4.
    Teller, J. K., Fahien, L. A. & Valdivia, E. (1990) Interactions among mitochondrial aspartate aminotransferase, malate dehydrogenase, and the inner mitochondria) membrane from heart, hepatoma, and liver, J. Biol. Chem. 265, 19486–19494.PubMedGoogle Scholar
  5. 5.
    Röhlen, D. A., Hoffmann, J., Van der Pas, J. C., Nehls, U., Preis, D., Sackmann, U. & Weiss, H. (1991) Relationship between a subunit of NADH dehydrogenase (complex I) and a protein family including subunits of cytochrome reductase and processing protease of mitochondria, FEBS Lett. 278, 75–78.PubMedGoogle Scholar
  6. 6.
    Rojo, M., Hovius, R., Demel, R. A., Nicolay, K. & Wallimann, T. (1991) Mitochondria) creatine kinase mediates contact formation between mitochondrial membranes, J. Biol. Chem. 266, 2029020 295.Google Scholar
  7. 7.
    Polakis, P. G. & Wilson, J. E. (1985) An intact hydrophobic N-terminal sequence is critical for binding of rat brain hexokinase to mitochondria, Arch. Biochem. Biophys. 236, 328–337.PubMedGoogle Scholar
  8. 8.
    Mikelsaar, R. (1987) A view of early cellular evolution, J. Mol. Evol. 25, 168–183.PubMedGoogle Scholar
  9. 9.
    Gray, M. W. (1989) Origin and evolution of mitochondria) DNA, Annu. Rev. Cell Biol. 5, 25–50.PubMedGoogle Scholar
  10. 10.
    Hartmann, C., Christen, P. & Jaussi, R. (1991) Mitochondria) protein charge, Nature 352, 762–763.PubMedGoogle Scholar
  11. 11.
    Creighton, T. E. (1993) Proteins: structures and molecular properties,W. H. Freeman and Company, New York, 2nd edn, p. 108.Google Scholar
  12. 12.
    Graf-Hausner, U., Wilson, K. J. & Christen, P. (1983) The covalent structure of mitochondria) aspartate aminotransferase from chicken. Identification of segments of the polypeptide chain invariant specifically in the mitochondria) isoenzyme, J. Biol. Chem. 258, 8813–8826.PubMedGoogle Scholar
  13. 13.
    Küntzel, H. & Köchel, H. G. (1981) Evolution of rRNA and origin of mitochondria, Nature 293, 751–755.PubMedGoogle Scholar
  14. 14.
    Gray, M. W. & Doolittle, W. F. (1982) Has the endosymbiotic hypothesis been proven? Microbiol. Rev. 46, 1–42.PubMedGoogle Scholar
  15. 15.
    Gray, M. W. (1989) The evolutionary origins of organelles, Trends Genet. 5, 294–299.PubMedGoogle Scholar
  16. 16.
    Devereux, J., Haeberli, P. & Smithies, O. (1984) A comprehensive set of sequence analysis programs for the VAX, Nucleic Acids Res. 12, 387–395.PubMedGoogle Scholar
  17. 17.
    Sander, C. & Schneider, R. (1991) Database of homology-derived protein structures and the structural meaning of sequence alignment, Proteins 9, 56–68.PubMedGoogle Scholar
  18. 18.
    Birktoft, J. J., Fernley, R. T., Bradshaw, R. A. & Banaszak, L. J. (1982) Amino acid sequence homology among the 2-hydroxy acid dehydrogenases: mitochondrial and cytoplasmic malate dehydrogenases form a homologous system with lactate dehydrogenase, Proc. Natl Acad. Sci. USA 79, 6166–6170.PubMedGoogle Scholar
  19. 19.
    Roderick, S. L. & Banaszak, L. J. (1986) The three-dimensional structure of porcine heart mitochondria) malate dehydrogenase at 3.0-A resolution, J. Biol. Chem. 261, 9461–9464.PubMedGoogle Scholar
  20. 20.
    Setoyama, C., Joh, T., Tsuzuki, T. & Shimada, K. (1988) Structural organization of the mouse cytosolic malate dehydrogenase gene: comparison with that of the mouse mitochondria) malate dehydrogenase gene, J. Mol. Biol. 202, 355–364.PubMedGoogle Scholar
  21. 21.
    Christen, P. & Metzler, D. E. (1985) Transaminases, John Wiley & Sons, New York, p. 176.Google Scholar
  22. 22.
    Mehta, P. K., Hale, T. I. & Christen, P. (1993) Aminotransferases: demonstration of homology and division into evolutionary subgroups, Eur. J. Biochem. 214, 549–561.PubMedGoogle Scholar
  23. 23.
    Mehta, P. K., Hale, T. I. & Christen, R. (1989) Evolutionary relationships among aminotransferases. Tyrosine aminotransferase, histidinol-phosphate aminotransferase, and aspartate aminotransferase are homologous proteins, Eur. J. Biochem. 186, 249–253.PubMedGoogle Scholar
  24. 24.
    Christen, R, Jaussi, R., Juretic, N., Mehta, P. K., Hale, T. I. & Ziak, M. (1990) Evolutionary and biosynthetic aspects of aspartate aminotransferase isoenzymes and other aminotransferases, Ann. N. Y. Acad. Sci. 585, 331–338.Google Scholar
  25. 25.
    Mehta, R. K., Hale, T. I. & Christen, R. (1991) Enzymes dependent on pyridoxal phosphate and other carbonyl compounds as cofactors, in Proc. 8th Int. Symp. on Vitamin B 6 and Carbonyl Catalysis in Osaka, Japan ( Fukui, T., Kagamiyama, H., Soda, K. & Wada, H., eds) pp. 35–42, Pergamon Press, Oxford.Google Scholar
  26. 26.
    Birolo, L., Arnone, M. I., Cubellis, M. V., Andreotti, G., Nitti, G., Marino, G. & Sannia, G. (1991) The active site of Sulfolobus solfataricus aspartate aminotransferase, Biochim. Biophys. Acta 1080, 198–204.PubMedGoogle Scholar
  27. 27.
    Talesa, V., Rosi, G., Contenti, S., Mangiabene, C., Lupattelli, M., Norton, S. J., Giovannini, E. & Principato, G. B. (1990) Presence of glyoxalase II in mitochondria from spinach leaves: cornparison with the enzyme from cytosol, Biochem. Int. 22, 1115 1120.Google Scholar
  28. 28.
    Glick, B. & Schatz, G. (1991) Import of proteins into mitochondria, Annu. Rev. Genet. 25, 21–44.PubMedGoogle Scholar
  29. 29.
    Pfanner, N., Rassow, J., van der Klei, I. J. & Neupert, W. (1992) A dynamic model of the mitochondria) protein import machinery, Cell 68, 999–1002.PubMedGoogle Scholar
  30. 30.
    Brandt, U., Yu, L., Yu, C.-A. & Trumpower, B. L. (1993) The mitochondrial targeting presequence of the Rieske iron-sulfur protein is processed in a single step after insertion into the cytochrome bc, complex in mammals and retained as a subunit in the complex, J. Biol. Chem. 268, 8387–8390.PubMedGoogle Scholar
  31. 31.
    Galanis, M., Devenish, R. J. & Nagley, R. (1991) Duplication of leader sequence for protein targeting to mitochondria leads to increased import efficiency, FEBS Lett. 282, 425–430.PubMedGoogle Scholar
  32. 32.
    Hartmann, C. M., Lindenmann, J.-M., Christen, R. & Jaussi, R. (1991) The precursor of mitochondrial aspartate aminotransferase is imported into mitochondria faster than the homologous cytosolic isoenzyme with the same presequence attached, Biochem. Biophys. Res. Commun. 174, 1232–1238.PubMedGoogle Scholar
  33. 33.
    Von Heijne, G. (1986) Mitochondria) targeting sequences may form amphiphilic helices, EMBO J. 5, 1335–1342.Google Scholar
  34. 34.
    Verner, K. & Schatz, G. (1988) Protein translocation across membranes, Science 241, 1307–1313.PubMedGoogle Scholar
  35. 35.
    Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K. & Watson, J. D. (1989) Molecular biology of the cell, pp. 341–401, Garland Publishing Inc., New York and London.Google Scholar
  36. 36.
    Ogawa, S., Rottenberg, H., Brown, T. R., Shulman, R. G., Castillo, C. L. & Glynn, R (1978) High-resolution 31P nuclear magnetic resonance study of rat liver mitochondria, Proc. Natl Acad. Sci. USA 75, 1796–1800.PubMedGoogle Scholar
  37. 37.
    Srere, P. A. (1980) The infrastructure of the mitochondrial matrix, Trends Biochem. Sci. 5, 120–121.Google Scholar
  38. 38.
    Meer, L. (1988) Limitierte Spaltung der nativen Isoenzyme der Aspartat-Aminotransferase vom Huhn and Schwein durch Trypsin. Chemische and immunologische Charakterisierung der proteolytisch modifizierten Proteine, Diploma thesis, University of Zürich.Google Scholar
  39. 39.
    Behra, R. & Christen, R. (1986) In vitro import into mitochondria of the precursor of mitochondria) aspartate aminotransferase, J. Biol. Chem. 261, 257–263.Google Scholar
  40. 40.
    Hartmann, C. M. (1992) Contribution of the mature moiety of mitochondrial precursor proteins to the efficiency of their importation, Ph. D. thesis, University of Zürich, pp. 1–51.Google Scholar
  41. 41.
    Hartmann, C. M., Gehring, H. & Christen, R (1993) The mature form of imported mitochondrial proteins undergoes conformational changes upon binding to isolated mitochondria, Eue. J. Biochem. 218, 905–910.Google Scholar
  42. 42.
    Wallimamn, T. & Eppenberger, H. M. (1990) The subcellular cornpartmentation of creatine kinase isozymes as a precondition for a proposed phosphoryl-creatine circuit, Prog. Clin. Biol. Res. 344, 877–889.Google Scholar
  43. 43.
    Levitsky, D. O., Levchenko, T. S., Saks, V. A., Sharov, V. G. & Smirnov, V. N. (1977) The functional coupling between Ca2+ATPase and creatine kinase in heart muscle sarcoplasmic reticulum, Biochimia 42, 1766–1773.Google Scholar
  44. 44.
    Suzuki, T., Sato, M., Yoshida, T. & Tuboi, S. (1989) Rat liver mitochondria) and cytosolic fumarases with identical amino acid sequences are encoded from a single gene, J. Biol. Chem. 264, 2581–2586.PubMedGoogle Scholar
  45. 45.
    Tuboi, S., Suzuki, T., Sato, M. & Yoshida, T. (1990) Rat liver mitochondrial and cytosolic fumarases with identical amino acid sequences are encoded from a single mRNA with two alternative in-phase AUG initiation sites, Adv. Enzyme Regul. 30, 289–304.PubMedGoogle Scholar
  46. 46.
    Petrova-Benedict, R., Robinson, B. H., Stacey, T. E., Mistry, J. & Chalmers, R. A. (1987) Deficient fumarase activity in an infant with fumaricacidemia and its distribution between the different forms of the enzyme seen on isoelectric focusing, Am. J. Hum. Genet. 40, 257–266.PubMedGoogle Scholar
  47. 47.
    Luzikov, V. N. (1985) Mitochondrial biogenesis and breakdown, Consultants Bureau, New York, pp. 1–362.Google Scholar
  48. 48.
    Luzikov, V. N. (1986) Proteolytic control over topogenesis of membrane proteins, FEBS Lett. 200, 259–264.PubMedGoogle Scholar
  49. 49.
    Jaussi, R. (1994) Homologous nuclear-encoded mitochondria) and cytosolic isoproteins: a review of structure, biosynthesis and genes, Habilitationsschrift, University of Zürich, pp. 1–29.Google Scholar
  50. 50.
    Juretic, N., Jaussi, R., Mattes, U. & Christen, P. (1987) Genes of nuclear encoded mitochondrial proteins: evidence for a variant of the 3’ splice-site consensus sequence, Nucleic Acids Res. 15, 10083–10086.PubMedGoogle Scholar
  51. 51.
    Mount, S. M. (1982) A catalogue of splice junction sequences, Nucleic Acids Res. 10, 459–472.PubMedGoogle Scholar
  52. 52.
    Juretic, N., Mattes, U., Ziak, M, Christen, R. & Jaussi, R. (1990) Structure of the genes of two homologous intracellularly hetero-topic isoenzymes. Cytosolic and mitochondria) aspartate aminotransferase of chicken, Eur. J. Biochem. 192, 119–126.PubMedGoogle Scholar
  53. 53.
    Wu, M. & Tzagoloff, A. (1987) Mitochondrial and cytoplasmic fumarases in Saccharomyces cerevisiae are encoded by a single nuclear gene FUMI, J. Biol. Chem. 262, 12275–12282.PubMedGoogle Scholar
  54. 54.
    Tropschug, M., Nicholson, D. W., Hartl, F.-U., Köhler, H., Pfanner, N., Wachter, E. & Neupert, W. (1988) Cyclosporin A-binding protein (cyclophilin) of Neurospora crassa. One gene codes for both the cytosolic and mitochondrial forms, J. Biol. Chem. 263, 14 433–14 440.Google Scholar
  55. 55.
    Natsoulis, G., Hilger, F. & Fink, G. R. (1986) The HTS1 gene encodes both the cytoplasmic and mitochondrial histidine tRNA synthetases of S. cerevisiae, Cell 46, 235–243.PubMedGoogle Scholar
  56. 56.
    Kubelik, A. R., Turcq, B. & Lambowitz, A. M. (1991) The Neuro-spora crassa cyt-20 gene encodes cytosolic and mitochondria) valyl-tRNA synthetases and may have a second function in addition to protein synthesis, Mol. Cell. Biol. 11, 4022–4035.PubMedGoogle Scholar
  57. 57.
    Chatton, B., Walter, R, Ebel, J. R, Lacroute, F. & Fasiolo, F. (1988) The yeast VAS] gene encodes both mitochondrial and cytoplasmic valyl-tRNA synthetases, J. Biol. Chem. 263, 52–57.PubMedGoogle Scholar
  58. 58.
    Boguta, M., Hunter, L. A., Shen, W.-C., Gillman, E. C., Martin, N. C. & Hopper, A. K. (1994) Subcellular locations of MODS proteins: mapping of sequences sufficient for targeting to mitochondria and demonstration that mitochondria) and nuclear isoforms comingle in the cytosol, Mol. Cell. Biol. 14, 2298–2306.PubMedGoogle Scholar
  59. 59.
    Hopper, A. K., Furukawa, A. H., Pham, H. D. & Martin, N. C. (1982) Defects in modification of cytoplasmic and mitochondria) Jaussi (Eur. J. Biochem. 228) transfer RNAs are caused by single nuclear mutations, Cell 28, 543–550.Google Scholar
  60. 60.
    Ellis, S. R., Morales, M. J., Li, J. M., Hopper, A. K. & Martin, N. C. (1986) Isolation and characterization of the TRM1 locus, a gene essential for the Nz,NN-dimethylguanosine modification of both mitochondrial and cytoplasmic tRNA in Saccharomyces cerevisiae, J. Biol. Chem. 261, 9703–9709.PubMedGoogle Scholar
  61. 61.
    Slusher, L. B., Gillman, E. C., Martin, N. C. & Hopper, A. K. (1991) mRNA leader length and initiation codon context determine alternative AUG selection for the yeast gene MODS, Proc. Natl Acad. Sci. USA 88, 9789–9793.Google Scholar
  62. 62.
    Brown, W. M. (1980) Polymorphism in mitochondria) DNA of humans as revealed by restriction endonuclease analysis, Proc. Natl Acad. Sci. USA 77, 3605–3609.PubMedGoogle Scholar
  63. 63.
    Monnat, R. J. & Loeb, L. A. (1985) Nucleotide sequence preservation of human mitochondria) DNA, Proc. Natl Acad. Sci. USA 82, 2895–2899.PubMedGoogle Scholar
  64. 64.
    Monnat, R. J., Maxwell, C. L. & Loeb, L. A. (1985) Nucleotide sequence preservation of human leukemic mitochondrial DNA, Cancer Res. 45, 1809–1814.PubMedGoogle Scholar
  65. 65.
    Avise, J. C. (1991) Ten unorthodox perspectives on evolution prompted by comparative population genetic findings on mitochondrial DNA, Anno. Rev. Genet. 25, 45–69.Google Scholar
  66. 66.
    Farrelly, F. & Butow, R. A. (1983) Rearranged mitochondrial genes in the yeast nuclear genome, Nature 301, 296–301.PubMedGoogle Scholar
  67. 67.
    Wright, R. M. & Cummings, D. J. (1983) Integration of mitochondria) gene sequences within the nuclear genome during senescence in a fungus, Nature 302, 86–88.PubMedGoogle Scholar
  68. 68.
    Gellissen, G., Bradfield, J. Y., White, B. N. & Wyatt, G. R. (1983) Mitochondrial DNA sequences in the nuclear genome of a locust, Nature 301, 631–634.PubMedGoogle Scholar
  69. 69.
    Jacobs, H. T., Posakony, J. W., Grula, J. W., Roberts, J. W., Xin, J., Britten, R. J. & Davidson, E. H. (1983) Mitochondrial DNA sequences in the nuclear genome of Strongylocentrotus purpuratus, J. Mol. Biol. 165, 609–632.PubMedGoogle Scholar
  70. 70.
    Kemble, R. J., Mans, R. J., Gabay-Laughnan, S. & Laughnan, J. R. (1983) Sequences homologous to episomal mitochondrial DNAs in the maize nuclear genome, Nature 304, 744–747.Google Scholar
  71. 71.
    Hadler, H. I., Dimitrijevic, B. & Mahalingam, R. (1983) Mitochondrial DNA and nuclear DNA from normal rat liver have a common sequence, Proc. Natl Acad. Sci. USA 80, 6495–6499.PubMedGoogle Scholar
  72. 72.
    Nomiyama, H., Fukuda, M., Wakasugi, S., Tsuzuki, T. & Shimada, K. (1985) Molecular structures of mitochondrial-DNA-like sequences in human nuclear DNA, Nucleic Acids Res. 13, 1649–1658.PubMedGoogle Scholar
  73. 73.
    Diffley, J. F. X. & Stillman, B. (1991) A close relative of the nuclear, chromosomal high-mobility group protein HMG1 in yeast mitochondria, Proc. Natl Acad. Sci. USA 88, 7864–7868.PubMedGoogle Scholar
  74. 74.
    Shay, J. W., Baba, T., Zhan, Q., Kamimura, N. & Cuthbert, J. A. (1991) HeLaTG cells have mitochondrial DNA inserted into the c-rnyc oncogene, Oncogene 6, 1869–1874.PubMedGoogle Scholar
  75. 75.
    Fukuchi, M., Shikanai, T., Kossykh, V. G. & Yamada, Y. (1991) Analysis of nuclear sequences homologous to the B4 plasmidlike DNA of rice mitochondria: evidence for sequence transfer from mitochondria to nuclei, Current Genet. 20, 487–494.Google Scholar
  76. 76.
    Ossorio, P. N., Sibley, L. D. & Boothroyd, J. C. (1991) Mitochondrial-like DNA sequences flanked by direct and inverted repeats in the nuclear genome of Toxoplasma gondii, J. Mol. Biol. 222, 525–536.PubMedGoogle Scholar
  77. 77.
    Smith, M. F., Thomas, W. K. & Patton, J. L. (1992) Mitochondrial DNA-like sequence in the nuclear genome of an akodontine rodent, Mol. Biol. Evol. 9, 204–215.PubMedGoogle Scholar
  78. 78.
    Thorsness, P. E. & Fox, T. D. (1993) Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus, Genetics 134, 21–28.PubMedGoogle Scholar
  79. 79.
    Thorsness, P. E. & Fox, T. D. (1990) Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae, Nature 346, 376–379.PubMedGoogle Scholar
  80. 80.
    Rand, D. M. & Harrison, R. G. (1986) Mitochondrial transmission genetics in crickets, Genetics 114, 955–970.PubMedGoogle Scholar
  81. 81.
    Wallis, G. P. (1987) Mitochondrial DNA insertion polymorphism and germ line heteroplasmy in the Triturus cristatus species complex, Heredity 58, 229–238.PubMedGoogle Scholar
  82. 82.
    Sugiyama, S., Hattori, K., Hayakawa, M. & Ozawa, T. (1991) Quantitative analysis of age-associated accumulation of mitochondria) DNA with deletion in human hearts, Biochem. Biophys. Res. Commun. 180, 894–899.PubMedGoogle Scholar
  83. 83.
    Katayama, M., Tanaka, M., Yamamoto, H., Ohbayashi, T., Nimura, Y. & Ozawa, T. (1991) Deleted mitochondrial DNA in the skeletal muscle of aged individuals, Biochem. Mt. 25, 47–56.Google Scholar
  84. 84.
    Yen, T.-C., Pang, C.-Y., Hsieh, R.-H., Su, C.-H., King, K.-L. & Wei, Y.-H. (1992) Age-dependent 6 kb deletion in human liver mitochondrial DNA, Biochem. Int. 26, 457–468.PubMedGoogle Scholar
  85. 85.
    Koehler, C. M., Lindberg, G. L., Brown, D. R., Beitz, D. C., Freeman, A. E., Mayfield, J. E. & Myers, A. M. (1991) Replacement of bovine mitochondrial DNA by a sequence variant within one generation, Genetics 129, 247–255.PubMedGoogle Scholar
  86. 86.
    Sonderegger, P. & Christen, P. (1978) Comparison of the evolution rates of cytosolic and mitochondrial aspartate aminotransferase, Nature 275, 157–159.PubMedGoogle Scholar
  87. 87.
    Ward, R. D. & Skibinski, D. O. (1988) Evidence that mitochondria) isozymes are genetically less variable than cytoplasmic isozymes, Genet. Res. 51, 121–127.PubMedGoogle Scholar
  88. 88.
    Guthrie, C. (1991) Messenger RNA splicing in yeast: clues to why the spliceosome is a ribonucleoprotein, Science 253, 157–163.PubMedGoogle Scholar
  89. 89.
    Kennell, J. C., Moran, J. V., Perlman, P. S., Butow, R. A. & Lambowitz, A. M. (1993) Reverse transcriptase activity associated with maturase-encoding group II introns in yeast mitochondria, Cell 73, 133–146.PubMedGoogle Scholar
  90. 90.
    Ohtaka, C. & Ishikawa, H. (1993) Accumulation of adenine and thymine in a groE-homologous operon of an intracellular symbiont, J. Mol. Evol. 36, 121–126.PubMedGoogle Scholar
  91. 91.
    Montzka, K. A. & Steitz, J. A. (1988) Additional low-abundance human small nuclear ribonucleoproteins: U11, U12, etc, Proc. Natl Acad. Sci. USA 85, 8885–8889.PubMedGoogle Scholar
  92. 92.
    Hancock, K. & Hajduk, S. L. (1990) The mitochondrial tRNAs of Trypanosoma brucei are nuclear encoded, J. Biol. Chem. 265, 19208–19215.Google Scholar
  93. 93.
    Schneider, A., Martin, J. & Agabian, N. (1994) A nuclear encoded tRNA of Trypanosoma brucei is imported into mitochondria, Mol. Cell. Biol. 14, 2317–2322.PubMedGoogle Scholar
  94. 94.
    Dietrich, A., Weil, J. H. & Maréchal-Drouard, L. (1992) Nuclear-encoded transfer RNAs in plant mitochondria, Annu. Rev. Cell Biol. 8, 115–131.PubMedGoogle Scholar
  95. 95.
    Gavel, Y. & Von Heijne, G. (1992) The distribution of charged amino acids in mitochondrial inner-membrane proteins suggests different modes of membrane integration for nuclearly and mitochondrially encoded proteins, Eue J. Biochem. 205,1207—1215.Google Scholar
  96. 96.
    Welch, G. R. & Easterby, J. S. (1994) Metabolic channeling versus free diffusion: transition-time analysis, Trends Biochem. Sci. 19, 193 —197.PubMedGoogle Scholar
  97. 97.
    Frank, R., Trosin, M., Tomasselli, A. G., Schulz, G. E. & Schirmer, R. H. (1984) Mitochondrial adenylate kinase (AK2) from bovine heart. Homology with the cytosolic isoenzyme in the catalytic region, Eur. J. Biochem. 141, 629–636.PubMedGoogle Scholar
  98. 98.
    Eanes, R. Z. & Kun, E. (1971) Separation and characterization of aconitate hydratase isoenzymes from pig tissues, Biochim. Biophys. Acta 227, 204–210.PubMedGoogle Scholar
  99. 99.
    Sapico, V., Litwack, G. & Criss, W. E. (1972) Purification of rat liver adenylate kinase isozyme II and comparison with isozyme III, Biochim. Biophys. Acta 258, 436–445.PubMedGoogle Scholar
  100. 100.
    Kubo, S. & Noda, H. (1974) Adenylate kinase of porcine heart, Eur. J. Biochem. 48, 325–331.PubMedGoogle Scholar
  101. 101.
    Frank, R., Trosin, M., Tomasselli, A. G., Noda, L., Krauth-Siegel, R. L. & Schirmer, R. H. (1986) Mitochondrial adenylate kinase (AK2) from bovine heart. The complete primary structure, Eur. J. Biochem. 154, 205–211.PubMedGoogle Scholar
  102. 102.
    Ruscak, M., Orlicky, J., Zubor, V. & Hager, H. (1982) Alanine aminotransferase in bovine brain: purification and properties, J. Neurochem. 39, 210–216.PubMedGoogle Scholar
  103. 103.
    De Rosa, G., Burk, T. L. & Swick, R. W. (1979) Isolation and characterization of mitochondria) alanine aminotransferase from porcine tissue, Biochim. Biophys. Acta 567, 116–124.PubMedGoogle Scholar
  104. 104.
    Koivula, T. & Koivusalo, M. (1975) Different forms of rat liver aldehyde dehydrogenase and their subcellular distribution, Biochim. Biophys. Acta 397, 9–23.PubMedGoogle Scholar
  105. 105.
    Dickinson, F. M. & Berrieman, S. (1979) The separation of sheep liver cytoplasmic and mitochondrial aldehyde dehydrogenases by isoelectric focusing, and observations on the purity of preparations of the cytoplasmic enzyme, and their sensitivity towards inhibition by disulfiram, Biochem. J. 179, 709–712.PubMedGoogle Scholar
  106. 106.
    Agnew, K. E. M., Bennett, A. F., Crow, K. E., Greenway, R. M., Blackwell, L. F. & Buckley, P. D. (1981) A reinvestigation of the purity, iosoelectric points and some kinetic properties of the aldehyde dehydrogenases from sheep liver, Eur. J. Biochem. 119, 79–84.PubMedGoogle Scholar
  107. 107.
    Braun, T., Bober, E., Singh, S., Agarwal, D. P. & Goedde, H. W. (1987) Isolation and sequence analysis of a full-length cDNA clone coding for human mitochondrial aldehyde dehydrogenase, Nucleic Acids Res. 15, 3179.PubMedGoogle Scholar
  108. 108.
    Sonderegger, P., Jaussi, R., Christen, P. & Gehring, H. (1982) Biosynthesis of aspartate aminotransferases. Both the higher molecular mass precursor of mitochondrial aspartate aminotransferase and the cytosolic isoenzyme are synthesized on free polysomes, J. Biol. Chem. 257, 3339–3345.PubMedGoogle Scholar
  109. 109.
    Kuramitsu, S., Inoue, K., Kondo, K., Aki, K. & Kagamiyama, H. (1985) Aspartate aminotransferase isozymes from rabbit liver: purification and properties, J. Biochem. (Tokyo) 97, 1337–1345.Google Scholar
  110. 110.
    Taniguchi, M. & Sugiyama, T. (1990) Aspartate aminotransferase from Eleusine coracana, a C4 plant: purification, characterization, and preparation of antibody, Arch. Biochem. Biophys. 282, 427–432.PubMedGoogle Scholar
  111. 111.
    Romestant, M., Jerebzoff, S., Noaillac-Depeyre, J., Gas, N. & Dargent, R. (1989) Aspartate aminotransferase isoenzymes in Leptosphaeria michotii Properties and intracellular location (published erratum appears in Eur. J. Biochem. 182,737), Eur. J. Biochem. 180,153–159.PubMedGoogle Scholar
  112. 112.
    Cronin, V. B., Maras, B., Barra, D. & Doonan, S. (1991) The amino acid sequence of the aspartate aminotransferase from baker’s yeast (Saccharomyces cerevisiae), Biochem. J. 277, 335–340.PubMedGoogle Scholar
  113. 113.
    Rosenberg, U. B., Eppenberger, H. M. & Perriard, J. C. (1981) Occurrence of heterogeneous forms of the subunits of creatine kinase in various muscle and nonmuscular tissues and their behaviour during myogenesis, Eur. J. Biochem. 116, 87–92.PubMedGoogle Scholar
  114. 114.
    Schlegel, J., Wyss, M., Schürch, U., Schnyder, T., Quest, A., Wegmann, G., Eppenberger, H. M. & Wallimann, T. (1988) Mitochondrial creatine kinase from cardiac muscle and brain are two distinct isoenzymes but both form octameric molecules, J. Biol. Chem. 263, 16 963 —16 969.Google Scholar
  115. 115.
    Talesa, V., Uotila, L., Koivusalo, M., Principato, G., Giovannini, E. & Rosi, G. (1988) Demonstration of glyoxalase H in rat liver mitochondria. Partial purification and occurrence in multiple forms, Biochim. Biophys. Acta 955, 103–110.PubMedGoogle Scholar
  116. 116.
    Clinkenbeard, K. D., Reed, W. D., Mooney, R. A. & Lane, M. D. (1975) Intracellular localization of the 3-hydroxy-3-methylglutaryl coenzyme A cycle enzymes in liver, J. Biol. Chem. 250, 3108–3116.PubMedGoogle Scholar
  117. 117.
    Hagele, E., Neeff, J. & Mecke, D. (1978) The malate dehydrogenase isoenzymes of Saccharomyces cerevisiae. Purification, characterisation and studies on their regulation, Eur. J. Biochem. 83, 67–76.PubMedGoogle Scholar
  118. 118.
    Beneviste, K. & Munkres, K. D. (1970) Cytoplasmic and mitochondrial malate dehydrogenases of Neurospora, Biochim. Biophys. Acta 220, 161–177.Google Scholar
  119. 119.
    Dölken, G., Leisner, E. & Pette, D. (1974) Turnover of malatedehydrogenase isoenzymes in rabbit liver and heart, Eue J. Biochem. 47, 333–342.Google Scholar
  120. 120.
    Jo, J.-S., Ishihara, N. & Kikuchi, G. (1974) Occurrence and properties of four forms of phosphoenolpyruvate carboxykinase in the chicken liver, Arch. Biochem. Biophys. 160, 246–254.PubMedGoogle Scholar
  121. 121.
    Weldon, S. L., Rando, A., Matathias, A. S., Hod, Y., Kalonick, R A., Savon, S., Cook, J. S. & Hanson, R. W. (1990) Mitochondrial phosphoenolpyruvate carboxykinase from the chicken. Comparison of the cDNA and protein sequences with the cytosolic isozyme, J. Biol. Chem. 265, 7308–7317.PubMedGoogle Scholar
  122. 122.
    Gallwitz, W. E., Jacoby, G. H., Ray, R D. & Lambeth, D. O. (1988) Purification and characterization of the isozymes of phosphoenolpyruvate carboxykinase from rabbit liver, Biochim. Biophys. Acta 964, 36–45.PubMedGoogle Scholar
  123. 123.
    Masuda, T., Sakamoto, M., Nishizaki, I., Hayashi, H., Yamamoto, M. & Wada, H. (1987) Affinity purification and characterization of serine hydroxymethyltransferases from rat liver, J. Biochem. (Tokyo) 101, 643–652.Google Scholar

Copyright information

© FEBS 1995

Authors and Affiliations

  • Rolf Jaussi
    • 1
  1. 1.Institute of Medical RadiobiologyUniversity of Zürich and Paul Scherrer InstituteSwitzerland

Personalised recommendations