Abstract
Cytochromesc andc 1 are essential components of the mitochondrial respiratory chain. In both cytochromes the heme group is covalently linked to the polypeptide chain via thioether bridges. The location of the two cytochromes is in the intermembrane space; cytochromec is loosely attached to the surface of the inner mitochondrial membrane, whereas cytochromec 1 is firmly anchored to the inner membrane. Both cytochromec andc 1 are encoded by nuclear genes, translated on cytoplasmic ribosomes, and are transported into the mitochondria where they become covalently modified and assembled. Despite the many similarities, the import pathways of cytochromec andc 1 are drastically different. Cytochromec 1 is made as a precursor with a complex bipartite presequence. In a first step the precursor is directed across outer and inner membranes to the matrix compartment of the mitochondria where cleavage of the first part of the presequence takes place. In a following step the intermediate-size form is redirected across the inner membrane; heme addition then occurs on the surface of the inner membrane followed by the second processing reaction. The import pathway of cytochromec is exceptional in practically all aspects, in comparison with the general import pathway into mitochondria. Cytochromec is synthesized as apocytochromec without any additional sequence. It is translocated selectively across the outer membrane. Addition of the heme group, catalyzed by cytochromec heme lyase, is a requirement for transport. In summary, cytochromec 1 import appears to follow a “conservative pathway” reflecting features of cytochromec 1 sorting in prokaryotic cells. In contrast, cytochromec has “invented” a rather unique pathway which is essentially “non-conservative.”
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Allison, D. S., and Schatz, G. (1986).Proc. Natl. Acad. Sci. USA 83, 9011–9015.
Böhni, P. C., Daum, G., and Schatz, G. (1983).J. Biol. Chem. 258, 4937–4943.
Chen, W.-J., and Douglas, M. G. (1987).Cell. 49, 651–658.
Cheng, M. Y., Hartl, F.-U., Martin, J., Pollock, R. A., Kalousek, F., Neupert, W., Hallberg, E. M., Hallberg, R. L., and Horwich, A. L. (1989).Nature (London)337, 620–625.
Conboy, J. G., Fenton, W. A., and Rosenberg, L. E. (1982).Biochem. Biophys. Res. Commun. 105, 1–7.
Daldal, F., Cheng, S., Appelbaum, J., Davidson, E., and Prince, R. C. (1986).Proc. Natl. Acad. Sci. 83, 2012–2016.
Deshaies, R. J., Koch, B. D., Werner-Washburne, M., Craig, E. A., and Schekman, R. (1988).Nature (London)332, 800–805.
Drygas, M. E., Lambowitz, A. M., and Nargang, F. E. (1989).J. Biol. Chem. 264, 17897–17906.
Dumont, M. E., and Richards, F. M. (1984).J. Biol. Chem. 259, 6704–6707.
Dumont, M. E., Ernst, J. F., Hampsey, D. M., and Sherman, F. (1987).EMBO J. 6, 235–241.
Eilers, M., Oppliger, W., and Schatz, G. (1987).EMBO J. 6, 1073–1077.
Fisher, W. R., Taniuchi, H., and Anfinsen, C. B. (1973).J. Biol. Chem. 248, 3188–3195.
Gabellini, N., and Sebald, W. (1986).Eur. J. Biochem. 154, 569–579.
Gabellini, N., Harnish, U., McCarthy, J. E. G., Hauska, G., and Sebald, W. (1985).EMBO J. 4, 549–553.
Gasser, S. M., Daum, G., and Schatz, G. (1982a).J. Biol. Chem. 257, 13034–13041.
Gasser, S. M., Ohashi, A., Daum, G., Böhni, P. C., Gibson, J., Reid, G. A., Yonetani, T., and Schatz, G. (1982b).Proc. Natl. Acad. Sci. USA 79, 267–271.
Hackenbrock, C. R. (1968).Proc. Natl. Acad. Sci. USA 61, 589–602.
Hallermayer, G., Zimmermann, R., and Neupert, W. (1977).Eur. J. Biochem. 81, 523–532.
Halpin, C., Elderfield, P. D., James, H. D., Zimmermann, R., Dunbar, B., and Robinson, C. (1989).EMBO J. 8, 3917–3821.
Harmey, M. A., Hallermayer, G., and Neupert, W. (1977).Eur. J. Biochem. 81, 533–544.
Hartl, F.-U., and Neupert, W. (1990).Science 247, 930–938.
Hartl, F.-U., Schmidt, B., Wachter, E., Weiss, H., and Neupert, W. (1986).Cell 47, 939–951.
Hartl, F.-U., Ostermann, J., Guiard, B., and Neupert, W. (1987).Cell 51, 1027–1037.
Hartl, F.-U., Pfanner, N., Nicholson, D. W., and Neupert, W. (1989).Biochim. Biophys. Acta 988, 1–45.
Hawlitschek, G., Schneider, H., Tropschug, M., Hartl, F.-U., and Neupert, W. (1988).Cell 53, 795–806.
Hennig, B., and Neupert, W. (1981).Eur. J. Biochem. 121, 203–212.
Hennig, B., Köhler, H., and Neupert, W. (1983).Proc. Natl. Acad. Sci. USA 80, 4963–4967.
Kellems, R. E., Allison,, V. G., and Butow, R. A. (1975).J. Cell. Biol. 65, 1–14.
Korb, H., and Neupert, W. (1978).Eur. J. Biochem. 91, 609–620.
McAda, P. C., and Douglas, M. G. (1982).J. Biol. Chem. 257, 3177–3182.
Nargang, F. E., Drygas, M. E., Kwong, P. L., Nicholson, D. W., and Neupert, W. (1988).J. Biol. Chem. 263, 9388–9394.
Nicholson, D. W., and Neupert, W. (1989).Proc. Natl. Acad. Sci. USA 86, 4340–4344.
Nicholson, D. W., Köhler, H., and Neupert, W. (1987).Eur. J. Biochem. 164, 147–157.
Nicholson, D. W., Hergersberg, C., and Neupert, W. (1988).J. Biol. Chem. 263, 19034–19042.
Nicholson, D. W., Stuart, R. A., and Neupert, W. (1989).J. Biol. Chem. 264, 10156–10168.
Ohashi, A., Gibson, J., Gregor, I., and Schatz, G. (1982).J. Biol. Chem. 257, 13042–13047.
Ostermann, J., Horwich, A. L., Neupert, W., and Hartl, F.-U. (1989).Nature (London)341, 125–130.
Pfaller, R., and Neupert, W. (1987).EMBO J. 6, 2635–2642.
Pfaller, R., Freitag, H., Harmey, M. A., Benz, R., and Neupert, W. (1985).J. Biol. Chem. 260, 8188–8193.
Pfaller, R., Steger, H. F., Rassow, J., Pfanner, N., and Neupert, W. (1988).J. Cell. Biol. 107, 2483–2490.
Pfanner, N., and Neupert, W. (1985).EMBO J. 4, 2819–2825.
Pfanner, N., and Neupert, W. (1986).FEBS Lett. 209, 152–156.
Pfanner, N., and Neupert, W. (1987a).Curr. Top. Bioenerg. 15, 177–219.
Pfanner, N., and Neupert, W. (1987b).J. Biol. Chem. 262, 7528–7536.
Pfanner, N., Müller, H. K., Harmey, M. A., and Neupert, W. (1987a).EMBO J. 6, 3449–3454.
Pfanner, N., Tropschug, M., and Neupert, W. (1987b).Cell. 49, 815–823.
Pollock, R. A., Hartl, F.-U., Cheng, M. Y., Ostermann, J. Horwich, A., and Neupert, W. (1988).EMBO J. 7, 3493–3500.
Rassow, J., Guiard, B., Wienhues, U., Herzog, V., Hartl, F.-U., and Neupert, W. (1989).J. Cell. Biol. 109, 1421–1428.
Rietveld, A., Ponjee, G. A. E., Schiffers, P., Jordi, W., van de Coolwijk, P. J. F. M., Demel, R. A., Marsh, D., and de Kruijff, B. (1985).Biochim. Biophys. Acta 818, 398–409.
Rietveld, A., Jordi, W., and de Kruijff, B. (1986).J. Biol. Chem. 261, 3846–3856.
Riezman, H., Hay, R., Gasser, S., Daum, G., Schneider, G., Witte, C., and Schatz, G. (1983).EMBO J. 2, 1105–1111.
Römisch, J., Tropschug, M., Sebald, W., and Weiss, H. (1987).Eur. J. Biochem. 164, 111–115.
Roise, D., Horvath, S. J., Tomich, J. M., Richards, J. H., and Schatz, G. (1986).EMBO J. 5, 1327–1334.
Sadler, I., Suda, K., Schatz, G., Kaudewitz, F., and Haid, A. (1984).EMBO J. 3, 2137–2143.
Schatz, G. (1979).FEBS Lett. 103, 203–211.
Schleyer, M., and Neupert, W. (1985).Cell 43, 339–350.
Schleyer, M., Schmidt, B., and Neupert, W. (1982).Eur. J. Biochem. 125, 109–116.
Schmidt, B., Wachter, E., and Neupert, W. (1984).Eur. J. Biochem. 144, 581–588.
Schwaiger, M., Herzog, V., and Neupert, W. (1987).J. Cell. Biol. 105, 235–246.
Söllner, T., Griffiths, G., Pfaller, R., Pfanner, N., and Neupert, W. (1989).Cell 59, 1061–1070.
Söllner, T., Pfaller, R., Griffiths, G., Pfanner, N., and Neupert, W. (1990).Cell 62, 107–115.
Stewart, J. W., Sherman, F., Shipman, N. A., and Jackson, M. (1971).J. Biol. Chem. 246, 7429–7445.
Stuart, R. A., Nicholson, D. W., and Neupert, W. (1990).Cell. 60, 31–43.
Taniuchi, H., Basile, G., Taniuchi, M., and Veloso, D. (1983).J. Biol. Chem. 258, 10963–10966.
Teintze, M., Slaughter, M., Weiss, H., and Neupert, W. (1982).J. Biol. Chem. 257, 10364–10371.
van Loon, A. P. G. M., and Schatz, G. (1987).EMBO J. 6, 2241–2248.
van Loon, A. P. G. M., Brändli, A. W., and Schatz, G. (1986).Cell. 44, 801–812.
Verner, H., and Schatz, G. (1987).EMBO J. 6, 2449–2456.
Vestweber, D., and Schatz, G. (1988).J. Cell. Biol. 107, 2037–2043.
von Heijne, G. (1986)EMBO J. 5, 1335–1342.
Zimmermann, R., Paluch, V., and Neupert, W. (1979).FEBS Lett. 108, 141–146.
Zimmermann, R., Hennig, B., and Neupert, W. (1981).Eur. J. Biochem. 116, 455–460.
Zitomer, R. S., and Hall, B. D. (1976).J. Biol. Chem. 251, 6320–6326.
Zwizinski, C., and Neupert, W. (1983).J. Biol. Chem. 258, 13340–13346.
Zwizinski, C., Schleyer, M., and Neupert, W. (1983).J. Biol. Chem. 258, 4071–4074.
Zwizinski, C., Schleyer, M., and Neupert, W. (1984).J. Biol. Chem. 259, 7850–7856.
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Gonzales, D.H., Neupert, W. Biogenesis of mitochondrialc-type cytochromes. J Bioenerg Biomembr 22, 753–768 (1990). https://doi.org/10.1007/BF00786929
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DOI: https://doi.org/10.1007/BF00786929