Abstract
Theunc (or atp) operon ofEscherichia coli comprises eight genes encoding the known subunits of the proton-translocating ATP synthase (H+-ATPase) plus a ninth gene (uncI) of unknown function. The subunit stoichiometry of the H+-ATPase (α 3β3γ1δ1ε1a1b2c10–15) requires that the respectiveunc genes be expressed at different rates. This review discusses the experimental methods applied to determining how differential synthesis is achieved, and evaluates the results obtained. It has been found that the primary level of control is translational initiation. The translational efficiencies of theunc genes are determined by primary and secondary mRNA structures within their respective translational initiation regions. The respective rates of translation are matched to the subunit requirements of H+-ATPase assembly. Finally, points of uncertainty remain and experimental strategies which will be important in future work are discussed.
Similar content being viewed by others
References
Amzel, M. (1981).J. Bioenerg. Biomembr. 13, 109–121.
Brawermann, G. (1987).Cell 48, 5–6.
Brusilow, W. S. A., Klionsky, D. J., and Simoni, R. D. (1982).J. Bacteriol. 151, 1363–1371.
Brusilow, W. S. A., Porter, A. C. G., and Simoni, R. D. (1983).J. Bacteriol. 155, 1265–1270.
Butlin, J. D., Cox, G. B., and Gibson, F. (1971).Biochem. J. 124, 75–81.
Cannistraro, V. J., Subbarao, M. N., and Kennell, D. (1986).J. Mol. Biol. 192, 257–274.
Cozens, A. L., and Walker, J. E. (1987).J. Mol. Biol. 194, 359–383.
Dennis, P. P. (1984).J. Biol. Chem. 259, 3202–3209.
Downie, J. A., Gibson, F., and Cox, G. B. (1979).Annu. Rev. Biochem. 48, 103–131.
Downie, J. A., Langman, L., Cox, G. B., Yanofsky, C., and Gibson, F. (1980).J. Bacteriol. 143, 8–17.
Fillingame, R. H. (1981).Curr. Top. Bioenerg. 11, 35–106.
Foster, D. L., and Fillingame, R. H. (1979).J. Biol. Chem. 254, 8230–8236.
Foster, D. L., and Fillingame, R. H. (1982).J. Biol. Chem. 257, 2009–2015.
Friedl, P., Friedl, C., and Schairer, H. U. (1979).Eur. J. Biochem. 100, 175–180.
Futai, M., and Kanazawa, H. (1983).Microbiol. Rev. 47, 285–312.
Ganoza, M. C., Marliere, P., Kofoid, E. C., and Louis, B. G. (1985).Proc. Natl. Acad. Sci. USA 82, 4587–4591.
Gay, N. J. (1984).J. Bacteriol. 158, 820–825.
Gay, N. J., and Walker, J. E. (1981).Nucleic Acids Res. 9, 3919–3926.
Gibson, F. (1983).Proc. R. Soc. London Ser. B 215, 1–18.
Gibson, F., Downie, J. A., Cox, J. B., and Radik, J. (1978).J. Bacteriol. 134, 728–736.
Goelz, S., and Steitz, J. A. (1977).J. Biol. Chem. 252, 5177–5179.
Gold, L., Pribnow, D., Schneider, T., Shinedling, S., Singer, B. S., and Stormo, G. (1981).Annu. Rev. Microbiol. 35, 365–403.
Grantham, R., Gautier, D., Gouy, M., Jacobzone, M., and Mercier, R. (1981).Nucleic Acids Res. 9, 43–74.
Grosjean, H., and Fiers, W. (1982).Gene 18, 199–209.
Hansen, F. G., Nielsen, J., Riise, E., and von Meyenburg, K. (1981).Mol. Gen. Genet. 183, 463–472.
Holm, L. (1986).Nucleic Acids Res. 14, 3075–3087.
Ikemura, T. (1981a).J. Mol. Biol. 146, 1–21.
Ikemura, T. (1981b).J. Mol. Biol. 151, 389–409.
Jay, E., Seth, A. K., Rommens, J., Sood, A., and Jay, G. (1982).Nucleic Acids Res. 10, 6319–6329.
Jones, H. M., Brajkovich, C. M., and Gunsalus, R. P. (1983).J. Bacteriol. 155, 1279–1287.
Kanazawa, H., Kiyasu, T., Noumi, T. and Futai, M. (1984).J. Bacteriol. 158, 300–306.
Kennell, D., and Riezman, H. (1977).J. Mol. Biol. 114, 1–21.
Klionsky, D. J., Skalnik, D. G., and Simoni, R. D. (1986).J. Biol. Chem. 261, 8096–8099.
Kozak, M. (1983).Microbiol. Rev. 47, 1–45.
Kurland, C. G. (1987).Trends Biochem. Sci. 12, 126–128.
Lindahl, L., and Zengel, J. M. (1982).Adv. Genet. 21, 53–121.
Little, S., Campbell, K., Hyde, S., and Robinson, M. K. (1986).Abstracts Microbe 86, P.B, 21–10.
Lünsdorf, H., Ehrig, K., Friedl, P., and Schairer, H. U. (1984).J. Mol. Biol. 173, 131–136.
Maaloe, O. (1979). InBiological Regulation and Development (Goldberger, R. F., ed.), Plenum Press, New York, pp. 487–542.
Mahajna, J., Oppenheim, A. B., Rattray, A., and Gottesman, M. (1986).J. Bacteriol. 165, 167–174.
McCarthy, J. E. G., Schairer, H. U., and Sebald, W. (1984). EBEC Rep. 3, pp. 587, 588.
McCarthy, J. E. G., Schairer, H. U., and Sebald, W. (1985).EMBO J. 4, 519–526.
McCarthy, J. E. G., Sebald, W., Gross, G., and Lammers, R. (1986).Gene 41, 201–206.
Miki, T., Hiraga, S., Nagata, T., and Yura, T. (1978).Proc. Natl. Acad. Sci. USA 75, 5099–5103.
Miller, E. S., Karam, J., Dawson, M., Trojanowska, M., Gauss, P., and Gold, L. (1987).J. Mol. Biol. 194, 397–410.
Nelson, N. (1981).Curr. Top. Bioenerg. 11, 1–34.
Newbury, S. F., Smith, N. H., Robinson, E. C., Hiles, I. D., and Higgins, C. F. (1987).Cell 48, 297–310.
Nielsen, J., Jorgensen, B. B., Hansen, F. G., Petersen, P. E., and von Meyenburg, K. (1982). EBEC Rep. 2, pp. 611–612.
Nielsen, J., Jorgensen, B. B., von Meyenburg, K., and Hansen, F. G. (1984).Mol. Gen. Genet. 193, 64–71.
Oppenheim, S. D., and Yanofsky, C. (1980).Genetics 95, 785–795.
Pedersen, S. (1984).EMBO J. 3 2895–2898.
Porter, A. G. G., Brusilow, W. S. A., and Simoni, R. D. (1983).J. Bacteriol. 155, 1271–1278.
Ray, P. N., and Pearson, M. L. (1974).J. Mol. Biol. 85, 163–175.
Ray, P. N., and Pearson, M. L. (1975).Nature (London)253, 647–650.
Russell, D. R., and Bennett, G. N. (1982).Gene 20, 231–243.
Schauder, B., Blöcker, H., Frank, R., and McCarthy, J. E. G. (1987).Gene 52, 279–283.
Scherer, G. F. E., Walkinshaw, M. D., Arnott, S., and Morré, D. J. (1980).Nucleic Acids Res. 8, 3895–3907.
Schneider, E., and Altendorf, K. (1982).Eur. J. Biochem. 126, 149–153.
Senior, A. E. (1979). InMembrane Proteins in Energy Transduction (Capaldi, R. A., ed.), Marcel Dekker, New York, pp. 233–276.
Simoni, R. D. (1984). InH +-ATPase (ATP Synthase): Structure, Function, Biogenesis. The F0F1 Complex of Coupling Membranes (Papa, S., Altendorf, K., Ernster, L., and Packer, L., eds.), ICSU Press,, Adriatica Editrice, Bari, Italy, pp. 77–88.
Stanssens, P., Remaut, E., and Fiers, W. (1986).Cell 44, 711–718.
Steitz, J. A. (1979). InBiological Regulation and Development (Goldberger, R. F., ed.), Plenum Press, New York, pp. 349–399.
Talkad, V., Schneider, E., and Kennell, D. (1976).J. Mol. Biol. 104, 299–303.
Tinoco, I., Borer, P. N., Dengler, B., Levine, M. D., Uhlenbeck, O. C., Crothers, D. M., and Gralla, J. (1973).Nature New Biol. 246, 40–41.
Trifonov, E. N. (1987).J. Mol. Biol. 194, 643–652.
Varenne, S., Buc, I., Lloubes, R., and Lazdunski, C. (1984).J. Mol. Biol. 180, 549–576.
von Meyenburg, K., Hansen, F. G., Riise, E., Bergmans, H. E. N., Meijer, M., and Messer, W. (1979).Cold Spring Harbor Symp. Quant. Biol. 43, 121–128.
von Meyenburg, K., Jorgenson, B. B., Nielsen, J., Hansen, F. G., and Michelsen, O. (1982a).Tokai J. Exp. Clin. Med. Suppl. 7, 23–31.
von Meyenburg, K., Jorgenson, B. B., Nielsen, J., and Hansen, F. G. (1982b).Mol. Gen. Genet. 188, 240–248.
von Meyenburg, K., Nielsen, J., Jorgensen, B. B., Michelsen, O., Hansen, F. G., and Van Deurs, B. (1984a). EBEC Rep. 3, pp. 67–68.
von Meyenburg, K., Jorgensen, B. B., and van Deurs, B. (1984b).EMBO J. 3, 1791–1797.
von Meyenburg, K., Jorgensen, B. B., Michelsen, O., Sorensen, L., and McCarthy, J. E. G. (1985).EMBO J. 4, 2357–2363.
Walker, J. E., Saraste, M., and Gay, N. J. (1984).Biochim. Biophys. Acta 768, 164–200.
Zuker, M., and Stiegler, P. (1981).Nucleic Acids Res. 9, 133–148.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
McCarthy, J.E.G. Expression of theunc genes inEscherichia coli . J Bioenerg Biomembr 20, 19–39 (1988). https://doi.org/10.1007/BF00762136
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00762136