Abstract
The export of the maltose-binding protein (MBP), themalE gene product, to the periplasm ofEschericha coli cells has been extensively investigated. The isolation of strains synthesizing MalE-LacZ hybrid proteins led to a novel genetic selection for mutants that accumulate export-defective precursor MBP (preMBP) in the cytoplasm. The export defects were subsequently shown to result from alterations in the MBP signal peptide. Analysis of these and a variety of mutants obtained in other ways has provided considerable insight into the requirements for an optimally functional MBP signal peptide. This structure has been shown to have multiple roles in the export process, including promoting entry of preMBP into the export pathway and initiating MBP translocation across the cytoplasmic membrane. The latter has been shown to be a late event relative to synthesis and can occur entirely posttranslationally, even many minutes after the completion of synthesis. Translocation requires that the MBP polypeptide exist in an export-competent conformation that most likely represents an unfolded state that is not inhibitory to membrane transit. The signal peptide contributes to the export competence of preMBP by slowing the rate at which the attached mature moiety folds. In addition, preMBP folding is thought to be further retarded by the binding of a cytoplasmic protein, SecB, to the mature moiety of nascent preMBP. In cells lacking this antifolding factor, MBP export represents a race between delivery of newly synthesized, export-competent preMBP to the translocation machinery in the cytoplasmic membrane and folding of preMBP into an export-incompetent conformation. SecB is one of threeE. coli proteins classified as “molecular chaperones” by their ability to stabilize precursor proteins for membrane translocation.
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Arfmann, H.-A., Labitzke, R., and Wagner, K. G. (1977).Biopolymers 16, 1815–1826.
Bacallao, R., Crooke, E., Shiba, K., Wickner, W., and Ito, K. (1986).J. Biol. Chem. 261, 12907–12910.
Bankaitis, V. A., and Bassford, P. J., Jr. (1984).J. Biol. Chem. 259, 12193–12200.
Bankaitis, V. A., and Bassford, P. J., Jr. (1985).J. Bacteriol. 161, 169–178.
Bankaitis, V. A., Rasmussen, B. A., and Bassford, P. J., Jr. (1984).Cell 37, 243–252.
Bankaitis, V. A., Ryan, J. P., Rasmussen, B. A., and Bassford, P. J., Jr. (1985).Curr. Top. Memb. Transp. 24, 105–150.
Bassford, P. J., Jr., and Beckwith, J. (1979).Nature (London)277, 538–541.
Bassford, P. J., Jr., Silhavy, T. J., and Beckwith, J. R. (1979).J. Bacteriol. 139, 19–31.
Bayer, M. H., Costello, G. P., and Bayer, M. E. (1982).J. Bacteriol. 149, 758–767.
Bedouelle, H., and Hofnung, M. (1981). InMembrane Transport and Neuroreceptors (Oxender, D., ed.), Alan R. Liss, New York, pp. 309–343.
Bedouelle, H., Bassford, P. J., Jr., Fowler, A. V., Zabin, I., Beckwith, J., and Hofnung, M. (1980).Nature (London)285, 78–81.
Benson, S. A., Bremer, E., and Silhavy, T. J. (1984).Proc. Natl. Acad. Sci. USA 81, 3830–3834.
Bernstein, H. D. (1989).Cell 58, 1017–1019.
Bieker, K. L., and Silhavy, T. J. (1989).Proc. Natl. Acad. Sci. USA 86, 968–972.
Blobel, G., and Dobberstein, B. (1975).J. Cell Biol. 67, 835–851.
Bochkareva, E. S., Lissin, N. M., and Girsohovich, A. S. (1988).Nature (London)336, 254–257.
Bosch, D., de Boer, P., Bitter, W., and Tommassen, J. (1989).Biochim. Biophys. Acta 979, 69–76.
Boyd, D., and Beckwith, J. (1989).Proc. Natl. Acad. Sci. USA 86, 9446–9450.
Briggs, M. S., Gierasch, L. M., Zlotnick, A., Lear, J. D., and DeGrado, W. F. (1985).Science 228, 1096–1099.
Cancedda, R., and Schlessinger, M. (1974).J. Bacteriol. 117, 290–301.
Chen, L., Rhoads, D., and Tai, P. C. (1985).J. Bacteriol. 161, 973–980.
Collier, D. N., and Bassford, P. J., Jr. (1989).J. Bacteriol. 171, 4640–4647.
Collier, D. N., Bankaitis, V. A., Weiss, J. B., and Bassford, P. J., Jr. (1988).Cell 53, 273–283.
Cover, W. H., Ryan, J. P., Bassford, P. J., Jr., Walsh, K. A., Bollinger, J., and Randall, L. L. (1987).J. Bacteriol. 169, 1794–1800.
Crooke, E., and Wickner, W. (1987).Proc. Natl. Acad. Sci. USA 84, 5216–5220.
Crooke, E., Brundage, L., Rice, M. and Wickner, W. (1988a).EMBO J. 7, 1831–1835.
Crooke, E., Guthrie, B., Lecker, S., Lill, R., and Wickner, W. (1988b).Cell 54, 1003–1011.
Cunningham, K., and Wickner, W. (1989).Proc. Natl. Acad. Sci. USA 86, 8630–8634.
Dalbey, R. E., and Wickner, W. (1985).J. Biol. Chem. 260, 15925–15931.
Date, T., Goodman, J. M., and Wickner, W. T. (1980).Proc. Natl. Acad. Sci. USA 77, 4669–4673.
Davis, N. G., and Model, P. (1985).Cell 41, 607–614.
Dean, D. A., Fikes, J. D., Gehring, K., Bassford, P. J., Jr., and Nikaido, H. (1989).J. Bacteriol. 171, 503–510.
Dierstein, R., and Wickner, W. (1985).J. Biol. Chem. 260, 15919–15924.
Duffaud, G. D., Lehnhardt, S. K., March, P. E., and Inouye, M. (1985).Curr. Top. Membr. Transp. 24, 65–104.
Duplay, P., Bedouelle, H., Fowler, A., Zabin, I., Saukinm, W., and Hofnung, M. (1984).J. Biol. Chem. 259, 10606–10613.
Eilers, M., and Schatz, G. (1988).Cell 52, 481–483.
Ellis, R. J., and Hemmingsen, S. M. (1989).Trends Biochem. Sci. 14, 339–342.
Emr, S. D., and Bassford, P. J., Jr. (1982).J. Biol. Chem. 257, 5852–5860.
Emr, S. D., and Silhavy, T. J. (1983).Proc. Natl. Acad. Sci. USA 80, 4599–4603.
Emr, S. D., Hanley-Way, S., and Silhavy, T. J. (1981).Cell 23, 79–88.
Engelman, D. M., and Steitz, T. A. (1981).Cell 23, 411–422.
Ferenci, T., and Randall, L. L. (1979).J. Biol. Chem. 254, 9979–9981.
Ferenci, T., and Silhavy, T. J. (1987).J. Bacteriol. 169, 5339–5342.
Fikes, J. D., and Bassford, P. J., Jr. (1987).J. Bacteriol. 169, 2352–2359.
Fikes, J. D., and Bassford, P. J., Jr. (1989).J. Bacteriol. 171, 402–409.
Fikes, J. D., Bankaitis, V. A., Ryan, J. P., and Bassford, P. J., Jr. (1987).J. Bacteriol. 169, 2345–2351.
Fikes, J. D., Barkocy-Gallagher, G. A., Klapper, D. G., and Bassford, P. J., Jr. (1990).J. Biol. Chem. 265, 3417–3423.
Freudi, R., Schwarz, H., Kramps, S., Hindennach, I., and Henning, U. (1988).J. Biol. Chem. 263, 17084–17091.
Gannon, P. M., Li, P., and Kumamoto, C. A. (1989).J. Bacteriol. 171, 813–818.
Georgopoulos, C. P., and Hohn, B. (1978).Proc. Natl. Acac. Sci. USA 75, 131–135.
Goloubinoff, P., Gatenby, A. A., and Lorimer, G. H. (1989).Nature (London)337, 44–47.
Goodman, J. M., Watts, C., and Wickner, W. (1981).Cell 24, 437–441.
Hall, M. N., Gabay, J., and Schwartz, M. (1983).EMBO J. 2, 15–19.
Hemmingsen, S. M., Woolford, C., van der Vies, S. M., Tilly, K., Dennis, D. T., Georgopoulos, C. P., Hendrix, R., and Ellis, R. J. (1988).Nature (London)333, 330–334.
Hendrix, R. W. (1979).J. Mol. Biol. 129, 375–392.
Herrero, E., Jackson, M., Bassford, P. J., Sinden, D., and Holland, I. B. (1982).J. Bacteriol. 152, 133–139.
Hohn, T., Hohn, B., Engel, A., Wurtz, M., and Smith, P. R. (1979).J. Mol. Biol. 129 359–373.
Iino, T., and Sako, T. (1988).J. Biol. Chem. 263, 19077–19082.
Iino, T., Takahashi, M., and Sako, T. (1987).J. Biol. Chem. 262, 7412–7417.
Inouye, M., and Halegoua, S. (1980).Crit. Rev. Biochem. 7, 339–371.
Inouye, S., Soberon, X., Franceschini, T., Nakamura, K., and Inouye, M. (1982).Proc. Natl. Acad. Sci. USA 79, 3138–3141.
Ito, K. (1984).Mol. Gen. Genet. 197, 204–208.
Ito, K., and Beckwith, J. (1981).Cell 25, 143–150.
Ito, K., Mandel, G., and Wickner, W. (1979).Proc. Natl. Acad. Sci. USA 76, 1199–1203.
Ito, K., Bassford, P. J., Jr., and Beckwith, J. (1981).Cell 24, 707–717.
Josefsson, L.-G., and Randall, L. L. (1981a).J. Biol. Chem. 256, 2504–2507.
Josefsson, L.-G., and Randall, L. L. (1981b).Cell 25, 151–157.
Kaiser, C. A., Preuss, D., Grisafi, P., and Botstein, D. (1987).Science 235, 312–317.
Kendall, D. A., and Kaiser, E. T. (1988).J. Biol. Chem. 263, 7261–7265.
Kendall, D. A., Boch, S. C., and Kaiser, E. T. (1986).Nature (London)321, 706–708.
Koshland, D., and Botstein, D. (1980).Cell 25, 151–157.
Kuhn, A., and Wickner, W. (1985).J. Biol. Chem. 260, 15914–15918.
Kumamoto, C. A. (1989).Proc. Natl. Acad. Sci. USA 86, 5320–5324.
Kumamoto, C. A., and Beckwith, J. (1983).J. Bacteriol. 154, 253–260.
Kumamoto, C. A., and Beckwith, J. (1985).J. Bacteriol. 163, 267–274.
Kumamoto, C. A., and Gannon, P. M. (1988).J. Biol. Chem. 263, 11554–11558.
Kumamoto, C. A., and Nault, A. K. (1989).Gene 75, 167–175.
Kusukawa, N., Yura, T., Ueguchi, C., Akiyama, Y., and Ito, K. (1989).EMBO J. 8, 3517–3521.
Lee, C., Li, P., Inouye, H., Brickman, E. R., and Beckwith, J. (1989).J. Bacteriol. 171, 4609–4616.
Lecker, S., Lill, R., Ziegelhoffer, T., Georgopoulos, C., Bassford, P. J., Jr., Kumamoto, C. A., and Wickner, W. (1989).EMBO J. 8, 2703–2709.
Li, P., Beckwith, J., and Inouye, H. (1988).Proc. Natl. Acad. Sci. USA 85, 7685–7689.
Lill, R., Crooke, E., Guthrie, B., and Wickner, W. (1988).Cell 54, 1013–1018.
Liu, G., Topping, T. B., Cover, W. H., and Randall, L. L. (1988).J. Biol. Chem. 263, 14790–14793.
Liu, G., Topping, T. B., and Randall, L. L. (1989).Proc. Natl. Acad. Sci. USA 86, 9213–9217.
Meyer, D. I. (1988).Trends Biochem. Sci. 13, 471–474.
Michaelis, S., Hunt, J. F., and Beckwith, J. (1986).J. Bacteriol. 167, 160–167.
Millan, J. L. S., Boyd, D., Dalbey, R., Wickner, W., and Beckwith, J. (1989).J. Bacteriol. 171, 5536–5541.
Moreno, F., Fowler, A. V., Hall, M., Silhavy, T. J., Zabin, I., and Schwartz, M. (1980).Nature (London)286, 356–359.
Müller, M., and Blobel, G. (1984).Proc. Natl. Acad. Sci. USA 81, 7421–7425.
Oliver, D. B., and Beckwith, J. (1981).Cell 25, 765–772.
Oliver, D. B., and Beckwith, J. (1982).J. Bacteriol. 150, 686–691.
Park, S., Liu, G., Topping, T. B., Cover, W. H., and Randall, L. L. (1988).Science 239, 1033–1035.
Perlman, D., and Halvorson, H. O. (1983).J. Mol. Biol. 167, 391–409.
Puziss, J. W., Fikes, J. D., and Bassford, P. J., Jr. (1989).J. Bacteriol. 171, 2303–2311.
Randall, L. L. (1983).Cell 33, 231–240.
Randall, L. L. (1987).Annu. Rev. Microbiol. 41, 507–541.
Randall, L. L., and Hardy, S. J. S. (1975).Mol. Gen. Genet. 137, 151–160.
Randall, L. L., and Hardy, S. J. S. (1977).Eur. J. Biochem. 75, 43–53.
Randall, L. L., and Hardy, S. J. S. (1986).Cell 46, 921–928.
Randall, L. L., and Hardy, S. J. S. (1989).Science 243, 1156–1159.
Randall, L. L., Hardy, S. J. S., and Josefsson, L. -G. (1978).Proc. Natl. Acad. Sci. USA 75, 1209–1212.
Rasmussen, B. A., and Bassford, P. J., Jr. (1985).J. Bacteriol. 161, 258–264.
Rasmussen, B. A., and Silhavy, T. J. (1987).Genes Dev. 1, 185–196.
Rasmussen, B. A., Bankaitis, V. A., and Bassford, P. J., Jr. (1984).J. Bacteriol. 160, 612–617.
Rasmussen, B. A., MacGregor, C. H., Ray, P. H., and Bassford, P. J., Jr. (1985).J. Bacteriol. 164, 665–673.
Rhoads, D. B., Tai, P. C., and Davis, B. D. (1984).J. Bacteriol. 159, 63–70.
Rothman, J. A. (1989).Cell 59, 591–601.
Ryan, J. P., and Bassford, P. J., Jr. (1985).J. Biol. Chem. 260, 14832–14837.
Ryan, J. P., Duncan, M. C., Bankaitis, V. A., and Bassford, P. J., Jr. (1986a).J. Biol. Chem. 261, 3389–3395.
Ryan, J. P., Fikes, J. D., Bankaitis, V. A., Duncan, M. C., and Bassford, P. J., Jr. (1986b). InMicrobiology 1986 (Leive, L., ed.), American Society for Microbiology, Washington, DC, pp. 254–259.
Schmidt, M. G., Rollo, E. E., Grodberg, J., and Oliver, D. B. (1988).J. Bacteriol. 170, 3404–3414.
Schwartz, M., Roa, M., and Debarbouille, M. (1981).Proc. Natl. Acad. Sci. USA 78, 2937–2941.
Silhavy, T. J., Shuman, H. A., Beckwith, J., and Schwartz, M. (1977).Proc. Natl. Acad. Sci. USA 74, 5411–5415.
Silhavy, T. J., Benson, S. A., and Emr, S. D. (1983).Microbiol. Rev. 47, 313–344.
Sjöström, M., Wold, S., Wieslander, A., and Rilfors, L. (1987).EMBO J. 6, 823–831.
Stader, J., Benson, S. A., and Silhavy, T. J. (1986).J. Biol. Chem. 261, 15075–15080.
Stader, J. A., Gansheroff, L. J., and Silhavy, T. J. (1989).Genes Dev. 3, 1045–1052.
Summers, R. G., and Knowles, J. R. (1989).J. Biol. Chem. 264, 20074–20081.
Summers, R. G., Harris, C. R., and Knowles, J. R. (1989).J. Biol. Chem. 264, 20082–20088.
Szczesna-Skopupa, E., Browne, N., Mead, D., and Kemper, B. (1988).Proc. Natl. Acad. Sci. USA 85, 738–742.
Thom, J. R., and Randall, L. L. (1988).J. Bacteriol. 170, 5654–5661.
Verner, K., and Schatz, G. (1988).Science 241, 1307–1313.
Vlasuk, G. P., Inouye, S., Ito, H., Itakura, K., and Inouye, M. (1983).J. Biol. Chem. 258, 7141–7148.
von Heijne, G. (1983).Eur. J. Biochem. 133, 17–21.
von Heijne, G. (1985).J. Mol. Biol. 184, 99–105.
von Heijne, G. (1986).Nucleic Acids Res. 14, 4683–4690.
von Heijne, G., Wickner, W., and Dalbey, R. E. (1988).Proc. Natl. Acad. Sci. USA 85, 3363–3366.
Walter, P., and Lingappa, V. R. (1986).Annu. Rev. Cell Biol. 2, 499–516.
Watanabe, M., and Blobel, G. (1989a).Proc. Natl. Acad. Sci. USA 86, 2248–2252.
Watanabe, M., and Blobel, G. (1989b).Proc. Natl. Acad. Sci. USA 86, 2728–2732.
Watanabe, M., and Blobel, G. (1989c).Cell 58, 695–705.
Weiss, J. B., and Bassford, P. J., Jr. (1990).J. Bacteriol. 172, in press.
Weiss, J. B., Ray, P. H., and Bassford, P. J., Jr. (1988).Proc. Natl. Acad. Sci. USA 85, 8978–8982.
Weiss, J. B., MacGregor, C. H., Collier, D. N., Fikes, J. D., Ray, P. H., and Bassford, P. J., Jr. (1989).J. Biol. Chem. 264, 3021–3027.
Wickner, W. (1979).Annu. Rev. Biochem. 48, 23–45.
Wu, H., and Tokunaga, M. (1986).Curr. Top. Microbiol. Immunol. 125, 128–157.
Yamane, K., Ichihara, S., and Mizushima, S. (1987).J. Biol. Chem. 262, 2358–2362.
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Bassford, P.J. Export of the periplasmic maltose-binding protein ofEscherichia coli . J Bioenerg Biomembr 22, 401–439 (1990). https://doi.org/10.1007/BF00763175
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DOI: https://doi.org/10.1007/BF00763175