DOI: 10.1128/jb.171.9.4609-4616.1989. Genetic studies on the inability of beta-galactosidase to be translocated across the Escherichia coli cytoplasmic membrane

Genetic studies on the inability of beta-galactosidase to be translocated across the Escherichia coli cytoplasmic membrane

10.1128/jb.171.9.4609-4616.1989

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

When a signal sequence is attached to beta-galactosidase, the normally cytoplasmic protein is unable to fully traverse the cytoplasmic membrane. We used a genetic approach to study those features of beta-galactosidase responsible for the block in translocation. By using both in vivo and in vitro techniques, fragments of beta-galactosidase were interposed between a signal sequence and alkaline phosphatase. The alkaline phosphatase acts as a sensor for any blocking effects of beta-galactosidase on export. From these studies, we show that multiple regions of beta-galactosidase contribute to its failure to be translocated. These results are most easily interpreted if the folding of beta-galactosidase or of domains of it is responsible for the block in export. In addition, in certain constructs, positively charged amino acids directly following the signal sequence interfered with export.

Bibliography

Lee, C., Li, P., Inouye, H., Brickman, E. R., & Beckwith, J. (1989). Genetic studies on the inability of beta-galactosidase to be translocated across the Escherichia coli cytoplasmic membrane. Journal of Bacteriology, 171(9), 4609â4616.

Authors 5

C Lee (first)
P Li (additional)
H Inouye (additional)
E R Brickman (additional)
J Beckwith (additional)

References 22 Referenced 77

Akiyama , Y. , and K. Ito . 1987 . Topological analysis of the SecY protein, an integral membrane protein involved in protein export in Escherichia coli . EMBO J. 6 : 3465 - 3470 . (10.1002/j.1460-2075.1987.tb02670.x) / EMBO J. / Topological analysis of the SecY protein, an integral membrane protein involved in protein export in Escherichia coli by Akiyama Y. (1987)
Bankaitis , V. A. , B. A. Rasmussen , and P. J. Bassford , Jr. 1984 . Intragenic suppressor mutations that restore export of maltose binding protein with a truncated signal peptide . Cell 37 : 243 - 252 . (10.1016/0092-8674(84)90320-9) / Cell / Intragenic suppressor mutations that restore export of maltose binding protein with a truncated signal peptide by Bankaitis V. A. (1984)
Bassford , P. J. , Jr. , T. J. Silhavy , and J. R. Beckwith . 1979 . Use of gene fusion to study secretion of maltose-binding protein into Escherichia coli periplasm . J. Bacteriol. 139 : 19 - 31 . (10.1128/JB.139.1.19-31.1979) / J. Bacteriol. / Use of gene fusion to study secretion of maltose-binding protein into Escherichia coli periplasm by Bassford P. J. (1979)
Beckwith , J. , and S. Ferro-Novick . 1985 . Genetic studies on protein export in bacteria . Curr. Top. Microbiol. Immunol. 125 : 5 - 27 . / Curr. Top. Microbiol. Immunol. / Genetic studies on protein export in bacteria by Beckwith J. (1985)
Boyd D. C.-D. Guan S. Willard W. Wright and J. Beckwith. 1987. The enzymatic activity of alkaline phosphatase precursor depends on its cellular location. p. 89-98. In A. M. Torriani F. G. Rothman S. Silver A. Wright and E. Yagil (ed.) Phosphate metabolism and cellular regulation in microorganisms. American Society for Microbiology Washington D.C.
Emr , S. D. , I. Schauer , W. Hansen , P. Esmon , and R. Schekman . 1984 . Invertase-f-galactosidase hybrid proteins fail to be transported from the endoplasmic reticulum in Saccharomyces cerevisiae . Mol. Cell. Biol. 4 : 2347 - 2355 . (10.1128/MCB.4.11.2347) / Mol. Cell. Biol. / Invertase-f-galactosidase hybrid proteins fail to be transported from the endoplasmic reticulum in Saccharomyces cerevisiae by Emr S. D. (1984)
Gannon , P. M. , P. Li , and C. A. Kumamoto . 1989 . The mature portion of Escherichia coli maltose-binding protein determines its dependence upon SecB for export . J. Bacteriol. 171 : 813 - 818 . (10.1128/jb.171.2.813-818.1989) / J. Bacteriol. / The mature portion of Escherichia coli maltose-binding protein determines its dependence upon SecB for export by Gannon P. M. (1989)
Gutierrez , C. , J. Barondess , C. Manoil , and J. Beckwith . 1987 . The use of transposon TnphoA to detect genes for cell envelope proteins subject to a common regulatory stimulus: analysis of osmotically-regulated genes in Escherichia coli . J. Mol. Biol. 195 : 289 - 297 . (10.1016/0022-2836(87)90650-4) / J. Mol. Biol. / The use of transposon TnphoA to detect genes for cell envelope proteins subject to a common regulatory stimulus: analysis of osmotically-regulated genes in Escherichia coli by Gutierrez C. (1987)
Hoffman , C. S. , and A. Wright . 1985 . Fusions of secreted proteins to alkaline phosphatase: an approach for studying protein secretion . Proc. Natl. Acad. Sci. USA 82 : 5107 - 5111 . (10.1073/pnas.82.15.5107) / Proc. Natl. Acad. Sci. USA / Fusions of secreted proteins to alkaline phosphatase: an approach for studying protein secretion by Hoffman C. S. (1985)
Kunkel , T. A. 1985 . The mutational specificity of DNA polymerase-,B during in vitro DNA synthesis . J. Biol. Chem. 260 : 5787 - 5796 . (10.1016/S0021-9258(18)89090-1) / J. Biol. Chem. / The mutational specificity of DNA polymerase-,B during in vitro DNA synthesis by Kunkel T. A. (1985)
Laemmli , U. K. 1970 . Cleavage of structural proteins during the assembly of the head of bacteriophage T4 . Nature (London) 222 : 680 - 685 . (10.1038/227680a0) / Nature (London) / Cleavage of structural proteins during the assembly of the head of bacteriophage T4 by Laemmli U. K. (1970)
Li , P. , J. Beckwith , and H. Inouye . 1988 . Alteration of the amino terminus of the mature sequence of a periplasmic protein can severely affect protein export in Escherichia coli . Proc. Natl. Acad. Sci. USA 85 : 7685 - 7689 . (10.1073/pnas.85.20.7685) / Proc. Natl. Acad. Sci. USA / Alteration of the amino terminus of the mature sequence of a periplasmic protein can severely affect protein export in Escherichia coli by Li P. (1988)
Maniatis T. E. F. Fritsch and K. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
Manoil , C. , and J. Beckwith . 1985 . TnphoA: a transposon probe for protein export signals . Proc. Natl. Acad. Sci. USA 82 : 8129 - 8133 . (10.1073/pnas.82.23.8129) / Proc. Natl. Acad. Sci. USA / TnphoA: a transposon probe for protein export signals by Manoil C. (1985)
Manoil , C. , and J. Beckwith . 1986 . A genetic approach to analyzing membrane protein topology . Science 233 : 1403 - 1408 . (10.1126/science.3529391) / Science / A genetic approach to analyzing membrane protein topology by Manoil C. (1986)
Michaelis , S. , H. Inouye , D. Oliver , and J. Beckwith . 1983 . Mutations that alter the signal sequence of alkaline phosphatase in Escherichia coli . J. Bacteriol. 154 : 366 - 374 . (10.1128/JB.154.1.366-374.1983) / J. Bacteriol. / Mutations that alter the signal sequence of alkaline phosphatase in Escherichia coli by Michaelis S. (1983)
Miller J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
Newton , J. , J. Beckwith , D. Zipser , and S. Brenner . 1965 . Nonsense mutants and polarity in the lac operon of E. coli . J. Mol. Biol. 14 : 290 - 296 . (10.1016/S0022-2836(65)80250-9) / J. Mol. Biol. / Nonsense mutants and polarity in the lac operon of E. coli by Newton J. (1965)
Randall , L. L. , and S. J. S. Hardy . 1986 . Correlation of competence for export with lack of tertiary structure of the mature species; a study in vivo of maltose binding protein in E. coli . Cell 46 : 921 - 928 . (10.1016/0092-8674(86)90074-7) / Cell / Correlation of competence for export with lack of tertiary structure of the mature species; a study in vivo of maltose binding protein in E. coli by Randall L. L. (1986)
Rasmussen , B. A. , V. A. Bankaitis , and P. J. Bassford , Jr. 1984 . Export and processing of MalE-LacZ hybrid proteins in Escherichia coli . J. Bacteriol. 160 : 612 - 617 . (10.1128/JB.160.2.612-617.1984) / J. Bacteriol. / Export and processing of MalE-LacZ hybrid proteins in Escherichia coli by Rasmussen B. A. (1984)
Sarthy , A. , S. Michaelis , and J. Beckwith . 1981 . Use of gene fusions to determine the orientation of gene phoA on the Escherichia coli chromosome . J. Bacteriol. 145 : 293 - 298 . (10.1128/JB.145.1.293-298.1981) / J. Bacteriol. / Use of gene fusions to determine the orientation of gene phoA on the Escherichia coli chromosome by Sarthy A. (1981)
Schwartz , M. , M. Roa , and M. Debarbouille . 1981 . Mutations that affect lamB gene expression at a posttranslational level . Proc. Nati. Acad. Sci. USA 78 : 2937 - 2941 . (10.1073/pnas.78.5.2937) / Proc. Nati. Acad. Sci. USA / Mutations that affect lamB gene expression at a posttranslational level by Schwartz M. (1981)

Dates

Type	When
Created	8 years, 9 months ago (Nov. 4, 2016, 1:48 p.m.)
Deposited	4 years ago (July 29, 2021, 1:45 p.m.)
Indexed	1 year, 9 months ago (Nov. 6, 2023, 10:09 a.m.)
Issued	35 years, 11 months ago (Sept. 1, 1989)
Published	35 years, 11 months ago (Sept. 1, 1989)
Published Print	35 years, 11 months ago (Sept. 1, 1989)

Funders 0

None

BibTeX

@article{Lee_1989, title={Genetic studies on the inability of beta-galactosidase to be translocated across the Escherichia coli cytoplasmic membrane}, volume={171}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.171.9.4609-4616.1989}, DOI={10.1128/jb.171.9.4609-4616.1989}, number={9}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Lee, C and Li, P and Inouye, H and Brickman, E R and Beckwith, J}, year={1989}, month=sep, pages={4609–4616} }

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