Heat-shock Proteins Can Substitute for SecB Function During Protein Export in Escherichia Coli

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1991 Feb 1

PMID 1671351

Citations 34

Authors

E Altman

C A Kumamoto

S D Emr

Affiliations

Soon will be listed here.

Abstract

In this study we have shown that (i) induction of the heat-shock response can substitute for SecB function in Escherichia coli, (ii) SecB itself is not a heat-shock protein and (iii) a basal level of heat-shock proteins is required for cells to grow in the absence of a functional SecB protein. Overproduction of DnaK, or GroEL/ES, which were candidates for the heat-shock proteins that could substitute for SecB function, did not rescue the export defect caused when SecB was limiting or absent. In an attempt to identify the heat-shock protein(s) which could substitute for SecB function, unlinked suppressors of secB were isolated and characterized. Interestingly, most of the suppressors mapped to the rpoH locus. Since rpoH encodes sigma 32, the heat-shock transcription factor, it is likely that these suppressors affect the synthesis levels of heat-shock proteins that can substitute for SecB function. The remaining suppressors did not map to any known heat-shock or export genes. Collectively, our data suggest that these suppressors may represent unidentified heat-shock proteins or export factors that act in a manner similar to SecB in facilitating the export process in E. coli.

Citing Articles

How Quality Control Systems AID Sec-Dependent Protein Translocation.

Jiang C, Wynne M, Huber D Front Mol Biosci. 2021; 8:669376.

PMID: 33928127 PMC: 8076867. DOI: 10.3389/fmolb.2021.669376.

The Sec System: Protein Export in .

Crane J, Randall L EcoSal Plus. 2017; 7(2).

PMID: 29165233 PMC: 5807066. DOI: 10.1128/ecosalplus.ESP-0002-2017.

Multitasking SecB chaperones in bacteria.

Sala A, Bordes P, Genevaux P Front Microbiol. 2014; 5:666.

PMID: 25538690 PMC: 4257090. DOI: 10.3389/fmicb.2014.00666.

Lon protease quality control of presecretory proteins in Escherichia coli and its dependence on the SecB and DnaJ (Hsp40) chaperones.

Sakr S, Cirinesi A, Ullers R, Schwager F, Georgopoulos C, Genevaux P J Biol Chem. 2010; 285(30):23506-14.

PMID: 20504766 PMC: 2906341. DOI: 10.1074/jbc.M110.133058.

Secretion of GOB metallo-beta-lactamase in Escherichia coli depends strictly on the cooperation between the cytoplasmic DnaK chaperone system and the Sec machinery: completion of folding and Zn(II) ion acquisition occur in the bacterial periplasm.

Moran-Barrio J, Limansky A, Viale A Antimicrob Agents Chemother. 2009; 53(7):2908-17.

PMID: 19433552 PMC: 2704670. DOI: 10.1128/AAC.01637-08.

References

Randall L, Hardy S . 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. 1986; 46(6):921-8. DOI: 10.1016/0092-8674(86)90074-7. View

Yamamori T, Yura T . Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1982; 79(3):860-4. PMC: 345852. DOI: 10.1073/pnas.79.3.860. View

Ellis J . Proteins as molecular chaperones. Nature. 1987; 328(6129):378-9. DOI: 10.1038/328378a0. View

Collier D, Bankaitis V, Weiss J, Bassford Jr P . The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein. Cell. 1988; 53(2):273-83. DOI: 10.1016/0092-8674(88)90389-3. View

Weiss J, Ray P, Bassford Jr P . Purified secB protein of Escherichia coli retards folding and promotes membrane translocation of the maltose-binding protein in vitro. Proc Natl Acad Sci U S A. 1988; 85(23):8978-82. PMC: 282643. DOI: 10.1073/pnas.85.23.8978. View

Fayet O, Louarn J, Georgopoulos C . Suppression of the Escherichia coli dnaA46 mutation by amplification of the groES and groEL genes. Mol Gen Genet. 1986; 202(3):435-45. DOI: 10.1007/BF00333274. View

Pelham H . Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 1986; 46(7):959-61. DOI: 10.1016/0092-8674(86)90693-8. View

Kumamoto C, Gannon P . Effects of Escherichia coli secB mutations on pre-maltose binding protein conformation and export kinetics. J Biol Chem. 1988; 263(23):11554-8. View

Ellis R, Hemmingsen S . Molecular chaperones: proteins essential for the biogenesis of some macromolecular structures. Trends Biochem Sci. 1989; 14(8):339-42. DOI: 10.1016/0968-0004(89)90168-0. View

10.

Kusukawa N, Yura T, Ueguchi C, Akiyama Y, Ito K . Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J. 1989; 8(11):3517-21. PMC: 401509. DOI: 10.1002/j.1460-2075.1989.tb08517.x. View

11.

Lecker S, Lill R, Ziegelhoffer T, Georgopoulos C, Bassford Jr P, Kumamoto C . Three pure chaperone proteins of Escherichia coli--SecB, trigger factor and GroEL--form soluble complexes with precursor proteins in vitro. EMBO J. 1989; 8(9):2703-9. PMC: 401277. DOI: 10.1002/j.1460-2075.1989.tb08411.x. View

12.

Ellis R, Van Der Vies S, Hemmingsen S . The molecular chaperone concept. Biochem Soc Symp. 1989; 55:145-53. View

13.

Watanabe M, Blobel G . Cytosolic factor purified from Escherichia coli is necessary and sufficient for the export of a preprotein and is a homotetramer of SecB. Proc Natl Acad Sci U S A. 1989; 86(8):2728-32. PMC: 286991. DOI: 10.1073/pnas.86.8.2728. View

14.

Kumamoto C, Chen L, Fandl J, Tai P . Purification of the Escherichia coli secB gene product and demonstration of its activity in an in vitro protein translocation system. J Biol Chem. 1989; 264(4):2242-9. View

15.

Zhou Y, Kusukawa N, Erickson J, Gross C, Yura T . Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor sigma 32. J Bacteriol. 1988; 170(8):3640-9. PMC: 211339. DOI: 10.1128/jb.170.8.3640-3649.1988. View

16.

Chirico W, Waters M, Blobel G . 70K heat shock related proteins stimulate protein translocation into microsomes. Nature. 1988; 332(6167):805-10. DOI: 10.1038/332805a0. View

17.

Deshaies R, Koch B, Werner-Washburne M, Craig E, Schekman R . A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature. 1988; 332(6167):800-5. DOI: 10.1038/332800a0. View

18.

Bankaitis V, Bassford Jr P . The synthesis of export-defective proteins can interfere with normal protein export in Escherichia coli. J Biol Chem. 1984; 259(19):12193-200. View

19.

Grossman A, Straus D, WALTER W, Gross C . Sigma 32 synthesis can regulate the synthesis of heat shock proteins in Escherichia coli. Genes Dev. 1987; 1(2):179-84. DOI: 10.1101/gad.1.2.179. View

20.

Kumamoto C, Beckwith J . Evidence for specificity at an early step in protein export in Escherichia coli. J Bacteriol. 1985; 163(1):267-74. PMC: 219108. DOI: 10.1128/jb.163.1.267-274.1985. View