Subunit Interactions in ABC Transporters: a Conserved Sequence in Hydrophobic Membrane Proteins of Periplasmic Permeases Defines an Important Site of Interaction with the ATPase Subunits

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1997 Jun 2

PMID 9214624

Citations 65

Authors

M Mourez

M Hofnung

E Dassa

Affiliations

Soon will be listed here.

Abstract

The cytoplasmic membrane proteins of bacterial binding protein-dependent transporters belong to the superfamily of ABC transporters. The hydrophobic proteins display a conserved, at least 20 amino acid EAA---G---------I-LP region exposed in the cytosol, the EAA region. We mutagenized the EAA regions of MalF and MalG proteins of the Escherichia coli maltose transport system. Substitutions at the same positions in MalF and MalG have different phenotypes, indicating that EAA regions do not act symmetrically. Mutations in malG or malF that slightly affect or do not affect transport, determine a completely defective phenotype when present together. This suggests that EAA regions of MalF and MalG may interact during transport. Maltose-negative mutants fall into two categories with respect to the cellular localization of the MalK ATPase: in the first, MalK is membrane-bound, as in wild-type strains, while in the second, it is cytosolic, as in strains deleted in the malF and malG genes. From maltose-negative mutants of the two categories, we isolated suppressor mutations within malK that restore transport. They map mainly in the putative helical domain of MalK, suggesting that EAA regions may constitute a recognition site for the ABC ATPase helical domain.

Citing Articles

Structural basis for negative regulation of the Escherichia coli maltose system.

Wu Y, Sun Y, Richet E, Han Z, Chai J Nat Commun. 2023; 14(1):4925.

PMID: 37582800 PMC: 10427625. DOI: 10.1038/s41467-023-40447-y.

The repertoire of ABC proteins in .

Pipatthana M, Harnvoravongchai P, Pongchaikul P, Likhitrattanapisal S, Phanchana M, Chankhamhaengdecha S Comput Struct Biotechnol J. 2021; 19:2905-2920.

PMID: 34094001 PMC: 8144104. DOI: 10.1016/j.csbj.2021.05.012.

The functional analysis of ABCG transporters in the adaptation of pigeon pea () to abiotic stresses.

Niu L, Li H, Song Z, Dong B, Cao H, Liu T PeerJ. 2021; 9:e10688.

PMID: 33552725 PMC: 7821757. DOI: 10.7717/peerj.10688.

The Operon Encodes a Predicted ABC Importer Required for Fitness and Virulence during Group A Invasive Infection.

Braza R, Le Breton Y, McIver K Infect Immun. 2019; 87(12).

PMID: 31591169 PMC: 6867869. DOI: 10.1128/IAI.00613-19.

An integrated transport mechanism of the maltose ABC importer.

Machtel R, Narducci A, Griffith D, Cordes T, Orelle C Res Microbiol. 2019; 170(8):321-337.

PMID: 31560984 PMC: 6906923. DOI: 10.1016/j.resmic.2019.09.004.

References

Szmelcman S, Hofnung M . Maltose transport in Escherichia coli K-12: involvement of the bacteriophage lambda receptor. J Bacteriol. 1975; 124(1):112-8. PMC: 235871. DOI: 10.1128/jb.124.1.112-118.1975. View

Wilken S, Schmees G, Schneider E . A putative helical domain in the MalK subunit of the ATP-binding-cassette transport system for maltose of Salmonella typhimurium (MalFGK2) is crucial for interaction with MalF and MalG. A study using the LacK protein of Agrobacterium radiobacter as.... Mol Microbiol. 1996; 22(4):655-66. DOI: 10.1046/j.1365-2958.1996.d01-1724.x. View

Humphreys G, Willshaw G, Smith H, Anderson E . Mutagenesis of plasmid DNA with hydroxylamine: isolation of mutants of multi-copy plasmids. Mol Gen Genet. 1976; 145(1):101-8. DOI: 10.1007/BF00331564. View

Szmelcman S, Schwartz M, Silhavy T, Boos W . Maltose transport in Escherichia coli K12. A comparison of transport kinetics in wild-type and lambda-resistant mutants as measured by fluorescence quenching. Eur J Biochem. 1976; 65(1):13-9. DOI: 10.1111/j.1432-1033.1976.tb10383.x. View

Diedrich D, Summers A, Schnaitman C . Outer membrane proteins of Escherichia coli. V. Evidence that protein 1 and bacteriophage-directed protein 2 are different polypeptides. J Bacteriol. 1977; 131(2):598-607. PMC: 235469. DOI: 10.1128/jb.131.2.598-607.1977. View

Towbin H, Staehelin T, Gordon J . Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979; 76(9):4350-4. PMC: 411572. DOI: 10.1073/pnas.76.9.4350. View

Shuman H, Silhavy T, Beckwith J . Labeling of proteins with beta-galactosidase by gene fusion. Identification of a cytoplasmic membrane component of the Escherichia coli maltose transport system. J Biol Chem. 1980; 255(1):168-74. View

Dassa E, Hofnung M . Sequence of gene malG in E. coli K12: homologies between integral membrane components from binding protein-dependent transport systems. EMBO J. 1985; 4(9):2287-93. PMC: 554499. DOI: 10.1002/j.1460-2075.1985.tb03928.x. View

Boyd D, Manoil C, Beckwith J . Determinants of membrane protein topology. Proc Natl Acad Sci U S A. 1987; 84(23):8525-9. PMC: 299577. DOI: 10.1073/pnas.84.23.8525. View

10.

AMES G, Mimura C, Shyamala V . Bacterial periplasmic permeases belong to a family of transport proteins operating from Escherichia coli to human: Traffic ATPases. FEMS Microbiol Rev. 1990; 6(4):429-46. DOI: 10.1111/j.1574-6968.1990.tb04110.x. View

11.

Mimura C, Holbrook S, AMES G . Structural model of the nucleotide-binding conserved component of periplasmic permeases. Proc Natl Acad Sci U S A. 1991; 88(1):84-8. PMC: 50753. DOI: 10.1073/pnas.88.1.84. View

12.

Davidson A, Nikaido H . Purification and characterization of the membrane-associated components of the maltose transport system from Escherichia coli. J Biol Chem. 1991; 266(14):8946-51. View

13.

Wang R, Kushner S . Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene. 1991; 100:195-9. View

14.

Shyamala V, Baichwal V, Beall E, AMES G . Structure-function analysis of the histidine permease and comparison with cystic fibrosis mutations. J Biol Chem. 1991; 266(28):18714-9. View

15.

Schneider E, Walter C . A chimeric nucleotide-binding protein, encoded by a hisP-malK hybrid gene, is functional in maltose transport in Salmonella typhimurium. Mol Microbiol. 1991; 5(6):1375-83. DOI: 10.1111/j.1365-2958.1991.tb00784.x. View

16.

Davidson A, Shuman H, Nikaido H . Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins. Proc Natl Acad Sci U S A. 1992; 89(6):2360-4. PMC: 48657. DOI: 10.1073/pnas.89.6.2360. View

17.

Walter C, Honer zu Bentrup K, Schneider E . Large scale purification, nucleotide binding properties, and ATPase activity of the MalK subunit of Salmonella typhimurium maltose transport complex. J Biol Chem. 1992; 267(13):8863-9. View

18.

Walter C, Wilken S, Schneider E . Characterization of site-directed mutations in conserved domains of MalK, a bacterial member of the ATP-binding cassette (ABC) family [corrected]. FEBS Lett. 1992; 303(1):41-4. DOI: 10.1016/0014-5793(92)80473-t. View

19.

Blasiak M, Otrebski S, Pacyk G . [Twenty-four hour heart rate variability in patients with acute myocardial infarction depending on treatment]. Pol Merkur Lekarski. 1997; 2(8):107-8. View

20.

Reyes M, Shuman H . Overproduction of MalK protein prevents expression of the Escherichia coli mal regulon. J Bacteriol. 1988; 170(10):4598-602. PMC: 211497. DOI: 10.1128/jb.170.10.4598-4602.1988. View