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. 1992 Mar 15;89(6):2360–2364. doi: 10.1073/pnas.89.6.2360

Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins.

A L Davidson 1, H A Shuman 1, H Nikaido 1
PMCID: PMC48657  PMID: 1549599

Abstract

Maltose transport across the cytoplasmic membrane of Escherichia coli is dependent on the presence of a periplasmic maltose-binding protein (MBP), the product of the malE gene. The products of the malF, malG, and malK genes form a membrane-associated complex that catalyzes the hydrolysis of ATP to provide energy for the transport event. Previously, mutants were isolated that had gained the ability to grow on maltose in the absence of MBP. After reconstitution of the transport complex into proteoliposomes, measurement of the ATPase activity of wild-type and mutant complexes in the presence and absence of MBP revealed that the wild-type complex hydrolyzed ATP rapidly only when MBP and maltose were both present. In contrast, the mutant complexes have gained the ability to hydrolyze ATP in the absence of maltose and MBP. The basal rate of hydrolysis by the different mutant complexes was directly proportional to the growth rate of that strain on maltose, a result indicating that the constitutive ATP hydrolysis and presumably the resultant cyclic conformational changes of the complex produce maltose transport in the absence of MBP. These results also suggest that ATP hydrolysis is not directly coupled to ligand transport even in wild-type cells and that one important function of MBP is to transmit a transmembrane signal, through the membrane-spanning MalF and MalG proteins, to the MalK protein on the other side of the membrane, so that ATP hydrolysis can occur.

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Selected References

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  1. Bargmann C. I., Hung M. C., Weinberg R. A. Multiple independent activations of the neu oncogene by a point mutation altering the transmembrane domain of p185. Cell. 1986 Jun 6;45(5):649–657. doi: 10.1016/0092-8674(86)90779-8. [DOI] [PubMed] [Google Scholar]
  2. Cotecchia S., Exum S., Caron M. G., Lefkowitz R. J. Regions of the alpha 1-adrenergic receptor involved in coupling to phosphatidylinositol hydrolysis and enhanced sensitivity of biological function. Proc Natl Acad Sci U S A. 1990 Apr;87(8):2896–2900. doi: 10.1073/pnas.87.8.2896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dardonville B., Raibaud O. Characterization of malT mutants that constitutively activate the maltose regulon of Escherichia coli. J Bacteriol. 1990 Apr;172(4):1846–1852. doi: 10.1128/jb.172.4.1846-1852.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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 Sep;4(9):2287–2293. doi: 10.1002/j.1460-2075.1985.tb03928.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Davidson A. L., Nikaido H. Overproduction, solubilization, and reconstitution of the maltose transport system from Escherichia coli. J Biol Chem. 1990 Mar 15;265(8):4254–4260. [PubMed] [Google Scholar]
  6. Davidson A. L., Nikaido H. Purification and characterization of the membrane-associated components of the maltose transport system from Escherichia coli. J Biol Chem. 1991 May 15;266(14):8946–8951. [PubMed] [Google Scholar]
  7. Dean D. A., Davidson A. L., Nikaido H. Maltose transport in membrane vesicles of Escherichia coli is linked to ATP hydrolysis. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9134–9138. doi: 10.1073/pnas.86.23.9134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ferenci T., Klotz U. Affinity chromatographic isolation of the periplasmic maltose binding protein of Escherichia coli. FEBS Lett. 1978 Oct 15;94(2):213–217. doi: 10.1016/0014-5793(78)80940-5. [DOI] [PubMed] [Google Scholar]
  9. Froshauer S., Beckwith J. The nucleotide sequence of the gene for malF protein, an inner membrane component of the maltose transport system of Escherichia coli. Repeated DNA sequences are found in the malE-malF intercistronic region. J Biol Chem. 1984 Sep 10;259(17):10896–10903. [PubMed] [Google Scholar]
  10. Hengge R., Boos W. Maltose and lactose transport in Escherichia coli. Examples of two different types of concentrative transport systems. Biochim Biophys Acta. 1983 Aug 11;737(3-4):443–478. doi: 10.1016/0304-4157(83)90009-6. [DOI] [PubMed] [Google Scholar]
  11. Higgins C. F., Hiles I. D., Whalley K., Jamieson D. J. Nucleotide binding by membrane components of bacterial periplasmic binding protein-dependent transport systems. EMBO J. 1985 Apr;4(4):1033–1039. doi: 10.1002/j.1460-2075.1985.tb03735.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hofnung M. Divergent operons and the genetic structure of the maltose B region in Escherichia coli K12. Genetics. 1974 Feb;76(2):169–184. doi: 10.1093/genetics/76.2.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lill R., Cunningham K., Brundage L. A., Ito K., Oliver D., Wickner W. SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli. EMBO J. 1989 Mar;8(3):961–966. doi: 10.1002/j.1460-2075.1989.tb03458.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Miller D. M., 3rd, Newcomer M. E., Quiocho F. A. The thiol group of the L-arabinose-binding protein. Chromophoric labeling and chemical identification of the sugar-binding site. J Biol Chem. 1979 Aug 25;254(16):7521–7528. [PubMed] [Google Scholar]
  15. Mutoh N., Oosawa K., Simon M. I. Characterization of Escherichia coli chemotaxis receptor mutants with null phenotypes. J Bacteriol. 1986 Sep;167(3):992–998. doi: 10.1128/jb.167.3.992-998.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Petronilli V., Ames G. F. Binding protein-independent histidine permease mutants. Uncoupling of ATP hydrolysis from transmembrane signaling. J Biol Chem. 1991 Sep 5;266(25):16293–16296. [PubMed] [Google Scholar]
  17. Quiocho F. A. Atomic structures of periplasmic binding proteins and the high-affinity active transport systems in bacteria. Philos Trans R Soc Lond B Biol Sci. 1990 Jan 30;326(1236):341–352. doi: 10.1098/rstb.1990.0016. [DOI] [PubMed] [Google Scholar]
  18. Reyes M., Shuman H. A. Overproduction of MalK protein prevents expression of the Escherichia coli mal regulon. J Bacteriol. 1988 Oct;170(10):4598–4602. doi: 10.1128/jb.170.10.4598-4602.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shuman H. A. Active transport of maltose in Escherichia coli K12. Role of the periplasmic maltose-binding protein and evidence for a substrate recognition site in the cytoplasmic membrane. J Biol Chem. 1982 May 25;257(10):5455–5461. [PubMed] [Google Scholar]
  20. Shuman H. A., Silhavy T. J., Beckwith J. R. 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 Jan 10;255(1):168–174. [PubMed] [Google Scholar]
  21. Shuman H. A., Silhavy T. J. Identification of the malK gene product. A peripheral membrane component of the Escherichia coli maltose transport system. J Biol Chem. 1981 Jan 25;256(2):560–562. [PubMed] [Google Scholar]
  22. Silhavy T. J., Szmelcman S., Boos W., Schwartz M. On the significance of the retention of ligand by protein. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2120–2124. doi: 10.1073/pnas.72.6.2120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Szmelcman S., Schwartz M., Silhavy T. J., 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 May 17;65(1):13–19. doi: 10.1111/j.1432-1033.1976.tb10383.x. [DOI] [PubMed] [Google Scholar]
  24. Treptow N. A., Shuman H. A. Allele-specific malE mutations that restore interactions between maltose-binding protein and the inner-membrane components of the maltose transport system. J Mol Biol. 1988 Aug 20;202(4):809–822. doi: 10.1016/0022-2836(88)90560-8. [DOI] [PubMed] [Google Scholar]
  25. Treptow N. A., Shuman H. A. Genetic evidence for substrate and periplasmic-binding-protein recognition by the MalF and MalG proteins, cytoplasmic membrane components of the Escherichia coli maltose transport system. J Bacteriol. 1985 Aug;163(2):654–660. doi: 10.1128/jb.163.2.654-660.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ullrich A., Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell. 1990 Apr 20;61(2):203–212. doi: 10.1016/0092-8674(90)90801-k. [DOI] [PubMed] [Google Scholar]

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