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EcoSal Plus

Domain 3:

Metabolism

Binding Protein-Dependent Uptake of Maltose into Cells via an ATP-Binding Cassette Transporter

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  • Authors: Amy L. Davidson1, and Frances Joan D. Alvarez2
  • Editor: Valley Stewart3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Chemistry, Purdue University West Lafayette, IN 47907; 2: Department of Chemistry, Purdue University West Lafayette, IN 47907; 3: University of California, Davis, Davis, CA
  • Received 04 June 2009 Accepted 10 August 2009 Published 14 September 2010
  • Address correspondence to Amy L. Davidson adavidso@purdue.edu
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  • Abstract:

    Maltose and maltodextrins are actively transported across the cytoplasmic membrane of and by a periplasmic binding protein (BP)- dependent transport system. Since 1996, there have been many advances in the understanding of the structure and mechanism of the maltose transporter, in the assembly of the membrane-associated transporter complex, and in the mechanism of regulation of transport both at the DNA and the protein level. The transporter has been studied in detergent and reconstituted in liposome vesicles, and while many features, including the ability of maltose-binding protein (MBP) to stimulate ATPase activity, are retained in detergent, it has been noted that the basal ATPase activity of the transporter is elevated in detergent compared with liposomes. This review focuses on these recent developments, which have culminated in a high resolution structure of MBP in a complex with the MalFGK transporter. While this review focuses on the maltose system, complementary work has been carried out on many different ATP binding cassette (ABC) transporters, all of which has contributed in important ways to the understanding of the maltose transport system. The regulation of the maltose transport system, at the DNA level, is implemented by the synergistic action of MalT and cAMP/CAP complex and, at the protein level, by interactions of MalK with unphosphorylated EIIA, a signal-transducing component of the phosphoenolpyruvate-glucose phosphotransferase system.

  • Citation: Davidson A, Alvarez F. 2010. Binding Protein-Dependent Uptake of Maltose into Cells via an ATP-Binding Cassette Transporter, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.3

Key Concept Ranking

Major Histocompatibility Complex Class I
0.40065184
0.40065184

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/content/journal/ecosalplus/10.1128/ecosalplus.3.3.3
2010-09-14
2017-05-30

Abstract:

Maltose and maltodextrins are actively transported across the cytoplasmic membrane of and by a periplasmic binding protein (BP)- dependent transport system. Since 1996, there have been many advances in the understanding of the structure and mechanism of the maltose transporter, in the assembly of the membrane-associated transporter complex, and in the mechanism of regulation of transport both at the DNA and the protein level. The transporter has been studied in detergent and reconstituted in liposome vesicles, and while many features, including the ability of maltose-binding protein (MBP) to stimulate ATPase activity, are retained in detergent, it has been noted that the basal ATPase activity of the transporter is elevated in detergent compared with liposomes. This review focuses on these recent developments, which have culminated in a high resolution structure of MBP in a complex with the MalFGK transporter. While this review focuses on the maltose system, complementary work has been carried out on many different ATP binding cassette (ABC) transporters, all of which has contributed in important ways to the understanding of the maltose transport system. The regulation of the maltose transport system, at the DNA level, is implemented by the synergistic action of MalT and cAMP/CAP complex and, at the protein level, by interactions of MalK with unphosphorylated EIIA, a signal-transducing component of the phosphoenolpyruvate-glucose phosphotransferase system.

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Figures

Image of Figure 1
Figure 1

Just one of two subunits in the ATP-bound MalK (PDB ID code 1Q12) is shown. The helical subdomain is blue, the nucleotide-binding subdomain is green, and the C-terminal regulatory domain (truncated) is yellow. Conserved residues and motifs discussed in the text are highlighted and labeled in the figure. Two ATPs, which lie along the interface in the actual dimer structure (see Fig. 2 ), are colored according to the scheme developed by Corey, Pauling, and Koltun. This figure was prepared with Pymol.

Citation: Davidson A, Alvarez F. 2010. Binding Protein-Dependent Uptake of Maltose into Cells via an ATP-Binding Cassette Transporter, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.3
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Image of Figure 2
Figure 2

In the absence of nucleotide (ground state, 1Q1B), the nucleotide-binding interface between the two NBDs (different shades of blue and green) of MalK are separated with dimer contacts maintained through contact of the regulatory domains (yellow). In the ATP-bound structure (1Q12), the nucleotide-binding interface is closed. In the ADP-bound structure (2AWO), the interface is again open, suggestive of a cycle of ATP hydrolysis linked to conformational change. Reprinted from reference 54 , with permission of the publisher. Copyright 2005 National Academy of Sciences, USA.

Citation: Davidson A, Alvarez F. 2010. Binding Protein-Dependent Uptake of Maltose into Cells via an ATP-Binding Cassette Transporter, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.3
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Image of Figure 3
Figure 3

In the absence of maltose, the transporter rests in a conformation in which the nucleotide-binding interface is open and the sugar-binding site in the membrane is exposed to the cytoplasm, even in the presence of ATP. When maltose binds MBP, it closes, and the closed form of MBP initiates a cycle of transport. In a concerted motion, MBP opens as it becomes more tightly bound by the transporter, and the nucleotide-binding interface closes as TM helices reorient to alternate exposure of the sugar-binding site from the cytoplasm to the periplasm to receive maltose as it is released from MBP. ATP hydrolysis occurs in this conformation, and following hydrolysis, the nucleotide-binding interface becomes unstable, returning the transporter to a resting state. Adapted from reference 61 , with permission of the publisher. Copyright 2001 National Academy of Sciences, USA.

Citation: Davidson A, Alvarez F. 2010. Binding Protein-Dependent Uptake of Maltose into Cells via an ATP-Binding Cassette Transporter, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.3
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Image of Figure 4
Figure 4

In the structure (2R6G), MBP is trapped in complex with ATP-bound MalFGK by use of an E159Q substitution in MalK to prevent ATP hydrolysis. Subunits are colored as indicated in the figure. On the right, a space-filling model is cut away to reveal an outward-facing occluded pocket containing bound maltose. Modified from reference 51 .

Citation: Davidson A, Alvarez F. 2010. Binding Protein-Dependent Uptake of Maltose into Cells via an ATP-Binding Cassette Transporter, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.3
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Image of Figure 5
Figure 5

In the structure (3FH6), MalF lacking the first two TM helices was used for crystallization. Subunits are colored as indicated. On the right, a space-filling model is cut away to reveal an inward-facing empty maltose binding pocket. Reprinted from reference 113 , with permission.

Citation: Davidson A, Alvarez F. 2010. Binding Protein-Dependent Uptake of Maltose into Cells via an ATP-Binding Cassette Transporter, EcoSal Plus 2010; doi:10.1128/ecosalplus.3.3.3
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