Membrane topology of the melibiose permease of Escherichia coli studied by melB-phoA fusion analysis

Biochemistry. 1996 Apr 2;35(13):4161-8. doi: 10.1021/bi9527496.

Abstract

In order to study the secondary structure of the melibiose permease of Escherichia coli, 57 melB-phoA gene fusions were constructed and assayed for alkaline phosphatase activity. In general agreement with a previously suggested secondary structure model of melibiose permease [Botfield, M. C., Naguchi, K., Tsuchiya, T., & Wilson, T.H. (1992) J. Biol. Chem. 267, 1818], clusters of fusions exhibiting low and high phosphatase activity fusions alternate along the primary sequence. Fusions with high activity generally cluster at residues predicted to be in the periplasmic half of transmembrane domains or in periplasmic loops, while fusions with low activity cluster at residues predicted to be in the cytoplasmic half of transmembrane domains or in cytoplasmic loops. Taken together, the findings strongly support the contention that melibiose permease contains 12 transmembrane domains that traverse the membrane in zigzag fashion connected by hydrophilic loops that are exposed alternatively on the periplasmic or cytoplasmic surfaces of the membrane with the N and C termini on the cytoplasmic face of the membrane. Moreover, on the basis of the finding that the cytoplasmic half of an out-going segment is sufficient for alkaline phosphatase export to the periplasm while the periplasmic half of an in-going segment prevents it [Calamia, T., & Manoil, C. (1990) Proc. Natl. Acad. Sci. U.S.A. 87, 4937], the activity profile of the melibiose permease-alkaline phosphatase fusions is consistent with the predicted topology of seven of 12 transmembrane segments. However, five transmembrane domains require adjustment, and as a consequence, the size of the central cytoplasmic loop is reduced and a significant number of charged residues are shifted from a hydrophilic to a hydrophobic domain in this region of the transporter.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkaline Phosphatase / biosynthesis
  • Alkaline Phosphatase / chemistry
  • Amino Acid Sequence
  • Base Sequence
  • Cell Membrane / enzymology*
  • Cell Membrane / ultrastructure
  • DNA Primers
  • Escherichia coli / enzymology*
  • Escherichia coli / genetics
  • Genes, Bacterial
  • Membrane Transport Proteins / biosynthesis
  • Membrane Transport Proteins / chemistry*
  • Models, Structural
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Plasmids
  • Protein Structure, Secondary*
  • Recombinant Fusion Proteins / biosynthesis
  • Recombinant Fusion Proteins / chemistry
  • Restriction Mapping
  • Symporters*

Substances

  • DNA Primers
  • Membrane Transport Proteins
  • Recombinant Fusion Proteins
  • Symporters
  • melibiose permease
  • Alkaline Phosphatase