Conformational changes of the bacterial type I ATP-binding cassette importer HisQMP2 at distinct steps of the catalytic cycle

Biochim Biophys Acta. 2014 Jan;1838(1 Pt B):106-16. doi: 10.1016/j.bbamem.2013.08.024. Epub 2013 Sep 7.

Abstract

Prokaryotic solute binding protein-dependent ATP-binding cassette import systems are divided into type I and type II and mechanistic differences in the transport process going along with this classification are under intensive investigation. Little is known about the conformational dynamics during the catalytic cycle especially concerning the transmembrane domains. The type I transporter for positively charged amino acids from Salmonella enterica serovar Typhimurium (LAO-HisQMP2) was studied by limited proteolysis in detergent solution in the absence and presence of co-factors including ATP, ADP, LAO/arginine, and Mg(2+) ions. Stable peptide fragments could be obtained and differentially susceptible cleavage sites were determined by mass spectrometry as Lys-258 in the nucleotide-binding subunit, HisP, and Arg-217/Arg-218 in the transmembrane subunit, HisQ. In contrast, transmembrane subunit HisM was gradually degraded but no stable fragment could be detected. HisP and HisQ were equally resistant under pre- and post-hydrolysis conditions in the presence of arginine-loaded solute-binding protein LAO and ATP/ADP. Some protection was also observed with LAO/arginine alone, thus reflecting binding to the transporter in the apo-state and transmembrane signaling. Comparable digestion patterns were obtained with the transporter reconstituted into proteoliposomes and nanodiscs. Fluorescence lifetime spectroscopy confirmed the change of HisQ(R218) to a more apolar microenvironment upon ATP binding and hydrolysis. Limited proteolysis was subsequently used as a tool to study the consequences of mutations on the transport cycle. Together, our data suggest similar conformational changes during the transport cycle as described for the maltose ABC transporter of Escherichia coli, despite distinct structural differences between both systems.

Keywords: (3-(N-morpholino)-propanesulfonic acid); ABC; ABC transporter; ATP-binding cassette; Alternate access model; DBD; DDM; Fluorescence lifetime; His-tag; Histidine transport; IPTG; Limited proteolysis; MOPS; MSP; NBD; OG; PMSF; SBP; TMD; Type I importer; [1,3]dioxolo[4,5-f][1,3]benzodioxole; hexahistidine tag; isopropyl-β-D-thio-galactopyranoside; membrane scaffold protein; n-dodecyl-β-D-maltopyranoside; nucleotide binding domain; octyl-β-D-glucopyranoside; phenylmethylsulfonylfluoride; solute binding protein; transmembrane domain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP-Binding Cassette Transporters / chemistry*
  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism
  • Adenosine Diphosphate / chemistry
  • Adenosine Diphosphate / metabolism
  • Adenosine Triphosphate / chemistry
  • Adenosine Triphosphate / metabolism
  • Amino Acid Sequence
  • Amino Acid Transport Systems, Basic / chemistry*
  • Amino Acid Transport Systems, Basic / genetics
  • Amino Acid Transport Systems, Basic / metabolism
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Biocatalysis
  • Biological Transport, Active
  • Carrier Proteins / chemistry*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cations, Divalent
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Histidine / chemistry*
  • Histidine / metabolism
  • Hydrolysis
  • Magnesium / chemistry
  • Magnesium / metabolism
  • Models, Molecular
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Peptide Fragments / chemistry*
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Protein Conformation
  • Protein Subunits / chemistry*
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • Proteolipids / chemistry
  • Proteolipids / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Salmonella typhimurium / chemistry*
  • Salmonella typhimurium / enzymology
  • Sequence Homology, Amino Acid

Substances

  • ATP-Binding Cassette Transporters
  • Amino Acid Transport Systems, Basic
  • Bacterial Proteins
  • Carrier Proteins
  • Cations, Divalent
  • Peptide Fragments
  • Protein Subunits
  • Proteolipids
  • Recombinant Proteins
  • lysyl-arginyl-ornithine-binding protein, bacteria
  • proteoliposomes
  • Histidine
  • Adenosine Diphosphate
  • histidine permease, Bacteria
  • Adenosine Triphosphate
  • Magnesium