The fourth transmembrane segment of the Na,K-ATPase alpha subunit: a systematic mutagenesis study

J Biol Chem. 2004 Jul 9;279(28):29542-50. doi: 10.1074/jbc.M400585200. Epub 2004 Apr 28.

Abstract

The Na,K-ATPase is a major ion-motive ATPase of the P-type family responsible for many aspects of cellular homeostasis. To determine the structure of the pathway for cations across the transmembrane portion of the Na,K-ATPase, we mutated 24 residues of the fourth transmembrane segment into cysteine and studied their function and accessibility by exposure to the sulfhydryl reagent 2-aminoethyl-methanethiosulfonate. Accessibility was also examined after treatment with palytoxin, which transforms the Na,K-pump into a cation channel. Of the 24 tested cysteine mutants, seven had no or a much reduced transport function. In particular cysteine mutants of the highly conserved "PEG" motif had a strongly reduced activity. However, most of the non-functional mutants could still be transformed by palytoxin as well as all of the functional mutants. Accessibility, determined as a 2-aminoethyl-methanethiosulfonate-induced reduction of the transport activity or as inhibition of the membrane conductance after palytoxin treatment, was observed for the following positions: Phe(323), Ile(322), Gly(326), Ala(330), Pro(333), Glu(334), and Gly(335). In accordance with a structural model of the Na,K-ATPase obtained by homology modeling with the two published structures of sarcoplasmic and endoplasmic reticulum calcium ATPase (Protein Data Bank codes 1EUL and 1IWO), the results suggest the presence of a cation pathway along the side of the fourth transmembrane segment that faces the space between transmembrane segments 5 and 6. The phenylalanine residue in position 323 has a critical position at the outer mouth of the cation pathway. The residues thought to form the cation binding site II ((333)PEGL) are also part of the accessible wall of the cation pathway opened by palytoxin through the Na,K-pump.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acrylamides / metabolism
  • Amino Acid Sequence
  • Animals
  • Bufo marinus
  • Cnidarian Venoms
  • Cysteine / metabolism
  • Ethyl Methanesulfonate / analogs & derivatives*
  • Ethyl Methanesulfonate / metabolism
  • Female
  • Membrane Potentials / physiology
  • Models, Molecular
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Oocytes / physiology
  • Patch-Clamp Techniques
  • Protein Structure, Secondary*
  • Protein Subunits / chemistry*
  • Protein Subunits / genetics*
  • Protein Subunits / metabolism
  • Sequence Alignment
  • Sodium-Potassium-Exchanging ATPase / chemistry*
  • Sodium-Potassium-Exchanging ATPase / genetics*
  • Sodium-Potassium-Exchanging ATPase / metabolism
  • Sulfhydryl Reagents / metabolism
  • Xenopus laevis

Substances

  • Acrylamides
  • Cnidarian Venoms
  • Protein Subunits
  • Sulfhydryl Reagents
  • methanethiosulfonate ethylammonium
  • Ethyl Methanesulfonate
  • Sodium-Potassium-Exchanging ATPase
  • Cysteine
  • palytoxin