Critical hydrophobic interactions between phosphorylation and actuator domains of Ca2+-ATPase for hydrolysis of phosphorylated intermediate

J Biol Chem. 2005 Jul 15;280(28):26508-16. doi: 10.1074/jbc.M503789200. Epub 2005 May 17.

Abstract

Functional roles of seven hydrophobic residues on the interface between the actuator (A) and phosphorylation (P) domains of sarcoplasmic reticulum Ca2+-ATPase were explored by alanine and serine substitutions. The residues examined were Ile179/Leu180/Ile232 on the A domain, Val705/Val726 on the P domain, and Leu119/Tyr122 on the loop linking the A domain and M2 (the second transmembrane helix). These residues gather to form a hydrophobic cluster around Tyr122 in the crystal structures of Ca2+-ATPase in Ca2+-unbound E2 (unphosphorylated) and E2P (phosphorylated) states but are far apart in those of Ca2+-bound E1 (unphosphorylated) and E1P (phosphorylated) states. The substitution-effects were also compared with those of Ile235 on the A domain/M3 linker and those of T181GE of the A domain, since they are in the immediate vicinity of the Tyr122-cluster. All these substitutions almost completely inhibited ATPase activity without inhibiting Ca2+-activated E1P formation from ATP. Substitutions of Ile235 and T181GE blocked the E1P to E2P transition, whereas those in the Tyr122-cluster blocked the subsequent E2P hydrolysis. Substitutions of Ile235 and Glu183 also blocked EP hydrolysis. Results indicate that the Tyr122-cluster is formed during the E1P to E2P transition to configure the catalytic site and position Glu183 properly for hydrolyzing the acylphosphate. Ile235 on the A domain/M3 linker likely forms hydrophobic interactions with the A domain and thereby allowing the strain of this linker to be utilized for large motions of the A domain during these processes. The Tyr122-cluster, Ile235, and T181GE thus seem to have different roles and are critical in the successive events in processing phosphorylated intermediates to transport Ca2+.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / chemistry
  • Adenosine Triphosphate / chemistry
  • Alanine / chemistry
  • Animals
  • Calcium / chemistry
  • Calcium / metabolism
  • Calcium-Transporting ATPases / chemistry*
  • Calcium-Transporting ATPases / metabolism
  • Catalytic Domain
  • Crystallography, X-Ray
  • Hydrolysis
  • Isoleucine / chemistry
  • Kinetics
  • Leucine / chemistry
  • Models, Chemical
  • Models, Molecular
  • Mutagenesis, Site-Directed
  • Phosphates / chemistry
  • Phosphorylation
  • Potassium / chemistry
  • Protein Binding
  • Protein Conformation
  • Protein Structure, Tertiary
  • Rabbits
  • Sarcoplasmic Reticulum / metabolism
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Serine / chemistry
  • Temperature
  • Time Factors
  • Tyrosine / chemistry

Substances

  • Phosphates
  • Isoleucine
  • Tyrosine
  • Serine
  • Adenosine Triphosphate
  • Adenosine Triphosphatases
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Calcium-Transporting ATPases
  • Leucine
  • Alanine
  • Potassium
  • Calcium