Different inhibition of Gβγ-stimulated class IB phosphoinositide 3-kinase (PI3K) variants by a monoclonal antibody. Specific function of p101 as a Gβγ-dependent regulator of PI3Kγ enzymatic activity

Biochem J. 2015 Jul 1;469(1):59-69. doi: 10.1042/BJ20150099.

Abstract

Class IB phosphoinositide 3-kinases γ (PI3Kγ) are second-messenger-generating enzymes downstream of signalling cascades triggered by G-protein-coupled receptors (GPCRs). PI3Kγ variants have one catalytic p110γ subunit that can form two different heterodimers by binding to one of a pair of non-catalytic subunits, p87 or p101. Growing experimental data argue for a different regulation of p87-p110γ and p101-p110γ allowing integration into distinct signalling pathways. Pharmacological tools enabling distinct modulation of the two variants are missing. The ability of an anti-p110γ monoclonal antibody [mAb(A)p110γ] to block PI3Kγ enzymatic activity attracted us to characterize this tool in detail using purified proteins. In order to get insight into the antibody-p110γ interface, hydrogen-deuterium exchange coupled to MS (HDX-MS) measurements were performed demonstrating binding of the monoclonal antibody to the C2 domain in p110γ, which was accompanied by conformational changes in the helical domain harbouring the Gβγ-binding site. We then studied the modulation of phospholipid vesicles association of PI3Kγ by the antibody. p87-p110γ showed a significantly reduced Gβγ-mediated phospholipid recruitment as compared with p101-p110γ. Concomitantly, in the presence of mAb(A)p110γ, Gβγ did not bind to p87-p110γ. These data correlated with the ability of the antibody to block Gβγ-stimulated lipid kinase activity of p87-p110γ 30-fold more potently than p101-p110γ. Our data argue for differential regulatory functions of the non-catalytic subunits and a specific Gβγ-dependent regulation of p101 in PI3Kγ activation. In this scenario, we consider the antibody as a valuable tool to dissect the distinct roles of the two PI3Kγ variants downstream of GPCRs.

Keywords: G-protein; Gβγ; p101; p87; phosphoinositide 3-kinase γ (PI3Kγ); signal transduction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal, Murine-Derived / chemistry*
  • Class Ib Phosphatidylinositol 3-Kinase* / chemistry
  • Class Ib Phosphatidylinositol 3-Kinase* / genetics
  • Class Ib Phosphatidylinositol 3-Kinase* / metabolism
  • Deuterium Exchange Measurement
  • GTP-Binding Protein beta Subunits* / chemistry
  • GTP-Binding Protein beta Subunits* / genetics
  • GTP-Binding Protein beta Subunits* / metabolism
  • GTP-Binding Protein gamma Subunits* / chemistry
  • GTP-Binding Protein gamma Subunits* / genetics
  • GTP-Binding Protein gamma Subunits* / metabolism
  • HEK293 Cells
  • Humans
  • Sf9 Cells
  • Spodoptera

Substances

  • Antibodies, Monoclonal, Murine-Derived
  • GTP-Binding Protein beta Subunits
  • GTP-Binding Protein gamma Subunits
  • Class Ib Phosphatidylinositol 3-Kinase