Engineered kinase activation reveals unique morphodynamic phenotypes and associated trafficking for Src family isoforms

Proc Natl Acad Sci U S A. 2014 Aug 26;111(34):12420-5. doi: 10.1073/pnas.1404487111. Epub 2014 Aug 12.

Abstract

The Src kinase family comprises nine homologous members whose distinct expression patterns and cellular distributions indicate that they have unique roles. These roles have not been determined because genetic manipulation has not produced clearly distinct phenotypes, and the kinases' homology complicates generation of specific inhibitors. Through insertion of a modified FK506 binding protein (insertable FKBP12, iFKBP) into the protein kinase isoforms Fyn, Src, Lyn, and Yes, we engineered kinase analogs that can be activated within minutes in living cells (RapR analogs). Combining our RapR analogs with computational tools for quantifying and characterizing cellular dynamics, we demonstrate that Src family isoforms produce very different phenotypes, encompassing cell spreading, polarized motility, and production of long, thin cell extensions. Activation of Src and Fyn led to patterns of kinase translocation that correlated with morphological changes in temporally distinct stages. Phenotypes were dependent on N-terminal acylation, not on Src homology 3 (SH3) and Src homology 2 (SH2) domains, and correlated with movement between a perinuclear compartment, adhesions, and the plasma membrane.

Keywords: image analysis; live cell imaging; motion classification; protein engineering; rapamycin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acylation
  • Amino Acid Sequence
  • Amino Acid Substitution
  • Animals
  • Biophysical Phenomena
  • COS Cells
  • Chlorocebus aethiops
  • Enzyme Activation
  • Isoenzymes / chemistry
  • Isoenzymes / genetics
  • Isoenzymes / metabolism
  • Models, Molecular
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Phenotype
  • Protein Engineering
  • Proto-Oncogene Proteins c-fyn / chemistry
  • Proto-Oncogene Proteins c-fyn / genetics
  • Proto-Oncogene Proteins c-fyn / metabolism
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Sequence Homology, Amino Acid
  • Tacrolimus Binding Protein 1A / chemistry
  • Tacrolimus Binding Protein 1A / genetics
  • Tacrolimus Binding Protein 1A / metabolism
  • src Homology Domains
  • src-Family Kinases / chemistry*
  • src-Family Kinases / genetics
  • src-Family Kinases / metabolism*

Substances

  • Isoenzymes
  • Recombinant Fusion Proteins
  • Proto-Oncogene Proteins c-fyn
  • src-Family Kinases
  • Tacrolimus Binding Protein 1A