Allosteric modulation of a human protein kinase with monobodies

Proc Natl Acad Sci U S A. 2019 Jul 9;116(28):13937-13942. doi: 10.1073/pnas.1906024116. Epub 2019 Jun 25.

Abstract

Despite being the subject of intense effort and scrutiny, kinases have proven to be consistently challenging targets in inhibitor drug design. A key obstacle has been promiscuity and consequent adverse effects of drugs targeting the ATP binding site. Here we introduce an approach to controlling kinase activity by using monobodies that bind to the highly specific regulatory allosteric pocket of the oncoprotein Aurora A (AurA) kinase, thereby offering the potential for more specific kinase modulators. Strikingly, we identify a series of highly specific monobodies acting either as strong kinase inhibitors or activators via differential recognition of structural motifs in the allosteric pocket. X-ray crystal structures comparing AurA bound to activating vs inhibiting monobodies reveal the atomistic mechanism underlying allosteric modulation. The results reveal 3 major advantages of targeting allosteric vs orthosteric sites: extreme selectivity, ability to inhibit as well as activate, and avoidance of competing with ATP that is present at high concentrations in the cells. We envision that exploiting allosteric networks for inhibition or activation will provide a general, powerful pathway toward rational drug design.

Keywords: Aurora A; allosteric drugs; allostery; kinase; monobody.

Publication types

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

MeSH terms

  • Adenosine Triphosphate / chemistry
  • Adenosine Triphosphate / metabolism
  • Allosteric Regulation / genetics
  • Aurora Kinase A / antagonists & inhibitors
  • Aurora Kinase A / chemistry*
  • Aurora Kinase A / genetics
  • Aurora Kinase B / antagonists & inhibitors
  • Aurora Kinase B / chemistry*
  • Aurora Kinase B / genetics
  • Binding Sites / genetics
  • Carrier Proteins / chemistry
  • Carrier Proteins / genetics
  • Crystallography, X-Ray
  • Drug Design
  • Fibronectin Type III Domain / genetics
  • Humans
  • Protein Conformation
  • Protein Kinase Inhibitors / chemistry*
  • Protein Kinases / chemistry*
  • Protein Kinases / genetics

Substances

  • Carrier Proteins
  • Protein Kinase Inhibitors
  • Adenosine Triphosphate
  • Protein Kinases
  • AURKA protein, human
  • AURKB protein, human
  • Aurora Kinase A
  • Aurora Kinase B

Associated data

  • PDB/5G15
  • PDB/6C83