Oral Presentation The 46th Lorne Conference on Protein Structure and Function 2021

Negative regulation of RAF kinase activity by ATP is overcome by 14-3-3-induced dimerization. (#21)

Nicholas PD Liau 1 , Timothy J Wendorff 1 , John G Quinn 1 , Micah Steffek 1 , Wilson Phung 1 , Peter Liu 1 , Jia Tang 1 , Flaviyan J Irudayanathan 1 , Saeed Izadi 1 , Andrey S Shaw 1 , Shiva Malek 1 , Sarah G Hymowitz 1 , Jawahar Sudhamsu 1
  1. Genentech Inc., South San Francisco, CA, United States

BRAF is a protein kinase that drives cell proliferation through a phosphorylation cascade of downstream kinases MEK and ERK. Because it is one of the most mutated proteins in human cancers, BRAF is an important target of research for cancer therapies.

Dimerization is known to be crucial for the upregulation of BRAF catalytic activity. We have solved an X-ray crystal structure of a BRAF-MEK1 in complex with the ATP analog AMP-PCP (ACP), which surprisingly reveals a monomeric form of BRAF in a catalytically inactive state. This conformation of BRAF is incompatible with dimerization due to a twisting of the N lobe of the kinase domain with respect to its C lobe. We have performed biochemical experiments showing ACP is able to break wild type RAF dimers in solution, though is unable to break dimers of oncogenic RAF mutants. This reveals a novel molecular mechanism through which wild type BRAF remains inactive under resting conditions, but oncogenic mutants escape such inactivation.

We have also determined how the RAFs overcome the negative regulatory effect of cellular ATP when signaling is required. The 14-3-3 proteins are constitutive dimers that are known to be necessary for activation through the interaction with a phosphorylated C terminal motif on BRAF, though the molecular mechanism for such activation was unknown until recently. We have solved an X-ray crystal structure of a BRAF-BRAF homodimer in the active conformation, bound to a 14-3-3 dimer. We have also performed biochemical experiments showing that BRAF kinase activity is greatly upregulated by 14-3-3 binding, whilst ATP is unable to break a BRAF dimer when 14-3-3 is bound to its C terminus. These data show that 14-3-3 binding is able to overcome the negative regulatory effect of ATP, which at cellular concentrations would otherwise downregulate wild type BRAF activity.

  1. Liau NPD*, Wendorff TJ*, Quinn JG, Steffek M, Phung W, Liu P, Tang J, Irudayanathan FJ, Izadi S, Shaw AS, Malek S, Hymowitz SG, Sudhamsu J. Negative regulation of RAF kinase activity by ATP is overcome by 14-3-3-induced dimerization. Nat Struct Mol Biol. 2020 Feb;27(2):134-141. *Co-first authors.
  2. Liau NPD, Venkatanarayan A, Quinn JG, Phung W, Malek S, Hymowitz SG, Sudhamsu J. Dimerization Induced by C-Terminal 14-3-3 Binding Is Sufficient for BRAF Kinase Activation. Biochemistry. 2020 Oct 2. (Online ahead of print)