Characterizing KRAS Membrane Structures by Data-Driven Molecular Docking

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Stanley, Christopher B., Que N. Van, Frank Heinrich, Mathias Losche, Debsindhu Bhowmik, Arvind Ramanathan, Cesar A. Lopez, Sandrasegaram Gnanakaran, Dwight V. Nissley, and Andrew G. Stephen. "Characterizing KRAS Membrane Structures by Data-Driven Molecular Docking." Biophysical Journal 120, no. 3 (2021): 25a.

Computational Sciences and Engineering Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA, 2 NCI RAS Initiative, Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Frederick, MD, USA, 3 Department of Physics, Carnegie Mellon University, Pittsburgh, PA, USA, 4 Center for Neutron Research, National Institute of Standards and Technology, Gaithersburg, MD, USA, 5 Data Science, Argonne National Laboratory, Lemont, IL, USA, 6 Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM, USA. KRAS is a GTPase that plays an important role in cell growth and signaling pathways. of the different RAS isoforms, KRAS also has the highest prevalence of mutations related to human cancers, making it an attractive therapeutic target in these cases. Once attached to the membrane, KRAS in the active (GTP) form is capable to bind effector proteins, like RAF kinase. However, certain molecular details concerning KRAS conformation and orientational changes when interacting with the membrane and binding partners are not fully understood. To provide new insights, we used a variety of biophysical approaches to characterize KRAS structure and dynamics. Here, we focus on our results utilizing data-driven computational docking to investigate both KRAS and KRAS/ RAF1-RBD (RAS Binding Domain) complex at the membrane. with the HADDOCK program, we incorporated experimental restraints derived from our NMR paramagnetic relaxation enhancement (PRE) and neutron reflectivity (NR) measurements to dock these KRAS forms to a 70:30 POPC:POPS lipid membrane surface. Using NMR-PRE restraints alone, we performed one series of docking runs with the KRAS G-domain directly interacting with the membrane to discern membrane-proximal states. Based on our experimental evidence, and particularly from NR, a highly populated membrane-distal state also exists, where the G-domain does not directly contact the membrane but KRAS remains tethered via the C-terminal hypervariable region (HVR). Therefore, we also conducted a second series of docking runs that incorporated both NMR-PRE and NR restraints to better elucidate the conformations in this state. From these results, we were able to generate atomistic models for KRAS and KRAS/RAF1-RBD with averaged 1-D profiles closely matching the respective NR profiles. Overall, the findings should assist in elucidating the role of KRAS structural dynamics in recruiting effectors, like RAF kinase, to the membrane for activation.

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