Active Learning-Guided Hit Optimization for the Leucine-Rich Repeat Kinase 2 WDR Domain Based on In Silico Ligand-Binding Affinities.

Journal: Journal of chemical information and modeling
Published Date:

Abstract

The leucine-rich repeat kinase 2 (LRRK2) is the most mutated gene in familial Parkinson's disease, and its mutations lead to pathogenic hallmarks of the disease. The LRRK2 WDR domain is an understudied drug target for Parkinson's disease, with no known inhibitors prior to the first phase of the Critical Assessment of Computational Hit-Finding Experiments (CACHE) Challenge. A unique advantage of the CACHE Challenge is that the predicted molecules are experimentally validated in-house. Here, we report the design and experimental confirmation of LRRK2 WDR inhibitor molecules. We used an active learning (AL) machine learning (ML) workflow based on optimized free-energy molecular dynamics (MD) simulations utilizing the thermodynamic integration (TI) framework to expand a chemical series around two of our previously confirmed hit molecules. We identified 8 experimentally verified novel inhibitors out of 35 experimentally tested (23% hit rate). These results demonstrate the efficacy of our free-energy-based active learning workflow to explore large chemical spaces quickly and efficiently while minimizing the number and length of expensive simulations. This workflow is widely applicable to screening any chemical space for small-molecule analogs with increased affinity, subject to the general constraints of RBFE calculations. The mean absolute error of the TI MD calculations was 2.69 kcal/mol, with respect to the measured of hit compounds.

Authors

  • Filipp Gusev
    Department of Chemistry, Mellon College of Science, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, United States.
  • Evgeny Gutkin
    Department of Chemistry, Mellon College of Science, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, United States.
  • Francesco Gentile
    Vancouver Prostate Centre, Department of Urologic Sciences, The University of British Columbia, Vancouver, BC V6H 3Z6, Canada.
  • Fuqiang Ban
    Vancouver Prostate Centre, Department of Urologic Sciences , Faculty of Medicine, University of British Columbia , 2660 Oak Street , Vancouver , British Columbia V6H 3Z6 , Canada.
  • S Benjamin Koby
    Department of Chemistry, Mellon College of Science, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, United States.
  • Fengling Li
    Department of Pathology, West China Hospital, Sichuan University, Chengdu, 610041, China.
  • Irene Chau
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Suzanne Ackloo
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Cheryl H Arrowsmith
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Albina Bolotokova
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Pegah Ghiabi
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Elisa Gibson
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Levon Halabelian
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Scott Houliston
    Princess Margaret Cancer Centre, University Health Network, Toronto, Ontario M5G 2M9, Canada.
  • Rachel J Harding
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Ashley Hutchinson
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Peter Loppnau
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Sumera Perveen
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Almagul Seitova
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Hong Zeng
    School of Computer Science and Technology, Hangzhou Dianzi University, China.
  • Matthieu Schapira
    Structural Genomics Consortium, University of Toronto, Toronto, Ontario M5G 1L7, Canada.
  • Artem Cherkasov
    Vancouver Prostate Centre, Department of Urologic Sciences , Faculty of Medicine, University of British Columbia , 2660 Oak Street , Vancouver , British Columbia V6H 3Z6 , Canada.
  • Olexandr Isayev
    Department of Chemistry, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, United States.
  • Maria G Kurnikova
    Department of Chemistry, Mellon College of Science, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, United States.