Machine Learning and Structural Dynamics-Based Approach to Reveal Molecular Mechanism of PTEN Missense Mutations Shared by Cancer and Autism Spectrum Disorder.

Journal: Journal of chemical information and modeling
PMID:

Abstract

Missense mutations in oncogenic proteins that are concurrently associated with neurodevelopmental disorders have garnered significant attention. Phosphatase and tensin homologue (PTEN) serves as a paradigmatic model for mapping its mutational landscape and identifying genotypic predictors of distinct phenotypic outcomes, including cancer and autism spectrum disorder (ASD). Despite extensive research into the genotype-phenotype correlations of PTEN mutations, the mechanisms underlying the dual association of specific PTEN mutations with both cancer and ASD (PTEN-cancer/ASD mutations) remain elusive. This study introduces an integrative approach that combines machine learning (ML) with structural dynamics to elucidate the molecular effects of PTEN-cancer/ASD mutations. Analysis of biophysical and network-biology-based signatures reveals a complex energetic and functional landscape. Subsequently, an ML model and corresponding integrated score were developed to classify and predict PTEN-cancer/ASD mutations, underscoring the significance of protein dynamics in predicting cellular phenotypes. Further molecular dynamics simulations demonstrated that PTEN-cancer/ASD mutations induce dynamic alterations characterized by open conformational changes restricted to the P loop and coupled with interdomain allosteric regulation. This research aims to enhance the genotypic and phenotypic understanding of PTEN-cancer/ASD mutations through an interpretable ML model integrated with structural dynamics analysis. By identifying shared mechanisms between cancer and ASD, the findings pave the way for the development of novel therapeutic strategies.

Authors

  • Miao Yang
    MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Key Laboratory of Pathogen Bioscience and Anti-infective Medicine, Department of Bioinformatics and Computational Biology, School of Life Sciences, Suzhou Medical College of Soochow University, Suzhou 215123, China.
  • Jingran Wang
    MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Key Laboratory of Pathogen Bioscience and Anti-infective Medicine, Department of Bioinformatics and Computational Biology, School of Life Sciences, Suzhou Medical College of Soochow University, Suzhou 215123, China.
  • Ziyun Zhou
    MOE Key Laboratory of Geriatric Diseases and Immunology, Suzhou Key Laboratory of Pathogen Bioscience and Anti-infective Medicine, Department of Bioinformatics and Computational Biology, School of Life Sciences, Suzhou Medical College of Soochow University, Suzhou 215123, China.
  • Wentian Li
    Wuhan Hospital for Psychotherapy, Tongji Medical College of Huazhong University of Science and Technology, Wuhan, China.
  • Gennady Verkhivker
    Keck Center for Science and Engineering, Graduate Program in Computational and Data Sciences, Schmid College of Science and Technology, Chapman University, Orange, CA 92866, USA.
  • Fei Xiao
    Peking University Fifth School of Clinical Medicine, Beijing, China.
  • Guang Hu
    Epigenetics & Stem Cell Biology Laboratory, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, Durham, North Carolina, United States of America.