Conformational coupling by trans-phosphorylation in calcium calmodulin dependent kinase II

Pandini, Alessandro; Schulman, Howard; Khan, Shahid; de Groot, Bert L.

doi:10.1371/journal.pcbi.1006796

Title: Conformational coupling by trans-phosphorylation in calcium calmodulin dependent kinase II

Journal Article · 31 May 2019 · PLoS Computational Biology (Online)

DOI: https://doi.org/10.1371/journal.pcbi.1006796 · OSTI ID:1627258

^[1];

^[2];

^[3]; de Groot, Bert L. ^[4]

Brunel Univ., Uxbridge (United Kingdom); The Thomas Young Centre for Theory and Simulation of Materials, London (United Kingdom); Francis Crick Inst., London (United Kingdom). Computational Cell and Molecular Biology
Allosteros Therapeutics, Inc., Sunnyvale, CA (United States)
Francis Crick Inst., London (United Kingdom). Computational Cell and Molecular Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biology Consortium
Max Planck Inst. for Biophysical Chemistry (Germany)

The calcium calmodulin-dependent protein kinase II (CaMKII) is a dodecameric holoenzyme important for encoding memory. Its activation, triggered by binding of calcium-calmodulin, persists autonomously after calmodulin dissociation. One (receiver) kinase captures and subsequently phosphorylates the regulatory domain peptide of a donor kinase forming a chained dimer as the first stage of autonomous activation. Protein dynamics simulations examined the conformational changes triggered by dimer formation and phosphorylation, aimed to provide a molecular rationale for human mutations that result in learning disabilities. Ensembles generated from X-ray crystal structures were characterized by network centrality and community analysis. Mutual information related collective motions to local fragment dynamics encoded with a structural alphabet. Implicit solvent tCONCOORD conformational ensembles revealed the dynamic architecture of inactive kinase domains was co-opted in the activated dimer but the network hub shifted from the nucleotide binding cleft to the captured peptide. Explicit solvent molecular dynamics (MD) showed nucleotide and substrate binding determinants formed coupled nodes in long-range signal relays between regulatory peptides in the dimer. Strain in the extended captured peptide was balanced by reduced flexibility of the receiver kinase C-lobe core. The relays were organized around a hydrophobic patch between the captured peptide and a key binding helix. The human mutations aligned along the relays. Thus, these mutations could disrupt the allosteric network alternatively, or in addition, to altered binding affinities. Non-binding protein sectors distant from the binding sites mediated the allosteric signalling; providing possible targets for inhibitor design. Phosphorylation of the peptide modulated the dielectric of its binding pocket to strengthen the patch, non-binding sectors, domain interface and temporal correlations between parallel relays. These results provide the molecular details underlying the reported positive kinase cooperativity to enrich the discussion on how autonomous activation by phosphorylation leads to long-term behavioural effects.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; U.S National Institutes of Health; Royal Society Collaborative Exchange

Grant/Contract Number:: AC02-05CH11231; GM101277; U1175.70592

OSTI ID:: 1627258

Journal Information:: PLoS Computational Biology (Online), Vol. 15, Issue 5; ISSN 1553-7358

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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