Molecular mechanism of activation-triggered subunit exchange in Ca 2+ /calmodulin-dependent protein kinase II

Bhattacharyya, Moitrayee; Stratton, Margaret M.; Going, Catherine C.; McSpadden, Ethan D.; Huang, Yongjian; Susa, Anna C.; Elleman, Anna; Cao, Yumeng Melody; Pappireddi, Nishant; Burkhardt, Pawel; Gee, Christine L.; Barros, Tiago; Schulman, Howard; Williams, Evan R.; Kuriyan, John

doi:10.7554/eLife.13405

Molecular mechanism of activation-triggered subunit exchange in Ca ²⁺ /calmodulin-dependent protein kinase II

Journal Article · Mon Mar 07 00:00:00 EST 2016 · eLife

DOI:https://doi.org/10.7554/eLife.13405· OSTI ID:1379139

Bhattacharyya, Moitrayee ^[1]; Stratton, Margaret M. ^[1]; Going, Catherine C. ^[2]; McSpadden, Ethan D. ^[1]; Huang, Yongjian ^[3]; Susa, Anna C. ^[2]; Elleman, Anna ^[1]; Cao, Yumeng Melody ^[1]; Pappireddi, Nishant ^[1]; Burkhardt, Pawel ^[4]; ^[1]; ^[1]; Schulman, Howard ^[5]; Williams, Evan R. ^[2]; ^[6]

Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology, California Inst. for Quantitative Biosciences, Howard Hughes Medical Inst.
Univ. of California, Berkeley, CA (United States). Dept. of Chemistry
Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology, California Inst. for Quantitative Biosciences, Howard Hughes Medical Inst., Biophysics Graduate Group
Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology, Howard Hughes Medical Inst.
Allosteros Therapeutics, Sunnyvale, CA (United States)
Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology, California Inst. for Quantitative Biosciences, Howard Hughes Medical Inst., Biophysics Graduate Group; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division

Activation triggers the exchange of subunits in Ca²⁺/calmodulin-dependent protein kinase II (CaMKII), an oligomeric enzyme that is critical for learning, memory, and cardiac function. The mechanism by which subunit exchange occurs remains elusive. We show that the human CaMKII holoenzyme exists in dodecameric and tetradecameric forms, and that the calmodulin (CaM)-binding element of CaMKII can bind to the hub of the holoenzyme and destabilize it to release dimers. The structures of CaMKII from two distantly diverged organisms suggest that the CaM-binding element of activated CaMKII acts as a wedge by docking at intersubunit interfaces in the hub. This converts the hub into a spiral form that can release or gain CaMKII dimers. Our data reveal a three-way competition for the CaM-binding element, whereby phosphorylation biases it towards the hub interface, away from the kinase domain and calmodulin, thus unlocking the ability of activated CaMKII holoenzymes to exchange dimers with unactivated ones.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1379139

Journal Information:: eLife, Journal Name: eLife Journal Issue: MARCH2016 Vol. 5; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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Variation in assembly stoichiometry in non‐metazoan homologs of the hub domain of Ca ²⁺ /calmodulin‐dependent protein kinase II McSpadden, Ethan D.; Xia, Zijie; Chi, Chris C. Protein Science, Vol. 28, Issue 6 https://doi.org/10.1002/pro.3614	journal	April 2019
The CaMKII holoenzyme structure in activation-competent conformations Myers, Janette B.; Zaegel, Vincent; Coultrap, Steven J. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15742	journal	June 2017
Structure and assembly of calcium homeostasis modulator proteins Syrjanen, Johanna L.; Michalski, Kevin; Chou, Tsung-Han Nature Structural & Molecular Biology, Vol. 27, Issue 2 https://doi.org/10.1038/s41594-019-0369-9	journal	January 2020
From molecular chaperones to membrane motors: through the lens of a mass spectrometrist Robinson, Carol V. Biochemical Society Transactions, Vol. 45, Issue 1 https://doi.org/10.1042/bst20160395	journal	February 2017
FRET-based sensor for CaMKII activity (FRESCA): A useful tool for assessing CaMKII activity in response to Ca ²⁺ oscillations in live cells Ardestani, Goli; West, Megan C.; Maresca, Thomas J. Journal of Biological Chemistry, Vol. 294, Issue 31 https://doi.org/10.1074/jbc.ra119.009235	journal	June 2019
Mechanics of CaMKII-actin networks Khan, Shahid; Downing, Kenneth H.; Molloy, Justin E. BioRxiv https://doi.org/10.1101/308353	posted_content	May 2018
Evolution of protein kinase substrate recognition at the active site Bradley, David; Beltrao, Pedro https://doi.org/10.1101/443945	posted_content	October 2018
Heterogeneity in human hippocampal CaMKII transcripts reveals allosteric hub-dependent regulation Sloutsky, Roman; Dziedzic, Noelle; Dunn, Matthew J. Science Signaling, Vol. 13, Issue 641 https://doi.org/10.1126/scisignal.aaz0240	journal	July 2020
Evolution of protein kinase substrate recognition at the active site Bradley, David; Beltrao, Pedro PLOS Biology, Vol. 17, Issue 6 https://doi.org/10.1371/journal.pbio.3000341	journal	June 2019
A multi-state model of the CaMKII dodecamer suggests a role for calmodulin in maintenance of autophosphorylation Pharris, Matthew C.; Patel, Neal M.; VanDyk, Tyler G. PLOS Computational Biology, Vol. 15, Issue 12 https://doi.org/10.1371/journal.pcbi.1006941	journal	December 2019
Adaptation of Plants to Salt Stress: Characterization of Na+ and K+ Transporters and Role of CBL Gene Family in Regulating Salt Stress Response Ketehouli, Toi; Idrice Carther, Kue Foka; Noman, Muhammad Agronomy, Vol. 9, Issue 11 https://doi.org/10.3390/agronomy9110687	journal	October 2019
Subunit exchange enhances information retention by CaMKII in dendritic spines Singh, Dilawar; Bhalla, Upinder Singh eLife, Vol. 7 https://doi.org/10.7554/eLife.41412	journal	November 2018
A homozygous loss-of-function CAMK2A mutation causes growth delay, frequent seizures and severe intellectual disability Chia, Poh Hui; Zhong, Franklin Lei; Niwa, Shinsuke eLife, Vol. 7 https://doi.org/10.7554/elife.32451	journal	May 2018

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