Activation-triggered subunit exchange between CaMKII holoenzymes facilitates the spread of kinase activity

Stratton, Margaret; Lee, Il-Hyung; Bhattacharyya, Moitrayee; Christensen, Sune M.; Chao, Luke H.; Schulman, Howard; Groves, Jay T.; Kuriyan, John

doi:10.7554/elife.01610

Activation-triggered subunit exchange between CaMKII holoenzymes facilitates the spread of kinase activity

Journal Article · Tue Jan 28 00:00:00 EST 2014 · eLife

DOI:https://doi.org/10.7554/elife.01610· OSTI ID:1628804

Stratton, Margaret ^[1]; Lee, Il-Hyung ^[2]; Bhattacharyya, Moitrayee ^[3]; Christensen, Sune M. ^[2]; Chao, Luke H. ^[3]; Schulman, Howard ^[4]; Groves, Jay T. ^[5]; Kuriyan, John ^[6]

Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences, (QB3); Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.; DOE/OSTI
Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences, (QB3); Univ. of California, Berkeley, CA (United States). 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; Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences, (QB3); Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.
Allosteros Therapeutics, Sunnyvale, CA (United States)
Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences, (QB3); Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Materials Sciences Division; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division
Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences, (QB3); Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.; Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division

The activation of the dodecameric Ca²⁺/calmodulin dependent kinase II (CaMKII) holoenzyme is critical for memory formation. We now report that CaMKII has a remarkable property, which is that activation of the holoenzyme triggers the exchange of subunits between holoenzymes, including unactivated ones, enabling the calcium-independent phosphorylation of new subunits. We show, using a single-molecule TIRF microscopy technique, that the exchange process is triggered by the activation of CaMKII, and that exchange is modulated by phosphorylation of two residues in the calmodulin-binding segment, Thr 305 and Thr 306. Based on these results, and on the analysis of molecular dynamics simulations, we suggest that the phosphorylated regulatory segment of CaMKII interacts with the central hub of the holoenzyme and weakens its integrity, thereby promoting exchange. Our results have implications for an earlier idea that subunit exchange in CaMKII may have relevance for information storage resulting from brief coincident stimuli during neuronal signaling.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1628804

Journal Information:: eLife, Journal Name: eLife Vol. 3; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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Conformational coupling by trans-phosphorylation in calcium calmodulin dependent kinase II Pandini, Alessandro; Schulman, Howard; Khan, Shahid The Francis Crick Institute https://doi.org/10.25418/crick.11558742.v1	text	January 2020
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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Activation-triggered subunit exchange between CaMKII holoenzymes facilitates the spread of kinase activity

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