Structure of the Autoinhibited Kinase Domain of CaMKII and SAXS Analysis of the Holoenzyme
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Ca2+/calmodulin-dependent protein kinase-II (CaMKII) is unique among protein kinases for its dodecameric assembly and its complex response to Ca2+. The crystal structure of the autoinhibited kinase domain of CaMKII, determined at 1.8 A resolution, reveals an unexpected dimeric organization in which the calmodulin-responsive regulatory segments form a coiled-coil strut that blocks peptide and ATP binding to the otherwise intrinsically active kinase domains. A threonine residue in the regulatory segment, which when phosphorylated renders CaMKII calmodulin independent, is held apart from the catalytic sites by the organization of the dimer. This ensures a strict Ca2+ dependence for initial activation. The structure of the kinase dimer, when combined with small-angle X-ray scattering data for the holoenzyme, suggests that inactive CaMKII forms tightly packed autoinhibited assemblies that convert upon activation into clusters of loosely tethered and independent kinase domains.
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CaMKII contains an autoinhibitory regulatory segment that binds across the substrate binding groove.
“As is the case with many kinases, CaMKII contains an autoinhibitory regulatory segment (FIGURE 2, A, B1, AND B2) that binds across the substrate binding groove, whose structure and function have been delineated by peptides, mutations, and crystallography (71–77).”
From Synaptic memory and CaMKII (2023) · cites this paper as [76]
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[20] Processing of X-ray diffraction data collected in oscillation mode
Otwinowski, Z., & Minor, W. (1997) · Methods in Enzymology · doi:10.1016/s0076-6879(97)76066-x · Cited by 33,475 · see citing works
The PyMOL Molecular Graphics System
DeLano, W. L. (2002) · Medical Entomology and Zoology · Cited by 18,147 · see citing works
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination
Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse‐Kunstleve, R. W., Jiang, J., Kuszewski, J. J., Nilges, M., Pannu, N., et al. (1998) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444998003254 · Cited by 15,720 · see citing works
Nicholls, A. O., Sharp, K. A., & Honig, B. H. (1991) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340110407 · Cited by 5,253 · see citing works
Predicting coiled coils from protein sequences.
Lupas, A., Van Dyke, M., & Stock, J. (1991) · Science · doi:10.1126/science.252.5009.1162 · Cited by 3,953 · see citing works
Svergun, D. I. (1992) · Journal of Applied Crystallography · doi:10.1107/s0021889892001663 · Cited by 3,709 · see citing works
Svergun, D. I., Barberato, C., & Koch, M. (1995) · Journal of Applied Crystallography · doi:10.1107/s0021889895007047 · Cited by 3,388 · see citing works
PRIMUS: a Windows PC-based system for small-angle scattering data analysis
Konarev, P. V., Волков, В. В., Sokolova, A. V., Koch, M. H. J., & Svergun, D. I. (2003) · Journal of Applied Crystallography · doi:10.1107/s0021889803012779 · Cited by 2,850 · see citing works
Svergun, D. I. (1999) · Biophysical Journal · doi:10.1016/s0006-3495(99)77443-6 · Cited by 2,229 · see citing works
Uniqueness of ab initio shape determination in small-angle scattering
Волков, В. В., & Svergun, D. I. (2003) · Journal of Applied Crystallography · doi:10.1107/s0021889803000268 · Cited by 1,911 · see citing works
The molecular basis of CaMKII function in synaptic and behavioural memory
Lisman, J., Schulman, H., & Cline, H. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn753 · Cited by 1,860 · see citing works
Likelihood-enhanced fast translation functions
McCoy, A. J., Grosse‐Kunstleve, R. W., Storoni, L. C., & Read, R. J. (2005) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444905001617 · Cited by 1,641 · see citing works
The packing of α-helices: simple coiled-coils
Crick, F. H. C. (1953) · Acta Crystallographica · doi:10.1107/s0365110x53001964 · Cited by 1,578 · see citing works
Sensitivity of CaM Kinase II to the Frequency of Ca <sup>2+</sup> Oscillations
De Koninck, P., & Schulman, H. (1998) · Science · doi:10.1126/science.279.5348.227 · Cited by 1,269 · see citing works
Nolen, B. J., Taylor, S. S., & Ghosh, G. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.08.024 · Cited by 1,171 · see citing works
Miller, S. (1986) · Cell · doi:10.1016/0092-8674(86)90008-5 · Cited by 864 · see citing works
Calmodulin Trapping by Calcium-Calmodulin-Dependent Protein Kinase
Meyer, T., Hanson, P. I., Stryer, L., & Schulman, H. (1992) · Science · doi:10.1126/science.256.5060.1199 · Cited by 637 · see citing works
Structure–function of the multifunctional Ca2+/calmodulin-dependent protein kinase II
HUDMON, A., & SCHULMAN, H. (2002) · Biochemical Journal · doi:10.1042/bj20020228 · Cited by 615 · see citing works
Modulation of Calmodulin Plasticity in Molecular Recognition on the Basis of X-Ray Structures
Meador, W. E., Means, A. R., & Quiocho, F. A. (1993) · Science · doi:10.1126/science.8259515 · Cited by 608 · see citing works
Situs: A Package for Docking Crystal Structures into Low-Resolution Maps from Electron Microscopy
Wriggers, W. R., Milligan, R. A., & McCammon, J. A. (1999) · Journal of Structural Biology · doi:10.1006/jsbi.1998.4080 · Cited by 521 · see citing works
Hanson, P. I., Meyer, T., Stryer, L., & Schulman, H. (1994) · Neuron · doi:10.1016/0896-6273(94)90306-9 · Cited by 500 · see citing works
Young, M. A., Gonfloni, S., Superti‐Furga, G., Roux, B., & Kuriyan, J. (2001) · Cell · doi:10.1016/s0092-8674(01)00301-4 · Cited by 386 · see citing works
Self-citationStructural basis for activation of the titin kinase domain during myofibrillogenesis
Mayans, O. M., van der Ven, P. F. M., Wilm, M. S., Mues, A., Young, P. W., Fürst, D. O., Wilmanns, M., & Gautel, M. (1998) · Nature · doi:10.1038/27603 · Cited by 362 · see citing works
Walshaw, J., & Woolfson, D. N. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4545 · Cited by 357 · see citing works
Structural Basis for the Autoinhibition of Calcium/Calmodulin-Dependent Protein Kinase I
Goldberg, J. D., Nairn, A. C., & Kuriyan, J. (1996) · Cell · doi:10.1016/s0092-8674(00)81066-1 · Cited by 324 · see citing works
Self-citationLai, Y., Nairn, A. C., & Greengard, P. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.12.4253 · Cited by 292 · see citing works
Self-citationMiller, S. G., Patton, B. L., & Kennedy, M. B. (1988) · Neuron · doi:10.1016/0896-6273(88)90109-2 · Cited by 279 · see citing works
Hanson, P. I., & Schulman, H. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)41915-1 · Cited by 216 · see citing works
Lowe, E. D., Noble, M. E. M., Skamnaki, V. T., Oikonomakos, N. G., Owen, D. J., & Johnson, L. N. (1997) · The EMBO Journal · doi:10.1093/emboj/16.22.6646 · Cited by 200 · see citing works
Gaertner, T. R., Kolodziej, S. J., Wang, D., Kobayashi, R., Koomen, J. M., Stoops, J. K., & Waxham, M. N. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313597200 · Cited by 193 · see citing works
Schworer, C. M., Colbran, R. J., Keefer, J. R., & Soderling, T. R. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)68264-x · Cited by 191 · see citing works
Insights into autoregulation from the crystal structure of twitchin kinase
Hu, S., Parker, M. W., Lei, J. Y., Wilce, M. C. J., Benian, G. M., & Kemp, B. E. (1994) · Nature · doi:10.1038/369581a0 · Cited by 190 · see citing works
Bradshaw, J. M., Kubota, Y., Meyer, T., & Schulman, H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1932759100 · Cited by 189 · see citing works
Hoelz, A., Nairn, A. C., & Kuriyan, J. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00171-0 · Cited by 182 · see citing works
Self-citationThiel, G., Czernik, A. J., Gorelick, F. S., Nairn, A. C., & Greengard, P. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.17.6337 · Cited by 176 · see citing works
Self-citationKolodziej, S. J., Hudmon, A., Waxham, M. N., & Stoops, J. K. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.19.14354 · Cited by 170 · see citing works
Rich, R. C., & Schulman, H. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.43.28424 · Cited by 162 · see citing works
Lou, L., & Schulman, H. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-06-02020.1989 · Cited by 161 · see citing works
Inactivation of Ca2+/calmodulin-dependent protein kinase II by basal autophosphorylation.
Colbran, R. J. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53160-4 · Cited by 157 · see citing works
Yang, E., & Schulman, H. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.37.26199 · Cited by 152 · see citing works
The calmodulin‐dependent glycogen synthase kinase from rabbit skeletal muscle
Woodgett, J. R., Davison, M. T., & Cohen, P. (1983) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1983.tb07766.x · Cited by 150 · see citing works
Efficient Rebuilding of Protein Structures
Kleywegt, G. J., & Jones, T. A. (1996) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444996001783 · Cited by 146 · see citing works
Davies, J. M., Tsuruta, H., May, A. P., & Weis, W. I. (2005) · Structure · doi:10.1016/j.str.2004.11.014 · Cited by 117 · see citing works
Nelson, A., Gittis, A. H., & du Lac, S. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.009 · Cited by 110 · see citing works
Regulation of the Ca2+/CaM-Responsive Pool of CaMKII by Scaffold-Dependent Autophosphorylation
Lu, C. S., Hodge, J. J. L., Mehren, J. E., Sun, X. X., & Griffith, L. C. (2003) · Neuron · doi:10.1016/s0896-6273(03)00786-4 · Cited by 100 · see citing works
Smith, M. K., Colbran, R. J., Brickey, D. A., & Soderling, T. R. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)46011-5 · Cited by 95 · see citing works
A Peptide Model for Calmodulin Trapping by Calcium/Calmodulin-dependent Protein Kinase II
Putkey, J. A., & Waxham, M. N. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.47.29619 · Cited by 94 · see citing works
Shields, S. M., Vernon, P. J., & Kelly, P. T. (1984) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1984.tb06084.x · Cited by 94 · see citing works
Oligomeric structure of α-calmodulin-dependent protein kinase II11Edited by A. R. Fersht
Morris, E. P., & Török, K. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4584 · Cited by 86 · see citing works
Bradshaw, J. M., Hudmon, A., & Schulman, H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202154200 · Cited by 76 · see citing works
Mutational analysis of the autoinhibitory domain of calmodulin kinase II.
Brickey, D. A., Bann, J. G., Fong, Y. L., Perrino, L. A., Brennan, R. G., & Soderling, T. R. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)62011-9 · Cited by 68 · see citing works
Identification of the Substrate and Pseudosubstrate Binding Sites of Phosphorylase Kinase γ-Subunit
Huang, C. F., Yuan, C., Blumenthal, D., & Graves, D. J. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.13.7183 · Cited by 28 · see citing works
King, M. M., Shell, D. J., & Kwiatkowski, A. P. (1988) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(88)90052-5 · Cited by 21 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Steinberg, G. R., & Kemp, B. E. (2009) · Physiological Reviews · doi:10.1152/physrev.00011.2008 · Cited by 1,633 · see citing works
Putnam, C. D., Hammel, M., Hura, G. L., & Tainer, J. A. (2007) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583507004635 · Cited by 1,184 · see citing works
Mechanisms of CaMKII action in long-term potentiation
Lisman, J., Yasuda, R., & Raghavachari, S. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3192 · Cited by 1,134 · see citing works
A Dynamic Pathway for Calcium-Independent Activation of CaMKII by Methionine Oxidation
Erickson, J. R., Joiner, M.-L. A., Guan, X., Kutschke, W., Yang, J., Oddis, C. V., Bartlett, R. K., Lowe, J. S., O'Donnell, S. E., Aykin-Burns, N., et al. (2008) · Cell · doi:10.1016/j.cell.2008.02.048 · Cited by 1,122 · see citing works
Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation
Erickson, J. R., Pereira, L., Wang, L., Han, G., Ferguson, A., Dao, K., Copeland, R. J., Despa, F., Hart, G. W., Ripplinger, C. M., et al. (2013) · Nature · doi:10.1038/nature12537 · Cited by 601 · see citing works
Calmodulin-kinases: modulators of neuronal development and plasticity.
Wayman, G. A., Lee, Y.-S., Tokumitsu, H., Silva, A., & Soderling, T. R. (2008) · Neuron · doi:10.1016/j.neuron.2008.08.021 · Cited by 567 · see citing works
The molecular sociology of the cell
Robinson, C. V., Šali, A., & Baumeister, W. P. (2007) · Nature · doi:10.1038/nature06523 · Cited by 533 · see citing works
CaMKII: a central molecular organizer of synaptic plasticity, learning and memory
Yasuda, R., Hayashi, Y., & Hell, J. W. (2022) · Nature Reviews Neuroscience · doi:10.1038/s41583-022-00624-2 · Cited by 431 · see citing works
CaMKII Triggers the Diffusional Trapping of Surface AMPARs through Phosphorylation of Stargazin
Opazo, P., Labrecque, S., Tigaret, C. M., Frouin, A., Wiseman, P. W., Koninck, P. D., & Choquet, D. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.007 · Cited by 403 · see citing works
Ca2+/Calmodulin-dependent Protein Kinases
Swulius, M. T., & Waxham, M. N. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8086-2 · Cited by 394 · see citing works
CaM Kinase: Still Inspiring at 40
Bayer, K. U., & Schulman, H. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.033 · Cited by 307 · see citing works
Signaling by G-protein-coupled receptor (GPCR): Studies on the GnRH receptor
Naor, Z. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.07.001 · Cited by 322 · see citing works
CaMKII regulation in information processing and storage
Coultrap, S. J., & Bayer, K. U. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.05.003 · Cited by 313 · see citing works
Small-Angle X-Ray Scattering from RNA, Proteins, and Protein Complexes
Lipfert, J., & Doniach, S. (2007) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.biophys.36.040306.132655 · Cited by 297 · see citing works
Rellos, P., Pike, A. C. W., Niesen, F. H., Salah, E., Lee, W. H., von Delft, F., & Knapp, S. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000426 · Cited by 279 · see citing works
Synaptic Signaling in Learning and Memory
Kennedy, M. B. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016824 · Cited by 270 · see citing works
Transition from Reversible to Persistent Binding of CaMKII to Postsynaptic Sites and NR2B
Bayer, K. U., LeBel, É., McDonald, G. L., O’Leary, H., Schulman, H., & Koninck, P. D. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3116-05.2006 · Cited by 253 · see citing works
Chao, L. H., Stratton, M. M., Lee, I., Rosenberg, O. S., Levitz, J., Mandell, D. J., Kortemme, T., Groves, J. T., Schulman, H., & Kuriyan, J. (2011) · Cell · doi:10.1016/j.cell.2011.07.038 · Cited by 253 · see citing works
Self-citationClassen, S., Hura, G. L., Holton, J. M., Rambo, R. P., Rodic, I., McGuire, P. J., Dyer, K. N., Hammel, M., Meigs, G., Frankel, K. A., et al. (2013) · Journal of Applied Crystallography · doi:10.1107/s0021889812048698 · Cited by 243 · see citing works
Wernimont, A. K., Artz, J. D., Finerty, P. J., Lin, Y.-H., Amani, M., Allali‐Hassani, A., Senisterra, G. A., Vedadi, M., Tempel, W., MacKenzie, F., et al. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1795 · Cited by 241 · see citing works
CaMKII in the Cardiovascular System: Sensing Redox States
Erickson, J. R., He, B. J., Grumbach, I. M., & Anderson, M. E. (2011) · Physiological Reviews · doi:10.1152/physrev.00018.2010 · Cited by 238 · see citing works
CaMKII inhibitors: from research tools to therapeutic agents
Pellicena, P., & Schulman, H. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00021 · Cited by 235 · see citing works
Molecular anatomy of the postsynaptic density.
Okabe, S. (2007) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2007.01.006 · Cited by 225 · see citing works
Reversible protein inactivation by optogenetic trapping in cells
Lee, S., Park, H., Kyung, T., Kim, N. Y., Kim, S., Kim, J.-H., & Heo, W. D. (2014) · Nature Methods · doi:10.1038/nmeth.2940 · Cited by 218 · see citing works
Analysis of X-ray and neutron scattering from biomacromolecular solutions
Petoukhov, M. V., & Svergun, D. I. (2007) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2007.06.009 · Cited by 215 · see citing works
Calcium/calmodulin-dependent kinase II and Alzheimer’s disease
Ghosh, A., & Giese, K. P. (2015) · Molecular Brain · doi:10.1186/s13041-015-0166-2 · Cited by 205 · see citing works
Smooth muscle signalling pathways in health and disease
Kim, H. R., Appel, S., Vetterkind, S., Gangopadhyay, S. S., & Morgan, K. G. (2008) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2008.00552.x · Cited by 200 · see citing works
Dual Mechanism of a Natural CaMKII Inhibitor
Vest, R. S., Davies, K. D., O’Leary, H., Port, J. D., & Bayer, K. U. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-02-0185 · Cited by 188 · see citing works
Davies, J. M., Brünger, A. T., & Weis, W. I. (2008) · Structure · doi:10.1016/j.str.2008.02.010 · Cited by 192 · see citing works
Physiological and unappreciated roles of CaMKII in the heart
Beckendorf, J., van den Hoogenhof, M. M. G., & Backs, J. (2018) · Basic Research in Cardiology · doi:10.1007/s00395-018-0688-8 · Cited by 173 · see citing works
Singh, S., & Parniske, M. (2012) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2012.04.002 · Cited by 167 · see citing works
Activation segment dimerization: a mechanism for kinase autophosphorylation of non‐consensus sites
Pike, A. C. W., Rellos, P., Niesen, F., Turnbull, A. P., Oliver, A. W., Parker, S. A., Turk, B. E., Pearl, L. H., & Knapp, S. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.8 · Cited by 167 · see citing works
Cytoskeletal signaling: is memory encoded in microtubule lattices by CaMKII phosphorylation?
Craddock, T. J. A., Tuszynski, J. A., & Hameroff, S. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002421 · Cited by 160 · see citing works
Buard, I., Coultrap, S. J., Freund, R. K., Lee, Y.-S., Dell'Acqua, M. L., Silva, A. J., & Bayer, K. U. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1469-10.2010 · Cited by 160 · see citing works
CaMKII oxidative activation and the pathogenesis of cardiac disease
Luczak, E. D., & Anderson, M. E. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.02.004 · Cited by 153 · see citing works
Small-molecule therapies for cardiac hypertrophy: moving beneath the cell surface
McKinsey, T. A., & Kass, D. A. (2007) · Nature Reviews Drug Discovery · doi:10.1038/nrd2193 · Cited by 151 · see citing works
Coultrap, S. J., Vest, R. S., Ashpole, N. M., Hudmon, A., & Bayer, K. U. (2011) · Acta Pharmacologica Sinica · doi:10.1038/aps.2011.68 · Cited by 145 · see citing works
Shifman, J. M., Choi, M. H., Mihalas, S., Mayo, S. L., & Kennedy, M. B. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606433103 · Cited by 143 · see citing works
STDP in a Bistable Synapse Model Based on CaMKII and Associated Signaling Pathways
Graupner, M., & Brunel, N. (2007) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0030221 · Cited by 143 · see citing works
Mechanisms of CaMKII Activation in the Heart
Erickson, J. R. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00059 · Cited by 137 · see citing works
The CaMKII holoenzyme structure in activation-competent conformations
Myers, J. B., Zaegel, V., Coultrap, S. J., Miller, A. P., Bayer, K. U., & Reichow, S. (2017) · Nature Communications · doi:10.1038/ncomms15742 · Cited by 130 · see citing works
Analysis of CaM-kinase signaling in cells
Wayman, G. A., Tokumitsu, H., Davare, M. A., & Soderling, T. R. (2011) · Cell Calcium · doi:10.1016/j.ceca.2011.02.007 · Cited by 128 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
Li, L., Stefan, M. I., & Novère, N. G. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043810 · Cited by 119 · see citing works
Intersubunit capture of regulatory segments is a component of cooperative CaMKII activation
Chao, L. H., Pellicena, P., Deindl, S., Barclay, L. A., Schulman, H., & Kuriyan, J. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1751 · Cited by 119 · see citing works
Self-citationAiba, T., Hesketh, G. G., Liu, T., Carlisle, R. A., Villa‐Abrille, M. C., O'Rourke, B. P., Akar, F. G., & Tomaselli, G. F. (2009) · Cardiovascular Research · doi:10.1093/cvr/cvp324 · Cited by 119 · see citing works
Structural Transitions and Thermodynamics of a Glycine-Dependent Riboswitch from Vibrio cholerae
Lipfert, J., Das, R., Chu, V. B., Kudaravalli, M., Boyd, N., Herschlag, D., & Doniach, S. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.10.022 · Cited by 117 · see citing works
Conserved α-Helix Acts as Autoinhibitory Sequence in AMP-activated Protein Kinase α Subunits
Pang, T., Xiong, B., Li, J.-Y., Qiu, B., Jin, G.-Z., Shen, J., & Li, J. X. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605790200 · Cited by 113 · see citing works
Stratton, M., Lee, I.-H., Bhattacharyya, M., Christensen, S. M., Chao, L. H., Schulman, H., Groves, J. T., & Kuriyan, J. (2014) · eLife · doi:10.7554/elife.01610 · Cited by 114 · see citing works
Self-citationCaMKIIβ Association with the Actin Cytoskeleton Is Regulated by Alternative Splicing
O'Leary, H., Lasda, E., & Bayer, K. U. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-03-0252 · Cited by 113 · see citing works
Bhattacharyya, M., Stratton, M. M., Going, C. C., McSpadden, E. D., Huang, Y., Susa, A. C., Elleman, A., Cao, Y. M., Pappireddi, N., Burkhardt, P., et al. (2016) · eLife · doi:10.7554/elife.13405 · Cited by 112 · see citing works
Self-citationEvolution of CASK into a Mg 2+ -Sensitive Kinase
Mukherjee, K., Sharma, M., Jahn, R., Wahl, M. C., & Südhof, T. C. (2010) · Science Signaling · doi:10.1126/scisignal.2000800 · Cited by 110 · see citing works
Derepression of pathological cardiac genes by members of the CaM kinase superfamily
McKinsey, T. A. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.11.036 · Cited by 106 · see citing works
Protein–protein interactions in the allosteric regulation of protein kinases
Pellicena, P., & Kuriyan, J. (2006) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2006.10.007 · Cited by 106 · see citing works
Self-citationMolecular Basis of the Death-Associated Protein Kinase–Calcium/Calmodulin Regulator Complex
de Diego, I., Kuper, J., Bakalova, N., Kursula, P., & Wilmanns, M. (2010) · Science Signaling · doi:10.1126/scisignal.2000552 · Cited by 104 · see citing works
Oligomerization states of the association domain and the holoenyzme of Ca2+/CaM kinase II
Rosenberg, O. S., Deindl, S., Comolli, L. R., Hoelz, A., Downing, K. H., Nairn, A. C., & Kuriyan, J. (2006) · FEBS Journal · doi:10.1111/j.1742-4658.2005.05088.x · Cited by 105 · see citing works
Self-citationCaMKII Autonomy Is Substrate-dependent and Further Stimulated by Ca2+/Calmodulin
Coultrap, S. J., Buard, I., Kulbe, J. R., Dell’Acqua, M. L., & Bayer, K. U. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.069351 · Cited by 103 · see citing works
Erickson, J. R., Patel, R., Ferguson, A., Bossuyt, J., & Bers, D. M. (2011) · Circulation Research · doi:10.1161/circresaha.111.247148 · Cited by 103 · see citing works
Sørensen, A. B., Søndergaard, M. T., & Overgaard, M. T. (2013) · FEBS Journal · doi:10.1111/febs.12337 · Cited by 101 · see citing works
Kim, E. Y., Rumpf, C. H., Fujiwara, Y., Cooley, E. S., Petegem, F. V., & Minor, D. L. (2008) · Structure · doi:10.1016/j.str.2008.07.010 · Cited by 100 · see citing works
Fujii, H., Inoue, M., Okuno, H., Sano, Y., Takemoto‐Kimura, S., Kitamura, K., Kano, M., & Bito, H. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.03.033 · Cited by 94 · see citing works
Novel insights into CaMKII function and regulation during memory formation
Lucchesi, W., Mizuno, K., & Giese, K.-P. (2010) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2010.10.009 · Cited by 95 · see citing works
Bhattacharyya, M., Karandur, D., & Kuriyan, J. (2020) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a035147 · Cited by 95 · see citing works
Self-citationIdentification of the Calmodulin Binding Domain of Connexin 43
Zhou, Y., Yang, W., Lurtz, M. M., Ye, Y., Huang, Y., Lee, H., Chen, Y., Louis, C. F., & Yang, J. J. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m707728200 · Cited by 94 · see citing works
Pepke, S., Kinzer-Ursem, T., Mihalas, S., & Kennedy, M. B. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000675 · Cited by 92 · see citing works
αCaMKII autophosphorylation: a fast track to memory
Irvine, E. E., von Hertzen, L. S. J., Plattner, F., & Giese, K.-P. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.06.009 · Cited by 92 · see citing works
Shimoda, Y., Han, L., Yamazaki, T., Suzuki, R., Hayashi, M., & Imaizumi‐Anraku, H. (2012) · The Plant Cell · doi:10.1105/tpc.111.092197 · Cited by 88 · see citing works
Structural rearrangement of CaMKIIα catalytic domains encodes activation
Thaler, C., Koushik, S. V., Puhl, H. L., Blank, P. S., & Vogel, S. S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901913106 · Cited by 86 · see citing works
Structural studies on the regulation of Ca2+/calmodulin dependent protein kinase II
Stratton, M. M., Chao, L. H., Schulman, H., & Kuriyan, J. (2013) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2013.04.002 · Cited by 89 · see citing works
Self-citationRostas, J. A. P., & Skelding, K. A. (2023) · Cells · doi:10.3390/cells12030401 · Cited by 85 · see citing works
Calmodulin and CaMKII as molecular switches for cardiac ion channels: Fig. 1
Pitt, G. S. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.10.019 · Cited by 86 · see citing works
Structure and function of AMP‐activated protein kinase
Oakhill, J. S., Scott, J. W., & Kemp, B. E. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2009.01977.x · Cited by 85 · see citing works
Brzozowski, J. S., & Skelding, K. A. (2019) · Pharmaceuticals · doi:10.3390/ph12010008 · Cited by 84 · see citing works
Ghenoiu, C., Wheelock, M., & Funabiki, H. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.10.002 · Cited by 82 · see citing works
An Autoinhibited Coiled-Coil Design Strategy for Split-Protein Protease Sensors
Shekhawat, S. S., Porter, J. R., Sriprasad, A., & Ghosh, I. (2009) · Journal of the American Chemical Society · doi:10.1021/ja9050857 · Cited by 77 · see citing works
Atrial remodelling in atrial fibrillation: CaMKII as a nodal proarrhythmic signal
Mesubi, O. O., & Anderson, M. E. (2016) · Cardiovascular Research · doi:10.1093/cvr/cvw002 · Cited by 81 · see citing works
O’Leary, H., Liu, W. H., Rorabaugh, J. M., Coultrap, S. J., & Bayer, K. U. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.233668 · Cited by 76 · see citing works
Anderson, M. E. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.12.009 · Cited by 78 · see citing works
A critical evaluation of protein kinase regulation by activation loop autophosphorylation
Reinhardt, R., & Leonard, T. A. (2023) · eLife · doi:10.7554/elife.88210 · Cited by 76 · see citing works
Mechanisms of Ca2+/calmodulin-dependent kinase II activation in single dendritic spines
Chang, J.-Y., Nakahata, Y., Hayano, Y., & Yasuda, R. (2019) · Nature Communications · doi:10.1038/s41467-019-10694-z · Cited by 77 · see citing works
CaMKII Activity in the Inflammatory Response of Cardiac Diseases
Rusciano, M. R., Sommariva, E., Douin‐Echinard, V., Ciccarelli, M., Poggio, P., & Maione, A. S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20184374 · Cited by 76 · see citing works
βCaMKII Regulates Actin Assembly and Structure
Sanabria, H., Swulius, M. T., Kolodziej, S. J., Liu, J., & Waxham, M. N. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m809518200 · Cited by 75 · see citing works
Signalling pathways underlying structural plasticity of dendritic spines
Patterson, M., & Yasuda, R. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01328.x · Cited by 73 · see citing works
Tsutakawa, S. E., Hura, G. L., Frankel, K. A., Cooper, P. K., & Tainer, J. A. (2006) · Journal of Structural Biology · doi:10.1016/j.jsb.2006.09.008 · Cited by 73 · see citing works
Joint use of small-angle X-ray and neutron scattering to study biological macromolecules in solution
Petoukhov, M. V., & Svergun, D. I. (2006) · European Biophysics Journal · doi:10.1007/s00249-006-0063-9 · Cited by 71 · see citing works
Calmodulin and STIM proteins: Two major calcium sensors in the cytoplasm and endoplasmic reticulum
Marshall, C. B., Nishikawa, T., Osawa, M., Stathopulos, P. B., & Ikura, M. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.01.106 · Cited by 64 · see citing works
Sałaciak, K., Koszałka, A., Żmudzka, E., & Pytka, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094307 · Cited by 66 · see citing works
CaMKII, an emerging molecular driver for calcium homeostasis, arrhythmias, and cardiac dysfunction
Grueter, C. E., Colbran, R. J., & Anderson, M. E. (2006) · Journal of Molecular Medicine · doi:10.1007/s00109-006-0125-6 · Cited by 61 · see citing works
Toxoplasma and Plasmodium protein kinases: Roles in invasion and host cell remodelling
Lim, D., Cooke, B. M., Doerig, C., & Saeij, J. P. J. (2011) · International Journal for Parasitology · doi:10.1016/j.ijpara.2011.11.007 · Cited by 64 · see citing works
Li, L., Khanna, M., Jo, I., Wang, F., Ashpole, N. M., Hudmon, A., & Meroueh, S. O. (2011) · Journal of Chemical Information and Modeling · doi:10.1021/ci100490w · Cited by 63 · see citing works
Timing in Cellular Ca2+ Signaling
Boulware, M. J., & Marchant, J. S. (2008) · Current Biology · doi:10.1016/j.cub.2008.07.018 · Cited by 62 · see citing works
CaMKII binds both substrates and activators at the active site
Özden, C., Sloutsky, R., Mitsugi, T., Santos, N., Agnello, E., Gaubitz, C., Foster, J., Lapinskas, E., Esposito, E. A., Saneyoshi, T., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111064 · Cited by 61 · see citing works
Wynne, J. P., Wu, J., Su, W., Mor, A., Patsoukis, N., Boussiotis, V. A., Hubbard, S. R., & Philips, M. R. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201201157 · Cited by 61 · see citing works
Allosteric activation of apicomplexan calcium-dependent protein kinases
Ingram, J. R., Knockenhauer, K. E., Markus, B. M., Mandelbaum, J., Ramek, A., Shan, Y., Shaw, D. E., Schwartz, T., Ploegh, H. L., & Lourido, S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1505914112 · Cited by 60 · see citing works
Regulation of CaMKII signaling in cardiovascular disease
Mollova, M. Y., Katus, H. A., & Backs, J. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00178 · Cited by 60 · see citing works
Liu, J., Sudom, A. M., Min, X., Cao, Z., Gao, X., Ayres, M., Lee, F., Cao, P., Johnstone, S., Plotnikova, O. V., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.366658 · Cited by 60 · see citing works
Toward a Molecular Structure of the Eukaryotic Kinetochore
Welburn, J. P. I., & Cheeseman, I. M. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.10.011 · Cited by 59 · see citing works
Song, Y. H., Cho, H., Ryu, S.-Y., Yoon, J., Park, S.-H., Noh, C.-I., Lee, S., & Ho, W. (2009) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2009.10.020 · Cited by 59 · see citing works
An electrostatic network and long‐range regulation of Src kinases
Özkırımlı, E., Yadav, S. S., Miller, W. T., & Post, C. B. (2008) · Protein Science · doi:10.1110/ps.037457.108 · Cited by 58 · see citing works
Flexible linkers in CaMKII control the balance between activating and inhibitory autophosphorylation
Bhattacharyya, M., Lee, Y. K., Muratcioglu, S., Qiu, B., Nyayapati, P., Schulman, H., Groves, J. T., & Kuriyan, J. (2020) · eLife · doi:10.7554/elife.53670 · Cited by 58 · see citing works
Self-citation
- Authors
- Rosenberg, O. S., Deindl, S., Sung, R.-J., Nairn, A. C., & Kuriyan, J.
- Affiliations
- Howard Hughes Medical Institute (US)
- Yale University (US)
- Corresponding author
- Kuriyan, John
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2005-12
- Volume
- 123
- Issue
- 5
- Pages
- 849-860
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2023129668
- Cited by
- 333
- References
- 53
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 14 · 2023: 21 · 2022: 16 · 2021: 14 · 2020: 20 · 2019: 14 · 2018: 11 · 2017: 9 · 2016: 7 · 2015: 13 · 2014: 13 · 2013: 13 · 2012: 22
- FWCI
- 8.44
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
- Keywords
- CaMKII, calcium/calmodulin-dependent protein kinase II, autoinhibition, kinase domain, threonine phosphorylation, calcium dependence, holoenzyme structure, protein kinase activation
- MeSH terms
- Amino Acid Sequence, Animals, Binding Sites, Calcium, Calmodulin, Models, Molecular, Molecular Sequence Data, Sequence Alignment, Caenorhabditis elegans, Protein Structure, Secondary, Protein Structure, Tertiary, Calcium-Calmodulin-Dependent Protein Kinases, Crystallography, X-Ray, Dimerization, Holoenzymes, Protein Structure, Quaternary, Caenorhabditis elegans Proteins, Calcium-Calmodulin-Dependent Protein Kinase Type 2
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