CoChat
Sign Up
Cited by 112Protein Kinase Regulation and GTPase SignalingProtein Structure and DynamicsSignaling Pathways in Disease

Molecular mechanism of activation-triggered subunit exchange in Ca2+/calmodulin-dependent protein kinase II

Open access
Bhattacharyya, Moitrayee, Stratton, Margaret M, Going, Catherine C, McSpadden, Ethan D, Huang, Yongjian, Susa, Anna C, Elleman, Anna, Cao, Yumeng Melody +7 more·2016·eLife
DOI 10.7554/elife.13405PMC PMC4859805
Open this paper in CoChat — free account

Abstract

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.7554/elife.13405

Cites

13 of 13 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The subunit exchange process requires CaMKII activation and is initiated after phosphorylation of T305/T306 in the CaM footprint, which blocks rebinding of CaM and frees the CaM-binding element to interact with the hub of the holoenzyme.

    “This subunit exchange process requires CaMKII activation and is initiated after phosphorylation of T305/T306 in the CaM footprint, which blocks rebinding of CaM and frees the CaM-binding element to interact with the hub of the holoenzyme (407).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [407]

    The Introduction says phosphorylation of Thr 305/306 prevents Ca2+/CaM rebinding, and the Results and discussion describe activation-triggered exchange and a model in which the freed CaM-binding element interacts with the hub (pages not provided). But the paper says Thr 305/306 phosphorylation potentiates exchange; it does not establish that exchange must be initiated after that phosphorylation. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • A basic portion of the CaM binding domain exposed after activation and free of CaM may dock at the intersubunit interface of the hub and act as a wedge that breaks integrity of the hub and facilitates release of dimeric units.

    “A basic portion of the CaM binding domain exposed after activation and free of CaM may dock at the intersubunit interface of the hub and act as a wedge that breaks integrity of the hub and facilitates release of dimeric units (407, 408).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [407]

  • Recent biochemical evidence suggests that CaMKII may also satisfy the second requirement, i.e., for subunit exchange.

    “Recent biochemical evidence suggests that CaMKII may also satisfy this second requirement, i.e., for subunit exchange (28, 406–408).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [407]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 93

  1. Adams PD Afonine PV Bunkóczi G Chen VB Davis IW Echols N Headd JJ Hung LW Kapral GJ Grosse-Kunstleve RW McCoy AJ Moriarty NW Oeffner R Read RJ Richardson DC Richardson JS Terwilliger TC Zwart PH 2010 Phenix: A comprehensive python-based system for macromolecular structure solution Acta Crystallographica. Section D, Biological Crystallography 66 213 221 10.1107/S0907444909052925 20124702 PMC2815670 · DOI · Paper page
  2. Bahar I Rader AJ 2005 Coarse-grained normal mode analysis in structural biology Current Opinion in Structural Biology 15 586 592 10.1016/j.sbi.2005.08.007 16143512 PMC1482533 · DOI
  3. Berendsen HJC van der Spoel D van Drunen R 1995 Gromacs: A message-passing parallel molecular dynamics implementation Computer Physics Communications 91 43 56 10.1016/0010-4655(95)00042-E · DOI
  4. Bradshaw JM Kubota Y Meyer T Schulman H 2003 An ultrasensitive ca2+/calmodulin-dependent protein kinase ii-protein phosphatase 1 switch facilitates specificity in postsynaptic calcium signaling Proceedings of the National Academy of Sciences of the United States of America 100 10512 10517 10.1073/pnas.1932759100 12928489 PMC193592 · DOI · Paper page
  5. Bulleit RF Bennett MK Molloy SS Hurley JB Kennedy MB 1988 Conserved and variable regions in the subunits of brain type II ca2+/calmodulin-dependent protein kinase Neuron 1 63 72 10.1016/0896-6273(88)90210-3 2856087 · DOI
  6. Burkhardt P Grønborg M McDonald K Sulur T Wang Q King N 2014 Evolutionary insights into premetazoan functions of the neuronal protein homer Molecular Biology and Evolution 31 2342 2355 10.1093/molbev/msu178 24899667 PMC4137706 · DOI · Paper page
  7. Campos EI Stafford JM Reinberg D 2014 Epigenetic inheritance: Histone bookmarks across generations Trends in Cell Biology 24 664 674 10.1016/j.tcb.2014.08.004 25242115 PMC4254315 · DOI
  8. Carr M Leadbeater BS Hassan R Nelson M Baldauf SL 2008 Molecular phylogeny of choanoflagellates, the sister group to metazoa Proceedings of the National Academy of Sciences of the United States of America 105 16641 16646 10.1073/pnas.0801667105 18922774 PMC2575473 · DOI · Paper page
  9. Chao LH Stratton MM Lee IH Rosenberg OS Levitz J Mandell DJ Kortemme T Groves JT Schulman H Kuriyan J 2011 A mechanism for tunable autoinhibition in the structure of a human ca2+/calmodulin- dependent kinase II holoenzyme Cell 146 732 745 10.1016/j.cell.2011.07.038 21884935 PMC3184253 · DOI
  10. Chen VB Arendall WB Headd JJ Keedy DA Immormino RM Kapral GJ Murray LW Richardson JS Richardson DC 2010 Molprobity: All-atom structure validation for macromolecular crystallography Acta Crystallographica. Section D, Biological Crystallography 66 12 21 10.1107/S0907444909042073 20057044 PMC2803126 · DOI · Paper page
  11. Chowdhury SK Katta V Chait BT 1990 Probing conformational changes in proteins by mass spectrometry Journal of the American Chemical Society 112 9012 9013 10.1021/ja00180a074 · DOI
  12. Colbran RJ Fong YL Schworer CM Soderling TR 1988 Regulatory interactions of the calmodulin-binding, inhibitory, and autophosphorylation domains of ca2+/calmodulin-dependent protein kinase II The Journal of Biological Chemistry 263 18145 18151 2848027
  13. Colbran RJ Schworer CM Hashimoto Y Fong YL Rich DP Smith MK Soderling TR 1989a Calcium/calmodulin-dependent protein kinase II Biochemical Journal 258 313 325 2539803 PMC1138364
  14. Colbran RJ Smith MK Schworer CM Fong YL Soderling TR 1989b Regulatory domain of calcium/calmodulin-dependent protein kinase II. mechanism of inhibition and regulation by phosphorylation The Journal of Biological Chemistry 264 4800 4804 2538462
  15. Coultrap SJ Zaegel V Bayer KU 2014 Camkii isoforms differ in their specific requirements for regulation by nitric oxide FEBS Letters 588 4672 4676 10.1016/j.febslet.2014.10.039 25447522 PMC4312479 · DOI
  16. Crivici A Ikura M 1995 Molecular and structural basis of target recognition by calmodulin Annual Review of Biophysics and Biomolecular Structure 24 85 116 10.1146/annurev.bb.24.060195.000505 7663132 · DOI
  17. De Koninck P Schulman H 1998 Sensitivity of cam kinase II to the frequency of ca2+ oscillations Science 279 227 230 10.1126/science.279.5348.227 9422695 · DOI · Paper page
  18. Emsley P Lohkamp B Scott WG Cowtan K 2010 Features and development of coot Acta Crystallographica. Section D, Biological Crystallography 66 486 501 10.1107/S0907444910007493 20383002 PMC2852313 · DOI
  19. Erickson JR Joiner ML Guan X Kutschke W Yang J Oddis CV Bartlett RK Lowe JS O'Donnell SE Aykin-Burns N Zimmerman MC Zimmerman K Ham AJ Weiss RM Spitz DR Shea MA Colbran RJ Mohler PJ Anderson ME 2008 A dynamic pathway for calcium-independent activation of camkii by methionine oxidation Cell 133 462 474 10.1016/j.cell.2008.02.048 18455987 PMC2435269 · DOI · Paper page
  20. Erickson JR Nichols CB Uchinoumi H Stein ML Bossuyt J Bers DM 2015 S-nitrosylation induces both autonomous activation and inhibition of calcium/calmodulin-dependent protein kinase II δ The Journal of Biological Chemistry 290 25646 25656 10.1074/jbc.M115.650234 26316536 PMC4646208 · DOI
  21. Erickson JR Pereira L Wang L Han G Ferguson A Dao K Copeland RJ Despa F Hart GW Ripplinger CM Bers DM 2013 Diabetic hyperglycaemia activates camkii and arrhythmias by o-linked glycosylation Nature 502 372 376 10.1038/nature12537 24077098 PMC3801227 · DOI
  22. Fairclough SR Chen Z Kramer E Zeng Q Young S Robertson HM Begovic E Richter DJ Russ C Westbrook MJ Manning G Lang BF Haas B Nusbaum C King N 2013 Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate salpingoeca rosetta Genome Biology 14 R15 10.1186/gb-2013-14-2-r15 23419129 PMC4054682 · DOI
  23. Gaertner TR Kolodziej SJ Wang D Kobayashi R Koomen JM Stoops JK Waxham MN 2004 Comparative analyses of the three-dimensional structures and enzymatic properties of alpha, beta, gamma and delta isoforms of ca2+-calmodulin-dependent protein kinase II The Journal of Biological Chemistry 279 12484 12494 10.1074/jbc.M313597200 14722083 · DOI
  24. Giese KP Fedorov NB Filipkowski RK Silva AJ 1998 Autophosphorylation at thr286 of the alpha calcium-calmodulin kinase II in LTP and learning Science 279 870 873 10.1126/science.279.5352.870 9452388 · DOI · Paper page
  25. Giese KP Mizuno K 2013 The roles of protein kinases in learning and memory Learning & Memory (Cold Spring Harbor, N.Y.) 20 540 552 10.1101/lm.028449.112 24042850 · DOI
  26. Goldberg J Nairn AC Kuriyan J 1996 Structural basis for the autoinhibition of calcium/calmodulin-dependent protein kinase I Cell 84 875 887 10.1016/S0092-8674(00)81066-1 8601311 · DOI
  27. Hanley RM Means AR Ono T Kemp BE Burgin KE Waxham N Kelly PT 1987 Functional analysis of a complementary DNA for the 50-kilodalton subunit of calmodulin kinase II Science 237 293 297 10.1126/science.3037704 3037704 · DOI
  28. Hanson PI Meyer T Stryer L Schulman H 1994 Dual role of calmodulin in autophosphorylation of multifunctional cam kinase may underlie decoding of calcium signals Neuron 12 943 956 10.1016/0896-6273(94)90306-9 8185953 · DOI · Paper page
  29. Hashimoto Y Schworer CM Colbran RJ Soderling TR 1987 Autophosphorylation of Ca2+/calmodulin-dependent protein kinase II. effects on total and Ca2+-independent activities and kinetic parameters The Journal of Biological Chemistry 262 8051 8055 3110142
  30. Hoelz A Nairn AC Kuriyan J 2003 Crystal structure of a tetradecameric assembly of the association domain of ca2+/calmodulin-dependent kinase II Molecular Cell 11 1241 1251 10.1016/S1097-2765(03)00171-0 12769848 · DOI
  31. Hook SS Means AR 2001 Ca(2+)/CaM-dependent kinases: From activation to function Annual Review of Pharmacology and Toxicology 41 471 505 10.1146/annurev.pharmtox.41.1.471 11264466 · DOI
  32. Hu SH Parker MW Lei JY Wilce MC Benian GM Kemp BE 1994 Insights into autoregulation from the crystal structure of twitchin kinase Nature 369 581 584 10.1038/369581a0 8202162 · DOI
  33. Huse M Kuriyan J 2002 The conformational plasticity of protein kinases Cell 109 275 282 10.1016/S0092-8674(02)00741-9 12015977 · DOI
  34. Johnson LN Noble ME Owen DJ 1996 Active and inactive protein kinases: Structural basis for regulation Cell 85 149 158 10.1016/S0092-8674(00)81092-2 8612268 · DOI
  35. Jurchen JC Williams ER 2003 Origin of asymmetric charge partitioning in the dissociation of gas-phase protein homodimers Journal of the American Chemical Society 125 2817 2826 10.1021/ja0211508 12603172 PMC1325210 · DOI
  36. Kageyama H Nishiwaki T Nakajima M Iwasaki H Oyama T Kondo T 2006 Cyanobacterial circadian pacemaker: Kai protein complex dynamics in the kaic phosphorylation cycle in vitro Molecular Cell 23 161 171 10.1016/j.molcel.2006.05.039 16857583 · DOI
  37. Kanaseki T Ikeuchi Y Sugiura H Yamauchi T 1991 Structural features of ca2+/calmodulin-dependent protein kinase II revealed by electron microscopy The Journal of Cell Biology 115 1049 1060 10.1083/jcb.115.4.1049 1659571 PMC2289961 · DOI
  38. Kandel ER Dudai Y Mayford MR 2014 The molecular and systems biology of memory Cell 157 163 186 10.1016/j.cell.2014.03.001 24679534 · DOI · Paper page
  39. Kolb SJ Hudmon A Ginsberg TR Waxham MN 1998 Identification of domains essential for the assembly of calcium/calmodulin-dependent protein kinase II holoenzymes The Journal of Biological Chemistry 273 31555 31564 10.1074/jbc.273.47.31555 9813071 · DOI
  40. Kolodziej SJ Hudmon A Waxham MN Stoops JK 2000 Three-dimensional reconstructions of calcium/calmodulin-dependent (cam) kinase iialpha and truncated cam kinase iialpha reveal a unique organization for its structural core and functional domains The Journal of Biological Chemistry 275 14354 14359 10.1074/jbc.275.19.14354 10799516 · DOI
  41. Lander GC Stagg SM Voss NR Cheng A Fellmann D Pulokas J Yoshioka C Irving C Mulder A Lau PW Lyumkis D Potter CS Carragher B 2009 Appion: An integrated, database-driven pipeline to facilitate EM image processing Journal of Structural Biology 166 95 102 10.1016/j.jsb.2009.01.002 19263523 PMC2775544 · DOI
  42. Lickteig R Shenolikar S Denner L Kelly PT 1988 Regulation of Ca2+/calmodulin-dependent protein kinase II by ca2+/calmodulin-independent autophosphorylation The Journal of Biological Chemistry 263 19232 19239 2848818
  43. Lin CR Kapiloff MS Durgerian S Tatemoto K Russo AF Hanson P Schulman H Rosenfeld MG 1987 Molecular cloning of a brain-specific calcium/calmodulin-dependent protein kinase Proceedings of the National Academy of Sciences of the United States of America 84 5962 5966 10.1073/pnas.84.16.5962 3475713 PMC298983 · DOI
  44. Lindorff-Larsen K Piana S Palmo K Maragakis P Klepeis JL Dror RO Shaw DE 2010 Improved side-chain torsion potentials for the amber ff99sb protein force field Proteins 78 1950 1958 10.1002/prot.22711 20408171 PMC2970904 · DOI
  45. Lisman J Raghavachari S 2015 Biochemical principles underlying the stable maintenance of LTP by the camkii/nmdar complex Brain Research 1621 51 61 10.1016/j.brainres.2014.12.010 25511992 PMC4466085 · DOI
  46. Lisman J Schulman H Cline H 2002 The molecular basis of camkii function in synaptic and behavioural memory Nature Reviews. Neuroscience 3 175 190 10.1038/nrn753 11994750 · DOI · Paper page
  47. Lisman JE Goldring MA 1988 Feasibility of long-term storage of graded information by the ca2+/calmodulin-dependent protein kinase molecules of the postsynaptic density Proceedings of the National Academy of Sciences of the United States of America 85 5320 5324 10.1073/pnas.85.14.5320 3393540 PMC281742 · DOI · Paper page
  48. Lisman JE 1985 A mechanism for memory storage insensitive to molecular turnover: A bistable autophosphorylating kinase Proceedings of the National Academy of Sciences of the United States of America 82 3055 3057 10.1073/pnas.82.9.3055 2986148 PMC397705 · DOI · Paper page
  49. Lou LL Lloyd SJ Schulman H 1986 Activation of the multifunctional ca2+/calmodulin-dependent protein kinase by autophosphorylation: Atp modulates production of an autonomous enzyme Proceedings of the National Academy of Sciences of the United States of America 83 9497 9501 10.1073/pnas.83.24.9497 3467320 PMC387167 · DOI · Paper page
  50. Lou LL Schulman H 1989 Distinct autophosphorylation sites sequentially produce autonomy and inhibition of the multifunctional Ca2+/calmodulin-dependent protein kinase The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 9 2020 2032 2542484 PMC6569737
  51. Luo M Anderson ME 2013 Mechanisms of altered Ca²⁺ handling in heart failure Circulation Research 113 690 708 10.1161/CIRCRESAHA.113.301651 23989713 PMC4080816 · DOI
  52. Mallick SP Carragher B Potter CS Kriegman DJ 2005 Ace: Automated CTF estimation Ultramicroscopy 104 8 29 10.1016/j.ultramic.2005.02.004 15935913 · DOI
  53. Markson JS O'Shea EK 2009 The molecular clockwork of a protein-based circadian oscillator FEBS Letters 583 3938 3947 10.1016/j.febslet.2009.11.021 19913541 PMC2810098 · DOI
  54. McCoy AJ Grosse-Kunstleve RW Adams PD Winn MD Storoni LC Read RJ 2007 Phaser crystallographic software Journal of Applied Crystallography 40 658 674 10.1107/S0021889807021206 19461840 PMC2483472 · DOI · Paper page
  55. Meador WE Means AR Quiocho FA 1992 Target enzyme recognition by calmodulin: 2.4 A structure of a calmodulin-peptide complex Science 257 1251 1255 10.1126/science.1519061 1519061 · DOI
  56. Meador WE Means AR Quiocho FA 1993 Modulation of calmodulin plasticity in molecular recognition on the basis of x-ray structures Science 262 1718 1721 10.1126/science.8259515 8259515 · DOI
  57. Meyer T Hanson PI Stryer L Schulman H 1992 Calmodulin trapping by calcium-calmodulin-dependent protein kinase Science 256 1199 1202 10.1126/science.256.5060.1199 1317063 · DOI · Paper page
  58. Miller DJ Ball EE 2008 Cryptic complexity captured: The nematostella genome reveals its secrets Trends in Genetics: TIG 24 1 4 10.1016/j.tig.2007.10.002 18054114 · DOI
  59. Miller SG Kennedy MB 1986 Regulation of brain type II ca2+/calmodulin-dependent protein kinase by autophosphorylation: A ca2+-triggered molecular switch Cell 44 861 870 10.1016/0092-8674(86)90008-5 3006921 · DOI · Paper page
  60. Miller SG Patton BL Kennedy MB 1988 Sequences of autophosphorylation sites in neuronal type II cam kinase that control ca2(+)-independent activity Neuron 1 593 604 10.1016/0896-6273(88)90109-2 2856100 · DOI · Paper page
  61. Mindell JA Grigorieff N 2003 Accurate determination of local defocus and specimen tilt in electron microscopy Journal of Structural Biology 142 334 347 10.1016/S1047-8477(03)00069-8 12781660 · DOI
  62. Morris EP Török K 2001 Oligomeric structure of alpha-calmodulin-dependent protein kinase II Journal of Molecular Biology 308 1 8 10.1006/jmbi.2001.4584 11302701 · DOI
  63. Mukherji S Soderling TR 1994 Regulation of ca2+/calmodulin-dependent protein kinase II by inter- and intrasubunit-catalyzed autophosphorylations The Journal of Biological Chemistry 269 13744 13747 8188649
  64. Musacchio A 2015 Closing the mad2 cycle eLife 4 e13405 10.7554/eLife.08283 PMC4439612 25997937 · DOI
  65. Ogura T Iwasaki K Sato C 2003 Topology representing network enables highly accurate classification of protein images taken by cryo electron-microscope without masking Journal of Structural Biology 143 185 200 10.1016/j.jsb.2003.08.005 14572474 · DOI
  66. Pearson RB Wettenhall RE Means AR Hartshorne DJ Kemp BE 1988 Autoregulation of enzymes by pseudosubstrate prototopes: Myosin light chain kinase Science 241 970 973 10.1126/science.3406746 3406746 · DOI
  67. Páll S Abraham MJ Kutzner C Hess B Lindahl E 2015 Tackling Exascale Software Challenges in Molecular Dynamics Simulations with GROMACS Laure E Solving Software Challenges for Exascale Cham Springer International Publishing 3 27
  68. Rich RC Schulman H 1998 Substrate-directed function of calmodulin in autophosphorylation of ca2+/calmodulin-dependent protein kinase II The Journal of Biological Chemistry 273 28424 28429 10.1074/jbc.273.43.28424 9774470 · DOI · Paper page
  69. Rosenberg OS Deindl S Comolli LR Hoelz A Downing KH Nairn AC Kuriyan J 2006 Oligomerization states of the association domain and the holoenyzme of ca2+/cam kinase II The FEBS Journal 273 682 694 10.1111/j.1742-4658.2005.05088.x 16441656 · DOI
  70. Scheres SH Núñez-Ramírez R Sorzano CO Carazo JM Marabini R 2008 Image processing for electron microscopy single-particle analysis using XMIPP Nature Protocols 3 977 990 10.1038/nprot.2008.62 18536645 PMC2778070 · DOI
  71. Schworer CM Colbran RJ Keefer JR Soderling TR 1988 Ca2+/calmodulin-dependent protein kinase II. identification of a regulatory autophosphorylation site adjacent to the inhibitory and calmodulin-binding domains The Journal of Biological Chemistry 263 13486 13489 3417668
  72. Schworer CM Colbran RJ Soderling TR 1986 Reversible generation of a ca2+-independent form of ca2+(calmodulin)-dependent protein kinase II by an autophosphorylation mechanism The Journal of Biological Chemistry 261 8581 8584 3722161
  73. Selwood T Jaffe EK 2012 Dynamic dissociating homo-oligomers and the control of protein function Archives of Biochemistry and Biophysics 519 131 143 10.1016/j.abb.2011.11.020 22182754 PMC3298769 · DOI
  74. Sharon M Robinson CV 2007 The role of mass spectrometry in structure elucidation of dynamic protein complexes Annual Review of Biochemistry 76 167 193 10.1146/annurev.biochem.76.061005.090816 17328674 · DOI
  75. Silva AJ Paylor R Wehner JM Tonegawa S 1992 Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice Science 257 206 211 10.1126/science.1321493 1321493 · DOI
  76. Stewart M Kent HM McCoy AJ 1998 Structural basis for molecular recognition between nuclear transport factor 2 (NTF2) and the gdp-bound form of the ras-family gtpase ran Journal of Molecular Biology 277 635 646 10.1006/jmbi.1997.1602 9533885 · DOI
  77. Stratton M Lee IH Bhattacharyya M Christensen SM Chao LH Schulman H Groves JT Kuriyan J 2014 Activation-triggered subunit exchange between camkii holoenzymes facilitates the spread of kinase activity eLife 3 e13405 10.7554/eLife.01610 PMC3901001 24473075 · DOI · Paper page
  78. Stratton MM Chao LH Schulman H Kuriyan J 2013 Structural studies on the regulation of ca2+/calmodulin dependent protein kinase II Current Opinion in Structural Biology 23 292 301 10.1016/j.sbi.2013.04.002 23632248 PMC3788167 · DOI
  79. Suhre K Sanejouand YH 2004 Elnemo: A normal mode web server for protein movement analysis and the generation of templates for molecular replacement Nucleic Acids Research 32 W610 W614 10.1093/nar/gkh368 15215461 PMC441506 · DOI
  80. Suloway C Pulokas J Fellmann D Cheng A Guerra F Quispe J Stagg S Potter CS Carragher B 2005 Automated molecular microscopy: The new leginon system Journal of Structural Biology 151 41 60 10.1016/j.jsb.2005.03.010 15890530 · DOI
  81. Taylor SS Knighton DR Zheng J Ten Eyck LF Sowadski JM 1992 Structural framework for the protein kinase family Annual Review of Cell Biology 8 429 462 10.1146/annurev.cb.08.110192.002241 1335745 · DOI
  82. Thiel G Czernik AJ Gorelick F Nairn AC Greengard P 1988 Ca2+/calmodulin-dependent protein kinase II: Identification of threonine-286 as the autophosphorylation site in the alpha subunit associated with the generation of ca2+-independent activity Proceedings of the National Academy of Sciences of the United States of America 85 6337 6341 10.1073/pnas.85.17.6337 2842767 PMC281965 · DOI
  83. Tombes RM Faison MO Turbeville JM 2003 Organization and evolution of multifunctional ca(2+)/cam-dependent protein kinase genes Gene 322 17 31 10.1016/j.gene.2003.08.023 14644494 · DOI
  84. Tse JK Giannetti AM Bradshaw JM 2007 Thermodynamics of calmodulin trapping by ca2+/calmodulin-dependent protein kinase II: Subpicomolar kd determined using competition titration calorimetry Biochemistry 46 4017 4027 10.1021/bi700013y 17352496 · DOI
  85. van Heel M Harauz G Orlova EV Schmidt R Schatz M 1996 A new generation of the IMAGIC image processing system Journal of Structural Biology 116 17 24 10.1006/jsbi.1996.0004 8742718 · DOI
  86. Voss NR Yoshioka CK Radermacher M Potter CS Carragher B 2009 Dog picker and tiltpicker: Software tools to facilitate particle selection in single particle electron microscopy Journal of Structural Biology 166 205 213 10.1016/j.jsb.2009.01.004 19374019 PMC2768396 · DOI
  87. Waldmann R Hanson PI Schulman H 1990 Multifunctional ca2+/calmodulin-dependent protein kinase made ca2+ independent for functional studies Biochemistry 29 1679 1684 10.1021/bi00459a002 2158811 · DOI
  88. Wang ZX 1995 An exact mathematical expression for describing competitive binding of two different ligands to a protein molecule FEBS Letters 360 111 114 10.1016/0014-5793(95)00062-E 7875313 · DOI
  89. Waugh DS 2011 An overview of enzymatic reagents for the removal of affinity tags Protein Expression and Purification 80 283 293 10.1016/j.pep.2011.08.005 21871965 PMC3195948 · DOI
  90. Wayman GA Lee YS Tokumitsu H Silva AJ Silva A Soderling TR 2008 Calmodulin-kinases: Modulators of neuronal development and plasticity Neuron 59 914 931 10.1016/j.neuron.2008.08.021 18817731 PMC2664743 · DOI · Paper page
  91. Woodgett JR Davison MT Cohen P 1983 The calmodulin-dependent glycogen synthase kinase from rabbit skeletal muscle. purification, subunit structure and substrate specificity European Journal of Biochemistry / FEBS 136 481 487 10.1111/j.1432-1033.1983.tb07766.x 6315430 · DOI
  92. Wu ZR Ebrahimian S Zawrotny ME Thornburg LD Perez-Alvarado GC Brothers P Pollack RM Summers MF 1997 Solution structure of 3-oxo-delta5-steroid isomerase Science 276 415 418 10.1126/science.276.5311.415 9103200 · DOI
  93. Xu M Long C Chen X Huang C Chen S Zhu B 2010 Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly Science 328 94 98 10.1126/science.1178994 20360108 · DOI

Cited by

Sorted by citations

Authors
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., Gee, C. L., Barros, T., Schulman, H., Williams, E. R., & Kuriyan, J.
Affiliations
  • QB3 (US)
  • University of California, Berkeley (US)
  • Howard Hughes Medical Institute (US)
  • Allosteros Therapeutics, Sunnyvale, United States
Corresponding author
Kuriyan, John
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2016-03-07
Volume
5
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.13405
PMC
PMC4859805
OpenAlex
W2313905667
Cited by
112
References
13
Citations by year
2026: 4 · 2025: 11 · 2024: 16 · 2023: 10 · 2022: 12 · 2021: 11 · 2020: 15 · 2019: 12 · 2018: 12 · 2017: 5 · 2016: 4
FWCI
5.71
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Marine Biological Association (acceptedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • National Institutes of Health (R01GM101277, R01GM097357)
  • Human Frontier Science Program
  • Jane Coffin Childs Memorial Fund for Medical Research
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, subunit exchange, kinase activation, phosphorylation, intersubunit interface, learning and memory, cardiac function
MeSH terms
Humans, Models, Biological, Models, Molecular, Molecular Conformation, Protein Subunits, Calcium-Calmodulin-Dependent Protein Kinase Type 2, Protein Multimerization

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review