Roger J. Colbran, Ph.D.
Professor of Molecular Physiology and Biophysics
Vanderbilt University Medical Center
Nashville, TN 37232-0617
Structure, function and subcellular targeting of Ca2+/calmodulin-dependent protein kinase II in health and disease
Many hormones and neurotransmitters act on cell surface receptors to elevate cytosolic levels of soluble second messengers such as cyclic AMP and calcium. These molecules diffuse freely but the dynamics of second messenger generation and removal are such that their concentrations are only elevated locally and transiently. This spatial heterogeneity implies that cellular proteins that are sensitive to second messengers have discrete subcellular localization(s). The overall goal of this laboratory is to understand how localization of signal transduction molecules is achieved and how this impacts cellular regulation.
Multiple synaptic roles for calcium/calmodulin-dependent protein kinase II (CaMKII)
Neurons are highly asymmetric cells due to their extensive dendritic and axonal processes. Moreover, the dendrites are covered with thousands of dendritic spines that receive synaptic inputs from many different neurons. Each synapse can be independently modulated on time scales ranging from milliseconds to the lifetime of the animal. Of particular interest are long-term potentiation (LTP) and long-term depression (LTD) in the hippocampus, opposing forms of synaptic plasticity that are induced by calcium influx via NMDA-type glutamate receptors. High frequency stimulation of a synapse generally results in induction of LTP, where as low frequency stimulation induces LTD. Thus, calcium-dependent signaling molecules are able to generate different physiological responses depending on the frequency with which a synapse is stimulated. Furthermore, LTP and LTD are confined to synapse(s) that received the initial high or low frequency stimulation, respectively, without any “spill-over” to nearby unstimulated synapses. The major focus of this laboratory is to determine the molecular mechanisms that permit synapse specific generation of LTP or LTD. Calcium/calmodulin-dependent protein kinase II (CaMKII) plays a pivotal role in synaptic plasticity, learning and memory.
CaMKII as an integrator of diverse calcium signals
Dodecameric CaMKII holoenzymes require calcium and calmodulin for initial activation. Autophosphorylation at Thr286 converts the kinase to a form that has calcium/calmodulin-independent kinase activity, requiring a protein phosphatase to be inactivated. The activity of PP1γ1 targeted to the neuronal postsynaptic density by spinophilin and/or neurabin is believed to play a critical role in gating CaMKII autophosphorylation during synaptic plasticity. Thus, the opposing actions of calcium/calmodulin and protein phosphatases allow CaMKII to integrate information conveyed by the frequency, amplitude and duration of transient elevations of calcium that occur at synapses and induce LTP or LTD. In addition, it is very well established that Thr286 autophosphorylation is essential to normal synaptic plasticity, learning and memory.
Mechanisms of CaMKII Targeting
Our central hypothesis is that specific synaptic actions of CaMKII require the assembly of specific multiprotein complexes containing CaMKII and downstream mediators of individual signaling pathways, and are opposed by specific PP1 complexes. We are investigating several synaptic proteins that dynamically interact with CaMKII or PP1 by distinct biochemical mechanisms, including subunits of NMDA-type glutamate receptors and voltage-gated calcium channels, densin-180, alpha-actinin, spinophilin and neurabin, as well as some novel interactions. Our goal is to understand the biochemical/structural basis for these interactions and use this information to help us identify specific roles for these interactions in controlling synaptic function both physiologically (e.g., LTP/LTD) and pathologically (e.g., in Parkinson's Disease). These studies employ a diverse array of biochemical, molecular and cell biological, immunological, proteomic, fluorescent imaging and electrophysiological techniques.
- Baucum, AJ, Strack, S, Colbran, RJ Age-dependent targeting of protein phosphatase 1 to Ca2+/calmodulin-dependent protein kinase II by spinophilin in mouse striatum. PLoS One, 7(2), e31554, 2012.
- Baucum, AJ, Brown, AM, Colbran, RJ Differential association of postsynaptic signaling protein complexes in striatum and hippocampus. J Neurochem, 2012.
- Klug, JR, Mathur, BN, Kash, TL, Wang, HD, Matthews, RT, Robison, AJ, Anderson, ME, Deutch, AY, Lovinger, DM, Colbran, RJ, Winder, DG Genetic Inhibition of CaMKII in Dorsal Striatal Medium Spiny Neurons Reduces Functional Excitatory Synapses and Enhances Intrinsic Excitability. PLoS One, 7(9), e45323, 2012.
- Wills, TA, Klug, JR, Silberman, Y, Baucum, AJ, Weitlauf, C, Colbran, RJ, Delpire, E, Winder, DG GluN2B subunit deletion reveals key role in acute and chronic ethanol sensitivity of glutamate synapses in bed nucleus of the stria terminalis. Proc Natl Acad Sci U S A, 109(5), E278-87, 2012.
- Jalan-Sakrikar, N, Bartlett, RK, Baucum, AJ, Colbran, RJ Substrate-selective and calcium-independent activation of CaMKII by ¿¿-actinin. J Biol Chem, 287(19), 15275-83, 2012.
- Jiao, Y, Jalan-Sakrikar, N, Robison, AJ, Baucum, AJ, Bass, MA, Colbran, RJ Characterization of a central Ca2+/calmodulin-dependent protein kinase IIalpha/beta binding domain in densin that selectively modulates glutamate receptor subunit phosphorylation. J Biol Chem, 286(28), 24806-18, 2011.
- Hoffman, L, Stein, RA, Colbran, RJ, McHaourab, HS Conformational changes underlying calcium/calmodulin-dependent protein kinase II activation. EMBO J, 2011.
- Gustin, RM, Shonesy, BC, Robinson, SL, Rentz, TJ, Baucum, AJ, Jalan-Sakrikar, N, Winder, DG, Stanwood, GD, Colbran, RJ Loss of Thr286 phosphorylation disrupts synaptic CaMKII¿¿ targeting, NMDAR activity and behavior in pre-adolescent mice. Mol Cell Neurosci, 47(4), 286-92, 2011.
- Jenkins, MA, Christel, CJ, Jiao, Y, Abiria, S, Kim, KY, Usachev, YM, Obermair, GJ, Colbran, RJ, Lee, A Ca2+-dependent facilitation of Cav1.3 Ca2+ channels by densin and Ca2+/calmodulin-dependent protein kinase II. J Neurosci, 30(15), 5125-35, 2010.
- Nikandrova, YA, Jiao, Y, Baucum, AJ, Tavalin, SJ, Colbran, RJ Ca2+/calmodulin-dependent protein kinase II binds to and phosphorylates a specific SAP97 splice variant to disrupt association with AKAP79/150 and modulate alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-type glutamate receptor (AMPAR) activity. J Biol Chem, 285(2), 923-34, 2010.
- Abiria, SA, Colbran, RJ CaMKII associates with CaV1.2 L-type calcium channels via selected beta subunits to enhance regulatory phosphorylation. J Neurochem, 112(1), 150-61, 2010.
- Koval, OM, Guan, X, Wu, Y, Joiner, ML, Gao, Z, Chen, B, Grumbach, IM, Luczak, ED, Colbran, RJ, Song, LS, Hund, TJ, Mohler, PJ, Anderson, ME CaV1.2 beta-subunit coordinates CaMKII-triggered cardiomyocyte death and afterdepolarizations. Proc Natl Acad Sci U S A, 107(11), 4996-5000, 2010.
- Bowton, E, Saunders, C, Erreger, K, Sakrikar, D, Matthies, HJ, Sen, N, Jessen, T, Colbran, RJ, Caron, MG, Javitch, JA, Blakely, RD, Galli, A Dysregulation of dopamine transporters via dopamine D2 autoreceptors triggers anomalous dopamine efflux associated with attention-deficit hyperactivity disorder. J Neurosci, 30(17), 6048-57, 2010.
- Baucum, AJ, Jalan-Sakrikar, N, Jiao, Y, Gustin, RM, Carmody, LC, Tabb, DL, Ham, AJ, Colbran, RJ Identification and validation of novel spinophilin-associated proteins in rodent striatum using an enhanced ex vivo shotgun proteomics approach. Mol Cell Proteomics, 9(6), 1243-59, 2010.
- Brigman, JL, Wright, T, Talani, G, Prasad-Mulcare, S, Jinde, S, Seabold, GK, Mathur, P, Davis, MI, Bock, R, Gustin, RM, Colbran, RJ, Alvarez, VA, Nakazawa, K, Delpire, E, Lovinger, DM, Holmes, A Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning. J Neurosci, 30(13), 4590-600, 2010.
- Gustin, RM, Bichell, TJ, Bubser, M, Daily, J, Filonova, I, Mrelashvili, D, Deutch, AY, Colbran, RJ, Weeber, EJ, Haas, KF Tissue-specific variation of Ube3a protein expression in rodents and in a mouse model of Angelman syndrome. Neurobiol Dis, 39(3), 283-91, 2010.
- Kash, TL, Baucum, AJ, Conrad, KL, Colbran, RJ, Winder, DG Alcohol exposure alters NMDAR function in the bed nucleus of the stria terminalis. Neuropsychopharmacology, 34(11), 2420-9, 2009.
- Neely, MD, Robert, EM, Baucum, AJ, Colbran, RJ, Muly, EC, Deutch, AY Localization of myocyte enhancer factor 2 in the rodent forebrain: regionally-specific cytoplasmic expression of MEF2A. Brain Res, 127455-65, 2009.
- 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 A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell, 133(3), 462-74, 2008.
- Brown, AM, Baucum, AJ, Bass, MA, Colbran, RJ Association of protein phosphatase 1 gamma 1 with spinophilin suppresses phosphatase activity in a Parkinson disease model. J Biol Chem, 283(21), 14286-94, 2008.
- Colbran, RJ "CaMKII: Mechanisms of a prototypical memory molecule." In J. David Sweatt (Ed.), Molecular Mechanisms of Memory. Vol.  of Learning and Memory: A Comprehensive Reference, 4 vols. (J.Byrne Editor), pp. 469-488, 2008.
- Khoo, MS, Grueter, CE, Eren, M, Yang, J, Zhang, R, Bass, MA, Lwin, ST, Mendes, LA, Vaughan, DE, Colbran, RJ, Anderson, ME Calmodulin kinase II inhibition disrupts cardiomyopathic effects of enhanced green fluorescent protein. J Mol Cell Cardiol, 44(2), 405-10, 2008.
- Jiao, Y, Robison, AJ, Bass, MA, Colbran, RJ Developmentally regulated alternative splicing of densin modulates protein-protein interaction and subcellular localization. J Neurochem, 105(5), 1746-60, 2008.
- Grueter, CE, Abiria, SA, Wu, Y, Anderson, ME, Colbran, RJ Differential regulated interactions of calcium/calmodulin-dependent protein kinase II with isoforms of voltage-gated calcium channel beta subunits. Biochemistry, 47(6), 1760-7, 2008.
- Carmody, LC, Baucum, AJ, Bass, MA, Colbran, RJ Selective targeting of the gamma1 isoform of protein phosphatase 1 to F-actin in intact cells requires multiple domains in spinophilin and neurabin. FASEB J, 22(6), 1660-71, 2008.
- Binda, F, Dipace, C, Bowton, E, Doughty, SE, Lute, BJ, Fog, JU, Zhang, M, Sen, N, Colbran, RJ, Gnegy, ME, Gether, U, Javitch, JA, Erreger, K, Galli, A Syntaxin1A Interaction with the Dopamine Transporter Promotes Amphetamine-Induced Dopamine Efflux. Mol Pharmacol, 2008.
- Grueter, CE, Colbran, RJ, Anderson, ME CaMKII, an emerging molecular driver for calcium homeostasis, arrhythmias, and cardiac dysfunction. J Mol Med, 85(1), 5-14, 2007.
- Robison, AJ, Winder, DG, Colbran, RJ, Bartlett, RK Oxidation of calmodulin alters activation and regulation of CaMKII. Biochem Biophys Res Commun, 35697-101, 2007.
- Deutch, AY, Colbran, RJ, Winder, DJ Striatal plasticity and medium spiny neuron dendritic remodeling in parkinsonism. Parkinsonism Relat Disord, 13 Suppl 3S251-8, 2007.
- Fog, JU, Khoshbouei, H, Holy, M, Owens, WA, Vaegter, CB, Sen, N, Nikandrova, Y, Bowton, E, McMahon, DG, Colbran, RJ, Daws, LC, Sitte, HH, Javitch, JA, Galli, A, Gether, U Calmodulin kinase II interacts with the dopamine transporter C terminus to regulate amphetamine-induced reverse transport. Neuron, 51(4), 417-29, 2006.
- Khoo, MS, Li, J, Singh, MV, Yang, Y, Kannankeril, P, Wu, Y, Grueter, CE, Guan, X, Oddis, CV, Zhang, R, Mendes, L, Ni, G, Madu, EC, Yang, J, Bass, M, Gomez, RJ, Wadzinski, BE, Olson, EN, Colbran, RJ, Anderson, ME Death, cardiac dysfunction, and arrhythmias are increased by calmodulin kinase II in calcineurin cardiomyopathy. Circulation, 114(13), 1352-9, 2006.
- Grueter, CE, Abiria, SA, Dzhura, I, Wu, Y, Ham, AJ, Mohler, PJ, Anderson, ME, Colbran, RJ L-type Ca2+ channel facilitation mediated by phosphorylation of the beta subunit by CaMKII. Mol Cell, 23(5), 641-50, 2006.
- Yao, J, Davies, LA, Howard, JD, Adney, SK, Welsby, PJ, Howell, N, Carey, RM, Colbran, RJ, Barrett, PQ Molecular basis for the modulation of native T-type Ca2+ channels in vivo by Ca2+/calmodulin-dependent protein kinase II. J Clin Invest, 116(9), 2403-12, 2006.
- Zhang, R, Dzhura, I, Grueter, CE, Thiel, W, Colbran, RJ, Anderson, ME A dynamic alpha-beta inter-subunit agonist signaling complex is a novel feedback mechanism for regulating L-type Ca2+ channel opening. FASEB J, 19(11), 1573-5, 2005.
- Norman ED, Egli RE, Colbran RJ, Winder DG A potassium channel blocker induces a long-lasting enhancement of corticostriatal responses. Neuropharmacology, 48(2), 311-21, 2005.
- Sessoms-Sikes, Suzanne, Honse, Yumiko, Lovinger, David M, Colbran, Roger J CaMKIIalpha enhances the desensitization of NR2B-containing NMDA receptors by an autophosphorylation-dependent mechanism. Mol Cell Neurosci, 29(1), 139-47, 2005.
- Zhang, Rong, Khoo, Michelle S C, Wu, Yuejin, Yang, Yingbo, Grueter, Chad E, Ni, Gemin, Price, Edward E, Thiel, William, Guatimosim, Silvia, Song, Long-Sheng, Madu, Ernest C, Shah, Anisha N, Vishnivetskaya, Tatiana A, Atkinson, James B, Gurevich, Vsevolod V, Salama, Guy, Lederer, W J, Colbran, Roger J, Anderson, Mark E Calmodulin kinase II inhibition protects against structural heart disease. Nat Med, 11(4), 409-17, 2005.
- Robison, AJ, Bartlett, RK, Bass, MA, Colbran, RJ Differential modulation of Ca2+/calmodulin-dependent protein kinase II activity by regulated interactions with N-methyl-D-aspartate receptor NR2B subunits and alpha-actinin. J Biol Chem, 280(47), 39316-23, 2005.
- Brown, Abigail M, Deutch, Ariel Y, Colbran, Roger J Dopamine depletion alters phosphorylation of striatal proteins in a model of Parkinsonism. Eur J Neurosci, 22(1), 247-56, 2005.
- Robison, AJ, Bass, MA, Jiao, Y, MacMillan, LB, Carmody, LC, Bartlett, RK, Colbran, RJ Multivalent interactions of calcium/calmodulin-dependent protein kinase II with the postsynaptic density proteins NR2B, densin-180, and alpha-actinin-2. J Biol Chem, 280(42), 35329-36, 2005.
- Carmody LC, Bauman PA, Bass MA, Mavila N, DePaoli-Roach AA, Colbran RJ A protein phosphatase-1gamma1 isoform selectivity determinant in dendritic spine-associated neurabin. J Biol Chem, 279(21), 21714-23, 2004.
- Colbran RJ, Brown AM Calcium/calmodulin-dependent protein kinase II and synaptic plasticity. Curr Opin Neurobiol, 14(3), 318-27, 2004.
- Wu Y, Kimbrough JT, Colbran RJ, Anderson ME Calmodulin kinase is functionally targeted to the action potential plateau for regulation of L-type Ca2+ current in rabbit cardiomyocytes. J Physiol, 554(Pt 1), 145-55, 2004.
- Colbran, RJ Protein phosphatases and calcium/calmodulin-dependent protein kinase II-dependent synaptic plasticity. J Neurosci, 24(39), 8404-9, 2004.
- Colbran, RJ Targeting of calcium/calmodulin-dependent protein kinase II. Biochem J, 378(Pt 1), 1-16, 2004.
- Welsby PJ, Wang H, Wolfe JT, Colbran RJ, Johnson ML, Barrett PQ A mechanism for the direct regulation of T-type calcium channels by Ca2+/calmodulin-dependent kinase II. J Neurosci, 23(31), 10116-21, 2003.
- Colbran RJ, Carmody LC, Bauman PA, Wadzinski BE, Bass MA Analysis of specific interactions of native protein phosphatase 1 isoforms with targeting subunits. Methods Enzymol, 366156-75, 2003.
- Dzhura I, Wu Y, Zhang R, Colbran RJ, Hamilton SL, Anderson ME C terminus L-type Ca2+ channel calmodulin-binding domains are auto-agonist ligands in rabbit ventricular myocytes. J Physiol, 550(Pt 3), 731-8, 2003.
- Brady AE, Wang Q, Colbran RJ, Allen PB, Greengard P, Limbird LE Spinophilin stabilizes cell surface expression of alpha 2B-adrenergic receptors. J Biol Chem, 278(34), 32405-12, 2003.
- Wu Y, Temple J, Zhang R, Dzhura I, Zhang W, Trimble R, Roden DM, Passier R, Olson EN, Colbran RJ, Anderson ME Calmodulin kinase II and arrhythmias in a mouse model of cardiac hypertrophy. Circulation, 106(10), 1288-93, 2002.
- Dzhura I, Wu Y, Colbran RJ, Corbin JD, Balser JR, Anderson ME Cytoskeletal disrupting agents prevent calmodulin kinase, IQ domain and voltage-dependent facilitation of L-type Ca2+ channels. J Physiol, 545(Pt 2), 399-406, 2002.
- Richman JG, Brady AE, Wang Q, Hensel JL, Colbran RJ, Limbird LE Agonist-regulated Interaction between alpha2-adrenergic receptors and spinophilin. J Biol Chem, 276(18), 15003-8, 2001.
- Wu Y, Dzhura I, Colbran RJ, Anderson ME Calmodulin kinase and a calmodulin-binding IQ domain facilitate L-type Ca2+ current in rabbit ventricular myocytes by a common mechanism.. J Physiol, 535(Pt 3), 679-87, 2001.
- Wu Y, Colbran RJ, Anderson ME Calmodulin kinase is a molecular switch for cardiac excitation-contraction coupling.. Proc Natl Acad Sci U S A, 98(5), 2877-81, 2001.
- Chen HX, Otmakhov N, Strack S, Colbran RJ, Lisman JE Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP?. J Neurophysiol, 85(4), 1368-76, 2001.
- Strack S, Robison AJ, Bass MA, Colbran RJ Association of calcium/calmodulin-dependent kinase II with developmentally regulated splice variants of the postsynaptic density protein densin-180. J Biol Chem, 275(33), 25061-4, 2000.
- Dzhura I, Wu Y, Colbran RJ, Balser JR, Anderson ME Calmodulin kinase determines calcium-dependent facilitation of L-type calcium channels. Nat Cell Biol, 2(3), 173-7, 2000.
- Strack S, McNeill RB, Colbran RJ Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B subunit of the N-methyl-D-aspartate receptor. J Biol Chem, 275(31), 23798-806, 2000.
- Barrett PQ, Lu HK, Colbran R, Czernik A, Pancrazio JJ Stimulation of unitary T-type Ca(2+) channel currents by calmodulin-dependent protein kinase II. Am J Physiol Cell Physiol, 279(6), C1694-703, 2000.
- MacMillan LB, Bass MA, Cheng N, Howard EF, Tamura M, Strack S, Wadzinski BE, Colbran RJ Brain actin-associated protein phosphatase 1 holoenzymes containing spinophilin, neurabin, and selected catalytic subunit isoforms. J Biol Chem, 274(50), 35845-54, 1999.
- Wu Y, MacMillan LB, McNeill RB, Colbran RJ, Anderson ME CaM kinase augments cardiac L-type Ca2+ current: a cellular mechanism for long Q-T arrhythmias. Am J Physiol, 276(6 Pt 2), H2168-78, 1999.
- Strack S, Chang D, Zaucha JA, Colbran RJ, Wadzinski BE Cloning and characterization of B delta, a novel regulatory subunit of protein phosphatase 2A. FEBS Lett, 460(3), 462-6, 1999.
- Strack S, Kini S, Ebner FF, Wadzinski BE, Colbran RJ Differential cellular and subcellular localization of protein phosphatase 1 isoforms in brain. J Comp Neurol, 413(3), 373-84, 1999.
- Strack S, Colbran RJ Autophosphorylation-dependent targeting of calcium/ calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl- D-aspartate receptor. J Biol Chem, 273(33), 20689-92, 1998.
- Strack S, Zaucha JA, Ebner FF, Colbran RJ, Wadzinski BE Brain protein phosphatase 2A: developmental regulation and distinct cellular and subcellular localization by B subunits. J Comp Neurol, 392(4), 515-27, 1998.
- Colbran RJ, Bass MA, McNeill RB, Bollen M, Zhao S, Wadzinski BE, Strack S Association of brain protein phosphatase 1 with cytoskeletal targeting/regulatory subunits. J Neurochem, 69(3), 920-9, 1997.
- Strack S, Barban MA, Wadzinski BE, Colbran RJ Differential inactivation of postsynaptic density-associated and soluble Ca2+/calmodulin-dependent protein kinase II by protein phosphatases 1 and 2A. J Neurochem, 68(5), 2119-28, 1997.
- Strack, S, Westphal, RS, Colbran, RJ, Ebner, FF, Wadzinski, BE Protein serine/threonine phosphatase 1 and 2A associate with and dephosphorylate neurofilaments. Brain Res Mol Brain Res, 49(1-2), 15-28, 1997.
- Strack, S, Choi, S, Lovinger, DM, Colbran, RJ Translocation of autophosphorylated calcium/calmodulin-dependent protein kinase II to the postsynaptic density. J Biol Chem, 272(21), 13467-70, 1997.
- McNeill RB, Colbran RJ Interaction of autophosphorylated Ca2+/calmodulin-dependent protein kinase II with neuronal cytoskeletal proteins. Characterization of binding to a 190-kDa postsynaptic density protein. J Biol Chem, 270(17), 10043-9, 1995.
- Colbran, RJ Inactivation of Ca2+/calmodulin-dependent protein kinase II by basal autophosphorylation. J Biol Chem, 268(10), 7163-70, 1993.
- Smith, MK, Colbran, RJ, Brickey, DA, Soderling, TR Functional determinants in the autoinhibitory domain of calcium/calmodulin-dependent protein kinase II. Role of His282 and multiple basic residues. J Biol Chem, 267(3), 1761-8, 1992.
- Colbran, RJ Regulation and role of brain calcium/calmodulin-dependent protein kinase II. Neurochem Int, 21(4), 469-97, 1992.
- Soderling, TR, Fukunaga, K, Brickey, DA, Fong, YL, Rich, DP, Smith, K, Colbran, RJ Molecular and cellular studies on brain calcium/calmodulin-dependent protein kinase II. Prog Brain Res, 89169-83, 1991.
- Colbran, RJ, Soderling, TR Calcium/calmodulin-dependent protein kinase II. Curr Top Cell Regul, 31181-221, 1990.
- Colbran, RJ, Soderling, TR Calcium/calmodulin-independent autophosphorylation sites of calcium/calmodulin-dependent protein kinase II. Studies on the effect of phosphorylation of threonine 305/306 and serine 314 on calmodulin binding using synthetic peptides. J Biol Chem, 265(19), 11213-9, 1990.
- Brickey, DA, Colbran, RJ, Fong, YL, Soderling, TR Expression and characterization of the alpha-subunit of Ca2+/calmodulin-dependent protein kinase II using the baculovirus expression system. Biochem Biophys Res Commun, 173(2), 578-84, 1990.
- Rich, DP, Schworer, CM, Colbran, RJ Soderling, TR "Proteolytic activation of calcium/calmodulin dependent protein kinase II: Putative function in synaptic plasticity." Mol. Cell. Neurosci., 1107-116, 1990.
- Soderling, TR, Fukunaga, K, Rich, DP, Fong, YL, Smith, K, Colbran, RJ Regulation of brain Ca2+/calmodulin-dependent protein kinase II. Adv Second Messenger Phosphoprotein Res, 24206-11, 1990.
- Smith, MK, Colbran, RJ, Soderling, TR Specificities of autoinhibitory domain peptides for four protein kinases. Implications for intact cell studies of protein kinase function. J Biol Chem, 265(4), 1837-40, 1990.
- Colbran, RJ, Schworer, CM, Hashimoto, Y, Fong, YL, Rich, DP, Smith, MK, Soderling, TR Calcium/calmodulin-dependent protein kinase II. Biochem J, 258(2), 313-25, 1989.
- Garton, AJ, Campbell, DG, Carling, D, Hardie, DG, Colbran, RJ, Yeaman, SJ Phosphorylation of bovine hormone-sensitive lipase by the AMP-activated protein kinase. A possible antilipolytic mechanism. Eur J Biochem, 179(1), 249-54, 1989.
- Colbran, RJ, Smith, MK, Schworer, CM, Fong, YL, Soderling, TR Regulatory domain of calcium/calmodulin-dependent protein kinase II. Mechanism of inhibition and regulation by phosphorylation. J Biol Chem, 264(9), 4800-4, 1989.
- Rich, DP, Colbran, RJ, Schworer, CM, Soderling, TR Regulatory properties of calcium/calmodulin-dependent protein kinase II in rat brain postsynaptic densities. J Neurochem, 53(3), 807-16, 1989.
- Schworer, CM, Colbran, RJ, Keefer, JR, Soderling, TR Ca2+/calmodulin-dependent protein kinase II. Identification of a regulatory autophosphorylation site adjacent to the inhibitory and calmodulin-binding domains. J Biol Chem, 263(27), 13486-9, 1988.
- Payne, ME, Fong, YL, Ono, T, Colbran, RJ, Kemp, BE, Soderling, TR, Means, AR Calcium/calmodulin-dependent protein kinase II. Characterization of distinct calmodulin binding and inhibitory domains. J Biol Chem, 263(15), 7190-5, 1988.
- Colbran, RJ, Fong, YL, Schworer, CM, Soderling, TR Regulatory interactions of the calmodulin-binding, inhibitory, and autophosphorylation domains of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem, 263(34), 18145-51, 1988.
- Hashimoto, Y, Schworer, CM, Colbran, RJ, Soderling, TR Autophosphorylation of Ca2+/calmodulin-dependent protein kinase II. Effects on total and Ca2+-independent activities and kinetic parameters. J Biol Chem, 262(17), 8051-5, 1987.
- Cordle, SR, Colbran, RJ, Yeaman, SJ Hormone-sensitive lipase from bovine adipose tissue. Biochim Biophys Acta, 887(1), 51-7, 1986.
- Colbran, RJ, Garton, AJ, Cordle, SR, Yeaman, SJ Regulation of cholesterol ester hydrolase by cyclic AMP-dependent protein kinase. FEBS Lett, 201(2), 257-61, 1986.
- Schworer, CM, Colbran, RJ, Soderling, TR Reversible generation of a Ca2+-independent form of Ca2+(calmodulin)-dependent protein kinase II by an autophosphorylation mechanism. J Biol Chem, 261(19), 8581-4, 1986.
- Cook, KG, Colbran, RJ, Snee, J, Yeaman, SJ Cytosolic cholesterol ester hydrolase from bovine corpus luteum. Its purification, identification, and relationship to hormone-sensitive lipase. Biochim Biophys Acta, 752(1), 46-53, 1983.