αcaMKII autophosphorylation controls exploratory activity to threatening novel stimuli

Neuropharmacology

Volumn 61, Issue 8, 2011, Pages 1424-1431

  Easton, Alanna C ^a   Lucchesi, Walter ^a   Schumann, Gunter ^a   Peter Giese, K ^a   Müller, Christian P ^a,b   Fernandes, Cathy ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

AlphaCaMKII; Anxiety; Autophosphorylation; Hyperlocomotion; Novelty; Threat

Indexed keywords

ALPHA CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; FEMALE; GENOTYPE; HETEROZYGOTE; HOMOZYGOTE; HYPERACTIVITY; LIGHT DARK CYCLE; LOCOMOTION; MALE; MOUSE; MUTANT; NONHUMAN; OPEN FIELD TEST; PHENOTYPE; PRIORITY JOURNAL; STIMULUS RESPONSE; THREAT; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; DARK ADAPTATION; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEAR; FEMALE; LOCOMOTION; MALE; MAZE LEARNING; MICE; MICE, TRANSGENIC; MUTATION; PHOSPHORYLATION;

EID: 80053588698     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.08.036     Document Type: Article

References (61)

1. R. Adamec Transmitter systems involved in neural plasticity underlying increased anxiety and defense-implications for understanding anxiety following traumatic stress Neurosci. Biobehav. Rev. 21 1997 755 765 (Pubitemid 27524770)
2. R.L. Albin, R.L. Makowiec, Z. Hollingsworth, L.S.T. Dure, J.B. Penney, and A.B. Young Excitatory amino acid binding sites in the periaqueductal gray of the rat Neurosci. Lett. 118 1990 112 115 (Pubitemid 20337018)
3. K. Amunts, O. Kedo, M. Kindler, P. Pieperhoff, H. Mohlberg, N.J. Shah, U. Habel, F. Schneider, and K. Zilles Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps Anat. Embryol. (Berl.) 210 2005 343 352 (Pubitemid 41754499)
4. J.L. Armony, and J.E. LeDoux How the brain processes emotional information Ann. N.Y. Acad. Sci. 821 1997 259 270 (Pubitemid 27343027)
5. R. Bandler, A. Depaulis, and M. Vergnes Identification of midbrain neurones mediating defensive behavior in the rat by microinjections of excitatory amino acids Behav. Brain Res. 15 1985 107 119 (Pubitemid 15090331)
6. R. Bandler, and P. Carrive Integrated defense reaction elicited by excitatory amino acid microinjection in the midbrain periaqueductal grey region of the unrestrained cat Brain Res. 439 1988 95 106 (Pubitemid 18067510)
7. A. Barria, D. Muller, V. Derkach, L.C. Griffith, and T.R. Soderling Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation Science 276 1997 2042 2045 (Pubitemid 27443609)
8. R.J. Blanchard, and D.C. Blanchard Attack and defense in rodents as ethoexperimental models for the study of emotion Prog. Neuropsychopharmacol. Biol. Psychiatry 13 1989 S3 14
9. R.K. Butler, A.C. Sharko, E.M. Oliver, P. Brito-Vargas, K.F. Kaigler, J.R. Fadel, and M.A. Wilson Activation of phenotypically-distinct neuronal subpopulations of the rat amygdala following exposure to predator odor Neuroscience 175 2011 133 144
10. K. Carlsson, K.M. Petersson, D. Lundqvist, A. Karlsson, M. Ingvar, and A. Ohman Fear and the amygdala: manipulation of awareness generates differential cerebral responses to phobic and fear-relevant (but nonfeared) stimuli Emotion 4 2004 340 353 (Pubitemid 39525114)
11. A.P. Carobrez, J.E. Krieger, J.C. De Aguiar, and F.G. Graeff Antagonism by l-glutamic acid diethyl ester (GDEE) of the defense reaction caused by microinjection of glutamate into the dorsal periacqueductal gray-matter of the rat Braz. J. Med. Biol. Res. 18 1985 A656
12. O.M. Carvalho, A.J. Silva, and B.W. Balleine Evidence of selective learning deficits on tests of Pavlovian and instrumental conditioning in α-CaMKIIT286A mutant mice Int. J. Comp. Psychol. 14 2001 161 174
13. C. Chen, D.G. Rainnie, R.W. Greene, and S. Tonegawa Abnormal fear response and aggressive behavior in mutant mice deficient for alpha-calcium-calmodulin kinase II Science 266 1994 291 294 (Pubitemid 24343517)
14. R.J. Colbran, and A.M. Brown Calcium/calmodulin-dependent protein kinase II and synaptic plasticity Curr. Opin. Neurobiol. 14 2004 318 327 (Pubitemid 38759862)
15. J. Crawley, and F.K. Goodwin Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines Pharmacol. Biochem. Behav. 13 1980 167 170 (Pubitemid 11225713)
16. W.E. Crusio, D. Goldowitz, A. Holmes, and D. Wolfer Standards for the publication of mouse mutant studies Genes Brain Behav. 8 2009 1 4
17. V. de Paula Soares, and H. Zangrossi Jr. Stimulation of 5-HT1A or 5-HT2A receptors in the ventrolateral periaqueductal gray causes anxiolytic-, but not panicolytic-like effect in rats Behav. Brain Res. 197 2009 178 185
18. E. Dere, J.P. Huston, and M.A. De Souza Silva The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents Neurosci. Biobehav. Rev. 31 2007 673 704 (Pubitemid 46670336)
19. V. Derkach, A. Barria, and T.R. Soderling Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionate type glutamate receptors Proc. Natl. Acad. Sci. U.S.A. 96 1999 3269 3274 (Pubitemid 29148880)
20. J.A. Esteban AMPA receptor trafficking: a road map for synaptic plasticity Mol. Interv. 3 2003 375 385
21. C. Ferreira-Netto, K.G. Borelli, and M.L. Brandao Neural segregation of Fos-protein distribution in the brain following freezing and escape behaviors induced by injections of either glutamate or NMDA into the dorsal periaqueductal gray of rats Brain Res. 1031 2005 151 163 (Pubitemid 40093068)
22. K. Fukunaga, L. Stoppini, E. Miyamoto, and D. Muller Long-term potentiation is associated with an increased activity of Ca2+/calmodulin- dependent protein kinase II J. Biol. Chem. 268 1993 7863 7867 (Pubitemid 23120362)
23. J. Garzón, M. Rodriguez-Munoz, and P. Sanchez-Blazquez Do pharmacological approaches that prevent opioid tolerance target different elements in the same regulatory machinery? Curr. Drug Abuse Rev. 1 2008 222 238
24. K.P. Giese, N.B. Fedorov, R.K. Filipkowski, and A.J. Silva Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning Science 279 1998 870 873 (Pubitemid 28106282)
25. F.G. Graeff Minor tranquilizers and brain defense systems Braz. J. Med. Biol. Res. 14 1981 239 265 (Pubitemid 12106975)
26. J. Gray, and N. McNaughton The Neuropsychology of Anxiety second ed. 2000 Oxford University Press Oxford
27. C.S. Hall Drive and emotionality: factors associated with adjustment in the rat J. Comp. Psychol. 17 1921 89 108
28. S. Hasegawa, T. Furuichi, T. Yoshida, K. Endoh, K. Kato, M. Sado, R. Maeda, A. Kitamoto, T. Miyao, R. Suzuki, S. Homma, S. Masushige, Y. Kajii, and S. Kida Transgenic up-regulation of alpha-CaMKII in forebrain leads to increased anxiety-like behaviors and aggression Mol. Brain 2 2009 6
29. Y. Hayashi, A. Ishida, H. Katagiri, M. Mishina, H. Fujisawa, T. Manabe, and T. Takahashi Calcium- and calmodulin-dependent phosphorylation of AMPA type glutamate receptor subunits by endogenous protein kinases in the post-synaptic density Brain Res. Mol. Brain Res. 46 1997 338 342 (Pubitemid 27214383)
30. E.E. Irvine, J. Vernon, and K.P. Giese AlphaCaMKII autophosphorylation contributes to rapid learning but is not necessary for memory Nat. Neurosci. 8 2005 411 412 (Pubitemid 41007554)
31. E.E. Irvine, L.S. von Hertzen, F. Plattner, and K.P. Giese alphaCaMKII autophosphorylation: a fast track to memory Trends Neurosci. 29 2006 459 465 (Pubitemid 44118444)
32. F. Jenck, J.L. Moreau, and J.R. Martin Dorsal periaqueductal gray-induced aversion as a simulation of panic anxiety: elements of face and predictive validity Psychiatry Res. 57 1995 181 191
33. J.E. LeDoux Emotion: clues from the brain Ann. Rev. Psycho. 46 1995 209 235
34. I. Lengyel, K. Voss, M. Cammarota, K. Bradshaw, V. Brent, K.P. Murphy, K.P. Giese, J.A. Rostas, and T.V. Bliss Autonomous activity of CaMKII is only transiently increased following the induction of long-term potentiation in the rat hippocampus Eur. J. Neurosci. 20 2004 3063 3072 (Pubitemid 40007301)
35. L.W. Lim, A. Blokland, V. Visser-Vandewalle, R. Vlamings, T. Sesia, H. Steinbusch, K. Schruers, E. Griez, and Y. Temel High-frequency stimulation of the dorsolateral periaqueductal gray and ventromedial hypothalamus fails to inhibit panic-like behavior Behav. Brain Res. 193 2008 197 203
36. R.G. Lister The use of a plus-maze to measure anxiety in the mouse Psychopharmacology (Berl.) 92 1987 180 185 (Pubitemid 17072893)
37. L. Lo Iacono, and C. Gross Alpha-Ca2+/calmodulin-dependent protein kinase II contributes to the developmental programming of anxiety in serotonin receptor 1A knock-out mice J. Neurosci. 28 2008 6250 6257
38. T.A. Lovick Panic disorder-A malfunction of multiple transmitter control systems within the midbrain periaqueductal gray matter? Neuroscientist 6 2000 48 59 (Pubitemid 30140107)
39. S. Maren Neuroscience. The threatened brain Science 317 2007 1043 1044
40. A.J. McDonald, J.F. Muller, and F. Mascagni GABAergic innervation of alpha type II calcium/calmodulin-dependent protein kinase immunoreactive pyramidal neurons in the rat basolateral amygdala J. Comp. Neurol. 446 2002 199 218 (Pubitemid 34246040)
41. J. Mill, M.J. Galsworthy, J.L. Paya-Cano, F. Sluyter, L.C. Schalkwyk, R. Plomin, and P. Asherson Home-cage activity in heterogeneous stock (HS) mice as a model of baseline activity Genes Brain Behav. 1 2002 166 173 (Pubitemid 36717674)
42. S.G. Miller, and M.B. Kennedy Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch Cell 44 1986 861 870 (Pubitemid 16045332)
43. V.M. Moers-Hornikx, J.S. Vles, L.W. Lim, M. Ayyildiz, S. Kaplan, A.W. Gavilanes, G. Hoogland, H.W. Steinbusch, and Y. Temel Periaqueductal grey stimulation induced panic-like behavior is accompanied by deactivation of the deep cerebellar nuclei Cerebellum 10 2011 61 69
44. M.L. Molchanov, and F.S. Guimarães Defense reaction induced by a metabotropic glutamate receptor agonist microinjected into the dorsal periaqueductal gray of rats Braz. J. Med. Biol. Res. 32 1999 1533 1537 (Pubitemid 30053340)
45. T. Moriya, Y. Kouzu, S. Shibata, H. Kadotani, K. Fukunaga, E. Miyamoto, and T. Yoshioka Close linkage between calcium/calmodulin kinase II alpha/beta and NMDA-2A receptors in the lateral amygdala and significance for retrieval of auditory fear conditioning Eur. J. Neurosci. 12 2000 3307 3314
46. J.S. Morris, A. Ohman, and R.J. Dolan Conscious and unconscious emotional learning in the human amygdala Nature 393 1998 467 470 (Pubitemid 28292192)
47. A.C. Need, and K.P. Giese Handling and environmental enrichment do not rescue learning and memory impairments in alphaCamKII(T286A) mutant mice Genes Brain Behav. 2 2003 132 139 (Pubitemid 36898799)
48. L.P. Noldus, A.J. Spink, and R.A. Tegelenbosch EthoVision: a versatile video tracking system for automation of behavioral experiments Behav. Res. Methods Instrum. Comput. 33 2001 398 414 (Pubitemid 33594754)
49. A. Öhman, and J.J. Soares "Unconscious anxiety": phobic responses to masked stimuli J. Abnorm. Psychol. 103 1994 231 240 (Pubitemid 24152796)
50. R.G. Phillips, and J.E. LeDoux Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning Behav. Neurosci. 106 1992 274 285
51. L.R. Reznikov, L.P. Reagan, and J.R. Fadel Activation of phenotypically distinct neuronal subpopulations in the anterior subdivision of the rat basolateral amygdala following acute and repeated stress J. Comp. Neurol. 508 2008 458 472 (Pubitemid 351562029)
52. R.J. Rodgers Animal models of 'anxiety': where next? Behav. Pharmacol. 8 1997 477 496 (discussion 497-504) (Pubitemid 27504695)
53. S.M. Rodrigues, C.R. Farb, E.P. Bauer, J.E. LeDoux, and G.E. Schafe Pavlovian fear conditioning regulates Thr286 autophosphorylation of Ca2+/calmodulin-dependent protein kinase II at lateral amygdala synapses J. Neurosci. 24 2004 3281 3288 (Pubitemid 38451894)
54. L.C. Schenberg, A.S. Bittencourt, E.C. Sudre, and L.C. Vargas Modeling panic attacks Neurosci. Biobehav. Rev. 25 2001 647 659 (Pubitemid 34136894)
55. N.R. Selden, B.J. Everitt, L.E. Jarrard, and T.W. Robbins Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues Neuroscience 42 1991 335 350
56. M.B. Shaikh, K. Schubert, and A. Siegel Basal amygdaloid facilitation of midbrain periaqueductal gray elicited defensive rage behavior in the cat is mediated through NMDA receptors Brain Res. 635 1994 187 195 (Pubitemid 24031403)
57. A.J. Spink, R.A. Tegelenbosch, M.O. Buma, and L.P. Noldus The EthoVision video tracking system-a tool for behavioral phenotyping of transgenic mice Physiol. Behav. 73 2001 731 744 (Pubitemid 32885562)
58. T. Suenaga, S. Morinobu, K. Kawano, T. Sawada, and S. Yamawaki Influence of immobilization stress on the levels of CaMKII and phospho-CaMKII in the rat hippocampus Int. J. Neuropsychopharmacol. 7 2004 299 309 (Pubitemid 39166464)
59. D.L. Walker, J.V. Cassella, Y. Lee, T.C. De Lima, and M. Davis Opposing roles of the amygdala and dorsolateral periaqueductal gray in fear-potentiated startle Neurosci. Biobehav. Rev. 21 1997 743 753 (Pubitemid 27524769)
60. G.A. Wayman, Y.S. Lee, H. Tokumitsu, A.J. Silva, and T.R. Soderling Calmodulin-kinases: modulators of neuronal development and plasticity Neuron 59 2008 914 931
61. N. Yamasaki, M. Maekawa, K. Kobayashi, Y. Kajii, J. Maeda, M. Soma, K. Takao, K. Tanda, K. Ohira, K. Toyama, K. Kanzaki, K. Fukunaga, Y. Sudo, H. Ichinose, M. Ikeda, N. Iwata, N. Ozaki, H. Suzuki, M. Higuchi, T. Suhara, S. Yuasa, and T. Miyakawa Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders Mol. Brain 1 2008 6