Protein Kinase C is Essential for Kainate-Induced Anxiety-Related Behavior and Glutamatergic Synapse Upregulation in Prelimbic Cortex

CNS Neuroscience and Therapeutics

Volumn 20, Issue 11, 2014, Pages 982-990

  Liu, Bei ^a,b   Feng, Jing ^a,b   Wang, Jin Hui ^a,b,c  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b INSTITUTE OF BIOPHYSICS   (China)

^c QINGDAO UNIVERSITY   (China)

Author keywords

Anxiety; Glutamate; Prefrontal cortex; Protein kinase C; Synapse

Indexed keywords

CHELERYTHRINE; GLUTAMATE RECEPTOR; KAINIC ACID; PROTEIN KINASE C; AMINO ACID RECEPTOR STIMULATING AGENT; BACTERIAL PROTEIN; BENZOPHENANTHRIDINE DERIVATIVE; ENZYME INHIBITOR; GLUTAMIC ACID; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; CONTROLLED STUDY; DENDRITIC SPINE; LIMBIC CORTEX; LOCOMOTION; MOLECULAR MECHANICS; MOOD DISORDER; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION; UPREGULATION; ANIMAL; ANXIETY; C57BL MOUSE; CHEMICALLY INDUCED; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; IN VITRO STUDY; MAZE TEST; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANXIETY; BACTERIAL PROTEINS; BENZOPHENANTHRIDINES; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; IN VITRO TECHNIQUES; KAINIC ACID; LUMINESCENT PROTEINS; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PREFRONTAL CORTEX; PROTEIN KINASE C; SYNAPSES; UP-REGULATION;

EID: 84911472014     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/cns.12313     Document Type: Article

References (90)

1. Bishop SJ. Neurocongnitive mechanisms of anxiety: an integrative account. Trends Cogn Sci 2007;11:307-316.
2. Rickeles K, Rynn M. Overview and clinical presentation of generalized anxiety disorder. Psychiatr Clin North Am 2001;24:1-17.
3. Anand A, Shekhar A. Brain imaging studies in mood and anxiety disorders: Special emphasis on the amygdala. Ann N Y Acad Sci 2003;985:370-388.
4. Adams JD Jr. Chemical interactions with pyramidal neurons in layer 5 of the cerebral cortex: Control of pain and anxiety. Curr Med Chem 2009;16:3476-3479.
5. Bondi CO, Rodriguez G, Gould GG, Frazer A, Morilak DA. Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 2008;33:320-331.
6. Bremner JD. Brain imaging in anxiety disorders. Exp Rev Neurother 2004;4:275-284.
7. Craske MG, Rauch SL, Ursano R, Prenoveau JP, D.S., Zinbarg RE. What is an anxiety disorder? Depress Anx 2009;26:1066-1085.
8. Damsa C, Kosel M, Moussally J. Current status of brain imaging in anxiety disorders. Curr Opin Psychiatry 2009;22:96-110.
9. Davidson RJ. Anxiety and affective style: One of prefrontal cortex and amygdala. Biol Psychiatry 2002;51:68-80.
10. Davis M, Walker DL, Miles L, Grillon C. Phasic versus sustained fear in rats and humans: Role of the extended amygdala in fear versus anxiety. Neuropsychopharmacology 2010;35:105-135.
11. Freitas-Feerrari MC, Hallak JE, Trzesniak C, Filho AS et al. Neuroimaging in social anxiety disorder: A systematic review of the literature. Prog Neuropyschopharmacol Biol Psychiatry 2010;34:565-580.
12. Gross C, Hen R. The developmental origins of anxiety. Nat Rev Neurosci 2004;5:545-552.
13. Garrett A, Chang K. The role of the amygdala in bipolar disorder development. Dev Psychopathol 2008;20:1285-1296.
14. LeDoux J. Emotion circuits in the brain. Annu Rev Neurosci 2000;23:155-184.
15. Milad MR, Rauch SL. The role of the orbitofrontal cortex in anxiety disorders. Ann N Y Acad Sci 2007;1121:546-561.
16. Mennes M, Stiers P, Lagae L, Van den Bergh B. Long-term cognitive sequelae of antenatal maternal anxiety: Involvement of the orbitofrontal cortex. Neurosci Biobehav Rev 2006;30:1078-1086.
17. Myers-Schulz B, Koenigs M. Functional anatomy of ventromedial prefrontal cortex: Implications for mood and anxiety disorders. Mol Psychiatry 2011;17:132-141.
18. Neugebauer V, Li W, Bird GC, Han JS. The amygdala and persistent pain. Neuroscientist 2004;10:221-234.
19. Rauch SL, Shin LM, Wright CI. Neuroimaging studies of amygdala function in anxiety disorders. Ann N Y Acad Sci 2003;985:389-410.
20. Roozendaal B, McEwen BS, Chattarji S. Stress, memory and amygdala. Nat Rev Neurosci 2009;10:423-433.
21. Stein MB, Stein DJ. Social anxiety disorders. Lancet 2008;371:1115-1125.
22. Yu T, Guo M, Garza J, Rendon S, Sun XL, Zhang W, Lu XY. Cognitive and neural correlates of depression-like behaviour in socially defeated mice: An animal model of depression with cognitive dysfunction. Int J Neuropsychopharmacol 2010;14:303-317.
23. Amano T, Unal CT, Pare D. Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 2010;13:489-495.
24. Crestani F, Lorez M, Bear K. Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cue. Nat Neurosci 1999;2:833-839.
25. Delgado MR, Olsson A, Phelps EA. Extending animal models of fear conditioning to humans. Biol Psychol 2006;73:39-48.
26. DuBios DW, A.P, Floyd DW, Weiner JL, McCool BA. et al. Distinct functional characteristics of the lateral/basolateral amygdala GABAergic system in C57BL/6J and DBA/2J mice. J Pharmacol Exp Ther 2006;318:629-640.
27. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Luthi A. Amygdala inhibitory circuits and the control of fear memory. Neuron 2009;62:757-771.
28. Liu J, Garza JC, Truong HV, Henschel J, Zhang W, Lu XY. The melanocortinergic pathway is rapidly recruited by emotional stress and contributes to stress-induced anorexia and anxiety-like behavior. Endocrinology 2007;148:5531-5540.
29. Pape HC, Pare D. Plastic synaptic networks of the amygdala for the acquisition, expression and extinction of conditioned fear. Physiol Rev 2010;90:419-463.
30. Shin LM, Liberzon I. The neurocircuitry of fear, stress and anxiety disorders. Neuropsychopharmacology 2010;35:169-191.
31. Shumyatsky GP, Tsvetkov E, Malleret G et al. Identification of a signaling network in lateral nucleus of amygdala important for inhibiting memory specifically related to learned fear. Cell 2002;111:905-918.
32. Zhang F, Liu B, Lei Z, Wang J. mGluR1, 5 activation improves network asynchrony and GABAergic synapse attenuation in the amygdala: Implication for anxiety-like behavior in DBA/2 mice. Mol Brain 2012;5:20.
33. Leuner B, Shors TJ. Stress, anxiety, and dendritic spines: What are the connections? Neuroscience 2012;251:108-119.
34. Wu LJ, Ko SW, Toyoda H et al. Increased anxiety-like behavior and enhanced synaptic efficacy in the amygdala of GluR5 knockout mice. PLoS ONE 2007;2:e167.
35. Furmaga H, Shah A, Frazer A. Serotonergic and noradrenergic pathways are required for the anxiolytic-like and antidepressant-like behavioral effects of repeated vagal nerve stimulation in rats. Biol Psychiatry 2011;70:937-945.
36. Graeff FG, Guimaraes FS, De Andrade TG, Deakin JF. Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 1996;54:129-141.
37. Bourin M, Hascoet M. Drug mechanisms in anxiety. Curr Opin Investig Drugs 2001;2:259-265.
38. Dell'Osso B, Buoli M, Baldwin DS, Altamura AC. Serotonin norepinephrine reuptake inhibitors (SNRIs) in anxiety disorders: A comprehensive review of their clinical efficacy. Hum Psychopharmacol 2010;25:17-29.
39. Amiel JM, Mathew SJ. Glutamate and anxiety disorders. Curr Psychiatry Rep 2007;9:278-283.
40. Bowden CL, Perlis RH, Thase ME et al. Aims and results of the NIMH systematic treatment enhancement program for bipolar disorder (STEP-BD). CNS Neurosci Ther 2012;18:243-249.
41. Vilhauer JS, Young S, Kealoha C et al. Treating major depression by creating positive expectations for the future: A pilot study for the effectiveness of future-directed therapy (FDT) on symptom severity and quality of life. CNS Neurosci Ther 2012;18:102-109.
42. Ravindran LN, Stein MB. The pharmacologic treatment of anxiety disorders: A review of progress. J Clin Psychiatry 2010;71:839-854.
43. Bergink V, van Megen HJ, Westenberg HG. Glutamate and anxiety. Eur Neuropsychopharmacol 2004;14:175-183.
44. Chaki S, Okubo T, Sekiguchi Y. Non-monoamine-based approach for the treatment of depression and anxiety disorders. Recent Pat CNS Drug Discov 2006;1:1-27.
45. Cortese BM, Phan KL. The role of glutamate in anxiety and related disorders. CNS Spectr 2005;10:820-830.
46. Simon AB, Gorman JM. Advances in the treatment of anxiety: Targeting glutamate. NeuroRx 2006;3:57-68.
47. Zhang G, Gao Z, Guan S, Zhu Y, Wang JH. Upregulation of excitatory neurons and downregulation of inhibitory neurons in barrel cortex are associated with loss of whisker inputs. Mol Brain 2013;6:2.
48. Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972;32:281-294.
49. McLin JP, Steward O. Comparison of seizure phenotype and neurodegeneration induced by systemic kainic acid in inbred, outbred, and hybrid mouse strains. Eur J Neurosci 2006;24:2191-2202.
50. Pellow S, Chopin P. Validation of open: Closed arm entries in an elevated plus-maze as a measure of anxiety in the rats. J Neurosci Methods 1985;14:149-167.
51. Walf AA, Frye CA. The use of elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2007;2:322-328.
52. Ge R, Qian H, Wang JH. Physiological synaptic signals initiate sequential spikes at soma of cortical pyramidal neurons. Mol Brain 2011;4:19.
53. Wang J-H. Short-term cerebral ischemia causes the dysfunction of interneurons and more excitation of pyramidal neurons. Brain Res Bull 2003;60:53-58.
54. Yu J, Qian H, Chen N, Wang JH. Quantal glutamate release is essential for reliable neuronal encodings in cerebral networks. PLoS ONE 2011;6:e25219.
55. Yang Z, Gu E, Lu X, Wang JH. Essential role of axonal VGSC inactivation in time-dependent deceleration and unreliability of spike propagation at cerebellar Purkinje cells. Mol Brain 2014;7:1.
56. Wang J-H, Stelzer A. Shared calcium signaling pathways in the induction of long-term potentiation and synaptic disinhibition in CA1 pyramidal cell dendrites. J Neurophysiol 1996;75:1687-1702.
57. 2+-calmodulin signalling pathway upregulates GABA synaptic transmission through cytoskeleton-mediated mechanisms. Neuroscience 2004;127:637-647.
58. Chen N, Yu J, Qian H, Ge R, Wang JH. Axons amplify somatic incomplete spikes into uniform amplitudes in mouse cortical pyramidal neurons. PLoS ONE 2010;5:e11868.
59. Chen N, Chen X, Wang J-H. Homeostasis established by coordination of subcellular compartment plasticity improves spike encoding. J Cell Sci 2008;121:2961-2971.
60. Ge R, Qian H, Chen N, Wang JH. Input-dependent subcellular localization of spike initiation between soma and axon at cortical pyramidal neurons. Mol Brain 2014;7:26.
61. Lu W, Wen B, Zhang F, Wang JH. Voltage-independent sodium channels emerge for an expression of activity-induced spontaneous spikes in GABAergic neurons. Mol Brain 2014;7:38.
62. Wang JH, Wei J, Chen X, Yu J, Chen N, Shi J. The gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding. J Cell Sci 2008;121:2951-2960.
63. Ni H, Huang L, Chen N et al. Upregulation of barrel GABAergic neurons is associated with cross-modal plasticity in olfactory deficit. PLoS ONE 2010;5:e13736.
64. 2+ regulates spike encoding at cortical GABAergic neurons and cerebellar Purkinje cells differently. Biochem Biophys Res Commun 2009;381:129-133.
65. Herbert JM, Augereau JM, Gleye J, Maffrand JP. Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun 1990;172:993-999.
66. Alt A, Weiss B, Ogden AM et al. In vitro and in vivo studies in rats with LY293558 suggest AMPA/kainate receptor blockade as a novel potential mechanism for the therapeutic treatment of anxiety disorders. Psychopharmacology 2006;185:240-247.
67. Dos Santos L, de Andrade TG, Zangrossi H Jr. Serotonergic neurons in the median raphe nucleus regulate inhibitory avoidance but not escape behavior in the rat elevated T-maze test of anxiety. Psychopharmacology 2005;179:733-741.
68. Pobbe RL, Zangrossi H Jr. Involvement of the lateral habenula in the regulation of generalized anxiety- and panic-related defensive responses in rats. Life Sci 2008;82:1256-1261.
69. Govoni S, Amadio M, Battaini F, Pascale A. Senescence of the brain: Focus on cognitive kinases. Curr Pharm Des 2010;16:660-671.
70. Sun MK, Alkon DL. Protein kinase C pharmacology: Perspectives on therapeutic potentials as antidementic and cognitive agents. Recent Pat CNS Drug Discov 2006;1:147-156.
71. Van Kolen K, Pullan S, Neefs JM, Dautzenberg FM. Nociceptive and behavioural sensitisation by protein kinase Cepsilon signalling in the CNS. J Neurochem 2008;104:1-13.
72. Wang JH, Feng DP. Postsynaptic protein kinase C essential to induction and maintenance of long-term potentiation in the hippocampal CA1 region. Proc Natl Acad Sci USA 1992;89:2576-2580.
73. Begon S, Pickering G, Eschalier A, Mazur A, Rayssiguier Y, Dubray C. Role of spinal NMDA receptors, protein kinase C and nitric oxide synthase in the hyperalgesia induced by magnesium deficiency in rats. Br J Pharmacol 2001;134:1227-1236.
74. Keenan C, Goode N, Pears C. Isoform specificity of activators and inhibitors of protein kinase C gamma and delta. FEBS Lett 1997;415:101-108.
75. Kukreja RC, Qian YZ, Okubo S, Flaherty EE. Role of protein kinase C and 72 kDa heat shock protein in ischemic tolerance following heat stress in the rat heart. Mol Cell Biochem 1999;195:123-131.
76. Serrano PA, Rodriguez WA, Pope B, Bennett EL, Rosenzweig MR. Protein kinase C inhibitor chelerythrine disrupts memory formation in chicks. Behav Neurosci 1995;109:278-284.
77. Wang JH, Ko G, Kelly PT. Cellular and molecular bases of memory: Synaptic and neuronal plasticity. J Clin Neurophysiol 1997;14:264-293.
78. Zucker RS, Regehr WG. Short-term synaptic plasticity. Ann Rev Physiol 2002;25:355-405.
79. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 2010;33:121-129.
80. Wu L-J, Kim SS, Zhuo M. Molecular targets of anxiety: From membrane to nucleus. Neurochem Res 2008;33:1925-1932.
81. Xia K, Xiong H, Shin Y et al. Roles of KChIP1 in the regulation of GABA-mediated transmission and behavioral anxiety. Mol Brain 2010;3:23.
82. Del Arco A, Mora F. Neurotransmitters and prefrontal cortex-limbic system interactions: Implications for plasticity and psychiatric disorders. J Neural Transm 2009;116:941-952.
83. Mega MS, Cummings JL, Salloway S, Malloy P. The limbic system: An anatomic, phylogenetic, and clinical perspective. J Neuropsychiatry Clin Neurosci 1997;9:315-330.
84. Stathis P, Panourias IG, Themistocleous MS, Sakas DE. Connections of the basal ganglia with the limbic system: Implications for neuromodulation therapies of anxiety and affective disorders. Acta Neurochir Suppl 2007;97:575-586.
85. Charney DS. Neuroanatomical circuits modulating fear and anxiety behavior. Acta Psychiatry Scand Suppl 2003;417:38-50.
86. Mathew SJ, Price RB, Charney DS. Recent advances in the neurobiology of anxiety disorders: Implications for novel therapeutics. Am J Med Genet C Semin Med Genet 2008;148C:89-98.
87. Siever LJ, Weinstein LN. The neurobiology of personality disorders: Implications for psychoanalysis. J Am Psychoanal Assoc 2009;57:361-398.
88. Krystal JH, Mathew SJ, D'Souza DC, Garakani A, Gunduz-Bruce H, Charney DS. Potential psychiatric applications of metabotropic glutamate receptor agonists and antagonists. CNS Drugs 2010;24:669-693.
89. Lima VC, Molchanov ML, Aguiar DC, Campos AC, Guimaraes FS. Modulation of defensive responses and anxiety-like behaviors by group I metabotropic glutamate receptors located in the dorsolateral periaqueductal gray. Prog Neuropsychopharmacol Biol Psychiatry 2008;32:178-185.
90. Muly EC, Mania I, Guo JD, Rainnie DG. Group II metabotropic glutamate receptors in anxiety circuitry: Correspondence of physiological response and subcellular distribution. J Comp Neurol 2007;505:682-700.