Phosphatidylinositide dependent kinase deficiency increases anxiety and decreases GABA and serotonin abundance in the amygdala

Cellular Physiology and Biochemistry

Volumn 22, Issue 5-6, 2008, Pages 735-744

  Ackermann, Teresa F ^a   Hörtnagl, Heide ^b   Wolfer, David P ^c   Colacicco, Giovanni ^c   Sohr, Reinhard ^b   Lang, Florian ^a   Hellweg, Rainer ^b   Lang, Undine E ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Amygdala; Anxiety; BDNF; Behavior; Depression; GABA; PDK1; PI3K; Serotonin

Indexed keywords

4 AMINOBUTYRIC ACID; 5 HYDROXYINDOLEACETIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; DOPAMINE; GLUTAMIC ACID; NERVE GROWTH FACTOR; NORADRENALIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; SEROTONIN; TAURINE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN WEIGHT; DEPRESSION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; OLFACTORY BULB; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

MUS;

EID: 57649192506     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000185557     Document Type: Article

References (86)

1. Maren S, Quirk GJ: Neuronal signalling of fear memory. Nat Rev Neurosci 2004;5:844-852.
2. Ou LC, Gean PW: Regulation of amygdala-dependent learning by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol-3-kinase. Neuropsychopharmacology 2006;31:287-296.
3. Davis M, Whalen PJ: The amygdala: vigilance and emotion. Mol Psychiatry 2001;6:13-34.
4. Groves JO: Is it time to reassess the BDNF hypothesis of depression? Mol Psychiatry 2007;12:1079-1088.
5. Martinowich K, Manji H, Lu B: New insights into BDNF function in depression and anxiety. Nat Neurosci 2007;10:1089-1093.
6. Atwal JK, Massie B, Miller FD, Kaplan DR: The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron 2000;27:265-277.
7. Chikahisa S, Sei H, Morishima M, Sano A, Kitaoka K, Nakaya Y, Morita Y: Exposure to music in the perinatal period enhances learning performance and alters BDNF/TrkB signaling in mice as adults. Behav Brain Res 2006;169:312-319.
8. Kumar V, Zhang MX, Swank MW, Kunz J, Wu GY: Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J Neurosci 2005;25:11288-11299.
9. Martin-Pena A, Acebes A, Rodriguez JR, Sorribes A, de Polavieja GG, Fernandez-Funez P, Ferrus A: Age-independent synaptogenesis by phosphoinositide 3 kinase. J Neurosci 2006;26:10199-10208.
10. Peltier J, O'Neill A, Schaffer DV: PI3K/ Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev Neurobiol 2007;67:1348-1361.
11. Vanhaesebroeck B, Alessi DR: The PI3K-PDK1 connection: more than just a road to PKB. Biochem J 2000;346 Pt 3:561-576.
12. Mora A, Komander D, van Aalten DM, Alessi DR: PDK1, the master regulator of AGC kinase signal transduction. Semin Cell Dev Biol 2004;15:161-170.
13. Stahl SM: Independent actions on fear circuits may lead to therapeutic synergy for anxiety when combining serotonergic and GABAergic agents. J Clin Psychiatry 2002;63:854-855.
14. Lawlor MA, Mora A, Ashby PR, Williams MR, Murray-Tait V, Malone L, Prescott AR, Lucocq JM, Alessi DR: Essential role of PDK1 in regulating cell size and development in mice. EMBO J 2002;21:3728-3738.
15. Sandu C, Artunc F, Palmada M, Rexhepaj R, Grahammer F, Hussain A, Yun C, Alessi DR, Lang F: Impaired intestinal NHE3 activity in the PDK1 hypomorphic mouse. Am J Physiol Gastrointest Liver Physiol 2006;291:G868-G876.
16. Wolfer DP, Madani R, Valenti P, Lipp HP: Extended analysis of path data from mutant mice using the public domain software Wintrack. Physiol Behav 2001;73:745-753.
17. Lang UE, Wolfer DP, Grahammer F, Strutz-Seebohm N, Seebohm G, Lipp HP, McCormick JA, Hellweg R, Dawson K, Wang J, Pearce D, Lang F: Reduced locomotion in the serum and glucocorticoid inducible kinase 3 knock out mouse. Behav Brain Res 2006;167:75-86.
18. Madani R, Kozlov S, Akhmedov A, Cinelli P, Kinter J, Lipp HP, Sonderegger P, Wolfer DP: Impaired explorative behavior and neophobia in genetically modified mice lacking or overexpressing the extracellular serine protease inhibitor neuroserpin. Mol Cell Neurosci 2003;23:473-494.
19. Crawley J, Goodwin FK: Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 1980;13:167-170.
20. Konig M, Zimmer AM, Steiner H, Holmes PV, Crawley JN, Brownstein MJ, Zimmer A: Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin. Nature 1996;383:535-538.
21. Dulawa SC, Grandy DK, Low MJ, Paulus MP, Geyer MA: Dopamine D4 receptor-knock-out mice exhibit reduced exploration of novel stimuli. J Neurosci 1999;19:9550-9556.
22. Paylor R, Crawley JN: Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacology (Berl) 1997;132:169-180.
23. Hellweg R, Thomas H, Arnswald A, von Richthofen S, Kay S, Fink H, Morgenstern R, Hortnagl H: Serotonergic lesion of median raphe nucleus alters nerve growth factor content and vulnerability of cholinergic septohippocampal neurons in rat. Brain Res 2001;907:100-108.
24. Hellweg R, Hock C, Hartung HD: An improved rapid and highly sensitive enzyme immunoassay for nerve growth factor. Technique J Meth Cell Mol Biol 1989;1:43-49.
25. Hellweg R, von Arnim CA, Buchner M, Huber R, Riepe MW: Neuroprotection and neuronal dysfunction upon repetitive inhibition of oxidative phosphorylation. Exp Neurol 2003;183:346-354.
26. Hellweg R, Lohmann P, Huber R, Kuhl A, Riepe MW: Spatial navigation in complex and radial mazes in APP23 animals and neurotrophin signaling as a biological marker of early impairment. Learn Mem 2006;13:63-71.
27. Sperk G: Simultaneous determination of serotonin, 5-hydroxindoleacetic acid, 3,4-dihydroxyphenylacetic acid and homovanillic acid by high performance liquid chromatography with electrochemical detection. J Neurochem 1982;38:840-843.
28. Felice LJ, Felice JD, Kissinger PT: Determination of catecholamines in rat brain parts by reverse-phase ion-pair liquid chromatography. J Neurochem 1978;31:1461-1465.
29. Sperk G, Berger M, Hortnagl H, Hornykiewicz O: Kainic acid-induced changes of serotonin and dopamine metabolism in the striatum and substantia nigra of the rat. Eur J Pharmacol 1981;74:279-286.
30. Piepponen TP, Skujins A: Rapid and sensitive step gradient assays of glutamate, glycine, taurine and gamma-aminobutyric acid by high-performance liquid chromatography-fluorescence detection with o- phthalaldehydemercaptoethanol derivatization with an emphasis on microdialysis samples. J Chromatogr B Biomed Sci Appl 2001;757:277-283.
31. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, Gulbins E, Haussinger D: Functional significance of cell volume regulatory mechanisms. Physiol Rev 1998;78:247-306.
32. Lang F, Cohen P: Regulation and physiological roles of serum- and glucocorticoid-induced protein kinase isoforms. Sci STKE 2001;2001:RE17.
33. Lang F, Bohmer C, Palmada M, Seebohm G, Strutz-Seebohm N, Vallon V: (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol Rev 2006;86:1151-1178.
34. Artunc F, Rexhepaj R, Volkl H, Grahammer F, Remy C, Sandulache D, Nasir O, Wagner CA, Alessi DR, Lang F: Impaired intestinal and renal glucose transport in PDK-1 hypomorphic mice. Am J Physiol Regul Integr Comp Physiol 2006;291:R1533-R1538.
35. Rexhepaj R, Grahammer F, Volkl H, Remy C, Wagner CA, Sandulache D, Artunc F, Henke G, Nammi S, Capasso G, Alessi DR, Lang F: Reduced intestinal and renal amino acid transport in PDK1 hypomorphic mice. FASEB J 2006;20:2214-2222.
36. Arban R, Maraia G, Brackenborough K, Winyard L, Wilson A, Gerrard P, Large C: Evaluation of the effects of lamotrigine, valproate and carbamazepine in a rodent model of mania. Behav Brain Res 2005;158:123-132.
37. Gould TD, Einat H, O'Donnell KC, Picchini AM, Schloesser RJ, Manji HK: Beta-catenin overexpression in the mouse brain phenocopies lithium-sensitive behaviors. Neuropsychopharmacology 2007;32:2173-2183.
38. Shaltiel G, Maeng S, Malkesman O, Pearson B, Schloesser RJ, Tragon T, Rogawski M, Gasior M, Luckenbaugh D, Chen G, Manji HK: Evidence for the involvement of the kainate receptor subunit GluR6 (GRIK2) in mediating behavioral displays related to behavioral symptoms of mania. Mol Psychiatry 2008;13:858-872.
39. Horwood JM, Dufour F, Laroche S, Davis S: Signalling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur J Neurosci 2006;23:3375-3384.
40. Pandey SC, Roy A, Zhang H: The decreased phosphorylation of cyclic adenosine monophosphate (cAMP) response element binding (CREB) protein in the central amygdala acts as a molecular substrate for anxiety related to ethanol withdrawal in rats. Alcohol Clin Exp Res 2003;27:396-409.
41. Pandey SC, Zhang H, Roy A, Xu T: Deficits in amygdaloid cAMP-responsive element-binding protein signaling play a role in genetic predisposition to anxiety and alcoholism. J Clin Invest 2005;115:2762-2773.
42. Pandey SC, Zhang H, Roy A, Misra K: Central and medial amygdaloid brain-derived neurotrophic factor signaling plays a critical role in alcohol-drinking and anxiety-like behaviors. J Neurosci 2006;26:8320-8331.
43. Ozaita A, Puighermanal E, Maldonado R: Regulation of PI3K/Akt/GSK-3 pathway by cannabinoids in the brain. J Neurochem 2007;102:1105-1114.
44. Garcia-Segura LM, Sanz A, Mendez P: Cross-talk between IGF-I and estradiol in the brain: focus on neuroprotection. Neuroendocrinology 2006;84:275-279.
45. Malberg JE, Platt B, Rizzo SJ, Ring RH, Lucki I, Schechter LE, Rosenzweig-Lipson S: Increasing the levels of insulin-like growth factor-I by an IGF binding protein inhibitor produces anxiolytic and antidepressant-like effects. Neuropsychopharmacology 2007;32:2360-2368.
46. Toufexis DJ, Myers KM, Davis M: The effect of gonadal hormones and gender on anxiety and emotional learning. Horm Behav 2006;50:539-549.
47. Chen MJ, Russo-Neustadt AA: Exercise activates the phosphatidylinositol 3-kinase pathway. Brain Res Mol Brain Res 2005;135:181-193.
48. Salmon P: Effects of physical exercise on anxiety, depression, and sensitivity to stress: a unifying theory. Clin Psychol Rev 2001;21:33-61.
49. Lang UE, Hellweg R, Gallinat J: Association of BDNF serum concentrations with central serotonergic activity: evidence from auditory signal processing. Neuropsychopharmacology 2005;30:1148-1153.
50. Lang UE, Hellweg R, Kalus P, Bajbouj M, Lenzen KP, Sander T, Kunz D, Gallinat J: Association of a functional BDNF polymorphism and anxiety-related personality traits. Psychopharmacology (Berl) 2005;180:95-99.
51. Chhatwal JP, Stanek-Rattiner L, Davis M, Ressler KJ: Amygdala BDNF signaling is required for consolidation but not encoding of extinction. Nat Neurosci 2006;9:870-872.
52. Opazo P, Watabe AM, Grant SG, O'Dell TJ: Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J Neurosci 2003;23:3679-3688.
53. Rattiner LM, Davis M, French CT, Ressler KJ: Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning. J Neurosci 2004;24:4796-4806.
54. Sanna PP, Cammalleri M, Berton F, Simpson C, Lutjens R, Bloom FE, Francesconi W: Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J Neurosci 2002;22:3359-3365.
55. Boucher AA, Arnold JC, Duffy L, Schofield PR, Micheau J, Karl T: Heterozygous neuregulin 1 mice are more sensitive to the behavioural effects of Delta9-tetrahydrocannabinol. Psychopharmacology (Berl) 2007;192:325-336.
56. Ren-Patterson RF, Cochran LW, Holmes A, Lesch KP, Lu B, Murphy DL: Gender-dependent modulation of brain monoamines and anxiety-like behaviors in mice with genetic serotonin transporter and BDNF deficiencies. Cell Mol Neurobiol 2006;26:755-780.
57. Chen MJ, Russo-Neustadt AA: Running exercise- and antidepressant-induced increases in growth and survival-associated signaling molecules are IGF-dependent. Growth Factors 2007;25:118-131.
58. Wang D, Noda Y, Tsunekawa H, Zhou Y, Miyazaki M, Senzaki K, Nabeshima T: Behavioural and neurochemical features of olfactory bulbectomized rats resembling depression with comorbid anxiety. Behav Brain Res 2007;178:262-273.
59. Shibata S, Watanabe S: Facilitatory effect of olfactory bulbectomy on 2-deoxyglucose uptake in rat amygdala slices. Brain Res 1994;665:147-150.
60. Nemeroff CB: The role of GABA in the pathophysiology and treatment of anxiety disorders. Psychopharmacol Bull 2003;37:133-146.
61. Salgado H, Bellay T, Nichols JA, Bose M, Martinolich L, Perrotti L, Atzori M: Muscarinic M2 and M1 receptors reduce GABA release by Ca2+ channel modulation through activation of PI3K/ Ca2+ -independent and PLC/Ca2+ - dependent PKC. J Neurophysiol 2007;98:952-965.
62. Kong WX, Chen SW, Li YL, Zhang YJ, Wang R, Min L, Mi X: Effects of taurine on rat behaviors in three anxiety models. Pharmacol Biochem Behav 2006;83:271-276.
63. McCool BA, Chappell A: Strychnine and taurine modulation of amygdala-associated anxiety-like behavior is 'state' dependent. Behav Brain Res 2007;178:70-81.
64. Murphy DL, Wichems C, Li Q, Heils A: Molecular manipulations as tools for enhancing our understanding of 5-HT neurotransmission. Trends Pharmacol Sci 1999;20:246-252.
65. Muller JF, Mascagni F, McDonald AJ: Serotonin-immunoreactive axon terminals innervate pyramidal cells and interneurons in the rat basolateral amygdala. J Comp Neurol 2007;505:314-335.
66. Rauch SL: Neuroimaging and neurocircuitry models pertaining to the neurosurgical treatment of psychiatric disorders. Neurosurg Clin N Am 2003;14:213-viii.
67. Sheline YI, Barch DM, Donnelly JM, Ollinger JM, Snyder AZ, Mintun MA: Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol Psychiatry 2001;50:651-658.
68. de La Paz LD, Lezama R, Torres-Marquez ME, Pasantes-Morales H: Tyrosine kinases and amino acid efflux under hyposmotic and ischaemic conditions in the chicken retina. Pflugers Arch 2002;445:87-96.
69. Malyala A, Zhang C, Bryant DN, Kelly MJ, Ronnekleiv OK: PI3K signaling effects in hypothalamic neurons mediated by estrogen. J Comp Neurol 2008;506:895-911.
70. Cruz-Rangel S, Hernandez-Benitez R, Vazquez-Juarez E, Lopez-Dominguez A, Pasantes-Morales H: Potentiation by thrombin of hyposmotic glutamate and taurine efflux from cultured astrocytes: signalling chains. Neurochem Res 2008;33:1518-1524.
71. Franco R, Torres-Marquez ME, Pasantes-Morales H: Evidence for two mechanisms of amino acid osmolyte release from hippocampal slices. Pflugers Arch 2001;442:791-800.
72. Pasantes-Morales H, Franco R: Influence of protein tyrosine kinases on cell volume change-induced taurine release. Cerebellum 2002;1:103-109.
73. Green CJ, Goransson O, Kular GS, Leslie NR, Gray A, Alessi DR, Sakamoto K, Hundal HS: Use of Akti and a drug-resistant mutant validates a critical role for PKB/Akt in the insulin-dependent regulation of glucose and system A amino acid uptake. J Biol Chem 2008;283:27653-27667.
74. Hills CE, Bland R, Bennett J, Ronco PM, Squires PE: High glucose up-regulates ENaC and SGK1 expression in HCD-cells. Cell Physiol Biochem 2006;18:337-346.
75. Ishiki M, Klip A: Minireview: recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 2005;146:5071-5078.
76. Luo J, Sun D: Physiology and pathophysiology of Na(+)/H(+) exchange isoform 1 in the central nervous system. Curr Neurovasc Res 2007;4:205-215.
77. Maier G, Palmada M, Rajamanickam J, Shumilina E, Bohmer C, Lang F: Upregulation of HERG channels by the serum and glucocorticoid inducible kinase isoform SGK3. Cell Physiol Biochem 2006;18:177-186.
78. Sato JD, Chapline MC, Thibodeau R, Frizzell RA, Stanton BA: Regulation of human cystic fibrosis transmembrane conductance regulator (CFTR) by serum- and glucocorticoid-inducible kinase (SGK1). Cell Physiol Biochem 2007;20:91-98.
79. Sen P, Mukherjee S, Ray D, Raha S: Involvement of the Akt/PKB signaling pathway with disease processes. Mol Cell Biochem 2003;253:241-246.
80. Strutz-Seebohm N, Shojaiefard M, Christie D, Tavare J, Seebohm G, Lang F: PIKfyve in the SGK1 mediated regulation of the creatine transporter SLC6A8. Cell Physiol Biochem 2007;20:729-734.
81. Tessier M, Woodgett JR: Serum and glucocorticoid-regulated protein kinases: variations on a theme. J Cell Biochem 2006;98:1391-1407.
82. Whiteman EL, Cho H, Birnbaum MJ: Role of Akt/protein kinase B in metabolism. Trends Endocrinol Metab 2002;13:444-451.
83. Wyatt AW, Hussain A, Amann K, Klingel K, Kandolf R, Artunc F, Grahammer F, Huang DY, Vallon V, Kuhl D, Lang F: DOCA-induced phosphorylation of glycogen synthase kinase 3beta. Cell Physiol Biochem 2006;17:137-144.
84. Gould TD, Manji HK: Glycogen synthase kinase-3: a putative molecular target for lithium mimetic drugs. Neuropsychopharmacology 2005;30:1223-1237.
85. Lang UE, Puls I, Muller DJ, Strutz-Seebohm N, Gallinat J: Molecular mechanisms of schizophrenia. Cell Physiol Biochem 2007;20:687-702.
86. Rowe MK, Wiest C, Chuang DM: GSK-3 is a viable potential target for therapeutic intervention in bipolar disorder. Neurosci Biobehav Rev 2007;31:920-931.