Selective deletion of forebrain glycogen synthase kinase 3β reveals a central role in serotonin-sensitive anxiety and social behaviour

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1601, 2012, Pages 2460-2474

  Latapy, Camille ^a   Rioux, Véronique ^a   Guitton, Matthieu J ^a,b   Beaulieu, Jean Martin ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

Author keywords

Anxiety; Cortex; Glycogen synthase kinase 3 ; Mood disorders; Serotonin; Sociability

Indexed keywords

ENZYME ACTIVITY; GENE EXPRESSION; INHIBITION; MENTAL HEALTH; RODENT; SOCIAL BEHAVIOR;

MUS;

EID: 84864198258     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0094     Document Type: Article

References (83)

1. Gustavsson, A. et al. 2011 Cost of disorders of the brain in Europe 2010. Eur. Neuropsychopharmacol. 21, 718-779. (doi:10.1016/j.euroneuro.2011.08.008)
2. Wittchen, H. U. et al. 2011 The size and burden of mental disorders and other disorders of the brain in Europe 2010. Eur. Neuropsychopharmacol. 21, 655-679. (doi:10.1016/j.euroneuro.2011.07.018)
3. Glowinski, J. & Axelrod, J. 1964 Inhibition of uptake of tritiated-noradrenaline in the intact rat brain by imipramine and structurally related compounds. Nature 204, 1318-1319. (doi:10.1038/2041318a0)
4. Carlsson, A., Fuxe, K. & Ungerstedt, U. 1968 The effect of imipramine on central 5-hydroxytryptamine neurons. J. Pharm. Pharmacol. 20, 150-151. (doi:10.1111/j.2042-7158.1968.tb09706.x)
5. Snyder, S. H. 1976 The dopamine hypothesis of schizophrenia: focus on the dopamine receptor. Am. J. Psychiatry 133, 197-202.
6. Roth, B. L., Sheffler, D. J. & Kroeze, W. K. 2004 Magic shotguns versus magic bullets: selectively non-selective drugs for mood disorders and schizophrenia. Nat. Rev. Drug Discov. 3, 353-359. (doi:10.1038/nrd1346)
7. Kapur, S. & Remington, G. 2001 Atypical antipsychotics: new directions and new challenges in the treatment of schizophrenia. Annu. Rev. Med. 52, 503-517. (doi:10.1146/annurev.med.52.1.503)
8. Seeman, P. et al. 2005 Dopamine super sensitivity correlates with D2High states, implying many paths to psychosis. Proc. Natl Acad. Sci. USA 102, 3513-3518. (doi:10.1073/pnas.0409766102)
9. Carlsson, A. 1987 Perspectives on the discovery of central monoaminergic neurotransmission. Annu. Rev. Neurosci. 10, 19-40. (doi:10.1146/annurev.ne.10.030187.000315)
10. Blier, P. & de Montigny, C. 1980 Effect of chronic tricylic antidepressant treatment on the serotoninergic autoreceptor: a microiontophoretic study in the rat. Naunyn Schmiedebergs Arch. Pharmacol. 314, 123-128.(doi:10.1007/BF00504527)
11. Nguyen, H. T., Guiard, B. P., Bacq, A., David, D. J., David, I., Quesseveur, G., Gautron, S., Sanchez, C. & Gardier, A. M. 2012 Blockade of the high-affinity norepinephrine transporter (NET) by the selective serotonin reuptake inhibitor escitalopram: an in vivo microdialysis study in mice. Br. J. Pharmacol. (doi:10.1111/j.1476-5381.2012.01850.x)
12. Deltheil, T. et al. 2008 Behavioral and serotonergic consequences of decreasing or increasing hippocampus brain-derived neurotrophic factor protein levels in mice. Neuropharmacology 55, 1006-1014. (doi:10.1016/j.neuropharm.2008.08.001)
13. Walther, D. J., Peter, J. U., Bashammakh, S., Hortnagl, H., Voits, M., Fink, H. & Bader, M. 2003 Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 299, 76. (doi:10.1126/science.1078197)
14. Zhang, X., Beaulieu, J. M., Sotnikova, T. D., Gainetdinov, R. R. & Caron, M. G. 2004 Tryptophan hydroxylase-2 controls brain serotonin synthesis. Science 305, 217. (doi:10.1126/science.1097540)
15. Zhang, X., Gainetdinov, R. R., Beaulieu, J. M., Sotnikova, T. D., Burch, L. H., Williams, R. B., Schwartz, D. A., Krishnan, K. R. & Caron, M. G. 2005 Loss-of-function mutation in tryptophan hydroxylase- 2 identified in unipolar major depression. Neuron 45,11-16. (doi:10.1016/j.neuron.2004.12.014)
16. Zhang, X. et al. 2010 A functional alternative splicing mutation in human tryptophan hydroxylase-2. Mol. Psychiatry 16, 1169-1176. (doi:10.1038/mp.2010.99)
17. Lesch, K. P. et al. 1996 Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531.(doi:10.1126/science.274.5292.1527)
18. Blakely, R. D. 2005 Overview: a rare opportunity or just one less reason to be depressed. Neuron 48, 701-702 (author reply 705-706)
19. Beaulieu, J. M. 2011 A role for Akt and glycogen synthase kinase-3 as integrators of dopamine and serotonin neurotransmission in mental health. J. Psychiatry Neurosci. 36, 110011. (doi:10.1503/jpn.110011)
20. Beaulieu, J. M., Gainetdinov, R. R. & Caron, M. G. 2009 Akt/GSK3 signaling in the action of psychotropic drugs. Annu. Rev. Pharmacol. Toxicol. 49, 327-347.(doi:10.1146/annurev.pharmtox.011008.145634)
21. Li, X. & Jope, R. S. 2010 Is glycogen synthase kinase-3 a central modulator in mood regulation? Neuropsychopharmacology 35, 2143-2154. (doi:10.1038/npp.2010.105)
22. Li, X., Zhu, W., Roh, M. S., Friedman, A. B., Rosborough, K. & Jope, R. S. 2004 In vivo regulation of glycogen synthase kinase-3β (GSK3β) by serotonergic activity in mouse brain. Neuropsychopharmacology 29, 1426-1431. (doi:10.1038/sj.npp.1300439)
23. Li, X., Rosborough, K. M., Friedman, A. B., Zhu, W. & Roth, K. A. 2007 Regulation of mouse brain glycogen synthase kinase-3 by atypical antipsychotics. Int. J. Neuropsychopharmacol. 10, 7-19. (doi:10.1017/S1461145706006547)
24. Beaulieu, J. M. 2007 Not only lithium: regulation of glycogen synthase kinase-3 by antipsychotics and serotonergic drugs. Int. J. Neuropsychopharmacol. 10, 3-6.(doi:10.1017/S1461145706006857)
25. Beaulieu, J. M., Zhang, X., Rodriguiz, R. M., Sotnikova, T. D., Cools, M. J., Wetsel, W. C., Gainetdinov, R. R. & Caron, M. G. 2008 Role of GSK3β in behavioral abnormalities induced by serotonin deficiency. Proc. Natl Acad. Sci. USA 105, 1333-1338. (doi:10.1073/pnas.0711496105)
26. Polter, A. M., Yang, S., Jope, R. S. & Li, X. 2012 Functional significance of glycogen synthase kinase-3 regulation by serotonin. Cell Signal. 24, 265-271.(doi:10.1016/j.cellsig.2011.09.009)
27. Lemmon, M. A. & Schlessinger, J. 2010 Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134. (doi:10.1016/j.cell.2010.06.011)
28. Beaulieu, J. M., Sotnikova, T. D., Marion, S., Lefkowitz, R. J., Gainetdinov, R. R. & Caron, M. G. 2005 An Akt/ β-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122, 261-273. (doi:10.1016/j.cell.2005.05.012)
29. Beaulieu, J. M., Tirotta, E., Sotnikova, T. D., Masri, B., Salahpour, A., Gainetdinov, R. R., Borrelli, E. & Caron, M. G. 2007 Regulation of Akt signaling by D2 and D3 dopamine receptors in vivo. J. Neurosci. 27, 881-885.(doi:10.1523/JNEUROSCI.5074-06.2007)
30. Beaulieu, J. M., Gainetdinov, R. R. & Caron, M. G. 2007 The Akt-GSK-3 signaling cascade in the actions of dopamine. Trends Pharmacol. Sci. 28, 166-172.(doi:10.1016/j.tips.2007.02.006)
31. Peineau, S. et al. 2007 LTP inhibits LTD in the hippocampus via regulation of GSK3β. Neuron 53, 703-717. (doi:10.1016/j.neuron.2007.01.029)
32. Beaulieu, J. M., Sotnikova, T. D., Yao, W. D., Kockeritz, L., Woodgett, J. R., Gainetdinov, R. R. & Caron, M. G. 2004 Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc. Natl Acad. Sci. USA 101, 5099-5104. (doi:10.1073/pnas.0307921101)
33. Beaulieu, J. M., Del'guidice, T., Sotnikova, T. D., Lemasson, M. & Gainetdinov, R. R. 2011 Beyond cAMP: the regulation of Akt and GSK3 by dopamine receptors. Front. Mol. Neurosci. 4, 38. (doi:10.3389/fnmol.2011.00038)
34. Emamian, E. S., Hall, D., Birnbaum, M. J., Karayiorgou, M. & Gogos, J. A. 2004 Convergent evidence for impaired AKT1-GSK3β signaling in schizophrenia. Nat. Genet. 36, 131-137. (doi:10.1038/ng126)
35. Beurel, E., Song, L. & Jope, R. S. 2011 Inhibition of glycogen synthase kinase-3 is necessary for the rapid antidepressant effect of ketamine in mice. Mol. Psychiatry 16, 1068-1070. (doi:10.1038/mp.2011.47)
36. Beaulieu, J. M. et al. 2008 A β-arrestin 2 signaling complex mediates lithium action on behavior. Cell 132, 125-136. (doi:10.1016/j.cell.2007.11.041)
37. Beaulieu, J. M. & Caron, M. G. 2008 Looking at lithium: molecular moods and complex behaviour. Mol. Interv. 8, 230-241. (doi:10.1124/mi.8.5.8)
38. Klein, P. S. & Melton, D. A. 1996 A molecular mechanism for the effect of lithium on development. Proc. Natl Acad. Sci. USA 93, 8455-8459. (doi:10.1073/pnas.93.16.8455)
39. Stambolic, V., Ruel, L. & Woodgett, J. R. 1996 Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6, 1664-1668. (doi:10.1016/S0960-9822(02)70790-2)
40. Chalecka-Franaszek, E. & Chuang, D. M. 1999 Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc. Natl Acad. Sci. USA 96, 8745-8750.(doi:10.1073/pnas.96.15.8745)
41. Beaulieu, J. M., Sotnikova, T. D., Gainetdinov, R. R. & Caron, M. G. 2006 Paradoxical striatal cellular signaling responses to psychostimulants in hyperactive mice. J. Biol. Chem. 281, 32072-32080.
42. Kalinichev, M. & Dawson, L. A. 2011 Evidence for antimanic efficacy of glycogen synthase kinase-3 (GSK3) inhibitors in a strain-specific model of acute mania. Int. J. Neuropsychopharmacol. 14, 1051-1067. (doi:10.1017/S1461145710001495)
43. Prickaerts, J., Moechars, D., Cryns, K., Lenaerts, I., van Craenendonck, H., Goris, I., Daneels, G., Bouwknecht, J. A. & Steckler, T. 2006 Transgenic mice over expressing glycogen synthase kinase 3β: a putative model of hyperactivity and mania. J. Neurosci. 26, 9022-9029. (doi:10.1523/JNEUROSCI.5216-05.2006)
44. Hoeflich, K.P., Luo, J., Rubie, E.A., Tsao, M. S., Jin, O. & Woodgett, J. R. 2000 Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 406, 86-90. (doi:10.1038/35017574)
45. Polter, A. et al. 2010 Deficiency in the inhibitory serinephosphorylation of glycogen synthase kinase-3 increases sensitivity to mood disturbances. Neuropsychopharmacology 35, 1761-1774. (doi:10.1038/npp.2010.43)
46. Gould, T. D., Einat, H., Bhat, R. & Manji, H. K. 2004 AR-A014418, a selective GSK-3 inhibitor, produces antidepressant-like effects in the forced swim test. Int. J. Neuropsychopharmacol. 7, 387-390.
47. O'Brien, W. T., Harper, A. D., Jove, F., Woodgett, J. R., Maretto, S., Piccolo, S. & Klein, P. S. 2004 Glycogen synthase kinase-3β haploinsufficiency mimics the behavioral and molecular effects of lithium. J. Neurosci. 24, 6791-6798. (doi:10.1523/JNEUROSCI.4753-03.2004)
48. Beaulieu, J. M., Zhang, X., Rodriguiz, R. M., Sotnikova, T. D., Cools, M. J., Wetsel, W. C., Gainetdinov, R. R. & Caron, M. G. 2008 Reply to Belmaker et al.: GSK3β haploinsufficiency results in lithium-like effects in the forced swim test. Proc. Natl Acad. Sci. USA 105, E24.(doi:10.1073/pnas.0803026105)
49. Mines, M. A., Yuskaitis, C. J., King, M. K., Beurel, E. & Jope, R. S. 2010 GSK3 influences social preference and anxiety-related behaviors during social interaction in a mouse model of fragile X syndrome and autism. PLoS ONE 5, e9706. (doi:10.1371/journal.pone.0009706)
50. Kaidanovich-Beilin, O. et al. 2009 Abnormalities in brain structure and behavior in GSK-3α mutant mice. Mol. Brain 2, 35. (doi:10.1186/1756-6606-2-35)
51. Nadler, J. J. et al. 2004 Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav. 3, 303-314. (doi:10.1111/j.1601-183X.2004.0071.x)
52. Elliott, R., Zahn, R., Deakin, J. F. & Anderson, I. M. 2011 Affective cognition and its disruption in mood disorders. Neuropsychopharmacology 36, 153-182. (doi:10.1038/npp.2010.77)
53. Takahashi, A., Quadros, I. M., de Almeida, R. M. & Miczek, K. A. 2011 Brain serotonin receptors and transporters: initiation versus termination of escalated aggression. Psychopharmacology (Berl.) 213, 183-212. (doi:10.1007/s00213-010-2000-y)
54. Roberts, A. C. 2011 The importance of serotonin for orbitofrontal function. Biol. Psychiatry 69, 1185-1191. (doi:10.1016/j.biopsych.2010.12.037)
55. Huang, Z. J., Yu, W., Lovett, C. & Tonegawa, S. 2002 Cre/loxP recombination-activated neuronal markers in mouse neocortex and hippocampus. Genesis 32, 209-217. (doi:10.1002/gene.10054)
56. Patel, S., Doble, B. W., MacAulay, K., Sinclair, E. M., Drucker, D. J. & Woodgett, J. R. 2008 Tissue-specificrole of glycogen synthase kinase 3b in glucos e homeostasis and insulin action. Mol. Cell Biol. 28, 6314-6328.(doi:10.1128/MCB.00763-08)
57. Beaulieu, J. M. & Julien, J. P. 2003 Peripherin-mediated death of motor neurons rescued by overexpression of neurofilament NF-H proteins. J. Neurochem. 85, 248-256. (doi:10.1046/j.1471-4159.2003.01653.x)
58. Crowley, J. J., Jones, M. D., O'Leary, O. F. & Lucki, I. 2004 Automated tests for measuring the effects of antidepressants in mice. Pharmacol. Biochem. Behav. 78, 269-274. (doi:10.1016/j.pbb.2004.03.014)
59. Moy, S. S., Nadler, J. J., Perez, A., Barbaro, R. P., Johns, J. M., Magnuson, T. R., Piven, J. & Crawley, J. N. 2004 Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 3, 287-302. (doi:10.1111/j.1601-1848.2004.00076.x)
60. Guitton, M. J., Klin, Y. & Dudai, Y. 2008 Tastedependent sociophobia: when food and company do not mix. Behav. Brain Res. 191, 148-152. (doi:10.1016/j.bbr.2008.03.022)
61. Berton, O. et al. 2006 Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868. (doi:10.1126/science.1120972)
62. Patel, S., Macaulay, K. & Woodgett, J. R. 2011 Tissue specific analysis of glycogen synthase kinase-3α (GSK-3α) in glucose metabolism: effect of strain variation. PLoS ONE 6, e15845. (doi:10.1371/journal.pone.0015845)
63. Giros, B., Jaber, M., Jones, S. R., Wightman, R. M. & Caron, M. G. 1996 Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379, 606-612. (doi:10.1038/379606a0)
64. Kaidanovich-Beilin, O., Milman, A., Weizman, A., Pick, C. G. & Eldar-Finkelman, H. 2004 Rapid antidepressive- like activity of specific glycogen synthase kinase-3 inhibitor and its effect on b-catenin in mouse hippocampus. Biol. Psychiatry 55, 781-784. (doi:10.1016/j.biopsych.2004.01.008)
65. Gould, T. D., O'Donnell, K. C., Picchini, A. M. & Manji, H. K. 2007 Strain differences in lithium attenuation of d-amphetamine-induced hyper locomotion: a mouse model for the genetics of clinical response to lithium. Neuro psychopharmacology 32, 1321-1333. (doi:10.1038/sj.npp.1301254)
66. Wilkinson, M. B. et al. 2011 A novel role of the WNTdishevelled- GSK3β signaling cascade in the mouse nucleus accumbens in a social defeat model of depression. J. Neurosci. 31, 9084-9092. (doi:10.1523/JNEUROSCI.0039-11.2011)
67. Kimura, T., Yamashita, S., Nakao, S., Park, J. M., Murayama, M., Mizoroki, T., Yoshiike, Y., Sahara, N. & Takashima, A. 2008 GSK-3β is required for memory reconsolidation in adult brain. PLoS ONE 3, e3540. (doi:10.1371/journal.one.0003540)
68. Meltzer, H. Y. 1991 The mechanism of action of novel antipsychotic drugs. Schizophr. Bull. 17, 263-287.
69. Beaulieu, J. M. & Gainetdinov, R. R. 2011 The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol. Rev. 63, 182-217. (doi:10.1124/pr.110.002642)
70. Carlsson, A., Waters, N., Holm-Waters, S., Tedroff, J., Nilsson, M. & Carlsson, M. L. 2001 Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. Annu. Rev. Pharmacol. Toxicol. 41, 237-260. (doi:10.1146/annurev.pharmtox.41.1.237)
71. Du, J. et al. 2010 A kinesin signaling complex mediates the ability of GSK-3β to affect mood-associated behaviors. Proc. Natl Acad. Sci. USA 107, 11573-11578.
72. Jones, S. R., Gainetdinov, R. R., Wightman, R. M. & Caron, M. G. 1998 Mechanisms of amphetamine action revealed in mice lacking the dopamine transporter. J. Neurosci. 18, 1979-1986.
73. Bateup, H. S., Santini, E., Shen, W., Birnbaum, S., Valjent, E., Surmeier, D. J., Fisone, G., Nestler, E. J. & Greengard, P. 2010 Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc. Natl Acad. Sci. USA 107, 14845-14850.(doi:10.1073/pnas.1009874107)
74. Liu, H. Y., Potter, M. P., Woodworth, K. Y., Yorks, D. M., Petty, C. R., Wozniak, J. R., Faraone, S. V. & Biederman, J. 2011 Pharmacologic treatments for pediatric bipolar disorder: a review and meta-analysis. J. Am. Acad. Child Adolesc. Psychiatry 50, 749-762 e739. (doi:10.1016/j.jaac.2011.05.011)
75. Weerasinghe, G. R., Seemann, R., Rapoport, S. I. & Bosetti, F. 2003 Lithium chloride, administered chronically to rats, does not affect the fractional phosphorylation of brain cytosolic phospholipase A2, while reducing its net protein level. Brain Res. Bull. 59, 303-306. (doi:10.1016/S0361-9230(02)00913-9)
76. Menard, J. & Treit, D. 1999 Effects of centrally administered anxiolytic compounds in animal models of anxiety. Neurosci. Biobehav. Rev. 23, 591-613. (doi:10.1016/S0149-7634(98)00056-6)
77. York, R. L., Holinga, G. J., Guyer, D. R., McCrea, K. R., Ward, R. S. & Somorjai, G. A. 2008 A new optical parametric amplifier based on lithium thioindate used for sum frequency generation vibrational spectroscopic studies of the amide I mode of an interfacial model peptide. Appl. Spectrosc. 62, 937-940. (doi:10.1366/000370208785793227)
78. Ramboz, S., Oosting, R., Amara, D. A., Kung, H. F., Blier, P., Mendelsohn, M., Mann, J. J., Brunner, D. & Hen, R. 1998 Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc. Natl Acad. Sci. USA 95, 14476-14481. (doi:10.1073/pnas.95.24.14476)
79. Rao, J. S., Rapoport, S. I. & Bosetti, F. 2005 Decrease in the AP-2 DNA-binding activity and in the protein expression of AP-2 α and AP-2 β in frontal cortex of rats treated with lithium for 6 weeks. Neuropsychopharmacology 30, 2006-2013. (doi:10.1038/sj.npp.1300740)
80. Beurel, E. & Jope, R. S. 2009 Lipo polysaccharideinduced interleukin-6 production is controlled by glycogen synthase kinase-3 and STAT3 in the brain. J. Neuroinflammation 6, 9. (doi:10.1186/1742-2094-6-9)
81. Polter, A., Yang, S., Zmijewska, A. A., van Groen, T., Paik, J. H., Depinho, R. A., Peng, S. L., Jope, R. S. & Li, X. 2009 Forkhead box, class O transcription factors in brain: regulation and behavioral manifestation. Biol. Psychiatry 65, 150-159. (doi:10.1016/j.biopsych.2008.08.005)
82. Li, Y. C., Xi, D., Roman, J., Huang, Y. Q. & Gao, W. J. 2009 Activation of glycogen synthase kinase-3β is required for hyperdopamine and D2 receptor-mediated inhibition of synaptic NMDA receptor function in the rat prefrontal cortex. J. Neurosci. 29, 15551-15563.(doi:10.1523/JNEUROSCI.3336-09.2009)
83. Peineau, S., Bradley, C., Taghibiglou, C., Doherty, A., Bortolotto, Z. A., Wang, Y. T. & Collingridge, G. L. 2008 The role of GSK-3 in synaptic plasticity. Br. J. Pharmacol. 153(Suppl 1), S428-437.