Second messenger/signal transduction pathways in major mood disorders: Moving from membrane to mechanism of action, part II: Bipolar disorder

CNS Spectrums

Volumn 18, Issue 5, 2013, Pages 242-251

  Niciu, Mark J ^a   Ionescu, Dawn F ^a   Mathews, Daniel C ^a   Richards, Erica M ^a   Zarate, Carlos A ^a,b  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Bipolar disorder; intracellular cascades; lithium; mood stabilizers; second messenger; signal transduction

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DISHEVELLED 1; FRIZZLED PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITIDE; PLACEBO; PRAMIPEXOLE; PROTEIN BCL 2; PROTEIN KINASE C; TAMOXIFEN; VALPROIC ACID; WNT PROTEIN; X BOX BINDING PROTEIN 1;

BIPOLAR DISORDER; BIPOLAR II DISORDER; CELL SURVIVAL; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; DRUG SAFETY; ENZYME INHIBITION; HUMAN; MANIA; MITOCHONDRION; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

BIPOLAR DISORDER; HUMANS; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION;

EID: 84884650663     PISSN: 10928529     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1092852913000138     Document Type: Review

References (76)

1. Allison JH, Stewart MA. Reduced brain inositol in lithium-treated rats. Nat New Biol. 1971; 233(43): 267-268.
2. Machado-Vieira R, Manji HK, Zarate CA, Jr. The role of lithium in the treatment of bipolar disorder: convergent evidence for neurotrophic effects as a unifying hypothesis. Bipolar Disord. 2009; 11(suppl 2): 92-109.
3. Chen G, Manji HK, Wright CB, Hawver DB, Potter WZ. Effects of valproic acid on beta-adrenergic receptors, G-proteins, and adenylyl cyclase in rat C6 glioma cells. Neuropsychopharmacology. 1996; 15(3): 271-280. (Pubitemid 26285657)
4. Bosetti F, Bell JM, Manickam P. Microarray analysis of rat brain gene expression after chronic administration of sodium valproate. Brain Res Bull. 2005; 65(4): 331-338. (Pubitemid 41057803)
5. Ertley RN, Bazinet RP, Lee HJ, Rapoport SI, Rao JS. Chronic treatment with mood stabilizers increases membrane GRK3 in rat frontal cortex. Biol Psychiatry. 2007; 61(2): 246-249. (Pubitemid 46072779)
6. Post RM, Ballenger JC, Uhde TW, et al. Effect of carbamazepine on cyclic nucleotides in CSF of patients with affective illness. Biol Psychiatry. 1982; 17(9): 1037-1045. (Pubitemid 12035396)
7. Young LT, Li PP, Kish SJ, Siu KP, Warsh JJ. Postmortem cerebral cortex Gs alpha-subunit levels are elevated in bipolar affective disorder. Brain Res. 1991; 553(2): 323-326.
8. Friedman E, Wang HY. Receptor-mediated activation of G proteins is increased in postmortem brains of bipolar affective disorder subjects. J Neurochem. 1996; 67(3): 1145-1152. (Pubitemid 26277927)
9. Young LT, Li PP, Kamble A, Siu KP, Warsh JJ. Mononuclear leukocyte levels of G proteins in depressed patients with bipolar disorder or major depressive disorder. Am J Psychiatry. 1994; 151(4): 594-596. (Pubitemid 24115828)
10. Schreiber G, Avissar S, Danon A, Belmaker RH. Hyperfunctional G proteins in mononuclear leukocytes of patients with mania. Biol Psychiatry. 1991; 29(3): 273-280.
11. Spleiss O, van Calker D, Scharer L, et al. Abnormal G protein alpha(s)-and alpha(i2)-subunit mRNA expression in bipolar affective disorder. Mol Psychiatry. 1998; 3(6): 512-520.
12. Fields A, Li PP, Kish SJ, Warsh JJ. Increased cyclic AMP-dependent protein kinase activity in postmortem brain from patients with bipolar affective disorder. J Neurochem. 1999; 73: 1704-1710. (Pubitemid 29440174)
13. Chang A, Li PP, Warsh JJ. Altered cAMP-dependent protein kinase subunit immunolabeling in post-mortem brain from patients with bipolar affective disorder. J Neurochem. 2003; 84(4): 781-791. (Pubitemid 36176936)
14. Tardito D, Mori S, Racagni G, et al. Protein kinase A activity in platelets from patients with bipolar disorder. J Affect Disord. 2003; 76(1-3): 249-253. (Pubitemid 37013377)
15. Karege F, Schwald M, Papadimitriou P, Lachausse C, Cisse M. The cAMP-dependent protein kinase A and brain-derived neurotrophic factor expression in lymphoblast cells of bipolar affective disorder. J Affect Disord. 2004; 79(1-3): 187-192. (Pubitemid 38340542)
16. Ryan MM, Lockstone HE, Huffaker SJ, et al. Gene expression analysis of bipolar disorder reveals downregulation of the ubiquitin cycle and alterations in synaptic genes. Mol Psychiatry. 2006; 11(10): 965-978. (Pubitemid 44470218)
17. McDonald ML, Macmullen C, Liu DJ, Leal SM, Davis RL. Genetic association of cyclic AMP signaling genes with bipolar disorder. Transl Psychiatry. 2012; 2: e169.
18. Manji HK, Lenox RH. Signaling: cellular insights into the pathophysiology of bipolar disorder. Biol Psychiatry. 2000; 48(6): 518-530.
19. Sadana R, Dessauer CW. Physiological roles for G protein-regulated adenylyl cyclase isoforms: insights from knockout and overexpression studies. Neurosignals. 2009; 17(1): 5-22.
20. Ozaki N, Chuang DM. Lithium increases transcription factor binding to AP-1 and cyclic AMP-responsive element in cultured neurons and rat brain. J Neurochem. 1997; 69(6): 2336-2344. (Pubitemid 27495418)
21. Tardito D, Tiraboschi E, Kasahara J, Racagni G, Popoli M. Reduced CREB phosphorylation after chronic lithium treatment is associated with down-regulation of CaM kinase IV in rat hippocampus. Int J Neuropsychopharmacol. 2007; 10(4): 491-496. (Pubitemid 46985256)
22. Ferrendelli JA, Kinscherf DA. Inhibitory effects of anticonvulsant drugs on cyclic nucleotide accumulation in brain. Ann Neurol. 1979; 5(6): 533-538. (Pubitemid 9183592)
23. Van Calker D, Steber R, Klotz KN, Greil W. Carbamazepine distinguishes between adenosine receptors that mediate different second messenger responses. Eur J Pharmacol. 1991; 206(4): 285-290.
24. Basselin M, Chang L, Chen M, Bell JM, Rapoport SI. Chronic carbamazepine administration attenuates dopamine D2-like receptor-initiated signaling via arachidonic acid in rat brain. Neurochem Res. 2008; 33(7): 1373-1383.
25. Di Daniel E, Mudge AW, Maycox PR. Comparative analysis of the effects of four mood stabilizers in SH-SY5Y cells and in primary neurons. Bipolar Disord. 2005; 7(1): 33-41. (Pubitemid 40227834)
26. Xie N, Wang C, Lin Y, et al. The role of p38 MAPK in valproic acid induced microglia apoptosis. Neurosci Lett. 2010; 482(1): 51-56.
27. Tsui MM, Tai WC, Wong WY, Hsiao WL. Selective G2/M arrest in a p53(Val135)-transformed cell line induced by lithium is mediated through an intricate network of MAPK and beta-catenin signaling pathways. Life Sci. 2012; 91(9-10): 312-321.
28. Einat H, Yuan P, Gould TD, et al. The role of the extracellular signal-regulated kinase signaling pathway in mood modulation. J Neurosci. 2003; 23(19): 7311-7316. (Pubitemid 36999520)
29. Shimon H, Agam G, Belmaker RH, Hyde TM, Kleinman JE. Reduced frontal cortex inositol levels in postmortem brain of suicide victims and patients with bipolar disorder. Am J Psychiatry. 1997; 154(8): 1148-1150. (Pubitemid 27328834)
30. Jope RS, Song L, Li PP, et al. The phosphoinositide signal transduction system is impaired in bipolar affective disorder brain. J Neurochem. 1996; 66(6): 2402-2409. (Pubitemid 26159075)
31. Brown AS, Mallinger AG, Renbaum LC. Elevated platelet membrane phosphatidylinositol-4,5-bisphosphate in bipolar mania. Am J Psychiatry. 1993; 150(8): 1252-1254. (Pubitemid 23218911)
32. Baum AE, Akula N, Cabanero M, et al. A genome-wide association study implicates diacylglycerol kinase eta (DGKH) and several other genes in the etiology of bipolar disorder. Mol Psychiatry. 2008; 13(2): 197-207.
33. Xu C, Li PP, Cooke RG, et al. TRPM2 variants and bipolar disorder risk: confirmation in a family-based association study. Bipolar Disord. 2009; 11(1): 1-10.
34. Xu C, Warsh JJ, Wang KS, Mao CX, Kennedy JL. Association of the iPLA2beta gene with bipolar disorder and assessment of its interaction with TRPM2 gene polymorphisms. Psychiatr Genet. In press.
35. Wang HY, Friedman E. Enhanced protein kinase C activity and translocation in bipolar affective disorder brains. Biol Psychiatry. 1996; 40(7): 568-575. (Pubitemid 26356388)
36. Wang H, Friedman E. Increased association of brain protein kinase C with the receptor for activated C kinase-1 (RACK1) in bipolar affective disorder. Biol Psychiatry. 2001; 50(5): 364-370. (Pubitemid 32816950)
37. Friedman E, Hoau Yan W, Levinson D, Connell TA, Singh H. Altered platelet protein kinase C activity in bipolar affective disorder, manic episode. Biol Psychiatry. 1993; 33(7): 520-525. (Pubitemid 23167218)
38. Wang HY, Markowitz P, Levinson D, Undie AS, Friedman E. Increased membrane-associated protein kinase C activity and translocation in blood platelets from bipolar affective disorder patients. J Psychiatr Res. 1999; 33(2): 171-179. (Pubitemid 29134745)
39. Pandey GN, Dwivedi Y, SridharaRao J, et al. Protein kinase C and phospholipase C activity and expression of their specific isozymes is decreased and expression of MARCKS is increased in platelets of bipolar but not in unipolar patients. Neuropsychopharmacology. 2002; 26(2): 216-228. (Pubitemid 34093084)
40. Yoon IS, Li PP, Siu KP, et al. Altered IMPA2 gene expression and calcium homeostasis in bipolar disorder. Mol Psychiatry. 2001; 6(6): 678-683. (Pubitemid 33020587)
41. Manji HK, Etcheberrigaray R, Chen G, Olds JL. Lithium decreases membrane-associated protein kinase C in hippocampus: selectivity for the alpha isozyme. J Neurochem. 1993; 61(6): 2303-2310. (Pubitemid 23354093)
42. Chen G, Masana MI, Manji HK. Lithium regulates PKC-mediated intracellular cross-talk and gene expression in the CNS in vivo. Bipolar Disord. 2000; 2(3 pt. 2): 217-236.
43. Lenox RH, Watson DG, Patel J, Ellis J. Chronic lithium administration alters a prominent PKC substrate in rat hippocampus. Brain Res. 1992; 570(1-2): 333-340.
44. Szabo ST, Machado-Vieira R, Yuan P, et al. Glutamate receptors as targets of protein kinase C in the pathophysiology and treatment of animal models of mania. Neuropharmacology. 2009; 56(1): 47-55.
45. Chen G, Manji HK, Hawver DB, Wright CB, Potter WZ. Chronic sodium valproate selectively decreases protein kinase C alpha and epsilon in vitro. J Neurochem. 1994; 63(6): 2361-2364.
46. Watson DG, Watterson JM, Lenox RH. Sodium valproate down-regulates the myristoylated alanine-rich C kinase substrate (MARCKS) in immortalized hippocampal cells: a property of protein kinase C-mediated mood stabilizers. J Pharmacol Exp Ther. 1998; 285(1): 307-316. (Pubitemid 28207601)
47. Hasegawa H, Osada K, Misonoo A, et al. Chronic carbamazepine treatment increases myristoylated alanine-rich C kinase substrate phosphorylation in the rat cerebral cortex via down-regulation of calcineurin A alpha. Brain Res. 2003; 994(1): 19-26. (Pubitemid 37452433)
48. Einat H, Yuan P, Szabo ST, Dogra S, Manji HK. Protein kinase C inhibition by tamoxifen antagonizes manic-like behavior in rats: implications for the development of novel therapeutics for bipolar disorder. Neuropsychobiology. 2007; 55(3-4): 123-131. (Pubitemid 47525230)
49. Bebchuk JM, Arfken CL, Dolan-Manji S, et al. A preliminary investigation of a protein kinase C inhibitor in the treatment of acute mania. Arch Gen Psychiatry. 2000; 57(1): 95-97.
50. Kulkarni J, Garland KA, Scaffidi A, et al. A pilot study of hormone modulation as a new treatment for mania in women with bipolar affective disorder. Psychoneuroendocrinology. 2006; 31(4): 543-547. (Pubitemid 43375956)
51. Zarate CA, Jr., Singh JB, Carlson PJ, et al. Efficacy of a protein kinase C inhibitor (tamoxifen) in the treatment of acute mania: a pilot study. Bipolar Disord. 2007; 9(6): 561-570. (Pubitemid 47365623)
52. Yildiz A, Guleryuz S, Ankerst DP, Ongur D, Renshaw PF. Protein kinase C inhibition in the treatment of mania: a double-blind, placebo-controlled trial of tamoxifen. Arch Gen Psychiatry. 2008; 65(3): 255-263. (Pubitemid 351342442)
53. Sylvia LG, Peters AT, Deckersbach T, Nierenberg AA. Nutrient-based therapies for bipolar disorder: a systematic review. Psychother Psychosom. 2013; 82(1): 10-19.
54. van Calker D, Belmaker RH. The high affinity inositol transport system-implications for the pathophysiology and treatment of bipolar disorder. Bipolar Disord. 2000; 2(2): 102-107.
55. Willmroth F, Drieling T, Lamla U, et al. Sodium-myoinositol co-transporter (SMIT-1) mRNA is increased in neutrophils of patients with bipolar 1 disorder and down-regulated under treatment with mood stabilizers. Int J Neuropsychopharmacol. 2007; 10(1): 63-71. (Pubitemid 46122753)
56. Shaldubina A, Johanson RA, O'Brien WT, et al. SMIT1 haploinsufficiency causes brain inositol deficiency without affecting lithium-sensitive behavior. Mol Genet Metab. 2006; 88(4): 384-388. (Pubitemid 44107766)
57. Klein PS, Melton DA. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA. 1996; 93(16): 8455-8459. (Pubitemid 26269579)
58. Chen G, Huang LD, Jiang YM, Manji HK. The moodstabilizing agent valproate inhibits the activity of glycogen synthase kinase-3. J Neurochem. 1999; 72(3): 1327-1330. (Pubitemid 29085050)
59. Roh MS, Kang UG, Shin SY, et al. Biphasic changes in the Ser-9 phosphorylation of glycogen synthase kinase-3beta after electroconvulsive shock in the rat brain. Prog Neuropsychopharmacol Biol Psychiatry. 2003; 27(1): 1-5. (Pubitemid 36126640)
60. Polter A, Beurel E, Yang S, et al. Deficiency in the inhibitory serine-phosphorylation of glycogen synthase kinase-3 increases sensitivity to mood disturbances. Neuropsychopharmacology. 2010; 35(8): 1761-1774.
61. Gould TD, Einat H, O'Donnell KC, et al. Beta-catenin overexpression in the mouse brain phenocopies lithium-sensitive behaviors. Neuropsychopharmacology. 2007; 32(10): 2173-2183. (Pubitemid 47417687)
62. Benes FM, Matzilevich D, Burke RE, Walsh J. The expression of proapoptosis genes is increased in bipolar disorder, but not in schizophrenia. Mol Psychiatry. 2006; 11(3): 241-251.
63. Kim HW, Rapoport SI, Rao JS. Altered expression of apoptotic factors and synaptic markers in postmortem brain from bipolar disorder patients. Neurobiol Dis. 2010; 37(3): 596-603.
64. Bei E, Salpeas V, Pappa D, et al. Phosphorylation status of glucocorticoid receptor, heat shock protein 70, cytochrome c and Bax in lymphocytes of euthymic, depressed and manic bipolar patients. Psychoneuroendocrinology. 2009; 34(8): 1162-1175.
65. Machado-Vieira R, Pivovarova NB, Stanika RI, et al. The Bcl-2 gene polymorphism rs956572AA increases inositol 1,4,5-trisphosphate receptor-mediated endoplasmic reticulum calcium release in subjects with bipolar disorder. Biol Psychiatry. 2011; 69(4): 344-352.
66. Soeiro-de-Souza MG, Salvadore G, Moreno RA, et al. Bcl-2 rs956572 polymorphism is associated with increased anterior cingulate cortical glutamate in euthymic bipolar I disorder. Neuropsychopharmacology. 2013; 38(3): 468-475.
67. Kakiuchi C, Iwamoto K, Ishiwata M, et al. Impaired feedback regulation of XBP1 as a genetic risk factor for bipolar disorder. Nat Genet. 2003; 35(2): 171-175. (Pubitemid 37187636)
68. So J, Warsh JJ, Li PP. Impaired endoplasmic reticulum stress response in B-lymphoblasts from patients with bipolar-I disorder. Biol Psychiatry. 2007; 62(2): 141-147. (Pubitemid 46963251)
69. Hayashi A, Kasahara T, Kametani M, et al. Aberrant endoplasmic reticulum stress response in lymphoblastoid cells from patients with bipolar disorder. Int J Neuropsychopharmacol. 2009; 12(1): 33-43.
70. Kim B, Kim CY, Lee MJ, Joo YH. Preliminary evidence on the association between XBP1-116C/G polymorphism and response to prophylactic treatment with valproate in bipolar disorders. Psychiatry Res. 2009; 168(3): 209-212.
71. Song L, Zhou T, Jope RS. Lithium facilitates apoptotic signaling induced by activation of the Fas death domaincontaining receptor. BMC Neurosci. 2004; 5: 20.
72. Gomez-Sintes R, Lucas JJ. NFAT/Fas signaling mediates the neuronal apoptosis and motor side effects of GSK-3 inhibition in a mouse model of lithium therapy. J Clin Invest. 2010; 120(7): 2432-2445.
73. Li R, El-Mallahk RS. A novel evidence of different mechanisms of lithium and valproate neuroprotective action on human SY5Y neuroblastoma cells: caspase-3 dependency. Neurosci Lett. 2000; 294(3): 147-150.
74. Lowthert L, Leffert J, Lin A, et al. Increased ratio of antiapoptotic to pro-apoptotic Bcl2 gene-family members in lithium-responders one month after treatment initiation. Biol Mood Anxiety Disord. 2012; 2(1): 15.
75. Zarate CA, Jr., Payne JL, Singh J, et al. Pramipexole for bipolar II depression: a placebo-controlled proof of concept study. Biol Psychiatry. 2004; 56(1): 54-60. (Pubitemid 38813406)
76. Danial NN, Gimenez-Cassina A, Tondera D. Homeostatic functions of BCL-2 proteins beyond apoptosis. Adv Exp Med Biol. 2010; 687: 1-32.