Effects of mood-stabilizing drugs on dendritic outgrowth and synaptic protein levels in primary hippocampal neurons

Bipolar Disorders

Volumn 17, Issue 3, 2015, Pages 278-290

  Park, Sung Woo ^a   Lee, Jung Goo ^a,b   Seo, Mi Kyoung ^a   Cho, Hye Yeon ^a   Lee, Chan Hong ^a   Lee, Ji Heon ^b   Lee, Bong Ju ^b   Baek, Jun Hyung ^b   Seol, Wongi ^c   Kim, Young Hoon ^a,b  

^a Inje University   (South Korea)

^b Inje University College of Medicine   (South Korea)

^c Wonkwang University   (South Korea)

Author keywords

Dendritic outgrowth; Mood stabilizing drugs; Neural plasticity; Signaling; Synaptic proteins

Indexed keywords

BETA NEUREXIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CARBAMAZEPINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; LAMOTRIGINE; LITHIUM; MITOGEN ACTIVATED PROTEIN KINASE; NEUREXIN; NEUROLIGIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN; SYNAPTIC PROTEIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; VALPROIC ACID; DLGH4 PROTEIN, RAT; LITHIUM DERIVATIVE; MEMBRANE PROTEIN; NERVE CELL ADHESION MOLECULE; NEUROPROTECTIVE AGENT; SIGNAL PEPTIDE; SYP PROTEIN, RAT; TRANQUILIZER; TRIAZINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL DENSITY; CELL VIABILITY; CONTROLLED STUDY; DENDRITIC CELL; DENDRITIC OUTGROWTH; DRUG EFFECT; EMBRYO; NERVE CELL GROWTH; NERVE CELL PLASTICITY; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; BIPOLAR DISORDER; CYTOLOGY; DENDRITE; DRUG EFFECTS; HIPPOCAMPUS; METABOLISM; NERVE CELL;

ANIMALS; ANTIMANIC AGENTS; BIPOLAR DISORDER; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL ADHESION MOLECULES, NEURONAL; DENDRITES; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LITHIUM COMPOUNDS; MEMBRANE PROTEINS; NEURONS; NEUROPROTECTIVE AGENTS; PHOSPHATIDYLINOSITOL 3-KINASES; RATS; SYNAPTOPHYSIN; TRIAZINES; VALPROIC ACID;

EID: 84928213481     PISSN: 13985647     EISSN: 13995618     Source Type: Journal    
DOI: 10.1111/bdi.12262     Document Type: Article

References (70)

1. Young AH, Macpherson H. Detection of bipolar disorder. Br J Psychiatry 2011; 199: 3-4.
2. Martinowich K, Schloesser RJ, Manji HK. Bipolar disorder: from genes to behavior pathways. J Clin Invest 2009; 119: 726-736.
3. Manji HK, Duman RS. Impairments of neuroplasticity and cellular resilience in severe mood disorders: implications for the development of novel therapeutics. Psychopharmacol Bull 2001; 35: 5-49.
4. Schloesser RJ, Martinowich K, Manji HK. Mood-stabilizing drugs: mechanisms of action. Trends Neurosci 2012; 35: 36-46.
5. Rajkowska G. Cell pathology in bipolar disorder. Bipolar Disord 2002; 4: 105-116.
6. Strakowski SM, Delbello MP, Adler CM. The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Mol Psychiatry 2005; 10: 105-116.
7. Vawter MP, Freed WJ, Kleinman JE. Neuropathology of bipolar disorder. Biol Psychiatry 2000; 48: 486-504.
8. Carlson PJ, Singh JB, Zarate CA Jr et al. Neural circuitry and neuroplasticity in mood disorders: insights for novel therapeutic targets. NeuroRx 2006; 3: 22-41.
9. Goodwin GM. Consensus Group of the British Association for Psychopharmacology. Evidence-based guidelines for treating bipolar disorder: recommendations from the British Association for Psychopharmacology. J Psychopharmacol 2003; 17: 149-173.
10. Goodwin GM, Malhi GS. What is a mood stabilizer? Psychol Med 2007; 37: 609-614.
11. Calabrese JR, Rapport DJ, Youngstrom EA et al. New data on the use of lithium, divalproate, and lamotrigine in rapid cycling bipolar disorder. Eur Psychiatry 2005; 20: 92-95.
12. Bachmann RF, Schloesser RJ, Gould TD et al. Mood stabilizers target cellular plasticity and resilience cascades: implications for the development of novel therapeutics. Mol Neurobiol 2005; 32: 173-202.
13. Papadopoulos CM, Tsai SY, Guillen V et al. Motor recovery and axonal plasticity with short-term amphetamine after stroke. Stroke 2009; 40: 294-302.
14. Tang BL. Protein trafficking mechanisms associated with neurite outgrowth and polarized sorting in neurons. J Neurochem 2001; 79: 923-930.
15. Sassi RB, Nicoletti M, Brambilla P et al. Increased gray matter volume in lithium-treated bipolar disorder patients. Neurosci Lett 2002; 329: 243-245.
16. Pang L, Sawada T, Decker SJ et al. Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J Biol Chem 1995; 270: 13585-13588.
17. Kobayashi M, Nagata S, Kita Y et al. Expression of a constitutively active phosphatidylinositol 3-kinase induces process formation in rat PC12 cells. Use of Cre/loxP recombination system. J Biol Chem 1997; 272: 16089-16092.
18. Sánchez S, Jiménez C, Carrera AC et al. A cAMP-activated pathway, including PKA and PI3K, regulates neuronal differentiation. Neurochem Int 2004; 44: 231-242.
19. Sanchez S, Sayas CL, Lim F et al. The inhibition of phosphatidylinositol-3-kinase induces neurite retraction and activates GSK3. J Neurochem 2001; 78: 468-481.
20. Ji Y, Pang PT, Feng L et al. Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Nat Neurosci 2005; 8: 164-172.
21. Lessmann V, Gottmann K, Malcangio M. Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 2003; 69: 341-374.
22. Poo MM. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2001; 2: 24-32.
23. Lonze BE, Ginty DD. Function and regulation of CREB family transcription factors in the nervous system. Neuron 2002; 35: 605-623.
24. Washbourne P, Dityatev A, Scheiffele P et al. Cell adhesion molecules in synapse formation. J Neurosci 2004; 24: 9244-9249.
25. Kim E, Sheng M. PDZ domain proteins of synapses. Nat Rev Neurosci 2004; 5: 771-781.
26. Ehrlich I, Klein M, Rumpel S et al. PSD-95 is required for activity-driven synapse stabilization. Proc Natl Acad Sci USA 2007; 104: 4176-4181.
27. Han K, Kim E. Synaptic adhesion molecules and PSD-95. Prog Neurobiol 2008; 84: 263-283.
28. Dean C, Scholl FG, Choih J et al. Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 2003; 6: 708-716.
29. Rao A, Harms KJ, Craig AM. Neuroligation: building synapses around the neurexin-neuroligin link. Nat Neurosci 2000; 3: 747-749.
30. Wiedenmann B. Synaptophysin. A widespread constituent of small neuroendocrine vesicles and a new tool in tumor diagnosis. Acta Oncol 1991; 30: 435-440.
31. Bastianetto S, Danik M, Mennicken F et al. Prototypical antipsychotic drugs protect hippocampal neuronal cultures against cell death induced by growth medium deprivation. BMC Neurosci 2006; 30: 7-28.
32. Park SW, Lee CH, Cho HY et al. Effects of antipsychotic drugs on the expression of synaptic proteins and dendritic outgrowth in hippocampal neuronal cultures. Synapse 2013; 67: 224-234.
33. Kaech S, Banker G. Culturing hippocampal neurons. Nat Protoc 2006; 1: 2406-2415.
34. Brewer GJ, Torricelli JR, Evege EK et al. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 1993; 35: 567-576.
35. 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: 33-41.
36. Fröscher W, Keller F, Vogt H et al. Prospective study on concentration-efficacy and concentration-toxicity: correlations with lamotrigine serum levels. Epileptic Disord 2002; 4: 49-56.
37. Lom B, Cohen-Cory S. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J Neurosci 1999; 19: 9928-9938.
38. Klimaschewski L, Nindl W, Pimpl M et al. Biolistic transfection and morphological analysis of cultured sympathetic neurons. J Neurosci Methods 2002; 113: 63-71.
39. Lalli G, Hall A. Ral GTPases regulate neurite branching through GAP-43 and the exocyst complex. J Cell Biol 2005; 171: 857-869.
40. Wang Z, Wang J, Li J, Wang X et al. MEK/ERKs signaling is essential for lithium-induced neurite outgrowth in N2a cells. Int J Dev Neurosci 2011; 29: 415-422.
41. Mizutani R, Yamauchi J, Kusakawa S et al. Sorting nexin 3, a protein upregulated by lithium, contains a novel phosphatidylinositol-binding sequence and mediates neurite outgrowth in N1E-115 cells. Cell Signal 2009; 21: 1586-1594.
42. Laeng P, Pitts RL, Lemire AL et al. The mood stabilizer valproic acid stimulates GABA neurogenesis from rat forebrain stem cells. J Neurochem 2004; 91: 238-251.
43. Cross DA, Alessi DR, Cohen P et al. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995; 378: 785-789.
44. De Sarno P, Li X, Jope RS. Regulation of Akt and glycogen synthase kinase-3 beta phosphorylation by sodium valproate and lithium. Neuropharmacology 2002; 43: 1158-1164.
45. Jope RS, Bijur GN. Mood stabilizers, glycogen synthase kinase-3beta and cell survival. Mol Psychiatry 2002; 7: S35-S45.
46. Aubry JM, Schwald M, Ballmann E et al. Early effects of mood stabilizers on the Akt/GSK-3beta signaling pathway and on cell survival and proliferation. Psychopharmacology 2009; 205: 419-429.
47. Yuan PX, Huang LD, Jiang YM et al. The mood stabilizer valproic acid activates mitogen-activated protein kinases and promotes neurite growth. J Biol Chem 2001; 276: 31674-31683.
48. Mai L, Jope RS, Li X. BDNF-mediated signal transduction is modulated by GSK3beta and mood stabilizing agents. J Neurochem 2002; 82: 75-83.
49. Jope RS. A bimodal model of the mechanism of action of lithium. Mol Psychiatry 1999; 4: 21-25.
50. Lorenzi C, Pirovano A, Bosia M. Molecular mechanisms of lithium salts in enhancement of cAMP-stimulated CREB-dependent gene transcription. Pharmacogenomics 2013; 14: 127-128.
51. Biermann J, Grieshaber P, Goebel U et al. Valproic acid-mediated neuroprotection and regeneration in injured retinal ganglion cells. Invest Ophthalmol Vis Sci 2010; 51: 526-534.
52. Lewin E, Bleck V. Cyclic AMP accumulation in cerebral cortical slices: effect of carbamazepine, phenobarbital, and phenytoin. Epilepsia 1977; 18: 237-242.
53. Manji HK, Chen G, Hsiao JK et al. Regulation of signal transduction pathways by mood-stabilizing agents: implications for the delayed onset of therapeutic efficacy. J Clin Psychiatry 1996; 13: 34-46.
54. 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: 7311-7316.
55. Frey BN, Andreazza AC, Rosa AR et al. Lithium increases nerve growth factor levels in the rat hippocampus in an animal model of mania. Behav Pharmacol 2006; 17: 311-318.
56. Chang YC, Rapoport SI, Rao JS. Chronic administration of mood stabilizers upregulates BDNF and bcl-2 expression levels in rat frontal cortex. Neurochem Res 2009; 34: 536-541.
57. Abelaira HM, Réus GZ, Ribeiro KF et al. Lamotrigine treatment reverses depressive-like behavior and alters BDNF levels in the brains of maternally deprived adult rats. Pharmacol Biochem Behav 2012; 101: 348-353.
58. Li N, He X, Qi X et al. The mood stabilizer lamotrigine produces antidepressant behavioral effects in rats: role of brain-derived neurotrophic factor. J Psychopharmacol 2010; 24: 1772-17778.
59. Crowder RJ, Freeman RS. Glycogen synthase kinase-3 beta activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal. J Biol Chem 2000; 275: 34266-34271.
60. Foulstone EJ, Tavaré JM, Gunn-Moore FJ. Sustained phosphorylation and activation of protein kinase B correlates with brain-derived neurotrophic factor and insulin stimulated survival of cerebellar granule cells. Neurosci Lett 1999; 264: 125-128.
61. Okabe S, Kim HD, Miwa A et al. Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat Neurosci 1999; 2: 804-811.
62. Levinson JN, El-Husseini A. Building excitatory and inhibitory synapses: balancing neuroligin partnerships. Neuron 2005; 48: 171-174.
63. Kim HJ, Thayer SA. Lithium increases synapse formation between hippocampal neurons by depleting phosphoinositides. Mol Pharmacol 2009; 75: 1021-1030.
64. Hall AC, Lucas FR, Salinas PC. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 2000; 100: 525-535.
65. Hasan MR, Kim JH, Kim YJ et al. Effect of HDAC inhibitors on neuroprotection and neurite outgrowth in primary rat cortical neurons following ischemic insult. Neurochem Res 2013; 38: 1921-1934.
66. Phiel CJ, Zhang F, Huang EY et al. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 2001; 276: 36734-36741.
67. 2+ deregulation, and cytoskeletal pathology. Neurobiol Aging 1995; 16: 187-198.
68. Halbsgut LR, Fahim E, Kapoor K et al. Certain secondary antiepileptic drugs can rescue hippocampal injury following a critical growth period despite poor anticonvulsant activity and cognitive deficits. Epilepsy Behav 2013; 29: 466-477.
69. Casanovas A, Ribera J, Hukkanen M et al. Prevention by lamotrigine, MK-801 and N omega-nitro-L-arginine methyl ester of motoneuron cell death after neonatal axotomy. Neuroscience 1996; 71: 313-325.
70. Lang DG, Wang CM, Cooper BR. Lamotrigine, phenytoin and carbamazepine interactions on the sodium current present in N4TG1 mouse neuroblastoma cells. J Pharmacol Exp Ther 1993; 266: 829-835.