H3K4 tri-methylation in synapsin genes leads to different expression patterns in bipolar disorder and major depression

International Journal of Neuropsychopharmacology

Volumn 16, Issue 2, 2013, Pages 289-299

  Cruceanu, Cristiana ^a   Alda, Martin ^b   Nagy, Corina ^a   Freemantle, Erika ^a   Rouleau, Guy A ^c   Turecki, Gustavo ^a  

^a MCGILL UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

^c UNIVERSITY OF MONTREAL   (Canada)

Author keywords

Bipolar disorder; epigenetics; gene expression; H3K4me3; synapsin

Indexed keywords

HISTONE 3 LYSINE 4; HISTONE H3; LYSINE DERIVATIVE; MESSENGER RNA; SYNAPSIN; UNCLASSIFIED DRUG;

ADULT; ALTERNATIVE RNA SPLICING; ARTICLE; BIPOLAR DISORDER; BRAIN TISSUE; CLINICAL ARTICLE; CONTROLLED STUDY; EPIGENETICS; FEMALE; HISTONE MODIFICATION; HUMAN; HUMAN TISSUE; MAJOR DEPRESSION; MALE; METHYLATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; PH; PRIORITY JOURNAL; PROBABILITY; PROMOTER REGION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SUICIDE; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE;

ADULT; ANALYSIS OF VARIANCE; BIPOLAR DISORDER; BRAIN; CHROMATIN IMMUNOPRECIPITATION; DEPRESSIVE DISORDER, MAJOR; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; MALE; METHYLATION; MIDDLE AGED; PROBABILITY; PROMOTER REGIONS, GENETIC; STATISTICS AS TOPIC; SYNAPSINS;

EID: 84875931204     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145712000363     Document Type: Article

References (61)

1. Akbarian S (2010a). Epigenetics of schizophrenia. Current Top Behavioral Neuroscience 4, 611-628.
2. Akbarian S (2010b). The molecular pathology of schizophrenia-focus on histone and DNA modifications. Brain Research Bulletins 83, 103-107.
3. Arent CO, Valvassori SS, Fries GR, Stertz L, et al. (2011). Neuroanatomical profile of antimaniac effects of histone deacetylases inhibitors. Molecular Neurobiology 43, 207-214.
4. Bannister AJ, Kouzarides T (2011). Regulation of chromatin by histone modifications. Cell Research 21, 381-395.
5. Berger SL (2007). The complex language of chromatin regulation during transcription. Nature 447, 407-412.
6. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, et al. (2005). Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120, 169-181.
7. Blumberg HP, Leung HC, Skudlarski P, Lacadie CM, et al. (2003). A functional magnetic resonance imaging study of bipolar disorder, state-And trait-related dysfunction in ventral prefrontal cortices. Archives of General Psychiatry 60, 601-609.
8. Browning MD, Dudek EM, Rapier JL, Leonard S, et al. (1993). Significant reductions in synapsin but not synaptophysin specific activity in the brains of some schizophrenics. Biological Psychiatry 34, 529-535.
9. Cesca F, Baldelli P, Valtorta F, Benfenati F (2010). The synapsins, key actors of synapse function and plasticity. Progress in Neurobiology 91, 313-348.
10. Chen Q, He G, Qin W, Chen QY, et al. (2004). Family-based association study of synapsin II and schizophrenia. American Journal of Human Genetics 75, 873-877.
11. Chen G, Henter ID, Manji HK (2010). Presynaptic glutamatergic dysfunction in bipolar disorder. Biological Psychiatry 67, 1007-1009.
12. Corradi A, Zanardi A, Giacomini C, Onofri F, et al. (2008). Synapsin-I-And synapsin-II-null mice display an increased age-dependent cognitive impairment. Journal of Cell Science 121, 3042-3051.
13. Cruceanu C, Alda M, Grof P, Rouleau GA, et al. (2012). Synapsin II is involved in the molecular pathway of lithium treatment in bipolar disorder. PLoS One 7, e32680.
14. Damberg M, Ekblom J, Oreland L (2000). Chronic pharmacological treatment with certain antidepressants alters the expression and DNA-binding activity of transcription factor AP-2. Life Sciences 68, 669-678.
15. Eastwood SL, Harrison PJ (2010). Markers of glutamate synaptic transmission and plasticity are increased in the anterior cingulate cortex in bipolar disorder. Biological Psychiatry 67, 1010-1016.
16. Fassio A, Raimondi A, Lignani G, Benfenati F, et al. (2011). Synapsins: from synapse to network hyperexcitability and epilepsy. Seminars in Cell Developmental Biology 22, 408-415.
17. Feng J, Chi P, Blanpied TA, Xu Y, et al. (2002). Regulation of neurotransmitter release by synapsin III. Journal of Neuroscience 22, 4372-4380.
18. Ferreira A, Kao HT, Feng J, Rapoport M, et al. (2000). Synapsin III: developmental expression, subcellular localization, and role in axon formation. Journal of Neuroscience 20, 3736-3744.
19. Fiori LM, Turecki G (2011). Epigenetic regulation of spermidine/spermine N(1)-Acetyltransferase (SAT1) in suicide. Journal of Psychiatry Research 45, 1229-1235.
20. Gitler D, Cheng Q, Greengard P, Augustine GJ (2008). Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles. Journal of Neuroscience 28, 10835-10843.
21. Gitler D, Takagishi Y, Feng J, Ren Y, et al. (2004). Different presynaptic roles of synapsins at excitatory and inhibitory synapses. Journal of Neuroscience 24, 11368-11380.
22. Grafodatskaya D, Chung B, Szatmari P, Weksberg R (2010). Autism spectrum disorders and epigenetics. Journal of the American Academy of Child and Adolescent Psychiatry 49, 794-809.
23. Grebb JA, Greengard P (1990). An analysis of synapsin II, a neuronal phosphoprotein, in postmortem brain tissue from alcoholic and neuropsychiatrically ill adults and medically ill children and young adults. Archives of General Psychiatry 47, 1149-1156.
24. Hashimoto K, Sawa A, Iyo M (2007). Increased levels of glutamate in brains from patients with mood disorders. Biological Psychiatry 62, 1310-1316.
25. Huttner WB, Schiebler W, Greengard P, De Camilli P (1983). Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. Journal of Cell Biology 96, 1374-1388.
26. Kao HT, Porton B, Czernik AJ, Feng J, et al. (1998). A third member of the synapsin gene family. Proceedings of the National Academy of Sciences USA 95, 4667-4672.
27. Kielland A, Erisir A, Walaas SI, Heggelund P (2006). Synapsin utilization differs among functional classes of synapses on thalamocortical cells. Journal of Neuroscience 26, 5786-5793.
28. Kile BM, Guillot TS, Venton BJ, Wetsel WC, et al. (2010). Synapsins differentially control dopamine and serotonin release. Journal of Neuroscience 30, 9762-9770.
29. Kim AH, Reimers M, Maher B, Williamson V, et al. (2010). MicroRNA expression profiling in the prefrontal cortex of individuals affected with schizophrenia and bipolar disorders. Schizophrenia Research 124, 183-191.
30. Klempan TA, Rujescu D, Merette C, Himmelman C, et al. (2009). Profiling brain expression of the spermidine/spermine N1-Acetyltransferase 1 (SAT1) gene in suicide. American Journal of Medical Genetics B Neuropsychiatric Genetics 150B, 934-943.
31. Kouzarides T (2007). Chromatin modifications and their function. Cell 128, 693-705.
32. Kruger S, Alda M, Young LT, Goldapple K, et al. (2006). Risk and resilience markers in bipolar disorder: brain responses to emotional challenge in bipolar patients and their healthy siblings. American Journal of Psychiatry 163, 257-264.
33. Lee HJ, Song JY, Kim JW, Jin SY, et al. (2005). Association study of polymorphisms in synaptic vesicle-Associated genes, SYN2 and CPLX2, with schizophrenia. Behavioral and Brain Functions 1, 15.
34. Li L, Chin LS, Shupliakov O, Brodin L, et al. (1995). Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proceedings of the National Academy of Sciences USA 92, 9235-9239.
35. Lopez de Lara C, Jaitovich-Groisman I, Cruceanu C, Mamdani F, et al. (2010). Implication of synapse-related genes in bipolar disorder by linkage and gene expression analyses. International Journal of Neuropsychopharmacology 13, 1397-1410.
36. Machado-Vieira R, Ibrahim L, Zarate Jr. CA (2010). Histone deacetylases and mood disorders: epigenetic programming in gene-environment interactions. CNS Neuroscience and Therapeutics 17, 699-704.
37. Malhi GS, Ivanovski B, Hadzi-Pavlovic D, Mitchell PB, et al. (2007). Neuropsychological deficits and functional impairment in bipolar depression, hypomania and euthymia. Bipolar Disorders 9, 114-125.
38. Matevossian A, Akbarian S (2008). A chromatin assay for human brain tissue. Journal of Visual Experiments 13, 717.
39. Miller BH, Wahlestedt C (2010). MicroRNA dysregulation in psychiatric disease. Brain Research 1338, 89-99.
40. Mirnics K, Middleton FA, Marquez A, Lewis DA, et al. (2000). Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 28, 53-67.
41. Moreau MP, Bruse SE, David-Rus R, Buyske S, et al. (2011). Altered microRNA expression profiles in postmortem brain samples from individuals with schizophrenia and bipolar disorder. Biological Psychiatry 69, 188-193.
42. Nowakowski C, Kaufmann WA, Adlassnig C, Maier H, et al. (2002). Reduction of chromogranin B-like immunoreactivity in distinct subregions of the hippocampus from individuals with schizophrenia. Schizophrenia Research 58, 43-53.
43. Ongur D, Jensen JE, Prescot AP, Stork C, et al. (2008). Abnormal glutamatergic neurotransmission and neuronal-glial interactions in acute mania. Biological Psychiatry 64, 718-726.
44. Petersohn D, Schoch S, Brinkmann DR, Thiel G (1995). The human synapsin II gene promoter. Possible role for the transcription factor zif268/egr-1, polyoma enhancer activator 3, and AP2. Journal of Biological Chemistry 270, 24361-24369.
45. Porton B, Kao HT, Greengard P (1999). Characterization of transcripts from the synapsin III gene locus. Journal of Neurochemistry 73, 2266-2271.
46. Quraishi S, Frangou S (2002). Neuropsychology of bipolar disorder: a review. Journal of Affective Disorders 72, 209-226.
47. Rao JS, Bazinet RP, Rapoport SI, Lee HJ (2007). Chronic administration of carbamazepine down-regulates AP-2 DNA-binding activity and AP-2alpha protein expression in rat frontal cortex. Biological Psychiatry 61, 154-161.
48. Robinson JL, Monkul ES, Tordesillas-Gutierrez D, Franklin C, et al. (2008). Fronto-limbic circuitry in euthymic bipolar disorder: evidence for prefrontal hyperactivation. Psychiatry Research 164, 106-113.
49. Rosahl TW, Spillane D, Missler M, Herz J, et al. (1995). Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375, 488-493.
50. Sanacora G, Zarate CA, Krystal JH, Manji HK (2008). Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nature Reviews Drug Discovery 7, 426-437.
51. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, et al. (2002). Active genes are tri-methylated at K4 of histone H3. Nature 419, 407-411.
52. Saviouk V, Moreau MP, Tereshchenko IV, Brzustowicz LM (2007). Association of synapsin 2 with schizophrenia in families of Northern European ancestry. Schizophrenia Research 96, 100-111.
53. Schneider R, Bannister AJ, Myers FA, Thorne AW, et al. (2004). Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nature Cell Biology 6, 73-77.
54. Schroeder M, Krebs MO, Bleich S, Frieling H (2010). Epigenetics and depression: current challenges and new therapeutic options. Current Opinions in Psychiatry 23, 588-592.
55. Skoblenick KJ, Argintaru N, Xu Y, Dyck BA, et al. (2010). Role of AP-2alpha transcription factor in the regulation of synapsin II gene expression by dopamine D1 and D2 receptors. Journal of Molecular Neuroscience 41, 267-277.
56. Sudhof TC, Czernik AJ, Kao HT, Takei K, et al. (1989). Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science 245, 1474-1480.
57. Takamori S, Holt M, Stenius K, Lemke EA, et al. (2006). Molecular anatomy of a trafficking organelle. Cell 127, 831-846.
58. Thompson JM, Gallagher P, Hughes JH, Watson S, et al. (2005). Neurocognitive impairment in euthymic patients with bipolar affective disorder. British Journal of Psychiatry 186, 32-40.
59. Tsankova N, Renthal W, Kumar A, Nestler EJ (2007). Epigenetic regulation in psychiatric disorders. Nature Reviews Neuroscience 8, 355-367.
60. Ullrich B, Sudhof TC (1995). Differential distributions of novel synaptotagmins: comparison to synapsins. Neuropharmacology 34, 1371-1377.
61. Vawter MP, Thatcher L, Usen N, Hyde TM, et al. (2002). Reduction of synapsin in the hippocampus of patients with bipolar disorder and schizophrenia. Molecular Psychiatry 7, 571-578.