Proteomic investigation of epigenetics in neuropychiatric disorders: A missing link between genetics and behavior?

Journal of Proteome Research

Volumn 10, Issue 1, 2011, Pages 58-65

  Plazas Mayorca, Mariana D ^a   Vrana, Kent E ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Chromatin; Dna methylation; Epigenetics; Histone modification; Neuropsychiatric disorders

Indexed keywords

BEHAVIOR; CHROMATIN STRUCTURE; DEPRESSION; DNA METHYLATION; DRUG DEPENDENCE; EPIGENETICS; GENETICS; HISTONE MODIFICATION; MENTAL DISEASE; PRIORITY JOURNAL; PROTEOMICS; REVIEW; SCHIZOPHRENIA;

CHROMATIN; DEPRESSION; DNA METHYLATION; EPIGENOMICS; HIGH-THROUGHPUT SCREENING ASSAYS; MENTAL DISORDERS; PROTEOMICS; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; SUBSTANCE-RELATED DISORDERS;

EID: 79951522491     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100463y     Document Type: Review

References (123)

1. Autry, A. E.; Monteggia, L. M. Epigenetics in suicide and depression. Biol. Psychiatry 2009, 66 (9), 812-3.
2. Tsankova, N.; Renthal, W.; Kumar, A.; Nestler, E. J. Epigenetic regulation in psychiatric disorders. Nat. Rev. Neurosci. 2007, 8 (5), 355-67. (Pubitemid 46652469)
3. Rutten, B. P.; Mill, J. Epigenetic mediation of environmental influences in major psychotic disorders. Schizophr. Bull. 2009, 35 (6), 1045-56.
4. Urdinguio, R. G.; Sanchez-Mut, J. V.; Esteller, M. Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies. Lancet Neurol. 2009, 8 (11), 1056-72.
5. Wang, G. G.; Allis, C. D.; Chi, P. Chromatin remodeling and cancer, Part I: Covalent histone modifications. Trends Mol. Med. 2007, 13 (9), 363-72. (Pubitemid 47385381)
6. Hendrich, B.; Bickmore, W. Human diseases with underlying defects in chromatin structure and modification. Hum. Mol. Genet. 2001, 10 (20), 2233-42. (Pubitemid 32998837)
7. Renthal, W.; Nestler, E. J. Chromatin regulation in drug addiction and depression. Dialogues Clin. Neurosci. 2009, 11 (3), 257-68.
8. Polo, S. E.; Almouzni, G. Chromatin assembly: a basic recipe with various flavours. Curr. Opin. Genet. Dev. 2006, 16 (2), 104-11. (Pubitemid 43376055)
9. Waddington, C. H. Gene regulation in higher cells. Science 1969, 166 (905), 639-40.
10. Bird, A. Perceptions of epigenetics. Nature 2007, 447 (7143), 396-8. (Pubitemid 46816744)
11. Grewal, S. I.; Jia, S. Heterochromatin revisited. Nat. Rev. Genet. 2007, 8 (1), 35-46. (Pubitemid 46006048)
12. Craig, J. M. Heterochromatin-many flavours, common themes. Bioessays 2005, 27 (1), 17-28.
13. Luger, K.; Mader, A. W.; Richmond, R. K.; Sargent, D. F.; Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389 (6648), 251-60. (Pubitemid 27406632)
14. Catez, F.; Yang, H.; Tracey, K. J.; Reeves, R.; Misteli, T.; Bustin, M. Network of dynamic interactions between histone H1 and high-mobility-group proteins in chromatin. Mol. Cell. Biol. 2004, 24 (10), 4321-8. (Pubitemid 41071002)
15. Garcia, B. A.; Joshi, S.; Thomas, C. E.; Chitta, R. K.; Diaz, R. L.; Busby, S. A.; Andrews, P. C.; Ogorzalek Loo, R. R.; Shabanowitz, J.; Kelleher, N. L.; Mizzen, C. A.; Allis, C. D.; Hunt, D. F. Comprehensive phosphoprotein analysis of linker histone H1 from Tetrahymena thermophila. Mol. Cell. Proteomics 2006, 5 (9), 1593-609. (Pubitemid 44480388)
16. Luger, K. Structure and dynamic behavior of nucleosomes. Curr. Opin. Genet. Dev. 2003, 13 (2), 127-35. (Pubitemid 36369736)
17. Becker, P. B. Nucleosome sliding: facts and fiction. EMBO J. 2002, 21 (18), 4749-53.
18. Becker, P. B.; Horz, W. ATP-dependent nucleosome remodeling. Annu. Rev. Biochem. 2002, 71, 247-73. (Pubitemid 34800221)
19. Cosgrove, M. S.; Boeke, J. D.; Wolberger, C. Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 2004, 11 (11), 1037-43. (Pubitemid 39453330)
20. Jin, J.; Cai, Y.; Li, B.; Conaway, R. C.; Workman, J. L.; Conaway, J. W.; Kusch, T. In and out: histone variant exchange in chromatin. Trends Biochem. Sci. 2005, 30 (12), 680-7. (Pubitemid 41668861)
21. Probst, A. V.; Dunleavy, E.; Almouzni, G. Epigenetic inheritance during the cell cycle. Nat. Rev. Mol. Cell. Biol. 2009, 10 (3), 192-206.
22. Cheung, P.; Allis, C. D.; Sassone-Corsi, P. Signaling to chromatin through histone modifications. Cell 2000, 103 (2), 263-71.
23. Peterson, C. L.; Laniel, M. A. Histones and histone modifications. Curr. Biol. 2004, 14 (14), R546-51.
24. Garcia, B. A.; Pesavento, J. J.; Mizzen, C. A.; Kelleher, N. L. Pervasive combinatorial modification of histone H3 in human cells. Nat. Methods 2007, 4 (6), 487-9. (Pubitemid 46852073)
25. Strahl, B. D.; Allis, C. D. The language of covalent histone modifications. Nature 2000, 403 (6765), 41-5.
26. Cheung, W. L.; Ajiro, K.; Samejima, K.; Kloc, M.; Cheung, P.; Mizzen, C. A.; Beeser, A.; Etkin, L. D.; Chernoff, J.; Earnshaw, W. C.; Allis, C. D. Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 2003, 113 (4), 507-17. (Pubitemid 36603322)
27. Meshorer, E.; Misteli, T. Chromatin in pluripotent embryonic stem cells and differentiation. Nat. Rev. Mol. Cell. Biol. 2006, 7 (7), 540-6. (Pubitemid 44036459)
28. Fraga, M. F.; Ballestar, E.; Villar-Garea, A.; Boix-Chornet, M.; Espada, J.; Schotta, G.; Bonaldi, T.; Haydon, C.; Ropero, S.; Petrie, K.; Iyer, N. G.; Perez-Rosado, A.; Calvo, E.; Lopez, J. A.; Cano, A.; Calasanz, M. J.; Colomer, D.; Piris, M. A.; Ahn, N.; Imhof, A.; Caldas, C.; Jenuwein, T.; Esteller, M. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet. 2005, 37 (4), 391-400.
29. Evertts, A. G.; Zee, B. M.; Garcia, B. A. Modern Approaches for Investigating Epigenetic Signaling Pathways. J. Appl. Physiol. 2010.
30. Kouzarides, T. Chromatin modifications and their function. Cell 2007, 128 (4), 693-705. (Pubitemid 46273577)
31. Ruthenburg, A. J.; Li, H.; Patel, D. J.; Allis, C. D. Multivalent engagement of chromatin modifications by linked binding modules. Nat. Rev. Mol. Cell. Biol. 2007, 8 (12), 983-94. (Pubitemid 350174643)
32. Grewal, S. I.; Moazed, D. Heterochromatin and epigenetic control of gene expression. Science 2003, 301 (5634), 798-802. (Pubitemid 36962612)
33. Steward, M. M.; Lee, J. S.; O'Donovan, A.; Wyatt, M.; Bernstein, B. E.; Shilatifard, A. Molecular regulation of H3K4 trimethylation by ASH2L, a shared subunit of MLL complexes. Nat. Struct. Mol. Biol. 2006, 13 (9), 852-4. (Pubitemid 44338781)
34. Shi, Y.; Whetstine, J. R. Dynamic regulation of histone lysine methylation by demethylases. Mol. Cell 2007, 25 (1), 1-14. (Pubitemid 46049067)
35. Garcia, B. A.; Shabanowitz, J.; Hunt, D. F. Characterization of histones and their post-translational modifications by mass spectrometry. Curr. Opin. Chem. Biol. 2007, 11 (1), 66-73. (Pubitemid 46216127)
36. Cosgrove, M. S. Histone proteomics and the epigenetic regulation of nucleosome mobility. Expert Rev. Proteomics 2007, 4 (4), 465-78. (Pubitemid 47347595)
37. Wang, Y.; Fischle, W.; Cheung, W.; Jacobs, S.; Khorasanizadeh, S.; Allis, C. D. Beyond the double helix: writing and reading the histone code. Novartis Found. Symp. 2004, 259, 3-17; discussion 17-21, 163-9.
38. Daniel, J. A.; Pray-Grant, M. G.; Grant, P. A. Effector proteins for methylated histones: an expanding family. Cell Cycle 2005, 4 (7), 919-26. (Pubitemid 41359758)
39. Bernstein, B. E.; Meissner, A.; Lander, E. S. The mammalian epigenome. Cell 2007, 128 (4), 669-81. (Pubitemid 46273573)
40. Hirota, T.; Lipp, J. J.; Toh, B. H.; Peters, J. M. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 2005, 438 (7071), 1176-80. (Pubitemid 41831689)
41. Fischle, W.; Tseng, B. S.; Dormann, H. L.; Ueberheide, B. M.; Garcia, B. A.; Shabanowitz, J.; Hunt, D. F.; Funabiki, H.; Allis, C. D. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 2005, 438 (7071), 1116-22. (Pubitemid 41831675)
42. Fischle, W.; Wang, Y.; Allis, C. D. Binary switches and modification cassettes in histone biology and beyond. Nature 2003, 425 (6957), 475-9. (Pubitemid 37237036)
43. Latham, J. A.; Dent, S. Y. Cross-regulation of histone modifications. Nat. Struct. Mol. Biol. 2007, 14 (11), 1017-24. (Pubitemid 350060331)
44. Du, H. N.; Fingerman, I. M.; Briggs, S. D. Histone H3 K36 methylation is mediated by a trans-histone methylation pathway involving an interaction between Set2 and histone H4. Genes Dev. 2008, 22 (20), 2786-98.
45. Pesavento, J. J.; Mizzen, C. A.; Kelleher, N. L. Quantitative analysis of modified proteins and their positional isomers by tandem mass spectrometry: human histone H4. Anal. Chem. 2006, 78 (13), 4271-80.
46. Boyne, M. T., 2nd; Pesavento, J. J.; Mizzen, C. A.; Kelleher, N. L. Precise characterization of human histones in the H2A gene family by top down mass spectrometry. J. Proteome Res. 2006, 5 (2), 248-53. (Pubitemid 43222292)
47. Plazas-Mayorca, M. D.; Zee, B. M.; Young, N. L.; Fingerman, I. M.; LeRoy, G.; Briggs, S. D.; Garcia, B. A. One-pot shotgun quantitative mass spectrometry characterization of histones. J. Proteome Res. 2009, 8 (11), 5367-74.
48. Trelle, M. B.; Jensen, O. N. Functional proteomics in histone research and epigenetics. Expert Rev. Proteomics 2007, 4 (4), 491-503. (Pubitemid 47347597)
49. Young, N. L.; DiMaggio, P. A.; Plazas-Mayorca, M. D.; Baliban, R. C.; Floudas, C. A.; Garcia, B. A. High throughput characterization of combinatorial histone codes. Mol. Cell. Proteomics 2009, 8 (10), 2266-84.
50. Garcia, B. A.; Busby, S. A.; Shabanowitz, J.; Hunt, D. F.; Mishra, N. Resetting the epigenetic histone code in the MRL-lpr/lpr mouse model of lupus by histone deacetylase inhibition. J. Proteome Res. 2005, 4 (6), 2032-42. (Pubitemid 41814269)
51. Schones, D. E.; Zhao, K. Genome-wide approaches to studying chromatin modifications. Nat. Rev. Genet. 2008, 9 (3), 179-91. (Pubitemid 351271798)
52. Bernstein, B. E.; Kamal, M.; Lindblad-Toh, K.; Bekiranov, S.; Bailey, D. K.; Huebert, D. J.; McMahon, S.; Karlsson, E. K.; Kulbokas, E. J., 3rd; Gingeras, T. R.; Schreiber, S. L.; Lander, E. S. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 2005, 120 (2), 169-81. (Pubitemid 40174761)
53. Bernstein, B. E.; Humphrey, E. L.; Erlich, R. L.; Schneider, R.; Bouman, P.; Liu, J. S.; Kouzarides, T.; Schreiber, S. L. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (13), 8695-700. (Pubitemid 34693622)
54. Schubeler, D.; MacAlpine, D. M.; Scalzo, D.; Wirbelauer, C.; Kooperberg, C.; van Leeuwen, F.; Gottschling, D. E.; O'Neill, L. P.; Turner, B. M.; Delrow, J.; Bell, S. P.; Groudine, M. The histone modification pattern of active genes revealed through genomewide chromatin analysis of a higher eukaryote. Genes Dev. 2004, 18 (11), 1263-71. (Pubitemid 38720594)
55. Heintzman, N. D.; Stuart, R. K.; Hon, G.; Fu, Y.; Ching, C. W.; Hawkins, R. D.; Barrera, L. O.; Van Calcar, S.; Qu, C.; Ching, K. A.; Wang, W.; Weng, Z.; Green, R. D.; Crawford, G. E.; Ren, B. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007, 39 (3), 311-8. (Pubitemid 46328487)
56. Park, P. J. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet. 2009, 10 (10), 669-80.
57. Barski, A.; Cuddapah, S.; Cui, K.; Roh, T. Y.; Schones, D. E.; Wang, Z.; Wei, G.; Chepelev, I.; Zhao, K. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129 (4), 823-37. (Pubitemid 46802390)
58. Sananbenesi, F.; Fischer, A. The epigenetic bottleneck of neurodegenerative and psychiatric diseases. Biol. Chem. 2009, 390 (11), 1145-53.
59. Feng, J.; Fan, G. The role of DNA methylation in the central nervous system and neuropsychiatric disorders. Int. Rev. Neurobiol. 2009, 89, 67-84.
60. Nan, X.; Meehan, R. R.; Bird, A. Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucleic Acids Res. 1993, 21 (21), 4886-92. (Pubitemid 23330162)
61. Klose, R. J.; Bird, A. P. Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 2006, 31 (2), 89-97. (Pubitemid 43221841)
62. Singer-Sam, J.; Grant, M.; LeBon, J. M.; Okuyama, K.; Chapman, V.; Monk, M.; Riggs, A. D. Use of a HpaII-polymerase chain reaction assay to study DNA methylation in the Pgk-1 CpG island of mouse embryos at the time of X-chromosome inactivation. Mol. Cell. Biol. 1990, 10 (9), 4987-9.
63. Singer-Sam, J.; LeBon, J. M.; Tanguay, R. L.; Riggs, A. D. A quantitative HpaII-PCR assay to measure methylation of DNA from a small number of cells. Nucleic Acids Res. 1990, 18 (3), 687. (Pubitemid 20064048)
64. Guha, S. Determination of DNA sequences containing methylcytosine in Bacillus subtilis Marburg. J. Bacteriol. 1985, 163 (2), 573-9. (Pubitemid 15012629)
65. New England Biolabs. Restriction Endonucleases Overview. http://www.neb.com/nebecomm/tech-reference/restriction-enzymes/overview.asp (Accessed May 10th, 2010).
66. Yan, P. S.; Chen, C. M.; Shi, H.; Rahmatpanah, F.; Wei, S. H.; Caldwell, C. W.; Huang, T. H. Dissecting complex epigenetic alterations in breast cancer using CpG island microarrays. Cancer Res. 2001, 61 (23), 8375-80. (Pubitemid 33131108)
67. Hatada, I.; Kato, A.; Morita, S.; Obata, Y.; Nagaoka, K.; Sakurada, A.; Sato, M.; Horii, A.; Tsujimoto, A.; Matsubara, K. A microarraybased method for detecting methylated loci. J. Hum. Genet. 2002, 47 (8), 448-51. (Pubitemid 34857547)
68. Rollins, R. A.; Haghighi, F.; Edwards, J. R.; Das, R.; Zhang, M. Q.; Ju, J.; Bestor, T. H. Large-scale structure of genomic methylation patterns. Genome Res. 2006, 16 (2), 157-63. (Pubitemid 43200263)
69. Clark, S. J.; Statham, A.; Stirzaker, C.; Molloy, P. L.; Frommer, M. DNA methylation: bisulphite modification and analysis. Nat. Protoc. 2006, 1 (5), 2353-64.
70. Adorjan, P.; Distler, J.; Lipscher, E.; Model, F.; Muller, J.; Pelet, C.; Braun, A.; Florl, A. R.; Gutig, D.; Grabs, G.; Howe, A.; Kursar, M.; Lesche, R.; Leu, E.; Lewin, A.; Maier, S.; Muller, V.; Otto, T.; Scholz, C.; Schulz, W. A.; Seifert, H. H.; Schwope, I.; Ziebarth, H.; Berlin, K.; Piepenbrock, C.; Olek, A. Tumour class prediction and discovery by microarray-based DNA methylation analysis. Nucleic Acids Res. 2002, 30 (5), e21.
71. Gitan, R. S.; Shi, H.; Chen, C. M.; Yan, P. S.; Huang, T. H. Methylation-specific oligonucleotide microarray: a new potential for high-throughput methylation analysis. Genome Res. 2002, 12 (1), 158-64. (Pubitemid 34065599)
72. Bibikova, M.; Lin, Z.; Zhou, L.; Chudin, E.; Garcia, E. W.; Wu, B.; Doucet, D.; Thomas, N. J.; Wang, Y.; Vollmer, E.; Goldmann, T.; Seifart, C.; Jiang, W.; Barker, D. L.; Chee, M. S.; Floros, J.; Fan, J. B. High-throughput DNA methylation profiling using universal bead arrays. Genome Res. 2006, 16 (3), 383-93. (Pubitemid 43327509)
73. Cokus, S. J.; Feng, S.; Zhang, X.; Chen, Z.; Merriman, B.; Haudenschild, C. D.; Pradhan, S.; Nelson, S. F.; Pellegrini, M.; Jacobsen, S. E. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 2008, 452 (7184), 215-9. (Pubitemid 351380251)
74. Lister, R.; O'Malley, R. C.; Tonti-Filippini, J.; Gregory, B. D.; Berry, C. C.; Millar, A. H.; Ecker, J. R. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 2008, 133 (3), 523-36.
75. Lister, R.; Ecker, J. R. Finding the fifth base: genome-wide sequencing of cytosine methylation. Genome Res. 2009, 19 (6), 959-66.
76. Zhang, X.; Yazaki, J.; Sundaresan, A.; Cokus, S.; Chan, S. W.; Chen, H.; Henderson, I. R.; Shinn, P.; Pellegrini, M.; Jacobsen, S. E.; Ecker, J. R. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 2006, 126 (6), 1189-201. (Pubitemid 44380289)
77. Weber, M.; Davies, J. J.; Wittig, D.; Oakeley, E. J.; Haase, M.; Lam, W. L.; Schubeler, D. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet. 2005, 37 (8), 853-62. (Pubitemid 41077111)
78. Zilberman, D.; Gehring, M.; Tran, R. K.; Ballinger, T.; Henikoff, S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 2007, 39 (1), 61-9. (Pubitemid 46026502)
79. Shen, L.; Kondo, Y.; Guo, Y.; Zhang, J.; Zhang, L.; Ahmed, S.; Shu, J.; Chen, X.; Waterland, R. A.; Issa, J. P. Genome-wide profiling of DNA methylation reveals a class of normally methylated CpG island promoters. PLoS Genet. 2007, 3 (10), 2023-36.
80. Nestler, E. J. Epigenetic mechanisms in psychiatry. Biol. Psychiatry 2009, 65 (3), 189-90.
81. Krishnan, V.; Nestler, E. J. The molecular neurobiology of depression. Nature 2008, 455 (7215), 894-902.
82. World Health Organization. Depression. http://www.who.int/mental-health/ management/depression/definition/en/ (Last accessed on Dec. 3, 2009).
83. Greenberg, P. E.; Kessler, R. C.; Birnbaum, H. G.; Leong, S. A.; Lowe, S. W.; Berglund, P. A.; Corey-Lisle, P. K. The economic burden of depression in the United States: how did it change between 1990 and 2000. J. Clin. Psychiatry 2003, 64 (12), 1465-75. (Pubitemid 41270106)
84. Poulter, M. O.; Du, L.; Weaver, I. C.; Palkovits, M.; Faludi, G.; Merali, Z.; Szyf, M.; Anisman, H. GABAA receptor promoter hypermethylation in suicide brain: implications for the involvement of epigenetic processes. Biol. Psychiatry 2008, 64 (8), 645-52.
85. Dwivedi, Y.; Rizavi, H. S.; Conley, R. R.; Roberts, R. C.; Tamminga, C. A.; Pandey, G. N. Altered gene expression of brain-derived neurotrophic factor and receptor tyrosine kinase B in postmortem brain of suicide subjects. Arch. Gen. Psychiatry 2003, 60 (8), 804-15. (Pubitemid 36960912)
86. Karege, F.; Perret, G.; Bondolfi, G.; Schwald, M.; Bertschy, G.; Aubry, J. M. Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res. 2002, 109 (2), 143-8. (Pubitemid 34258493)
87. Ernst, C.; Deleva, V.; Deng, X.; Sequeira, A.; Pomarenski, A.; Klempan, T.; Ernst, N.; Quirion, R.; Gratton, A.; Szyf, M.; Turecki, G. Alternative splicing, methylation state, and expression profile of tropomyosin-related kinase B in the frontal cortex of suicide completers. Arch. Gen. Psychiatry 2009, 66 (1), 22-32.
88. Fuchikami, M.; Morinobu, S.; Kurata, A.; Yamamoto, S.; Yamawaki, S. Single immobilization stress differentially alters the expression profile of transcripts of the brain-derived neurotrophic factor (BDNF) gene and histone acetylation at its promoters in the rat hippocampus. Int. J. Neuropsychopharmacol. 2009, 12 (1), 73-82.
89. Tsankova, N. M.; Berton, O.; Renthal, W.; Kumar, A.; Neve, R. L.; Nestler, E. J. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 2006, 9 (4), 519-25.
90. Snyder, E. M.; Murphy, M. R. Schizophrenia therapy: beyond atypical antipsychotics. Nat. Rev. Drug Discovery 2008, 7 (6), 471-2. (Pubitemid 351767114)
91. Graff, J.; Mansuy, I. M. Epigenetic dysregulation in cognitive disorders. Eur. J. Neurosci. 2009, 30 (1), 1-8.
92. Chen, Y.; Sharma, R. P.; Costa, R. H.; Costa, E.; Grayson, D. R. On the epigenetic regulation of the human reelin promoter. Nucleic Acids Res. 2002, 30 (13), 2930-9. (Pubitemid 34778154)
93. Costa, E.; Chen, Y.; Davis, J.; Dong, E.; Noh, J. S.; Tremolizzo, L.; Veldic, M.; Grayson, D. R.; Guidotti, A. REELIN and schizophrenia: a disease at the interface of the genome and the epigenome. Mol. Interv. 2002, 2 (1), 47-57.
94. Akbarian, S. The molecular pathology of schizophrenia-Focus on histone and DNA modifications. Brain Res. Bull. 2009.
95. Abdolmaleky, H. M.; Smith, C. L.; Zhou, J. R.; Thiagalingam, S. Epigenetic alterations of the dopaminergic system in major psychiatric disorders. Methods Mol. Biol. 2008, 448, 187-212.
96. Abdolmaleky, H. M.; Cheng, K. H.; Faraone, S. V.; Wilcox, M.; Glatt, S. J.; Gao, F.; Smith, C. L.; Shafa, R.; Aeali, B.; Carnevale, J.; Pan, H.; Papageorgis, P.; Ponte, J. F.; Sivaraman, V.; Tsuang, M. T.; Thiagalingam, S. Hypomethylation of MB-COMT promoter is a major risk factor for schizophrenia and bipolar disorder. Hum. Mol. Genet. 2006, 15 (21), 3132-45. (Pubitemid 44607800)
97. Kundakovic, M.; Chen, Y.; Costa, E.; Grayson, D. R. DNA methyltransferase inhibitors coordinately induce expression of the human reelin and glutamic acid decarboxylase 67 genes. Mol. Pharmacol. 2007, 71 (3), 644-53. (Pubitemid 46294076)
98. Huang, H. S.; Matevossian, A.; Whittle, C.; Kim, S. Y.; Schumacher, A.; Baker, S. P.; Akbarian, S. Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters. J. Neurosci. 2007, 27 (42), 11254-62. (Pubitemid 47621326)
99. Kundakovic, M.; Chen, Y.; Guidotti, A.; Grayson, D. R. The reelin and GAD67 promoters are activated by epigenetic drugs that facilitate the disruption of local repressor complexes. Mol. Pharmacol. 2009, 75 (2), 342-54.
100. Koob, G. F.; Le Moal, M. Drug abuse: hedonic homeostatic dysregulation. Science 1997, 278 (5335), 52-8. (Pubitemid 27446270)
101. Koob, G. F.; Kenneth Lloyd, G.; Mason, B. J. Development of pharmacotherapies for drug addiction: a Rosetta stone approach. Nat. Rev. Drug Discovery 2009, 8 (6), 500-15.
102. Kauer, J. A.; Malenka, R. C. Synaptic plasticity and addiction. Nat. Rev. Neurosci. 2007, 8 (11), 844-58. (Pubitemid 350006216)
103. Kumar, A.; Choi, K. H.; Renthal, W.; Tsankova, N. M.; Theobald, D. E.; Truong, H. T.; Russo, S. J.; Laplant, Q.; Sasaki, T. S.; Whistler, K. N.; Neve, R. L.; Self, D. W.; Nestler, E. J. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 2005, 48 (2), 303-14. (Pubitemid 41476363)
104. Freeman, W. M.; Patel, K. M.; Brucklacher, R. M.; Lull, M. E.; Erwin, M.; Morgan, D.; Roberts, D. C.; Vrana, K. E. Persistent alterations in mesolimbic gene expression with abstinence from cocaine self-administration. Neuropsychopharmacology 2008, 33 (8), 1807-17. (Pubitemid 351832593)
105. Maze, I.; Covington, H. E., 3rd; Dietz, D. M.; LaPlant, Q.; Renthal, W.; Russo, S. J.; Mechanic, M.; Mouzon, E.; Neve, R. L.; Haggarty, S. J.; Ren, Y.; Sampath, S. C.; Hurd, Y. L.; Greengard, P.; Tarakhovsky, A.; Schaefer, A.; Nestler, E. J. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 2010, 327 (5962), 213-6.
106. Renthal, W.; Maze, I.; Krishnan, V.; Covington, H. E., 3rd; Xiao, G.; Kumar, A.; Russo, S. J.; Graham, A.; Tsankova, N.; Kippin, T. E.; Kerstetter, K. A.; Neve, R. L.; Haggarty, S. J.; McKinsey, T. A.; Bassel-Duby, R.; Olson, E. N.; Nestler, E. J. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 2007, 56 (3), 517-29. (Pubitemid 350030878)
107. Phillips, R. G.; LeDoux, J. E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992, 106 (2), 274-85.
108. Levenson, J. M.; O'Riordan, K. J.; Brown, K. D.; Trinh, M. A.; Molfese, D. L.; Sweatt, J. D. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 2004, 279 (39), 40545-59. (Pubitemid 39287646)
109. Levenson, J. M.; Sweatt, J. D. Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 2005, 6 (2), 108-18. (Pubitemid 40188945)
110. Chwang, W. B.; O'Riordan, K. J.; Levenson, J. M.; Sweatt, J. D. ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. Learn Mem. 2006, 13 (3), 322-8. (Pubitemid 43830678)
111. Korzus, E.; Rosenfeld, M. G.; Mayford, M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004, 42 (6), 961-72. (Pubitemid 38798234)
112. Miller, C. A.; Sweatt, J. D. Covalent modification of DNA regulates memory formation. Neuron 2007, 53 (6), 857-69. (Pubitemid 46367557)
113. Fischer, A.; Sananbenesi, F.; Wang, X.; Dobbin, M.; Tsai, L. H. Recovery of learning and memory is associated with chromatin remodelling. Nature 2007, 447 (7141), 178-82. (Pubitemid 46763080)
114. Peleg, S.; Sananbenesi, F.; Zovoilis, A.; Burkhardt, S.; Bahari-Javan, S.; Agis-Balboa, R. C.; Cota, P.; Wittnam, J. L.; Gogol-Doering, A.; Opitz, L.; Salinas-Riester, G.; Dettenhofer, M.; Kang, H.; Farinelli, L.; Chen, W.; Fischer, A. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 2010, 328 (5979), 753-6.
115. Sweatt, J. D. Neuroscience. Epigenetics and cognitive aging. Science 2010, 328 (5979), 701-2.
116. Mockus, S. M.; Vrana, K. E. Advances in the molecular characterization of tryptophan hydroxylase. J. Mol. Neurosci. 1998, 10 (3), 163-79. (Pubitemid 28427885)
117. 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. Loss-of-function mutation in tryptophan hydroxylase- 2 identified in unipolar major depression. Neuron 2005, 45 (1), 11-6. (Pubitemid 40075345)
118. Cichon, S.; Winge, I.; Mattheisen, M.; Georgi, A.; Karpushova, A.; Freudenberg, J.; Freudenberg-Hua, Y.; Babadjanova, G.; Van Den Bogaert, A.; Abramova, L. I.; Kapiletti, S.; Knappskog, P. M.; McKinney, J.; Maier, W.; Jamra, R. A.; Schulze, T. G.; Schumacher, J.; Propping, P.; Rietschel, M.; Haavik, J.; Nothen, M. M. Brainspecific tryptophan hydroxylase 2 (TPH2): a functional Pro206Ser substitution and variation in the 5?-region are associated with bipolar affective disorder. Hum. Mol. Genet. 2008, 17 (1), 87-97.
119. Haavik, J.; Blau, N.; Thony, B. Mutations in human monoaminerelated neurotransmitter pathway genes. Hum. Mutat. 2008, 29 (7), 891-902. (Pubitemid 351951283)
120. Lee, M. P. Genome-wide analysis of epigenetics in cancer. Ann. N.Y. Acad. Sci. 2003, 983, 101-9. (Pubitemid 36399323)
121. Lee, T. I.; Jenner, R. G.; Boyer, L. A.; Guenther, M. G.; Levine, S. S.; Kumar, R. M.; Chevalier, B.; Johnstone, S. E.; Cole, M. F.; Isono, K.; Koseki, H.; Fuchikami, T.; Abe, K.; Murray, H. L.; Zucker, J. P.; Yuan, B.; Bell, G. W.; Herbolsheimer, E.; Hannett, N. M.; Sun, K.; Odom, D. T.; Otte, A. P.; Volkert, T. L.; Bartel, D. P.; Melton, D. A.; Gifford, D. K.; Jaenisch, R.; Young, R. A. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006, 125 (2), 301-13. (Pubitemid 44313811)
122. Grayson, D. R.; Kundakovic, M.; Sharma, R. P. Is there a future for histone deacetylase inhibitors in the pharmacotherapy of psychiatric disorders. Mol. Pharmacol. 2010, 77 (2), 126-35.
123. Abel, T.; Zukin, R. S. Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders. Curr. Opin. Pharmacol. 2008, 8 (1), 57-64.