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    Schahram Akbarian MD

    TitleProfessor
    InstitutionUniversity of Massachusetts Medical School
    DepartmentPsychiatry
    AddressUniversity of Massachusetts Medical School
    303 Belmont Street
    Worcester MA 01605
    Phone508-856-2674
      Other Positions
      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentBioinformatics and Computational Biology

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentInterdisciplinary Graduate Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentMD/PhD Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentNeuroscience

      InstitutionUMMS - Programs, Centers and Institutes
      DepartmentBioinformatics and Integrative Biology

      InstitutionUMMS - Programs, Centers and Institutes
      DepartmentBrudnick Neuropsychiatric Research Institute

        Overview 
        Narrative

        Academic Background

          Clinical Assistant in Psychiatry
          Massachusetts General Hospital and McLean Hospital
          Harvard Medical School
          Belmont, MA
        M.D. Freie Universitaet Berlin, Germany 1989
        Ph.D. Freie Universitaet Berlin, Germany 1991
        Postdoctoral Fellow
        University of California, Irvine, CA
        1991-1994
        Residency in Psychiatry
        Massachusetts General Hospital
        Harvard Medical School, Boston, MA
        1995-1999
        Assistant Professor in Psychiatry
        Massachusetts General Hospital
        Harvard Medical School
        2000-2001

        Schahram Akbarian, PhD, MD

        Epigenetics and the Brain

        Epigenetic marks, including cytosine methylation of genomic DNA and a rich cache of post-translational modifications of nucleosome core histones, could provide a type of cellular memory, and potentially maintained for the remainder of a cell's life and transmitted to daughter cells. Furthermore, evidence is accumulating that there is epigenetic heritability across generations in human, at least in principle. Therefore, the general theme of epigenetics is of great interest to the field of biological psychiatry because (i) it could provide valid and testable alternatives to genetic heritability models and (ii) exploration of chromatin structure and function in healthy and diseased brain could provide novel insights into the pathophysiology of major psychiatric disease. The primary focus of our laboratory is on the exploration of neuronal epigenomes in preclinical model systems and in human (postmortem) brain tissue. The following example highlights an ongoing research project:

        Chromatin Alterations in Developing and Diseased Prefrontal Cortex

        Prolonged maturation of prefrontal cortex (PFC), extending into or even beyond the second decade, plays a key role for normal human development and the neurobiology of schizophrenia, mood spectrum disorders and other disease. Contemporary neurobiological models explaining the protracted maturation of prefrontal and other higher order association areas of the human cerebral cortex-such as (i) changes in supply and expression of certain neurotrophic factors; or (ii) increased axon fiber myelination, or (iii) synaptic pruning- in essence date back more than 20 years, and only few advancements have been made since then. Moreover, many of these hypotheses are built on correlative observations and there is little evidence for causality. Because a number of neuronal genes undergo progressive histone lysine methylation during early childhood years, changes in neuronal chromatin structure and function, in conjunction with transcriptional regulation, could take part in a molecular "clock" operating during an extended period of PFC development, thereby regulating the protracted maturation of its neuronal circuitry. These may involve dynamic adaptations of site-specific histone lysine methylation markings that are thought to contribute to epigenetic control of gene expression. We approach this topic by genome-wide mapping of histone methylation landscapes in prefrontal neurons: (1) across the lifespan to understand normal development and aging; (2) in subjects on the psychosis or autism spectrum in order to gain insight into mechanisms of disease; (3) in genetically engineered mice with brain-specific ablation, or siRNA-mediated knockdown, of selected histone methyltransferase and demethylase enzymes that specifically target the histone H3-lysine 4 residue which is highly regulated at enhancer sequences and transcription start sites (see Figure).

        Figure

        Figure



        Rotation Projects

        Potential Rotation Projects

        1. Drug-induced adaptations in neuronal circuitry contributing to psychosis or addiction could be viewed as a form of neuronal plasticity and thus may depend on similar molecular mechanisms that operate in learning and memory centers of the brain. The goal of this project is treat mice with chromatin modifying drugs and to explore the resulting molecular adaptations in nuclei of neurons located in fore- and hindbrain. Students will gain experience in mouse genetics, neuroanatomy and various chromatin assays. Furthermore, students will have the opportunity to study current models of major psychiatric disease, including schizophrenia, mood disorders and addiction.

        2. The genome of vertebrates is subject to epigenetic modifications, including the methylation of cytosine residues in symmetrically positioned CpG dinucleotides. DNA-methylation has profound effects on transcriptional activity and chromosomal stability. The goal of this project is to determine the regulation of DNA-methylation in developing and aging brain. Students will apply various techniques to examine DNA-methylation patterns of selected gene sequences in defined cell populations of the CNS.



        Bibliographic 
        selected publications
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        1. Hoss AG, Kartha VK, Dong X, Latourelle JC, Dumitriu A, Hadzi TC, Macdonald ME, Gusella JF, Akbarian S, Chen JF, Weng Z, Myers RH. MicroRNAs Located in the Hox Gene Clusters Are Implicated in Huntington's Disease Pathogenesis. PLoS Genet. 2014 Feb; 10(2):e1004188.
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        2. Ginns EI, Mak SK, Ko N, Karlgren J, Akbarian S, Chou VP, Guo Y, Lim A, Samuelsson S, Lamarca ML, Vazquez-Derose J, Manning-Bog AB. Neuroinflammation and a-synuclein accumulation in response to glucocerebrosidase deficiency are accompanied by synaptic dysfunction. Mol Genet Metab. 2014 Feb; 111(2):152-62.
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        3. Udagawa T, Farny NG, Jakovcevski M, Kaphzan H, Alarcon JM, Anilkumar S, Ivshina M, Hurt JA, Nagaoka K, Nalavadi VC, Lorenz LJ, Bassell GJ, Akbarian S, Chattarji S, Klann E, Richter JD. Genetic and acute CPEB1 depletion ameliorate fragile X pathophysiology. Nat Med. 2013 Nov; 19(11):1473-7.
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        4. Mitchell AC, Bharadwaj R, Whittle C, Krueger W, Mirnics K, Hurd Y, Rasmussen T, Akbarian S. The genome in three dimensions: a new frontier in human brain research. Biol Psychiatry. 2014 Jun 15; 75(12):961-9.
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        5. Bharadwaj R, Jiang Y, Mao W, Jakovcevski M, Dincer A, Krueger W, Garbett K, Whittle C, Tushir JS, Liu J, Sequeira A, Vawter MP, Gardner PD, Casaccia P, Rasmussen T, Bunney WE, Mirnics K, Futai K, Akbarian S. Conserved chromosome 2q31 conformations are associated with transcriptional regulation of GAD1 GABA synthesis enzyme and altered in prefrontal cortex of subjects with schizophrenia. J Neurosci. 2013 Jul 17; 33(29):11839-51.
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        6. Tushir JS, Akbarian S. Chromatin-bound RNA and the neurobiology of psychiatric disease. Neuroscience. 2014 Apr 4; 264:131-41.
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        7. Akbarian S, Beeri MS, Haroutunian V. Epigenetic determinants of healthy and diseased brain aging and cognition. JAMA Neurol. 2013 Jun; 70(6):711-8.
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        8. Jakovcevski M, Bharadwaj R, Straubhaar J, Gao G, Gavin DP, Jakovcevski I, Mitchell AC, Akbarian S. Prefrontal cortical dysfunction after overexpression of histone deacetylase 1. Biol Psychiatry. 2013 Nov 1; 74(9):696-705.
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        9. Akbarian S, Halene T. The neuroepigenetics of suicide. Am J Psychiatry. 2013 May 1; 170(5):462-5.
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        10. Shulha HP, Cheung I, Guo Y, Akbarian S, Weng Z. Coordinated cell type-specific epigenetic remodeling in prefrontal cortex begins before birth and continues into early adulthood. PLoS Genet. 2013 Apr; 9(4):e1003433.
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        11. Hasan A, Mitchell A, Schneider A, Halene T, Akbarian S. Epigenetic dysregulation in schizophrenia: molecular and clinical aspects of histone deacetylase inhibitors. Eur Arch Psychiatry Clin Neurosci. 2013 Jun; 263(4):273-84.
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        12. Hope BT, Skinner MK, Kenny PJ, Akbarian S. Exploring the epigenetics of cocaine resistance. Nat Med. 2013 Feb; 19(2):136-7.
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        13. Akbarian S, Nestler EJ. Epigenetic mechanisms in psychiatry. Neuropsychopharmacology. 2013 Jan; 38(1):1-2.
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        14. Shulha HP, Crisci JL, Reshetov D, Tushir JS, Cheung I, Bharadwaj R, Chou HJ, Houston IB, Peter CJ, Mitchell AC, Yao WD, Myers RH, Chen JF, Preuss TM, Rogaev EI, Jensen JD, Weng Z, Akbarian S. Human-specific histone methylation signatures at transcription start sites in prefrontal neurons. PLoS Biol. 2012; 10(11):e1001427.
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        15. Jakovcevski M, Akbarian S. Epigenetic mechanisms in neurological disease. Nat Med. 2012 Aug; 18(8):1194-204.
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        16. Connor CM, Dincer A, Straubhaar J, Galler JR, Houston IB, Akbarian S. Maternal immune activation alters behavior in adult offspring, with subtle changes in the cortical transcriptome and epigenome. Schizophr Res. 2012 Sep; 140(1-3):175-84.
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        17. Qin J, Whyte WA, Anderssen E, Apostolou E, Chen HH, Akbarian S, Bronson RT, Hochedlinger K, Ramaswamy S, Young RA, Hock H. The polycomb group protein L3mbtl2 assembles an atypical PRC1-family complex that is essential in pluripotent stem cells and early development. Cell Stem Cell. 2012 Sep 7; 11(3):319-32.
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        18. Houston I, Peter CJ, Mitchell A, Straubhaar J, Rogaev E, Akbarian S. Epigenetics in the human brain. Neuropsychopharmacology. 2013 Jan; 38(1):183-97.
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        19. Rane P, Shields J, Heffernan M, Guo Y, Akbarian S, King JA. The histone deacetylase inhibitor, sodium butyrate, alleviates cognitive deficits in pre-motor stage PD. Neuropharmacology. 2012 Jun; 62(7):2409-12.
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        20. Gavin DP, Akbarian S. Epigenetic and post-transcriptional dysregulation of gene expression in schizophrenia and related disease. Neurobiol Dis. 2012 May; 46(2):255-62.
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        21. Shulha HP, Cheung I, Whittle C, Wang J, Virgil D, Lin CL, Guo Y, Lessard A, Akbarian S, Weng Z. Epigenetic signatures of autism: trimethylated H3K4 landscapes in prefrontal neurons. Arch Gen Psychiatry. 2012 Mar; 69(3):314-24.
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        22. Marder SR, Roth B, Sullivan PF, Scolnick EM, Nestler EJ, Geyer MA, Welnberger DR, Karayiorgou M, Guidotti A, Gingrich J, Akbarian S, Buchanan RW, Lieberman JA, Conn PJ, Haggarty SJ, Law AJ, Campbell B, Krystal JH, Moghaddam B, Sawa A, Saw A, Caron MG, George SR, Allen JA, Solis M. Advancing drug discovery for schizophrenia. Ann N Y Acad Sci. 2011 Oct; 1236:30-43.
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        23. Peter CJ, Akbarian S. Balancing histone methylation activities in psychiatric disorders. Trends Mol Med. 2011 Jul; 17(7):372-9.
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        24. Yang C, Tan W, Whittle C, Qiu L, Cao L, Akbarian S, Xu Z. The C-terminal TDP-43 fragments have a high aggregation propensity and harm neurons by a dominant-negative mechanism. PLoS One. 2010; 5(12):e15878.
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        25. Akbarian S, Davis RJ. Keep the 'phospho' on MAPK, be happy. Nat Med. 2010 Nov; 16(11):1187-8.
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        26. Jiang Y, Matevossian A, Guo Y, Akbarian S. Setdb1-mediated histone H3K9 hypermethylation in neurons worsens the neurological phenotype of Mecp2-deficient mice. Neuropharmacology. 2011 Jun; 60(7-8):1088-97.
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        27. Mellios N, Galdzicka M, Ginns E, Baker SP, Rogaev E, Xu J, Akbarian S. Gender-specific reduction of estrogen-sensitive small RNA, miR-30b, in subjects with schizophrenia. Schizophr Bull. 2012 May; 38(3):433-43.
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        28. Connor CM, Crawford BC, Akbarian S. White matter neuron alterations in schizophrenia and related disorders. Int J Dev Neurosci. 2011 May; 29(3):325-34.
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        29. Huang HS, Cheung I, Akbarian S. RPP25 is developmentally regulated in prefrontal cortex and expressed at decreased levels in autism spectrum disorder. Autism Res. 2010 Aug; 3(4):153-61.
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        30. Connor C, Cheung I, Simon A, Jakovcevski M, Weng Z, Akbarian S. A simple method for improving the specificity of anti-methyl histone antibodies. Epigenetics. 2010 Jul 1; 5(5):392-5.
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        31. Qin J, Van Buren D, Huang HS, Zhong L, Mostoslavsky R, Akbarian S, Hock H. Chromatin protein L3MBTL1 is dispensable for development and tumor suppression in mice. J Biol Chem. 2010 Sep 3; 285(36):27767-75.
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        32. Jiang Y, Jakovcevski M, Bharadwaj R, Connor C, Schroeder FA, Lin CL, Straubhaar J, Martin G, Akbarian S. Setdb1 histone methyltransferase regulates mood-related behaviors and expression of the NMDA receptor subunit NR2B. J Neurosci. 2010 May 26; 30(21):7152-67.
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        33. Cheung I, Shulha HP, Jiang Y, Matevossian A, Wang J, Weng Z, Akbarian S. Developmental regulation and individual differences of neuronal H3K4me3 epigenomes in the prefrontal cortex. Proc Natl Acad Sci U S A. 2010 May 11; 107(19):8824-9.
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        34. Jakovcevski M, Guo Y, Su Q, Gao G, Akbarian S. rAAV9--a human-derived adeno-associated virus vector for efficient transgene expression in mouse cingulate cortex. Cold Spring Harb Protoc. 2010 Apr; 2010(4):pdb.prot5417.
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        35. Akbarian S. Epigenetics of schizophrenia. Curr Top Behav Neurosci. 2010; 4:611-28.
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        36. Akbarian S. The molecular pathology of schizophrenia--focus on histone and DNA modifications. Brain Res Bull. 2010 Sep 30; 83(3-4):103-7.
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        37. Febo M, Akbarian S, Schroeder FA, Ferris CF. Cocaine-induced metabolic activation in cortico-limbic circuitry is increased after exposure to the histone deacetylase inhibitor, sodium butyrate. Neurosci Lett. 2009 Nov 20; 465(3):267-71.
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        38. Connor CM, Guo Y, Akbarian S. Cingulate white matter neurons in schizophrenia and bipolar disorder. Biol Psychiatry. 2009 Sep 1; 66(5):486-93.
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        39. Mellios N, Huang HS, Baker SP, Galdzicka M, Ginns E, Akbarian S. Molecular determinants of dysregulated GABAergic gene expression in the prefrontal cortex of subjects with schizophrenia. Biol Psychiatry. 2009 Jun 15; 65(12):1006-14.
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        40. Akbarian S. Restoring GABAergic signaling and neuronal synchrony in schizophrenia. Am J Psychiatry. 2008 Dec; 165(12):1507-9.
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        41. Jiang Y, Langley B, Lubin FD, Renthal W, Wood MA, Yasui DH, Kumar A, Nestler EJ, Akbarian S, Beckel-Mitchener AC. Epigenetics in the nervous system. J Neurosci. 2008 Nov 12; 28(46):11753-9.
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        42. Akbarian S. Approaching the molecular pathology of suicide. Biol Psychiatry. 2008 Oct 15; 64(8):643-4.
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        43. Matevossian A, Akbarian S. Neuronal nuclei isolation from human postmortem brain tissue. J Vis Exp. 2008; (20).
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        44. Akbarian S, Huang HS. Epigenetic regulation in human brain-focus on histone lysine methylation. Biol Psychiatry. 2009 Feb 1; 65(3):198-203.
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        45. Mellios N, Huang HS, Grigorenko A, Rogaev E, Akbarian S. A set of differentially expressed miRNAs, including miR-30a-5p, act as post-transcriptional inhibitors of BDNF in prefrontal cortex. Hum Mol Genet. 2008 Oct 1; 17(19):3030-42.
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        46. Jiang Y, Matevossian A, Huang HS, Straubhaar J, Akbarian S. Isolation of neuronal chromatin from brain tissue. BMC Neurosci. 2008; 9:42.
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        47. Matevossian A, Akbarian S. A chromatin assay for human brain tissue. J Vis Exp. 2008; (13).
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        48. Connor CM, Akbarian S. DNA methylation changes in schizophrenia and bipolar disorder. Epigenetics. 2008 Mar-Apr; 3(2):55-8.
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        49. Schroeder FA, Penta KL, Matevossian A, Jones SR, Konradi C, Tapper AR, Akbarian S. Drug-induced activation of dopamine D(1) receptor signaling and inhibition of class I/II histone deacetylase induce chromatin remodeling in reward circuitry and modulate cocaine-related behaviors. Neuropsychopharmacology. 2008 Nov; 33(12):2981-92.
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        50. Huang HS, Matevossian A, Whittle C, Kim SY, Schumacher A, Baker SP, Akbarian S. Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters. J Neurosci. 2007 Oct 17; 27(42):11254-62.
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        51. Siegmund KD, Connor CM, Campan M, Long TI, Weisenberger DJ, Biniszkiewicz D, Jaenisch R, Laird PW, Akbarian S. DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS One. 2007; 2(9):e895.
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        52. Huang HS, Akbarian S. GAD1 mRNA expression and DNA methylation in prefrontal cortex of subjects with schizophrenia. PLoS One. 2007; 2(8):e809.
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        53. Schroeder FA, Lin CL, Crusio WE, Akbarian S. Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry. 2007 Jul 1; 62(1):55-64.
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        54. Akbarian S, Huang HS. Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders. Brain Res Rev. 2006 Sep; 52(2):293-304.
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        55. Shimazu K, Zhao M, Sakata K, Akbarian S, Bates B, Jaenisch R, Lu B. NT-3 facilitates hippocampal plasticity and learning and memory by regulating neurogenesis. Learn Mem. 2006 May-Jun; 13(3):307-15.
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        56. Huang HS, Matevossian A, Jiang Y, Akbarian S. Chromatin immunoprecipitation in postmortem brain. J Neurosci Methods. 2006 Sep 30; 156(1-2):284-92.
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        57. Rios M, Lambe EK, Liu R, Teillon S, Liu J, Akbarian S, Roffler-Tarlov S, Jaenisch R, Aghajanian GK. Severe deficits in 5-HT2A -mediated neurotransmission in BDNF conditional mutant mice. J Neurobiol. 2006 Mar; 66(4):408-20.
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        58. Akbarian S, Jiang Y, Laforet G. The molecular pathology of Rett syndrome: synopsis and update. Neuromolecular Med. 2006; 8(4):485-94.
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        59. Akbarian S, Ruehl MG, Bliven E, Luiz LA, Peranelli AC, Baker SP, Roberts RC, Bunney WE, Conley RC, Jones EG, Tamminga CA, Guo Y. Chromatin alterations associated with down-regulated metabolic gene expression in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry. 2005 Aug; 62(8):829-40.
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        60. Stadler F, Kolb G, Rubusch L, Baker SP, Jones EG, Akbarian S. Histone methylation at gene promoters is associated with developmental regulation and region-specific expression of ionotropic and metabotropic glutamate receptors in human brain. J Neurochem. 2005 Jul; 94(2):324-36.
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        61. Li J, Guo Y, Schroeder FA, Youngs RM, Schmidt TW, Ferris C, Konradi C, Akbarian S. Dopamine D2-like antagonists induce chromatin remodeling in striatal neurons through cyclic AMP-protein kinase A and NMDA receptor signaling. J Neurochem. 2004 Sep; 90(5):1117-31.
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        62. Akbarian S. The neurobiology of Rett syndrome. Neuroscientist. 2003 Feb; 9(1):57-63.
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        63. Tudor M, Akbarian S, Chen RZ, Jaenisch R. Transcriptional profiling of a mouse model for Rett syndrome reveals subtle transcriptional changes in the brain. Proc Natl Acad Sci U S A. 2002 Nov 26; 99(24):15536-41.
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        64. Albert KA, Hemmings HC, Adamo AI, Potkin SG, Akbarian S, Sandman CA, Cotman CW, Bunney WE, Greengard P. Evidence for decreased DARPP-32 in the prefrontal cortex of patients with schizophrenia. Arch Gen Psychiatry. 2002 Aug; 59(8):705-12.
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        65. Akbarian S. Diseases of the mind and brain: Rett's syndrome, part II. Am J Psychiatry. 2002 Aug; 159(8):1294.
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        66. Akbarian S. Diseases of the mind and brain: Rett's syndrome. Am J Psychiatry. 2002 Jul; 159(7):1103.
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        67. Akbarian S, Rios M, Liu RJ, Gold SJ, Fong HF, Zeiler S, Coppola V, Tessarollo L, Jones KR, Nestler EJ, Aghajanian GK, Jaenisch R. Brain-derived neurotrophic factor is essential for opiate-induced plasticity of noradrenergic neurons. J Neurosci. 2002 May 15; 22(10):4153-62.
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        68. Akbarian S. Clinical experts on Rett disorder. Pediatr Rehabil. 2002 Apr-Jun; 5(2):117-8.
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        69. Bates B, Hirt L, Thomas SS, Akbarian S, Le D, Amin-Hanjani S, Whalen M, Jaenisch R, Moskowitz MA. Neurotrophin-3 promotes cell death induced in cerebral ischemia, oxygen-glucose deprivation, and oxidative stress: possible involvement of oxygen free radicals. Neurobiol Dis. 2002 Feb; 9(1):24-37.
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        70. Akbarian S, Chen RZ, Gribnau J, Rasmussen TP, Fong H, Jaenisch R, Jones EG. Expression pattern of the Rett syndrome gene MeCP2 in primate prefrontal cortex. Neurobiol Dis. 2001 Oct; 8(5):784-91.
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        71. Akbarian S, Bates B, Liu RJ, Skirboll SL, Pejchal T, Coppola V, Sun LD, Fan G, Kucera J, Wilson MA, Tessarollo L, Kosofsky BE, Taylor JR, Bothwell M, Nestler EJ, Aghajanian GK, Jaenisch R. Neurotrophin-3 modulates noradrenergic neuron function and opiate withdrawal. Mol Psychiatry. 2001 Sep; 6(5):593-604.
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        72. Chen RZ, Akbarian S, Tudor M, Jaenisch R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet. 2001 Mar; 27(3):327-31.
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        73. Akbarian S, Kim JJ, Potkin SG, Hetrick WP, Bunney WE, Jones EG. Maldistribution of interstitial neurons in prefrontal white matter of the brains of schizophrenic patients. Arch Gen Psychiatry. 1996 May; 53(5):425-36.
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        74. Akbarian S, Sucher NJ, Bradley D, Tafazzoli A, Trinh D, Hetrick WP, Potkin SG, Sandman CA, Bunney WE, Jones EG. Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics. J Neurosci. 1996 Jan; 16(1):19-30.
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        75. Akbarian S, Smith MA, Jones EG. Editing for an AMPA receptor subunit RNA in prefrontal cortex and striatum in Alzheimer's disease, Huntington's disease and schizophrenia. Brain Res. 1995 Nov 20; 699(2):297-304.
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        76. Akbarian S, Huntsman MM, Kim JJ, Tafazzoli A, Potkin SG, Bunney WE, Jones EG. GABAA receptor subunit gene expression in human prefrontal cortex: comparison of schizophrenics and controls. Cereb Cortex. 1995 Nov-Dec; 5(6):550-60.
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        77. Sucher NJ, Akbarian S, Chi CL, Leclerc CL, Awobuluyi M, Deitcher DL, Wu MK, Yuan JP, Jones EG, Lipton SA. Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J Neurosci. 1995 Oct; 15(10):6509-20.
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        78. Akbarian S, Kim JJ, Potkin SG, Hagman JO, Tafazzoli A, Bunney WE, Jones EG. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry. 1995 Apr; 52(4):258-66.
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        79. Akbarian S, Bunney WE, Potkin SG, Wigal SB, Hagman JO, Sandman CA, Jones EG. Altered distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development. Arch Gen Psychiatry. 1993 Mar; 50(3):169-77.
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        80. Akbarian S, Viñuela A, Kim JJ, Potkin SG, Bunney WE, Jones EG. Distorted distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase neurons in temporal lobe of schizophrenics implies anomalous cortical development. Arch Gen Psychiatry. 1993 Mar; 50(3):178-87.
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        81. Akbarian S, Berndl K, Grüsser OJ, Guldin W, Pause M, Schreiter U. Responses of single neurons in the parietoinsular vestibular cortex of primates. Ann N Y Acad Sci. 1988; 545:187-202.
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