Region-specific alterations of A-to-I RNA editing of serotonin 2c receptor in the cortex of suicides with major depression

Translational Psychiatry

Volumn 6, Issue 8, 2016, Pages

  Weissmann, D ^a   van der Laan, S ^a   Underwood, M D ^b,c   Salvetat, N ^a   Cavarec, L ^d   Vincent, L ^e   Molina, F ^a   Mann, J J ^b,c   Arango, V ^b,c   Pujol, J F ^a  

^a Cap delta Parc Euromédecine   (France)

^b Columbia University College of Physicians and Surgeons ^*  (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^d Genomic Vision   (France)

^e INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; SEROTONIN 2C RECEPTOR;

ADOLESCENT; ADULT; AUTOMUTILATION; AUTOPSY; BRAIN CORTEX; CAPILLARY ELECTROPHORESIS; CASE CONTROL STUDY; CINGULATE GYRUS; DEAMINATION; FEMALE; GENETICS; HUMAN; MAJOR DEPRESSION; MALE; METABOLISM; MIDDLE AGED; PREFRONTAL CORTEX; RNA EDITING; SINGLE STRAND CONFORMATION POLYMORPHISM; SUICIDE; YOUNG ADULT;

ADOLESCENT; ADULT; AUTOPSY; CASE-CONTROL STUDIES; CEREBRAL CORTEX; DEAMINATION; DEPRESSIVE DISORDER, MAJOR; ELECTROPHORESIS, CAPILLARY; FEMALE; GYRUS CINGULI; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE-STRANDED CONFORMATIONAL; PREFRONTAL CORTEX; RECEPTOR, SEROTONIN, 5-HT2C; RNA EDITING; RNA, MESSENGER; SELF-INJURIOUS BEHAVIOR; SUICIDE; YOUNG ADULT;

EID: 85021213297     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/TP.2016.121     Document Type: Article

References (64)

1. WHO. Preventing Suicide: a Global Imperative WHO. 2014; URL: http://www.who. int.gate1.inist.fr/mental_health/suicide-prevention/world_report_2014/en/.
2. Cavanagh JT, Carson AJ, Sharpe M, Lawrie SM. Psychological autopsy studies of suicide: a systematic review. Psychol Med 2003; 33: 395–405.
3. Harris EC, Barraclough B. Suicide as an outcome for mental disorders. A meta-a-nalysis. Br J Psychiatry 1997; 170: 205–228.
4. Arango V, Huang YY, Underwood MD, Mann JJ. Genetics of the serotonergic system in suicidal behavior. J Psychiatric Res 2003; 37: 375–386.
5. Giorgetti M, Tecott LH. Contributions of 5-HT(2C) receptors to multiple actions of central serotonin systems. Eur J Pharmacol 2004; 488: 1–9.
6. Barnes NM, Sharp T. A review of central 5-HT receptors and their function. Neuro-pharmacology 1999; 38: 1083–1152.
7. Abramowski D, Rigo M, Duc D, Hoyer D, Staufenbiel M. Localization of the 5-hydroxytryptamine2C receptor protein in human and rat brain using specific antisera. Neuropharmacology 1995; 34: 1635–1645.
8. Karanovic J, Svikovic S, Pantovic M, Durica S, Brajuskovic G, Damjanovic A et al. Joint effect of ADARB1 gene, HTR2C gene and stressful life events on suicide attempt risk in patients with major psychiatric disorders. World J Biol Psychiatry 2015; 16: 261–271.
9. Jacobs MM, Fogg RL, Emeson RB, Stanwood GD. ADAR1 and ADAR2 expression and editing activity during forebrain development. Dev Neurosci 2009; 31: 223–237.
10. Bazak L, Haviv A, Barak M, Jacob-Hirsch J, Deng P, Zhang R et al. A-to-I RNA editing occurs at over a hundred million genomic sites, located in a majority of human genes. Genome Res 2014; 24: 365–376.
11. Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M, Shemesh R et al. Systematic identification of abundant A-to-I editing sites in the human tran-scriptome. Nat Biotechnol 2004; 22: 1001–1005.
12. Behm M, Ohman M. RNA editing: a contributor to neuronal dynamics in the mammalian brain. Trends Genet 2016; 32: 165–175.
13. Rosenthal JJ, Seeburg PH. A-to-I RNA editing: effects on proteins key to neural excitability. Neuron 2012; 74: 432–439.
14. Berg KA, Cropper JD, Niswender CM, Sanders-Bush E, Emeson RB, Clarke WP. RNA-editing of the 5-HT(2C) receptor alters agonist-receptor-effector coupling speci-ficity. Br J Pharmacol 2001; 134: 386–392.
15. Niswender CM, Copeland SC, Herrick-Davis K, Emeson RB, Sanders-Bush E. RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences con-stitutive activity.J Biol Chem 1999; 274: 9472–9478.
16. Price RD, Sanders-Bush E. RNA editing of the human serotonin 5-HT(2C) receptor delays agonist-stimulated calcium release. Mol Pharmacol 2000; 58: 859–862.
17. Price RD, Weiner DM, Chang MS, Sanders-Bush E. RNA editing of the human serotonin 5-HT2C receptor alters receptor-mediated activation of G13 protein. J Biol Chem 2001; 276: 44663–44668.
18. Yang W, Wang Q, Kanes SJ, Murray JM, Nishikura K, Altered RNA. editing of serotonin 5-HT2C receptor induced by interferon: implications for depression associated with cytokine therapy. Brain Res Mol Brain Res 2004; 124: 70–78.
19. Werry TD, Loiacono R, Sexton PM, Christopoulos A. RNA editing of the serotonin 5HT2C receptor and its effects on cell signalling, pharmacology and brain func-tion. Pharmacol Ther 2008; 119: 7–23.
20. Martin CB, Ramond F, Farrington DT, Aguiar AS Jr, Chevarin C, Berthiau AS et al. RNA splicing and editing modulation of 5-HT(2C) receptor function: relevance to anxiety and aggression in VGV mice. Mol Psychiatry 2013; 18: 656–665.
21. Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H, Sanders-Bush E et al. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 1997; 387: 303–308.
22. Di Giovanni G, Di Matteo V, Pierucci M, Benigno A, Esposito E. Central serotonin2C receptor: from physiology to pathology. Curr Topics Med Chem 2006; 6: 1909–1925.
23. Fitzgerald LW, Iyer G, Conklin DS, Krause CM, Marshall A, Patterson JP et al. Messenger RNA editing of the human serotonin 5-HT2C receptor. Neuropsycho-pharmacology 1999; 21(2 Suppl): 82S–90S.
24. Di Narzo AF, Kozlenkov A, Roussos P, Hao K, Hurd Y, Lewis DA et al. A unique gene expression signature associated with serotonin 2C receptor RNA editing in the prefrontal cortex and altered in suicide. Hum Mol Genet 2014; 23: 4801–4813.
25. Dracheva S, Chin B, Haroutunian V. Altered serotonin 2C receptor RNA splicing in suicide: association with editing. Neuroreport 2008; 19: 379–382.
26. Lyddon R, Dwork AJ, Keddache M, Siever LJ, Dracheva S. Serotonin 2c receptor RNA editing in major depression and suicide. World J Biol Psychiatry 2013; 14: 590–601.
27. Dracheva S, Patel N, Woo DA, Marcus SM, Siever LJ, Haroutunian V. Increased serotonin 2C receptor mRNA editing: a possible risk factor for suicide. Mol Psychiatry 2008; 13: 1001–1010.
28. Poyau A, Vincent L, Berthomme H, Paul C, Nicolas B, Pujol JF et al. Identification and relative quantification of adenosine to inosine editing in serotonin 2c receptor mRNA by CE. Electrophoresis 2007; 28: 2843–2852.
29. Cieslik EC, Zilles K, Caspers S, Roski C, Kellermann TS, Jakobs O et al. Is there "one" DLPFC in cognitive action control? Evidence for heterogeneity from co-activation-based parcellation. Cereb Cortex 2013; 23: 2677–2689.
30. Mayberg HS. Limbic-cortical dysregulation: a proposed model of depression. The Journal of neuropsychiatry and clinical neurosciences. 1997. Summer 9: 471–481.
31. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C et al. Deep brain stimulation for treatment-resistant depression. Neuron 2005; 45: 651–660.
32. Rajkowska G, Miguel-Hidalgo JJ, Wei J, Dilley G, Pittman SD, Meltzer HY et al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 1999; 45: 1085–1098.
33. Benes FM, Vincent SL, Todtenkopf M. The density of pyramidal and nonpyramidal neurons in anterior cingulate cortex of schizophrenic and bipolar subjects. Biol Psychiatry 2001; 50: 395–406.
34. Cotter D, Mackay D, Landau S, Kerwin R, Everall I. Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Arch Gen Psychiatry 2001; 58: 545–553.
35. Ongur D, Drevets WC, Price JL. Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci USA 1998; 95: 13290–13295.
36. Arango V, Underwood MD, Gubbi AV, Mann JJ. Localized alterations in pre-and postsynaptic serotonin binding sites in the ventrolateral prefrontal cortex of suicide victims. Brain Res 1995; 688: 121–133.
37. Boldrini M, Underwood MD, Hen R, Rosoklija GB, Dwork AJ, John Mann J et al. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 2009; 34: 2376–2389.
38. Mann JJ, Huang YY, Underwood MD, Kassir SA, Oppenheim S, Kelly TM et al. A serotonin transporter gene promoter polymorphism (5-HTTLPR) and prefrontal cortical binding in major depression and suicide. Arch Gen Psychiatry 2000; 57: 729–738.
39. Harrison PJ, Heath PR, Eastwood SL, Burnet PW, McDonald B, Pearson RC. The relative importance of premortem acidosis and postmortem interval for human brain gene expression studies: selective mRNA vulnerability and comparison with their encoded proteins. Neurosci Lett 1995; 200: 151–154.
40. Kelly TM, Mann JJ. Validity of DSM-III-R diagnosis by psychological autopsy: a comparison with clinician ante-mortem diagnosis. Acta Psychiatr Scand 1996; 94: 337–343.
41. Spitzer RL, Williams JBW, Gibbon M, First MB. Structured Clinican Interview for DSM-III-R Axis II Disorders, (SCID-II). American Psychiatric Press, Inc.: Washington, DC, 1990.
42. First MB, Spitzer RL, Gibbon M, Williams JMG, Benjamin L. Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II). American Psychiatric Press, Inc.: Washington, DC, 1997.
43. Arango V, Underwood MD, Boldrini M, Tamir H, Kassir SA, Hsiung S et al. Serotonin 1A receptors, serotonin transporter binding and serotonin transporter mRNA expression in the brainstem of depressed suicide victims. Neuropsychopharma-cology 2001; 25: 892–903.
44. Posner K, Oquendo MA, Gould M, Stanley B, Davies M. Columbia Classification Algorithm of Suicide Assessment (C-CASA): classification of suicidal events in the FDA's pediatric suicidal risk analysis of antidepressants. Am J Psychiatry 2007; 164: 1035–1043.
45. Oquendo MA, Currier D, Mann JJ. Prospective studies of suicidal behavior in major depressive and bipolar disorders: what is the evidence for predictive risk factors? Acta Pychiatr Scand 2006; 114: 151–158.
46. Mayberg HS. Defining the neural circuitry of depression: toward a new nosology with therapeutic implications. Biol Psychiatry 2007; 61: 729–730.
47. Petrides M, Pandya DN. Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci 2002; 16: 291–310.
48. Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR. Human cingulate cortex: surface fea-tures, flat maps, and cytoarchitecture. J Comp Neurol 1995; 359: 490–506.
49. Copois V, Bibeau F, Bascoul-Mollevi C, Salvetat N, Chalbos P, Bareil C et al. Impact of RNA degradation on gene expression profiles: assessment of different methods to reliably determine RNA quality. J Biotechnol 2007; 127: 549–559.
50. Developoment Core Team. R. A language and environment for statistical com-puting. R Foundation for Statistical Computing, 2012.
51. Schiffer HH, Heinemann SF. A quantitative method to detect RNA editing events. Anal Biochem 1999; 276: 257–260.
52. Mostafavi S, Battle A, Zhu X, Potash JB, Weissman MM, Shi J et al. Type I interferon signaling genes in recurrent major depression: increased expression detected by whole-blood RNA sequencing. Mol Psychiatry 2014; 19: 1267–1274.
53. Bonaccorso S, Marino V, Biondi M, Grimaldi F, Ippoliti F, Maes M. Depression induced by treatment with interferon-alpha in patients affected by hepatitis C virus. J Affect Disord 2002; 72: 237–241.
54. Bonaccorso S, Marino V, Puzella A, Pasquini M, Biondi M, Artini M et al. Increased depressive ratings in patients with hepatitis C receiving interferon-alpha-based immunotherapy are related to interferon-alpha-induced changes in the serotonergic system. J Clin Psychopharmacol 2002; 22: 86–90.
55. Dieperink E, Willenbring M, Ho SB. Neuropsychiatric symptoms associated with hepatitis C and interferon alpha: a review. Am J Psychiatry 2000; 157: 867–876.
56. Cavarec L, Vincent L, Le Borgne C, Plusquellec C, Ollivier N, Normandie-Levi P et al. In vitro screening for drug-induced depression and/or suicidal adverse effects: a new toxicogenomic assay based on CE-SSCP analysis of HTR2C mRNA editing in SH-SY5Y cells. Neurotox Res 2013; 23: 49–62.
57. Patterson JB, Samuel CE. Expression and regulation by interferon of a double-stranded-RNA-specific adenosine deaminase from human cells: evidence for two forms of the deaminase. Mol Cell Biol 1995; 15: 5376–5388.
58. Simmons M, Meador-Woodruff JH, Sodhi MS. Increased cortical expression of an RNA editing enzyme occurs in major depressive suicide victims. Neuroreport 2010; 21: 993–997.
59. Maes M, Meltzer HY, Bosmans E, Bergmans R, Vandoolaeghe E, Ranjan R et al. Increased plasma concentrations of interleukin-6, soluble interleukin-6, soluble interleukin-2 and transferrin receptor in major depression. J Affect Disord 1995; 34: 301–309.
60. Lindqvist D, Janelidze S, Hagell P, Erhardt S, Samuelsson M, Minthon L et al. Interleukin-6 is elevated in the cerebrospinal fluid of suicide attempters and related to symptom severity. Biol Psychiatry 2009; 66: 287–292.
61. Janelidze S, Mattei D, Westrin A, Traskman-Bendz L, Brundin L. Cytokine levels in the blood may distinguish suicide attempters from depressed patients. Brain Behav Immun 2011; 25: 335–339.
62. Black C, Miller BJ. Meta-analysis of cytokines and chemokines in suicidality: dis-tinguishing suicidal versus nonsuicidal patients. Biol Psychiatry 2015; 78: 28–37.
63. Torres-Platas SG, Hercher C, Davoli MA, Maussion G, Labonte B, Turecki G et al. Astrocytic hypertrophy in anterior cingulate white matter of depressed suicides. Neuropsychopharmacology 2011; 36: 2650–2658.
64. Brande-Eilat N, Golumbic YN, Zaidan H, Gaisler-Salomon I. Acquisition of condi-tioned fear is followed by region-specific changes in RNA editing of glutamate receptors. Stress 2015; 18: 309–318.