Gene expression analysis of bipolar disorder reveals downregulation of the ubiquitin cycle and alterations in synaptic genes

Molecular Psychiatry

Volumn 11, Issue 10, 2006, Pages 965-978

  Ryan, M M ^a   Lockstone, H E ^a   Huffaker, S J ^a   Wayland, M T ^a   Webster, M J ^b   Bahn, S ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Bipolar disorder; Microarray analysis; Neuronal plasticity; Prefrontal cortex; Synaptic transmission; Ubiquitin

Indexed keywords

MESSENGER RNA; UBIQUITIN;

ADULT; ARTICLE; AUTOPSY; BIPOLAR DISORDER; BRAIN TISSUE; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DIFFERENTIAL DISPLAY; DOWN REGULATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; INTRACELLULAR TRANSPORT; MALE; MICROARRAY ANALYSIS; ORBITAL CORTEX; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE; SYNAPSE; UBIQUITINATION; UPREGULATION; VALIDATION PROCESS;

ADULT; BIPOLAR DISORDER; CEREBRAL CORTEX; FEMALE; FRONTAL LOBE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREFRONTAL CORTEX; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED; REFERENCE VALUES; RNA, MESSENGER; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; UBIQUITIN;

EID: 33749130645     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/sj.mp.4001875     Document Type: Article

References (86)

1. OMIM Record 125480. National Center for Biotechnology Information website (cited 2006 March); Available from: http://www.ncbi.nlm.nih.gov/entrez/ dispomim.cgi?id=125480.
2. OMIM Record 309200. National Center for Biotechnology Information website (cited 2006 March); Available from: http://www.ncbi.nlm.nih.gov/entrez/ dispomim.cgi?id=309200.
3. Prabakaran S, Swatton JE, Ryan MM, Huffaker SJ, Huang JT, Griffin JL et al. Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 2004; 9: 684-697, 643.
4. Middleton FA, Mirnics K, Pierri JN, Lewis DA, Levitt P. Gene expression profiling reveals alterations of specific metabolic pathways in schizophrenia. J Neurosci 2002; 22: 2718-2729.
5. Vawter MP, Crook JM, Hyde TM, Kleinman JE, Weinberger DR, Becker KG et al. Microarray analysis of gene expression in the prefrontal cortex in schizophrenia: a preliminary study. Schizophr Res 2002; 58: 11-20.
6. Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD et al. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Natl Acad Sci USA 2001; 98: 4746-4751.
7. Mirnics K, Middleton FA, Marquez A, Lewis DA, Levitt P. Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 2000; 28: 53-67.
8. Iwamoto K, Bundo M, Kato T. Altered expression of mitochondriarelated genes in postmortem brains of patients with bipolar disorder or schizophrenia, as revealed by large-scale DNA microarray analysis. Hum Mol Genet 2005; 14: 241-253.
9. Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB et al. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 2003; 362: 798-805.
10. Benes FM, Matzilevich D, Burke RE, Walsh J. The expression of proapoptosis genes is increased in bipolar disorder, but not in schizophrenia. Mol Psychiatry 2006; 11: 241-251.
11. Nakatani N, Hattori E, Ohnishi T, Dean B, Iwayama Y, Matsumoto I et al. Genome-wide expression analysis detects eight genes with robust alterations specific to bipolar I disorder: relevance to neuronal network perturbation. Hum Mol Genet 2006; 15: 1949-1962.
12. Sun X, Wang JF, Tseng M, Young LT. Downregulation in components of the mitochondrial electron transport chain in the postmortem frontal cortex of subjects with bipolar disorder. J Psychiatry Neurosci 2006; 31: 189-196.
13. Iwamoto K, Kakiuchi C, Bundo M, Ikeda K, Kato T. Molecular characterization of bipolar disorder by comparing gene expression profiles of postmortem brains of major mental disorders. Mol Psychiatry 2004; 9: 406-416.
14. Konradi C, Eaton M, MacDonald ML, Walsh J, Benes FM, Heckers S. Molecular evidence for mitochondrial dysfunction in bipolar disorder. Arch Gen Psychiatry 2004; 61: 300-308.
15. Bezchlibnyk YB, Wang JF, McQueen GM, Young LT. Gene expression differences in bipolar disorder revealed by cDNA array analysis of post-mortem frontal cortex. J Neurochem 2001; 79: 826-834.
16. Vawter MP, Tomita H, Meng F, Bolstad B, Li J, Evans S et al. Mitochondrial-related gene expression changes are sensitive to agonal-pH state: implications for brain disorders. Mol Psychiatry 2006.
17. Lacerda AL, Keshavan MS, Hardan AY, Yorbik O, Brambilla P, Sassi RB et al. Anatomic evaluation of the orbitofrontal cortex in major depressive disorder. Biol Psychiatry 2004; 55: 353-358.
18. Ryan MM, Huffaker SJ, Webster MJ, Wayland M, Freeman T, Bahn S. Application and optimization of microarray technologies for human postmortem brain studies. Biol Psychiatry 2004; 55: 329-336.
19. Affymetrix. (cited 2006 March); Available from: www.affymetrix.com.
20. Bolstad B. affyPLM: Fitting probe level models. Bioconductor website. cited 2005; Available from: http://www.bioconductor.org/repository/devel/ vignette/AffyExtensions.pdf.
21. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4: 249-264.
22. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 1995; 57: 289-300.
23. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5: R80.
24. Pollard KS, Dudoit S, van der Laan MJ. Multiple Testing Procedures: R Multtest Package and Applications to Genomics, UC Berkeley Division of Biostatistics Working Paper Series, Working Paper No. 164. The Berkeley Electronic Press, 2004 [cited 2006, March]; Available from: http://www.bepress. com/ucbbiostat/paper164/
25. 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.
26. Tomita H, Vawter MP, Walsh DM, Evans SJ, Choudary PV, Li J et al. Effect of agonal and postmortem factors on gene expression profile: quality control in microarray analyses of postmortem human brain. Biol Psychiatry 2004; 55: 346-352.
27. Zhong S, Storch KF, Lipan O, Kao MC, Weitz CJ, Wong WH. GoSurfer: a graphical interactive tool for comparative analysis of large gene sets in gene ontologytrade mark space. Appl Bioinformat 2004; 3: 261-264.
28. GoSurfer. (cited 2006 March); Available from: http://www.biostat.harvard. edu/complab/gosurfer/.
29. Liu G, Loraine AE, Shigeta R, Cline M, Cheng J, Valmeekam Vet al. NetAffx: Affymetrix probesets and annotations. Nucleic Acids Res 2003; 31: 82-86.
30. Gene Ontology Database. The Gene Ontology Project, (cited 2006 March); Available from: http://www.geneontology.org/.
31. Zhong S, Li C, Wong WH. ChipInfo: software for extracting gene annotation and gene ontology information for microarray analysis. Nucleic Acids Res 2003; 31: 3483-3486.
32. Khatri P, Draghici S, Ostermeier GC, Krawetz SA. Profiling gene expression using onto-express. Genomics 2002; 79: 266-270.
33. Onto-Express. (cited 2006 March); Available from: http://vortex.cs.wayne. edu/research.htm.
34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
35. Bosetti F, Bell JM, Manickam P. Microarray analysis of rat brain gene expression after chronic administration of sodium valproate. Brain Res Bull 2005; 65: 331-338.
36. Pemberton LF, Paschal BM. Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 2005; 6: 187-198.
37. Petronis A. Epigenetics and bipolar disorder: new opportunities and challenges. Am J Med Genet C Semin Med Genet 2003; 123: 65-75.
38. Berrettini WH. Susceptibility loci for bipolar disorder: overlap with inherited vulnerability to schizophrenia. Biol Psychiatry 2000; 47: 245-251.
39. Fujiwara K, Tenno T, Sugasawa K, Jee JG, Ohki I, Kojima C et al. Structure of the ubiquitin-interacting motif of S5a bound to the ubiquitin-like domain of HR23B. J Biol Chem 2004; 279: 4760-4767.
40. Bremner JD, Vythilingam M, Vermetten E, Nazeer A, Adil J, Khan S et al. Reduced volume of orbitofrontal cortex in major depression. Biol Psychiatry 2002; 51: 273-279.
41. Haldane M, Frangou S. New insights help define the pathophysiology of bipolar affective disorder: neuroimaging and neuropathology findings. Prog Neuropsychopharmacol Biol Psychiatry 2004; 28: 943-960.
42. Blumberg HP, Stern E, Ricketts S, Martinez D, de Asis J, White T et al. Rostral and orbital prefrontal cortex dysfunction in the manic state of bipolar disorder. Am J Psychiatry 1999; 156: 1986-1988.
43. 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.
44. Cotter D, Hudson L, Landau S. Evidence for orbitofrontal pathology in bipolar disorder and major depression, but not in schizophrenia. Bipolar Disord 2005; 7: 358-369.
45. Roberts NA, Beer JS, Werner KH, Scabini D, Levens SM, Knight RT et al. The impact of orbital prefrontal cortex damage on emotional activation to unanticipated and anticipated acoustic startle stimuli. Cogn Affect Behav Neurosci 2004; 4: 307-316.
46. Rapaport MH, Guylai L, Whybrow P. Immune parameters in rapid cycling bipolar patients before and after lithium treatment. J Psychiatr Res 1999; 33: 335-340.
47. Liu HC, Yang YY, Chou YM, Chen KP, Shen WW, Leu SJ. Immunologic variables in acute mania of bipolar disorder. J Neuroimmunol 2004; 150: 116-122.
48. Lanningham-Foster L, Green CL, Langkamp-Henken B, Davis BA, Nguyen KT, Bender BS et al. Overexpression of CRIP in transgenic mice alters cytokine patterns and the immune response. Am J Physiol Endocrinol Metab 2002; 282: E1197-E1203.
49. Beyer J, Kuchibhatla M, Gersing K, Krishnan KR. Medical comorbidity in a bipolar outpatient clinical population. Neuropsychopharmacology 2005; 30: 401-404.
50. Wilkins K. Bipolar I disorder, social support and work. Health Rep 2004; 15(Suppl): 21-30.
51. Goodwin RD, Jacobi F, Thefeld W. Mental disorders and asthma in the community. Arch Gen Psychiatry 2003; 60: 1125-1130.
52. Brown ES, Suppes T, Khan DA, Carmody III TJ. Mood changes during prednisone bursts in outpatients with asthma. J Clin Psychopharmacol 2002; 22: 55-61.
53. Knox AJ, Higgins BG, Hall IP, Tattersfield AE. Effect of oral lithiumon bronchial reactivity in asthma. Clin Sci (London) 1992; 82: 407-412.
54. Kato T, Kato N. Molecular genetics of bipolar disorder]. Tanpakushitsu Kakusan Koso 1999; 44: 1975-1981.
55. Escriba PV, Ozaita A, Garcia-Sevilla JA. Increased mRNA expression of alpha2A-adrenoceptors, serotonin receptors and mu-opioid receptors in the brains of suicide victims. Neuropsychopharmacology 2004; 29: 1512-1521.
56. Nyegaard M, Borglum AD, Bruun TG, Collier DA, Russ C, Mors O et al. Novel polymorphisms in the somatostatin receptor 5 (SSTR5) gene associated with bipolar affective disorder. Mol Psychiatry 2002; 7: 745-754.
57. Rubinow DR. Cerebrospinal fluid somatostatin and psychiatric illness. Biol Psychiatry 1986; 21: 341-365.
58. Sharma RP, Bissette G, Janicak PG, Davis JM, Nemeroff CB. Elevation of CSF somatostatin concentrations in mania. Am J Psychiatry 1995; 152: 1807-1809.
59. Pazzaglia PJ, George MS, Post RM, Rubinow DR, Davis CL. Nimodipine increases CSF somatostatin in affectively ill patients. Neuropsychopharmacology 1995; 13: 75-83.
60. Rocheville M, Lange DC, Kumar U, Patel SC, Patel RC, Patel YC. Receptors for dopamine and somatostatin: formation of heterooligomers with enhanced functional activity. Science 2000; 288: 154-157.
61. Kapczinski F, Frey BN, Zannatto V. Physiopathology of bipolar disorders: what have changed in the last 10 years? Rev Bras Psiquiatr 2004; 26(Suppl 3): 17-21.
62. Bezchlibnyk Y, Young LT. The neurobiology of bipolar disorder: focus on signal transduction pathways and the regulation of gene expression. Can J Psychiatry 2002; 47: 135-148.
63. Gould TD, Manji HK. Signaling networks in the pathophysiology and treatment of mood disorders. J Psychosom Res 2002; 53: 687-697.
64. Brunello N, Tascedda F. Cellular mechanisms and second messengers: relevance to the psychopharmacology of bipolar disorders. Int J Neuropsychopharmacol 2003; 6: 181-189.
65. Hanz S, Fainzilber M. Integration of retrograde axonal and nuclear transport mechanisms in neurons: implications for therapeutics. Neuroscientist 2004; 10: 404-408.
66. Ciechanover A. The ubiquitin proteolytic system and pathogenesis of human diseases: a novel platform for mechanism-based drug targeting. Biochem Soc Trans 2003; 31: 474-481.
67. DiAntonio A, Hicke L. Ubiquitin-dependent regulation of the synapse. Annu Rev Neurosci 2004; 27: 223-246.
68. Ciechanover A, Schwartz AL. The ubiquitin system: pathogenesis of human diseases and drug targeting. Biochim Biophys Acta 2004; 1695: 3-17.
69. Wilson SM, Bhattacharyya B, Rachel RA, Coppola V, Tessarollo L, Householder DB et al. Synaptic defects in ataxia mice result from a mutation in Usp14, encoding a ubiquitin-specific protease. Nat Genet 2002; 32: 420-425.
70. Holler D, Dikic I. Receptor endocytosis via ubiquitin-dependent and -independent pathways. Biochem Pharmacol 2004; 67: 1013-1017.
71. Johnston JA, Madura K. Rings, chains and ladders: ubiquitin goes to work in the neuron. Prog Neurobiol 2004; 73: 227-257.
72. Hegde AN. Ubiquitin-proteasome-mediated local protein degradation and synaptic plasticity. Prog Neurobiol 2004; 73: 311-357.
73. Nakayama M, Miyake T, Gahara Y, Ohara O, Kitamura T. A novel RING-H2 motif protein downregulated by axotomy: its characteristic localization at the postsynaptic density of axosomatic synapse. J Neurosci 1995; 15(7 Part 2): 5238-5248.
74. Fernandez-Chacon R, Konigstorfer A, Gerber SH, Garcia J, Matos MF, Stevens CF et al. Synaptotagmin I functions as a calcium regulator of release probability. Nature 2001; 410: 41-49.
75. Walton MR, Dragunow I. Is CREB a key to neuronal survival? Trends Neurosci 2000; 23: 48-53.
76. Irazusta J, Larrinaga G, Gonzalez-Maeso J, Gil J, Meana JJ, Casis L. Distribution of prolyl endopeptidase activities in rat and human brain. Neurochem Int 2002; 40: 337-345.
77. Cunningham DF, O'Connor B. Proline specific peptidases. Biochim Biophys Acta 1997; 1343: 160-186.
78. Maes M, Goossens F, Scharpe S, Calabrese J, Desnyder R, Meltzer HY. Alterations in plasma prolyl endopeptidase activity in depression, mania, and schizophrenia: effects of antidepressants, mood stabilizers, and antipsychotic drugs. Psychiatry Res 1995; 58: 217-225.
79. Holsboer F. The role of peptides in treatment of psychiatric disorders. J Neural Transm Suppl 2003; 64: 17-34.
80. Williams RS, Cheng L, Mudge AW, Harwood AJ. A common mechanism of action for three mood-stabilizing drugs. Nature 2002; 417: 292-295.
81. Coyle JT, Duman RS. Finding the intracellular signaling pathways affected by mood disorder treatments. Neuron 2003; 38: 157-160.
82. Ogden CA, Rich ME, Schork NJ, Paulus MP, Geyer MA, Lohr JB et al. Candidate genes, pathways and mechanisms for bipolar (manic-depressive) and related disorders: an expanded convergent functional genomics approach. Mol Psychiatry 2004; 9: 1007-1029.
83. Kato T, Kato N. Mitochondrial dysfunction in bipolar disorder. Bipolar Disord 2000; 2(3 Part 1): 180-190.
84. Vawter MP, Barrett T, Cheadle C, Sokolov BP, Wood III WH, Donovan DM et al. Application of cDNA microarrays to examine gene expression differences in schizophrenia. Brain Res Bull 2001; 55: 641-650.
85. Altar CA, Jurata LW, Charles V, Lemire A, Liu P, Bukhman Y et al. Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts. Biol Psychiatry 2005; 58: 85-96.
86. Sokolov BP, Jiang L, Trivedi NS, Aston C. Transcription profiling reveals mitochondrial, ubiquitin and signaling systems abnormalities in postmortem brains from subjects with a history of alcohol abuse or dependence. J Neurosci Res 2003; 72: 756-767.