Intracellular compartment-specific proteasome dysfunction in postmortem cortex in schizophrenia subjects.
Aged
Autopsy
Brain
/ metabolism
Cerebral Cortex
/ metabolism
Chymotrypsin
/ analysis
Female
Humans
Male
Middle Aged
Proteasome Endopeptidase Complex
/ metabolism
Proteins
/ metabolism
Proteolysis
Proteomics
Schizophrenia
/ metabolism
Temporal Lobe
/ metabolism
Trypsin
/ analysis
Ubiquitin
/ metabolism
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
02
11
2018
accepted:
11
01
2019
revised:
19
12
2018
pubmed:
27
1
2019
medline:
18
2
2021
entrez:
27
1
2019
Statut:
ppublish
Résumé
Protein homeostasis is an emerging component of schizophrenia (SZ) pathophysiology. Proteomic alterations in SZ are well-documented and changes in transcript expression are frequently not associated with changes in protein expression in SZ brain. The underlying mechanism driving these changes remains unknown, though altered expression of ubiquitin proteasome system (UPS) components have implicated protein degradation. Previous studies have been limited to protein and transcript expression, however, and do not directly test the function of the proteasome. To address this gap in knowledge, we measured enzymatic activity associated with the proteasome (chymotrypsin-, trypsin-, and caspase-like) in the superior temporal gyrus (STG) of 25 SZ and 25 comparison subjects using flourogenic substrates. As localization regulates which cellular processes the proteasome contributes to, we measured proteasome activity and subunit expression in fractions enriched for nucleus, cytosolic, and membrane compartments. SZ subjects had decreased trypsin-like activity in total homogenate. This finding was specific to the nucleus-enriched fraction and was not associated with changes in proteasome subunit expression. Interestingly, both chymotrypsin-like activity and protein expression of 19S RP subunits, which facilitate ubiquitin-dependent degradation, were decreased in the cytosol-enriched fraction of SZ subjects. Intracellular compartment-specific proteasome dysfunction implicates dysregulation of protein expression both through altered ubiquitin-dependent degradation of cytosolic proteins and regulation of protein synthesis due to degradation of transcription factors and transcription machinery in the nucleus. Together, these findings implicate proteasome dysfunction in SZ, which likely has a broad impact on the proteomic landscape and cellular function in the pathophysiology of this illness.
Identifiants
pubmed: 30683941
doi: 10.1038/s41380-019-0359-7
pii: 10.1038/s41380-019-0359-7
pmc: PMC6658356
mid: NIHMS1518568
doi:
Substances chimiques
Proteins
0
Ubiquitin
0
Chymotrypsin
EC 3.4.21.1
Trypsin
EC 3.4.21.4
Proteasome Endopeptidase Complex
EC 3.4.25.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
776-790Subventions
Organisme : NIMH NIH HHS
ID : R01 MH053327
Pays : United States
Références
Davalieva K, Maleva Kostovska I, Dwork AJ. Proteomics research in schizophrenia. Front Cell Neurosci. 2016;10:18.
pubmed: 26909022
pmcid: 4754401
Karson CN, Mrak RE, Schluterman KO, Sturner WQ, Sheng JG, Griffin WS. Alterations in synaptic proteins and their encoding mRNAs in prefrontal cortex in schizophrenia: a possible neurochemical basis for ‘hypofrontality’. Mol Psychiatry. 1999;4:39–45.
pubmed: 10089007
Eastwood SL, Burnet PW, Gittins R, Baker K, Harrison PJ. Expression of serotonin 5-HT(2A) receptors in the human cerebellum and alterations in schizophrenia. Synapse. 2001;42:104–14.
pubmed: 11574947
Eastwood SL, Cotter D, Harrison PJ. Cerebellar synaptic protein expression in schizophrenia. Neuroscience. 2001;105:219–29.
pubmed: 11483314
Dracheva S, Elhakem SL, McGurk SR, Davis KL, Haroutunian V. GAD67 and GAD65 mRNA and protein expression in cerebrocortical regions of elderly patients with schizophrenia. J Neurosci Res. 2004;76:581–92.
pubmed: 15114630
Erdely HA, Tamminga CA, Roberts RC, Vogel MW. Regional alterations in RGS4 protein in schizophrenia. Synapse. 2006;59:472–9.
pubmed: 16565965
Verrall L, Walker M, Rawlings N, Benzel I, Kew JN, Harrison PJ, et al. d-Amino acid oxidase and serine racemase in human brain: normal distribution and altered expression in schizophrenia. Eur J Neurosci. 2007;26:1657–69.
pubmed: 17880399
pmcid: 2121142
Bauer D, Gupta D, Harotunian V, Meador-Woodruff JH, McCullumsmith RE. Abnormal expression of glutamate transporter and transporter interacting molecules in prefrontal cortex in elderly patients with schizophrenia. Schizophr Res. 2008;104:108–20.
pubmed: 18678470
pmcid: 2656372
Ben-Shachar D, Karry R. Neuroanatomical pattern of mitochondrial complex I pathology varies between schizophrenia, bipolar disorder and major depression. PLoS ONE. 2008;3:e3676.
pubmed: 18989376
pmcid: 2579333
Burnet PW, Hutchinson L, von Hesling M, Gilbert EJ, Brandon NJ, Rutter AR, et al. Expression of D-serine and glycine transporters in the prefrontal cortex and cerebellum in schizophrenia. Schizophr Res. 2008;102:283–94.
pubmed: 18400471
Oni-Orisan A, Kristiansen LV, Haroutunian V, Meador-Woodruff JH, McCullumsmith RE. Altered vesicular glutamate transporter expression in the anterior cingulate cortex in schizophrenia. Biol Psychiatry. 2008;63:766–75.
pubmed: 18155679
Tang J, LeGros RP, Louneva N, Yeh L, Cohen JW, Hahn CG, et al. Dysbindin-1 in dorsolateral prefrontal cortex of schizophrenia cases is reduced in an isoform-specific manner unrelated to dysbindin-1 mRNA expression. Hum Mol Genet. 2009;18:3851–63.
pubmed: 19617633
pmcid: 2748893
Uriguen L, Garcia-Fuster MJ, Callado LF, Morentin B, La Harpe R, Casado V, et al. Immunodensity and mRNA expression of A2A adenosine, D2 dopamine, and CB1 cannabinoid receptors in postmortem frontal cortex of subjects with schizophrenia: effect of antipsychotic treatment. Psychopharmacology. 2009;206:313–24.
pubmed: 19652957
Fatemi SH, Folsom TD, Reutiman TJ, Vazquez G. Phosphodiesterase signaling system is disrupted in the cerebella of subjects with schizophrenia, bipolar disorder, and major depression. Schizophr Res. 2010;119:266–7.
pubmed: 20299190
Fung SJ, Webster MJ, Sivagnanasundaram S, Duncan C, Elashoff M, Weickert CS. Expression of interneuron markers in the dorsolateral prefrontal cortex of the developing human and in schizophrenia. Am J Psychiatry. 2010;167:1479–88.
pubmed: 21041246
Kristiansen LV, Bakir B, Haroutunian V, Meador-Woodruff JH. Expression of the NR2B-NMDA receptor trafficking complex in prefrontal cortex from a group of elderly patients with schizophrenia. Schizophr Res. 2010;119:198–209.
pubmed: 20347576
pmcid: 2868940
Gigante AD, Andreazza AC, Lafer B, Yatham LN, Beasley CL, Young LT. Decreased mRNA expression of uncoupling protein 2, a mitochondrial proton transporter, in post-mortem prefrontal cortex from patients with bipolar disorder and schizophrenia. Neurosci Lett. 2011;505:47–51.
pubmed: 22001364
Sinclair D, Tsai SY, Woon HG, Weickert CS. Abnormal glucocorticoid receptor mRNA and protein isoform expression in the prefrontal cortex in psychiatric illness. Neuropsychopharmacology. 2011;36:2698–709.
pubmed: 21881570
pmcid: 3230493
Udawela M, Scarr E, Hannan AJ, Thomas EA, Dean B. Phospholipase C beta 1 expression in the dorsolateral prefrontal cortex from patients with schizophrenia at different stages of illness. Aust N Z J Psychiatry. 2011;45:140–7.
pubmed: 21091263
Joshi D, Fung SJ, Rothwell A, Weickert CS. Higher gamma-aminobutyric acid neuron density in the white matter of orbital frontal cortex in schizophrenia. Biol Psychiatry. 2012;72:725–33.
pubmed: 22841514
Perez-Costas E, Melendez-Ferro M, Rice MW, Conley RR, Roberts RC. Dopamine pathology in schizophrenia: analysis of total and phosphorylated tyrosine hydroxylase in the substantia nigra. Front Psychiatry. 2012;3:31.
pubmed: 22509170
pmcid: 3321522
Sinclair D, Webster MJ, Fullerton JM, Weickert CS. Glucocorticoid receptor mRNA and protein isoform alterations in the orbitofrontal cortex in schizophrenia and bipolar disorder. BMC Psychiatry. 2012;12:84.
pubmed: 22812453
pmcid: 3496870
Dean B, Gibbons AS, Tawadros N, Brooks L, Everall IP, Scarr E. Different changes in cortical tumor necrosis factor-alpha-related pathways in schizophrenia and mood disorders. Mol Psychiatry. 2013;18:767–73.
pubmed: 22801413
Drummond JB, Tucholski J, Haroutunian V, Meador-Woodruff JH. Transmembrane AMPA receptor regulatory protein (TARP) dysregulation in anterior cingulate cortex in schizophrenia. Schizophr Res. 2013;147:32–38.
pubmed: 23566497
pmcid: 3650109
Fatemi SH, Folsom TD, Rooney RJ, Thuras PD. Expression of GABAA alpha2-, beta1- and epsilon-receptors are altered significantly in the lateral cerebellum of subjects with schizophrenia, major depression and bipolar disorder. Transl Psychiatry. 2013;3:e303.
pubmed: 24022508
pmcid: 3784760
Fatemi SH, Folsom TD, Rooney RJ, Thuras PD. mRNA and protein expression for novel GABAA receptors theta and rho2 are altered in schizophrenia and mood disorders; relevance to FMRP-mGluR5 signaling pathway. Transl Psychiatry. 2013;3:e271.
pubmed: 23778581
pmcid: 3693405
Tao R, Cousijn H, Jaffe AE, Burnet PW, Edwards F, Eastwood SL, et al. Expression of ZNF804A in human brain and alterations in schizophrenia, bipolar disorder, and major depressive disorder: a novel transcript fetally regulated by the psychosis risk variant rs1344706. JAMA Psychiatry. 2014;71:1112–20.
pubmed: 25162540
pmcid: 5894803
Matosin N, Fernandez-Enright F, Fung SJ, Lum JS, Engel M, Andrews JL, et al. Alterations of mGluR5 and its endogenous regulators Norbin, Tamalin and Preso1 in schizophrenia: towards a model of mGluR5 dysregulation. Acta Neuropathol. 2015;130:119–29.
pubmed: 25778620
Udawela M, Money TT, Neo J, Seo MS, Scarr E, Dean B, et al. SELENBP1 expression in the prefrontal cortex of subjects with schizophrenia. Transl Psychiatry. 2015;5:e615.
pubmed: 26241353
pmcid: 4564563
Garcia-Bueno B, Gasso P, MacDowell KS, Callado LF, Mas S, Bernardo M, et al. Evidence of activation of the Toll-like receptor-4 proinflammatory pathway in patients with schizophrenia. J Psychiatry Neurosci. 2016;41:E46–55.
pubmed: 27070349
pmcid: 4853215
Nishiura K, Ichikawa-Tomikawa N, Sugimoto K, Kunii Y, Kashiwagi K, Tanaka M, et al. PKA activation and endothelial claudin-5 breakdown in the schizophrenic prefrontal cortex. Oncotarget. 2017;8:93382–91.
pubmed: 29212157
pmcid: 5706803
Purves-Tyson TD, Owens SJ, Rothmond DA, Halliday GM, Double KL, Stevens J, et al. Putative presynaptic dopamine dysregulation in schizophrenia is supported by molecular evidence from post-mortem human midbrain. Transl Psychiatry. 2017;7:e1003.
pubmed: 28094812
pmcid: 5545725
Udawela M, Scarr E, Boer S, Um JY, Hannan AJ, McOmish C, et al. Isoform specific differences in phospholipase C beta 1 expression in the prefrontal cortex in schizophrenia and suicide. NPJ Schizophr. 2017;3:19.
pubmed: 28560265
pmcid: 5441535
Pandey GN, Rizavi HS, Zhang H, Ren X. Abnormal gene and protein expression of inflammatory cytokines in the postmortem brain of schizophrenia patients. Schizophr Res. 2018;192:247–54.
pubmed: 28476335
Tremolizzo L, Carboni G, Ruzicka WB, Mitchell CP, Sugaya I, Tueting P, et al. An epigenetic mouse model for molecular and behavioral neuropathologies related to schizophrenia vulnerability. Proc Natl Acad Sci USA. 2002;99:17095–17100.
pubmed: 12481028
Hansen T, Olsen L, Lindow M, Jakobsen KD, Ullum H, Jonsson E, et al. Brain expressed microRNAs implicated in schizophrenia etiology. PLoS ONE. 2007;2:e873.
pubmed: 17849003
pmcid: 1964806
English JA, Fan Y, Focking M, Lopez LM, Hryniewiecka M, Wynne K, et al. Reduced protein synthesis in schizophrenia patient-derived olfactory cells. Transl Psychiatry. 2015;5:e663.
pubmed: 26485547
pmcid: 4930119
Voges D, Zwickl P, Baumeister W. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem. 1999;68:1015–68.
pubmed: 10872471
von Mikecz A. The nuclear ubiquitin-proteasome system. J Cell Sci. 2006;119(Pt 10):1977–84.
Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, et al. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell. 1994;78:761–71.
pubmed: 8087844
Ramachandran KV, Margolis SS. A mammalian nervous-system-specific plasma membrane proteasome complex that modulates neuronal function. Nat Struct Mol Biol. 2017;24:419–30.
pubmed: 28287632
pmcid: 5383508
Santos AR, Mele M, Vaz SH, Kellermayer B, Grimaldi M, Colino-Oliveira M, et al. Differential role of the proteasome in the early and late phases of BDNF-induced facilitation of LTP. J Neurosci. 2015;35:3319–29.
pubmed: 25716833
pmcid: 6605551
Djakovic SN, Marquez-Lona EM, Jakawich SK, Wright R, Chu C, Sutton MA, et al. Phosphorylation of Rpt6 regulates synaptic strength in hippocampal neurons. J Neurosci. 2012;32:5126–31.
pubmed: 22496558
pmcid: 3348785
Erturk A, Wang Y, Sheng M. Local pruning of dendrites and spines by caspase-3-dependent and proteasome-limited mechanisms. J Neurosci. 2014;34:1672–88.
pubmed: 24478350
pmcid: 6827581
Hamilton AM, Oh WC, Vega-Ramirez H, Stein IS, Hell JW, Patrick GN, et al. Activity-dependent growth of new dendritic spines is regulated by the proteasome. Neuron. 2012;74:1023–30.
pubmed: 22726833
pmcid: 3500563
Green MJ, Matheson SL, Shepherd A, Weickert CS, Carr VJ. Brain-derived neurotrophic factor levels in schizophrenia: a systematic review with meta-analysis. Mol Psychiatry. 2011;16:960–72.
pubmed: 20733577
Rajasekaran A, Venkatasubramanian G, Berk M, Debnath M. Mitochondrial dysfunction in schizophrenia: pathways, mechanisms and implications. Neurosci Biobehav Rev. 2015;48:10–21.
pubmed: 25446950
Moyer CE, Shelton MA, Sweet RA. Dendritic spine alterations in schizophrenia. Neurosci Lett. 2015;601:46–53.
pubmed: 25478958
Barroso-Chinea P, Thiolat ML, Bido S, Martinez A, Doudnikoff E, Baufreton J, et al. D1 dopamine receptor stimulation impairs striatal proteasome activity in Parkinsonism through 26S proteasome disassembly. Neurobiol Dis. 2015;78:77–87.
pubmed: 25766677
Caldeira MV, Curcio M, Leal G, Salazar IL, Mele M, Santos AR, et al. Excitotoxic stimulation downregulates the ubiquitin-proteasome system through activation of NMDA receptors in cultured hippocampal neurons. Biochim Biophys Acta. 2013;1832:263–74.
pubmed: 23069389
Ferreira JS, Schmidt J, Rio P, Aguas R, Rooyakkers A, Li KW, et al. GluN2B-containing NMDA receptors regulate AMPA receptor traffic through anchoring of the synaptic proteasome. J Neurosci. 2015;35:8462–79.
pubmed: 26041915
pmcid: 6605323
Liu C, Bousman CA, Pantelis C, Skafidas E, Zhang D, Yue W, et al. Pathway-wide association study identifies five shared pathways associated with schizophrenia in three ancestral distinct populations. Transl Psychiatry. 2017;7:e1037.
pubmed: 28221366
pmcid: 5438037
Vawter MP, Barrett T, Cheadle C, Sokolov BP, Wood WH 3rd, Donovan DM, et al. Application of cDNA microarrays to examine gene expression differences in schizophrenia. Brain Res Bull. 2001;55:641–50.
pubmed: 11576761
Middleton FA, Mirnics K, Pierri JN, Lewis DA, Levitt P. Gene expression profiling reveals alterations of specific metabolic pathways in schizophrenia. J Neurosci. 2002;22:2718–29.
pubmed: 11923437
pmcid: 6758309
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.
pubmed: 16038679
Chu TT, Liu Y, Kemether E. Thalamic transcriptome screening in three psychiatric states. J Hum Genet. 2009;54:665–75.
pubmed: 19834500
Arion D, Corradi JP, Tang S, Datta D, Boothe F, He A, et al. Distinctive transcriptome alterations of prefrontal pyramidal neurons in schizophrenia and schizoaffective disorder. Mol Psychiatry. 2015;20:1397–405.
pubmed: 25560755
pmcid: 4492919
Bousman CA, Chana G, Glatt SJ, Chandler SD, May T, Lohr J, et al. Positive symptoms of psychosis correlate with expression of ubiquitin proteasome genes in peripheral blood. Am J Med Genet Part B Neuropsychiatr Genet. 2010;153B:1336–41.
Bousman CA, Chana G, Glatt SJ, Chandler SD, Lucero GR, Tatro E, et al. Preliminary evidence of ubiquitin proteasome system dysregulation in schizophrenia and bipolar disorder: convergent pathway analysis findings from two independent samples. Am J Med Genet Part B Neuropsychiatr Genet. 2010;153B:494–502.
Rubio MD, Wood K, Haroutunian V, Meador-Woodruff JH. Dysfunction of the ubiquitin proteasome and ubiquitin-like systems in schizophrenia. Neuropsychopharmacology. 2013;38:1910–20.
pubmed: 23571678
pmcid: 3746696
Andrews JL, Goodfellow FJ, Matosin N, Snelling MK, Newell KA, Huang XF, et al. Alterations of ubiquitin related proteins in the pathology and development of schizophrenia: Evidence from human and animal studies. J Psychiatr Res. 2017;90:31–39.
pubmed: 28226265
Scott MR, Rubio MD, Haroutunian V, Meador-Woodruff JH. Protein expression of proteasome subunits in elderly patients with schizophrenia. Neuropsychopharmacology. 2016;41:896–905.
pubmed: 26202105
Curcic-Blake B, Ford JM, Hubl D, Orlov ND, Sommer IE, Waters F, et al. Interaction of language, auditory and memory brain networks in auditory verbal hallucinations. Prog Neurobiol. 2017;148:1–20.
pubmed: 27890810
pmcid: 5240789
Karagulla S, Robertson EE. Phychical phenomena in temporal lobe epilepsy and the psychoses. BMJ. 1955;1:748–52.
pubmed: 14351770
Slater E, Beard AW, Glithero E. Schizophrenia-like psychoses of epilepsy. Int J Psychiatry. 1965;1:6–30.
pubmed: 14252256
Korzeniowski L. [Diagnostic problems regarding delusion psychoses in the course of epilepsy]. Neurol Neurochir Psychiatr Pol. 1965;15:823–8.
pubmed: 5864776
Korzeniowski L. [Diagnostic problems concerning paranoic schizophreniform psychoses in epilepsy]. Ann Med Psychol. 1965;123:35–42.
Alsen V. [Epilepsy and psychosis]. Nervenarzt. 1965;36:490–3.
pubmed: 5887799
Hori H. [Hallucinations by the electrical stimulation of temporal lobe]. Psychiatria Neurol Jpn. 1962;64:1010–6.
Ishibashi T, Hori H, Endo K, Sato T. Hallucinations produced by electrical stimulation of the temporal lobes in schizophrenic patients. Tohoku J Exp Med. 1964;82:124–39.
pubmed: 14154974
Honea R, Crow TJ, Passingham D, Mackay CE. Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am J Psychiatry. 2005;162:2233–45.
pubmed: 16330585
Forsyth JK, Lewis DA. Mapping the consequences of impaired synaptic plasticity in schizophrenia through development: an integrative model for diverse clinical features. Trends Cogn Sci. 2017;21:760–78.
pubmed: 28754595
pmcid: 5610626
Powchik P, Davidson M, Haroutunian V, Gabriel SM, Purohit DP, Perl DP, et al. Postmortem studies in schizophrenia. Schizophr Bull. 1998;24:325–41.
pubmed: 9718627
Purohit DP, Perl DP, Haroutunian V, Powchik P, Davidson M, Davis KL. Alzheimer disease and related neurodegenerative diseases in elderly patients with schizophrenia: a postmortem neuropathologic study of 100 cases. Arch Gen Psychiatry. 1998;55:205–11.
pubmed: 9510214
Barksdale KA, Perez-Costas E, Gandy JC, Melendez-Ferro M, Roberts RC, Bijur GN. Mitochondrial viability in mouse and human postmortem brain. FASEB J. 2010;24:3590–9.
pubmed: 20466876
pmcid: 2923351
Kashihara K, Sato M, Fujiwara Y, Ogawa T, Fukuda K, Otsuki S. Effects of intermittent and continuous haloperidol administration on the dopaminergic system in the rat brain. Japanese J Psychopharmacol. 1986;6:275–80.
Harte MK, Bachus SB, Reynolds GP. Increased N-acetylaspartate in rat striatum following long-term administration of haloperidol. Schizophr Res. 2005;75:303–8.
pubmed: 15885521
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57:289–300.
Fountoulakis M, Hardmeier R, Hoger H, Lubec G. Postmortem changes in the level of brain proteins. Exp Neurol. 2001;167:86–94.
pubmed: 11161596
Beckstrom H, Julsrud L, Haugeto O, Dewar D, Graham DI, Lehre KP, et al. Interindividual differences in the levels of the glutamate transporters GLAST and GLT, but no clear correlation with Alzheimer’s disease. J Neurosci Res. 1999;55:218–29.
pubmed: 9972824
McKinnon C, Tabrizi SJ. The ubiquitin-proteasome system in neurodegeneration. Antioxid Redox Signal. 2014;21:2302–21.
pubmed: 24437518
Rund BR. The research evidence for schizophrenia as a neurodevelopmental disorder. Scand J Psychol. 2018;59:49–58.
pubmed: 29356007
Bradshaw NJ, Korth C. Protein misassembly and aggregation as potential convergence points for non-genetic causes of chronic mental illness. Molecular Psychiatry 2018. August 8, 2018. https://doi.org/10.1038/s41380-018-0133-2 .
Kisselev AF, Callard A, Goldberg AL. Importance of the different proteolytic sites of the proteasome and the efficacy of inhibitors varies with the protein substrate. J Biol Chem. 2006;281:8582–90.
pubmed: 16455650
Vigneron N, Van den Eynde BJ. Proteasome subtypes and regulators in the processing of antigenic peptides presented by class I molecules of the major histocompatibility complex. Biomolecules. 2014;4:994–1025.
pubmed: 25412285
pmcid: 4279167
Pickering AM, Koop AL, Teoh CY, Ermak G, Grune T, Davies KJ. The immunoproteasome, the 20S proteasome and the PA28alphabeta proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem J. 2010;432:585–94.
pubmed: 20919990
pmcid: 3133595
Boskovic M, Vovk T, Kores Plesnicar B, Grabnar I. Oxidative stress in schizophrenia. Curr Neuropharmacol. 2011;9:301–12.
pubmed: 22131939
pmcid: 3131721
Reyazuddin M, Azmi SA, Islam N, Rizvi A. Oxidative stress and level of antioxidant enzymes in drug-naive schizophrenics. Indian J Psychiatry. 2014;56:344–9.
pubmed: 25568474
pmcid: 4279291
Bingol B, Schuman EM. Synaptic protein degradation by the ubiquitin proteasome system. Curr Opin Neurobiol. 2005;15:536–41.
pubmed: 16150592
Hamilton AM, Zito K. Breaking it down: the ubiquitin proteasome system in neuronal morphogenesis. Neural Plast. 2013;2013:196848.
pubmed: 23476809
pmcid: 3586504
Javitt DC, Sweet RA. Auditory dysfunction in schizophrenia: integrating clinical and basic features. Nat Rev Neurosci. 2015;16:535–50.
pubmed: 26289573
pmcid: 4692466
Vaillant G. Schizophrenia in a woman with temporal lobe arterio-venous malformations: an unusual case report. Br J Psychiatry. 1965;111:307–8.
pubmed: 14286961
Hollender MH, Hirsch SJ, Goodwin FK, Kaplan EA, Rubert SL, Watkins ES, et al. Schizophrenia or temporal lobe disorder? Int Psychiatry Clin. 1965;2:667–89.
pubmed: 5852353
Debanth M, Berk M, Leboyer M, Tamouza R. The MHC/HLA gene complex in major psychiatric disorders: emerging roles and implications. Curr Behav Neurosci Rep. 2018;5:179–88.
Saez I, Vilchez D. The mechanistic links between proteasome activity, aging and age-related diseases. Curr Genom. 2014;15:38–51.
Tomaru U, Takahashi S, Ishizu A, Miyatake Y, Gohda A, Suzuki S, et al. Decreased proteasomal activity causes age-related phenotypes and promotes the development of metabolic abnormalities. Am J Pathol. 2012;180:963–72.
Torres C, Lewis L, Cristofalo VJ. Proteasome inhibitors shorten replicative life span and induce a senescent-like phenotype of human fibroblasts. J Cell Physiol. 2006;207:845–53.
pubmed: 16523493
Chondrogianni N, Petropoulos I, Franceschi C, Friguet B, Gonos ES. Fibroblast cultures from healthy centenarians have an active proteasome. Exp Gerontol. 2000;35:721–8.
pubmed: 11053662
Hsu CY, Qiu JT, Chan YP. Cellular degradation activity is maintained during aging in long-living queen bees. Biogerontology. 2016;17:829–40.
pubmed: 27230748