N-glycosylation of GABAA receptor subunits is altered in schizophrenia

Neuropsychopharmacology

Volumn 39, Issue 3, 2014, Pages 528-537

  Mueller, Toni Marie ^a   Haroutunian, Vahram ^b   Meador Woodruff, James H ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

GABRA1; GABRB1; GABRB2; post translational modification; postmortem brain; superior temporal gyrus

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA4; 4 AMINOBUTYRIC ACID A RECEPTOR BETA1; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; GLUTAMIC ACID; GLYCAN; LECTIN; 4 AMINOBUTYRIC ACID A RECEPTOR;

ADULT; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DEGLYCOSYLATION; FEMALE; GLUTAMATERGIC NEUROTRANSMISSION; HUMAN; HUMAN TISSUE; MALE; MIDDLE AGED; MOLECULAR WEIGHT; NEUROTRANSMISSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; SUPERIOR TEMPORAL GYRUS; WESTERN BLOTTING; AGED; ANALYSIS OF VARIANCE; DRUG EFFECT; GENETICS; GLYCOSYLATION; METABOLISM; PATHOLOGY; PHOSPHORYLATION; POSTMORTEM CHANGE; PROTEIN SUBUNIT; TEMPORAL LOBE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANALYSIS OF VARIANCE; FEMALE; GLYCOSYLATION; HUMANS; MALE; PHOSPHORYLATION; POSTMORTEM CHANGES; PROTEIN SUBUNITS; RECEPTORS, GABA-A; SCHIZOPHRENIA; TEMPORAL LOBE;

EID: 84892672874     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.190     Document Type: Article

References (43)

1. Barta PE, Pearlson GD, Powers RE, Richards SS, Tune LE (1990). Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry 147: 1457-1462.
2. Bauer D, Haroutunian V, Meador-Woodruff JH, McCullumsmith RE (2010). Abnormal glycosylation of EAAT1 and EAAT2 in prefrontal cortex of elderly patients with schizophrenia. Schizophr Res 117: 92-98.
3. Bauer DE, Haroutunian V, McCullumsmith RE, Meador-Woodruff JH (2009). Expression of four housekeeping proteins in elderly patients with schizophrenia. J Neural Transm 116: 487-491.
4. Benjamini Y, Hochberg Y (1995). Controlling the false discovery rate-a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57: 289-300.
5. Buchstaller A, Adamiker D, Fuchs K, Sieghart W (1991a). N-deglycosylation and immunological identification indicates the existence of beta-subunit isoforms of the rat GABAA receptor. FEBS Lett 287: 27-30.
6. Buchstaller A, Fuchs K, SieghartW(1991b). Identification of alpha 1-, alpha 2-and alpha 3-subunit isoforms of the GABAA-benzodiazepine receptor in the rat brain. Neurosci Lett 129: 237-241.
7. Buller AL, Hastings GA, Kirkness EF, Fraser CM (1994). Sitedirected mutagenesis of N-linked glycosylation sites on the gamma-aminobutyric acid type A receptor alpha 1 subunit. Mol Pharmacol 46: 858-865.
8. Chen ZW, Fuchs K, Sieghart W, Townsend RR, Evers AS (2012). Deep amino acid sequencing of native brain GABAA receptors using high-resolution mass spectrometry. MCP 11: M111 011445.
9. Connolly CN, Krishek BJ, McDonald BJ, Smart TG, Moss SJ (1996). Assembly and cell surface expression of heteromeric and homomeric gamma-aminobutyric acid type A receptors. J Biol Chem 271: 89-96.
10. Deng C, Huang XF (2006). Increased density of GABAA receptors in the superior temporal gyrus in schizophrenia. Exp Brain Res 168: 587-590.
11. Dennis JW, Lau KS, Demetriou M, Nabi IR (2009). Adaptive regulation at the cell surface by N-glycosylation. Traffic 10: 1569-1578.
12. Farriol-Mathis N, Garavelli JS, Boeckmann B, Duvaud S, Gasteiger E, Gateau A et al (2004). Annotation of post-translational modifications in the Swiss-Prot knowledge base. Proteomics 4: 1537-1550.
13. Gonzalez-Burgos G, Hashimoto T, Lewis DA (2010). Alterations of cortical GABA neurons and network oscillations in schizophrenia. Curr Psychiatry Rep 12: 335-344.
14. Gurba KN, Hernandez CC, Hu N, Macdonald RL (2012). GABRB3 mutation, G32R, associated with childhood absence epilepsy alters alpha1beta3gamma2L gamma-aminobutyric acid type A (GABAA) receptor expression and channel gating. J Biol Chem 287: 12083-12097.
15. Helenius A, Aebi M (2004). Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73: 1019-1049.
16. Katsel P, Davis KL, Gorman JM, Haroutunian V (2005). Variations in differential gene expression patterns across multiple brain regions in schizophrenia. Schizophrenia research 77: 241-252.
17. Khoury GA, Baliban RC, Floudas CA (2011). Proteome-wide posttranslational modification statistics: frequency analysis and curation of the swiss-prot database. Sci Rep 1: pii: srep00090.
18. Lewis DA, Hashimoto T, Volk DW (2005). Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6: 312-324.
19. Lewis DA, Moghaddam B (2006). Cognitive dysfunction in schizophrenia: convergence of gamma-aminobutyric acid and glutamate alterations. Arch Neurol 63: 1372-1376.
20. Lo WY, Lagrange AH, Hernandez CC, Harrison R, Dell A, Haslam SM et al (2010). Glycosylation of {beta}2 subunits regulates GABAA receptor biogenesis and channel gating. J Biol Chem 285: 31348-31361.
21. Nakazawa K, Zsiros V, Jiang Z, Nakao K, Kolata S, Zhang S et al (2012). GABAergic interneuron origin of schizophrenia pathophysiology. Neuropharmacology 62: 1574-1583.
22. Nenadic I, Smesny S, Schlosser RG, Sauer H, Gaser C (2010). Auditory hallucinations and brain structure in schizophrenia: voxel-based morphometric study. Br J Psychiatry 196: 412-413.
23. Ohtsubo K, Marth JD (2006). Glycosylation in cellular mechanisms of health and disease. Cell 126: 855-867.
24. Parodi AJ (2000). Role of N-oligosaccharide endoplasmic reticulum processing reactions in glycoprotein folding and degradation. Biochem J 348(Pt 1): 1-13.
25. Powchik P, Davidson M, Haroutunian V, Gabriel SM, Purohit DP, Perl DP et al (1998). Postmortem studies in schizophrenia. Schizophrenia Bull 24: 325-341.
26. Purohit DP, Davidson M, Perl DP, Powchik P, Haroutunian VH, Bierer LM et al (1993). Severe cognitive impairment in elderly schizophrenic patients: a clinicopathological study. Biol Psychiatry 33: 255-260.
27. Purohit DP, Perl DP, Haroutunian V, Powchik P, Davidson M, Davis KL (1998). Alzheimer disease and related neurodegenerative diseases in elderly patients with schizophrenia: a postmortem neuropathologic study of 100 cases. Arch Gen Psychiatry 55: 205-211.
28. Rajarethinam RP, DeQuardo JR, Nalepa R, Tandon R (2000). Superior temporal gyrus in schizophrenia: a volumetric magnetic resonance imaging study. Schizophr Res 41: 303-312.
29. Rubio MD, Wood K, Haroutunian V, Meador-Woodruff JH (2013). Dysfunction of the ubiquitin proteasome and ubiquitin-like systems in schizophrenia. Neuropsychopharmacology 38: 1910-1920.
30. Sieghart W, Fuchs K, Tretter V, Ebert V, Jechlinger M, Hoger H et al (1999). Structure and subunit composition of GABA(A) receptors. Neurochemistry international 34: 379-385.
31. Sieghart W, Sperk G (2002). Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr Top Med Chem 2: 795-816.
32. Silbersweig DA, Stern E, Frith C, Cahill C, Holmes A, Grootoonk S et al (1995). A functional neuroanatomy of hallucinations in schizophrenia. Nature 378: 176-179.
33. Stan AD, Ghose S, Gao XM, Roberts RC, Lewis-Amezcua K, Hatanpaa KJ et al (2006). Human postmortem tissue: what quality markers matter? Brain Res 1123: 1-11.
34. Sun J, Maller JJ, Guo L, Fitzgerald PB (2009). Superior temporal gyrus volume change in schizophrenia: a review on region of interest volumetric studies. Brain Res Rev 61: 14-32.
35. Sun Y, Farzan F, Barr MS, Kirihara K, Fitzgerald PB, Light GA et al (2011). Gamma oscillations in schizophrenia: mechanisms and clinical significance. Brain Res 1413: 98-114.
36. Tanaka M, Olsen RW, Medina MT, Schwartz E, Alonso ME, Duron RM et al (2008). Hyperglycosylation and reduced GABA currents of mutated GABRB3 polypeptide in remitting childhood absence epilepsy. Am J Hum Genet 82: 1249-1261.
37. Telford JE, Bones J, McManus C, Saldova R, Manning G, Doherty M et al (2012). Antipsychotic treatment of acute paranoid schizophrenia patients with olanzapine results in altered glycosylation of serum glycoproteins. J Proteome Res 11: 3743-3752.
38. Thompson M, Weickert CS, Wyatt E, Webster MJ (2009). Decreased glutamic acid decarboxylase(67) mRNA expression in multiple brain areas of patients with schizophrenia and mood disorders. J Psychiatr Res 43: 970-977.
39. Tucholski J, Simmons MS, Pinner AL, Haroutunian V, McCullumsmith RE, Meador-Woodruff JH (2013a). Abnormal N-linked glycosylation of cortical AMPA receptor subunits in schizophrenia. Schizophr Res 146: 177-183.
40. Tucholski J, Simmons MS, Pinner AL, McMillan LD, Haroutunian V, Meador-Woodruff JH (2013b). N-linked glycosylation of cortical N-methyl-D-aspartate and kainate receptor subunits in schizophrenia. Neuroreport 24: 688-691.
41. Uhlhaas PJ, Singer W (2006). Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52: 155-168.
42. Varki A (2009). Essentials of Glycobiology. 2nd edn. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, xxix, pp 784.
43. Zierhut KC, Schulte-Kemna A, Kaufmann J, Steiner J, Bogerts B, Schiltz K (2013). Distinct structural alterations independently contributing to working memory deficits and symptomatology in paranoid schizophrenia. Cortex 49: 1063-1072.