Changes in NMDA receptor subunits and interacting PSD proteins in dorsolateral prefrontal and anterior cingulate cortex indicate abnormal regional expression in schizophrenia

Molecular Psychiatry

Volumn 11, Issue 8, 2006, Pages 737-747

  Kristiansen, L V ^a   Beneyto, M ^a   Haroutunian, V ^b   Meador Woodruff, J H ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cortex; Glutamate; In situ hybridization; Postmortem; Translation; Western blotting

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT; SULFUR 35;

ADULT; AGED; AMINO ACID SEQUENCE; ARTICLE; BRAIN CORTEX; CINGULATE GYRUS; CLINICAL ARTICLE; FEMALE; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; ISOTOPE LABELING; MALE; MENTAL DISEASE; NEUROTRANSMISSION; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHIZOPHRENIA; WESTERN BLOTTING;

AGED; AGED, 80 AND OVER; BLOTTING, WESTERN; FEMALE; GENE EXPRESSION; GUANYLATE KINASE; GYRUS CINGULI; HUMANS; IN SITU HYBRIDIZATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MIDDLE AGED; NERVE TISSUE PROTEINS; NEUROFILAMENT PROTEINS; NUCLEAR PROTEINS; PREFRONTAL CORTEX; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 33746526525     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/sj.mp.4001844     Document Type: Article

References (82)

1. Meador-Woodruff JH, Clinton SM, Beneyto M, McCullumsmith RE. Molecular abnormalities of the glutamate synapse in the thalamus in schizophrenia. Ann NY Acad Sci 2003; 1003: 75-93.
2. Lyne J, Kelly BD, O'Connor WT. Schizophrenia: a review of neuropharmacology. Ir J Med Sci 2004; 173: 155-159.
3. Zukin RS, Bennett MV. Alternatively spliced isoforms of the NMDARI receptor subunit. Trends Neurosci 1995; 18: 306-313.
4. Huh KH, Wenthold RJ. Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J Biol Chem 1999; 274: 151-157.
5. Kato A, Rouach N, Nicoll RA, Bredt DS. Activity-dependent NMDA receptor degradation mediated by retrotranslocation and ubiquitination. Proc Natl Acad Sci USA 2005; 102: 5600-5605.
6. Rumbaugh G, Prybylowski K, Wang JF, Vicini S. Exon 5 and spermine regulate deactivation of NMDA receptor subtypes. J Neurophysiol 2000; 83: 1300-1306.
7. Lin JW, Wyszynski M, Madhavan R, Sealock R, Kim JU, Sheng M. Yotiao, a novel protein of neuromuscular junction and brain that interacts with specific splice variants of NMDA receptor subunit NR1. J Neurosci 1998; 18: 2017-2027.
8. Logan SM, Rivera FE, Leonard JP. Protein kinase C modulation of recombinant NMDA receptor currents: roles for the C-terminal C1 exon and calcium ions. J Neurosci 1999; 19: 974-986.
9. Cull-Candy S, Brickley S, Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 2001; 11: 327-335.
10. Loftis JM, Janowsky A. The N-methyl-D-aspartate receptor subunit NR2B: localization, functional properties, regulation, and clinical implications. Pharmacol Ther 2003; 97: 55-85.
11. Brickley SG, Misra C, Mok MH, Mishina M, Cull-Candy SG. NR2B and NR2D subunits coassemble in cerebellar golgi cells to form a distinct NMDA receptor subtype restricted to extrasynaptic sites. J Neurosci 2003; 23: 4958-4966.
12. Ratnam J, Teichberg VI. Neurofilament-light increases the cell surface expression of the N-methyl-D-aspartate receptor and prevents its ubiquitination. J Neurochem 2005; 92: 878-885.
13. Ehlers MD, Fung ET, O'Brien RJ, Huganir RL. Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments. J Neurosci 1998; 18: 720-730.
14. Standley S, Roche KW, McCallum J, Sans N, Wenthold RJ. PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 2000; 28: 887-898.
15. Okabe S, Miwa A, Okado H. Alternative splicing of the C-terminal domain regulates cell surface expression of the NMDA receptor NR1 subunit. J Neurosci 1999; 19: 7781-7792.
16. Mu Y, Otsuka T, Horton AC, Scott DB, Ehlers MD. Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors. Neuron 2003; 40: 581-594.
17. Takumi Y,Matsubara A, Rinvik E, Ottersen OP. The arrangement of glutamate receptors in excitatory synapses. Ann NY Acad Sci 1999; 868: 474-482.
18. Kennedy MB. The postsynaptic density at glutamatergic synapses. Trends Neurosci 1997; 20: 264-268.
19. Montgomery JM, Zamorano PL, Garner CC. MAGUKs in synapse assembly and function: an emerging view. Cell Mol Life Sci 2004; 61: 911-929.
20. Lau LF, Mammen A, Ehlers MD, Kindler S, Chung WJ, Garner CC et al. Interaction of the N-methyl-D-aspartate receptor complex with a novel synapse-associated protein, SAP102. J Biol Chem 1996; 271: 21622-21628.
21. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 1995; 269: 1737-1740.
22. Niethammer M, Kim E, Sheng M. Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J Neurosci 1996; 16: 2157-2163.
23. Nada S, Shima T, Yanai H, Husi H, Grant SG, Okada M et al. Identification of PSD-93 as a substrate for the Src family tyrosine kinase Fyn. J Biol Chem 2003; 278: 47610-47621.
24. Sheng M. The postsynaptic NMDA-receptor-PSD-95 signaling complex in excitatory synapses of the brain. J Cell Sci 2001; 114: 1251.
25. Funke L, Dakoji S, Bredt DS. Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu Rev Biochem 2004; 74: 219-243.
26. Perez-Otano I, Ehlers MD. Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci 2005; 28: 229-238.
27. Soto D, Pancetti F, Marengo JJ, Sandoval M, Sandoval R, Orrego F et al. Protein kinase CK2 in postsynaptic densities: phosphorylation of PSD-95/SAP90 and NMDA receptor regulation. Biochem Biophys Res Commun 2004; 322: 542-550.
28. Kalia LV, Salter MW. Interactions between Src family protein tyrosine kinases and PSD-95. Neuropharmacology 2003; 45: 720-728.
29. Iwamoto T, Yamada Y, Hori K, Watanabe Y, Sobue K, Inui M. Differential modulation of NR1-NR2A and NR1-NR2B subtypes of NMDA receptor by PDZ domain-containing proteins. J Neurochem 2004; 89: 100-108.
30. van Zundert B, Yoshii A, Constantine-Paton M. Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci 2004; 27: 428-437.
31. Sans N, Prybylowski K, Petralia RS, Chang K, Wang YX, Racca C et al. NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nat Cell Biol 2003; 5: 520-530.
32. Hoogenraad CC, Sheng M. The return of the exocyst. Nat Cell Biol 2003; 5: 493-495.
33. Setou M, Nakagawa T, Seog DH, Hirokawa N. Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 2000; 288: 1796-1802.
34. Kneussel M. Postsynaptic scaffold proteins at non-synaptic sites. The role of postsynaptic scaffold proteins in motor-protein-receptor complexes. EMBO Rep 2005; 6: 22-27.
35. Dracheva S, Marras SA, Elhakem SL, Kramer FR, Davis KL, Haroutunian V. N-methyl-D-aspartic acid receptor expression in the dorsolateral prefrontal cortex of elderly patients with schizophrenia. Am J Psychiatry 2001; 158: 1400-1410.
36. Meador-Woodruff JH, Healy DJ. Glutamate receptor expression in schizophrenic brain. Brain Res Brain Res Rev 2000; 31: 288-294.
37. Akbarian S, Sucher NJ, Bradley D, Tafazzoli A, Trinh D, Hetrick WP et al. Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics. J Neurosci 1996; 16: 19-30.
38. Clinton SM, Meador-Woodruff JH. Abnormalities of the NMDA receptor and associated intracellular molecules in the thalamus in schizophrenia and bipolar disorder. Neuropsychopharmacology 2004; 29: 1353-1362.
39. Kajimoto Y, Shirakawa O, Lin XH, Hashimoto T, Kitamura N, Murakami N et al. Synapse-associated protein 90/postsynaptic density-95-associated protein (SAPAP) is expressed differentially in phencyclidine-treated rats and is increased in the nucleus accumbens of patients with schizophrenia. Neuropsychopharmacology 2003; 28: 1831-1839.
40. Ohnuma T, Kato H, Arai H, Faull RL, McKenna PJ, Emson PC. Gene expression of PSD95 in prefrontal cortex and hippocampus in schizophrenia. Neuroreport 2000; 11: 3133-3137.
41. Kristiansen LV, Meador-Woodruff JH. Abnormal striatal expression of transcripts encoding NMDA interacting PSD proteins in schizophrenia, bipolar disorder and major depression. Schizophr Res 2005; 78: 87-93.
42. Tamminga CA, Holcomb HH. Phenotype of schizophrenia: a review and formulation. Mol Psychiatry 2005; 10: 27-39.
43. Lewis DA, Glantz LA, Pierri JN, Sweet RA. Altered cortical glutamate neurotransmission in schizophrenia: evidence from morphological studies of pyramidal neurons. Ann NY Acad Sci 2003; 1003: 102-112.
44. Purohit DP, Davidson M, Perl DP, Powchik P, Haroutunian VH, Bierer LM et al. Severe cognitive impairment in elderly schizophrenic patients: a clinicopathological study. Biol Psychiatry 1993; 33: 255-260.
45. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254.
46. Tingley WG, Roche KW, Thompson AK, Huganir RL. Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 1993; 364: 70-73.
47. Blahos II J, Wenthold RJ. Relationship between N-methyl-D-aspartate receptor NR1 splice variants and NR2 subunits. J Biol Chem 1996; 271: 15669-15674.
48. Clinton SM, Haroutunian V, Davis KL, Meador-Woodruff JH. Altered transcript expression of NMDA receptor-associated post-synaptic proteins in the thalamus of subjects with schizophrenia. Am J Psychiatry 2003; 160: 1100-1109.
49. Clinton SM, Meador-Woodruff JH. Nucleus-specific expression of NMDA receptor-associated postsynaptic density proteins in primate thalamus. Thalamus Relat Syst 2002; 1: 303-316.
50. Ibrahim HM, Healy DJ, Hogg Jr AJ, Meador-Woodruff JH. Nucleus-specific expression of ionotropic glutamate receptor subunit mRNAs and binding sites in primate thalamus. Brain Res Mol Brain Res 2000; 79: 1-17.
51. 14C-plastic standards for quantitative autoradiography using LKB ultrofilm or Amersham hyperfilm. Neurosci Lett 1991; 121: 211-214.
52. Emamian ES, Hall D, Birnbaum MJ, Karayiorgou M, Gogos JA. Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat Genet 2004; 36: 131-137.
53. Virgo L, Humphries C, Mortimer A, Barnes T, Hirsch S, de Belleroche J. Cholecystokinin messenger RNA deficit in frontal and temporal cerebral cortex in schizophrenia. Biol Psychiatry 1995; 37: 694-701.
54. Rioux L, Gelber EI, Parand L, Kazi HA, Yeh J, Wintering R et al. Characterization of olfactory bulb glomeruli in schizophrenia. Schizophr Res 2005; 77: 229-239.
55. Perrone-Bizzozero NI, Sower AC, Bird ED, Benowitz LI, Ivins KJ, Neve RL. Levels of the growth-associated protein GAP-43 are selectively increased in association cortices in schizophrenia. Proc Natl Acad Sci USA 1996; 93: 14182-14187.
56. Halim ND, Weickert CS, McClintock BW, Hyde TM, Weinberger DR, Kleinman JE et al. Presynaptic proteins in the prefrontal cortex of patients with schizophrenia and rats with abnormal prefrontal development. Mol Psychiatry 2003; 8: 797-810.
57. 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.
58. Siew LK, Love S, Dawbarn D, Wilcock GK, Allen SJ. Measurement of pre- and post-synaptic proteins in cerebral cortex: effects of post-mortem delay. J Neurosci Methods 2004; 139: 153-159.
59. Hilbig H, Bidmon HJ, Oppermann OT, Remmerbach T. Influence of post-mortem delay and storage temperature on the immunohistochemical detection of antigens in the CNS of mice. Exp Toxicol Pathol 2004; 56: 159-171.
60. Kingsbury AE, Foster OJ, Nisbet AP, Cairns N, Bray L, Eve DJ et al. Tissue pH as an indicator of mRNA preservation in human post-mortem brain. Brain Res Mol Brain Res 1995; 28: 311-318.
61. Catts VS, Catts SV, Fernandez HR, Taylor JM, Coulson EJ, Lutze-Mann LH. A microarray study of post-mortem mRNA degradation in mouse brain tissue. Brain Res Mol Brain Res 2005; 138: 164-177.
62. Brenman JE, Christopherson KS, Craven SE, McGee AW, Bredt DS. Cloning and characterization of postsynaptic density 93, a nitric oxide synthase interacting protein. J Neurosci 1996; 16: 7407-7415.
63. Sans N, Petralia RS, Wang YX, Blahos II J, Hell JW, Wenthold RJ. A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J Neurosci 2000; 20: 1260-1271.
64. Conti F. Localization of NMDA receptors in the cerebral cortex: a schematic overview. Braz J Med Biol Res 1997; 30: 555-560.
65. Pauly T, Schlicksupp A, Neugebauer R, Kuhse J. Synaptic targeting of N-methyl-D-aspartate receptor splice variants is regulated differentially by receptor activity. Neuroscience 2005; 131: 99-111.
66. Krebs MO. Glutamatergic hypothesis of schizophrenia: psychoses induced by phencyclidine and cortical-subcortical imbalance. Encephale 1995; 21: 581-588.
67. Meador-Woodruff JH, Hogg Jr AJ, Smith RE. Striatal ionotropic glutamate receptor expression in schizophrenia, bipolar disorder, and major depressive disorder. Brain Res Bull 2001; 55: 631-640.
68. Gao XM, Sakai K, Roberts RC, Conley RR, Dean B, Tamminga CA. Ionotropic glutamate receptors and expression of N-methyl-D-aspartate receptor subunits in subregions of human hippocampus: effects of schizophrenia. Am J Psychiatry 2000; 157: 1141-1149.
69. Tezuka T, Umemori H, Akiyama T, Nakanishi S, Yamamoto T. PSD-95 promotes Fyn-mediated tyrosine phosphorylation of the N-methyl-D-aspartate receptor subunit NR2A. Proc Natl Acad Sci USA 1999; 96: 435-440.
70. Tao YX, Rumbaugh G, Wang GD, Petralia RS, Zhao C, Kauer FW et al. Impaired NMDA receptor-mediated postsynaptic function and blunted NMDA receptor-dependent persistent pain in mice lacking postsynaptic density-93 protein. J Neurosci 2003; 23: 6703-6712.
71. Kleizen B, Braakman I. Protein folding and quality control in the endoplasmic reticulum. Curr Opin Cell Biol 2004; 16: 343-349.
72. Walsh CT. Posttranslational Modification of Proteins: Expanding Nature's Inventory. In: Walsh CT (ed). Roberts & Company Publishers: Greenwood Village, CO, USA, 2005, pp 576.
73. Rattan SI. Synthesis, modifications, and turnover of proteins during aging. Exp Gerontol 1996; 31: 33-47.
74. Olney JW, Newcomer JW, Farber NB. NMDA receptor hypofunction model of schizophrenia. J Psychiatr Res 1999; 33: 523-533.
75. Snitz BE, MacDonald III A, Cohen JD, Cho RY, Becker T, Carter CS. Lateral and medial hypofrontality in first-episode schizophrenia: functional activity in a medication-naive state and effects of short-term atypical antipsychotic treatment. Am J Psychiatry 2005; 162: 2322-2329.
76. MacDonald III AW, Cohen JD, Stenger VA, Carter CS. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 2000; 288: 1835-1838.
77. Kerns JG, Cohen JD, MacDonald III AW, Cho RY, Stenger VA, Carter CS. Anterior cingulate conflict monitoring and adjustments in control. Science 2004; 303: 1023-1026.
78. Zavitsanou K, Ward PB, Huang XF. Selective alterations in ionotropic glutamate receptors in the anterior cingulate cortex in schizophrenia. Neuropsychopharmacology 2002; 27: 826-833.
79. Muñoz A, Woods TM, Jones EG. Laminar and cellular distribution of AMPA, kainate, and NMDA receptor subunits in monkey sensory - motor cortex. J Comp Neurol 1999; 407: 472-490.
80. Conti F, Barbaresi P, Melone M, Ducati A. Neuronal and glial localization of NR1 and NR2A/B subunits of the NMDA receptor in the human cerebral cortex. Cereb Cortex 1999; 9: 110-120.
81. Giguere M, Goldman-Rakic PS. Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J Comp Neurol 1988; 277: 195-213.
82. Goff DC, Coyle JT. The emerging role of glutamate in the pathophysiology and treatment of schizophrenia. Am J Psychiatry 2001; 158: 1367-1377.