Schizophrenia Research
Volume 117, Issue 1 , Pages 92-98 , March 2010

Abnormal glycosylation of EAAT1 and EAAT2 in prefrontal cortex of elderly patients with schizophrenia

  • Deborah Bauer

      Affiliations

    • Department of Psychiatry and Behavioral Neurobiology, University of Alabama at Birmingham, Birmingham, AL, United States
    • Program in Neuroscience, University of Michigan, Ann Arbor, MI, United States
    • Corresponding Author InformationCorresponding author. Department of Psychiatry, University of Alabama at Birmingham, SC560, 1530 3rd Ave S., Birmingham, AL 35294-0017, United States. Fax: +1 205 975 4879.
  • ,
  • Vahram Haroutunian

      Affiliations

    • Department of Psychiatry, Mount Sinai School of Medicine, New York, NY, United States
  • ,
  • James H. Meador-Woodruff

      Affiliations

    • Department of Psychiatry and Behavioral Neurobiology, University of Alabama at Birmingham, Birmingham, AL, United States
    • Program in Neuroscience, University of Michigan, Ann Arbor, MI, United States
  • ,
  • Robert E. McCullumsmith

      Affiliations

    • Department of Psychiatry and Behavioral Neurobiology, University of Alabama at Birmingham, Birmingham, AL, United States

Received 25 June 2009 ,Revised 29 July 2009 ,Accepted 31 July 2009.

References 

  1. Barbeau D, Liang JJ, Robitalille Y, Quirion R, Srivastava LK. Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc. Natl. Acad. Sci. U. S. A. 1995;92(7):2785–2789
  2. 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(1–3):108–120
  3. 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
  4. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron. 1995;15(3):711–720
  5. Conradt M, Storck T, Stoffel W. Localization of N-glycosylation sites and functional role of the carbohydrate units of GLAST-1, a cloned rat brain l-glutamate/l-aspartate transporter. Eur. J. Biochem. 1995;229(3):682–687
  6. Escartin C, Brouillet E, Gubellini P, Trioulier Y, Jacquard C, Smadja C, et al. Ciliary neurotrophic factor activates astrocytes, redistributes their glutamate transporters GLAST and GLT-1 to raft microdomains, and improves glutamate handling in vivo. J. Neurosci. 2006;26(22):5978–5989
  7. Gegelashvili G, Civenni G, Racagni G, Danbolt NC, Schousboe I, Schousboe A. Glutamate receptor agonists up-regulate glutamate transporter GLAST in astrocytes. NeuroReport. 1996;8(1):261–265
  8. Holmseth S, Dehnes Y, Bjornsen LP, Boulland JL, Furness DN, Bergles D, et al. Specificity of antibodies: unexpected cross-reactivity of antibodies directed against the excitatory amino acid transporter 3 (EAAT3). Neuroscience. 2005;136(3):649–660
  9. Hung WY, Mold DE, Tourian A. Huntington's-chorea fibroblasts. Cellular protein glycosylation.. Biochem. J. 1980;190(3):711–719
  10. Jarvie KR, Niznik HB, Seeman P. Dopamine D2 receptor binding subunits of Mr congruent to 140, 000 and 94, 000 in brain: deglycosylation yields a common unit of Mr congruent to 44, 000. Mol. Pharmacol. 1988;34(2):91–97
  11. Jimenez-Huete A, Lievens PM, Vidal R, Piccardo P, Ghetti B, Tagliavini F, et al. Endogenous proteolytic cleavage of normal and disease-associated isoforms of the human prion protein in neural and non-neural tissues. Am. J. Pathol. 1998;153(5):1561–1572
  12. Kalandadze A, Wu Y, Fournier K, Robinson MB. Identification of motifs involved in endoplasmic reticulum retention-forward trafficking of the GLT-1 subtype of glutamate transporter. J. Neurosci. 2004;24(22):5183–5192
  13. Karlsson RM, Tanaka K, Saksida LM, Bussey TJ, Heilig M, Holmes A. Assessment of glutamate transporter GLAST (EAAT1)-deficient mice for phenotypes relevant to the negative and executive/cognitive symptoms of schizophrenia. Neuropsychopharmacology. 2009;34(6):1578–1589
  14. Kondo K, Hashimoto H, Kitanaka J, Sawada M, Suzumura A, Marunouchi T, et al. Expression of glutamate transporters in cultured glial cells. Neurosci. Lett. 1995;188(2):140–142
  15. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J. Neurosci. 1995;15(3 Pt 1):1835–1853
  16. Levenson J, Weeber E, Selcher JC, Kategaya LS, Sweatt JD, Eskin A. Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake. Nat. Neurosci. 2002;5(2):155–161
  17. Maguire TM, Thakore J, Dinan TG, Hopwood S, Breen KC. Plasma sialyltransferase levels in psychiatric disorders as a possible indicator of HPA axis function. Biol. Psychiatry. 1997;41(11):1131–1136
  18. Marcaggi P, Attwell D. Short- and long-term depression of rat cerebellar parallel fibre synaptic transmission mediated by synaptic crosstalk. J. Physiol. 2007;578(Pt 2):545–550
  19. Narayan S, Head SR, Gilmartin TJ, Dean B, Thomas EA. Evidence for disruption of sphingolipid metabolism in schizophrenia. J. Neurosci. Res. 2008;
  20. Nielsen D, Gyllberg H, Ostlund P, Bergman T, Bedecs K. Increased levels of insulin and insulin-like growth factor-1 hybrid receptors and decreased glycosylation of the insulin receptor alpha- and beta-subunits in scrapie-infected neuroblastoma N2a cells. Biochem. J. 2004;380(Pt 2):571–579
  21. Ohtsubo K, Marth JD. Glycosylation in cellular mechanisms of health and disease. Cell. 2006;126(5):855–867
  22. Overstreet LS, Kinney GA, Liu YB, Billups D, Slater NT. Glutamate transporters contribute to the time course of synaptic transmission in cerebellar granule cells. J. Neurosci. 1999;19(21):9663–9673
  23. Patil ST, Zhang L, Martenyi F, Lowe SL, Jackson KA, Andreev BV, et al. Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial. Nat. Med. 2007;13(9):1102–1107
  24. Rajkowska G, Goldman-Rakic PS. Cytoarchitectonic definition of prefrontal areas in the normal human cortex: I. Remapping of areas 9 and 46 using quantitative criteria. Cereb. Cortex. 1995;5(4):307–322
  25. Raunser S, Haase W, Bostina M, Parcej DN, Kuhlbrandt W. High-yield expression, reconstitution and structure of the recombinant, fully functional glutamate transporter GLT-1 from Rattus norvegicus. J. Mol. Biol. 2005;351(3):598–613
  26. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, et al. Localization of neuronal and glial glutamate transporters. Neuron. 1994;13(3):713–725
  27. Schmitt A, Asan E, Puschel B, Kugler P. Cellular and regional distribution of the glutamate transporter GLAST in the CNS of rats: nonradioactive in situ hybridization and comparative immunocytochemistry. J. Neurosci. 1997;17(1):1–10
  28. Schulte S, Stoffel W. UDP galactose:ceramide galactosyltransferase and glutamate/aspartate transporter. Copurification, separation and characterization of the two glycoproteins. Eur. J. Biochem. 1995;233(3):947–953
  29. Shashidharan P, Huntley GW, Murray JM, Buku A, Moran T, Walsh MJ, et al. Immunohistochemical localization of the neuron-specific glutamate transporter EAAC1 (EAAT3) in rat brain and spinal cord revealed by a novel monoclonal antibody. Brain Res. 1997;773(1–2):139–148
  30. Takeuchi M, Yamagishi S. Involvement of toxic AGEs (TAGE) in the pathogenesis of diabetic vascular complications and Alzheimer's disease. J. Alzheimer's Dis. 2009;16(4):845–858
  31. Toledo JR, Sanchez O, Montesino Segui R, Fernandez Garcia Y, Rodriguez MP, Cremata JA. Differential in vitro and in vivo glycosylation of human erythropoietin expressed in adenovirally transduced mouse mammary epithelial cells. Biochim. Biophys. Acta. 2005;1726(1):48–56
  32. Tong G, Jahr CE. Block of glutamate transporters potentiates postsynaptic excitation. Neuron. 1994;13(5):1195–1203
  33. Trotti D, Aoki M, Pasinelli P, Berger UV, Danbolt NC, Brown RH, et al. Amyotrophic lateral sclerosis-linked glutamate transporter mutant has impaired glutamate clearance capacity. J. Biol. Chem. 2001;276(1):576–582
  34. Tsvetkov E, Shin RM, Bolshakov VY. Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning. Neuron. 2004;41(1):139–151
  35. Tzingounis AV, Wadiche JI. Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat. Rev. Neurosci. 2007;8(12):935–947
  36. Varma R, Hoshino AY. Serum glycoproteins in schizophrenia. Carbohydr. Res. 1980;82(2):343–351
  37. Walsh T, McClellan JM, McCarthy SE, Addington AM, Pierce SB, Cooper GM, et al. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science. 2008;320(5875):539–543
  38. Williams SM, Sullivan RK, Scott HL, Finkelstein DI, Colditz PB, Lingwood BE, et al. Glial glutamate transporter expression patterns in brains from multiple mammalian species. Glia. 2005;49(4):520–541
  39. Yang W, Kilberg MS. Biosynthesis, intracellular targeting, and degradation of the EAAC1 glutamate/aspartate transporter in C6 glioma cells. J. Biol. Chem. 2002;277(41):38350–38357

PII: S0920-9964(09)00376-4

doi: 10.1016/j.schres.2009.07.025

Schizophrenia Research
Volume 117, Issue 1 , Pages 92-98 , March 2010