Detergent-insoluble EAAC1/EAAT3 aberrantly accumulates in hippocampal neurons of Alzheimer's disease patients

Brain Pathology

Volumn 19, Issue 2, 2009, Pages 267-278

  Duerson, Kevin ^b   Woltjer, Randall L ^c   Mookherjee, Paramita ^b   Leverenz, James B ^b   Montine, Thomas J ^b   Bird, Thomas D ^b   Pow, David V ^d   Rauen, Thomas ^e   Cook, David G ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^e UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Excitotoxicity; Glutamate toxicity; Glutamate Uptake; Memantine; Neurodegeneration; Protein aggregation; Synaptic dysfunction

Indexed keywords

4 AMINOBUTYRIC ACID; DETERGENT; GLUTAMIC ACID; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; TRITON X 100;

AGED; ALZHEIMER DISEASE; ARTICLE; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FOREBRAIN; FRONTAL CORTEX; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL; NEUROPATHOLOGY; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; REGULATORY MECHANISM; SOLUBILITY; SYNAPSE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BLOTTING, WESTERN; DETERGENTS; EXCITATORY AMINO ACID TRANSPORTER 3; FEMALE; FRONTAL LOBE; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEUROFIBRILLARY TANGLES; NEURONS; OCTOXYNOL; PARKINSON DISEASE; SENILE PLAQUES; SOLUBILITY;

EID: 61649090015     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2008.00186.x     Document Type: Article

References (71)

1. Ball M, Braak H, Goethe JW, Coleman P, Dickson D, Duyckaerts C, Gambetti P, Hansen L, Hyman B, Jellinger K, Markesbery W, Perl D, Powers J, Price J, Trojanowski JQ, Wisniewski H, Phelps C, Khachaturian Z (1997) Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Neurobiol Aging 18 : S1 2.
2. Aoyama K, Suh SW, Hamby AM, Liu J, Chan WY, Chen Y, Swanson RA (2006) Neuronal glutathione deficiency and age-dependent neurodegeneration in the EAAC1 deficient mouse. Nat Neurosci 9 : 119 126.
3. Arriza JL, Eliasof S, Kavanaugh MP, Amara SG (1997) Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci USA 94 : 4155 4160.
4. Baba M, Nakajo S, Tu PH, Tomita T, Nakaya K, Lee VM et al (1998) Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am J Pathol 152 : 879 884.
5. Bar-Peled O, Ben-Hur H, Biegon A, Groner Y, Dewhurst S, Furuta A, Rothstein JD (1997) Distribution of glutamate transporter subtypes during human brain development. J Neurochem 69 : 2571 2580.
6. Barry SC, Harder B, Brzezinski M, Flint LY, Seppen J, Osborne WR (2001) Lentivirus vectors encoding both central polypurine tract and posttranscriptional regulatory element provide enhanced transduction and transgene expression. Hum Gene Ther 12 : 1103 1108.
7. Berger UV, DeSilva TM, Chen W, Rosenberg PA (2005) Cellular and subcellular mRNA localization of glutamate transporter isoforms GLT1a and GLT1b in rat brain by in situ hybridization. J Comp Neurol 492 : 78 89.
8. Blanc EM, Keller JN, Fernandez S, Mattson MP (1998) 4-hydroxynonenal, a lipid peroxidation product, impairs glutamate transport in cortical astrocytes. Glia 22 : 149 160.
9. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl) 82 : 239 259.
10. Brustovetsky T, Purl K, Young A, Shimizu K, Dubinsky JM (2004) Dearth of glutamate transporters contributes to striatal excitotoxicity. Exp Neurol 189 : 222 230.
11. Chen Y, Swanson RA (2003) The glutamate transporters EAAT2 and EAAT3 mediate cysteine uptake in cortical neuron cultures. J Neurochem 84 : 1332 1339.
12. Churchyard A, Lees AJ (1997) The relationship between dementia and direct involvement of the hippocampus and amygdala in Parkinson's disease. Neurology 49 : 1570 1576.
13. Dabir DV, Robinson MB, Swanson E, Zhang B, Trojanowski JQ, Lee VM, Forman MS (2006) Impaired glutamate transport in a mouse model of tau pathology in astrocytes. J Neurosci 26 : 644 654.
14. Diamond JS (2002) A broad view of glutamate spillover. Nat Neurosci 5 : 291 292.
15. Diamond JS (2005) Deriving the glutamate clearance time course from transporter currents in CA1 hippocampal astrocytes: transmitter uptake gets faster during development. J Neurosci 25 : 2906 2916.
16. Fairman WA, Vandenberg RJ, Arriza JL, Kavanaugh MP, Amara SG (1995) An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375 : 599 603.
17. Galvin JE, Giasson B, Hurtig HI, Lee VM, Trojanowski JQ (2000) Neurodegeneration with brain iron accumulation, type 1 is characterized by alpha-, beta-, and gamma-synuclein neuropathology. Am J Pathol 157 : 361 368.
18. Galvin JE, Palamand D, Strider J, Milone M, Pestronk A (2006) The muscle protein dysferlin accumulates in the Alzheimer brain. Acta Neuropathol (Berl) 112 : 665 671.
19. Harris ME, Carney JM, Cole PS, Hensley K, Howard BJ, Martin L et al (1995) beta-Amyloid peptide-derived, oxygen-dependent free radicals inhibit glutamate uptake in cultured astrocytes: implications for Alzheimer's disease. Neuroreport 6 : 1875 1879.
20. +-dependent glutamate uptake in rat hippocampal astrocyte cultures. J Neurochem 67 : 277 286.
21. Haugeto O, Ullensvang K, Levy LM, Chaudhry FA, Honore T, Nielsen M et al (1996) Brain glutamate transporter proteins form homomultimers. J Biol Chem 271 : 27715 27722.
22. Hayes D, Wiessner M, Rauen T, McBean GJ (2005) Transport of L-[14C]cystine and L-[14C]cysteine by subtypes of high affinity glutamate transporters over-expressed in HEK cells. Neurochem Int 46 : 585 594.
23. Herman MA, Jahr CE (2007) Extracellular glutamate concentration in hippocampal slice. J Neurosci 27 : 9736 9741.
24. Holmseth S, Dehnes Y, Bjornsen LP, Boulland JL, Furness DN, Bergles D, Danbolt NC (2005) Specificity of antibodies: unexpected cross-reactivity of antibodies directed against the excitatory amino acid transporter 3 (EAAT3). Neuroscience 136 : 649 660.
25. Imamura K, Hishikawa N, Ono K, Suzuki H, Sawada M, Nagatsu T et al (2005) Cytokine production of activated microglia and decrease in neurotrophic factors of neurons in the hippocampus of Lewy body disease brains. Acta Neuropathol (Berl) 109 : 141 150.
26. Jacob CP, Koutsilieri E, Bartl J, Neuen-Jacob E, Arzberger T, Zander N et al (2007) Alterations in expression of glutamatergic transporters and receptors in sporadic Alzheimer's disease. J Alzheimers Dis 11 : 97 116.
27. Kanai Y, Hediger MA (1992) Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360 : 467 471.
28. Keller JN, Pang Z, Geddes JW, Begley JG, Germeyer A, Waeg G, Mattson MP (1997) Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid beta-peptide: role of the lipid peroxidation product 4-hydroxynonenal. J Neurochem 69 : 273 284.
29. Koller MF, Mohajeri MH, Huber M, Wollmer MA, Roth Z'graggen BV, Sandmeier E et al (2004) Active immunization of mice with an Abeta-Hsp70 vaccine. Neurodegener Dis 1 : 20 28.
30. Lagalwar S, Berry RW, Binder LI (2007) Relation of hippocampal phospho-SAPK/JNK granules in Alzheimer's disease and tauopathies to granulovacuolar degeneration bodies. Acta Neuropathol (Berl) 113 : 63 73.
31. Lauderback CM, Hackett JM, Huang FF, Keller JN, Szweda LI, Markesbery WR, Butterfield DA (2001) The glial glutamate transporter, GLT-1, is oxidatively modified by 4- hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Abeta1- 42. J Neurochem 78 : 413 416.
32. Lee VM, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24 : 1121 1159.
33. Levenson J, Weeber E, Selcher JC, Kategaya LS, Sweatt JD, Eskin A (2002) Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake. Nat Neurosci 5 : 155 161.
34. Li S, Mallory M, Alford M, Tanaka S, Masliah E (1997) Glutamate transporter alterations in Alzheimer disease are possibly associated with abnormal APP expression. J Neuropathol Exp Neurol 56 : 901 911.
35. Liao L, Cheng D, Wang J, Duong DM, Losik TG, Gearing M et al (2004) Proteomic characterization of postmortem amyloid plaques isolated by laser capture microdissection. J Biol Chem 279 : 37061 37068.
36. Lipton SA (2006) Paradigm shift in neuroprotection by NMDA receptor blockade: memantine and beyond. Nat Rev Drug Discov 5 : 160 170.
37. Lovell MA, Markesbery WR (2007) Oxidative damage in mild cognitive impairment and early Alzheimer's disease. J Neurosci Res
38. Malm TM, Iivonen H, Goldsteins G, Keksa-Goldsteine V, Ahtoniemi T, Kanninen K et al (2007) Pyrrolidine dithiocarbamate activates Akt and improves spatial learning in APP/PS1 mice without affecting beta-amyloid burden. J Neurosci 27 : 3712 3721.
39. Maragakis NJ, Dykes-Hoberg M, Rothstein JD (2004) Altered expression of the glutamate transporter EAAT2b in neurological disease. Ann Neurol 55 : 469 477.
40. Masliah E, Alford M, Mallory M, Rockenstein E, Moechars D, Van Leuven F (2000) Abnormal glutamate transport function in mutant amyloid precursor protein transgenic mice. Exp Neurol 163 : 381 387.
41. Mathews GC, Diamond JS (2003) Neuronal glutamate uptake contributes to GABA synthesis and inhibitory synaptic strength. J Neurosci 23 : 2040 2048.
42. Meredith SC (2005) Protein denaturation and aggregation: cellular responses to denatured and aggregated proteins. Ann NY Acad Sci 1066 : 181 221.
43. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM et al (1991) The Consortium to Establish a Registry for Alzheimer's disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41 : 479 486.
44. Morishima-Kawashima M, Ihara Y (1998) The presence of amyloid beta-protein in the detergent-insoluble membrane compartment of human neuroblastoma cells. Biochemistry 37 : 15247 15253.
45. Okamoto K, Hirai S, Iizuka T, Yanagisawa T, Watanabe M (1991) Reexamination of granulovacuolar degeneration. Acta Neuropathol (Berl) 82 : 340 345.
46. Peghini P, Janzen J, Stoffel W (1997) Glutamate transporter EAAC-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. EMBO J 16 : 3822 3832.
47. Pines G, Danbolt NC, Bjoras M, Zhang Y, Bendahan A, Eide L et al (1992) Cloning and expression of a rat brain L-glutamate transporter. Nature 360 : 464 467.
48. Pita-Almenar JD, Collado MS, Colbert CM, Eskin A (2006) Different mechanisms exist for the plasticity of glutamate reuptake during early long-term potentiation (LTP) and late LTP. J Neurosci 26 : 10461 10471.
49. Robinson MB (2002) Regulated trafficking of neurotransmitter transporters: common notes but different melodies. J Neurochem 80 : 1 11.
50. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D et al (1994) Localization of neuronal and glial glutamate transporters. Neuron 13 : 71 3 725.
51. Rothstein JD, Van Kammen M, Levey AI, Martin LJ, Kuncl RW (1995) Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 38 : 73 84.
52. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW et al (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16 : 675 686.
53. Saper CB, Sawchenko PE (2003) Magic peptides, magic antibodies: guidelines for appropriate controls for immunohistochemistry. J Comp Neurol 465 : 161 163.
54. Schneider A, Schulz-Schaeffer W, Hartmann T, Schulz JB, Simons M (2006) Cholesterol depletion reduces aggregation of amyloid-beta peptide in hippocampal neurons. Neurobiol Dis 23 : 573 577.
55. Schwab C, DeMaggio AJ, Ghoshal N, Binder LI, Kuret J, McGeer PL (2000) Casein kinase 1 delta is associated with pathological accumulation of tau in several neurodegenerative diseases. Neurobiol Aging 21 : 503 510.
56. Scott HL, Pow DV, Tannenberg AE, Dodd PR (2002) Aberrant expression of the glutamate transporter excitatory amino acid transporter 1 (EAAT1) in Alzheimer's disease. J Neurosci 22 : RC206.
57. Sepkuty JP, Cohen AS, Eccles C, Rafiq A, Behar K, Ganel R et al (2002) A neuronal glutamate transporter contributes to neurotransmitter GABA synthesis and epilepsy. J Neurosci 22 : 6372 6379.
58. Sergeant N, David JP, Champain D, Ghestem A, Wattez A, Delacourte A (2002) Progressive decrease of amyloid precursor protein carboxy terminal fragments (APP-CTFs), associated with tau pathology stages, in Alzheimer's disease. J Neurochem 81 : 663 672.
59. Shimamoto K, Sakai R, Takaoka K, Yumoto N, Nakajima T, Amara SG, Shigeri Y (2004) Characterization of novel L-threo-beta-benzyloxyaspartate derivatives, potent blockers of the glutamate transporters. Mol Pharmacol 65 : 1008 1015.
60. Storck T, Schulte S, Hofmann K, Stoffel W (1992) Structure, expression, and functional analysis of a Na(+)-dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci USA 89 : 10955 10959.
61. Sullivan R, Rauen T, Fischer F, Wiessner M, Grewer C, Bicho A, Pow DV (2004) Cloning, transport properties, and differential localization of two splice variants of GLT-1 in the rat CNS: implications for CNS glutamate homeostasis. Glia 45 : 155 169.
62. Sultana R, Reed T, Perluigi M, Coccia R, Pierce WM, Butterfield DA (2007) Proteomic identification of nitrated brain proteins in amnestic mild cognitive impairment: a regional study. J Cell Mol Med 11 : 839 851.
63. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K et al (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276 : 1699 1702.
64. Trotti D, Danbolt NC, Volterra A (1998) Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration? Trends Pharmacol Sci 19 : 328 334.
65. Tsvetkov E, Shin RM, Bolshakov VY (2004) Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning. Neuron 41 : 139 151.
66. Watase K, Hashimoto K, Kano M, Yamada K, Watanabe M, Inoue Y et al (1998) Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci 10 : 976 988.
67. Waxman EA, Baconguis I, Lynch DR, Robinson MB (2007) N-methyl-D-aspartate receptor-dependent regulation of the glutamate transporter excitatory amino acid carrier 1. J Biol Chem 282 : 17594 17607.
68. Woltjer RL, Cimino PJ, Boutte AM, Schantz AM, Montine KS, Larson EB et al (2005) Proteomic determination of widespread detergent-insolubility including Abeta but not tau early in the pathogenesis of Alzheimer's disease. FASEB J 19 : 1923 1925.
69. Yang W, Woltjer RL, Sokal I, Pan C, Wang Y, Brodey M et al (2007) Quantitative proteomics identifies surfactant-resistant alpha-Synuclein in cerebral cortex of Parkinsonism-dementia complex of Guam but not Alzheimer's disease or progressive supranuclear palsy. Am J Pathol 171 : 993 1002.
70. Yang Y, Kinney GA, Spain WJ, Breitner JC, Cook DG (2004) Presenilin-1 and intracellular calcium stores regulate neuronal glutamate uptake. J Neurochem 88 : 1361 1372.
71. Yernool D, Boudker O, Jin Y, Gouaux E (2004) Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature 431 : 811 818.