GAD65, GAD67, and GABAT Immunostaining in human brain and apparent GAD65 loss in alzheimer's disease

Journal of Alzheimer's Disease

Volumn 33, Issue 4, 2013, Pages 1073-1088

  Schwab, Claudia ^a   Yu, Sheng ^a   Wong, Winnie ^a   McGeer, Edith G ^a   McGeer, Patrick L ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

ABAT; Alzheimer's disease; GABAergic system; GABAT; GAD65; GAD67; human; immunohistochemistry; western blot

Indexed keywords

4 AMINOBUTYRIC ACID; GABA TRANSFERASE; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; UNCLASSIFIED DRUG;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BASAL GANGLION; BRAIN; CELL GRANULE; CELL LABELING; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENZYME LOCALIZATION; FEMALE; FLUORESCENCE; GABAERGIC SYSTEM; GLIA CELL; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MICROSCOPY; MIDDLE TEMPORAL GYRUS; NEOCORTEX; NERVE ENDING; NEUROPIL; PERIKARYON; PRIORITY JOURNAL; PUTAMEN; WESTERN BLOTTING;

EID: 84873651092     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-121330     Document Type: Article

References (91)

1. LewisDA, Hashimoto T, MorrisHM(2008) Cell and receptor type-specific alterations in markers of GABA neurotransmission in the prefrontal cortex of subjects with schizophrenia. Neurotox Res 14, 237-248
2. Erlander MG, Tobin AJ (1991) The structural and functional heterogeneity of glutamic acid decarboxylase:Areview. Neurochem Res 16, 215-226
3. Soghomonian JJ, Martin DL (1998) Two isoforms of glutamate decarboxylase: Why? Trends Pharmacol Sci 19, 500-505
4. WatanabeM,Maemura K, Kanbara K,TamayamaT, Hayasaki H (2002) GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol 213, 1-47
5. Tillakaratne NJ, Medina-Kauwe L, Gibson KM (1995) gamma-Aminobutyric acid (GABA) metabolism in mammalian neural and nonneural tissues. Comp Biochem Physiol A Physiol 112, 247-263
6. Petroff OA (2002) GABA and glutamate in the human brain. Neuroscientist 8, 562-573
7. Wong CG, Bottiglieri T, Snead OC 3rd (2003) GABA, gamma-hydroxybutyric acid, and neurological disease. Ann Neurol 54(SUPPL6), S3-S12
8. Hashimoto T, Arion D, Unger T, Maldonado-Aviles JG, Morris HM, Volk DW, Mirnics K, Lewis DA (2008) Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 13, 147-161
9. Costa E, Davis JM, Dong E, Grayson DR, Guidotti A, Tremolizzo L, VeldicM(2004) A GABAergic cortical deficit dominates schizophrenia pathophysiology. Crit Rev Neurobiol 16, 1-23
10. Todtenkopf MS, Benes FM (1998) Distribution of glutamate decarboxylase65 immunoreactive puncta on pyramidal and nonpyramidal neurons in hippocampus of schizophrenic brain. Synapse 29, 323-332
11. Karolewicz B, Maciag D, O'Dwyer G, Stockmeier CA, Feyissa AM, Rajkowska G (2010) Reduced level of glutamic acid decarboxylase-67 kDa in the prefrontal cortex in major depression. Int J Neuropsychopharmacol 13, 411-420
12. Benes FM, Todtenkopf MS, Logiotatos P,WilliamsM(2000) Glutamate decarboxylase(65)-immunoreactive terminals in cingulate and prefrontal cortices of schizophrenic and bipolar brain. J Chem Neuroanat 20, 259-269
13. Benes FM, Lim B, Matzilevich D, Walsh JP, Subburaju S, Minns M (2007) Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc Natl Acad Sci U S A 104, 10164-10169
14. Heckers S, Stone D, Walsh J, Shick J, Koul P, Benes FM (2002) Differential hippocampal expression of glutamic acid decarboxylase 65 and 67 messenger RNA in bipolar disorder and schizophrenia. Arch Gen Psychiatry 59, 521-529
15. Yip J, Soghomonian JJ, Blatt GJ (2009) Decreased GAD65 mRNA levels in select subpopulations of neurons in the cerebellar dentate nuclei in autism: An in situ hybridization study. Autism Res 2, 50-59
16. Dracheva S, Elhakem SL, McGurk SR, Davis KL, Haroutunian V (2004) GAD67 and GAD65 mRNA and protein expression in cerebrocortical regions of elderly patients with schizophrenia. J Neurosci Res 76, 581-592
17. Sibille E, Morris HM, Kota RS, Lewis DA (2011) GABArelated transcripts in the dorsolateral prefrontal cortex inmood disorders. Int J Neuropsychopharmacol 14(6), 721-734
18. Bielau H, Steiner J, Mawrin C, Trubner K, Brisch R, Meyer-Lotz G, Brodhun M, Dobrowolny H, Baumann B, Gos T, BernsteinHG,BogertsB(2007) Dysregulation ofGABAergic neurotransmission in mood disorders: A postmortem study. Ann N Y Acad Sci 1096, 157-169
19. Mathern GW, Mendoza D, Lozada A, Pretorius JK, Dehnes Y, Danbolt NC, Nelson N, Leite JP, Chimelli L, Born DE, Sakamoto AC, Assirati JA, Fried I, Peacock WJ, Ojemann GA, Adelson PD (1999) Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy. Neurology 52, 453-472
20. Rissman RA, De Blas AL, Armstrong DM (2007) GABA(A) receptors in aging and Alzheimer's disease. J Neurochem 103, 1285-1292
21. Davies P, Anderton B, Kirsch J, Konnerth A, Nitsch R, Sheetz M (1998) First one in, last one out: The role of gabaergic transmission in generation and degeneration. Prog Neurobiol 55, 651-658
22. Lanctot KL, Herrmann N, Mazzotta P, Khan LR, Ingber N (2004) GABAergic function in Alzheimer's disease: Evidence for dysfunction and potential as a therapeutic target for the treatment of behavioural and psychological symptoms of dementia. Can J Psychiatry 49, 439-453
23. Gsell W, Jungkunz G, Riederer P (2004) Functional neurochemistry of Alzheimer's disease. Curr Pharm Des 10, 265-293
24. Yates CM, Butterworth J, Tennant MC, Gordon A (1990) Enzyme activities in relation to pH and lactate in postmortem brain in Alzheimer-Type and other dementias. J Neurochem 55, 1624-1630
25. Takahashi H, Brasnjevic I, Rutten BP, Van Der Kolk N, Perl DP, Bouras C, SteinbuschHW, Schmitz C, Hof PR, Dickstein DL (2010) Hippocampal interneuron loss in an APP/PS1 double mutant mouse and in Alzheimer's disease. Brain Struct Funct 214, 145-160
26. Hof PR, Nimchinsky EA, Celio MR, Bouras C, Morrison JH (1993) Calretinin-immunoreactive neocortical interneurons are unaffected in Alzheimer's disease. Neurosci Lett 152, 145-148
27. Koliatsos VE, Kecojevic A, Troncoso JC, Gastard MC, Bennett DA, Schneider JA (2006) Early involvement of small inhibitory cortical interneurons in Alzheimer's disease. Acta Neuropathol 112, 147-162
28. Leuba G, Kraftsik R, Saini K (1998) Quantitative distribution of parvalbumin, calretinin, and calbindin D-28k immunoreactive neurons in the visual cortex of normal and Alzheimer cases. Exp Neurol 152, 278-291
29. Mikkonen M, Alafuzoff I, Tapiola T, Soininen H, Miettinen R (1999) Subfield-And layer-specific changes in parvalbumin, calretinin and calbindin-D28K immunoreactivity in the entorhinal cortex in Alzheimer's disease. Neuroscience 92, 515-532
30. Hwang IK, Li H, Yoo KY, Choi JH, Lee CH, Chung DW, Kim DW, Seong JK, Yoon YS, Lee IS, Won MH (2008) Comparison of glutamic acid decarboxylase 67 immunoreactive neurons in the hippocampal CA1 region at various age stages in dogs. Neurosci Lett 431, 251-255
31. Shi L, Argenta AE,Winseck AK, Brunso-Bechtold JK (2004) Stereological quantification of GAD-67-immunoreactive neurons and boutons in the hippocampus of middle-Aged and old Fischer 344×Brown Norway rats. J Comp Neurol 478, 282-291
32. Stanley DP, Shetty AK (2004) Aging in the rat hippocampus is associated with widespread reductions in the number of glutamate decarboxylase-67 positive interneurons but not interneuron degeneration. J Neurochem 89, 204-216
33. Benagiano V, Flace P, Virgintino D, Rizzi A, Roncali L, Ambrosi G (2000) Immunolocalization of glutamic acid decarboxylase in postmortem human cerebellar cortex. A light microscopy study. Histochem Cell Biol 114, 191-195
34. Benagiano V, Virgintino D, Rizzi A, Flace P, Troccoli V, Bormann J, Monaghan P, Robertson D, Roncali L, Ambrosi G (2000) Glutamic acid decarboxylase-positive neuronal cell bodies and terminals in the human cerebellar cortex. Histochem J 32, 557-564
35. Montine TJ, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Dickson DW, Duyckaerts C, Frosch MP, Masliah E, Mirra SS, Nelson PT, Schneider JA, Thal DR, Trojanowski JQ, Vinters HV, Hyman BT (2012) National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease: A practical approach. Acta Neuropathol 123, 1-11
36. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82, 239-259
37. Schnell SA, Staines WA, Wessendorf MW (1999) Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47, 719-730
38. Crook J, Hendrickson A, Robinson FR (2006) Co-localization of glycine and gaba immunoreactivity in interneurons in Macaca monkey cerebellar cortex. Neuroscience 141, 1951-1959
39. Flace P, Benagiano V, Lorusso L, Girolamo F, Rizzi A, Virgintino D, Roncali L, Ambrosi G (2004) Glutamic acid decarboxylase immunoreactive large neuron types in the granular layer of the human cerebellar cortex. Anat Embryol (Berl 208, 55-64
40. Rodrigo J, Fernandez AP, Serrano J, Monzon M, Monleon E, Badiola JJ, Climent S, Martinez-Murillo R, Martinez A (2006) Distribution and expression pattern of the nitrergic system in the cerebellum of the sheep. Neuroscience 139, 889-898
41. Fukuda T, Aika Y, HeizmannCW, Kosaka T (1998) GABAergic axon terminals at perisomatic and dendritic inhibitory sites show different immunoreactivities against two GAD isoforms, GAD67 and GAD65, in the mouse hippocampus: A digitized quantitative analysis. J Comp Neurol 395, 177-194
42. Young A, SunQQ(2009) GABAergic inhibitory interneurons in the posterior piriform cortex of the GAD67-GFP mouse. Cereb Cortex 19, 3011-3029
43. Stephenson DT, Li Q, Simmons C, Connell MA, Meglasson MD,Merchant K, EmborgME (2005) Expression of GAD65 and GAD67 immunoreactivity in MPTP-Treated monkeys with or without L-DOPA administration. Neurobiol Dis 20, 347-359
44. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR (1994) Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14, 1834-1855
45. Guo Y, Kaplan IV, Cooper NG, Mower GD (1997) Expression of two forms of glutamic acid decarboxylase (GAD67 and GAD65) during postnatal development of the cat visual cortex. Brain Res Dev Brain Res 103, 127-141
46. Mower GD, Guo Y (2001) Comparison of the expression of two forms of glutamic acid decarboxylase (GAD67 and GAD65) in the visual cortex of normal and dark-reared cats. Brain Res Dev Brain Res 126, 65-74
47. Hendrickson AE, Tillakaratne NJ, Mehra RD, Esclapez M, Erickson A, Vician L, Tobin AJ (1994) Differential localization of two glutamic acid decarboxylases (GAD65 and GAD67) in adult monkey visual cortex. J Comp Neurol 343, 566-581
48. Esclapez M, Houser CR (1999) Up-regulation of GAD65 and GAD67 in remaining hippocampalGABAneurons in a model of temporal lobe epilepsy. J Comp Neurol 412, 488-505
49. Kita H, Kitai ST (1988) Glutamate decarboxylase immunoreactive neurons in rat neostriatum: Their morphological types and populations. Brain Res 447, 346-352
50. Levesque M, Wallman MJ, Parent A (2004) Striosomes are enriched in glutamic acid decarboxylase in primates. Neurosci Res 50, 29-35
51. Martin DL, Barke KE (1998) Are GAD65 and GAD67 associated with specific pools of GABA in brain? Perspect Dev Neurobiol 5, 119-129
52. Chan-Palay V, Wu JY, Palay SL (1979) Immunocytochemical localization of gamma-Aminobutyric acid transaminase at cellular and ultrastructural levels. Proc Natl Acad Sci U S A 76, 2067-2071
53. Lee M, Schwab C, McGeer PL (2010) Astrocytes are GABAergic cells that modulate microglial activity. Glia 59, 152-165
54. Sherif FM (1994) GABA-Transaminase in brain and blood platelets: Basic and clinical aspects. Prog Neuropsychopharmacol Biol Psychiatry 18, 1219-1233
55. Hwang IK, Kim DW, Yoo KY, Kim DS, Kim KS, Kang JH, Choi SY, Kim YS, Kang TC, Won MH (2004) Agerelated changes of gamma-Aminobutyric acid transaminase immunoreactivity in the hippocampus and dentate gyrus of the Mongolian gerbil. Brain Res 1017, 77-84
56. Kang TC, Park SK, Bahn JH, Chang JS, Cho SW, Choi SY, Won MH (2001) Comparative studies on the GABAtransaminase immunoreactivity in rat and gerbil brains. Mol Cells 11, 321-325
57. Lolova I, Davidoff M (1990) Immuno-And histochemical data on changed GABA transmission in aged rat cerebellum. J Hirnforsch 31, 423-428
58. Lolova I, Davidoff M (1991) Changes in GABAimmunoreactivity and GABA-Transaminase activity in rat amygdaloid complex in aging. J Hirnforsch 32, 231-238
59. Reinikainen KJ, Paljarvi L, Huuskonen M, Soininen H, Laakso M, Riekkinen PJ (1988) A post-mortem study of noradrenergic, serotonergic and GABAergic neurons in Alzheimer's disease. J Neurol Sci 84, 101-116
60. Perry EK, Gibson PH, Blessed G, Perry RH, Tomlinson BE (1977) Neurotransmitter enzyme abnormalities in senile dementia. Choline acetyltransferase and glutamic acid decar boxylase activities in necropsy brain tissue. J Neurol Sci 34, 247-265
61. Boissiere F, Faucheux B, Duyckaerts C, Hauw JJ, Agid Y, Hirsch EC (1998) Striatal expression of glutamic acid decarboxylase gene in Alzheimer's disease. J Neurochem 71, 767-774
62. Lowe SL, Francis PT, Procter AW, Palmer AM, Davison AN, Bowen DM (1988) Gamma-Aminobutyric acid concentration in brain tissue at two stages of Alzheimer's disease. Brain 111(Pt 4), 785-799
63. Rossor M, Emson P, Dawbarn D, Dockray G, Mountjoy C, RothM(1986) Postmortem studies of peptides in Alzheimer's disease and Huntington's disease. Res Publ Assoc Res Nerv Ment Dis 64, 259-277
64. Aoyagi T, Wada T, Nagai M, Kojima F, Harada S, Takeuchi T, Takahashi H, Hirokawa K, Tsumita T (1990) Increased gamma-Aminobutyrate aminotransferase activity in brain of patients with Alzheimer's disease. Chem Pharm Bull (Tokyo) 38, 1748-1749
65. Sherif F, Ahmed SS, Eriksson L (1995) Brain aminobutyrate aminotransferase activity in Alzheimer's disease. Neurodegeneration 4, 114-115
66. Marczynski TJ (1998)GABAergic deafferentation hypothesis of brain aging and Alzheimer's disease revisited. Brain Res Bull 45, 341-379
67. Burianova J, Ouda L, Profant O, Syka J (2009) Age-related changes in GAD levels in the central auditory system of the rat. Exp Gerontol 44, 161-169
68. Stanley EM, Fadel JR, Mott DD (2012) Interneuron loss reduces dendritic inhibition and GABA release in hippocampus of aged rats. Neurobiol Aging 33, 431.e1-431.e13
69. Counts SE, Nadeem M, Lad SP, Wuu J, Mufson EJ, Honer WG (2006) Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment. J Neuropathol Exp Neurol 65, 592-601
70. Honer WG (2003) Pathology of presynaptic proteins in Alzheimer's disease: More than simple loss of terminals. Neurobiol Aging 24, 1047-1062
71. Garcia-Alloza M, TsangSW, Gil-Bea FJ, Francis PT, Lai MK, Marcos B, Chen CP, Ramirez MJ (2006) Involvement of the GABAergic system in depressive symptoms of Alzheimer's disease. Neurobiol Aging 27, 1110-1117
72. Lanctot KL, Herrmann N, Rothenburg L, Eryavec G (2007) Behavioral correlates of GABAergic disruption in Alzheimer's disease. Int Psychogeriatr 19, 151-158
73. Limon A, Reyes-Ruiz JM, Miledi R (2012) Loss of functional GABA(A) receptors in the Alzheimer diseased brain. Proc Natl Acad Sci U S A 109, 10071-10076
74. Krantic S, Isorce N, Mechawar N, Davoli MA, Vignault E, Albuquerque M, Chabot JG, Moyse E, Chauvin JP, Aubert I, McLaurin J, Quirion R (2012) HippocampalGABAergic neurons are susceptible to amyloid-beta toxicity in vitro and are decreased in number in the Alzheimer's disease TgCRND8 mouse model. J Alzheimers Dis 29, 293-308
75. Tiwari V, Patel AB (2012) Impaired glutamatergic and GABAergic function at early age in AbetaPPswe-PS1dE9 mice: Implications for Alzheimer's disease. J Alzheimers Dis 28, 765-769
76. Scheff SW, Price DA, Schmitt FA, Mufson EJ (2006) Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol Aging 27, 1372-1384
77. Garcia-Marin V, Blazquez-Llorca L, Rodriguez JR, Boluda S, Muntane G, Ferrer I, Defelipe J (2009) Diminished perisomatic GABAergic terminals on cortical neurons adjacent to amyloid plaques. Front Neuroanat 3, 28
78. Bell KF, de Kort GJ, Steggerda S, Shigemoto R, Ribeiroda-Silva A, Cuello AC (2003) Structural involvement of the glutamatergic presynaptic boutons in a transgenic mouse model expressing early onset amyloid pathology. Neurosci Lett 353, 143-147
79. Adams LA, Munoz DG (1993) Differential incorporation of processes derived from different classes of neurons into senile plaques in Alzheimer's disease. Acta Neuropathol 86, 365-370
80. Bell KF, Bennett DA, Cuello AC (2007) Paradoxical upregulation of glutamatergic presynaptic boutons during mild cognitive impairment. J Neurosci 27, 10810-10817
81. Popovic M, Caballero-Bleda M, Kadish I, Van Groen T (2008) Subfield and layer-specific depletion in calbindin-D28K, calretinin and parvalbumin immunoreactivity in the dentate gyrus of amyloid precursor protein/presenilin 1 transgenic mice. Neuroscience 155, 182-191
82. Pugliese M, Carrasco JL, Geloso MC, Mascort J, Michetti F, Mahy N (2004) Gamma-Aminobutyric acidergic interneuron vulnerability to aging in canine prefrontal cortex. J Neurosci Res 77, 913-920
83. Wang AY, Lohmann KM, Yang CK, Zimmerman EI, Pantazopoulos H, Herring N, Berretta S, Heckers S, Konradi C (2011) Bipolar disorder type 1 and schizophrenia are accompanied by decreased density of parvalbumin-And somatostatin-positive interneurons in the parahippocampal region. Acta Neuropathol 122, 615-626
84. Filippini N, MacIntosh BJ, HoughMG,GoodwinGM,Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE (2009) Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci U S A 106, 7209-7214
85. Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA,Mazziotta JC, SmallGW(2000) Patterns of brain activation in people at risk for Alzheimer's disease. N Engl J Med 343, 450-456
86. Dickerson BC, Sperling RA (2009) Large-scale functional brain network abnormalities in Alzheimer's disease: Insights from functional neuroimaging. Behav Neurol 21, 63-75
87. Sperling RA, Dickerson BC, Pihlajamaki M, Vannini P, LaViolette PS,VitoloOV, Hedden T, Becker JA, Rentz DM, Selkoe DJ, JohnsonKA(2010) Functional alterations in memory networks in early Alzheimer's disease. Neuromolecular Med 12, 27-43
88. Kocharyan A, Fernandes P, Tong XK, Vaucher E, Hamel E (2008) Specific subtypes of cortical GABA interneurons contribute to the neurovascular coupling response to basal forebrain stimulation. J Cereb Blood Flow Metab 28, 221-231
89. Cauli B, Tong XK, Rancillac A, Serluca N, Lambolez B, Rossier J, Hamel E (2004) Cortical GABA interneurons in neurovascular coupling: Relays for subcortical vasoactive pathways. J Neurosci 24, 8940-8949
90. de la Torre JC (2000) Critically attained threshold of cerebral hypoperfusion: Can it cause Alzheimer's disease? Ann N Y Acad Sci 903, 424-436
91. Bhat R, Axtell R, Mitra A, Miranda M, Lock C, Tsien RW, Steinman L (2010) Inhibitory role for GABA in autoimmune inflammation. Proc Natl Acad Sci U S A 107, 2580-2585