Tau pathology induces loss of GABAergic interneurons leading to altered synaptic plasticity and behavioral impairments

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Levenga, Josien ^a   Krishnamurthy, Pavan ^a   Rajamohamedsait, Hameetha ^a   Wong, Helen ^a   Franke, Thomas F ^a   Cain, Peter ^b   Sigurdsson, Einar M ^a   Hoeffer, Charles A ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EXCELSIOR COLLEGE   (United States)

Author keywords

Behavior; GABAergic interneurons; Hippocampus; P301L; Synaptic plasticity; Tau

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; MAPT PROTEIN, HUMAN; PYRIDINE DERIVATIVE; TAU PROTEIN; ZOLPIDEM;

ANIMAL; BRAIN CORTEX; C57BL MOUSE; CELL COUNT; DISEASE MODEL; DRUG EFFECTS; GENETICS; HIPPOCAMPUS; HUMAN; INTERNEURON; LONG TERM POTENTIATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SENSORY GATING; TAUOPATHIES; TRANSGENIC MOUSE;

ANIMALS; CELL COUNT; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; GABA-A RECEPTOR AGONISTS; GABAERGIC NEURONS; HIPPOCAMPUS; HUMANS; INTERNEURONS; LONG-TERM POTENTIATION; MICE, INBRED C57BL; MICE, TRANSGENIC; PYRIDINES; SENSORY GATING; TAU PROTEINS; TAUOPATHIES;

EID: 85048233747     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-1-34     Document Type: Article

References (59)

1. Lee G, Cowan N, Kirschner M: The primary structure and heterogeneity of tau protein from mouse brain. Science 1988,239(4837):285-288. 10.1126/science.3122323
2. Hirokawa N, et al.: Selective stabilization of tau in axons and microtubule-associated protein 2C in cell bodies and dendrites contributes to polarized localization of cytoskeletal proteins in mature neurons. J Cell Biol 1996,132(4):667-679. 10.1083/jcb.132.4.667
3. Aronov S, et al.: Axonal tau mRNA localization coincides with tau protein in living neuronal cells and depends on axonal targeting signal. J Neurosci 2001,21(17):6577-6587.
4. Ittner LM, et al.: Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010,142(3):387-397. 10.1016/j.cell.2010.06.036
5. Johnson GV, Stoothoff WH: Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 2004,117(Pt 24):5721-5729.
6. Spires TL, et al.: Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am J Pathol 2006,168(5):1598-1607. 10.2353/ajpath.2006.050840
7. Revett TJ, et al.: Glutamate system, amyloid ss peptides and tau protein: functional interrelationships and relevance to Alzheimer disease pathology. J Psychiatry Neurosci 2012,37(5):110190.
8. Neary D, Snowden J, Mann D: Frontotemporal dementia. Lancet Neurol 2005,4(11):771-780. 10.1016/S1474-4422(05)70223-4
9. Nalbantoglu J, et al.: Impaired learning and LTP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature 1997,387(6632):500-505. 10.1038/387500a0
10. Oddo S, et al.: Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003,39(3):409-421. 10.1016/S0896-6273(03)00434-3
11. Trinchese F, et al.: Progressive age-related development of Alzheimer-like pathology in APP/PS1 mice. Ann Neurol 2004,55(6):801-814. 10.1002/ana.20101
12. Shankar GM, et al.: Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 2008,14(8):837-842. 10.1038/nm1782
13. Walsh DM, et al.: Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002,416(6880):535-539. 10.1038/416535a
14. Roberson ED, et al.: Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 2007,316(5825):750-754. 10.1126/science.1141736
15. Andrews-Zwilling Y, et al.: Apolipoprotein E4 causes age- and Tau-dependent impairment of GABAergic interneurons, leading to learning and memory deficits in mice. J Neurosci 2010,30(41):13707-13717. 10.1523/JNEUROSCI.4040-10.2010
16. Shipton OA, et al.: Tau protein is required for amyloid (beta)-induced impairment of hippocampal long-term potentiation. J Neurosci 2011,31(5):1688-1692. 10.1523/JNEUROSCI.2610-10.2011
17. Boekhoorn K, et al.: Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy. J Neurosci 2006,26(13):3514-3523. 10.1523/JNEUROSCI.5425-05.2006
18. Rosenmann H, et al.: A novel transgenic mouse expressing double mutant tau driven by its natural promoter exhibits tauopathy characteristics. Exp Neurol 2008,212(1):71-84. 10.1016/j.expneurol.2008.03.007
19. Van der Jeugd A, et al.: Cognitive defects are reversible in inducible mice expressing pro-aggregant full-length human Tau. Acta Neuropathol 2012,123(6):787-805. 10.1007/s00401-012-0987-3
20. Amatniek JC, et al.: Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 2006,47(5):867-872. 10.1111/j.1528-1167.2006.00554.x
21. Snider BJ, et al.: Novel presenilin 1 mutation (S170F) causing Alzheimer disease with Lewy bodies in the third decade of life. Arch Neurol 2005,62(12):1821-1830. 10.1001/archneur.62.12.1821
22. Palop JJ, Mucke L: Epilepsy and cognitive impairments in Alzheimer disease. Arch Neurol 2009,66(4):435-440.
23. Buckner RL, et al.: Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J Neurosci 2005,25(34):7709-7717. 10.1523/JNEUROSCI.2177-05.2005
24. Sperling RA, et al.: Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 2009,63(2):178-188. 10.1016/j.neuron.2009.07.003
25. Crimins JL, Rocher AB, Luebke JI: Electrophysiological changes precede morphological changes to frontal cortical pyramidal neurons in the rTg4510 mouse model of progressive tauopathy. Acta Neuropathol 2012,124(6):777-795. 10.1007/s00401-012-1038-9
26. Fritschy JM: Epilepsy, E/I Balance and GABA(A) Receptor Plasticity. Front Mol Neurosci 2008, 1: 5.
27. Lydiard RB: The role of GABA in anxiety disorders. J Clin Psychiatry 2003,64(Suppl 3):21-27.
28. Luscher B, Shen Q, Sahir N: The GABAergic deficit hypothesis of major depressive disorder. Mol Psychiatry 2011,16(4):383-406. 10.1038/mp.2010.120
29. Bareggi SR, et al.: Decreased CSF concentrations of homovanillic acid and gamma-aminobutyric acid in Alzheimer's disease. Age- or disease-related modifications? Arch Neurol 1982,39(11):709-712. 10.1001/archneur.1982.00510230035010
30. Limon A, Reyes-Ruiz JM, Miledi R: Loss of functional GABA(A) receptors in the Alzheimer diseased brain. Proc Natl Acad Sci U S A 2012,109(25):10071-10076. 10.1073/pnas.1204606109
31. Greenberg SG, Davies P: A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci U S A 1990,87(15):5827-5831. 10.1073/pnas.87.15.5827
32. Noble W, et al.: Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 2003,38(4):555-565. 10.1016/S0896-6273(03)00259-9
33. Julien C, Bretteville A, Planel E: Biochemical isolation of insoluble tau in transgenic mouse models of tauopathies. Methods Mol Biol 2012, 849: 473-491. 10.1007/978-1-61779-551-0_32
34. Carney RS, et al.: Differential regulation of telencephalic pallial-subpallial boundary patterning by Pax6 and Gsh2. Cereb Cortex 2009,19(4):745-759.
35. Suvrathan A, et al.: Characterization and reversal of synaptic defects in the amygdala in a mouse model of fragile X syndrome. Proc Natl Acad Sci U S A 2010,107(25):11591-11596. 10.1073/pnas.1002262107
36. Lewis J, et al.: Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 2000,25(4):402-405. 10.1038/78078
37. Shao CY, et al.: Postsynaptic degeneration as revealed by PSD-95 reduction occurs after advanced Abeta and tau pathology in transgenic mouse models of Alzheimer's disease. Acta Neuropathol 2011,122(3):285-292. 10.1007/s00401-011-0843-x
38. Higashima M, Kinoshita H, Koshino Y: Differences in the effects of zolpidem and diazepam on recurrent inhibition and long-term potentiation in rat hippocampal slices. Neurosci Lett 1998,245(2):77-80. 10.1016/S0304-3940(98)00178-5
39. Esclapez M, Houser CR: Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy. J Comp Neurol 1999,412(3):488-505. 10.1002/(SICI)1096-9861(19990927)412:3<488::AID-CNE8>3.0.CO;2-6
40. Stone DJ, Walsh J, Benes FM: Localization of cells preferentially expressing GAD(67) with negligible GAD(65) transcripts in the rat hippocampus. A double in situ hybridization study. Brain Res Mol Brain Res 1999,71(2):201-209. 10.1016/S0169-328X(99)00185-0
41. Klausberger T, Somogyi P: Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008,321(5885):53-57. 10.1126/science.1149381
42. Tricoire L, et al.: A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J Neurosci 2011,31(30):10948-10970. 10.1523/JNEUROSCI.0323-11.2011
43. Bast T, Zhang WN, Feldon J: Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABA(A) receptor antagonist picrotoxin. Psychopharmacology (Berl) 2001,156(2-3):225-233.
44. Bolmont T, et al.: Induction of tau pathology by intracerebral infusion of amyloid-beta -containing brain extract and by amyloid-beta deposition in APP x Tau transgenic mice. Am J Pathol 2007,171(6):2012-2020. 10.2353/ajpath.2007.070403
45. Mocanu MM, et al.: The potential for beta-structure in the repeat domain of tau protein determines aggregation, synaptic decay, neuronal loss, and coassembly with endogenous Tau in inducible mouse models of tauopathy. J Neurosci 2008,28(3):737-748. 10.1523/JNEUROSCI.2824-07.2008
46. Verret L, et al.: Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 2012,149(3):708-721. 10.1016/j.cell.2012.02.046
47. Loreth D, et al.: Selective degeneration of septal and hippocampal GABAergic neurons in a mouse model of amyloidosis and tauopathy. Neurobiol Dis 2012,47(1):1-12. 10.1016/j.nbd.2012.03.011
48. Li G, et al.: GABAergic interneuron dysfunction impairs hippocampal neurogenesis in adult apolipoprotein E4 knockin mice. Cell Stem Cell 2009,5(6):634-645. 10.1016/j.stem.2009.10.015
49. Kaksonen M, et al.: Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory. Mol Cell Neurosci 2002,21(1):158-172. 10.1006/mcne.2002.1167
50. Uetani N, et al.: Impaired learning with enhanced hippocampal long-term potentiation in PTPdelta-deficient mice. EMBO J 2000,19(12):2775-2785. 10.1093/emboj/19.12.2775
51. Gerlai R, et al.: Multiple behavioral anomalies in GluR2 mutant mice exhibiting enhanced LTP. Behav Brain Res 1998,95(1):37-45. 10.1016/S0166-4328(98)00002-3
52. Bast T, Feldon J: Hippocampal modulation of sensorimotor processes. Prog Neurobiol 2003,70(4):319-345. 10.1016/S0301-0082(03)00112-6
53. Boy J, et al.: Expression mapping of tetracycline-responsive prion protein promoter: digital atlasing for generating cell-specific disease models. Neuroimage 2006,33(2):449-462. 10.1016/j.neuroimage.2006.05.055
54. Rissman RA, Mobley WC: Implications for treatment: GABAA receptors in aging, Down syndrome and Alzheimer's disease. J Neurochem 2011,117(4):613-622.
55. Rubio SE, et al.: Accelerated aging of the GABAergic septohippocampal pathway and decreased hippocampal rhythms in a mouse model of Alzheimer's disease. FASEB J 2012,26(11):4458-4467. 10.1096/fj.12-208413
56. Mendez MF, et al.: Seizures in Alzheimer's disease: clinicopathologic study. J Geriatr Psychiatry Neurol 1994,7(4):230-233.
57. Larner AJ, Doran M: Clinical phenotypic heterogeneity of Alzheimer's disease associated with mutations of the presenilin-1 gene. J Neurol 2006,253(2):139-158. 10.1007/s00415-005-0019-5
58. Sydow A, et al.: Tau-induced defects in synaptic plasticity, learning, and memory are reversible in transgenic mice after switching off the toxic Tau mutant. J Neurosci 2011,31(7):2511-2525. 10.1523/JNEUROSCI.5245-10.2011
59. Makhina T, et al.: Extracellular GAPDH binds to L1 and enhances neurite outgrowth. Mol Cell Neurosci 2009,41(2):206-218. 10.1016/j.mcn.2009.02.010