The Tau/A152T mutation, a risk factor for frontotemporal-spectrum disorders, leads to NR2B receptor-mediated excitotoxicity

EMBO Reports

Volumn 17, Issue 4, 2016, Pages 552-569

  Decker, Jochen Martin ^a   Krüger, Lars ^a   Sydow, Astrid ^a,b   Dennissen, Frank Ja ^a   Siskova, Zuzana ^a   Mandelkow, Eckhard ^a,b,c   Mandelkow, Eva Maria ^a,b,c  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^c CENTER OF ADVANCED EUROPEAN STUDIES AND RESEARCH CAESAR   (Germany)

Author keywords

CA3; excitotoxicity; frontotemporal spectrum disorders; NR2B; Tau

Indexed keywords

CALCIUM; CEFTRIAXONE; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEUROTRANSMITTER; TAU PROTEIN; VOLTAGE GATED SODIUM CHANNEL; CULTURE MEDIUM; NR2B NMDA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CONTROLLED STUDY; CORTICOBASAL DEGENERATION; EXCITOTOXICITY; FEMALE; FRONTOTEMPORAL DEMENTIA; HIPPOCAMPAL SLICE; MALE; MEMBRANE DEPOLARIZATION; MOSSY FIBER; MOUSE; NERVE CELL DEGENERATION; NERVE CELL PLASTICITY; NEUROTOXICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RISK FACTOR; SYNAPTIC TRANSMISSION; ANIMAL; CHEMISTRY; CULTURE MEDIUM; DISEASE MODEL; GENETICS; HIPPOCAMPAL CA3 REGION; HUMAN; METABOLISM; MUTATION; NERVE CELL; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PATHOPHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CA3 REGION, HIPPOCAMPAL; CALCIUM; CULTURE MEDIA; DISEASE MODELS, ANIMAL; FRONTOTEMPORAL DEMENTIA; GLUTAMIC ACID; HUMANS; MICE; MICE, TRANSGENIC; MUTATION; NEURONAL PLASTICITY; NEURONS; ORGAN CULTURE TECHNIQUES; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; TAU PROTEINS;

EID: 84959525235     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201541439     Document Type: Article

References (74)

1. Goedert M, Crowther RA, Spillantini MG, (1998) Tau mutations cause frontotemporal dementias. Neuron 21: 955-958
2. Barghorn S, Zheng-Fischhofer Q, Ackmann M, Biernat J, von Bergen M, Mandelkow EM, Mandelkow E, (2000) Structure, microtubule interactions, and paired helical filament aggregation by tau mutants of frontotemporal dementias. Biochemistry 39: 11714-11721
3. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, Miller BI, Geschwind DH, Bird TD, McKeel D, Goate A, et al, (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282: 1914-1917
4. Kovacs GG, Molnar K, Laszlo L, Strobel T, Botond G, Honigschnabl S, Reiner-Concin A, Palkovits M, Fischer P, Budka H, (2011) A peculiar constellation of tau pathology defines a subset of dementia in the elderly. Acta Neuropathol 122: 205-222
5. Kara E, Ling H, Pittman AM, Shaw K, de Silva R, Simone R, Holton JL, Warren JD, Rohrer JD, Xiromerisiou G, et al, (2012) The MAPT p.A152T variant is a risk factor associated with tauopathies with atypical clinical and neuropathological features. Neurobiol Aging 33: 2231 e7-2231 e14
6. Lee SE, Tartaglia MC, Yener G, Genc S, Seeley WW, Sanchez-Juan P, Moreno F, Mendez MF, Klein E, Rademakers R, et al, (2013) Neurodegenerative disease phenotypes in carriers of MAPT p. A152T, a risk factor for frontotemporal dementia spectrum disorders and Alzheimer disease. Alzheimer Dis Assoc Disord 27: 302-309
7. Coppola G, Chinnathambi S, Lee JJ, Dombroski BA, Baker MC, Soto-Ortolaza AI, Lee SE, Klein E, Huang AY, Sears R, et al, (2012) Evidence for a role of the rare p. A152T variant in MAPT in increasing the risk for FTD-spectrum and Alzheimer's diseases. Hum Mol Genet 21: 3500-3512
8. Binder LI, Frankfurter A, Rebhun LI, (1985) The distribution of tau in the mammalian central nervous system. J Cell Biol 101: 1371-1378
9. Brion JP, Guilleminot J, Couchie D, Flament-Durand J, Nunez J, (1988) Both adult and juvenile tau microtubule-associated proteins are axon specific in the developing and adult rat cerebellum. Neuroscience 25: 139-146
10. Gotz J, Ittner LM, Kins S, (2006) Do axonal defects in tau and amyloid precursor protein transgenic animals model axonopathy in Alzheimer's disease? J Neurochem 98: 993-1006
11. Thies E, Mandelkow EM, (2007) Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J Neurosci 27: 2896-2907
12. Hoover BR, Reed MN, Su J, Penrod RD, Kotilinek LA, Grant MK, Pitstick R, Carlson GA, Lanier LM, Yuan LL, et al, (2010) Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron 68: 1067-1081
13. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, Wolfing H, Chieng BC, Christie MJ, Napier IA, et al, (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 142: 387-397
14. Polydoro M, Dzhala VI, Pooler AM, Nicholls SB, McKinney AP, Sanchez L, Pitstick R, Carlson GA, Staley KJ, Spires-Jones TL, et al, (2014) Soluble pathological tau in the entorhinal cortex leads to presynaptic deficits in an early Alzheimer's disease model. Acta Neuropathol 127: 257-270
15. 2+ dysregulation. Acta Neuropathol Commun 3: 23
16. Messing L, Decker JM, Joseph M, Mandelkow E, Mandelkow EM, (2013) Cascade of tau toxicity in inducible hippocampal brain slices and prevention by aggregation inhibitors. Neurobiol Aging 34: 1343-1354
17. Zempel H, Thies E, Mandelkow E, Mandelkow EM, (2010) Abeta oligomers cause localized Ca(2+) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J Neurosci 30: 11938-11950
18. Morris M, Maeda S, Vossel K, Mucke L, (2011) The many faces of tau. Neuron 70: 410-426
19. Vossel KA, Xu JC, Fomenko V, Miyamoto T, Suberbielle E, Knox JA, Ho K, Kim DH, Yu GQ, Mucke L, (2015) Tau reduction prevents Abeta-induced axonal transport deficits by blocking activation of GSK3beta. J Cell Biol 209: 419-433
20. Roberson ED, Halabisky B, Yoo JW, Yao J, Chin J, Yan F, Wu T, Hamto P, Devidze N, Yu GQ, et al, (2011) Amyloid-beta/Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease. J Neurosci 31: 700-711
21. Holth JK, Bomben VC, Reed JG, Inoue T, Younkin L, Younkin SG, Pautler RG, Botas J, Noebels JL, (2013) Tau loss attenuates neuronal network hyperexcitability in mouse and Drosophila genetic models of epilepsy. J Neurosci 33: 1651-1659
22. Hauw JJ, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL, McKee A, Tabaton M, Litvan I, (1994) Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 44: 2015-2019
23. Amadoro G, Ciotti MT, Costanzi M, Cestari V, Calissano P, Canu N, (2006) NMDA receptor mediates tau-induced neurotoxicity by calpain and ERK/MAPK activation. Proc Natl Acad Sci USA 103: 2892-2897
24. Nilsen LH, Rae C, Ittner LM, Gotz J, Sonnewald U, (2013) Glutamate metabolism is impaired in transgenic mice with tau hyperphosphorylation. J Cereb Blood Flow Metab 33: 684-691
25. Hunsberger HC, Rudy CC, Batten SR, Gerhardt GA, Reed MN, (2015) P301L tau expression affects glutamate release and clearance in the hippocampal trisynaptic pathway. J Neurochem 132: 169-182
26. Nygaard TG, Duvoisin RC, Manocha M, Chokroverty S, (1989) Seizures in progressive supranuclear palsy. Neurology 39: 138-140
27. Maeda S, Djukic B, Taneja P, Yu G, Lo I, Davis A, Craft R, Guo W, Wang X, Kim D, et al, (2016) Expression of A152T human tau causes age-dependent neuronal dysfunction and loss in transgenic mice. EMBO Rep 17: 530-551
28. Bouabe H, Okkenhaug K, (2013) A protocol for construction of gene targeting vectors and generation of homologous recombinant embryonic stem cells. Methods Mol Biol 1064: 337-354
29. Mocanu MM, Nissen A, Eckermann K, Khlistunova I, Biernat J, Drexler D, Petrova O, Schonig K, Bujard H, Mandelkow E, et al, (2008) 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 28: 737-748
30. Siskova Z, Justus D, Kaneko H, Friedrichs D, Henneberg N, Beutel T, Pitsch J, Schoch S, Becker A, von der Kammer H, et al, (2014) Dendritic structural degeneration is functionally linked to cellular hyperexcitability in a mouse model of Alzheimer's disease. Neuron 84: 1023-1033
31. Foster KA, McLaughlin N, Edbauer D, Phillips M, Bolton A, Constantine-Paton M, Sheng M, (2010) Distinct roles of NR2A and NR2B cytoplasmic tails in long-term potentiation. J Neurosci 30: 2676-2685
32. Barria A, Malinow R, (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35: 345-353
33. Barria A, Malinow R, (2005) NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48: 289-301
34. Korinek M, Kapras V, Vyklicky V, Adamusova E, Borovska J, Vales K, Stuchlik A, Horak M, Chodounska H, Vyklicky L Jr, (2011) Neurosteroid modulation of N-methyl-D-aspartate receptors: molecular mechanism and behavioral effects. Steroids 76: 1409-1418
35. Xia P, Chen HS, Zhang D, Lipton SA, (2010) Memantine preferentially blocks extrasynaptic over synaptic NMDA receptor currents in hippocampal autapses. J Neurosci 30: 11246-11250
36. Cull-Candy SG, Leszkiewicz DN, (2004) Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004: re16
37. Cull-Candy S, Brickley S, Farrant M, (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11: 327-335
38. Hardingham GE, Bading H, (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11: 682-696
39. Paoletti P, Bellone C, Zhou Q, (2013) NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci 14: 383-400
40. Parsons MP, Raymond LA, (2014) Extrasynaptic NMDA receptor involvement in central nervous system disorders. Neuron 82: 279-293
41. Talantova M, Sanz-Blasco S, Zhang X, Xia P, Akhtar MW, Okamoto S, Dziewczapolski G, Nakamura T, Cao G, Pratt AE, et al, (2013) Abeta induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. Proc Natl Acad Sci USA 110: E2518-E2527
42. Hara MR, Snyder SH, (2007) Cell signaling and neuronal death. Annu Rev Pharmacol Toxicol 47: 117-141
43. Mantamadiotis T, Lemberger T, Bleckmann SC, Kern H, Kretz O, Martin Villalba A, Tronche F, Kellendonk C, Gau D, Kapfhammer J, et al, (2002) Disruption of CREB function in brain leads to neurodegeneration. Nat Genet 31: 47-54
44. Barco A, Bailey CH, Kandel ER, (2006) Common molecular mechanisms in explicit and implicit memory. J Neurochem 97: 1520-1533
45. Yuste R, Bonhoeffer T, (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24: 1071-1089
46. Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R, (2014) Engineering a memory with LTD and LTP. Nature 511: 348-352
47. Rothstein JD, Patel S, Regan MR, Haenggeli C, Huang YH, Bergles DE, Jin L, Dykes Hoberg M, Vidensky S, Chung DS, et al, (2005) Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 433: 73-77
48. Morgan JI, Cohen DR, Hempstead JL, Curran T, (1987) Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237: 192-197
49. Ronesi JA, Collins KA, Hays SA, Tsai NP, Guo W, Birnbaum SG, Hu JH, Worley PF, Gibson JR, Huber KM, (2012) Disrupted Homer scaffolds mediate abnormal mGluR5 function in a mouse model of fragile X syndrome. Nat Neurosci 15: 431-440, S1
50. Tang AH, Alger BE, (2015) Homer protein-metabotropic glutamate receptor binding regulates endocannabinoid signaling and affects hyperexcitability in a mouse model of fragile X syndrome. J Neurosci 35: 3938-3945
51. Danbolt NC, (2001) Glutamate uptake. Prog Neurobiol 65: 1-105
52. Moddel G, Jacobson B, Ying Z, Janigro D, Bingaman W, Gonzalez-Martinez J, Kellinghaus C, Prayson RA, Najm IM, (2005) The NMDA receptor NR2B subunit contributes to epileptogenesis in human cortical dysplasia. Brain Res 1046: 10-23
53. Li Z, Hall AM, Kelinske M, Roberson ED, (2014) Seizure resistance without parkinsonism in aged mice after tau reduction. Neurobiol Aging 35: 2617-2624
54. Xu CS, Liu AC, Chen J, Pan ZY, Wan Q, Li ZQ, Wang ZF, (2015) Overactivation of NR2B-containing NMDA receptors through entorhinal-hippocampal connection initiates accumulation of hyperphosphorylated tau in rat hippocampus after transient middle cerebral artery occlusion (MCAO). J Neurochem 134: 566-577
55. Van der Jeugd A, Hochgrafe K, Ahmed T, Decker JM, Sydow A, Hofmann A, Wu D, Messing L, Balschun D, D'Hooge R, et al, (2012) Cognitive defects are reversible in inducible mice expressing pro-aggregant full-length human Tau. Acta Neuropathol 123: 787-805
56. Sydow A, Van der Jeugd A, Zheng F, Ahmed T, Balschun D, Petrova O, Drexler D, Zhou L, Rune G, Mandelkow E, et al, (2011) Tau-induced defects in synaptic plasticity, learning, and memory are reversible in transgenic mice after switching off the toxic Tau mutant. J Neurosci 31: 2511-2525
57. Furukawa K, Wang Y, Yao PJ, Fu W, Mattson MP, Itoyama Y, Onodera H, D'Souza I, Poorkaj PH, Bird TD, et al, (2003) Alteration in calcium channel properties is responsible for the neurotoxic action of a familial frontotemporal dementia tau mutation. J Neurochem 87: 427-436
58. Vossel KA, Beagle AJ, Rabinovici GD, Shu H, Lee SE, Naasan G, Hegde M, Cornes SB, Henry ML, Nelson AB, et al, (2013) Seizures and epileptiform activity in the early stages of Alzheimer disease. JAMA Neurol 70: 1158-1166
59. Ruan YW, Lei Z, Fan Y, Zou B, Xu ZC, (2009) Diversity and fluctuation of spine morphology in CA1 pyramidal neurons after transient global ischemia. J Neurosci Res 87: 61-68
60. 2+ exchanger in excitotoxicity. Cell 120: 275-285
61. Fong H, Wang C, Knoferle J, Walker D, Balestra ME, Tong LM, Leung L, Ring KL, Seeley WW, Karydas A, et al, (2013) Genetic correction of tauopathy phenotypes in neurons derived from human induced pluripotent stem cells. Stem Cell Reports 1: 226-234
62. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, Wu T, Gerstein H, Yu GQ, Mucke L, (2007) Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 316: 750-754
63. 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
64. 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
65. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA, (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35: W71-W74
66. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F, (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034
67. Ramakers C, Ruijter JM, Deprez RH, Moorman AF, (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66
68. Braak H, Braak E, (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239-259
69. Siskova Z, Page A, O'Connor V, Perry VH, (2009) Degenerating synaptic boutons in prion disease: microglia activation without synaptic stripping. Am J Pathol 175: 1610-1621
70. Glaser EM, Van der Loos H, (1981) Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J Neurosci Methods 4: 117-125
71. Ricobaraza A, Cuadrado-Tejedor M, Marco S, Perez-Otano I, Garcia-Osta A, (2012) Phenylbutyrate rescues dendritic spine loss associated with memory deficits in a mouse model of Alzheimer disease. Hippocampus 22: 1040-1050
72. Stoppini L, Buchs PA, Muller D, (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37: 173-182
73. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450
74. Behrens CJ, van den Boom LP, de Hoz L, Friedman A, Heinemann U, (2005) Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks. Nat Neurosci 8: 1560-1567