Synapse Loss and Microglial Activation Precede Tangles in a P301S Tauopathy Mouse Model (DOI:10.1016/j.neuron.2007.01.010);Synapse Loss and Microglial Activation Precede Tangles in a P301S Tauopathy Mouse Model

Neuron

Volumn 53, Issue 3, 2007, Pages 337-351

  Yoshiyama, Yasumasa ^a,b,c   Higuchi, Makoto ^a,b,d,e   Zhang, Bin ^a,b   Huang, Shu Ming ^e   Iwata, Nobuhisa ^e   Saido, Takaomi C ^e   Maeda, Jun ^d   Suhara, Tetsuya ^d   Trojanowski, John Q ^a,b   Lee, Virginia M Y ^a,b  

^a Laboratory Medicine   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c SAKURA NATIONAL HOSPITAL   (Japan)

^d NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^e RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

HUMDISEASE; MOLNEURO

Indexed keywords

TACROLIMUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; CELL ACTIVATION; CELL LOSS; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE MODEL; HIPPOCAMPUS; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; LIFESPAN; MICROGLIA; MOUSE; NERVE CELL; NEUROFIBRILLARY TANGLE; NONHUMAN; PRIORITY JOURNAL; SYNAPSE; TAUOPATHY; WILD TYPE;

EID: 33846538660     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.03.022     Document Type: Erratum

References (62)

1. Akiyama H., Arai T., Kondo H., Tanno E., Haga C., and Ikeda K. Cell mediators of inflammation in the Alzheimer disease brain. Alzheimer Dis. Assoc. Disord. 14 suppl 1 (2000) S47-S53
2. Allen B., Ingram E., Takao M., Smith M.J., Jakes R., Virdee K., Yoshida H., Holzer M., Craxton M., Emson P.C., et al. Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J. Neurosci. 22 (2002) 9340-9351
3. Arriagada P.V., Growdon J.H., Hedley-Whyte E.T., and Hyman B.T. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42 (1992) 631-639
4. Bellucci A., Westwood A.J., Ingram E., Casamenti F., Goedert M., and Spillantini M.G. Induction of inflammatory mediators and microglial activation in mice transgenic for mutant human P301S tau protein. Am. J. Pathol. 165 (2004) 1643-1652
5. Bierer L.M., Hof P.R., Purohit D.P., Carlin L., Schmeidler J., Davis K.L., and Perl D.P. Neocortical neurofibrillary tangles correlate with dementia severity in Alzheimer's disease. Arch. Neurol. 52 (1995) 81-88
6. Bigio E.H., Vono M.B., Satumtira S., Adamson J., Sontag E., Hynan L.S., White III C.L., Baker M., and Hutton M. Cortical synapse loss in progressive supranuclear palsy. J. Neuropathol. Exp. Neurol. 60 (2001) 403-410
7. Binder L.I., Frankfurter A., and Rebhun L.I. The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101 (1985) 1371-1378
8. Borchelt D.R., Davis J., Fischer M., Lee M.K., Slunt H.H., Ratovitsky T., Regard J., Copeland N.G., Jenkins N.A., Sisodia S.S., and Price D.L. A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet. Anal. 13 (1996) 159-163
9. Bramblett G.T., Trojanowski J.Q., and Lee V.M.-Y. Regions with abundant neurofibrillary pathology in human brain exhibit a selective reduction in levels of binding-competent tau and accumulation of abnormal tau-isoforms (A68 proteins). Lab. Invest. 66 (1992) 212-222
10. Bramblett G.T., Goedert M., Jakes R., Merrick S.E., Trojanowski J.Q., and Lee V.M.-Y. Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10 (1993) 1089-1099
11. Bugiani O., Murrell J.R., Giaccone G., Hasegawa M., Ghigo G., Tabaton M., Morbin M., Primavera A., Carella F., Solaro C., et al. Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau. J. Neuropathol. Exp. Neurol. 58 (1999) 667-677
12. Bussiere T., Gold G., Kovari E., Giannakopoulos P., Bouras C., Perl D.P., Morrison J.H., and Hof P.R. Stereologic analysis of neurofibrillary tangle formation in prefrontal cortex area 9 in aging and Alzheimer's disease. Neuroscience 117 (2003) 577-592
13. Davies C.A., Mann D.M., Sumpter P.Q., and Yates P.O. A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease. J. Neurol. Sci. 78 (1987) 151-164
14. Dayanandan R., Van Slegtenhorst M., Mack T.G., Ko L., Yen S.H., Leroy K., Brion J.P., Anderton B.H., Hutton M., and Lovestone S. Mutations in tau reduce its microtubule binding properties in intact cells and affect its phosphorylation. FEBS Lett. 446 (1999) 228-232
15. D'Souza I., Poorkaj P., Hong M., Nochlin D., Lee V.M.-Y., Bird T.D., and Schellenberg G.D. Missense and silent tau gene mutations cause frontotemporal dementia with parkinsonism-chromosome 17 type, by affecting multiple alternative RNA splicing regulatory elements. Proc. Natl. Acad. Sci. USA 96 (1999) 5598-5603
16. Forman M.S., Trojanowski J.Q., and Lee V.M.-Y. Neurodegenerative diseases: A decade of discoveries paves the way for therapeutic breakthroughs. Nat. Med. 10 (2004) 1055-1063
17. Fukutani Y., Cairns N.J., Shiozawa M., Sasaki K., Sudo S., Isaki K., and Lantos P.L. Neuronal loss and neurofibrillary degeneration in the hippocampal cortex in late-onset sporadic Alzheimer's disease. Psychiatry Clin. Neurosci. 54 (2000) 523-529
18. Giasson B., Jakes R., Goedert M., Duda J.E., Leight S., Trojanowski J.Q., and Lee V.M.Y. A panel of epitope-specific antibodies detects protein domains distributed throughout human α-synuclein nitration in Lewy bodies of Parkinson's disease. J. Neurosci. Res. 59 (2000) 528-533
19. Goedert M., Jakes R., Crowther R.A., Cohen P., Vanmechelen E., Vandermeeren M., and Cras P. Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: identification of phosphorylation sites in tau protein. Biochem. J. 301 (1994) 871-877
20. Greenberg S.G., and Davies P. A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by poly-acrylamide gel electrophoresis. Proc. Natl. Acad. Sci. USA 87 (1990) 5827-5831
21. Harpin M.L., Delaere P., Javoy-Agid F., Bock E., Jacque C., Delpech B., Villarroya H., Duyckaerts C., Hauw J.J., and Baumann N. Glial fibrillary acidic protein and beta A4 protein deposits in temporal lobe of aging brain and senile dementia of the Alzheimer type: relation with the cognitive state and with quantitative studies of senile plaques and neurofibrillary tangles. J. Neurosci. Res. 27 (1990) 587-594
22. Hasegawa M., Smith M.J., and Goedert M. Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett. 437 (1998) 207-210
23. Higuchi M., Iwata N., Matsuba Y., Sato K., Sasamoto K., and Saido T.C. 19F- and 1H-MRI detection of amyloid-β plaques in vivo. Nat. Neurosci. 8 (2005) 527-533
24. Hong M., Zhukareva V., Vogelsberg-Ragaglia V., Wszolek Z., Reed L., Miller B.I., Geschwind D.H., Bird T.D., McKeel D., Goate A., et al. Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282 (1998) 1914-1917
25. Huang S.M., Mouri A., Kokubo H., Nakajima R., Suemoto T., Higuchi M., Staufenbiel M., Noda Y., Yamaguchi H., Nabeshima T., et al. Neprilysin-sensitive synapse-associated Abeta oligomers impair neuronal plasticity and cognitive function. J. Biol. Chem. 281 (2006) 17941-17951
26. Ikeda M., Shoji M., Kawarai T., Kawarabayashi T., Matsubara E., Murakami T., Sasaki A., Tomidokoro Y., Ikarashi Y., Kuribara H., et al. Accumulation of filamentous tau in the cerebral cortex of human tau R406W transgenic mice. Am. J. Pathol. 166 (2005) 521-531
27. Ishihara T., Hong M., Zhang B., Nakagawa Y., Lee M.K., Trojanowski J.Q., and Lee V.M.-Y. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 24 (1999) 751-762
28. Kitazawa M., Oddo S., Yamasaki T.R., Green K.N., and LaFerla F.M. Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J. Neurosci. 25 (2005) 8843-8853
29. Kosik K.S., Orecchio L.D., Binder L., Trojanowski J.Q., Lee V.M.-Y., and Lee G. Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1 (1988) 817-825
30. Kril J.J., Patel S., Harding A.J., and Halliday G.M. Neuron loss from the hippocampus of Alzheimer's disease exceeds extracellular neurofibrillary tangle formation. Acta Neuropathol. (Berl.) 103 (2002) 370-376
31. Lee V.M.-Y., Goedert M., and Trojanowski J.Q. Neurodegenerative tauopathies. Annu. Rev. Neurosci. 24 (2001) 1121-1159
32. Lee V.M.-Y., Kenyon T.K., and Trojanowski J.Q. Transgenic animal models of tauopathies. Biochim. Biophys. Acta 1739 (2005) 251-259
33. Li Y., Liu L., Barger S.W., and Griffin W.S. Interleukin-1 mediates pathological effects of microglia on tau phosphorylation and on synaptophysin synthesis in cortical neurons through a p38-MAPK pathway. J. Neurosci. 23 (2003) 1605-1611
34. Lipton A.M., Cullum C.M., Satumtira S., Sontag E., Hynan L.S., White III C.L., and Bigio E.H. Contribution of asymmetric synapse loss to lateralizing clinical deficits in frontotemporal dementias. Arch. Neurol. 58 (2001) 1233-1239
35. Lossor A., Reches A., Gal A., Newman J.P., Soffer D., Gomori J.M., Boher M., Ekstein D., Biran I., Meiner Z., et al. Frontotemporal dementia and parkinsonism with the P301S tau gene mutation in a Jewish family. J. Neurol. 250 (2003) 733-740
36. Maeda J., Suhara T., Zhang M.R., Okauchi T., Yasuno F., Ikoma Y., Inaji M., Nagai Y., Takano A., Obayashi S., and Suzuki K. Novel peripheral benzodiazepine receptor ligand [11C]DAA1106 for PET: an imaging tool for glial cells in the brain. Synapse. 52 (2004) 283-291
37. Masliah E. Altered expression of synaptic proteins occures early during progression of Alzheimer's disease. Neurology 56 (2001) 127-129
38. Mawal-Dewan M., Henley J., Van de Voorde A., Trojanowski J.Q., and Lee V.M.-Y. The phosphorylation state of tau in the developing rat brain is regulated by phosphoprotein phosphatases. J. Biol. Chem. 269 (1994) 30981-30987
39. Morris H.R., Khan M.N., Janssen J.C., Brown J.M., Perez-Tur J., Baker M., Ozansoy M., Hardy J., Hutton M., Wood N.W., et al. The genetic and pathological classification of familial frontotemporal dementia. Arch. Neurol. 58 (2001) 1813-1816
40. Muramori F., Kobayashi K., and Nakamura I. A quantitative study of neurofibrillary tangles, senile plaques and astrocytes in the hippocampal subdivisions and entorhinal cortex in Alzheimer's disease, normal controls and non-Alzheimer neuropsychiatric diseases. Psychiatry Clin. Neurosci. 52 (1998) 593-599
41. Murrell J.R., Spillantini M.G., Zolo P., Guazzelli M., Smith M.J., Hasegawa M., Redi F., Crowther R.A., Pietrini P., Ghetti B., and Goedert M. Tau gene mutation G389R causes a tauopathy with abundant pick body-like inclusions and axonal deposits. J. Neuropathol. Exp. Neurol. 58 (1999) 1207-1226
42. Price J.L., Ko A.I., Wade M.J., Tsou S.K., McKeel D.W., and Morris J.C. Neuron number in the entorhinal cortex and CA1 in preclinical Alzheimer disease. Arch. Neurol. 58 (2001) 1395-1402
43. Ramsden M., Kotilinek L., Forster C., Paulson J., McGowan E., SantaCruz K., Guimaraes A., Yue M., Lewis J., Carlson G., et al. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J. Neurosci. 25 (2005) 10637-10647
44. Rizzini C., Goedert M., Hodges J.R., Smith M.J., Jakes R., Hills R., Xuereb J.H., Crowther R.A., and Spillantini M.G. Tau gene mutation K257T causes a tauopathy similar to Pick's disease. J. Neuropathol. Exp. Neurol. 59 (2000) 990-1001
45. Rizzu P., Van Swieten J.C., Joosse M., Hasegawa M., Stevens M., Tibben A., Niermeijer M.F., Hillebrand M., Ravid R., Oostra B.A., et al. High prevalence of mutations in the microtubule-associated protein tau in a population study of frontotemporal dementia in the Netherlands. Am. J. Hum. Genet. 64 (1999) 414-421
46. Rodriguez E.M., Yulis R., Peruzzo B., Alvial G., and Andrade R. Standardization of various applications of methacrylate embedding and silver methenamine for light and electron microscopy immunocytochemistry. Histochemistry 81 (1984) 253-263
47. Roy S., Zhang B., Lee V.M.-Y., and Trojanowski J.Q. Axonal transport defects: A common theme in neurodegenerative diseases. Acta Neuropathol. (Berl.) 109 (2005) 5-13
48. Santacruz K., Lewis J., Spires T., Paulson J., Kotilinek L., Ingelsson M., Guimaraes A., DeTure M., Ramsden M., McGowan E., et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 309 (2005) 476-481
49. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 298 (2002) 789-791
50. Sperfeld A.D., Collatz M.B., Baier H., Palmbach M., Storch A., Schwarz J., Tatsch K., Reske S., Joosse M., Heutink P., and Ludolph A.C. FTDP-17: an early-onset phenotype with parkinsonism and epileptic seizures caused by a novel mutation. Ann. Neurol. 46 (1999) 708-715
51. Su J.H., Deng G., and Cotman C.W. Transneuronal degeneration in the spread of Alzheimer's disease pathology: immunohistochemical evidence for the transmission of tau hyperphosphorylation. Neurobiol. Dis. 4 (1997) 365-375
52. Suzuki M., Desmond T.J., Albin R.L., and Frey K.A. Cholinergic vesicular transporters in progressive supranuclear palsy. Neurology 58 (2002) 1013-1018
53. Takeuchi H., Mizuno T., Zhang G., Wang J., Kawanokuchi J., Kuno R., and Suzumura A. Neuritic beading induced by activated microglia is an early feature of neuronal dysfunction toward neuronal death by inhibition of mitochondrial respiration and axonal transport. J. Biol. Chem. 280 (2005) 10444-10454
54. Terry R.D. Physical basis of cognitive alternations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30 (1991) 572-580
55. Togo T., and Dickson D.W. Tau accumulation in astrocytes in progressive supranuclear palsy in a degenerative rather than a reactive process. Acta Neuropathol. (Berl.) 104 (2002) 398-402
56. Tu P.H., Elder G., Lazzarini R.A., Nelson D., Trojanowski J.Q., and Lee V.M.-Y. Overexpression of the human NFM subunit in transgenic mice modifies the level of endogenous NFL and the phosphorylation state of NFH subunits. J. Cell Biol. 129 (1995) 1629-1640
57. Werber E., Klein C., Grunfeld J., and Rabey J.M. Phenotypic presentation of frontotemporal dementia with Parkinsonism-chromosome 17 type P301S in a patient of Jewish-Algerian origin. Mov. Disord. 18 (2003) 595-598
58. Yasuda M., Yokoyama K., Nakayasu T., Nishimura Y., Matsui M., Yokoyama T., Miyoshi K., and Tanaka C. A Japanese patient with frontotemporal dementia and parkinsonism by a tau P301S mutation. Neurology 55 (2000) 1224-1227
59. Yoshiyama Y., Arai K., Oki T., and Hattori T. Expression of invariant chain and pro-cathepsin L in Alzheimer's brain. Neurosci. Lett. 290 (2000) 125-128
60. Zhang B., Higuchi M., Yoshiyama Y., Ishihara T., Forman M.S., Martinez D., Joyce S., Trojanowski J.Q., and Lee V.M.-Y. Retarded axonal transport of R406W mutant tau in transgenic mice with a neurodegenerative tauopathy. J. Neurosci. 24 (2004) 4657-4667
61. Zhang B., Maiti A., Shively S., Lakhani F., McDonald-Jones G., Bruce J., Lee E.B., Xie S.X., Joyce S., Li C., et al. Microtubule binding drugs offset tau sequestration by stabilizing microtubules and reversing fast axonal transport deficits in a murine neurodegenerative tauopathy model. Proc. Natl. Acad. Sci. USA 102 (2005) 227-231
62. Zhang M.R., Kida T., Noguchi J., Furutsuka K., Maeda J., Suhara T., and Suzuki K. [11C]DAA1106: radiosynthesis and in vivo binding to peripheral benzodiazepine receptors in mouse brain. Nucl. Med. Biol. 30 (2003) 513-519