Accelerated neurodegeneration and neuroinflammation in transgenic mice expressing P301L tau mutant and tau-tubulin kinase 1

American Journal of Pathology

Volumn 184, Issue 3, 2014, Pages 808-818

  Asai, Hirohide ^a   Ikezu, Seiko ^a   Woodbury, Maya E ^a   Yonemoto, Grant M S ^a   Cui, Libin ^a   Ikezu, Tsuneya ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAPT PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; TAU PROTEIN; TAU-TUBULIN KINASE;

ANIMAL; DISEASE MODEL; FRONTOTEMPORAL DEMENTIA; GENETICS; METABOLISM; MOUSE; MUTATION; NERVE CELL; NERVE DEGENERATION; PATHOLOGY; PHOSPHORYLATION; SPINAL CORD; TAUOPATHY; TRANSGENIC MOUSE;

ANIMALS; DISEASE MODELS, ANIMAL; FRONTOTEMPORAL DEMENTIA; MICE; MICE, TRANSGENIC; MUTATION; NERVE DEGENERATION; NEURONS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SPINAL CORD; TAU PROTEINS; TAUOPATHIES;

EID: 84894189382     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.11.026     Document Type: Article

References (50)

1. S. Sato, J. Xu, S. Okuyama, L.B. Martinez, S.M. Walsh, M.T. Jacobsen, R.J. Swan, J.D. Schlautman, P. Ciborowski, and T. Ikezu Spatial learning impairment, enhanced CDK5/p35 activity, and downregulation of NMDA receptor expression in transgenic mice expressing tau-tubulin kinase 1 J Neurosci 28 2008 14511 14521
2. S. Sato, R.L. Cerny, J.L. Buescher, and T. Ikezu Tau-tubulin kinase 1 (TTBK1), a neuron-specific tau kinase candidate, is involved in tau phosphorylation and aggregation J Neurochem 98 2006 1573 1584 (Pubitemid 44200447)
3. K. Iqbal, I. Grundke-Iqbal, A.J. Smith, L. George, Y.C. Tung, and T. Zaidi Identification and localization of a tau peptide to paired helical filaments of Alzheimer disease Proc Natl Acad Sci U S A 86 1989 5646 5650 (Pubitemid 19185601)
4. M. Morishima-Kawashima, M. Hasegawa, K. Takio, M. Suzuki, H. Yoshida, K. Titani, and Y. Ihara Proline-directed and non-proline-directed phosphorylation of PHF-tau J Biol Chem 270 1995 823 829
5. M. Morishima-Kawashima, M. Hasegawa, K. Takio, M. Suzuki, H. Yoshida, A. Watanabe, K. Titani, and Y. Ihara Hyperphosphorylation of tau in PHF Neurobiol Aging 16 1995 365 371
6. D.P. Hanger, J.C. Betts, T.L. Loviny, W.P. Blackstock, and B.H. Anderton New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nanoelectrospray mass spectrometry J Neurochem 71 1998 2465 2476 (Pubitemid 28531257)
7. I.E. Vega, L. Cui, J.A. Propst, M.L. Hutton, G. Lee, and S.H. Yen Increase in tau tyrosine phosphorylation correlates with the formation of tau aggregates Brain Res Mol Brain Res 138 2005 135 144 (Pubitemid 41138032)
8. H. Lund, R.F. Cowburn, E. Gustafsson, K. Strömberg, A. Svensson, L. Dahllund, D. Malinowsky, and D. Sunnemark Tau-tubulin kinase 1 expression, phosphorylation and co-localization with phospho-Ser422 tau in the Alzheimer's disease brain Brain Pathol 23 2013 378 389
9. J.L. Vázquez-Higuera, A. Martínez-Garcia, P. Sánchez-Juan, E. Rodriguez-Rodriguez, I. Mateo, A. Pozueta, A. Frank, F. Valdivieso, J. Berciano, M.J. Bullido, and O. Combarros Genetic variations in tau-tubulin kinase-1 are linked to Alzheimer's disease in a Spanish case-control cohort Neurobiol Aging 32 2011 550.e5-e9
10. N.N. Yu, J.T. Yu, J.T. Xiao, H.W. Zhang, R.C. Lu, H. Jiang, Z.H. Xing, and L. Tan Tau-tubulin kinase-1 gene variants are associated with Alzheimer's disease in Han Chinese Neurosci Lett 491 2011 83 86
11. J. Xu, S. Sato, S. Okuyama, R.J. Swan, M.T. Jacobsen, E. Strunk, and T. Ikezu Tau-tubulin kinase 1 enhances prefibrillar tau aggregation and motor neuron degeneration in P301L FTDP-17 tau-mutant mice FASEB J 24 2010 2904 2915
12. D.C. Lee, J. Rizer, M.L. Selenica, P. Reid, C. Kraft, A. Johnson, L. Blair, M.N. Gordon, C.A. Dickey, and D. Morgan LPS-induced inflammation exacerbates phospho-tau pathology in rTg4510 mice J Neuroinflammation 7 2010 56
13. M. Kitazawa, S. Oddo, T.R. Yamasaki, K.N. Green, and F.M. LaFerla 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 (Pubitemid 41384452)
14. Y. Yoshiyama, M. Higuchi, B. Zhang, S.M. Huang, N. Iwata, T.C. Saido, J. Maeda, T. Suhara, J.Q. Trojanowski, and V.M. Lee Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model Neuron 53 2007 337 351 (Pubitemid 46161268)
15. B. Allen, E. Ingram, M. Takao, M.J. Smith, R. Jakes, K. Virdee, H. Yoshida, M. Holzer, M. Craxton, P.C. Emson, C. Atzori, A. Migheli, R.A. Crowther, B. Ghetti, M.G. Spillantini, and M. Goedert Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein J Neurosci 22 2002 9340 9351 (Pubitemid 35356177)
16. A. Bellucci, A.J. Westwood, E. Ingram, F. Casamenti, M. Goedert, and M.G. Spillantini Induction of inflammatory mediators and microglial activation in mice transgenic for mutant human P301S tau protein Am J Pathol 165 2004 1643 1652 (Pubitemid 39435163)
17. K. Bhaskar, M. Konerth, O.N. Kokiko-Cochran, A. Cardona, R.M. Ransohoff, and B.T. Lamb Regulation of tau pathology by the microglial fractalkine receptor Neuron 68 2010 19 31
18. S. Gordon Alternative activation of macrophages Nat Rev Immunol 3 2003 23 35 (Pubitemid 37328697)
19. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol 25 2004 677 686 (Pubitemid 39457982)
20. M. Benoit, B. Desnues, and J.-L. Mege Macrophage polarization in bacterial infections J Immunol 181 2008 3733 3739
21. G.C. Brown Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase Biochem Soc Trans 35 2007 1119 1121 (Pubitemid 350206442)
22. Y. Tatebayashi, T. Miyasaka, D.H. Chui, T. Akagi, K. Mishima, K. Iwasaki, M. Fujiwara, K. Tanemura, M. Murayama, K. Ishiguro, E. Planel, S. Sato, T. Hashikawa, and A. Takashima Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau Proc Natl Acad Sci U S A 99 2002 13896 13901 (Pubitemid 35215477)
23. J. Lewis, E. McGowan, J. Rockwood, H. Melrose, P. Nacharaju, M. Van Slegtenhorst, K. Gwinn-Hardy, M. Paul Murphy, M. Baker, X. Yu, K. Duff, J. Hardy, A. Corral, W.L. Lin, S.H. Yen, D.W. Dickson, P. Davies, and M. Hutton Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein Nat Genet 25 2000 402 405 (Pubitemid 32983430)
24. M. Cronin, M. Pho, D. Dutta, J.C. Stephans, S. Shak, M.C. Kiefer, J.M. Esteban, and J.B. Baker Measurement of gene expression in archival paraffin-embedded tissues: development and performance of a 92-gene reverse transcriptase-polymerase chain reaction assay Am J Pathol 164 2004 35 42 (Pubitemid 38364587)
25. L. Izhak, G. Wildbaum, U. Weinberg, Y. Shaked, J. Alami, D. Dumont, B. Friedman, A. Stein, and N. Karin Predominant expression of CCL2 at the tumor site of prostate cancer patients directs a selective loss of immunological tolerance to CCL2 that could be amplified in a beneficial manner J Immunol 184 2010 1092 1101
26. X.Y. Jiang, S.L. Fu, B.M. Nie, Y. Li, L. Lin, L. Yin, Y.X. Wang, P.H. Lu, and X.M. Xu Methods for isolating highly-enriched embryonic spinal cord neurons: a comparison between enzymatic and mechanical dissociations J Neurosci Methods 158 2006 13 18 (Pubitemid 44528756)
27. A. Sasaki, T. Kawarabayashi, T. Murakami, E. Matsubara, M. Ikeda, H. Hagiwara, D. Westaway, P.S. George-Hyslop, M. Shoji, and Y. Nakazato Microglial activation in brain lesions with tau deposits: comparison of human tauopathies and tau transgenic mice TgTauP301L Brain Res 1214 2008 159 168
28. I.M. Chiu, H. Phatnani, M. Kuligowski, J.C. Tapia, M.A. Carrasco, M. Zhang, T. Maniatis, and M.C. Carroll Activation of innate and humoral immunity in the peripheral nervous system of ALS transgenic mice Proc Natl Acad Sci U S A 106 2009 20960 20965
29. O. Butovsky, S. Siddiqui, G. Gabriely, A.J. Lanser, B. Dake, G. Murugaiyan, C.E. Doykan, P.M. Wu, R.R. Gali, L.K. Iyer, R. Lawson, J. Berry, A.M. Krichevsky, M.E. Cudkowicz, and H.L. Weiner Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS J Clin Invest 122 2012 3063 3087
30. O. Butovsky, M. Koronyo-Hamaoui, G. Kunis, E. Ophir, G. Landa, H. Cohen, and M. Schwartz Glatiramer acetate fights against Alzheimer's disease by inducing dendritic-like microglia expressing insulin-like growth factor 1 Proc Natl Acad Sci U S A 103 2006 11784 11789 (Pubitemid 44182528)
31. N. Brouwer, M.W. Zuurman, T. Wei, R.M. Ransohoff, H.W. Boddeke, and K. Biber Induction of glial L-CCR mRNA expression in spinal cord and brain in experimental autoimmune encephalomyelitis Glia 46 2004 84 94 (Pubitemid 38468578)
32. R. Hanamsagar, M.L. Hanke, and T. Kielian Toll-like receptor (TLR) and inflammasome actions in the central nervous system Trends Immunol 33 2012 333 342
33. M.L. Hanke, and T. Kielian Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential Clin Sci (Lond) 121 2011 367 387
34. T. Liu, Y.J. Gao, and R.R. Ji Emerging role of Toll-like receptors in the control of pain and itch Neurosci Bull 28 2012 131 144
35. K. Loser, T. Vogl, M. Voskort, A. Lueken, V. Kupas, W. Nacken, L. Klenner, A. Kuhn, D. Foell, L. Sorokin, T.A. Luger, J. Roth, and S. Beissert The Toll-like receptor 4 ligands Mrp8 and Mrp14 are crucial in the development of autoreactive CD8+ T cells Nat Med 16 2010 713 717
36. M. Ueno, Y. Fujita, T. Tanaka, Y. Nakamura, J. Kikuta, M. Ishii, and T. Yamashita Layer V cortical neurons require microglial support for survival during postnatal development Nat Neurosci 16 2013 543 551
37. O. Butovsky, Y. Ziv, A. Schwartz, G. Landa, A.E. Talpalar, S. Pluchino, G. Martino, and M. Schwartz Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells Mol Cell Neurosci 31 2006 149 160 (Pubitemid 43049908)
38. A. Parachikova, M.G. Agadjanyan, D.H. Cribbs, M. Blurton-Jones, V. Perreau, J. Rogers, T.G. Beach, and C.W. Cotman Inflammatory changes parallel the early stages of Alzheimer disease Neurobiol Aging 28 2007 1821 1833 (Pubitemid 47539700)
39. M.T. Heneka, H. Wiesinger, L. Dumitrescu-Ozimek, P. Riederer, D.L. Feinstein, and T. Klockgether Neuronal and glial coexpression of argininosuccinate synthetase and inducible nitric oxide synthase in Alzheimer disease J Neuropathol Exp Neurol 60 2001 906 916 (Pubitemid 32880598)
40. H.J. Lüth, G. Münch, and T. Arendt Aberrant expression of NOS isoforms in Alzheimer's disease is structurally related to nitrotyrosine formation Brain Res 953 2002 135 143 (Pubitemid 35217815)
41. K. Westin, P. Buchhave, H. Nielsen, L. Minthon, S. Janciauskiene, and O. Hansson CCL2 is associated with a faster rate of cognitive decline during early stages of Alzheimer's disease PLoS One 7 2012 e30525
42. A. Sokolova, M.D. Hill, F. Rahimi, L.A. Warden, G.M. Halliday, and C.E. Shepherd Monocyte chemoattractant protein-1 plays a dominant role in the chronic inflammation observed in Alzheimer's disease Brain Pathol 19 2009 392 398
43. D. Galimberti, N. Schoonenboom, E. Scarpini, P. Scheltens Dutch-Italian Alzheimer Research Group Chemokines in serum and cerebrospinal fluid of Alzheimer's disease patients Ann Neurol 53 2003 547 548 (Pubitemid 36373272)
44. J.L. Jankowsky, H.H. Slunt, V. Gonzales, N.A. Jenkins, N.G. Copeland, and D.R. Borchelt APP processing and amyloid deposition in mice haplo-insufficient for presenilin 1 Neurobiol Aging 25 2004 885 892 (Pubitemid 38813168)
45. S. Jimenez, D. Baglietto-Vargas, C. Caballero, I. Moreno-Gonzalez, M. Torres, R. Sanchez-Varo, D. Ruano, M. Vizuete, A. Gutierrez, and J. Vitorica Inflammatory response in the hippocampus of PS1M146L/APP751SL mouse model of Alzheimer's disease: age-dependent switch in the microglial phenotype from alternative to classic J Neurosci 28 2008 11650 11661
46. Z. Zhong, R. Deane, Z. Ali, M. Parisi, Y. Shapovalov, M.K. O'Banion, K. Stojanovic, A. Sagare, S. Boillee, D.W. Cleveland, and B.V. Zlokovic ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration Nat Neurosci 11 2008 420 422 (Pubitemid 351441888)
47. J.S. Henkel, D.R. Beers, S. Wen, R. Bowser, and S.H. Appel Decreased mRNA expression of tight junction proteins in lumbar spinal cords of patients with ALS Neurology 72 2009 1614 1616
48. T. Kihira, S. Yoshida, M. Hironishi, H. Miwa, K. Okamoto, and T. Kondo Changes in the incidence of amyotrophic lateral sclerosis in Wakayama, Japan Amyotroph Lateral Scler Other Motor Neuron Disord 6 2005 155 163 (Pubitemid 41419202)
49. S. Kuzuhara, and Y. Kokubo Atypical parkinsonism of Japan: amyotrophic lateral sclerosis-parkinsonism-dementia complex of the Kii peninsula of Japan (Muro disease): an update Mov Disord 20 2005 S108 S113 (Pubitemid 41419563)
50. T. Kihira, A. Suzuki, T. Kondo, I. Wakayama, S. Yoshida, K. Hasegawa, and R.M. Garruto Immunohistochemical expression of IGF-I and GSK in the spinal cord of Kii and Guamanian ALS patients Neuropathology 29 2009 548 558