Altered Tau Isoform Ratio Caused by Loss of FUS and SFPQ Function Leads to FTLD-like Phenotypes

Cell Reports

Volumn 18, Issue 5, 2017, Pages 1118-1131

  Ishigaki, Shinsuke ^a   Fujioka, Yusuke ^a   Okada, Yohei ^b   Riku, Yuichi ^a,c   Udagawa, Tsuyoshi ^a   Honda, Daiyu ^a   Yokoi, Satoshi ^a   Endo, Kuniyuki ^a   Ikenaka, Kensuke ^a   Takagi, Shinnosuke ^a   Iguchi, Yohei ^a   Sahara, Naruhiko ^d   Takashima, Akihiko ^e   Okano, Hideyuki ^f   Yoshida, Mari ^c   Warita, Hitoshi ^g   Aoki, Masashi ^g   Watanabe, Hirohisa ^a   Okado, Haruo ^h   Katsuno, Masahisa ^a   Sobue, Gen ^a   more..

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b AICHI MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c AICHI MEDICAL UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^e GAKUSHUIN UNIVERSITY   (Japan)

^f KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^g TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^h TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

adult neurogenesis; FTLD; FUS; SFPQ; tau

Indexed keywords

PTB ASSOCIATED SPLICING FACTOR; RNA BINDING PROTEIN FUS; TAU PROTEIN; ISOPROTEIN; RNA BINDING PROTEIN;

ABNORMAL BEHAVIOR; ADULT; ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; CELL NUCLEUS; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; EXON SKIPPING; FRONTOTEMPORAL DEMENTIA; GENE; HIPPOCAMPUS; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; MAPT GENE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPEN FIELD TEST; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; C57BL MOUSE; EXON; METABOLISM; NERVE CELL; PHENOTYPE; PHYSIOLOGY; RNA SPLICING;

ALTERNATIVE SPLICING; ANIMALS; EXONS; FRONTOTEMPORAL LOBAR DEGENERATION; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; NEURONS; PHENOTYPE; PROTEIN ISOFORMS; PTB-ASSOCIATED SPLICING FACTOR; RNA SPLICING; RNA-BINDING PROTEIN FUS; RNA-BINDING PROTEINS; TAU PROTEINS;

EID: 85011659822     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.01.013     Document Type: Article

References (44)

1. D'Souza, I., Schellenberg, G.D., Arginine/serine-rich protein interaction domain-dependent modulation of a tau exon 10 splicing enhancer: Altered interactions and mechanisms for functionally antagonistic FTDP-17 mutations Delta280K AND N279K. J. Biol. Chem. 281 (2006), 2460–2469.
2. Deng, H.X., Zhai, H., Bigio, E.H., Yan, J., Fecto, F., Ajroud, K., Mishra, M., Ajroud-Driss, S., Heller, S., Sufit, R., et al. FUS-immunoreactive inclusions are a common feature in sporadic and non-SOD1 familial amyotrophic lateral sclerosis. Ann. Neurol. 67 (2010), 739–748.
3. Dickson, D.W., Kouri, N., Murray, M.E., Josephs, K.A., Neuropathology of frontotemporal lobar degeneration-tau (FTLD-tau). J. Mol. Neurosci. 45 (2011), 384–389.
4. Ferrer, I., Legati, A., García-Monco, J.C., Gomez-Beldarrain, M., Carmona, M., Blanco, R., Seeley, W.W., Coppola, G., Familial behavioral variant frontotemporal dementia associated with astrocyte-predominant tauopathy. J. Neuropathol. Exp. Neurol. 74 (2015), 370–379.
5. Fujioka, Y., Ishigaki, S., Masuda, A., Iguchi, Y., Udagawa, T., Watanabe, H., Katsuno, M., Ohno, K., Sobue, G., FUS-regulated region- and cell-type-specific transcriptome is associated with cell selectivity in ALS/FTLD. Sci. Rep., 3, 2013, 2388.
6. Fuster-Matanzo, A., Llorens-Martín, M., Jurado-Arjona, J., Avila, J., Hernández, F., Tau protein and adult hippocampal neurogenesis. Front. Neurosci., 6, 2012, 104.
7. Geser, F., Martinez-Lage, M., Kwong, L.K., Lee, V.M., Trojanowski, J.Q., Amyotrophic lateral sclerosis, frontotemporal dementia and beyond: The TDP-43 diseases. J. Neurol. 256 (2009), 1205–1214.
8. Ichiyanagi, N., Fujimori, K., Yano, M., Ishihara-Fujisaki, C., Sone, T., Akiyama, T., Okada, Y., Akamatsu, W., Matsumoto, T., Ishikawa, M., et al. Establishment of in vitro fus-associated familial amyotrophic lateral sclerosis model using human induced pluripotent stem cells. Stem Cell Reports 6 (2016), 496–510.
9. Iguchi, Y., Katsuno, M., Ikenaka, K., Ishigaki, S., Sobue, G., Amyotrophic lateral sclerosis: An update on recent genetic insights. J. Neurol. 260 (2013), 2917–2927.
10. Imayoshi, I., Sakamoto, M., Ohtsuka, T., Takao, K., Miyakawa, T., Yamaguchi, M., Mori, K., Ikeda, T., Itohara, S., Kageyama, R., Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci. 11 (2008), 1153–1161.
11. Ishigaki, S., Masuda, A., Fujioka, Y., Iguchi, Y., Katsuno, M., Shibata, A., Urano, F., Sobue, G., Ohno, K., Position-dependent FUS-RNA interactions regulate alternative splicing events and transcriptions. Sci. Rep., 2, 2012, 529.
12. Josephs, K.A., Hodges, J.R., Snowden, J.S., Mackenzie, I.R., Neumann, M., Mann, D.M., Dickson, D.W., Neuropathological background of phenotypical variability in frontotemporal dementia. Acta Neuropathol. 122 (2011), 137–153.
13. Kabashi, E., Bercier, V., Lissouba, A., Liao, M., Brustein, E., Rouleau, G.A., Drapeau, P., FUS and TARDBP but not SOD1 interact in genetic models of amyotrophic lateral sclerosis. PLoS Genet., 7, 2011, e1002214.
14. Kino, Y., Washizu, C., Aquilanti, E., Okuno, M., Kurosawa, M., Yamada, M., Doi, H., Nukina, N., Intracellular localization and splicing regulation of FUS/TLS are variably affected by amyotrophic lateral sclerosis-linked mutations. Nucleic Acids Res. 39 (2011), 2781–2798.
15. Kino, Y., Washizu, C., Kurosawa, M., Yamada, M., Miyazaki, H., Akagi, T., Hashikawa, T., Doi, H., Takumi, T., Hicks, G.G., et al. FUS/TLS deficiency causes behavioral and pathological abnormalities distinct from amyotrophic lateral sclerosis. Acta Neuropathol. Commun., 3, 2015, 24.
16. Kwiatkowski, T.J. Jr., Bosco, D.A., Leclerc, A.L., Tamrazian, E., Vanderburg, C.R., Russ, C., Davis, A., Gilchrist, J., Kasarskis, E.J., Munsat, T., et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323 (2009), 1205–1208.
17. Lagier-Tourenne, C., Cleveland, D.W., Rethinking ALS: The FUS about TDP-43. Cell 136 (2009), 1001–1004.
18. Lagier-Tourenne, C., Polymenidou, M., Hutt, K.R., Vu, A.Q., Baughn, M., Huelga, S.C., Clutario, K.M., Ling, S.C., Liang, T.Y., Mazur, C., et al. Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat. Neurosci. 15 (2012), 1488–1497.
19. Lashley, T., Rohrer, J.D., Mead, S., Revesz, T., Review: An update on clinical, genetic and pathological aspects of frontotemporal lobar degenerations. Neuropathol. Appl. Neurobiol. 41 (2015), 858–881.
20. Mackenzie, I.R., Ansorge, O., Strong, M., Bilbao, J., Zinman, L., Ang, L.C., Baker, M., Stewart, H., Eisen, A., Rademakers, R., Neumann, M., Pathological heterogeneity in amyotrophic lateral sclerosis with FUS mutations: two distinct patterns correlating with disease severity and mutation. Acta Neuropathol. 122 (2011), 87–98.
21. McMillan, P., Korvatska, E., Poorkaj, P., Evstafjeva, Z., Robinson, L., Greenup, L., Leverenz, J., Schellenberg, G.D., D'Souza, I., Tau isoform regulation is region- and cell-specific in mouse brain. J. Comp. Neurol. 511 (2008), 788–803.
22. Neumann, M., Rademakers, R., Roeber, S., Baker, M., Kretzschmar, H.A., Mackenzie, I.R., A new subtype of frontotemporal lobar degeneration with FUS pathology. Brain 132 (2009), 2922–2931.
23. Noro, T., Miyake, K., Suzuki-Miyake, N., Igarashi, T., Uchida, E., Misawa, T., Yamazaki, Y., Shimada, T., Adeno-associated viral vector-mediated expression of endostatin inhibits tumor growth and metastasis in an orthotropic pancreatic cancer model in hamsters. Cancer Res. 64 (2004), 7486–7490.
24. Okada, T., Shimazaki, K., Nomoto, T., Matsushita, T., Mizukami, H., Urabe, M., Hanazono, Y., Kume, A., Tobita, K., Ozawa, K., Kawai, N., Adeno-associated viral vector-mediated gene therapy of ischemia-induced neuronal death. Methods Enzymol. 346 (2002), 378–393.
25. Orozco, D., Tahirovic, S., Rentzsch, K., Schwenk, B.M., Haass, C., Edbauer, D., Loss of fused in sarcoma (FUS) promotes pathological Tau splicing. EMBO Rep. 13 (2012), 759–764.
26. Ray, P., Kar, A., Fushimi, K., Havlioglu, N., Chen, X., Wu, J.Y., PSF suppresses tau exon 10 inclusion by interacting with a stem-loop structure downstream of exon 10. J. Mol. Neurosci. 45 (2011), 453–466.
27. Renton, A.E., Chiò, A., Traynor, B.J., State of play in amyotrophic lateral sclerosis genetics. Nat. Neurosci. 17 (2014), 17–23.
28. Riku, Y., Watanabe, H., Yoshida, M., Tatsumi, S., Mimuro, M., Iwasaki, Y., Katsuno, M., Iguchi, Y., Masuda, M., Senda, J., et al. Lower motor neuron involvement in TAR DNA-binding protein of 43 kDa-related frontotemporal lobar degeneration and amyotrophic lateral sclerosis. JAMA Neurol. 71 (2014), 172–179.
29. Robberecht, W., Philips, T., The changing scene of amyotrophic lateral sclerosis. Nat. Rev. Neurosci. 14 (2013), 248–264.
30. Rogelj, B., Easton, L.E., Bogu, G.K., Stanton, L.W., Rot, G., Curk, T., Zupan, B., Sugimoto, Y., Modic, M., Haberman, N., et al. Widespread binding of FUS along nascent RNA regulates alternative splicing in the brain. Sci. Rep., 2, 2012, 603.
31. Sahara, N., DeTure, M., Ren, Y., Ebrahim, A.S., Kang, D., Knight, J., Volbracht, C., Pedersen, J.T., Dickson, D.W., Yen, S.H., Lewis, J., Characteristics of TBS-extractable hyperphosphorylated tau species: aggregation intermediates in rTg4510 mouse brain. J. Alzheimers Dis. 33 (2013), 249–263.
32. Scekic-Zahirovic, J., Sendscheid, O., El Oussini, H., Jambeau, M., Sun, Y., Mersmann, S., Wagner, M., Dieterlé, S., Sinniger, J., Dirrig-Grosch, S., et al. Toxic gain of function from mutant FUS protein is crucial to trigger cell autonomous motor neuron loss. EMBO J. 35 (2016), 1077–1097.
33. Schoch, K.M., DeVos, S.L., Miller, R.L., Chun, S.J., Norrbom, M., Wozniak, D.F., Dawson, H.N., Bennett, C.F., Rigo, F., Miller, T.M., Increased 4R-tau induces pathological changes in a human-tau mouse model. Neuron 90 (2016), 941–947.
34. Seelaar, H., Rohrer, J.D., Pijnenburg, Y.A., Fox, N.C., van Swieten, J.C., Clinical, genetic and pathological heterogeneity of frontotemporal dementia: a review. J. Neurol. Neurosurg. Psychiatry 82 (2011), 476–486.
35. Sharma, A., Lyashchenko, A.K., Lu, L., Nasrabady, S.E., Elmaleh, M., Mendelsohn, M., Nemes, A., Tapia, J.C., Mentis, G.Z., Shneider, N.A., ALS-associated mutant FUS induces selective motor neuron degeneration through toxic gain of function. Nat. Commun., 7, 2016, 10465.
36. Spillantini, M.G., Goedert, M., Tau pathology and neurodegeneration. Lancet Neurol. 12 (2013), 609–622.
37. Sun, S., Ling, S.C., Qiu, J., Albuquerque, C.P., Zhou, Y., Tokunaga, S., Li, H., Qiu, H., Bui, A., Yeo, G.W., et al. ALS-causative mutations in FUS/TLS confer gain and loss of function by altered association with SMN and U1-snRNP. Nat. Commun., 6, 2015, 6171.
38. Tsuiji, H., Iguchi, Y., Furuya, A., Kataoka, A., Hatsuta, H., Atsuta, N., Tanaka, F., Hashizume, Y., Akatsu, H., Murayama, S., et al. Spliceosome integrity is defective in the motor neuron diseases ALS and SMA. EMBO Mol. Med. 5 (2013), 221–234.
39. Udagawa, T., Fujioka, Y., Tanaka, M., Honda, D., Yokoi, S., Riku, Y., Ibi, D., Nagai, T., Yamada, K., Watanabe, H., et al. FUS regulates AMPA receptor function and FTLD/ALS-associated behaviour via GluA1 mRNA stabilization. Nat. Commun., 6, 2015, 7098.
40. van de Pol, L.A., Hensel, A., van der Flier, W.M., Visser, P.J., Pijnenburg, Y.A., Barkhof, F., Gertz, H.J., Scheltens, P., Hippocampal atrophy on MRI in frontotemporal lobar degeneration and Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 77 (2006), 439–442.
41. Van Langenhove, T., van der Zee, J., Van Broeckhoven, C., The molecular basis of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum. Ann. Med. 44 (2012), 817–828.
42. Vance, C., Rogelj, B., Hortobágyi, T., De Vos, K.J., Nishimura, A.L., Sreedharan, J., Hu, X., Smith, B., Ruddy, D., Wright, P., et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323 (2009), 1208–1211.
43. Wang, J.W., Brent, J.R., Tomlinson, A., Shneider, N.A., McCabe, B.D., The ALS-associated proteins FUS and TDP-43 function together to affect Drosophila locomotion and life span. J. Clin. Invest. 121 (2011), 4118–4126.
44. Wang, T., Jiang, X., Chen, G., Xu, J., Interaction of amyotrophic lateral sclerosis/frontotemporal lobar degeneration-associated fused-in-sarcoma with proteins involved in metabolic and protein degradation pathways. Neurobiol. Aging 36 (2015), 527–535.