Cytoplasmic sequestration of FUS/TLS associated with ALS alters histone marks through loss of nuclear protein arginine methyltransferase 1

Human Molecular Genetics

Volumn 24, Issue 3, 2015, Pages 773-786

  Tibshirani, Michael ^a   Tradewell, Miranda L ^a   Mattina, Katie R ^a   Minotti, Sandra ^a   Yang, Wencheng ^b   Zhou, Hongru ^c   Strong, Michael J ^b   Hayward, Lawrence J ^c   Durham, Heather D ^a  

^a MCGILL UNIVERSITY   (Canada)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; HISTONE; HISTONE H3; HISTONE H4; NUCLEAR PROTEIN ARGININE METHYLTRANSFERASE 1; PROTEIN ARGININE METHYLTRANSFERASE; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; FUS PROTEIN, HUMAN; FUS PROTEIN, MOUSE; PRMT1 PROTEIN, HUMAN; PRMT1 PROTEIN, MOUSE; REPRESSOR PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; HISTONE ACETYLATION; HISTONE METHYLATION; IN VIVO STUDY; MOTONEURON; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SPINAL CORD CELL CULTURE; TRANSGENIC MOUSE; ANIMAL; CELL CULTURE; CELL NUCLEUS; DISEASE MODEL; DNA METHYLATION; HUMAN; METABOLISM; PATHOLOGY; SPINAL CORD;

MUS MUSCULUS;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL NUCLEUS; CELLS, CULTURED; CYTOPLASM; DISEASE MODELS, ANIMAL; DNA METHYLATION; HISTONES; HUMANS; MICE; MICE, TRANSGENIC; MOTOR NEURONS; PROTEIN-ARGININE N-METHYLTRANSFERASES; REPRESSOR PROTEINS; RNA-BINDING PROTEIN FUS; SPINAL CORD;

EID: 84922423167     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu494     Document Type: Article

References (49)

1. Hewitt, C., Kirby, J., Highley, J.R., Hartley, J.A., Hibberd, R., Hollinger, H.C., Williams, T.L., Ince, P.G., McDermott, C.J. and Shaw, P.J. (2010) Novel FUS/TLS mutations and pathology in familial and sporadic amyotrophic lateral sclerosis. Arch. Neurol., 67, 455-461.
2. 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. (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science, 323, 1205-1208.
3. Vance, C., Rogelj, B., Hortobagyi, T., De Vos, K.J., Nishimura, A.L., Sreedharan, J., Hu, X., Smith, B., Ruddy, D., Wright, P. et al. (2009) Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science, 323, 1208-1211.
4. van Blitterswijk, M. and Landers, J.E. (2010) RNA processing pathways in amyotrophic lateral sclerosis. Neurogenetics, 11, 275-290.
5. Kovar, H. (2011) Dr. Jekyll and Mr. Hyde: the two faces of the FUS/EWS/TAF15 protein family. Sarcoma, 2011, 837474.
6. Fujii, R. and Takumi, T. (2005) TLS facilitates transport of mRNA encoding an actin-stabilizing protein to dendritic spines. J. Cell Sci., 118, 5755-5765.
7. 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. (2010) FUS-immunoreactive inclusions are a common feature in sporadic and non-SOD1 familial amyotrophic lateral sclerosis. Ann. Neurol., 67, 739-748.
8. Bedford, M.T. and Clarke, S.G. (2009) Protein arginine methylation in mammals: who, what, and why. Mol. Cell, 33, 1-13.
9. Yu, M.C. (2011) The role of protein arginine methylation in mRNP dynamics. Mol. Biol. Int., 2011, 163827.
10. Tang, J., Frankel, A., Cook, R.J., Kim, S., Paik, W.K., Williams, K.R., Clarke, S. and Herschman, H.R. (2000) PRMT1 is the predominant type I protein arginine methyltransferase in mammalian cells. J. Biol. Chem., 275, 7723-7730.
11. Tradewell, M.L., Yu, Z., Tibshirani, M., Boulanger, M.C., Durham, H.D. and Richard, S. (2012) Arginine methylation by PRMT1 regulates nuclear-cytoplasmic localization and toxicity of FUS/TLS harbouring ALS-linked mutations. Hum. Mol. Genet., 21, 136-149.
12. Dormann, D., Madl, T., Valori, C.F., Bentmann, E., Tahirovic, S., Abou-Ajram, C., Kremmer, E., Ansorge, O., Mackenzie, I.R., Neumann, M. et al. (2012) Arginine methylation next to thePY-NLSmodulates transportin binding and nuclear import of FUS. EMBO J., 31, 4258-4275.
13. Du, K., Arai, S., Kawamura, T., Matsushita, A. and Kurokawa, R. (2011) TLS and PRMT1 synergistically coactivate transcription at the survivin promoter through TLS arginine methylation. Biochem. Biophys. Res. Commun., 404, 991-996.
14. Scaramuzzino, C., Monaghan, J., Milioto, C., Lanson, N.A. Jr, Maltare, A., Aggarwal, T., Casci, I., Fackelmayer, F.O., Pennuto, M. and Pandey, U.B. (2013) Protein arginine methyltransferase 1 and 8 interact with FUS to modify its sub-cellular distribution and toxicity in vitro and in vivo. PLoS One, 8, e61576.
15. Yamaguchi, A. and Kitajo, K. (2012) The effect of PRMT1-mediated arginine methylation on the subcellular localization, stress granules, and detergent-insoluble aggregates of FUS/TLS. PLoS One, 7, e49267.
16. Di Lorenzo, A. and Bedford, M.T. (2011) Histone arginine methylation. FEBS Lett., 585, 2024-2031.
17. Lee, Y.-H. and Stallcup, M.R. (2009) Minireview: protein arginine methylation of nonhistone proteins in transcriptional regulation. Mol. Endocrinol., 23, 425-433.
18. Khan, A.U. and Krishnamurthy, S. (2005) Histone modifications as key regulators of transcription. Front. Biosci., 10, 866-872.
19. Cheung, P., Allis, C.D. and Sassone-Corsi, P. (2000) Signaling to chromatin through histone modifications. Cell, 103, 263-271.
20. Lee, J.S., Smith, E. and Shilatifard, A. (2010) The language of histone crosstalk. Cell, 142, 682-685.
21. Bergeron, C., Beric-Maskarel, K., Muntasser, S., Weyer, L., Somerville, M.J. and Percy, M.E. (1994) Neurofilament light and polyadenylatedmRNA levels are decreased in amyotrophic lateral sclerosis motor neurons. J. Neuropathol. Exp. Neurol., 53, 221-230.
22. Jiang, Y.M., Yamamoto, M., Kobayashi, Y., Yoshihara, T., Liang, Y., Terao, S., Takeuchi, H., Ishigaki, S., Katsuno, M., Adachi, H. et al. (2005) Gene expression profile of spinal motor neurons in sporadic amyotrophic lateral sclerosis. Ann. Neurol., 57, 236-251.
23. Campos-Melo, D., Droppelmann, C., He, Z., Volkening, K. and Strong, M. (2013) Altered microRNA expression profile in amyotrophic lateral sclerosis: a role in the regulation of NFL mRNA levels. Mol. Brain, 6, 26.
24. Strahl, B.D., Briggs, S.D., Brame, C.J., Caldwell, J.A., Koh, S.S., Ma, H., Cook, R.G., Shabanowitz, J., Hunt, D.F., Stallcup, M.R. et al. (2001) Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr. Biol., 11, 996-1000.
25. Wang, H., Huang, Z.Q., Xia, L., Feng, Q., Erdjument-Bromage, H., Strahl, B.D., Briggs, S.D., Allis, C.D., Wong, J., Tempst, P. et al. (2001) Methylation of histoneH4at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science, 293, 853-857.
26. Huang, S., Litt, M. and Felsenfeld, G. (2005) Methylation of histone H4 by arginine methyltransferase PRMT1 is essential in vivo for many subsequent histone modifications. Genes. Dev., 19, 1885-1893.
27. Conte, A., Lattante, S., Zollino, M., Marangi, G., Luigetti, M., Del Grande, A., Servidei, S., Trombetta, F. and Sabatelli, M. (2012) P525L FUS mutation is consistently associated with a severe form of juvenile amyotrophic lateral sclerosis. Neuromuscul. Disord., 22, 73-75.
28. Baumer, D., Hilton, D., Paine, S.M., Turner, M.R., Lowe, J., Talbot, K. and Ansorge, O. (2010) Juvenile ALS with basophilic inclusions is a FUS proteinopathy with FUS mutations. Neurology, 75, 611-618.
29. Aoki, N., Higashi, S., Kawakami, I., Kobayashi, Z., Hosokawa, M., Katsuse, O., Togo, T., Hirayasu, Y. and Akiyama, H. (2012) Localization of fused in sarcoma (FUS) protein to the post-synaptic density in the brain. Acta. Neuropathol., 124, 383-394.
30. Sama, R.R., Ward, C.L., Kaushansky, L.J., Lemay, N., Ishigaki, S., Urano, F. and Bosco, D.A. (2013) FUS/TLS assembles into stress granules and is a prosurvival factor during hyperosmolar stress. J. Cell. Physiol., 228, 2222-2231.
31. Sun, L., Wang, M., Lv, Z., Yang, N., Liu, Y., Bao, S., Gong, W. and Xu, R.-M. (2011) Structural insights into protein arginine symmetric dimethylation by PRMT5. Proc. Natl. Acad. Sci., 108, 20538-20543.
32. Bonham, K., Hemmers, S., Lim, Y.H., Hill, D.M., Finn, M.G. and Mowen, K.A. (2010) Effects of a novel arginine methyltransferase inhibitor on T-helper cell cytokine production. FEBS J., 277, 2096-2108.
33. Li, X., Hu, X., Patel, B., Zhou, Z., Liang, S., Ybarra, R., Qiu, Y., Felsenfeld, G., Bungert, J. and Huang, S. (2010) H4R3 methylation facilitates beta-globin transcription by regulating histone acetyltransferase binding and H3 acetylation. Blood, 115, 2028-2037.
34. Qiu, H., Lee, S., Shang, Y., Wang, W.Y., Au, K.F., Kamiya, S., Barmada, S.J., Finkbeiner, S., Lui, H., Carlton, C.E. et al. (2014) ALS-associated mutation FUS-R521C causes DNA damage and RNA splicing defects. J. Clin. Invest., 124, 981-999.
35. Hoell, J.I., Larsson, E., Runge, S., Nusbaum, J.D., Duggimpudi, S., Farazi, T.A., Hafner, M., Borkhardt, A., Sander, C. and Tuschl, T. (2011) RNA targets of wild-type and mutant FET family proteins. Nat. Struct. Mol. Biol., 18, 1428-1431.
36. Zhou, Y., Liu, S., Liu, G., Ozturk, A. and Hicks, G.G. (2013) ALS-associated FUS mutations result in compromised FUS alternative splicing and autoregulation. PLoS Genet., 9, e1003895.
37. Lagier-Tourenne, C. and Cleveland, D.W. (2009) Rethinking ALS: the FUS about TDP-43. Cell, 136, 1001-1004.
38. Dormann, D., Rodde, R., Edbauer, D., Bentmann, E., Fischer, I., Hruscha, A., Than, M.E., Mackenzie, I.R., Capell, A., Schmid, B. et al. (2010) ALS-associated fused in sarcoma (FUS) mutations disrupt transportin-mediated nuclear import. EMBO J., 29, 2841-2857.
39. Bosco, D.A., Lemay, N., Ko, H.K., Zhou, H., Burke, C., Kwiatkowski, T.J. Jr, Sapp, P., McKenna-Yasek, D., Brown, R.H. Jr and Hayward, L.J. (2010) Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum. Mol. Genet., 19, 4160-4175.
40. Ito, D., Seki, M., Tsunoda, Y., Uchiyama, H. and Suzuki, N. (2011) Nuclear transport impairment of amyotrophic lateral sclerosis-linked mutations in FUS/TLS. Ann. Neurol., 69, 152-162.
41. Nakano, I. and Hirano, A. (1987) Atrophic cell processes of large motor neurons in the anterior horn in amyotrophic lateral sclerosis: observation with silver impregnation method. J. Neuropathol. Exp. Neurol., 46, 40-49.
42. Waibel, S., Neumann, M., Rosenbohm, A., Birve, A., Volk, A.E., Weishaupt, J.H., Meyer, T., Muller, U., Andersen, P.M. and Ludolph, A.C. (2013) Truncating mutations in FUS/TLS give rise to a more aggressive ALS-phenotype than missense mutations: a clinico-genetic study in Germany. Eur. J. Neurol., 20, 540-546.
43. Goulet, I., Gauvin, G., Boisvenue, S. and Côté, J. (2007) Alternative splicing yields protein arginine methyltransferase 1 isoforms with distinct activity, substrate specificity, and subcellular localization. J. Biol. Chem., 282, 33009-33021.
44. Boisvert, F.-M., Lam, Y.W., Lamont, D. and Lamond, A.I. (2010) A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell. Prot., 9, 457-470.
45. Wang, W.Y., Pan, L., Su, S.C., Quinn, E.J., Sasaki, M., Jimenez, J.C., Mackenzie, I.R., Huang, E.J. and Tsai, L.H. (2013) Interaction of FUS and HDAC1 regulates DNA damage response and repair in neurons. Nat. Neurosci., 16, 1383-1391.
46. Schwartz, J.C., Ebmeier, C.C., Podell, E.R., Heimiller, J., Taatjes, D.J. and Cech, T.R. (2012) FUS binds the CTD of RNA polymerase II and regulates its phosphorylation at Ser2. Genes. Dev., 26, 2690-2695.
47. Roy, J., Minotti, S., Dong, L., Figlewicz, D.A. and Durham, H.D. (1998) Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by postsynaptic calcium-dependent mechanisms. J. Neurosci., 18, 9673-9684.
48. Durham, H.D., Roy, J., Dong, L. and Figlewicz, D.A. (1997) Aggregation of mutant Cu/Zn superoxide dismutase proteins in a culture model of ALS. J. Neuropathol. Exp. Neurol., 56, 523-530.
49. Shechter, D., Dormann, H.L., Allis, C.D. and Hake, S.B. (2007) Extraction, purification and analysis of histones. Nat. Prot., 2, 1445-1457.