Nucleic acid-binding specificity of human FUS protein

Nucleic Acids Research

Volumn 43, Issue 15, 2015, Pages 7535-7543

  Wang, Xueyin ^a   Schwartz, Jacob C ^a,b   Cech, Thomas R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED NUCLEIC ACID; FUSED IN SARCOMA PROTEIN; NUCLEIC ACID; SINGLE STRANDED DNA; SINGLE STRANDED RNA; UNCLASSIFIED DRUG; DNA; FUS PROTEIN, HUMAN; PROTEIN BINDING; RNA; RNA BINDING PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN RNA BINDING; RNA MOTIF; RNA SEQUENCE; RNA STRUCTURE; CHEMISTRY; METABOLISM; NUCLEOTIDE MOTIF;

DNA; DNA, SINGLE-STRANDED; HUMANS; NUCLEOTIDE MOTIFS; PROTEIN BINDING; RNA; RNA-BINDING PROTEIN FUS;

EID: 84941210457     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv679     Document Type: Article

References (35)

1. Cruz,S.D. and Cleveland,D.W. (2011) Understanding the role of TDP-43 and FUS/TLS in ALS and beyond. Curr. Opin. Neurobiol., 21, 904-919.
2. Fiesel,F.C. and Kahle,P.J. (2011) TDP-43 and FUS/TLS: cellular functions and implications for neurodegeneration. FEBS J., 278, 3550-3568.
3. Lagier-Tourenne,C., Polymenidou,M. and Cleveland,D.W. (2010) TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum. Mol. Genet., 19, R46-R64.
4. Kiernan,M.C., Vucic,S., Cheah,B.C., Turner,M.R., Eisen,A., Hardiman,O., Burrell,J.R. and Zoing,M.C. (2011) Amyotrophic lateral sclerosis. Lancet, 377, 942-955.
5. Hewitt,C., Kirby,J., Highley,J.R., Hartley,J.A., Hibberd,R., Hollinger,H.C., 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.
6. 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.
7. Liu,X., Niu,C., Ren,J., Zhang,J., Xie,X., Zhu,H., Feng,W. and Gong,W. (2012) The RRM domain of human fused in sarcoma protein reveals a non-canoical nucleic acid binding site. Biochim. Biophys. Acta, 1832, 375-385.
8. Iko,Y., Kodama,T.S., Kasai,N., Oyama,T., Morita,E.H., Muto,T., Okumura,M., Fujii,R., Takumi,T., Tate,S. et al. (2004) Domain architectures and characterization of an RNA-binding protein, TLS. J. Biol. Chem., 279, 44834-44840.
9. Schwartz,J.C., Wang,X., Podell,E.R. and Cech,T.R. (2013) RNA seeds higher-order assembly of FUS protein. Cell Rep., 5, 918-925.
10. Wang,X., Arai,S., Song,X., Reichart,D., Du,K., Gabriel,P., Tempst,P., Rosenfeld,M.G., Glass,C.K. and Kurokawa,R. (2008) Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature, 454, 126-131.
11. 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.
12. Lerga,A., Hallier,M., Delva,L., Orvain,C., Gallais,I., Marie,J. and Moreau-Gachelin,F. (2001) Identification of an RNA binding specificity for the potential splicing factor TLS. J. Biol. Chem., 276, 6807-6816.
13. 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.
14. Ishigaki,S., Masuda,A., Fujioka,Y., Iguchi,Y., Katsuno,M., Shibata,A., Urano,F., Sobue,G. and Ohno,K. (2012) Position-dependent FUS-RNA interactions regulate alternative splicing events and transcriptions. Sci. Rep., 2, 529.
15. 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. (2012) Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat. Neurosci., 15, 1488-1497.
16. Ray,D., Kazan,H., Cook,K.B., Weirauch,M.T., Najafabadi,H.S., Li,X., Gueroussov,S., Albu,M., Zheng,H., Yang,A. et al. (2013) A compendium of RNA-binding motifs for decoding gene regulation. Nature, 499, 172-177.
17. Takahama,K., Takada,A., Tada,S., Shimizu,M., Sayama,K., Kurokawa,R. and Oyoshi,T. (2013) Regulation of telomere length by G-quadruplex telomere DNA-and TERRA-binding protein TLS/FUS. Chem. Biol., 20, 341-350.
18. McKay,D.B., Xi,L., Barthel,K.K.B. and Cech,T.R. (2014) Structure and function of steroid receptor RNA activator protein, the proposed partner of SRA non-coding RNA. J. Mol. Biol., 426, 1766-1785.
19. Milligan,J.F. and Uhlenbeck,O.C. (1989) Synthesis of small RNAs using T7 RNA polymerase. Methods Enzymol., 180, 51-62.
20. Davidovich,C., Zheng,L., Goodrich,K.J. and Cech,T.R. (2013) Promiscuous RNA binding by polycomb repressive complex 2. Nat. Struct. Mol. Biol., 20, 1250-1257.
21. Johansson,H.E., Dertinger,D., LeCuyer,K.A., Behlen,L.S., Greef,C.H. and Uhlenbeck,O.C. (1998) A thermodynamic analysis of the sequence-specific binding of RNA by bacteriophage MS2 coat protein. Proc. Natl. Acad. Sci. U.S.A., 95, 9244-9249.
22. Bertolotti,A., Lutz,Y., Heard,D.J., Chambon,P. and Tora,L. (1996) hTAF(II)68, a novel RNA/ssDNA-binding protein with homology to the pro-oncoproteins TLS/FUS and EWS is associated with both TFIID and RNA polymerase II. EMBO J., 15, 5022-5031.
23. Baechtold,H., Kuroda,M., Sok,J., Ron,D., Lopez,B.S. and Akhmedov,A.T. (1999) Human 75-kDa DNA-pairing protein is identical to the pro-oncoprotein TLS/FUS and is able to promote D-loop formation. J. Biol. Chem., 274, 34337-34342.
24. 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. (2012) Widespread binding of FUS along nascent RNA regulates alternative splicing in the brain. Sci. Rep., 2, 603.
25. Azzalin,C.M., Reichenbach,P., Khoriauli,L., Giulotto,E. and Lingner,J. (2007) Telomeric repeat-containing RNA and RNA surveillance factors at mammalian chromosome ends. Science, 318, 798-801.
26. Williamson,J.R., Raghuraman,M.K. and Cech,T.R. (1989) Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell, 59, 871-880.
27. Davidovich,C.,Wang,X., Cifuentes-Rojas,C., Goodrich,K.J., Gooding,A.R., Lee,J.T. and Cech,T.R. (2015) Toward a consensus on the binding specificity and promiscuity of PRC2 for RNA. Mol. Cell, 57, 552-558.
28. Ding,J., Hayashi,M.K., Zhang,Y., Manche,L., Krainer,A.R. and Xu,R.M. (1998) Crystal structure of the two-RRM domain of hnRNPA1 (UP1) complexed with single-stranded telomeric DNA. Genes Dev., 13, 1102-1115.
29. Tan,A.Y., Riley,T.R., Coady,T., Bussemaker,H.J. and Manley,J.L. (2012) TLS/FUS regulates target gene transcription via single-stranded DNA response elements. Proc. Natl. Acad. Sci. U.S.A., 109, 6030-6035.
30. Calvio,C., Neubauer,G., Mann,M. and Lamond,A.I. (1995) Identification of hnRNP P2 as TLS/FUS using electrospray mass spectrometry. RNA, 1, 724-733.
31. 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. Nat. Neurosci., 16, 1383-1391.
32. Mastrocola,A.S., Kim,S.H., Trinh,A.T., Rodenkirch,L.A. and Tibbetts,R.S. (2013) The RNA-binding protein fused in sarcoma (FUS) functions downstream of poly (ADP-ribose) polymerase (PARP) in response to DNA damage. J. Biol. Chem., 288, 24731-24741.
33. Kwon,I., Kato,M., Xiang,S., Wu,L., Theodoropoulos,P., Mirzaei,H., Han,T., Xie,S., Corden,J.L. and McKnight,S.L. (2013) Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains. Cell, 155, 1049-1060.
34. Moretti,R., Donato,L.J., Brezinski,M.L., Stafford,R.L., Hoff,H., Thorson,J.S., Dervan,P.B. and Ansari,A.Z. (2008) Targeted chemical wedges reveal the role of allosteric DNA modulation in protein-DNA assembly. ACS Chem. Biol., 3, 220-229.
35. 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 the PY-NLS modulates transportin binding and nuclear import of FUS. EMBO J., 31, 4258-4275.