The crystal structure of TDP-43 RRM1-DNA complex reveals the specific recognition for UG- and TG-rich nucleic acids

Nucleic Acids Research

Volumn 42, Issue 7, 2014, Pages 4712-4722

  Kuo, Pan Hsien ^a   Chiang, Chien Hao ^a,b   Wang, Yi Ting ^a   Doudeva, Lyudmila G ^a   Yuan, Hanna S ^a,c  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE; RNA BINDING PROTEIN; RNA RECOGNITION MOTIF 1; RNA RECOGNITION MOTIF 2; SINGLE STRANDED DNA; TAR DNA BINDING PROTEIN; THYMINE; UNCLASSIFIED DRUG; URACIL;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BETA SHEET; BINDING AFFINITY; COMPUTER MODEL; CONTROLLED STUDY; CRYSTAL STRUCTURE; DATA ANALYSIS; DIMERIZATION; DNA DENATURATION; DNA PROTEIN COMPLEX; DNA RNA HYBRIDIZATION; DNA SEQUENCE; GENE CLUSTER; GENETIC CONSERVATION; MOLECULAR MODEL; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NUCLEIC ACID ANALYSIS; NUCLEIC ACID STRUCTURE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RESIDUE ANALYSIS; TDP 43 PROTEINOPATHY; WILD TYPE;

AMINO ACID MOTIFS; DNA; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; REPETITIVE SEQUENCES, NUCLEIC ACID; RNA; RNA-BINDING PROTEINS;

EID: 84898987950     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1407     Document Type: Article

References (43)

1. Wang, I.-F., Wu, L.-S. and Shen, C.-K.J. (2008) TDP-43: an emerging new player in neurodegenerative diseases. Trends Mol. Med., 14, 479-485.
2. Neumann, M., Sampathu, D.M., Kwong, L.K., Truax, A.C., Micsenyi, M.C., Chou, T.T., Bruce, J., Schuck, T., Grossman, M., Clark, C.M. et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science, 314, 130-133. (Pubitemid 44547757)
3. Arai, T., Hasegawa, M., Akiyama, H., Ikeda, K., Nonaka, T., Mori, H., Mann, D., Tsuchiya, K., Yoshida, M., Hashizume, Y. et al. (2006) TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Comm., 351, 602-611. (Pubitemid 44708852)
4. Gendron, T.F., Josephs, K.A. and Petrucelli, L. (2010) Review: transactive response DNA-binding protein 43 (TDP-43): mechanisms of neurodegeneration. Neuropathol. Appl. Neurobiol., 36, 97-112.
5. Geser, F., Lee, V.M. and Trojanowski, J.Q. (2010) Amyotrophic lateral sclerosis and frontotemporal lobar degeneration: a spectrum of TDP-43 proteinopathies. Neuropathology, 30, 103-112.
6. 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.
7. Lee, E.B., Lee, V.M. and Trojanowski, J.Q. (2012) Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat. Rev. Neurosci., 13, 38-50.
8. Ou, S.H., Wu, F., Harrich, D., Garcia-Martinez, L.F. and Gaynor, R.B. (1995) Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol., 69, 3584-3596.
9. Buratti, E. and Baralle, F.E. (2012) TDP-43: gumming up neurons through protein-protein and protein-RNA interactions. Trends Biochem. Sci., 37, 237-247.
10. Buratti, E. and Baralle, F.E. (2001) Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9. J. Biol. Chem., 276, 36337-36343.
11. Buratti, E., Brindisi, A., Pagani, F. and Baralle, F.E. (2004) Nuclear factor TDP-43 binds to the polymorphic TG repeats in CFTR intron 8 and causes skipping of exon 9: a functional link with disease penetrance. Am. J. Hum. Genet., 74, 1322-1325. (Pubitemid 38669335)
12. Mercado, P.A., Ayala, Y.M., Romano, M., Buratti, E. and Baralle, F.E. (2005) Depletion of TDP 43 overrides the need for exonic and intronic splicing enhancers in the human apoA-II gene. Nucleic Acids Res., 33, 6000-6010. (Pubitemid 41742619)
13. Passoni, M., De Conti, L., Baralle, M. and Buratti, E. (2012) UG repeats/TDP-43 interactions near 5' splice sites exert unpredictable effects on splicing modulation. J. Mol. Biol., 415, 46-60.
14. Fiesel, F.C., Weber, S.S., Supper, J., Zell, A. and Kahle, P.J. (2012) TDP-43 regulates global translational yield by splicing of exon junction complex component SKAR. Nucleic Acids Res., 40, 2668-2682.
15. Ayala, Y.M., De Conti, L., Avendano-Vazquez, S.E., Dhir, A., Romano, M., D'Ambrogio, A., Tollervey, J., Ule, J., Baralle, M., Buratti, E. et al. (2011) TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J., 30, 277-288.
16. Xiao, S., Sanelli, T., Dib, S., Sheps, D., Findlater, J., Bilbao, J., Keith, J., Zinman, L., Rogaeva, E. and Robertson, J. (2011) RNA targets of TDP-43 identified by UV-CLIP are deregulated in ALS. Mol. Cell. Neurosci., 47, 167-180.
17. Sephton, C.F., Cenik, C., Kucukural, A., Dammer, E.B., Cenik, B., Han, Y., Dewey, C.M., Roth, F.P., Herz, J., Peng, J. et al. (2011) Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. J. Biol. Chem., 286, 1204-1215.
18. Narayanan, R.K., Mangelsdorf, M., Panwar, A., Butler, T.J., Noakes, P.G. and Wallace, R.H. (2013) Identification of RNA bound to the TDP-43 ribonucleoprotein complex in the adult mouse brain. Amyotroph. Lateral Scler. Frontotemporal. Degener., 14, 252-260.
19. Tollervey, J.R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M., Konig, J., Hortobagyi, T., Nishimura, A.L., Zupunski, V. et al. (2011) Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci., 14, 452-458.
20. Polymenidou, M., Lagier-Tourenne, C., Hutt, K.R., Huelga, S.C., Moran, J., Liang, T.Y., Ling, S.C., Sun, E., Wancewicz, E., Mazur, C. et al. (2011) Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat. Neurosci., 14, 459-468.
21. Colombrita, C., Onesto, E., Megiorni, F., Pizzuti, A., Baralle, F.E., Buratti, E., Silani, V. and Ratti, A. (2012) TDP-43 and FUS RNA-binding proteins bind distinct sets of cytoplasmic messenger RNAs and differently regulate their post-transcriptional fate in motoneuron-like cells. J. Biol. Chem., 287, 15635-15647.
22. Clery, A., Blatter, M. and Allain, F.H. (2008) RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol., 18, 290-298.
23. Maris, C., Dominguez, C. and Allain, F.H.-T. (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J., 272, 2118-2131. (Pubitemid 40655326)
24. Shiina, Y., Arima, K., Tabunoki, H. and Satoh, J. (2010) TDP-43 dimerizes in human cells in culture. Cell. Mol. Neurobiol., 30, 641-652.
25. Kuo, P.H., Doudeva, L.G., Wang, Y.T., Shen, C.K. and Yuan, H.S. (2009) Structural insights into TDP-43 in nucleic-acid binding and domain interactions. Nucleic Acids Res., 37, 1799-1808.
26. Zhang, Y.J., Caulfield, T., Xu, Y.F., Gendron, T.F., Hubbard, J., Stetler, C., Sasaguri, H., Whitelaw, E.C., Cai, S., Lee, W.C. et al. (2013) The dual functions of the extreme N-terminus of TDP-43 in regulating its biological activity and inclusion formation. Hum. Mol. Genet., 22, 3112-3122.
27. Otwinowski, Z. and Minor, W. (1993) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326.
28. Kabashi, E., Valdmanis, P.N., Dion, P., Spiegelman, D., McConkey, B.J., Vande Velde, C., Bouchard, J.P., Lacomblez, L., Pochigaeva, K., Salachas, F. et al. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet., 40, 572-574. (Pubitemid 351601218)
29. Venter, J.C., Adams, M.D., Myers, E.W., Li, P.W., Mural, R.J., Sutton, G.G., Smith, H.O., Yandell, M., Evans, C.A., Holt, R.A. et al. (2001) The sequence of the human genome. Science, 291, 1304-1351. (Pubitemid 32173090)
30. Dreyfuss, G., Kim, V.N. and Kataoka, N. (2002) Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol., 3, 195-205.
31. Perez, I., McAfee, J.G. and Patton, J.G. (1997) Multiple RRMs contribute to RNA binding specificity and affinity for polypyrimidine tract binding protein. Biochemistry, 36, 11881-11890. (Pubitemid 27424116)
32. Deo, R.C., Bonanno, J.B., Sonenberg, N. and Burley, S.K. (1999) Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell, 98, 835-845. (Pubitemid 29446900)
33. Ding, J., Hayashi, M.K., Zhang, Y., Manche, L., Krainer, A.R. and Xu, R.M. (1999) Crystal structure of the two-RRM domain of hnRNP A1 (UP1) complexed with single-stranded telomeric DNA. Genes Dev., 13, 1102-1115. (Pubitemid 29233142)
34. Handa, N., Nureki, O., Kurimoto, K., Kim, I., Sakamoto, H., Shimura, Y., Muto, Y. and Yokoyama, S. (1999) Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature, 398, 579-585.
35. Crichlow, G.V., Zhou, H., Hsiao, H.-h., Frederick, K.B., Debrosse, M., Yang, Y., Folta-Stogniew, E.J., Chung, H.-J., Fan, C., De la Cruz, E.M. et al. (2008) Dimerization of FIR upon FUSE DNA binding suggests a mechanism of c-myc inhibition. EMBO J., 27, 277-289.
36. Martin-Tumasz, S., Richie, A.C., Clos, L.J., Brow, D.A. and Butcher, S.E. (2011) A novel occluded RNA recognition motif in Prp24 unwinds the U6 RNA internal stem loop. Nucleic Acids Res., 39, 7837-7847.
37. Wang, Y.T., Kuo, P.H., Chiang, C.H., Liang, J.R., Chen, Y.R., Wang, S., Shen, J.C. and Yuan, H.S. (2013) The truncated C-terminal RNA recognition motif of TDP-43 protein plays a key role in forming proteinaceous aggregates. J. Biol. Chem., 288, 9049-9057.
38. Buratti, E., Dork, T., Zuccato, E., Pagani, F., Romano, M. and Baralle, F.E. (2001) Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J., 20, 1774-1784. (Pubitemid 32299413)
39. Lukavsky, P.J., Daujotyte, D., Rollervey, J.R., Ule, J., Stuani, C., Buratti, E., Baralle, F.E., Damberger, F.F. and Allain, F.H. (2013) Molecular basis of UG-rich RNA recognition by the human splicing factor TDP-43. Nat. Struct. Mol. Biol., 20, 1443-1449.
40. Low, P. (2011) The role of ubiquitin-proteasome system in ageing. Gen. Comp. Endocrinol., 172, 39-43.
41. Sreedharan, J., Blair, I.P., Tripathi, V.B., Hu, X., Vance, C., Rogelj, B., Ackerley, S., Durnall, J.C., Williams, K.L., Buratti, E. et al. (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science, 319, 1668-1672. (Pubitemid 351432505)
42. Suzuki, H., Lee, K. and Matsuoka, M. (2011) TDP-43-induced death is associated with altered regulation of BIM and Bcl-xL and attenuated by caspase-mediated TDP-43 cleavage. J. Biol. Chem., 286, 13171-13183.
43. Ling, S.C., Albuquerque, C.P., Han, J.S., Lagier-Tourenne, C., Tokunaga, S., Zhou, H. and Cleveland, D.W. (2010) ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS. Proc. Natl Acad. Sci. USA, 107, 13318-13323.