The structure of human SFPQ reveals a coiled-coil mediated polymer essential for functional aggregation in gene regulation

Nucleic Acids Research

Volumn 43, Issue 7, 2015, Pages 3826-3840

  Lee, Mihwa ^a,c   Sadowska, Agata ^a   Bekere, Indra ^a   Ho, Diwei ^a   Gully, Benjamin S ^a   Lu, Yanling ^b   Iyer, K Swaminathan ^a   Trewhella, Jill ^b   Fox, Archa H ^a   Bond, Charles S ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HETERODIMER; POLYMER; SPLICING FACTOR PROLINE AND GLUTAMINE RICH PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; PTB-ASSOCIATED SPLICING FACTOR; RNA BINDING PROTEIN;

ARTICLE; CELL FUNCTION; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; GENE CONTROL; HUMAN; IN VITRO STUDY; MOLECULAR INTERACTION; NUCLEIC ACID METABOLISM; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; TRANSMISSION ELECTRON MICROSCOPY; X RAY CRYSTALLOGRAPHY; CHEMISTRY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; PHYSIOLOGY; PROTEIN CONFORMATION; WESTERN BLOTTING;

BLOTTING, WESTERN; CRYSTALLOGRAPHY, X-RAY; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; POLYMERS; PROTEIN CONFORMATION; RNA-BINDING PROTEINS;

EID: 84930505834     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv156     Document Type: Article

References (53)

1. Kowalska, E., Ripperger, J.A., Muheim, C., Maier, B., Kurihara, Y., Fox, A.H., Kramer, A. and Brown, S.A. (2012) Distinct roles of DBHS family members in the circadian transcriptional feedback loop. Mol. Cell. Biol., 32, 4585-4594.
2. Lowery, L.A., Rubin, J. and Sive, H. (2007) Whitesnake/sfpq is required for cell survival and neuronal development in the zebrafsh. Dev. Dyn., 236, 1347-1357.
3. Duong, H.A., Robles, M.S., Knutti, D. and Weitz, C.J. (2011) A molecular mechanism for circadian clock negative feedback. Science, 332, 1436-1439.
4. Chia, N.Y., Chan, Y.S., Feng, B., Lu, X., Orlov, Y.L., Moreau, D., Kumar, P., Yang, L., Jiang, J., Lau, M.S. et al. (2010) A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature, 468, 316-320.
5. Patton, J.G., Porro, E.B., Galceran, J., Tempst, P. and Nadal-Ginard, B. (1993) Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev., 7, 393-406.
6. Shav-Tal, Y. and Zipori, D. (2002) PSF and p54(nrb)/NonO-multi-functional nuclear proteins. FEBS Lett., 531, 109-114.
7. Song, X., Sun, Y. and Garen, A. (2005) Roles of PSF protein and VL30 RNA in reversible gene regulation. Proc. Natl. Acad. Sci. U.S.A., 102, 12189-12193.
8. Hirose, T., Virnicchi, G., Tanigawa, A., Naganuma, T., Li, R., Kimura, H., Yokoi, T., Nakagawa, S., Benard, M., Fox, A.H. et al. (2014) NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies. Mol. Biol. Cell, 25, 169-183.
9. Imamura, K., Imamachi, N., Akizuki, G., Kumakura, M., Kawaguchi, A., Nagata, K., Kato, A., Kawaguchi, Y., Sato, H., Yoneda, M. et al. (2014) Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol. Cell, 53, 393-406.
10. Morozumi, Y., Takizawa, Y., Takaku, M. and Kurumizaka, H. (2009) Human PSF binds to RAD51 and modulates its homologous-pairing and strand-exchange activities. Nucleic Acids Res., 37, 4296-4307.
11. Rajesh, C., Baker, D.K., Pierce, A.J. and Pittman, D.L. (2011) The splicing-factor related protein SFPQ/PSF interacts with RAD51D and is necessary for homology-directed repair and sister chromatid cohesion. Nucleic Acids Res., 39, 132-145.
12. Ha, K., Takeda, Y. and Dynan, W.S. (2011) Sequences in PSF/SFPQ mediate radioresistance and recruitment of PSF/SFPQ-containing complexes to DNA damage sites in human cells. DNA Rep., 10, 252-259.
13. Bond, C.S. and Fox, A.H. (2009) Paraspeckles: nuclear bodies built on long noncoding RNA. J. Cell Biol., 186, 637-644.
14. Takayama, K., Horie-Inoue, K., Katayama, S., Suzuki, T., Tsutsumi, S., Ikeda, K., Urano, T., Fujimura, T., Takagi, K., Takahashi, S. et al. (2013) Androgen-responsive long noncoding RNA CTBP1-AS promotes prostate cancer. EMBO J., 32, 1665-1680.
15. Ji, Q., Zhang, L., Liu, X., Zhou, L., Wang, W., Han, Z., Sui, H., Tang, Y., Wang, Y., Liu, N. et al. (2014) Long non-coding RNA MALAT1 promotes tumour growth and metastasis in colorectal cancer through binding to SFPQ and releasing oncogene PTBP2 from SFPQ/PTBP2 complex. Br. J Cancer, 111, 736-748.
16. Fox, A.H., Bond, C.S. and Lamond, A.I. (2005) P54nrb forms a heterodimer with PSP1 that localizes to paraspeckles in an RNA-dependent manner. Mol. Biol. Cell, 16, 5304-5315.
17. Lee, M., Passon, D.M., Hennig, S., Fox, A.H. and Bond, C.S. (2011) Construct optimization for studying protein complexes: obtaining diffraction-quality crystals of the pseudosymmetric PSPC1-NONO heterodimer. Acta Crystallogr. D Biol. Crystallogr., 67, 981-987.
18. Passon, D.M., Lee, M., Rackham, O., Stanley, W.A., Sadowska, A., Filipovska, A., Fox, A.H. and Bond, C.S. (2012) Structure of the heterodimer of human NONO and paraspeckle protein component 1 and analysis of its role in subnuclear body formation. Proc. Natl. Acad. Sci. U.S.A., 109, 4846-4850.
19. Li, Y.R., King, O.D., Shorter, J. and Gitler, A.D. (2013) Stress granules as crucibles of ALS pathogenesis. J. Cell Biol., 201, 361-372.
20. Ramaswami, M., Taylor, J.P. and Parker, R. (2013) Altered ribostasis: RNA-protein granules in degenerative disorders. Cell, 154, 727-736.
21. Kabsch, W. (2010) Xds. Acta crystallogr. D Biol. Crystallogr., 66, 125-132.
22. Evans, P. (2006) Scaling and assessment of data quality. Acta crystallogr. D Biol. Crystallogr., 62, 72-82.
23. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr., 40, 658-674.
24. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr., 66, 486-501.
25. Blanc, E., Roversi, P., Vonrhein, C., Flensburg, C., Lea, S.M. and Bricogne, G. (2004) Refnement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D Biol. Crystallogr., 60, 2210-2221.
26. Chen, V.B., Arendall, W.B. 3rd, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr., 66, 12-21.
27. Bond, C.S. (2003) Easy editing of Protein Data Bank formatted fles with EMACS. J. Appl. Crystallogr., 36, 350-351.
28. Bond, C.S. and Schuttelkopf, A.W. (2009) ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr. D, 65, 510-512.
29. Petoukhov, M.V., Franke, D., Shkumatov, A.V., Tria, G., Kikhney, A.G., Gajda, M., Gorba, C., Mertens, H.D.T., Konarev, P.V. and Svergun, D.I. (2012) New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr., 45, 342-350.
30. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol., 372, 774-797.
31. Walshaw, J. and Woolfson, D.N. (2001) Socket: a program for identifying and analysing coiled-coil motifs within protein structures. J. Mol. Biol., 307, 1427-1450.
32. Urban, R.J., Bodenburg, Y.H. and Wood, T.G. (2002) NH2 terminus of PTB-associated splicing factor binds to the porcine P450scc IGF-I response element. Am. J. Physiol. Endocrinol. Metab., 283, E423-E427.
33. Zhang, W.W., Zhang, L.X., Busch, R.K., Farres, J. and Busch, H. (1993) Purifcation and characterization of a DNA-binding heterodimer of 52 and 100 Kda from Hela-cells. Biochem. J., 290, 267-272.
34. Miyamoto, K., Sakurai, H. and Sugiura, T. (2008) Proteomic identifcation of a PSF/p54nrb heterodimer as RNF43 oncoprotein-interacting proteins. Proteomics, 8, 2907-2910.
35. Gromiha, M.M. and Parry, D.A. (2004) Characteristic features of amino acid residues in coiled-coil protein structures. Biophys. Chem., 111, 95-103.
36. Mathur, M., Tucker, P.W. and Samuels, H.H. (2001) PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors. Mol. Cell. Biol., 21, 2298-2311.
37. Hirose, T., Virnicchi, G., Tanigawa, A., Naganuma, T., Li, R., Kimura, H., Yokoi, T., Nakagawa, S., Benard, M., Fox, A.H. et al (2013) NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies. Mol. Biol. Cell, 25, 169-183.
38. West, J.A., Davis, C.P., Sunwoo, H., Simon, M.D., Sadreyev, R.I., Wang, P.I., Tolstorukov, M.Y. and Kingston, R.E. (2014) The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites. Mol. Cell, 55, 791-802.
39. Stepto, A., Gallo, J.M., Shaw, C.E. andHirth, F. (2014) Modelling C9ORF72 hexanucleotide repeat expansion in amyotrophic lateral sclerosis and frontotemporal dementia. Acta Neuropathol, 127, 377-389.
40. Naganuma, T, Nakagawa, S., Tanigawa, A., Sasaki, Y.F., Goshima, N and Hirose, T (2012) Alternative 3'-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J., 31, 4020-4034.
41. Tanaka, H., Kato, K., Yamashita, E., Sumizawa, T, Zhou, Y, Yao, M., Iwasaki, K., Yoshimura, M. and Tsukihara, T (2009) The structure of rat liver vault at 3.5 angstrom resolution. Science, 323, 384-388.
42. Sanchez, J.G., Okreglicka, K., Chandrasekaran, V, Welker, J.M., Sundquist, W.I. and Pornillos, O. (2014) The tripartite motif coiled-coil is an elongated antiparallel hairpin dimer. Proc. Natl Acad. Sci. U.S.A., 111, 2494-2499.
43. Souquere, S., Beauclair, G, Harper, F., Fox, A. and Pierron, G (2010) Highly ordered spatial organization of the structural long noncoding NEAT1 RNAs within paraspeckle nuclear bodies. Mol. Biol. Cell, 21, 4020-4027.
44. Mao Y.S., Sunwoo, H., Zhang, B. and Spector, D.L. (2011) Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs. Nat. Cell Biol, 13, 95-101.
45. Kuroda, N, Mikami, S., Pan, C.C, Cohen, R.J., Hes, O., Michal, M., Nagashima, Y, Tanaka, Y, Inoue, K., Shuin, T et al. (2012) Review of renal carcinoma associated with Xp11.2 translocations/TFE3 gene fusions with focus on pathobiological aspect. Histol. Histopathol., 27, 133-140.
46. Hidalgo-Curtis, C, Chase, A., Drachenberg, M., Roberts, M.W., Finkelstein, J.Z., Mould, S., Oscier, D., Cross, NC. and Grand, F.H. (2008) The t(1;9)(p34;q34) and t(8;12)(p11;q15) fuse pre-mRNA processing proteins SFPQ (PSF) and CPSF6 to ABL and FGFR1. Genes Chromosomes Cancer, 47, 379-385.
47. Rendahl, K.G, Gaukhshteyn, N, Wheeler, D.A., Fry, TA. and Hall, J.C. (1996) Defects in courtship and vision caused by amino acid substitutions in a putative RNA-binding protein encoded by the no-on-transient A (nonA) gene of Drosophila. J. Neurosci., 16, 1511-1522.
48. Ke Y.D, Dramiga, J., Schutz, U., Kril, J.J., Ittner, L.M., Schroder, H. and Gotz, J. (2012) Tau-mediated nuclear depletion and cytoplasmic accumulation of SFPQ in Alzheimer's and Pick's disease. PLoS One, 7, e35678.
49. Shelkovnikova, TA., Robinson, H.K., Troakes, C, Ninkina, N and Buchman, V.L. (2014) Compromised paraspeckle formation as a pathogenic factor in FUSopathies. Hum. Mol. Genet., 23, 2298-2312.
50. Wu, H. (2013) Higher-order assemblies in a new paradigm of signal transduction. Cell, 153, 287-292.
51. Kato, M., Han, TW., Xie, S., Shi, K., Du, X., Wu, L.C, Mirzaei, H., Goldsmith, E.J., Longgood, J., Pei, J. et al. (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fbers within hydrogels. Cell, 149, 753-767.
52. 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 fbrous polymers of low-complexity domains. Cell, 155, 1049-1060.
53. Meyer, GR., Aragao, D., Mudie, NJ., Caradoc-Davies, TT, McGowan, S., Bertling, PJ., Groenewegen, D., Quenette, S.M., Bond, CS., Buckle, A.M. et al. (2014) Operation of the Australian Store. Synchrotron for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr, 70, 2510-2519.