Structure-function studies of nucleocytoplasmic transport of retroviral genomic RNA by mRNA export factor TAP

Nature Structural and Molecular Biology

Volumn 18, Issue 9, 2011, Pages 990-998

  Teplova, Marianna ^a   Wohlbold, Lara ^b   Khin, Nyan W ^a   Izaurralde, Elisa ^b   Patel, Dinshaw J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; MESSENGER RNA; PROTEIN TAP; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; NUCLEOCYTOPLASMIC TRANSPORT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN MOTIF;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; BINDING SITES; CELL NUCLEUS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; RNA, MESSENGER; RNA, VIRAL; RNA-BINDING PROTEINS;

SIMIAE;

EID: 80052504962     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2094     Document Type: Article

References (55)

1. Chook, Y.M. & Blobel, G. Karyopherins and nuclear import. Curr. Opin. Struct. Biol. 11, 703-715 (2001). (Pubitemid 34076632)
2. Conti, E. & Izaurralde, E. Nucleocytoplasmic transport enters the atomic age. Curr. Opin. Cell Biol. 13, 310-319 (2001). (Pubitemid 32429495)
3. Conti, E., Muller, C.W. & Stewart, M. Karyopherin flexibility in nucleocytoplasmic transport. Curr. Opin. Struct. Biol. 16, 237-244 (2006).
4. Cook, A., Bono, F., Jinek, M. & Conti, E. Structural biology of nucleocytoplasmic transport. Annu. Rev. Biochem. 76, 647-671 (2007).
5. Köhler, A. & Hurt, E. Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol. 8, 761-773 (2007). (Pubitemid 47462133)
6. Stewart, M. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 8, 195-208 (2007).
7. Cook, A.G. & Conti, E. Nuclear export complexes in the frame. Curr. Opin. Struct. Biol. 20, 247-252 (2010).
8. Cook, A.G., Fukuhara, N., Jinek, M. & Conti, E. Structures of the tRNA export factor in the nuclear and cytosolic states. Nature 461, 60-65 (2009).
9. Okada, C. et al. A high-resolution structure of the pre-microRNA nuclear export machinery. Science 326, 1275-1279 (2009).
10. Braun, I.C., Rohrbach, E., Schmitt, C. & Izaurralde, E. TAP binds to the constitutive transport element (CTE) through a novel RNA-binding motif that is sufficient to promote CTE-dependent RNA export from the nucleus. EMBO J. 18, 1953-1965 (1999). (Pubitemid 29158538)
11. Grüter, P. et al. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell 1, 649-659 (1998). (Pubitemid 128379243)
12. Izaurralde, E. Friedrich Miescher Prize awardee lecture review. A conserved family of nuclear export receptors mediates the exit of messenger RNA to the cytoplasm. Cell. Mol. Life Sci. 58, 1105-1112 (2001). (Pubitemid 32756520)
13. Segref, A. et al. Mex67p, a novel factor for nuclear mRNA export, binds to both poly(A)+ RNA and nuclear pores. EMBO J. 16, 3256-3271 (1997). (Pubitemid 27234963)
14. Fribourg, S., Braun, I.C., Izaurralde, E. & Conti, E. Structural basis for the recognition of a nucleoporin FG repeat by the NTF2-like domain of the TAP/p15 mRNA nuclear export factor. Mol. Cell 8, 645-656 (2001). (Pubitemid 32946941)
15. Herold, A. et al. TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol. Cell. Biol. 20, 8996-9008 (2000). (Pubitemid 32245929)
16. Liker, E., Fernandez, E., Izaurralde, E. & Conti, E. The structure of the mRNA export factor TAP reveals a cis arrangement of a non-canonical RNP domain and an LRR domain. EMBO J. 19, 5587-5598 (2000).
17. Ho, D.N., Coburn, G.A., Kang, Y., Cullen, B.R. & Georgiadis, M.M. The crystal structure and mutational analysis of a novel RNA-binding domain found in the human Tap nuclear mRNA export factor. Proc. Natl. Acad. Sci. USA 99, 1888-1893 (2002). (Pubitemid 34168984)
18. Grant, R.P., Neuhaus, D. & Stewart, M. Structural basis for the interaction between the Tap/NXF1 UBA domain and FG nucleoporins at 1 resolution. J. Mol. Biol. 326, 849-858 (2003). (Pubitemid 36279324)
19. Bachi, A. et al. The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA 6, 136-158 (2000). (Pubitemid 30069044)
20. Ernst, R.K., Bray, M., Rekosh, D. & Hammarskjold, M.L. A structured retroviral RNA element that mediates nucleocytoplasmic export of intron-containing RNA. Mol. Cell. Biol. 17, 135-144 (1997). (Pubitemid 26425602)
21. Tabernero, C., Zolotukhin, A.S., Valentin, A., Pavlakis, G.N. & Felber, B.K. The posttranscriptional control element of the simian retrovirus type 1 forms an extensive RNA secondary structure necessary for its function. J. Virol. 70, 5998-6011 (1996). (Pubitemid 26266814)
22. Cullen, B.R. Viral RNAs: lessons from the enemy. Cell 136, 592-597 (2009).
23. Li, Y. et al. An intron with a constitutive transport element is retained in a Tap messenger RNA. Nature 443, 234-237 (2006). (Pubitemid 44387614)
24. Kang, Y. & Cullen, B.R. The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev. 13, 1126-1139 (1999). (Pubitemid 29233144)
25. Braun, I.C., Herold, A., Rode, M., Conti, E. & Izaurralde, E. Overexpression of TAP/p15 heterodimers bypasses nuclear retention and stimulates nuclear mRNA export. J. Biol. Chem. 276, 20536-20543 (2001).
26. Jin, L., Guzik, B.W., Bor, Y.C., Rekosh, D. & Hammarskjold, M.L. Tap and NXT promote translation of unspliced mRNA. Genes Dev. 17, 3075-3086 (2003). (Pubitemid 38040771)
27. Serganov, A., Polonskaia, A., Ehresmann, B., Ehresmann, C. & Patel, D.J. Ribosomal protein S15 represses its own translation via adaptation of an rRNA-like fold within its mRNA. EMBO J. 22, 1898-1908 (2003). (Pubitemid 36460146)
28. Batey, R.T., Rambo, R.P. & Doudna, J.A. Tertiary motifs in RNA structure and folding. Angew. Chem. Int. Edn Engl. 38, 2326-2343 (1999). (Pubitemid 29399554)
29. Hermann, T. & Patel, D.J. Adaptive recognition by nucleic acid aptamers. Science 287, 820-825 (2000). (Pubitemid 30084318)
30. Tereshko, V., Skripkin, E. & Patel, D.J. Encapsulating streptomycin within a small 40-mer RNA. Chem. Biol. 10, 175-187 (2003). (Pubitemid 36250976)
31. Dibrov, S.M., Johnston-Cox, H., Weng, Y.H. & Hermann, T. Functional architecture of HCV IRES domain II stabilized by divalent metal ions in the crystal and in solution. Angew. Chem. Int. Edn Engl. 46, 226-229 (2007). (Pubitemid 46071706)
32. Leontis, N.B. & Westhof, E. Geometric nomenclature and classification of RNA base pairs. RNA 7, 499-512 (2001). (Pubitemid 32416808)
33. Hermann, T. & Patel, D.J. RNA bulges as architectural and recognition motifs. Structure 8, R47-R54 (2000). (Pubitemid 30148687)
34. Jiang, F. et al. Anchoring an extended HTLV-1 Rex peptide within an RNA major groove containing junctional base triples. Structure 7, 1461-1472 (1999). (Pubitemid 30007232)
35. Cléry, A., Blatter, M. & Allain, F.H. RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18, 290-298 (2008).
36. Lunde, B.M., Moore, C. & Varani, G. RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol. 8, 479-490 (2007). (Pubitemid 46809150)
37. Serganov, A. & Patel, D.J. Towards deciphering the principles underlying an mRNA recognition code. Curr. Opin. Struct. Biol. 18, 120-129 (2008).
38. Price, S.R., Evans, P.R. & Nagai, K. Crystal structure of the spliceosomal U2B-U2A′ protein complex bound to a fragment of U2 small nuclear RNA. Nature 394, 645-650 (1998). (Pubitemid 28389783)
39. Teplova, M. et al. Structural basis for recognition and sequestration of UUU(OH) 3′ temini of nascent RNA polymerase III transcripts by La, a rheumatic disease autoantigen. Mol. Cell 21, 75-85 (2006). (Pubitemid 43017850)
40. Liu, L. et al. Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 320, 379-381 (2008). (Pubitemid 351555661)
41. Hautbergue, G.M., Hung, M.L., Golovanov, A.P., Lian, L.Y. & Wilson, S.A. Mutually exclusive interactions drive handover of mRNA from export adaptors to TAP. Proc. Natl. Acad. Sci. USA 105, 5154-5159 (2008). (Pubitemid 351738526)
42. Stutz, F. & Izaurralde, E. The interplay of nuclear mRNP assembly, mRNA surveillance and export. Trends Cell Biol. 13, 319-327 (2003). (Pubitemid 36638799)
43. Walsh, M.J., Hautbergue, G.M. & Wilson, S.A. Structure and function of mRNA export adaptors. Biochem. Soc. Trans. 38, 232-236 (2010).
44. Huang, Y., Gattoni, R., Stevenin, J. & Steitz, J.A. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell 11, 837-843 (2003). (Pubitemid 36385134)
45. CCP4. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
46. Pikovskaya, O., Serganov, A.A., Polonskaia, A., Serganov, A. & Patel, D.J. Preparation and crystallization of riboswitch-ligand complexes. Methods Mol. Biol. 540, 115-128 (2009).
47. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
48. Navaza, J. AMoRe: an automated package for molecular replacement. Acta Crystallogr. A 50, 157-163 (1994).
49. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997). (Pubitemid 27235885)
50. Winn, M.D., Isupov, M.N. & Murshudov, G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57, 122-133 (2001). (Pubitemid 32062682)
51. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
52. McCoy, A.J., Grosse-Kunstleve, R.W., Storoni, L.C. & Read, R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458-464 (2005). (Pubitemid 43934606)
53. Robertson, M.P. & Scott, W.G. A general method for phasing novel complex RNA crystal structures without heavy-atom derivatives. Acta Crystallogr. D Biol. Crystallogr. D64, 738-744 (2008). (Pubitemid 351872053)
54. Terwilliger, T.C. et al. Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. D Biol. Crystallogr. 64, 61-69 (2008). (Pubitemid 350308678)
55. Huang, X.J. et al. Minimal Rev-response element for type 1 human immunodeficiency virus. J. Virol. 65, 2131-2134 (1991).