The Spt6 SH2 domain binds Ser2-P RNAPII to direct Iws1-dependent mRNA splicing and export

Genes and Development

Volumn 21, Issue 2, 2007, Pages 160-174

  Yoh, Sunnie M ^a   Cho, Helen ^b   Pickle, Loni ^a   Evans, Ronald M ^b   Jones, Katherine A ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Nuclear mRNA export; RNAPII CTD; SH2 domain; Splicing; Spt6; Transcription elongation

Indexed keywords

ABELSON KINASE; BINDING PROTEIN; MESSENGER RNA; PHOSPHOSERINE; PHOSPHOTYROSINE; PROTEIN SH2; PROTEIN SUBUNIT; RNA POLYMERASE II; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR SPT6; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; NONHUMAN; ONCOGENE C MYC; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA BINDING; RNA PROCESSING; RNA SPLICING;

AMINO ACID SUBSTITUTION; ANIMALS; BLOTTING, FAR-WESTERN; CELL NUCLEUS; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; EXORIBONUCLEASES; HELA CELLS; HIV-1; HUMANS; MICE; NUCLEAR PROTEINS; PHOSPHOSERINE; POINT MUTATION; PROMOTER REGIONS (GENETICS); PROTEINS; RECOMBINANT PROTEINS; RNA POLYMERASE II; RNA SPLICING; RNA, MESSENGER; SRC HOMOLOGY DOMAINS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA;

EID: 33846525436     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1503107     Document Type: Article

References (66)

1. Abruzzi, K.C., Lacadie, S., and Rosbash, M. 2004. Biochemical analysis of TREX complex recruitment to intronless and intron-containing yeast genes. EMBO J. 23: 2620-2631.
2. Adelman, K., Wei, W., Ardehali, M.B., Werner, J., Zhu, B., Reinberg, D., and Lis, J.T. 2006. Drosophila Paf1 modulates chromatin structure at actively transcribed genes. Mol. Cell. Biol. 26: 250-260.
3. Adkins, M.W. and Tyler, J.K. 2006. Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions. Mol. Cell 21: 405-416.
4. Aguilera, A. 2005. Cotranscriptional mRNP assembly: From the DNA to the nuclear pore. Curr. Opin. Cell Biol. 17: 242-250.
5. Ahn, S.H., Kim, M., and Buratowski, S. 2004. Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3′ end processing. Mol. Cell 13: 67-76.
6. Andrulis, E.D., Guzman, E., Doring, P., Werner, J., and Lis, J.T. 2000. High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: Roles in promoter proximal pausing and transcription elongation. Genes & Dev. 14: 2635-2649.
7. Andrulis, E.D., Werner, J., Nazarian, A., Erdjument-Bromage, H., Tempst, P., and Lis, J.T. 2002. The RNA processing exosome is linked to elongating RNA polymerase II in Drosophila. Nature 420: 837-841.
8. Baskaran, R., Chiang, G.G., Mysliwiec, T., Kruh, G.D., and Wang, J.Y. 1997. Tyrosine phosphorylation of RNA polymerase II carboxyl-terminal domain by the Abl-related gene product. J. Biol. Chem. 272: 18905-18909.
9. Belotserkovskaya, R., Oh, S., Bondarenko, V.A., Orphanides, G., Studitsky, V.M., and Reinberg, D. 2003. FACT facilitates transcription-dependent nucleosome alteration. Science 301: 1090-1093.
10. Bentley, D.L. 2005. Rules of engagement: Co-transcriptional recruitment of pre-mRNA processing factors. Curr. Opin. Cell Biol. 17: 251-256.
11. Bird, G., Zorio, D.A., and Bentley, D.L. 2004. RNA polymerase II carboxy-terminal domain phosphorylation is required for cotranscriptional pre-mRNA splicing and 3′-end formation. Mol. Cell. Biol. 24: 8963-8969.
12. Bortvin, A. and Winston, F. 1996. Evidence that Spt6p controls chromatin structure by a direct interaction with histones. Science 272: 1473-1476.
13. Bres, V., Gomes, N., Pickle, L., and Jones, K.A. 2005. A human splicing factor, SKIP, associates with P-TEFb and enhances transcription elongation by HIV-1 Tat. Genes & Dev. 19: 1211-1226.
14. Cho, H., Kim, T.K., Mancebo, H., Lane, W.S., Flores, O., and Reinberg, D. 1999. A protein phosphatase functions to recycle RNA polymerase II. Genes & Dev. 13: 1540-1552.
15. DeSilva, H., Lee, K., and Osley, M.A. 1998. Functional dissection of yeast Hir1p, a WD repeat-containing transcriptional corepressor. Genetics 148: 657-667.
16. Dimaano, C. and Ullman, K.S. 2004. Nucleocytoplasmic transport: Integrating mRNA production and turnover with export through the nuclear pore. Mol. Cell. Biol. 24: 3069-3076.
17. Endoh, M., Zhu, W., Hasegawa, J., Watanabe, H., Kim, D.K., Aida, M., Inukai, N., Narita, T., Yamada, T., Furuya, A., et al. 2004. Human Spt6 stimulates transcription elongation by RNA polymerase II in vitro. Mol. Cell. Biol. 24: 3324-3336.
18. Fischbeck, J.A., Kraemer, S.M., and Stargell, L.A. 2002. SPN1, a conserved gene identified by suppression of a postrecruitment-defective yeast TATA-binding protein mutant. Genetics 162: 1605-1616.
19. Gatfield, D. and Izaurralde, E. 2002. REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J. Cell Biol. 159: 579-588.
20. Kaplan, C.D., Morris, J.R., Wu, C., and Winston, F. 2000. Spt5 and Spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster. Genes & Dev. 14: 2623-2634.
21. Kaplan, C.D., Laprade, L., and Winston, F. 2003. Transcription elongation factors repress transcription initiation from cryptic sites. Science 301: 1096-1099.
22. Kaplan, C.D., Holland, M.J., and Winston, F. 2005. Interaction between transcription elongation factors and mRNA 3′-end formation at the Saccharomyces cerevisiae GAL10-GAL7 locus. J. Biol. Chem. 280: 913-922.
23. Kizer, K.O., Phatnani, H.P., Shibata, Y., Hall, H., Greenleaf, A.L., and Strahl, B.D. 2005. A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol. Cell. Biol. 25: 3305-3316.
24. Lei, E.P. and Silver, P.A. 2002. Intron status and 3′-end formation control cotranscriptional export of mRNA. Genes & Dev. 16: 2761-2766.
25. Lei, E.P., Krebber, H., and Silver, P.A. 2001. Messenger RNAs are recruited for nuclear export during transcription. Genes & Dev. 15: 1771-1782.
26. Li, Y., Wang, X., Zhang, X., and Goodrich, D.W. 2005. Human hHpr1/p84/Thoc1 regulates transcriptional elongation and physically links RNA polymerase II and RNA processing factors. Mol. Cell. Biol. 25: 4023-4033.
27. Licatalosi, D.D., Geiger, G., Minet, M., Schroeder, S., Cilli, K., McNeil, J.B., and Bentley, D.L. 2002. Functional interaction of yeast pre-mRNA 3′ end processing factors with RNA polymerase II. Mol. Cell 9: 1101-1111.
28. Lindstrom, D.L., Squazzo, S.L., Muster, N., Burckin, T.A., Wachter, K.C., Emigh, C.A., McCleery, J.A., Yates III, J.R., and Hartzog, G.A. 2003. Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5-associated proteins. Mol. Cell. Biol. 23: 1368-1378.
29. Lischka, P., Toth, Z., Thomas, M., Mueller, R., and Stamminger, T. 2006. The UL69 transactivator protein of human cytomegalovirus interacts with DEXD/H-Box RNA helicase UAP56 to promote cytoplasmic accumulation of unspliced RNA. Mol. Cell. Biol. 26: 1631-1643.
30. Luna, R., Jimeno, S., Marin, M., Huertas, P., Garcia-Rubio, M., and Aguilera, A. 2005. Interdependence between transcription and mRNP processing and export, and its impact on genetic stability. Mol. Cell 18: 711-722.
31. Luo, M.L., Zhou, Z., Magni, K., Christoforides, C., Rappsilber, J., Mann, M., and Reed, R. 2001. Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature 413: 644-647.
32. Maclennan, A.J. and Shaw, G. 1993. A yeast SH2 domain. Trends Biochem. Sci. 18: 464-465.
33. Maldonado, E., Drapkin, R., and Reinberg, D. 1996. Purification of human RNA polymerase II and general transcription factors. Methods Enzymol. 274: 72-100.
34. Mandal, S.S., Cho, H., Kim, S., Cabane, K., and Reinberg, D. 2002. FCP1, a phosphatase specific for the heptapeptide repeat of the largest subunit of RNA polymerase II, stimulates transcription elongation. Mol. Cell. Biol. 22: 7543-7552.
35. Masuda, S., Das, R., Cheng, H., Hurt, E., Dorman, N., and Reed, R. 2005. Recruitment of the human TREX complex to mRNA during splicing. Genes & Dev. 19: 1512-1517.
36. Meinhart, A. and Cramer, P. 2004. Recognition of RNA polymerase II carboxy-terminal domain by 3′-RNA-processing factors. Nature 430: 223-226.
37. Meinhart, A., Kamenski, T., Hoeppner, S., Baumli, S., and Cramer, P. 2005. A structural perspective of CTD function. Genes & Dev. 19: 1401-1415.
38. Mueller, C.L., Porter, S.E., Hoffman, M.G., and Jaehning, J.A. 2004. The Paf1 complex has functions independent of actively transcribing RNA polymerase II. Mol. Cell 14: 447-456.
39. Ni, Z., Schwartz, B.E., Werner, J., Suarez, J.R., and Lis, J.T. 2004. Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol. Cell 13: 55-65.
40. Nollau, P. and Mayer, B.J. 2001. Profiling the global tyrosine phosphorylation state by Src homology 2 domain binding. Proc. Natl. Acad. Sci. 98: 13531-13536.
41. Orphanides, G., LeRoy, G., Chang, C.H., Luse, D.S., and Reinberg, D. 1998. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92: 105-116.
42. Pavri, R., Zhu, B., Li, G., Trojer, P., Mandal, S., Shilatifard, A., and Reinberg, D. 2006. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125: 703-717.
43. Pawson, T. 2004. Specificity in signal transduction: From phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116: 191-203.
44. Penheiter, K.L., Washburn, T.M., Porter, S.E., Hoffman, M.G., and Jaehning, J.A. 2005. A posttranscriptional role for the yeast Paf1-RNA polymerase II complex is revealed by identification of primary targets. Mol. Cell 20: 213-223.
45. Peterlin, B.M. and Price, D.H. 2006. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23: 297-305.
46. Phatnani, H.P. and Greenleaf, A.L. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes & Dev. 20: 2922-2936.
47. Porter, S.E., Penheiter, K.L., and Jaehning, J.A. 2005. Separation of the Saccharomyces cerevisae Paf1 complex from RNA polymerase II results in changes in its subnuclear localization. Eukaryot. Cell 4: 209-220.
48. Reed, R. and Cheng, H. 2005. TREX, SR proteins and export of mRNA. Curr. Opin. Cell Biol. 17: 269-273.
49. Rehwinkel, J., Herold, A., Gari, K., Kocher, T., Rode, M., Ciccarelli, F.L., Wilm, M., and Izaurralde, E. 2004. Genomewide analysis of mRNAs regulated by the THO complex in Drosophila melanogaster. Nat. Struct. Mol. Biol. 11: 558-566.
50. Reinberg, D. and Sims III, R.J. 2006. de FACTo nucleosome dynamics. J. Biol. Chem. 281: 23297-23301.
51. Rodriguez-Navarro, S., Fischer, T., Luo, M.J., Antunez, O., Brettschneider, S., Lechner, J., Perez-Ortin, J.E., Reed, R., and Hurt, E. 2004. Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell 116: 75-86.
52. Rondon, A.G., Jimeno, S., Garcia-Rubio, M., and Aguilera, A. 2003. Molecular evidence that the eukaryotic THO/TREX complex is required for efficient transcription elongation. J. Biol. Chem. 278: 39037-39043.
53. Saguez, C., Olesen, J.R., and Jensen, T.H. 2005. Formation of export-competent mRNP: Escaping nuclear destruction. Curr. Opin. Cell Biol. 17: 287-293.
54. Saunders, A., Werner, J., Andrulis, E.D., Nakayama, T., Hirose, S., Reinberg, D., and Lis, J.T. 2003. Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301: 1094-1096.
55. Sims III, R.J., Belotserkovskaya, R., and Reinberg, D. 2004. Elongation by RNA polymerase II: The short and long of it. Genes & Dev. 18: 2437-2468.
56. Sommer, P. and Nehrbass, U. 2005. Quality control of messenger ribonucleoprotein particles in the nucleus and at the pore. Curr. Opin. Cell Biol. 17: 294-301.
57. Srinivasan, S., Armstrong, J.A., Deuring, R., Dahlsveen, I.K., McNeill, H., and Tamkun, J.W. 2005. The Drosophila trithorax group protein Kismet facilitates an early step in transcription elongation by RNA polymerase II. Development 132: 1623-1635.
58. Strasser, K. and Hurt, E. 2001. Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p. Nature 413: 648-652.
59. Vasudevan, S. and Peltz, S.W. 2003. Nuclear mRNA surveillance. Curr. Opin. Cell Biol. 15: 332-337.
60. Vinciguerra, P. and Stutz, F. 2004. mRNA export: An assembly line from genes to nuclear pores. Curr. Opin. Cell Biol. 16: 285-292.
61. Winkler, M., Aus Dem Siepen, T., and Stamminger, T. 2000. Functional interaction between pleiotropic transactivator pUL69 of human cytomegalovirus and the human homolog of yeast chromatin regulatory protein SPT6. J. Virol. 74: 8053-8064.
62. Wood, A., Shukla, A., Schneider, J., Lees, J.S., Stanton, J.D., Dzuiba, T., Swanson, S.K., Florens, L., Washburn, M.P., Wyrick, J., et al. 2006. Ctk complex mediated regulation of histone methylation by COMPASS. Mol. Cell. Biol., doi: 10.1128/MCB.01627-06.
63. Xiao, T., Hall, H., Kizer, K.O., Shibata, Y., Hall, M.C., Borchers, C.H., and Strahl, B.D. 2003. Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes & Dev. 17: 654-663.
64. Xiao, T., Shibata, Y., Rao, B., Laribee, R.N., O'Rourke, R., Buck, M.J., Greenblatt, J.F., Krogan, N.J., Lieb, J.D., and Strahl, B.D. 2006. The RNA Pol II kinase Ctk1 regulates positioning of a 5xy: unknown character box histone methylation boundary along genes. Mol. Cell. Biol., doi: 10.1128/MCB.01628-06.
65. Zenklusen, D., Vinciguerra, P., Wyss, J.C., and Stutz, F. 2002. Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p. Mol. Cell. Biol. 22: 8241-8253.
66. Zhu, B., Mandal, S.S., Pham, A.D., Zheng, Y., Erdjument-Bromage, H., Batra, S.K., Tempst, P., and Reinberg, D. 2005. The human PAF complex coordinates transcription with events downstream of RNA synthesis. Genes & Dev. 19: 1668-1673.