DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs

Genes and Development

Volumn 12, Issue 3, 1998, Pages 343-356

  Wada, Tadashi ^a   Takagi, Toshiyuki ^a   Yamaguchi, Yuki ^a   Ferdous, Anwarul ^a   Imai, Takeshi ^a   Hirose, Susumu ^b   Sugimoto, Seiji ^c   Yano, Keiichi ^c   Hartzog, Grant A ^d   Winston, Fred ^d   Buratowski, Stephen ^d   Handa, Hiroshi ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c KYOWA HAKKO KOGYO CO LTD   (Japan)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

DRB; DSIF; NusG; Protein phosphorylation; Transcription elongation; Transcription elongation factor; Transcription inhibitor

Indexed keywords

5,6 DICHLOROBENZIMIDAZOLE RIBOSIDE; DELTA SLEEP INDUCING PEPTIDE; ELONGATION FACTOR; RNA POLYMERASE II;

AMINO ACID SEQUENCE; ARTICLE; ENZYME CONFORMATION; ENZYME REGULATION; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION;

BACTERIA (MICROORGANISMS); SACCHAROMYCES CEREVISIAE;

EID: 14444275279     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.3.343     Document Type: Article

References (72)

1. Akoulitchev, S., T.P. Makela, R.A. Weinberg, and D. Reinberg. 1995. Requirement for TFIIH kinase activity in transcription by RNA polymerase II. Nature 377: 557-560.
2. Aso, T., W.S. Lane, J.W. Conaway, and R.C. Conaway. 1995. Elongin (SIII): A multisubunit regulator of elongation by RNA polymerase II. Science 269: 1439-1443.
3. Bengal, E., O. Flores, A. Krauskopf, D. Reinberg, and Y. Aloni. 1991. Role of the mammalian transcription factors IIF, IIS, and IIX during elongation by RNA polymerase II. Mol. Cell. Biol. 11: 1195-1206.
4. Bortvin, A. and F. Winston. 1996. Evidence that Spt6p controls chromatin structure by a direct interaction with histones. Science 272: 1473-1476.
5. Bradsher, J.N., K.W. Jackson, R.C. Conaway, and J.W. Conaway. 1993a. RNA polymerase II transcription factor SIII. I. Identification, purification, and properties. J. Biol. Chem. 268: 25587-25593.
6. Bradsher, J.N., S. Tan, H.J. McLaury, J.W. Conaway, and R.C. Conaway. 1993b. RNA polymerase II transcription factor SIII. II. Functional properties and role in RNA chain elongation. J. Biol. Chem. 268: 25594-25603.
7. Brown, S.A., A.N. Imbalzano, and R.E. Kingston. 1996. Activator-dependent regulation of transcriptional pausing on nucleosomal templates. Genes & Dev. 10: 1479-1490.
8. Buermeyer, A.B., N.E. Thompson, L.A. Strasheim, R.R. Burgess, and P.J. Farnham. 1992. The HIP1 initiator element plays a role in determining the in vitro requirement of the dihydrofolate reductase gene promoter for the C-terminal domain of RNA polymerase II. Mol. Cell. Biol. 12: 2250-2259.
9. Burns, C.M. and J.P. Richardson. 1995. NusG is required to overcome a kinetic limitation to Rho function at an intragenic terminator. Proc. Natl. Acad. Sci. 92: 4738-4742.
10. Burova, E., S.C. Hung, V. Sagitov, B.L. Stitt, and M.E. Gottesman. 1995. Escherichia coli NusG protein stimulates transcription elongation rates in vivo and in vitro. J. Bacteriol. 177: 1388-1392.
11. Chiang, P.-W., E. Fogel, C.L. Jackson, K. Lieuallen, G. Lennon, X. Qu, S.-Q. Wang, and D.M. Kurnit. 1996a. Isolation, sequencing, and mapping of the human homologue of the yeast transcription factor, Spt5. Genomics 38: 421-424.
12. Chiang, P.-W., S.Q. Wang, P. Smithivas, W.J. Song, E. Crombez, A. Akhtar, R. Im, J. Greenfield, S. Ramamoorthy, M. Van Keuren et al. 1996b. Isolation and characterization of the human and mouse homologues (SUPT4H and Supt4h) of the yeast SPT4 gene. Genomics 34: 368-375.
13. Chodosh, L.A., A. Fire, M. Samuels, and P.A. Sharp. 1989. 5,6-Dichloro-1-β-D-ribofuranosylbenzimidazole inhibits transcription elongation by RNA polymerase II in vitro. J. Biol. Chem. 264: 2250-2257.
14. Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16: 10881-10890.
15. Dahmus, M.E. 1996. Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J. Biol. Chem. 271: 19009-19012.
16. Dignam, J.D., R.M. Lebovitz, and R.G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475-1489.
17. Dikstein, R., S. Ruppert, and R. Tjian. 1996. TAFII250 is a bipartite protein kinase that phosphorylates the basal transcription factor RAP74. Cell 84: 781-790.
18. Egyhazi, E. 1974. A tentative initiation inhibitor of chromosomal heterogeneous RNA synthesis. J. Mol Biol. 84: 173-183.
19. _. 1975. Inhibition of Balbiani ring RNA synthesis at the initiation level. Proc. Natl. Acad. Sci. 72: 947-950.
20. _. 1976. Initiation inhibition and reinitiation of the synthesis of heterogenous nuclear RNA in living cells. Nature 262: 319-321.
21. Frohman, M.A., M.K. Dush, and G.R. Martin. 1988. Rapid production of full-length cDNAs from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. 85: 8998-9002.
22. Granick, D. 1975. Nucleolar necklaces in chick embryo fibroblast cells. I. Formation of necklaces by dichlororibobenzimidazole and other adenosine analogues that decrease RNA synthesis and degrade preribosomes. J. Cell. Biol. 65: 398-417.
23. Greenblatt, J., J.R. Nodwell, and S.W. Mason. 1993. Transcriptional antitermination. Nature 364: 401-406.
24. Harlow, E. and D. Lane. 1988. Antibodies: A laboratory manual Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
25. Hartzog, G.A., M.A. Basrai, S.L. Ricupero-Hovasse, P. Hieter, and F. Winston. 1996. Identification and analysis of a functional human homolog of the SPT4 gene of Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 2848-2856.
26. Hartzog, G.A., T. Wada, H. Handa, and F. Winston. 1998. Evidence that Spt4, Spt5, and Spt6 control transcription elongation by RNA polymerase II in Saccharomyces cerevisiae. Genes & Dev. (this issue).
27. Hidaka, H., M. Inagaki, S. Kawamoto, and Y. Sasaki. 1984. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 23: 5036-5041.
28. Jones, K.A. 1997. Taking a new TAK on tat transactivation. Genes & Dev. 11: 2593-2599.
29. Kato, H., H. Sumimoto, P. Pognonec, C.H. Chen, C.A. Rosen, and R.G. Roeder. 1992. HIV-1 Tat acts as a processivity factor in vitro in conjunction with cellular elongation factors. Genes & Dev. 6: 655-666.
30. Krumm, A., T. Meulia, M. Brunvand, and M. Groudine. 1992. The block to transcriptional elongation within the human c-myc gene is determined in the promoter-proximal region. Genes & Dev. 6: 2201-2213.
31. Kyrpides, N.C., C.R. Woese, and C.A. Ouzounis. 1996. KOW: A novel motif linking a bacterial transcription factor with ribosomal proteins. Trends Biochem. Sci. 21: 425-426.
32. Li, J., R. Horwitz, S. McCracken, and J. Greenblatt. 1992. NusG, a new Escherichia coli elongation factor involved in transcriptional antitermination by the N protein of phage λ. J. Biol. Chem. 267: 6012-6019.
33. Li, J., S.W. Mason, and J. Greenblatt. 1993. Elongation factor NusG interacts with termination factor ρ to regulate termination and antitermination of transcription. Genes & Dev. 7: 161-172.
34. Makela, T.P., J.D. Parvin, J. Kim, L.J. Huber, P.A. Sharp, and R.A. Weinberg. 1995. A kinase-deficient transcription factor TFIIH is functional in basal and activated transcription. Proc. Natl. Acad. Sci. 92: 5174-5178.
35. Malik, S., K. Hisatake, H. Sumimoto, M. Horikoshi, and R.G. Roeder. 1991. Sequence of general transcription factor TFIIB and relationships to other initiation factors. Proc. Natl. Acad. Sci. 88: 9553-9557.
36. Malone, E.A., J.S. Fassler, and F. Winston. 1993. Molecular and genetic characterization of SPT4, a gene important for transcription initiation in Saccharomyces cerevisiae. Mol. Gen. Genet. 237: 449-459.
37. Mancebo, H.S., G. Lee, J. Flygare, J. Tomassini, P. Luu, Y. Zhu, J. Peng, C. Blau, D. Hazuda, D. Price, and O. Flores. 1997. P-TEFb kinase is required for HIV tat transcriptional activation in vivo and in vitro. Genes & Dev. 11: 2633-2644.
38. Marciniak, R.A. and P.A. Sharp. 1991. HIV-1 Tat protein promotes formation of more-processive elongation complexes. EMBO J. 10: 4189-4196.
39. Marshall, N.F. and D.H. Price. 1995. Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J. Biol. Chem. 270: 12335-12338.
40. Marshall, N.F., J. Peng, Z. Xie, and D.H. Price. 1996. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J. Biol. Chem. 271: 27176-27183.
41. Meggio, F., D. Shugar, and L.A. Pinna. 1990. Ribofuranosylbenzimidazole derivatives as inhibitors of casein kinase-2 and casein kinase-1. Eur. J. Biochem. 187: 89-94.
42. Mogridge, J., T.F. Mah, and J. Greenblatt. 1995. A protein-RNA interaction network facilitates the template-independent cooperative assembly on RNA polymerase of a stable antitermination complex containing the λ N protein. Genes & Dev. 9: 2831-2845.
43. O'Brien, T. and J.T. Lis. 1991. RNA polymerase II pauses at the 5′ end of the transcriptionally induced Drosophila hsp70 gene. Mol Cell. Biol. 11: 5285-5290.
44. Price, D.H., A.E. Sluder, and A.L. Greenleaf. 1989. Dynamic interaction between a Drosophila transcription factor and RNA polymerase II. Mol Cell. Biol. 9: 1465-1475.
45. Reines, D., J.W. Conaway, and R.C. Conaway. 1996. The RNA polymerase II general elongation factors. Trends Biochem. Sci. 21: 351-355.
46. Roeder, R.G. 1996. The role of general transcription factors in transcription by RNA polymerase II. Trends Biochem. Sci. 21: 327-335.
47. Rougvie, A.E. and J.T. Lis. 1988. The RNA polymerase II molecule at the 5′ end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell 54: 795-804.
48. Samuels, M., A. Fire, and P.A. Sharp. 1982. Separation and characterization of factors mediating accurate transcription by RNA polymerase II. J. Biol. Chem. 257: 14419-14427.
49. Sehgal, P.B., J.E. Darnell, and I. Tamm. 1976a. The inhibition by DRB (5,6-dichloro-1-β-D-ribofuranosylbenzimidazole) of hnRNA and mRNA production in HeLa cells. Cell 9: 473-480.
50. Sehgal, P.B., E. Derman, G.R. Molloy, I. Tamm, and J.E. Darnell. 1976b. 5,6-Dichloro-1-β-D-ribofuranosylbenzimidazole inhibits initiation of nuclear heterogeneous RNA chains in HeLa cells. Science 194: 431-433.
51. Sekimizu, K., N. Kobayashi, D. Mizuno, and S. Natori. 1976. Purification of a factor from Ehrlich ascites tumor cells specifically stimulating RNA polymerase II. Biochemistry 15: 5064-5070.
52. Serizawa, H., J.W. Conaway, and R.C. Conaway. 1993. Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription. Nature 363: 371-374.
53. Stachora, A.A., R.E. Schafer, M. Pohlmeier, G. Maier, and H. Ponstingl. 1997. Human Supt5h protein, a putative modulator of chromatin structure, is reversibly phosphorylated in mitosis. FEBS Lett. 409: 74-78.
54. Strobl, L.J. and D. Eick. 1992. Hold back of RNA polymerase II at the transcription start site mediates down-regulation of c-myc in vivo. EMBO J. 11: 3307-3314.
55. Sullivan, S.L. and M.E. Gottesman. 1992. Requirement for E. coli NusG protein in factor-dependent transcription termination. Cell 68: 989-994.
56. Swanson, M.S. and F. Winston. 1992. SPT4, SPT5 and SPT6 interactions: Effects on transcription and viability in Saccharomyces cerevisiae. Genetics 132: 325-336.
57. Swanson, M.S., E.A. Malone, and F. Winston. 1991. SPT5, an essential gene important for normal transcription in Saccharomyces cerevisiae, encodes and acidic nuclear protein with a carboxy-terminal repeat. Mol Cell. Biol. 11: 3009-3019.
58. Takada, R., Y. Nakatani, A. Hoffman, T. Kokubo, S. Hasegawa, R.G. Roeder, and M. Horikoshi. 1992. Identification of human TFIID components and direct interaction between a 250-kDa polypeptide and the TATA box-binding protein (TFIIDt). Proc. Natl. Acad. Sci. 89: 11809-11813.
59. Tamm, I., R. Hand, and L.A. Caliguiri. 1976. Action of dichlorobenzimidazole riboside on RNA synthesis in L-929 and HeLa cells. J. Cell. Biol. 69: 229-240.
60. Usuda, Y., A. Kubota, A.J. Berk, and H. Handa. 1991. Affinity purification of transcription factor IIA from HeLa cell nuclear extracts. EMBO J. 10: 2305-2310.
61. Wada, T., H. Watanabe, Y. Usuda, and H. Handa. 1991. Different biological activities of the hetero- and homodimers formed by the 47- and 43-kilodalton proteins of transcription factor ATF/E4TF3. J. Virol. 65: 557-564.
62. Wada, T., T. Takagi, Y. Yamaguchi, H. Kawase, M. Hiramoto, A. Ferdous, M. Takayama, K.A. Lee, H.C. Hurst, and H. Handa. 1996. Copurification of casein kinase II with transcription factor ATF/E4TF3. Nucleic Acids Res. 24: 876-884.
63. Wang, W., M. Carey, and J.D. Gralla. 1992. Polymerase II promoter activation: closed complex formation and ATP-driven start site opening. Science 255: 450-453.
64. Watanabe, H., J. Sawada, K. Yano, K. Yamaguchi, M. Goto, and H. Handa. 1993. cDNA cloning of transcription factor E4TF1 subunits with Ets and notch motifs. Mol. Cell. Biol. 13: 1385-1391.
65. Winston, F. 1992. Analysis of SPT genes: A genetic approach toward analysis of TFIID, histones and other transcription factors of yeast. In Transcriptional regulation, pp. 1271-1293. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
66. Winston, F. and M. Carlson. 1992. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 8: 387-391.
67. Yankulov, K., K. Yamashita, R. Roy, J.M. Egly, and D.L. Bentley. 1995. The transcriptional elongation inhibitor 5,6-dichloro-1-β-D-ribofuranosylbenzimidazole inhibits transcription factor IIH-associated protein kinase. J. Biol. Chem. 270: 23922-23925.
68. Yankulov, K.Y., M. Pandes, S. McCracken, D. Bouchard, and D.L. Bentley. 1996. TFIIH functions in regulating transcriptional elongation by RNA polymerase II in Xenopus oocytes. Mol Cell. Biol. 16: 3291-3299.
69. Zandomeni, R., D. Bunick, S. Ackerman, B. Mittleman, and R. Weinmann. 1983. Mechanism of action of DRB. III. Effect on specific in vitro initiation of transcription. J. Mol. Biol. 167: 561-574.
70. Zandomeni, R., M.C. Zandomeni, D. Shugar, and R. Weinmann. 1986. Casein kinase type II is involved in the inhibition by 5,6-dichloro-1-β-D-ribofuranosylbenzimidazole of specific RNA polymerase II transcription. J. Biol. Chem. 261: 3414-3419.
71. Zhou, Q. and P.A. Sharp. 1995. Novel mechanism and factor for regulation by HIV-1 Tat. EMBO J. 14: 321-328.
72. Zhu, Y., T. Pe'ery, J. Peng, Y. Ramanathan, N. Marshall, T. Marshall, B. Amendt, M.B. Mathews, and D.H. Price. 1997. Transcription elongation factor P-TEFb is required for HIV-1 tat transactivation in vitro. Genes & Dev. 11: 2622-2632.