Transcriptional properties of mammalian elongin a and its role in stress response

Journal of Biological Chemistry

Volumn 288, Issue 34, 2013, Pages 24302-24315

  Kawauchi, Junya ^a   Inoue, Makoto ^a   Fukuda, Mizue ^a   Uchida, Yohei ^a   Yasukawa, Takashi ^b   Conaway, Ronald C ^c,d   Conaway, Joan W ^c,d   Aso, Teijiro ^b   Kitajima, Shigetaka ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b KOCHI MEDICAL SCHOOL   (Japan)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KINASE INHIBITORS; RATE-LIMITING STEPS; RNA POLYMERASE II; STRESS RESPONSE GENES; STRESS RESPONSE REGULATORS; STRUCTURE-FUNCTION STUDIES; TRANSCRIPTIONAL ELONGATIONS; TRANSCRIPTIONAL PROPERTIES;

CHEMICAL ACTIVATION; ELONGATION; GENES; MAMMALS; RNA;

TRANSCRIPTION;

ACTIVATING TRANSCRIPTION FACTOR 3; DOXORUBICIN; ELONGIN; ELONGIN A; PROTEIN P21; RNA POLYMERASE II; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; ATF3 GENE; CHEMICAL GENETICS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE; GENETIC REGULATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; P21 GENE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA TRANSCRIPTION; RNA TRANSLATION; STRESS; UBIQUITINATION;

ATF3; ELONGIN A; GENE REGULATION; MAMMAL; RNA POLYMERASE II; STRESS RESPONSE; TRANSCRIPTION ELONGATION FACTORS;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; ENZYME INHIBITORS; HELA CELLS; HUMANS; MICE; RATS; RNA POLYMERASE II; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION, GENETIC;

EID: 84883155221     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.496703     Document Type: Article

References (68)

1. Shilatifard, A., Conaway, R. C., and Conaway, J. W. (2003) The RNA polymerase II elongation complex. Annu. Rev. Biochem. 72, 693-715
2. Sims, R. J., 3rd, Belotserkovskaya, R., and Reinberg, D. (2004) Elongation by RNA polymerase II: the short and long of it. Genes Dev. 18, 2437-2468
3. Wada, T., Takagi, T., Yamaguchi, Y., Ferdous, A., Imai, T., Hirose, S., Sugimoto, S., Yano, K., Hartzog, G. A., Winston, F., Buratowski, S., and Handa, H. (1998) DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev. 12, 343-356
4. Yamaguchi, Y., Takagi, T., Wada, T., Yano, K., Furuya, A., Sugimoto, S., Hasegawa, J., and Handa, H. (1999) NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97, 41-51
5. Saunders, A., Core, L. J., and Lis, J. T. (2006) Breaking barriers to transcription elongation. Nat. Rev. Mol. Cell Biol. 7, 557-567
6. Zhou, Q., Li, T., and Price, D. H. (2012) RNA polymerase II elongation control. Annu. Rev. Biochem. 81, 119-143
7. 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
8. Otero, G., Fellows, J., Li, Y., de Bizemont, T., Dirac, A. M., Gustafsson, C. M., Erdjument-Bromage, H., Tempst, P., and Svejstrup, J. Q. (1999) Elongator, a multisubunit component of a novel RNA polymerase II holoenzyme for transcriptional elongation. Mol. Cell 3, 109-118
9. Shilatifard, A., Lane, W. S., Jackson, K. W., Conaway, R. C., and Conaway, J. W. (1996) An RNA polymerase II elongation factor encoded by the human ELL gene. Science 271, 1873-1876
10. Kong, S. E., Banks, C. A., Shilatifard, A., Conaway, J. W., and Conaway, R. C. (2005) ELL-associated factors 1 and 2 are positive regulators of RNA polymerase II elongation factor ELL. Proc. Natl. Acad. Sci. U.S.A. 102, 10094-10098
11. Price, D. H., Sluder, A. E., and Greenleaf, A. L. (1989) Dynamic interaction between a Drosophila transcription factor and RNA polymerase II. Mol. Cell. Biol. 9, 1465-1475
12. Tan, S., Aso, T., Conaway, R. C., and Conaway, J. W. (1994) Roles for both the RAP30 and RAP74 subunits of transcription factor IIF in transcription initiation and elongation by RNA polymerase II. J. Biol. Chem. 269, 25684-25691
13. Kitajima, S., Chibazakura, T., Yonaha, M., and Yasukochi, Y. (1994) Regulation of the human general transcription initiation factor TFIIF by phosphorylation. J. Biol. Chem. 269, 29970-29977
14. Selby, C. P., and Sancar, A. (1997) Cockayne syndrome group B protein enhances elongation by RNA polymerase II. Proc. Natl. Acad. Sci. U.S.A. 94, 11205-11209
15. Bradsher, J. N., Jackson, K. W., Conaway, R. C., and Conaway, J. W. (1993) RNA polymerase II transcription factor SIII. I. Identification, purification, and properties. J. Biol. Chem. 268, 25587-25593
16. Bradsher, J. N., Tan, S., McLaury, H. J., Conaway, J. W., and Conaway, R. C. (1993) RNA polymerase II transcription factor SIII. II. Functional properties and role in RNA chain elongation. J. Biol. Chem. 268, 25594-25603
17. Wind, M., and Reines, D. (2000) Transcription elongation factor SII. BioEssays 22, 327-336
18. Fish, R. N., and Kane, C. M. (2002) Promoting elongation with transcript cleavage stimulatory factors. Biochim. Biophys. Acta 1577, 287-307
19. Yasukawa, T., Bhatt, S., Takeuchi, T., Kawauchi, J., Takahashi, H., Tsutsui, A., Muraoka, T., Inoue, M., Tsuda, M., Kitajima, S., Conaway, R. C., Conaway, J. W., Trainor, P. A., and Aso, T. (2012) Transcriptional elongation factor Elongin A regulates retinoic acid-induced gene expression during neuronal differentiation. Cell Rep. 2, 1129-1136
20. Garrett, K. P., Tan, S., Bradsher, J. N., Lane, W. S., Conaway, J. W., and Conaway, R. C. (1994) Molecular cloning of an essential subunit of RNA polymerase II elongation factor SIII. Proc. Natl. Acad. Sci. U.S.A. 91, 5237-5241
21. Aso, T., Lane, W. S., Conaway, J. W., and Conaway, R. C. (1995) Elongin (SIII): a multisubunit regulator of elongation by RNA polymerase II. Science 269, 1439-1443
22. Yasukawa, T., Sugimura, K., Fukuda, M., Yamazaki, K., Kitajima, S., Okumura, K., and Aso, T. (2007) Functional characterization of a mammalian transcription factor, Elongin A. Biochem. Biophys. Res. Commun. 352, 237-243
23. Aso, T., Yamazaki, K., Amimoto, K., Kuroiwa, A., Higashi, H., Matsuda, Y., Kitajima, S., and Hatakeyama, M. (2000) Identification and characterization of Elongin A2, a new member of the Elongin family of transcription elongation factors, specifically expressed in the testis. J. Biol. Chem. 275, 6546-6552
24. Yamazaki, K., Guo, L., Sugahara, K., Zhang, C., Enzan, H., Nakabeppu, Y., Kitajima, S., and Aso, T. (2002) Identification and biochemical characterization of a novel transcription elongation factor, Elongin A3. J. Biol. Chem. 277, 26444-26451
25. Aso, T., Haque, D., Barstead, R. J., Conaway, R. C., and Conaway, J. W. (1996) The inducible elongin A elongation activation domain: structure, function and interaction with the elongin BC complex. EMBO J. 15, 5557-5566
26. Yasukawa, T., Kamura, T., Kitajima, S., Conaway, R. C., Conaway, J. W., and Aso, T. (2008) Mammalian Elongin A complex mediates DNA-damage-induced ubiquitylation and degradation of Rpb1. EMBO J. 27, 3256-3266
27. Harreman, M., Taschner, M., Siqurdsson, S., Anindya, R., Reid, J., Somesh, B., Kong, S. E., Banks, C. A., Conaway, R. C., Conaway, J. W., and Svejstrup, J. Q. (2009) Distinct ubiquitin ligases act sequentially for RNA polymerase II polyubiquitylation. Proc. Natl. Acad. Sci. U.S.A. 106, 20705-20710
28. Yamazaki, K., Aso, T., Ohnishi, Y., Ohno, M., Tamura, K., Shuin, T., Kitajima, S., and Nakabeppu, Y. (2003) Mammalian elongin A is not essential for cell viability but is required for proper cell cycle progression with limited alteration of gene expression. J. Biol. Chem. 278, 13585-13589
29. Miyata, K., Yasukawa, T., Fukuda, M., Takeuchi, T., Yamazaki, K., Sakumi, K., Tamamori-Adachi, M., Ohnishi, Y., Ohtsuki, Y., Nakabeppu, Y., Kitajima, S., Onishi, S., and Aso, T. (2007) Induction of apoptosis and cellular senescence in mice lacking transcription elongation factor, Elongin A. Cell Death Differ. 14, 716-726
30. Levine, M. (2011) Paused RNA polymerase II as a developmental checkpoint. Cell 145, 502-511
31. Lis, J. T., Mason, P., Peng, J., Price, D. H., and Werner, J. (2000) P-TEFb kinase recruitment and function at heat shock loci. Genes Dev. 14, 792-803
32. Andrulis, E. D., Guzmán, E., Döring, 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
33. Wu, C. H., Yamaguchi, Y., Benjamin, L. R., Horvat-Gordon, M., Washinsky, J., Enerly, E., Larsson, J., Lambertsson, A., Handa, H., and Gilmour, D. (2003) NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila. Genes Dev. 17, 1402-1414
34. 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
35. Gerber, M., Tenney, K., Conaway, J. W., Conaway, R. C., Eissenberg, J. C., and Shilatifard, A. (2005) Regulation of heat shock gene expression by RNA polymerase II elongation factor, Elongin A. J. Biol. Chem. 280, 4017-4020
36. Yamada, T., Yamaguchi, Y., Inukai, N., Okamoto, S., Mura, T., and Handa, H. (2006) P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol. Cell 21, 227-237
37. Ryser, S., Fujita, T., Tortola, S., Piuz, I., and Schlegel, W. (2007) The rate of c-fos transcription in vivo is continuously regulated at the level of elongation by dynamic stimulus-coupled recruitment of positive transcription elongation factor b. J. Biol. Chem. 282, 5075-5084
38. Aida, M., Chen, Y., Nakajima, K., Yamaguchi, Y., Wada, T., and Handa, H. (2006) Transcriptional pausing caused by NELF plays a dual role in regulating immediate-early expression of the junB gene. Mol. Cell. Biol. 26, 6094-6104
39. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
40. Hua, B., Tamamori-Adachi, M., Luo, Y., Tamura, K., Morioka, M., Fukuda, M., Tanaka, Y., and Kitajima, S. (2006) A splice variant of stress response gene ATF3 counteracts NF-κB-dependent anti-apoptosis through inhibiting recruitment of CREB-binding protein/p300 coactivator. J. Biol. Chem. 281, 1620-1629
41. Dignam, J. D., Lebovitz, R. M., and Roeder, R. G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489
42. van Steensel, B., van Binnendijk, E. P., Hornsby, C. D., van der Voort, H. T., Krozowski, Z. S., de Kloet, E. R., and van Driel, R. (1996) Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons. J. Cell Sci. 109, 787-792
43. Morita, S., Kojima, T., and Kitamura, T. (2000) Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7, 1063-1066
44. Tamura, K., Hua, B., Adachi, S., Guney, I., Kawauchi, J., Morioka, M., Tamamori-Adachi, M., Tanaka, Y., Nakabeppu, Y., Sunamori, M., Sedivy, J. M., and Kitajima, S. (2005) Stress response gene ATF3 is a target of c-myc in serum-induced cell proliferation. EMBO J. 24, 2590-2601
45. Miyazaki, K., Inoue, S., Yamada, K., Watanabe, M., Liu, Q., Watanabe, T., Adachi, M. T., Tanaka, Y., and Kitajima, S. (2009) Differential usage of alternate promoters of the human stress response gene ATF3 in stress response and cancer cells. Nucleic Acids Res. 37, 1438-1451
46. 2-terminal kinase and promoter response element. Blood 96, 2140-2148
47. Zhang, C., Gao, C., Kawauchi, J., Hashimoto, Y., Tsuchida, N., and Kitajima, S. (2002) Transcriptional activation of the human stress-inducible transcriptional repressor ATF3 gene promoter by p53. Biochem. Biophys. Res. Commun. 297, 1302-1310
48. Pan, G., Aso, T., and Greenblatt, J. (1997) Interaction of elongation factors TFIIS and elongin A with a human RNA polymerase II holoenzyme capable of promoter-specific initiation and responsive to transcriptional activators. J. Biol. Chem. 272, 24563-24571
49. Kim, B., Nesvizhskii, A. I., Rani, P. G., Hahn, S., Aebersold, R., and Ranish, J. A. (2007) The transcription elongation factor TFIIS is a component of RNA polymerase II preinitiation complexes. Proc. Natl. Acad. Sci. U.S.A. 104, 16068-16073
50. Guglielmi, B., Soutourina, J., Esnault, C., and Werner, M. (2007) TFIIS elongation factor and Mediator act in conjunction during transcription initiation in vivo. Proc. Natl. Acad. Sci. U.S.A. 104, 16062-16067
51. Takahashi, H., Parmely, T. J., Sato, S., Tomomori-Sato, C., Banks, C. A., Kong, S. E., Szutorisz, H., Swanson, S. K., Martin-Brown, S., Washburn, M. P., Florens, L., Seidel, C. W., Lin, C., Smith, E. R., Shilatifard, A., Conaway, R. C., and Conaway, J. W. (2011) Human Mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 146, 92-104
52. Grande, M. A., van der Kraan, I., de Jong, L., and van Driel, R. (1997) Nuclear distribution of transcription factors in relation to sites of transcription and RNA polymerase II. J. Cell Sci. 110, 1781-1791
53. Zeng, C., Kim, E., Warren, S. L., and Berget, S. M. (1997) Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity. EMBO J. 16, 1401-1412
54. Bregman, D. B., Du, L., van der Zee, S., and Warren, S. L. (1995) Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129, 287-298
55. Roeder, R. G. (1996) The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem. Sci. 21, 327-335
56. Yan, Q., Moreland, R. J., Conaway, J. W., and Conaway, R. C (1999) Dual roles for transcription factor IIF in promoter escape by RNA polymerase II. J. Biol. Chem. 274, 35668-35675
57. Pokholok, D. K., Hannett, N. M., and Young, R. A. (2002) Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell 9, 799-809
58. Hai, T., Wolfgang, C. D., Marsee, D. K., Allen, A. E., and Sivaprasad, U. (1999) ATF3 and stress responses. Gene Expr. 7, 321-335
59. Lin, C., Garrett, A. S., De Kumar, B., Smith, E. R., Gogol, M., Seidel, C., Krumlauf, R., and Shilatifard, A. (2011) Dynamic transcriptional events in embryonic stem cells mediated by the super elongation complex (SEC). Genes Dev. 25, 1486-1498
60. Larochelle, S., Amat, R., Glover-Cutter, K., Sansó, M., Zhang, C., Allen, J. J., Shokat, K. M., Bentley D. L., and Fisher, R. P. (2012) Cyclin-dependent kinase control of the initiation-to-elongation switch of RNA polymerase II. Nat. Struct. Mol. Biol. 19, 1108-1115
61. Cheng, B., Li, T., Rahl, P. B., Adamson, T. E., Loudas, N. B., Guo, J., Varzavand, K., Cooper, J. J., Hu, X., Gnatt, A., Young, R. A., and Price D. H. (2012) Functional association of Gdown1 with RNA polymerase II poised on human genes. Mol. Cell 45, 38-50
62. Colgan, J., and Manley, J. L. (1992) TFIID can be rate limiting in vivo for TATA-containing, but not TATA-lacking, RNA polymerase II promoters. Genes Dev. 6, 304-315
63. Takagi, Y., Conaway, R. C., and Conaway, J. W. (1996) Characterization of elongin C functional domains required for interaction with elongin B and activation of elongin A. J. Biol. Chem. 271, 25562-25568
64. Gerber, M., Eissenberg, J. C., Kong, S., Tenney, K., Conaway, J. W., Conaway, R. C., and Shilatifard, A. (2004) In vivo requirement of the RNA polymerase II elongation factor elongin A for proper gene expression and development. Mol. Cell. Biol. 24, 9911-9919
65. Booth, V., Koth, C. M., Edwards, A. M., and Arrowsmith, C. H. (2000) Structure of a conserved domain common to the transcription factors TFIIS, elongin A, and CRSP70. J. Biol. Chem. 275, 31266-31268
66. Wery, M., Shematorova, E., Van Driessche, B., Vandenhaute, J., Thuriaux, P., and Van Mullem, V. (2004) Members of the SAGA and Mediator complexes are partners of the transcription elongation factor TFIIS. EMBO J. 23, 4232-4242
67. Bhat, K. P., and Greer, S. F. (2011) Proteolytic and non-proteolytic roles of ubiquitin and the ubiquitin proteasome system in transcriptional regulation. Biochim. Biophys. Acta 1809, 150-155
68. Selth, L. A., Sigurdsson, S., and Svejstrup, J. Q. (2010) Transcript elongation by RNA polymerase II. Annu. Rev. Biochem. 79, 271-293