The Myc transactivation domain promotes global phosphorylation of the RNA polymerase II carboxy-terminal domain independently of direct DNA binding

Molecular and Cellular Biology

Volumn 27, Issue 6, 2007, Pages 2059-2073

  Cowling, Victoria H ^a   Cole, Michael D ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 7; CYCLIN DEPENDENT KINASE 9; DNA; MESSENGER RNA; MUTANT PROTEIN; MYC PROTEIN; PROTEIN SUBUNIT; RNA POLYMERASE II; TRANSCRIPTION FACTOR IIH;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA BINDING MOTIF; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; ENZYME SUBUNIT; FIBROBLAST; GENE CONTROL; KNOCKOUT GENE; NONHUMAN; ONCOGENE MYC; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; RNA METABOLISM; RNA METHYLATION; RNA PROCESSING; TRANSACTIVATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; TRANSLATION REGULATION;

ANIMALS; CELL LINE; CELL PROLIFERATION; CELL SHAPE; CYCLIN-DEPENDENT KINASE 9; CYCLIN-DEPENDENT KINASES; CYCLINS; DNA; METHYLATION; MUTATION; PHOSPHORYLATION; POLYRIBOSOMES; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-MYC; RATS; RNA POLYMERASE II; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTOR TFIIH;

EID: 33947285072     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01828-06     Document Type: Article

References (59)

1. Adhikary, S., F. Marinoni, A. Hock, E. Hulleman, N. Popov, R. Beier, S. Bernard, M. Quarto, M. Capra, S. Goettig, U. Kogel, M. Scheffner, K. Helin, and M. Eilers. 2005. The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 123:409-421.
2. Amati, B., T. D. Littlewood, G. I. Evan, and H. Land. 1993. The c-Myc protein induces cell cycle progression and apoptosis through dimerization with Max. EMBO J. 12:5083-5087.
3. Arabi, A., S. Wu, K. Ridderstrale, H. Bierhoff, C. Shiue, K. Fatyol, S. Fahlen, P. Hydbring, O. Soderberg, I. Grummt, L. G. Larsson, and A. P. Wright. 2005. c-Myc associates with ribosomal DNA and activates RNA polymerase I transcription. Nat. Cell Biol. 7:303-310.
4. Armelin, H. A., M. C. Armelin, K. Kelly, T. Stewart, P. Leder, B. H. Cochran, and C. D. Stiles. 1984. Functional role for c-myc in mitogenic response to platelet-derived growth factor. Nature 10:55-660.
5. Bentley, D. L. 2005. Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr. Opin. Cell Biol. 17:251-256.
6. Blackwell, T. K., L. Kretzner, E. M. Blackwood, R. N. Eisenman, and H. Weintraub. 1990. Sequence-specific DNA binding by the c-Myc protein. Science 250:1149-1151.
7. Bochnig, P., R. Reuter, P. Bringmann, and R. Luhrmann. 1987. A monoclonal antibody against 2,2,7-trimethylguanosine that reacts with intact, class U, small nuclear ribonucleoproteins as well as with 7-methylguanosine- capped RNAs. Eur. J. Biochem. 68:61-467.
8. Boxer, L. M., and C. V. Dang. 2001. Translocations involving c-myc and c-myc function. Oncogene 20:5595-5610.
9. Brewer, G., and J. Ross. 1990. Messenger RNA turnover in cell-free extracts. Methods Enzymol. 181:202-209.
10. Cawley, S., S. Bekiranov, H. H. Ng, P. Kapranov, E. A. Sekinger, D. Kampa, A. Piccolboni, V. Sementchenko, J. Cheng, A. J. Williams, R. Wheeler, B. Wong, J. Drenkow, M. Yamanaka, S. Patel, S. Brubaker, H. Tammana, G. Helt, K. Struhl, and T. R. Gingeras. 2004. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 116:499-509.
11. Cho, E. J., T. Takagi, C. R. Moore, and S. Buratowski. 1997. mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 1:319-3326.
12. Cole, M. D. 1986. The myc oncogene: its role in transformation and differentiation. Annu. Rev. Genet. 0:61-385.
13. Coppola, J. A., A. S. Field, and D. S. Luse. 1983. Promoter-proximal pausing by RNA polymerase II in vitro: transcripts shorter than 20 nucleotides are not capped. Proc. Natl. Acad. Sci. USA 80:1251-1255.
14. 2 arrest. Mol. Cell. Biol. 26:4226-4239.
15. Cowling, V. H., and M. D. Cole. 2006. Mechanism of transcriptional activation by the Myc oncoproteins. Semin. Cancer Biol. 16:242-252.
16. Dang, C. V., K. A. O'Donnell, K. I. Zeller, T. Nguyen, R. C. Osthus, and F. Li. 2006. The c-Myc target gene network. Semin. Cancer Biol. 16:253-264.
17. DiRenzo, J., S. Signoretti, N. Nakamura, R. Rivera-Gonzalez, W. Sellers, M. Loda, and M. Brown. 2002. Growth factor requirements and basal phenotype of an immortalized mammary epithelial cell line. Cancer Res. 62:89-98.
18. Eberhardy, S. R., and P. J. Farnham. 2002. Myc recruits P-TEFb to mediate the final step in the transcriptional activation of the cad promoter. J. Biol. Chem. 277:40156-40162.
19. Eilers, M., D. Picard, K. R. Yamamoto, and J. M. Bishop. 1989. Chimaeras of Myc oncoprotein and steroid receptors cause hormone-dependent transformation of cells. Nature 340:66-68.
20. Fernandez, P. C., S. R. Frank, L. Wang, M. Schroeder, S. Liu, J. Greene, A. Cocito, and B. Amati. 2003. Genomic targets of the human c-Myc protein. Genes Dev. 17:1115-1129.
21. Grandori, C., N. Gomez-Roman, Z. A. Felton-Edkins, C. Ngouenet, D. A. Galloway, R. N. Eisenman, and R. J. White. 2005. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat. Cell Biol. 7:311-318.
22. Grewal, S. S., L. Li, A. Orian, R. N. Eisenman, and B. A. Edgar. 2005. Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nat. Cell Biol. 7:295-302.
23. Harper, J. W., and S. J. Elledge. 1998. The role of Cdk7 in CAK function, a retro-retrospective. Genes Dev. 12:285-289.
24. Kim, S. Y., A. Herbst, K. A. Tworkowski, S. E. Salghetti, and W. P. Tansey. 2003. Skp2 regulates Myc protein stability and activity. Mol. Cell 11:1177-1188.
25. Komarnitsky, P., E. J. Cho, and S. Buratowski. 2000. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14:2452-2460.
26. Li, Z., S. Van Calcar, C. Qu, W. K. Cavenee, M. Q. Zhang, and B. Ren. 2003. A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells. Proc. Natl. Acad. Sci. USA 100:8164-8169.
27. Lutz, W., M. Stohr, J. Schurmann, A. Wenzel, A. Lohr, and M. Schwab. 1996. Conditional expression of N-myc in human neuroblastoma cells increases expression of alpha-prothymosin and ornithine decarboxylase and accelerates progression into S-phase early after mitogenic stimulation of quiescent cells. Oncogene 13:803-812.
28. Mäkelä, 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. USA 92:5174-5178.
29. Maniatis, T., and R. Reed. 2002. An extensive network of coupling among gene expression machines. Nature 416:499-506.
30. Mao, D. Y., J. D. Watson, P. S. Yan, D. Barsyte-Lovejoy, F. Khosravi, W. W. Wong, P. J. Farnham, T. H. Huang, and L. Z. Penn. 2003. Analysis of Myc bound loci identified by CpG island arrays shows that Max is essential for Myc-dependent repression. Curr. Biol. 13:882-886.
31. Mateyak, M. K., A. J. Obaya, S. Adachi, and J. M. Sedivy. 1997. Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Differ. 8:1039-1048.
32. Mateyak, M. K., A. J. Obaya, and J. M. Sedivy. 1999. c-Myc regulates cyclin D-Cdk4 and -Cdk6 activity but affects cell cycle progression at multiple independent points. Mol. Cell. Biol. 19:4672-4683.
33. McCracken, S., N. Fong, E. Rosonina, K. Yankulov, G. Brothers, D. Siderovski, A. Hessel, S. Foster, S. Shuman, and D. L. Bentley. 1997. 5′-capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev. 11:3306-3318.
34. McMahon, S. B., H. A. Van Buskirk, K. A. Dugan, T. D. Copeland, and M. D. Cole. 1998. The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 94:363-374.
35. McMahon, S. B., M. A. Wood, and M. D. Cole. 2000. The essential cofactor TRRAP recruits the histone acetyltransferase hGCN5 to c-Myc. Mol. Cell. Biol. 20:556-562.
36. Mezquita, P., S. S. Parghi, K. A. Brandvold, and A. Ruddell. 2005. Myc regulates VEGF production in B cells by stimulating initiation of VEGF mRNA translation. Oncogene 24:889-901.
37. Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131-134.
38. Moteki, S., and D. Price. 2002. Functional coupling of capping and transcription of mRNA. Mol. Cell 10:599-609.
39. Muratani, M., C. Rung, K. M. Shokat, and W. P. Tansey. 2005. The F box protein Dsg1/Mdm30 is a transcriptional coactivator that stimulates Gal4 turnover and cotranscriptional mRNA processing. Cell 120:887-899.
40. Muthukrishnan, S., G. W. Both, Y. Furuichi, and A. J. Shatkin. 1975. 5′-terminal 7-methylguanosine in eukaryotic mRNA is required for translation. Nature 255:33-37.
41. Obaya, A. J., M. K. Mateyak, and J. M. Sedivy. 1999. Mysterious liaisons: the relationship between c-Myc and the cell cycle. Oncogene 18:2934-2941.
42. O'Brien, T., S. Hardin, A. Greenleaf, and J. T. Lis. 1994. Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation. Nature 370:75-77.
43. O'Connell, B. C., A. F. Cheung, C. P. Simkevich, W. Tam, X. Ren, M. K. Mateyak, and J. M. Sedivy. 2003. A large scale genetic analysis of c-Myc-regulated gene expression patterns. J. Biol. Chem. 278:12563-12573.
44. Orian, A., B. van Steensel, J. Delrow, H. J. Bussemaker, L. Li, T. Sawado, E. Williams, L. W. Loo, S. M. Cowley, C. Yost, S. Pierce, B. A. Edgar, S. M. Parkhurst, and R. N. Eisenman. 2003. Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev. 17:1101-1114.
45. Pelengaris, S., M. Khan, and G. Evan. 2002. c-MYC: more than just a matter of life and death. Nat. Rev. Cancer 2:764-776.
46. Rasmussen, E. B., and J. T. Lis. 1993. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc. Natl. Acad. Sci. USA 0:923-7927.
47. Schmidt, E. V. 2004. The role of c-myc in regulation of translation initiation. Oncogene 23:3217-3221.
48. Schroeder, S. C., B. Schwer, S. Shuman, and D. Bentley. 2000. Dynamic association of capping enzymes with transcribing RNA polymerase II. Genes Dev. 14:2435-2440.
49. Schuhmacher, M., F. Kohlhuber, M. Holzel, C. Kaiser, H. Burtscher, M. Jarsch, G. W. Bornkamm, G. Laux, A. Polack, U. H. Weidle, and D. Eick. 2001. The transcriptional program of a human B cell line in response to Myc. Nucleic Acids Res. 29:397-406.
50. Schwer, B., X. Mao, and S. Shuman. 1998. Accelerated mRNA decay in conditional mutants of yeast mRNA capping enzyme. Nucleic Acids Res. 26:2050-2057.
51. Schwer, B., N. Saha, X. Mao, H. W. Chen, and S. Shuman. 2000. Structure-function analysis of yeast mRNA cap methyltransferase and high-copy suppression of conditional mutants by AdoMet synthase and the ubiquitin conjugating enzyme Cdc34p. Genetics 155:1561-1576.
52. Sims, R. J., III, S. S. Mandal, and D. Reinberg. 2004. Recent highlights of RNA-polymerase-II-mediated transcription. Curr. Opin. Cell Biol. 6:63-271.
53. Sommer, A., K. Bousset, E. Kremmer, M. Austen, and B. Luscher. 1998. Identification and characterization of specific DNA-binding complexes containing members of the Myc/Max/Mad network of transcriptional regulators. J. Biol. Chem. 273:6632-6642.
54. Stone, J., T. de Lange, G. Ramsay, E. Jakobovits, J. M. Bishop, H. Varmus, and W. Lee. 1987. Definition of regions in human c-myc that are involved in transformation and nuclear localization. Mol. Cell. Biol. 7:1697-1709.
55. Takagi, T., C. R. Moore, F. Diehn, and S. Buratowski. 1997. An RNA 5′-triphosphatase related to the protein tyrosine phosphatases. Cell 89:867-873.
56. von der Lehr, N., S. Johansson, S. Wu, F. Bahram, A. Castell, C. Cetinkaya, P. Hydbring, I. Weidung, K. Nakayama, K. I. Nakayama, O. Soderberg, T. K. Kerppola, and L. G. Larsson. 2003. The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. Mol. Cell 1:189-1200.
57. Welcker, M., A. Orian, J. Jin, J. E. Grim, J. W. Harper, R. N. Eisenman, and B. E. Clurman. 2004. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc. Natl. Acad. Sci. USA 101:9085-9090.
58. Yada, M., S. Hatakeyama, T. Kamura, M. Nishiyama, R. Tsunematsu, H. Imaki, N. Ishida, F. Okumura, K. Nakayama, and K. I. Nakayama. 2004. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J. 23:2116-2125.
59. Yue, Z., E. Maldonado, R. Pillutla, H. Cho, D. Reinberg, and A. J. Shatkin. 1997. Mammalian capping enzyme complements mutant Saccharomyces cerevisiae lacking mRNA guanylyltransferase and selectively binds the elongating form of RNA polymerase II. Proc. Natl. Acad. Sci. USA 94:12898-12903.