Evidence of the involvement of O-GlcNAc-modified human RNA polymerase II CTD in transcription in vitro and in vivo

Journal of Biological Chemistry

Volumn 287, Issue 28, 2012, Pages 23549-23561

  Ranuncolo, Stella M ^a   Ghosh, Salil ^b   Hanover, John A ^b   Hart, Gerald W ^c   Lewis, Brian A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; IN-VITRO; N-ACETYLGLUCOSAMINIDASE; POLYMERASE II; PREINITIATION COMPLEX; REGULATION OF TRANSCRIPTION; RNA POLYMERASE II; SERINE RESIDUES;

AMINO ACIDS; MACHINERY; RNA; TRANSCRIPTION;

POLYMERS;

ACETYLGLUCOSAMINIDASE; N ACETYLGLUCOSAMINE; RNA POLYMERASE II; SERINE; SHORT HAIRPIN RNA;

ARTICLE; B LYMPHOCYTE; CARBOXY TERMINAL SEQUENCE; ENZYME INHIBITION; ENZYME MODIFICATION; ENZYME SUBSTRATE; EUKARYOTE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

ACETYLGLUCOSAMINE; ACETYLGLUCOSAMINIDASE; BINDING SITES; BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; N-ACETYLGLUCOSAMINYLTRANSFERASES; OXIMES; PHENYLCARBAMATES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA POLYMERASE II; SERINE; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 84863610013     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.330910     Document Type: Article

References (55)

1. Dahmus, M. E. (1996) Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J. Biol. Chem. 271, 19009-19012
2. Phatnani, H. P., and Greenleaf, A. L. (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20, 2922-2936 (Pubitemid 44771726)
3. Saunders, A., Core, L. J., and Lis, J. T. (2006) Breaking barriers to transcription elongation. Nat. Rev. Mol. Cell Biol. 7, 557-567 (Pubitemid 44325347)
4. Egloff, S., and Murphy, S. (2008) Cracking the RNA polymerase II CTD code. Trends Genet. 24, 280-288
5. 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 (Pubitemid 39362887)
6. Kang, M. E., and Dahmus, M. E. (1993)RNApolymerases IIA and IIO have distinct roles during transcription from the TATA-less murine dihydrofolate reductase promoter. J. Biol. Chem. 268, 25033-25040
7. Chesnut, J. D., Stephens, J. H., and Dahmus, M. E. (1992) The interaction of RNA polymerase II with the adenovirus-2 major late promoter is precluded by phosphorylation of the C-terminal domain of subunit IIa. J. Biol. Chem. 267, 10500-10506
8. Laybourn, P. J., and Dahmus, M. E. (1990) Phosphorylation of RNA polymerase IIA occurs subsequent to interaction with the promoter and before the initiation of transcription. J. Biol. Chem. 265, 13165-13173
9. Payne, J. M., Laybourn, P. J., and Dahmus, M. E. (1989) The transition of RNA polymerase II from initiation to elongation is associated with phosphorylation of the carboxyl-terminal domain of subunit IIa. J. Biol. Chem. 264, 19621-19629 (Pubitemid 20008067)
10. Lu, H., Flores, O., Weinmann, R., and Reinberg, D. (1991) The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex. Proc. Natl. Acad. Sci. U.S.A. 88, 10004-10008 (Pubitemid 21915763)
11. Buratowski, S., and Sharp, P. A. (1990) Transcription initiation complexes and upstream activation with RNA polymerase II lacking the C-terminal domain of the largest subunit. Mol. Cell. Biol. 10, 5562-5564 (Pubitemid 20293904)
12. Kim, W. Y., and Dahmus, M. E. (1989) The major late promoter of adenovirus-2 is accurately transcribed by RNA polymerases IIO, IIA, and IIB. J. Biol. Chem. 264, 3169-3176
13. Mäkelä, T. P., Tassan, J. P., Nigg, E. A., Frutiger, S., Hughes, G. J., and Weinberg, R. A. (1994)Acyclin associated with the CDK-activating kinase MO15. Nature 371, 254-257 (Pubitemid 24293025)
14. Serizawa, H., Conaway, J. W., and Conaway, R. C. (1993) Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription. Nature 363, 371-374 (Pubitemid 23161537)
15. Lux, C., Albiez, H., Chapman, R. D., Heidinger, M., Meininghaus, M., Brack-Werner, R., Lang, A., Ziegler, M., Cremer, T., and Eick, D. (2005) Transition from initiation to promoter proximal pausing requires the CTD of RNA polymerase II. Nucleic Acids Res. 33, 5139-5144 (Pubitemid 41487822)
16. Meininghaus, M., Chapman, R. D., Horndasch, M., and Eick, D. (2000) Conditional expression of RNA polymerase II in mammalian cells. Deletion of the carboxyl-terminal domain of the large subunit affects early steps in transcription. J. Biol. Chem. 275, 24375-24382 (Pubitemid 30626527)
17. Gerber, H. P., Hagmann, M., Seipel, K., Georgiev, O., West, M. A., Litingtung, Y., Schaffner, W., and Corden, J. L. (1995) RNA polymerase II C-terminal domain required for enhancer-driven transcription. Nature 374, 660-662
18. Kim, Y. J., Björklund, S., Li, Y., Sayre, M. H., and Kornberg, R. D. (1994) A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell 77, 599-608 (Pubitemid 24153999)
19. Koh, S. S., Ansari, A. Z., Ptashne, M., and Young, R. A. (1998) An activator target in the RNA polymerase II holoenzyme. Mol. Cell 1, 895-904 (Pubitemid 128379073)
20. Liao, S. M., Taylor, I. C., Kingston, R. E., and Young, R. A. (1991) RNA polymerase II carboxy-terminal domain contributes to the response to multiple acidic activators in vitro. Genes Dev. 5, 2431-2440 (Pubitemid 21905930)
21. Myers, L. C., Gustafsson, C. M., Bushnell, D. A., Lui, M., Erdjument-Bromage, H., Tempst, P., and Kornberg, R. D. (1998) The Med proteins of yeast and their function through the RNA polymerase II carboxy-terminal domain. Genes Dev. 12, 45-54 (Pubitemid 28083657)
22. Thompson, C. M., Koleske, A. J., Chao, D. M., and Young, R. A. (1993) A multisubunit complex associated with the RNA polymerase II CTD and TATA-binding protein in yeast. Cell 73, 1361-1375 (Pubitemid 23201149)
23. Kelly, W. G., Dahmus, M. E., and Hart, G. W. (1993) RNA polymerase II is a glycoprotein. Modification of the COOH-terminal domain by O-GlcNAc. J. Biol. Chem. 268, 10416-10424 (Pubitemid 23150226)
24. Haltiwanger, R. S., Blomberg, M. A., and Hart, G. W. (1992) Glycosylation of nuclear and cytoplasmic proteins. Purification and characterization of a uridine diphospho-N-acetylglucosamine:polypeptide β-N- acetylglucosaminyltransferase. J. Biol. Chem. 267, 9005-9013
25. Gao, Y., Wells, L., Comer, F. I., Parker, G. J., and Hart, G. W. (2001) Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic β-N-acetylglucosaminidase from human brain. J. Biol. Chem. 276, 9838-9845
26. Comer, F. I., and Hart, G. W. (2001) Reciprocity between O-GlcNAc and O-phosphate on the carboxyl-terminal domain of RNA polymerase II. Biochemistry 40, 7845-7852 (Pubitemid 32622975)
27. Lee, D. H., Gershenzon, N., Gupta, M., Ioshikhes, I. P., Reinberg, D., and Lewis, B. A. (2005) Functional characterization of core promoter elements: the downstream core element is recognized by TAF1. Mol. Cell. Biol. 25, 9674-9686 (Pubitemid 41507864)
28. Lewis, B. A., Sims, R. J., 3rd, Lane, W. S., and Reinberg, D. (2005) Functional characterization of core promoter elements: DPE-specific transcription requires the protein kinase CK2 and the PC4 coactivator. Mol. Cell 18, 471-481 (Pubitemid 40704761)
29. Lubas, W. A., Frank, D. W., Krause, M., and Hanover, J. A. (1997) OLinked GlcNAc transferase is a conserved nucleocytoplasmic protein containing tetratricopeptide repeats. J. Biol. Chem. 272, 9316-9324 (Pubitemid 27154944)
30. Lazarus, B. D., Love, D. C., and Hanover, J. A. (2006) Recombinant O-GlcNAc transferase isoforms: identification of O-GlcNAcase, yes tyrosine kinase, and tau as isoform-specific substrates. Glycobiology 16, 415-421
31. Zhou, M., Halanski, M. A., Radonovich, M. F., Kashanchi, F., Peng, J., Price, D. H., and Brady, J. N. (2000) Tat modifies the activity of CDK9 to phosphorylate serine 5 of the RNA polymerase II carboxyl-terminal domain during human immunodeficiency virus type 1 transcription. Mol. Cell. Biol. 20, 5077-5086 (Pubitemid 30431561)
32. Zachara, N. E., Hart, G. W., Cole, R. N., and Gao, Y. (2002) Detection and Analysis of Proteins Modified by O-Linked N-Acetylglucosamine, Curr. Protoc. Mol. Biol. Chapter 17, Unit 17.6
33. Hanover, J. A., Forsythe, M. E., Hennessey, P. T., Brodigan, T. M., Love, D. C., Ashwell, G., and Krause, M. (2005) A Caenorhabditis elegans model of insulin resistance: altered macronutrient storage and dauer formation in an OGT-1 knock-out. Proc. Natl. Acad. Sci. U.S.A. 102, 11266 -11271
34. Ngo, V. N., Davis, R. E., Lamy, L., Yu, X., Zhao, H., Lenz, G., Lam, L. T., Dave, S., Yang, L., Powell, J., and Staudt, L. M. (2006) A loss-of-function RNA interference screen for molecular targets in cancer. Nature 441, 106-110
35. Comer, F. I., Vosseller, K., Wells, L., Accavitti, M. A., and Hart, G. W. (2001) Characterization of a mouse monoclonal antibody specific for Olinked N-acetylglucosamine. Anal. Biochem. 293, 169-177 (Pubitemid 32547901)
36. Kreppel, L. K., and Hart, G. W. (1999) Regulation of a cytosolic and nuclear O-GlcNAc transferase. Role of the tetratricopeptide repeats. J. Biol. Chem. 274, 32015-32022
37. Lubas, W. A., and Hanover, J. A. (2000) Functional expression of O-linked GlcNAc transferase. Domain structure and substrate specificity. J. Biol. Chem. 275, 10983-10988 (Pubitemid 30212736)
38. Chalkley, R. J., Thalhammer, A., Schoepfer, R., and Burlingame, A. L. (2009) Identification of protein O-GlcNAcylation sites using electron transfer dissociation mass spectrometry on native peptides. Proc. Natl. Acad. Sci. U.S.A. 106, 8894-8899
39. Comtesse, N., Maldener, E., and Meese, E. (2001) Identification of a nuclear variant of MGEA5, a cytoplasmic hyaluronidase and a β-N- acetylglucosaminidase. Biochem. Biophys. Res. Commun. 283, 634-640 (Pubitemid 32917936)
40. Kim, E. J., Kang, D. O., Love, D. C., and Hanover, J. A. (2006) Enzymatic characterization of O-GlcNAcase isoforms using a fluorogenic GlcNAc substrate. Carbohydr. Res. 341, 971-982
41. Lewis, B. A., Kim, T. K., and Orkin, S. H. (2000) A downstream element in the human β-globin promoter: evidence of extended sequence-specific transcription factor IID contacts. Proc. Natl. Acad. Sci. U.S.A. 97, 7172-7177 (Pubitemid 30431436)
42. Lewis, B. A., and Orkin, S. H. (1995) A functional initiator element in the human β-globin promoter. J. Biol. Chem. 270, 28139-28144
43. Gross, B. J., Kraybill, B. C., and Walker, S. (2005) Discovery of O-GlcNAc transferase inhibitors. J. Am. Chem. Soc. 127, 14588-14589 (Pubitemid 41510995)
44. Dong, D. L., and Hart, G. W. (1994) Purification and characterization of an O-GlcNAc selective N-acetyl-β-D-glucosaminidase from rat spleen cytosol. J. Biol. Chem. 269, 19321-19330
45. Burke, T. W., and Kadonaga, J. T. (1996) Drosophila TFIID binds to a conserved downstream basal promoter element that is present in many TATA-box-deficient promoters. Genes Dev. 10, 711-724 (Pubitemid 26112425)
46. Burke, T. W., and Kadonaga, J. T. (1997) The downstream core promoter element, DPE, is conserved from Drosophila to humans and is recognized by TAFII60 of Drosophila. Genes Dev. 11, 3020-3031 (Pubitemid 27508512)
47. Konrad, R. J., Zhang, F., Hale, J. E., Knierman, M. D., Becker, G. W., and Kudlow, J. E. (2002) Alloxan is an inhibitor of the enzymeO-linkedN- acetylglucosamine transferase. Biochem. Biophys. Res. Commun. 293, 207-212
48. Lee, T. N., Alborn, W. E., Knierman, M. D., and Konrad, R. J. (2006) Alloxan is an inhibitor of O-GlcNAc-selective N-acetyl-β-D-glucosaminidase. Biochem. Biophys. Res. Commun. 350, 1038-1043
49. Macauley, M. S., Whitworth, G. E., Debowski, A. W., Chin, D., and Vocadlo, D. J. (2005) O-GlcNAcase uses substrate-assisted catalysis. Kinetic analysis and development of highly selective mechanism-inspired inhibitors. J. Biol. Chem. 280, 25313-25322 (Pubitemid 40962233)
50. Reason, A. J., Dell, A., Romero, P. A., and Herscovics, A. (1991) Specificity of the mannosyltransferase which initiates outer chain formation in Saccharomyces cerevisiae. Glycobiology 1, 387-391
51. Gebara, M. M., Sayre, M. H., and Corden, J. L. (1997) Phosphorylation of the carboxy-terminal repeat domain in RNA polymerase II by cyclin-dependent kinases is sufficient to inhibit transcription. J. Cell. Biochem. 64, 390-402 (Pubitemid 27098625)
52. Love, D. C., Ghosh, S., Mondoux, M. A., Fukushige, T., Wang, P., Wilson, M. A., Iser, W. B., Wolkow, C. A., Krause, M. W., and Hanover, J. A. (2010) DynamicO-GlcNAc cycling at promoters of Caenorhabditis elegans genes regulating longevity, stress, and immunity. Proc. Natl. Acad. Sci. U.S.A. 107, 7413-7418
53. Pavri, R., Lewis, B., Kim, T. K., Dilworth, F. J., Erdjument-Bromage, H., Tempst, P., de Murcia, G., Evans, R., Chambon, P., and Reinberg, D. (2005) PARP-1 determines specificity in a retinoid signaling pathway via direct modulation of mediator. Mol. Cell 18, 83-96 (Pubitemid 40444650)
54. Zheng, L., Roeder, R. G., and Luo, Y. (2003) S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114, 255-266 (Pubitemid 36936918)
55. Maldonado, E., Drapkin, R., and Reinberg, D. (1996) Purification of human RNA polymerase II and general transcription factors. Methods Enzymol. 274, 72-100 (Pubitemid 26353069)